[en] Meat constitutes one of the major vehicles for human foodborne infections. This study aimed to assess the retail conditions and to determine the microbiological quality and safety of meat retailed within the establishments of Kigali (Rwanda). A questionnaire survey was carried out in 150 retail outlets to characterise meat retail conditions. Additionally, 270 retail meat samples were analysed for the enumeration of hygiene indicator bacteria (total mesophilic bacteria and Escherichia coli) and for the qualitative detection of Salmonella, using conventional culture methods. The results revealed that beef was the predominant meat sold within the retail premises of Kigali city, while meat from non-bovine animal species was mainly sold in large establishments. Salmonella was detected in 19.6% of all the retailed meat samples evaluated, whereas the mean loads for total mesophilic bacteria and E. coli were 7.3 and 3.5 log cfu/g, respectively. Three factors, namely the temperature conditions of the meat under retail, the cleanability of the used meat cutting boards, and the training of personnel in hygienic meat handling practices, were found to be significantly (p ≤ 0.05) associated with the risk of Salmonella occurrence in the retailed meat. The findings from this study highlight the need for improvements in hygienic meat handling practices, particularly, in small and medium meat retail establishments in Kigali.
Ongol, Martin Patrick; University of Rwanda, College of Agriculture Animal Science and Veterinary Medicine, School of Food Science and Technology, Food Safety and Quality Management Department. Avenue de l’armée P.O. Box 3900, Kigali, Rwanda.
Brostaux, Yves ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Modélisation et développement
Korsak Koulagenko, Nicolas ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Département de sciences des denrées alimentaires (DDA)
Daube, Georges ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Kimonyo, Anastase; University of Rwanda, College of Agriculture Animal Science and Veterinary Medicine, School of Food Science and Technology, Food Safety and Quality Management Department. Avenue de l’armée P.O. Box 3900, Kigali, Rwanda.
Sindic, Marianne ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Chimie des agro-biosystèmes
Language :
English
Title :
Meat retail conditions within the establishments of Kigali city (Rwanda): bacteriological quality and risk factors for Salmonella occurrence
Publication date :
March 2018
Journal title :
Tropical Animal Health and Production
ISSN :
0049-4747
eISSN :
1573-7438
Publisher :
Kluwer Academic Publishers, Boston, United States - Massachusetts
Abdalla, M., Suliman, S. E., & Bakhiet, A. O. (2009). Food safety knowledge and practices of street food vendors in Atbara city (Naher Elneel State Sudan). African Journal of Biotechnology, 8(24), 6997–6971.
Adekunle, J. (2007). Social custom and life style. In Culture and Customs of Rwanda (1st ed., pp. 115–132). Westport Conneticut, USA: Greenwood.
Adzitey, F., Teye, G. A., Kutah, W. N., & Adday, S. (2011). Microbial quality of beef sold on selected markets in the Tamale Metropolis in the Northern Region of Ghana. Livestock Research for Rural Development, 23(1), 1–6.
Bolton, D. J., Pearce, R. a., Sheridan, J. J., Blair, I. S., McDowell, D. a., & Harrington, D. (2002). Washing and chilling as critical control points in pork slaughter hazard analysis and critical control point (HACCP) systems. Journal of Applied Microbiology, 92(5), 893–902.
Borch, E., Nesbakken, T., & Christensen, H. (1996). Hazard identification in swine slaughter with respect to foodborne bacteria. International Journal of Food Microbiology, 30(1–2), 9–25.
Cardinale, E., Perrier Gros-Claude, J. D., Tall, F., Guèye, E. F., & Salvat, G. (2005). Risk factors for contamination of ready-to-eat street-vended poultry dishes in Dakar, Senegal. International Journal of Food Microbiology, 103(2), 157–165.
Carrasco, E., Morales-Rueda, A., & García-Gimeno, R. M. (2012). Cross-contamination and recontamination by Salmonella in foods: A review. Food Research International, 45, 545–556.
de Carvalho, A. M., César, C. L. G., Fisberg, R. M., & Marchioni, D. M. (2014). Meat consumption in São Paulo-Brazil: Trend in the last decade. PloS One, 9(5), e96667.
Centers for Disease Control and Prevention. (2013). An atlas of Salmonella in the United States, 1968–2011: Laboratory-based Enteric Disease Surveillance. Atlanta,Georgia: US Department of Health and Human Services.
Delhalle, L., Saegerman, C., Farnir, F., Korsak, N., Maes, D., Messens, W., … Daube, G. (2009a). Salmonella surveillance and control at post-harvest in the Belgian pork meat chain. Food Microbiology, 26, 265–271.
Delhalle, L., Saegerman, C., Messens, W., Farnir, F., Korsak, N., Van der Stede, Y., & Daube, G. (2009b). Assessing interventions by quantitative risk assessment tools to reduce the risk of human salmonellosis from fresh minced pork meat in Belgium. Journal of Food Protection, 72(11), 2252–2263.
Doulgeraki, A. I., Ercolini, D., Villani, F., & Nychas, G.-J. E. (2012). Spoilage microbiota associated to the storage of raw meat in different conditions. International Journal of Food Microbiology, 157(2), 130–141.
EFSA, & ECDC. (2015). The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne outbreaks in 2014. EFSA Journal, 13(12), 4329.
European Commission. (2005). Regulation No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Official Journal of the European Union, L338, 1–26.
Food and Agriculture Organization. (2015). Food Production by countries. Retrieved September 18, 2015, from http://faostat3.fao.org/download/Q/QL/E
Gopinath, S., Carden, S., & Monack, D. (2012). Shedding light on Salmonella carriers. Trends in Microbiology, 20(7), 320–327.
Greig, J. D., & Ravel, A. (2009). Analysis of foodborne outbreak data reported internationally for source attribution. International Journal of Food Microbiology, 130(2), 77–87.
Haileselassie, M., Taddele, H., Adhana, K., Kalayou, S., & Tadesse, G. (2013). Food safety knowledge and practices of abattoir and butchery shops and the microbial profile of meat in Mekelle City, Ethiopia. Asian Pacific Journal of Tropical Biomedicine, 3(5), 407–412.
Hassan Ali, N., Farooqui, A., Khan, A., Khan, A. Y., & Kazmi, S. U. (2010). Microbial contamination of raw meat and its environment in retail shops in Karachi, Pakistan. Journal of Infection in Developing Countries, 4(6), 382–388.
Heinz, G., & Hautzinger, P. (2007). Principle of meat processing technology. In Meat Processing Technology for Small to Medium Scale Producers (pp. 17–43). Rome Italy: Food and Agriculture Organization.
International Organization for Standardization. (2001). Microbiologyof food and animal feeding stuffs—Horizontal method for the enumeration of β-glucuronidase-positive Escherichia coli. Part 2: Colony-count technique at 44°C using 5-bromo-4-chloro-3-indolyl β-glucuronide. ISO 16649–2: 2001 (Vol. 2001). Geneva: International Organization for Standardization.
International Organization for Standardization. (2002). Microbiology of food and animal feeding stuffs—Horizontal method for the detection of Salmonella spp. ISO 6579:2002 (Vol. 6). Geneva: International Organization for Standardization.
International Organization for Standardization. (2003). Microbiology of food and animal feeding stuffs—Horizontal method for the enumeration of microorganisms—Colony-count technique at 30°C. ISO 4833:2003 (Vol. 1). Geneva: International Organization for Standardization.
International Organization for Standardization. (2007). Microbiology of food and animal feeding stuffs—General requirements and guidance for microbiological examinations. ISO 7218:2007. Geneva: International Organization for Standardization.
Jianu, C., & Goleţ, I. (2014). Knowledge of food safety and hygiene and personal hygiene practices among meat handlers operating in western Romania. Food Control, 42, 214–219.
Kabwang, R. (2013). Prevalence of enteropathogenic bacteria isolated from meat sold at retail outlet in Lubumbashi, R.D. Congo. University of Liege.
Kago, J., Roesel, K., Kang’ethe, E., Wangoh, J., Makita, K., & Grace, D. (2014). A sigle slip may cause lasting injury: Beef in Kenya contaminated from the start. In K. Roesel & D. Grace (Eds.), Food safety and informal markets: Animal products in sub-Saharan Africa (1st ed., p. 284). London: Routledge.
Lues, J. F. R., Rasephei, M. R., Venter, P., & Theron, M. M. (2006). Assessing food safety and associated food handling practices in street food vending. International Journal of Environmental Health Research, 16(5), 319–328.
McAfee, A. J., McSorley, E. M., Cuskelly, G. J., Moss, B. W., Wallace, J. M. W., Bonham, M. P., & Fearon, A. M. (2010). Red meat consumption: an overview of the risks and benefits. Meat Science, 84(1), 1–13.
McEntire, J., Acheson, D., Siemens, A., Eilert, S., & Robach, M. (2014). The Public Health Value of Reducing Salmonella Levels in Raw Meat and Poultry. Food Protection Trends, 34(6), 386–392.
Muyanja, C., Nayiga, L., Brenda, N., & Nasinyama, G. (2011). Practices, knowledge and risk factors of street food vendors in Uganda. Food Control, 22(10), 1551–1558.
Newell, D. G., Koopmans, M., Verhoef, L., Duizer, E., Aidara-Kane, A., Sprong, H., … Kruse, H. (2010). Food-borne diseases—The challenges of 20 years ago still persist while new ones continue to emerge. International Journal of Food Microbiology, 139(SUPPL. 1), S3–S15.
Niyonzima, E., Bora, D., & Ongol, M. P. (2013). Assessment of beef meat microbial contamination during skinning, dressing, transportation and marketing at a commercial abattoir in Kigali city, Rwanda. Pakistan Journal of Food Science, 23(3), 133–138.
Niyonzima, E., Ongol, M. P., Kimonyo, A., & Sindic, M. (2015). Risk Factors and Control Measures for Bacterial Contamination in the Bovine Meat Chain: A Review on Salmonella and Pathogenic E.coli. Journal of Food Research, 4(5), 98–121.
Niyonzima, E., Ongol, M. P., Brostaux, Y., Koulagenko, N. K., Daube, G., Kimonyo, A., & Sindic, M. (2016). Daily intake and bacteriological quality of meat consumed in the households of Kigali, Rwanda. Food Control, 69, 108–114.
Niyonzima, E., Ongol, M. P., Brostaux, Y., Korsak, N., Daube, G., Kimonyo, A., & Sindic, M. (2017). Consumption patterns, bacteriological quality and risk factors for Salmonella contamination in meat-based meals consumed outside the home in Kigali, Rwanda. Food Control, 73, 546–554.
Nychas, G.-J. E., Skandamis, P. N., Tassou, C. C., & Koutsoumanis, K. P. (2008). Meat spoilage during distribution. Meat Science, 78(1–2), 77–89.
Oranusi, S., Obioha, T., & Adekeye, B. (2014). Investigation on the microbial profile of frozen foods: Fish and Meat. International Journal of Advanced Research in Biological Sciences, 1(2), 71–78.
Rhoades, J. R., Duffy, G., & Koutsoumanis, K. (2009). Prevalence and concentration of verocytotoxigenic Escherichia coli, Salmonella enterica and Listeria monocytogenes in the beef production chain: a review. Food Microbiology, 26(4), 357–376.
Roesel, K., Grace, D., Kago, J., Desissa, F., Spengler, M., Amenu, K., … Heeb, A. (2014). Farmers, traders and retailers are risk managers. In K. Roesel & D. Grace (Eds.), Food safety and informal markets: Animal products in sub-Saharan Africa. (1st ed., p. 284). London, United Kingdom: Routledge.
Sans, P., & Combris, P. (2015). World meat consumption patterns: An overview of the last fifty years (1961–2011). Meat Science, 109, 106–111.
Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauxe, R. V., Widdowson, M.-A., Roy, S. L., … Griffin, P. M. (2011). Foodborne Illness Acquired in the United States—Major Pathogens. Emerging Infectious Diseases, 17(1), 7–15.
Small, A., & Buncic, S. (2009). Potential for the cross-contamination of the hides of cattle while they are held in lairage. The Veterinary Record, 164(9), 260–265.
Smigic, N., Antic, D., Blagojevic, B., Tomasevic, I., & Djekic, I. (2016). The level of food safety knowledge among meat handlers. British Food Journal, 118(1), 9–25.
Soyiri, I. N., Agbobli, H. K., & Dongdem, J. T. (2008). A pilot microbial assessment of beef sold in the ashiman market, a suburb of Accra, Ghana. African Journal of Food Agriculture Nutrition and Development, 8(1), 91–103.
Stevens, A., Kaboré, Y., Perrier-Gros-Claude, J.-D., Millemann, Y., Brisabois, A., Catteau, M., … Dufour, B. (2006). Prevalence and antibiotic-resistance of Salmonella isolated from beef sampled from the slaughterhouse and from retailers in Dakar (Senegal). International Journal of Food Microbiology, 110(2), 178–186.
Vipham, J., Brashears, M., Loneragan, G., Echeverry, A., Brooks, J., Chaney, W., & Miller, M. (2012). Salmonella and Campylobacter baseline in retail ground beef and whole-muscle cuts purchased during 2010 in the United States. Journal of Food Protection, 75(12), 2110–2115.
Warriner, K., Aldsworth, T. G., Kaur, S., & Dodd, C. E. R. (2002). Cross-contamination of carcasses and equipment during pork processing. Journal of Applied Microbiology, 93(1), 169–177.
Wong, L. F., Hald, T., Wolf, P. J., & Swanenburg, M. (2002). Epidemiology and control measures for Salmonella in pigs and pork. Livestock Production Science, 76, 215–222.
Wu, X., Zhuang, M., Adhikari, B., & Sun, J. (2017). Recent developments in novel freezing and thawing technologies applied to foods. Critical Reviews in Food Science and Nutrition, 17, 3620–3631.
