Comparative prevalence of pathogenic and spoilage microbes in chicken sausages from Egypt and Greece

Abstract

This study investigated the spread of foodborne pathogens: Listeria monocytogenes, Es-cherichia coli O157:H7, Staphylococcus aureus and Salmonella in chicken sausage samples collected from retail markets in Greece and Egypt during 2006 and from Egypt through 2010. Other microbiological parameters; total viable count (TVC), lactic acid bacteria (LAB), pseudomonads (PS), staphylococci (STAPH), Brochothrix thermosphacta (BT), Enterobacteriaceae (EN), Escherichia coli (EC), yeasts and moulds (Y&M) were also counted. Egyptian chicken sausage samples were found to harbor L. mono- cytogenes, Staph. aureus and E. coli O157:H7; with frequencies equivalent to 24%, 60% and 26% of the total samples during 2006 and 37.87%, 64.44% and 41.11% of the total samples during 2010, respectively, while Greek samples were entirely free of theses pathogens. Enrichment techniques indicated the absence of Salmonella from both Greek and Egyptian samples. The obtained results may mobilize food producers and handlers in developing countries to take the due measures reducing food-borne pathogen risks and spoilage flora alongside the poultry chain.

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Mahgoub, S. and Sitohy, M. (2013) Comparative prevalence of pathogenic and spoilage microbes in chicken sausages from Egypt and Greece. Health, 5, 274-284. doi: 10.4236/health.2013.52037.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] European Commission Regulation (EC) (2004) No. 852/ 2004 of the European Parliament and of the Council of 29 April 2004 on the hygiene of foodstuffs. Official Journal of the European Union, 139, 1-54.
[2] CAC (Codex Alimentarius Commission) (1997) Recommended international code of practice general principles of food hygiene. CAC/ RCP 1-1969, Rev 3 Food and Agriculture Organization of the United Nations World Health Organization, Rome.
[3] CAC (Codex Alimentarius Commission) (2010) Thirty Third Session International Conference Centre, Geneva. www.codexalimentarius.net
[4] Mead, P.S., Slutsker, L., Dietz, V., McCaig, L.F., Bresee, J.S., Shapiro, C., Grifn, P.M. and Tauxe, R.V. (1999) Food related illness and death in the United States. Emerging Infectious Diseases, 5, 607-625. doi:10.3201/eid0505.990502
[5] Teratanavat, R. and Hooker, N.H. (2004) Understanding the characteristics of US meat and poultry recalls: 1994 2002. Food Control, 15, 359-367. doi:10.1016/S0956-7135(03)00098-7
[6] Uyttendaele, M., De Troy, D. and Debevere, J. (1999) Incidence of Listeria monocytogenes in different types of meat products on the Belgian retail market. International Journal of Food Microbiology, 53, 75-80. doi:10.1016/S0168-1605(99)00155-5
[7] R?rvik, L.M., Aase, B., Alvestad, T. and Caugant, D.A. (2003) Molecular epidemiological survey of Listeria monocytogenes in broilers and poultry products. Journal of Applied Microbiology, 94, 633-640. doi:10.1046/j.1365-2672.2003.01895.x
[8] Soultos, N., Koidis, P. and Madden, R.H. (2003) Presence of Listeria and Salmonella spp. in retail chicken in Northern Ireland. Letters in Applied Microbiology, 37, 421-423. doi:10.1046/j.1472-765X.2003.01423.x
[9] Farber, J.M. and Peterkin, P.I. (1991) Listeria monocyto genes, a food-borne pathogen. Microbiology Reviews, 55, 476-511.
[10] Rocourt, J., BenEmbarak, P., Toyofuku, H. and Schlundt, J. (2003) Quantitative risk assessment of Listeria mono cytogenes in ready-to-eat foods: The FAO/WHO approach. FEMS Immunology and Medical Microbiology, 35, 263 267. doi:10.1016/S0928-8244(02)00468-6
[11] McLauchlin, J., Mitchell, R.T., Smerdon, W.J. and Jewell, K. (2004) Listeria monocytogenes and listeriosis: A re view of hazard characterisation for use in microbiological risk assessment of foods. International Journal of Food Microbiology, 92, 15-33. doi:10.1016/S0168-1605(03)00326-X
[12] Little, C.L., Barrett, N.J., Grant, K. and McLauchlin, J. (2008) Microbiological safety of sandwiches from hospitals and other health care establishments in the United Kingdom with a focus on Listeria monocytogenes and other Listeria species. Journal of Food Protection, 71, 309-318.
[13] Chapman, P.A., Malo, A.T.C., Ellin, M., Ashton, R. and Harkin, M.A. (2001) Escherichia coli O157 in cattle and sheep at slaughter, on beef and lamb carcasses and in raw beef and lamb products in South Yorkshire, UK. International Journal of Food Microbiology, 64, 139-150. doi:10.1016/S0168-1605(00)00453-0
[14] Chinen, I., Tanaro, J.D., Miliwebsky, E., Lound, L.H., Illemi, G., Ledri, S., et al. (2001) Isolation and characterization of Escherichia coli O157:H7 from retail meats in Argentina. Journal of Food Protection, 64, 1346-1351.
[15] Pilip?inec, E., Tká?iková, L., Naas, H.T., Cabadaj, R. and Mikula, I. (1999) Isolation of verotoxigenic Escherichia coli O157 from poultry. Folia Microbiologica, 44, 455-456. doi:10.1007/BF02903722
[16] Smerdon, W.J., Adak, G.D., O’Brien, S.J., Gilespie, I.A. and Reacher, M. (2001) General outbreaks of infectious intestinal disease linked with red meat, England and Wales, 1992-1999. Communicable Disease and Public Health, 4, 259-267.
[17] Rubio, B., Martínez, B., González-Fernández, C., García Cachán, M.D., Rovira, J. and Jaim, E.I. (2006) Influence of storage period and packaging method on sliced dry cured beef “Cecina de Leon”: Effects on microbiological, physicochemical and sensory quality. Meat Science, 74, 710-717. doi:10.1016/j.meatsci.2006.06.002
[18] Korkeala, H., Suortti, T. and M?kel?, P. (1988) Ropy slime formation in vacuum-packed cooked meat products caused by homofermentative lactobacilli and a Leuconostoc species. International Journal of Food Microbiology, 7, 339-347. doi:10.1016/0168-1605(88)90060-8
[19] Von Holy, A. and Holzapfel, W.H. (1989) Spoilage of vacuum packaged processed meats by lactic acid bacteria, and economic consequences. Proceedings of the Interna tional Symposium of the World Association of Veterinary Food Hygienists Stockholm, Sweden, 185.
[20] Tirado, C. and Schmidt, K., Eds. (2000) WHO surveillance programme for control of foodborne infections and intoxications in Europe, 7th report, 1993-1998. BGVV FAO/WHO Collaborating Centre for Research and Training in Food Hygiene and Zoonoses.
[21] Marth, E.H. (1998) Extended shelf life refrigerated foods. Food Technology, 52, 57-62.
[22] ISO 11290-2 (1998) Microbiology of food and animal feeding stuffs—Horizontal method for the detection and enumeration of Listeria monocytogenes—Part 2: Enu meration method.
[23] Allerberger, F. (2003) Listeria: Growth, phenotypic dif ferentiation and molecular microbiology. FEMS Immunology and Medical Microbiology, 35, 183-189. doi:10.1016/S0928-8244(02)00447-9
[24] ISO 16654 (2001) Microbiology of food and animal feeding stuffs—Horizontal method for the detection of Escherichia coli O157.
[25] ISO 6579 (2002) Microbiology of food and animal feeding stuffs—Horizontal method for the detection of Sal monella spp.
[26] Luiz, A.F., Moreira, F.C., Corréa, E.F. and Falc?o, D.P. (2004) Monitoring of the dissemination of Salmonella in the chicken Frankfurt-sausage productionline of a sausage factory in the state of S?o Paulo, Brazil. Brazil, Memórias do Instituto Oswaldo Cruz, Rio de Janeiro, 99, 477-480. doi:10.1590/S0074-02762004000500003
[27] Y?lmaz, I., ?im?ek, O. and I??k?, M. (2002) Fatty acid composition and quality characteristics of low-fat cooked sausages made with beef and chicken meat, tomato juice and sunflower oil. Meat Science, 62, 253-258.
[28] Angelidis, A.S., Chronis, E.N., Papageoriou, D.K., Kazakis, I.I., Arsenoglou, K.C. and Stathopoulos, G.A. (2006) Non lactic acid, contaminating microbial flora in ready-to-eat foods: A potential food-quality index. Food Microbiology, 23, 95-100. doi:10.1016/j.fm.2005.01.015
[29] ICMSF, International Commission on Microbiological Specifications for Foods (2002) Microorganisms in foods 7: Microbiological testing in food safety management. Kluwer Academic/Plenum Publishers, New York.
[30] El-Khateib, T., Abd El-Rahman, H., Hamdy, M. and Lotfi, A. (1988) Poultry meat products in Egypt “proximal che mical composition and microbiological quality”. Fleis chwirtsch, 68, 756-757.
[31] Zahran, D.A., Hendy, E., Bassam, A. and El-Hifnawi, H.N. (2008) Incidence and radiation sensitivity of Bacillus cereus, Listeria monocytogenes and their toxins in some chicken products. Journal of World Applied Science, 5, 182-188.
[32] álvarez-Astorga, M., Capita, R., Alonso-Calleja, C., Moreno, B. and García-Fernández, M.D. (2002) Microbi ological quality of retail chicken by-products in Spain. Meat Science, 62, 45-50. doi:10.1016/S0309-1740(01)00225-X
[33] Ismail, S.A.S., Deak, T., Abd El-Rahman, H.A., Yassien, M.A.M. and Beuchat, L.R. (2000) Presence and changes in populations of yeasts on raw and processed poultry products stored at refrigeration temperature. International Journal of Food Microbiology, 62, 113-121. doi:10.1016/S0168-1605(00)00414-1
[34] Beuchat, L.R. and Ryu, J.H. (1997) Emerging Infectious Disease Journal, 3, 459-465. doi:10.3201/eid0304.970407
[35] N?rrung, B., Andersen, J.K. and Schlundt, J. (1999) Inci dence and control of Listeria monocytogenes in foods in Denmark. International Journal of Food Microbiology, 53, 195-203. doi:10.1016/S0168-1605(99)00157-9
[36] US Department of Agriculture, Food Safety and Inspec tion Service (USDA-FSIS) (2003) Control of Listeria mo nocytogenes in ready-to-eat meat and poultry products; final rule, 9 CFR 430.4. Federal Register, 68, 34208 34254. http://www.fsis.usdaov/OPPDE/rdad/FRPubs/97-013F.htm
[37] Mor-Mur, M. and Yuste, J. (2010) Emerging bacterial pathogens in meat and poultry: An overview. Food and Bioprocess Technology, 3, 24-35. doi:10.1007/s11947-009-0189-8
[38] S?r?ken, B., Pamuk, S., ?zakin, C., Gedikoglu, S. and Eyig?r, M. (2006) A note on the incidences of Salmonella spp., Listeria spp. and Escherichia coli O157:H7 serotypes in Turkish sausage (Soudjouck). Meat Science, 72, 177-181. doi:10.1016/j.meatsci.2005.05.025
[39] Vitas, A.I. and Garcia-Jalon, V.A.I. (2004) Occurrence of Listeria monocytogenes in fresh and processed foods in Navarra (Spain). International Journal of Food Microbiology, 90, 349-356. doi:10.1016/S0168-1605(03)00314-3
[40] Noack, D.J. and Joeckel, J. (1993) Listeria monocyto genes, occurrence and significance in meat and meat products and experience with recommendations for its detection and assessment. Fleischwirtschaft, 73, 581-584.
[41] Little, C.L., Taylor, F.C., Sagoo, S.K., Gillespie, I.A., Grant, K. and McLauchlin, J. (2007) Prevalence and level of Listeria monocytogenes and other Listeria species in re tail pre-packaged mixed vegetable salads in the UK. Food Microbiology, 24, 711-717. doi:10.1016/j.fm.2007.03.009
[42] Inoue, S., Nakama, A., Arai, Y., Kokubo, Y., Maruyama, T., Saito, A., Yoshida, T., Terao, T., et al. (2000) Prevalence and contamination levels of Listeria monocytogenes in retail foods in Japan. International Journal of Food Microbiology, 59, 73-77. doi:10.1016/S0168-1605(00)00284-1
[43] Franco, C.M., Quinto, E.J., Fente, C., Rodriguez-Otero, L. and Cepeda, A. (1995) Determination of the principal sources of Listeria spp. contamination in poultry meat and a poultry processing plant. Journal of Food Protection, 58, 1320-1325.
[44] Mead, G.C., Hudson, W.R. and Hinton, M.H. (1993) Micro biological survey of five poultry processing plants in the UK. British Poultry Science, 34, 497. doi:10.1080/00071669308417605
[45] Sandel, M.K. and McKillip, J.L. (2004) Virulence and recovery of Staphylococcus aureus relevant to the food industry using improvements on traditional approaches. Food Control, 15, 5-10. doi:10.1016/S0956-7135(02)00150-0
[46] Jay, J.M., Loessner, M.J., Golden, A.A. (2005) Modern food microbiology. 7th Edition, Aspen Publishers Inc., Gaithersburg.
[47] De Roever, C. (1998) Microbiological safety evaluations and recommendations on fresh produce. Food Control, 9, 321-347. doi:10.1016/S0956-7135(98)00022-X
[48] Taulo, S., Wetlesen, A., Abrahamsen, R., Kululanga, G., Mkakosya, R. and Grimason, A. (2008) Microbiological hazard identification and exposure assessment of food prepared and served in rural households of Lungwena, Malawi. International Journal of Food Microbiology, 125, 111-116. doi:10.1016/j.ijfoodmicro.2008.02.025
[49] Samadpour, M., Barbour, M.W., Nguyen, T., Cao, T.M., Buck, F., Depavia, G.A., Mazengia, E., Yang, P., Alfi, D., Lopes, M. and Stopforth, J.D. (2006) Incidence of en terohemorrhagic Escherichia coli, Escherichia coli O157, Salmonella, and Listeria monocytogenes in retail fresh ground beef, sprouts, and mushrooms. Journal of Food Protection, 69, 441-443.

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