Research Article
BibTex RIS Cite

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

Year 2021, Volume: 7 Issue: 3, 172 - 178, 01.07.2021
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.

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, Volume: 7 Issue: 3, 172 - 178, 01.07.2021
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 2021Volume: 7 Issue: 3

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

16339

Journal is licensed under a

CreativeCommons Attribtion-ShareAlike 4.0 International Licence  14627 1331027042
Diamond Open Access refers to a scholarly publication model in which journals and platforms do not charge fees to either authors or readers.

Open Access Statement:

This is an open access journal which means that all content is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles, or use them for any other lawful purpose, without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of open access.

Archiving Policy:

27222

Archiving is done according to ULAKBİM "DergiPark" publication policy (LOCKSS).