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Prevalence of Clostridium difficile isolated from various raw meats in Korea

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Abstract

Clostridium difficile is an anaerobic, toxin-producing pathogen that causes human infection possibly through the consumption of meat. Clostridium difficile was isolated from 45 of 415 (10.8%) various raw meat samples collected in nationwide markets in Korea between 2013 and 2014. Among the 45 isolated strains, the highest prevalence rate was found in September (28.6%) and detected in chicken (16.4%), pork (8.3%) and beef (6.8%). According to an antibiotic resistance test, resistance was found only for clindamycin (2.2%). The genetic similarity of ribotypes O78 and O27 and strains isolated from raw meats was determined using DiversiLab. Among the isolates studied, four different rep-PCR types were identified, genetically distinct from ribotypes O78 and O27. An ELISA reaction confirmed that the two strains have toxin A and toxin B and showed 89% genetic similarity. This study suggests that food animals could be potential routes of foodborne transmission in C. difficile-associated human infection.

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References

  1. Lyon SA. Clostridium difficile in healthy food animals and development of a PCR assay for detection in enriched food and fecal samples. PhD thesis, University of Georgia, Athens (2009)

  2. Houser BA, Soehnlen MK, Wolfgang DR, Lysczek HR, Burns CM., Jayarao BM. Prevalence of Clostridium difficile toxin genes in the feces of veal calves and incidence of ground veal contamination. Foodborne Pathog. Dis. 9: 32–36 (2012)

    Article  CAS  PubMed  Google Scholar 

  3. Rodriguez-Palacios A, Stämpfli HR, Duffield T, Peregrine AS, Trotz-Williams LA, Arroyo LG, Brazier JS, Weese JS. Clostridium difficile PCR ribotypes in calves, Canada. Emerg retail ground meat, Canada. Emerg. Infect Dis. 13: 485–487 (2006)

    Article  Google Scholar 

  4. De Boer E, Zwartkruis-Nahuis A, Heuvelink AE, Harmanus C, Kuijper EJ. Prevalence of Clostridium difficile in retailed meat in the Netherlands. Int. J. Food Microbiol. 144: 561–564 (2011)

    Article  PubMed  Google Scholar 

  5. Harvey RB, Norman KN, Andrews K, Hume ME, Scanlan CM, Callaway TR, Anderson RC, Nisbet, DJ. Clostridium difficile in poultry and poultry meat. Foodborne Pathog. Dis. 8: 1321–1323 (2011)

    Article  CAS  PubMed  Google Scholar 

  6. Hoffer E, Haechler H, Frei R, Stephan R. Low occurrence of Clostridium difficile in fecal samples of healthy calves and pigs at slaughter and in minced meat in Switzerland. J. Food Protect. 73: 973–975 (2010)

    Article  CAS  Google Scholar 

  7. McDonald LC, Killgore GE, Thompson A, Owens Jr RC, Kazakova SV, Sambol SP, Johnson S, Gerding DN. An epidemic, toxin gene–variant strain of Clostridium difficile. New Engl. J. Med. 353: 2433–2441 (2005)

    Article  CAS  PubMed  Google Scholar 

  8. Kuijper E, Coignard B, Tüll P. Emergence of Clostridium difficile‐associated disease in North America and Europe. Clin. Microbiol. Infec. 12: 2–18 (2006)

    Article  CAS  Google Scholar 

  9. Loo VG, Poirier L, Miller MA, Oughton M, Libman MD, Michaud S, Bourgault AM., Nguyen T, Frenette C, Kelly M. A predominantly clonal multi-institutional outbreak of Clostridium difficile–associated diarrhea with high morbidity and mortality. New Engl. J. Med. 353: 2442–2449 (2005)

    Article  CAS  PubMed  Google Scholar 

  10. Thomas C, Stevenson M, Riley TV. Antibiotics and hospital-acquired Clostridium difficile-associated diarrhoea: a systematic review. J. Antimicrob. Chemoth. 51: 1339–1350 (2003)

    Article  Google Scholar 

  11. Yan Q, Zhang J, Chen C, Zhou H., Du P, Cui Z, Cen R, Liu L, Li W, Cao B. Multilocus sequence typing (MLST) analysis of 104 Clostridium difficile strains isolated from China. Epidemiol. Infect. 141: 195–199 (2013)

    Article  CAS  PubMed  Google Scholar 

  12. Kim H, Lee Y, Moon HW, Lim CS, Lee K, Chong Y. Emergence of Clostridium difficile ribotype 027 in Korea. Kor. J. Lab. Med. 31: 191–196 (2011)

    Article  CAS  Google Scholar 

  13. Huang H, Weintraub A, Fang H, Wu S, Zhang Y, Nord CE. Antimicrobial susceptibility and heteroresistance in Chinese Clostridium difficile strains. Anaerobe. 16: 633–635 (2010)

    Article  CAS  PubMed  Google Scholar 

  14. George W, Rolfe R, Finegold S. Clostridium difficile and its cytotoxin in feces of patients with antimicrobial agent-associated diarrhea and miscellaneous conditions. J. Clin. Microbiol. 15: 1049–1053 (1982)

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Pépin J, Valiquette L, Alary ME, Villemure P, Pelletier A., Forget K, Pépin K, Chouinard D. Clostridium difficile-associated diarrhea in a region of Quebec from 1991 to 2003: a changing pattern of disease severity. Can. Med. Assoc. J. 171: 466–472 (2004)

    Article  Google Scholar 

  16. Walk ST, Micic D, Jain R, Lo ES, Trivedi I, Liu EW. Almassalha LM, Ewing SA, Ring C, Galecki AT. Clostridium difficile ribotype does not predict severe infection. Clin. Infect. Dis. 55: 1661–1668 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Faris B, Blackmore A, Haboubi N. Review of medical and surgical management of Clostridium difficile infection. Tech. Coloproctol. 14: 97–105 (2010)

    Article  CAS  PubMed  Google Scholar 

  18. Debast SB, Van Leengoed LA, Goorhuis A, Harmanus C, Kuijper EJ, Bergwerff AA. Clostridium difficile PCR ribotype 078 toxinotype V found in diarrhoeal pigs identical to isolates from affected humans. Environ. Microbial. 11: 505–511 (2009)

    Article  CAS  Google Scholar 

  19. Hensgens MP, Keessen EC, Squire MM, Riley TV, Koene MG, de Boer E, Lipman LJ, Kuijper EJ. Clostridium difficile infection in the community: a zoonotic disease? Clin. Microbiol. Infec. 18: 635–645 (2012)

    Article  CAS  Google Scholar 

  20. Lee YJ, Choi MG, Lim CH, Jung WR, Cho HS, Sung HY, Nam KW, Chang JH, Cho YK, Park JM. Change of Clostridium difficile Colitis during Recent 10 Years in Korea. Korean J. Gastroenterology. 55: 169–174 (2010)

    Article  Google Scholar 

  21. Lee JH, Lee SY, Kim YS, Park SW, Park SW, Jo SY, Ryu SH, Lee JH, Moon JS, Whang DH. The incidence and clinical features of Clostridium difficile infection; single center study. Korean J. Gastroenterology. 55: 175–182 (2010)

    Article  Google Scholar 

  22. Chung HT, Jung SA, Song HJ, Kim SE. First Case of Antibiotic-associated Colitis by Clostridium difficile PCR Ribotype 027 in Korea. J. Korean Med. Sci. 24: 520–524 (2009)

    Article  CAS  Google Scholar 

  23. Rodriguez-Palacios A, Staempfli HR, Duffield T, Weese JS. Clostridium difficile in retail ground meat, Canada. Emerg. Infect. Dis. 13: 485-487 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Hecht DW, Citron DM, Cox M. Methods for antimicrobial susceptibility testing of anaerobic bacteria; approved standard. Clin. Lab. Stand. Inst. 27: NO. 2 (2007)

  25. Songer JG, Trinh HT, Killgore GE, Thompson AD, McDonald LC, Limbago BM. Clostridium difficile in retail meat products, USA, 2007. Emerg. Infect. Dis. 15: No. 5 (2009)

  26. Weese J, Reid-Smith R, Avery B, Rousseau J. Detection and characterization of Clostridium difficile in retail chicken. Lett. Appl. Microbiol. 50: 362–365 (2010)

    Article  CAS  PubMed  Google Scholar 

  27. Martirani Von Abercron SM, Karlsson F, Trowald Wigh G, Wierup M., Krovacek K. Low occurrence of Clostridium difficile in retail ground meat in Sweden. J. Food Protect. 72: 1732–1734 (2009)

    Article  Google Scholar 

  28. Eckert C, Burghoffer B, Barbut F. Contamination of ready-to-eat raw vegetables with Clostridium difficile in France. J. Medi. Microbiol. 62: 1435–1438 (2013)

    Article  CAS  Google Scholar 

  29. Jöbstl M, Heuberger S, Indra A, Nepf R, Köfer J, Wagner M. Clostridium difficile in raw products of animal origin. Int. J. Food Microbiol. 138: 172–175 (2010)

    Article  CAS  PubMed  Google Scholar 

  30. Gould LH, Limbago B. Clostridium difficile in food and domestic animals: a new foodborne pathogen? Clin. Infect. Dis. 51: 577–582 (2010)

    Article  PubMed  Google Scholar 

  31. Ed J. Kuijper MD, Jaap T. van Dissel MD. Spectrum of Clostridium difficile infections outside health care facilities. Can. Medi. Assoc. 179: 747–748 (2008)

  32. Simango, C. and S. Mwakurudza. Clostridium difficile in broiler chickens sold at market places in Zimbabwe and their antimicrobial susceptibility. Int. J. Food Microbiol. 124:268–270 (2008)

    Article  CAS  PubMed  Google Scholar 

  33. Simango, C. Prevalence of Clostridium difficile in the environment in a rural community in Zimbabwe. T. Roy. Soc. Trop. Med. H. 100:1146–1150 (2006)

    Article  Google Scholar 

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Acknowledgements

This research was supported by Main Research Program (E0156500-03) of the Korea Food Research Institute (KFRI) funded by the Ministry of Science, ICT.

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Authors and Affiliations

  1. Food Analysis Center, Korea Food Research Institute, 245, Nongsaengmyeong-ro, Iseo-myeon, Wanju-gun, Jeollabuk-do, 55365, Republic of Korea

    Joo Young Lee, Da Yeon Lee & Yong Sun Cho

  2. Department of Food Science and Biotechnology, Sungkyunkwan University, Jangan-gu, Suwon, South Korea

    Joo Young Lee

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  1. Joo Young Lee
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Correspondence to Yong Sun Cho.

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Lee, J.Y., Lee, D.Y. & Cho, Y.S. Prevalence of Clostridium difficile isolated from various raw meats in Korea. Food Sci Biotechnol 27, 883–889 (2018). https://doi.org/10.1007/s10068-018-0318-0

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  • DOI: https://doi.org/10.1007/s10068-018-0318-0

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