Korean Journal of Food Science and Technology (한국식품과학회지)

Korean Society of Food Science and Technology (한국식품과학회)
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Risk assessment of Staphylococcus aureus infection in ready-to-eat Samgak-Kimbap

즉석섭취 삼각김밥에서의 Staphylococcus aureus 위해평가 연구

  • Lee, Chae Lim (Department of Food and Nutrition, Kyung Hee University) ;
  • Kim, Yeon Ho (Department of Food and Nutrition, Kyung Hee University) ;
  • Ha, Sang-Do (School of Food Science and Technology, Chung-Ang University) ;
  • Yoon, Yo Han (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Yoon, Ki Sun (Department of Food and Nutrition, Kyung Hee University)
  • 이채림 (경희대학교 식품영양학과) ;
  • 김연호 (경희대학교 식품영양학과) ;
  • 하상도 (중앙대학교 식품공학부) ;
  • 윤요한 (숙명여자대학교 식품영양학과) ;
  • 윤기선 (경희대학교 식품영양학과)
  • Received : 2020.08.20
  • Accepted : 2020.10.30
  • Published : 2020.12.31
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Abstract

Samgak-Kimbap is a popular ready-to-eat (RTE) food at convenience stores, in Korea. Although Samgak-Kimbap is distributed through the cold chain supply system, inappropriate temperature storage conditions prior to consumption are a cause of concern. The objective of this study was to evaluate the risk of Staphylococcus aureus growth in Samgak-Kimbap in the retail market. The prevalence and contamination levels of S. aureus in Samgak-Kimbap (n=170) were monitored, and the predictive growth model of a five-strain cocktail of enterotoxin-producing S. aureus (SEA, SEB, SEC, SED, and SEE) was developed in Samgak-Kimbap as a function of temperature (4, 10, 11, 20, 25, and 37℃). We could not observe the growth of S. aureus and enterotoxin-producing S. aureus in Samgak-Kimbap at temperatures below 10℃. The probability of illness with S. aureus per serving of Samgak-Kimbap was 1.44×10-10 per day. The most influential factor in increasing the risk of foodborne illnesses was the contamination level of S. aureus in Samgak-Kimbap.

본 연구는 삼각김밥에서 황색포도상구균 위해평가를 통해 삼각김밥의 섭취에 따른 황색포도상구균 식중독 발생 가능성을 분석하였다. 삼각김밥에 대한 황색포도상구균 오염도를 조사한 결과 170개의 시료가 모두 황색포도상구균 음성이었으며, 확률분포 조사를 통해 확인된 삼각김밥에서의 황색포도상구균의 초기 오염수준은 평균 -3.88 log CFU/g이었다. 삼각김밥의 섭취량 및 섭취자 비율은 미생물 위해평가를 위한 50대 주요 식품의 섭취량 및 섭취패턴 자료를 바탕으로 적정 확률분포모델을 도출하였으며, 삼각김밥의 1일 평균 섭취량과 섭취자 비율은 각각 191.31 g과 0.033으로 나타났다. 유통환경에 따라 시나리오를 구성하여 최종적으로 1일 1회 삼각김밥을 섭취하였을 때 황색포도상구균에 의한 식중독 발생확률은 평균 1.44×10-10로 추정되었다. 민감도 분석에서는 황색포도상구균 오염수준, 섭취량, 편의점 보관온도, 편의점 보관시간 등의 변수가 위해도와 가장 높은 양의 상관관계를 보였다. 본 연구에서는 삼각김밥에서의 황색포도상구균 식중독 발생 가능성은 인구 100,000명이 삼각김밥을 1일 1회 섭취했을 때 0.0000144명에게서 식중독이 발생할 수 있는 것으로 나타나 계속적으로 안전한 삼각김밥이 소비자에게 유통되기 위해서는 지속적으로 삼각김밥의 안전한 제조, 매장 내 보관온도 및 시간에 대한 모니터링이 필요할 것으로 사료된다.

Keywords

References

  1. Bahk GJ, Oh DH, Ha SD, Park KW, Joung MS, Chun SJ, Park JS, Woo GJ, Hong CH. Quantitative microbial risk assessment model for Staphylococcus aureus in Kimbab. Korean J. Food Sci. Technol. 37: 484-491 (2005)
  2. Baranyi J, Ross T, Roberts TA, MeMeekin TA. Effects of parameterization on the performance of empirical models used in 'predictive microbiology'. Food Microbiol. 13: 83-91 (1996) https://doi.org/10.1006/fmic.1996.0011
  3. Cha JO, Lee JK, Jung YH, Yoo JI, Park YK, Kim BS, Lee YS. Molecular analysis of Staphylococcus aureus isolates associated with staphylococcal food poisoning in South Korea. J. Appl. Microbiol. 101: 864-871 (2006) https://doi.org/10.1111/j.1365-2672.2006.02957.x
  4. Chen Q, Xie S. Genotypes, Enterotoxin Gene Profiles, and Antimicrobial resistance of Staphylococcus aureus associated with foodborne outbreaks in Hangzhou, China. Toxins. 11: 307 (2019) https://doi.org/10.3390/toxins11060307
  5. Cho YS, Lee JY, Lee MK, Shin DB, Kim DH, Park KM. Prevalence and characterization of Staphylcoccus aureus pathogenic factors isolated from various foods in Korea. Korean J. Food Sci. Technol. 43: 648-654 (2011) https://doi.org/10.9721/KJFST.2011.43.5.648
  6. Choi WS, Son N, Cho JI, Joo IS, Han JA, Kwak HS, Hong JH, Suh SH. Predictive model of Staphylococcus aureus growth on egg products. Food Sci. Biotechnol. 28: 913-922 (2019) https://doi.org/10.1007/s10068-018-0529-4
  7. Davey KR. Applicability of the Davey (linear Arrhenius) predictive model to the lag phase of microbial growth. J. Appl. Bacteriol. 70: 253-257 (1991) https://doi.org/10.1111/j.1365-2672.1991.tb02933.x
  8. Ding T, Shim YH, Kim HN, Ha SD, Chung MS, Hwang IG, Oh DH. Development of predictive model for the growth of Staphylococcus aureus in Kimbab. Food Sci. Biotechnol. 20: 471-476 (2011) https://doi.org/10.1007/s10068-011-0065-y
  9. Evenson ML, Hinds MW, Bernstein RS, Bergdoll MS. Estimation of human dose of staphylococcal enterotoxin A from a large outbreak of staphylococcal food poisoning involving chocolate milk. Int. J. Food Microbiol. 7: 311-316 (1988) https://doi.org/10.1016/0168-1605(88)90057-8
  10. Finger JA, Baroni WS, Maffei DF, Bastos DH, Pinto UM. Overview of foodborne disease outbreaks in Brazil from 2000 to 2018. Foods 8: 434 (2019) https://doi.org/10.3390/foods8100434
  11. Food Information Statistic System (FIS). Status of processed food segment markets 2019-convenience food market. Available from: https://www.atfis.or.kr/article/M001050000/view.do?articleId=3260&page=&searchKey=&searchString=&searchCategory=.Accessed Aug. 05. 2019
  12. Gibson AM, Bratchell N, Roberts TA. The effect of sodium chloride and temperature on rate and extent of growth of Clostridium botulinum type A in pasteurized pork slurry. J. Appl. Bacteriol. 62: 479-490 (1987) https://doi.org/10.1111/j.1365-2672.1987.tb02680.x
  13. Gormley FJ, Little CL, Rawal N, Gillespie IA, Lebaigue S, Adak GK. A 17-year review of foodborne outbreaks: describing the continuing decline in England and Wales (1992-2008). Epidemiol. Infect. 139: 688-699 (2011) https://doi.org/10.1017/S0950268810001858
  14. Johler S, Giannini P, Jermini M, Hummerjohann J, Baumgartner A, Stephan R. Further evidence for staphylococcal food poisoning outbreaks caused by egc-encoded enterotoxins. Toxins. 7: 997-1004 (2015) https://doi.org/10.3390/toxins7030997
  15. Jung H. Consumer survey and hazard analysis for the improvement of food hygiene and safety in purchase. MS Thesis, Korea University, Seoul, Korea (2011)
  16. Kang KA, Kim YW, Yoon KS. Development of predictive growth models for Staphylococcus aureus and Bacillus cereus on various food matrices consisting of ready-to-eat (RTE) foods. Food Sci. Anim. Resour. 30: 730-738 (2010) https://doi.org/10.5851/kosfa.2010.30.5.730
  17. Kang YS, Yoon SK, Jwa SH, Lee DH, Woo GJ, Park YS, Kim CM. Prevalence of Staphylococcus aureus in Kimbap. J. Food Hyg. Saf. 17: 31-35 (2002)
  18. Kim HK, Lee HT, Kim JH, Lee SS. Analysis of microbiological contamination in ready-to-eat foods. J. Food Hyg. Saf. 23: 285-290 (2008)
  19. Kim NH, Yun AR, Rhee MS. Prevalence and classification of toxigenic Staphylococcus aureus isolated from refrigerated ready-toeat foods (sushi, kimbab and California rolls) in Korea. J. Appl. Microbiol. 111: 1456­1464 (2011) https://doi.org/10.1111/j.1365-2672.2011.05168.x
  20. Kim TH, Bae HJ. Microbiological quality assessment of Kimbab with Applied HACCP. J. Korean Soc. Food Sci. Nutr. 48: 268-275 (2019) https://doi.org/10.3746/jkfn.2019.48.2.268
  21. Korea Centers for Disease Control Prevention (KCDC). Staphylococcal infection. Available from: http://www.kdca.go.kr/npt/biz/npp/portal/nppSumryMain.do?icdCd=ND0608&icdgrpCd=04&icdSubgrpCd=ND0006. Accessed Sep. 11. 2020
  22. Korea Rural Economic Institute (KREI). In-depth analysis report on processed food consumer attitude survey. Available from: https://atfis.or.kr/article/M001080000/view.do?articleId=3143&page=&searchKey=&searchString=&searchCategory=. Accessed Feb. 14. 2019
  23. Krouanton A, Hennekinnea JA, Letertrea C, Petita L, Chesneaub O, Brisaboisa A, De Buysera ML. Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France. Int. J. Food Microbiol. 115: 369-375 (2007) https://doi.org/10.1016/j.ijfoodmicro.2006.10.050
  24. Le Loir Y, Baron F, Gautier M. Staphylococcus aureus and food poisoning. Genet. Mol. Res. 2: 63-­76 (2003)
  25. Mcmeekin TA, Olley J, Ross T. Predictive microbiology: theory and application. John Wiley & sons Ltd. Taunton, UK. p. 340 (1993)
  26. Ministry of Food and Drug Safety (MFDS). Development of HACCP mandatory item selection tool. Available from: https://www.ndsl.kr/ndsl/search/detail/report/reportSearchResultDetail.do?cn=TRKO201900001078. Accessed Jun. 30. 2016
  27. Ministry of Food and Drug Safety (MFDS). Food poisoning statistics. Available from: https://www.foodsafetykorea.go.kr/portal/healthyfoodlife/foodPoisoningStat.do?menu_no=3724&menu_grp=MENU_NEW02. Accessed Dec. 30. 2019a
  28. Ministry of Food and Drug Safety (MFDS). Intake and intake patterns of 50 major foods for microbial risk assessment. Available from: https://viewer.nanet.go.kr/view/sd;streamdocsId=72059162118777952;currentPage=1;certificationId=7f1f495e-f743-45ab-a195-ce8de73ffd61;searchWord=. Accessed May. 30. 2012a
  29. Ministry of Food and Drug Safety (MFDS). Korea Food Code. Available from: https://www.foodsafetykorea.go.kr/foodcode/01_03.jsp?idx=63. Accessed Dec. 30. 2019b
  30. Ministry of Food and Drug Safety (MFDS). Microbial risk assessment guideline. Available from: http://www.nifds.go.kr/brd/m_15/view.do?seq=12733. Accessed Oct. 21. 2019c
  31. Ministry of Food and Drug Safety (MFDS). Study on the reduction of foodborne pathogenic bacteria in ready-to-eat (RTE) foods. Available from: http://www.ndsl.kr/ndsl/search/detail/report/reportSearchResultDetail.do?cn=TRKO200500002392. Accessed Dec. 02. 2004
  32. Ministry of Food and Drug Safety (MFDS). The study of minimum infective dose and dose-response models for foodborne pathogens. Available from: http://www.ndsl.kr/ndsl/search/detail/report/reportSearchResultDetail.do?cn=TRKO201300028880. Accessed Nov. 30. 2012b
  33. Ministry of Food and Drung Safety (MFDS). A study on the effective risk management of ready to eat foods via the application of predictive model. Available from : http://www.ndsl.kr/ndsl/search/detail/report/reportSearchResultDetail.do?cn=TRKO201000014801. Accessed April. 30. 2009
  34. Ministry of Food and Drung Safety (MFDS). Picture book of pathogenic microbiology. Available from: http://www.nifds.go.kr/brd/m_18/view.do?seq=5687&srchFr=&srchTo=&srchWord=&srchTp=&itm_seq_1=0&itm_seq_2=0&multi_itm_seq=0&company_cd=&company_nm=&page=19. Accessed Oct. 04. 2013
  35. Oh SK, Koo M, Lee N, Kim HJ, Oh SW, Choi SY. Distribution of newly described enterotoxin-like genes in Staphylococcus aureus isolated from ready-to-eat foods in Korea. Food Sci. Biotechnol. 20: 579­-584 (2011) https://doi.org/10.1007/s10068-011-0082-x
  36. Oscar TP. Development and validation of primary, secondary, and tertiary models for growth of Salmonella Typhimurium on sterile chicken. J. Food Prot. 68: 2606­-2613 (2005) https://doi.org/10.4315/0362-028X-68.12.2606
  37. Park SY, Choi JW, Yeon JH, Lee MJ, Lee DH, Kim KS, Park KH, Ha SD. Assessment of contamination levels of foodborne pathogens isolated in major RTE foods marketed in convenience stores. Korean J. Food Sci. Technol. 37: 274-278 (2005a)
  38. Park SY, Choi JW, Yeon JH, Lee MJ, Oh DH, Hong CH, Bahk GJ, Woo GJ, Park JS, Ha SD. Assessment of contamination level of foodborne pathogens in the main ingredients of Kimbab during the preparing process. Korean J. Food Sci. Technol. 37: 122-128 (2005b)
  39. Pinchuk IV, Beswick EJ, Reyes VE. Staphylococcal enterotoxins. Toxins. 2: 2177-2197 (2010) https://doi.org/10.3390/toxins2082177
  40. Ratkowsky DA, Olley J, Mcmeekin TA, Ball A. Relationship between temperature and growth rate of bacterial cultures. J. Bacteriol. 149: 1-5 (1982) https://doi.org/10.1128/jb.149.1.1-5.1982
  41. Rose JB, Haas CN. A risk assessment framework for the evaluation of skin infections and the potential impact of antibacterial soap washing. AM. J. Infect. Control. 27: 26-33 (1999)
  42. Ross T. Indices for performance evaluation of predictive models in food microbiology. J. Appl. Bacteriol. 81: 501-508 (1996) https://doi.org/10.1111/j.1365-2672.1996.tb03539.x
  43. Sanaa M, Coroller L, Cerf O. Risk assessment of listeriosis linked to the consumption of two soft cheeses made from raw milk: Camembert of Normandy and Brie of Meaux. Risk Anal. 24: 389-399 (2004) https://doi.org/10.1111/j.0272-4332.2004.00440.x
  44. Suzuki Y, Omoe K, Hu DL, Sato'o Y, Ono HK, Monma C, Arai, T, Konishi N, Kato R, Hirai A, Nakama A, Kai A, Kamata Y. Molecular epidemiological characterization of Staphylococcus aureus isolates originating from food poisoning outbreaks that occurred in Tokyo, Japan. Microbiol. Immunol. 58: 570-580 (2014) https://doi.org/10.1111/1348-0421.12188
  45. Valero A, Prez-Rodrguez F, Carrasco E, Fuentes-Alventosa JM, Garca-Gimeno RM, Zurera G. Modelling the growth boundaries of Staphylococcus aureus: effect of temperature, pH and water activity. Int. J. Food Microbiol. 133: 186-194 (2009) https://doi.org/10.1016/j.ijfoodmicro.2009.05.023
  46. Yoon SK, Ghafoor K, Kang YS, Sohn MG, Hwang IG, Kwon KS, Park J. Exposure assessment of Staphyloccocus aureus in Kimbab, a ready-to-eat Korean food. Food Sci. Biotechnol. 20: 23-28 (2011) https://doi.org/10.1007/s10068-011-0004-y
  47. Yoon SK, Kang YS, Sohn MG, Kim CM, Park JY. Prevalence of enterotoxigenic Staphylococcus aureus in retail ready-to-eat Korean Kimbab rolls. Food Sci. Biotechnol. 16: 621-625 (2007)