Staphylococcus spp. infections

Staphylococcus spp. infections

Staphylococcus spp., are Gram-positive bacteria, some of which cause suppurative disease processes in animals and humans. Of the over 40 species recognized at present (Table 1) 9, 15 only four (Staphylococcus aureus, S. epidermidis, S. pseudintermedius and S. hyicus) are significant in livestock. These cause various suppurative infections, especially abscesses, mastitis and pyoderma (Table 2). They occur as part of the normal microbial flora on the skin and mucous membranes of healthy humans and animals, and, to a lesser extent, in the environment.

The causation of lesions in the skin and mucous membranes by Staphylococcus depends on a number of factors, such as trauma, the immune status of the animal, disturbance of the normal microflora and whether or not the particular Staphylococcus strain produces certain toxins and enzymes.

Micrococcus spp. are common in the environment and on skin but they are not regarded as pathogenic and are distinguished from Staphylococcus spp. only in that they are strict aerobes. Planococcus spp. are found only in marine habitats, and in clams, shrimps and prawns.17

Stomatococcus, previously thought to have belonged to the family Micococcae, is now known to belong to Rothia. 4 Staphylococcus spp. are Gram-positive cocci (0,8 to 1,0 µm in diameter), non-motile, facultatively anaerobic, and catalase-positive, and in pus they form clusters like bunches of grapes.

Table 1 Currently recognized Staphylococcus spp

S. aureus S. epidermidis group S. epidermidis
    S. capitis
S. pseudintermedius   S. warneri
    S. haemolyticus
S. hyicus   S. hominis
    S. saccharolyticus
S. schleiferi subsp. coagulans    
S. delphini    
S. lutrae    
  S. saprophyticus group S. saprophyticus
    S. cohnii
    S. xylosus
  S. simulans group S. simulans
    S. carnosus
  S. sciuri group S. sciur
    S. lentus
  Other unrelated species S. auricularis
    S. gallinarum
    S. caprae
    S. arlettae
    S. chromogenes
    S. condimenti
    S. equorum
    S. felis
    S. fleurettii
    S. kloosii
    S. lugdumensis
    S. pasteuri
    S. piscifermentans
    S. schleiferi subsp. schleiferi
    S. succinus
    S. vitulinus

Table 2 Most common diseases caused by Staphylococcus spp. in livestock

Staphylococcus aureus Mastitis Cattle, sheep, goats
  Botryomycosis Horses, cattle, pigs
  Suppurative wound infections All livestock species
  Abscesses All livestock species
  Tick pyaemia Lambs
S. hyicus Exudative epidermitis (greasy pig disease) Pigs
  Polyarthritis Pigs
  Mastitis Cattle
S. epidermidis Causes no specific disease entity: occurs on normal skin (opportunistic pathogen) Wide variety of animal species and humans
S. pseudintermedius Pyoderma Dogs
  Mastitis Cattle

Table 3 Characteristics that differentiate the pathogenic Staphylococcus spp.16

Pigment +w
Haemolysis + −w d
Maltose + + w
Mannitol + d
Coagulase + + d
Clumping factor + d
Deoxyribonuclease + −w + +

+ 90 per cent or more strains positive

− 90 per cent or more strains negative

d 11–89 per cent of strains positive

w weak reaction

They grow well on conventional culture media such as blood tryptose agar or nutrient agar, forming white to yellowish-orange, butyrous colonies, the colour being due to the production of a carotenoid pigment. The colonies of some species, especially S. aureus, may be surrounded by a zone of haemolysis, due to the effect of haemolysins, such as alpha and delta haemolysins, produced by them. The individual species of Staphylococcus are biochemically distinct (Table 3) and ferment sugars with the formation of acid but not gas.

Staphylococcus organisms are among the most resistant of the non-sporing bacteria to dehydration, are relatively heat-resistant (they are destroyed by a temperature of 60 °C maintained for 30 minutes), tolerate common disinfectants better than most other bacteria, and are generally resistant to many of the commonly used antimicrobial drugs.20

Staphylococcus, depending on the species, may be ubiquitous or may occupy very specific ecological niches. An example is S. epidermidis, which inhabits the skin of mammals, especially humans and domestic animals.

Its preferred site is the skin close to natural openings, where it is well placed to opportunistically infect adjacent organs such as the udder or to cause wound infections. In contrast, S. saccharolyticus is only found on the skin of the human forehead and S. auricularis in the external auditory meatus of humans, while S. gallinarum occurs on the skin of poultry, and S. lentus on the skin of goats and sheep.16

Phage-typing and biochemical differences are used to differentiate between biotypes of S. aureus, 5, 14, 21, 28 of which four are now recognized. These are S. aureus biovar A (human), biovar B (porcine), biovar C (bovine and ovine) and biovar D (hares). The biovars previously referred to as E and F are not species-specific (dogs, pigeons, mink and horses), and are now nearly all known to be S. pseudintermedius. 13, 14 Reference to coagulase-positive S. aureus strains in the older literature may include S. pseudintermedius. Phage typing of S. pseudintermedius has been described19 but is not generally used.

Some S. aureus strains are able to produce capsules which are an extracellular polysaccharide layer or layers surrounding the cell wall.2 Twelve capsular serotypes are known, and the incidence of serotypes varies geographically.12, 25, 27 The capsule promotes virulence as encapsulated strains are more resistant to phagocytosis.2

The cell wall of Staphylococcus spp. contains peptidoglycan, in which L-lysine is the diamino acid, and teichoic acid.16 Staphylococcus aureus also contains a small basic protein, protein A, in its cell wall, that reacts with the Fc fragment of the IgG molecules, and is antiphagocytic and fixes complement.24

Various toxins and enzymes are produced by S. aureus but, with the exception of the exfoliative toxin produced by S. hyicus, few, if any, toxins or enzymes are produced by the other Staphylococcus spp. Toxins produced by S. aureus include haemolysins (alpha, beta, gamma and delta), leukocidin and enterotoxin. The alpha haemolysin is dermonecrotic and leukocidal, and produces complete haemolysis of erythrocytes of rabbits, sheep and cattle, but it has no effect on those of humans and horses.1 This haemolysin is thought to play a major role in the pathogenesis of blue udder or gangrenous mastitis in sheep, not only because of its haemolytic and leukocidal effects, but also because it destroys blood platelets and causes vasoconstriction.3 The beta haemolysin is unique to animal biotypes of S. aureus. It is a sphingomyelinase C and produces incomplete haemolysis of sheep and bovine erythrocytes, but it does not affect those of horses when incubated at 37 °C. Complete haemolysis does, however, occur when cultures containing horse red blood cells are stored at 4 to 15 °C after being incubated.26 The gamma haemolysin only produces weak haemolysis, while the delta haemolysin is a phospholipase with effects similar to those of alpha haemolysinin thatit causes haemolysis of erythrocytes of humans, sheep, rabbits, guinea pigs and horses, and is also leukocidal and dermonecrotic.

Many strains of S. aureus produce heat-stable enterotoxins, which, when ingested by humans in food, cause food poisoning manifested by gastroenteritis. Six (A–E and H)8 serologically distinct enterotoxin types are recognized. The enterotoxin types produced do not correspond to S. aureus biotypes, which are alphabetically named. About 40 per cent of human strains produce enterotoxin.7 Enterotoxin producing strains of S. aureus may produce more than one type of enterotoxin.

Staphylococcal enterotoxin C is divided into five subtypes, 1, 2, 3, ovine and bovine. Another subtype of staphylococcal enterotoxin type C has been described from canine isolates of S. pseudintermedius. 8

Strains of S. aureus that produce enterotoxin A, or both enterotoxins A and B are responsible for about 70 per cent of outbreaks of food poisoning.11

Enterotoxins are relatively heat-resistant proteins, and the usual boiling of food inactivates them slowly, e.g. enterotoxins A and B are both slowly inactivated at 100 °C, requiring between 10 and nearly 40 minutes depending on the concentration of the toxin and the substrate,7 but temperatures used in canning food usually destroy any enterotoxin present. Enterotoxins can withstand the action of proteases such as trypsin and chymotrypsin.7 Strains implicated in food poisoning should be examined for enterotoxin production.16

Enterotoxin is optimally produced in foods which can support satisfactory growth of the contaminating S. aureus strain at a temperature of 35 to 40 °C; lesser amounts are produced at lower temperatures.11 Milk of mastitic cows infected with S. aureus may contain enterotoxins and may therefore cause food poisoning in humans who consume it. Certain stains of S. auerus may also produce a number of other enzymes, including coagulase, deoxyribonuclease, hyaluronidase, fibrinolysin, lipase and protease. The presence of coagulase and deoxyribonuclease correlates positively with virulence of the bacterium and is used for identification purposes.16 Hyaluronidase,6 fibrinolysin (staphylokinase) which causes the lysis of thrombi by activating plasminogen, and protease enhance the spread of Staphylococcus in tissues, while the lipase degrades bacterial fatty acids on the skin.20

Coagulase has the ability to clot plasma prepared from blood which has been treated with an anticoagulant such as heparin, EDTA or oxalate. Two forms of coagulase are produced: bound coagulase or clumping factor, which is produced by S. aureus subspecies aureus, S. schleiferi subsp. schleiferi and most strains of S pseudintermedius, and free coagulase, which is produced by S. aureus (both S. aureus subsp. aureus and S. aureus subsp. anaerobius), S. pseudintermedius, S. schleiferi subsp. coagulans, S. delphini, S. lutrae and some strains of S. hyicus subsp. hyicus. 8, 16, 22 Bound coagulase is detected by a slide test, while free coagulase is detected by a tube test. The slide test is usually used as a screening test as it is rapidly performed, and the tube coagulase test is regarded as the definitive test. Rabbit or human plasma is used and must always be tested with known coagulase positive and coagulase-negative strains before being put into general use, as the plasma from certain individuals may not react correctly in the test.17 The coagulase test should be carried out under carefully standardized conditions to ensure optimal results.16, 18


  1. ARBUTHNOTT, J.P., 1970. Staphylococcal alpha-toxin. In: MONTIE, T.C., KADIS, S. & AJL, S.J., (eds). Microbial Toxins. Vol. III. New York, London: Academic Press, Inc.
  2. BASELGA, R., ALBIZU, I. & AMORENA, B., 1994. Staphylococcus aureus capsule and slime as virulence factors in ruminant mastitis. A review. Veterinary Microbiology, 39, 195–204.
  3. BROWN, R.W. & SHERER, R.K., 1958. A study of the necrotising action of staphylococci alpha toxin. American Journal of Veterinary Research, 19, 354–362.
  4. COLLINS, M.D., HUTSON, R.A., BÅVERUD, V. & FALSEN, E., 2000. Characterization of a Rothis-like organism from a mouse: Description of Rothis nasimurium sp. nov., and reclassification of Stomatococcus mucilaginosus as Rothia mucilaginosa comb. nov. International Journal of Systematic and Evolutionary Microbiology, 50, 1247–1251.
  5. DAVIDSON, I., 1961. A set of bacteriophages for typing bovine staphylococci. Research in Veterinary Science, 2, 396–407.
  6. DURAN-REYNALS, F., 1942. Tissue permeability and the spreading factors in infection. Bacteriological Reviews, 6, 197–252.
  7. EASMON, C.S.F. & GOODFELLOW, M., 1990. Staphylococcus and Micrococcus. In: PARKER, M.T. & COLLIER, L.H., (eds). Topley and Wilson’s Principles of Bacteriology, Virology and Immunity. 8th edn. London: Edward Arnold.
  8. EDWARDS, V.M., DERINGER, J.R., CALLANTINE, S.D., DEOBALD, C.F., BERGER, P.H., KAPUR, V., STAUFFACHER, C.V. & BOHACH, G.A., 1997. Characterization of the canine type C enterotoxin produced by Staphylococcus pseudintermedius pyoderma isolates. Infection and Immunity, 65, 2346–2352
  9. EUZÉBE, J.P., 1997. List of bacterial names with standing in nomenclature: A folder available on the Internet. (Updated to 2002, 47, 590–592.
  10. FOSTER, G., ROSS, H.M., HUTSON, R.A. & COLLINS, M.D., 1997. Staphylococcus lutrae sp. nov., a new coagulase-positive species isolated from otters. International Journal of Systematic Bacteriology, 47, 724–726.
  11. GILBERT, R.J., ROBERTS, D. & SMITH, G., 1984. Food-borne diseases and botulism. In: WILSON, G.S., MILES, A.A. & PARKER, M.T., (eds). Topley and Wilson’s Principles of Bacteriology, Virology and Immunity. 7th edn. London: Edward Arnold.
  12. GUIDRY, A., FATTORN, A., PATEL, A., O’BRIEN, C., SHEPHERD, S. & LOHUIS, J., 1998. Serotyping scheme for Staphylococcus aureus isolated from cows with mastitis. American Journal of Veterinary Research, 59, 1537–1539.
  13. HÁJEK, V., 1976. Staphylococcus pseudintermedius, a new species isolated from animals. International Journal of Systematic Bacteriology, 26, 401–408.
  14. HÁJEK, V. & MARSÁLEK, E., 1971. The differentiation of pathogenic staphylococci and a suggestion for their taxonomic classification. Zentralblatt für Bakteriologie, Parasitenkunde, Infectionskrankheiten und Hygiene, Abteilung 1 Original A 217, 176–182
  15. HOLT, J.G., KRIEK, N.R., SNEATH, P.H.A., STALEY, J.T. & WILLIAMS, S.T., 2000. Bergey’s Manual of Determinative Bacteriology. 9th edn. Philadelphia, Baltimore, New York, London, Buenos Aires, Hong Kong, Sydney, Tokyo: Lippincott Willimas & Wilkins
  16. KLOOS, W.E. & SCHLEIFER, K.H., 1986. Genus IV. Staphylococcus. In: SNEATH, P.H.A., MAIR, N.S., SHARPE, M.E. & HOLT, J.G., (eds). Bergey’s Manual of Systematic Bacteriology. Vol. II. Baltimore: Williams & Wilkins.
  17. KOCUR, M. 1986. Genus III. Staphylococcus. In: sneath, p.h.a., mair, n.s., sharpe, m.e. & holt, j.g., (eds). Bergey’s Manual of Systematic Bacteriology. Vol. II. Baltimore: Williams & Wilkins.
  18. MACFADDIN, J.F., 1980. Biochemical Tests for Identification of Medical Bacteria. 2nd edn. Baltimore: Williams & Wilkins.
  19. OVERTURF, G.D., TALAN, D.A., SINGER, K., ANDERSON, N., MILLER, J.I., GREENE, R.T. & FROMAN, S., 1991. Phage typing of Staphylococcus pseudintermedius. Journal of Clinical Microbiology, 29, 373–375.
  20. PARKER, M.T., 1983. Staphylococcus and Micrococcus; the anaerobic Gram-positive cocci. In: PARKET, M.T., (ed.). Topley and Wilson’s Principles of Bacteriology, Virology and Immunity. 7th edn. London: Edward Arnold.
  21. PARKER, M.T., 1983. The significance of phage-typing patterns of Staphylococcus aureus: In: EASMON, C.S.F. & ADLAM, C., (eds). Staphylococci and Staphylococcal Infections. London: Academic Press, Inc.
  22. PHILLIPS, W.E. & KLOOS, W.E., 1981. Identification of coagulase-positive Staphylococcus pseudintermedius and Staphylococcus hyicus subsp. hyicus isolates from veterinary clinical specimens. Journal of Clinical Microbiology, 14, 671–673.
  23. SCHLIEFER, K.H., 1986. Gram-positive cocci. In: SNEATH, P.H.A., MAIR, N.S., SHARPE, M.E. & HOLT, J.G., (eds). Bergey’s Manual of Systematic Bacteriology. Vol. II. Baltimore: Williams and Wilkins.
  24. SJOQUIST, J., MOVITZ, J., JOHANSSON, I-B. & HJELM, H., 1972. Localization of Protein A in the bacteria. European Journal of Biochemistry, 30, 190–194.
  25. SORDELLI, D.O., BUZZOLA, F.R., GOMEZ, M.I., STEELE-MOORE, L., BERG, D., GENTILINI, E., CATALANO, M., REITZ, A.J., TOLLERSRUD, T., DENAMIEL, G., JERIC, P. & LEE, J.C., 2000. Capsule expression by bovine isolates of Staphylococcus aureus from Argentina: Genetic and Epidemiologic Analyses. Journal of Clinical Microbiology, 38, 846–850
  26. TIMONEY, J.F., GILLESPIE, J.H., SCOTT, F.W. & BARLOUGH, J.E., 1989. Hagan and Bruner’s Microbiology and Infectious Diseases of Domestic Animals. 8th edn. Ithaca, London: Comstock Publishing Associates.
  27. TOLLERSRUD, T., KENNY, K., REITZ, A.R.JR. & LEE, J.C., 2000. Genetic and serologic evaluation of capsule production by bovine mammary isolates of Staphylococcus aureus and other Staphylococcus spp. from Europe and the United States. Journal of Clinical Microbiology, 38, 2998–3003.
  28. WANG, C.T., 1978. Bacteriophage typing of canine staphylococci. I. Typing by use of the international phage sets for human and bovine staphylococci. Japanese Journal of Veterinary Science, 40, 401–405.