Prevalence and antibiotic susceptibility pattern of Yersinia enterocolitica in broiler meat and edible offal at Ardabil retails
Subject Areas :
Food Science and Technology
S. Shekari
1
,
M. Ghiami Rad
2
1 - M.Sc Graduate in Microbiology, Ahar Branch, Islamic Azad University, Ahar, Iran
2 - Assistant Professor in Microbiology, Ahar Branch, Islamic Azad University, Ahar, Iran
Received: 2016-12-13
Accepted : 2018-06-09
Published : 2018-12-22
Keywords:
Yersinia enterocolitica,
Poultry meat,
Edible offal,
Antibiotic susceptibility pattern,
Abstract :
Yersinia enterocolitica is one of the most important food-borne bacteria and it can cause yersiniosis. This study was conducted to investigate the occurrence of Y. enterocolitica in poultry meat and offal marketed in Ardabil, as well as to assess the antibiotic resistance pattern of the isolates. In this descriptive cross-sectional study, a total of 344 samples including 264 poultry meat and 80 offal samples were randomly obtained during the spring and summer of 2016. The samples were investigated for the presence of Y. enterocolitica using Iranian National Standard. Moreover, antibiotic susceptibility was examined by Kerby-Bauer method. Based on results, 22.34% of the poultry meat samples and 37.5% of the offals were contaminated with Y. enterocolitica. Antibiogram results revealed that 84.74% of the isolates were resistant to Ampicillin; in the cases of Cephalothin and Cephalexin, it was estimated at 69.49% and 64.4% of the isolates, respectively. However, resistance was observed for Chloramphenicol and Syprufluxasine. Regarding the high occurrence Y. enterocolitica in chicken meat and offal and the presence of antibiotic-resistant strains of this bacterium, the implementation of hygienic measures to reduce the occurrence of Y. enterocolitica in chicken meat and the prudent use of antibiotics in the poultry industry to prevent the spread of strains resistant to antibiotics and transferring them to the human food chain is essential.
References:
· Anju, P., Latha, C., Sunil, B. and Sethulekshmi, C. (2014). Antimicrobial resistance profile of Yersinia enterocolitica and Yersinia intermedia isolates from retail pork. International Journal of Current Microbiology and Applied Sciences .3(8): 231-234.
· Arnold, T., Neubauer, H., Nikolaou, K., Roesler, U. and Hensel, A. (2004). Identification of Yersinia enterocolitica in minced meat: A comparative analysis of API 20 E, Yersinia identification kit and 16S rRNA- based PCR method. Journal of Veterinary Medicine, 51: 23-26.
· Ashrafi, F. (2009). Study on percentage of Yersinia contamination in red and white meat in food markets in Shemiran. Journal of Microbiology Knowledge, 1-2: 49-52.
· Atobla, K., Karou, T.G., Dadie, A.T., Niamke, L.S. and Dje, K.M. (2012). Isolation and characterization of pathogenic Yersinia enterocolitica from pigs in Abidjan, Côte d'Ivoire. Journal of Applied Bioscinces, 50: 3540-3548.
· Baumgartner, A., Kuffer, M., Suter, D., Jemmi, T. and Rohner, P. (2007). Antimicrobial resistance of Yersinia enterocolitica strains from human patients, pigs and retail pork in Switzerland. International Journal of Food Microbiology, 115: 110-114.
· Bonardi, S., Paris, A., Bassi, L., Salmi, F., Bacci, C., Riboldi, E., et al. (2010). Detection, semiquantitative enumeration, and antimicrobial susceptibility of Yersinia enterocolitica in pork and chicken meats in Italy. Journal Food Protection, 73(10): 1785-1792.
· Bonardi, S., Brindania, F., Pizzina, G., Lucidia, L., D'Incaub, M., Liebanac, E., et al. (2002). Detection of Salmonella spp., Yersinia enterocolitica and verocytotoxin producing Escherichia coli O157 in pigs at slaughter in Italy. International Journal of Food Microbiology, 85: 101–110.
· Cox, N.A., Del Corral, F., Bailey, J.S., Shotts, E.B. and Papa, C.M. (1990). The presence of Yersinia enterocolitica and other Yersinia species on the carcasses of market broilers. Poultry Science, 69(3): 482-485.
· CSLI. (2012). Method for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard- 9th edition. Report No: M07-A9.
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· Logue, C.M., Sheridan, J.J., Wauters, G., McDowell, D.A. and Blair I.S. (1996) Yersinia spp. and numbers with particular reference to Yersinia enterocolitica bio/serotypes, occurring on Irish meat and meat products, and the influence of alkali treatment on their isolation. International Journal of Food Microbiology. 33: 851-854.
· Mahdavi, S., Farshchian, M.R., Amini, K., Abbasi, M., Ghiami Rad, M. and Ebadi, AR. (2012). Survey of Yersinia enterocolitica contamination in distributed broiler meats in Tabriz City, Iran. African Journal of Microbiology Research, 6(12): 3019-3023.
· Mielczarek, P., Bagłaj, M. (2004). Yersiniosis-rarely diagnosed disease of gastrointestinal system. Gastroenterologia Polska, 11: 69-74.
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· Ramirez, E.I., Vázquez-Salinas, C., Rodas-Suárez, O.R., Pedroche, F.F. (2000). Isolation of Yersinia from raw meat (pork and chicken) and precooked meat (porcine tongues and sausages) collected from commercial establishments in Mexico City. Journal Food Protection, 63(4): 542-544.
· Saberianpour, Sh., Tajbakhsh, E. and Doudi, M. (2012). Prevalence of Yersinia enterocolitica serotype O: 3 isolated from in Shahrekord. Iran Pejouhande, 17(3): 152-156. [In Persian]
· Saleh, I., Barbour, E., Shaib, H. and Harakeh, S. (2012). Highly Resistant Yersinia enterocolitica isolated from dairy based foods in Lebanon. The International Arabic Journal of Antimicrobial Agents. 2(1, 2): 1-6.
· Sharifin Yazdi, M.K., Soltan-Dallal, M.M., Zali M.R., Avadisians, S. and Bakhtiari, R. (2011). Incidence and antibiotic susceptibilities of Yersinia enterocolitica and other Yersinia species recovered from meat and chicken in Tehran, Iran: African Journal of Microbiology Research, 5(18): 2649-2653.
· Shakerian, A., Sharifzadeh, A., Aghanejad, P., Tajmiri Riahi, M. and Salehi, E. (2012). A preliminary study on prevalence of Yersinia enterocolitica in Beef, lamb and poultry at retails of Shahrekord. Journal of Food Hygiene, 2(1): 11-15. [In Persian]
· Siriken, B. (2004). The presence of Yersinia enterocolitica and other Yersinia species in ground beef in Aydin, Turkey. Turkish Journal of Veterinary Animal Science, 28: 489-495
· Soltan Dalal, M.M, Izadpour, F., Khalifegholi, M., Zareii, H., and Bakhtiari, R. (2006). The prevalence of Yersinia in chicken and red meat in southern of Tehran. Journal of School of Public Health and Institute of Public Health Research, 4(4): 49-56. [In Persian]
· TassinariAdos, R., Franco, BD. and Landgraf, M. (1994). Incidence of Yersinia spp. in food in Sao Paulo, Brazil. International Journal of Food Microbiology, 21(3): 263-270.
· Terentjeva, M. and Bērziņs, A. (2010). Prevalence and antimicrobial resistance of Yersinia enterocolitica and Yersinia pseudotuberculosis in slaughter pigs in Latvia. Journal Food Journal Food Protection .73(7):1335-1338.
· Van Damme. I., Berkvens, D., Botteldoorn, N., Dierick, K., Wits, J., Pochet, B. et al. (2013). Evaluation of the ISO 10273:2003 method for the isolation of human pathogenic Yersinia enterocolitica from pig carcasses and minced meat. Food Microbiology, 36(2): 170-174.
· Wojciechowska, B., Minkulska-Skupine, E., Platt-Samoraj, A. and Szczerba-Turek, A. (2010). Occurrence of Yersinia enterocolitica in canine excrements contaminating urban lawns. Bulletin of the Veterinary Institute in Pulawy, 54: 153-159.
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Anju, P., Latha, C., Sunil, B. and Sethulekshmi, C. (2014). Antimicrobial resistance profile of Yersinia enterocolitica and Yersinia intermedia isolates from retail pork. International Journal of Current Microbiology and Applied Sciences .3(8): 231-234.
· Arnold, T., Neubauer, H., Nikolaou, K., Roesler, U. and Hensel, A. (2004). Identification of Yersinia enterocolitica in minced meat: A comparative analysis of API 20 E, Yersinia identification kit and 16S rRNA- based PCR method. Journal of Veterinary Medicine, 51: 23-26.
· Ashrafi, F. (2009). Study on percentage of Yersinia contamination in red and white meat in food markets in Shemiran. Journal of Microbiology Knowledge, 1-2: 49-52.
· Atobla, K., Karou, T.G., Dadie, A.T., Niamke, L.S. and Dje, K.M. (2012). Isolation and characterization of pathogenic Yersinia enterocolitica from pigs in Abidjan, Côte d'Ivoire. Journal of Applied Bioscinces, 50: 3540-3548.
· Baumgartner, A., Kuffer, M., Suter, D., Jemmi, T. and Rohner, P. (2007). Antimicrobial resistance of Yersinia enterocolitica strains from human patients, pigs and retail pork in Switzerland. International Journal of Food Microbiology, 115: 110-114.
· Bonardi, S., Paris, A., Bassi, L., Salmi, F., Bacci, C., Riboldi, E., et al. (2010). Detection, semiquantitative enumeration, and antimicrobial susceptibility of Yersinia enterocolitica in pork and chicken meats in Italy. Journal Food Protection, 73(10): 1785-1792.
· Bonardi, S., Brindania, F., Pizzina, G., Lucidia, L., D'Incaub, M., Liebanac, E., et al. (2002). Detection of Salmonella spp., Yersinia enterocolitica and verocytotoxin producing Escherichia coli O157 in pigs at slaughter in Italy. International Journal of Food Microbiology, 85: 101–110.
· Cox, N.A., Del Corral, F., Bailey, J.S., Shotts, E.B. and Papa, C.M. (1990). The presence of Yersinia enterocolitica and other Yersinia species on the carcasses of market broilers. Poultry Science, 69(3): 482-485.
· CSLI. (2012). Method for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard- 9th edition. Report No: M07-A9.
· Fabrega, A. and Vila, J. (2012). Yersinia enterocolitica: Pathogenesis, virulence and antimicrobial resistance. Enfermedades Infecciosasy Microbiolgia Clinica, 30(1): 24–32.
· Fabrega, A. and Vila, J. (2012). Yersinia enterocolitica: Pathogenesis, virulence and antimicrobial resistance. Enfermedades Infecciosas y Microbiología Clínica, 30(1): 24-32.
· Hanifian, S. and Khani, S. (2012). Prevalence of virulent Yersinia enterocolitica in bulk raw milk and retail cheese in northern-west of Iran. International Journal of Food Microbiology, 155: 89–92.
· Jorgensen, J.H. and Ferraro, M.J. (2009). Antimicrobial susceptibility testing: A review of general principles and contemporary practices. Clinical Infectious Diseases, 49: 1749-1755
· Institute of Standards and Industrial Research of Iran. (1998). Microbiology of food and animal. Feeding stuffs-Horizontal method for the detection presumptive pathogenic Yersinia enterocolitica f-Test method. 3rd edition, ISIRI No. 4556. [In Persian]
· International Organization for Standardization (ISO), (2003). Microbiology of food and animal feeding stuffs - Horizontal method for the detection of presumptive pathogenic Yersinia enterocolitica. ISO No. 10273: 2003(E).
· Logue, C.M., Sheridan, J.J., Wauters, G., McDowell, D.A. and Blair I.S. (1996) Yersinia spp. and numbers with particular reference to Yersinia enterocolitica bio/serotypes, occurring on Irish meat and meat products, and the influence of alkali treatment on their isolation. International Journal of Food Microbiology. 33: 851-854.
· Mahdavi, S., Farshchian, M.R., Amini, K., Abbasi, M., Ghiami Rad, M. and Ebadi, AR. (2012). Survey of Yersinia enterocolitica contamination in distributed broiler meats in Tabriz City, Iran. African Journal of Microbiology Research, 6(12): 3019-3023.
· Mielczarek, P., Bagłaj, M. (2004). Yersiniosis-rarely diagnosed disease of gastrointestinal system. Gastroenterologia Polska, 11: 69-74.
· Momtaz, H., Davood Rahimian, M. and Safarpoor Dehkordi, F. (2013). Identification and characterization of Yersinia enterocolitica isolated from raw chicken meat based on molecular and biological techniques. Journal of Applied Poultry Research, 22: 137-145.
· Ramirez, E.I., Vázquez-Salinas, C., Rodas-Suárez, O.R., Pedroche, F.F. (2000). Isolation of Yersinia from raw meat (pork and chicken) and precooked meat (porcine tongues and sausages) collected from commercial establishments in Mexico City. Journal Food Protection, 63(4): 542-544.
· Saberianpour, Sh., Tajbakhsh, E. and Doudi, M. (2012). Prevalence of Yersinia enterocolitica serotype O: 3 isolated from in Shahrekord. Iran Pejouhande, 17(3): 152-156. [In Persian]
· Saleh, I., Barbour, E., Shaib, H. and Harakeh, S. (2012). Highly Resistant Yersinia enterocolitica isolated from dairy based foods in Lebanon. The International Arabic Journal of Antimicrobial Agents. 2(1, 2): 1-6.
· Sharifin Yazdi, M.K., Soltan-Dallal, M.M., Zali M.R., Avadisians, S. and Bakhtiari, R. (2011). Incidence and antibiotic susceptibilities of Yersinia enterocolitica and other Yersinia species recovered from meat and chicken in Tehran, Iran: African Journal of Microbiology Research, 5(18): 2649-2653.
· Shakerian, A., Sharifzadeh, A., Aghanejad, P., Tajmiri Riahi, M. and Salehi, E. (2012). A preliminary study on prevalence of Yersinia enterocolitica in Beef, lamb and poultry at retails of Shahrekord. Journal of Food Hygiene, 2(1): 11-15. [In Persian]
· Siriken, B. (2004). The presence of Yersinia enterocolitica and other Yersinia species in ground beef in Aydin, Turkey. Turkish Journal of Veterinary Animal Science, 28: 489-495
· Soltan Dalal, M.M, Izadpour, F., Khalifegholi, M., Zareii, H., and Bakhtiari, R. (2006). The prevalence of Yersinia in chicken and red meat in southern of Tehran. Journal of School of Public Health and Institute of Public Health Research, 4(4): 49-56. [In Persian]
· TassinariAdos, R., Franco, BD. and Landgraf, M. (1994). Incidence of Yersinia spp. in food in Sao Paulo, Brazil. International Journal of Food Microbiology, 21(3): 263-270.
· Terentjeva, M. and Bērziņs, A. (2010). Prevalence and antimicrobial resistance of Yersinia enterocolitica and Yersinia pseudotuberculosis in slaughter pigs in Latvia. Journal Food Journal Food Protection .73(7):1335-1338.
· Van Damme. I., Berkvens, D., Botteldoorn, N., Dierick, K., Wits, J., Pochet, B. et al. (2013). Evaluation of the ISO 10273:2003 method for the isolation of human pathogenic Yersinia enterocolitica from pig carcasses and minced meat. Food Microbiology, 36(2): 170-174.
· Wojciechowska, B., Minkulska-Skupine, E., Platt-Samoraj, A. and Szczerba-Turek, A. (2010). Occurrence of Yersinia enterocolitica in canine excrements contaminating urban lawns. Bulletin of the Veterinary Institute in Pulawy, 54: 153-159.