DOI QR코드

DOI QR Code

Quantitative Risk Assessment of Listeria monocytogenes in Smoked and Raw Salmon

훈제 및 생연어에서 Listeria monocytogenes의 정량적 미생물 위해성 평가

  • Song, Ki Young (Department of Food and Nutrition, Kyung Hee University) ;
  • Yang, So Young (Department of Food and Nutrition, Kyung Hee University) ;
  • Lee, Eun Woo (Department of Life Science and Biotechnology, Dong Eui University) ;
  • Yoon, Ki Sun (Department of Food and Nutrition, Kyung Hee University)
  • Received : 2021.01.26
  • Accepted : 2021.03.03
  • Published : 2021.04.30

Abstract

Salmon is recognized as a health-promoting functional food due to its high content of unsaturated fatty acids such as eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), and thus demand has increased globally. This study compared the risk of Listeria monocytogenes between smoked and raw salmon samples from online and offline markets. L. monocytogenes was in two out of 375 smoked salmon samples, while no L. monocytogenes was detected in 350 samples of raw salmons. L. monocytogenes began to grow after 3 and 6 d storage at 4℃ in both raw and smoked salmon, respectively. The contamination level of L. monocytogenes increased in both smoked and raw salmon from the market to home. The lag time of L. monocytogenes growing in smoked salmons was longer than that in raw salmons, but no significant difference in the growth rates was observed between the two products. Although the growth potential of L. monocytogenes was higher in raw than smoked salmon, the longer shelf life of smoked salmon at refrigerated temperature increased the risk of consuming smoked salmon. The probability risk of listeriosis due to smoked salmon consumption (2.27×10-9) was higher than that of raw salmon (1.55×10-14) for the general population. However, the risk of foodborne illness for the susceptible population increased 10 and 100 times with both smoked and raw salmon consumption.

본 연구에서는 훈제연어와 연어회 및 샐러드 등에 많이 활용되는 생연어 섭취에 따른 L. monocytogenes 에 의한 식중독 발생 리스크를 비교하기 위해 정량적 미생물 위해성 평가를 수행하였다. 연구 결과 하루에 1회 훈제연어와 생연어 섭취로 L. monocytogenes로 인한 식중독 발생 가능성은 취약계층의 경우 1.02×10-7, 6.99×10-13이며, 일반계층에서는 2.27×10-9, 1.55×10-14으로 나타나 취약계층에서 식중독 발생 가능성은 훈제연어의 경우 100배, 생연어의 경우 10배로 증가하는 것으로 확인되었다. 또한 생연어가 훈제연어보다 식중독 발생 가능성이 낮은 것으로 확인되었는데, 이는 생연어는 짧은 유통기한 때문에 냉장온도에서 최고농도로 증가할 수 있는 가능성이 매우 낮기 때문인 것으로 나타났다. 그러나 L. monocytogenes 최소 감염량이 102-103 cells로 매우 낮은 것을 고려할 때 임신부, 고령층과 같은 취약계층에 대한 식품안전 교육이 더욱 필요할 것으로 사료된다. 훈제연어에서는 염지, 훈연공정 때문에 4℃, 10℃ 냉장보관 초기에는 L. monocytogenes의 성장이 다소 저해되었으나 각각 6.4일, 2.7일 후 다시 증식하는 것으로 확인되었다. 결론적으로 훈제연어에서 L. monocytogenes 오염수준이 높고 냉장보관온도가 남용(10℃) 되었을 때 냉장유통 기간인 2주 동안에도 최고 농도로 성장해 식중독 발생 리스크가 높아질 수 있다. 따라서 훈제연어의 공정과정에서 L. monocytogenes가 오염되지 않도록 철저한 위생관리가 필요하며 온·오프라인 유통환경관리에 대한 재점검이 필요할 것으로 사료된다.

Keywords

Acknowledgement

본 연구는 2019년도 식품의약품안전처 용역연구개발과제 연구개발비(18162축산선524) 지원에 의해 수행되었으며 감사드립니다.

References

  1. Bastias, J.M., Balladares, P., Acuna, S., Quevedo, R., Munoz, O., Determining the effect of different cooking methods on the nutritional composition of salmon (Salmo salar) and chilean jack mackerel (Trachurus murphyi) fillets. PloS ONE, 12, e0180993 (2017). https://doi.org/10.1371/journal.pone.0180993
  2. Katikou, P., Hughes, S.I., Robb, D.H.F., Lipid distribution within Atlantic salmon (Salmo salar) fillets. Aquaculture, 202, 89-99 (2001). https://doi.org/10.1016/S0044-8486(01)00562-2
  3. Korea Maritime Institute, (2019, August 20). 2017 Weekly report (Vol.51). Retrieved from https://www.kmi.re.kr/web/trebook/view.do?rbsIdx=273&page=26&idx=63
  4. Ministry of Food and Drug Safety, (2021, March 3). 2019 Risk assessment and reduction of Listeria monocytogenes in agriculture, livestock and fishery products. Report of MFDS, Seoul, Korea. Retrieved from https://scienceon.kisti.re.kr/srch/selectPORSrchReport.do?cn=TRKO202000029896&dbt=TRKO
  5. Lovdal, T., The microbiology of cold smoked salmon. Food Control, 54, 360-373 (2015). https://doi.org/10.1016/j.foodcont.2015.02.025
  6. Jeong, H.W., Park, S.H., Lee, J.H., Kim, S.J., Ryu, S.H., Song, M.O., Park, S.H., Jo, J.Y., Park, G.Y., Choi, S.M., Prevalence and antibiotic resistance patterns in Listeria monocytogenes isolated from food. J. Food Hyg. Saf., 29, 26-30 (2014). https://doi.org/10.13103/JFHS.2014.29.1.026
  7. Gonzalez, D., Vitas, A. I., Diez-Leturia, M., Garcia-Jalon, I.. Listeria monocytogenes and ready-to-eat seafood in Spain: Study of prevalence and temperatures at retail. Food Microbiol., 36, 374-378 (2013). https://doi.org/10.1016/j.fm.2013.06.023
  8. Domenech, E., Jimenez-Belenguer, A., Amoros, J.A., Ferrus, M.A., Escriche, I., Prevalence and antimicrobial resistance of Listeria monocytogenes and Salmonella strains isolated in ready-to-eat foods in Eastern Spain. Food Control, 47, 120-125 (2015). https://doi.org/10.1016/j.foodcont.2014.06.043
  9. Abdollahzadeh, E., Ojagh, S.M., Hosseini, H., Irajian, G., Ghaemi, E.A., Prevalence and molecular characterization of Listeria spp. and Listeria monocytogenes isolated from fish, shrimp, and cooked ready-to-eat(RTE) aquatic products in Iran. LWT-Food Sci. Technol., 73, 205-211 (2016). https://doi.org/10.1016/j.lwt.2016.06.020
  10. Norton, D.M., McCamey, M.A., Gall, K.L., Scarlett, J.M., Boor, K.J., Wiedmann, M.. Molecular studies on the ecology of Listeria monocytogenes in the smoked fish processing industry. Appl. Environ. Microbiol., 67, 198-205 (2001). https://doi.org/10.1128/AEM.67.1.198-205.2001
  11. Busani, L., Cigliano, A., Taioli, E., Caligiuri, V., Chiavacci, L., Di Bella, C., Battisti, A., Duranti, A., Gianfranceschi, M., Nardella, M.C., Ricci, A., Rolesu, S., Tamba, M., Marabelli, R., Caprioli, A., Prevalence of Salmonella enterica and Listeria monocytogenes contamination in foods of animal origin in Italy. J. Food Prot., 68, 1729-1733 (2015). https://doi.org/10.4315/0362-028X-68.8.1729
  12. Kramarenko, T., Roasto, M., Keto-Timonen, R., Maesaar, M., Meremae, K., Kuningas, M., Horman, A., Korkeala, H., Listeria monocytogenes in ready-to-eat vacuum and modified atmosphere packaged meat and fish products of Estonian origin at retail level. Food Control, 67, 48-52 (2016). https://doi.org/10.1016/j.foodcont.2016.02.034
  13. Wieczorek, K., Osek, J., Prevalence, genetic diversity and antimicrobial resistance of Listeria monocytogenes isolated from fresh and smoked fish in Poland. Food Microbiol., 64, 164-171 (2017). https://doi.org/10.1016/j.fm.2016.12.022
  14. Food and Drug Administration, (2021, March 26). Foodborne pathogenic microorganisms and natural toxins handbook. Retrieved from https://pdf.usaid.gov/pdf_docs/pnado152.pdf
  15. Ministry of Food and Drug Safety, (2019, August 16). The study of minimum infective dose and dose-response models for foodborne pathogens. Retrieved from https://scienceon.kisti.re.kr/commons/util/originalView.do?cn=TRKO201300028880&dbt=TRKO&rn=
  16. Allerberger, F., Wagner, M., Listeriosis: A resurgent food-borne infection. Clin. Microbiol. Infect., 16, 16-23 (2010). https://doi.org/10.1111/j.1469-0691.2009.03109.x
  17. Vit, M., Olejnik, R., Dlhy, J., Karpiskova, R., Castkova, J., Prikazsky, V., Prikazska, M., Benes, C., Petras, P., Outbreak of listeriosis in the Czech Republic, late 2006-preliminary report. Euro Sureill., 12, E070208.1 (2007).
  18. Pichler, J., Much, P., Kasper, S., Fretz, R., Auer, B., Kathan, J., Mann, M., Huhulescu, S., Ruppitsch, W., Pietzka, A., Silberbauer, K., Neumann, C., Gschiel, E., Martin, A.D., Schuetz, A., Gindl, J., Neugschwandtner, E., Allerberger, F., An outbreak of febrile gastroenteritis associated with jellied pork contaminated with Listeria monocytogenes. Wien. Klin. Wochenschr., 121, 149-156 (2009). https://doi.org/10.1007/s00508-009-1137-3
  19. World Health Organization, (2019, August 14). 2019 Listeriosis-South Africa. Retrieved from https://www.who.int/csr/don/28-march-2018-listeriosis-south-africa/en/
  20. European Food Safety Authority, (2019, August 20). 2005 Commission Regulation (EC) No 2073/2005 on microbiological criteria for foods. Retrieved from https://eur-lex.europa.eu/legal-content/EN/ALL/?uri=CELEX%3A32005R2073
  21. Health Canada, (2019, August 14). 2011 Policy on Listeria monocytogenes inready to eat foods. Retrieved from https://www.canada.ca/content/dam/hc-sc/migration/hc-sc/fn-an/alt_formats/pdf/legislation/pol/policy_listeria_monocytogenes_2011-eng.pdf
  22. Food and Drug Administration, (2021, March 18). Draft guidance for industry: Control of listeria monocytogenes in ready-to-eat foods. Retrieved from https://www.fda.gov/regulatory-information/search-fda-guidance-documents/draftguidance-industry-control-listeria-monocytogenes-ready-eat-foods
  23. Codex Alimentarius, (2019, August 15). Principles and guidelines for the conduct of microbiological risk assessment. Retrieved from http://www.fao.org/fao-who-codexalimentarius/sh-proxy/en/?lnk=1&url=https%253A%252F%252Fworkspace.fao.org%252Fsites%252Fcodex%252FStandards%252FCXG%2B30-1999%252FCXG_030e_2014.pdf
  24. Rocourt, J., BenEmbarek, P., Toyofuku, H., Schlundt, J., Quantitative risk assessment of Listeria monocytogenes in ready-to-eat foods: the FAO/WHO approach. FEMS Immunol. Med. Microbiol., 35, 263-267 (2003). https://doi.org/10.1016/S0928-8244(02)00468-6
  25. Perez-Rodriguez, F., van Asselt, E.D., Garcia-Gimeno, R.M., Zurera, G., Zwietering, M.H., Extracting additional risk managers information from a risk assessment of Listeria monocytogenes in deli meats. J. Food Prot., 70, 1137-1152 (2007). https://doi.org/10.4315/0362-028X-70.5.1137
  26. Carrasco, E., Perez-Rodriguez, F., Valero, A., Garcia-Gimeno, R.M., Zurera, G., Risk assessment and management of Listeria monocytogenes in ready-to-eat lettuce salads. Compr. Rev. Food Sci. Food Saf., 9, 498-512 (2010). https://doi.org/10.1111/j.1541-4337.2010.00123.x
  27. Franz, E., Tromp, S.O., Rijgersberg, H., van der Fels-Klerx, H.J., Quantitative microbial risk assessment for Escherichia coli O157: H7, Salmonella, and Listeria monocytogenes in leafy green vegetables consumed at salad bars. J. Food Prot., 73, 274-285 (2010). https://doi.org/10.4315/0362-028X-73.2.274
  28. Foerster, C., Figueroa, G., Evers, E., Risk assessment of Listeria monocytogenes in poultry and beef. Br. Food J., 117, 779-792 (2015). https://doi.org/10.1108/BFJ-03-2014-0131
  29. Lindqvist, R., Westoo, A., Quantitative risk assessment for Listeria monocytogenes in smoked or gravad salmon and rainbow trout in Sweden. Int. J. Food Microbiol., 58, 181-196 (2000). https://doi.org/10.1016/S0168-1605(00)00272-5
  30. Pouillot, R., Goulet, V., Delignette-Muller, M.L., Mahe, A., Cornu, M., Quantitative risk assessment of Listeria monocytogenes in French cold-smoked salmon: II. Risk characterization. Risk Anal., 29, 806-819 (2009). https://doi.org/10.1111/j.1539-6924.2008.01200.x
  31. Pasonen, P., Ranta, J., Tapanainen, H., Valsta, L., Tuominen, P., Listeria monocytogenes risk assessment on cold smoked and salt-cured fishery products in Finland-A repeated exposure model. Int. J. Food Microbiol., 304, 97-105 (2019). https://doi.org/10.1016/j.ijfoodmicro.2019.04.007
  32. Vose, D.J., The application of quantitative risk assessment to microbial food safety. J. Food Prot., 61, 640-648 (1998). https://doi.org/10.4315/0362-028X-61.5.640
  33. 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
  34. Gibson, A.M., Bratchell, N., Roberts, T., The effect of sodium chloride and temperature on the 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
  35. Davey, K.R., 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
  36. Ratkowsky, D.A., Olley, J., McMeekin, T.A., 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
  37. McMeekin, T.A., Olley, J.N., Ross, T., Ratkowsky D.A., Predictive microbiology: Theory and application. Biotechnologia, 2, 94 (1993).
  38. Choi, E.J., Kim, M.H., Bahk, G.J., Sanitary conditions for cold and frozen food storage warehouses in Korea. J. Food Hyg. Saf., 26, 283-288 (2011).
  39. Jung, H., Consumer survey and hazard analysis for the improvement of food hygiene and safety in purchase. Master's thesis, Korea University, Seoul, Korea (2011).
  40. Korea Meteorological Administration, (2019, August 15). 2018 Weather information. Retrieved from https://web.kma.go.kr/eng/index.jsp
  41. Ministry of Food and Drug Safety, (2019, August 5). Food intake for microbial risk assessment. Retrieved from https://policy.nl.go.kr/search/searchDetail.do?rec_key=SH1_UMO20140092676&kwd=#dummy
  42. Golden, N.J., Crouch, E.A., Latmer, H., Kadrt, A.R., Kause, J., Risk assessment for Clostridium perfringens in ready-to-eat and partially cooked meat and poultry products. J. Food Prot., 72, 1376-1384 (2009). https://doi.org/10.4315/0362-028X-72.7.1376
  43. Palisade, (2019 August 14). 2016 @RISK User's Guide. Retrieved from http://www.palisade.com/downloads/documentation/75/EN/RISK7_EN.pdf
  44. Cho, J.I., Lee, S.H., Lim, J.S., Kwak, H.S., Hwang, I.G., Predictive mathematical model for the growth kinetics of Listeria monocytogenes on smoked salmon. J. Food Hyg. Saf., 26, 120-124 (2011).
  45. Gimenez, B., Dalgaard, P.. Modelling and predicting the simultaneous growth of Listeria monocytogenes and spoilage micro-organisms in cold-smoked salmon. J. Appl. Microbiol., 96, 96-109 (2004). https://doi.org/10.1046/j.1365-2672.2003.02137.x
  46. Sperber, W.H., Influence of water activity on foodborne bacteria-a review. J. Food Prot., 46, 142-150 (1983). https://doi.org/10.4315/0362-028x-46.2.142
  47. Ministry of Food and Drug Safety, (2021, February 23). Food Code. Retrieved from https://www.foodsafetykorea.go.kr/foodcode/01_03.jsp?idx=13