Abstract
Objectives
To quantify salmonellosis risk in humans through consumption of boiled pork in urban Hung Yen Province, Vietnam, using a quantitative microbial risk assessment.
Methods
We collected 302 samples along the pork value chain in Hung Yen between April 2014 and February 2015. We developed a model in @Risk, based on microbiological, market, and household surveys on cooking, cross-contamination and consumption, and conducted sensitivity analysis.
Results
Salmonella prevalence of pen floor swabs, slaughterhouse carcasses and cut pork were 33.3, 41.7 and 44.4%, respectively. The annual incidence rate of salmonellosis in humans was estimated to be 17.7% (90% CI 0.89–45.96). Parameters with the greatest influence risk were household pork handling practice followed by prevalence in pork sold in the central market. Wide confidence interval in the incidence estimate was mainly due to the variability in the degree of reduction in bacteria concentration by cooking, and pork consumption pattern.
Conclusions
The risk of salmonellosis in humans due to boiled pork consumption appears to be high. Control measures may include improving the safety of retailed pork and improving household hygiene.
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References
Baranyi J, Roberts TA (1994) A dynamic approach to predicting bacterial growth in food. Int J Food Microbiol 23(3–4):277–294
CAC/GL 30 (1999) Principles and guidelines for the conduct of microbiological risk management. Codex Alimentarius-Joint FAO/WHO Food Standards Programme, Rome
de Man JC (1983) MPN tables, corrected. Eur J Appl Microbiol Biotechnol 17:301–305
Fahrion AS, Lapar ML, Nguyen-Ngoc T, Do-Ngoc T, Grace D (2013) Food-borne hazards in a transforming pork value chain in Ha Noi: basis for future risk assessments. Vietnamese J Prev Med 24:18–25
Grace D (2015) Food safety in low and middle income countries. Int J Environ Res Public Health 12(9):10490–10507
Grace D, McDermott J (2015) Food safety: reducing and managing food scares, 2014–2015 Global Food Policy Report. USA, International Food Policy Research Institute, Washington
Grace D, Makita K, Kang’ethe EK, Bonfoh B (2010) Safe food, fair food: participatory risk analysis for improving the safety of informally produced and marketed food in sub-Saharan Africa. Revue Africaine de Santé et de Productions Animales 8(S):3–11
GSO (2014) General Statistics Office of Vietnam: Administrative Unit and Climate in 2014. Retrieved 15 April, 2016, from https://www.gso.gov.vn/default.aspx?tabid=732
Havelaar AH, Kirk MD, Torgerson PR, Gibb HJ, Hald T, Lake RJ, Praet N, Bellinger DC, de Silva NR, Gargouri N, Speybroeck N, Cawthorne A, Mathers C, Stein C, Angulo FJ, Devleesschauwer B (2015) World Health Organization global estimates and regional comparisons of the burden of foodborne disease in 2010. PLoS Med 12(12):e1001923
Hien PTT (2009) Microbiological contamination of fresh minced pork from the retail market in Hanoi, Viet Nam. Mater thesis, Chiang Mai University and Freie University of Berlin
Hung NV (2015) Task force of risk assessment for food safety in Vietnam: operational research to assist policy and capacity building. Retrieved April 4, 2016, from https://cgspace.cgiar.org/handle/10568/69432
ICMSF (1986) Microorganisms in Foods 2. Sampling for microbiological analysis: principles and specific applications, 2nd edn. International Commission on Microbiological Specifications for Foods
ISO:21528-1 (2004) Microbiology of food and animal feeding stuffs-Horizontal methods for the detection and enumeration of Enterobacteriaceae—part 1: detection and enumeration by MPN technique with pre-enrichement. International Organization for Standardization. Geneva, Switzerland
Lapar M, Tiongco M (2011) Private standards in pork value chains: role, impact and potential for local innovation to improve food safety and enhance smallholder competitiveness. Farm Policy J 8(3):39–53
Makita K, Desissa F, Teklu A, Zewde G, Grace D (2012) Risk assessment of staphylococcal poisoning due to consumption of informally-marketed milk and home-made yoghurt in Debre Zeit, Ethiopia. Int J Food Microbiol 153(1–2):135–141
Mataragas M, Skandamis PN, Drosinos EH (2008) Risk profiles of pork and poultry meat and risk ratings of various pathogen/product combinations. Int J Food Microbiol 126(1–2):1–12
Mullner P, Jones G, Noble A, Spencer SE, Hathaway S, French NP (2009) Source attribution of food-borne zoonoses in New Zealand: a modified Hald model. Risk Anal 29(7):970–984
O’Connor AM, Wang B, Denagamage T, McKean J (2012) Process mapping the prevalence of salmonella contamination on pork carcass from slaughter to chilling: a systematic review approach. Foodborne Pathog Dis 9(5):386–395
OECD (2016) Meat consumption (indicator). Retrieved March 1, 2016, from https://data.oecd.org/agroutput/meat-consumption.htm
Phan TT, Khai LTL, Ogasawara N, Tam NT, Okatani AT, Akiba M, Hayashidani H (2005) Contamination of Salmonella in retail meats and shrimps in the Mekong Delta, Vietnam. J Food Prot 68(5):1077–1080
Ratkowsky DA, Lowry RK, McMeekin TA, Stokes AN, Chandler RE (1983) Model for bacterial culture growth rate throughout the entire biokinetic temperature range. J Bacteriol 154(3):1222–1226
Sanguankiat A, Pinthong R, Padungtod P, Baumann MPO, Zessin KH, Srikitjakarn L, Fries R (2010) a cross-sectional study of Salmonella in pork products in Chiang Mai, Thailand. Foodborne Pathog Dis 7(8):873–878
Sinh DX, Phuc PD, Nam NH, Thanh NT, Hue VTK, Long NH, Hung NV (2014) Salmonella crosscontamination of pork for health risk assessment: simulation of cooking preparation at households. Vietnam J Pract Med 5(933–934):233–237
Swart AN, van Leusden F, Nauta MJ (2016) A QMRA model for Salmonella in pork products during preparation and consumption. Risk Anal 36(3):516–530
Teunis PF, Kasuga F, Fazil A, Ogden ID, Rotariu O, Strachan NJ (2010) Dose-response modeling of Salmonella using outbreak data. Int J Food Microbiol 144(2):243–249
Thai TH, Hirai T, Lan NT, Yamaguchi R (2012) Antibiotic resistance profiles of Salmonella serovars isolated from retail pork and chicken meat in North Vietnam. Int J Food Microbiol 156(2):147–151
Thayer DW, Muller WS, Buchanan RL, Phillips JG (1987) Effect of NaCl, pH, temperature, and atmosphere on growth of Salmonella typhimurium in glucose-mineral salts medium. Appl Environ Microbiol 53(6):1311–1315
Toan LQ, Nguyen-Viet H, Huong BM (2013) Risk assessment of Salmonella in pork in Hanoi, Vietnam. Vietnam J Prev Med 24:10–17
Tuyet-Hanh TT, Minh NH, Vu-Anh L, Dunne M, Toms LM, Tenkate T, Thi MH, Harden F (2015) Environmental health risk assessment of dioxin in foods at the two most severe dioxin hot spots in Vietnam. Int J Hyg Environ Health 218(5):471–478
Valkenburgh SM, VanOosterom RA, Stenvers OFJ, Steijn K, VanPelt W (2004) Report on trends and sources of zoonotic agents: The Netherlands 2003, The Dutch Food and Consumer Product Safety Authority and the Ministry of Agriculture, Nature and Food Quality
Van TT, Moutafis G, Istivan T, Tran LT, Coloe PJ (2007) Detection of Salmonella spp. in retail raw food samples from Vietnam and characterization of their antibiotic resistance. Appl Environ Microbiol 73(21):6885–6890
Velugoti PR, Bohra LK, Juneja VK, Huang L, Wesseling AL, Subbiah J, Thippareddi H (2011) Dynamic model for predicting growth of Salmonella spp. in ground sterile pork. Food Microbiol 28(4):796–803
WB-Vietnam (2016) Abstracts: World Bank Vietnam Food Safety management. Retrieved 4 April, 2016, from http://www.eurochamvn.org/sites/default/files/uploads/Sector%20Committees/FAASC/News/Abstracts%20WB%20Vietnam%20Food%20Safety%20management%201.2016.pdf
Wilhelm B, Rajic A, Parker S, Waddell L, Sanchez J, Fazil A, Wilkins W, McEwen SA (2012) Assessment of the efficacy and quality of evidence for five on-farm interventions for Salmonella reduction in grow-finish swine: a systematic review and meta-analysis. Prev Vet Med 107(1–2):1–20
Yokozawa T, Sinh DX, Hung NV, Lapar L, Makita K (2016) Transition of Salmonella prevalence in pork value chain from pig slaughterhouses to markets in Hung Yen, Vietnam. J Jpn Soc Vet Epidemiol 20(1):51–58
Zaidi MB, McDermott PF, Fedorka-Cray P, Leon V, Canche C, Hubert SK, Abbott J, Leon M, Zhao S, Headrick M, Tollefson L (2006) Nontyphoidal Salmonella from human clinical cases, asymptomatic children, and raw retail meats in Yucatan, Mexico. Clin Infect Dis 42(1):21–28
Acknowledgements
We thank the collaborations of colleagues from Vietnam National University of Agriculture (Vietnam) in conducting field works and facilitation of the study. We thank all the farmers, slaughterhouse and pork stall owners for their help. Staff from the National Institute of Veterinary Research, veterinary hygiene group is acknowledged for their microbial analysis work. We thank Mr. Nguyen Tien Thanh and Nguyen Duy Tien for their assistance. This study was conducted under the project: “Reducing disease risks and improving food safety in smallholder pig value chains in Vietnam” (PigRISK), and funded by the Australian Centre for International Agricultural Research (ACIAR) and the Consultative Group on International Agricultural Research (CGIAR), Research Program Agriculture for Nutrition and Health (A4NH).
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This study was a part of PigRISK project funded by the Australian Centre for International Agricultural Research (ACIAR) (Grant Number: LPS/2010/047) and the Consultative Group on International Agricultural Research (CGIAR), Research Program Agriculture for Nutrition and Health (A4NH).
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All authors declare that they have no conflict of interest. All authors were involved in the writing of the manuscript and have approved the final version for publication.
Ethical approval
Ethical approval for this study was obtained from Institutional Review Board of the Hanoi School of Public Health (No. 148/2012/YTCC-HD3). Informed consent was obtained from all individual participants included in the study.
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This article is part of the supplement “Health and social determinants of health in Vietnam: local evidence and international implications”.
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Dang-Xuan, S., Nguyen-Viet, H., Unger, F. et al. Quantitative risk assessment of human salmonellosis in the smallholder pig value chains in urban of Vietnam. Int J Public Health 62 (Suppl 1), 93–102 (2017). https://doi.org/10.1007/s00038-016-0921-x
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DOI: https://doi.org/10.1007/s00038-016-0921-x