Prevalence of contamination of sandwiches with pathogenic microorganisms and antibiotic resistance of isolates in Kermanshah city, Iran.
Subject Areas :
Food Hygiene
Mohammad amin Heidarzadi
1
,
Nadia Ayazi
2
,
Najmeh Vahed dehkordi
3
,
Mohsen Karami
4
,
Sayedeh Khadijeh Ahmadi
5
,
Seyed Erfan Hoseini nasab
6
1 - Ph.D. student in food hygiene, Faculty of Veterinary Medicine, Shahrekord University, Shahrekord, Iran
2 - -Graduated in Microbiology, Department of Biology, Sanandaj Branch, Islamic Azad University, Sanandaj, Iran
3 - PhD student in food hygiene, Shahrekord Branch, Islamic Azad University, Shahrekord, Iran
4 - Graduated in Microbiology, Department of Biology, Sanandaj Branch, Islamic Azad University, Sanandaj, Iran
5 - Ph.D. student in food hygiene, Faculty of Veterinary Medicine, Shahrekord University, Shahrekord, Iran
6 - Graduated in Food Hygiene, Department of Food Hygiene, Shahrekord Branch, Islamic Azad University, Shahrekord, Iran
Received: 2023-08-19
Accepted : 2023-12-09
Published : 2023-09-23
Keywords:
Antibiotic resistance,
food,
Sandwich,
Pathogenic microorganisms,
Abstract :
Meat products are one of the suppliers of human food needs, and like other food products, they have special nutritional values. If these products are contaminated with pathogenic microorganisms, they cause gastroenteritis in humans. The purpose of the present study is the prevalence of contamination of sandwiches with pathogenic microorganisms and the antibiotic resistance of isolates in Kermanshah, Iran. A number of 210 samples, including ready-made sandwiches, sauces and salads, were taken from the supply centers of these products and transferred to the laboratory of Kermanshah University of Medical Sciences and according to the standard instructions, to identify the microorganisms of Escherichia coli, Salmonella, Clostridium, coliform, Mold and yeast, Bacillus cereus, Staphylococcus aureus and Yersinia enterocolitica were evaluated. Antibiotic resistance of isolates was evaluated by disk diffusion method. The results showed that the highest contamination was related to mold and yeast (83.64 percent), Staphylococcus aureus (42.71 percent), Salmonella (32.1 percent), and Escherichia coli (27.8 percent). Clostridium perfringens (13.3), Yersinia enterocolitica (5.25) and Bacillus cereus (3.94). Also, the results showed that the most contaminated food items are salad (43.81 percent), sauce (42.38 percent), traditional hamburger (36.48 percent), samosa (32.85 percent), falafel (24.28 percent), respectively. percent), sausage (24.12 percent) and sausage (13.9 percent). The high and alarming prevalence of bacterial contamination as well as the antibiotic resistance of isolates in sandwiches is a warning to apply accurate and quick health monitoring to these products.
References:
Arnedo-Pena, A., Sabater-Vidal, S., Herrera-León, S., Bellido-Blasco, J.B., Silvestre-Silvestre, E., Meseguer-Ferrer, et al. (2016). An outbreak of monophasic and biphasic Salmonella Typhimurium, and Salmonella Derby associated with the consumption of dried pork sausage in Castellon (Spain). Enfermedades infecciosas y microbiologia clinica, 34 (9): 544-550.
Ayazi, N., Heidarzadi, M.A., Kohneh Poushi, M., Karami, M., Sabzibalkhkanlo, A. and Gorgin Karaji, K. (2022). Investigating the Amount of Microbial Contamination of Pasteurized Milk in Kermanshah City with Coliform and the Total Number of Bacteria. Journal of Alternative Veterinary Medicine, 5 (12): 702-709.
Bahlinger, E., Dorn-In, S., Beindorf, P.-M., Mang, S., Kaltner, F., Gottschalk, C., et al. (2021). Development of two specific multiplex qPCRs to determine amounts of Pseudomonas, Enterobacteriaceae, Brochothrix thermosphacta and Staphylococcus in meat and heat-treated meat products. International Journal of Food Microbiology, 337 (16): 1-10.
Baldwin, M.R., Tepp, W.H., Pier, C.L., Bradshaw, M., Ho, M., Wilson, B.A., et al. (2005). Characterization of the antibody response to the receptor binding domain of botulinum neurotoxin serotypes A and E. Infection and immunity, 73 (10): 6998-7005.
Broner, S., Torner, N., Dominguez, A., Martinez, A. and Godoy, P. (2010). The Working Group for the Study of Outbreaks of Acute Gastroenteritis in Cataloniathe. Sociodemographic inequalities and outbreaks of foodborne diseases: An ecologic study. Food Control, 21 (6): 947-951.
Bucher, M., Meyer, C., Grötzbach, B., Wacheck, S., Stolle, A. and Fredriksson-Ahomaa, M. (2008). Epidemiological data on pathogenic Yersinia enterocolitica in Southern Germany during 2000–2006. Foodborne pathogens and disease, 5 (3): 273-280.
Cavalin, P.B.B., Sarmiento, J.J.P., Kobayashi, R.K.T., Nakazato, G., Ocaña, A.N. and Oliveira, T.C.R.M. (2018). Detection of Salmonella spp. and diarrheagenic Escherichia coli in fresh pork sausages. Semina: Ciências Agrárias, 39 (4): 1533-1545.
Dan, S.-D., Mihaiu, M., Reget, O. and Tăbăran, A. (2019). Microbiological risk assessment represented by the psychrotrophic microflora from some meat products. Journalof Applied Life Sciences and Environment, 62 (4): 296-303.
Ed-Dra, A., Filali, F.R., Bouymajane, A., Benhallam, F., El Allaoui, A., Chaiba, A., et al. (2018). Antibiotic susceptibility profile of Staphylococcus aureus isolated from sausages in Meknes, Morocco. Veterinary World, 11 (10): 1459–1465.
F, n., E, R., E, s. (2015). Prevalence of Staphylococcus aureus in meat and meat products. Journal of Food Microbiology, 1(1): 41-46.
Gill, C. (1988). Microbiology of edible meat by-products. Advances in meat research (USA).
Guo, P., Zhang, K., Ma, X. and He, P., (2020). Clostridium species as probiotics: potentials and challenges. Journal of Animal Science and Biotechnology, 11(1): 1-10.
Heidarzadi, M.A., Rahnama, M., Alipoureskandani, M., Saadati, D. and Afsharimoghadam, A. (2021). Salmonella and Escherichia coli contamination in samosas presented in Sistan and Baluchestan province and antibiotic resistance of isolates. Journal of Food Hygiene, 11 (2): 81-90. [In persian]
Huong, B.T.M., Mahmud, Z.H., Neogi, S.B., Kassu, A., Van Nhien, N., Mohammad, A., et al. (2010). Toxigenicity and genetic diversity of Staphylococcus aureus isolated from Vietnamese ready-to-eat foods. Food Control, 21 (5): 166-171.
Jalali, M., Abedi, D., Pourbakhsh, S.A. and Ghoukasin, K. (2008). Prevalence of salmonella spp. in raw and cooked foods in Isfahan‐Iran. Journal of Food Safety, 28 (3): 442-452.
Juneja, V.K. and Sofos, J.N. (2009). Pathogens and toxins in foods: challenges and interventions. Wiley Online Library.
Lambertz, S.T., Nilsson, C., Hallanvuo, S. and Lindblad, M. (2008). Real-time PCR method for detection of pathogenic Yersinia enterocolitica in food. Applied and Environmental Microbiology, 74 (19): 6060-6067.
Lee, T.-S., Lee, S.-W., Seok, W.-S., Yoo, M.-Y., Yoon, J.-W., Park, et al. (2004). Prevalence, antibiotic susceptibility, and virulence factors of Yersinia enterocolitica and related species from ready-to-eat vegetables available in Korea. Journal of Food Protection, 67 (6): 1123-1127.
Liang, W., Wang, F., Li, T., Kang, J., Hao, Y., Shi, S., et al. (2022). Analysis of Dominant Spoilage Bacteria in Beijing Sausages, 4(1): 84-88.
Lindqvist, R. and Lindblad, M., (2009). Inactivation of Escherichia coli, Listeria monocytogenes and Yersinia enterocolitica in fermented sausages during maturation/storage. International Journal of Food Microbiology, 129 (1): 59-67.
Madahi, H., Rahimi, E. and Jalali, M. (2015). Detection of enterotoxin genes of staphylococcus aureus isolates from chicken nugget in Esfahan province by PCR technique. Biological Journal of Microorganism, 4 (13): 25-34.
Muratoglu, K., Akkaya, E., Hampikyan, H., Bingol, E.B., Cetin, O. and Colak, H. (2020). Detection, characterization and antibiotic susceptibility of clostridioides (Clostridium) difficile in meat products. Food Science of Animal Resources, 40 (4): 578-587.
Nur, D.F.A., Yulistiani, R., Rosida, D.F. and Raharjo, D. (2022). Occurrences Salmonella sp. and Escherichia Coli in Bulk and Packaged Chicken Sausages in Surabaya, Indonesia. Asian Journal of Applied Research for Community Development and Empowerment, 6 (2): 35-41.
Organization, W.H. (2011). Enterohaemorrhagic Escherichia coli in raw beef and beef products: approaches for the provision of scientific advice: meeting report. World Health Organization.
Pérez-Rodríguez, F., Castro, R., Posada-Izquierdo, G., Valero, A., Carrasco, E., García-Gimeno, R., et al. (2010). Evaluation of hygiene practices and microbiological quality of cooked meat products during slicing and handling at retail. Meat Science, 86 (2): 479-485.
Pernu, N., Keto-Timonen, R., Lindström, M. and Korkeala, H. (2020). High prevalence of Clostridium botulinum in vegetarian sausages. Food Microbiology, 91 (1): 2-5.
Pishadast, S., Rahnama, M., Alipour Eskandani, M., Saadati, D., Noori Jangi, A. and Heidarzadi, M., (2021). Study of antimicrobial effect of nisin and alcoholic extract of garlic on the activity of staphylococcus aureus ATCC 1113 in Tilapia minced meat during storage at 4 °C. Journal of Food Hygiene, 11(3): 37-47. [In Persian]
Redondo-Solano, M., Cordero-Calderón, V., Araya-Morice, A. (2023). Calidad microbiológica del chorizo crudo expendido en el Gran Área Metropolitana de Costa Rica. Agronomía Mesoamericana, 34 (1): 1-12.
Sabala, R.F., Usui, M., Tamura, Y., Abd-Elghany, S.M., Sallam, K.I. and Elgazzar, M.M. (2021). Prevalence of colistin-resistant Escherichia coli harbouring mcr-1 in raw beef and ready-to-eat beef products in Egypt. Food Control, 119 (14): 107-136.
Scannell, A., Hill, C., Buckley, D. and Arendt, E. (1997). Determination of the influence of organic acids and nisin on shelf‐life and microbiologicalsafety aspects of fresh pork sausage. Journal of Applied Microbiology, 83(4): 407-412.
Seakamela, E.M., Diseko, L., Malatji, D., Makhado, L., Motau, M., Jambwa, K., et al. (2022). Characterisation and antibiotic resistance of Yersinia enterocolitica from various meat categories, South Africa. Onderstepoort Journal of Veterinary Research, 89 (1): 1-11.
Sepidarkish, M. and Ghane, M. (2014). Isolation, identification and the presence of enterotoxin A gene in Staphylococcus aureus from meat products. Journal of Food Hygiene, 4 (2): 47-52. [In persian]
Shamloo, E., Hosseini, H., Moghadam, Z.A., Larsen, M.H., Haslberger, A. and Alebouyeh, M. (2019). Importance of Listeria monocytogenes in food safety: a review of its prevalence, detection, and antibiotic resistance. Iranian Journal of Veterinary Research, 20 (4): 241-250.
Shekarforoush, S., Kiaie, S., Karim, G., Razavi Rohani, S., Rokni, N., Abbasvali, M., (2013). Study on the overview on foodborne bacteria in food with animal origin in Iran; Part four: Poultry and egg. Journal of Food Hygiene, 3 (1): 45-64. [In persian]
Song, M., Bai, Y., Xu, J., Carter, M.Q., Shi, C. and Shi, X. (2015). Genetic diversity and virulence potential of Staphylococcus aureus isolates from raw and processed food commodities in Shanghai. International Journal of Food Microbiology, 195 (1): 1-8.
Tominaga, T. (2019). Rapid detection of coliform bacteria using a lateral flow test strip assay. Journal of Microbiological Methods, 160 (1): 29-35.
Trimoulinard, A., Beral, M., Henry, I., Atiana, L., Porphyre, V. and Tessier, C. (2017). Contamination by Salmonella spp., Campylobacter spp. and Listeria spp. of most popular chicken-and pork-sausages sold in Reunion Island. International Journal of Food Microbiology, 250 (5): 68-74.
Vidic, J., Chaix, C., Manzano, M. and Heyndrickx, M. (2020). Food sensing: detection of Bacillus cereus spores in dairy products. Biosensors, 10 (3): 3-15.
Xu, L., Ntakatsane, M., Wang, L., Meng, X., Sun, W., Bi, Y., et al. (2021). Improved sensitive fluorescent/visible dual detection count plate for mold and yeast in food. Food Control, 128 (4) 108-118.
Zeleny, R., Emteborg, H., Charoud-Got, J., Schimmel, H., Nia, Y., Mutel, I., et al. (2015). Development of a reference material for Staphylococcus aureus enterotoxin A in cheese: feasibility study, processing, homogeneity and stability assessment. Food Chemistry, 168 (10): 241-246.
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Arnedo-Pena, A., Sabater-Vidal, S., Herrera-León, S., Bellido-Blasco, J.B., Silvestre-Silvestre, E., Meseguer-Ferrer, et al. (2016). An outbreak of monophasic and biphasic Salmonella Typhimurium, and Salmonella Derby associated with the consumption of dried pork sausage in Castellon (Spain). Enfermedades infecciosas y microbiologia clinica, 34 (9): 544-550.
Ayazi, N., Heidarzadi, M.A., Kohneh Poushi, M., Karami, M., Sabzibalkhkanlo, A. and Gorgin Karaji, K. (2022). Investigating the Amount of Microbial Contamination of Pasteurized Milk in Kermanshah City with Coliform and the Total Number of Bacteria. Journal of Alternative Veterinary Medicine, 5 (12): 702-709.
Bahlinger, E., Dorn-In, S., Beindorf, P.-M., Mang, S., Kaltner, F., Gottschalk, C., et al. (2021). Development of two specific multiplex qPCRs to determine amounts of Pseudomonas, Enterobacteriaceae, Brochothrix thermosphacta and Staphylococcus in meat and heat-treated meat products. International Journal of Food Microbiology, 337 (16): 1-10.
Baldwin, M.R., Tepp, W.H., Pier, C.L., Bradshaw, M., Ho, M., Wilson, B.A., et al. (2005). Characterization of the antibody response to the receptor binding domain of botulinum neurotoxin serotypes A and E. Infection and immunity, 73 (10): 6998-7005.
Broner, S., Torner, N., Dominguez, A., Martinez, A. and Godoy, P. (2010). The Working Group for the Study of Outbreaks of Acute Gastroenteritis in Cataloniathe. Sociodemographic inequalities and outbreaks of foodborne diseases: An ecologic study. Food Control, 21 (6): 947-951.
Bucher, M., Meyer, C., Grötzbach, B., Wacheck, S., Stolle, A. and Fredriksson-Ahomaa, M. (2008). Epidemiological data on pathogenic Yersinia enterocolitica in Southern Germany during 2000–2006. Foodborne pathogens and disease, 5 (3): 273-280.
Cavalin, P.B.B., Sarmiento, J.J.P., Kobayashi, R.K.T., Nakazato, G., Ocaña, A.N. and Oliveira, T.C.R.M. (2018). Detection of Salmonella spp. and diarrheagenic Escherichia coli in fresh pork sausages. Semina: Ciências Agrárias, 39 (4): 1533-1545.
Dan, S.-D., Mihaiu, M., Reget, O. and Tăbăran, A. (2019). Microbiological risk assessment represented by the psychrotrophic microflora from some meat products. Journalof Applied Life Sciences and Environment, 62 (4): 296-303.
Ed-Dra, A., Filali, F.R., Bouymajane, A., Benhallam, F., El Allaoui, A., Chaiba, A., et al. (2018). Antibiotic susceptibility profile of Staphylococcus aureus isolated from sausages in Meknes, Morocco. Veterinary World, 11 (10): 1459–1465.
F, n., E, R., E, s. (2015). Prevalence of Staphylococcus aureus in meat and meat products. Journal of Food Microbiology, 1(1): 41-46.
Gill, C. (1988). Microbiology of edible meat by-products. Advances in meat research (USA).
Guo, P., Zhang, K., Ma, X. and He, P., (2020). Clostridium species as probiotics: potentials and challenges. Journal of Animal Science and Biotechnology, 11(1): 1-10.
Heidarzadi, M.A., Rahnama, M., Alipoureskandani, M., Saadati, D. and Afsharimoghadam, A. (2021). Salmonella and Escherichia coli contamination in samosas presented in Sistan and Baluchestan province and antibiotic resistance of isolates. Journal of Food Hygiene, 11 (2): 81-90. [In persian]
Huong, B.T.M., Mahmud, Z.H., Neogi, S.B., Kassu, A., Van Nhien, N., Mohammad, A., et al. (2010). Toxigenicity and genetic diversity of Staphylococcus aureus isolated from Vietnamese ready-to-eat foods. Food Control, 21 (5): 166-171.
Jalali, M., Abedi, D., Pourbakhsh, S.A. and Ghoukasin, K. (2008). Prevalence of salmonella spp. in raw and cooked foods in Isfahan‐Iran. Journal of Food Safety, 28 (3): 442-452.
Juneja, V.K. and Sofos, J.N. (2009). Pathogens and toxins in foods: challenges and interventions. Wiley Online Library.
Lambertz, S.T., Nilsson, C., Hallanvuo, S. and Lindblad, M. (2008). Real-time PCR method for detection of pathogenic Yersinia enterocolitica in food. Applied and Environmental Microbiology, 74 (19): 6060-6067.
Lee, T.-S., Lee, S.-W., Seok, W.-S., Yoo, M.-Y., Yoon, J.-W., Park, et al. (2004). Prevalence, antibiotic susceptibility, and virulence factors of Yersinia enterocolitica and related species from ready-to-eat vegetables available in Korea. Journal of Food Protection, 67 (6): 1123-1127.
Liang, W., Wang, F., Li, T., Kang, J., Hao, Y., Shi, S., et al. (2022). Analysis of Dominant Spoilage Bacteria in Beijing Sausages, 4(1): 84-88.
Lindqvist, R. and Lindblad, M., (2009). Inactivation of Escherichia coli, Listeria monocytogenes and Yersinia enterocolitica in fermented sausages during maturation/storage. International Journal of Food Microbiology, 129 (1): 59-67.
Madahi, H., Rahimi, E. and Jalali, M. (2015). Detection of enterotoxin genes of staphylococcus aureus isolates from chicken nugget in Esfahan province by PCR technique. Biological Journal of Microorganism, 4 (13): 25-34.
Muratoglu, K., Akkaya, E., Hampikyan, H., Bingol, E.B., Cetin, O. and Colak, H. (2020). Detection, characterization and antibiotic susceptibility of clostridioides (Clostridium) difficile in meat products. Food Science of Animal Resources, 40 (4): 578-587.
Nur, D.F.A., Yulistiani, R., Rosida, D.F. and Raharjo, D. (2022). Occurrences Salmonella sp. and Escherichia Coli in Bulk and Packaged Chicken Sausages in Surabaya, Indonesia. Asian Journal of Applied Research for Community Development and Empowerment, 6 (2): 35-41.
Organization, W.H. (2011). Enterohaemorrhagic Escherichia coli in raw beef and beef products: approaches for the provision of scientific advice: meeting report. World Health Organization.
Pérez-Rodríguez, F., Castro, R., Posada-Izquierdo, G., Valero, A., Carrasco, E., García-Gimeno, R., et al. (2010). Evaluation of hygiene practices and microbiological quality of cooked meat products during slicing and handling at retail. Meat Science, 86 (2): 479-485.
Pernu, N., Keto-Timonen, R., Lindström, M. and Korkeala, H. (2020). High prevalence of Clostridium botulinum in vegetarian sausages. Food Microbiology, 91 (1): 2-5.
Pishadast, S., Rahnama, M., Alipour Eskandani, M., Saadati, D., Noori Jangi, A. and Heidarzadi, M., (2021). Study of antimicrobial effect of nisin and alcoholic extract of garlic on the activity of staphylococcus aureus ATCC 1113 in Tilapia minced meat during storage at 4 °C. Journal of Food Hygiene, 11(3): 37-47. [In Persian]
Redondo-Solano, M., Cordero-Calderón, V., Araya-Morice, A. (2023). Calidad microbiológica del chorizo crudo expendido en el Gran Área Metropolitana de Costa Rica. Agronomía Mesoamericana, 34 (1): 1-12.
Sabala, R.F., Usui, M., Tamura, Y., Abd-Elghany, S.M., Sallam, K.I. and Elgazzar, M.M. (2021). Prevalence of colistin-resistant Escherichia coli harbouring mcr-1 in raw beef and ready-to-eat beef products in Egypt. Food Control, 119 (14): 107-136.
Scannell, A., Hill, C., Buckley, D. and Arendt, E. (1997). Determination of the influence of organic acids and nisin on shelf‐life and microbiologicalsafety aspects of fresh pork sausage. Journal of Applied Microbiology, 83(4): 407-412.
Seakamela, E.M., Diseko, L., Malatji, D., Makhado, L., Motau, M., Jambwa, K., et al. (2022). Characterisation and antibiotic resistance of Yersinia enterocolitica from various meat categories, South Africa. Onderstepoort Journal of Veterinary Research, 89 (1): 1-11.
Sepidarkish, M. and Ghane, M. (2014). Isolation, identification and the presence of enterotoxin A gene in Staphylococcus aureus from meat products. Journal of Food Hygiene, 4 (2): 47-52. [In persian]
Shamloo, E., Hosseini, H., Moghadam, Z.A., Larsen, M.H., Haslberger, A. and Alebouyeh, M. (2019). Importance of Listeria monocytogenes in food safety: a review of its prevalence, detection, and antibiotic resistance. Iranian Journal of Veterinary Research, 20 (4): 241-250.
Shekarforoush, S., Kiaie, S., Karim, G., Razavi Rohani, S., Rokni, N., Abbasvali, M., (2013). Study on the overview on foodborne bacteria in food with animal origin in Iran; Part four: Poultry and egg. Journal of Food Hygiene, 3 (1): 45-64. [In persian]
Song, M., Bai, Y., Xu, J., Carter, M.Q., Shi, C. and Shi, X. (2015). Genetic diversity and virulence potential of Staphylococcus aureus isolates from raw and processed food commodities in Shanghai. International Journal of Food Microbiology, 195 (1): 1-8.
Tominaga, T. (2019). Rapid detection of coliform bacteria using a lateral flow test strip assay. Journal of Microbiological Methods, 160 (1): 29-35.
Trimoulinard, A., Beral, M., Henry, I., Atiana, L., Porphyre, V. and Tessier, C. (2017). Contamination by Salmonella spp., Campylobacter spp. and Listeria spp. of most popular chicken-and pork-sausages sold in Reunion Island. International Journal of Food Microbiology, 250 (5): 68-74.
Vidic, J., Chaix, C., Manzano, M. and Heyndrickx, M. (2020). Food sensing: detection of Bacillus cereus spores in dairy products. Biosensors, 10 (3): 3-15.
Xu, L., Ntakatsane, M., Wang, L., Meng, X., Sun, W., Bi, Y., et al. (2021). Improved sensitive fluorescent/visible dual detection count plate for mold and yeast in food. Food Control, 128 (4) 108-118.
Zeleny, R., Emteborg, H., Charoud-Got, J., Schimmel, H., Nia, Y., Mutel, I., et al. (2015). Development of a reference material for Staphylococcus aureus enterotoxin A in cheese: feasibility study, processing, homogeneity and stability assessment. Food Chemistry, 168 (10): 241-246.
