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Characterization of antimicrobial resistance and application of RFLP for epidemiological monitoring of thermophilic Campylobacter spp. isolated from dogs and humans in Korea

  • Cho, Hyun-Ho (Animal, Plant and Fisheries Quarantine and Inspection Agency) ;
  • Kim, Sang-Hyun (Viral Infectious Disease Research Center, Korea Research Institute of Bioscience & Biotechnology) ;
  • Min, Wongi (College of Veterinary Medicine, Research Institute of Life Science, Institute of animal medicine, Gyeongsang National University) ;
  • Ku, Bok-Kyung (Animal, Plant and Fisheries Quarantine and Inspection Agency) ;
  • Kim, Jong-Hyun (Division of Enteric Bacteria Infections, Center for Infectious Disease, National Institute of Health) ;
  • Kim, Yong-Hwan (College of Veterinary Medicine, Research Institute of Life Science, Institute of animal medicine, Gyeongsang National University)
  • Received : 2013.08.01
  • Accepted : 2014.03.17
  • Published : 2014.06.30

Abstract

An antimicrobial susceptibility test was conducted to compare the resistance rates among Campylobacter spp. isolates from dogs (n = 50) raised under diverse conditions and humans (n = 50). More than 60% of Campylobacter (C.) jejuni from dogs and humans showed resistance to nalidixic acid, enrofloxacin and ciprofloxacin. C. jejuni isolates from humans showed higher resistance to tetracycline (83.3%) and ampicillin (91.3%) than those from dogs. None of the C. jejuni or Campylobacter coli isolates from humans or dogs were resistant to erythromycin. Overall, 85% of Campylobacter spp. isolates showed a multidrug resistant phenotype. Nucleotide sequencing analysis of the gryA gene showed that 100% of $NA^R/CIP^R$ C. jejuni isolates from dogs and humans had the Thr-$86^{th}$-Ile mutation, which is associated with fluoroquinolone resistance. flaA PCR restriction fragment length polymorphism (RFLP) typing to differentiate the isolates below the species level revealed 12 different clusters out of 73 strains. The human isolates belonged to eight different RFLP clusters, while five clusters contained dog and human isolates.

Keywords

References

  1. Acke E, McGill K, Quinn J, Jones BR, Fanning S, Whyte P. Antimicrobial resistance profile and mechanisms of resistance in Campylobacter jejuni isolates from pets. Foodborne Pathog Dis 2009, 6, 705-710. https://doi.org/10.1089/fpd.2008.0225
  2. Andersen SR, Saadbye P, Shukri NM, Rosenguist H, Nielsen NL, Boel J. Antimicrobial resistance among Campylobacter jejuni isolated from raw poultry meat at retail level in Denmark. Int J Food Microbial 2006, 107, 250-255. https://doi.org/10.1016/j.ijfoodmicro.2005.04.029
  3. Andzejewska M, Szczepa ska B, Klawe JJ, Spica D, Chudzi ska M. Prevalence of Campylobacter jejuni and Campylobacter coli species in cats and dogs from Bydgoszcz (Poland) region. Pol J Vet sci 2013, 16, 115-120.
  4. Butzler JP. Campylobacter, from obscurity to celebrity. Clin Microbial Infect 2004, 10, 868-876. https://doi.org/10.1111/j.1469-0691.2004.00983.x
  5. CLSI. Method for Antimicrobial Dilution and Disk Susceptibility Testing of Infrequently Isolated or Fastidious Bacteria; Approved Guideline. CLSI document M45-A. Clinical and Laboratory Standard Institute, Wayne, 2006.
  6. Cooper R, Segal H, Lastovica AJ, Elisha BG. Genetic basis of quinolone resistance and epidemiology of resistant and susceptible isolates of porcine Campylobacter coli strains. J Appl Microbiol 2002, 93, 241-249. https://doi.org/10.1046/j.1365-2672.2002.01650.x
  7. Corcoran D, Quinn T, Cotter L, Whyte P, Fanning S. Antimicrobial resistance profiling and fla-typing of Irish thermophillic Campylobacter spp. of human and poultry origin. Lett Appl Microbiol 2006, 43, 560-565. https://doi.org/10.1111/j.1472-765X.2006.01987.x
  8. Dingle KE, Van Den Braak N, Colles FM, Price LJ, Woodward DL, Rodgers FG, Endtz HP, Van Belkum A, Maiden MCJ. Sequence typing confirms that Campylobacter jejuni strains associated with Gullian-Barré and Miller- Fisher syndromes are of diverse genetic lineage, serotype, and flagella type. J Clin Microbial 2001, 39, 3346-3349. https://doi.org/10.1128/JCM.39.9.3346-3349.2001
  9. Drlica K, Zhao X. DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol Mol Biol Rev 1997, 61, 377-392.
  10. Erta HB, Centinkya B, Muz A, Ongor H. Genotyping of broiler-originated Campylobacter jejuni and Campylobacter coli isolates using fla typing and random amplified polymorphic DNA methods. Int J Food Microbiol 2004, 94, 203-209. https://doi.org/10.1016/S0168-1605(03)00312-X
  11. Hakanen A, Jalava J, Kotilainen P, Jousimies-Somer H, Siitonen A, Huovinen P. gyrA polymorphism in Campylobacter jejuni: detection of gyrA mutations in 162 C. jejuni isolates by single-strand conformation polymorphism and DNA sequencing. Antimicrob Agents Chemother 2002, 46, 2644-2647. https://doi.org/10.1128/AAC.46.8.2644-2647.2002
  12. Hald B, Madsen M. Healthy puppies and kittens as carriers of Campylobacter spp., with special reference to Campylobacter upsaliensis. J Clin Microbiol 1997, 35, 3351-3352.
  13. Harrington CS, Moran L, Ridley AM, Newell DG, Madden RH. Inter-laboratory evaluation of three flagellin PCR/RFLP methods for typing Campylobacter jejuni and C. coli: the CAMPYNET experience. J Appl Microbiol 2003, 95, 1321-1333. https://doi.org/10.1046/j.1365-2672.2003.02101.x
  14. Kapperud G, Skjerve E, Bean NH, Ostroff SM, Lassen J. Risk factors for sporadic Campylobacter infections: results of a case-control study in southeastern Norway. J Clin Microbiol 1992, 30, 3117-3121.
  15. Kayman T, Abay S, Hizlisoy H. Identification of Campylobacter spp. isolates with phenotypic methods and multiplex polymerase chain reaction and their antibiotic susceptibilities. Mikrobiyol Bul 2013, 47, 230-239. https://doi.org/10.5578/mb.4532
  16. Lee MK, Billington SJ, Joens LA. Potential virulence and antimicrobial susceptibility of Campylobacter jejuni isolates from food and companion animals. Foodborne Pathog Dis 2004, 1, 223-230. https://doi.org/10.1089/fpd.2004.1.223
  17. Lienau JA, Ellerbroek L, Klein G. Tracing flock-related Campylobacter clones from broiler farms through slaughter to retail products by pulsed-field gel electrophoresis. J Food Prot 2007, 70, 536-542. https://doi.org/10.4315/0362-028X-70.3.536
  18. McGill K, Cowley D, Moran L, Scates P, O'Leary A, Madden RH, Carroll C, McNamara E, Moore JE, Fanning S, Collins JD, Whyte P. Antibiotic resistance of retail food and human Campylobacter isolates on the island of Ireland from 2001-2002. Epidemiol Infect 2006, 134, 1282-1291. https://doi.org/10.1017/S0950268806006200
  19. Nachamkin I, Bohachick K, Patton CM. Flagellin gene typing of Campylobacter jejuni by restriction fragment length polymorphism analysis. J Clin Microbiol 1993, 31, 1531-1536.
  20. Nachamkin I, Engberg J, Aerestrup FM. Diagnosis and antimicrobial susceptibility of Campylobacter species. In: Nachamkin I, Blaser MJ (eds.). Campylobacter spp. 2nd ed. pp. 45-66, ASM press, Washington DC, 2000.
  21. Parkhill J, Wren BW, Mungall K, Ketley JM, Churcher C, Basham D, Chillingworth T, Davies RM, Feltwell T, Holroyd S, Jagels K, Karlyshev AV, Moule S, Pallen MJ, Penn CW, Quail MA, Rajandream MA, Rutherford KM, van Vliet AHM, Whitehead S, Barrell BG. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 2000, 403, 665-668. https://doi.org/10.1038/35001088
  22. Piddock LJV, Ricci V, Pumbwe L, Everett MJ, Griggs DJ. Fluoroquinolone resistance in Campylobacter species from man and animals: detection of mutations in topoisomerase genes. J Antimicrob Chemother 2003, 51, 19-26. https://doi.org/10.1093/jac/dkg033
  23. Quinn JP. Clinical strategies for serious infection: a North American perspective. Diagn Microbiol Infect Dis 1998, 31, 389-395. https://doi.org/10.1016/S0732-8893(98)00023-6
  24. Robinson RA, Pugh RN. Dogs, zoonoses and immunosuppression. J R Soc Promot Health 2002, 122, 95-98. https://doi.org/10.1177/146642400212200210
  25. Ruiz J, Goni P, Marco F, Gallardo F, Mirelis B, Jimenez De Anta T, Vila J. Increased resistance to quinolones in Campylobacter jejuni: a genetic analysis of gyrA gene mutations in quinolone-resistant clinical isolates. Microbiol Immunol 1998, 42, 223-226. https://doi.org/10.1111/j.1348-0421.1998.tb02274.x
  26. Segreti J, Gootz TD, Goodman LJ, Parkhurst GW, Quinn JP, Martin BA, Trenholme GM. High-level quinolone resistance in clinical isolates of Campylobacter jejuni. J Infect Dis 1992, 165, 667-670. https://doi.org/10.1093/infdis/165.4.667
  27. Tauxe RJ. Epidemiology of Capylobacter jejuni infections in the United States and other industrialized nations. In: Nachamkin I, Blaser MJ, Tomkins LS (eds.). Campylobacter Jejuni: Current Status and Future Trends. pp. 9-19, American Society for Microbiology, Washington DC, 1992.
  28. Thakur S, Zhao S, McDermott PF, Harbottle H, Abbott J, English L, Gebreyes WA, White DG. Antimicrobial resistance, virulence, and genotypic profile comparison of Campylobacter jejuni and Campylobacter coli isolated from humans and retail meats. Foodborne Pathog Dis 2010, 7, 835-844. https://doi.org/10.1089/fpd.2009.0487
  29. Tsai HJ, Huang HC, Lin CM, Lien YY, Chou CH. Salmonellae and Campylobacters in household and stray dogs in northern Taiwan. Vet Res Commun 2007, 31, 931-939. https://doi.org/10.1007/s11259-007-0009-4
  30. Van Looveren M, Daube G, De Zutter L, Dumont JM, Lammens C, Wijdooghe M, Vandamme P, Jouret M, Cornelis M, Goossens H. Antimicrobial susceptibilities of Campylobacter strains isolated from food animals in Belgium. J Antimicrob Chemother 2001, 48, 235-240. https://doi.org/10.1093/jac/48.2.235
  31. Wassenaar TM, Newell DG. Genotyping of Campylobacter spp. Appl Environ Microbiol 2000, 66, 1-9. https://doi.org/10.1128/AEM.66.1.1-9.2000
  32. Yong JR, Wu HS, Chiang CS, Mu JJ. Pediatric campylobacteriosis in northern Taiwan from 2003-2005. BMC Infect Dis 2008, 8, 151. https://doi.org/10.1186/1471-2334-8-151
  33. Zirnstein G, Li Y, Swaminathan B, Angulo F. Ciprofloxacin resistance in Campylobacter jejuni isolates: detection of gyrA resistance mutations by mismatch amplification mutation assay PCR and DNA sequence analysis. J Clin Microbiol 1999, 37, 3276-3280.

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