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Research article

Clinical Microbiology and Biomedical Sciences

Characterization of Veterinary Hospital-Associated Isolates of Enterococcus Species in Korea

Yeon Soo Chung 1, Ka Hee Kwon 1, Sook Shin 1, Jae Hong Kim 1, Yong Ho Park 1 and Jang Won Yoon 1, 2*

1Department of Veterinary Microbiology, College of Veterinary Medicine, Seoul National University, Seoul 151-742, Republic of Korea, 1College of Veterinary Medicine, Kangwon National University, Chuncheon 200-701, Republic of Korea

Received: October 24, 2013; Accepted: November 24, 2013

J. Microbiol. Biotechnol. 2014; 24(3): 386-393

Published March 28, 2014 https://doi.org/10.4014/jmb.1310.10088

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

Possible cross-transmission of hospital-associated enterococci between human patients, medical staff, and hospital environments has been extensively studied. However, limited information is available for veterinary hospital-associated Enterococcus isolates. This study investigated the possibility of cross-transmission of antibiotic-resistant enterococci between dog patients, their owners, veterinary staff, and hospital environments. Swab samples (n =46 5) were obtained from five veterinary hospitals in Seoul, Korea, during 2011. Forty-three Enterococcus strains were isolated, representing seven enterococcal species. E. faecalis and E. faecium were the most dominant species (16 isolates each, 37.2%). Although slight differences in the antibiotic resistance profiles were observed between the phenotypic and the genotypic data, our antibiogram analysis demonstrated high prevalence of the multiple drug-resistant (MDR) isolates of E. faecalis (10/16 isolates, 62.5%) and E. faecium (12/16 isolates, 75.0%). Pulsed-field gel electrophoretic comparison of the MDR isolates revealed three different clonal sets of E. faecalis and a single set of E. faecium, which were isolated from different sample groups or dog patients at the same or two separate veterinary hospitals. These results imply a strong possibility of cross-transmission of the antibiotic-resistant enterococcal species between animal patients, owners, veterinary staff, and hospital environments.

Keywords

Antibiotic resistance, Enterococci, Veterinary hospitals, Genetic relatedness, Cross-transmission

References

  1. 2012. T he r ise of the Enterococcus:beyond vancomycin resistance. Nat. Rev. Microbiol. 10: 266278.
    CrossRef
  2. Bohme H, Konigsmark C, Klare I, Zischka M, Werner G. 2012. Cross-transmission rates of enterococcal isolates among newborns in a neonatal intensive care unit. Pediatr. Rep. 4:e15.
  3. Bozdogan B, Leclercq R. 1999. Effects of genes encoding resistance to streptogramins A and B on the activity of quinupristin-dalfopristin against Enterococcus faecium. Antimicrob. Agents Chemother. 43: 2720-2725.
    CrossRef
  4. Cauwerts K, Decostere A, De Graef EM, Haesebrouck F, Pasmans F. 2007. High prevalence of tetracycline resistance in Enterococcus isolates from broilers carrying the erm(B) gene. Avian Pathol. 36: 395-399.
    CrossRef
  5. Cetinkaya Y, Falk P, Mayhall CG. 2000. Vancomycinresistant enterococci. Clin. Microbiol. Rev. 13: 686-707.
  6. Clark NC, Cooksey RC, Hill BC, Swenson JM, Tenover FC. 1993. Characterization of glycopeptide-resistant enterococci from U.S. hospitals. Antimicrob. Agents Chemother. 37: 2 31 12317.
    CrossRef
  7. Clewell DB. 1990. Movable genetic elements and antibiotic resistance in enterococci. Eur. J. Clin. Microbiol. Infect. Dis. 9:90-102.
    CrossRef
  8. Dina J, Malbruny B, Leclercq R. 2003. Nonsense mutations in the lsa-like gene in Enterococcus faecalis isolates susceptible to lincosamides and streptogramins A. Antimicrob. Agents Chemother. 47: 2307-2309.
    CrossRef
  9. Duh RW, Singh KV, Malathum K, Murray BE. 2001 . In vitro activity of 19 antimicrobial agents against enterococci from healthy subjects and hospitalized patients and use of an ace gene probe from Enterococcus faecalis for species identification. Microb. Drug Resist. 7: 39-46.
    CrossRef
  10. Dupre I, Zanetti S, Schito AM, Fadda G, Sechi LA. 2003. Incidence of virulence determinants in clinical Enterococcus faecium and Enterococcus faecalis isolates collected in Sardinia (Italy). J. Med. Microbiol. 52: 491-498.
    CrossRef
  11. Fisher K, Phillips C. 2009. The ecology, epidemiology and virulence of Enterococcus. Microbiology 155: 1749-1757.
  12. Ghosh A, Kukanich K, Brown CE, Zurek L. 2012. Resident cats in small animal veterinary hospitals carry multi-drug resistant enterococci and are likely involved in crosscontamination of the hospital environment. Front Microbiol. 3: 62.
    CrossRef
  13. Giraffa G. 2002. Enterococci from foods. FEMS Microbiol. Rev. 26: 163-171.
    CrossRef
  14. Hummel A, Holzapfel WH, Franz CM. 2007. Characterisation and transfer of antibiotic resistance genes from enterococci isolated from food. Syst. Appl. Microbiol. 30: 1-7.
    CrossRef
  15. Huycke MM, Sahm DF, Gilmore MS. 1998. Multiple-drug resistant enterococci: the nature of the problem and an agenda for the future. Emerg. Infect. Dis. 4: 239-249.
    CrossRef
  16. Jackson CR, Fedorka-Cray PJ, Barrett JB. 2004. Use of a genus- and species-specific multiplex PCR for identification of enterococci. J. Clin. Microbiol. 42: 3558-3565.
  17. Jackson CR, Fedorka-Cray PJ, Davis JA, Barrett JB, Brousse JH, Gustafson J, Kucher M. 2010. Mechanisms of antimicrobial resistance and genetic relatedness among enterococci isolated from dogs and cats in the United States. J. Appl. Microbiol. 108: 2171-2179.
    CrossRef
  18. Jackson CR, Fedorka-Cray PJ, Davis JA, Barrett JB, Frye JG. 2009. Prevalence, species distribution and antimicrobial resistance of enterococci isolated from dogs and cats in the United States. J. Appl. Microbiol. 107: 1269-1278.
  19. Jensen LB, Frimodt-Moller N, Aarestrup FM. 1999. Presence of erm gene classes in gram-positive bacteria of animal and human origin in Denmark. FEMS Microbiol. Lett. 170: 1 51158.
  20. Ke D, Picard FJ, Martineau F, Menard C, Roy PH, Ouellette M, Bergeron MG. 1999. Development of a PCR assay for rapid detection of enterococci. J. Clin. Microbiol. 37: 34973503.
    CrossRef
  21. Kobayashi N, Alam M, Nishimoto Y, Urasawa S, Uehara N, Watanabe N. 2001. Distribution of aminoglycoside resistance genes in recent clinical isolates of Enterococcus faecalis, Enterococcus faecium and Enterococcus avium. Epidemiol. Infect. 126: 197-204.
  22. Kos VN, Desjardins CA, Griggs A, Cerqueira G, Van Tonder A, Holden MT, et al. 2012. Comparative genomics of vancomycin-resistant Staphylococcus aureus strains and their positions within the clade most commonly associated with methicillin-resistant S. aureus hospital-acquired infection in the United States. MBio. 3.
    CrossRef
  23. KuKanich KS, Ghosh A, Skarbek JV, Lothamer KM, Zurek L. 2012. Surveillance of bacterial contamination in small animal veterinary hospitals with special focus on antimicrobial resistance and virulence traits of enterococci. J. Am. Vet. Med. Assoc. 240: 437-445.
    CrossRef
  24. Kwon KH, Hwang SY, Moon BY, Park YK, Shin S, Hwang CY, Park YH. 2012. Occurrence of antimicrobial resistance and virulence genes, and distribution of enterococcal clonal complex 17 from animals and human beings in Korea. J. Vet. Diagn. Invest. 24: 924-931.
    CrossRef
  25. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. 2012. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect. 18: 268-281.
    CrossRef
  26. Malhotra-Kumar S, Lammens C, Piessens J, Goossens H. 2005. Multiplex PCR for simultaneous detection of macrolide and tetracycline resistance determinants in streptococci. Antimicrob. Agents Chemother. 49: 4798-4800.
  27. Marothi YA, Agnihotri H, Dubey D. 2005. Enterococcal resistance - an overview. Indian J. Med. Microbiol. 23: 2 1 4219.
  28. Murray BE. 1990. The life and times of the Enterococcus. Clin. Microbiol. Rev. 3: 46-65.
  29. NCCLS. 2009. Performance Standards for Antimicrobial Susceptibility Testing, Nineteenth Informational Supplement. CLSI document M100-S19 NCCLS, Wayne, PA.
    CrossRef
  30. Poeta P, Costa D, Rodrigues J, Torres C. 2006. Antimicrobial resistance and the mechanisms implicated in faecal enterococci from healthy humans, poultry and pets in Portugal. Int. J. Antimicrob. Agents 27: 131-137.
    CrossRef
  31. Top J , Willems R, van der Velden S, Asbroek M, Bonten M. 2008. Emergence of clonal complex 17 Enterococcus faecium in The Netherlands. J. Clin. Microbiol. 46: 214-219.

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Article

Research article

J. Microbiol. Biotechnol. 2014; 24(3): 386-393

Published online March 28, 2014 https://doi.org/10.4014/jmb.1310.10088

Copyright © The Korean Society for Microbiology and Biotechnology.

Characterization of Veterinary Hospital-Associated Isolates of Enterococcus Species in Korea

Yeon Soo Chung 1, Ka Hee Kwon 1, Sook Shin 1, Jae Hong Kim 1, Yong Ho Park 1 and Jang Won Yoon 1, 2*

1Department of Veterinary Microbiology, College of Veterinary Medicine, Seoul National University, Seoul 151-742, Republic of Korea, 1College of Veterinary Medicine, Kangwon National University, Chuncheon 200-701, Republic of Korea

Received: October 24, 2013; Accepted: November 24, 2013

Abstract

Possible cross-transmission of hospital-associated enterococci between human patients,
medical staff, and hospital environments has been extensively studied. However, limited
information is available for veterinary hospital-associated Enterococcus isolates. This study
investigated the possibility of cross-transmission of antibiotic-resistant enterococci between
dog patients, their owners, veterinary staff, and hospital environments. Swab samples (n =46 5)
were obtained from five veterinary hospitals in Seoul, Korea, during 2011. Forty-three
Enterococcus strains were isolated, representing seven enterococcal species. E. faecalis and E.
faecium were the most dominant species (16 isolates each, 37.2%). Although slight differences
in the antibiotic resistance profiles were observed between the phenotypic and the genotypic
data, our antibiogram analysis demonstrated high prevalence of the multiple drug-resistant
(MDR) isolates of E. faecalis (10/16 isolates, 62.5%) and E. faecium (12/16 isolates, 75.0%).
Pulsed-field gel electrophoretic comparison of the MDR isolates revealed three different clonal
sets of E. faecalis and a single set of E. faecium, which were isolated from different sample
groups or dog patients at the same or two separate veterinary hospitals. These results imply a
strong possibility of cross-transmission of the antibiotic-resistant enterococcal species between
animal patients, owners, veterinary staff, and hospital environments.

Keywords: Antibiotic resistance, Enterococci, Veterinary hospitals, Genetic relatedness, Cross-transmission

References

  1. 2012. T he r ise of the Enterococcus:beyond vancomycin resistance. Nat. Rev. Microbiol. 10: 266278.
    CrossRef
  2. Bohme H, Konigsmark C, Klare I, Zischka M, Werner G. 2012. Cross-transmission rates of enterococcal isolates among newborns in a neonatal intensive care unit. Pediatr. Rep. 4:e15.
  3. Bozdogan B, Leclercq R. 1999. Effects of genes encoding resistance to streptogramins A and B on the activity of quinupristin-dalfopristin against Enterococcus faecium. Antimicrob. Agents Chemother. 43: 2720-2725.
    CrossRef
  4. Cauwerts K, Decostere A, De Graef EM, Haesebrouck F, Pasmans F. 2007. High prevalence of tetracycline resistance in Enterococcus isolates from broilers carrying the erm(B) gene. Avian Pathol. 36: 395-399.
    CrossRef
  5. Cetinkaya Y, Falk P, Mayhall CG. 2000. Vancomycinresistant enterococci. Clin. Microbiol. Rev. 13: 686-707.
  6. Clark NC, Cooksey RC, Hill BC, Swenson JM, Tenover FC. 1993. Characterization of glycopeptide-resistant enterococci from U.S. hospitals. Antimicrob. Agents Chemother. 37: 2 31 12317.
    CrossRef
  7. Clewell DB. 1990. Movable genetic elements and antibiotic resistance in enterococci. Eur. J. Clin. Microbiol. Infect. Dis. 9:90-102.
    CrossRef
  8. Dina J, Malbruny B, Leclercq R. 2003. Nonsense mutations in the lsa-like gene in Enterococcus faecalis isolates susceptible to lincosamides and streptogramins A. Antimicrob. Agents Chemother. 47: 2307-2309.
    CrossRef
  9. Duh RW, Singh KV, Malathum K, Murray BE. 2001 . In vitro activity of 19 antimicrobial agents against enterococci from healthy subjects and hospitalized patients and use of an ace gene probe from Enterococcus faecalis for species identification. Microb. Drug Resist. 7: 39-46.
    CrossRef
  10. Dupre I, Zanetti S, Schito AM, Fadda G, Sechi LA. 2003. Incidence of virulence determinants in clinical Enterococcus faecium and Enterococcus faecalis isolates collected in Sardinia (Italy). J. Med. Microbiol. 52: 491-498.
    CrossRef
  11. Fisher K, Phillips C. 2009. The ecology, epidemiology and virulence of Enterococcus. Microbiology 155: 1749-1757.
  12. Ghosh A, Kukanich K, Brown CE, Zurek L. 2012. Resident cats in small animal veterinary hospitals carry multi-drug resistant enterococci and are likely involved in crosscontamination of the hospital environment. Front Microbiol. 3: 62.
    CrossRef
  13. Giraffa G. 2002. Enterococci from foods. FEMS Microbiol. Rev. 26: 163-171.
    CrossRef
  14. Hummel A, Holzapfel WH, Franz CM. 2007. Characterisation and transfer of antibiotic resistance genes from enterococci isolated from food. Syst. Appl. Microbiol. 30: 1-7.
    CrossRef
  15. Huycke MM, Sahm DF, Gilmore MS. 1998. Multiple-drug resistant enterococci: the nature of the problem and an agenda for the future. Emerg. Infect. Dis. 4: 239-249.
    CrossRef
  16. Jackson CR, Fedorka-Cray PJ, Barrett JB. 2004. Use of a genus- and species-specific multiplex PCR for identification of enterococci. J. Clin. Microbiol. 42: 3558-3565.
  17. Jackson CR, Fedorka-Cray PJ, Davis JA, Barrett JB, Brousse JH, Gustafson J, Kucher M. 2010. Mechanisms of antimicrobial resistance and genetic relatedness among enterococci isolated from dogs and cats in the United States. J. Appl. Microbiol. 108: 2171-2179.
    CrossRef
  18. Jackson CR, Fedorka-Cray PJ, Davis JA, Barrett JB, Frye JG. 2009. Prevalence, species distribution and antimicrobial resistance of enterococci isolated from dogs and cats in the United States. J. Appl. Microbiol. 107: 1269-1278.
  19. Jensen LB, Frimodt-Moller N, Aarestrup FM. 1999. Presence of erm gene classes in gram-positive bacteria of animal and human origin in Denmark. FEMS Microbiol. Lett. 170: 1 51158.
  20. Ke D, Picard FJ, Martineau F, Menard C, Roy PH, Ouellette M, Bergeron MG. 1999. Development of a PCR assay for rapid detection of enterococci. J. Clin. Microbiol. 37: 34973503.
    CrossRef
  21. Kobayashi N, Alam M, Nishimoto Y, Urasawa S, Uehara N, Watanabe N. 2001. Distribution of aminoglycoside resistance genes in recent clinical isolates of Enterococcus faecalis, Enterococcus faecium and Enterococcus avium. Epidemiol. Infect. 126: 197-204.
  22. Kos VN, Desjardins CA, Griggs A, Cerqueira G, Van Tonder A, Holden MT, et al. 2012. Comparative genomics of vancomycin-resistant Staphylococcus aureus strains and their positions within the clade most commonly associated with methicillin-resistant S. aureus hospital-acquired infection in the United States. MBio. 3.
    CrossRef
  23. KuKanich KS, Ghosh A, Skarbek JV, Lothamer KM, Zurek L. 2012. Surveillance of bacterial contamination in small animal veterinary hospitals with special focus on antimicrobial resistance and virulence traits of enterococci. J. Am. Vet. Med. Assoc. 240: 437-445.
    CrossRef
  24. Kwon KH, Hwang SY, Moon BY, Park YK, Shin S, Hwang CY, Park YH. 2012. Occurrence of antimicrobial resistance and virulence genes, and distribution of enterococcal clonal complex 17 from animals and human beings in Korea. J. Vet. Diagn. Invest. 24: 924-931.
    CrossRef
  25. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. 2012. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect. 18: 268-281.
    CrossRef
  26. Malhotra-Kumar S, Lammens C, Piessens J, Goossens H. 2005. Multiplex PCR for simultaneous detection of macrolide and tetracycline resistance determinants in streptococci. Antimicrob. Agents Chemother. 49: 4798-4800.
  27. Marothi YA, Agnihotri H, Dubey D. 2005. Enterococcal resistance - an overview. Indian J. Med. Microbiol. 23: 2 1 4219.
  28. Murray BE. 1990. The life and times of the Enterococcus. Clin. Microbiol. Rev. 3: 46-65.
  29. NCCLS. 2009. Performance Standards for Antimicrobial Susceptibility Testing, Nineteenth Informational Supplement. CLSI document M100-S19 NCCLS, Wayne, PA.
    CrossRef
  30. Poeta P, Costa D, Rodrigues J, Torres C. 2006. Antimicrobial resistance and the mechanisms implicated in faecal enterococci from healthy humans, poultry and pets in Portugal. Int. J. Antimicrob. Agents 27: 131-137.
    CrossRef
  31. Top J , Willems R, van der Velden S, Asbroek M, Bonten M. 2008. Emergence of clonal complex 17 Enterococcus faecium in The Netherlands. J. Clin. Microbiol. 46: 214-219.
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