- Infectious Diseases of Livestock
- Part 3
- GENERAL INTRODUCTION: ANAEROBIC GRAM-NEGATIVE, IRREGULAR RODS
- GENERAL INTRODUCTION: SPIROCHAETES
- DISEASE COMPLEXES / UNKNOWN AETIOLOGY: Epivag
- Neurotoxin-producing group of Clostridium spp.
- Swine dysentery
- Borrelia theileri infection
- Tyzzer's disease
- Borrelia suilla infection
- Lyme disease in livestock
- GENERAL INTRODUCTION: AEROBIC ⁄ MICRO-AEROPHILIC, MOTILE, HELICAL ⁄ VIBROID GRAM-NEGATIVE BACTERIA
- Genital campylobacteriosis in cattle
- Proliferative enteropathies of pigs
- Campylobacter jejuni infection
- GENERAL INTRODUCTION: GRAM-NEGATIVE AEROBIC OR CAPNOPHILIC RODS AND COCCI
- Moraxella spp. infections
- Bordetella bronchiseptica infections
- Pseudomonas spp. infections
- Brucella spp. infections
- Bovine brucellosis
- Brucella ovis infection
- Brucella melitensis infection
- Brucella suis infection
- Brucellosis in wildlife
- GENERAL INTRODUCTION: FACULTATIVELY ANAEROBIC GRAM NEGATIVE RODS
- Klebsiella spp. infections
- Escherichia coli infections
- Salmonella spp. infections
- Bovine salmonellosis
- Ovine and caprine salmonellosis
- Porcine salmonellosis
- Equine salmonellosis
- Yersinia spp. infections
- Haemophilus and Histophilus spp. infections
- Haemophilus parasuis infection
- Histophilus somni disease complex in cattle
- Actinobacillus spp. infections
- Actinobacillus lignieresii infections
- Actinobacillus equuli infections
- Gram-negative pleomorphic infections: Actinobacillus seminis, Histophilus ovis and Histophilus somni
- Porcine pleuropneumonia
- Actinobacillus suis infections
- Pasteurella and Mannheimia spp. infections
- Pneumonic pasteurellosis of cattle
- Haemorrhagic septicaemia
- Pasteurellosis in sheep and goats
- Porcine pasteurellosis
- Progressive atrophic rhinitis
- Contagious equine metritis
- GENERAL INTRODUCTION: ANAEROBIC GRAM-NEGATIVE, IRREGULAR RODS
- Fusobacterium necrophorum, Dichelobacter (Bacteroides) nodosus and Bacteroides spp. infections
- GENERAL INTRODUCTION: GRAM-POSITIVE COCCI
- Staphylococcus spp. infections
- Staphylococcus aureus infections
- Exudative epidermitis
- Other Staphylococcus spp. infections
- Streptococcus spp. infections
- Streptococcus suis infections
- Streptococcus porcinus infections
- Other Streptococcus spp. infections
- GENERAL INTRODUCTION: ENDOSPORE-FORMING GRAM-POSITIVE RODS AND COCCI
- Clostridium perfringens group infections
- Clostridium perfringens type A infections
- Clostridium perfringens type B infections
- Clostridium perfringens type C infections
- Clostridium perfringens type D infections
- Malignant oedema⁄gas gangrene group of Clostridium spp.
- Clostridium chauvoei infections
- Clostridium novyi infections
- Clostridium septicum infections
- Other clostridial infections
- GENERAL INTRODUCTION: REGULAR, NON-SPORING, GRAM-POSITIVE RODS
- Erysipelothrix rhusiopathiae infections
- GENERAL INTRODUCTION: IRREGULAR, NON-SPORING, GRAM-POSITIVE RODS
- Corynebacterium pseudotuberculosis infections
- Corynebacterium renale group infections
- Bolo disease
- Actinomyces bovis infections
- Trueperella pyogenes infections
- Actinobaculum suis infections
- Actinomyces hyovaginalis infections
- GENERAL INTRODUCTION: MYCOBACTERIA
- GENERAL INTRODUCTION: ACTINOMYCETES
- Rhodococcus equi infections
- GENERAL INTRODUCTION: MOLLICUTES
- Contagious bovine pleuropneumonia
- Contagious caprine pleuropneumonia
- Mycoplasmal pneumonia of pigs
- Mycoplasmal polyserositis and arthritis of pigs
- Mycoplasmal arthritis of pigs
- Bovine genital mycoplasmosis
- Bovine haemobartonellosis
- MYCOTIC AND ALGAL DISEASES: Mycoses
- MYCOTIC AND ALGAL DISEASES: Pneumocystosis
- MYCOTIC AND ALGAL DISEASES: Protothecosis and other algal diseases
- DISEASE COMPLEXES / UNKNOWN AETIOLOGY: Ulcerative balanoposthitis and vulvovaginitis of sheep
- DISEASE COMPLEXES / UNKNOWN AETIOLOGY: Ill thrift
GENERAL INTRODUCTION: ANAEROBIC GRAM-NEGATIVE, IRREGULAR RODS
This content is distributed under the following licence: Attribution-NonCommercial CC BY-NC View Creative Commons Licence details here
ANAEROBIC GRAM-NEGATIVE, IRREGULAR RODS
A General Introduction has been added to each disease chapter in an attempt to give a brief updated overview of the taxonomic, biological and other characteristics of the virus family or group of bacteria /protozoa that cause disease in livestock and, where relevant, involve wildlife. As the text of the three-volume book Infectious Diseases of Livestock is currently under revision the Editors are aware that there are inconsistencies between the updated introductions to chapters and the content of the chapters themselves. Once the chapters have been updated – a process that is currently underway – these inconsistencies will be removed.
Of the many bacteria within this group only the genera Fusobacterium, Bacteroides, Porphyromonas, Prevotella and Dichelobacter are commonly associated with specific (Table 1) or nonspecific (abscesses in a variety of organs and tissues, dental and oral lesions, chronic pleuropneumonia, and chronic sinusitis) diseases in livestock and humans. Fusobacterium necrophorum is the most important pathogenic species in this group and, apart from the diseases with which it is primarily associated, it may secondarily infect and complicate lesions of infectious diseases in which the mucous membranes of the gastrointestinal tract are involved, such as foot-and-mouth disease, rinderpest and orf. Other important species include Dichelobacter (Bacteroides) nodosus, the agent of ovine footrot, and Prevotella melaninogenica (Bacteroides melaninogenicus), a cause of foot lesions in cattle.
These bacteria are obligately anaerobic, Gram-negative, non-sporeforming bacteria that commonly occur on mucous membranes of the mouth, the upper respiratory tract and the gastrointestinal and urogenital systems of healthy animals and humans.
They often occur in lesions in association with aerobic or other facultatively anaerobic bacteria, e.g. Trueperella pyogenes. Fusobacterium necrophorum and Bacteroides spp. appear, in many instances, to depend on these bacteria to reduce the redox potential in the affected tissues to a level that allows their growth and subsequent tissue invasion.8, 26, 27, 31, 38, 39
Before the advent of the newer methods used in molecular genetics, these bacteria were very difficult to study because they are fastidious in their nutritive and atmospheric requirements, and they are usually found in association with other microorganisms such as T. pyogenes, Pasteurella multocida, Escherichia coli, streptococci and others, and are therefore possibly overlooked.7, 51 In these mixed infections it does, however, seem likely that anaerobic species such as Bacteroides act synergistically with the other bacteria in the production of suppurative and necrotizing lesions.7 This emphasizes the importance that bacteriological examinations of exudates should include both aerobic and strict anaerobic culturing techniques.
Table 1 Most common specific diseases in livestock in which Fusobacterium necrophorum, Dichelobacter nodosus or Prevotella melaninogenica are the primary causative agent. Bacteria that may play a secondary role are indicated in brackets
|DISEASE||ANIMAL SPECIES AFFECTED||INFECTIOUS AGENT|
|Bovine foot rot||Cattle||F. necrophorum (P. melaninogenica, D. nodosus, T. pyogenes)|
|Ovine foot rot||Sheep and goats||D. nodosus (F. necrophorum, T. pyogenes|
|Interdigital dermatitis||Cattle||D. nodosus: benign strains|
|Sheep and goats||F. necrophorum, T. pyogenes|
|Digital dermatitis||Cattle||F. necrophorum?|
|Heel erosion||Cattle||P. melaninogenica?|
|Foot abscess||Sheep and goats||F. necrophorum, T. pyogenes|
|Toe abscess||Sheep||F. necrophorum, T. pyogenes|
|Hepatic necrobacillosis||Cattle, sheep and goats||F. necrophorum (T. pyogenes and other bacteria)|
|Necrotic and ulcerative stomatitis and laryngitis||Calves, lambs and kids||F. necrophorum|
|Necrotic rhinitis||Pigs (bull nose)||F. necrophorum (spirochaetes and other bacteria)|
|Porcine foot rot||Pigs||F. necrophorum (T. pyogenes, spirochaetes and other bacteria)|
|Cara inchada||Cattle||P. melaninogenica? (T. pyogenes, Bacteroides bivius, F. nucleatum, Actinomyces israelii )|
One of the hallmarks of infection by anaerobic bacteria, including Bacteroides, is an exudate with a putrid odour, although the absence of such an odour does not preclude an anaerobic infection.7, 50 The odour is primarily the result of metabolic end-products such as volatile amines, shortchain fatty acids and organic acids.50
Fusobacterium necrophorum is an obligately, anaerobic, Gram-negative, non-spore-forming, non-motile and pleomorphic bacterium which varies in shape from small cocci (0,5 to 1,75 mm in diameter) to filaments. The bacteria have irregular swellings along their length and blunt or tapering ends.33
On blood agar, colonies of F. necrophorum are convex, translucent to opaque, 1 to 2 mm in diameter, and have a circular outline with scalloped to eroded edges. The colonies are often ridged or uneven.
Fusobacterium necrophorum produces haemolysin and indole but does not reduce nitrate. Most strains cause either alpha or beta haemolysis on rabbit blood agar. Generally, beta-haemolytic strains are lipase-positive, and alphahaemolytic and non-haemolytic strains are lipase-negative. No lecithinase is produced.29
There is considerable doubt about the validity of conclusions concerning the involvement of F. necrophorum in diseases that appear in publications prior to 1970, because it was referred to by a variety of names (e.g. Fusiformis, Bacteroides, Sphaerophorus).29 In 1970 a subcommittee of the International Committee on Nomenclature of Bacteria published a report recommending that members of the genera Sphaerophorus and Fusobacterium be incorporated into a single genus Fusobacterium and that the genus Bacteroides should be retained because of the inability of its species to produce butyric acid — a feature which distinguishes them from the species of Fusobacterium. 1
Based on cell morphology, haemagglutination properties, haemolytic activities and virulence in mice, strains of F. necrophorum are grouped into biovars (phases) A, AB, B and C.3, 13, 21, 40, 43The pathogenic strains of biovars A, B and AB are haemolytic and produce a leukotoxin (leukocidin); strains of biovar B are, however, less pathogenic than those of biovars A and AB. Biovars A and B have been designated as F. necrophorum subsp. necrophorum and F. necrophorum subsp. funduliforme respectively.43 Although biovar AB is closely related to both subspecies, its taxonomic status is unclear.36 The strains of biovar C are neither haemolytic nor pathogenic and are now known as F. pseudonecrophorum. Strains of F. necrophorum subsp. necrophorum are commonly found in cattle, biovar AB in cases of ovine footrot while those of subsp. funduliforme and F. pseudonecrophorum are more often isolated from humans than from animals.34
Although further study is required of the virulence factors of F. necrophorum its cell wall contains a lipopolysaccharide with endotoxic activities similar to those of the Enterobacteriaceae (see Escherichia coli infections).5, 28, 37 An important virulence factor is leukotoxin which is produced in the late-log and early-stationary phase of growth and is toxic for bovine and ovine neutrophils and bovine ruminal cells.51 A haemolysin which is thought to be a phospholipase A and lysophospholipase is thought to aid the bacterium in acquiring iron from the host and in maintaining an anaerobic environment. Haemagglutinins, the capsule and fimbriae are thought to be mediators of attachment to host cells but their exact role still needs to be elucidated.20, 35, 51
Dichelobacter (Bacteroides) nodosus
The designation ‘Dichelobacter’ means ‘rod of the cloven hoof’ and ‘nodosus’ means ‘knobbed’ which refers to the terminal (sometimes central) enlarged areas of the cells of D. nodosus. Terminal enlargements are more pronounced in bacteria that are present in lesions than in those grown in cultures. Dichelobacter nodosus is more closely related to the Enterobacteriaceae and is now a member of the family Cardiobacteraceae.8 These bacteria are fairly large (1–1,7 × 3,0–6,0 mm), non-motile, straight or slightly curved rods. Varying numbers of pili are found on the surface of different strains of D. nodosus. Reports differ as to whether or not D. nodosus possesses a capsule.29
Surface colonies of the type strain of D. nodosus are 0,5 to 2,0 mm in diameter, smooth, convex, and translucent or semi-opaque. Colonies often etch into the surface of the medium immediately beneath them, producing a sunken appearance. Three basic colony types, namely papillate or beaded (B)-type, mucoid (M)-type, and circular (C)-type, have been described.4, 41
Ten major serogroups, designated A to I, and more recently M,54 have been defined according to the antigenicity of their pili which is determined by employing a slide agglutination technique.11-12, 25, 47 Cross-reactions between strains of specific serogroups have been reported.11 At least 19 different serovars of D. nodosus are recognized among the ten serogroups, and their distribution varies around the world. Serovars that belong to serogroups A, B, C and G have been found in South Africa.2
Various factors appear to influence the pathogenicity of D. nodosus. Earlier studies suggested that increased virulence is correlated with increased production and activity of protease (of which there are two forms, thermostable and thermolabile), the presence of large numbers of pili, increased degree of motility of the bacteria, and specific types of colony morphology on culture. Variation in colony morphology has also been linked to the degree of piliation of D.nodosus. 14–16, 19, 24, 45, 48, 52
Recent studies, however, indicate that the virulence of D. nodosus strains appears to be coupled with the combined effect of the thermostable protease and the degree of motility of D. nodosus, and that it is not strongly correlated to the total protease activity, colony morphology (other than size) or the degree of piliation.4, 16, 53 Based on these studies it has been suggested that strains of D. nodosus may be grouped into two major categories:
- benign strains which have thermolabile, extracellular protease and a low degree of motility. These strains cause benign foot rot of sheep and interdigital dermatitis in cattle and goats; and
- intermediate and virulent strains which produce thermostable protease. These cause intermediate and virulent foot rot in sheep, which varies in severity according to the degree of motility of the strain.
The type IV fimbriae coded for by FimA gene are considered essential in the virulence of F. necrophorum. 32 Agglutinating antibodies against pili of D. nodosus are the most important in protective immunity induced by killed whole-cell vaccines.22, 25, 47, 49, 53
The gene regions associated with virulence have been mapped with FimA coding for the type IV fimbriae and brpV and aprV5 for the thermostable proteases and brpB and bprB5 for the thermolabile protease.8, 30
The isolation of D. nodosus is often unsuccessful notwithstanding the application of correct procedures in the collection and transportation of tissue specimens and the use of recommended culturing media and methods. To ensure optimal results when attempting to isolate D. nodosus, specimens should be collected by detaching pieces of affected skin or hoof from active and untreated lesions. These are placed in a suitable transport medium such as Thorley’s medium. Stringent anaerobic conditions should be maintained during transportation of the specimens to the laboratory. Best results are obtained when hoof agar plates are inoculated in the field and then placed in an anaerobic jar with an attached anaerobic gas-generating kit, in which the agar plates are transported to the laboratory.4 Dichelobacter nodosus has fastidious growth requirements. Variable success has been achieved when media such as Thorley’s, Stuart’s and modified Stuart’s containing L-cystine are used to isolate D. nodosus. 4, 18 It grows well in solidified trypicasearginine-serine (TAS) medium at 37 °C under anaerobic conditions.53
Dichelobacter nodosus is an obligate parasite of the skin of the feet of sheep, goats, cattle and deer and cannot survive in the environment for more than 14 days.46
Other Bacteroides spp. and related genera (Porphyromonas and Prevotella)
Because many previous studies of organisms called Bacteroides melaninogenicus included strains that might have been members of any nine currently recognized species, earlier literature is difficult to correlate with present designations.29
Pigmented species of Bacteroides have been reclassified into the genera Porphyromonas and Prevotella. 41, 42 For example, Bacteroides melaninogenicusis now known as Prevotella melaninogenica. 23, 42
Members of Bacteroides, Porphyromonas and Prevotella are all Gram-negative pleomorphic rods, which produce as fermentation products succinate, acetate, lactate, formate or propionate and only rarely small amounts of butyrate. This distinguishes them from those of Fusobacterium spp. in which butyrate is a major product.29
Historically, the predominant differentiating characteristic of P. melaninogenica (B. melaninogenicus) was its production of darkly pigmented colonies on a blood-containing medium. This pigmentation is the result of the production of a dark brown to black pigment, protohemin, and not of melanin as was originally thought. Surface colonies of P. melaninogenica on blood agar are 0,5 to 2,0 mm in diameter, circular, entire, convex and shiny. They are usually darker in the centre of the colony with the edges being grey to light brown. The colonies become darker as they age and the pigmentation usually develops more rapidly when laked blood, rather than blood containing intact red blood cells, is used. All strains produce pigment when cultured on agar containing rabbit blood, while only certain strains produce pigment when cultured on agar containing horse blood. A few strains are beta-haemolytic on rabbit blood agar.29
Bacteroides, Porphyromonas and Prevotella spp. cause a variety of purulent conditions of soft tissues, e.g. liver abscesses and may be present in infected bite wounds. These infections are generally polymicrobial (i.e. more than one species of bacterium are involved): Trueperella, which requires oxygen for its multiplication, is often present in lesions.
- ANON., 1970. Report of the International Committee on Nomenclature of Bacteria. Taxonomic subcommittee for Gram-negative anaerobic rods. International Journal of Systematic Bacteriology, 20, 297–300.
- ANON., 1985. Annual Report, Alleton Regional Veterinary Laboratory, Private Bag X2, Cascades 3202, South Africa.
- BEERENS, H., FIEVAZ, L., WATTRE, P., 1971. Observations concernant souches appartenant aux espèces Sphaerophorus necrophorus, Sphaerophorus funduliformis, Sphaerophorus pseudonecrophorus. Annales Institute Pasteur (Paris), 121, 37–41.
- BELFIELD, A.J.M., 1986. Evaluation of laboratory tests for distinguishing between field strains of Bacteroides nodosus. In: STERWART, D.J., PETERSON, J.E., MCKERN, N.M. & EMERY, D.L., (eds). Proceedings of a Workshop, Melbourne 1985, CSIRO Division of Animal Health, Australian Wool Corporation, Australia.
- BERG, J.N. & SCANLAN, C.M., 1982. Studies of Fusobacterium necrophorum from bovine hepatic abscesses: Biotypes, quantitation, virulence, and antibiotic susceptibility. American Journal of Veterinary Research, 43, 1580–1586.
- BERKHOFF, G.A., 1977. Recovery and identification of anaerobes in veterinary medicine: A two-year experience. Veterinary Microbiology, 2, 237–252.
- BIBERSTEIN, E.L., KNIGHT, H.D. & ENGLAND, K., 1968. Bacteroides melaninogenicus in diseases of domestic animals. Journal of the American Veterinary Medical Association, 153, 1045–1049.
- BILLINGTON, S.J., JOHNSTON, J.L. & ROOD, J.I., 1996. Virulence regions and virulence factors of the ovine footrot pathogen, Dichelobacter nodosus. FEMS Microbiology Letters, 145, 147–156.
- BROOK, I. & WALKER, R.I., 1986. The relationship between Fusobacterium species and other flora in mixed infection. Journal of Medical Microbiology, 21, 93–100.
- CLAXTON, P.D., 1981. Serogrouping of Bacteroides nodosus in relation to protection by vaccination. In: BEVERIDGE, W.I.B. & EGERTON, J.R., (eds). Ovine footrot. A report of a workshop at the University of Sydney, 3–6 May 1981. Revesby, N.S.W. Craig Copying Co.
- CLAXTON, P.D., 1986. Serogrouping of Bacteroides nodosus isolates. In: STERWART, D.J., PETERSON, J.E., MCKERN, N.M. & EMERY, D.L., (eds). Proceedings of a Workshop, Melbourne 1985, CSIRO Division of Animal Health, Australian Wool Corporation, Australia.
- CLAXTON, P.D., RIBEIRO, L.A. & EGERTON, J.R., 1983. Classification of Bacteroides nodosus by agglutination tests. Australian Veterinary Journal, 60, 331–334.
- COYLE-DENNIS, J.E. & LAUERMAN, L.H., 1978. Biological and biochemical characteristics of Fusobacterium necrophorum leukocidin. American Journal of Veterinary Research, 39, 1790–1793.
- DEPIAZZI, L.J. & RICHARDS, R.B., 1979. A degrading proteinase test to distinguish benign and virulent ovine isolates of Bacteroides nodosus. Australian Veterinary Journal, 55, 25–28.
- DEPIAZZI, L.J. & RICHARDS, R.B., 1985. Motility in relation to virulence of Bacteroides nodosus. Veterinary Microbiology, 10, 107–116.
- DEPIAZZI, L.J., RICHARDS, R.B., MCQUADE, N.C. & ROOD, J.I., 1986. Virulence, protease, pilus and motility characteristics of Bacteroides nodosus. In: STERWART, D.J., PETERSON, J.E., MCKERN, N.M. & EMERY, D.L., (eds). Proceedings of a Workshop, Melbourne 1985, CSIRO Division of Animal Health, Australian Wool Corporation, Australia.
- DEWHIRST, F.E., PASTER, B.J., LA FONTAINE, S. & ROOD, J.I., 1990. Transfer of Kingella indologenes (Snell & La Page, 1976) to the genus Suttonella gen. nov. as Suttonella indologenes comb. nov., transfer of Bacteroides nodosus (Beveridge, 1941) to the genus Dichelobacter gen. nov. as Dichelobacter nodosus comb. nov. and assignment of the genera Cardiobacterium, Dichelobacter and Suttonella to Cardiobacteriaceae fam. nov. in the gamma division of Proteobacteria based on 16 S ribosomal ribonucleic acid sequence comparisons. International Journal of Systematic Bacteriology, 40, 426–433.
- DUNCAN, S.P., VALERA, R.C., MANZANO, J.V. & MACHOTA, S.V., 1990. Isolation and identification of anaerobic bacteria from ovine foot rot in Spain. Research in Veterinary Science, 49, 245–247.
- EGERTON, J.R. & PARSONSON, I.M., 1969. Benign footrot — a specific interdigital dermatitis of sheep associated with infection by less proteolytic strains of Bacteroides nodosus. Australian Veterinary Journal, 45, 345–349.
- EMERY, D.L., 1987. Immunity against anaerobic bacterial infections. Veterinary Immunology and Immunopathology, 15, 1–57.
- EMERY, D.L., DUFTY, J.H. & CLARK, B.L., 1984. Biochemical and functional properties of a leucocidin produced by several strains of Fusobacterium necrophorum. Australian Veterinary Journal, 61, 382–387.
- EMERY, D.L., STEWART, D.J., CLARK, B.L. & ELLEMAN, T.C., 1986. Protective parts of pili from Bacteroides nodosus. In: STEWART, D.J., PETERSON, J.E., MCKERN, N.M. & EMERY, D.L., (eds). Proceedings of a Workshop, Melbourne 1985, CSIRO Division of Animal Health, Australian Wool Corporation, Australia.
- ENGELKIRK, P.G., DUBEN-ENGELKIRK, J. & DOWELL, V.R., 1992. Principles and practice of clinical anaerobic bacteriology. Belmont, California: Star.
- EVERY, D., 1982. Proteinase isoenzyme patterns of Bacteroides nodosus: Distinction between ovine virulent isolates, ovine benign isolates and bovine isolates. Journal of General Microbiology, 128, 809–812.
- EVERY, D. & SKERMAN, T.M., 1982. Protection of sheep against experimental footrot by vaccination with pili purified from Bacteroides nodosus. New Zealand Veterinary Journal, 30, 156–158.
- GYLES, L.C. & THOEN, C.O., 1986. Pathogenesis of Bacterial Infections in Animals. Ames: Iowa State University Press.
- HITE, K.E., LOCKE, M. & HESSELTINE, H.C., 1949. Synergism in experimental infections with nonsporulating anaerobic bacteria. Journal of Infectious Diseases, 84, 1–9.
- HOFSTAD, T., 1982. Immunochemical studies of partially hydrolysed lipopolysaccharide from Fusobacterium nucleatum ATCC 10953. Acta Pathologica, Microbiologica et Immunologica Scandinavica, B90, 289–293.
- HOLDEMAN, L.V., KELLY, R.W. & MOORE, W.E.C., 1984. Family 1 Bacteroidaceae. In: KRIEG, N.R. & HOLT, J.G., (eds). Bergey’s Manual of Systematic Bacteriology. Vol I. Baltimore, London: Williams & Wilkins.
- KATZ, M.E., HOWARTH, P.M., YONK, W.K., RIFFKIN, G.G., DEPIAZZI, L.J. & ROOD, J.I., 1991. Identification of three gene regions associated with virulence in Dichelobacter nodosus, the causative agent of ovine footrot. Journal of General Microbiology, 137, 2117–2124
- KELLY, M.J., 1978. The quantitative and histological demonstration of pathogenic synergy between Escherichia coli and Bacteroides fragilis in guinea-pig wounds. Journal of Medical Microbiology, 11, 513–523.
- KENNAN, R.M., DHUNGUEL, O.P., WHITTINGTON, R.J., EGERTON, J.R. & ROOD, J.L., 2001. The type IV fimbrial subunit gene (fimA) of Dichelobacter nodosus is essential for virulence, protease secretion and natural competence. Journal of Bacteriology, 183, 4451–4458.
- LANGWORTH, B.F., 1977. Fusobacterium necrophorum: Its characteristics and role as an animal pathogen. Bacteriological Reviews, 41, 373–390.
- MOORE, W.E.C., HOLDEMAN, L.V. & KELLEY, R.W., 1984. Genus II Fusobacterium. In: KRIEG, N.R. & HOLT, J.G., (eds). Bergey’s Manual of Systematic Bacteriology. Vol. I. Baltimore, London: Williams and Wilkins
- NAGAI, S., KANOE, M. & TODA, M., 1984. Purification and partial characterization of Fusobacterium necrophorum haemagglutinin. Zentralblat für Bakteriologie, Microbiologie und Hygiene, Series A, 258, 232–241.
- NICHOLSON, L.A., MORROW, C.J., CORNER, L.A. & HODGSON, A.L.M., 1994. Phylogenetic relationship of Fusobacterium necrophorum A, AB and B biotypes based upon 16S + RNA gene sequence analysis. International Journal of Systematic Bacteriology, 44, 315–319.
- OKAHASHI, N., KOGA, Y., NISHIHARA, T., FUJIWARA, T. & HAMADA, S., 1988. Immunobiological properties of lipopolysaccharides isolated from Fusobacterium nucleatum and F. necrophorum. Journal of General Microbiology, 134, 1707–1715.
- ROBERTS, D.S., 1967. The pathogenic synergy of Fusiformis necrophorus and Corynebacterium pyogenes. I. Influence of the leucocidal exotoxin of F. necrophorus. British Journal of Experimental Pathology, 48, 665–673.
- ROBERTS, D.S., 1967. The pathogenic synergy of Fusiformis necrophorus and Corynebacterium pyogenes. II. The response of F. necrophorus to a filterable product of C. pyogenes. British Journal of Experimental Pathology, 48, 674–679.
- ROBERTS, D.S., 1970. Toxic, allergenic and immunogenic factors of Fusiformis necrophorus. Journal of Comparative Pathology, 80, 247–257.
- SHAH, H.N. & COLLINS, M.D., 1988. Proposal for reclassification of Bacteroides asaccharolyticus, Bacteroides gingivalis and Bacteroides endodontalis in a new genus, Porphyromonas. International Journal of Systematic Bacteriology, 38, 128–131.
- SHAH, H.N. & COLLINS, M.D., 1990. Prevotella, a new genus to include Bacteroides melaninogenicus and related species formerly classified in the genus Bacteroides. International Journal of Systematic Bacteriology, 40, 205–208.
- SHINJO, T., FUJISAWA, T. & MASUOKA, T., 1991. Proposal of two subspecies of Fusobacterium necrophorum (Flugge) Moore and Holdeman: Fusobacterium necrophorum subsp. necrophorum subsp. nov., nom. rev. (ex Flugge 1886), and Fusobacterium necrophorum subsp. funduliforme subsp. nov., nom. rev. (ex Hallé 1898). International Journal of Systematic Bacteriology, 41, 395–397.
- SHINJO, T., HIRAIWA, K. & MIYAZATO, S., 1990. Recognition of biovar C of Fusobacterium necrophorum (Flugge) Moore and Holdeman as Fusobacterium pseudonecrophorum sp. nov., nom. rev. (ex Prevot 1940). International Journal of Systematic Bacteriology, 40, 71–73.
- SKERMAN, T.M., ERASMUSON, S.K. & EVERY, D., 1981. Differentiation of Bacteroides nodosus biotypes and colony variants in relation to their virulence and immunoprotective properties in sheep. Infection and Immunity, 32, 788–795.
- SMITH, L.D.S., 1975. The Pathogenic Anaerobic Bacteria. 2nd edn. Illinois: Charles C. Thomas.
- STEWART, D.J., 1978. The role of various antigenic fractions of Bacteroides nodosus in eliciting protection against footrot in vaccinated sheep. Research in Veterinary Science, 24, 14–19
- STEWART, D.J., 1979. The role of elastase in the differentiation of Bacteroides nodosus infections in sheep and cattle. Research in Veterinary Science, 27, 99–105.
- STEWART, D.J., CLARK, B.L., PETERSON, J.E., GRIFFITHS, D.A. & SMITH, E.F., 1982. Importance of pilus-associated antigen in Bacteroides nodosus vaccines. Research in Veterinary Science, 32, 140–147
- SWEENEY, C.R., DIVERS, T.J. & BENSON, C.E., 1985. Anaerobic bacteria in 21 horses with pleuropneumonia. Journal of the American Veterinary Medical Association, 187, 721–724.
- TAN, Z.L., NAGARAJA, T.G. & CHENGAPPA, M.M., 1996. Fusobacterium infections: virulence factors, pathogenic mechanism and control measures. Veterinary Research Communications, 20, 113–140.
- THORLEY, C.M., 1976. A simplified method for the isolation of Bacteroides nodosus from ovine footrot and studies on its colony morphology and serology. Journal of Applied Bacteriology, 40, 301–309.
- YONG, W.K., MOSES, E.K. & RIFFKIN, G.G., 1986. Characterisation of virulence-associated antigens for differentiating virulent and benign strains of Bacteroides nodosus. In: STERWART, D.J., PETERSON, J.E., MCKERN, N.M. & EMERY, D.L., (eds). Proceedings of a Workshop, Melbourne 1985, CSIRO Division of Animal Health, Australian Wool Corporation, Australia.
- ZHOU, H. & HICKFORD, J.G.H., 2001. Short communication. Dichelobacter nodosus serotype M fimbrial subunit gene: Implications for serological classification. Veterinary Microbiology, 79, 367–374.