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Risk Assessment for Salmonellosis in Chicken in South Korea: The Effect of Salmonella Concentration in Chicken at Retail

  • Jeong, Jaewoon (Center for One Health, College of Veterinary Medicine, Konkuk University) ;
  • Chon, Jung-Whan (Center for One Health, College of Veterinary Medicine, Konkuk University) ;
  • Kim, Hyunsook (Department of Food & Nutrition, College of Human Ecology, Hanyang University) ;
  • Song, Kwang-Young (Center for One Health, College of Veterinary Medicine, Konkuk University) ;
  • Seo, Kun-Ho (Center for One Health, College of Veterinary Medicine, Konkuk University)
  • Received : 2018.07.14
  • Accepted : 2018.09.12
  • Published : 2018.10.31

Abstract

Salmonellosis caused by chicken consumption has been a critical issue in food safety worldwide, including in Korea. The probability of illness from consumption of chicken was simulated in study, based on the recipe of Dakgalbi, a commonly eaten chicken dish in Korea. Additionally, the processing stage at slaughterhouses to decrease Salmonella concentration in broilers was modeled to explore its effect on the likelihood of illness. A Monte Carlo simulation model was created using @RISK. Prevalence of Salmonella in chickens at the retail stage was found to be predominantly important in determining the probability of illness. Other than the prevalence, cooking temperature was found to have the largest impact on the probability of illness. The results also demonstrated that, although chlorination is a powerful tool for decreasing the Salmonella concentration in chicken, this effect did not last long and was negated by the following stages. This study analyzes the effects of variables of the retail-to-table pathway on the likelihood of salmonellosis in broiler consumption, and also evaluates the processing step used to decrease the contamination level of Salmonella in broilers at slaughterhouses. According to the results, we suggest that methods to decrease the contamination level of Salmonella such as chlorination had little effect on decreasing the probability of illness. Overall, these results suggest that preventing contamination of broiler with Salmonella must be a top priority and that methods to reduce the concentration of Salmonella in broilers at slaughterhouses hardly contribute to safe consumption of Salmonella-contaminated chicken.

Keywords

References

  1. Asoshima N, Matsuda M, Shigemura K, Honda M, Yoshida H, Oda T, Hiwaki H. 2015. Isolation of Escherichia albertii from raw chicken liver in Fukuoka City, Japan. Jpn J Infect Dis 68:248-250. https://doi.org/10.7883/yoken.JJID.2014.530
  2. Chung YH, Kim SY, Chang YH. 2003. Prevalence and antibiotic susceptibility of Salmonella isolated from foods in Korea from 1993 to 2001. J Food Prot 66:1154-1157. https://doi.org/10.4315/0362-028X-66.7.1154
  3. Fatsecret. 2018. Available from: www.fatsecret.kr/%EC%B9%BC%EB%A1%9C%EB%A6%AC-%EC%98%81%EC%96%91%EC%86%8C/%EC%9D%BC%EB%B0%98%EB%AA%85/%EB%8B%AD%EA%B0%80%EC%8A%B4%EC%82%B4?portionid=9981348&portionamount=1.000. Accessed at Jan 1, 2018.
  4. Hong Y, Ku K, Kim M, Won M, Chung K, Song KB. 2008. Survival of Escherichia coli O157: H7 and Salmonella typhimurium inoculated on chicken by aqueous chlorine dioxide treatment. J Microbiol Biotechnol 18:742-745.
  5. Huang J, Zong Q, Zhao F, Zhu J, Jiao XA. 2016. Quantitative surveys of Salmonella and Campylobacter on retail raw chicken in Yangzhou, China. Food Control 59:68-73. https://doi.org/10.1016/j.foodcont.2015.05.009
  6. Hue O, Le Bouquin S, Laisney MJ, Allain V, Lalande F, Petetin I, Rouxel S, Quesne S, Gloaguen PY, Picherot M, Santolini J, Salvat G, Bougeard S, Chemaly M. 2010. Prevalence of and risk factors for Campylobacter spp. contamination of broiler chicken carcasses at the slaughterhouse. Food Microbiol 27:992-999. https://doi.org/10.1016/j.fm.2010.06.004
  7. Hyeon JY, Chon JW, Hwang IG, Kwak HS, Kim MS, Kim SK, Choi IS, Song CS, Park C, Seo KH. 2011. Prevalence, antibiotic resistance, and molecular characterization of Salmonella serovars in retail meat products. J Food Prot 74:161-166. https://doi.org/10.4315/0362-028X.JFP-10-327
  8. James C, Vincent C, de Andrade Lima T, James SJ. 2006. The primary chilling of poultry carcasses-A review. Int J Refrig 29:847-862. https://doi.org/10.1016/j.ijrefrig.2005.08.003
  9. James WO, Brewer RL, Prucha JC, Williams Jr W, Parham DR. 1992. Effects of chlorination of chill water on the bacteriologic profile of raw chicken carcasses and giblets. J Am Vet Med Assoc 200:60-63.
  10. Juneja VK, Melendres MV, Huang L, Gumudavelli V, Subbiah J, Thippareddi H. 2007. Modeling the effect of temperature on growth of Salmonella in chicken. Food Microbiol 24:328-335. https://doi.org/10.1016/j.fm.2006.08.004
  11. Kim MS, Lim TH, Jang JH, Lee DH, Kim BY, Kwon JH, Choi SW, Noh JY, Hong YH, Lee SB, Yang SY, Lee HJ, Lee JB, Park SY, Choi IS, Song CS. 2012. Prevalence and antimicrobial resistance of Salmonella species isolated from chicken meats produced by different integrated broiler operations in Korea. Poult Sci 91:2370-2375. https://doi.org/10.3382/ps.2012-02357
  12. Korea Meteorological Administration. 2018. Temperature Database of Seoul. Available from: http://www.kma.go.kr/weather/climate/average_30years.jsp?yy_st=2011&stn=108&norm=M&x=12&y=10&obs=0&mm=5&dd=15. Accessed at Jan 1, 2018.
  13. Lee SK, Choi WH, Muhlisin M, Kang SM, Kim CJ, Ahn BK, Kang CW. 2011. Quality comparison of Chuncheon dakgalbi made from Korean native chickens and broilers. Korean J Food Sci An 31:731-740. https://doi.org/10.5851/kosfa.2011.31.5.731
  14. Liu H, Gong J, Chabot D, Miller SS, Cui SW, Ma J, Zhong F, Wang Q. 2015. Protection of heat-sensitive probiotic bacteria during spray-drying by sodium caseinate stabilized fat particles. Food Hydrocoll 51:459-467. https://doi.org/10.1016/j.foodhyd.2015.05.015
  15. Lu Y, Wu C. 2012. Reductions of Salmonella enterica on chicken breast by thymol, acetic acid, sodium dodecyl sulfate or hydrogen peroxide combinations as compared to chlorine wash. Int J Food Microbiol 152:31-34. https://doi.org/10.1016/j.ijfoodmicro.2011.09.015
  16. Luber P. 2009. Cross-contamination versus undercooking of poultry meat or eggs-Which risks need to be managed first? Int J Food Microbiol 134:21-28. https://doi.org/10.1016/j.ijfoodmicro.2009.02.012
  17. Moore JE, Matsuda M. 2007. Consumption of raw chicken sashimi, Kyushu Island, Japan-Risk of campylobacteriosis or not? Travel Med Infect Dis 5:64-65. https://doi.org/10.1016/j.tmaid.2006.02.003
  18. Muhlisin M, Kang SM, Choi WH, Kim CJ, An BK, Kang CW, Lee SK. 2012. New approach to Chuncheon Dakgalbi processing by various chicken materials, seasoning and cooking methods. Korean J Food Sci An 32:740-748. https://doi.org/10.5851/kosfa.2012.32.6.740
  19. Murphy RY, Duncan LK, Johnson ER, Davis MD, Smith JN. 2002. Thermal inactivation D-and z-values of Salmonella serotypes and Listeria innocua in chicken patties, chicken tenders, franks, beef patties, and blended beef and turkey patties. J Food Prot 65:53-60. https://doi.org/10.4315/0362-028X-65.1.53
  20. Nauta M, van Der Fels-Klerx I, Havelaar A. 2005. A poultry-processing model for quantitative microbiological risk assessment. Risk Anal 25:85-98. https://doi.org/10.1111/j.0272-4332.2005.00569.x
  21. Northcutt JK, Smith DP, Musgrove MT, Ingram KD, Hinton Jr A. 2005. Microbiological impact of spray washing broiler carcasses using different chlorine concentrations and water temperatures. Poult Sci 84:1648-1652. https://doi.org/10.1093/ps/84.10.1648
  22. Nyachuba DG. 2010. Foodborne illness: Is it on the rise? Nutr Rev 68:257-269. https://doi.org/10.1111/j.1753-4887.2010.00286.x
  23. Oscar TE. 2005. Validation of lag time and growth rate models for Salmonella Typhimurium: acceptable prediction zone method. J Food Sci 70:129-137. https://doi.org/10.1111/j.1365-2621.2005.tb07103.x
  24. Oscar TP. 2004. A quantitative risk assessment model for Salmonella and whole chickens. Int J Food Microbiol 93:231-247. https://doi.org/10.1016/j.ijfoodmicro.2003.12.002
  25. Paul NC, Sullivan TS, Shah DH. 2017. Differences in antimicrobial activity of chlorine against twelve most prevalent poultry-associated Salmonella serotypes. Food Microbiol 64:202-209. https://doi.org/10.1016/j.fm.2017.01.004
  26. Portal of Food Safety Information. Statistics of food poisoning. Available at: https://www.foodsafetykorea.go.kr/main.do. Accessed at Jan 1, 2018.
  27. Rose N, Beaudeau F, Drouin P, Toux JY, Rose V, Colin P. 1999. Risk factors for Salmonella enterica subsp. enterica contamination in French broiler-chicken flocks at the end of the rearing period. Prev Vet Med 39:265-277. https://doi.org/10.1016/S0167-5877(99)00002-1
  28. Silva RR, Moraes CA, Bessan J, Vanetti MCD. 2009. Validation of a predictive model describing growth of Salmonella in enteral feeds. Braz J Microbiol 40:149-154. https://doi.org/10.1590/S1517-83822009000100026
  29. Smadi H, Sargeant JM. 2012. Quantitative risk assessment of human salmonellosis in Canadian broiler chicken breast from retail to consumption. Risk Anal 33:232-248.
  30. Song YR, Kim DS, Muhlisin M, Seo TS, Jang A, Pak JI, Lee SK. 2014. Effect of chicken skin and pork backfat on quality of dakgalbi-taste chicken sausage. Korean J Poult Sci 41:181-189. https://doi.org/10.5536/KJPS.2014.41.3.181
  31. Trendmonitor. 2018. Available at: www.trendmonitor.co.kr/tmweb/trend/allTrend/detail.do?bIdx=574&code=0201&trendType=CKOREA. Accessed at Jan 1, 2018.
  32. van Asselt ED, Zwietering MH. 2006. A systematic approach to determine global thermal inactivation parameters for various food pathogens. Int J Food Microbiol 107:73-82. https://doi.org/10.1016/j.ijfoodmicro.2005.08.014
  33. van Boekel MAJS. 2002. On the use of the weibull model to describe thermal inactivation of microbial vegetative cells. Int J Food Microbiol 74:139-159. https://doi.org/10.1016/S0168-1605(01)00742-5
  34. Whiting RC, Buchanan RL. 1997. Development of a quantitative risk assessment model for Salmonella enteritidis in pasteurized liquid eggs. Int J Food Microbol 36:111-125. https://doi.org/10.1016/S0168-1605(97)01262-2
  35. WHO [World Health Organization]. 2002. Risk assessments of Salmonella in eggs and broiler chickens. Food & Agriculture Org, Geneva, Switzerland.
  36. Woo YK. 2007. Survey on the status of microbial contamination of chicken meats collected from poultry processing plants in nationwide. Korean J Microbiol 43:186-192.
  37. Zhu J, Wang Y, Song X, Cui S, Xu H, Yang B, Huang J, Liu G, Chen Q, Zhou G, Chen Q, Li F. 2014. Prevalence and quantification of Salmonella contamination in raw chicken carcasses at the retail in China. Food Control 44:198-202. https://doi.org/10.1016/j.foodcont.2014.03.050
  38. Zwietering MH, van Gerwen SJC. 2000. Sensitivity analysis in quantitative microbial risk assessment. Int J Food Microbiol 58:213-221. https://doi.org/10.1016/S0168-1605(00)00275-0

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