Strain typing and antimicrobial susceptibility of methicillin-resistant coagulase-positive staphylococcal species in dogs and people associated with dogs in Thailand

Journal of Applied Microbiology

Volumn 117, Issue 2, 2014, Pages 572-586

  Chanchaithong, P ^a   Perreten, V ^b   Schwendener, S ^b   Tribuddharat, C ^c   Chongthaleong, A ^d   Niyomtham, W ^a   Prapasarakul, N ^a  

^a CHULALONGKORN UNIVERSITY   (Thailand)

^b VETSUISSE FACULTY UNIVERSITY OF ZURICH   (Switzerland)

^c MAHIDOL UNIVERSITY   (Thailand)

^d CHULALONGKORN UNIVERSITY   (Thailand)

Author keywords

Antimicrobial resistance; Dogs; Genetic characteristics; Humans; Methicillin resistant Staphylococcus pseudintermedius

Indexed keywords

BACTERIA; ELECTROPHORESIS; GENES;

ANTIMICROBIAL RESISTANCES; ANTIMICROBIAL SUSCEPTIBILITY; DOG; GENETIC CHARACTERISTICS; HUMAN; METHICILLIN; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; METHICILLIN-RESISTANT STAPHYLOCOCCUS PSEUDINTERMEDIUS; RESISTANCE GENES; THAILAND;

HEALTH HAZARDS;

CHLORAMPHENICOL; CIPROFLOXACIN; CLINDAMYCIN; DALFOPRISTIN PLUS QUINUPRISTIN; ERYTHROMYCIN; FUSIDIC ACID; GENTAMICIN; KANAMYCIN; LINEZOLID; OXACILLIN; PENICILLIN DERIVATIVE; PSEUDOMONIC ACID; RIFAMPICIN; STREPTOMYCIN; SULFAMETHOXAZOLE; TETRACYCLINE; TRIMETHOPRIM; VANCOMYCIN; COAGULASE;

CANID; COAGULATION; DISEASE TRANSMISSION; GENE EXPRESSION; GENOTYPE; MICROBIAL ACTIVITY; PHENOTYPE; PUBLIC HEALTH;

ANIMAL EXPERIMENT; ANTIBIOTIC SENSITIVITY; ARTICLE; BROTH DILUTION; COAGULASE POSITIVE STAPHYLOCOCCUS; CONTROLLED STUDY; DNA FINGERPRINTING; EXPERIMENTAL DOG; FEMALE; GENOTYPE; MALE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; METHICILLIN RESISTANT STAPHYLOCOCCUS PSEUDINTERMEDIUS; METHICILLIN RESISTANT STAPHYLOCOCCUS SCHLEIFERI; MICROARRAY ANALYSIS; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PHENOTYPE; PULSED FIELD GEL ELECTROPHORESIS; SPECIES IDENTIFICATION; STAPHYLOCOCCUS PSEUDINTERMEDIUS; STAPHYLOCOCCUS SCHLEIFERI; THAILAND; VETERINARIAN; ANIMAL; ANTIBIOTIC RESISTANCE; CLASSIFICATION; DOG; DRUG EFFECTS; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; PENICILLIN RESISTANCE; STAPHYLOCOCCUS;

THAILAND;

ANIMALIA; CANIS FAMILIARIS; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS; STAPHYLOCOCCUS PSEUDINTERMEDIUS; STAPHYLOCOCCUS SCHLEIFERI SUBSP. COAGULANS;

ANIMALS; COAGULASE; DOGS; DRUG RESISTANCE, BACTERIAL; ELECTROPHORESIS, GEL, PULSED-FIELD; HUMANS; METHICILLIN RESISTANCE; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MULTILOCUS SEQUENCE TYPING; STAPHYLOCOCCUS; THAILAND;

EID: 84904696131     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12545     Document Type: Article

References (45)

1. Argudín, M.A., Rudicio, M.R. and Guerra, B. (2010) The emerging methicillin-resistant Staphylococcus aureus ST398 clone can easily be typed using the Cfr9I SmaI-neoschizomer. Lett Appl Microbiol 50, 127-130.
2. Bannoehr, J., Ben Zakour, N.L., Waller, A.S., Guardabassi, L., Thoday, K.L., van den Broek, A.H. and Fitzgerald, J.R. (2007) Population genetic structure of the Staphylococcus intermedius group: insights into agr diversification and the emergence of methicillin-resistant strains. J Bacteriol 189, 8685-8692.
3. Beck, K.M., Waisglass, S.E., Dick, H.L.N. and Weese, J.S. (2012) Prevalence of meticillin-resistant Staphylococcus pseudintermedius (MRSP) from skin and carriage sites of dogs after treatment of their meticillin-resistant or meticillin-sensitive staphylococcal pyoderma. Vet Dermatol 23, 369-e367.
4. Bemis, D.A., Jones, R.D., Frank, L.A. and Kania, S.A. (2009) Evaluation of susceptibility test breakpoints used to predict mecA-mediated resistance in Staphylococcus pseudintermedius isolated from dogs. J Vet Diagn Invest 21, 53-58.
5. Black, C.C., Solyman, S.M., Eberlein, L.C., Bemis, D.A., Woron, A.M. and Kania, S.A. (2009) Identification of a predominant multilocus sequence type, pulsed-field gel electrophoresis cluster, and novel staphylococcal chromosomal cassette in clinical isolates of mecA-containing, methicillin-resistant Staphylococcus pseudintermedius. Vet Microbiol 139, 333-338.
6. Boerlin, P., Burnens, A.P., Frey, J., Kuhnert, P. and Nicolet, J. (2001) Molecular epidemiology and genetic linkage of macrolide and aminoglycoside resistance in Staphylococcus intermedius of canine origin. Vet Microbiol 79, 155-169.
7. Boost, M.V., So, S.Y. and Perreten, V. (2009) Low rate of methicillin-resistant coagulase-positive staphylococcal colonization of veterinary personnel in Hong Kong. Zoonoses Public Health 58, 36-40.
8. Brown, D.F.J., Edwards, D.I., Hawkey, P.M., Morrison, D., Ridgway, G.L., Towner, K.J. and Wren, M.W.D. (2005) Guidelines for laboratory diagnosis and susceptibility testing of methicillin-resistant Staphylococcus aureus (MRSA). J Antimicrob Chemother 56, 1000-1018.
9. Cain, C.L., Morris, D.O., O'Shea, K. and Rankin, S.C. (2011) Genotypic relatedness and phenotypic characterization of Staphylococcus schleiferi subspecies in clinical samples from dogs. Am J Vet Res 72, 96-102.
10. Chanchaithong, P. and Prapasarakul, N. (2011) Biochemical markers and protein pattern analysis for canine coagulase-positive staphylococci and their distribution on dog skin. J Microbiol Methods 86, 175-181.
11. Chuang, C.Y., Yang, Y.L., Hsueh, P.R. and Lee, P.I. (2010) Catheter-related bacteremia caused by Staphylococcus pseudintermedius refractory to antibiotic-lock therapy in a hemophilic child with dog exposure. J Clin Microbiol 48, 1497-1498.
12. Clinical Laboratory Standards Institute (2013) Performance standard for antimicrobial susceptibility testing; twenty-third informational supplement. In CLSI Document M100-S23. ed. Tertel, M.L. pp. 72-86. Wayne, PA: Clinical Laboratory Standards Institute.
13. Descloux, S., Rossano, A. and Perreten, V. (2008) Characterization of new staphylococcal cassette chromosome mec (SCCmec) and topoisomerase genes in fluoroquinolone and methicillin-resistant Staphylococcus pseudintermedius. J Clin Microbiol 46, 1818-1823.
14. van Duijkeren, E., Kamphuis, M., van der Mije, I.C., Laarhoven, L.M., Duim, B., Wagenaar, J.A. and 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. Vet Microbiol 150, 338-343.
15. Enright, M.C., Day, N.P.J., Davies, C.E., Peacock, S.J. and Spratt, B.G. (2000) Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38, 1008-1015.
16. Feng, Y., Tian, W., Lin, D., Luo, Q., Zhou, Y., Yang, T., Deng, Y., Liu, Y.-H. et al. (2012) Prevalence and characterization of methicillin-resistant Staphylococcus pseudintermedius in pets from South China. Vet Microbiol 160, 517-524.
17. Igimi, S., Takahashi, E. and Mitsuoka, T. (1990) Staphylococcus schleiferi subsp. coagulans subsp. nov., isolated from the external auditory meatus of dogs with external ear otitis. Int J Syst Bacteriol 40, 409-411.
18. International Working Group on the Classification of Staphylococcal Cassette Chromosome Elements (IWG-SCC) (2009) Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements. Antimicrob Agents Chemother 53, 4961-4967.
19. Kadlec, K. and Schwarz, S. (2012) Antimicrobial resistance of Staphylococcus pseudintermedius. Vet Dermatol 23, 276-e255.
20. Kadlec, K., Feßler, A.T., Hauschild, T. and Schwarz, S. (2012) Novel and uncommon antimicrobial resistance genes in livestock-associated methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 18, 745-755.
21. Kluytmans, J., van Belkum, A. and Verbrugh, H. (1997) Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev 10, 505-520.
22. Kondo, Y., Ito, T., Ma, X.X., Watanabe, S., Kreiswirth, B.N., Etienne, J. and Hiramatsu, K. (2007) Combination of multiplex PCRs for staphylococcal cassette chromosome mec type assignment: rapid identification system for mec, ccr, and major differences in junkyard regions. Antimicrob Agents Chemother 51, 264-274.
23. Kumar, D., Cawley, J.J., Irizarry-Alvarado, J.M., Alvarez, A. and Alvarez, S. (2007) Case of Staphylococcus schleiferi subspecies coagulans endocarditis and metastatic infection in an immune compromised host. Transpl Infect Dis 9, 336-338.
24. Laarhoven, L.M., de Heus, P., van Luijn, J., Duim, B., Wagenaar, J.A. and van Duijkeren, E. (2011) Longitudinal study on methicillin-resistant Staphylococcus pseudintermedius in households. PLoS One 6, e27788.
25. May, E.R., Kinyon, J.M. and Noxon, J.O. (2012) Nasal carriage of Staphylococcus schleiferi from healthy dogs and dogs with otitis, pyoderma ot both. Vet Microbiol 160, 443-448.
26. Morris, D.O., Boston, R.C., O'Shea, K. and Rankin, S.C. (2010) The prevalence of carriage of meticillin-resistant staphylococci by veterinary dermatology practice staff and their respective pets. Vet Dermatol 21, 400-407.
27. Nhan, T.X., Leclercq, R. and Cattoir, V. (2011) Prevalence of toxin genes in consecutive clinical isolates of Staphylococcus aureus and clinical impact. Eur J Clin Microbiol 30, 719-725.
28. Pan, A., Battisti, A., Zoncada, A., Bernieri, F., Boldini, M., Franco, A., Giorgi, M., Iurescia, M. et al. (2009) Community-acquired methicillin-resistant Staphylococcus aureus ST398 infection, Italy. Emerg Infect Dis 15, 845-847.
29. Paul, N.C., Moodley, A., Ghibaudo, G. and Guardabassi, L. (2011) Carriage of methicillin-resistant Staphylococcus pseudintermedius in small animal veterinarians: indirect evidence of zoonotic transmission. Zoonoses Public Health 58, 533-539.
30. Perreten, V., Vorlet-Fawer, L., Slickers, P., Ehricht, R., Kuhnert, P. and Frey, J. (2005) Microarray-based detection of 90 antibiotic resistance genes of gram-positive bacteria. J Clin Microbiol 43, 2291-2302.
31. Perreten, V., Kadlec, K., Schwarz, S., Andersson, U.G., Finn, M., Greko, C., Moodley, A., Kania, S.A. et al. (2010) Clonal spread of methicillin-resistant Staphylococcus pseudintermedius in Europe and North America: an international multicentre study. J Antimicrob Chemother 65, 1145-1154.
32. Perreten, V., Chanchaithong, P., Prapasarakul, N., Rossano, A., Blum, S.E., Elad, D. and Schwendener, S. (2013) Novel pseudo-staphylococcal cassette chromosome mec element (ΨSCCmec57395) in methicillin-resistant Staphylococcus pseudintermedius CC45. Antimicrob Agents Chemother 57, 5509-5515.
33. Roberts, S., O'Shea, K., Morris, D., Robb, A., Morrison, D. and Rankin, S. (2005) A real-time PCR assay to detect the Panton Valentine Leukocidin toxin in staphylococci: screening Staphylococcus schleiferi subspecies coagulans strains from companion animals. Vet Microbiol 107, 139-144.
34. Sasaki, T., Kikuchi, K., Tanaka, Y., Takahashi, N., Kamata, S. and Hiramatsu, K. (2007) Methicillin-resistant Staphylococcus pseudintermedius in a veterinary teaching hospital. J Clin Microbiol 45, 1118-1125.
35. Sasaki, T., Tsubakishita, S., Tanaka, Y., Sakusabe, A., Ohtsuka, M., Hirotaki, S., Kawakami, T., Fukata, T. et al. (2010) Multiplex-PCR method for species identification of coagulase-positive staphylococci. J Clin Microbiol 48, 765-769.
36. Shore, A.C., Deasy, E.C., Slickers, P., Brennan, G., O'Connell, B., Monecke, S., Ehricht, R. and Coleman, D.C. (2011) Detection of staphylococcal cassette chromosome mec type XI carrying highly divergent mecA, mecI, mecR1, blaZ, and ccr genes in human clinical isolates of clonal complex 130 methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 55, 3765-3773.
37. Soedarmanto, I., Kanbar, T., Ülbegi-Mohyla, H., Hijazin, M., Alber, J., Lämmler, C., Akineden, Ö., Weiss, R. et al. (2011) Genetic relatedness of methicillin-resistant Staphylococcus pseudintermedius (MRSP) isolated from a dog and the dog owner. Res Vet Sci 91, e25-e27.
38. Solyman, S.M., Black, C.C., Duim, B., Perreten, V., van Duijkeren, E., Wagenaar, J.A., Eberlein, L.C., Sadeghi, L.N. et al. (2013) Multilocus sequence typing (MLST) for characterization of Staphylococcus pseudintermedius. J Clin Microbiol 51, 306-310.
39. Stegmann, R., Burnens, A., Maranta, C.A. and Perreten, V. (2010) Human infection associated with methicillin-resistant Staphylococcus pseudintermedius ST71. J Antimicrob Chemother 65, 2047-2048.
40. Strommenger, B., Kettlitz, C., Werner, G. and Witte, W. (2003) Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in Staphylococcus aureus. J Clin Microbiol 41, 4089-4094.
41. Vakulenko, S.B., Donabedian, S.M., Voskresenskiy, A.M., Zervos, M.J., Lerner, S.A. and Chow, J.W. (2003) Multiplex PCR for detection of aminoglycoside resistance genes in enterococci. Antimicrob Agents Chemother 47, 1423-1426.
42. Walther, B., Hermes, J., Cuny, C., Wieler, L.H., Vincze, S., Abou Elnaga, Y., Stamm, I., Kopp, P.A. et al. (2012) Sharing more than friendship-nasal colonization with coagulase-positive staphylococci (CPS) and co-habitation aspects of dogs and their owners. PLoS One 7, e35197.
43. Wang, Y., Yang, J., Logue, C.M., Liu, K., Cao, X., Zhang, W., Shen, J. and Wu, C. (2012) Methicillin-resistant Staphylococcus pseudintermedius isolated from canine pyoderma in North China. J Appl Microbiol 112, 623-630.
44. Weese, J.S. and van Duijkeren, E. (2010) Methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius in veterinary medicine. Vet Microbiol 140, 418-429.
45. Wendlandt, S., Lozano, C., Kadlec, K., Gómez-Sanz, E., Zarazaga, M., Torres, C. and Schwarz, S. (2013) The enterococcal ABC transporter gene lsa(E) confers combined resistance to lincosamides, pleuromutilins and streptogramin A antibiotics in methicillin-susceptible and methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother 68, 473-475.