Incidence and contamination level of Clostridium perfringens in meat and meat products sold in Sakarya province of Turkey

Serap Coşansu Akdemir; Şeyma Ersöz

doi:10.3153/FH21018

Research Article

Incidence and contamination level of Clostridium perfringens in meat and meat products sold in Sakarya province of Turkey

Year 2021, , 172 - 178, 01.07.2021

Serap Coşansu Akdemir , Şeyma Ersöz

https://doi.org/10.3153/FH21018

Abstract

Totally 101 meat and meat product samples obtained from local markets and restaurants were analyzed for incidence and contamination level of Clostridium perfringens. The typical colonies grown anaerobically on Tryptose Sulfite Cycloserine Agar supplemented with 4-Methyliumbelliferyl (MUP) were confirmed by biochemical tests. Forty-eight of the samples (47.5%) were contaminated with C. perfringens. The highest incidence of the pathogen was determined in uncooked meatball samples (72.2%) followed by ground beef samples (61.3%). The incidence of C. perfringens in chicken meat, cooked meat döner, cooked chicken döner and emulsified meat product samples were 33.3, 33.3, 28.6 and 16.7%, respectively. Thirteen out of 101 samples (12.9%) yielded typical colonies on TSC-MUP Agar, but could not be confirmed as C. perfringens. Average contamination levels in sample groups ranged from 8.3 to 1.5×102 cfu/g, with the highest ground beef and the lowest chicken meat.

Keywords

Clostridium perfringens, Incidence, Meat, Meat products, Ground beef, Meatball

Supporting Institution

Commission of Scientific Research Projects of Sakarya University

Project Number

BAP-2012-01-16-009

Thanks

References

Clostridium perfringens by using chromogenic and fluorogenic substrates. Applied Environmental Microbiology, 67(9), 4382-4384. https://doi.org/10.1128/AEM.67.9.4382-4384.2001
Andersson, A., Ronner, U., Granum, P.E. (1995). What problems does the food industry have with the spore-forming pathogens Bacillus cereus and Clostridium perfringens? International Journal of Food Microbiology, 28, 145-155. https://doi.org/10.1016/0168-1605(95)00053-4
Anonymous (1999). Microbiology of food and animal feeding stuffs-Horizontal method for the enumeration of Clostridium perfringens. Colonies count technique (ISO 7937: 1997 Modified). European Standard (EN 13401).
Anonymous (2011). Türk Gıda Kodeksi Mikrobiyolojik Kriterler Yönetmeliği Retrieved from https://www.resmigazete.gov.tr/eskiler/2011/12/20111229M3-6.htm (Accessed 01.06.2020).
Apaydin, G., Ceylan, Z.G., Kaya, M. (2003). Değişik firmalara ait salamların bazı mikrobiyolojik ve kimyasal özellikleri. Turkish Journal of Veterinary and Animal Science, 27, 1299-1303.
Araujo, M., Sueiro, R.A., Gómez, M.J., Garrido, M.J. (2001). Evaluation of fluorogenic TSC agar for recovering Clostridium perfringens in groundwater samples. Water Science and Technology, 43(12), 201-204. https://doi.org/10.2166/wst.2001.0738
Başkaya, R., Karaca, T., Sevinç, İ., Çakmak, Ö., Yildiz, A., Yörük, M. (2004). İstanbul'da Satışa Sunulan Hazır Kıymaların Histolojik, Mikrobiyolojik ve Serolojik Kalitesi. Yüzüncü Yıl Üniversitesi Veteriner Fakültesi Dergisi, 15(1), 41-46.
Bostan, K., Yılmaz, F., Muratoğlu, K., Aydın, A. (2011). Pişmiş döner kebaplarda mikrobiyolojik kalite ve mikrobiyel gelişim üzerine bir araştırma. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 17(5), 781-786. https://doi.org/10.9775/kvfd.2011.4438
Brown, K.L. (2000). Control of bacterial spores. British Medical Bulletin, 56 (1), 158-171. https://doi.org/10.1258/0007142001902860 Brynestad, S., Granum, P.E. (2002). Clostridium perfringens and foodborne infections. International Journal of Food Microbiology, 74(3), 195-202. https://doi.org/10.1016/S0168-1605(01)00680-8
Byrne, B., Dunne, G., Bolton, D.J. (2006). Thermal inactivation of Bacillus cereus and Clostridium perfringens vegetative cells and spores in pork luncheon roll. Food Microbiology, 23(8), 803-808. https://doi.org/10.1016/j.fm.2006.02.002
Çakmak, Ö., Ormancı, F.S.B., Tayfur, M., Erol, İ. (2006). Presence and contamination level of Clostridium perfringens in raw frozen ground poultry and poultry burgers. Turkish Journal of Veterinary and Animal Sciences, 30(1), 101-105.
De Boer, E., Spiegelenberg, W.M., Janssen, F.W. (1985). Microbiology of spices and herbs. Antonie van Leeuwenhoek, 51(4), 435-438. https://doi.org/10.1007/BF02275058
EFSA-ECDC (European Food Safety Authority-European Centre for Disease Prevention and Control), (2015). The European Union summary report on trends and sources of zoonoses, zoonotic agents, and food-borne outbreaks in 2014. EFSA Journal, 13(4329), 191. https://doi.org/10.2903/j.efsa.2015.4329
Elmalı, M., Ulukanlı, Z., Yaman, H. (2005). Microbiological quality of emulsified type meat products (salami-frankfurter sausage) marketed in Kars. Journal of Faculty of Veterinary Medicine, Erciyes University, 2(1), 15-21.
Fischer, M., Zhu, S., de Ree, E. (2012). Culture media for the detection and enumeration of clostridia in food. In: Handbook of Culture Media for Food and Water Microbiology, J.E.L Corry, G.D.W. Curtis, R.M. Baird (Eds.), Royal Society of Chemistry Publishing, p. 66-89. https://doi.org/10.1039/9781847551450-00066
Garcia, S., Heredia, N. (2011). Clostridium perfringens: a dynamic foodborne pathogen. Food and Bioprocess Technology, 4(4), 624-630. https://doi.org/10.1007/s11947-009-0182-2
García, S., Vidal, J.E., Heredia, N., Juneja, V.K. (2019). Clostridium perfringens. In: Food Microbiology: Fundamentals And Frontiers, Michael P. Doyle, Francisco Diez-Gonzalez, Colin Hill (Editors), 5th Edition, ASM Books, pp. 513-540. https://doi.org/10.1128/9781555819972.ch19
Guran, H.S., Oksuztepe, G. (2013). Detection and typing of Clostridium perfringens from retail chicken meat parts. Letters in Applied Microbiology, 57(1), 77-82. https://doi.org/10.1111/lam.12088
Guran, H.S., Vural, A., Erkan, M.E. (2014). The prevalence and molecular typing of Clostridium perfringens in ground beef and sheep meats. Journal für Verbraucherschutz und Lebensmittelsicherheit, 9(2), 121-128. https://doi.org/10.1007/s00003-014-0866-z
Immerseel, F.V., Buck, J.D., Pasmans, F., Huyghebaert, G., Haesebrouck, F., Ducatelle, R. (2004). Clostridium perfringens in poultry: an emerging threat for animal and public health. Avian pathology, 33(6), 537-549. https://doi.org/10.1080/03079450400013162 Jaloustre, S., Guillier, L., Poumeyrol, G., Morelli, E., Delignette-Muller, M.L. (2013). Efficiency of a reheating step to inactivate Clostridium perfringens vegetative cells: How to measure it? Food Control, 29(2), 422-428. https://doi.org/10.1016/j.foodcont.2012.07.003
Juneja, V.K., Novak, J.S., Labbe, R.J. (2010). Clostridium perfringens. In: Pathogens and Toxins in Foods: Challenges and Interventions, V.K. Juneja, J.N. Sofos (Eds.), ASM Press, Washington DC, USA. p. 53-70. https://doi.org/10.1128/9781555815936.ch4
Kamber, U., Gokce, H.I., Elmalı, M. (2007). Clostridium perfringens and its toxins in minced meat from Kars, Turkey. Food Additives and Contaminants, 24(7), 673-678. https://doi.org/10.1080/02652030601186129
Kouassi, K.A., Dadie, A.T., N'Guessan, K.F., Dje, K.M., Loukou, Y.G. (2014). Clostridium perfringens and Clostridium difficile in cooked beef sold in Cote d'Ivoire and their antimicrobial susceptibility. Anaerobe, 28, 90-94. https://doi.org/10.1016/j.anaerobe.2014.05.012
Labbe, R.G., Juneja, V.K. (2017). Clostridium perfringens. In Foodborne Diseases (pp. 235-242). Academic Press. https://doi.org/10.1016/B978-0-12-385007-2.00010-3
McClane, B.A., Robertson, S.L., Li, J. (2012). Clostridium perfringens. In: Food Microbiology: Fundamentals and Frontiers, M.P. Doyle, R.L. Buchanan (Eds.), American Society for Microbiology Press, p.465-489. https://doi.org/10.1128/9781555818463.ch18
Mead, P.S., Slutsker, L., Dietz, V., McCaig, L.F., Bresee, J.S., Shapiro, C., Griffin, P.M., Tauxe, R.V. (1999). Food-related illness and death in the United States. Emerging Infectious Diseases, 5, 607-625. https://doi.org/10.3201/eid0505.990502
Mellou, K., Kyritsi, M., Chrysostomou, A., Sideroglou, T., Georgakopoulou, T., Hadjichristodoulou, C. (2019). Clostridium perfringens foodborne outbreak during an athletic event in Northern Greece, June 2019. International Journal of Environmental Research and Public Health, 16(20), 3967. https://doi.org/10.3390/ijerph16203967
Pafumi, J. (1986). Assessment of the microbiological quality of spices and herbs. Journal of Food Protection, 49(12), 958-963. https://doi.org/10.4315/0362-028X-49.12.958
Rhodehamel, J., Harmon, S. (1998). Clostridium perfringens, Bacteriological Analytical Manual, 8th Edition, Revision A, Chapter 16.
Shaltout, F.A., Osman, I.M., Kamel, E.A., Abd-Alla, A.K. (2017). Isolation of Clostridium perfringens from Meat Samples Obtained from the University Students’ Hostel. EC Nutrition, 9(3), 142-150.
Taormina, P.J., Bartholomew, G.W., Dorsa, W.J. (2003). Incidence of Clostridium perfringens in commercially produced cured raw meat product mixtures and behavior in cooked products during chilling and refrigerated storage. Journal of Food Protection, 66(1), 72-81. https://doi.org/10.4315/0362-028X-66.1.72
Vazgecer, B., Ulu, H., Oztan, A. (2004). Microbiological and chemical qualities of chicken döner kebab retailed on the Turkish restaurants. Food Control, 15(4), 261-264. https://doi.org/10.1016/S0956-7135(03)00065-3
Wen, Q., McClane, B.A. (2004). Detection of enterotoxigenic Clostridium perfringens type A isolates in American retail foods. Applied and Environmental Microbiology, 70(5), 2685-2691. https://doi.org/10.1128/AEM.70.5.2685-2691.2004
Yıldırım, Z., Ceylan, Ş., Öncül, N. (2015). Tokat piyasasında satışa sunulan tavuk etlerinin mikrobiyolojik kalitesinin belirlenmesi. Akademik Gıda, 13(4), 304-316.

Year 2021, , 172 - 178, 01.07.2021

Serap Coşansu Akdemir , Şeyma Ersöz

https://doi.org/10.3153/FH21018

Abstract

Project Number

BAP-2012-01-16-009

References

Clostridium perfringens by using chromogenic and fluorogenic substrates. Applied Environmental Microbiology, 67(9), 4382-4384. https://doi.org/10.1128/AEM.67.9.4382-4384.2001
Andersson, A., Ronner, U., Granum, P.E. (1995). What problems does the food industry have with the spore-forming pathogens Bacillus cereus and Clostridium perfringens? International Journal of Food Microbiology, 28, 145-155. https://doi.org/10.1016/0168-1605(95)00053-4
Anonymous (1999). Microbiology of food and animal feeding stuffs-Horizontal method for the enumeration of Clostridium perfringens. Colonies count technique (ISO 7937: 1997 Modified). European Standard (EN 13401).
Anonymous (2011). Türk Gıda Kodeksi Mikrobiyolojik Kriterler Yönetmeliği Retrieved from https://www.resmigazete.gov.tr/eskiler/2011/12/20111229M3-6.htm (Accessed 01.06.2020).
Apaydin, G., Ceylan, Z.G., Kaya, M. (2003). Değişik firmalara ait salamların bazı mikrobiyolojik ve kimyasal özellikleri. Turkish Journal of Veterinary and Animal Science, 27, 1299-1303.
Araujo, M., Sueiro, R.A., Gómez, M.J., Garrido, M.J. (2001). Evaluation of fluorogenic TSC agar for recovering Clostridium perfringens in groundwater samples. Water Science and Technology, 43(12), 201-204. https://doi.org/10.2166/wst.2001.0738
Başkaya, R., Karaca, T., Sevinç, İ., Çakmak, Ö., Yildiz, A., Yörük, M. (2004). İstanbul'da Satışa Sunulan Hazır Kıymaların Histolojik, Mikrobiyolojik ve Serolojik Kalitesi. Yüzüncü Yıl Üniversitesi Veteriner Fakültesi Dergisi, 15(1), 41-46.
Bostan, K., Yılmaz, F., Muratoğlu, K., Aydın, A. (2011). Pişmiş döner kebaplarda mikrobiyolojik kalite ve mikrobiyel gelişim üzerine bir araştırma. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 17(5), 781-786. https://doi.org/10.9775/kvfd.2011.4438
Brown, K.L. (2000). Control of bacterial spores. British Medical Bulletin, 56 (1), 158-171. https://doi.org/10.1258/0007142001902860 Brynestad, S., Granum, P.E. (2002). Clostridium perfringens and foodborne infections. International Journal of Food Microbiology, 74(3), 195-202. https://doi.org/10.1016/S0168-1605(01)00680-8
Byrne, B., Dunne, G., Bolton, D.J. (2006). Thermal inactivation of Bacillus cereus and Clostridium perfringens vegetative cells and spores in pork luncheon roll. Food Microbiology, 23(8), 803-808. https://doi.org/10.1016/j.fm.2006.02.002
Çakmak, Ö., Ormancı, F.S.B., Tayfur, M., Erol, İ. (2006). Presence and contamination level of Clostridium perfringens in raw frozen ground poultry and poultry burgers. Turkish Journal of Veterinary and Animal Sciences, 30(1), 101-105.
De Boer, E., Spiegelenberg, W.M., Janssen, F.W. (1985). Microbiology of spices and herbs. Antonie van Leeuwenhoek, 51(4), 435-438. https://doi.org/10.1007/BF02275058
EFSA-ECDC (European Food Safety Authority-European Centre for Disease Prevention and Control), (2015). The European Union summary report on trends and sources of zoonoses, zoonotic agents, and food-borne outbreaks in 2014. EFSA Journal, 13(4329), 191. https://doi.org/10.2903/j.efsa.2015.4329
Elmalı, M., Ulukanlı, Z., Yaman, H. (2005). Microbiological quality of emulsified type meat products (salami-frankfurter sausage) marketed in Kars. Journal of Faculty of Veterinary Medicine, Erciyes University, 2(1), 15-21.
Fischer, M., Zhu, S., de Ree, E. (2012). Culture media for the detection and enumeration of clostridia in food. In: Handbook of Culture Media for Food and Water Microbiology, J.E.L Corry, G.D.W. Curtis, R.M. Baird (Eds.), Royal Society of Chemistry Publishing, p. 66-89. https://doi.org/10.1039/9781847551450-00066
Garcia, S., Heredia, N. (2011). Clostridium perfringens: a dynamic foodborne pathogen. Food and Bioprocess Technology, 4(4), 624-630. https://doi.org/10.1007/s11947-009-0182-2
García, S., Vidal, J.E., Heredia, N., Juneja, V.K. (2019). Clostridium perfringens. In: Food Microbiology: Fundamentals And Frontiers, Michael P. Doyle, Francisco Diez-Gonzalez, Colin Hill (Editors), 5th Edition, ASM Books, pp. 513-540. https://doi.org/10.1128/9781555819972.ch19
Guran, H.S., Oksuztepe, G. (2013). Detection and typing of Clostridium perfringens from retail chicken meat parts. Letters in Applied Microbiology, 57(1), 77-82. https://doi.org/10.1111/lam.12088
Guran, H.S., Vural, A., Erkan, M.E. (2014). The prevalence and molecular typing of Clostridium perfringens in ground beef and sheep meats. Journal für Verbraucherschutz und Lebensmittelsicherheit, 9(2), 121-128. https://doi.org/10.1007/s00003-014-0866-z
Immerseel, F.V., Buck, J.D., Pasmans, F., Huyghebaert, G., Haesebrouck, F., Ducatelle, R. (2004). Clostridium perfringens in poultry: an emerging threat for animal and public health. Avian pathology, 33(6), 537-549. https://doi.org/10.1080/03079450400013162 Jaloustre, S., Guillier, L., Poumeyrol, G., Morelli, E., Delignette-Muller, M.L. (2013). Efficiency of a reheating step to inactivate Clostridium perfringens vegetative cells: How to measure it? Food Control, 29(2), 422-428. https://doi.org/10.1016/j.foodcont.2012.07.003
Juneja, V.K., Novak, J.S., Labbe, R.J. (2010). Clostridium perfringens. In: Pathogens and Toxins in Foods: Challenges and Interventions, V.K. Juneja, J.N. Sofos (Eds.), ASM Press, Washington DC, USA. p. 53-70. https://doi.org/10.1128/9781555815936.ch4
Kamber, U., Gokce, H.I., Elmalı, M. (2007). Clostridium perfringens and its toxins in minced meat from Kars, Turkey. Food Additives and Contaminants, 24(7), 673-678. https://doi.org/10.1080/02652030601186129
Kouassi, K.A., Dadie, A.T., N'Guessan, K.F., Dje, K.M., Loukou, Y.G. (2014). Clostridium perfringens and Clostridium difficile in cooked beef sold in Cote d'Ivoire and their antimicrobial susceptibility. Anaerobe, 28, 90-94. https://doi.org/10.1016/j.anaerobe.2014.05.012
Labbe, R.G., Juneja, V.K. (2017). Clostridium perfringens. In Foodborne Diseases (pp. 235-242). Academic Press. https://doi.org/10.1016/B978-0-12-385007-2.00010-3
McClane, B.A., Robertson, S.L., Li, J. (2012). Clostridium perfringens. In: Food Microbiology: Fundamentals and Frontiers, M.P. Doyle, R.L. Buchanan (Eds.), American Society for Microbiology Press, p.465-489. https://doi.org/10.1128/9781555818463.ch18
Mead, P.S., Slutsker, L., Dietz, V., McCaig, L.F., Bresee, J.S., Shapiro, C., Griffin, P.M., Tauxe, R.V. (1999). Food-related illness and death in the United States. Emerging Infectious Diseases, 5, 607-625. https://doi.org/10.3201/eid0505.990502
Mellou, K., Kyritsi, M., Chrysostomou, A., Sideroglou, T., Georgakopoulou, T., Hadjichristodoulou, C. (2019). Clostridium perfringens foodborne outbreak during an athletic event in Northern Greece, June 2019. International Journal of Environmental Research and Public Health, 16(20), 3967. https://doi.org/10.3390/ijerph16203967
Pafumi, J. (1986). Assessment of the microbiological quality of spices and herbs. Journal of Food Protection, 49(12), 958-963. https://doi.org/10.4315/0362-028X-49.12.958
Rhodehamel, J., Harmon, S. (1998). Clostridium perfringens, Bacteriological Analytical Manual, 8th Edition, Revision A, Chapter 16.
Shaltout, F.A., Osman, I.M., Kamel, E.A., Abd-Alla, A.K. (2017). Isolation of Clostridium perfringens from Meat Samples Obtained from the University Students’ Hostel. EC Nutrition, 9(3), 142-150.
Taormina, P.J., Bartholomew, G.W., Dorsa, W.J. (2003). Incidence of Clostridium perfringens in commercially produced cured raw meat product mixtures and behavior in cooked products during chilling and refrigerated storage. Journal of Food Protection, 66(1), 72-81. https://doi.org/10.4315/0362-028X-66.1.72
Vazgecer, B., Ulu, H., Oztan, A. (2004). Microbiological and chemical qualities of chicken döner kebab retailed on the Turkish restaurants. Food Control, 15(4), 261-264. https://doi.org/10.1016/S0956-7135(03)00065-3
Wen, Q., McClane, B.A. (2004). Detection of enterotoxigenic Clostridium perfringens type A isolates in American retail foods. Applied and Environmental Microbiology, 70(5), 2685-2691. https://doi.org/10.1128/AEM.70.5.2685-2691.2004
Yıldırım, Z., Ceylan, Ş., Öncül, N. (2015). Tokat piyasasında satışa sunulan tavuk etlerinin mikrobiyolojik kalitesinin belirlenmesi. Akademik Gıda, 13(4), 304-316.

There are 34 citations in total.

Details

Primary Language	English
Subjects	Food Engineering
Journal Section	Research Articles
Authors	Serap Coşansu Akdemir 0000-0003-2875-1335 Şeyma Ersöz 0000-0001-7481-1170
Project Number	BAP-2012-01-16-009
Publication Date	July 1, 2021
Submission Date	June 12, 2020
Published in Issue	Year 2021

Cite

APA	Coşansu Akdemir, S., & Ersöz, Ş. (2021). Incidence and contamination level of Clostridium perfringens in meat and meat products sold in Sakarya province of Turkey. Food and Health, 7(3), 172-178. https://doi.org/10.3153/FH21018

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