Korean Journal of Food Science and Technology (한국식품과학회지)

Korean Society of Food Science and Technology (한국식품과학회)
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Occurrence and antibiotic resistance of Enterococcus spp. from retail fresh-cut products in Korea

국내 신선 편이식품으로부터 분리한 Enterococcus의 항생제 저항성

  • Kim, Hyun Jung (Research Group of Consumer Safety, Korea Food Research Institute) ;
  • Kim, Seung Min (Department of Human Ecology, Korea National Open University)
  • 김현정 (한국식품연구원 소비안전연구단) ;
  • 김승민 (한국방송통신대학교 생활과학과)
  • Received : 2018.10.16
  • Accepted : 2018.11.26
  • Published : 2018.12.31
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Abstract

Enterococcus spp. have been considered major indicator organisms for antibiotic resistance due to their ability to easily acquire and to harbor antibiotic resistance. In this study, Enterococcus spp. were isolated from 174 retail fresh-cut products (fresh vegetable salads, microgreens, and sprouts) in Korea. Among the 20 Enterococcus isolates obtained, 18 (90.0%) were Enterococcus faecalis and 2 (10.0%) were Enterococcus faecium. The patterns of antibiotic resistance against nine antimicrobials were analyzed. Most of the isolates (85.0%) were resistant to quinupristin/dalfopristin, 40.0% and 50.0% of the isolates showed intermediate resistance to two critically important antimicrobials for human medicine, ciprofloxacin and erythromycin, respectively. Vancomycin-resistant enterococci were not detected in this study. Given the importance of antimicrobial resistance of enterococci in food safety as well as in public health, our results regarding the occurrence (level of contamination) and antimicrobial resistance of Enterococcus spp. could provide useful information that aids the risk analysis of antibiotic resistance.

본 연구에서는 서울과 경기도 지역 소매점 및 대형마트에서 판매되고 있는 샐러드, 어린잎, 새싹채소로부터 Enterococcus의 존재를 파악하고 9개 항생제에 대한 항생제 저항성 프로파일을 확보했다. Quinupristin/dalfopristin에 저항성을 가지는 분리주가 85.0%에 이르렀고, 특히 E. faecalis 분리주는 18종 중 17종이 저항성을 나타냈다. 또한 critically important 항생제 중 highest priority로 분류되는 ciprofloxacin과 erythromycin에 대해 각각 40.0, 50.0%가 중간 정도의 저항성을 보였으며, vancomycin에 대한 저항성을 가지는 분리주는 검출되지 않았다. Enterococci의 항생제 저항성 정도는 식품 안전뿐만 아니라 공중 보건에 있어서도 중요하다는 측면에서 본 연구의 Enterococcus 오염 정도, 항생제 내성율에 대한 결과는 향후 신선 편이식품 섭취가 인체 건강에 미치는 위험분석을 위한 기초자료로서 유용한 정보를 제공할 것으로 보이며 앞으로 특별한 열처리 없이 섭취하는 신선 편이식품에 대한 지속적인 모니터링이 필요할 것이라 사료된다.

Keywords

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Fig. 1. Comparison of antimicrobial resistance patterns of E. faecalis and E. faecium isolated from fresh-cut products (Veg) and pork meat products (Pork).

Table 1. Oligonucleotides used in this study

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Table 2. Occurrence of Enterococcus spp. in fresh-cut products

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Table 3. Classifications of antimicrobials used for susceptibility testing

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Table 4. Antibiotic resistance profiles of Enterococcus faecalis and Enterococcus faecium against 9 antibiotics

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Table 5. Drug resistance patterns of Enterococcus spp. isolated form fresh-cut products

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References

  1. Agudelo Higuita NI, Huycke MM. Enterococcal disease, epidemiology, and implications for treatment. pp. 1-27. In: Enterococci: From Commensals to Leading Causes of Drug Resistant Infection. Massachusetts Eye and Ear Infirmary. Boston, MA, USA (2014)
  2. Baselice A, Colantuoni F, Lass DA, Nardone G, Stasi A. Trends in EU consumers' attitude towards fresh-cut fruit and vegetables. Food Qual. Prefer. 59: 87-96 (2017) https://doi.org/10.1016/j.foodqual.2017.01.008
  3. Clewell DB, Flannagan SE, Jaworski DD. Unconstrained bacterial promiscuity: the Tn916-Tn1545 family of conjugative transposons. Trends. Microbiol. 3: 229-236 (1995) https://doi.org/10.1016/S0966-842X(00)88930-1
  4. CLSI (Clinical and Laboratory Standards Institute). Performance standards for antimicrobial susceptibility testing; Twentieth informational supplement. CLSI document M100-S20. Wayne, PA, USA (2010)
  5. Courvalin P. Transfer of antibiotic resistance genes between grampositive and gram-negative bacteria. Antimicrob. Agents Chemother. 38: 1447-1451 (1994) https://doi.org/10.1128/AAC.38.7.1447
  6. de Fatima Silva Lopes M, Ribeiro T, Abrantes M, Figueiredo Marques JJ, Tenreiro R, Crespo MT. Antimicrobial resistance profiles of dairy and clinical isolates and type strains of enterococci. Int. J. Food Microbiol. 103: 191-198 (2005) https://doi.org/10.1016/j.ijfoodmicro.2004.12.025
  7. Dutka-Malen SD, Evers S, courvalin P. Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J. Clin. Microbiol. 33: 24-27 (1995)
  8. Fantin B, Leclercq R, Garry L, Carbon C. Influence of inducible cross-resistance to macrolides, lincosamides, and streptogramin Btype antibiotics in Enterococcus faecium on activity of quinupristin-dalfopristin in vitro and in rabbits with experimental endocarditis. Antimicrob. Agents Chemother. 5: 931-935 (1997)
  9. Franz CMAP, Holzapfel WH, Stiles ME. Enterococci at the crossroads of food safety? Int. J. Food Microbiol. 47: 1-24 (1999) https://doi.org/10.1016/S0168-1605(99)00007-0
  10. Giraffa G. Enterococci from foods. FEMS Microbiol. Rev. 744: 1-9 (2002)
  11. Ham H. Distributions of Bacillus cereus, Pseudomonas, Enterococcus, and coliforms isolated from agricultural products. J. Bacteriol. Virol. 47: 139-147 (2017) https://doi.org/10.4167/jbv.2017.47.3.139
  12. Hanchi H, Mottawea W, Sebei K, Hammami R. The genus Enterococcus: Between probiotic potential and safety concerns-an update. Front. Microbiol. 9: 1791 (2018) https://doi.org/10.3389/fmicb.2018.01791
  13. ISO (International Organization for Standardization). 7899-1: Water quality-Detection and enumeration of intestinal enterococci in surface and waste water. Part I: Miniaturized method (Most Probable Number) by inoculation in liquid medium. Switzerland (1998)
  14. Johnston LM, Jaykus LA. Antimicrobial resistance of Enterococcus species isolated from produce. Appl. Environ. Microbiol. 70: 3133-3137 (2004) https://doi.org/10.1128/AEM.70.5.3133-3137.2004
  15. Kang HM, Kim IS. Comparison of storability of some sprout vegetables in MA storage. J. Bio-Environ. Control. 16: 415-419 (2007)
  16. Kariyama R, Mitsuhata R, Chow JW, Clewell DB, Kumon H. Simple and reliable multiplex PCR assay for surveillance isolates of vancomycin-resistant enterococci. J. Clin. Microbiol. 38: 3092-3095 (2000)
  17. Kim GH. Development of minimal processing technology for Korean fruit and vegetables. Korean J. Soc. Food Sci. 16: 577-583 (2000)
  18. Kim AR, Cho YM, Her M, Jung BY, Lim SK, Jung SC, Song CS, Lee JY. Quinupristin/dalfopristin resistance patterns in Enterococcus faecium isolated from chicken farms in South Korea. Kor. J. Vet. Publ. Hlth. 35: 91-96 (2011)
  19. Klein G. Taxonomy, ecology and antibiotic resistance of enterococci from food and the gastro-intestinal tract. Int. J. Food Microbiol. 88: 123-131 (2003) https://doi.org/10.1016/S0168-1605(03)00175-2
  20. Koo M, Cho AR, Jeong AR, Kim HJ, Park YH, Kwak HS, Hwang IG. Antibiotic susceptibility and molecular typing of Enterococcus faecalis from retail pork meat products in Korea. J. Kor. Soc. Appl. Biol. Chem. 56: 295-299 (2013) https://doi.org/10.1007/s13765-012-3212-0
  21. Lim SK, Lee JE, Lee HS, Nam HM, Moon DC, Jang GC, Park YJ, Jung YG, Jung SC, Wee SH. Trends in antimicrobial sales for livestock and fisheries in Korea during 2003-2012. Kor. J. Vet. Res. 54: 81-86 (2014) https://doi.org/10.14405/kjvr.2014.54.2.81
  22. Ma L, Zhang M, Bhandari B, Gao Z. Recent developments in novel shelf life extension technologies of fresh-cut fruits and vegetables. Trends. Food Sci. Tech. 64: 23-38 (2017) https://doi.org/10.1016/j.tifs.2017.03.005
  23. MAFRA (Ministry of Agriculture, Food and Rural Affairs), APQA (Animal and Plant Quarantine Agency), MFDS (Ministry of Food and Drug Safety). Monitoring and characterization of antimicrobial resistance of bacteria from livestock products in 2017. Available from: http://ebook.qia.go.kr/home/view.php?host=main&site=20180704_110723. Accessed Nov. 19, 2018.
  24. Mundy LM, Sahm DF, Gilmore M. Relationships between enterococcal virulence and antimicrobial resistance. Clin. Microbiol. Rev. 13: 513-522 (2000) https://doi.org/10.1128/CMR.13.4.513
  25. Noble WC, Virani Z, Cree RG. Co-transfer of vancomycin and other resistance genes from Enterococcus faecalis NCTC 12201 to Staphylococcus aureus. FEMS. Microbiol. Lett. 93: 195-198 (1992) https://doi.org/10.1111/j.1574-6968.1992.tb05089.x
  26. Nwosu VC. Antibiotic resistance with particular reference to soil microorganisms. Res. Microbiol. 152: 421-430 (2001) https://doi.org/10.1016/S0923-2508(01)01215-3
  27. Pesavento G, Calonico C, Ducci B, Magnanini A, Lo Nostro A. Prevalence and antibiotic resistance of Enterococcus spp. isolated from retail cheese, ready-to-eat salads, ham, and raw meat. Food Microbiol. 41: 1-7 (2014) https://doi.org/10.1016/j.fm.2014.01.008
  28. Pesavento G, Ducci B, Nieri D, Comodo N, Lo Nostro A. Prevalence and antibiotic susceptibility of Listeria spp. isolated from raw meat and retail foods. Food Control 21: 708-713 (2010) https://doi.org/10.1016/j.foodcont.2009.10.012
  29. Quednau M, Ahrne S, Petersson AC, Molin G. Antibiotic-resistant strains of Enterococcus isolated from Swedish and Danish retailed chicken and pork. J. Appl. Microbiol. 84: 1163-1170 (1998) https://doi.org/10.1046/j.1365-2672.1998.00463.x
  30. Schaberg DR, Dillon WI, Terpenning MS. Robinson KA, Bradley SF, Kauffman CA. Increasing resistance of enterococci to ciprofloxacin. Antimicrob. Agents Chemother. 36: 2533-2535 (1992) https://doi.org/10.1128/AAC.36.11.2533
  31. Sengelov G, Yvonne A, Halling-Sorenson B, Baloda S, Andersen JS, Jensen LB. Bacterial antibiotic resistance levels in Danish farmland as a result of treatment with pig manure slurry. Environ. Int. 953: 1-9 (2002)
  32. Seo KS, Kim JY, Yoo HS, Bae WK, and Park YH. Comparison of vancomycin-resistant enterococci isolates from human, poultry and pigs in Korea. Vet. Microbiol. 106: 225-233 (2005) https://doi.org/10.1016/j.vetmic.2004.11.017
  33. Singh KV, Weinstock GM, Murray BE. An Enterococcus faecalis ABC homologue (Lsa) is required for the resistance of this species to clindamycin and quinupristin-dalfopristin. Antimicrob. Agents Chemother. 6: 1845-1850 (2002)
  34. Sparo M, Urbizu L, Solana MV, Pourcel G, Delpech G, Confalonieri A, Ceci M, Sanchez Bruni SF. High-level resistance to gentamicin: genetic transfer between Enterococcus faecalis isolated from food of animal origin and human microbiota. Lett. Appl. Microbiol. 54: 119-125 (2011)
  35. Weiss A, Domig KJ, Kneifel W. Comparison of selective media for the enumeration of probiotic enterococci from animal feed. Food Technol. Biotechnol. 43: 147-155 (2005)
  36. Weiss A, Konrad JD, Kneifel W, Mayer HK. Evaluation of PCRbased typing methods for the identification of probiotic Enterococcus faecium strains from animal feeds. Animal Feed Sci. Technol. 158: 187-196 (2010) https://doi.org/10.1016/j.anifeedsci.2010.04.004
  37. WHO AGISAR (World Health Organnization Advisory Group on Integrated Surveillance of Antimicrobial Resistance). Critically Important Antimicrobials for Human Medicine-5th Revision 2017. Geneva, Switzerland (2017)
  38. Woodford N, Levermore DM. Infections caused by Gram-positive bacteria: a review of the global challenge. J. Infect. 59: S4-16 (2009) https://doi.org/10.1016/S0163-4453(09)60003-7