Journal of Food Hygiene and Safety (한국식품위생안전성학회지)

The Korean Society of Food Hygiene and Safety (한국식품위생안전성학회)
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Antimicrobial Resistance and Genetic Characterization of Pathogenic Campylobacter spp. Isolated from Distribution Poultry in Gwangju Metropolitan City

광주지역 유통 가금육에서 분리된 캠필로박터균의 유전적 특성 및 항생제 내성

  • Min Gyou Lee (Health and Environment Research Institute of Gwangju) ;
  • Hye Jin Jeong (Health and Environment Research Institute of Gwangju) ;
  • Se mi Lee (Health and Environment Research Institute of Gwangju) ;
  • Hyang Hee Lee (Health and Environment Research Institute of Gwangju) ;
  • Eun Jin Seo (Health and Environment Research Institute of Gwangju) ;
  • Jung Hee Park (Health and Environment Research Institute of Gwangju) ;
  • Geu Ne Oh (Health and Environment Research Institute of Gwangju) ;
  • Si Eun Seo (Health and Environment Research Institute of Gwangju) ;
  • Jung Mi Seo (Health and Environment Research Institute of Gwangju) ;
  • Ae Gyeong Kim (Health and Environment Research Institute of Gwangju)
  • 이민규 (광주광역시 보건환경연구원) ;
  • 정혜진 (광주광역시 보건환경연구원) ;
  • 이세미 (광주광역시 보건환경연구원) ;
  • 이향희 (광주광역시 보건환경연구원) ;
  • 서은진 (광주광역시 보건환경연구원) ;
  • 박정희 (광주광역시 보건환경연구원) ;
  • 오그네 (광주광역시 보건환경연구원) ;
  • 서시은 (광주광역시 보건환경연구원) ;
  • 서정미 (광주광역시 보건환경연구원) ;
  • 김애경 (광주광역시 보건환경연구원)
  • Received : 2023.12.07
  • Accepted : 2024.02.07
  • Published : 2024.02.28
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Abstract

This study investigated the prevalence of Campylobacter spp. In poultry meat and its association with foodborne illnesses in Gwangju, South Korea. It was found that out of the 307 samples of poultry meat examined, 111 (36.2%) were infected with Campylobacter spp. Among the isolated strains, 102 were identified as Campylobacter jejuni and 14 as Campylobacter coli. The detection rate of Campylobacter spp. was higher in duck meat (63.1%) than in chicken meat (26.0%). In 5 samples (1 chicken, 4 duck), both Campylobacter jejuni and Campylobacter coli were found together. The antimicrobial resistance test showed that 99 strains were resistant to more than one antimicrobial. The most common antimicrobial resistance was seen against ciprofloxacin (84.5%), followed by nalidixic acid (82.8%), tetracycline (44.0%), and gentamicin (2.6%). The isolated Campylobacter spp. were serotyped and the results showed the presence of HS2 (20 strains), HS15 (11 strains), HS19 (9 strains), and HS8 (8 strains). Considering the findings, it is recommended to maintain hygienic practices during the cooking process and to take necessary precautions to prevent the spread of pathogenic bacteria.

본 연구는 광주광역시에 유통·판매되고 있는 가금육을 대상으로 식중독 발생 가능성 높은 캠필로박터균의 검출여부와 분리된 균주의 항생제 내성 및 유전적 특성을 조사하였다. 전체 307건의 가금육(닭 223건, 오리84건) 중 111건에서 캠필로박터균이 검출(36.2%)되었고 116균주(Campylobacter jejuni 102균주, Campylobacter coli 14균주)를 분리하였다. 가금류별 캠필로박터균 검출률은 닭고기 26.0%, 오리고기 63.1% 이었고, 5건(닭 1건, 오리 4건)의 시료에서 Campylobacter jejuni, Campylobacter coli가 동시에 검출되었다. 분리된 균주의 항생제 내성 시험결과 99균주(85.3%)는 1가지 이상의 항생제에 대하여 내성을 보였다. 그 중 ciprofloxacin, nalidixic acid에 내성을 보이는 균주가 각각 98균주(84.5%), 96균주(82.8%)로 가장 많았고, 그 외에 tetracycline (44.0%), gentamicin (2.6%)에 내성을 나타냈다. 분리된 균주의 혈청형 확인 결과, HS2형 20균주, HS15형 11균주, HS19형 9균주, HS8형 8균주 등이 확인 되었고, HS42형, HS6형, HS53형, HS4A형, HS5형, HS18형, HS12형, HS27형 그리고 HS37형이 확인 되었다. 따라서 조리 가공 시 교차오염이 발생하지 않도록 조리기구 등에 대한 위생적 관리와 충분한 가열 조리 등의 식중독 예방을 위한 주의가 필요할 것으로 생각된다.

Keywords

Acknowledgement

본 연구는 광주광역시보건환경연구원 연구사업 및 식품의약품안전처 식중독균추적관리사업의 지원으로 수행하였으며, 이에 감사드립니다.

References

  1. Moran, A.P., Upton, M.E., Factors affecting production of coccoid forms by Campylobacter jejuni on solid media during incubation. J. Appl. Bacteriol., 62, 527-537 (1987). https://doi.org/10.1111/j.1365-2672.1987.tb02685.x
  2. Park, H.K., Sim, C.H., Sim, W.M., Seo, H.C., 2004. Foodmicrobiology, Munundang, Seoul, Korea, pp. 52-61.
  3. Duffy, G., Lynch, O.A., Cagney, C., Tracking emerging zoonotic pathogens from farm to fork. Meat Sci., 78, 34-42 (2008). https://doi.org/10.1016/j.meatsci.2007.05.023
  4. Bryan, F.L., Doyle, M.P., Health risks and consequences of Salmonella and Campylobacter jejuni in raw poultry. J. Food Prot., 58, 326-344 (1995).
  5. Altekruse, S.F., Stern, N.J., Fields, P.I., Swerdlow, D.L., Campylobacter jejuni an emerging foodborne pathogen. Emerg. Infect. Dis., 5, 28-35 (1999). https://doi.org/10.3201/eid0501.990104
  6. Fujimoto, S., Yuki, N., Itoh, T., Amako, K., Specific serotype of Campylobacter jejuni associated with Guillain-Barre syndrome. J. Infect. Dis., 165, 183 (1992).
  7. Kirk, M.D., Pires, S.M., Black, R.E., Caipo, M., Crump, J.A., Devleesschauwer, B., Dopfer, D., Fazil, A., Fischer-Walker, C.L., Hald, T., Hall, A.J., Keddy, K.H., Lake, R.J., Lanata, C.F., Torgerson, P.R., Havelaar, A.H., Angulo, F.J., World Health Organization estimates of the global and regional disease burden of 22 foodborne bacterial, protozoal, and viral diseases, 2010: a data synthesis., PLoS. Med., 12, 1-21 (2015).
  8. Ministry of Food and Drug Safety (MFDS), (2023. October, 16). Food poisoning statistics. retrieved from https://www.foodsafetykorea.go.kr/portal/healthyfoodlife/foodPoisoningStat.do?menu_no=3724&menu_grp=MENU_NEW02&menu_no=3724&menu_grp=MENU_NEW02
  9. Korea Institute for Animal Products Quality Evaluation (KAPE), (2023, October, 17). Annual price of animal products. retrieved from https://www.ekapepia.com/priceComparison/poducerPrice/retail/periodPriceYear.do
  10. Korea Rural Economic Institute (KREI), 2020. Consumer behavior for meat consumption and tasks to respond to its changes, Naju, Korea, pp. 32-33.
  11. Korea Instirute for Health and Social Affairs (KIHASA), 2010. Improving national diet by promoting the nutrition management of institutional foodservice, Seoul, Korea, pp.31-36.
  12. Mullner, P., Spencer, S.E., Wilson, D.J., Jones, G., Noble, A.D., Midwinter, A.C., Collins-Emerson, J.M., Carter, P., Hathaway, S., French, N.P., Assigning the source of human campylobacteriosis in New Zealand: a comparative genetic and epidemiological approach. Infect Genet. Evol., 9, 1311-1319 (2009). https://doi.org/10.1016/j.meegid.2009.09.003
  13. World Health Organization (WHO), 2017. Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics, Geneva, Switzerland, pp. 5.
  14. Ministry of Food and Drug Safety (MFDS), 2022. Detection method for foodborne pathogens investigation (2021), Osong, Korea, pp. 3-11, 94-100.
  15. Ministry of Food and Drug Safety (MFDS), 2022. Korea food code (2020), Osong, Korea, pp. 532-533.
  16. Bang, D.D., Borck, B., Nielsen, E.M., Scheutz, F., Pedersen, K., Madsen, M., Detection of seven virulence and toxin genes of Campylobacter jejuni isolates from Danish turkeys by PCR and cytolethal distending toxin production of the isolates. J. Food Prot., 67, 2171-2177 (2004). https://doi.org/10.4315/0362-028X-67.10.2171
  17. Konkel, M.E., Gray, S.A., Kim, B.J., Garvis, S.G., Yoon, J., Identification of the enteropathogens Campylobacter jejuni and Campylobacter coli based on the cadF virulence gene and its product. J. Clin. Microbiol., 37, 510-517 (1999). https://doi.org/10.1128/JCM.37.3.510-517.1999
  18. Nawaz, M.S., Wang, R.F., Khan, S.A., Khan, A.A., Detection of galE gene by polymerase chain reaction in campylobacters associated with Guillain-Barre syndrome. Mol. Cell Probes., 17, 313-317 (2003).
  19. Wassenaar, T.M., Wagenaar, J.A., Rigter, A., Fearnley, C., Newell, D.G., Duim, B., Homonucleotide stretches in chromosomal DNA of Campylobacter jejuni display high frequency polymorphism as detected by direct PCR analysis. FEMS. Microbiol. Lett., 212, 77-85 (2002). https://doi.org/10.1111/j.1574-6968.2002.tb11248.x
  20. Poly, F., Serichantalergs, O., Kuroiwa, J., Pootong, P., Mason, C., Guerry, P., Parker, C.T., Updated Campylobacter jejuni capsule PCR multiplex typing system and its application to clinical isolates from south and southeast asia. PLoS. One., 10, 1-17 (2015).
  21. Klena, J.D., Parker, C.T., Knibb, K., Ibbitt, J.C., Devane, P.M., Horn, S.T., Miller, W.G., Konkel, M.E., Differentiation of Campylobacter coli, Campylobacter jejuni, Campylobacter lari, and Campylobacter upsaliensis by a multiplex PCR developed from the nucleotide sequence of the lipid A gene lpxA. J. Clin. Microbiol., 42, 5549-5557 (2004). https://doi.org/10.1128/JCM.42.12.5549-5557.2004
  22. Park, J.H., Kim, Y.J., Kim, J.H., Song, S.W., Heo, E.J., Kim, H.J., Ku, B.K., Lee, S.W., Lee, J.Y., Moon, J.S., Wee, S.H., Prevalence of Campylobacter jejuni and Campylobacter coli isolated from domestic and imported meats in Korea, 2005-2009. J. Prev. Vet. Med., 34, 181-187 (2010).
  23. Wei, B., Cha, S.Y., Yoon, R.H., Kang, M., Roh, J.H., Seo, H.S., Lee, J.A., Jang, H.K., Prevalence and antimicrobial resistance of Campylobacter spp. isolated from retail chicken and duck meat in South Korea. Food Control, 62, 63-68 (2016). https://doi.org/10.1016/j.foodcont.2015.10.013
  24. Kim, J.S., Park, H.E., Kim, J.H., Kim, J.H., Jung, J.I., Cho, S.B., Ryu, S.R., Jeon, B.H., Comparative analysis of aerotolerance, antibiotic resistance, and virulence gene prevalence in Campylobacter jejuni isolates from retail raw chicken and duck meat in South Korea. Microorganisms, 7, 1-13 (2019). https://doi.org/10.3390/microorganisms7100433
  25. Chon, J.W., Lee, S.K., Yoon, Y., Yoon, K.S., Kwak, H.S., Joo, I.S., Seo, K.H., Quantitative prevalence and characterization of Campylobacter from chicken and duck carcasses from poultry slaughterhouses in South Korea. Poult. Sci., 97, 2909-2916 (2018). https://doi.org/10.3382/ps/pey120
  26. Lee, A., Smith, S.C., Coloe, P.J., Survival and growth of Campylobacter jejuni after artificial inoculation onto chicken skin as a function of temperature and packaging conditions. J. Food Prot., 61, 1609-1614 (1998). https://doi.org/10.4315/0362-028X-61.12.1609
  27. Wei, B., Characteristics of Campylobacter species isolated from domestic ducks in korea. PhD thesis, Chonbuk National University, Jeonju, Korea (2014).
  28. Kim, S.H., Park, S.H., Park, Y.S., Kim, C.M., Campylobacter infection and its prevention. Food Sci. Ind., 31, 56-67 (1998).
  29. Pearson, A.D., Greenwood, M., Healing, T.D., Rollins, D., Shahamat, M., Donaldson, J., Colwell, R.R., Colonization of broiler chickens by waterborne Campylobacter jejuni. Appl. Environ. Microbiol., 59, 987-996 (1993). https://doi.org/10.1128/aem.59.4.987-996.1993
  30. Wempe, J.M., Genigeorgis, C.A., Farver, T.B., Yusufu, H.I., Prevalence of Campylobacter jejuni in two California chicken processing plants. Appl. Environ. Microbiol., 45, 355-359 (1983). https://doi.org/10.1128/aem.45.2.355-359.1983
  31. Genigeorgis, C., Hassuneh, M., Collins, P., Campylobacter jejuni infection on poultry farms and its effect on poultry meat contamination during slaughtering. J. Food Prot., 49, 895-903 (1986). https://doi.org/10.4315/0362-028X-49.11.895
  32. Jones, F.T., Axtell, R.C., Rives, D.V., Scheideler, S.E., Tarver, F.R.Jr., Walker, R.L., Wineland, M.J., A survey of Campylobacter jejuni contamination in modern broiler production and processing systems. J. Food Prot., 54, 259-262 (1991). https://doi.org/10.4315/0362-028X-54.4.259
  33. Konkel, M.E., Garvis, S.G., Tipton, S.L., Anderson, D.E.Jr., Cieplak, W.Jr., Identification and molecular cloning of a gene encoding a fibronectin-binding protein (CadF) from Campylobacter jejuni. Mol. Microbiol., 24, 953-963 (1997). https://doi.org/10.1046/j.1365-2958.1997.4031771.x
  34. Wassenaar, T.M., Bleumink-Pluym, N.M., van der Zeijst, B.A., Inactivation of Campylobacter jejuni flagellin genes by homologous recombination demonstrates that flaA but not flaB is required for invasion. EMBO. J., 10, 2055-2061 (1991). https://doi.org/10.1002/j.1460-2075.1991.tb07736.x
  35. Linton, D., Gilbert, M., Hitchen, P.G., Dell, A., Morris, H.R., Wakarchuk, W.W., Gregson, N.A., Wren, B.W., Phase variation of a beta-1,3 galactosyltransferase involved in generation of the ganglioside GM1-like lipo-oligosaccharide of Campylobacter jejuni. Mol. Microbiol., 37, 501-514 (2000). https://doi.org/10.1046/j.1365-2958.2000.02020.x
  36. Ministry of Food and Drug Safety (MFDS), 2020. Korean culture collection for foodborne pathogens newsletter, Osong, Korea, pp. 4-7.
  37. Sierra-Arguello, Y.M., Perdoncini, G., Rodrigues, L.B., Ruschel Dos Santos, L., Apellanis Borges, K., Quedi Furian, T., Pippi Salle, C.T., de Souza Moraes, H.L., Pereira Gomes, M.J., Pinheiro do Nascimento, V., Identification of pathogenic genes in Campylobacter jejuni isolated from broiler carcasses and broiler slaughterhouses. Sci. Rep. 11, 4588 (2021).
  38. Ministry of Agriculture, Food and Rural Affairs (MAFRA), 2022. National antibiotic use and resistance monitoring, Sejong, Korea. pp. 13-17, 129.
  39. Animal and Plant Quarantine Agency (APQA), 2020. Poultry antibiotic prescribing guidelines, Kimcheon, Korea, pp. 31.
  40. Asai, T., Kojima, A., Harada, K., Ishihara, K., Takahashi, T., Tamura, Y., Correlation between the usage volume of veterinary therapeutic antimicrobials and resistance in Escherichia coli isolated from the feces of food-producing animals in Japan. Jpn. J. Infect. Dis., 58, 369-372 (2005). https://doi.org/10.7883/yoken.JJID.2005.369
  41. Animal and Plant Quarantine Agency (APQA), 2017. The evaluation of human health impact of fluoroquinolone resistant bacteria attributed to the consumption of chicken through the antimicrobial resistance risk analysis, Kimcheon, Korea, pp. 3-12.
  42. Kim, S.M., Chong, S.J., Prevalence and in vitro antimicrobial activity against Campylobacter jejuni / coli from chickens. Korean J. Clin. Lab. Sci., 28, 20-28 (1996).
  43. Yang, J.W., Kim, S.H., Lee, W.W., Kim, Y.H., Prevalence of virulence-associated genes and antimicrobial resistance of Campylobacter jejuni from ducks in Gyeongnam province, Korea. Korean J. Vet. Serv., 37, 85-96 (2014). https://doi.org/10.7853/kjvs.2014.37.2.85
  44. Noormohamed, A., Fakhr, M.K., Prevalence and antimicrobial susceptibility of Campylobacter spp. in Oklahoma conventional and organic retail poultry. Open Microbiol. J., 8, 130-137 (2014). https://doi.org/10.2174/1874285801408010130
  45. Sproston, E.L., Wimalarathna, H,M,L., Sheppard, S.K., Trends in fluoroquinolone resistance in Campylobacter. Microb. Genom., 4, 1-8 (2018).
  46. Skjot-Rasmussen, L., Ethelberg, S., Emborg, H.D., Agerso, Y., Larsen, L.S., Nordentoft, S., Olsen, S.S., Ejlertsen, T., Holt, H., Nielsen, E.M., Hammerum, A.M., Trends in occurrence of antimicrobial resistance in Campylobacter jejuni isolates from broiler chickens, broiler chicken meat, and human domestically acquired cases and travel associated cases in Denmark. Int. J. Food Microbiol., 131, 277-279 (2009). https://doi.org/10.1016/j.ijfoodmicro.2009.03.006
  47. Engberg, J., Aarestrup, F.M., Taylor, D.E., Gerner-Smidt, P., Nachamkin, I., Quinolone and macrolide resistance in Campylobacter jejuni and C. coli: resistance mechanisms and trends in human isolates. Emerg. Infect. Dis., 7, 24-34 (2001). https://doi.org/10.3201/eid0701.010104
  48. Nachamkin, I., Ung, H., Li, M., Increasing fluoroquinolone resistance in Campylobacter jejuni, Pennsylvania, USA, 1982-2001. Emerg. Infect. Dis., 8, 1501-1503 (2002). https://doi.org/10.3201/eid0812.020115
  49. Zeitouni, S., Guyard-Nicodeme, M., Kempf, I., Comparison of adhesion, invasion, motility, and toxin production of Campylobacter strains and their resistant mutants. Microb. Drug Resist., 19, 130-137 (2013).
  50. Nielsen, E.M., Engberg, J., Madsen, M., Distribution of serotypes of Campylobacter jejuni and C. coli from Danish patients, poultry, cattle and swine. FEMS. Immunol. Med. Microbiol., 19, 47-56 (1997). https://doi.org/10.1111/j.1574-695X.1997.tb01071.x
  51. Kim, W.H., Choi, O.K., Jeong, J.A., Park, S.H., Lee, Y.E., Park, G.H., Yoon, M.H., Genetic analysis of Campylobacter jejuni isolates from diarrhea patients in Gyeonggi-do. Korean J. Microbiol., 54, 31-37 (2018).
  52. Pike, B.L., Guerry, P., Poly, F., Global distribution of Campylobacter jejuni penner serotypes: a systematic review. PLoS. One, 8, 1-8 (2013).
  53. Takahashi, M., Koga, M., Yokoyama, K., Yuki, N., Epidemiology of Campylobacter jejuni isolated from patients with Guillain-Barre and Fisher syndromes in Japan. J. Clin. Microbiol., 43, 335-339 (2005). https://doi.org/10.1128/JCM.43.1.335-339.2005
  54. Jung, S.M., Kim, N.O., Na, H.Y., Hong, S.H., Chung G.T., Prevalence of Campylobacter causing acute diarrhea in Korea, 2012-2015. Public Health Wkly. Rep., 9, 526-530 (2016).