What's happened to Staphylococcus intermedius? Taxonomic revision and emergence of multi-drug resistance

Journal of Small Animal Practice

Volumn 53, Issue 3, 2012, Pages 147-154

  Bond, R ^a   Loeffler, A ^a  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT;

ANIMAL; ANIMAL DISEASE; CLASSIFICATION; DOG; DOG DISEASE; DRUG EFFECT; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIOLOGY; MULTIDRUG RESISTANCE; PENICILLIN RESISTANCE; PHYLOGENY; REVIEW; STAPHYLOCOCCAL SKIN INFECTION; STAPHYLOCOCCUS INFECTION; STAPHYLOCOCCUS INTERMEDIUS;

ANIMALS; ANTI-BACTERIAL AGENTS; DOG DISEASES; DOGS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; METHICILLIN RESISTANCE; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; PHYLOGENY; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCAL SKIN INFECTIONS; STAPHYLOCOCCUS INTERMEDIUS;

ANIMALIA; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INTERMEDIUS; STAPHYLOCOCCUS PSEUDINTERMEDIUS;

EID: 84857945441     PISSN: 00224510     EISSN: 17485827     Source Type: Journal    
DOI: 10.1111/j.1748-5827.2011.01165.x     Document Type: Review

References (81)

1. Abraham, J. L., Morris, D. O., Griffeth, G. C., Shofer, F. S. & Rankin, S. C. (2007) Surveillance of healthy cats and cats with inflammatory skin disease for colonization of the skin by methicillin-resistant coagulase-positive staphylococci and Staphylococcus schleiferi ssp. schleiferi. Veterinary Dermatology 18, 252-259.
2. Allaker, R. P., Lloyd, D. H. & Bailey, R. M. (1992) Population sizes and frequency of staphylococci at mucocutaneous sites on healthy dogs. Veterinary Record 130, 303-304.
3. Baines, B. J., Loeffler, A., Milsom, S., Edwards, E. & Lloyd, D. H. (2008) Susceptibility of methicillin-resistant and methicillin-susceptible Staphylococcus aureus and Staphylococcus intermedius isolates from dogs and cats to three antiseptics. Scientific Proceedings, 51st BSAVA Congress. Birmingham, UK. p 452.
4. Bannoehr, J., Ben Zakour, N. L., Waller, A. S., Guardabassi, L., Thoday, K. L., Van Den Broek, A. H. & Fitzgerald, J. R. (2007) Population genetic structure of the Staphylococcus intermedius group: insights into agr diversification and the emergence of methicillin-resistant strains. Journal of Bacteriology 189, 8685-8692.
5. Bannoehr, J., Franco, A., Iurescia, M., Battisti, A. & Fitzgerald, J. R. (2009) Molecular diagnostic identification of Staphylococcus pseudintermedius. Journal of Clinical Microbiology 47, 469-471.
6. Barrow, G. I. & Feltham, R. K. A. (1993) Characterization tests. In: Cowan and Steel's Manual for the Identification of Medical Bacteria. 3rd edn. Eds G. I. Barrow and R. K. A. Feltham. Cambridge University Press, Cambridge. pp 219-238.
7. Boost, M. V., So, S. Y., Perreten, V. (2011) Low rate of methicillin-resistant coagulase-positive staphylococcal colonization of veterinary personnel in Hong Kong. Zoonoses Public Health 58, 36-40.
8. Campanile, F., Bongiorno, D., Borbone, S., Venditti, M., Giannella, M., Franchi, C. & Stefani, S. (2007) Characterization of a variant of the SCCmec element in a bloodstream isolate of Staphylococcus intermedius. Microbial Drug Resistance 13, 7-10.
9. CCAR. Canadian Committee on Antibiotic Resistance. Infection Prevention and Control Best Practices. For Small Animal Veterinary Clinics. August 2008.
10. Chesneau, O., Morvan, A., Aubert, S. & El Solh, N. (2000) The value of rRNA gene restriction site polymorphism analysis for delineating taxa in the genus Staphylococcus. International Journal Systematic and Evolutionary Microbiology 50, 689-697.
11. Coombs, G. W., Nimmo, G. R., Bell, J. M., Huygens, F., O'Brien, F. G., Malkowski, M. J., Pearson, J. C., Stephens, A. J. & Giffard, P. M. (2004) Australian Group for Antimicrobial Resistance. Genetic diversity among community methicillin-resistant Staphylococcus aureus strains causing outpatient infections in Australia. Journal of Clinical Microbiology 42, 4735-4743.
12. Cox, H. U., Hoskins, J. D., Newman, S. S., Turnwald, G. H., Foil, C. S., Roy, A. F. & Kearney, M. T. (1985a) Distribution of staphylococcal species on clinically healthy cats. American Journal of Veterinary Research 46, 1824-1828.
13. Cox, H. U., Newman, S. S., Roy, A. F., Hoskins, J. D. & Foil, C. S. (1985b) Comparison of coagulase test methods for identification of Staphylococcus intermedius from dogs. American Journal of Veterinary Research 46, 1522-1525.
14. Cox, H. U., Hoskins, J. D., Newman, S. S., Foil, C. S., Turnwald, G. H. & Roy, A. F. (1988) Temporal study of staphylococcal species on healthy dogs. American Journal of Veterinary Research 49, 747-751.
15. De Lucia, M., Moodley, A., Latronico, F., Giordano, A., Caldin, M., Fondati, A. & Guardabassi, L. (2010) Prevalence of canine methicillin resistant Staphylococcus pseudintermedius in a veterinary diagnostic laboratory in Italy. Research in Veterinary Science. DOI:10.1016/j.rvsc.2010.09.014.
16. Descloux, S., Rossano, A. & Perreten, V. (2008) Characterization of new staphylococcal cassette chromosome mec (SCCmec) and topoisomerase genes in fluoroquinolone- and methicillin-resistant Staphylococcus pseudintermedius. Journal of Clinical Microbiology 46, 1818-1823.
17. Devriese, L. A. & De Pelsmaecker, K. (1987) The anal region as a main carrier site of Staphylococcus intermedius and Streptococcus canis in dogs. Veterinary Record 121, 302-303.
18. Devriese, L. A. & Van De Kerckhove, A. (1979) A comparison of methods and the validity of deoxyribonuclease tests for the characterization of staphylococci isolated from animals. Journal of Applied Bacteriology 46, 385-393.
19. Devriese, L. A., Vancanneyt, M., Baele, M., Vaneechoutte, M., De Graef, E., Snauwaert, C., Cleenwerck, I., Dawyndt, P., Swings, J., Decostere, A. & Haesebrouck, F. (2005) Staphylococcus pseudintermedius sp. nov., a coagulase-positive species from animals. International Journal of Systematic and Evolutionary Microbiology 55, 1569-1573.
20. Devriese, L. A., Hermans, K., Baele, M. & Haesebrouck, F. (2009) Staphylococcus pseudintermedius versus Staphylococcus intermedius. Veterinary Microbiology 133, 206-207.
21. Frank, L. A., Kania, S. A., Kirzeder, E. M., Eberlein, L. C. & Bemis, D. A. (2009) Risk of colonization or gene transfer to owners of dogs with meticillin-resistant Staphylococcus pseudintermedius. Veterinary Dermatology 20, 496-501.
22. Freney, J., Kloos, W. E., Hajek, V., Webster, J. A., Bes, M., Brun, Y. & Vernozy-Rozand, C. (1999) Recommended minimal standards for description of new staphylococcal species. Subcommittee on the taxonomy of staphylococci and streptococci of the International Committee on Systematic Bacteriology. International Journal of Systematic and Evolutionary Microbiology 49, 489-502.
23. Gerstadt, K., Daly, J. S., Mitchell, M., Wessolossky, M. & Cheeseman, S. H. (1999) Methicillin-resistant Staphylococcus intermedius pneumonia following coronary artery bypass grafting. Clinical Infectious Diseases 29, 218-219.
24. Ghebremedhin, B., Layer, F., Konig, W. & Konig, B. (2008) Genetic classification and distinguishing of Staphylococcus species based on different partial gap, 16S rRNA, hsp60, rpoB, sodA, and tuf gene sequences. Journal of Clinical Microbiology 46, 1019-1025.
25. Goodacre, R., Harvey, R. G., Howell, S. A., Greenham, L. W. & Noble, W. C. (1997) An epidemiological study of Staphylococcus intermedius strains isolated from dogs, their owners and veterinary surgeons. Journal of Applied and Analytical Pyrolysis 44, 49-64.
26. Gortel, K., Campbell, K. L., Kamona, I., Whittem, T., Schaeffer, D. J. & Weisiger, R. M. (1999) Methicillin resistance among staphylococci isolated from dogs. American Journal of Veterinary Research 60, 1526-1530.
27. Greiner, M., Wolf, G. & Hartmann, K. (2007) Bacteraemia and antimicrobial susceptibility in dogs. Veterinary Record 160, 529-530.
28. Griffeth, G. C., Morris, D. O., Abraham, J. L., Shofer, F. S. & Rankin, S. C. (2008) Screening for skin carriage of methicillin-resistant coagulase-positive staphylococci and Staphylococcus schleiferi in dogs with healthy and inflamed skin. Veterinary Dermatology 19, 142-149.
29. Guardabassi, L., Loeber, M. E. & Jacobson, A. (2004) Transmission of multiple antimicrobial-resistant Staphylococcus intermedius between dogs affected by deep pyoderma and their owners. Veterinary Microbiology 98, 23-27.
30. Hajek, V. (1976). Staphylococcus intermedius, a new species isolated from animals. International Journal of Systematic and Evolutionary Microbiology 26, 401-408.
31. Hanselman, B. A., Kruth, S. A., Rousseau, J. & Weese, J. S. (2009) Coagulase positive staphylococcal colonization of humans and their household pets. Canadian Veterinary Journal 50, 954-958.
32. Harvey, R. G., Marples, R. R. & Noble, W. C. (1994) Nasal carriage of Staphylococcus intermedius in humans in contact with dogs. Microbial Ecology in Health and Disease 7, 225-227.
33. Hermans, K., Devriese, L. A. & Haesebrouck F. (2010) Staphylococcus. In: Pathogenesis of Bacterial Infections in Animals. Eds CL Gyles, JF Prescott, JG Songer, CO Thoen. Wiley-Blackwell, Ames, IA, USA. p 75-89.
34. Hill, P. B., Lo, A., Eden, C. A., Huntley, S., Morey, V., Ramsey, S., Richardson, C., Smith, D. J., Sutton, C., Taylor, M. D., Thorpe, E., Tidmarsh, R. & Williams, V. (2006) Survey of the prevalence, diagnosis and treatment of dermatological conditions in small animals in general practice. Veterinary Record 158, 533-539.
35. Hillier, A., Pinchbeck, L. R., Bannerman, T., Cole, L. K. & York, S. (2007) Coagulase-positive staphylococci at carriage sites post-cefpodoxime therapy in dogs. Veterinary Dermatology 18, 182.
36. Ishihara, K., Shimokubo, N., Sakagami, A., Ueno, H., Muramatsu, Y., Kadosawa, T. (2010) Occurrence and molecular characteristics of methicillin-resistant Staphylococcus aureus and methicillin-resistant Staphylococcus pseudintermedius in an academic veterinary hospital. Applied and Environmental Microbiology 76, 5165-5174.
37. Kadlec, K., Schwarz, S., Perreten, V., Andersson, U. G., Finn, M., Greko, C., Moodley, A., Kania, S. A., Frank, L. A., Bemis, D. A., Franco, A., Iurescia, M., Battisti, A., Duim, B., Wagenaar, J. A., Van Duijkeren, E., Weese, J. S., Fitzgerald, J. R., Rossano, A. & Guardabassi, L. (2010) Molecular analysis of methicillin-resistant Staphylococcus pseudintermedius of feline origin from different European countries and North America. Journal of Antimicrobial Chemotherapy 65, 1826-1828.
38. Kadlec, K., Van Duijkeren, E., Wagenaar, J. A. & Schwarz, S. (2011) Molecular basis of rifampicin resistance in methicillin-resistant Staphylococcus pseudintermedius isolates from dogs. Journal of Antimicrobial Chemotherapy 66, 1236-1242.
39. Kempker, R., Mangalat, D., Kongphet-Tran, T. & Eaton, M. (2009) Beware of the pet dog: a case of Staphylococcus intermedius infection. American Journal of the Medical Sciences 338, 425-427.
40. Kloos, W. E. & Bannerman, T. L. (1999) Staphylococcus and Micrococcus. In: Manual of Clinical Microbiology. 7th edn. Eds P. R. Murray. ASM Press, Washington, DC, USA. pp 264-277.
41. Lilenbaum, W., Nunes, E. L. & Azeredo, M. A. (1998) Prevalence and antimicrobial susceptibility of staphylococci isolated from the skin surface of clinically normal cats. Letters in Applied Microbiology 27, 224-228.
42. Lloyd, D. H. (2010) Recognising and controlling risk factors for antimicrobial resistance. Schweizer Archiv för Tierheilkunde 152, 131-134.
43. Lloyd, D. H., Lamport, A. I. & Feeney, C. (1996) Sensitivity to antibiotics amongst cutaneous and mucosal isolates of canine pathogenic staphylococci in the UK, 1980-96. Veterinary Dermatology 7, 171-175.
44. Loeffler, A., Boag, A. K., Sung, J., Lindsay, J. A., Guardabassi, L., Dalsgaard, A., Smith, H., Stevens, K. B. & Lloyd, D. H. (2005) Prevalence of methicillin-resistant Staphylococcus aureus among staff and pets in a small animal referral hospital in the UK. Journal of Antimicrobial Chemotherapy 56, 692-697.
45. Loeffler, A., Linek, M., Moodley, A., Guardabassi, L., Sung, J. M., Winkler, M., Weiss, R. & Lloyd, D. H. (2007) First report of multiresistant, mecA-positive Staphylococcus intermedius in Europe: 12 cases from a veterinary dermatology referral clinic in Germany. Veterinary Dermatology 18, 412-421.
46. MacFaddin, J. F. (1980) Biochemical Tests for Identification of Medical Bacteria. 2nd edn. Baltimore, MD, USA: Wiliams & Wilkins, p 523.
47. Mackay, A. D., Quick, A., Gillespie, S. H. & Kibbler, C. C. (1993) Coagulase-negative methicillin-resistant Staphylococcus aureus infection. Lancet 342, 492.
48. Mahoudeau, I., Delabranche, X., Prevost, G., Monteil, H. & Piemont, Y. (1997) Frequency of isolation of Staphylococcus intermedius from humans. Journal of Clinical Microbiology 35, 2153-2154.
49. Meyer, S. A. & Schleifer, K. H. (1978) Deoxyribonucleic acid reassociation in the classification of coagulase-positive staphylococci. Archives of Microbiology 117, 183-188.
50. Morris, D. O., Rook, K. A., Shofer, F. S. & Rankin, S. C. (2006) Screening of Staphylococcus aureus, Staphylococcus intermedius, and Staphylococcus schleiferi isolates obtained from small companion animals for antimicrobial resistance: a retrospective review of 749 isolates (2003-04). Veterinary Dermatology 17, 332-337.
51. Morris, D. O., Boston, R. C., O'Shea, K. & Rankin, S. C. (2010) The prevalence of carriage of meticillin-resistant staphylococci by veterinary dermatology practice staff and their respective pets. Veterinary Dermatology. DOI:10.1111/j.1365-3164.2010.00866.x.
52. National Association of State Public Health Veterinarians (NASPHV). (2008) Compendium of veterinary standard precautions for zoonotic disease prevention in veterinary personnel. JAVMA 233, 415-432.
53. Neely, A. N. & Maley, M. P. (2000) Survival of Enterococci and Staphylococci on hospital fabrics and plastic. Journal of Clinical Microbiology 38, 724-726.
54. Noble, W. C. (1992) Staphylococci on the skin. In: The Skin Microflora and Microbial Skin Disease. Ed W. C. Noble. Cambridge University Press, Cambridge. pp 135-52.
55. Ohara-Nemoto, Y., Haraga, H., Kimura, S. & Nemoto, T. K. (2008) Occurrence of staphylococci in the oral cavities of healthy adults and nasal oral trafficking of the bacteria. Journal of Medical Microbiology 57, 95-99.
56. Pellerin, J. L., Bourdeau, P., Sebbag, H. & Person, J. M. (1998) Epidemiosurveillance of antimicrobial compound resistance of Staphylococcus intermedius clinical isolates from canine pyodermas. Comparative Immunology, Microbiology & Infectious Diseases 21, 115-133.
57. Perreten, V., Kadlec, K., Schwarz, S., Gronlund-Andersson, U., Finn, M., Greko, C., Moodley, A., Kania S.A., Frank, L.A., Bemis, D. A., Franko, A., Iurescia, M., Battisti, A., Duim, B, Wagenaar, J.A., Van Duijkeren, E., Weese, J. S., Fitzgerald, J. R., Rossano, A. & Guardabassi, L. (2010) Clonal spread of methicillin-resistant Staphylococcus pseudintermedius in Europe and North America: an international multicentre study. Journal of Antimicrobial Chemotherapy 65, 1145-1154.
58. Pinchbeck, L. R., Cole, L. K., Hillier, A., Kowalski, J. J., Rajala-Schultz, P. J., Bannerman, T. L. & York, S. (2006) Genotypic relatedness of staphylococcal strains isolated from pustules and carriage sites in dogs with superficial bacterial folliculitis. American Journal of Veterinary Research 67, 1337-1346.
59. Pottumarthy, S., Schapiro, J. M., Prentice, J. L., Houze, Y. B., Swanzy, S. R., Fang, F. C. & Cookson B. T. (2004) Clinical isolates of Staphylococcus intermedius masquerading as methicillin-resistant Staphylococcus aureus. Journal of Clinical Microbiology 42, 5881-5884.
60. Rantala, M., Lahti, E., Kuhalampil, J., Pesonen, S., Järvinen, A. K., Saijonmaa-Koulumies, L. & Honkanen-Buzalski, T. (2004) Antimicrobial resistance in Staphylococcus spp., Escherichia coli and Enterococcus spp. in dogs given antibiotics for chronic dermatological disorders, compared with non-treated control dogs. Acta Veterinaria Scandinavica 45, 37-45.
61. Rao, J. G., Qamruddin, A. O., Hassan, I. A., Burnie, J. P. & Ganner, M. (2002) Cluster of clinical isolates of epidemic methicillin-resistant Staphylococcus aureus (EMRSA) with a negative deoxyribonuclease (DNase) test-implications for laboratory diagnosis and infection control. Journal of Hospital Infection 51, 238-239.
62. Ruscher, C., Lubke-Becker, A., Wleklinski, C. G., Soba, A., Wieler, L. H. & Walther, B. (2009) Prevalence of methicillin-resistant Staphylococcus pseudintermedius isolated from clinical samples of companion animals and equidaes. Veterinary Microbiology 136, 197-201.
63. Ruscher, C., Lubke-Becker, A., Semmler, T., Wleklinski, C. G., Paasch, A., Soba, A., Wieler, L. H. & Walther, B. (2010) Widespread rapid emergence of a distinct methicillin- and multidrug-resistant Staphylococcus pseudintermedius (MRSP) genetic lineage in Europe. Veterinary Microbiology 144, 340-346.
64. Saijonmaa-Koulumies, L., Parsons, E. & Lloyd, D. H. (1998) Elimination of Staphylococcus intermedius in healthy dogs by topical treatment with fusidic acid. Journal of Small Animal Practice 39, 341-347.
65. Sasaki, T., Kikuchi, K., Tanaka, Y., Takahashi, N., Kamata, S. & Hiramatsu, K. (2007) Reclassification of phenotypically identified Staphylococcus intermedius strains. Journal of Clinical Microbiology 45, 2770-2778.
66. Schwarz, S., Kadlec, K. & Strommenger, B. (2008) Methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius detected in the BfT-GermVet monitoring programme 2004-2006 in Germany. Journal of Antimicrobial Chemotherapy 61, 282-285.
67. Slettemeas, J. S., Mikalsen, J. & Sunde, M. (2010) Further diversity of the Staphylococcus intermedius group and heterogeneity in the MboI restriction site used for Staphylococcus pseudintermedius species identification. Journal of Veterinary Diagnostic Investigation 22, 756-759.
68. Steen, S. & Webb, P. (2010) Differing patterns of antimicrobial sensitivity among meticillin-resistant coagulase-positive staphylococci isolated from canines. In: British Veterinary Dermatology Study Group Spring Meeting 2010. Eds S. Warren. British Veterinary Dermatology Study Group, Birmingham. p 33.
69. Stegmann, R., Burnens, A., Maranta, C. A. & Perreten, V. (2010) Human infection associated with methicillin-resistant Staphylococcus pseudintermedius ST71. Journal of Antimicrobial Chemotherapy 65, 2047-2048.
70. Takahashi, T., Satoh, I. & Kikuchi, N. (1999) Phylogenetic relationships of 38 taxa of the genus Staphylococcus based on 16S rRNA gene sequence analysis. International Journal of Systematic and Evolutionary Microbiology 49, 725-728.
71. Talan, D. A., Staatz, D., Staatz, A. & Overturf, G. D. (1989) Frequency of Staphylococcus intermedius as human nasopharyngeal flora. Journal of Clinical Microbiology 27, 2393.
72. Tanner, M. A., Everett, C. L. & Youvan, D. C. (2000) Molecular phylogenetic evidence for noninvasive zoonotic transmission of Staphylococcus intermedius from a canine pet to a human. Journal of Clinical Microbiology 38, 1628-1631.
73. Vandenesch, F., Celard, M., Arpin, D., Bes, M., Greenland, T. & Etienne, J. (1995) Catheter-related bacteremia associated with coagulase-positive Staphylococcus intermedius. Journal of Clinical Microbiology 33, 2508-2510.
74. Van Duijkeren, E., Houwers, D. J., Schoormans, A., Broekhuizen-Stins, M. J., Ikawaty, R., Fluit, A. C. & Wagenaar, J. A. (2008) Transmission of methicillin-resistant Staphylococcus intermedius between humans and animals. Veterinary Microbiology 128, 213-215.
75. Van Duijkeren, E., Kamphuis, M., Van Der Mije, I. C., Laarhoven, L. M., Duim, B., Wagenaar, J. A. & Houwers, D. J. (2011) Transmission of methicillin-resistant Staphylococcus pseudintermedius between infected dogs and cats and contact pets, humans and the environment in households and veterinary clinics. Veterinary Microbiology 150, 338-343.
76. Van Hoovels, L., Vankeerberghen, A., Boel, A., Van Vaerenbergh, K. & De Beenhouwer H. (2006) First case of Staphylococcus pseudintermedius infection in a human. Journal of Clinical Microbiology 44, 4609-4612.
77. Varaldo, P. E., Kilpper-Balz, R., Biavasco, F., Satta, G. & Schleifer, K. H. (1988) Staphylococcus delphini sp. nov., a coagulase-positive species isolated from dolphins. International Journal of Systematic and Evolutionary Microbiology 38, 436-439.
78. Von Eiff, C., Becker, K., Machka, K., Stammer, H. & Peters, G. (2001) Nasal carriage as a source of Staphylococcus aureus bacteremia. New England Journal of Medicine 344, 11-16.
79. Wagenvoort, J. H. T., Sluijsmans, W. & Penders, R. J. R. (2000) Better environmental survival of outbreak vs. sporadic MRSA isolates. Journal of Hospital Infection 45, 231.
80. Waller, A. The creation of a new monster: MRSA and MRSI - important emerging veterinary and zoonotic diseases. The Veterinary Journal 169, 315-316.
81. WHO 2009.