- Veterinary Helminthology 1st Edition
- Species accounts
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Helminths of ruminants
Author: J BOOMKER
With the exception of two Dictyocaulus species –Muellerius capillaris and two Mammomonogamus species –no adult helminths occur in the lungs or trachea of ruminants. Several others, however, may pass through the lungs as larvae on their way to their favoured sites elsewhere in the body. Infections with lungworms are not always obvious, clinically speaking. However, in cattle in Europe and sheep in Africa they invariably cause disease in na ïve animals, and, when not treated, often have fatal consequences.
The Dictyocaulus species belong to the superfamily Trichostrongyloidea, family Dictyocaulidae –and are colloquially known as lungworms. They are large, milky-white worms that are easily seen in the trachea of their hosts. Males are 3 to 8 cm long and females 5 to 10 cm long. The spicules are stout, boot-shaped, and intricately sculptured. Females are ovoviviparous and lay eggs with a thin shell containing a fully developed first stage larva.
Dictyocaulus species occur worldwide and are particularly important in temperate climates.
Sheep, goats and occasionally some antelope are the hosts of D. filaria , and cattle, deer, reindeer, water buffaloes and camels are the hosts of D. viviparus .
The life cycle of Dictyocaulus species is direct (monoxenous) and the helminths are sometimes referred to as 'geohelminths'. Eggs may hatch in the lungs, but are usually coughed up and swallowed, and the first stage larvae then hatch when they pass through the intestinal tract. The first stage larva of D. filaria has a small cuticular knob at the anterior extremity, which is lacking in D. viviparus . Brown food granules are present in the intestinal cells of the larvae of both species, and the free-living stages live off the food granules. After a few days, the larvae reach the second stage but retain the cuticle of the first stage. Once they reach the third (infective) stage, the cuticle of the first stage is cast off, but that of the second stage is retained. The infective stage is reached after six or seven days.
Infection of the host occurs per os. Larvae penetrate the intestinal wall and pass to the mesenteric lymph nodes –where the third moult takes place. The now fourth stage larvae pass via the lymph and blood vessels to the lungs where they are trapped in the capillaries and break through into the alveoli. They then migrate to the bronchi and trachea to mature into the adult male and female worms. The pre-patent period is about 28 days for D. filaria , and 22 days for D. viviparus .
Although D. filaria is cosmopolitan in its distribution, it is only responsible for sporadic outbreaks –even in warmer areas such as parts of Africa and the Mediterranean. Larvae are extremely sensitive to heat and desiccation, but are resistant to cold and can overwinter in colder areas. Carrier animals are important as a source of pasture contamination in Africa, where the climate is often unsuitable for larval survival. Outbreaks of disease are usually seen after prolonged rain around the time that lambs and kids are weaned. Fountains, marshes, streams and rivers provide adequate moisture for the survival of free-living stages, and irrigated pastures can be potential foci of infection.
D. viviparus is similar to D. filaria in many respects, but its epidemiology is largely unknown. Isolated foci of infection occur wherever the climate is suitable for the survival of free-living stages –usually in the cool, moist parts of a region. The parasites are highly prevalent on irrigated pastures. In temperate regions like Europe and North America, these parasites are particularly important (see Urquhart et al . (1991) and http://www.merckmanual.com for a detailed description of the epidemiology in these countries).
Outbreaks of parasitic bronchopneumonia occur sporadically, and then mostly on irrigated pastures, or in the cool, moist areas of a country. Animals lose condition, and unless treated, some deaths may occur.
The pathogenesis of dictyocaulosis can be divided into four phases:
- The penetration phase (days 1 to 7) during which the larvae migrate from the intestine to the lungs via the mesenteric lymph nodes and lymphatic system. Neither clinical signs nor pulmonary lesions are seen.
- The pre-patent phase (days 8 to 25) starts when the larvae arrive in the lungs. They cause alveolitis, followed by bronchiolitis, and finally bronchitis as they reach the bronchi. Cellular infiltrates (neutrophils, eosinophils, and macrophages) temporarily block the bronchioli –causing atelectasis when groups of alveoli collapse. The first clinical signs –tachypnoea and coughing –are now observed. Heavily infected animals may start dying from day 15 onwards, due to respiratory failure after the development of severe interstitial emphysema and lung oedema. Epithelialisation and the formation of hyaline membranes in the alveoli commence at this stage.
- The patent phase (days 26 to 60) is associated with two main lesions –a parasitic bronchitis and a parasitic pneumonia respectively. The former is characterised by the presence of many adult worms in the bronchi and distal trachea, which are embedded in a frothy white mucus. There is severe damage to these tissues, which is manifested by a hyperplastic epithelium infiltrated by inflammatory cells, especially eosinophils. The parasitic pneumonia –detectable as collapsed areas around infected bronchi –is the result of the presence of aspirated eggs and first stage larvae that act as foreign bodies. Pronounced polymorph, macrophage and multinucleated giant-cell infiltrations are provoked by the presence of the eggs and larvae. Varying degrees of oedema and emphysema may be seen, and alveolar epithelialisation and hyaline membrane formation become more obvious with progression and increased severity of the lesions.
- The post-patent phase (days 60 to 90) is the recovery phase, after the adult worms have been expelled. The inflammatory exudate in the lungs undergoes organisation, and, clinically, the respiratory rate decreases, coughing is less frequent, and weight gain is resumed. Severe epithelialisation may persist in some animals, 90 days after infection when the worms are usually absent. The remaining lesions consist of peri-bronchial fibrosis and epithelialisation of a few alveoli surrounding some bronchi.
Animals mildly affected with Dictyocaulus cough intermittently –especially during exercise. Those moderately affected have frequent bouts of coughing, even at rest, and tachypnoea and hyperpnoea are evident. On auscultation, moist r âles are heard over the posterior lung lobes. Severely affected animals show severe tachypnoea and dyspnoea. They often stand with their head with neck outstretched and elbows held away from the chest. A deep, harsh cough is present and r âles are heard over the posterior lung lobes.
With very heavy infections there may be enteritis resulting from the infective larvae burrowing through the intestinal wall. In Dictyocaulus infections, depending on the severity, lung lesions may be pronounced. Usually there are small foci of pneumonia, resulting from the fifth-stage worms breaking through the alveoli. From about the 10th day after infection, frothy fluid is present in the alveoli and terminal bronchioles, and there may be oedema and emphysema of the interlobular septa. Most of the bronchioles contain plugs of exudate. As the worms mature and move to the bronchi, these plugs may resolve. The mature worms in the bronchi are easy to see. They are surrounded by a frothy bronchial exudate and cause atelectasis and emphysema secondary to the bronchitis –the latter being provoked by aspirated eggs and larvae. The lung lesions appear as large dark-red or grey, wedge-shaped areas slightly sunken below the surface of the surrounding tissue, and are usually situated in the posterior border of the diaphragmatic lobes ( Figure 19 ). In cases where bacterial infections took place, the lesions are complicated purulent pneumonia. There is no pleuritis.
The diagnosis of lungworm infection is based on the presence of rapid breathing, bronchitis and coughing, and the demonstration of larvae in fresh faeces by the Baermann method. To avoid contamination with soil nematodes, faecal specimens should be collected from the rectum. Eggs may be found in nasal or oral discharges, but their absence is not an indication that the worms are absent.
Other causes of bronchitis and pneumonia, such as Pasteurella , contagious bovine pleuropneumonia, and jaagsiekte, and causes of a purulent nasal discharge such as Oestrus ovis –should be considered.
In the case of Dictyocaulus species, control is difficult as it involves water and grazing management. Because of the rapid build-up of larvae, wet areas, especially in the cooler parts of a country, should not be used for grazing unless all animals have been treated and are free of the worms. In temperate regions, the only reliable method of control is vaccination with irradiated larvae. The vaccine is only available in Europe.
Muellerius capillaris is a member of the superfamily Metastrongyloidea, and family Protostrongylidae. Males are 12 to 14 mm and females 19 to 23 mm long. The posterior end of the male is spirally coiled and the spicules are 0.15 mm long. Each spicule consists of a proximal alate part and two serrated distal 'arms'. The eggs measure 0.1 by 0.02 mm. Cystocaulus, Spiculocaulus and Neostrongylus are minor related genera. Mammomonogamus belongs to the superfamily Strongyloidea, and family Syngamidae . They are red in colour, and males and females are permanently joined. Males are 4 to 10 mm long and females 8.5 to 23 mm long. Eggs are ellipsoidal and measure 0.075 to 0.098 by 0.042 to 0.054 mm.
Muellerius also occurs worldwide, with the exception of the arctic and subarctic regions, and is possibly the commonest lungworm of sheep in Europe, the eastern USA and the winter rainfall regions of Australia. In South Africa, it occurs in the winter rainfall area of the Western Cape Province. Mammomonogamus is a parasite of the tropical and subtropical regions and occurs in India, Malaysia, Vietnam, South America, and parts of Africa. Cattle in the Ethiopian lowlands are often infected with this worm.
Muellerius capillaris is a heteroxenous parasite or 'biohelminth' that uses snails and slugs as intermediate hosts. The eggs develop in the lungs of the host and the first stage larvae pass out with the faeces. The tail of the larva has a spine and an undulating tip. These larvae can resist a fair amount of desiccation, are not killed by freezing, and are most active at temperatures of about 17-27 °C. For further development, they must enter a mollusc –the intermediate host –by penetrating the foot of the mollusc. The infective stage (L3) is reached after 12 to 14 days. These larvae can live in the snail/slug for as long as it lives –and for a week after its death. The final host becomes infected when it consumes the mollusc with its food. Larvae pass through the intestinal wall into the mesenteric lymph nodes, where they moult to the fourth stage. They then go to the lungs via the lymph and blood vessels. Trans-placental transmission takes place and larvae have been found in the liver and lungs of foetuses and new-born lambs. The pre-patent period is 6 to 10 weeks. The life cycle of Mammomonogamus is unknown.
The epidemiology of Muellerius capillaris and Mammomonogamus is largely unknown. However, Muellerius is usually not found in animals younger than 6 months. Its prevalence increases with age and 100% of animals older than 3 years may be infected. The ability of the L1 to survive for months in faecal pellets, together with the survival of L3 in the snail or slug for the duration of the mollusc's lifetime, ensure the endemicity of this worm. Muellerius is not considered to be pathogenic and even in severe infections clinical signs are rare. Occasionally, heavily infected goats show clinical signs varying from moderate dyspnoea and a persistent cough, through to frank pneumonia. All infected animals are predisposed to secondary bacterial infection because of the damage done to the lungs by the parasite.
Mammomonogamus is not considered to be a serious pathogen, although coughing and some loss of condition are seen when several worms are attached to the larynx. In humans infected with this parasite, coughing and haemoptysis may occur. Adult Muellerius are contained in nodules varying from 2 to 3 mm to 200 mm in diameter, and within the nodules they are contained within an inflammatory reaction characterised by the presence of leukocytes, a few giant cells, and a connective-tissue capsule.
lives in the alveoli and lung parenchyma and produces nodules up to 20 mm in diameter. These consist of necrotic material, leukocytes, and a few giant cells surrounded by a connective-tissue capsule. The content of the nodules may calcify. The eggs cause the formation of smaller nodules due to a leukocyte and epithelioid cell reaction; the reaction usually subsides once the eggs have hatched. In some (rare) cases, an adenoma-like proliferation of the bronchial epithelium occurs. However, despite the nature of the lesions, clinical cases are rarely seen. Muellerius infection is associated with the presence of small, spherical nodules that usually occur near or on the lung surface. On palpation, these feel like lead shot. Nodules in which single worms occur are small and cannot be seen macroscopically, while the larger ones contain several adult worms and eggs, larvae, and some cellular infiltrate.
The pathogenesis of Mammomonogamus is unknown.
Treatment and control
Snails and slugs must be controlled where Muellerius is a problem. However, due to the worm's low pathogenicity, snail/slug control is seldom applied. Both lungworms may be treated with levamisole, any of the benzimidazoles, or the macrocyclic lactones at the recommended dose.
With the exception of a single nematode, Gongylonema, helminths do not occur in the oesophagus of ruminants.
Gongylonema is a nematode in the Order Spirurida. It is a large worm that inhabits the sub-epithelial tissue mucosa or submucosa of the oesophagus –where it lies in a characteristic zigzag pattern. It is non-pathogenic and is usually an incidental finding at necropsy.
Gongylonema is distributed worldwide, wherever dung beetles –the intermediate hosts –occur.
Although most helminths pass through the rumen at some stage in their life –few live there. The nematode Gongylonema can occasionally be found at the oesophagoruminal opening, but it prefers the oesophagus itself. Trematodes belonging to the family Paramphistomatidae are virtually the only ones that colonise the rumen, but only as adults, as the immature stages occur elsewhere.
Conical fluke (Amphistomes)
Calicophoron microbothrium (previously Paramphistomum microbothrium) , the conical fluke, is found in the small intestines (immatures) ( Figure 21 ) and the rumen (mature flukes) ( Figure 20 ) of cattle, sheep, goats and most wild ruminants in the tropical and subtropical regions of the world. Other genera are also involved.
The genus occurs in sheep, goats, cattle, buffalo and pigs –and less frequently in horses, donkeys, and camels. It also occurs in the crop of domestic chickens, and has also been found in the oesophagus of humans.
Dung beetles of the genera Aphodius, Onthophagus, Blaps (and others) transmit Gongylonema. It has also been shown that the cockroach, Blatella germanica , can act as an intermediate host. Infection of the final host takes place by ingestion of infected beetles.
The life cycle, as described below, is the same for all genera, with the exception of the developmental times which vary in different genera and species. Eggs are passed with the faeces and hatch in water 12 to 26 days later. Miracidia enter the young of the aquatic snail Bulinus tropicus (or any other suitable snail intermediate host) at birth, and up to the age of 3 weeks. Older snails are not infected. Sporocysts are found after one day and may persist for up to 11 days. The first rediae are present 14 days after the snail has been infected, and daughter rediae occur after 20 to 28 days. Cercariae are present after 30 days and start emerging from the snail by the 43rd day. Snails may remain infected and shed cercariae for up to 1 year. The cercariae encyst on vegetation to form the metacercariae. They will die if desiccated or completely submerged, but remain viable for 2 months under cool, moist conditions. Once ingested, the metacercariae excyst in the first three metres of the small intestine, and the young flukes attach to the mucosa. After about 15 to 56 days in the small intestine, the young flukes start migrating to the rumen. Their entire life cycle from the time that the eggs are laid until the next generation eggs are laid, takes a minimum of 110 days.
Conical flukes occur worldwide wherever ruminants occur or are farmed –with the possible exception of North America. They are of little significance in the northern parts of the northern hemisphere (Europe, Canada, Russia and the United States), although a species of Calicophoron occurs in Scotland, Ireland and Holland. They only occasionally cause disease in the tropics and subtropics.
Apart from Calicophoron, amphistomosis is caused by several other genera in different parts of the world. Cotylophoron and Calicophoron are responsible for outbreaks of amphistomosis in a variety of ruminants all over the world. Ceylonocotyle occurs in water buffaloes and cattle in Asia and cattle in Australasia, and Bilatorchis in cattle in Indonesia. Several genera of lesser importance are sometimes encountered; these include Homologaster in Asia, Carmeyerius in India and Africa, and Gastrothylax in India, Ceylon and China. In short, members of the Paramphistomatidae occur all over the world, but abound in the tropics and subtropics –probably because of environmental factors which favour the snails and the survival of the metacercariae.
Many different ruminants are the hosts of the various genera of Paramphistomatidae –or amphistomes as they are known colloquially. This includes the domesticated ones and a number of wild ruminants and hippopotami.
The flukes are ingested as metacercariae that adhere to vegetable matter or any other solid object at the water's edge. Metacercariae may be transmitted over short distances by waterfowl, and by irrigation. Clinical cases have been encountered in cattle that have grazed irrigated pastures and had no access to open water.
Adult amphistomes have little socio-economic effect per se. Tripe could be condemned as "aesthetically objectionable" –but once cleaned and cooked it can be consumed with safety.
Any pathogenic effect associated with amphistomes is associated with the immatures in the intestine. Adults are thus of little consequence in causing disease.
No clinical signs are associated with adult amphistome infections.
The adult flukes are well tolerated and cause no lesions in the rumen, even when thousands are present. Occasional discolouration of the rumen papillae –to which the flukes attach –may be encountered.
Since clinical signs are absent with adult fluke infections, a faecal trematode egg count should be done –either by sedimentation or by using the Visser filter. The presence of large, operculated eggs, approximately 0.170 x 0.1 mm, and grey-white in appearance, is indicative. The eggs must be differentiated from those of Fasciola , which are slightly smaller, approximately 0.150 x 0.09 mm in size, and yellow.
Since the condition is asymptomatic, differential diagnoses are not applicable. However, the eggs of Fasciola species could cause confusion. Also refer to "Diagnosis".
Control of adult amphistomes is readily achieved with anthelmintics. Biological control methods such as water supply, snail control and rotational grazing should be employed, and are discussed in greater detail under "Parasitic gastro-enteritis" –specifically the section dealing with trematodes.
There are only a few genera of nematodes that occur in the abomasum of ruminants. Haemonchus, Ostertagia and Trichostrongylus axei are probably the most important causes of disease in cattle, and Haemonchus, Teladorsagia and Trichostrongylus axei in sheep. The genera Ashworthius , Marshallagia and Mecistocirrus are occasionally encountered in cattle and camels.
The nematodes of cattle can also be classified as those of primary, secondary and tertiary importance, but it is generally accepted that they do not cause problems to the same extent as those of sheep. Immunity to the parasites develops faster in cattle –and calves are able to reduce their parasite burdens significantly after 6 months of age.
Occasionally, due to poor management and malnutrition, cattle –particularly calves –may show clinical signs of helminthoses.
It should be noted that all these worms thrive on irrigated pastures and this makes them ideal candidates for the development of anthelmintic resistance.
The socio-economic impact of the helminths of the abomasum of ruminants is severe, not only because of direct losses through death of the animals (as is often the case with H. contortus and the ostertagiids), but also because of the erosive effects of the disease caused by T. axei (hence the colloquial name "stomach bankrupt worm"). The rapidly developing resistance to anthelmintics is an additional socio-economic factor and is discussed in more detail under anthelmintic resistance.
The various abomasal worms all have a direct life cycle; infection is acquired per os, and the free-living third stage larva is the infective stage. Some species of antelope can act as reservoir hosts and may thus be responsible for the dissemination of various species.
Barber ’s pole worm or wireworm
Wireworm of cattle
Haemonchus are known as barber's pole worms or wireworms. The adults are easily identified by their presence in the abomasum and their large size (2 to 3 cm). Fresh female specimens are conspicuous in having a large vulvar flap and white ovaries twisted spirally around the blood-filled intestine –giving them a barber's pole appearance. The male has a large, asymmetrical, Y-shaped dorsal ray.
The life cycle is direct. The females produce about 10 000 eggs per day. The L1 hatch on the pastures and infective stages can occur within 5 days –during warm, moist weather. However, under adverse conditions development of the L4 stage may be retarded for weeks or even months (hypobiosis). Adults move freely across the abomasal mucosa and suck blood wherever they are. The developmental period is 18 to 21 days. Although Haemonchus placei –the wireworm of cattle –is difficult to distinguish from H. contortus of sheep ( Figure 22 ), its ecological requirements, epidemiology and general behaviour differ so much that –according to many authors –it warrants classification as a separate species. Not all helminthologists, support this, however, and the name H. contortus of cattle may still be found in the literature. The species is widely distributed throughout the world. The developmental period is 23 to 28 days.
Haemonchus contortus, Haemonchus placei, Haemonchus similis, Teladorsagia circumcincta, Ostertagia ostertagi and Trichostrongylus axei have a wide distribution wherever cattle, sheep and goats are kept in the temperate, subtropical and tropical regions of the world. This wide distribution is due to the large host spectrum. In Africa, and perhaps in the Middle East and central Asia, Haemonchus longistipes is an important parasite of camels. Longistrongylus elongata and Mecistocirrus are limited to East and North Africa. The temperate regions –such as Europe and the north Americas –are probably the least favoured by Haemonchus .
Infections develop in two ways. Firstly, infective larvae develop from eggs deposited by ruminants, especially sheep, in late summer or autumn. These larvae become arrested in the abomasal mucosa as fourth stages (hypobiosis) and will only complete their development the following spring. This spring rise is associated with pregnancy –especially when the ewes are about to lamb or shortly thereafter –but it is not limited to female animals. The spring rise is also referred to as the peri-parturient relaxation of resistance (PPRR) and has an immunological basis. Clinical signs may be seen during maturation of the larvae. Secondly, the worms that have overwintered are responsible for the summer burden, which –depending on the rainfall –may be significant. In the subtropical and tropical regions, haemonchosi s is the primary helminth infection in sheep, and outbreaks are largely seen during summer. Both temperature and humidity are high –facilitating larval growth and development and survival on the pastures. The disease in cattle that is sometimes caused by H. similis and H. placei in tropical and subtropical regions, is similar to the disease in sheep. Severe outbreaks, however, are usually seen during seasonal rains, but have also been recorded at the end of long, dry spells due to the maturation of hypobiotic larvae.
The pathogenesis of haemonchosis is essentially that of haemorrhagic anaemia, due to the blood-sucking habits of the worms ( Figure 23 ). Each worm can remove up to 0,05 ml of blood per day by ingestion and seepage from the lesion. There are 3 different forms of haemonchosis:
- Peracute: After infection with 20 000 to 35 000 L3, the resulting L4 cause petechiae, while the 5th stages and adults cause frank haemorrhage and erosions at their attachment sites. Sheep can lose 1 000 to 1 750 ml of blood per day. Death in apparently healthy sheep occurs suddenly as a result of severe blood loss and anaemia.
- Acute: A burden of 2 000 to 20 000 adult worms cause a daily blood loss of 100 to 1 000 ml. Anaemia becomes apparent from about 2 weeks after infection, and is accompanied by a progressive and dramatic fall in the PCV. Subsequently, the haematocrit stabilises and intense compensatory erythropoiesis (visible as hyperplasia of bone marrow) at the expense of the iron reserves occurs. Together with the continual loss of iron and protein (albumin) into the gastrointestinal tract, the bone marrow eventually becomes exhausted, and shortly before death the PCV falls even further.
- Chronic: About 100 to 2 000 adult worms can cause blood loss of about 5 to 100 ml per day. Chronic haemonchosis usually develops during winter when reinfection is negligible, but the pastures become deficient in nutrients, notably protein and iron. The continual blood loss depletes the iron reserves completely, causing marked anaemia to develop before death.
- Per-acute cases show few changes, as death occurs too rapidly for lesions to become established. The carcass is anaemic, and there are many petechiae and small erosions in the abomasal mucosa. Coagulated blood –which is often dark brown due to blood seepage –may be present in the abomasal contents. Masses of worms are usually present in the watery, blood-stained abomasal content.
- Acute cases are the most frequently encountered manifestation of the infection. The outstanding features of the acute disease are the extreme anaemia, emaciation, and oedema of the carcass. Compensatory erythropoiesis is seen as hyperplasia of the bone marrow. The abomasal mucosa is hyperaemic, many petechiae and focal erosions are present, and a few small ulcers may occur. The sub-mucosa is thickened and oedematous. The abomasal content is scant, watery and slightly brown, and semi-digested blood clots are sometimes present. The worms are easily seen, but if the necropsy has been delayed for 24 hours or more, the worms may no longer be detectable because of post-mortem changes. However, upwards of 10 000 epg are usually encountered if a faecal examination is done.
- Chronic cases are generally emaciated and pale. The abomasal mucosa shows hyperplasia and metaplasia, and the folds are opaque and thickened. There is evidence of chronic, red bone marrow hyperplasia combined with reversion to white bone marrow –the latter being the result of iron depletion.
Haemonchosis in cattle shows the same clinical signs as those seen in sheep –but they are generally milder, especially in animals older than 2 years.
Haemonchosis in sheep shows the following clinical signs:
- Animals suffering from the hyper-acute disease die suddenly, with few signs except anaemia and dark brown to black faeces. The hyper-acute form is rarely seen.
- Animals suffering from the acute disease manifest anaemia, bottle jaw, weight loss despite increased food intake, and dry, dark brown to black faeces. Ewes stop producing milk and suckling lambs die of starvation. Lethargy and a break in the wool set in before death. This form of the disease is commonly seen.
- In the chronic from of the disease, animals lose weight progressively over several months –but show neither severe anaemia nor submandibular oedema. Eventually the animal becomes weaker and anorexia sets in. Anaemia is present shortly before death, as is submandibular oedema.
Brown stomach worm of small stock
Brown stomach worm of cattle
Teladorsagia , the brown stomach worm of small stock, occurs worldwide in the abomasum of sheep and goats. The life cycle is direct. Infective larvae enter the gastric pits where they develop and moult to the young adult worms that start emerging from the gastric glands after 18 to 21 days (developmental or pre-patent period). L4 may still be found in the mucosa 8 to 12 weeks after infection; this is a prolonged histotropic phase and should not be confused with hypobiosis.
Ostertagia , the brown stomach worm of the abomasum of cattle, occurs world-wide, and in South Africa they are common in the Eastern and Western Cape Provinces. The life cycle is direct and the developmental period is 18 to 24 days. Like Teladorsagia , infective larvae also enter the gastric pits where they moult to young adults after 9 to 11 days. Adult worms start emerging from the gastric glands after 18 days (pre-patent period). However, L4 may still be found in the mucosa 8 to 12 weeks after infestation –the histotropic phase.
Epidemiology and distribution
Ostertagia and Teladorsagia both prefer cooler climates. In South Africa, the former occurs mainly in the Eastern and Western Cape Provinces from April to September –i.e. autumn to spring –and the latter in the areas adjacent to the former Transkei (Eastern Cape) and Lesotho, from February to June, and again from October to December. In the Highveld of Gauteng and the Free State Provinces, adult worms occur in peak numbers in April, and as hypobiotic L4 from May to October.
The L3 and L4 of Ostertagia and Teladorsagia , and presumably of other ostertagiids, cause pressure necrosis in the glandular epithelium and destroy the function of the parietal and zymogen cells. The result is that the pH of the abomasal content rises from 2 to 7 –in which environment pepsinogen is not activated to pepsin (above pH 5 pepsin activity is negligible), meaning that digestion of food cannot take place. In addition, protein is not denatured and bacteriostatic activity is lost, causing an increase in the number of bacteria in the abomasum. The pepsinogen output is further reduced, again resulting in reduced pepsin activity. Blood serum albumin levels remain low until recovery or death. Adult worms suck much blood, as is evidenced by the fall in the haematocrit and haemoglobin values 3 to 4 weeks after infection. However, haemorrhage into the abomasal lumen does not occur.
Anaemia, submandibular and sternal oedema, and emaciated and dehydrated carcasses with evidence of diarrhoea –are typical changes seen in teladorsagiosis. There is nodular abomasitis (the nodules sometimes being confluent and covered with tenacious mucus), hyperaemic abomasal mucosa, sometimes small abscesses in the gastric pits where the larvae live, and sometimes –depending on the duration –scar tissue where the gastric pits used to be. The entire mucosa has an 'ostrich leather' appearance ( Figure 24 ) –each nodule having a small, central opening through which the worms can be seen. The picture is one of severe diffuse hyperplastic abomasitis. Angora goats in South Africa develop anasarca and ascites.
Ostertagiosis in cattle presents as a profuse watery diarrhoea, anorexia, loss of mass, severe chronic diarrhoea, dehydration, thirst, emaciation, and death. In the northern hemisphere, a distinction is made between Type I and Type II ostertagiosis. Type I occurs in calves in summer and the larvae ingested develop normally into adults –with the resulting pathogenic effects. Type II is seen in yearlings. The animals are heavily infected, but most larvae remain inhibited as L4. These larvae remain in stabled calves, but cause no clinical signs until they emerge as adults.
In teladorsagiosis in sheep there is anorexia, a marked loss of weight, anaemia, submandibular oedema, occasional diarrhoea and death. In Angora goats there is a marked oedematous subcutaneous swelling of the abdomen and limbs –known as 'waterpens' (literally “water stomach ”) in Afrikaans.
Stomach bankrupt worm
T. axei is found in all the domestic ruminants, pigs, horses and occasionally in humans. They occur worldwide, wherever ruminants are kept, and are present in the abomasum or stomach. The life cycle is direct, and the developmental period in ruminants is 24 days. They are very small, thin worms that are not easily seen with the naked eye. Under the microscope, both sexes have a ventral cervical notch into which the excretory pore opens, and the female tail is sharply pointed. Because of the size of the worms, few eggs are present in the uteri. Males are readily recognized by the unequal spicules –of which the right one bears a distinct spine.
Epidemiology and distribution
Trichostrongylus axei occurs from about March to September in winter and nonseasonal rainfall areas, and from March to September in the Gauteng and Free State Highveld.
Fair numbers of infectiveTrichostrongylus larvae are necessary to cause clinical disease, e.g. 40 000 larvae cause death in Dorper sheep –but not in Merinos. The worms cause an increase in the abomasal pH, abomasal and serum pepsinogen, and a decrease in the available nitrogen –similar to that seen in ostertagiosis/teladorsagiosis, but not nearly as severe. In abomasal or stomach trichostrongylosis, the carcass is emaciated, the abomasal or stomach content is filled with foul-smelling ingesta, and there is oedema of the stomach mucosa. Catarrhal abomasitis or gastritis is due to larval action, whereas mature worms cause thickening of the mucosa, which resembles wart-like plaques or "ringworm-like" lesions. If these thickenings are removed, an erosion with an intensely hyperaemic base remains. In heavy infections, the thickened areas coalesce to produce a diffuse hypertrophic gastritis.
Infection with Trichostrongylus axei is no longer as common as it used to be. This is probably because of the frequent drenching of ruminants to control Haemonchus . In all animals where T. axei occurs, the clinical signs develop quickly and include rapid loss of body mass –leading to emaciation, diarrhoea and anorexia, which are then followed by weakness and death.
Diagnosis of abomasal worms
When attempting to make a diagnosis of helminth infection, one must consider the age and sex of the animals, and the season, rainfall and the geographic locality of the farm. A detailed history should also be taken. The diagnosis of helminthoses is best done by necropsy, as this is the only way to determine the size and cause of infection. If dead animals are not available or are too decomposed, ask the owner to slaughter an animal. However, this is becoming increasingly difficult because of the value of the animals. Egg counts can be carried out on 10% of the herd or flock. In large flocks of over 500 animals, one should select the tops (fat animals) and the tails (skinny animals) –and then do the egg counts on 10% of each group. Otherwise, one could look for animals with soiled breeches and bottle jaws, and do egg counts on them. Reinecke (1983) stated that "All sheep will be infected as well as young calves and yearlings. The mere detection of infection must therefore be treated with great reserve. No faecal examination can detect immature worms which may have marked pathogenic effects... .”Examples are the L4 of Ostertagia and Teladorsagia. It is clear that egg counts are not the most accurate method to establish a diagnosis as the number of eggs present per gram of faeces depends on a variety of factors; one may have to rely on the identification of L3 larvae obtained by faecal culture.
In the case of haemonchosis, the first differential diagnosis that comes to mind is fasciolosis (because of the anaemia) –followed by other helminth infections, infections with protozoa that cause anaemia, and poisonings that cause anaemia. For the other two abomasal worms, the differential diagnoses would include infection with other helminths and certain poisonings. Chronic cases or mild infections with either of the three genera mentioned here are often difficult to distinguish from malnutrition.
Treatment and control
Because anthelmintic resistance is widespread in Haemonchus contortus –and some strains of Teladorsagia and Trichostrongylus in sheep are also resistant to certain anthelmintics –a programme must be implemented which will control clinical disease and limit the development of resistance.
The following is suggested:
- Quarantine treatment: since resistant worms are often acquired by bringing new animals onto a farm, treatment in quarantine is essential. The animals should be dosed sequentially with two different remedies. The use of new actives such as derquantel or monepantel is suggested to ensure that resistant worms are destroyed.
- Identify the worms present on the farm: this can be done by sampling animals at necropsy or using faecal samples for analysis.
- Select a suitable remedy: refer to the MIMS IVS Desk Reference which lists all commercial products currently registered for use against the endoparasites of livestock in South Africa. It is updated annually to include newly registered products. The spectrum of the selected remedy must be carefully considered as it may have to include activity against other gastrointestinal nematodes.
- Use a Targeted Selected Treatment (TST): as discussed under the general chapter on control, the FAMACHA method identifies anaemic animals for treatment for H. contortus infection. For non-bloodsucking worms, animals for treatment can be selected using Body Condition Scoring.
- Vaccination: for additional control of H. contortus , use vaccination to improve the immune status of young animals, in particular.
- Monitor anthelmintic efficacy: using a regular FEC, the efficacy of the anthelmintic in use can be assessed.
- Ensure refugia: dosed animals should not be placed on clean pastures ( see discussion of Refugia under Control, in Chapter 1 ).
- Environmental management: to reduce the worm burdens on pastures, use other species to graze contaminated pastures, as discussed in the section on control.
Outbreaks of these helminthoses occur only sporadically in cattle and are best controlled with one of the anthelmintics. Apart from some anthelmintic resistance of Ostertagia in cattle in South Africa, most remedies are effective.
By far the majority of helminths occur in the small intestine of ruminants; this includes members of all the classes –including the Acanthocephala. One can only speculate on why such a diversity of parasites occurs in the intestines, and it is possible that the state of digestion of the food plays a role. The small intestine is also much less harsh an environment than the acidity of the abomasum. Many of the helminths that inhabit the intestine are quite pathogenic (Nematodirus, Trichostrongylus species, Gaigeria, Bunostomum and Calicophoron ), while some are considered to be apathogenic (Cooperia species and the tapeworms). For the purpose of this section, the worms are grouped into the trichostrongylids (Trichostrongylus, Nematodirus and Cooperia) , the hookworms (Bunostomum and Gaigeria), Strongyloides, and Toxocara. The other groups are the tapeworms and Calicophoron.
Trichostrongylus, Nematodirus, Cooperia
Bunostomum, Gaigeria, Strongyloides, Toxocara
Several nematodes, cestodes, and a trematode occur in the small intestine of sheep, goats, cattle, and a variety of antelope species:
- The bankrupt worm, Trichostrongylus colubriformis, Trichostrongylus rugatus, Trichostrongylus falculatus and Trichostrongylus vitrinus . All these species are known by the same common name and occur worldwide. They tend to occur in the first 7 m of the small intestine, and rarely in the abomasum or in the stomach. The parasites behave similarly in cattle and sheep, but the condition is usually less severe in cattle and only occurs in young calves. Humans have also been shown to become infected with some of the Trichostrongylus species, as are antelope species, pigs, hares, and rodents. The life cycle is direct and the developmental period is 18 to 20 days.
- The long-necked bankrupt worm, Nematodirus spathiger, is found in the small intestines of sheep, goats and various antelope –and Nematodirus helvetianus in cattle. They occur worldwide wherever sheep and cattle are kept. The life cycle is direct. The first three stages of this worm develop inside the egg, and the infective L3 hatches. The developmental period is 14 to 21 days.
- The white bankrupt worm, Strongyloides papillosus –of sheep, goats, cattle and wild ruminants –occurs all over the world. The life cycle may be homo- or heterogonic. The developmental period is 8 to 14 days.
- Bunostomum trigonocephalum, also known as the grassveld hookworm, affects sheep, goats and certain antelope species. The life cycle is direct, and the developmental period is about 30 to 60 days. Infection occurs either percutaneously or per os. The cattle hookworm, Bunostomum phlebotomum –as its name implies –occurs mostly in cattle, but water buffaloes are probably also susceptible. The life cycle is direct. The developmental period is 52 to 56 days and infestation only takes place percutaneously.
- The sandveld hookworm, Gaigeria pectinata, occurs in sheep and goats worldwide, and in impala and wildebeest in Africa. The life cycle is direct. Only percutaneous infection takes place and the developmental period is 70 days.
- The Cooperia species involved with ruminants are C. pectinata, C. punctata, C. spatulata, C. oncophora, C. mcmasteri and C. curticei –and they occur in a wide range of ruminants worldwide. In severe infestations, i.e. animals receiving 300 000 larvae within 10 days, there are clinical signs –but generally these worms are of little importance. The prepatent period is 11 to 19 days.
- Toxocara vitulorum –known as the ascarid of cattle –is seen in suckling calves only. It is morphologically very similar to Toxocara canis . The eggs have a thick wall and are finely pitted. Infection takes place via the milk of the cow and adult worms are present after 33 days.
- The tapeworms that parasitize ruminants are Moniezia expansa and Moniezia benedeni, Avitellina and Thysaniezia . All have indirect life cycles that involve an arthropod –usually one of the oribatids (soil mites) or a psocid (book louse).
- Calicophoron is the only trematode of veterinary importance, as it causes quite severe disease of the small intestine. It has an indirect life cycle and freshwater snails of the genus Bulinus are the intermediate hosts.
Epidemiology and distribution
The helminths occurring in the small intestine occur worldwide, wherever ruminants are present or are kept –with the possible exception of North America.
A large variety of ruminants are the hosts of the various genera of intestinal helminths. This includes the domesticated ones and a number of wild ruminants and hippopotami.
The trichostrongylids (Trichostrongylus, Cooperia, Nematodirus) and the hookworms (Bunostomum and Gaigeria) have direct life cycles, and transmission is thus per os in the former and either per os or percutaneous in the latter. Strongyloides has a homogonic and a heterogonic life cycle, and infects either percutaneously or through the milk –while Toxocara is transmitted mainly through the milk. Calicophoron has an indirect life cycle ( see “rumen ”) and infects per os, as do the tapeworms which utilise oribatid mites or psocid insects as intermediate hosts.
The socio-economic impact of the helminths of the small intestine of ruminants is severe. This is not only in terms of direct losses through death of the animals, but also through the erosive diseases caused by Trichostrongylus species in sheep and Strongyloides in goats –hence the colloquial names "bankrupt ’’and “white bankrupt worms" respectively. Treatment is expensive and few farmers can afford it, which adds to the impact that these worms have.
The larval stages of the trichostrongylids and Strongyloides appear to be the most pathogenic, and, with minor differences, all cause an enteritis, diarrhoea, dehydration, and eventually death with heavy infections. The L3 of Trichostrongylus species burrow underneath the mucosa of the duodenum and the first 6 or 7 m of the jejunum. When these tunnels rupture to release the young adult worms, there is oedema and haemorrhage and a loss of plasma proteins. The Cooperia species have a similar pathogenesis. The L4 and fifth stages of Nematodirus severely damage the villi of especially the ileum –and this leads to villous atrophy and erosion of the mucosa. The larvae of Strongyloides cause erythematous lesions where they penetrate the skin and petechiae in the lungs, and the adults produce a catarrhal enteritis of the duodenum and anterior jejunum. The hookworm larvae cause skin lesions on penetrations and anaemia; hypoalbuminaemia and occasionally diarrhoea are caused by the adults. Initial infection causes swelling at the site of skin penetration and within 24 hours the formation of small isolated scabs. Repeated infections cause severe swelling that may persist for several days. The large mouths of the adults that cut the intestinal villi at their bases, cause intestinal lesions. The crypts of Lieberk ühn and the lamina propria are infiltrated by large numbers of eosinophils, monocytes and lymphocytes. Exposed, haemorrhaging ulcers remain when the worms move to a new feeding site. Anaemia develops gradually and haemoglobin levels drop to as low as 0.35 g/l. The anaemia is of the progressive aplastic type –with no regenerative changes occurring in circulating red cells. The young Calicophoron in the small intestine are “plug feeders ”(Urquhart et al., 1993), which causes erosions on the mucosa.
In heavy infections, enteritis characterised by oedema, haemorrhage and ulceration occurs.
The tapeworms are considered to be nonpathogenic, and even in heavy infections there is little damage to the intestine. They do, however, cause unthriftiness by competing with the host for available nutrients, and may cause the deaths of young lambs and malnourished pregnant sheep.
In acute cases of trichostrongylosis the carcass is emaciated and there is atrophy of the fatty tissues. The intestines show catarrhal inflammation with numerous small petechiae in the first few metres of the small intestine. The intestinal walls are thickened and the mesenteric lymph nodes are enlarged. Adult parasites are found beneath the greyish white film that covers the mucosa, but their presence can only be determined by examining a scraping of the mucosa against the light. Changes such as fluid accumulations in the serous cavities, ruminal atony and food retention in the rumen and abomasum, dry ingesta, and distension of the small intestine by fluid may also occur. Carcasses from chronic cases are markedly emaciated, and there is muscular and myocardial atrophy. Mucous membranes are generally pale and the intestinal walls may be thickened.
In nematodirosis the carcass has a dehydrated appearance, and there is loss of the intestinal villi and necrosis of the lamina propria. It is seldom seen in cattle –because they are rarely infected.
In strongyloidosis the carcass is emaciated and wet, and most of the skeletal muscles are atrophied. There are serous effusions in the body cavities and widespread serous atrophy of fat. Intestines are red and the mucosa is lacking in severe infections. The worms can sometimes be seen clumped together and they resemble pieces of cotton wool.
Bunostomum causes emaciation, and bleeding ulcers occur in the mucosa of the small intestines of sheep. In cattle, a typical anaemic carcass with pale mucous membranes and watery blood, is seen. Lesions are present in the mucosa, but free blood in the lumen is seldom seen. The haemopoietic tissues may show signs of compensation –i.e. metaplasia to red bone marrow. Young animals show skin lesions due to larval penetration. Gaigeria causes the same lesions as Bunostomum species.
Cooperia is more of a problem in cattle –in which necrotic enteritis with parasites penetrating the mucosa, haemorrhages in the first 3 m of the small intestine, and catarrhal exudate in the posterior half of the small intestine, are seen on necropsy.
The carcass of a Calicophoron -infected animal is emaciated, dehydrated and there is severe fibrino-catarrhal inflammation of the small intestine, and occasionally the abomasum. Large numbers of small, immature flukes can be found on the mucosa. Ulceration and haemorrhage of the small intestinal mucosa is also evident.
The clinical signs caused by any one of the Trichostrongylus species appear in acute and chronic forms. The acute disease develops when approximately 250 000 infective larvae are ingested. Pain caused by the parasite causes anorexia, closure of the pyloric sphincter, and retention of food in the abomasum and rumen. Sheep become listless, signs of submandibular oedema develop, and there is a yellow foetid diarrhoea. Sheep die 16 to 17 days after infection. Death is due to the combined effects of starvation, liver impairment, circulatory failure, and pulmonary oedema. Acute disease is rarely seen.
The chronic disease is more commonly seen and develops when about 100 000 larvae are ingested. Anorexia gets progressively worse, with concomitant loss of body mass. Anaemia is caused by a lack of available protein to form haemoglobin. The overall result is emaciation, atrophy of muscles, hydrothorax, hydropericardium and ascites. The clinical signs may be aggravated by poor grazing –especially during winter. Dorper sheep seem to be more susceptible to trichostrongylosis and develop a slight transient bottle jaw. Faeces become putty-like –but not fluid –and animals become weak and listless. Mucous membranes become pale. Merino sheep show slightly pale mucous membranes and putty-like faeces. On lush green pastures, the sheep may have a dark diarrhoea.
The clinical signs in Nematodirus infection are depression, listlessness, anorexia, fluid faeces and death 10 to 14 days after infection. The clinical signs are caused by the L4 rather than by the adults. Animals with a severe infestation of Cooperia species –i.e. those receiving 300 000 larvae within 10 days –have a fluid foetid diarrhoea, selective anorexia, bottle jaw and eventually death resulting from starvation, dehydration and exhaustion.
Like most helminths infecting percutaneously, Strongyloides larvae cause marked urticaria at the site of infection. In goats, adult worms cause anorexia, diarrhoea or constipation, sunken eyes with a purulent discharge, a frothy mucous discharge from the nose, muscle atrophy, and paresis just before death.
Bunostomum causes itching of the skin –particularly that of the limbs (often accompanied by foot-stamping) –and wet eczema. Rapid mass loss occurs, with emaciation, anaemia, submandibular oedema and constipation followed by diarrhoea, with the faeces being foetid and tarry. Animals lie down for a few days before they die. A massive dose (4 000 larvae) can kill adult sheep or young calves without any ante mortal clinical signs. However, more commonly, as few as 200 to 300 adults can produce severe anaemia –causing a fall in the haematocrit levels as well as hypoalbuminaemia.
Gaigeria is a voracious bloodsucker in sheep, and severe anaemia that develops over a period of about 13 weeks is seen together with emaciation, weakness, and loss of weight and appetite. It is usually fatal in under-nourished animals.
Unthriftiness and intermittent diarrhoea are the only clinical signs seen in Toxocara infections –and then only in calves less than 6 months old.
Calicophoron immatures cause anorexia, foetid diarrhoea, mass loss and occasionally bottle jaw. In severe cases death occurs 5 to 9 days after the onset of diarrhoea. Sheep are very susceptible, show severe clinical signs, and quickly die of amphistomosis –whereas cattle rapidly develop a good immunity.
Both Moniezia benedeni and M. expansa tend to occur only in young animals, and a good immunity develops after the first infection. They do not cause significant clinical effects –even with large worm burdens. However, clinical signs may include unthriftiness, diarrhoea, respiratory signs and even convulsions –but then only with massive burdens. Thysaniezia giardi and Avitellina are considered to be apathogenic.
See “abomasal worms ”for general principles of diagnosis, including autopsy and egg detection. Several of the eggs can be identified to genus level, but the eggs of the trichostrongylids and hookworms are difficult to distinguish from one another.
Differential diagnoses for intestinal helminthoses includes such conditions as poisoning with certain plants or metals, malnutrition, and –in the case of the hookworms Bunostomum and Gaigeria –causes of anaemia like fasciolosis or haemonchosis.
Control of nematodes
The anthelmintic selected must be suitable for the endoparasites on the farm. Although no resistance has been detected so far in intestinal nematodes, good basic practice should be implemented as in the discussion under the control of abomasal worms in small stock.
Control of cestodes
Although considered apathogenic, in practice heavy burdens of Moniezia have been shown to cause mortalities in calves, lambs, and pregnant ewes on dry lands. This can be prevented by strategic dosing of ewes on old lands and of young ruminants when they begin to graze. There is anecdotal evidence of niclosamide resistance in the field, and in such cases suitable alternatives like praziquantel can be used.
Few helminths utilise the large intestine, but those that do are often severely pathogenic. Nematodes that occur here are Oesophagostomum species, Chabertia ovina, and the Trichuris species. Trematodes and cestodes are not, as a rule, found in the large intestine of ruminants.
Large-mouthed bowel worm
AdultOesophagostomum are also known as nodular worm and occur in the caecum and colon, while immature stages are found in nodules in the wall of the small and large intestines. They are present in ruminants in the tropical and subtropical regions of the world. The life cycle of Oesophagostomum columbianum of sheep and goats, and Oesophagostomum radiatum of cattle, is direct. The developmental period of the former is 35 to 39 days for the first infection, increasing to 46 to 47 days to many months for subsequent infections. The developmental period of Oesophagostomum radiatum is 32 to 34 days. Wet, warm weather, overgrazed camps or unhygienic kraals and pens will predispose calves and they can be expected to show clinical signs. A third species, Oesophagostomum venulosum , seems to be of lesser importance in sheep and goats. Chabertia ovina is the largemouthed bowel worm of sheep, goats and rarely cattle, and also occurs in some antelope species. Their habitat is the colon and they are found wherever sheep are kept and the climate is suitable. The life cycle is direct and the developmental perio d is 49 days or more. The whipworms (Trichuris species) are named for their long, thin anterior end and a short, thicker posterior. They are found in the caecum and colon. The eggs are lemon-shaped and have a plug at each end.
Epidemiology and distribution
Oesophagostomum columbianum is present in the summer rainfall areas, where rainfall is in excess of 360 mm per annum. It is absent in the semi-arid, non-seasonal and winter rainfall areas.
Oesophagostomum radiatum does not occur in the arid, non-seasonal and winter rainfall areas. In semi-arid areas, it is found in modest numbers in calves in May. In the summer rainfall areas, calves are infested throughout the year, with burdens rising to a peak in August and declining in spring. Irrigated pastures are an unsuitable habitat for this parasite.
Chabertia ovina is confined to winter- and non-seasonal rainfall areas, and is present throughout the year in moderate numbers. Trichuris species occur throughout the world –wherever ruminants, domesticated animals and wildlife are present.
Ruminants are the main hosts of Oesophagostomum species, although there are about nine other species that occur in domestic pigs, warthogs and bushpigs. These species are not transmissible to ruminants. Chabertia is only known in sheep, and Trichuris species are present in ruminants, carnivores, suids, and even in humans. Wild antelope are often the reservoir host for the nodular worms and whipworms of domesticated ruminants.
The life cycle of all the worms of the large intestine is direct, and infection takes place per os. The free-living stages of Oesophagostomum species are susceptible to desiccation and require hot, moist conditions for optimal development to the infective stages. The species are present in the summer rainfall areas where rainfall exceeds 360 mm per annum. They are absent in the semi-arid, non-seasonal and winter rainfall areas. Sheep quickly expel the worms on improved pastures, and the parasite is absent on irrigated pastures. Trichuris also has a direct life cycle, but in this case the eggs contain the infective L1 and can survive for years in dry pellets. The eggs are also resistant to desiccation and survive temperatures of - 20 °C to 50 °C.
The socio-economic impact of the helminths of the large intestine of ruminants is severe –not only in direct losses through death of the animals, but also through the erosive disease caused by Trichuris species in sheep and O. radiatum in cattle. Treatment is expensive and few farmers are able to afford it, which further adds to the impact that these worms have.
Anorexia is the most important finding with ovine and caprine oesophagostomosis. It is caused by the intestinal discomfort starting with the larval migration to the intestinal lumen –and persists until death or recovery. A mild mucoid to projectile foetid diarrhoea sets in, and this may lead to intussusception. Death caused by starvation, dehydration and exhaustion may occur from days 18 to 22. Calves pass blood from as early day 16. This becomes more severe from the 19th and 20th day as the worms moult (M4). Like lambs and kids, calves die of dehydration and exhaustion, or recover from the 10th week onwards.
Chabertia browse on the mucosa causing haemorrhage from the 4th week onwards –and faeces become blood-flecked. Larval stages of Trichuris cause haemorrhage and local oedema when they penetrate the intestinal wall. These injuries are considered to predispose to the development of secondary bacterial infections. Unless they are present in large numbers, adult worms are not pathogenic.
In O. columbianum infections, thickened patches are noted on the intestinal mucosa and, as the larvae leave the mucosa, ecchymoses appear. Extensive nodule formation and thickening of the mucosa of the colon occurs –together with peritonitis and adhesions ( Figure 25 ). There may be a diphtheritic jejunitis, typhlitis and colitis –with numerous perforations and adhesions. At a later stage the nodules may calcify. Once the worms have reached patency, only nodules and a thickened intestinal wall with adhesions may be visible. The lesions caused by O. radiatum are similar to those of O. columbianum, but calcified nodules are rare and haemorrhage is a more common finding.
The mucosa of the caecum and colon of sheep infected with Chabertia contain haemorrhages and inflammatory areas which are produced by the adult worms. The adults cause extensive damage because they frequently move to new sites to feed. Only in heavy infections do the immature stages cause tissue damage –and then throughout the entire intestine from the pylorus to the ileocaecal valve.
Acute oesophagostomosis is seldom seen in sheep and then only in na ïve animals. It is caused by larvae that have not yet reached patency and is characterised by pain, a rise in temperature, diarrhoea and rapid dehydration. In the chronic disease food and water consumption decreases and then improves again. Diarrhoea starts from the 10th day onwards, and persists until death. The faeces vary in consistency –from putty-like to mucopurulent, green and foul smelling. Intussusception may occur. This form of oesophagostomosis used to be quite common, but, due to intensive treatment aimed mainly at Haemonchus contortus , it has become scarce.
In calves, pain, anorexia, loss in mass, hypoproteinaemia, anaemia and diarrhoea are seen. Submandibular oedema and progressive cachexia occur after 7 weeks. Chabertiosis manifests with weight loss, diarrhoea and faeces that may be flecked with blood.
Adult Trichuris worms are not pathogenic –unless present in large numbers when they may cause abdominal pains, mucoid diarrhoea, anaemia, loss of body mass, and, rarely, death.
Faecal nematode egg counts are of little value for a diagnosis of oesophagostomosis. Clinical signs –and the presence of nodules in the wall of the small intestine and colon –are diagnostic at necropsy of sheep; nodules are seldom seen in cattle. To make a diagnosis of chabertiosis, consider the clinical signs, the season and the area. Lesions in the intestines and the presence of small numbers of the worms are diagnostic. The eggs of Trichuris are diagnostic. As mentioned above, large numbers of the worms –and thus their eggs –must be present before a diagnosis can be made, as the worms are usually apathogenic.
Causes of diarrhoea such as coccidiosis and nutritional causes should be taken into account for Oesophagostomum and Trichuris species. For Chabertia , consider causes of anaemia like haemonchosis, trichostrongylosis, fasciolosis, coccidiosis and nutritional issues. Also consider causes of diarrhoea like other helminth infections, nutritional deficiencies, poisonings, and coccidiosis.
On commercial farms, where sheep are regularly drenched, oesophagostomosis should not be a problem. The drenching interval for Haemonchus is such that Oesophagostomum is exposed to the anthelmintic twice during its pre-patent period. Sheep also develop a local immunity against the larvae –mainly in the large intestine –and adult worms are expelled in subsequent infections.
Cattle in the field develop a strong immunity after 8 to 12 months of age. The immunity may cause a great reduction in the number of re-infesting larvae developing to adults during the normal pre-patent period. The immunity will persist if adult worms are removed by anthelmintics. Living Chabertia stimulate high levels of reaginic antibody, which is probably linked to cell-mediated immunity. It is almost impossible to control Trichuris in the environment and only in intensive situations where floors can be cleaned daily, is environmental control possible. No anthelmintic resistance is known for any of the worms in the large intestine. Select a suitable anthelmintic using the process discussed under the control of abomasal worms in small stock. Encourage “good practice ”by monitoring the effect of anthelmintics, ensuring refugia, and using environmental controls.
Apart from the trematodes that migrate through the liver on their way to their predilection sites, the larvae of Taenia hydatigena, Echinococcus granulosus, and Echinococcus multilocularis also cause significant damage. Various Schistosoma species may be found in the blood vessels of the liver. The pentastome genus Linguatula bores tunnels of about 1 mm in diameter in the parenchyma. Nematode larvae, mostly ascarids, may occasionally be found.
Ruminants are also the intermediate hosts for some tapeworms –of which Taenia hydatigena and Echinococcus granulosus are possibly the most commonly encountered in Africa. The pentastome genera Linguatula and Armillifer are also occasionally found, but their prevalence seems to be higher in wild animals. Eggs of Taenia are eaten with the food and the hexacanth larvae (oncospheres) hatch in the small intestine. These burrow through the wall of the intestine, and, depending on the species, are transported by the blood to the liver, lungs, heart, or striated muscles. In the case of T. hydatigena , the larvae migrate in the liver for about four weeks –before emerging and attaching to the peritoneum. Here they develop to cysticerci up to 8 cm in diameter –the socalled Cysticercus tenuicollis ( Figures 27 and 28 ). The life cycle of E. granulosus is similar. Oncospheres are carried to the liver by the blood or to the lungs by the lymph –the two commonest sites for development –where they form hydatid cysts ( Figure 26 ). The eggs of the pentastomes are also ingested and the primary larvae hatch in the small intestine. In the case of Linguatula , the larvae moult several times to form infective nymphs that keep migrating through the body, and these are often found free in the liver or heart.
Cysticercosis is common throughout the world wherever sheep and goats occur, and wherever the cestode Taenia hydatigena is present. Somalia, Sudan, Uganda, Kenya, Nigeria and the Ivory Coast have a prevalence of more than 10% of cystic echinococcosis in domestic stock. In Ethiopia, the Central African Republic, Tanzania, Madagascar, Mozambique, Zambia and South Africa, the prevalence is 1 to 10%, and in Malawi, Namibia, Botswana, Zimbabwe, Angola and the Democratic Republic of the Congo it is less that 1%. It has not been recorded from Benin and Gabon (FAO, 1993). Pentastomes are widely spread but do not occur in large numbers, and are therefore seldom encountered.
The definitive hosts of Taenia hydatigena are domestic dogs and other canids and the intermediate hosts are primarily sheep and goats –although cattle and camels are infected on occasion. The definitive hosts of Echinococcus granulosus are domestic dogs and cats and a variety of wild carnivores, e.g. coyote, dingo, wolf, Cape hunting dog, and other canids. The list of intermediate hosts comprises ruminants –including camels, suids, horses, and rodents. Humans are accidental, but entirely suitable, intermediate hosts. The pentastome genera Linguatula and Armillifer use ruminants as an intermediate host. As a final host, Linguatula parasitises the nasal sinuses and respiratory passages of carnivores, while Armillifer is a parasite of the lungs of snakes.
In all cases, the acquisition of larval cestodes occurring in the liver is through ingestion of eggs by the intermediate host. Eggs are dispersed in the environment by various agents –notably insects and rain. Adult worms develop after ingestion of the metacestodes by the final host, and in the case of the pentastomes, the infective nymph.
The socio-economic influence of cysticercosis is considerable. Few animals die as a result of acute infection, but chronic infection leads to condemnation of the liver. The cysticerci on the outside of the liver are often just trimmed away and fed to dogs, which further compounds the problem. Cystic echinococcosis has a severe influence on those populations –human or animal –where it occurs, and cost is only one of them. Cost can be categorised as the cost due to the disease in humans (e.g. medical and non-medical costs, lost productivity), the cost due to the disease in animals (e.g. condemnation of edible organs, destruction of rejected organs, reduced yield of milk, meat, wool and hides, and reduced number of viable offspring), and the cost of control programmes (e.g. personnel, equipment, travel, surveillance, education, drugs and destruction of animals). Humans are occasionally infected with pentastomes –but to what extent, is unknown.
In sheep and goats the hexacanth larvae occasionally cause a severe hepatitis during the four weeks they migrate through and grow in the liver. This resembles acute fasciolosis, and death occurs due to haemorrhage into the abdominal cavity. Once they have attained a certain size, they leave that organ and attach to the peritoneum –usually close to the liver. After another four weeks they have become large, flabby structures –Cysticercus tenuicollis –which are filled with fluid through which the protoscoleces can easily be seen ( Figure 27 ). Hydatids in the liver and lungs are well tolerated and most infections are discovered at necropsy. Where the oncospheres have been carried in the blood to other organs, a variety of clinical signs may present, depending on the organ in which the oncospheres lodged. Pentastomes are also well tolerated, and even with heavy infections there is little haemorrhage into the abdominal cavity.
In most cases infection with cestode or pentastome larvae goes unnoticed and is detected only at meat inspection or necropsy. Infrequently, however, large numbers of developing cysticerci migrate in the liver, causing hepatitis cysticercosa. This is a condition that is similar to acute fasciolosis and is often fatal (refer to pathogenesis and pathology). Once the cysticerci have developed, there are no clinical signs. Cystic echinococcosis refers to an infection with hydatid cysts, and is a common occurrence in Africa. As a clinical entity, it is rarely suspected –but is frequently diagnosed at necropsy. Pentastomes often encapsulate in the liver or peritoneum of ruminant intermediate hosts, but no clinical signs have been ascribed to them.
Acute hepatitis cysticercosa in sheep is characterised by an enlarged liver in the parenchyma in which numerous migration tracts are seen. The surface of particularly the ventral lobe is covered with a fibrinous exudate. Subcapsular haemorrhages are common, and these may rupture so that blood is found in the abdominal cavity. Acute hepatitis cysticercosa is seldom seen in cattle. Depending on the number of oncospheres invading, there may or may not be significant damage. In the former case, it will resemble chronic fasciolosis and the large cysticerci can be seen on the peritoneum or close to the gall bladder. In the case of cystic hydatidosis, the lesions are associated with pressure –which in the different organs (i.e. liver, lungs, long bones and others) may cause different clinical signs and gross pathological lesions.
Acute hepatitis cysticercosa resembles acute fasciolosis –in its sudden onset and rapid death. Chronic cysticercosis is usually only diagnosed at the abattoir or at necropsy, as is infection with pentastomes.
Cystic echinococcosis in humans can be diagnosed by various imaging techniques, e.g. X-ray, ultrasound, CT scan or magnetic resonance, or by serological methods –of which a whole battery is available. Commonly used methods are ELISA tests, immuno-electrophoresis and complement fixation. In animals the diagnosis of cystic echinococcosis is seldom called for, and is usually only diagnosed at the abattoir or at necropsy. The diagnosis of infection in dogs is difficult because of the small size of the tapeworm and few proglottids are shed. In some countries a purgative like arecoline hydrochloride is administered –which results in the expulsion of the entire tapeworm.
Differential diagnoses for acute deaths from acute hepatitis cysticercosa would include acute fasciolosis.
Cysticercosis and cystic hydatidosis are both relatively easy to control, but the lack of knowledge in many parts of Africa still makes for large numbers of infected animals and humans. Firstly, dogs should never be fed uncooked offal –this may contain the cysticerci or hydatid cysts. Secondly, humans should wash their hands thoroughly before eating or drinking, especially if they have been playing with dogs or gardening. Thirdly, where possible, dogs should be dewormed using praziquantel and the faeces disposed of so that the tapeworm eggs cannot contaminate the pastures where ruminants graze. Fourthly, where dogs are found positive for Echinococcus , contamination of vegetables and water is possible, and therefore everything, including the water, should be boiled before consumption. It is not possible to control the pentastomes, since the final hosts are either wild carnivores or snakes.
Although many helminths pass through the liver during their development in their respective hosts, few adult parasites occur here. The major trematode genera are Fasciola, Fascioloides, and Dicrocoelium. Eurytrema occurs mainly in the pancreatic duct, and more rarely in the bile ducts. The only adult cestode found here is Stilesia hepatica. Apart from the trematodes that migrate through the liver on their way to their predilection sites, the larvae of Taenia hydatigena, Echinococcus granulosus and Echinococcus multilocularis also cause significant damage. Various Schistosoma species may be found in the blood vessels of the liver. The pentastome genus Linguatula bores tunnels of about 1 mm in diameter in the parenchyma. Nematode larvae –mostly ascarids –may occasionally be found.
The trematodes have indirect life cycles involving either a terrestrial or an aquatic snail –and in some genera an arthropod intermediate host. The Fasciola life cycle starts with an egg that contains a miracidium ( Figure 30 ) and which must fall in a wet or damp area in order to release the miracidium ( Figure 29 ). The miracidium must enter a suitable snail within three hours of hatching from the egg. In the snail, development proceeds through the sporocyst and redial stages to cercariae that are the final stage of development in the intermediate host. The motile cercariae are shed, and attach to any solid object in the water like vegetation, dead leaves and even twigs and dead insects –where they encyst to the metacercariae. The latter are infective for the final host. Once ingested by the final host, the metacercariae excyst in the small intestine, pass through the intestinal wall, cross the abdominal cavity, and then penetrate the liver. The young flukes tunnel through the parenchyma and enter the small bile ducts after 6 to 8 weeks. They migrate to the larger bile ducts where they develop to adults ( Figure 31 ). The prepatent period of F. hepatica varies from 8 to 13 weeks or 10 to 12 weeks, and that of F. gigantica from 11 to 16 weeks.
The life cycle of Dicrocoelium is different in that a second intermediate host is utilised. The egg –which contains a miracidium –must be eaten by a terrestrial snail in order to hatch. Two generations of sporocysts develop, which then produce cercariae, but there are no rediae. The cercariae are extruded in masses cemented together with mucus. The slime balls of cercariae are ingested by an ant of the genus Formica (D. dendriticum) or Campanotus (D. hospes) in which they develop to metacercariae –usually in the haemocoel, but occasionally in the brain of the ant. Those ants with metacercariae in the brain show aberrant behaviour and climb to the top of vegetation and remain there even after “normal ”ants have returned to their nest. This presumably increases the possibility that infected ants will be eaten by the final host. The metacercariae excyst in the small intestine and the young flukes migrate up the main bile duct into the smaller ones, where they attain sexual maturity. The pre-patent period is 10 to 12 weeks.
The life cycle of Eurytrema is similar, in that a terrestrial snail is the first intermediate host and a tree cricket or grasshopper the second. The metacercariae hatch in the small intestine and enter the pancreatic duct; occasionally the main bile duct is entered and the flukes are found in the smaller bile ducts in the liver. Stilesia hepatica are shed with the faeces, and a soil mite –probably of the family Oribateidae –is used as an intermediate host. A cysticercoid develops in the mite and the mite must be eaten by the final host for the life cycle to continue. In the final host, the cysticercoid evaginates its scolex and moves to the opening of the common bile duct, through which it enters to lodge in the very small bile ducts.
In Africa, the major helminths infecting the liver are the trematodes Fasciola hepatica , Fasciola gigantica and Dicrocoelium hospes . In Europe and North America Fascioloides magna is fairly common, while Dicrocoelium dendriticum is widespread. The genus Eurytrema occurs in Brazil and Asia. The small cestode Stilesia hepatica occurs worldwide; it is also common in ruminants in Africa, except cattle. A prerequisite, which ultimately determines the distribution of the trematodes, is the presence of suitable snail intermediate hosts for the trematodes, and a suitable arthropod for Stilesia. The snails can be terrestrial (Eurytrema, Dicrocoelium) or aquatic (Fasciola, Fascioloides) , and, in some cases, a second intermediate host –usually an arthropod –is required. Stilesia requires one of the soil mites, probably of the family Oribateidae.
The main hosts of trematodes and the cestode are ruminants. Sheep, goats, cattle and a variety of wild ruminants are affected, but often not to the same degree. Dicrocoelium is present in rabbits and in ruminants, and Stilesia is rare in cattle.
In all cases the transmission of helminths parasitising the liver is through ingestion of metacercariae (the trematodes) or cysticercoids (Stilesia) that occur either on vegetation or in an intermediate host. The epidemiology of the snails is also important for the transmission of the parasites. Some snails are aquatic, others are semi-aquatic, and suitable habitats must be present. The aquatic snail Lymnaea truncatula prefers wet mud to free water, and temporary habitats like hoof marks and rain ponds that develop after heavy rain or excessive irrigation, are colonised. Temperatures in excess of 15 ºC are required for the multiplication of both the snails and the developing stages of the parasite in the snails ( Figure 35 ). During winter, the snails hibernate and the development of the fluke larvae is halted. Development resumes when temperatures rise and metacercariae are available during spring. There is some evidence that the prevalence of fasciolosis in warm countries is higher after several months of drought –possibly because animals congregate around watering places, so increasing the chances of snails becoming infected. Rainfall should exceed the transpiration rate of the vegetation in order for the eggs to develop, the miracidia to find the snails, and the cercariae to disperse after having left the snails.
The socio-economic influence of trematode infection of the liver –and, in particular, fasciolosis –can be considerable. Many animals die as a result of infection, and in developing countries this has a major impact on the cash flow and economics of a region. During the acute phase of infection, the immature flukes burrow through the parenchyma and their rapid growth during this period causes substantial damage –especially just before they enter the bile ducts. Depending on the number of flukes present, this causes severe haemorrhage and often the death of the animal. Similarly, the fibrosis in the parenchyma and thickened bile ducts seen in chronic cases lead to condemnation of the liver, which is a further economic loss. It is estimated that 37% of sheep livers are condemned in South Africa because of Stilesia infection. Worldwide, the estimated loss due to fasciolosis is US$2 billion.
Humans are occasionally infected with liver fluke, but it seems to be under-reported in the literature. Recent estimates, based on serodiagnosis, indicate that as many as 17 million people in the world suffer from fasciolosis. In humans, clinical manifestations appear early in the infection, long before parasitologic diagnosis is possible, and the symptoms and clinical signs are as severe as they are in ruminants.
The pathogenesis of fasciolosis depends on the host species, the stage of the infection, and the number of infecting flukes. In field situations, animals acquire infections over an extended period, so that flukes of all developmental stages are in the liver. This results in clinical signs of both acute and chronic disease. The passage of the young Fasciola species through the intestinal wall into the peritoneal cavity causes little damage, and the changes that do occur are mostly localized and transient. Once in the liver the young flukes burrow through the parenchyma creating tracks or tunnels, and this is the acute stage. Blood vessels and small bile ducts are damaged –resulting in haemorrhage, thrombosis and disruption of the flow of bile. During their migration, the young flukes feed on hepatic cells and blood, and also secrete proteolytic enzymes. They grow rapidly, causing even more damage, especially during the period just before they enter the bile ducts. Haemorrhage may become severe in the late acute stage, and may cause the death of the host either through haemorrhage into the abdominal cavity or beneath the capsule of the liver ( Figure 32 and 34) . If the host survives, hepatic fibrosis and hyperplastic cholangitis develop. The chronic stage develops slowly and is the result of the presence of the fluke in the bile ducts, where they become sexually mature. Chronic fasciolosis is a combination of cholangitis, biliary obstruction, destruction of hepatic tissue, and the release of a haemolytic substance by the fluke.
The tracts in the parenchyma heal and connective tissue forms in and between tracts. Foci of coagulative necrosis form parallel and adjacent to the healing tracts –which, in turn, also eventually heal by fibrosis ( Figure 33 ). A peri-biliary fibrosis occurs throughout the liver, even around the small bile ducts where there are no flukes. Lastly, monolobular fibrosis develops and the portal canals become linked together by fibrous tissue. In addition, there are changes in the blood supply to the liver. The inlet venules that arise from the portal vein are occluded, and this causes disruption, degeneration and necrosis of the hepatic limiting plate. Bile-duct proliferation occurs with accompanying fibrosis around the portal canals that surround the hepatocytes and small bile ducts. Eventually, phlebitis of the portal vein develops, which leads to oedema and fibrosis, and the occlusion of the vein. Adult Fasciola in the bile ducts cause erosion and necrosis of the biliary mucosa and intense inflammation of the adjacent lamina propria. These changes, however, are less important than the anaemia caused by the adult flukes –which will eventually lead to an iron deficiency. Migration of young Fasciola, and in some areas Dicrocoelium , through a liver that contains spores of Clostridium novyi type B may cause infectious necrotic hepatitis (black disease) to develop in sheep and cattle. Dicrocoelium dendriticum and D. hospes are of low pathogenicity –depending on the number of flukes infecting. In heavy infections, there is a lymphocytic infiltrate around larger bile ducts, which is sometimes accompanied by fibroblastic proliferation around portal ducts, veins and arteries. There is slight hyperplasia of the bile ducts that continues as the infection progresses.
Eurytrema pancreaticum rarely invades the bile ducts of cattle, and its pathogenesis is unknown.
Fascioloides magna is a large, broad fluke that causes little harm in the Cervidae, its natural host. Early infections involve portal areas with extensive zones of fibrosis and an extremely pronounced influx of eosinophils. The flukes encyst rapidly once in the liver parenchyma, and the cyst expands as the fluke grows in size. However, the fibrosis is such that the afferent and efferent bile ducts still have access to the cyst cavity –thereby allowing the fluke eggs to be released into the intestine. In cattle, and in heavy infections in deer, the marked tissue reaction to the fluke produces large fibrous cysts up to 40 mm in diameter. The worms are contained in the cyst, which is completely occluded. Eggs are therefore not found in cattle. The cyst and tissues adjacent to it are black due to extensive pigmentation. The pigment is a haeme compound, which is believed to be produced by the fluke.
Sheep and goats show little host reaction to the flukes, and cysts do not form. This indicates that sheep are not natural hosts. The flukes continue migrating through the parenchyma, destroying it in the process, and leaving black, tortuous tracts. The presence of this fluke in certain areas has made it impossible to farm with sheep.
Acute fasciolosis occurs when animals consume 2000 or more metacercariae –and manifests as dullness, weakness, lack of appetite, pallor and oedema of the mucosae and conjunctivae, and also pain when pressure is applied over the area of the liver. Deaths occur quickly, often in less than 48 hours, and may be accompanied by blood-stained discharges from the nostrils and anus. Outbreaks are more common in young sheep and are of short duration; most deaths occur within 2 to 3 weeks. Fluke eggs are not found in the faeces.
Subacute fasciolosis results when animals ingest 500 to 1500 metacercariae over an extended period. Some flukes have already reached the bile ducts, where they cause cholangitis. Others are still migrating in the parenchyma where they cause less severe, but similar lesions as are seen in the acute disease. Sheep show clinical signs for 1 to 2 weeks prior to death. There is rapid loss of condition, pallor of the mucous membranes, and an enlarged and palpable liver. Chronic fasciolosis manifests as gradual wasting, severe anaemia with ascites, oedema, bottle jaw, and very high fluke egg counts. Sheep have diarrhoea and shed their wool. The course of the disease is often as long as 2 to 3 months in those animals that die, but many survive and remain emaciated for long periods.
Although acute and subacute clinical disease occasionally occur in heavy infections –especially in calves –the chronic form is, by far, the one most often encountered in cattle. Aberrant migration is more common and flukes are often seen in the lungs. With heavy burdens there is anaemia and bottle jaw, but with smaller burdens the clinical signs are minimal. Diarrhoea is not a feature of fasciolosis in cattle.
The large liver fluke, Fascioloides magna, wanders through the liver parenchyma of cattle for a short while, whereafter it is encapsulated and does little harm. However, in sheep it never gets encapsulated and keeps on wandering through the liver parenchyma –causing severe clinical signs and death.
Infection with Dicrocoelium is usually chronic. The clinical signs are similar to those produced by Fasciola, but are much milder since the flukes do not destroy the liver parenchyma to the same extent. Because of their small size, Dicrocoelium may be found in the smaller bile ducts.
Stilesia is not known to produce clinical signs.
An enlarged liver –in the parenchyma of which numerous migration tracts are seen –characterises acute fasciolosis in sheep. The surface of particularly the ventral lobe is covered with a fibrinous exudate. Subcapsular haemorrhages are common, and these may rupture so that blood is found in the abdominal cavity.
Acute fasciolosis is seldom seen in cattle. The lesions of subacute fasciolosis are similar to those of acute fasciolosis, but rupture of subcapsular haemorrhages is rare; this form of the disease is seldom seen in cattle.
With chronic fasciolosis, the liver has an irregular outline, and is firm and pale. The ventral lobe is most affected and is smaller. Hepatic fibrosis and hyperplastic cholangitis are commonly seen. Several types of fibrosis are present. Post-necrotic scarring is associated with the healing of migration tracts. Ischaemic fibrosis is a sequel of infarction caused by damage to and thrombosis of large vessels. Peribiliary fibrosis develops when the young flukes reach the small bile ducts and monolobular fibrosis develops –which can be seen as white strands of fibrous tissue demarcating the hepatic lobule. Chronic fasciolosis is often seen in cattle. The pathology is essentially the same as that in sheep. In addition, the bile ducts tend to calcify and the gall bladder becomes enlarged. Aberrant migration of the flukes is more common in cattle, and encapsulated parasites may be found in the lungs.
The lesions caused by both acute and chronic Fascioloides infection in cattle are milder than those of Fasciola . In sheep, lesions are severe, as the flukes are large, and, as they never encyst as in cattle and deer, they destroy the liver parenchyma. The lesions are also discussed in the section on pathogenesis.
Dicrocoelium does not –as a rule –cause serious lesions to the liver, even though a few thousand may be present. In heavier infections, fibrosis of the smaller bile ducts and extensive cirrhosis can occur. Sometimes the bile ducts become markedly distended.
Although large numbers of Stilesia can often be found in the bile ducts, they cause neither clinical signs nor significant pathology.
Acute fasciolosis occurs when the flukes are still migrating, and eggs will therefore not be found. Animals often die before any clinical signs are apparent, and those surviving will be severely anaemic (refer to clinical signs for more diagnostic features).
A diagnosis of chronic fasciolosis is made by examining the faeces for eggs. The eggs of F. gigantica are larger than those of F. hepatica –but both have a golden colour imparted by the bile. Liver function tests –particularly GLDH (glutamate dehydrogenase) and GGT (gamma glutamyl transpeptidase) –can give an indication of liver damage, which may be due to fasciolosis. Antibodies of the flukes may be detected in serum or milk with an ELISA (enzyme-linked immunosorbent assay) test and the passive haemagglutination test may also be used.
Differential diagnoses for acute deaths from fasciolosis would include acute hepatitis cysticercosa, acute haemonchosis, anthrax, enterotoxaemia, infectious necrotic hepatitis or black disease (Clostridium novyi) –and for chronic cases Senecio and other hepatotoxic plant poisonings and chronic haemonchosis.
Environmental control and reducing exposure: Decreasing exposure to liver fluke and reducing pasture contamination are critical for limiting liver fluke infestations. This can be done by reducing snail populations through drainage of water-logged areas to eliminate snail habitats. Draining is the best long-term method for managing aquatic snail habitats but may not be feasible due to cost implications. Waterlogged areas can also be fenced off, which prevents animals from grazing in liver fluke-infested pastures during high risk times of the year when the snails are active. Animals should ideally be withheld from high risk pastures during times of peak snail activity ( see Figure 35 ). Vegetation at the edges of standing water can be cut away to make the environment less suitable for snails.
It is important to fix leaking water troughs, as water that accumulates around them provides an ideal environment for aquatic snails to thrive –so increasing the risk of exposure to liver flukes.
Anthelmintics used at carefully chosen periods will lower the number of flukes present in the host, thus reducing pasture contamination. Animals newly introduced into a farm should be quarantined and dewormed with a product which is effective against immature and adult flukes in order to avoid introduction of flukes into uninfected farms.
Strategic control: Strategic control is best applied during late winter (early spring) and autumn (April/May).
Strategic treatment during late winter –when the intermediate host is inactive –is aimed at killing adult flukes present in the liver. The aim is to prevent infection of the intermediate host during the ensuing spring. Animals can be dosed with products containing closantel, nitroxynil, rafoxanide, oxyclozanide or triclabendazole.
Strategic treatment in autumn (April/ May) is aimed at clearing animals of both immature and mature liver fluke stages before winter. The active of choice for strategic treatment in autumn is triclabendazole which should be given 2 weeks after the first frost has occurred or where the minimum temperature is maintained below 10 °C.
Tactical control: Tactical control is aimed at reducing clinical disease and production loss. It is implemented during periods when there is heavy infestation of the pastures. This is to manage the contamination of immature liver flukes in high risk areas when environmental conditions are optimal for the survival of aquatic snails. Treatment during these periods is critical in order to avoid liver damage caused by migration of immature flukes. It is advisable to use a product containing triclabendazole –which is highly effective against immature liver flukes from 2 weeks of age ( Figure 36 ).
Treatment: Acute and subacute disease due to immature flukes may occur from August to May the following year when aquatic snails are most active. Triclabendazole is the treatment of choice, as it removes all developing stages from 2 weeks of age. A single dose of triclabendazole should be given –after which the animals should be moved to a well drained, fluke-free pasture.
Subacute fasciolosis occurs when a large number of immature flukes are present in the liver, but the disease is not rapidly fatal. The parasites will have developed further –resulting in a portion of the population being present as adults in the bile ducts. Triclabendazole is the treatment of choice as it kills all stages of liver fluke present in the animal. However, rafoxanide, closantel or nitroxynil may also be used in cases of subacute fasciolosis. It must however be kept in mind that these actives are not effective against the early, immature, liver fluke stages.
It is also advisable –in cases of subacute fasciolosis –to move animals to flukefree, dry pastures following treatment. In cases where animals cannot be moved to clean camps the treatment should be repeated after 4-8 weeks, in order to eliminate maturing flukes.
Chronic fasciolosis is characterised by the presence of adult flukes in the bile ducts. Mature flukes can be successfully treated with products containing closantel, nitroxynil, rafoxanide, oxyclozanide or triclabendazole. Movement to dry, flukefree pastures is important, as any eggs being eliminated will not hatch given that the environment is unfavourable –thus preventing reinfection of treated animals and infection of snails in water-logged areas.
Several products are registered for the treatment of liver flukes ( Figure 36 ). Most flukicides available are effective against adult flukes, with variable activity against immature stages.
Clorsulon is a benzenesulfonamide and is effective against adult stages of F. hepatica , and may be used for the treatment of immature flukes older than 10 weeks. Clorsulon is also effective against Fasciola gigantica and Fascioloides magna . Clorsulon is commonly combined with ivermectin for simultaneous treatment of F. hepatica and nematode infections.
Oxyclozanide is a narrow-spectrum flukicide that belongs to the salicylanide group and is mostly used in livestock. It is effective against adult liver flukes (F. hepatica) from the age of 10 weeks. Oxyclozanide is the only flukicide registered for use in lactating cows, as it has a zero-day milk withdrawal.
Albendazole belongs to the benzimidazole group and is effective against adult liver flukes (Fasciola hepatica and Fascioloides magna) from 10 weeks of age.
Nitroxynil belongs to the nitrophenolic group and is highly effective against adult stages of liver fluke and can be used to treat immature flukes from 6 weeks of age. Nitroxynil is also effective against a few gastrointestinal round worms like Bunostomum spp., Oesophagostomum spp., Haemonchus spp. and Parafilaria bovicola .
Closantel is the most used of the salicylanilides and is highly effective for the treatment of adult liver flukes. It can also be used to treat immature flukes from 6 weeks of age.
Closantel is well absorbed from either parenteral or oral administration routes –in both sheep and cattle. Closantel is also effective against H. contortus and nasal bots (Oestrus ovis) in sheep and other adult nematodes like Oesophagostumum spp., Bunostomum spp. and Ostertagia spp. in cattle and sheep.
Rafoxanide is a halogenated salicylanilide. It has been used extensively against fasciolosis and haemonchosis in cattle and sheep, but its principal use is as an adulticide against F. hepatica and F. gigantica .
Rafoxanide may be used for the treatment of early immature liver flukes from the age of 4 weeks, but is only considered to be highly effective against immature flukes older than 6 weeks. It is also indicated for the treatment of . contortus and Bunostomum spp., as well as nasal bots (Oestrus ovis) in sheep.
Triclabendazole is an anthelmintic flukicide belonging to the benzimidazole group. It is highly effective against adult as well as immature stages. Triclabendazole is the only flukicide effective for the treatment of early immature liver fluke larvae from 2 weeks of age. Treatment of the early stages plays a critical role in preventing liver damage caused by migrating larvae.
The trematode helminths of the genera Schistosoma and Orientobilharzia occur in the cardiovascular system of ruminants. Several Schistosoma species –e.g. S. mattheei, S. margrebowiei, S. curassoni and S. leiperi –have been recorded from the mesenteric veins of cattle and sheep. More species occur in Asia, where domestic stock are the reservoir hosts for S. japonicum of humans. Four species of the related Orientobilharzia occur in livestock in Asia.
Two species of the nematode Elaeophora, E. sagitta and E. poeli occur in the coronary and pulmonary arteries of African buffalo, a number of tragelaphine antelope, and occasionally cattle (for illustrations see Helminths of game).
Table 5 Distribution of Schistosoma spp.
|Schistosoma bovis||Africa, the Middle East and southern Europe|
|Schistosoma japonicum||Far East|
|Schistosoma spindale||Asia and the Far East|
|Schistosoma incognitum||India and Pakistan|
|Schistosoma mansoni||Africa, South America and the Middle East|
|Schistosoma nasalis||India and Pakistan|
|Schistosoma (syn Orientobilharzia) turkestanica||Asia|
Bilharzia or schistosomosis
The Schistosoma species –also known as blood flukes –inhabit a wide variety of host species, including ruminants. The life cycle is heteroxenous, and freshwater snails of the genera Biomphalaria, Bulinus and Physopsis are of particular importance in the transmission to sheep and cattle. The male and female flukes live in permanent association –the female being carried in the gynaecophoric canal of the male ( Figure 37 ). She lays eggs in the mesenteric venules, and, aided by their spines and proteolytic enzymes secreted by the miracidia, the eggs work their way through several layers of tissue to end up in the lumen of the intestine. They are then voided and must reach water for the miracidia to hatch, a process that only takes minutes. The miracidia enter the snail, change into primary and secondary sporocysts and eventually cercariae. The cercariae are furcocercous (forked tails) ( Figure 38 ) and usually enter the host percutaneously. Upon entering the host, the cercariae lose their tails and transform to schistosomulae. There are no redial or metacercarial stages. The schistosomulae reach the lungs via the bloodstream, and after four or five days migrate against the flow of blood to the liver. The flukes become sexually mature in the liver and then migrate to the mesenteric veins. The pre-patent period is 6 to 9 weeks.
The life cycle of Elaeophora is largely unknown, and it is assumed that an intermediate host is involved –probably a tabanid fly.
Schistosoma species are widely distributed throughout Africa, the Middle East, Asia, and some countries bordering the Mediterranean –i.e. mostly in the tropics and subtropics –where suitable intermediate snail hosts are present ( Table 5 ).
Elaeophora contains five species. E. poeli and E. sagitta are common in Africa, and the remaining three occur in Europe and North America. Again, the distribution depends very much on the availability of a suitable intermediate host –a horsefly (Diptera: Tabanidae).
The host-parasite list for the various Schistosoma species has been adapted from Urquhart et al. (1993). Each of the hosts can act as reservoir host for the other parasite species mentioned ( Table 6 ).
Table 6 Host species of Schistosoma .
|Schistosoma mattheei||Ruminants and occasionally humans|
|Schistosoma japonicum||Humans and most domestic animals|
|Schistosoma spindale||Ruminants, horses and pigs|
|Schistosoma incognitum||Pigs and dogs|
|Schistosoma mansoni||Humans and wild animals|
|Schistosoma nasalis||Ruminants and horses|
|Schistosoma (syn Orientobilharzia) turkestanica||Ruminants|
The transmission of Schistosoma is similar to that of Fasciola and Calicophoron , with all three genera being fully dependent on water as a medium for infection of both the intermediate and final hosts. Subclinical carriers release eggs in the water, and new hosts are infected when they wade or swim in the water. Elaeophora is thought to use a tabanid as intermediate host, and its distribution is therefore limited to the distribution of the fly. In South Africa, the fly concerned occurs in the extreme northern and eastern regions.
Schistosomosis is invariably more serious in sheep than in cattle, and sheep die in large numbers. The disseminated granulomata, haematin pigmentation of the lungs, liver and kidneys that is so typical of schistosomosis, and also the emaciated carcass, causes considerable economic loss as the carcass has to be condemned. The effect on cattle is less, but some organs may have to be condemned because of the pathological changes. Since Elaeophora affects mainly the heart and the lungs, the socio-economic effects are not as dramatic. However, it is postulated that deaths in cattle do occur due to ruptured aneurysms or occluded coronary vessels.
The eggs work their way through the different layers of blood vessel walls, assisted by proteolytic enzymes secreted by the miracidium and the mechanical action of the spine during normal peristaltic motions of the bowel. The eggs form granulomas that can cause thrombosis of the portal vessels. Many eggs are drained through the portal system to the liver and the lungs, where they also form granulomas ( Figure 39 ). Adult worms are bloodsuckers with blind caecae –which causes them to periodically regurgitate digested and partly digested blood. Haematin is phagocytosed by the macrophages, and many of them end up in the lungs. The lungs of sheep infected with S. mattheei have a grey colour –which is highly indicative of the infection ( Figure 42 ). The adult worms cause considerable damage to the blood-vessel walls, and this may interfere with the normal flow of blood. Dead and dying worms are removed to the portal system. The worms accumulate in the liver on a temporary or permanent basis. This may lead to thrombosis, infarction, and death. Cercariae sensitise the host when penetrating the skin. Subsequent infections cause a severe allergic dermatitis –which traps and destroys the cercariae.
The major clinical signs associated with acute intestinal schistosomosis in sheep are diarrhoea, sometimes haemorrhagic, anaemia, and also emaciation. These signs only develop after the onset of egg production by the trematode. Severely affected animals rapidly lose condition and usually die a few months after infection. Those less heavily infected develop chronic disease and their growth is retarded. Cattle seem to be more resistant, although the clinical signs in naive animals are often more severe than in sheep. Diarrhoea is severe, with large blood clots being present, eyes are sunken, and animals gnash on their teeth. Older cattle have an effective level of immunity against reinfection, but if they are challenged with massive doses of cercariae, the immunity breaks down and clinical signs resembling Matricaria nigellaefolia poisoning appear over a period of time. These signs include an anxious expression in the eyes, emaciation, knuckling over of the hind fetlocks, disorientation, constipation, and intermittent straining. Cattle tend to lean against any convenient object (“stootsiekte ”) ( Figure 40 ). It must be emphasised, however, that even in areas with a high prevalence, clinical disease in cattle is seldom seen.
The worst lesions are produced by the presence of schistosome eggs in the tissues. These work their way through the different layers of the blood vessel walls and many eggs are drained through the portal system to the liver and the lungs, where they cause the development of granulomas. Haematin regurgitated by the worms is phagocytised by the macrophages and many of them end up in the lungs. The lungs of sheep infected with S. mattheei have a distinctive dark greyish colour, which is highly indicative of the infection. In both sheep and cattle the liver, intestine, bladder and kidneys, are greyish-brown ( Figure 41 ). In severely infected animals, atelectasis and emphysema may develop as a result of these granulomas. The adult worms cause considerable damage to the blood vessel walls, which may interfere with the normal flow of blood. Dead and dying worms end up in the portal system and accumulate in the liver, which in turn may lead to embolism, infarction and death. Cercariae sensitise the host when penetrating the skin. Subsequent infections cause a severe allergic dermatitis.
The lesions caused by Elaeophora are usually large and well defined and consist of aneurysms and a proliferative endarteritis in the coronary and pulmonary arteries. The endothelium of the aneurysms on the coronary vessels thickens somewhat –while that of the pulmonary vessels becomes hyperplastic and resembles cotton towelling.
The diagnosis of schistosomosis is based mainly on the clinical-pathological picture. The demonstration of the characteristic eggs in the faeces and/ or in “squash ”preparations of blood from the faeces is useful in the early stages of the disease –but not in the later stages, as egg production decreases. When schistosomosis is suspected, it is best to perform a detailed necropsy, which will show the lesions, and, if the mesentery is inspected before removal, the numerous worms in the veins. The diagnosis of elaeophorosis is usually incidental, and worms are seen in the coronary and pulmonary vessels at necropsy or after slaughter.
Coccidiosis, fasciolosis and Matricaria poisoning are possible differential diagnoses for cattle –and coccidiosis, fasciolosis and a variety of helminthoses for sheep.
The control of schistosomosis is the same as that described for Fasciola and Calicophoron . The snail population varies according to the temperature and rainfall. Efforts should be made to determine the months during which time snail numbers are highest –when access to dangerous sections of water can be denied to the animals. Treatment should be carried out with care as dislodgement of the flukes causes them to act as parasitic emboli that drain to the smaller vessels of the portal vein: the so-called liver shift. Infarction of parts of the liver is possible, and in heavily infected animals treatment may have fatal consequences. The drugs still widely used are the antimonial compounds that have to be given over a period of days at a high dosage rate. Praziquantel at 25 mg/kg body mass is effective, although it may be necessary to give another treatment 3 to 5 weeks later.
The nematodes that occur in the skin, subcutis and adnexa of cattle, are Parafilaria bovicola, Onchocerca gibsoni, Onchocerca gutturosa, Onchocerca armillata, Setaria labiatopapillosa and Setaria digitata. Parafilaria occurs in the subcutis, O. gibsoni in nodules in the brisket or limbs, O. gutturosa in the ligamentum nuchae, O. armillata in the wall of the aorta, and Setaria in the abdominal cavity. A Stephanofilaria species has been reported from cattle in the northern parts of South Africa. Apart from Stephanofilaria dedoesi, which occurs in goats, helminths have not been recorded from sheep and goats. None of these nematode infections is life threatening, but they cause much damage to the hide –and carcasses have to be trimmed.
The nematodes that occur in the skin and adnexa belong to the superfamily Filarioidea. Parafilaria and Stephanofilaria belong to the family Filariidae, and Setaria and Onchocerca to the Onchocercidae. Parafilaria are slender white worms, 3 to 6 cm long, and they occur in the subcutaneous tissues. Anteriorly there are numerous cuticular papillae and circular ridges. The male has large pre- and post-cloacal papillae, and the spicules are unequal. The female has a bluntly rounded posterior end, and the vulva is situated near the mouth. Eggs are thin-walled, 0.04 to 0.05 mm long, 0.023 to 0.033 mm wide, and contain a fully developed first stage larva which is about 0.2 mm long.
The Onchocerca species are of little veterinary importance, but one species –Onchocerca volvulus –is of major concern in human medicine, as it is the cause of river blindness. The worms are 3 to 6 cm (males) to 14 to 50 cm (females) long, and are tightly coiled in nodules in connective or muscle tissue. Microfilariae are present in the skin.
The Setaria species in cattle are S. labiatopapillosa and S. digitata –and both occur free in the abdominal cavity. They are large worms, 4 to 12 cm long, and with complex cephalic structures and a cluster of spikes on the tip of the female tail. The male spicules are unequal. Sheathed microfilariae, 0.14 to 0.23 mm long, are produced and these are found in the blood. The Stephanofilaria species are small worms, 3.2 to 6.8 mm long –that live in tunnels in the dermis. Microfilariae are produced and these move to the dermal papillae. Depending on the species, microfilariae are 0.04 to 0.18 mm long.
Epidemiology and distribution
Parafilaria bovicola occurs in the warmer regions of the world –notably Africa, Asia and southern Europe. It has been introduced into Sweden where it is now well established. In South Africa it occurs in areas that receive an annual rainfall of 400-700 mm, have at least 120 frost-free days per year, and lie at an altitude of 800 to 1200 m. Setaria has a worldwide distribution wherever cattle are kept and mosquitoes occur. Onchocerca gutturosa occurs world-wide, O. gibsoni occurs in Africa, Asia and Australasia, and O. armillata in the middle East, Africa and India. There are five species of Stephanofilaria that parasitise domesticated ruminants. S. stilesi occurs in the USA, S. dedoesi in Malaysia, S. assamensis in India, Malaysia and Japan, S. zaheeri in Asia, and S. dinniki in Africa.
Parafilaria bovicola is limited to cattle and water buffaloes, although a closely related species, Parafilaria bassoni , occurs in African buffaloes. Many species of Setaria are known and two species –S. digitata and S. labiatopapillosa –occur in cattle. All four Onchocerca species occur in cattle and most probably in African and water buffaloes. The Stephanofilaria species inhabit the dermis of African and water buffaloes, cattle, goats, the black rhinoceros, hippopotami, and elephants.
All these nematodes have a heteroxenous life cycle –Diptera being the intermediate hosts. Musca lusoria and Musca xanthomelas, also known as face flies, are the main intermediate hosts of P. bovicola in Africa. In Europe, Musca autumnalis is the intermediate host. In South Africa, for Setaria , the mosquito genera Aedes and Culex are the intermediate hosts, while the various species of Simulium and Culicoides are the intermediate hosts for Onchocerca species.
The female Parafilaria in the subcutis bores a small opening through the skin to the exterior to lay thin-shelled eggs which contain a fully developed first-stage larva. A small amount of blood exudes from the wound –the so-called 'bleeding point' –to form the blood streaks that are clinically so typical of parafilariosis ( Figure 44 ). Flies are attracted to the blood and ingest the nematode eggs or first stage larvae. The larvae develop to the third or infective stage in several weeks to months, depending on the ambient temperature. Infection of cattle takes place through wounds or the mucous membranes of the eye, where the flies deposit the infective larvae. The pre-patent period is about 7 to 9 months, during which time the larvae migrate through the subcutis to eventually reach their predilection sites.
The haematophagous flies Simulium and Culicoides transmit the Onchocerca species. Unlike Parafilaria , these worms produce live first-stage larvae, known as microfilariae, that migrate to the blood vessels and end up in the capillaries. When the fly sucks blood, the microfilariae are ingested and develop to the third or infective stage in the fly. The infective worm larvae are transmitted to the new host when the fly feeds again. The Setaria species are transmitted in the same way. The culicine mosquitoes Aedes, Anopheles and Culex are the intermediate hosts.
Flies of the genera Lyperosia, Haematobia and Musca transmit Stephanofilaria . Since the infection is a superficial one and the worms occur in tunnels in the dermis, the flies readily access the first stage larvae. In the flies, the larvae develop to the third stage, and are then transmitted to another animal when the flies feed on a wound.
The socio-economic effects of the helminths that affect the skin can be considerable. Not only does infection ruin the hides –but helminth migration in the subcutis (Parafilaria and Stephanofilaria) and the formation of nodules and abscesses (Onchocerca) may lead to excessive trimming of an otherwise good quality carcass.
The pathogenesis of parafilariosis consists of two phases: one during which the L3 migrates in the subcutis and attains maturity ( Figure 43 ), and, secondly, the egg-laying phase. Once the L3 have escaped from the proboscis of the intermediate fly host, they penetrate various tissues to eventually reach the subcutaneous tissue. Inflammation and oedema occur, and the migration tracts are filled with masses of eosinophils. Lesions are slimy to the touch, yellowish-green in colour, and resemble superficial bruising ( Figure 45 ). Lesions may extend into the inter-muscular fascia. When the gravid female punctures the skin, a small amount of blood exudes from the lesion and mats the surrounding hair. These lesions bleed only for a short time and then heal quickly.
Onchocerca , depending on the species, are associated with different changes.
O. gutturosa in the large ligaments is of little consequence, and O. gibsoni causes a fibrous reaction in the muscles.
The Setaria species are apathogenic. Dead worms may sometimes be encountered on the surface of abdominal organs where they become encapsulated and eventually become calcified there.
Lesions caused by Stephanofilaria appear about 2 weeks after infection. Small skin nodules are seen and these rapidly form papules that rupture. Papules may coalesce to form large areas that exude a haemorrhagic exudate.
The macroscopic lesions that are produced by Parafilaria are the bleeding points and the discoloration of the subcutis and superficial muscle layers. Live or dead worms can be encountered under the skin. During the development period of the larvae, the discolouration is more yellowish to yellowish-green. The older lesions, once the female has produced a bleeding spot, are yellowish-brown to brown. The lesions are slimy with a characteristic coppery odour. Histologically, the lesions are characterised by a massive influx of eosinophils –accompanied by a mild to moderate oedema. In older lesions, pigment-laden macrophages are present in large numbers and moderate numbers of lymphocytes, some plasma cells, and also histiocytes are present.
The adult Onchocerca cause a chronic inflammatory response. This leads to the formation of dense fibrous nodules adjacent to the ligamentum nuchae or fascia next to the major bones of the limbs (O. gutturosa) or in the subcutaneous tissue of the brisket and hind limbs (O. gibsoni) .
Other than these, few lesions are caused by the infection.
Apart from the calcification of dead worms, no lesions are seen with setariosis. However, occasionally, the immatures of Setaria digitata cause cerebrospinal setariosis. See "Nervous system" for a detailed description.
The lesion caused by Stephanofilaria stilesi is located near the mid-ventral line, while the other species cause lesions in the skin on the sides of the neck, withers, dewlap, shoulders, and around the eyes. Irrespective of the species, the lesion is essentially a circumscribed focal dermatitis. Histologically, the nematodes are present in the dermis near the epidermis, and are surrounded by a zone of inflammation characterised by the presence of eosinophils, lymphocytes, some neutrophils, and histiocytes. Hyperkeratosis and parakeratosis can be seen and crusts of exuded serum and detritus collect on the surface. Sensitisation to, and death of, the worms causes a severe dermatitis.
Clinical signs of parafilariosis are limited to actively bleeding spots which occur especially on the withers, but may also be present on the flanks, back and rump. These spots –referred to as bleeding points –appear during warm weather, in order to coincide with fly activity.
No clinical signs are apparent with setariosis. Onchocercosis presents as nodules and lumps of varying sizes in the brisket and external surfaces of the limbs.
Stephanofilaria in the skin usually presents as papules that erupt with a slightly bloody exudate. In the centre of the lesion, the skin tends to slough, and there usually is some hyperkeratosis around the edges. It can best be described as an exudative dermatitis that is often haemorrhagic.
A diagnosis of parafilariosis is made on the presence of bleeding points during the warmer months of the year, and also during the warm hours of the day. A smear made from the blood that oozes out will –on microscopic examination –reveal thinwalled eggs and larvae.
The microfilariae of Onchocerca are concentrated where the intermediate hosts, Simulium and Culicoides , prefer to feed –which is the shady, ventral parts of the host. For diagnostic purposes, a piece of skin about 5 mm square, is removed and placed in warm saline. It is carefully teased apart to help the microfilariae emerge, and is then incubated for 6 hours or more. The microfilariae can be seen moving at the bottom of the container. The diagnosis can also be confirmed by making a blood smear in which microfilariae may be found.
Stephanofilaria adults and microfilariae are present in the skin lesions, but are difficult to find in skin scrapings. The diagnosis, therefore, is mostly presumptive and based on the site of the lesions. Removing a piece of affected skin and carefully dissecting the parasites from the tunnels they create in the dermis can reveal the presence of adult Stephanofilaria .
Differential diagnoses for all of the helminths that affect the skin include injuries caused by thorns or barbed wire, contact with Euphorbia latex, tick and insect bites, abscesses, and focal proliferative neoplastic conditions of the skin.
Parafilaria should be controlled by controlling face flies. This can be achieved by dipping with or applying pyrethroids –preferably deltamethrin –which has the best action against flies. The macrocyclic lactones are effective in killing the adult worms, but there is uncertainty about their efficacy against the immature stages. Cattle should not be slaughtered for at least 70 days after treatment, in order to allow the lesions caused by the worms to heal fully.
Since both Culicoides and Simulium are intermediate hosts of the Onchocerca species, it may be of value to control these flies. This can be achieved by destroying breeding places and by dipping animals. Occasional cases can be treated with one of the macrocyclic lactones –which seem to be quite effective.
Setaria is transmitted by mosquitoes (Aedes and Culex) and, theoretically, breeding places of the flies should be destroyed and cattle dipped with residual insecticides. Because the nematodes are non-pathogenic, however, control is seldom resorted to and routine tick control seems to reduce the incidence of the worms.
Stephanofilaria can be treated with the topical application of pyrethroids, macrocyclic lactones and levamisole.
With the exception of the larvae of Taenia multiceps , and rarely Echinococcus , no helminths primarily target the brain of ruminants –although several may end up there following aberrant migration. The final hosts of Taenia multiceps are dogs and wild carnivores, and the intermediate hosts are sheep, goats and man. When the oncosphere hatches in the intermediate host, it bores through the wall of the intestines and is carried by the blood stream to all parts of the body. In sheep, only those that settle in the spinal cord or brain will develop into the larval stage coenurus cerebralis. In goats the coenuri occur in the brain, in the muscles, and subcutaneously. In wild ruminants they predominantly occur subcutaneously.
Coenurosis in South Africa occurs in Western and Eastern Cape Provinces, the Free State Province, and at two localities in Gauteng and Northwest Province (1979 data). The distribution in the rest of Africa is unknown –but it is assumed to be worldwide.
Carnivores like the various species of jackals and foxes, and hunting and domestic dogs, are the usual hosts of Taenia multiceps –and the foregoing species and wild and domestic cats, of Echinococcus granulosus .
Transmission to the intermediate host is by the faecal-oral route and the final host acquires the infection by eating the infective larval stage in the intermediate host.
The socio-economic impact of this condition is moderate, as the overall infection rate of T. multiceps is about 1%. However, when valuable animals are affected, the situation changes considerably. The treatment of coenurosis and cerebral echinococcosis is expensive, and a successful outcome is not guaranteed. Certain cases are untreatable because of the localisation of the parasite.
The presence of oncospheres in the central nervous system (CNS) cause a syndrome known as ‘gid ’or ‘turning disease ’; the clinical manifestations depend on the location of the coenuri in the brain ( Figure 46 and 47 ). Thus, circling, visual defects, peculiarities in the gait, hyperaesthesia, or paraplegia can be seen. Coenuri may grow so large that they cause pressure atrophy of the surrounding bone of the cranium or the vertebral column ( Figure 48 and 49 ).
The oncospheres are eaten by the intermediate host. When the oncospheres hatch, they bore through the wall of the small intestine and are carried by the blood stream to all parts of the body. Only those in the spinal cord and brain will develop into the larval stage, which is known as coenurus cerebralis. The coenuri grow slowly, taking months to mature. The pathogenesis of the lesions in the CNS is essentially that of gradual pressure atrophy and malacia of the nervous tissue –which progressively interferes with a particular cerebral function depending on where the cyst is located.
The gross lesion of Taenia multiceps is compression of the nervous tissue and sometimes atrophy of the cranial bones –by the space-occupying larva. When mature the larva is easily seen, as it is large, often larger than 5 cm in diameter, and has a fluidfilled cyst bearing clusters of protoscoleces on its internal wall. The hydatid cyst of Echinococcus is as large as or even larger –but does not have the thin, transparent wall of a coenurus. Secondary lesions, which may not be present, include abrasions and other traumatic lesions incurred by the abnormal behaviour of the ruminant.
The diagnosis is based on positive identification of the tapeworms in carnivores, and the clinical signs. The presence of taeniid eggs in the faeces of carnivores is of no particular value, as the eggs of the taeniids all look the same.
Differential diagnoses would include many infective, toxic and traumatic conditions affecting the CNS.
Control of these tapeworms depends entirely on preventing ruminants from consuming the taeniid eggs. This includes regular deworming of the carnivore final hosts where possible, feeding them only well-cooked offal, and fencing off areas contaminated with tapeworm eggs.
Surgical removal of the coenurus is possible only when it is on the surface of the brain.
To salvage valuable animals the following treatment can be attempted: administer praziquantel 100mg/kg once (or 50mg/ kg twice). At the same time, give the normal dose of cortisone and aspirin 100 mg/kg, twice a day. Continue the treatment with the anti-inflammatory drugs for 5 days. Thirty six hours after having given the praziquantel, start giving a diuretic. Depending on the reaction of the sheep, give it at 12 or 24- hour intervals. Obviously, clean water should be available at all times and the animal should not be stressed in any way.
Taeniosis occurs in humans after ingestion of under-cooked pork (Taenia solium) or beef (Taenia saginata) infected with metacestodes –the larval stages of these parasites. Pigs and cattle acquire cysticercosis following the ingestion of eggs or proglottids of T. solium and T. saginata respectively. Following the accidental ingestion of eggs, humans can get cysticercosis, or, more specifically, neurocysticercosis (NCC). (For more discussions on T. solium see under pigs).
Several species of can infect humans as definitive hosts –primarily T. saginata (the beef tapeworm) and T. solium (the pork tapeworm). In addition, the larval stage of other Taenia species (e.g. T. multiceps, T. serialis, T. brauni, T. taeniaeformis and T. crassiceps) can infect humans in various sites of the body.
Recently, a new species of taeniid tapeworm that appeared to be T. saginata was described from people in Asian countries –even though they had eaten only pork (the so-called Asian Taenia ). This organism is now known as T. asiatica , and has been found in Taiwan, Korea, China, Vietnam, and Indonesia. Differentiation between T. saginata acquired from beef and the Asian Taenia from pork, is difficult.
The eggs of Taenia species are characteristically ellipsoid, approximately 0.04 mm in diameter, and with a thick, smooth radially striated embryophore. The egg contains a hexacanth embryo with larval hooks. Eggs of all the Taenia species look alike. Usually only a few eggs are found in the stools, but, more often, a few are found on the perianal skin.
Morphologically, the adult Taenia species can be differentiated on the number of sacculations arising from the uterus. In T. solium there are 7 to 15 lateral branches on each side, whereas in T. saginata there are 15 to 20 on each side. In addition, T. solium has a scolex with four suckers and a double crown of hooks (26 to 36 in number) of different sizes (small hooks of 0.12 to 0.15 mm and large hooks of 0.16 to 0.18 mm), and a narrow neck. The scolex of T. saginata is slightly larger and has four suckers, and no hooks. The adult of T. saginata generally is longer than T. solium –attaining an average length of 5 m. However, occasionally it may grow to more than 15 m.
The adult tapeworm of T. saginata occurs in the definitive host ’s small intestine. Proglottids –which contain eggs –break off the posterior end of the tapeworm, and are then voided with the host ’s faeces. They can be either intact or, if broken up in the host intestines, only eggs will be found in the faeces. The intermediate host becomes infected by the ingestion of eggs. Once ingested, the eggs hatch to release the hexacanth larva, which migrates through the intestinal wall to reach the blood and lymphatic systems –which carry it to the tissues, particularly the heart and other muscles of cattle, and the muscles and brain of pigs and/or humans. Here the larval stage develops to a cysticercus, with an invaginated scolex.
Taenia saginata has a cosmopolitan distribution, with an estimated 50 million cases of infection reported annually.
Taenia saginata uses cattle or related animals as intermediate hosts, although other animals such as camels, llamas and antelope may also occasionally be infected. Up to now, only humans have been described as a definitive host.
Cattle are infected with T. saginata by ingestion of grass, water or soil which is contaminated with eggs that have likely been disseminated through the faeces of infected humans.
T. saginata infections are seldom associated with clinical disease in both the intermediate and definitive host. Hence, socio-economic implications of the disease relate mainly to the costs of condemnation of contaminated carcasses, meaning that the impact can best be evaluated in terms of financial losses to the farmers.
Larvae: Infection with the larval stage of T. saginata (cysticercus bovis) is restricted to cattle –but is completely asymptomatic.
Adults: Most patients infected with T. saginata notice the passage of proglottids that are motile, more numerous, and larger than those of T. solium. The lesions of T. saginata infection are highly variable. Infections are often completely asymptomatic, but in some cases they may cause intestinal obstruction. Vitamin deficiency may be the result of excessive absorption of nutrients by the parasite –although this is more a feature of infection with the fish tapeworm Diphyllobotrium latum. Finally, a broad range of non-specific clinical signs such as abdominal pains, digestive disturbance, excessive appetite or loss of appetite, weakness, and loss of weight can accompany infection.
Microscopic identification of eggs and proglottids in faeces is diagnostic for taeniosis –but is not possible during the first 3 months following infection, prior to development of adult tapeworms. The intermittent nature of egg excretion often leads to underestimation of the prevalence of taeniosis. Repeated examination and concentration techniques will increase the likelihood of detecting light infections. Nevertheless, species differentiation of Taenia species is impossible based solely on microscopic examination of their eggs –because all Taenia species produce morphologically identical eggs. Eggs of Taenia species are also indistinguishable from those produced by cestodes of the genus Echinococcus (tapeworms of dogs and other canid hosts). Microscopic identification of gravid proglottids (or, more rarely, examination of the scolex) allows species determination. Immunodiagnostic tests for the differentiation of taeniid eggs were developed using either monoclonal or affinity-purified polyclonal antibodies in an immunofluorescent assay. These techniques were successfully applied to the identification of T. solium eggs. However, this relies on the ability to recover oncospheres, which leaves the issue of test sensitivity unresolved. The detection of parasite antigens in host faeces has been used for the diagnosis of taeniosis.
The following features were consistent across the different studies:
- Antigen detection in faecal samples is genus-specific, with T. saginata and T. solium both reacting in the assay, but with no cross reaction with other parasite infections –including the cestode Hymenolepis .
- Coproantigen detection is possible prior to patency of the worms, and the sensitivity of the tests is independent of the presence or the number of eggs.
- Coproantigens are no longer detectable within a week after treatment.
- Coproantigens are stable for weeks in unfixed faecal samples kept at room temperature, and for years in frozen samples or samples fixed in, e.g. formalin, and kept at room temperature.
These tests are available as a standard ELISA, as well as in a more easily applicable dipstick ELISA form. The sensitivity and specificity of the latter are lower compared with the standard ELISA –but remains higher than normal coprological methods. Currently, researchers are investigating the nature of antigens detected, with the aim of improving the test performance and evolving to a species-specific test that allows diagnosis of T. solium and T. saginata separately.
Recently, new PCR-based techniques have been developed that enable a speciesspecific diagnosis of T. saginata and T. solium in human faecal samples. Although very promising in terms of sensitivity and specificity, these tests are still not widely applied. Furthermore, the implementation of PCR-based technologies in areas where taeniosis/cysticercosis is endemic, does not occur –given the required infrastructure and cost associated with this technology.
Cysticercosis and neurocysticercosis (NCC)
The definitive diagnosis of cysticercosis is dependent on demonstrating the cysticercus in the tissue concerned. Demonstration of eggs and proglottids in the faeces is useful in the diagnosis of taeniosis, but not cysticercosis. Some of the diagnostic tests used in humans are antibody detection, electro-immunotransfer blot (EITB), and CT or MRI imaging.
Differentiation of T. and T. saginata based on DNA analysis has been possible for several years. The main advantage of this technique is the ability to differentiate between T. saginata and T. asiatica –which is impossible when solely based on morphology. Differentiation of these human host species may be important, especially in epidemiological surveys, since Taenia species may travel around the world in their human definitive hosts.
In cattle small abscesses in the muscles could be a differential diagnosis. In humans, the eventual differential diagnosis will depend on the localisation of the cysticercus in the brain.
To prevent infection of cattle on farms, defecation on pastures must be prevented by supplying toilets to workers. To prevent human infections, South African public health legislation specifies that heavily infected meat be condemned at controlled/ licensed abattoirs, in order to prevent it entering the food chain. Carcasses with low levels of infection may be kept for 14 days at -14 ºC, to ensure the death of the larvae and to reduce the risk of infection.
Preventive measures (vaccination)
Early research on Taenia species showed that immunity to re-infection plays an important role in the natural regulation of transmission of these parasites. In addition, it was demonstrated that host-protective immune responses are directed towards the oncosphere stage in the early developing embryo. A recombinant vaccine has been developed against T. ovis cysticercosis in sheep. This was the first effective, definedantigen vaccine against a parasitic infection. Based on the homology of host-protective antigens between T. ovis and T. saginata , a recombinant vaccine was subsequently developed against T. saginata cysticercosis in cattle. Despite the high level of protection induced by these vaccines, the vaccines have not been commercialised due to financial considerations.
Helminths of horses
Author: E VOLKER SCHWAN
Equine helminth infections are probably less economically important now than they were several decades ago when horses were used extensively for transport and farming. In South Africa, helminth infections are now of importance mainly in horses owned by rural communities which are dependent on work horses, and also horses used for sport and leisure activities.
The use of macrocyclic lactones has resulted in the large strongyles becoming a less important cause of colic in horses –while small strongyles are now of greater importance. Apart from the strongyles and helminths that cause mortalities in foals, most of the other helminth infections either occur sporadically, or have a limited pathogenic impact.
Large strongyles (Strongylosis)
Strongylosis of horses is caused by Strongylus vulgaris, Strongylus edentatus, and Strongylus equinus . These species are collectively also referred to as ‘large strongyles ’, which, in contrast to the ‘small strongyles ’of horses –are migratory (termed ‘migratory strongyles ’). The genus name derives from the Greek word ‘strongylos ’ (= rounded) –referring to the cylindrical shape of the worms. Adult worms are medium-sized and stoutbodied. Microscopically, the species have a large buccal capsule, which can be armed with teeth. Typically, the buccal capsule is surrounded by leaf crowns. The posterior end of males terminates in a typical, well-developed, strongylate bursa with spicules.
Strongylus vulgaris male worms are 10 to 19 mm long and female worms 13 to 25 mm long. Both are 1.0 to 1.4 mm wide. The oval buccal capsule is armed with two typically ear-shaped teeth at its base.
Strongylus edentatus male worms are 19 to 28 mm long and female worms 28 to 45 mm long. Both are 1.3 to 2.2 mm wide. As the species name indicates, Latin ‘e ‘(= without) and ‘dens ’(= tooth) –the cupshaped buccal capsule is ‘toothless ’.
Strongylus equinus male worms are 24 to 35 mm long and female worms 35 to 50 mm long. Both are 1.1 to 2.3 mm wide. The oval buccal capsule is armed with one dorsal tooth with a bifid tip and also two sub-ventral teeth at its base.
Fresh adult strongyles are dark red, and are sometimes almost black in colour. The predilection site in the definitive host is the caecum and colon ( Figure 52 ).
The eggs of the large strongyles are of the strongylid-type, which are oval and thin-shelled. The surface of the egg is smooth. They contain 4 to 8 blastomeres when laid, and these measure 64-99 x 36-58 μm. The eggs are indistinguishable morphologically and morphometrically from those of other equine GIT strongylids.
Apart from the horse, the definitive host range includes donkeys, mules and zebra species.
The large strongyles have a cosmopolitan distribution; Strongylus vulgaris is the most common species.
The large strongyles have a direct life cycle. Sexually mature females are oviparous. Eggs are shed with the faeces into the environment. Depending on the prevailing climatic conditions, there is a typical pre-parasitic development from egg to free-living L1, L2, and then finally the sheathed infective L3 –this all in as little as 3 days.
Ingestion of sheathed free-living larvae is the only mode of infection for definitive hosts. Following uptake, the larvae of the large strongyles typically undergo extensive intra-abdominal migration –which differs markedly in the three species.
Strongylus vulgaris: Infective larvae exsheath in the stomach and undergo a histotropic phase in the mucosa of the caecum and colon –where they develop to L4. The L4 stage then enters arterioles of the gut and migrates on the endothelium to the cranial mesenteric artery and its main branches, where development to pre-adult stages takes place. Pre-adult stages are carried back via the arterial bloodstream to the wall of the caecum and colon –where they form nodules which eventually rupture and release the worms into the lumen of the caecum and colon. The pre-patent period is 6 to 7 months and the patent period is up to 18 months.
Strongylus edentatus: Infective larvae pass into veins of the intestinal mucosa and migrate via the portal system to the liver, where they migrate into the parenchyma –becoming encapsulated in granulomas in which they develop to L4. L4-stages emerge from granulomas and migrate to the liver capsule, which they cannot penetrate. Eventually, they enter the hepatic ligaments and migrate retroperitoneally of the abdominal wall –where they are found in large numbers in the flanks. Aberrant migration of larvae is, however, common. Under the peritoneum, L4 develop to pre-adult stages. Probably via the hepatorenal ligament, pre-adult stages migrate back to the colon, where they eventually penetrate the lumen. Final maturation takes place in the caecum and colon. The pre-patent period is 10 to 11 months and the patent period up to 18 months.
Strongylus equinus: Infective larvae exsheath in the stomach and undergo a histotropic phase in the mucosa of the caecum and colon, where they develop to L4. The L4-stage migrates via the peritoneal cavity into the liver parenchyma –where extensive migration continues. Eventually, L4 enter the pancreas, and partially also the peritoneal cavity. In the pancreas, larvae develop to pre-adult stages which enter the lumen of the gut via the connective-tissue adhesion of the pancreas and head of the caecum. Final maturation takes place in the caecum and colon. Aberrant migration of L4 is common. The pre-patent period is 8-9 months and the patent period is up to 18 months.
Large strongyles occur concurrently with cyathostomins. However, in contrast to the cyathostomins, large strongyle worm burdens are small, and do not exceed a few hundred worms.
Together with the small strongyles, the large strongyles were once regarded as the most common and most important helminth parasites of horses. Both worm groups are major causes of colic. However, with the introduction and wide use of macrocyclic lactones the importance of large strongyles has largely diminished.
Pathogenesis and pathology
The pathogenesis of the large strongyles is mainly associated with the intra-abdominal migration of the larval stages. Strongylus vulgaris is regarded as the most pathogenic nematode of horses.
Strongylus vulgaris : Larvae migrating in the cranial mesenteric artery cause verminous arteritis with subsequent thrombosis and embolism ( Figure 53 ). Depending on the extent of the vascular lesions, the blood flow is impaired or can become interrupted which can result in infarction of parts of the small and large intestine. Aberrant larval migration in other arteries –such as the aorta, coronary arteries or external iliac artery –is well documented and involves similar vascular changes and lesions in their areas of blood supply.
Strongylus edentatus: Migrating larvae in the liver cause extensive haemorrhage, and larvae accumulating in the flank region cause oedema. Aberrant larval migration results in the formation of granulomatous lesions, in, for example, the diaphragm, lungs and omentum.
Strongylus equinus: The pathogenic effects are similar to those of S. edentatus. The lumenal pre-adult and adult stages are mainly histophagic and to a lesser extent haematophagic, and are regarded as insignificantly pathogenic.
The appearance and severity of clinical signs are directly related to the number and period over which larvae were acquired –as well as the immune status of the host.
Vulgaris strongylosis : In this type of strongylosis, two main syndromes –acute and chronic verminous arteritis –are encountered. Acute verminous arteritis follows strong primary or superinfections of foals and yearlings, which present with anorexia, colic (thrombo-embolic colic), cyanosis, constipation, fever, dilated bowel, sweating, tachycardia and weight loss. In chronic verminous arteritis, intermittent (sporadic) colic attacks, inappetence, weight loss and a rough hair coat are observed. Aberrant larval migration can clinically manifest in far less common conditions like ‘intermittent lameness ’.
Edentatus and equinus strongylosis: Clinical signs seen in the acute form are colic and diarrhoea. The chronic form presents with similar clinical signs as listed for chronic verminous arteritis caused by S. vulgaris .
The diagnosis in live animals is problematic, since clinical signs are observed during the pre-patent period.
A presumptive clinical diagnosis can be based on : Careful evaluation of the case history –considering epidemiological factors and the clinical picture.
Discolouration of the peritoneal fluid (dark yellow), serum biochemistry (hypoproteinaemia, hypoalbuminaemia, increased alkaline phosphatase and γ-glutamyl transpeptidase), and haematological findings (leukocytosis, eosinophilia, and anaemia) are indicative.
Parasitological diagnosis : The parasitological diagnosis in live animals is based on the identification of infective larvae harvested from faecal cultures. Identification of larvae in faecal cultures should be entrusted to an experienced diagnostician. Mere demonstration of strongylid-type eggs in faecal samples is inappropriate to derive a definitive diagnosis.
Cyathostominosis is the most important GIT helminth infection of horses to consider when finding strongylid-type eggs in faecal samples.
Other more important helminths to consider in the syndrome of colic are the cyathostomins, Parascaris equorum (particularly in foals and yearlings), Anoplocephala perfoliata , and Gastrodiscus aegyptiacus .
Treatment: There are several anthelmintics belonging to various chemical groups which are indicated for the control of strongylosis in horses.
The drugs differ in their duration of activity –measured by the egg reappearance period (ERP) and the spectrum of developmental stages that they control (adults ‘A ’, migratory larval stages ‘L ’):
- Tetrahydropyrimidines: Pyrantel (A)
- Benzimidazoles: Fenbendazole (L [7.5 mg/kg for 5 consecutive days] + A)
- Macrocyclic lactones: Abamectin, ivermectin, moxidectin (L + A)
Lesions caused by intra-abdominal migrating stages are mostly reversible –following treatment with larvicidal anthelmintics.
Prevention: See under cyathostomins.
Cyathostomins or small strongyles (Cyathostominosis)
Cyathostominosis of horses is caused by ‘small strongyles ’. In contrast to the ‘large strongyles ’, the ‘small strongyles ’of horses are non-migratory (‘non-migratory strongyles ’) and comprise a group of about 60 different nematode species –the most important of which belong to the subfamily Cyathostominae. Other subfamilies of less importance are Strongylinae and Gyalocephalinae. In the clinical literature the ‘small strongyles ’are often collectively referred to as ‘cyathostomins ’or ‘cyathostomes ’, although strictly speaking the term only comprises members of the subfamily Cyathostominae. The group name ‘cyathostomin ’is derived from the Latin word ‘cyathus ’ (beaker) and the Greek word ‘stoma ’ (mouth), which is highly descriptive as it refers to the well developed, small to medium-sized, beakershaped buccal capsule of the worms. Teeth are present in some species. Typically, the buccal capsule is surrounded by leaf crowns. Adult worms are medium- sized, 0.5 to 3.0 cm long and 1.5 mm wide. Fresh specimens vary in colour from yellowish-white to dark red and are therefore sometimes also referred to as ‘blood worms ’or ‘red worms ’. The posterior end of the males has a strongly developed bursa, with bursal rays and spicules. The predilection sites in the definitive host are the caecum and colon ( Figure 54 ).
The eggs of the cyathostomins are of the strongylid-type. Strongylid-type eggs are oval and medium-sized (60- 125 x 30-60 μm). They have a thin and smooth shell and contain 4 to 8 blastomeres when laid. The eggs are indistinguishable morphologically and morphometrically from those of other equine GIT strongylids.
Apart from horses, the definitive host range includes donkeys, mules and zebras.
The cyathostomins have a cosmopolitan distribution.
All cyathostomins have a direct life cycle. Females are oviparous. Eggs are shed with the faeces into the environment. Depending on prevailing climatic conditions, there is a typical pre-parasitic development from egg to free-living L1, L2, and finally an infective, sheathed L3 in as little as 3 days.
Ingestion of sheathed, free-living L3 is the only mode of infection for definitive hosts. Infective larvae exsheath in the stomach and undergo a histotropic phase in the mucosa of the caecum and colon –where L3 develop into L4. The usual duration of the histotropic phase is 1 to 2 months. Under certain conditions (e.g. unfavourable climate, established adult population in the caecum and colon) L3 can become hypobiotic, which results in a prolonged histotropic phase of up to 3 years.
The final moult and maturation take place in the caecal and colonic lumen. The usual pre-patent period varies from 5.5 to 14 weeks. The patent period is for up to 2.5 years. Cyathostomins always occur as a mixed population of several species. Adult worm burdens of 500 000 are common in horses.
The cyathostomins are the commonest and clinically most significant helminth parasites of horses, as they are regarded as a major contributing factor of diarrhoea, colic, sudden weight loss and debilitation. Colic is the most important cause of morbidity and mortality in horses. With the introduction of the macrocyclic lactones, the significance of the previously equally important large strongyles has diminished considerably compared to the cyathostomins. The emergence of anthelmintic resistance in the cyathostomins is another factor leading to their increase in importance. Managing of cyathostomin infections requires considerable input in terms of expert advice, diagnostics and anthelmintics –which is often very expensive.
Pathogenesis and pathology
The pathogenesis is associated with the two developmental phases of the parasite in the definitive host.
Histotropic phase: The larval stages are the most pathogenic. Depending on the infection rate, immunological status of the host, and age, exsheathed L3 entering the mucosa cause a catarrhal, haemorrhagic or fibrinous inflammation of the colon and caecum –known as typhlocolitis. Eventually, L3 larvae provoke a granulomatous inflammatory reaction in the mucosa, resulting in the formation of nodular lesions (0.5 to 5.0 mm in diameter) that significantly affect nutritional metabolism. There can be as many as 60 nodules per cm2. Subsequent synchronised mass excystation and migration of L4 into the lumen leads to mucosal ulceration and haemorrhages. This is usually seen in late winter or early spring. The damaged mucosa allows endotoxins originating from the intestinal contents to enter, which then cause endotoxaemia. The seepage of protein and fluids into the intestine eventually results in hypoalbuminaemia.
Lumenal phase: Adult stages are mainly histophagic and to a lesser extent haematophagic, and feed largely on mucosa. Extensive mucosal damage can be the consequence of high worm burdens, which manifests as diarrhoea, debilitation and weight-loss.
Several clinical forms of cyathostominosis have been described in the literature –of which larval cyathostominosis is the most important.
Larval cyathostominosis: An acute clinical syndrome, which is mostly seen in horses younger than 6 years. A history that horses were dewormed during the previous 2 weeks is typical and indicative of the infection. Onset is highly seasonal –mostly during winter and spring –and is the result of a synchronised reactivation, excystation and emergence of previously hypobiotic stages from the mucosa. There is a sudden onset of diarrhoea, which may be intermittent or persistent. This is accompanied with rapid weight-loss and deterioration of body condition. In severe cases, muscle wasting is apparent. Animals are very weak and lethargic, but their appetite and water intake are unaffected. On the ventral abdomen and limbs a marked subcutaneous oedema develops. There is fever and intermittent attacks of colic. The mortality rate is up to 60%.
To make a diagnosis in live animals is problematic as clinical signs are mostly observed during the pre-patent period.
A presumptive clinical diagnosis is based on:
- Careful evaluation of the case history considering epidemiological factors (season) and the clinical picture (chronic/acute diarrhoea, weight-loss, oedema, lethargy, fever, colic) –can provide evidence to suspect clinical cyathostominosis.
- Serum biochemistry (hypoalbuminaemia, hyper-β-globulinaemia, increased alkaline phosphatase) and haematological findings (neutrophilia, anaemia with or without eosinophilia and/ or lymphocytosis) are highly indicative that cyathostomins are involved.
- Large numbers of dark red L4 and preadult stages in the faeces are sometimes noticed.
Parasitological diagnosis: The parasitological diagnosis in live animals is based on the identification of infective larvae harvested from faecal cultures. Identification of larvae in faecal cultures should be entrusted to an experienced diagnostician. Mere demonstration of strongylid-type eggs in faecal samples is inappropriate to derive to a definitive diagnosis.
Other causes of typhlocolitis that should be considered are fungal and bacterial infections and drug-related side effects caused by, for example, non-steroidal anti-inflammatory drugs, antibiotics and sulphonamides.
Other important helminth infections to consider in the syndrome of colic include Parascaris equorum particularly in foals and yearlings, Anoplocephala perfoliata, Gastrodiscus aegyptiacus and large strongyles.
Treatment: There are several anthelmintics belonging to various chemical groups which are used for the control of cyathostomins in horses. The drugs differ in their duration of activity –measured by the egg reappearance period (ERP) and the spectrum of developmental stages they control (adults ‘A ’, developing larval stages ‘L ’, hypobiotic larval stages ‘H ’):
Piperazine salts (A)
Fenbendazole (L + A [5 mg/kg], H [10 mg/kg for 5 consecutive days])
- Macrocyclic lactones:
Abamectin, ivermectin (L + A), moxidectin (L + A + H)
The largely anthelmintic-based control programmes of the last few decades have strongly selected for resistant cyathostomin strains which affect all anthelmintic groups used in horses. The faecal egg count reduction test (FECRT) is the most appropriate and practical means to detect anthelmintic resistance.
Prevention: The aim is to manage the level of cyathostomins in order to prevent the syndrome of larval cyathostominosis. Control programmes need to be adapted to individual farms/studs. In the past, control programmes relied predominantly on the repeated use of anthelmintics. However, anthelmintic resistance has developed and is spreading fast in the cyathostomins, meaning that a situation in which no anthelmintics remain to treat infections is approaching. Therefore, it is imperative to take cognisance of the dilemma and act in a proactive manner to slow down the development of anthelmintic resistance.
Control programmes should aim to reduce infective larval stages on pastures and to reduce the number of anthelmintic treatments as far as possible (see selective dosing ) .
Current control measures comprise environmental, non-chemical and chemical procedures which can be summarised as follows:
Environmental/non-chemical control procedures:
- Pasture hygiene by implementing regular collection and proper disposal of faeces (‘clean pasture approach ’) can reduce the availability of infective L3 on the ground.
- Pasture management –taking into consideration ‘stocking density ’, ‘alternate grazing ’(grazing different host species on a rotational basis) and ‘rotational grazing ’where applicable.
Anthelmintic dosing practices:
- Interval dosing (synchronised treatment of an entire group of animals or single animal at intervals): This dosing practice is particularly aimed at yearlings. The intervals are based on the egg reappearance periods after treatment (these are different for each anthelmintic group). A strong selective pressure is exerted on the parasite population.
- Strategic dosing (treatment of an entire group of animals or single animal at set times based on epidemiological information). This dosing practice usually consists of seasonal treatments before winter [May] and after winter [October].
- Selective dosing (treatment only of those animals with significant faecal egg counts; the cut-off point is 100 or 200 eggs per gram [epg] of faeces). This dosing practice requires regular and individual faecal egg counts. Selective dosing allows establishment of naturally acquired protective immunity, while minimising anthelmintic use. However, it is not recommended in yearlings because of inadequate acquired immunity.
- Continuous in-feed dosing consists of year-round daily treatment. Pyrantel was mostly used in this approach. Since there is a very high selective pressure exerted on the helminth population, this dosing practice should no longer be considered.
Strongyloides or thread worms (Strongyloidosis)
Strongyloidosis of horses is caused by Strongyloides westeri. Strongyloides species are also known as ‘threadworms ’. The genus name is derived from the Greek word ‘strongylos ’(= rounded) and ‘-eides/- oides ’ (= similar) –referring to the cylindrical shape of the worms. The parasitic worm population consists of parthenogenetic females only, which are small and slender, with a tapering anterior end. Females are 8 to 9 mm long and 80 to 95 μm wide. Strongyloides species have a cylindrical oesophagus that extends through the anterior third of the body. The posterior end is conical. Fresh adult specimens are colourless.
The predilection site in the definitive host is the small intestine –especially the duodenum and jejunum. The eggs of S. westeri are oval and thin-shelled. The surface of the egg is smooth. They measure 40 to 50 μm by 30 to 40 μm and are embryonated when laid.
Apart from horses, the definitive host range includes donkeys and zebras.
Strongyloides westeri has a cosmopolitan distribution.
Strongyloides westeri has a direct life cycle. Parthenogenetic females are ovoviviparous –i.e. they produce embryonated eggs. Eggs are shed with the faeces into the environment. Depending on prevailing climatic conditions, there is a typical pre-parasitic development from embryonated egg to free-living L1, L2 and finally unsheathed infective L3 –in as little as 3 days. This scenario is part of what is known as the homogonic life cycle. Alternatively, a heterogonic life cycle is followed, in which L1 develop via L2, L3 and L4 to free-living male and female worms reproducing on the ground.
With sufficient moisture provided, infective larvae can survive for about 3 weeks on the ground.
There are various modes of infection for definitive hosts:
- Trans-mammary (lactogenic) infection following ingestion of reactivated arrested (somatic) larvae from the lactating mare, is the most important mode of infection of foals. The pre-patent period is only 8 to 10 days.
- Percutaneous infection and ingestion of free-living infective L3 is less important.
Infective larvae undergo lymphatic-tracheal migration in non-immune hosts –before developing into females in the small intestine. Infection induces immunity, with infective larvae becoming dormant (arrested, hypobiotic) in the udder and other parts of the body. Depending on the mode of infection, the pre-patent period varies from 3 to 14 days. The patent period is 2 to 9 months.
Strongyloidosis of horses seldom requires veterinary intervention. However, Strongyloides westeri is the most significant parasitic aetiological factor of diarrhoea in foals. Humans can act as paratenic hosts for all animal Strongyloides species. Infection is percutaneous, and the developing clinical picture is that of cutaneous larva migrans. This, however, is more commonly caused by animal hookworm species.
Pathogenesis and pathology
Strongyloides species are mucosal dwellers. Depending on the immunological status and worm burden, infection causes villous atrophy, cellular infiltration, and destruction of the epithelium –which results in malabsorption, hypo- proteinaemia, hypo- albuminaemia and eventually subcutaneous oedema.
Clinical strongyloidosis is only seen in very young foals –mostly 9 to 16 days after birth - harbouring heavy worm burdens. Intermittent watery diarrhoea (‘scouring ’), inappetence, exsiccosis (insufficient intake of water) and diarrhoea are common clinical signs. Death is possible, but is not characteristic for equine strongyloidosis.
Presumptive clinical diagnosis: Severe diarrhoea of foals during the first 3 weeks post partum –as well as hypoproteinaemia, hypoalbuminaemia, anaemia, and sub cutaneous oedema –are highly indicative.
Parasitological diagnosis: The parasitological diagnosis is based on the demonstration of embryonated eggs in faecal samples, by means of flotation. Preparing faecal cultures with subsequent identification of L3 is more sensitive, and should be considered if faecal flotation is negative.
Other causes of diarrhoea in nursing foals –to be considered include rotavirus, Cryptosporidium and Clostridium perfringens infections.
Treatment: The benzimidazole fenbendazole (50 mg/kg) and the macrocyclic lactones –abamectin, ivermectin and moxidectin –are effective against the lumenal stages. Lactogenic infections can be reduced by treating mares on the day of foaling with a macrocyclic lactone.
Prevention: Hygiene is the most important consideration in the successful control of equine strongyloidosis. Boxes should be cleaned regularly and thoroughly. Disinfection of floors with 2% sodium hydroxide solution, once a week, is an inexpensive and highly effective choice. Daily removal of faeces from boxes and paddocks is another important measure to reduce the number of free-living infective larvae. Depending on availability and feasibility, alternate grazing is a worthwhile consideration.
Oxyuris or pin worms (oxyuriosis)
Oxyuriosis of horses is caused by Oxyuris equi. The genus name is derived from the Greek words ‘oxys ’ (= pointed) and ‘ura ’ (= tail), which –like the common name ‘pinworm ’–are descriptive terms referring to the long, pointed tail of the female worm. Quite unusual for the group of the oxyuroids, Oxyuris equi is a small to large, thick-bodied nematode. Male worms are only 9 to 12 mm long, and female worms are 40-150 mm long. Microscopically, the worms have a small buccal capsule which leads into a typical oxyuroid oesophagus. The posterior end of the male is truncate with a pair of caudal alae. There is a single, needleshaped spicule, which is 120 to 200 μm long. Females have a typical long, gradually tapering pointed tail –which is up to twice the length of the body. Fresh adult specimens of O. equi are whitish in colour ( Figure 56 ).
The typical predilection site of O. equi is the caecum and colon.
Eggs of O. equi are slightly asymmetrical, thick-shelled, and have an operculum at one pole. They measure 85 to 95 μm by 40 to 45 μm and contain a larva (L1 stage) when shed in the faeces.
Apart from horses, the definitive host range includes donkeys, mules and zebra.
Oxyuris equi has a cosmopolitan distribution.
Oxyuris equi has a direct life cycle. Females only oviposit once. They partially migrate out of the anus to deposit the eggs in strings in the perianal area. In only 3 to 7 days, an infective L3 develops within the egg. Egg strings –on drying off –detach from the skin and fall to the ground as small flakes. Eggs are highly sensitive to desiccation and are viable for only a few days on the ground. However, in moist surroundings, eggs can remain viable for several weeks. Ingestion of eggs containing infective larvae is the only mode of infection. Infective larvae hatch in the small intestine and undergo a histotropic phase for 3 to 10 days in the mucosal crypts of the caecum and colon –during which time the third moult takes place. The emerging L4 stages migrate to the dorsal colon, where they are found attached to the mucosa. After 2 months the final moult takes place, and sexual maturity is reached after another 2 to 3 months. The pre-patent period is 4.5 to 5 months and the patent period of females is 6 months, after migrating back into the rectum. Male worms die soon after fertilisation has taken place.
Oxyuris equi is a very common nematode parasite of horses, but is only mildly pathogenic. The species does not have any zoonotic implications. The apparent zoonotic potential of O. equi is a common misconception –not only among horse owners, but also with health professionals. Oxyuroids in general are highly host specific. Pinworm infection of humans, commonly seen in children, is caused by Enterobius vermicularis .
Pathogenesis and pathology
Pathogenesis is associated with the emerging L4-stages in the caecum and ventral colon feeding on mucosa and the mature female worms: large numbers of L4 stages in the caecum and ventral colon can cause inflammatory reactions and ulceration of the mucosa, which are clinically inapparent. Females partially migrating out of the anus to deposit eggs cause intense pruritus in the perianal area.
Oxyuriosis is typically seen in stabled horses. As a result of intense pruritus in the perianal area, horses are restless –which also impacts on feeding and subsequently body condition. Horses rub their tail-base against walls, fence posts, tree trunks and other objects, causing hairs to break off which eventually gives the tail an untidy or “rat tailed ”appearance in severe cases ( Figure 55 ).
Diagnosis in live animals
Presumptive clinical diagnosis: Clinical signs and the presence of whitish-greyish streaks or smudges in the perianal area, are indicative of infection.
Parasitological diagnosis: The parasitological diagnosis in live animals is based on the demonstration of eggs in the perianal area –by means of the adhesive tape-swab technique. Since eggs are deposited outside the gut, they are unlikely to be found in faecal samples. Female worms are sometimes voided with the faeces and are easily recognised by their size, thick-bodied appearance, and long pointed tail.
Infections with the oxyuroid Probstmayria vivipara should be taken into consideration. However, the species is regarded as nonpathogenic and infected horses –even with high worm burdens –do not develop clinical signs. Diagnosis in live horses is difficult, since females are viviparous.
Treatment: Several anthelmintics belonging to various chemical groups are indicated for the treatment of oxyuriosis in horses:
- Piperazines: Piperazine salts
- Tetrahydropyrimidines: Pyrantel
- Benzimidazoles: Fenbendazole
- Macrocyclic lactones: Abamectin, ivermectin, moxidectin
Control: Infections can be prevented by regular check-ups of the perianal area and by wiping off egg masses with a wet cloth. Other important measures that will assist in control are frequent changing of bedding and the provision of proper cribs and troughs installed off the ground.
Summer sores (Habronematidosis)
Habronematidosis of horses is caused by Habronema muscae, Habronema majus and Draschia megastoma . The genera Habronema and Draschia belong to the family Habronematidae –a name derived from the Greek words ‘habros ’ (= delicate) and ‘nema ’ (= thread). Habronematids are slender and 7 to 25 mm long. The species have a mediumsized, thick-walled buccal capsule with large pseudolabia. The posterior end of the male is spirally coiled and has caudal alae. The spicules are unequal. The female posterior end is conical. The vulva is located near the middle of the body.
Habronema muscae male worms are 8 to 14 mm long and female worms 12-22 mm long. The worms have a cylindrical buccal capsule, which is unarmed. Spicules are unequal and measure 2.5 mm (left) and 0.5 mm (right) in length, respectively.
Habronema majus male worms are 9 to 22 mm long and female worms are 15 to 35 mm long. The worms have a cylindrical buccal capsule, which is armed with two teeth. Spicules are unequal and measure 750 to 880 μm (left) and 350 to 380 μm (right) in length, respectively.
Draschia megastoma male worms are 7 to 10 mm long and female worms 10 to 13 mm long. The worms have a funnelshaped buccal capsule, which is unarmed. Spicules are unequal and measure 460 μm (left) and 240 to 280 μm (right) in length, respectively.
Fresh adult specimens of H. muscae are orange in colour, whereas H. majus and D. megastoma are whitish in colour.
The typical predilection site of the Habronema species is the mucosa of the fundus region of the stomach –where they are covered by a thick mucus layer.
Draschia megastoma is found in colonies embedded in granulomatous, chickenegg- sized nodules in the fundus region of the stomach. Nodules protrude into the lumen of the stomach.
Eggs of the Habronema species are cigar- shaped and thin-shelled. They measure 40 to 50 μm by 10 to 16 μm, and are embryonated when laid.
Female worms of D. megastoma are viviparous. The L1 stages are 330 to 350 μm long and 8 μm wide.
Apart from horses, the definitive host range includes donkeys, mules and zebra.
The habronematids have a cosmopolitan distribution.
The habronematids have an indirect life cycle. Females of H. muscae and H. majus are ovoviviparous, whereas females of D. megastoma are viviparous. Embryonated eggs and larvae are shed with the faeces into the environment.
Non-biting and biting muscid flies act as intermediate hosts (vectors). Musca domestica and other Musca species are known vectors for H. muscae, H. majus and D. megastoma. Stomoxys calcitrans has been identified as a vector for H. majus only. Embryonated eggs and larvae are ingested by the dung-inhabiting larvae of the muscids. The development to infective L3 stages is synchronised with the development of the vectors, and is completed when the flies are emerging from the pupae. The incubation period in muscid vectors is largely temperature dependent and can last as little as 7 days.
Horses become infected by ingestion of infective larvae breaking out of the fly ’s mouthparts while feeding on the lips and nostrils, or by ingestion of dead infected flies in water and feed. There is no migration involved and larvae will develop to adults in the stomach –leading to ‘gastric habronematidosis ’. The pre-patent period is 2 months.
Flies also commonly settle on skin wounds and the conjunctivae of the eyes, in which case emerging larvae invade tissues, but do not complete the life cycle and succumb after a few weeks. Migration of larvae will result in granulomatous lesions referred to as summer sores (‘cutaneous/ophthalmic habronematidosis ’).
Habronematids are common and important nematode parasites of horses –responsible for granulomatous skin lesions.
Pathogenesis and pathology
Gastric habronematidosis ( Figure 58 ): Habronema species can cause a chronic catarrhal gastritis with excessive mucous production. Draschia megastoma causes a typical granulomatous reaction in the fundic region of the stomach –resulting in the formation of chicken-egg-sized nodular lesions which protrude into the gastric lumen. Gastric perforation with subsequent peritonitis has been reported, but is extremely rare.
Cutaneous habronematidosis (‘summer sores ’) ( Figure 57 ): Infective larvae entering skin wounds cause the formation of pruritic, reddish-brown, granulomatous lesions that protrude in a cauliflower-like fashion above the surface of the skin.
Despite a high prevalence of gastric habronematidosis, it very rarely manifests clinically as chronic gastritis. However, cutaneous habronematidosis is a common clinical observation in horses worldwide, and is known as ‘summer sores ’. Common parts of the body affected are those subjected to superficial injury, such as the head region (head, eyelids, conjunctivae), withers, inner parts of the lower limbs, and the coronet, prepuce and penis. Secondary bacterial infections can result in further aggravation. Lesions are typically seasonal and coincide with the fly season –after which larvae slowly die off in the wounds, and self healing with formation of scar tissue takes place.
The diagnosis in live animals is problematic and is almost exclusively based on the clinical signs. Histopathological examination of biopsy specimens may help differentiate it from other proliferative lesions, including neoplasms such as squamous cell carcinoma that may occur in similar areas of the skin.
Presumptive diagnosis: The clinical diag nosis is based on the seasonal appearance of proliferative and pruritic granulomatous skin lesions
Parasitological diagnosis: The parasitological diagnosis of patent gastric infections is impractical as embryonated eggs or larvae are rarely detected in faecal examinations. Since gastric habronematidosis has very little clinical significance, diagnosis in live animals is irrelevant.
The filarial parasites Parafilaria multipapillosa and Onchocerca reticulata should be considered since both are known to cause open skin lesions, which resemble those observed in cutaneous habronematidosis.
Treatment: Macrocyclic lactones are effective for the treatment of cutaneous and gastric habronematidosis.
Control: Fly control is beneficial in the control of habronematidosis. Skin wounds –especially during the fly season –should be adequately attended to in order to prevent infestation by muscid flies.
Ascarid worms (Parascariosis)
Parascariosis of horses is caused by the nematode Parascaris equorum. The genus name is derived from the Greek word ‘ascaris ’ (= worm of the entrails). Being a typical ascarid, adult worms are easily recognisable because of their large size. Male worms are 15 to 28 cm long and female worms 16 to 50 cm long. Both are about 3 to 8 mm wide.
Microscopically, the species has a small buccal capsule, surrounded by 3 large, heart-shaped lips. The posterior end of the male is conical and has small caudal alae. The spicules are equal and measure 2.0 to 2.5 mm in length. The posterior end of the female terminates in a short conical process. The vulva is located at the posterior end of the anterior quarter of the body.
As for all ascarids the predilection site in the definitive host is the small intestine.
Eggs of P. equorum are subspherical and medium-sized (90 to 100 μm in diameter). They have a thick, pitted, brown shell and contain a single cell when laid.
Apart form the horse, the definitive host range includes donkeys, mules and zebra.
Parascaris equorum has a cosmopolitan distribution.
Parascaris equorum has a direct life cycle. As with all ascarids, females have a characteristically high biotic potential. Eggs are shed with the faeces into the environment. They are highly resistant and remain viable for up to 5 years.
Depending on temperature, an infective L3 develops within the egg in as little as 10 to 15 days.
Ingestion of larvated eggs is the only mode of infection for definitive hosts. Larvae hatch in the small intestine and subsequently burrow into the intestinal wall, where they enter small blood vessels. Following a hepatic-tracheal migration, L4 stages settle in the small intestine, where the final moult takes place ( Figure 59 ). The pre-patent period is 72 to 115 days and the patent period is up to 2 years.
As a significant cause of diarrhoea and colic, Parascaris equorum is the most important endoparasite of foals. The expense of registered products for deworming and veterinary treatment in surgical cases is considerable, and is beyond the reach of resource-poor animal owners.
Pathogenesis and pathology
The pathogenesis is associated with the two developmental phases of the parasite.
Larval migratory phase: Migration of larvae through the liver and lungs causes microlesions and inflammatory reactions, which lead to alveolitis, bronchiolitis and bronchitis.
Lumenal phase: After reaching the small intestine, the worms cause a chronic catarrhal enteritis and hypoalbuminaemia. Because of the large size of the developing worms, intestinal impaction, intussusception and perforation with subsequent peritonitis, are common if high burdens prevail. Migration of worms to aberrant sites such as the bile duct may occur.
Clinical parascariosis is almost exclusively seen in foals and yearlings. From about 6 months of age, protective immune mechanisms become effective –with the result that occasional infections are mostly clinically inapparent in older horses.
The clinical signs are also associated with the two developmental phases of the parasite in the definitive host.
Larval migratory phase: During this phase coughing and nasal discharge are sometimes noticed.
Lumenal phase: Clinical signs observed are diarrhoea and colic attacks, together with poor growth, weight loss, sometimes a pot-bellied appearance, changing appetite, and a dull hair coat.
Presumptive clinical diagnosis: Clinical signs in foals and yearlings –as listed above –give reason to suspect Parascaris infection. Respiratory clinical signs are the earliest seen in heavily infected foals during the pre-patent period, in which an aetiological diagnosis cannot be made. However, a marked blood eosinophilia is indicative.
Parasitological diagnosis: The parasitological diagnosis in live animals is based on the demonstration of eggs in faecal samples.
Other causes of diarrhoea that should be considered are improper nutrition, common side effects of drugs (non-steroidal anti-inflammatory drugs, antibiotics, sulphonamides), fungal infections, bacterial infections, and other helminth infections (cyathostominosis, strongyloidosis, anoplocephalosis). Regarding respiratory clinical signs, microbial causes and infections with the horse lungworm Dictyocaulus arnfieldi should be taken into account.
Treatment: There are several anthelmintics belonging to various chemical groups which are used for the control of parascariosis in horses. The drugs differ in their duration of activity, measured by the egg reappearance period (ERP):
- Piperazines: Various piperazine salts
- Tetrahydropyrimidines: Pyrantel
- Benzimidazoles: Fenbendazole
- Macrocyclic lactones: Abamectin, ivermectin, moxidectin
Pyrantel-resistant isolates of P. equorum have only been reported from North America. The emergence of macrocyclic lactone-resistant isolates of P. equorum , however, is of great concern –as macrocyclic lactones are widely relied on in roundworm control for foals and yearlings.
Foals become infected soon after birth and should first be treated at 9 to 10 weeks of age, with subsequent treatments at intervals of 2 months until they become yearlings. The efficacy of the anthelmintic should be monitored annually. Other important considerations in the control are the regular removal of faeces.
Trichostrongylosis of horses is caused by the nematode Trichostrongylus axei . The genus name is derived from the Greek words ‘trichos ’ (= hair) and ‘strongylos ’ (= rounded). Adult worms are small, slender, and have a tapering anterior end. Male worms are 2.3 to 6.0 mm long and 50 to 70 μm wide. Female worms are 3.0 to 2-8 mm long and 55 to 75 μm wide. The species has no buccal capsule. The posterior end of the male has a strongly developed bursa. Spicules are dissimilar in size and shape; they measure 96 to 128 μm (left) and 74 to 104 μm (right) in length, respectively. The posterior end of the female is cone-shaped. The vulva is located in the posterior sixth of the body. Fresh adult specimens of T. axei are pale reddish-brown.
The predilection site in horses is the stomach –particularly the glandular part.
The eggs of T. axei are of the strongylidtype. Strongylid-type eggs are oval and thin-shelled, and have a smooth surface. They contain 4 to 8 blastomeres when laid and measure 79 to 92 by 31 to 41 μm. The eggs are morphologically and morphometrically indistinguishable from those of other equine GIT strongylids.
Apart from horses, the definitive host range includes donkeys, mules, sheep, goats, cattle, deer, antelope, warthogs –and occasionally pigs and humans.
Trichostrongylus axei has a cosmopolitan distribution.
Trichostrongylus axei has a direct life cycle. Sexually mature females are oviparous. Eggs are voided with the faeces into the environment. Depending on prevailing climatic conditions, there is a typical preparasitic development from egg to freeliving L1, L2 and finally sheathed infective L3 in as little as 4 to 6 days.
Ingestion of sheathed free-living L3 is the only mode of infection for definitive hosts. Infective larvae exsheath in the stomach and enter the mucosa and glandular pits –where they develop after 2 moults into adults. The pre-patent period is 3 weeks, but can be much longer under unfavourable environmental conditions.
Clinical trichostrongylosis can only develop where communal grazing or alternate grazing with ruminants is practised. Diagnosis in live animals requires specialist diagnostic facilities, which are expensive and out of reach for resource-poor animal owners. Furthermore, the choice of effective anthelmintics is limited.
Pathogenesis and pathology
In heavy infections, invasion of the gastric mucosa results in a chronic hyperplastic gastritis –which becomes macroscopically visible as circumscribed proliferative areas in the glandular part of the stomach. At a later stage these areas become eroded and are devoid of epithelium.
Clinical signs observed in clinical trichostrongylosis are varied and range from a changing appetite, progressive weight-loss, through to general loss of condition. There is no diarrhoea.
The parasitological diagnosis in live animals is based on the identification of infective larvae harvested from faecal cultures. Identification of larvae in faecal cultures should be entrusted to an experienced diagnostician. However, in most instances, the proof of T. axei infection is clinically insignificant. Mere demonstration of strongylid-type eggs in faecal samples cannot be used to confirm the diagnosis.
Particularly cyathostominosis, and to a lesser extent strongylosis, are more important GIT helminth infections of horses to consider when finding strongylid-type eggs in faecal samples.
Treatment: The macrocyclic lactones abamectin, ivermectin and moxidectin are effective for the treatment of trichostrongylosis in horses.
Prevention: Although advocated as a tool to manage helminths in the environment, communal grazing and alternate grazing with ruminants should be avoided.
Onchocerca species (Onchocercosis)
Onchocercosis of horses is caused by Onchocerca cervicalis and Onchocerca reticulata. The genus name is derived from the Greek words ‘onkos ’ (= tumour, lump) and ‘kerkos ’ (= tail) –which refer to the formation of lumps in the connective tissues, which are caused by the presence of the adult worms. Onchocerca species are medium to large-sized filiform nematodes. The cuticle of the body is often transversely striated. They have an atrophied stoma.
The posterior end of the male is spirally coiled. The spicules are dissimilar in size and shape. The posterior end of the female is rounded. The vulva is located in the anterior or posterior oesophageal region of the body.
O. cervicalis typically occurs in the nuchal ligament and surrounding sub-dermal and inter-muscular connective tissue, while O. reticulata occurs in the flexor tendon and suspensory ligament of the fetlocks.
Female worms are viviparous and produce unsheathed L1 stages –known as microfilariae.
See Table 7 for the comparative morphological details of O. cervicalis and O. reticulata.
Apart from horses, the definitive host range of the two species includes mules and donkeys.
Both species have a cosmopolitan distribution.
Onchocerca species follow an indirect life cycle. Microfilariae produced by females appear in the lymph spaces of the skin.
Biting midges of the genus Culicoides act as intermediate hosts (vectors) for O. cervicalis and O. reticulata . Female biting midges become infected by obtaining blood meals from microfilaraemic horses. In the vector, microfilariae develop to infective L3 stages (metacyclic larvae), which eventually assemble in the proboscis. The incubation period in vectors is largely temperature dependent and may take as little as 14 to 15 days. Definitive hosts become infected during blood feeding of vectors, during which metacyclic larvae actively leave the labella of the proboscis onto the skin, and subsequently enter the puncture wound on their own. The pre-patent period is up to 16 months for O. cervicalis , but is unknown for O. reticulata. Onchocerca species are long-lived and microfilariae in the skin remain viable and infective for vectors, for up to 30 months.
Onchocercosis in horses appears to be of minor clinical importance.
Pathogenesis and pathology
Macrofilariae (adult and pre-adult stages) and microfilariae can cause lesions in horses and other equids:
Effects on the ligamentum nuchae (‘fistulous withers ’): Large nodules (1 to 4 cm in diameter) caused by a verminous granulomatous inflammatory reaction, develop in the nuchal ligament. The inflammatory exudate contains fragments of degenerated worms embedded in caseous necrotic material, that eventually becomes calcified.
Effects on the skin (‘cutaneous onchocercosis ’): Microfilariae of O. cervicalis migrate into the epidermis and dermis of the ventral abdomen along the linea alba, head, neck and ventral thorax. These locations coincide with the preferential feeding sites of the vectors. Microfilariae can elicit a hypersensitivity reaction in these skin parts.
Effects on the eye (‘periodic ophthalmia ’): As in human onchocerciasis, microfilariae of O. cervicalis can migrate to particularly the cornea and sclera of the eye. Vascularisation of the cornea is a common feature, which is interpreted as a reaction to dead microfilariae.
Effects on the distal parts of fore and hind limbs (parasitic suspensory desmitis, tendonitis, sesamoiditis, navicular disease): Adults of O. reticulata cause nodular lesions mainly in the suspensory ligament and flexor tendon of the fore and hind limbs. Depending on their location, nodules can exert pressure on nerves –resulting in lameness. Tumour-like granulomatous lesions are sometimes noticed on overlying skin parts.
Fistulous withers: Calcified nodules in the nuchal ligament can cause considerable irritation in horses used extensively for riding or as pack animals. Localised oedema, seromas, followed by perforation of fistulous channels originating from a lesion in the nuchal ligament can be observed.
Cutaneous onchocercosis: Hypersensitivity reaction to the presence of microfilariae of O. cervicalis can present as pruritic dermatitis –with erythema, alopecia, depigmentation, a papular rash, excoriation and the formation of crusts.
Periodic ophthalmia: Corneal vascularisation is commonly observed in periodic ophthalmia. Severely swollen eyelids, hyperaemic and oedematous conjunctivae –as well as excessive lachrymation –are seen in acute attacks.
Parasitic suspensory desmitis, tendonitis, sesamoiditis, and navicular disease: There is often a history of chronic lameness which is unresponsive to treatment. Nodular lesions in the suspensory ligaments can be highly sensitive to pressure. Eventually, open, tumour-like granulomatous lesions might develop on the bruised overlying skin.
Presumptive diagnosis: Fistulous lesions in the withers region, periodic ophthalmia, and pruritic dermatitis on the ventral abdomen, ventral thorax, head and neck, can be indicative of onchocercosis caused by O. cervicalis .
A history of chronic lameness unresponsive to treatment, nodular lesions in mainly the suspensory ligament and flexor tendon of the fore and hind limbs, along with open, tumour-like, granulomatous lesions on the bruised overlying skin, can be indicative of onchocercosis caused by O. reticulata .
Parasitological diagnosis: The parasitological diagnosis in live horses is based on the identification of unsheathed microfilariae found in skin biopsies obtained from the ventral abdomen, ventral thorax, head and neck. Skin samples –about 3 mm in diameter –are teased and incubated in saline at 37 °C for 12 hours. Subsequently, the suspension is filtered through gauze and centrifuged at 200 g for 5 minutes. The sediment is examined microscopically for microfilariae. The microfilariae of the two Onchocerca species can easily be differentiated by their size ( see Table 7 ).
Fistulous withers: Apart from bacterial infections, rare infections with the bovine species Onchocerca gutturosa have been reported to cause similar lesions.
Cutaneous onchocercosis: Dermatitis caused by the feeding of blood-sucking insects –such as ceratopogonids, biting muscids and simuliids –presents with the same clinical picture as is observed in cutaneous onchocercosis.
Periodic ophthalmia: Infections with Setaria equina have to be considered in cases of periodic ophthalmia.
Parasitic suspensory desmitis, tendonitis, sesamoiditis, and navicular disease: Apart from O. reticulata, Elaeophora boehmi has to be considered as a possible parasitological cause in cases of suspensory desmitis, tendonitis, sesamoiditis and navicular disease. However, currently, E. boehmi infections have only been reported in Europe and Asia. In concurrently occurring granulomatous lesions, habronematids (Habronema/Draschia species) as the cause of summer sores, should be considered.
Distinguishing between various causes of similar skin lesions is aided by histopathological examination of appropriate skin biopsies taken from the edges of the lesions.
Treatment: There are no effective macrofilaricidal (adulticidal) drugs available in horses. The macrocyclic lactones ivermectin and moxidectin are effective microfilaricides.
Nodulectomy is indicated in some cases of O. reticulata infections affecting the distal parts of the limbs.
Control: Stabling of horses at night could be considered –since biting midges are mostly nocturnal feeders and exophagic.
Table 7 Onchocerca species of horses
|O. cervicalis||O. reticulate|
| Adult stages ||500-700 mm x 260-570 μm 60-103 mm x 100-190 μm 320-380 μm (left) and 97-125 μm (right)||450-750 mm x 275-400 μm 105-270 mm x 150-185 μm 248-315 μm (left) and 115-130 μm (right)|
| Microfilariae ||Unsheathed 178-240 μm x 4-6 μm Skin||Unsheathed 310-395 μm x 6-7 μm Skin|
|Definitive hosts||Horse, donkey, mule||Horse, donkey, mule|
|Intermediate hosts (vectors)||Culicoides species||Culicoides species|
Setariosis of horses is caused by Setaria equina . The genus name is derived from the Latin word ‘saeta ’ (= thick hair, bristle) –which refers to the appearance of the adult worms. Setaria species are large, filiform nematodes. The cuticle of the body is finely transversely striated. Microscopically, they have a small buccal capsule with an opening that is surrounded by a peri-buccal crown. Male worms are 51 to 66 mm long and 470 to 560 μm wide. The posterior end of the male is spirally coiled. Spicules are dissimilar in size and shape. They measure 280 to 290 μm (right) and 610 to 640 μm (left) in length. The smaller spicule terminates in a claw through which the larger spicule slips. Female worms are 72 to 190 mm long and 1.0 to 1.2 mm wide. The vulva is located in the oesophageal region of the body. The posterior end of the female is conical. Fresh specimens are whitish in colour.
Setaria equina typically occurs mainly in the peritoneal cavity. Sometimes the worms localise in the scrotum and the eye, and underneath the serosal surfaces of the liver, spleen, lungs, and heart.
Female worms are viviparous and produce sheathed L1 stages known as microfilariae. Microfilariae are 240 to 290 μm long and 5 to 8 μm wide.
Apart from horses, the definitive host range of S. equina includes mules, donkeys, zebra and dromedaries.
Setaria equina has a cosmopolitan distribution.
Setaria species have an indirect life cycle. Microfilariae produced by females appear in the blood. The appearance of microfilariae in the peripheral blood of horses is nocturnal sub-periodic, with a maximum microfilaraemia observed at night between 22:00 and 23:00.
Mainly culicine mosquito species belonging to the genera Aedes and Culex act as intermediate hosts (vectors). Obtaining blood meals from microfilaraemic final hosts infects female mosquitoes. In the vector, microfilariae develop to infective L3 stages (metacyclic larvae) –which eventually assemble in the proboscis. The incubation period in vectors is largely temperature-dependent, and may take as little as 15 to 16 days.
Definitive hosts become infected during blood feeding of vectors –during which metacyclic larvae actively leave the labella of the proboscis, are deposited onto the skin, and subsequently enter the puncture wound on their own. The pre-patent period is up to 12 months.
Equine setariosis is only of minor clinical importance and usually does not require veterinary intervention.
Pathogenesis and pathology
Microfilariae are regarded as non-pathogenic. Although rare, adult and pre-adult stages (macrofilariae) lodging in sites other than the peritoneal cavity can have pathogenic effects on the CNS of the host (‘verminous meningoencephalomyelitis ’). Setaria equina is regarded as the most common cause of equine verminous meningoencephalomyelitis in some tropical and subtropical parts of the world. Aberrant migration and definitive development of S. equina in the CNS causes acute focal encephalomyelomalacia –with degeneration of nerve tracts and an eosinophilic inflammatory reaction.
Eye: Infection of the anterior eye chamber and vitreous body can illicit severe inflammatory reactions. The reaction to degenerating microfilariae can cause blindness.
Scrotum: Aberrant migration into the scrotum can result in local inflammatory reactions accompanied by painful swelling of affected tissues.
Although high prevalence has been reported in some endemic areas, setariosis is mostly clinically inapparent. Clinical signs can be severe in cases of aberrant migration and definitive development of worms in the CNS and eyes.
Verminous meningoencephalomyelitis: Most reports come from Sri Lanka, India and Burma, where setariosis is known as ‘kumri ’ (word derived from Hindustani, meaning ‘weak back ’). The clinical signs include muscular weakness, incoordination, ataxia, and paralysis.
Ocular setariosis: Ophthalmia with photophobia, excessive lachrymation, conjunctivitis, opacity of the cornea, hypopyon and iridocyclitis in the anterior chamber of the eye, and eventually blindness can be observed. Whitish worms rapidly moving in the anterior chamber of the eye are sometimes noticed.
Presumptive diagnosis: Neurological clinical signs and ophthalmia can be indicative of setariosis. The definitive diagnosis of parasitic encephalomyelitis and its aetiology is only possible following a post-mortem examination.
Parasitological diagnosis: The parasitological diagnosis in live horses is based on the identification of microfilariae found in blood. Microfilariae can be detected microscopically in wet blood films, and stained thin and thick blood films. For increased sensitivity, concentration techniques like membrane filtration, the modified Knott ’s test, or microhaematocrit centrifugation should be used.
Whitish worms rapidly moving in the anterior chamber of the eye are sometimes visible. Specimens removed surgically can be identified on morphological criteria.
Other microfilariae reported in the blood of horses are Elaeophora boehmi . However, these microfilariae are unsheathed and larger (length: 300 to 330 μm, width: 6 to 7 μm). Elaeophora boehmi has only been reported from Europe and Asia.
Other causes of equine parasitic encephalomyelitis in horses include Strongylus vulgaris, Strongylus equinus, Angiostrongylus cantonensis, Draschia megastoma, Halicephalobus deletrix, Hypoderma species and Sarcocystis neurona.
Treatment: The macrocyclic lactone ivermectin has been reported to have both macrofilaricidal and microfilaricidal properties. Macrofilariae in the anterior chamber of the eye can be removed surgically.
Control: Control is not necessary because of the very minor clinical importance of S. equina.
Horse tapeworm (Anoplocephalidosis)
Anoplocephalidosis of horses is caused by Anoplocephala perfoliata, Anoplocephala magna, and Anoplocephaloides mamillana (syn. Paranoplocephala mamillana) –all members of the family Anoplocephalidae. Also known collectively as anoplocephalids, many characteristics are shared particularly with respect to morphology, life cycle and epidemiology. In South Africa, as in Europe and North America, A. perfoliata is the most commonly encountered tapeworm of horses.
The family and genus names are derived from the Greek words ‘anoplos ’ (unarmed) and ‘kephale ’ (head) –which is descriptive and refers to the scoleces that lack a rostellum and are fitted with 4 unarmed (devoid of hooks) suckers. The anoplocephalids of horses are small to mediumsized tapeworms ranging from 1 to 52 cm in length ( Figure 60 ). Depending on the species, the strobila consists of numerous proglottids of the craspedote type –which are wider than long and are provided with 1 set of reproductive organs. Genital pores are unilateral.
The eggs of all species of Anoplocephalidae are collectively referred to as anoplocephalid- type eggs or anoplocephalid eggs. Anoplocephalid eggs are thick-shelled and have an irregularly spherical shape. Inside the egg, the first larval stage, known as an oncosphere, is covered by the embryophore. The embryophore is typically elongated and pear-shaped, and is known as the pyriform apparatus (Latin ‘pirum ’ - pear, Latin ‘formis ’ - shaped).
The type of metacestode (second larval stage developing in intermediate hosts and infective stage for definitive host) developing in the life cycle of anoplocephalids is a cysticercoid.
The predilection site of the strobilar stages of A. magna and A. mamillana is the small intestine. The predilection site of A. perfoliata is the ileo-caecal valve –which is unusual for strobilar stages of tapeworms. Comparative morphological details regarding the anoplocephalids of horses covered in this chapter can be obtained from Table 8.
Apart from horses, the definitive host range for the three species also includes mules, donkeys and zebras.
The three species have a cosmopolitan distribution.
Anoplocephalids have an indirect life cycle, which requires an oribatid mite as an intermediate host.
Gravid proglottids containing eggs –as well as eggs released from proglottids in the intestines –are shed into the environment with the faeces. The already embryonated eggs are immediately infective for oribatid mites and are ingested by the mites on the ground. Released oncospheres penetrate the gut wall and develop in the haemocoel to cysticercoids. The incubation period in mites is temperature-dependent and may take 2 to 4 months. Definitive hosts become infected by ingesting oribatid mites harbouring cysticercoids while grazing. The pre-patent period is 6 to 10 weeks.
Colic is the most important cause of morbidity and mortality in horses and Anoplocephala perfoliata is regarded as a risk factor for this syndrome. The expense of diagnostic procedures, registered products for deworming, and veterinary costs in surgical colic cases are considerable –and beyond the reach of resource-poor animal owners.
Pathogenesis and pathology
Anoplocephala perfoliata and A. magna are associated with lesions and clinical signs whose severity is related to the worm burden. No pathogenic effects have been ascribed to A. mamillana.
Anoplocephala perfoliata: Attachment of the strobilar stage commonly causes obstructive lesions due to mucosal inflammation, oedema, ulceration and the formation of diphtheritic membranes. Eventually, this may result in catarrhal enteritis, ileal impaction, intussusceptions, caecal torsions and ruptures, with subsequent peritonitis developing.
Anoplocephala magna: Catarrhal or haemorrhagic enteritis –and even rupture of the small intestine –has been described in horses harbouring heavy worm burdens.
The appearance and severity of clinical signs in horses is related to the worm burden. Apart from indigestion and episodes of diarrhoea, Anoplocephala perfoliata is regarded as a significant risk factor for colic in horses.
Catarrhal and haemorrhagic diarrhoea can be seen in horses harbouring heavy worm burdens of A. magna.
Diagnosis in live animals
Presumptive clinical diagnosis: A history of diarrhoea and recurrent episodes of colic might indicate the involvement of anoplocephalid tapeworms.
Parasitological diagnosis: The parasitological diagnosis is based on the demonstration of eggs in faecal samples. Since most eggs are retained in gravid proglottids, shedding of eggs is erratic and occurs at a very low level. Therefore, the sensitivity of faecal examination –irrespective of the coprological technique used –is unsatisfactory and leads to an underestimation of prevalence. The coprological technique of choice is combined centrifugal sedimentation/ flotation, which is more sensitive than routine faecal flotation techniques. There are numerous variations of the sedimentation/ flotation technique described in the literature.
Diagnostic deworming: Considering the difficulties in making a diagnosis in live animals, treatment with a specific cestocidal drug in suspected anoplocephalidosis should be considered.
Other important helminth infections to consider in the syndrome of colic are cyathostomins, Parascaris equorum in particularly foals and yearlings, Gastrodiscus aegyptiacus , and large strongyles.
Treatment: There are comparatively few anthelmintics that are reported to be effective for the treatment of anoplocephalidosis. As for many other cestode infections of domestic and wild animals, the isoquinoline praziquantel (1 mg/kg) is highly effective for anoplocephalidosis. Also indicated is the salicylanilide niclosamide (80 to 100 mg/ kg), and, although variable efficacy has been reported, also the tetrahydropyrimidine pyrantel (6.6 mg base/kg, 13.2 mg base/ kg, 19.8 mg base/kg).
Prevention: The control of this infection is highly problematic due to the ubiquity of oribatid mites. Regular removal of faeces, rotational grazing, ploughing and veld burning are measures to consider in problem studs –as they affect the oribatid mite populations.
Table 8 Anoplocephalids of horses
|Characteristics||A. perfoliata||A. magna||A. mamillana|
|Maximum width of strobila (mm)||8-14||25||4-6|
| Scolex ||2-3 Spherical Ear-shaped lappet posterior to each sucker||3-5 Circular No lappets||1 Slit-like No lappets|
| Egg ||Irregularly spherical 65-80 8-10 16||Irregularly spherical 70-84 4 8||Irregularly spherical 37-51 4 22|
|Predilection site||Ileocaecal valve (caudal ileum, caecum, proximal colon)||Small intestine||Small intestine|
Conical Fluke (Gastrodiscosis)
Gastrodiscosis of horses is caused by Gastrodiscus aegyptiacus . The genus name is derived from the Greek words ’gastros ‘ (stomach, belly) and ’discus ‘ (disc). The species is a hermaphrodite, dorsoventrally flattened amphistome with a small, anterior conical part (4 mm long and 3 mm wide) and a disc-shaped posterior part that gives the worm the typical ‘tennis-racket ’-shaped appearance ( Figure 61 ). The oral and ventral suckers are situated terminally at the anterior and posterior extremities of the body, respectively. Fresh specimens are pink in colour. Adult worms are 12 to 18 mm long and 10 to 14 mm wide.
The predilection site of G. aegyptiacus is the caecum and colon. The eggs are oval and large-sized (140 to 170 x 90 to 100 μm). They are colourless, thin-shelled with a distinct operculum, and contain coarse granular material.
Apart from horses, the definitive host range includes other equids, domestic pigs, and warthogs.
Gastrodiscus aegyptiacus occurs through out Africa and there are also isolated records from India, Guyana, Suriname, Cuba and Guadeloupe.
Gastrodiscus aegyptiacus has an indirect life cycle, which requires a freshwater snail as intermediate host. Sexually mature worms are oviparous. Eggs are shed with the faeces into the environment, but are highly sensitive to desiccation. Provided there is sufficient ambient moisture, eggs remain viable for several months. Depending on the prevailing temperature and availability of water, a first larval stage, known as miracidium, develops within the egg in as little as 14 to 16 days. The miracidium hatches from the egg and swims actively in the water.
The aquatic pulmonate freshwater snail Bulinus forskalii serves as the only known intermediate host. Typical habitats are permanent collections of water (swamps, lake margins, irrigation systems) –as well as small temporary and permanent water bodies. The snail has an Afrotropical distribution, but is not encountered in the cool highlands and the Western Cape Province of South Africa. The miracidium invades the snail and develops to a sporocyst. Within the sporocyst, several rediae are produced by means of polyembryony. Asexual reproduction continues within the rediae –which results in the formation of cercariae. The incubation period in the snail is temperature dependent and may be as short as 5 weeks. Cercariae leave the snail and encyst within 1 hour on partially inundated vegetation, near the water surface.
Similar to other paramphistomids and the liver flukes, the metacercarial stage appears to be partially resistant to desiccation. Ingesting metacercariae while grazing in swampy areas or by consuming contaminated hay harvested from infested areas, infects definitive hosts. Metacercariae excyst following ingestion. The emerging immature flukes do not undergo any extra-intestinal development, and attach to the mucosa of the colon. The pre-patent period for G. aegyptiacus –in horses –is about 5 months.
Gastrosdiscus aegyptiacus can be an important cause of diarrhoea and colic in horses.
Pathogenesis and pathology
Pathogenicity appears to be related to worm burden. Although generally regarded as non-pathogenic in the past, there is evidence from South Africa and Guyana that a severe haemorrhagic and oedematous colitis could be attributed to the presence of large numbers of the parasite.
Mild infections in horses are clinically inapparent and mostly undetectable. Recurrent colic attacks, chronic diarrhoea, weight loss, poor performance, and anaemia –as well as incoordination and collapse –were reported in horses with high worm burdens prior to death.
The diagnosis in live animals is based on the demonstration of eggs in faecal samples, using sedimentation.
Although rarely reported in South Africa, infections with Fasciola hepatica and Fasciola gigantica have to be taken into consideration. Fasciola eggs are also large-sized, oval, thin-shelled and operculate. However, in contrast to G.aegyptiacus, they are yellowish-brown and contain fine granular material.
Other important helminth infections to consider as a cause of colic are particularly cyathostomins, Parascaris equorum in foals and yearlings, Anoplocephala perfoliata , and large strongyles.
Treatment: The organophosphate dichlorvos given at a dose rate of 35-40 mg/kg is highly effective against G. aegyptiacus infection in horses; however, there are no longer registered products available. As the only known alternative, the salicylanilide oxyclozanide at a dose rate of 8.5 mg/kg is used off label. Important to consider, is that oxyclozanide is only available in combination with levamisole in South Africa. Because of the low safety margin in equids and the limited efficacy against many equine nematodes, the use of levamisole is restricted to ruminants, pigs and poultry.
Prevention: Clinical gastrodiscosis in horses can be effectively prevented by proper farm and grazing management. Horses and other equids should ideally not share pastures with free-ranging pigs or be kept on pastures that can be accessed by warthogs. Horses should be watered with fresh water and the origin of hay should be carefully investigated. Banks of perennial and seasonal, stagnant, or flowing water bodies should be avoided as they are typical habitats of B. forskalii. Where possible, fencing off identified snail habitats can be effective.
Liver fluke (Fasciolosis)
Fasciolosis of horses is caused by Fasciola hepatica and Fasciola gigantica, which are also colloquially known as the ‘liver fluke ’and ‘giant liver fluke ’, respectively. The genus name is derived from the Latin word ‘fasciola ’ (small ribbon). Fasciola species are hermaphrodite, dorsoventrally flattened, leaf-like distomes, with a distinct head cone. Microscopically, the cuticle is covered with scale-like spines. The oral sucker and the slightly larger ventral sucker are situated in close proximity at the head cone. Fresh specimens are pale brown.
Fasciola hepatica adult worms are 20 to 50 mm long and 4 to 13 mm wide (length to width ratio is ±2). Fasciola gigantica adult worms have a narrower body and are 25 to 75 mm long and 3 to 11 mm wide (length to width ratio is ±4.5).
The predilection sites of both species in the definitive host are the hepatic bile ducts. The immature and mature flukes are haematophagous and histophagous.
The eggs are oval, large-sized (F. hepatica 130-150 x 63-90 μm, F. gigantica 156-197 x 90-104 μm) and contain fine granular material. They are typically yellowishbrown in colour, thin-shelled, and have an indistinct operculum.
The metacercariae are circular, 310-350 μm in diameter and are attached to herbage in water or flotsam. They can detach and float free in water or settle at the bottom of water bodies.
The definitive host range includes a broad spectrum of herbivorous and omnivorous mammals –including humans. The principal definitive hosts are cattle and small stock. Although horses and other equids are regarded as unusual hosts for Fasciola species, a high prevalence has been reported in endemic areas.
Fasciola hepatica has a cosmopolitan distribution with a higher prevalence in temperate climates. In Africa it appears to be more restricted to the northern Mediterranean countries, as well as to southern Zimbabwe and South Africa.
Fasciola gigantica is more common in tropical and subtropical regions and is widespread in Africa and Asia.
Fasciola species have an indirect life cycle, which requires a freshwater snail as an intermediate host.
Sexually mature worms are oviparous. Eggs are shed with the faeces into the environment, and are highly sensitive to desiccation and temperatures below freezing point. With sufficient ambient moisture, eggs remain viable for several months. Depending on the prevailing temperature and availability of water, a first larval stage, known as a miracidium, develops within the egg within as little as 10 to 15 days. The miracidium hatches from the egg and swims actively in the water.
Various freshwater snail species of the family Lymnaeidae act as intermediate hosts. According to their habitat requirements, lymnaeids can be divided into amphibious and aquatic species. In South Africa the aquatic snail Lymnaea (Pseudosuccinea) columella is an intermediate host for both Fasciola species. Likewise, the amphibious Lymnaea (Galba) truncatula is an intermediate host for F. hepatica and the aquatic (Radix) natalensis for F. gigantica. Lymnaea columella was originally a North American species. Introduced into South Africa, it is widely distributed and found with L. natalensis. The snail is known to move out of the water onto vegetation and objects. The species has an Afrotropical distribution, but in South Africa is not found in the Western Cape Province. Typical habitats are permanent water bodies (streams, impoundments, dams). Lymnaea truncatula has a mainly Holarctic distribution (in the northern hemisphere), and in South Africa is found in the cooler areas and Lesotho. Typical habitats are permanent collections of water (banks and edges of small streams and ponds) –as well as temporary bodies of rainwater such as puddles, hoof marks and wheel ruts. The miracidium invades the snail and develops to a sporocyst. Within the sporocyst, several rediae are produced by means of polyembryony. Under unfavourable conditions a second redial generation might also develop. Asexual reproduction continues within the rediae, which results in the formation of cercariae. The incubation period in the snail is temperature dependent and may take as little as 6 to 10 weeks. Cercariae leave the snail and encyst on aquatic vegetation, flotsam or directly in the water. The metacercarial stage is partially resistant to desiccation and is known to remain infective for 4 to 6 months in contaminated hay. High temperatures of over 40 °C, and excessive dryness, will kill the metacercariae within hours. Definitive hosts become infected by ingesting metacercariae attached to hay, aquatic vegetation, or drinking water from the bottom of infested water bodies. Metacercariae excyst following ingestion. The emerging immature flukes penetrate the wall of the small intestine and migrate intra-abdominally to the liver, where they are found in the parenchyma within 24 hours of infection. Migration in the liver parenchyma continues for 6 to 7 weeks before the flukes settle in the hepatic bile ducts. The pre-patent period for Fasciola species in horses is 2 to 3 months. Not all infections become patent in horses.
In contrast to cattle and small stock, fasciolosis in horses is of minor clinical importance and seldom requires treatment.
Humans can act as definitive host for both Fasciola species. Cases of human fasciolosis have been reported from Africa, the Americas, Asia, Australia, Europe and Oceania. It is believed that human infection is under-reported. Vegetables grown in snail-infested habitats which are grazed by ruminants are a common source of human infection.
Pathogenesis and pathology
Horses demonstrate a pronounced resistance to liver fluke infection. Only a small percentage of ingested metacercariae reach the bile ducts –where they become sexually mature. Nevertheless, a high prevalence has been reported in various endemic areas. A chronic and a subacute form of fasciolosis have been described in horses. The chronic form is characterised by mild cholangitis, interstitial fibrosis, and eosinophilia. The subacute form is characterised by perihepatic fibrosis and peritonitis caused by immature flukes migrating through the liver parenchyma. Infection is easily overlooked during necropsy, as macroscopic lesions are rarely noticed –even in heavily infected horses.
Most infections in horses are clinically inapparent. Only rarely does fasciolosis clinically manifest in its chronic or subacute form. The clinical signs observed in chronic fasciolosis are unspecific and comprise inappetence, weight loss, diarrhoea, light anaemia, and icterus. Abdominal oedema and colic-like symptoms have also been reported in the subacute form.
The diagnosis in live animals is based on the demonstration of eggs in faecal samples by using sedimentation. Since only small numbers of eggs are shed, larger faecal samples (50 g) should be examined.
Common infections with Gastrodiscus aegyptiacus have to be taken into consideration. The eggs of G. aegyptiacus are also large, oval, thin-shelled and operculated. However, in contrast to Fasciola species, they are colourless and contain coarse granular material.
Treatment: The benzimidazole triclabendazole (12 mg/kg) is highly effective for adults of Fasciola hepatica; however, immature flukes are not always completely removed.
Prevention: Fasciolosis in horses can be effectively prevented by proper farm and grazing management. Horses should ideally not share pastures with ruminants. Marshy areas, which constitute potential lymnaeid snail habitats, should be avoided –particularly if grazed previously by domestic ruminants. Fencing off identified snail habitats can be effective.
Helminths of companion animals
Author: E VOLKER SCHWAN
Ancylostomosis of dogs and cats is caused by the nematodes Ancylostoma caninum, Ancylostoma braziliense and Ancylostoma tubaeforme . The genus name derives from the Greek words ‘ankylos ’ (= bent) and ‘stoma ’ (= mouth), which, like the common name ‘hookworm ’, are descriptive terms referring to their dorsally bent (‘hook posture ’) anterior end. Hookworms are medium-sized, with a length of 5-25 mm. They have a large buccal capsule, which is armed with teeth. The posterior end of the males terminates in a strongylate bursa. The spicules are equal. The female ’s caudal end tapers gradually and the vulva is located in the posterior third of the body.
Male Ancylostoma caninum worms are 10- 13 mm long and the female worms 14-21 mm long. Both are about 0.5 mm wide. The worms have a large buccal capsule, which is armed with 3 pairs of ventral teeth. Spicules are equal and measure 800-950 μm in length.
Male Ancylostoma braziliense are 5-8 mm long and the females 7-11 mm long. Both are about 0.3 mm wide. The worms have a large elongated buccal capsule armed with 2 pairs of ventral teeth, of which the lateral ones are large and the medial ones small. Spicules are equal and measure 700-1 000 μm in length.
Ancylostoma tubaeforme closely resembles A. caninum but is smaller. Male worms are 9.5-11.0 mm long and female worms 12- 15 mm long. Both are about 0.4 mm wide. Their spicules are larger than those of A. caninum and measure 1 100-1 700 μm in length.
As for all hookworms, the small intestine is the site of predilection of the three species in their definitive hosts.
The eggs of the ancylostomatids of dogs and cats are of the strongylid-type. They are oval, thin-shelled, contain 4-8 blastomeres when laid, and measure 55-95 by 32-58 μm. The eggs of the three species are indistinguishable.
- Ancylostoma caninum: In addition to dogs, the definitive host range includes sylvatic canids, and some of the sylvatic felids, ursids, procyonids and mustelids.
- Ancylostoma braziliense: In addition to dogs and cats, the definitive host range includes sylvatic canids, felids and mustelids.
- Ancylostoma tubaeforme: In addition to cats, the definitive host range includes a wide range of sylvatic felids.
Ancylostoma caninum is mainly encountered in subtropical and tropical areas, but its range extends into the temperate zones of all continents. Ancylostoma braziliense is found exclusively in tropical and subtropica l areas, while Ancylostoma tubaeforme has a cosmopolitan distribution.
All hookworm species have a direct life cycle. Eggs are shed with the faeces and –depending on the environmental temperature and humidity –there is typically a pre-parasitic development from egg to free-living L1, L2 and then finally, a sheathed infective L3, in as few as 4-5 days. Free-living infective larvae can remain viable for 3-4 months in damp soil.
There are various modes of infection for dogs and cats that vary depending on the species of hookworm involved:
- Percutaneous infection (A. caninum, A. braziliense, A. tubaeforme)
- Transmammary (lactogenic) infection (A. caninum)
- Infection by predation on paratenic hosts (A. caninum, A. braziliense, A. tubaeforme)
- Infection by ingestion of free-living infective larvae (A. caninum, A. braziliense, A. tubaeforme)
- Autoinfection (A. caninum)
Ancylostoma caninum: Following percutaneous infection, infective larvae follow a blood-tracheal migration route. However, when larvae are ingested orally –for example during transmammary ingestion, ingestion of free-living larvae or ingestion of paratenic hosts, –there appears to be no larval migration. The larvae remain in the intestinal tract and develop directly in the small intestine. Transmammary infection in dogs is regarded as the most important mode of infection.
Infection induces immunity with the result that larvae acquired by older dogs largely adopt a somatic migratory route. These larvae do not develop further and eventually become arrested in the musculature and fat tissue. Arrested larvae remain viable for several years and are reactivated during pregnancy. Reactivated larvae are the source for transmammary infection of litters and autoinfection of bitches. Also, in paratenic hosts, larvae do not develop further and become arrested during the course of their somatic migration. Depending on the mode of infection, the prepatent period is 15-26 days.
Ancylostoma braziliense: Little is known about the modes of infection in dogs and cats. The prepatent period is 13-27 days.
Ancylostoma tubaeforme: Percutaneous infection and infection by ingestion of paratenic hosts and free-living infective larvae appear to be equally important. The prepatent period is 19-22 days.
With the Toxocara spp., A. caninum and A. tubaeforme are the most common and important nematodes of young dogs and cats, and, as the main causes of clinical verminosis, deworming programmes in cats and dogs focus mainly on these two species.
Ancylostoma braziliense is only mildly pathogenic and is of lesser importance.
All hookworm species of dogs, cats and other domestic animals have zoonotic implications and they are one of the causes of cutaneous larva migrans in humans. Cutaneous larva migrans is also colloquially known as ‘creeping eruption ’, ‘plumber ’s itch ’or ‘duckhunter ’s itch ’. Humans are infected percutaneously by free-living infective larvae. Infection is acquired following direct contact of the skin with damp ground which is contaminated with dog or cat faeces.
Larval migration in humans is restricted to the subcutaneous tissue and manifests clinically as itching and the appearance of serpiginous, tunnel-like skin lesions. Larvae migrate 3-5 cm a day and can remain active for several weeks –after which they eventually die off. Many of the cases resolve spontaneously without treatment.
Pathogenesis and pathology
Ancylostoma caninum and A. tubaeforme can be highly pathogenic –particularly when large worm burdens occur. In contrast, Ancylostoma braziliense is only mildly pathogenic. The pathogenesis varies according to the developmental phase of the parasites (migratory and lumenal).
Larval migratory phase: Penetration of the skin by large numbers of invading larvae occurs particularly in the interdigital spaces of the paws, on the limbs, the ventral part of chest, and on the abdomen. Continued exposure elicits a hypersensitivity –causing severe itching. Larval migration of A. caninum through the lungs in puppies can cause alveolar haemorrhage, oedema, and bronchopneumonia, following secondary bacterial infection.
Lumenal phase: Hookworm larvae and adults in the small intestine are haematophagous and histophagous. The volume of blood consumed by the worms differs between species; of the hookworms, A. caninum (80-200 μl/worm/day) and A. tubaeforme consume the most blood. The worms continuously change their site of attachment every 4-6 hours. As a result of the trauma inflicted by attaching to the mucosa, small petechial haemorrhages develop and blood oozes into the intestinal lumen and mucosal lesions. Heavy worm burdens cause a haemorrhagic enteritis ( Figure 62 ). Progressive blood loss over time causes anaemia, metabolic acidosis, and hypoproteinaemia.
Ancylostoma braziliense does not cause anaemia in their hosts, since individual worms consume only a minute amount of blood (1-2 μl/worm/day).
The severity of clinical signs depends on the size of the worm burden, the age, and the nutritional and immunological status of the infected animal. Mild infections in both puppies and kittens and in older dogs and cats can be subclinical.
Puppies with heavy A. caninum burdens, –especially those acquired via the transmammary route –are prone to develop severe and often fatal clinical infections. Bronchopneumonia is the most common clinical picture in these cases. Coughing, a nasal discharge, and rarely epistaxis, are the result of tracheal migration in puppies. Heavy intestinal burdens of Ancylostoma caninum and A. tubaeforme cause progressive development of anaemia, diarrhoea containing mucus and sometimes blood, and also dehydration. Other signs observed during this phase are impaired development, weight loss, a dull coat and inappetence.
Following severe percutaneous infections, localized pruritus with urticaria and alopecia develop in the interdigital spaces of the paws, on the limbs, and on the ventral part of the chest and abdomen. This skin condition is also known as ‘moist summer eczema ’.
Presumptive clinical diagnosis: The concurrent presence of anaemia, mucoid or haemorrhagic diarrhoea, weight loss, inappetence, anorexia, and retarded development –in particularly puppies and kittens –is a strong indication of hookworm infection.
Parasitological diagnosis: The parasitological diagnosis in live animals is confirmed by demonstrating worm eggs in faecal material, by means of direct flotation. In the early stages of heavy infections it is difficult to make an etiological diagnosis since the parasites are still in their prepatent period, and the diagnosis cannot be confirmed by faecal flotation.
There are numerous other causes of anaemia and diarrhoea that should be considered as a differential diagnosis for hookworm infection. These are canine and feline babesiosis, canine leishmaniosis, canine monocytic ehrlichiosis, other helminth infections such as toxocarosis, trichuriosis, feline immunodeficiency virus and feline leukaemia virus infections, viral gastroenteritis caused by parvovirus and coronavirus, giardiasis, bacterial enteritis, poor nutrition, and drug reactions. For puppies with respiratory signs, other causes such as toxocarosis, kennel cough, and oslerosis should be excluded.
Treatment and control
With the exception of the piperazines, the same spectrum of anthelmintics listed for the treatment of toxocarosis is applicable for the treatment of ancylostomosis in dogs and cats. For details, see under Control section of Toxocara ( below ).
Ascarid worms (Toxocarosis)
Toxocarosis of dogs is caused by infections with Toxocara canis, and toxocarosis of cats by Toxocara cati (syn Toxocara mystax) . The genus name is derived from the Greek words ‘toxon ’(= arrow, projectile, arch) which refers to the lanceolate or arrow-like appearance of the parasite ’s head and ‘ascaris ’ (= intestinal worm). Adult worms are easily recognized by their large size and typical ascarid appearance ( Figure 63 ).
In contrast to the related ascarid species Toxascaris leonina , the oesophagus of Toxocara spp. has a prominent posterior muscular bulb. The posterior end of the male tail of Toxocara has a finger-like process. In females, the vulva is located in the anterior fourth of the body.
Male Toxocara canis worms are 10-12 cm long and females 12-18 cm long. Both are about 2-3 mm wide. A pair of prominent, lanceolate cervical alae is visible microscopically. The spicules are slightly unequal and they are 750-1 300 μm long.
Male Toxocara cati worms are 6-7 cm long and females up to 10 cm long. Both are about 2 mm wide. A pair of prominent alae is visible microscopically, and they have an arrowhead-like shape.
The eggs of both Toxocara spp. are subspherical and have a thick, finely pitted, brown shell, which gives them a golf balllike appearance. Toxocara canis eggs are 75-90 μm in diameter and T. cati eggs 65-75 μm in diameter.
Toxocara ascarids are intestinal parasites, and in companion animals they have a direct life cycle. Intestinal migration, somatic migration (prenatal infection in dogs) and transmammary infection are the most important modes of infection. Tracheal migration is not very common in Toxocara spp.
In addition to dogs, the definitive host range of T. canis includes a wide range of sylvatic canids. The definitive host range of T. cati includes domestic cats and a wide range of sylvatic felids, martens, mongooses, coatis, and civets.
Toxocara canis and T. cati have a cosmopolitan distribution.
Both species have a direct life cycle. The eggs are shed with the faeces into the environment. The eggs are highly resistant to the effects of the environment and can remain viable for up to 4 years. Depending on the ambient temperature, the infective L3 develops within the egg in as little as 2 weeks. Depending on the route of infection, the prepatent period ranges between 3 and 5 weeks.
There are various routes and methods of infection in dogs and cats:
- Infection by ingestion of larvated eggs (T. canis, T. cati)
- Transmammary (lactogenic) infection (T. canis, T. cati)
- Prenatal infection (T. canis)
- Infection by predation on paratenic hosts (T. canis, T. cati)
- Post-partum infection of bitches (T. canis)
The predilection site in ascarids of dogs and cats is the small intestine. Following ingestion of larvated eggs, infected paratenic hosts or milk in the case of transmammary infection, infective larvae enter the small blood vessels in the small intestine and migrate via the hepatotracheal route in non-immune hosts. L4 stages settle in the small intestine, where the final moult takes place. Infection induces immunity with the result that newly acquired larvae do not develop; they migrate somatically and eventually become arrested to remain as dormant larvae in various organs and in the musculature, liver, kidneys and CNS. Arrested larvae remain viable for several years and can become reactivated during pregnancy to become the source of larvae for transmammary and prenatal infections of litters. Infective larvae in paratenic hosts do not develop and become arrested in granulomas during the course of somatic migration. Post-partum infection of bitches occurs by ingestion of larvae passed in the faeces of heavily infected puppies.
Hookworms and the Toxocara ascarid worms are the most common and important nematodes of puppies and kittens. Deworming of adult dogs and cats mainly focuses on these helminths.
Toxocara canis and T. mystax have zoonotic implications and are one of the causes of visceral larva migrans in humans. Humans become infected by ingesting larvated eggs. Clinical visceral larva migrans mainly features in young children, who contract infection by playing in contaminated soil or playgrounds through geophagia or by direct contact with infected dogs. Hatched larvae do not develop further and localise –as in other paratenic hosts –in the musculature, liver, CNS, eyes and other organs where they become entrapped in granulomas elicited by their presence. Most infections are sub-clinical.
The clinical signs of Toxocara visceral larval migrans are non-specific and include fever, respiratory signs, lymphadenopathy, hepato- splenomegaly, and indistinct neurological signs. Ocular larval migrans is a specific form of visceral larva migrans in which the eye is affected. Larvae migrating in the eye can cause endophthalmitis and formation of granulomas mostly in the retina, which can lead to irreversible, partial or complete blindness.
Most cases resolve without treatment. Treatment of problematic cases is usually unsatisfactory.
Pathogenesis and pathology
The development and locality of the lesions are associated with the following two developmental phases of the parasites:
Larval migratory phase: Larval migration through the liver and lungs causes the formation of widely disseminated microgranulomas in the liver, lungs, kidneys, and heart.
Lumenal phase: In the small intestine the worms are responsible for mucosal defects, intestinal obstruction, and occasional intestinal perforation. Migration of worms to aberrant sites such as the bile and pancreatic ducts may occur where they cause obstruction of the ducts and related clinical signs.
Metabolic products of the ascarids can interfere with parathormone production, which may result in rickets.
Mild infections in both puppies and kittens, and older dogs and cats, are often clinically inapparent.
Puppies and kittens that become heavily infected via the transmammary route or in the case of T. canis, the prenatal route, show clinical signs that are dependent on the developmental phases of the parasite in the definitive host. During larval migration, coughing and nasal discharge are common clinical signs. Intestinal parasitism results in frequent vomiting, the development of a ‘pot-bellied ’abdomen which is sensitive to pressure, colic, and constipation alternating with diarrhoea. Sometimes intact worms are found in vomit and stools. Other signs that may be observed include anorexia, weight loss, impaired development, a dull coat, nervous disorders, and bone deformities.
Presumptive clinical diagnosis: Clinical signs in puppies and kittens as listed are indicative of a Toxocara infection. Respiratory signs are initially seen during the prepatent period in animals with heavy infections. Haematology will show a marked eosinophilia.
Parasitological diagnosis: The parasitological diagnosis in live animals is based on the demonstration of eggs in faecal samples by means of direct flotation and faecal smears. Towards the end of the prepatent period, immature worms may be passed in stools and vomitus. Worms passed in stools and vomit should be differentiated from the related Toxascaris leonina.
The differential diagnosis will differ depending on the stage and therefore site of the infection
During the respiratory phase prepatent hookworm infections, kennel cough, and oslerosis should be considered.
In animals with the intestinal phase, the differential diagnosis should consider other causes of diarrhoea and vomiting such as viral gastroenteritis (parvovirus and coronavirus infections), other helminth infections (toxocarosis, trichuriosis), giardiosis, bacterial enteritis, poor nutrition, and side effects of drugs.
The control of hookworm and ascarid roundworms in dogs and cats is very important, not only from an animal health and welfare point of view, but also because of the zoonotic potential –as discussed above.
The eggs of both Toxocara spp. are very resistant to environmental conditions, thus making it impractical to control dog and cat roundworms via environmental decontamination. Toxocara eggs can also survive composting and sewage treatment. Environmental contamination –the removal of dog and cat faeces on residential properties and the prevention of dogs defecating in public areas –is very important for controlling the spread of roundworm eggs. Cleaning of bedding and floors in kennels is critical for preventing contamination of kennels. The floors of kennels must preferably be concrete to make cleaning of the kennels easier. Overcrowding in kennels and catteries and long-term confinement must also be avoided. The prevention of environmental contamination must be combined with the treatment of infected dogs and cats by an effective anthelmintic.
Suitable remedies: There are several anthelmintics belonging to various chemical groups that can be used for the treatment of hookworm and toxocarosis in dogs and cats. Some registered products contain two nematocides and may include a cestocide such as praziquantel. Note that a few of the actives mentioned below are only suitable for use in dogs. The following are registered for use in the treatment of roundworm infections in dogs and cats:
- Piperazines: Piperazine salts
- Benzimidazoles: Fenbendazole
- Probenzimidazoles: Febantel (D)
- Imidazothiazoles: Levamisole
- Tetrahydropyrimidines: Pyrantel
(hookworm only), oxantel (D)
- Isothyocyanates: Nitroscanate (D)
- Macrocyclic lactones: milbemycin,
moxidectin, selamectin, ivermectin
- Cyclic octadepsipeptides: Emodepside (C)
Treatment and control:
- Pregnant and lactating animals: Suckling puppies and kittens are very susceptible to roundworm infection from hookworm (Ancylostoma spp.) and roundworm (Toxocara spp.). Bitches and queens therefore need to be treated with an anthelmintic at mating time and again at whelping –to decrease prenatal infections. During lactation the dam needs to be treated every two weeks to prevent reactivated larvae from being established in the dam ’s gut and infecting the puppies/kittens, and to prevent the dam from getting re-infected from the environment. The most common route of infection in suckling puppies is via the transmammary and prenatal infection route from the reactivation of encysted larvae in the dam. Treatment of these arrested larvae will be beneficial in decreasing the incidents of prenatal infections. Most anthelmintics given at the recommended dose will not treat these dormant larvae present in the tissues of the bitch. Fenbendazole given to a pregnant bitch at 25mg/kg daily from the 40th day of pregnancy –until 2 days post-partum –has been shown to substantially reduce postnatal infection. This is, however, a time consuming and expensive treatment regime for owners to follow. Alternatively, macrocyclic lactones, iver mectin and doramectin (injected at 1mg/kg subcutaneously), given once on day 55 or 56 of pregnancy, or moxidectin (injected at 1mg/kg subcutaneously) given on days 40 and 50 has been known to decrease vertical infection of roundworms from the dam to puppies, while still in utero. Note, however, that the treatment of a pregnant dam as described above is extralabel, as none of the canine and feline anthelmintic products are registered for the treatment regimens described above. Certain herding type dog breeds, primarily Collies, Shetland Sheep Dogs and Australian Shepherds are known to be highly sensitive to macrocyclic lactones, and treatment in these breeds must be done with extreme caution.
- Puppies and kittens: Intestinal parasite infections in neonates may cause serious illness or even death before a diagnosis is possible via faecal examination –thus making the control of roundworms in neonates very important. Neonates can get infected with roundworms by picking up larvae in the environment or via the transmammary route from an infected dam. The selection of the correct anthelmintic for use in neonates is important. The products that can be safely used in neonates are those containing piperazine, fenbendazole, febantel, pyrantel and oxantel(D), nitroscanate(D) and milbemycin. It takes 2 weeks for hookworms to mature and to start laying eggs and therefore effective control in neonates will require treatment every two weeks starting from 2 weeks of age in puppies and 6 weeks of age in kittens –until weaning at 12 weeks. After weaning, puppies and kittens need to be treated monthly until they are 6 months of age –after which they can be treated every 3 months.
- Dog and cats over 6 months of age: The aim of treatment of dogs and cats over 6 months of age is to lower environmental contamination of roundworms, prevent zoonotic transmission, and to prevent clinical signs of infection in dogs and cats. Most companies that market worm treatments advise deworming adult cats and dogs every 3 months, 4 times a year. This can be increased to monthly treatment in areas where the risk of infection is higher. Ideally, this should be combined with regular faecal examination to ascertain the response to treatment.
- Cost of treatment for hookworm and ascarid prevention: The frequency of treatment required for adequate control of these roundworms can be expensive, in particular the macrocyclic lactones including milbemycin and selamectin, as well as the newer remedy emodepside. Pyrantel and oxantel are cheaper, while nitroscanate and generic piperazines are even more economical. Fenbendazole intended for livestock use can be used extra-label by veterinarians as another cheaper option.
- Pyrantel resistance: Pyrantel resistance in A. caninum has been confirmed in Brisbane in Australia and it is suspected that this may occur in other subtropical cities. The situation in South Africa is unknown.
Toxascariosis of dogs and cats is caused by infection with the nematode Toxascaris leonina . The genus name is derived from the Greek word ‘toxon ’ (= arrow, projectile, arch) which refers to the lanceolate appearance of the head, and ‘ascaris ’ (= intestinal worm). Its predilection site is the small intestine. Being a typical ascarid, adult worms are easily recognisable because of their comparatively large size. In contrast to the related Toxocara spp., the oesophagus of T. leonina , which can be visualised in cleared specimens, lacks a posterior bulb. Male worms are 6-7 cm long and female worms 6-10 cm long –and both are about 2 mm wide. A pair of prominent lanceolate cervical alae can be seen microscopically. Eggs of T. leonina are spherical, 70-85 μm in diameter and have a thick, smooth and colourless shell.
Apart from dogs and cats, the definitive host range includes a wide range of sylvatic carnivores.
Toxascaris has a cosmopolitan distribution.
Toxascaris leonina has a direct life cycle. Female worms lay a large number of eggs which are shed with the faeces into the environment. The eggs are highly resistant to adverse environmental conditions and can remain viable for several years. Depending on the ambient temperature, an infective L3 can develop in the egg within 8 days.
The only modes of infection in dogs and cats are ingestion of larvated eggs or of infected paratenic hosts (eg mice). Infective larvae undergo a histotropic phase in the mucosa of the small intestine during which time the third moult takes place. Larvae re-enter the intestinal lumen where they develop to adults. The prepatent period is 7-10 weeks.
Toxascaris leonina is less common and less important than the Toxocara spp. There are no reports of infections in humans.
Pathogenesis and pathology
Since there is no prenatal or transmammary transmission, worm burdens are smaller and their pathogenic effects minor compared to those of Toxocara infections in puppies and kittens.
Toxascaris leonina can cause enteritis if dogs and cats carry large worm burdens.
The parasitological diagnosis in live animals is based on the demonstration of eggs in faecal samples by means of direct flotation and faecal smears.
As for Toxocarosis .
The drug spectrum and hygiene measures listed for toxocarosis are also applicable to the control of toxascariosis.
Spirocerca lupi (spirocercosis)
Spirocercosis of dogs is caused by the nematode Spirocerca lupi . The genus name is derived from the Greek word ‘speira ’ (= coil, thread) which refers to the appearance of fresh adult specimens which are blood-red and coiled. Adult worms are medium-sized. Male worms are 3-5 cm long and females 5-8 cm long, and they are about 1 mm wide. The worms have a typically hexagonal mouth opening that can be seen microscopically, while the male ’s posterior end is spiral in shape and bears caudal alae. The spicules are unequal and are 2.4-2.8 mm (left) and 0.47-0.75 mm (right) long. The tail of the female is blunt and the vulva is located in the oesophageal region.
The typical predilection sites are the wall of the caudal part of the thoracic oesophagus and the cardia of the stomach –where they are found embedded in fibrous nodules that protrude into the lumen. To a lesser extent, worms are found in aberrant locations such as in the kidneys and under the skin.
Eggs of S. lupi are small (22-37 x 11-15 μm), elongate with parallel sides, thickshelled, and larvated (embryonated) when laid.
Apart from dogs, which are the predominant definitive host, infections have also been reported from a range of sylvatic carnivores, and occasionally from domestic ruminants and equids.
Spirocerca lupi is widespread in tropical and subtropical parts of the world. In South Africa, infection is commonly seen in farming areas and even urban areas like Pretoria.
Spirocerca lupi has an indirect life cycle. The females are ovoviviparous –shedding embryonated eggs in the faeces and vomitus.
Various dung beetle genera are intermediate hosts of S. lupi . Following ingestion of the eggs, the L1-stages hatch and develop to the infective L3- stage. A wide spectrum of domestic and wild birds, amphibia, reptiles, and small mammals commonly prey on dung beetles and may be paratenic hosts.
Dogs are infected by either ingesting infected dung beetles or paratenic hosts (chicken scraps, birds, lizards and other potential hosts). The migratory route and larval development within the definitive host is complex and determines the distribution of the lesions caused by the parasites. After ingestion, the thirdstage larvae penetrate the gastric mucosa and enter the wall of gastric arteries to eventually reach the abdominal aorta –from where they migrate to the thoracic aorta and where they remain for up to 3 months and develop to L4-stages. From the aorta, fourth-stage larvae migrate through the thoracic cavity and reach the oesophagus 15 weeks after infection. The larvae occur in the oesophageal subepithelial connective tissue, from where they perforate the oesophageal epithelium. Once the worms are mature, eggs are shed through this perforation into the oesophageal lumen –from where they enter the intestinal tract and are shed in the faeces. The final development to the adult stage takes place in fibrous nodules in the oesophageal wall that form as a result of the host ’s inflammatory response to the worm.
The prepatent period is 4-6 months and the patent period lasts about 2 years.
In endemic and particularly in hyperendemic areas, S. lupi is one of the most important helminths of dogs due to the severity of the lesions induced, and because of the expense of diagnosis and treatment.
In addition, the diagnosis in live animals requires specialist diagnostic facilities.
The prognosis of complicated spirocercosis is poor –even with intensive treatment.
The risk of human infection worldwide is low and there is only a single report of an infant in Italy being infected.
Pathogenesis and pathology
The lesions caused by the parasite and their locality are determined by the migratory route and developmental phases of the parasite.
Larval migration phase: Larval migration in the thoracic aorta results in ‘scarring ’, which is recognised as a pathognomonic lesion of S. lupi infection. Depending on the severity of infection, this can lead to extensive internal haemorrhages and consequently death. Larvae migrating in the wall of the thoracic aorta cause degeneration of elastic tissue and replacement of collagen –which is followed by calcification and ossification. The result is the formation of aneurysms and stenosis. Sudden death as a result of rupture of an aortic aneurysm is not uncommon.
The mechanism of malignant transformation into oesophageal fibrosarcomas and osteosarcomas is poorly understood. Dogs with intrathoracic sarcomas often develop hypertrophic osteopathy (Marie ’s disease). Deformative ossifying spondylitis affecting the thoracic vertebrae is another poorly understood sequel to the infection.
Several clinical forms of spirocercosis can be differentiated.
Subclinical form: Apart from occasional regurgitation or vomiting, usually no clinical signs are observed. This is common in areas of high prevalence.
Acute haemorrhagic form: This occurs due to the invasion of the aortic wall by larvae, resulting in rupture of the aorta and consequent sudden death.
Chronic form: This results from the establishment of parasites in the oesophagus and the development of fibrous nodules ( Figure 64 ). Clinical signs observed are decreased appetite, vomiting, regurgitation, dysphagia, salivation, oedema of the throat, coughing, dyspnoea, thoracic pain, weight loss, anaemia, and weakness.
Neoplastic form: The parasitic nodules undergo neoplastic transformation, which is followed by cachexia, vomiting, regurgitation, and hypertrophic osteopathy.
Cutaneous form: Following aberrant migration, worms may localise in the subcutaneous tissues, causing protruding nodules in the skin.
The diagnosis in live dogs is problematic because of the long prepatent period of the parasite –which can be up to 6 months long. The detection of the migrating parasites during the prepatent period is difficult. The clinical diagnosis can only be confirmed by the demonstration of adult worms in oesophageal nodules or by demonstration of S. lupi eggs in the eggs using faecal flotation.
Presumptive clinical diagnosis: Animal particulars and history should be considered –for example, breed, age, origin, conditions under which animal is kept and used, changes in behaviour, changes in appetite, contact with and ingestion of lizards and other small vertebrates and insects, and a tendency to coprophagia.
General clinical signs such as chronic weight loss, vomiting, regurgitation, anaemia and weakness are indicative of the infection.
Clinical diagnosis: An initial diagnosis can be made via radiography. A typical oesophageal mass will usually be seen in radiographs. The mass is usually found in the caudal oesophagus. A moderate amount of air may be present, cranial to the mass. The mass can best be seen via a ventrodorsal (VD) or dorsoventral (DV) view as a single midline soft tissue opacity superimposing on the caudal cardiac border and diaphragmatic cupula. However, cases presented before oesophageal nodules have formed cannot be diagnosed via radiography. Small nodules or atypically located nodules may also not be visible on radiographs. Endoscopy is regarded as the technique of choice which allows the demonstration of oesophageal nodules, as it is more sensitive than radiography in diagnosing S. lupi infection where the nodules are too small to be detected on radiographs. It is important to inflate the oesophagus adequately to prevent oesophageal folds being misdiagnosed as small S. lupi nodules. Early nodules are smooth and rounded and have a pink, nipple-like protuberance through which the female lays her eggs. The nodules are typically found caudal to the heart and may extend through the cardia into the stomach. Over time the nodules may enlarge and become roughened, lobulated, cauliflowerlike masses that obliterate the oesophageal lumen. At this stage the nodules have often undergone neoplastic transformation.
Parasitological diagnosis: The parasitological diagnosis in live dogs is based on the demonstration of eggs in faecal samples by means of direct faecal flotation or combined centrifugal sedimentation/ flotation techniques ( Figure 65 ). It is essential to use flotation fluids with a high specific gravity (SG) of not less than 1.3 (eg saturated MgSO4 ). Because of the relatively small size and the small number of the eggs, faecal examination should be entrusted to the experienced laboratory diagnostician. Failure to detect eggs in a flotation procedure does not necessarily indicate a negative result since the sensitivity of faecal examination is 70-80%.
Differential diagnosisAs a result of the varied and often general clinical signs associated with S. lupi infection, the differential diagnosis list is very long.
Treatment: Uncomplicated S. lupi infections (non-neoplastic granulomas) can be treated effectively with macrocyclic lactones (MLs). Topical application of moxidectin 2.5% m/v combined with imidacloprid 10% m/v (Advocate ®Bayer) weekly for 19 weeks –starting 170 days after infection –showed a 98.5% efficacy in the treatment of S. lupi infection in eight dogs. Milbemycin oxime (Milbemax ®Novartis) at a minimum dose of 0.5 mg/kg bodyweight, given as a once-off dose 30 days post infection with S. lupi was 79.8% effective at preventing the establishment of S. lupi in the oesophagus in seven dogs. In a second study, milbimycin oxime was given at a minimum dose of 0.5 mg/kg bodyweight 28 days post-S. lupi infection to 4 dogs. The dose was repeated at 14 or 28 day intervals up to 169 days post infection. The treatment was found to be 100% effective in preventing the formation of S. lupi nodules in the oesophagus. Doramectin (Dectomax ®Zoetis, extra label) has also been used for the treatment of S. infection. A standard dosage of 0.4 mg/kg SC or orally should be given either weekly or every two weeks, until the resolution of clinical signs.
Control: In a study in the Eastern Cape Province of South Africa, 58 puppies from a S. lupi endemic area were selected for treatment. Thirty eight of these puppies received Milbemycin oxime (Milbemax ®Novartis) at a minimum dose of 0.5 mg/ kg bodyweight at 2-6 weeks of age. The puppies received five further treatments at approximately 28-day intervals. The remainder of the puppies were left as untreated controls. Twenty four of the 27 control dogs became infected with S. lupi infection as demonstrated by aortic nodules. This treatment regime reduced the severity of the aortic lesions and significantly reduced the number of oesophageal nodules in the treated dogs.
Use of MLs in dog breeds prone to ABCB1 (formerly MDR1 gene) mutations: MLs must be used with caution in dog breeds that are prone to ABCB1 gene (formerly MDR1 gene) mutations –which predispose them to toxicity.
The mutation is typically seen in the herding type breeds –primarily Collies, Shetland Sheep Dogs and Australian Shepherds. The mutation has also been detected in Longhaired Whippets, Old English Sheepdogs, German Shepherd Dogs, Swiss Shepherd Dogs and some crosses of these breeds. Moxidectin 2.5% m/v combined with imidacloprid 10% m/v (Advocate ®Bayer) has been applied topically to confirmed ivermectin sensitive collies at five times the recommended dose –with no adverse effects.
Canine lungworm (Oslerosis)
Oslerosis of dogs is caused by the nematode Oslerus osleri (syn Filaroides osleri) . The genus is named after the Canadian physician W Osler, who first described the species. The typical predilection sites are the trachea and bronchi, where the nematodes are found within typical, flat, up to bean-sized raised nodules in the mucosa.
Outbreaks of clinical oslerosis are seen occasionally, under specific conditions, usually where dogs are kept in crowded and unhygienic conditions –for example in boarding kennels. Infection is most often seen in weaned puppies, not less than 10 weeks old.
Male worms are 4-7 mm long and females 10-15 mm long. Both are slender. The posterior end of the male is rounded and lacks a bursa. The spicules are slightly unequal and are 99-113 μm long. In females, the vulva is located close to the anus.
The eggs of O. osleri are oval and thinshelled and measure 80-120 x 60-70 μm. They contain a larva (L1-stage) when laid. Some of the eggs hatch in the trachea and may be seen in faecal examination. Larvae have a typical S-shaped tail.
The definitive host range includes sylvatic carnivores, but O. osleri is not a common parasite of dogs.
Oslerus osleri has a cosmopolitan distribution.
Oslerus osleri is an unusual nematode since no development is required outside of the definitive host. Oslerus osleri has a direct life cycle. Females are ovoviviparous, i.e . they produce embryonated eggs.
Dogs of all ages are susceptible to the infection. The definitive host is infected by ingesting L1-stage larvae shed in expectorations, saliva, vomitus and faeces (coprophagia). Infection is mainly acquired by young puppies from the bitch through licking and cleaning soon after birth and by regurgitational feeding of puppies. After entering the intestinal wall, infective larvae migrate via the lymphatictracheal route. The prepatent period is 10 weeks and the patent period extends over several years.
Oslerosis in dogs is of minor importance. There are no reports of O. osleri in humans.
Pathogenesis and pathology
In the trachea and bronchi, worms develop in submucosal nodules which form as a result of an inflammatory host response. Nodules are flat and millet- to beansized. Nodules narrow the lumen of the air passages, which impacts on breathing ( Figure 66 ).
Many infections are clinically inapparent. The clinical picture is that of chronic tracheobronchitis. Clinical signs usually include respiratory distress and a chronic, dry (non-productive) paroxysmal cough, which can be induced by exercise. Other signs include inappetence, vomiting and weight loss.
Presumptive clinical diagnosis: A febrile chronic tracheobronchitis not responding to antibiotics is indicative for oslerosis. Important to consider are animal details and history (e.g. age, when and where acquired, and recent stay in boarding kennel).
Clinical diagnosis: Endoscopy is regarded as the technique of choice, which allows the demonstration of nodular lesions in the trachea and bronchi. Radiography is unsatisfactory.
Parasitological diagnosis: Some of the infective L1-stage larvae already hatch in the respiratory tract and occur together with unhatched eggs in sputum and faeces.
The parasitological diagnosis in live dogs is based on the demonstration of larvated eggs and larvae in the sediment of tracheal lavage samples. Demonstration of larvae in faecal samples is less sensitive and can be attempted by flotation with ZnSO4 .
Other causes of chronic tracheobronchitis that should be considered as differential diagnoses include infectious tracheobronchitis (kennel cough), prepatent toxocarosis and ancylostomosis, other metastrongylid infections, dirofilariosis, tracheal collapse, and cardiovascular disease.
Treatment: Fenbendazole and oxfendazole at a dose rate of 50 mg/kg daily for 15 consecutive days and ivermectin have been used successfully extra-label for the treatment of oslerosis in dogs.
Control: Hygiene in boarding and breeding kennels is essential to prevent infections. Regular removal of faeces, washing and disinfection of cages is essential.
Filarial worms of dogs (Acanthocheilonemosis)
Acanthocheilonemosis of dogs is caused by the nematodes Acanthocheilonema reconditum, and Acanthocheilonema dracunculoides. Acanthocheilonemosis is of minor clinical importance and therefore only very occasionally might require veterinary intervention. A. reconditum occurs in the subcutaneous fascia of the limbs and back, while A. dracunculoides occurs mainly in the abdominal and to a lesser extent in the thoracic cavity
The genus name is derived from the Greek words ‘acantha ’ (= spiny, thorny), ‘cheilos ’ (= lip) and ‘nema ’ (= thread). Acanthocheilonema species are medium to large nematodes and have an atrophied stoma. The posterior end of males is tapering and spirally coiled, and the spicules are dissimilar in length and shape. The posterior end of females is digitate and the vulva is located in the oesophageal region of the body. Female worms are viviparous and produce unsheathed L1-stages known as microfilariae.
Refer to Table 9 for the comparative morphological details of A. reconditum and A. dracunculoides .
In domestic carnivores, A. reconditum , and A. dracunculoides are only found in dogs –but their host range includes some wild canids and hyaenids.
Acanthocheilonema reconditum has a cosmopolitan distribution. Only sparse information is available regarding Africa, but it is known to be endemic in South Africa and neighbouring Botswana and Mozambique. In South Africa, A. reconditum is commonly encountered in neglected dogs.
Acanthocheilonema dracunculoides has been reported from Africa, Asia and Europe. In Africa it is widely distributed and is also endemic in South Africa and neighbouring Namibia, Zimbabwe, and Mozambique. Infection is commonly encountered in dogs in Namibia –but rarely in South Africa.
All Acanthocheilonema species have an indirect life cycle. Microfilariae produced by females appear in the blood nonperiodically.
The Acanthocheilonema species are transmitted by a number of vectors. The vectors become infected by obtaining blood-meals from microfilaraemic dogs. In the vector, the microfilariae develop to the infective L3-stages (metacyclic larvae). The incubation period for A. reconditum in the cat flea (Ctenocephalides felis) may be as short as 7 days. Fleas (Ctenocephalides canis, Ctenocephalides felis, Pulex irritans) and to a lesser extent lice (Heterodoxus spiniger, Linognathus setosus) act as intermediate hosts (vectors) for A. reconditum. The louse fly (Hippobosca longipennis ) and the kennel tick (Rhipicephalus sanguineus) are the vectors of A. dracunculoides .
Definitive hosts become infected when the vectors feed. The migration pattern after infection with metacyclic larvae, and their further development in definitive hosts, is unknown for both species. The prepatent period for A. reconditum is 2-3 ½months, but it is not known for A. dracunculoides .
Acanthocheilonemosis is important as a differential diagnosis of heartworm infection. Diagnosis of the disease in live animals requires specialist diagnostic procedures –which are expensive.
Acanthocheilonema reconditum and A. dracunculoides do not have zoonotic implications.
Pathogenesis and pathology
Acanthocheilonema reconditum and A. dracunculoides are regarded as largely non-pathogenic.
Isolated cases of pruritic dermatitis and focal alopecia have been attributed to A. reconditum infections with high microfilaraemias. Similarly, there are reports of animals infected with A. dracunculoides presenting with pruritus, alopecia, erythema of the skin, skin ulcers, ascites, pleural effusion, ataxia, incoordination and cachexia.
The parasitological diagnosis in live animals is based on the demonstration of unsheathed microfilariae found in blood. Microfilariae can be detected in wet blood films, stained thin blood films and by the capillary haematocrit tube method. For increased sensitivity, concentration techniques such as membrane filtration, preferably, or the modified Knott ’s test should be used. In order to determine the species, histochemical staining for acid phosphatase activity is required ( Table 9 ). Adult worms in the abdominal cavity are commonly encountered during spays.
Infections with filariids of the genus Dirofilaria and Brugia have to be taken into consideration. For a complete discussion of the differential diagnosis and how to distinguish between the different microfilaria, refer to the section dealing with dirofilariosis.
Table 9 Comparative morphology of the Acanthocheilonema spp. of dogs
|A. reconditum||A. dracunculoides|
| Adult stages ||21-36 mm x 0.07-0.2 mm 9-17 mm x 0.07-0.13 mm 220-300 μm (l) and 92-104 μm (r)||30-60 mm x 0.2-0.37 mm 15-31 mm x 0.1-0.31 mm 320-402 μm (l) and 120-186 μm (r)|
| Microfilariae ||Unsheathed 168-292 μm x 4-6.7 μm Uniform with lighter area from cephalic end to excretory vesicle or diffuse denser staining at excretory pore, inner body and anal pore||Unsheathed 121-277 μm x 3.1-7.4 μm Cephalic space, excretory pore, inner body, anal pore|
Treatment: Macrocyclic lactones are suitable for the treatment of microfilaraemic dogs. Refer to the section dealing with dirofilariosis for full detail of treatment regimes
Control: Infection with A. reconditum is commonly seen in neglected dogs in South Africa. Flea control can effectively prevent infection.
Dirofilariosis of dogs and cats is caused by the nematodes Dirofilaria immitis and Dirofilaria repens. Dirofilaria immitis is also known by the common names ‘heartworm ’and ‘canine heartworm ’, and it typically occurs in the right ventricle, right auricle, and the pulmonary artery. Infection is also referred to as cardiovascular dirofilariosis. Dirofilaria repens typically occurs in the subcutaneous connective tissue and the fascial sheaths of the hind legs. Infection is also referred to as cutaneous dirofilariosis. Dirofilaria repens is mainly important as a differential diagnosis of heartworm infection.
The genus name is derived from the Latin words ‘diruo ’ (= to destroy, to ruin) and ‘filum ’ (= thread) and refers to the pathogenic effects of some of these filiform (thread-like) worms. Dirofilaria species are medium to large nematodes and have an atrophied stoma. The posterior end of the male is spirally coiled, rounded and fitted with alae. The spicules are dissimilar in length and shape. The posterior end of the female is rounded and the vulva is located just posterior to the oesophageal region.
Female worms are viviparous and produce unsheathed L1-stages known as microfilariae.
Refer to Table 10 for the comparative morphological details of D. immitis and D. repens .
Dogs are the principal definitive hosts of Dirofilaria immitis . Cats are less susceptible and are regarded as an insignificant reservoir. The host range also includes some wild canids, felids, other mammals and humans. However, in most of these hosts infection is amicrofilaraemic and the worms are located in aberrant sites.Dogs and cats are the principal definitive hosts of Dirofilaria repens. Infection has also been reported in wild canids, felids and humans.
Increasing climatic changes and movement of people with their pets are important factors for the continuous spreading of the parasite.
Dirofilaria immitis has an almost cosmopolitan distribution and occurs in tropical, subtropical and temperate regions. In Africa it is known to be endemic in Morocco, Algeria, Tunisia, Egypt, Senegal, Ethiopia, Kenya, Tanzania, Malawi, Mozambique, Gabon, DRC, Angola, Madagascar, Mauritius and R éunion. In South Africa heartworm has so far only been reported in imported dogs.
Dirofilaria repens has been reported from Europe, Asia and Africa. In Africa it is widely distributed and is also endemic in South Africa, where it is common –particularly in the coastal areas of KwaZulu-Natal.
Dirofilaria species have an indirect life cycle. Microfilariae produced by females appear in the blood. The presence of microfilariae of D. immitis and D. repens in the peripheral blood of dogs and cats is irregular and mainly nocturnal. Only 20% of D. immitisinfected cats become microfilaraemic and then only for a very short period.
Various culicine and anopheline mosquitoes act as intermediate hosts (vectors) for both Dirofilaria spp. Female mosquitoes become infected by obtaining blood meals from microfilaraemic dogs and cats. In the vector, microfilariae develop to infective L3-stages (metacyclic larvae), which eventually accumulate in the proboscis. The incubation period in vectors is largely temperature-dependent and may be as short as 10 days.
Definitive hosts become infected during feeding by the vectors when the metacyclic larvae actively leave the labella of the proboscis and enter the puncture wound on their own.
In the definitive hosts the metacyclic larvae of D. immitis develop further during a complex migration through various body tissues and reach the predilection sites after 70-120 days.
The migratory route of metacyclic larvae of D. repens and their further development in definitive hosts is unknown. The prepatent period is 6-9 months for D. immitis and 6-8 months for D. repens . Filarial helminths of the genus Dirofilaria are long-lived. Similarly microfilariae in the blood remain viable and infective for up to 2 ½years.
In endemic and particularly hyperendemic areas, heartworm is one of the most important helminths of dogs and cats, due to its severe pathogenic effects and the financial implications for owners.
Diagnosis in live animals requires specialist diagnostic facilities, which are expensive as is treatment. The availability of drugs is also problematic in many endemic countries.
Dirofilaria immitis infection of humans is very rare with about 230 cases reported worldwide and it is mostly asymptomatic. Adult worms are mainly found in the lungs, and present incidentally as ‘coin lesions ’during chest radiography. However, Dirofilaria repens infection of humans is more common and probably underdiagnosed and under-reported. In the more common superficial form, worms are found in nodules in the subcutaneous and submucosal connective tissue of the head, chest and upper limbs. The head, eyelids and conjunctivae are most frequently affected. Nodular lesions in the less common visceral form can be misdiagnosed as neoplastic growths.
Pathogenesis and pathology
In cardiovascular dirofilariosis ( Figure 67 ), the pathogenic stages are the pre-adult and adult worms, also referred to as macrofilariae –at the predilection sites. Microfilariae are largely non-pathogenic. Depending on worm burden, duration of infection and host response, cardiovascular dirofilariosis ultimately develops into a multisystemic disorder which affects the lungs, heart, liver and kidneys. Inflammatory reactions in the pulmonary arterial system and associated mechanical effects interfere with the blood flow which eventually results in pulmonary hypertension and right-sided heart failure, causing chronic venous congestion. Chronic venous congestion is often accompanied by ascites, oedema of limbs, hydrothorax and hydropericard.
In the past, Dirofilaria repens has been regarded as non-pathogenic in dogs and cats. However, there are several reports of pruritic dermatitis which are thought to be caused by microfilariae and the movement of adults in the subcutaneous tissue. Protruding nodules in the skin of infected animals are sometimes noticed.
Cardiovascular dirofilariosis of dogs and cats can go clinically unnoticed. Clinical signs associated with heartworm infection are principally a reflection of the macrofilarial worm burden, duration of infection, and host-parasite interaction. Clinically, cardiovascular dirofilariosis can be classified into various forms:
- Mild, asymptomatic form which is mostly detected incidentally.
- Moderate form, which presents with exercise intolerance, chronic cough, dyspnoea, and progressive weight loss.
- Severe form characterised by rightsided congestive heart failure, syncope, an acute or chronic vena cava syndrome, and sudden death (particularly in cats).
Cutaneous dirofilariosis of dogs and cats, in contrast, is largely asymptomatic and non-pathogenic. Adults can sometimes provoke the formation of protruding nodules in the skin. Microfilariae and migrating adults are known to cause a pruritic pseudo-eczematous dermatitis in some dogs.
The diagnosis of cardiovascular dirofilariosis in live animals is problematic, due to the long prepatent period of D. immitis .
Presumptive diagnosis: The typical clinical signs, and a history of the animal originating or having stayed temporarily in an endemic or suspected endemic area, are indicative of cardiovascular dirofilariosis.
Parasitological diagnosis: The parasitological diagnosis in live dogs is based on the demonstration of unsheathed microfilariae in blood. Microfilariae can be detected in wet blood films, stained thin and thick blood films, and by the capillary haematocrit tube method. For increased sensitivity, concentration techniques such as membrane filtration, preferably, or the modified Knott ’s test, should be used. To differentiate between the microfilariae of the two Dirofilaria species and microfilariae of the genus Acanthocheilonema , histochemical staining for acid phosphatase activity is required. Acid phosphatase staining is considered the most reliable, consistent and practical technique for species identification of microfilariae in dogs and cats ( Table 10 ).
Dealing with the differential diagnosis and interpretation of blood from infected animals may be challenging and should be done by diagnosticians with specialist training. When interpreting the findings, infections with filariids of the genus Acanthocheilonema and Brugia should also be taken into consideration. Acanthocheilonema reconditum and Acanthocheilonema dracunculoides have unsheathed microfilariae that appear in blood and are similar to the Dirofilaria spp. The microfilariae of Brugia species are sheathed. With the exception of Brugia patei , which is endemic in Kenya and Tanzania, all other Brugia species found in dogs and cats –namely Brugia malayi, Brugia pahangi and Brugia ceylonensis –are endemic and limited to Asia, and should be considered in imported animals presenting with signs of heartworm disease.
Cats infected with heartworm are usually amicrofilaraemic and the confirmation of the final diagnosis largely depends on serology.
Antigen detection methods: enzymelinked immunosorbent (ELISA) and immunochromatographic assays are available. These methods have the advantage of detecting occult (amicrofilaraemic), patent infections. However, their lack of sensitivity poses a problem in areas of low prevalence and in newly-colonised areas. In these cases, the use of concentration techniques is recommended. The tests are also not specific enough to exclude false positives due to D. repens infections.
Serological tests are used in cats due to their amicrofilaraemic infections and low worm burdens.
Clinical diagnosis: Further clinical diagnostic procedures such as radiography and echocardiography might also be required.
The clinical differential diagnosis is dependent on the parasite species and the stage of development of the disease.
Treatment: Cardiovascular dirofilariosis in dogs is treated initially by administering macrofilaricides (adulticides), followed by the application of microfilaricides.
Table 10 Comparative morphology of Dirofilaria spp. of dogs and cats
|D. immitis||D. repens|
| Adult stages ||21-31 cm x 1.0-1.3 mm 12-20 cm x 0.6-0.9 mm 300-355 μm (l) and 175-229 μm (r)||8.4-17.0 cm x 0.38-0.65 mm 3.9-7.0 cm x 0.27-0.45 mm 338-590 μm (l) and 123-206 μm (r)|
| Microfilariae ||Unsheathed 180-340 μm x 5-7 μm Excretory and anal pore||Unsheathed 207-385 μm x 5-9 μm Anal pore or anal pore and inner body|
The arsenical melarsomine is currently the drug of choice in dogs. Treatment may cause systemic reactions precipitated by disintegrating worms, which may necessitate supportive treatment with anti-inflammatories and parenteral fluids. This is a problem –particularly in cats.
The concurrent administration of the antibiotic doxycycline is recommended in conjunction with melarsomine, because it targets the Wolbachia endosymbionts of D. immitis .
Microfilaricidal therapy should be applied 3-4 weeks after completion of the macrofilaricidal therapy in dogs. The macrocyclic lactones ivermectin, milbemycin, moxidectin and selamectin are suitable for this purpose. As with the macrofilarial treatment, severe systemic reactions may occur and therefore treated animals should be hospitalised and closely monitored for 12 hours following treatment.
To prevent establishing cardiovascular dirofilarosis in non-endemic areas, infected dogs should be quarantined in mosquito-proof cages during treatment.
Due to the largely non-pathogenic nature of D. repens , treatment is not recommended.
Control: Prophylactic treatment for heartworm is indicated for those dogs and cats living in or travelling to an endemic area. The macrocyclic lactones ivermectin, milbemycin oxime, moxidectin and selamectin given monthly –are suitable for this purpose.
Cardiovascular dirofilariosis is a notifiable disease in South Africa. To prevent D. immitis from becoming endemic in South Africa, imported dogs are quarantined and screened for infection.
Trichuriosis of dogs is caused by the nematode Trichuris vulpis . Feline trichuriosis is caused by Trichuris campanula and Trichuris serrata , both of which are comparatively rare and have only been described in the Americas, some Caribbean Islands, and Australia. The parasites typically occur in the caecum and colon.
The genus name is derived from the Greek words ‘trichos ’ (= hair) and ‘ura ’ (= tail), which, like the common name ‘whipworm ’, are descriptive and refer to the peculiar filament-like, slender cephalic end and a thick caudal end. Males of T. vulpis are 45-60 mm long and female worms 62-75 mm long. The anterior part, which constitutes ⅔ of the body length, is 0.1-0.2 mm wide, whereas the posterior part is about 0.5 mm wide.
Microscopically, the presence of a stylet protruding from the small buccal capsule can be seen. The buccal capsule leads into a long typical trichuroid oesophagus. The posterior end of the male is coiled and there is a single spicule, 8.5-11.0 mm long. The spicule is surrounded by a protrusible, spinous sheath. The female caudal end is blunt and the vulva is located at the level of the end of the oesophagus.
Eggs of T. vulpis are medium-sized (70- 93 μm by 37-40 μm), characteristically lemon-shaped, yellowish-brown and have a thick, smooth shell with prominent projecting plugs at both poles.
Dogs and a range of sylvatic canids are the definitive hosts of T. vulpis. All ages are susceptible. The effects of trichuriosis are more severe under poor husbandry conditions. However, clinical trichuriosis also occurs in well-kept and regularly dewormed dogs, often as the result of being exposed to a heavily infected environment which is a source of continual reinfection.
Trichuris vulpis has a cosmopolitan distribution.
Trichuris vulpis has a direct life cycle. The females are oviparous and the eggs are voided with the faeces into the environment. Trichuris spp. eggs are highly resistant and can remain viable in the environment for 4-5 years.
Depending on the ambient temperature, infective L1-larvae develop in the egg within 9-10 days.
Dogs become infected by ingesting larvated eggs, either via contaminated food, drinking water, by coprophagia, or by grooming the coat of infected dogs. The ingested larvae hatch and migrate into the mucosa of the small and large intestines (histotropic phase) for 10 days –during which time they develop to L2. Second-stage larvae migrate back into the lumen of the caecum and colon, where they remain attached to the mucosa and mature to adults. The prepatent period is 2-3 months.
Trichuris vulpis is an important nematode of dogs, although they are less commonly encountered than hookworms and ascarids. Because of the long prepatent period, patent infections are only seen in animals older than 3 months.
Trichuris vulpis is not a zoonosis. Trichuriosis of humans is caused by Trichuris trichiura.
Pathogenesis and pathology
The lumenal developmental stages are haematophagic and they burrow with their anterior ends into the caecal and colonic mucosa.
The worms are not stationary, but continuously change their site of attachment. Small petechial haemorrhages with blood oozing into the lumen, catarrhal inflammation with small epithelial defects, hyperaemia, and oedema are caused by the trauma inflicted by the worms attaching to the mucosa. Haemorrhagic inflammation with intestinal contents containing blood can be observed when large worm burdens occur. Although the worms are haematophagic, the amount of blood withdrawn by individual worms (±5 μl blood/worm/day) is negligible. The anaemia seen in these cases is most likely the result of indirect blood loss due to haemorrhage from the injured mucosa where the worms attach.
Dogs mostly harbour low worm burdens, and the infection remains clinically inapparent. Build-up of large worm burdens, particularly in older dogs, is not uncommon and they may then present with severe clinical signs reflecting typhlitis and colitis. They manifest abdominal pain, chronic diarrhoea alternating with constipation, tenesmus, and vomiting. Stools are mucoid and often contain blood.
There are also signs of chronic weight loss, dehydration, a dull coat, anaemia, and inappetence. The outcome is rarely fatal.
Presumptive clinical diagnosis: A history of chronic diarrhoea alternating with constipation, the voiding of mucoid bloodtinged stools, and weight loss is indicative of trichuriosis.
Parasitological diagnosis: The parasitological diagnosis in live animals is based on the detection of eggs in faecal samples by means of direct flotation. Direct flotation is more sensitive when flotation fluids with a high specific gravity of 1,3 is used (saturated MgSO4 or ZnSO4 solution).
Other causes of diarrhoea that should be considered include helminth infections (toxocarosis, trichuriosis), giardiosis, viral gastroenteritis (parvovirus and coronavirus infections), bacterial infections, poor nutrition, and side effects of drugs.
When doing faecal examinations, Trichuris eggs should be distinguished from those of the Capillaria spp. Capillaria eggs are colourless and have less prominent projecting ‘plugs ’at either pole. Depending on the species, they are either barrelshaped with sides almost parallel, or lemon-shaped. False positive faecal flotation results can be obtained when animals ingest trichurid eggs with prey –for example rodents or as a result of coprophagia.
Treatment: There are a number of anthelmintics from the various anthelmintic groups that are effective when used for the treatment of trichuriosis in dogs. Most drugs are used in combinations and also together with specific cestocides such as praziquantel.
The following are effective:
- Benzimidazoles: Fenbendazole
- Probenzimidazoles: Febantel
- Tetrahydropyrimidines: Oxantel
- Macrocyclic lactones: Milbemycin, Moxidectin
Control: See the section on the control of toxocarosis for general control principles.
Taeniosis of domestic carnivores is caused by the strobilar stages of Taenia hydatigena, Taenia pisiformis, Taenia ovis, Taenia multiceps, Taenia serialis and Taenia taeniaeformis. The Taenia spp., together with the Echinococcus spp. in the family Taeniidae , are collectively referred to as taeniids. These parasites share many characteristics –particularly with respect to their morphology, life cycle, and epidemiology. The small intestine is the predilection site of the strobilar stages of Taenia hydatigena, Taenia pisiformis, Taenia ovis, Taenia multiceps, Taenia serialis, and Taenia taeniaeformis .
The genus name Taenia is derived from the Greek word ‘tainia ’ , which was later latinized to ‘taenia ’ , meaning tape. Taenia spp. are typically large tapeworms and the species found in dogs and cats range from 0.2 m to 2.5 m in length. The scolex of the Taenia spp. of dogs and cats has four suckers and a rostellum armed with one row of small, and one row of large hooks. The size and number of the rostellar hooks are of diagnostic importance and allow identification to species level. The strobila is typically large and consists of up to several 100 proglottids. Mature proglottids are rectangular, wider than long and are provided with one set of reproductive organs. Genital pores are marginal and alternate irregularly. Gravid proglottids are also rectangular, but longer (1-2 cm) than wide (0.5-1.0 cm), and contain a uterus with a median stem and lateral diverticula. Depending on the species, gravid proglottids contain between 15 000 and 100 000 eggs each.
Comparative information on the Taenia spp. of dogs and cats is presented in Table 11 .
The eggs of all species in the family Taeniidae (including Echinococcus spp.) are indistinguishable morphologically and morphometrically. Collectively they are referred to as taeniid-type eggs or taeniid eggs. Taeniid eggs are spherical, about 40 μm in diameter and consist of an oncosphere (first larval stage), which is surrounded by a 5 μm-thick striated embryophore.
The types of metacestode (second larval stage developing in intermediate hosts and infective stage for definitive host) in the life cycle of Taenia spp. are the cysticercus, coenurus and strobilocercus. Macroscopically, the metacestode types have no or small similarities with the intestinal strobilar stages. Descriptive scientific names were allocated to the metacestodes of some Taenia spp. developing in intermediate hosts, and although no longer regarded as valid, they are still much in use in the literature and meat-inspection regulations of various countries ( Table 11 ).
Apart from dogs and cats, the Taenia spp. covered in this chapter have a wide range of definitive hosts, particularly amongst sylvatic canids and to a lesser extent in felids. Regarding domestic carnivores, T. hydatigena, T. ovis and T. multiceps are only found in dogs and T. taeniaeformis is only encountered in cats. Taenia pisiformis is found in dogs and rarely in cats. Taenia serialis is a parasite of both dogs and cats. In South Africa, infections with T. hydatigena, T. multiceps and T. taeniaeformis are most commonly seen ( Figures 68 - 71 ).
Table 11 Comparative characteristics of Taenia spp. of dogs and cats
|T. hydatigena||T. pisiformis||T. ovis||T. multiceps||T. serialis||T. taeniaeformis|
|Strobila r stage (length)||50-250 cm||36-200 cm||45-146 cm||21-120 cm||20-27 cm||15-60 cm|
|Scolex (number of large and small hooks)||26-44||34-48||24-38||11-34||26-34||26-52|
|Large hooks (length)||169-224 μm||200-294 μm||156-197 μm||120-185 μm||110-177 μm||294-485 μm|
|Small hooks (length)||110-160 μm||114-177 μm||96-138 μm||73-160 μm||63-129 μm||187-293 μm|
|Number of lateral diverticula of uterus||5-10||8-20||11-25||9-26||8-25||5-11|
|Definitive hosts||Dog||Dog, cat (rare)||Dog||Dog||Dog, cat||Cat|
|Common intermediate hosts||Sheep, goat, pig||Lagomorphs||Sheep, goat||Sheep, goat||Lagomorphs, rodents||Rodents|
|‘Scientific name ’of metacestode||Cysticercus tenuicollis||Cysticercus pisiformis||Cysticercus ovis||Coenurus cerebralis||Coenurus serialis||Strobilocercus fasciolaris|
|Morphology of metacestode||Semitransparent, chicken eggsized cyst with single invaginated scolex||Pea-sized cyst with single invaginated scolex||Pea-sized cyst with single invaginated scolex||Semitransparent, chicken egg-sized cyst with several invaginated scoleces arranged in random groups||Walnut-sized with several invaginated scoleces arranged in crowded lines||Strobilar-like connected to small terminal bladder, enclosed in cyst about 1 cm in Ø|
|Predilection site of metacestode in intermediate hosts (IH)||Abdominal serous surfaces||Abdominal serous surfaces||Heart, diaphragm, skeletal musculature||Brain (sheep), subcutaneous and intermuscular connective tissue (goat and other IH)||Subcutaneous and intermuscular connective tissue||Liver|
All listed Taenia spp. have a cosmopolitan distribution.
All Taenia spp. have an indirect life cycle, which requires two mammalian hosts for completion. Taenia spp. have a high biotic potential; a single gravid proglottid can contain 15 000 to 100 000 eggs. Gravid proglottids and eggs already released in the gut are voided with the faeces. However, the majority of proglottids appear to leave the host spontaneously –since gravid proglottids of Taenia spp. are motile. This implies that an infected definitive host can contaminate its environment with eggs without defaecation. Insects (especially flies), earthworms, birds, rainfall and sewage are also important for the dispersal of eggs. Embryonated eggs in gravid proglottids are immediately infective for intermediate hosts. In a suitable environment, taeniid eggs are highly resistant to physical factors and can remain infective for up to one year. Intermediate hosts become infected by ingesting eggs. Liberated oncospheres enter small blood vessels in the intestinal wall and eventually reach their predilection sites via the blood stream, and then develop into metacestodes ( Table 11 ). Metacestodes become infective for definitive hosts 2-3 months after ingestion of eggs. Dogs and cats as definitive hosts eventually become infected by ingestion of metacestodes. The prepatent period in dogs and cats is 1-3 months. Strobilar stages of Taenia spp. are long-lived; the patent period can be several years.
Figures 68 and 69 Taenia hydatigena tapeworm and the metacestode (C. tenuicollis) in a herbivore liver.
Figures 70 and 71 Taenia multiceps tapeworm and the metacestode (C. cerebralis) in the brain of a sheep.
Immunity appears not to develop in infections with Taenia spp. –as both dogs and cats become readily re-infected.
The cestode family Taeniidae has the greatest relevance in public health. For aesthetic reasons or because of zoonotic implications, infected carcasses or organs of intermediate hosts (sheep, goat, cattle, water buffalo, pigs, rabbits and game) are downgraded, destroyed or confiscated. Humans can potentially act as accidental intermediate hosts for T. multiceps and T. serialis by ingesting eggs. Sources of infection are direct contact with infected dogs and/or cats as well as contaminated drinking water and food. Coenuri may develop in the brain, eye (T. multiceps) ( Figure 71 ) and the subcutaneous or intermuscular connective tissues (T. serialis, T. multiceps) .
Pathogenesis and pathology
Other tapeworm infections such as echinococcosis, dipylidiosis, joyeuxiellosis and mesocestoidosis should be considered.
Treatment: There are several anthelmintics registered for the treatment of taeniosis in dogs and cats. None of the listed drugs has ovicidal properties:
- Isoquinolines: Praziquantel
- Isothyocyanates: Nitroscanate (dogs only)
- Diphenylmethanes: Dichlorophen
- Salicylanilides: Niclosamide
- Benzimidazoles: Fenbendazole
Control: See Echinococcosis .
Echinococcus granulosus is the principal cause of canine echinococcosis worldwide. Together with the Taenia spp., the Echinococcus spp. are grouped in the family Taeniidae and are collectively referred to as taeniids. Many characteristics are shared between the two genera, particularly with respect to morphology, life cycle and epidemiology.
The genus name Echinococcus is derived from the Greek word ‘echinos ’ (= hedgehog, hook) which refers to the rostellar hooks, and the Greek word ‘kokkos ’ (= pip, seed) which refers to the appearance and small size of the tapeworms. Echinococcus granulosus , similar to other species within the genus, does not exceed 7 mm in length. The scolex of Echinococcus spp. has four suckers and a rostellum, which is armed with one row of small hooks and one row of large hooks. The strobila usually consists of 3 proglottids, which have similar morphological features to Taenia spp. The penultimate proglottid is the mature one and the terminal proglottid is the gravid one. Gravid proglottids are longer (2-3 mm) than wide (<1 mm) and are difficult to see macroscopically. Gravid proglottids contain 600-1 500 eggs.
The eggs are typically taeniid and cannot be differentiated morphologically or morphometrically from other Echinococcus spp. and Taenia spp. Taeniid eggs are spherical, about 40 μm in diameter, and consist of an oncosphere (first larval stage), which is surrounded by a 5-μm thick striated embryophore( see taeniosis) .
The type of metacestode (second larval stage developing in intermediate hosts and infective stage for definitive host) in the life cycle of E. granulosus is a hydatid (hydatid cyst) which is a unilocular, fluidfilled bladder with a thin inner germinal layer, a thick outer acellular laminated layer, and a host-derived adventitial layer ( Figure 73 ). The germinal layer generates brood capsules which generate protoscoleces asexually. The size of hydatids can range from 1 to 20 cm in diameter; however, the usual size is 5-10 cm. The cyst fluid of fertile hydatids contains hydatid sand which consists of free-floating protoscoleces, brood capsules, detached hooklets, and calcareous bodies.
The small intestine, as with most tapeworms, is the predilection site of the strobilar stage of E. granulosus ( Figure 72 ).
Since asexual reproduction occurs in hydatid cysts, high worm burdens with thousands of specimens are common in dogs.
E. granulosus has a wide range of definitive hosts amongst sylvatic canids and felids, in addition to domestic dogs. Domestic cats, however, are not susceptible.
E. granulosus has a cosmopolitan distribution.
Echinococcus spp. have an indirect life cycle which requires two mammalian hosts for completion. Compared to Taenia, Echinococcus spp. have a far lower biotic potential. A single proglottid of E. granulosus contains 600-1 500 eggs and only a few oncospheres eventually develop into fertile hydatid cysts in intermediate hosts. Gravid proglottids contain eggs that are already released in the gut and voided with the faeces. Gravid proglottids of E. granulosus are motile, which implies that a definitive host can contaminate its environment without defaecation. Eggs are dispersed by insects (flies, beetles, ants), earthworms, birds and rainfall. As in Taenia , eggs are already embryonated and immediately infective for intermediate hosts. Echinococcus eggs are highly sensitive to desiccation. At low temperatures (10 °C) and sufficient humidity, they can remain viable for at least 7 months.
Domestic herbivorous and omnivorous ungulates including sheep, goats, cattle, water buffalo, camels, horses, and pigs act as the principal intermediate hosts. Intermediate hosts become infected by ingesting eggs. Liberated oncospheres enter small blood vessels in the intestinal wall. Many oncospheres are retained in the liver while others pass on further to settle in the lungs and less in other organs where they develop into hydatids. Hydatids become infective for definitive hosts no sooner than 6 months after ingestion of eggs. The development of protoscoleces does not depend on cyst size. In horses, fertile hydatids as small as 2 mm in diameter can be found. Dogs as definitive hosts become infected by ingestion of fertile hydatid cysts. The prepatent period is 33-58 days. The patent period is up to one year. In hyperendemic areas, dogs develop a partial immunity –with higher prevalences and worm burdens in young dogs.
Cystic echinococcosis (CE), also known as cystic hydatid disease or hydatidosis, is the result of humans becoming accidentally infected by ingesting eggs of E. granulosus. Cystic echinococcosis can be regarded as the most important and widespread zoonotic disease of canine origin. Humans act as intermediate hosts with the metacestode developing mostly in the liver (>50%), followed by the lungs and less so in other sites such as the spleen, kidneys, central nervous system, subcutaneous connective tissue, and bone. Hydatid cysts typically grow slowly to a large size in humans and can be up to 25 cm in diameter. Infection is often asymptomatic with infections diagnosed on routine examination. Abdominal distension is commonly noticed in advanced cases. Hydatids developing in the central nervous system cause intracranial pressure and paralysis. Sudden rupture of hydatids and spillage of cyst fluid into body cavities may culminate in a fatal anaphylactic reaction. The most common sources of infection are direct contact with infected dogs and contaminated drinking water and food (especially vegetables and fruit). In areas where hydatidosis is prevalent, the financial implications of the expense of diagnosis and particularly treatment can be considerable for a health-care system.
Pathogenesis and pathology
Taenia and Echinococcus spp. are largely non-pathogenic in their definitive hosts. The strobilar stages attach to the mucosa of the small intestine by the rostellar hooks and suckers of the scolex. At these attachment sites, inflammatory infiltration –as well as desquamation and destruction of epithelial cells –can be noticed, although it is insignificant. Very high worm burdens (T. multiceps) can cause impaction of the small intestine, which is rare. Gravid proglottids of taeniids are motile and can leave the host spontaneously, which causes discomfort in the anal area.
Taeniid infections in dogs and cats are mostly asymptomatic. Pruritus caused by gravid proglottids migrating out of the anus may cause animals to drag and rub their anus over the ground –a behaviour which is referred to as ‘scooting ’.
Presumptive clinical diagnosis: Dogs and cats dragging and rubbing their anus over the ground can be indicative of tapeworm infection.
Parasitological diagnosis in live dogs and cats: Gravid proglottids of taeniids are motile and can be demonstrated on occasion in faeces, the perianal area or directly emerging from the anus. Gravid proglottids of Taenia spp. are whitish, longer than wide, 1-2 cm long and 0.5- 1 cm wide. Gravid proglottids of E. granulosus are also whitish and longer than wide, but only 2-3 mm long and <1 mm wide, and are very seldom noticed.
Eggs may be demonstrated following direct faecal flotation, on faecal smears or best by means of the adhesive-tape swab technique under the tail and in the perianal area. However, taeniid eggs cannot be differentiated morphometrically or morphologically. Taeniid eggs, particularly in dogs, can be those of Taenia or Echinococcus.
Coproantigen tests are highly specific and sensitive but, unfortunately, are not available commercially.
Diagnostic deworming with arecoline hydrobromide, applied as a drench or enema, is mainly used in surveys and during control campaigns for E. granulosus.
Parasitological diagnosis during necropsy: While Taenia spp. are easy to demonstrate, Echinococcus spp. are often overlooked because of their small size. For stereomicroscopic examination of intestinal content, small pieces of intestine as well as mucosal scrapings are required to positively identify carriers with low worm burdens. Considering the severe zoonotic implications of Echinococcus spp., necropsies conducted on dogs and sylvatic carnivores, as well as implementing the above-mentioned laboratory procedures, should adhere to safety precautions as recommended by WHO.
Other tapeworm infections such as taeniosis, dipylidiosis, joyeuxiellosis and mesocestoidosis should be considered.
Treatment: The isoquinoline praziquantel is the drug of choice for the treatment of echinococcosis in dogs. Although praziquantel is highly effective, treatment should be repeated to prevent residual worm burdens. Since no cestocidal drug, including praziquantel, has ovicidal properties, extreme care should be exercised when opting for treatment of infected dogs. Dogs should be confined to cages that can be cleaned and disinfected easily (concrete or tiled floors). Faeces passed up to 5 days after final treatment should be properly disposed of. After completion of treatment, dogs should be bathed to eliminate eggs attached to the fur, and cages should be disinfected. Personnel involved in the procedure should wear protective clothing.
Figures 72 and 73 Echinococcus granulosus tapeworm in a carnivore intestine and metacestode or hydatid cyst in the liver of a goat.
Control: In principle, control of canine taeniosis/echinococcosis is simple. The access to raw offal must be prevented. Abattoirs should strictly enforce the regulations of meat inspection. Infected organs should be confiscated and destroyed appropriately. Domestic carnivores, and, in particular dogs, should not have access to abattoirs.
Systematic community education in rural endemic areas is critical –where home slaughtering is practised and where dogs are utilised for herding and hunting. Feeding dogs on home-butchered domestic and hunted animals may result in high prevalence rates and massive contamination of the environment with taeniid eggs. Offal frozen at a temperature of -20 °C for at least 3 days, or, preferably cooked offal, is safe. In hyperendemic areas regular chemotherapy (every 5-6 weeks) as an individual prophylaxis can be considered, in order to prevent the establishment of patent infections with particularly Echinococcus in shepherd and hunting dogs. Taeniid eggs can be killed by temperatures of over 80 °C within a few minutes. Common disinfectants, including ethanol, propanol and formalin, have virtually no effect on taeniid eggs. Sodium hypochlorite at a concentration of 3.75% (undiluted household bleach or industrial bleach) is a suitable ovicide. The WHO has published detailed guidelines for the control of echinococcosis/ hydatidoses, which should be consulted thoroughly for the planning and execution of control programmes.
Dipylidiosis of dogs and cats is caused by the strobilar stage of Dipylidium caninum. Together with the genus Joyeuxiella, Dipylidium belongs in the family Dipylidiidae and both genera share many characteristics with respect to morphology and life cycle. As for most tapeworms, the small intestine is the predilection site of the strobilar stage of D. caninum. Dogs and cats become infected by ingesting fleas or lice harbouring cysticercoids. The prepatent period is 2-3 weeks. The patent period is up to 3 years.
Dipylidium caninum is usually 0.2-0.5 m long and only rarely reaches 0.8 m. The scolex has four suckers and a conical rostellum, which is armed with 3-5 rows of rose-thorn-shaped hooks. The large hooks are ±13 μm long, and the small hooks ±7 μm. Mature proglottids are provided with 2 sets of reproductive organs, the genital pores are bilateral (Greek ‘pylos ’ = pore, Greek ‘di ’= two, hence the genus and family names Dipylidium and Dipylidiidae) and post-equatorial. Gravid proglottids are longer than wide and typically resemble cucumber seeds. They have a reddish tinge when freshly passed and are 7-12 mm long and 1.5-3 mm wide. Within gravid proglottids, the uterus breaks up and forms egg capsules.
The egg capsules are oval and large (120 x 200 μm), and contain 2-38 eggs. The eggs are spherical, 30-50 μm in diameter, and consist of an oncosphere, which is surrounded by a very thin, striated embryophore. Within the capsule, the eggs are covered by a vitelline membrane.
The type of metacestode (second larval stage developing in an intermediate host and infective stage for the definitive host) in the life cycle of D. caninum is a cysticercoid.
In addition to dogs and cats, D. caninum has a wide range of definitive hosts that include wild canids, wild felids, and very occasionally humans
Dipylidium caninum has a cosmopolitan distribution. It is the most common tapeworm of dogs and cats in many parts of the world.
Dipylidium caninum has an indirect life cycle, which requires an arthropod and a mammalian host for completion.
Gravid proglottids containing egg capsules and egg capsules already released in the gut are voided with the faeces. As in the taeniids, the gravid proglottids of D. caninum are motile and can also leave the host spontaneously. The embryonated eggs contained in the egg capsules are immediately infective for intermediate hosts.
Fleas (Ctenocephalides felis and Ctenocephalides canis) which commonly infest dogs and cats, are the principal intermediate hosts (vectors). The human flea Pulex irritans and the chewing louse Trichodectes canis have also been identified as intermediate hosts. Eggs containing oncospheres are ingested by flea larvae or nymphal stages of T. canis . Released oncospheres penetrate the intestinal wall and develop into cysticercoids in the body fat. The development to cysticercoids is synchronised with the development of the vectors and is completed when fleas emerge from their cocoons. The incubation period in vectors is largely temperature-dependent, as is the flea development, and may be as short as 2-3 weeks.
Humans can act as definitive hosts for D. caninum. Infection in humans is accidental and is caused by swallowing adult fleas, or as a result of dogs and cats licking the owner ’s face and thereby transferring crushed fleas. Infection is very rare and mainly seen in children because of their close contact with pets. Most cases are asymptomatic.
Pathogenesis and pathology
As in the taeniids, D. caninum is largely non-pathogenic in their definitive hosts. Gravid proglottids of D. caninum are motile and can leave the host spontaneously –causing discomfort in the anal area (see Echinococcosis ).
Dipylidiosis of dogs and cats is mostly asymptomatic. Pruritus caused by gravid proglottids migrating out of the anus may cause animals to drag and rub their anus over the ground.
Presumptive clinical diagnosis: Dogs and cats dragging and rubbing their anus over the ground can be indicative of tapeworm infection.
Parasitological diagnosis in live dogs and cats: Gravid proglottids of D. caninum are motile and can occasionally be detected in faeces, the perianal area, or directly emerging from the anus. Gravid proglottids of D. caninum have a reddish tinge when freshly passed, and are longer (7-12 mm) than wide (1.5-3 mm). Dried and distorted rice-grain-like proglottids have first to be rehydrated and broken up before the egg capsules (containing several eggs; egg capsules containing a single egg are those of Joyeuxiella spp.) can be demonstrated. Eggs capsules may be demonstrated following direct faecal flotation.
Other tapeworm infections such as taeniosis, echinococcosis, joyeuxiellosis and mesocestoidosis should be considered.
Treatment: The isoquinoline praziquantel is effective for the treatment of dipylidiosis in dogs and cats. Alternatively, the isothyocyanate nitroscanate can be used for treatment of dogs –but not cats.
Control: Control of fleas and lice is essential in order to prevent dipylidiosis of dogs and cats.
Joyeuxiellosis of dogs and cats is caused by the strobilar stage of Joyeuxiella pasqualei, Joyeuxiella fuhrmanni and Joyeuxiella echinorhynchoides . The genus Joyeuxiella is named after the French parasitologist Charles Joyeux. Together with the genus Dipylidium, Joyeuxiella belongs in the family Dipylidiidae and both genera share many characteristics with respect to morphology and life cycle. As for most tapeworms, the predilection site of the strobilar stages is the small intestine.
Joyeuxiella spp. are 8-50 cm long. The scolex has four oval-shaped suckers and a conical rostellum (J. pasqualei, J. fuhrmanni) or a cylindrical rostellum with a bulbous anterior part (J. echinorhynchoides). The rostellum is armed with 8-30 rows of rose-thorn-shaped, tiny hooks –which decrease in size from the anterior towards the posterior end of the rostellum. Mature proglottids are provided with 2 sets of reproductive organs, and the genital pores are bilateral and pre-equatorial. Gravid proglottids are longer (1-6 mm) than wide (0.5-2 mm). Within gravid proglottids the uterus breaks up into egg capsules.
The egg capsules are spherical, 35-95 μm in diameter, and contain a single egg. Eggs are spherical, 28-50 μm in diameter, and consist of an oncosphere surrounded by a very thin, striated embryophore.
The type of metacestode (second larval stage developing in intermediate host and infective stage for definitive host) in the life cycle of Joyeuxiella spp. –is a cysticercoid.
In addition to dogs and cats, the definitive host range of J. pasqualei and J. echinorhynchoides includes a variety of sylvatic felids and canids. Joyeuxiella fuhrmanni, is only found in cats and in sylvatic felids and canids.
Joyeuxiella pasqualei has been reported from several countries in Europe, Asia, Africa (South Africa, Zambia and other countries) and Australia.
Joyeuxiella fuhrmanni has only been reported from Africa (South Africa, Zimbabwe, DRC).
Joyeuxiella echinorhynchoides has been reported from several countries in Europe, Asia and Africa (South Africa).
Joyeuxiella spp. have an indirect life cycle, which requires three hosts for completion. Like D. caninum , gravid proglottids are motile and can also leave the host spontaneously. Embryonated eggs contained in gravid proglottids are immediately infective for intermediate hosts.The eggs are ingested by coprophagous beetles. Reptiles and small mammals act as paratenic (transport) hosts. Definitive hosts become infected, mostly by ingesting paratenic hosts.
Joyeuxiella spp. are one of the most common cestode species of cats in some parts of the world. There are no reports of infections in humans.
Pathogenesis and pathology
See dipylidiosis .
See dipylidiosis .
See dipylidiosis .
Other tapeworm infections such as taeniosis, echinococcosis, dipylidiosis and mesocestoidosis should be considered.
Treatment: The isoquinoline praziquantel is highly effective for the treatment of the strobilar stage of Joyeuxiella spp. in dogs and cats.
Control: The control is problematic due to the large spectrum of, particularly, paratenic hosts.
Mesocestoidosis of domestic dogs and cats is caused by species of the tapeworm genus Mesocestoides. No reference is made to individual species since their taxonomic status is uncertain. As for most tapeworms, the predilection site of the strobilar stages is the small intestine. Mesocestoides spp. are medium-sized tapeworms ranging from 0.3-1.5 m in length. The scolex has four suckers and no rostellum. Mature proglottids are wider than long, and gravid proglottids are usually longer than wide. There is a single set of reproductive organs in each mature proglottid and an inconspicuous ventromedian genital pore. Gravid proglottids are barrel-shaped or club-shaped and are 4-6 mm long and 2-3 mm wide. They have a conspicuous par-uterine organ, which is 0.5 mm in diameter.
The eggs are referred to as mesocestoidid- type eggs or mesocestoidid eggs. Mesocestoidid eggs are subspherical, medium-sized (60 x 40 μm) and consist of an oncosphere surrounded by a very thin embryophore.
The type of larval stage developing in the assumed first intermediate host is unknown. The metacestode developing in the second intermediate host is known as a tetrathyridium. Tetrathyridia have a tapelike, unsegmented body with an invaginated scolex provided with four suckers. The length ranges from 1 mm to 70 mm.
In addition to dogs and cats, the definitive host range includes sylvatic carnivores, birds, and occasionally humans.
Mesocestoides spp. have a cosmopolitan distribution.
Mesocestoides spp. have an indirect life cycle, which requires three hosts for completion.
Mostly gravid proglottids containing eggs are voided with the faeces. Knowledge of the life cycle is incomplete. A diverse range of vertebrates such as amphibians, reptiles, birds and mammals are known to act as intermediate hosts which, however, cannot become directly infected by eggs. Therefore, the existence of a first intermediate host is assumed –in which the oncosphere develops into an unknown larval stage for the second intermediate host. The metacestode developing in the second intermediate hosts is a tetrathyridium which can reproduce asexually. Tetrathyridia are most commonly found in the abdominal cavity but are also in other body cavities, the liver, lungs and other sites. Infection in second intermediate hosts is also referred to as peritoneal or larval mesocestoidosis.
Definitive hosts become infected by ingestion of tetrathyridia in intermediate hosts –where they develop into strobilar stages in the small intestine. Tetrathyridia can also invade the abdominal cavity by penetrating the gut and continue to reproduce asexually or settle in various organs. The prepatent period in dogs and cats is approximately 3 weeks.
Humans can become infected accidentally by ingesting tetrathyridia in raw organs of various intermediate hosts. Most cases have been described from Asia and seem to have originated from snakes.
Pathogenesis and pathology
The strobilar stages of Mesocestoides spp. are largely non-pathogenic in dogs and cats. Migrating tetrathyridia may illicit inflammatory reactions with severe peritonitis and development of granulomas in affected organs.
Mesocestoidosis of dogs and cats is mostly asymptomatic. Peritoneal (larval) Mesocestoides infection caused by invading tetrathyridia can be severe, with animals presenting with abdominal distension, anorexia, apathy, fever, vomiting, diarrhoea, and weight loss.
Parasitological diagnosis of strobilar infections in live dogs and cats: Gravid proglottids are rarely seen in faeces. Gravid proglottids of Mesocestoides spp. are barrel- or club-shaped, and up to 4-6 mm long and 2 to 3 mm wide. Even in unstained gravid proglottids, the characteristic par-uterine organ (diameter 0.5 mm) is clearly visible. Eggs in faeces are only rarely detected successfully.
Parasitological diagnosis of peritoneal (larval) mesocestoidosis in dogs and cats: Diagnosis is based on the demonstration of tetrathyridia in abdominal exudate following abdominocentesis.
Other tapeworm infections such as taeniosis, echinococcosis, dipylidiosis, and joyeuxiellosis should be considered.
Treatment: The isoquinoline praziquantel given at the recommended dose rate is effective for the treatment of mesocestoidosis.
Peritoneal mesocestoidosis requires longterm treatment with the benzimidazole fenbendazole.
Control: No control measures can be suggested due to the incomplete knowledge of the life cycle and the large spectrum of intermediate hosts harbouring tetrathyridia.
Helminths of pigs
Author: J BOOMKER
Commercial piggeries seldom have problems with helminths because animals are raised on concrete or slatted floors which are regularly cleaned. There is, however, a growing trend to raise pigs under semi-intensive conditions –which may result in a resurgence of helminthiasis. In rural areas, pigs infected with Taenia solium via human faeces are a threat to human health since they can develop a severe form of infection called neurocysticercosis. Pigs can also be intermediate hosts of canine tapeworms such as E. granulosus granulosus and Taenia hydatigena , which can also be human pathogens. The domestic pig is a potential host of Trichinella spiralis , which is a serious human pathogen.
The helminths which occur in the various organ systems of pigs will be discussed in this section.
These nematodes cause only minor pathology –with gastritis as an occasional finding.
These species have an indirect life cycle –using dung beetles as an intermediate host. Pigs become infected by ingesting the larval stage as a result of eating dung beetles or paratenic hosts.
The worms are non-migratory and develop in the mucosa of the stomach under the mucous layer. The pre-patent period is 6 weeks.
The adult worms of both species are similar –being small (up to 22 mm) and filiform in shape. The eggs are up to 22 mm long.
The eggs of the two species can be differentiated by their appearance and size: Ascarops eggs are small, oval and roughly 45-51 x 22-26 μm; Physocephalus eggs are thick-shelled, larvated, and roughly 34-39 x 15-17 μm in size.
Diagnosis (patent infections)
The eggs can be seen in faecal samples using the flotation method.
This nematode is mainly a helminth of ruminants, but is occasionally found in the stomach of pigs (see under helminths of ruminants ) .
Ascaris suum is a highly host specific species which infects pigs.
Ascaris suum is one of the commonest roundworms of pigs, but is, however, much over-rated as a pathogen. There is a high incidence in young pigs, and repeated infections induce partial immunity. ‘Milk spots ’–or multiple parasitic interstitial hepatitis, may if extensive, lead to entire livers being condemned during meat inspection.
The pre-parasitic life cycle takes 3 weeks to be completed. In the host, the larvated eggs hatch and the larvae migrate through the liver and then into the lungs via the trachea. The pre-patent period is 6-8 weeks.
The adult worms are pinkish, large and stout (up to 2.5 mm thick) ( Figure 74 ). The sexes can be distinguished since males are up to 25 cm long with a slightly curled tail, while females can grow up to 40 cm long and are 2-5 mm thick. The eggs are medium sized (56-87 x 46-57 μm), subspherical, and with a thick, irregularly mammillated, yellowish-brown shell.
Diagnosis (patent infections)
Eggs can be seen in faecal samples using faecal flotation or faecal smears.
A. suum has a one-host lifecycle with no intermediate hosts. Most infected animals develop immunity.
Pathogenesis and pathology
After ingestion the eggs hatch in the intestine, penetrate the gut wall and the L2 larvae infect the liver. Here they undergo a second moult to L3. They reach the lungs via tracheal migration and establish themselves in the small intestine where the L4 and adult worms are found.
Liver: The migration of larvae causes multiple parasitic interstitial hepatitis (‘milk spots ’) ( Figure 75 ) –which is seen as greyish-white, pinhead-sized foci (1 cm) on the surface of liver, with reticular marking. Other aetiologies for ‘milk spots ’are the nematodes Toxocara canis and Toxocara mystax .
Lung: Multiple lesions may be seen in the lungs.
Intestinal phase: Gastroenteritis, intestinal obstruction (rare). The worms may also sometimes migrate to aberrant sites like the bile ducts.
Clinical signs are seen mainly in piglets. During the migratory phase, piglets may have coughing, dyspnoea (‘thumps ’or ‘heaves ’) and nasal discharge. In the intestinal phase, piglets have one or more of the following signs: a distended abdomen sensitive to pressure, constipation accompanied by light colic, inappetence, weakness, and retarded growth.
- Piperazine and benzimidazoles (fenbendazole and flubendazole).
- Macrocyclic lactones (abamectin, doramectin, ivermectin).
Infected piglets must be treated to prevent clinical signs. Breeding stock must be treated to prevent massive contamination, which results even from light infestation. Pens must have concrete or slatted floors, which will allow thorough and regular mechanical/steam cleaning and chemical disinfection.
Treatment schedule for pregnant sows and piglets: Treat pregnant sows 14 days before farrowing; treatment should be completed at least 4 days before entering farrowing pens. Sows should be washed down thoroughly –particularly the udder and teats –before being transferred to farrowing pens. Treat sows and piglets again after weaning, and decontaminate farrowing pens.
- Mainly young piglets are clinically affected, as resistance develops early in life.
- Most important in warmer, humid areas.
- Anthropozoonosis: Cutaneous larval migrans in humans.
Strongyloides species have both sexual and asexual cycles of reproduction. Free living males and females can reproduce and give rise to female worms. These female worms infect the host subcutaneously and then migrate to various organs in the host. They are parthenogenetic –producing eggs which are shed in the faeces. S. ransomi infects pigs of all ages transcutaneously. They migrate to the lung and then up the trachea, where they are swallowed and enter the intestine. Migration to the lactating udder of the sows results in piglets being infected during suckling. The prepatent period is 3-14 days.
The parasitic worm population consists of parthenogenetic females only. They are small, ±6 mm long and colourless, and so are only microscopically visible in clear water over a smooth and dark surface.
Females are ovoviviparous. The egg is oval, medium-sized (50-60 x 25-30 μm), thinshelled, and larvated.
Diagnosis (patent infections)
Eggs can be demonstrated in faecal samples by the flotation method. Faecal cultures can yield larvae which can be identified. On postmortem, intestinal stages may be shown in mucosal scrapings, intestinal washings, or squashed samples of small intestine.
Free-living, infective larvae can survive for up to 4 months, but because they are unsheathed they are susceptible to extreme climatic conditions. Warmth and moisture promote the development and allow a build-up of large numbers of infective larvae –in particularly the summer months. Lactogenic and percutaneous modes of infection favour transmission. Clinical strongyloidosis is mainly seen in stabled piglets, where resting places under infrared lamps are hotspots for infection. Piglets are susceptible up to weaning age, when immunity starts developing. However, the immunity does not incapacitate the hypobiotic somatic larvae.
Pathogenesis and pathology
On reinfection, the migratory phase can cause erythema and urticaria of the skin in the inguinal area and on the coronary bands, petechiae in the lung, and also interstitial pneumonia. In the intestine, a catarrhal enteritis may be seen which is characterised by hyperaemic mucosa, mucosal petechiae, and ecchymoses. Villous atrophy may cause malabsorption, hypoalbuminaemia, and hypoproteinaemia –which give rise to subcutaneous oedema and anaemia.
Strongyloidosis manifests clinically in very young animals during the first few weeks of life. During the migratory phase, clinical signs caused by the migration are rarely observed. In the intestinal phase, piglets show inappetence, intermittent watery diarrhoea, weight loss, reduced growth rate, anaemia, apathy, sunken eyes with purulent discharge, and frothy discharge from the nose. Strongyloides can be highly pathogenic in suckling pigs; the mortality rate in a litter can be as high as 75%.
- Benzimidazoles (fenbendazole and flubendazole).
- Macrocyclic lactones (abamectin, ivermectin and doramectin).
Raising of Strongyloides -free piglets is made possible by removing them from the sow immediately after birth.
Like other Strongyloides species, S. ransomi can cause cutaneous larval migrans. Percutaneous infection can occur when there is contact of skin with damp ground which is contaminated with faeces of domestic stock.
Caecum and colon
Nodular worm of pigs
O. dentatum and quadrispinulatum are important pathogens of young pigs as they can cause severe wasting disease –with enteritis and colitis. The nodular lesions that result render the gut unsuitable for processing as sausage casings.
Cosmopolitan in free-living pigs.
After the ingestion of infective larvae, there is a non-migratory histotrophic phase in the caecum and colon, which causes formation of nodules (hypobiosis). The prepatent period is 30-40 days.
Stout, white worms, 1.0-2.5 cm long, with body often slightly curled. The head is usually bent so that –except for the predilection site –there is a slight possibility that they may be confused with hookworms. They produce strongylid-type eggs.
Diagnosis (patent infections)
Eggs can be demonstrated in faecal samples using flotation, and they can be identified by using subsequent faecal cultures.
O. dentatum and O. quadrispinulatum produce free living, infective larvae which can survive for as long as 14 months on pastures.
Pathogenesis and pathology
The histotrophic phase produces the most severe effects; the mucosa of the caecum and colon develop localised inflammation around each larva. The inflammatory foci become encapsulated, causing nodule formation (millet seed to pea-sized) in the caecum and colon. Following repeated infections, the nodules become larger and the inflammatory reaction more severe. Extensive formation of nodules interferes with absorption, bowel movement, and digestion. Nodules often show abscessation due to bacterial infection, and may rupture to the peritoneal surface –causing peritonitis and multiple adhesions. Ulcerative colitis may occur due to ulceration of the mucosa when larvae emerge. Widespread haemorrhages and the formation of diphtheritic membranes and regional lymphadenopathy may occur. During the luminal phase, the late larval stages and adults are plug feeders –which can cause colonic mucosa to be hyperaemic, thickened, and covered with mucus when a large number of adult worms are present.
Blood-stained mucoid diarrhoea, inappetence, general weakness, unthriftiness, progressive weight loss, retarded growth, and anaemia.
The following anthelmintic groups are suitable for use in pigs:
- Benzimidazoles: fenbendazole and flubendazole.
- Macrocyclic lactones: abamectin, doramectin, ivermectin.
The aim is to limit infections in sows and to produce Oesophagostomum -free piglets. This is achieved by strict hygiene. Pens, open ranges and pastures should be kept dry, and farrowing pens should be cleaned daily and disinfected once every week. Sows should be treated shortly before farrowing and then transferred to the farrowing pen.
Whipworm of pigs
T. suis is a cause of colitis, with haemorrhagic diarrhoea.
The infective L1 develops within the egg. Animals ingest the larvated eggs and a non-migratory histotrophic phase develops in the mucosa of the large intestine ( Figure 76 ). The pre-patent period is 2-3 months.
The worms are medium-sized (3.5-8 cm long), whitish, and with a whip-like tail. The eggs are lemon-shaped, mediumsized (70-80 x 30-42 μm), yellow brown, thick-shelled –with a projecting plug at each end.
Diagnosis (patent infections)
Demonstration of eggs in faecal samples (faecal flotation).
Trichuris eggs can survive extreme temperatures and are resistant to desiccation. In a cool environment the eggs can survive for 4-5 years on pastures.
Pathogenesis and pathology
The pathology is related to worm burden. Adult worms tunnel into intestinal mucosa with their thin anterior ends and cause catarrhal inflammation with small epithelial defects, hyperaemia, and oedema. Whipworms suck blood –but the amount of blood withdrawn (±5 μl/worm/ day) is not regarded as significant enough to cause anaemia. Rather, this is caused indirectly as a result of bleeding from the damaged mucosa. There is colitis and formation of diphtheritic membranes.
The main symptom is diarrhoea with mucus and blood ( Figure 76 ). Pigs show weight loss and retarded growth.
- Benzimidazoles: fenbendazole and flubendazole.
- Macrocyclic lactones: abamectin, ivermectin and doramectin.
The aim is to prevent clinical infection by treatment –as part of a regular control programme.
Taenia solium larvae
Liver and kidney
Echinococcus spp. larvae
These are canine tapeworms which occasionally infect pigs and present a human health risk.
Infestation with these trematodes is occasionally seen in pigs ( see F. hepatica under ruminants ).
Importance: The worms migrate through the liver and lodge in the kidneys. They are not regarded as particularly pathogenic.
As under liver and kidney.
Importance: The adult worms are found in the lungs of free-living pigs –as the intermediate hosts are earthworms.
Muscles and tendons
This is a zooanthroponosis, since it can result in neurocysticercosis in humans, which is an important cause of epilepsy. Taenia solium is founds mainly in free-living pigs, and only occasionally in commercial piggeries. Production losses result from the condemnation of meat containing cysticerci, known as ‘measles’, at abattoirs.
Reliable information on the distribution of Taenia solium is scarce, but it is endemic in most countries in South and Central America, Africa, and South and Southeast Asia where pigs are kept, mainly affecting subsistence pig farmers; it is absent from North America, Australia, New Zealand and most of Western Europe (https://www.who.int/taeniasis/epidemiology/en/) but imported cases are experienced sporadically in non-endemic areas.
Humans are the sole final host –in which the adult tapeworm is found in the small intestine. The eggs are expelled with detached proglottids in faeces. When pigs ingest T. solium eggs, they lodge in the muscle in the form of a cysticercoid, which lies dormant until the pork is eaten.
The adult tapeworm in humans can be up to several metres in length ( Figure 77 ). The intermediate form or cysticercus is most commonly found in the striated muscles and muscle of the heart in pigs. These appear as small, white nodules, roughly 1-2 mm in diameter and are often referred to as pearly pork or measles ( Figures 78 and 79 ).
Human faeces are the only source of infection for pigs. This usually occurs where free-living pigs ingest human excreta deposited around dwellings. Human infection usually occurs by ingesting undercooked pork containing cysts or ‘measles’ results in taeniasis. The larvae are released into the large intestine, where they develop into an adult worm. Egg-filled segments of the tapeworm known as proglottids are shed in the faeces and the eggs are released into the environment. After being eaten by a pig the larvae hatch and migrate to the striated muscles or sometimes the brain, where they form cysts. However humans can also inadvertently ingest tapeworm eggs, shed either by themselves (auto-infection) or via food contaminated by another person, and they then assume the role of an intermediate host; in these cases cysts developing in the brain can be a major cause of epilepsy.
In South Africa there is a high prevalence of T. solium infection in pigs kept in rural areas. A number of studies undertaken in the Eastern Cape show that there is a very high incidence of neurocysticercosis (NCC) in humans. Carabin et al. (2004) showed that there were 34 000 NCCassociated epilepsy cases due to T. solium infection, which they estimated to be a burden on the health services to the tune of US$20-30 million. Serrano Ocana (2009) showed that 60% of CT scans to investigate epilepsy cases could be attributed to NCC, with the highest prevalence in the 10-19 year-old age group.
Figure 79 Higher magnification of the T. solium cysts in muscle, showing the inverted scolices in the bladders.
Pathogenesis and pathology
The ingested egg hatches in the intestine of the pig and bores its way through the intestinal wall and into the skeletal muscle –sometimes also affecting the heart. The cysticercus remains dormant here until eaten by the main host. Taenia solium can cause neurocysticercosis (NCC) in humans, dogs and cats ( Figure 80 ).
The T. solium cysticercus which occurs in the muscle of pigs does not affect them adversely. However, Taenia solium NCC of humans, dogs and cats occurs when the host autoinfects itself, resulting in cysticercosis in the brain tissue. In South Africa this is the most common source of epilepsy in rural human populations.
Pigs: Treatment of pigs with cysticercosis has been shown to be successful using oxfendazole –an inexpensive benzimidazole. A single oral dose of 30 mg/ kg is almost 100% effective. Although it should be considered as an important, cost-effective addition to the control of cysticercosis, its application has been hampered by the lack of convenient formulations.
Humans: Although it has been applied for several years, the treatment of patients infected with NCC, with cysticidal or anthelmintic drugs such as albendazole or praziquantel, remains controversial because of lack of evidence that the treatment is beneficial. Guidelines for treatment of cysticercosis have been proposed, but no adequate studies on efficacy have been reported. In addition in some patients –for example those with subarachnoidal cysts –therapy might be harmful. The drugs may cause arachnoiditis and arteritis, and consequently hydrocephalus.
Vaccination of pigs
Early research on the immunobiology of Taenia spp. indicated that immunity to re-infection plays an important role in the natural regulation of transmission of this group of parasites. In addition, it was demonstrated that host-protective immune responses are directed towards the oncosphere stage in the early developing embryo.
A recombinant vaccine has been developed against cysticercosis caused by T. ovis in sheep. This was the first effective, defined antigen vaccine against a parasitic infection. Based on the homology of host-protective antigens between T. ovis and T. saginata, a recombinant vaccine was developed against T. saginata cysticercosis in cattle. Despite the high level of protection induced by these vaccines, the vaccines were not commercialised because of financial considerations.
Using the same approach as above, one oncospheric antigen (TSOL 18) achieved complete protection against the development of cysticerci in vaccinated pigs. These experiments demonstrate the potential of recombinant oncosphere antigens in the development of a practical vaccine against porcine cysticercosis. Field trials showed protection against naturally acquired infection. The use of this vaccine is therefore expected to reduce the transmission of T. solium and reduce the incidence of NCC in humans.
Since man is the only definitive host of T. solium , the infective cycle is easily broken by preventing faecal contamination of pastures –simply through the provision and use of toilets. Meat inspection must be carried out in abattoirs and infected pig carcasses must be condemned and destroyed. To prevent NCC, strict hand washing after defaecation should be practised stringently.
Public health importance: Trichinella spp. are non-pathogenic in animals and hence of no clinical importance in the veterinary field. However, trichinosis is a potentially fatal zoonotic disease in humans, which results from eating inadequately cooked or processed meat. Trichinella spp. have never been demonstrated in domestic pigs in Africa south of the Sahara, but a sylvatic cycle has been shown in the Kruger National Park where the cysts have been detected in the venison of antelope, crocodiles, warthog and bushpig.
A sylvatic cycle occurs in which the encysted larvae are eaten and then develop to adult worms ( Figure 81 ). Adult worms develop within 24-36 hours of infection –the pre-patent period being 5-6 days and the patent period 4-6 weeks. Females are viviparous. Larvae (L1) enter lymphatic vessels and travel via the bloodstream to the skeletal muscles where they become encapsulated by stimulating the host genes to lay down collagen. Larvae (L1) become infective for new hosts 17-21 days after infection. Humans are accidental hosts –ingesting the larval cysts when eating venison or pork.
Very small worms (1-4 mm long, up to 70 μm wide); the encapsulated larvae are not visible macroscopically. Microscopically, a lemon-shaped capsule (0.2-1.0 mm long) is shown to contain a single coiled-up larva (L1).
There is no method of diagnosis in live animals, and infections are uncovered during meat inspection ( Figure 82 ). One method used for detection is an artificial digestion or trichinoscopy –used, for example, on the diaphragm and biceps muscle in crocodiles intended for consumption. Trichinella inspection is not compulsory in South Africa, but is required for meat intended for export.
While both adults and encysted larvae develop within the same host, two hosts are required to complete the life cycle. South of the Sahara, trichinosis appears to be maintained in sylvatic cycles only –but the potential for introduction into domestic pigs exists.
Pathogenesis and pathology
Non-pathogenic in animals; highly pathogenic in man.
Prevention of human infection, by Trichinella inspection.
Public health aspects (anthropozoonosis)
- Potentially fatal zoonotic disease.
- Infection by ingestion of inadequately cooked or processed pork, horsemeat or venison (drying, curing or smoking does not kill encysted larvae).
- Enteric phase: clinical signs resemble those seen in acute food poisoning (2-6 days after infection).
- Migratory (invasion) phase: myositis accompanied by severe myalgia, periorbital oedema, difficulty in chewing, breathing, and swallowing; muscular paralysis; remittent fever; splinter haemorrhages under nails and conjunctivae.
- Encystment phase: cachexia, oedema and extreme dehydration.
- Treatment only possible during enteric phase.
This worm is found in subcutaneous tissue and intramuscular connective tissue. The female is longer than male (32-40 mm). There is an abrupt end to the tail and it is studded with tubercles. The eggs contain L1 when shed. The life cycle is unknown. The worms cause white nodules which may develop into micro-abscesses if they become infected. They may be confused with the larval stage of T. solium .
Helminths of poultry and ostriches
Author: C NKUNA
Worm infections are a common problem in indigenous chickens, free-range commercial layers, breeders, and other types of poultry that have direct contact with their faeces and the intermediate hosts of helminths. Worms are usually not a problem in broilers due to their very short lifespan which is too short for the worms to complete their life cycles. In addition, end-of-cycle cleanouts of broiler houses also ensure that any worms in the litter are cleaned out.
In a study conducted by Mukaratirwa et al. (2001) on free-range chickens in KwaZulu-Natal, 16 helminth species were found, 12 nematodes and 4 cestodes. This supports previous studies that demonstrated that nematodes were dominant in the free-range birds in Zimbabwe and Ghana. Molla et al. (2012) found that in local backyard chickens on Ethiopia ’s North Gondar –although there were more species of cestodes isolated, the infection burden of the nematodes was higher than that of cestodes (60.38% compared with 54.62%).
Commercially farmed ostriches are generally kept on pasture for very long periods since they are grazers. They are therefore exposed to both nematodes and cestodes. Worm infestation can severely affect health and viability –especially of young ostriches.
Nematodes are the commonest and most important helminth group in poultry. More than 50 species have been described in poultry. Of these, most cause pathological damage to the host. The nematodes of poultry –unlike those of mammalian livestock –often have intermediate hosts, which is probably an adaptation to their foraging lifestyle and omnivorous feeding habits.
Crop and oesophagus
Capillary or Threadworms
The Capillaria spp. are small roundworms and are found in many mammals –but are most important in poultry. Various Capillaria species are found in different organs in the birds. Species of importance in poultry are: C. annulata, C. anatis, C. obsignata, C. caudinflata, C. aerophilia and C. contorta. C. annulata and C. contorta are found in the crop and oesophagus.
Capillaria species are very small and hairlike worms that are very difficult to see in the stomach contents. Size ranges from as small as 6 mm through to 80 mm. C. annulata females are the largest at 37- 80 mm long, with the males being 15-25 mm long. The eggs have bipolar plugs and measure 60 x 25 μm. C. contorta males are the same length as C. annulata males, while the females are shorter –measuring only 27-38 mm. The C. contorta eggs are equal in size to the C. annulata eggs –at 60 x 25 μm.
C. annulata and C. contorta have indirect life cycles –with earthworms being the intermediate hosts. Unembryonated eggs are shed in the faeces and are ingested by the earthworms, where they develop into the first larval stage in 9 to 14 days. The host then ingests the earthworm and becomes infected. C. contorta can also have a direct life cycle, with the L1 embryonated eggs as the infective stage. This means that poultry kept in houses –away from the intermediate host –can still be infected.
Clinical signs and pathogenicity
Capillaria spp. can be highly pathogenic for birds kept in deep-litter and freerange systems –both commercial and indigenous –where a build-up of infective eggs in litter or soil can occur. Young birds are more susceptible than older birds. Adult worms burrow into the anterior end of the oesophageal mucosa –causing inflammation. Heavy burdens can result in inflammation and thickening of the oesophageal and crop mucosal walls, which can cause death. C. contorta infections can result in severe anaemia, which can be fatal. Less severe burdens can cause loss of weight and condition, which in turn leads to a loss of production.
G. ingluvicola is a roundworm with a predilection for the crop, oesophagus, and rarely the proventriculus, of chickens, turkeys, pheasants and quails.
The female worm is 32-55 mm long and the males are 17-20 mm long. The eggs are approximately 35 x 58 μm. The anterior part of the body has numerous characteristic round or oval thickenings –called cuticular plaques –on the cuticle.
The life cycle is indirect and includes the beetle Copris minutus and the cockroach Blatella germanica as intermediate hosts. The eggs are shed in the faeces and are eaten by beetles and cockroaches. The worm develops in the intermediate host into infective larvae over 30 days. Birds become infected after eating the intermediate hosts that contain the infective larvae L3.
Clinical signs and pathogenicity
Adult parasites may cause inflammation and hypertrophy –with cornification of the epithelium in chronic infections. The pathogenicity is dependent on the burden of infection.
Proventriculus and gizzard
T. americana and T. fissispina are found in various bird species in Africa. The adult worms are found in the proventriculus –detriculus and the walls of the gizzard.
Clinical signs and pathogenicity
Infected birds may be emaciated and sluggish or weak. The worm infection weakens the immunity of the birds –making then susceptible to other infections. Adult D. nasuta attach to the wall of the proventriculus, causing ulcerations at the attachment sites. When the worm burdens are high, a proliferative proventriculitis with necrosis and sloughing of the mucosa is evident. The inside of the proventriculus is then filled with thick, white, slimy mucous and sloughed gastric tissue. There is also thickening of the tissues below the lining of the proventriculus. The lumen of the proventriculus can become completely blocked –thereby preventing the passage of food. Some birds may die from starvation in very severe cases. Adult worms may be found beneath and in the proliferating tissue. The proventriculus may become enlarged and flaccid due to the destruction of the glandular tissue and muscle layer. In some severe cases, it may be perforated –resulting in peritonitis.
Wireworm or stomach worm of ostriches
L. douglassi is a parasite of the digestive system causing libyostrongylosis (rotten stomach/vrotmaag ). It is the most economically significant gastro-intestinal parasite in ostriches. The wireworm is a nematode in the family Trichostrongylidae (Nemejc et al ., 2012). In South Africa, it has been reported to cause as much as 50% mortality in juvenile ostriches (Reinecke, 1983).
Wireworms are very small, round, wirelike, yellowish-red worms. They are about 3 mm long (males 4-6 mm and females 5-6 mm). The mature worms and late larval stages live in the crypts of the glandular portion of the proventriculus and gizzard wall ( Figure 83 ).
Eggs shed in the faeces of the infected host hatch and develop from first to second and finally to the third larval stage. This development takes place at temperatures ranging from 7-10 °C to a maximum of 37 °C (McKenna, 2005). Infective larvae tend to climb to the tips of blades of grass in films of moisture (Anderson, 1992; McKenna, 2005). Infection of susceptible hosts is by ingestion of third-stage larvae. The fourth-stage larvae develop in the proventriculus some 4 to 5 days later. The development of fifth-stage larvae and the production of eggs occur at about 20 days and 33 days post infection, respectively. The eggs will be passed from the proventriculus and appear in the faeces after 3 to 4 days (McKenna, 2005).
Clinical signs and pathogenicity
The different stages have predilection for different sites within the gut. The immatures penetrate deep into the glands of the proventriculus and adults are found on the surface of the proventriculus, where they cause damage by sucking blood –resulting in severe inflammation (McKenna, 2005) ( Figure 84 ). This causes proventriculitis which can lead to impaction of the organ (McKenna, 2005). Clinical signs in young birds are wasting, anorexia, anaemia and death. Mature birds can sustain infections with no visible clinical signs (McKenna, 2005).
Young ostriches raised in commercial systems should be raised in pens which have the floors regularly cleaned. Regular faecal monitoring should be done to check for worms. Infections can be treated with injections of ivermectin or dosed with levamisole or fenbendazole. Young ostriches should be fed lucerne from pastures which have been ostrich free for three years.
A. hamulosa is found in chickens and turkeys worldwide. The adults have an affinity for the area below the keratinised layer of the gizzard –where they embed themselves.
The males are 10-14 mm long –while the females are longer at 16-29 mm. The worms have four cuticular cordons, which are irregular and wavy –extending twothirds the length down the body. The males have long and slender spicules on the left side measuring 1.63-1.8 mm, while on the right side they are only 0.23-0.25 mm long.
The worms have an indirect life cycle –with grasshoppers, beetles, sandhoppers and weevils as possible intermediate hosts. The eggs are found in the faeces and are ingested by the birds when they eat the intermediate hosts. The eggs develop into the infective stage inside the intermediate hosts over 21 days.
Clinical signs and pathogenicity
The clinical signs seen in birds with heavy infections include droopiness, weakness, anaemia and emaciation. In severe cases the gizzard may rupture. The worms are found in soft, yellow-red nodules. The keratinised layer of the gizzard may be destroyed or can even die off in severe infections.
Ascaridia galli, A. dissimilis ,
Ascaridia spp. are large, round white worms which infect various avian species. Of the many species, those important in domestic birds are: A. galli in fowl, A. dissimilis in turkeys, and A. columbae in pigeons. They are found mainly in the intestines (jejunum and duodenum) where they can cause obstruction, when in large numbers. The adult worms can migrate through the large intestine and cloaca to the oviduct –where they can be found in the eggs.
These are large worms; the females can be as long as 72-116 mm, while the males are 51-76 mm long ( Figure 85 ). The mouthpart has three prominent lips. The male has a pre-anal sucker and two equal spicules which are 1.0-2.4 mm long. The females have an opening in the middle of the body. The eggs are oval, with smooth shells, and are 73-92 x 45-57 μm in size.
The ascarids have a direct life cycle. Sexually mature worms live in the lumen of the small intestine, and infective-stage larvae (L3) develop in the environment (Permin, 1997; Tarbiat, 2012). The route of infection is oral –usually by direct ingestion of the embryonated egg –and there is a 5-10 week prepatent period, which is shorter in young birds. The larvae moult in the eggs until L3. The development process from fertile eggs to fully mature infective larvae (L3) takes 7 to 20 days –depending on environmental conditions (Permin et al ., 1998; Tarbiat, 2012).
Clinical signs and pathogenicity
Penetration of the parasite into the duodenal or jejunal mucosa may cause haemorrhagic enteritis. In some cases the larvae can cause destruction of the glandular epithelium and adhesions of the mucosal villi (Permin, 1997; Tarbiat 2012). Ascarids can cause a variety of symptoms, including anorexia, diarrhoea, dehydration, stunted growth, unthriftiness, drooping wings, ruffled feathers, weight loss, and misshapen eggs with soft and thin shells. Clinical signs are more pronounced in chickens up to 3 months of age, after which the worm burden normally decreases, but can still be very high.
H. gallinarum closely resembles Ascaridia galli . It is found in the small intestine of chickens in West and South Africa –as well as Asia.
The females are 60-100 mm long, while the males are only 28-40 mm long. Embryonated eggs are shed in the faeces. They have thick shells and measure 45- 53 by 27-33 μm.
The parasite has an indirect life cycle –with termites as intermediate hosts.
Clinical signs and pathogenicity
Severe infections cause diarrhoea, weight loss, and decreased egg production. The birds become emaciated and very weak.
Caeca and large intestine
Heterakis are among the most important roundworms in poultry. They are seen in chickens, turkeys, ducks, geese, guinea fowls and pheasants. There are three species that are believed to be important: H. gallinarum, H. isolonche and H. dispar.
All three species are found in the lumen of the caeca.
Heterakis spp. have typical roundworm morphology –with features such as a cuticle, an oesophagus ending in a valved bulb, and three papillae-lined lips and alae. The alae, which run almost the entire length of the body, are ridges formed by the thickening of the cuticle –that may act as receptors for molecules which stimulate reproduction. Adult female and male caecal worms differ in length, with the female (10-15 mm) generally being larger than the male (7-13 mm). Both sexes have a pointed tail, and males having a precloacal sucker at the posterior end. The eggs of H. gallinarum are approximately 65-77 x 35-48 μm –with visibly thick, smooth shells (Carron, 2012). The eggs are thick, smooth-shelled and very similar to those of A. galli .
The eggs develop to the infective stage in 12 to 14 days at 22 °C and can remain infective for 4 years in the soil. Infection occurs when eggs are eaten by the host. Earthworms and houseflies can act as transport or paratenic hosts –in which the worm can survive for a number of years. The second stage juveniles hatch in the gizzard or duodenum and pass down to the caeca. Most complete their development in the lumen, but some penetrate the mucosa where they remain for 2 to 5 days without further development. Returning to the lumen, they mature about 14 days after infection. If eaten by an earthworm, the juvenile may hatch and become dormant in the earthworm ’s tissues, remaining infective to chickens for at least a year.
Clinical signs and pathogenicity
The damage is evident on the cloacal mucosa which becomes inflamed and thickened, with petechial haemorrhages. The clinical signs are not readily visible. However, infections with H. isolonche can produce nodular typhilitis, diarrhoea, emaciation and death. The most important feature of H. gallinurum is that it can transmit the protozoon Histomonas meleagridis to fowls. The H. meleagridis parasite can remain viable in H. gallinarum eggs for many years.
C. struthionis is a roundworm found in the large intestine and distal third of the ostrich caecum.
The parasite is about 1.0-1.5 cm long and white in colour. The infective larva of C. struthionis has a tapered tail-end –otherwise its morphology is very similar to that of Libyostrongylus dentatus (Fagundes et al ., 2012).
The life cycle of C. struthionis has not yet been determined –but it is believed to be simple and direct (Fagundes, 2012).
Clinical signs and pathogenicity
Heavy infestations can be pathogenic. C. struthionis causes lesions in the caecum of ostriches; the severity of the lesions depends on the worm burden (Fagundes et al ., 2012).
Eyes and nose
Oxyspirura mansoni (Cobbold, 1879; Permin, 1998)
O. mansoni infections occur in chickens, turkeys, guinea fowl and peafowl in tropical and subtropical areas. The parasite is located under the nictitating membrane and in the naso-lacrimal ducts or conjunctival sacs.
The female worm is 12-19 mm long and the male reaches 10-16 mm in length. The worm is slender and the cuticle smooth. The pharynx is shaped like an hourglass. The male tail is curved ventrally and has no alae. The two spicules are uneven in size; the left is slender, 3-3.5 mm long and the right one is stout and 0.2-0.22 mm long. The vulva is to the posterior end of the female worm.
The life cycle is indirect. After the eggs have passed through the lacrimal duct, are swallowed and passed out with the faeces, the intermediate stages develop in cockroaches (Pycnoscelus surinamensis) . After ingestion of the intermediate host, the larvae migrate via the oesophagus, pharynx and lacrimal duct to the eye.
Clinical signs and pathogenicity
The eyes become irritated and the birds start to scratch them. After a while, the affected birds develop ophthalmitis with inflamed and watery eyes.
(syn. S. parvis, S. gracilis)
S. trachea is found in chickens, turkeys, pheasants, guinea fowl, geese and various wild birds throughout the world. The adult worms are found in the trachea or in the lungs.
The worms are red in colour and the two sexes are found in permanent copulation. The female is bigger than the male –measuring 5-20 mm –while the male is 2-6 mm long. S. trachea has a wide mouth opening, without leaf-crowns. The buccal capsule is cup-shaped with 6 to 10 teeth at the base. The males have two spicules which measure 53- 82 μm. The eggs have a thick operculum in both poles and they measure 70-100 x 43-46 μm.
The life cycle may be direct or indirect: some intermediate hosts are earthworms, snails, flies or other arthropods. When these hosts are swallowed by poultry the larvae migrate through the intestinal wall and are carried by the blood to the lungs. Here they develop into the adult stage. The prepatent period is three weeks. Eggs are coughed up and swallowed and passed with the faeces. Depending on the temperature and humidity, the eggs become infective in 2 to 7 days. Infections with S. trachea mainly affect young birds –except for turkeys which are affected at any age. Pheasants and other reared game birds are highly susceptible.
Clinical signs and pathogenicity
The characteristic signs of S. trachea infections are dyspnoea due to mucous accumulating in the trachea (gaping). Asphyxia and death follow when the mucus blocks the trachea. Emaciation, anaemia and weakness are also seen as clinical signs. On post-mortem examination the carcass is emaciated and anaemic and the adult worm is seen macroscopically when opening the trachea.
Diagnosis and control of nematodes of poultry
In commercial systems –for example free-range layers or breeders –faecal monitoring for nematode eggs may be necessary, especially if clinical signs are present. Careful post-mortem examinations of any birds dying should be done as a routine.
Birds with clinical signs can be treated with nematocides registered for use in poultry –such as ivermectin (injectable), levamisole, piperazine or one of the benzimidazoles –by dosing, or in feed or water.
Regular rotation of camps will help reduce the level of infection.
Poultry reared under free-range conditions are likely to be infected with tapeworms. All tapeworms of poultry have indirect life cycles, with intermediate hosts like earthworms, beetles, flies, ants or grasshoppers. The intermediate hosts are essential to perpetuate the life cycle –and infections are therefore rare in indoor systems. More than 1 400 tapeworm species have been described in domesticated poultry and wild birds. The pathogenicity of most of these species is unknown. A great number are harmless or have a mild pathogenicity, but a few species cause severe reactions in the host. Poultry tapeworms are mainly intestinal and most are small –but some may reach 30-50 cm in length.
Broad-Headed and nodular Tapeworms
There are three species of importance in poultry. These are: R. cesticillus (Skrijabinia cesticillus) (broad-headed tape worm), R. echinobothrida (nodular tapeworm), and R. tetragona . These tapeworms have chickens, turkey, geese and other wild and domestic birds as their final hosts (Junquera, 2013).
Raillietina adults are whitish, mediumsized tapeworms measuring 5-30 cm long and 1-4 mm wide. The head –termed the scolex –has hooks, spines and four suckers to attach to the wall of the host. The segments of the worm have both male and female organs. The segments also have excretory cells known as flame cells. The eggs are 74 x 93 μm and the highest number is found in the gravid proglottid of R. tetragona .
The gravid proglottids are shed with the faeces, and the eggs can survive for years outside the host. The intermediate hosts are beetles for R. cesticillus , ants for R. echinobothrida , and ants and houseflies for R. tetragona (Junquera, 2013). The intermediate hosts get infected when they ingest individual eggs, and the larvae hatch in the intestine of the intermediate host. The larvae then develop further into cysticercoids in the intestine of the intermediate host –until ingested by the final host. The cysticercoids are activated by the bile and release the young tapeworms that attach to the mucosa in the small intestine ( Figure 86 ). The prepatent period lasts 2 to 3 weeks.
Clinical signs and pathogenicity
The worms affect the weight gain and egg production of various poultry species. R. echinobothrida can cause the appearance of large nodules in the gut –a phenomenon called ‘nodular tapeworm disease ’.
Heavy, chronic infections may cause diarrhoea, anaemia, weight loss and intestinal inflammation and haemorrhage. Young birds and free-range birds are commonly affected (Junquera, 2013).
C. infundibulum is a tapeworm that affects domestic fowls and turkeys. The worms have a predilection for the mucosa of the upper end of the small intestine.
The worms are 56 mm long and 1.8 mm wide in the region of mature proglottids. The scolex is 0.456 mm in diameter, and 0.373 mm to 0.581 mm in length. The neck is 0.47-0.52 mm long (Sawada, 1970). The segments are wider at the posterior end of the parasite. The eggs have a distinctly long filament and measure 47 x 54 μm.
The eggs are excreted with the faeces and are swallowed by the intermediate hosts. Houseflies and beetles are natural hosts. Experimental hosts include beetles, grasshoppers and termites. The gravid proglottids are released into the intestines of the fowls after swallowing the intermediate host.
Clinical signs and pathogenicity
Adult worms cause weight loss.
This very small tapeworm is found in chickens, turkey, guinea fowl, and other domestic and wild birds. They have a predilection for the mucosa of the duodenum. The worms are found worldwide –and most commonly in free-range poultry (Junquera, 2013).
The adult worms are 0.5-3 mm long and have 4 to 9 proglottids. The eggs are 28- 40 nm in size. The scolex has numerous hammer-shaped hooks, and also suckers armed with spines and numerous hooks. Only the last segment is gravid. Each segment has both male and female reproductive organs (Junquera, 2013).
The gravid proglottids are shed with the faeces. The eggs hatch after being swallowed by various species of gastropod molluscs –such as species of Limax, Cepaea, Agriolimax and Arion . Cystecercoids develop after 3 weeks and develop into adult tapeworms 2 weeks after ingestion by the final hosts.
Clinical signs and pathogenicity
D. proglottina is one of the most pathogenic tapeworms. Sudden massive infections can cause haemorrhagic enteritis and intestinal necrosis that can be fatal for young birds. Clinical signs include dull plumage, slow movements, reduced weight gain, emaciation, difficulty in breathing, leg paralysis, and death. Histology shows mucosal thickening with haemorrhages, and necrosis.
This is a tapeworm of chickens and other domesticated and wild birds. It has predilection for the small intestine.
A. spheniodes are very small –no longer that 4 cm in length. The head has suckers and 12 to 14 hooks and there are no more than 25 segments. The segments have both male and female reproductive organs. The embryonated eggs are almost spherical, and about 35 μm in diameter (Junquera, 2013).
A spheniodes has an indirect life cycle –with earthworms as the intermediate hosts. The gravid segments are passed with the faeces and earthworms ingest them. The eggs develop to cysticercoids in the earthworm ’s body cavity. The birds become infected by ingesting the infected earthworms. After ingestion, the earthworms release young tapeworms that attach in the gut of the bird. The time between infection and shedding of the first eggs is 4 weeks.
Clinical signs and pathogenicity
High worm burdens can cause haemorrhagic enteritis. Severely affected birds can be apathetic and tend to isolate themselves (Junquera, 2013).
H. struthionis is a cestode occurring in the intestines of ostriches in Africa.
The tapeworms are long, large, flat, segmented, and about 50-100 cm long. The scolex has a retractile rostellum bearing two rows of large hammer-shaped hooks, and is equipped with four unarmed suckers. The proglottids are wider than long.
Clinical signs and pathogenicity
Ostrich chicks are most susceptible and show gradual loss of condition, lethargy, anaemia, loss of appetite, and sometimes mild diarrhoea (Nemejc, 2012).
There are three pathogenic and economically important Hymenolepis species that affect poultry. These are H. carioca and H. contaniana which are seen in fowls in most parts of the world, and Drepanidotaenia lanceolata which is seen in geese and ducks.
H. carioca is 20-100 mm long. The neck is 75-150 μm wide and the posterior end is 0.4-0.8 mm wide (Guberlet, 1919). The suckers are armed with hooks. The segments have both male and female reproductive organs. H. contaniana is smaller and may reach a length of 20 mm. The adults of D. lanceolata may reach 130 mm in length and 18 mm in wide –with segments wider than long.
Hymenolepids have an indirect life cycle –with beetles as intermediate hosts for H. carioca and H. contaniana . Crustaceans are intermediate hosts for D. lanceolata. The prepatent time is 3 to 4 weeks.
Clinical signs and pathogenicity
Heavy infections with thousands of worms may result in catarrhal enteritis, diarrhoea and death. Severe signs have been seen with D. lanceolata in ducks and geese.
Diagnosis and control of cestodes in poultry
- Post-mortem examination of the intestinal tract when mortality is seen.
- Treatment –if necessary –with cestodicides (like niclosamide, resorantel and praziquantel) which are registered for use in birds.
All poultry trematodes belong to the subclass Digenea which utilise an intermediate host. Some species use a second or even a third intermediate host. More than 500 species are known from birds, but only a few are known to be pathogenic. Digenean life cycles vary in complexity and can involve up to four hosts –but two or three is more common. After the hatching of the egg in water (usually) or in the gut of the host after ingestion of the egg (more rare) the miracidium is released and penetrates the tissues of a mollusc –and develops into a mother sporocyst.
Germinal cells in the mother sporocyst give rise to daughter sporocysts or rediae. Germinal cells in the daughter sporocysts or rediae develop into cercariae. The cercariae then leave the snail, may encyst in the open or after penetrating another host –or may not encyst at all. Each cercaria gives rise to one metacercaria which in turn gives rise to one adult after it enters the gut or other appropriate site in the final host (Permin, 1998).
The primary hosts for E. revolutum are ducks and geese, but the species may also be found in other water birds, pigeons, fowls, and humans. The worms are located in the rectum and caeca. The parasite can be found in the snail species Lymnaea elodes and in other lymnaeid species.
E. revolutum is 10-22 mm long and 2.25 mm wide. Echinostomes have a headcollar armed with spines. The eggs are 90-126 μm x 59-71 μm.
Eggs are shed in the faeces and mature in three weeks –under conditions of high humidity and temperature. The miracidium penetrates the snail, and in the snail the cercariae develop in 2 to 3 weeks. These either encyst or enter into another snail. The birds become infected when they eat infected snails. The prepatent period is 15 to 19 days.
Clinical signs and pathogenicity
Heavy infections result in emaciation and catarrhal diarrhoea. Young animals may die from heavy infections.
There are three Prosthogonimus species of interest: P. pellucidus, P. macrorchis, and P. ovatus. They are trematode parasites of chickens, ducks, turkey and other domestic and wild birds as final hosts (Junquera, 2013). The adult worms are located in the Bursa of Fabricius, the oviduct, and in the cloaca/rectum (Permin, 1998).
Prosthogonimus has a complex, indirect life cycle with two intermediate hosts: a freshwater snail (e.g. Bithynia) as the first intermediate host, and dragonflies as second intermediate hosts. The fluke eggs shed in the faeces of a final host continue development only after getting into water. They are eaten by aquatic snails. Inside the snails ’intestine they develop to miracidia that penetrate the intestine ’s wall and develop into sporocysts. Sporocysts multiply asexually to daughter sporocysts –and to the next larval stage, the cercariae. Mature cercariae leave the snail with its faeces and can swim. In the water, cercariae find a dragonfly larva (= naiad) and penetrate its body through the anus. They encyst in the muscles of the abdominal wall and form metacercariae. About two months later these metacercariae become infective for birds.
Chickens, ducks, geese and other birds become infected by eating contaminated dragonflies –either naiads or adult. Inside the bird ’s gut the metacercariae release the young flukes, which migrate to the Bursa of Fabricius and later on to the oviduct through the cloaca, where they complete development to mature flukes and start producing eggs again. The prepatent period in the birds takes one to several weeks –depending on the fluke and the bird species (Junquera, 2013).
Clinical signs and pathogenicity
Prosthogonimus are the most pathogenic of trematodes that affect fowls and ducks. Clinical signs include a milky discharge from the cloaca. The birds may lay softshelled or shell-less eggs. In chronic cases, peritonitis may occur (Permin, 1998). Heavily affected birds may refuse to feed, become listless and thirsty, walk abnormally, show difficulty in breathing and have a tense and hot abdomen. In some cases, mortalities may occur (Junquera, 2013).
Helminth infections of wildlife
Author: J BOOMKER
Considering the diversity of the wildlife of Africa –the second largest continent –we really know very little about the helminths that affect them and even less about the diseases caused by helminths. Animals that die of helminthoses are quickly devoured by scavengers, especially in the larger nature reserves, and data on the cause of death and the necropsy findings are therefore usually not available. Another complicating factor is that the study of helminth biodiversity is an invasive process that is frowned upon by ecologists, game reserve managers, and animal rights ’activists. Because parasites are internal, it is not possible to remove them and leave the host alive, and artificial media for maintaining parasitic larval and adult stages are not in common usage. For many years helminths of mammals have been collected incidentally, usually during hunting expeditions and incidental postmortem examinations, and also from road kills. Until about 1940, numerous helminths new to science were described and the life cycles of several elucidated. During the Second World War and for a considerable period thereafter, the emphasis shifted to investigations of the pathogenic effects of helminths of domestic animals –and thus away from the helminths themselves. Helminths of wildlife received little attention and only a few new species or isolated and interesting cases were reported. From about 1973 onwards there was, however, a renewed interest in the helminths of wildlife. Conservation authorities made material that would otherwise have been discarded or ignored available to scientists of various disciplines, who then advised the conservation authorities of their results –to assist them with better management of existing conservation areas.
Round ’s Check list of the helminth parasites of African mammals of the orders Carnivora, Tubulidentata, Proboscidea, Hyracoidea, Artiodactyla and Perissodactyla, published in 1968, is still the only relatively complete and fully annotated check-list, but, particularly in East and South Africa, numerous additions have since been made.
Helminths of wild ruminants
In the same way that many host species have well-defined geographic distributions, so do several parasitic species. For example, eland are widespread in South Africa. Consequently, because several of the parasites infecting eland have specific geographic distributions, the composition of the parasitic fauna of these antelope in the Western Cape Province will differ from that of eland in the Karoo, which in turn will differ from that of eland in the Mpumalanga Lowveld or the Kalahari. Conversely, Trichostrongylus falculatus , which is widespread in South Africa, will infect blue wildebeest in the Mpumalanga Lowveld, springbok in the Karoo, and bontebok in the Western Cape Province. All these antelope also have a defined geographic range.
Gemsbok translocated to Langebaan Nature Reserve in the south-western part of the Western Cape Province acquired 20 times as many worms as their counterparts in the arid Etosha Game Reserve. Sheep introduced into the North West Province are exposed to Gaigeria pachyscelis, probably of blue wildebeest origin, and may die. Springbok introduced into the Bontebok National Park at Swellendam brought with them the lungworm, Bronchonema magna , which caused clinical disease in the indigenous bontebok.
Climate directly influences parasites by its effect on the free-living stages and on the vegetation, which in turn determines the distribution of the antelope hosts.
Because of climatic differences, it is important to give the regional distribution of the parasites when compiling parasite lists for the country.
The climatological regions of southern Africa are illustrated in Figure 87, and the helminths are classified as host specific, definitive, occasional or accidental parasites of their respective hosts in Tables 12 to 15. At the same time, their geographic distribution according to climate is presented.
Figure 87 The climatic regions of South Africa (redrawn from Horak (1981), and published with kind permission of the Journal of the South African Veterinary Association) .
|A||Temperate, warm and moist, occasional hot and dry bergwinds|
|D||Warm, temperate, monsoonal type of climate|
|E||Warm and moist|
|H||Warm, temperate, monsoonal type of climate, dry winter|
|K||Desert and transition zone from winter to summer rains|
|L||Subtropical, warm and muggy, except in winter|
|M||Winter rains, and a hot, dry summer|
|SE||Warm, temperate and moist|
|SS||Semi-arid, summer rain|
|SN||Semi-arid, summer rain|
|B||Climate similar to SS and SN|
|NAM||Climate similar to SS and SN|
From the tables it can be seen that only a few species qualify as definitive parasites. Most are accidental parasites, which are acquired indirectly from other ruminants –domestic or wild. The definitive parasites, however, generally make up the bulk of the total nematode burden, with only a small contribution coming from the occasional and accidental parasites.
Some interesting observations emerge from these tables. Firstly, it appears that certain parasites are absent from some localities and are replaced by other species. A case in point is that no definitive parasites of grey duikers were recovered from these animals in Valley Bushveld. The probable reason is that this vegetation type is unfavourable for the free-living stages of the definitive parasites of these antelopes –because of the extremes in temperature and the frequently low rainfall during the summer months.
Another example is Cooperia neitzi , which is a common parasite of kudus in the Lowveld of Mpumalanga and Limpopo, but is absent in the Eastern Cape. Cooperia rotundispiculum is abundant in nyala in the moist, warm regions of KwaZulu-Natal and in kudus in the Eastern Cape Province –but is infrequently encountered in the Lowveld of Mpumalanga and in Limpopo Province.
The reason why the latter species is present in habitats with almost opposing climates is unknown, and reflects the dearth of knowledge about the distribution, epidemiology and ecological requirements of the nematodes of wildlife in general.
Table 12 Definitive and occasional helminths of impala and their distribution in the South Africa according to climate. For the distribution code, see Figure 87 .
|Cooperia fuelleborni||NT, L, E|
|Cooperia hungi||NT, L, E|
|Cooperioides hamiltoni||NT, L, E|
|Cooperioides hepaticae||NT, L, E|
|Gaigeria pachyscelis||L, E|
|Haemonchus bedfordi||L, E|
|Impalaia tuberculata||NT, L, E|
|Longistrongylus sabie||NT, L|
|Oesophagostomum columbianum||NT, L|
|Pneumostrongylus calcaratus||L, E|
|Strongyloides papillosus||NT, L, E|
|Trichostrongylus colubriformis||NT, L, E|
|Trichostrongylus axei||NT, E|
|Stilesia hepatica||L, E|
Table 13 Definitive, occasional, and accidental parasites of blesbok, and their distribution in South Africa according to climate. For the distribution code, see Figure 87 .
|Cooperia yoshidai||H, E|
|Haemonchus contortus||NT, H|
|Impalaia nudicollis||NT, H|
|Skrjabinema alata||NT, H|
|Trichostrongylus axei||NT, H|
|Trichostrongylus falculatus||NT, H|
|Avitellina spp.||NT, H|
Table 14 Definitive, occasional and accidental parasites of nyala, and their distribution in South Africa according to climate. For the distribution code, see Figure 87 .
|Cooperia rotundispiculum||E, L|
|Haemonchus vegliai||E, L|
Table 15 Definitive, occasional and accidental parasites of kudus and their distribution in South Africa according to climate. For the distribution code, see Figure 87.
|Cooperia neitzi||L, NAM|
|Haemonchus vegliai||L, NAM, NT|
|Trichostrongylus deflexus||NT, L|
|Cooperia acutispiculum||L, NAM|
|Impalaia tuberculata||L, NAM, NT|
|Paracooperia devossi||L, NAM|
|Trichostrongylus falculatus||L, NAM|
Table 16 Worms recovered in surveys conducted during the 1980s ranked here in ascending sequence, according to the number of host species infected. Figures in parentheses indicate the number of animals that were infected.
|Mean burdens of infected animals|
|Helminth species||Blue duiker (n=4)||Red duiker (n=27)||Bushbuck (n=29)||Grey duiker (n=45)||Nyala (n=79)||Kudu (n=151)||Grey rhebuck (n=47)||Suni (n=4)|
|one host species infected|
|Fasciola hepatica||0||0||0||0||0||0||2 (1)||0|
|Echinococcus sp. larvae||0||0||0||0||0||1 (1)||0||0|
|Agriostomum gorgonis||0||0||0||0||0||52 (42)||0||0|
|Cooperia fuelleborni||0||0||0||0||0||89 (4)||0||0|
|Cooperia punctata||0||0||0||0||0||275 (1)||0||0|
|Cooperioides hamiltoni||0||0||0||0||0||73 (4)||0||0|
|Haemonchus horaki||0||0||0||0||0||0)||202 (19)||0|
|Hyostrongylus rubidus||0||68 (20)||0||0||0||0||0||0|
|Impalaia nudicollis||0||0||0||0||0||207 (3)||0||0|
|Longistrongylus curvispiculum||0||0||0||0||0||0||25 (15)||0|
|Longistrongylus namaquensis||0||0||0||0||0||0||32 (11)||0|
|Longistrongylus sabie||0||0||41 (2)||0||0||0||0||0|
|Megacooperia woodfordi||0||0||0||0||0||0||0||22 (3)|
|Nematodirus abnormalis||0||0||60 (1)||0||0||0||0||0|
|Nematodirus helvetianus||0||0||0||0||0||275 (3)||0||0|
|Onchocerca spp.||0||0||0||0||0||3 (9)||0||0|
|Ostertagia hamata||0||0||0||0||0||0||303 (41)||0|
|Ostertagia ostertagi||0||0||0||0||0||63 (2)||0||0|
|Paracooperia horaki||0||0||0||0||95 (35)||0||0||0|
|Paracooperioides peleae||0||0||0||0||0||0||196 (37)||0|
|Pneumostrongylus calcaratus||0||0||0||1 (1)||0||0||0||0|
|Setaria africana||0||0||0||2 (8)||0||0||0||0|
|Skrjabinodera kueltzii||0||0||1 (1)||0||0||0||0||0|
|Trichostrongylus colubriformis||0||0||2 (3)||0||0||0||0||0|
|Trichostrongylus colubriformis||0||0||2 (3)||0||0||0||0||0|
|Two host species infected|
|Schistosoma mattheei||0||0||0||0||5 (1)||21 (18)||0||0|
|Avitellina spp.||0||0||4 (3)||0||0||9 (2)||0||0|
|Moniezia benedeni||0||3 (6)||0||0||0||2 (13)||0||0|
|Moniezia expansa||0||0||11 (2)||0||0||# (1)||0||0|
|Stilesia hepatica||0||# (4)||# (2)||0||0||0||0||0|
|Taenia hydatigena larvae||5 (1)||0||1 (5)||0||0||0||0||0|
|Cooperia acutispiculum||0||0||66 (2)||0||0||348 (87)||0||0|
|Cooperia pectinata||0||0||328 (1)||0||0||78 (1)||0||0|
|Cooperia yoshidai||0||204 (2)||0||0||0||118 (1)||0||0|
|Gaigeria pachyscelis||0||0||0||25 (2)||25 (2)||0||0||0|
|Longistrongylus schrenki||0||13 (1)||0||0||0||0||6 (2)||0|
|Nematodirus spathiger||0||0||148 (5)||0||0||0||117 (17)||0|
|Paracooperia devossi||0||0||0||150 (19)||0||91 (5)||0||0|
|Setaria scalprum||0||2 (3)||3 (4)||0||0||0||0||0|
|Teladorsagia circumcincta||0||36 (2)||12 (2)||0||0||0||0||0|
|Trichostrongylus angistris||0||11 (3)||704 (22||0||0||0||0||0|
|Trichostrongylus rugatus||0||1 (1)||0||0||0||0||3 (1)||0|
|Three host species infected|
|Thysaniezia spp.||0||0||2 (2)||0||# (1)||# (1)||0||0|
|Cooperia hungi||0||0||254 (5)||0||0||193 (8)||0||1 (1)|
|Cooperia neitzi||0||0||121 (2)||58 (3)||0||1 230 (100)||0||0|
|Elaeophora sagitta||0||0||0||3 (3)||6 (6)||15 (70)||0||0|
|Dictyocaulus viviparus||0||7 (4)||0||12 (3)||3 (4)||0||0||0|
|Gongylonema spp.||1 (1)||0||0||4 (3)||9 (3)||0||0||0|
|Haemonchus contortus spp.||0||27 (11)||13 (4)||0||0||0||68 (4)||0|
|Strongyloides papillosus spp.||0||11 (2)||0||0||0||742 (6)||0||26 (1)|
|Oesophagostomum spp.||0||0||4 (3)||10 (1)||1 (1)||0||0||0|
|Ostertagia harrisi||0||105 (17)||0||233 (21)||463 (72)||0||0||0|
|Setaria cornuta||0||2 (2)||3 (8)||0||0||0||0||1 (1)|
|Trichostrongylus anomalus||1 (1)||281 (16)||0||0||0||0||0||44 (4)|
|Trichostrongylus axei||410 (1)||1 060 (1)||319 (24)||0||0||0||0||0|
|Trichostrongylus thomasi||0||3 (1)||41 (3)||0||0||38 (2)||0||0|
|Trichuris spp.||0||38 (5)||18 (6)||0||0||25 (5)||0||0|
|Four host species infected|
|Taenia spp. larvae||0||0||3 (4)||2 (3)||1 (1)||2 (11)||0||0|
|Impalaia tuberculata||0||13 (6)||247 (15)||0||50 (1)||194 (30)||0||0|
|Five host species infected|
|Calicophoron spp.||0||258 (8)||69 (9)||14 (1)||306 (28)||96 (32)||0||0|
|Haemonchus vegliai||0||0||14 (7)||105 (10)||44 (14)||252 (107)||0||19 (4)|
|Setaria spp.||1 (2)||2 (3)||3 (11)||0||3 (16)||1 (3)||0||0|
|six host species infected|
|Trichostrongylus deflexus||0||0||2 (1)||368 (2)||74 (6)||631 (45)||740 (1)||36 (1)|
|Trichostrongylus falculatus||1 (1)||0||22 (2)||222 (3)||20 (5)||123 (7)||160 (11)||0|
|seven host species infected|
|Cooperia rotundispiculum||16 (1)||842 (25)||51 (9)||795 (4)||422 (36)||664 (13)||0||1 (1)|
Many internal and external parasites display distinct periods of seasonal abundance. It is thus probable that animals of a particular species examined during summer will not only harbour different levels of infection to those examined in winter, but the actual species composition of the parasites may also differ. As with parasites of domestic stock, the patterns of seasonal abundance are brought about by the parasites employing survival strategies so that their most sensitive stages of development –usually the free-living stages –are protected against regularly occurring unfavourable environmental conditions. Therefore, hypobiosis takes place in one or more of the stages of a parasite ’s life cycle, and life cycles last approximately one year –ensuring that favourable climatic conditions for the parasites are encountered at some time in the future (Horak, 1978).
Seasonal abundance may also be influenced by competition for a limited resource. Thus peak adult burdens of Haemonchus bedfordi and Trichostrongylus thomasi –which both occur in the abomasum of blue wildebeest –are staggered. Trichostrongylus thomasi reaches peak abundance one or two months after the larger nematode H. bedfordi has passed its peak. Peak burdens of the tapeworm Moniezia benedeni , which is a large species, have been encountered in the small intestines of blue wildebeest calves aged six to eight months, while Avitellina sp., which is a smaller tapeworm, only peaked once the calves had reached ten months of age (Horak, De Vos &Brown, 1983).
Most wild herbivores suffer stress during winter because of the paucity of quality grazing or browse. This type of stress is generally accompanied by increased parasitic burdens. However, even though the burdens are increased, the parasites themselves are simultaneously employing strategies to escape the unfavourable external winter climate (Horak, 1978). Thus, herbivores may harbour large parasite burdens during winter, but many of these parasites will be in a state of hypobiosis and thus pose little threat to the health of the host. Many Haemonchus spp., Longistrongylus spp. and Cooperia spp. will be arrested in the fourth larval stage.
The most severe effects of drought on herbivores are generally apparent in spring. By that time the animals have been through a previous spring, summer and autumn with little or poor quality grazing and browse –followed by a winter in which very little feed of any kind was available. Nutritional stress is thus severe and their immune status compromised. At the same time many of the nematodes which have overwintered in the host as larvae, in an arrested stage of development, develop to become adults. Animals may concentrate around green patches or waterholes where contamination levels with parasites become high. If these animals die they are generally cachectic and harbour large burdens of both helminth and arthropod parasites.
Prolonged droughts, lasting two or more years, can have a number of unexpected results. The vegetation and surfacesoil microhabitat in which the free-living stages of the parasitic nematodes develop and survive, may be destroyed –with a concomitant reduction in free-living parasite levels. This is reflected in reduced parasite loads of host animals. Many of the hosts may have died because of the drought or migrated to a more favourable habitat. This in turn leads to a reduction in contamination by host animals of the original habitat. Animals may thus harbour reduced parasite loads for several years, until the microhabitat recovers and host numbers increase again.
Peri-parturient relaxation of resistance (PPRR) in female antelope could be responsible for an increase in the number of helminths in these animals and in the previous year ’s yearlings (Horak, 1978; Horak, McIvor &Greeff, 2001). Some helminths, such as Strongyloides spp., are transmitted through the milk.
During the rutting season, male animals continuously defend their territories and can be severely stressed. This is reflected in increased parasite burdens.
Disease, injury or age
Diseased, injured or aged animals are all stressed animals with compromised immune systems –and therefore usually harbour large parasite burdens. In addition, their mobility may be impaired and consequently they contaminate their own immediate environment, from which they will then in turn become reinfected.
Stressed animals will have larger nematode burdens than normal animals and a greater proportion of female nematodes is likely to mature and lay eggs.
Most wild animal species are distributed in fairly well-defined geographic regions. Within these regions particular species will have preferred habitats. Animal species, geographic distribution and habitat preference, will each contribute towards determining the species composition of parasite burdens, as well as their numerical magnitude in a given host. Normal, healthy wild animals in large ecosystems frequently harbour nematode burdens exceeding several thousand. Many of these nematodes are in an immature stage of development and cause few pathogenic effects. It is generally only when adult nematodes exceed several hundred or, in some cases several thousand, that problems can be expected.
Dispersion of Parasites
According to Petney, Van Ark and Spickett (1990), parasites are generally overdispersed within host populations ( see Figure 88 ). This means that most hosts have only a few parasites, but some have many. This implies that a few hosts harbour a high proportion of the total population of a particular parasite within a specific environment.
The reasons for overdispersion are:
- Free-living parasites are not randomly dispersed within the host ’s environment (dung pats contain large numbers of worm eggs).
- Variation within habitat (thickets, stream, dam).
- Host ’s feeding preference (grazer, browser, mixed feeder).
- The presence of an intermediate host in the life cycle, and the number of intermediate hosts present.
- Variation in the host ’s ability to reduce or limit parasites by immunity or other means.
- Some of the host ’s behavioural traits (communal dung heaps, spreading dung, pellets or pats).
The role of parasites
In large ecosystems free from human interference, parasites and predators drive an adaptive selection process. Young animals –usually until the age of 12 to 18 months –are often subject to large parasite infections (Horak, 1978; Horak et al., 1983). Weaker individuals and those that do not develop an effective immune response often succumb, and are caught by predators before they can contribute to the gene pool. Diseased, injured, stressed or maladapted young or older animals and aged animals frequently have compromised immune systems. They become heavily infected with parasites –resulting in a further deterioration in their condition and their rapid removal from the environment by predators.
Human activities have interfered with the host-parasite balance. Not only have humans translocated wild animals to regions in which they did not originally occur, but they have eliminated predators –as they have perceived these to be competition for a limited resource. The humans have themselves then failed to assume the role of the predators, or even worse have selectively taken out the fittestlooking individuals for consumption, sale or as trophies.
Translocated animals often suffer severe stress and may never adapt to the new habitat or to the resident parasites, which are foreign to them. They thus become a source of infection, not only for themselves, but for the wildlife endemic to the region. Because of the cost involved in the translocated wild animals ’purchase and transportation, it is unlikely that they will be purposely exposed to predators, nor will their owners destroy them if they become heavily parasitised –and consequently they persist as reservoirs of infection.
s ²/x=Variance to mean ratio
Figure 88 Parasite dispersion pattern theory
Humans have also introduced domestic livestock into wildlife regions and reintroduced wildlife into regions now used for stock farming. This has led to the introduction of parasites foreign to either one of these host groups and to crossinfection taking place. In some cases the parasites have adapted to the new host species with little visible reaction, while in others morbidity or mortality may be high.
The erection of fences has not only interfered with wildlife movement but also with their migration, and has also placed a finite size on the area available. Movement, and more particularly migration, allows animals to leave areas of high parasite contamination, while containment ensures their confinement –often at high stocking densities –in highly contaminated localities. In the latter type of environment, cross-infection with parasites between host species is very likely.
Host specificity implies the unique occurrence of a helminth species in a particular host species, and studies have shown that host specificity is not present to any great extent amongst the ruminants (antelopes). Helminths are often shared amongst the different species occurring in a geographic region. Certain helminths occurring in a subfamily of antelopes are largely limited to that subfamily, and are rarely found in other hosts. When the wild ruminants share pastures with domestic stock, both groups often acquire each other ’s worms. However, there are a number of helminths that occur only in a particular host species, while others are generalists and occur in hares, warthogs, grazers and browsers, mixed-feeding wild ruminants and even in zebra (e.g. Trichostrongylus thomasi) . To determine host specificity, large numbers of animals from various localities must be examined, and both the immature and adult stages of the parasite must be recovered, counted and identified (Horak 1981).
The various helminths that have been recovered from sheep, cattle, impala and blesbok in South Africa have been listed by Horak (1980) as definitive, occasional or accidental parasites of their respective hosts. He suggests that definitive parasites are present in a large percentage of a host population, often occur in large numbers, and can reproduce and survive for long periods in these hosts. Occasional parasites are present in varying numbers in some of the hosts only. They may be capable of reproduction, but survive only for a limited period. Accidental parasites are present in small numbers in a small percentage of hosts. They may not be able to develop into adults and, even if they do, they may not be able to reproduce. Their survival period in the host may also be short.
The worms recovered in the surveys conducted during the 1980s (Boomker, 1990) are ranked in Table 16 in ascending sequence according to the number of host species infected. None of the worms listed occurred in all eight host species. Cooperia rotundispiculum occurred in seven host species, and T. falculatus and Trichostrongylus deflexus each occurred in six host species. This situation could be due to variable host specificity or whether the worms are definitive, occasional or accidental parasites of their respective hosts.
Host specificity of helminths within groups of antelope species that have similar ecological requirements and habits seems to be more indicative of the adaptation of a particular worm species to an environment, and thus indirectly to specific hosts. This adaptation is an ongoing evolutionary process, which –when host species become geographically isolated and the gene flow within the helminth species is reduced or cut off –eventually leads to the differentiation of new helminth species.
Table 17 Some helminths of domestic ruminants and their counterparts in wild ruminants.
|Helminths of domestic ruminants||Counterpart in wild ruminants|
|Gaigeria pachyscelis||Gaigeria pachyscelis|
|Cooperia pectinata||Cooperia pectinata|
|Cooperia punctata||Cooperia punctate|
|Dictyocaulus viviparus||Dictyocaulus viviparus|
|Elaeophora sagitta||Elaeophora sagitta|
|Gongylonema spp.||Gongylonema spp.|
|Haemonchus contortus||Haemonchus contortus|
|Ostertagia ostertagi||Ostertagia ostertagi|
|Teladorsagia circumcincta||Teladorsagia circumcincta|
|Nematodirus helvetianus||Nematodirus helvetianus|
|Nematodirus spathiger||Nematodirus spathiger|
|Oesophagostomum columbianum||Oesophagostomum columbianum|
|Setaria labiatopapillosa||Setaria labiatopapillosa|
|Strongyloides papillosus||Strongyloides papillosus|
|Trichostrongylus axei||Trichostrongylus axei|
|Trichostrongylus colubriformis||Trichostrongylus colubriformis|
|Trichostrongylus rugatus||Trichostrongylus rugatus|
|Trichostrongylus falculatus||Trichostrongylus falculatus|
|Trichinella spiralis||Trichinella nelsoni|
|Avitellina spp.||Avitellina spp.|
|Echinococcus sp. larvae spp.||Echinococcus sp. larvae spp.|
|Moniezia benedeni||Moniezia benedeni|
|Moniezia expansa||Moniezia expansa|
|Stilesia hepatica||Stilesia hepatica|
|Taenia hydatigena larvae||Taenia hydatigena larvae|
|Taenia crocutae larvae|
|Taenia hyaenae larvae|
|Thysaniezia sp.||Thysaniezia sp.|
|Taenia regis larvae|
|Fasciola hepatica||Fasciola hepatica|
|Fasciola gigantica||Fasciola gigantica|
|Calicophoron microbothrium||Calicophoron microbothrium|
|Calicophoron calicophorum||Calicophoron calicophorum|
|Cotylophoron cotylophorum||Cotylophoron cotylophorum|
|Schistosoma mattheei||Schistosoma mattheei|
From the foregoing discussion it follows that host specificity in the broad sense is largely absent in browsers. The term ‘host specificity ’should therefore be disregarded in favour of the classification suggested by Horak (1980). This classification should be slightly modified by adding ‘host specific ’, and the categories should thus be host specific, definitive, occasional, and accidental. This modification has become necessary to accommodate parasites like Megacooperia woodfordi, Paracooperioides peleae and Paracooperia horaki