Molecular Characterization and Antibiotic Resistance Patterns of Listeria Species in Frozen Beef and Chicken Sold in Benin City, Nigeria
Keywords:
Listeria spp., Frozen beef product, Frozen chicken product, Antibiotic resistance, Food-borne pathogenAbstract
Frozen beef and chicken products were purchased from four markets in Benin City and examined for the presence of Listeria species using standard microbiological procedures. Listeria species were characterized by biochemical tests and confirmed by polymerase chain reaction (PCR). Antibiotic resistance of the isolates was carried out using the disc diffusion method. Bacterial plasmids were isolated and separated by agarose gel electrophoresis. The Listeria isolates in the beef samples ranged between 3.11 ± 0.69 × 103 to 1.36 ± 0.39 × 104 CFU/g while for chicken samples ranged between 1.56 ± 0.24 × 103 to 1.84 ± 0.45 × 104 CFU/g. The isolated Listeria species were L. monocytogenes, L. ivanovii, L. grayi and L. innocua. Among the Listeria isolates, L. monocytogenes (34.78%) and L. innocua (31.82%) had the highest frequency in beef and chicken respectively. Antibiotics sensitivity revealed that the most resisted drugs were ampiclox, amoxicillin and septrin while isolates were most susceptible to gentamycin and ciprofloxacin. The strains of organisms identified from DNA sequencing were: L. monocytogenes (KM010020.1), L. monocytogenes (KF588563.1), L. ivanovii subsp. Ivanovii (CP009577.1), L. grayi (JN852815.1), L. monocytogenes (CP013724.1), L. ivanovii subsp. londoniensis (CP009575.1), L. grayi (NR116351.1) and L. innocua (KU208087.1). The food-borne pathogens isolated from meat products of this study may be the indicator of poor hygienic practices.
References
Adzitey, F. and Huda, N. 2010. Listeria monocytogenes in foods: incidence and possible control measures. African Journal of Microbiology Research. 4(25): 2848–2855.
Akano, S.O., Moro, D.D., Deji-Agboola, A.M., and Oluwadun, A.D. 2013. Public health implication of Listeria species and other bacteria isolates of abattoir effluent in Lagos, Nigeria. International Research Journal of Microbiology. 4(7): 162–167.
Alsheikh, A.D.I, Mohammed, G.E., and Abdalla, M.A. 2013. Isolation and identification of Listeria monocytogenes from retail broiler chicken ready to eat meat products in Sudan. International Journal of Animal and Veterinary Advances. 5(1): 9–14.
Awaisheh, S.S. 2010. Incidence and contamination level of Listeria monocytogenes and other Listeria spp. in ready-to-eat meat products in Jordan. Journal of Food Protection. 73: 535–540.
Baek, S.Y., Lim, S.Y., Lee, D.H., Min, K.H., and Kim, C.M. 2000. Incidence and characterization of Listeria monocytogenes from domestic and imported foods in Korea. Journal of Food Protection. 63: 186–189.
Balouiri, M., Sadiki, M. and Ibnsouda, S.K. 2016. Methods for in vitro evaluating antimicrobial activity. Journal of Pharmaceutical Analysis. 6(2): 71–79.
Barbuddhe, S.B., Malik, S.V.S., Bhilegaonkar, K.N., Kumar, P. and Gupta, L.K. 2000. Isolation of Listeria monocytogenes and anti-listeriolysin detection in sheep and goats. Small Ruminant Research. 38(2): 151–155.
Bohaychuk, V.M., Gensler, G.E., King, R.K., Manninen, K.I., Sorensen, O., Wu, J.T., Stiles, M.E., and McMullen, L.M. 2006. Occurrence of pathogens in raw and ready-to-eat meat and poultry products collected from the retail marketplace in Edmonton, Alberta, Canada. Journal of Food Protection. 69: 2176–2182.
Border, P.M., Howard, J.J., Plastow, G.S.,and Siggens, K.W. 1990. Detection of Listeria species and Listeria monocytogenes using polymerase chain reaction. Letters of Applied Microbiology. 11(3): 158–162.
Bubert, A., Hein, I., Raugh, M., Lehner, A.,Yoon, B., Goebel, W., and Wagner, M. 1999. Detection and differentiation of Listeria spp. by a single reaction based on multiplex PCR. Journal of Applied and Environmental Microbiology. 65(10): 4688–4692.
Capita, R., Alonso-Calleja, C., Moreno, B., and Garcia-Fernandez, M.C. 2001. Occurrence of Listeria species in retail poultry meat and comparison of a cultural/ immunoassay for their detection. International Journal of Food Microbiology. 65: 75–82.
Chukwu, O.C., Ogbonna, C.I., Olabode, A.O., Chukwu, A.I., Onwuliri, F.C., and Nwakiti, O.O. 2006. Listeria monocytogenesin Nigerian processed meat and ready-to- eat-dairy products. Nigerian Journal of Microbiology. 20(2): 900–904.
Daniel, S.T., Umeh, E., U., and Iheukwumere, C.C. 2015. Contamination and antibiotic susceptibility profile of Listeria species in frozen and fresh chicken sold in Makurdi, Nigeria. International Journal of Current Microbiology and Applied Science. 4(7): 617–623.
De Simon, M., Tarrago, C., and Ferrer, M.D. 2002. Incidence of Listeria monocytogenes in freshfoods in Barcelona (Spain). International Journal of Food Microbiology. 116: 153–156.
Dhanashee, B., Otta, S.K., Karunaserger, J., and Goebel, W. 2003. Incidence of Listeria monocytogenes in clinical and food samples in Mangalove, India. International Journal of Food Microbiology. 20: 447–453.
El-Malek, A.M., Hassan, S., Ali, F., Hassanein, R., Abdelazeem, M., and Elsayh, K.I. 2010. Occurrence of Listeria species in meat, chicken product and human stools in Assiut city, Egypt with PCR use for rapid identification of Listeria monocytogenes. Journal of Veterinary World. 3(8): 353–359.
Ennaji, H., Mohammed, T., Ennaji, M., Mohammed, H., and Nozha, C. 2008. Characterization and antibiotic susceptibility of Listeria monocytogenes isolated from poultry and red meat in Morocco. Infectious Drug Resistant. 1: 45–50.
Filiousis, G., Johansson, A., Frey, J., and Perreten, V. 2009. Prevalence, genetic diversity and antimicrobial susceptibility of Listeria monocytogenes isolated from open-air food markets in Greece. Food Control. 20(3): 314–317.
Gebretsadik, S., Kassa, T., Alemayehu, H., Huruy, K., and Kebede, N. 2011. Isolation and characterization of Listeria monocytogenes and other Listeria species in foods of animal origin in Addis Ababa, Ethiopia. Journal of Infectious Diseases and Public Health. 4: 22–29.
Hanchung, Y., Sheng, C., David, G., Shaohua, Z., Patrick, M., Robert, W., and Jianghong, M. 2004. Characterization of multiple antimicrobial-resistant Escherichia coli Isolates from Chicken and Swine in China. Journal of Clinical Microbiology. 42: 3484–3489.
Hassan, E.L., Ferage, M., and Nahla, T. 2006. Lactic acid and PH as indication for bacterial spoilage of meat and some meat products. Journal of Applied Science and Research. 2(8): 522–528.
Ikeh, M.A., Obi, S.K., Ezeasor, D.N., Ezeonu, I.M., and Moneke, A.N. 2010. Incidence and pathogenicity profile of Listeria spp isolated from food environmental samples in Nsukka, Nigeria. African Journal of Biotechnology. 9(30): 4776–4782.
Indrawattana N, Nibaddhasobon T, Sookrung N, Chongsa-Nguan M, Tungtrongchitr A., and Makino S. 2011. Prevalence of Listeria monocytogenes in raw meats marketed in bangkok and characterization of the isolates by phenotypic and molecular methods. Journal of Health and Population Nutrition. 29(1): 26–38.
Jay J.M. 1996. Prevalence of Listeria spp. in meat and poultry products. Food Control. 7(4): 209–214.
Johnson, J.L., Doyle, M.P. and Cassens, R.G. 1990. Listeria monocytogenes and other Listeria spp in meat and meat products. Journal of Food Protection. 53(1): 81–91.
Karakolev, R. 2009. Incidence of Listeria monocytogenes in beef, pork, raw-dried and raw smoked sausages in Bulguria. Food Control. 20(10): 953–955.
Lawan, F.A., Tijjani, A.N., Raufu, A.I., Ameh, J.A., Ngoshe, I.Y. and Auwal, M.S. 2013. Isolation and characterization of Listeria species from ruminants in Maiduguri North–eastern Nigeria. African Journal of Biotechnology. 12(50): 6997–7000.
Liu, D, Lawrence, L.M., Austin, F.W. and Ainsworth, A.J.A. 2007. Multiplex PCR for species- and virulence-specific determination of Listeria monocytogenes. Journal of Microbiology Methods. 71(2): 133–140.
Molla, B., Yilma, R., and Alemayehu, D. 2004. Listeria monocytogenesand other Listeria species in retail meat and milk products in Addis Ababa, Ethiopia.Ethiopian Journal of Health Development. 18(3): 208–212.
Monique, P., Michel, B., and Catherine, D. (2003). Fatal Case of Listeria innocua Bacteremia. Journal of Clinical Microbiology. 41(11): 5308–5309.
Montero, D., Bodero, M., Riveros, G., Lapierre, L., Gaggero, A., and Vidal, R., M. 2015. Molecular epidemiology and genetic diversity of Listeria monocytogenes isolates from a wide variety of ready-to-eat foods and their relationship to clinical strains from listeriosis outbreaks in Chile. Frontiers Microbiology. 6: 384–394.
Ogbeibu, E.A. (2005). Biostatistics: A practical approach to research and data handling. Mindex Publishing, Benin City. 264 pp.
Ohue, L.A., Enurah, L.U., and Aboaba, O.O. 2015. Prevalence and antibiotics susceptibility profile of Listeria monocytogenes isolated from processed and unprocessed meat products in Lagos, Nigeria. Nigerian Journal of Science and Technology. 1(1): 12–18.
Okutni, A., Okada, Y., Yamamoto, S., and Igimi, S. 2004. Overview of Listeria monocytogenes contamination in Japan. International Journal of Food Microbiology. 93(2): 131–140.
Pesavento, G., Ducci, B., Nieri, D.,Comodo, N., and Lo Nostro, A. 2010. Prevalence and antibiotic susceptibility of Listeria spp. isolated from raw meat and retail foods. Food Control. 21(5): 708–713.
Pourshaban, M., Ferrini, A.M., Cannoni, V., Oliva, B.,and Aurelli, P. 2002. Transferable tetracycline resistance in Listeria monocytogenes from food in Italy. Journal of Medical Microbiology. 51(7): 564–566.
Ramaswamy, V., Cresence, V.M., Rejitha, J., Mohandas, U.L., Dharsana, K.S., Suryaprasad, P., and Helan, M.V. 2007. Listeria: Review of epidemiology and pathogenesis. Journal of Microbiology, Immunology and Infection. 40: 4–13.
Rapose, A., Lick, S, and Ismail N. (2008). Listeria grayi bacteremia in a heart transplant recipient. Transplant Infectious Diseases. 10(6): 434–436.
Rorvik, L.M., Yindestad, M., and Skgerve, E. 2001. Growth of Listeria monocytogenes in meatproducts. International Journal of Food Microbiology. 14: 111–118.
Safdara, A. and Armstrong, D. 2003. Antimicrobial activities against 84 Listeria monocytogenes isolates from patients with systemic listeriosis at a comprehensive cancer center. (1955–1997). Journal of Clinical Microbiology. 41: 483–485.
Taurai, T., Jochen, K., Jacques, B., Roger S., Tasara T., Klumpp, J., Bille, J., and Stephan, R. 2016. Genome sequences of Listeria monocytogenes strains responsible for cheese- and cooked ham product-associated Swiss listeriosis outbreaks in 2005 and 2011. Genome Announcement. 4(2): 106–116.
Uyttendaele, M., Busschaert, P., Valero, A., Geeraerd, A.H., Vermeulen, A., Jacxsens, L., Goh K.K., De Loy, A., Van Impe, J.F., andDeviieghere, F. 2009. Prevalence and challenge tests of Listeria monocytogenes in Belgian produced and retailed mayonnaise-based deli-salads, cooked meat products and smoked fish between 2005 and 2007. International Journal of Food Microbiology.133: 94–104.
Uyttendaele, M., Troy, P.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.
Vitals, A.I., Aguadoes, V.D., and Garcia-Jalon, J.E. 2004. Occurrence of Listeria monocytogenes in fresh and processed foods in Navarra, Spain. International Journal of Food Microbiology. 90: 349–356.
Akano, S.O., Moro, D.D., Deji-Agboola, A.M., and Oluwadun, A.D. 2013. Public health implication of Listeria species and other bacteria isolates of abattoir effluent in Lagos, Nigeria. International Research Journal of Microbiology. 4(7): 162–167.
Alsheikh, A.D.I, Mohammed, G.E., and Abdalla, M.A. 2013. Isolation and identification of Listeria monocytogenes from retail broiler chicken ready to eat meat products in Sudan. International Journal of Animal and Veterinary Advances. 5(1): 9–14.
Awaisheh, S.S. 2010. Incidence and contamination level of Listeria monocytogenes and other Listeria spp. in ready-to-eat meat products in Jordan. Journal of Food Protection. 73: 535–540.
Baek, S.Y., Lim, S.Y., Lee, D.H., Min, K.H., and Kim, C.M. 2000. Incidence and characterization of Listeria monocytogenes from domestic and imported foods in Korea. Journal of Food Protection. 63: 186–189.
Balouiri, M., Sadiki, M. and Ibnsouda, S.K. 2016. Methods for in vitro evaluating antimicrobial activity. Journal of Pharmaceutical Analysis. 6(2): 71–79.
Barbuddhe, S.B., Malik, S.V.S., Bhilegaonkar, K.N., Kumar, P. and Gupta, L.K. 2000. Isolation of Listeria monocytogenes and anti-listeriolysin detection in sheep and goats. Small Ruminant Research. 38(2): 151–155.
Bohaychuk, V.M., Gensler, G.E., King, R.K., Manninen, K.I., Sorensen, O., Wu, J.T., Stiles, M.E., and McMullen, L.M. 2006. Occurrence of pathogens in raw and ready-to-eat meat and poultry products collected from the retail marketplace in Edmonton, Alberta, Canada. Journal of Food Protection. 69: 2176–2182.
Border, P.M., Howard, J.J., Plastow, G.S.,and Siggens, K.W. 1990. Detection of Listeria species and Listeria monocytogenes using polymerase chain reaction. Letters of Applied Microbiology. 11(3): 158–162.
Bubert, A., Hein, I., Raugh, M., Lehner, A.,Yoon, B., Goebel, W., and Wagner, M. 1999. Detection and differentiation of Listeria spp. by a single reaction based on multiplex PCR. Journal of Applied and Environmental Microbiology. 65(10): 4688–4692.
Capita, R., Alonso-Calleja, C., Moreno, B., and Garcia-Fernandez, M.C. 2001. Occurrence of Listeria species in retail poultry meat and comparison of a cultural/ immunoassay for their detection. International Journal of Food Microbiology. 65: 75–82.
Chukwu, O.C., Ogbonna, C.I., Olabode, A.O., Chukwu, A.I., Onwuliri, F.C., and Nwakiti, O.O. 2006. Listeria monocytogenesin Nigerian processed meat and ready-to- eat-dairy products. Nigerian Journal of Microbiology. 20(2): 900–904.
Daniel, S.T., Umeh, E., U., and Iheukwumere, C.C. 2015. Contamination and antibiotic susceptibility profile of Listeria species in frozen and fresh chicken sold in Makurdi, Nigeria. International Journal of Current Microbiology and Applied Science. 4(7): 617–623.
De Simon, M., Tarrago, C., and Ferrer, M.D. 2002. Incidence of Listeria monocytogenes in freshfoods in Barcelona (Spain). International Journal of Food Microbiology. 116: 153–156.
Dhanashee, B., Otta, S.K., Karunaserger, J., and Goebel, W. 2003. Incidence of Listeria monocytogenes in clinical and food samples in Mangalove, India. International Journal of Food Microbiology. 20: 447–453.
El-Malek, A.M., Hassan, S., Ali, F., Hassanein, R., Abdelazeem, M., and Elsayh, K.I. 2010. Occurrence of Listeria species in meat, chicken product and human stools in Assiut city, Egypt with PCR use for rapid identification of Listeria monocytogenes. Journal of Veterinary World. 3(8): 353–359.
Ennaji, H., Mohammed, T., Ennaji, M., Mohammed, H., and Nozha, C. 2008. Characterization and antibiotic susceptibility of Listeria monocytogenes isolated from poultry and red meat in Morocco. Infectious Drug Resistant. 1: 45–50.
Filiousis, G., Johansson, A., Frey, J., and Perreten, V. 2009. Prevalence, genetic diversity and antimicrobial susceptibility of Listeria monocytogenes isolated from open-air food markets in Greece. Food Control. 20(3): 314–317.
Gebretsadik, S., Kassa, T., Alemayehu, H., Huruy, K., and Kebede, N. 2011. Isolation and characterization of Listeria monocytogenes and other Listeria species in foods of animal origin in Addis Ababa, Ethiopia. Journal of Infectious Diseases and Public Health. 4: 22–29.
Hanchung, Y., Sheng, C., David, G., Shaohua, Z., Patrick, M., Robert, W., and Jianghong, M. 2004. Characterization of multiple antimicrobial-resistant Escherichia coli Isolates from Chicken and Swine in China. Journal of Clinical Microbiology. 42: 3484–3489.
Hassan, E.L., Ferage, M., and Nahla, T. 2006. Lactic acid and PH as indication for bacterial spoilage of meat and some meat products. Journal of Applied Science and Research. 2(8): 522–528.
Ikeh, M.A., Obi, S.K., Ezeasor, D.N., Ezeonu, I.M., and Moneke, A.N. 2010. Incidence and pathogenicity profile of Listeria spp isolated from food environmental samples in Nsukka, Nigeria. African Journal of Biotechnology. 9(30): 4776–4782.
Indrawattana N, Nibaddhasobon T, Sookrung N, Chongsa-Nguan M, Tungtrongchitr A., and Makino S. 2011. Prevalence of Listeria monocytogenes in raw meats marketed in bangkok and characterization of the isolates by phenotypic and molecular methods. Journal of Health and Population Nutrition. 29(1): 26–38.
Jay J.M. 1996. Prevalence of Listeria spp. in meat and poultry products. Food Control. 7(4): 209–214.
Johnson, J.L., Doyle, M.P. and Cassens, R.G. 1990. Listeria monocytogenes and other Listeria spp in meat and meat products. Journal of Food Protection. 53(1): 81–91.
Karakolev, R. 2009. Incidence of Listeria monocytogenes in beef, pork, raw-dried and raw smoked sausages in Bulguria. Food Control. 20(10): 953–955.
Lawan, F.A., Tijjani, A.N., Raufu, A.I., Ameh, J.A., Ngoshe, I.Y. and Auwal, M.S. 2013. Isolation and characterization of Listeria species from ruminants in Maiduguri North–eastern Nigeria. African Journal of Biotechnology. 12(50): 6997–7000.
Liu, D, Lawrence, L.M., Austin, F.W. and Ainsworth, A.J.A. 2007. Multiplex PCR for species- and virulence-specific determination of Listeria monocytogenes. Journal of Microbiology Methods. 71(2): 133–140.
Molla, B., Yilma, R., and Alemayehu, D. 2004. Listeria monocytogenesand other Listeria species in retail meat and milk products in Addis Ababa, Ethiopia.Ethiopian Journal of Health Development. 18(3): 208–212.
Monique, P., Michel, B., and Catherine, D. (2003). Fatal Case of Listeria innocua Bacteremia. Journal of Clinical Microbiology. 41(11): 5308–5309.
Montero, D., Bodero, M., Riveros, G., Lapierre, L., Gaggero, A., and Vidal, R., M. 2015. Molecular epidemiology and genetic diversity of Listeria monocytogenes isolates from a wide variety of ready-to-eat foods and their relationship to clinical strains from listeriosis outbreaks in Chile. Frontiers Microbiology. 6: 384–394.
Ogbeibu, E.A. (2005). Biostatistics: A practical approach to research and data handling. Mindex Publishing, Benin City. 264 pp.
Ohue, L.A., Enurah, L.U., and Aboaba, O.O. 2015. Prevalence and antibiotics susceptibility profile of Listeria monocytogenes isolated from processed and unprocessed meat products in Lagos, Nigeria. Nigerian Journal of Science and Technology. 1(1): 12–18.
Okutni, A., Okada, Y., Yamamoto, S., and Igimi, S. 2004. Overview of Listeria monocytogenes contamination in Japan. International Journal of Food Microbiology. 93(2): 131–140.
Pesavento, G., Ducci, B., Nieri, D.,Comodo, N., and Lo Nostro, A. 2010. Prevalence and antibiotic susceptibility of Listeria spp. isolated from raw meat and retail foods. Food Control. 21(5): 708–713.
Pourshaban, M., Ferrini, A.M., Cannoni, V., Oliva, B.,and Aurelli, P. 2002. Transferable tetracycline resistance in Listeria monocytogenes from food in Italy. Journal of Medical Microbiology. 51(7): 564–566.
Ramaswamy, V., Cresence, V.M., Rejitha, J., Mohandas, U.L., Dharsana, K.S., Suryaprasad, P., and Helan, M.V. 2007. Listeria: Review of epidemiology and pathogenesis. Journal of Microbiology, Immunology and Infection. 40: 4–13.
Rapose, A., Lick, S, and Ismail N. (2008). Listeria grayi bacteremia in a heart transplant recipient. Transplant Infectious Diseases. 10(6): 434–436.
Rorvik, L.M., Yindestad, M., and Skgerve, E. 2001. Growth of Listeria monocytogenes in meatproducts. International Journal of Food Microbiology. 14: 111–118.
Safdara, A. and Armstrong, D. 2003. Antimicrobial activities against 84 Listeria monocytogenes isolates from patients with systemic listeriosis at a comprehensive cancer center. (1955–1997). Journal of Clinical Microbiology. 41: 483–485.
Taurai, T., Jochen, K., Jacques, B., Roger S., Tasara T., Klumpp, J., Bille, J., and Stephan, R. 2016. Genome sequences of Listeria monocytogenes strains responsible for cheese- and cooked ham product-associated Swiss listeriosis outbreaks in 2005 and 2011. Genome Announcement. 4(2): 106–116.
Uyttendaele, M., Busschaert, P., Valero, A., Geeraerd, A.H., Vermeulen, A., Jacxsens, L., Goh K.K., De Loy, A., Van Impe, J.F., andDeviieghere, F. 2009. Prevalence and challenge tests of Listeria monocytogenes in Belgian produced and retailed mayonnaise-based deli-salads, cooked meat products and smoked fish between 2005 and 2007. International Journal of Food Microbiology.133: 94–104.
Uyttendaele, M., Troy, P.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.
Vitals, A.I., Aguadoes, V.D., and Garcia-Jalon, J.E. 2004. Occurrence of Listeria monocytogenes in fresh and processed foods in Navarra, Spain. International Journal of Food Microbiology. 90: 349–356.
Downloads
Published
2018-12-11
How to Cite
Omogbai, Barry Aigbodion, and David Eguasa Esokpunwu. 2018. “Molecular Characterization and Antibiotic Resistance Patterns of Listeria Species in Frozen Beef and Chicken Sold in Benin City, Nigeria”. Food and Applied Bioscience Journal 7 (1):68-86. https://li01.tci-thaijo.org/index.php/fabjournal/article/view/144711.
Issue
Section
Food Processing and Engineering
