DOI QR코드

DOI QR Code

Antibiotic Resistance Profiles of Staphylococcus pseudintermedius Isolates from Canine Patients in Korea

  • Yoon, Jang-Won (Department of Food Science and Engineering, Ewha Womans University) ;
  • Lee, Ki-Jong (BK21 Basic and Diagnostic Veterinary Specialist Program for Animal Diseases and Department of Veterinary Internal Medicine, College of Veterinary Medicine, Konkuk University) ;
  • Lee, So-Young (BK21 Basic and Diagnostic Veterinary Specialist Program for Animal Diseases and Department of Veterinary Internal Medicine, College of Veterinary Medicine, Konkuk University) ;
  • Chae, Min-Joo (BK21 Basic and Diagnostic Veterinary Specialist Program for Animal Diseases and Department of Veterinary Internal Medicine, College of Veterinary Medicine, Konkuk University) ;
  • Park, Jae-Keun (BK21 Basic and Diagnostic Veterinary Specialist Program for Animal Diseases and Department of Veterinary Internal Medicine, College of Veterinary Medicine, Konkuk University) ;
  • Yoo, Jong-Hyun (BK21 Basic and Diagnostic Veterinary Specialist Program for Animal Diseases and Department of Veterinary Internal Medicine, College of Veterinary Medicine, Konkuk University) ;
  • Park, Hee-Myung (BK21 Basic and Diagnostic Veterinary Specialist Program for Animal Diseases and Department of Veterinary Internal Medicine, College of Veterinary Medicine, Konkuk University)
  • Received : 2010.01.15
  • Accepted : 2010.09.03
  • Published : 2010.12.28

Abstract

In this study, the prevalence of antibiotic resistance was examined among 74 Staphylococcus pseudintermedius strains recently isolated from clinical cases of canine pyoderma and otitis externa at the veterinary teaching hospital at Konkuk University, Korea. Bacterial resistance to the nine commonly used antibiotics was evaluated by a standard disk diffusion technique based on the guidelines of the Clinical and Laboratory Standards Institute. The results demonstrated that most S. pseudintermedius isolates were resistant to penicillin (95.9%) or tetracycline (91.9%), but highly susceptible to amoxicillin/clavulanic acid (90.5%). Among the 74 isolates, 13 mecA-positive and methicillin-resistant S. pseudintermedius (MRSP) strains were identified, displaying a high level of resistance (84.6-100%) to each of the individual antibiotics evaluated, with the exception of amoxicillin/clavulanic acid (46.2% resistance). Notably, all of the MRSP isolates exhibited simultaneous resistance to four or more different antibiotics, indicating that they are multiple drug resistant (MDR) strains. Taken together, these results imply that more careful selection or prescription of antibiotics for canine pyoderma and otitis externa should be required for reducing the emergence and/or spread of MDR strains, especially MDR-MRSP isolates, in veterinary pet clinics in Korea.

Keywords

References

  1. Bannoehr, J., A. Franco, M. Iurescia, A. Battisti, and J. R. Fitzgerald. 2009. Molecular diagnostic identification of Staphylococcus pseudintermedius. J. Clin. Microbiol. 47: 469-471. https://doi.org/10.1128/JCM.01915-08
  2. Bes, M., L. Saidi Slim, F. Becharnia, H. Meugnier, F. Vandenesch, J. Etienne, and J. Freney. 2002. Population diversity of Staphylococcus intermedius isolates from various host species: Typing by 16S-23S intergenic ribosomal DNA spacer polymorphism analysis. J. Clin. Microbiol. 40: 2275-2277. https://doi.org/10.1128/JCM.40.6.2275-2277.2002
  3. Descloux, S., A. Rossano, and V. Perreten. 2008. Characterization of new staphylococcal cassette chromosome mec (SCCmec) and topoisomerase genes in fluoroquinolone- and methicillinresistant Staphylococcus pseudintermedius. J. Clin. Microbiol. 46: 1818-1823. https://doi.org/10.1128/JCM.02255-07
  4. El Zubeir, I. E. M., T. Kanbar, J. Alber, C. Lammler, O. Akineden, R. Weiss, and M. Zschock. 2007. Phenotypic and genotypic characteristics of methicillin/oxacillin-resistant Staphylococcus intermedius isolated from clinical specimens during routine veterinary microbiological examinations. Vet. Microbiol. 121: 170-176. https://doi.org/10.1016/j.vetmic.2006.11.014
  5. Goodacre, R., R. Harvey, S. Howell, L. Greenham, and W. Noble. 1997. An epidemiological study of Staphylococcus intermedius strains isolated from dogs, their owners and veterinary surgeons. J. Anal. Appl. Pyrolysis 44: 49-64. https://doi.org/10.1016/S0165-2370(97)00076-4
  6. Griffeth, G. C., D. O. Morris, J. L. Abraham, F. S. Shofer, and S. C. Rankin. 2008. Screening for skin carriage of methicillinresistant coagulase-positive staphylococci and Staphylococcus schleiferi in dogs with healthy and inflamed skin. Vet. Dermatol. 19: 142-149. https://doi.org/10.1111/j.1365-3164.2008.00663.x
  7. Hanselman, B. A., S. Kruth, and J. S. Weese. 2008. Methicillin-resistant staphylococcal colonization in dogs entering a veterinary teaching hospital. Vet. Microbiol. 126: 277-281. https://doi.org/10.1016/j.vetmic.2007.06.015
  8. Harvey, R., R. Marples, and W. Noble. 1994. Nasal carriage of Staphylococcus intermedius in humans in contact with dogs. Microb. Ecol. Health Dis. 7: 225-227. https://doi.org/10.3109/08910609409141358
  9. Ihrke, P. J. 1987. An overview of bacterial skin disease in the dog. Br. Vet. J. 143: 112-118. https://doi.org/10.1016/0007-1935(87)90002-9
  10. Jones, R. D., S. A. Kania, B. W. Rohrbach, L. A. Frank, and D. A. Bemis. 2007. Prevalence of oxacillin- and multidrug-resistant staphylococci in clinical samples from dogs: 1,772 samples (2001-2005). J. Am. Vet. Med. Assoc. 230: 221-227. https://doi.org/10.2460/javma.230.2.221
  11. Kim, H. B., H. C. Jang, H. J. Nam, Y. S. Lee, B. S. Kim, W. B. Park, et al. 2004. In vitro activities of 28 antimicrobial agents against Staphylococcus aureus isolates from tertiary-care hospitals in Korea: A nationwide survey. Antimicrob. Agents Chemother. 48: 1124-1127. https://doi.org/10.1128/AAC.48.4.1124-1127.2004
  12. Loeffler, A., M. Linek, A. Moodley, L. Guardabassi, J. M. Sung, M. Winkler, R. Weiss, and D. H. Lloyd. 2007. First report of multiresistant, mecA-positive Staphylococcus intermedius in Europe: 12 cases from a veterinary dermatology referral clinic in Germany. Vet. Dermatol. 18: 412-421. https://doi.org/10.1111/j.1365-3164.2007.00635.x
  13. Martineau, F., F. J. Picard, L. Grenier, P. H. Roy, M. Ouellette, and M. G. Bergeron. 2000. Multiplex PCR assays for the detection of clinically relevant antibiotic resistance genes in staphylococci isolated from patients infected after cardiac surgery. The ESPRIT Trial. J. Antimicrob. Chemother. 46: 527-534. https://doi.org/10.1093/jac/46.4.527
  14. McDougal, L. K., C. D. Steward, G. E. Killgore, J. M. Chaitram, S. K. McAllister, and F. C. Tenover. 2003. Pulsedfield gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: Establishing a national database. J. Clin. Microbiol. 41: 5113-5120. https://doi.org/10.1128/JCM.41.11.5113-5120.2003
  15. Morris, D. O., E. A. Mauldin, K. O'Shea, F. S. Shofer, and S. C. Rankin. 2006. Clinical, microbiological, and molecular characterization of methicillin-resistant Staphylococcus aureus infections of cats. Am. J. Vet. Res. 67: 1421-1425. https://doi.org/10.2460/ajvr.67.8.1421
  16. Morris, D. O., K. A. Rook, F. S. Shofer, and S. C. Rankin. 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). Vet. Dermatol. 17: 332-337. https://doi.org/10.1111/j.1365-3164.2006.00536.x
  17. National Committee for Clinical Laboratory Standards. 2008. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals; approved standard. NCCLS, Wayne, PA.
  18. Pak, S. I. 2003. Study on the methicillin-resistant gene distribution of staphylococci isolated from dogs and cats. J. Vet. Clin. 20: 302-307.
  19. Park, S., S. B. Soumerai, A. S. Adams, J. A. Finkelstein, S. Jang, and D. Ross-Degnan. 2005. Antibiotic use following a Korean national policy to prohibit medication dispensing by physicians. Health Policy Plan. 20: 302-309. https://doi.org/10.1093/heapol/czi033
  20. Sasaki, T., K. Kikuchi, Y. Tanaka, N. Takahashi, S. Kamata, and K. Hiramatsu. 2007. Methicillin-resistant Staphylococcus pseudintermedius in a veterinary teaching hospital. J. Clin. Microbiol. 45: 1118-1125. https://doi.org/10.1128/JCM.02193-06
  21. Schwarz, S., K. Kadlec, and B. Strommenger. 2008. Methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius detected in the BfT-GermVet monitoring programme 2004-2006 in Germany. J. Antimicrob. Chemother. 61: 282-285.
  22. Scott, D., G. Muller, and C. Griffin. 2001. Bacterial skin diseases, pp. 274-335. Muller & Kirk's Small Animal Dermatology, 6th Ed. W. B. Saunders, Philadelphia.
  23. Tanner, M. A., C. L. Everett, and D. C. Youvan. 2000. Molecular phylogenetic evidence for noninvasive zoonotic transmission of Staphylococcus intermedius from a canine pet to a human. J. Clin. Microbiol. 38: 1628-1631.
  24. Tomasz, A., H. B. Drugeon, H. M. de Lencastre, D. Jabes, L. McDougall, and J. Bille. 1989. New mechanism for methicillin resistance in Staphylococcus aureus: Clinical isolates that lack the PBP 2a gene and contain normal penicillin-binding proteins with modified penicillin-binding capacity. Antimicrob. Agents Chemother. 33: 1869-1874. https://doi.org/10.1128/AAC.33.11.1869
  25. Yoo, J. H., J. W. Yoon, S. Y. Lee, and H. M. Park. 2010. High prevalence of fluoroquinolone- and methicillin-resistant Staphylococcus pseudintermedius isolates from canine pyoderma and otitis externa in veterinary teaching hospital. J. Microbiol. Biotechnol. 20: 798-802. https://doi.org/10.4014/jmb.0910.10044

Cited by

  1. Treatment outcome of dogs with meticillin‐resistant and meticillin‐susceptible Staphylococcus pseudintermedius pyoderma vol.23, pp.4, 2010, https://doi.org/10.1111/j.1365-3164.2012.01034.x
  2. In vitro miconazole susceptibility of meticillin‐resistant Staphylococcus pseudintermedius and Staphylococcus aureus vol.23, pp.5, 2010, https://doi.org/10.1111/j.1365-3164.2012.01068.x
  3. Genetic and phenotypic characterization of methicillin-resistant staphylococci isolated from veterinary hospitals in South Korea vol.24, pp.3, 2012, https://doi.org/10.1177/1040638712440985
  4. High prevalence of Enterococcus spp. from dogs with otitis externa vol.35, pp.2, 2010, https://doi.org/10.7853/kjvs.2012.35.2.099
  5. Prevalence of and risk factors for isolation of meticillin‐resistant Staphylococcus spp. from dogs with pyoderma in northern California, USA vol.24, pp.1, 2013, https://doi.org/10.1111/j.1365-3164.2012.01051.x
  6. A brief multi-disciplinary review on antimicrobial resistance in medicine and its linkage to the global environmental microbiota vol.4, pp.None, 2013, https://doi.org/10.3389/fmicb.2013.00096
  7. Staphylococci Isolated from Carriage Sites and Infected Sites of Dogs as a Reservoir of Multidrug Resistance and Methicillin Resistance vol.66, pp.2, 2010, https://doi.org/10.1007/s00284-012-0254-9
  8. Phage Type 187 as a Separate Subunit MboI Restriction Site Within the Staphylococcus aureus Species vol.66, pp.6, 2010, https://doi.org/10.1007/s00284-013-0319-4
  9. Canine superficial bacterial pyoderma: evaluation of skin surface sampling methods and antimicrobial susceptibility of causal Staphylococcus isolates vol.92, pp.5, 2010, https://doi.org/10.1111/avj.12176
  10. Antibiotic resistance and molecular characterization of ophthalmic Staphylococcus pseudintermedius isolates from dogs vol.15, pp.3, 2014, https://doi.org/10.4142/jvs.2014.15.3.409
  11. Pharmacokinetics and pharmacokinetic/pharmacodynamic integration of marbofloxacin after intravenous and intramuscular administration in beagle dogs vol.45, pp.3, 2010, https://doi.org/10.3109/00498254.2014.969794
  12. A Bioengineered Nisin Derivative to Control Biofilms of Staphylococcus pseudintermedius vol.10, pp.3, 2010, https://doi.org/10.1371/journal.pone.0119684
  13. Comparison of Harboring the Resistance Gene and Disc Diffusion Susceptibility Test Result in Staphylococcus pseudintermedius from the Bacterial Dermatitis vol.32, pp.2, 2010, https://doi.org/10.17555/jvc.2015.04.32.2.158
  14. Clinicopathological evaluation of non-parasitic dermatoses in canines vol.8, pp.11, 2010, https://doi.org/10.14202/vetworld.2015.1346-1350
  15. In Vitro Activities of Nisin and Nisin Derivatives Alone and In Combination with Antibiotics against Staphylococcus Biofilms vol.7, pp.None, 2010, https://doi.org/10.3389/fmicb.2016.00508
  16. Prevalence and risk factors of Staphylococcus spp. carriage among dogs and their owners: A cross-sectional study vol.212, pp.None, 2010, https://doi.org/10.1016/j.tvjl.2015.10.059
  17. 개와 고양이에서 분리한 methicillin 내성 및 감수성 Staphylococcus pseudintermedius vol.39, pp.3, 2010, https://doi.org/10.7853/kjvs.2016.39.3.175
  18. Prior antimicrobial use as a risk factor for resistance in selected Staphylococcus pseudintermedius isolates from the skin and ears of dogs vol.27, pp.6, 2010, https://doi.org/10.1111/vde.12382
  19. Antimicrobial susceptibility profiles of Staphylococcus spp. from domestic and wild animals vol.46, pp.12, 2016, https://doi.org/10.1590/0103-8478cr20160373
  20. Identification and Antimicrobial Susceptibility of Bacteria Isolated from Dogs with Chronic Otitis Externa vol.34, pp.1, 2017, https://doi.org/10.17555/jvc.2017.02.34.1.23
  21. Virulence Genes Detection and Antimicrobial Susceptibility of Staphylococcus pseudintermedius Isolates from Canine Skin Infection in Chennai, India vol.88, pp.1, 2010, https://doi.org/10.1007/s40011-016-0760-9
  22. 경북지역 개와 고양이에서 methicillin-resistant Staphylococcus. pseudintermedius (MRSP) 검출률 조사 vol.41, pp.4, 2010, https://doi.org/10.7853/kjvs.2018.41.4.229
  23. Carriage of Staphylococcus schleiferi from canine otitis externa: antimicrobial resistance profiles and virulence factors associated with skin infection vol.20, pp.2, 2010, https://doi.org/10.4142/jvs.2019.20.e6
  24. 인천지역 반려견 유래 세균의 항생제 내성 모니터링 조사 vol.42, pp.2, 2010, https://doi.org/10.7853/kjvs.2019.42.2.53
  25. Lytic Activity of Polyvalent Staphylococcal Bacteriophage PhiSA012 and Its Endolysin Lys-PhiSA012 Against Antibiotic-Resistant Staphylococcal Clinical Isolates From Canine Skin Infection Sites vol.7, pp.None, 2010, https://doi.org/10.3389/fmed.2020.00234
  26. Contamination of the urban environment with excrements of companion animals as an underestimated source of Staphylococcus species posing a threat to public health vol.68, pp.1, 2010, https://doi.org/10.1556/004.2020.00018
  27. Contamination of the urban environment with excrements of companion animals as an underestimated source of Staphylococcus species posing a threat to public health vol.68, pp.1, 2010, https://doi.org/10.1556/004.2020.00018
  28. Staphylococcus pseudintermedius: an undocumented, emerging pathogen in humans vol.15, pp.None, 2020, https://doi.org/10.3205/dgkh000367