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Abstract
A cross sectional study was conducted to detect Extended-Spectrum β-lactams (ESBLs) producing E. coli and Klebsiella species in dressed chicken meat in Maiduguri Metropolis, Borno State, Nigeria. A total of 384 samples were collected (chicken meat swab and intestinal contents) from two (Abbaganaram and Monday Markets) live bird markets (LBMs) in Maiduguri Metropolitan Council (MMC) and one (Tashan Bama) in Jere Local Government Area (LGA). Colony count, culture, isolation and determination of microbial quality of meat were performed based on standard bacteriological protocols. Biochemical tests were conducted to differentiate the isolates, and antimicrobial susceptibility test was performed using Kirby Bauer disk diffusion method. Tashan Bama LBM had 6.4 x 107 CFU/g dressed chicken meat contamination, while, E. coli and Klebsiella species had the highest number of isolates, 178 (46.4%) 28 (7.3%), respectively. The study also revealed 14 (93.3%) and 5 (71.4%) β‑lactam antimicrobial resistant isolates due to E. coli and Klebsiella species, respectively. The phenotypic expression of multi_drug resistance (n=10) patterns of those isolates; further revealed the β‑lactam producing E. coli and Klebsiella species in dressed chicken meat. Critical control points should be established to minimize contamination and the zoonotic risk of multi-drug resistance pathogens in chicken meat in Maiduguri
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References
- Abdissa, R., Haile W., Fite, A. T., Beyi, A. F., Agga, G. E., Edao, B. M., Tadesse, F., Korsa, M.G., Beyene, T., Beyene, T. J. and De Zutter, L.(2017). Prevalence of Escherichia coli O157:H7 in beef cattle at slaughter and beef carcasses at retail shops in Ethiopia. BMC Infect Dis., 17: 1-6. https://doi.org/10.1186/s12879-017-2372-2
- Adzitey, F., Teye, G. A, Kutah, W. N. and Adday, S. (2011). Microbial Quality of Beef Sold on Selected Markets in the Tamale Metropolis in the Northern Region of Ghana. Livestock Res. Rural Dev., 23(1): 5. http://hdl.handle.net/123456789/953
- Agerso, Y., Jensen, J. D., Hasman, H., and Pedersen, K. (2014). Spread of extended spectrum cephalosporinase-producing Escherichia coli clones and plasmids from parent animals to broilers and to broiler meat in a production without use of cephalosporins. Foodborne Path. Dis., 11, 740–746. doi: 10.1089/fpd.2014.1742.
- Bennett, S. D, Walsh, K. A. and Gould, L. H. (2013). Foodborne disease outbreaks caused by Bacillus cereus, Clostridium perfringens, and Staphylococcus aureus—United States, 1998–2008. Clin. Infect. Dis., 57: 425–433.
- Berkel, B. M., Boogaard B. V. and Heijnen, C. (2004). Preservation of fish and meat. Agromisa Foundation, Wageningen. The Netherlands, 8: 78-80.
- Blodgett, R. (2008). Mathematical treatment of plates with colony counts outside the acceptable range. Food microbiol., 25: 92-8.
- Börjesson, S., Ny, S., Egervarn, M., Bergstrom, J., Rosengren, A., Englund, S., et al. (2016). Limited Dissemination of Extended-Spectrum beta-Lactamase-and Plasmid-Encoded AmpC-Producing Escherichia coli from Food and Farm Animals, Sweden. Emerg. Infect. Dis., 22(4): 634–40. pmid:26982890.
- Bortolaia, L. G., Bisgaard, M., Larsen, J. and Bojesen, A. M. (2010). Escherichia coli producing CTX-M-1, -2, and -9 group β-lactamases in organic chicken egg production. Antimicrobial Agents Chem., 54(8): 3527–3528.
- Briñas, L., Moreno, M. A. and Zarazaga, M. (2003). Detection of CMY-2, CTX-M-14, and SHV-12β-lactamases in Escherichia coli fecal-sample isolates from healthy chickens. Antimicrobial Agents and Chem., 47(6): 2056–2058.
- Bunning, V. K., Lindsay, J. A. and Archer, D. L. (1997). Chronic health effects of microbial foodborne disease. World Health Stat., Quarterly, 50(1-2): 51–56.
- Carattoli, A. (2013). Plasmids and the spread of resistance. Intl. J. Med. Microbiol. 303: 298–304. doi: 10.1016/j.ijmm.2013.02.001.
- Clark, W. M. and Lubs, A. H. (1978). Oyo State Government of Nigeria (OYSGN), Oyo State of Nigeria Gazette. The Meat Edict. 23 (31): June 1978-Part A.
- Codex Alimentarius Commission, FAO/WHO (2011). Joint FAO/WHO Food Standards Programme Codex Committee on Contaminants in Foods. Fifth Session, 21-25 March 2011.
- Cohen, N., Ennaji, H., Bouchrif, B., Hassar, M. and Karib, H. (2007). Comparative Study of Microbiological Quality of Raw Poultry Meat at Various Seasons and Different Slaughter Process in Casablanca. Morocco J. Appl. Poult. Res., 16(4): 502-508.
- Goksoy, E. O., Kirkan, S. and Kok, F. (2004). Microbiological Quality of broiler carcasses during processing in two slaughterhouses in Turkey. Poult Sci., 83(8): 1427-32.
- Henry, C. J. K. and Xin, J. L. W. (2014). Application of Hazard Analysis Critical Control Point in the Local Manufacture of Ready-to-Use Therapeutic Foods (RUTFs). Food and Nutr. Bull., 35(2): S57–S63.
- Iramiot, J., Kajumbula, H., Bazira, J., Kansiime, C. and Asiimwe, B. B. (2020). Antimicrobial resistance at the human-animal interface in the communities of Kasese District, South Western Uganda. Sci. Rep., 10, 14737
- Karmali, A. M., Gannon, V. and Sargeant, M. J. (2010). Verocytotoxin-producing Escherichia coli (VTEC), Vet. Microbiol., 140(3-4): 360-370.
- Katakweba, A. A. S., Mtambo, M. M. A., Olsen, J. E. and Muhairwa, A. P. (2012). Awareness of human health risks associated with the use of antibiotics among livestock keepers and factors that contribute to selection of antibiotic resistance bacteria within livestock in Tanzania. Livestock Res. Rural Dev., 24(10): 170. Retrieved March 27, 2022, from http://www.lrrd.org/lrrd24/10/kata24170.htm
- Kwoji, I. D., Musa, J. A., Daniel, N., Mohzo, D. L., Bitrus, A. A., Ojo, A. A. and Ezema, K. U. (2019). Extended-spectrum beta-lactamase-producing Escherichia coli in chickens from small-scale (backyard) poultry farms in Maiduguri, Nigeria. Intl. J. One Health, 5: 26-30. www.onehealthjournal.org/vol.5/4.pdf
- McGaugh, S. E. and Noor, M. A. (2012). Genomic impacts of chromosomal inversions in parapatric Drosophila species. Philosophical transactions of the Royal Society of London. Series B, Biol. Sci., 367(1587): 422–429.
- Miller, R. K. (2002). Factors affecting the quality of raw meat. Meat Process., 27–63. https://doi.org/10.1533/9781855736665.1.27.
- Mohammed, Y., Gadzama, G. B., Zailani, S. B. and Aboderin, A. O. (2016). Characterization of extended-spectrum beta-lactamase from Escherichia coli and Klebsiella species from North Eastern Nigeria. J. Cli. Diagn. Res, JCDR, 10(2), DC07.
- Mohamed-Noor, S. E., Shuaib, Y.A., Suliman, S. E. and Aballa, M. A. (2012). Study of Microbial Contamination of Broilers in Modern Abattoirs in Khartoum State. Food Tech., 36(1): 74-80.
- Nafarnda, W. D., Ajayi, I. E., Shawulu, J. C., Kawe, M. S., Omeiza, G. K., Sani, N. A., Tenuche, O. Z. and Dantong, D. D. (2012). Bacteriological Quality of Abattoir Effluents Discharged into Water Bodies in Abuja, Nigeria. ISRN Vet. Sci. pp.15.
- National Action Plan for Antimicrobial Resistance (2017). https://ncdc.gov.ng/themes/common/docs/ protocols/77_1511368219.pdf. Accessed 25/03/2022.
- Nordmann, P., Naas, T. and Poirel, L. (2011). Global spread of carbapenemase-producing Enterobacteriaceae. Emerg. Infect. Dis., 17: 1791–1798.
- Nsofor, C.A. and Iroegbu, C. U. (2013). Antibiotic resistance profile of Eschetichia coli isolated from five major geopolitical zones of Nigeria. J. Bacteriol. Res., 5(3): 29-34.
- Okorie-Kanu, O. J., Madubuike, U. A. Ezenduka, E. V., Mgbeahuruike, A. C., Okorie-Kanu, C. O., Ugwuijem, E. E., Okorie-Kanu, C.O., Agbowo, P., Olorunleke, S. and Nwanta, J.A. (2020). Occurrence and antibiogram of Listeria species in raw pork, beef and chicken meats marketed in Enugu State, Southern Nigeria. Vet. World, 13(2): 317-325. https://doi.org/10.1371/journal.pone.0232913
- Onuoha, S. C., S.C. Eluu and Okata, M.O. 2016. In-vitro Antimicrobial Resistance of Shigella and Salmonella species Recovered from Abattoir effluent in Afikpo, South Eastern Nigeria. Int. J. Curr. Microbiol. App. Sci., 5(4): 488_497. doi:http://dx.doi.org/10.20546/ijcmas.2016.504.05
- Projan, S. J. (2010). Francis Tally and the discovery and development of tigecycline: a personal reminiscence. Clinical infectious diseases: an official publication of the Infect. Dis. Soc. Am., 50 (1): S24–S25. https://doi.org/10.1086/647941
- Randall, L. P., Clouting, C., Horton, R. A., Coldham, N. G., Wu, G., Clifton-Hadley, F. A., Davies, R.H. and Teale, C. J. (2011). Prevalence of Escherichia coli carrying extended-spectrum β-lactamases (CTX-M and TEM-52) from broiler chickens and turkeys in Great Britain between 2006 and 2009. The J. Antimicrobial Chem., 66(1): 86–95.
- https://doi.org/10.1093/jac/dkq396
- Rasheed, M. U., Thajuddin, N., Ahamed, P., Teklemariam, Z. and Jamil, K. (2014). Antimicrobial drug resistance in strains of Escherichia coli isolated from food sources. Rev. Instituto de Med. Trop. São Paulo, 56(4): 341–346.
- Rottier, W. C., Ammerlaan, H. S. M. and Bonten, M. J. M. (2012). Effects of confounders and intermediates on the association of bacteraemia caused by extended-spectrum β lactamase producing Enterobacteriaceae and patient outcome: a meta-analysis, J. Antimicrobial Chem., 67(6): 1311–1320.
- Schrijver, R., Stijntjes, M., Rodríguez-Baño, J., Tacconelli, E., Babu-Rajendran N. and Voss A. (2018). Review of antimicrobial resistance surveillance programmes in livestock and meat in EU with focus on humans. Clin. Microbiol. Infect. 24, 577–590. 10.1016/j.cmi.2017.09.013.
- Shaikh, S., Fatima, J., Shakil, S., Rizvi, S. M., Kamal, M. A. (2015). Antibiotic resistance and extended spectrum beta-lactamases: types, epidemiology and treatment. Saudi J. Biol. Sci., 22: 90–101.
- Sharma, K. P. and Chattopadhyay, U. K. (2015). Assessment of microbial load of raw meat samples sold in open markets of city of Kolkata. J. Agric. Vet. Sci., 8: 24–7.
- Silvia, L. M. and Jacoby, A. G. (2014). Extended Spectrum Beta-Lactamases. Up-to-date. Antimicrobial Agents Chem., 58: 833.
- Steve, P. (2017). Antibodies for the Prevention Treatment, and Preemption of Infectious Diseases. Pp. 611–20. https://doi.org/10.1002/9783527699124.ch18.
- Thrushfield, M. (2013). Veterinary Epidemiology. (6th Edition). Elsevier Science. Available at: https://www.perlego.com/book/1898785/veterinary-epidemiology-pdf (Accessed Oct., 12th, 2021).
- Tille, P.M. (2014). Bailey and Scott’s diagnostic microbiology, Thirteen edition, Mosby, Inc., an affiliate of Elsevier Inc., 3251 Riverport Lane, St. Louis, Missouri, 63043.
- WHO, World Health Organization (1982). World Health Organisation, Geneva. Guidelines for organization and management of surveillance of food-borne disease. WHO monograph No. VPH/82. 39.
- WHO, World Health Organization (2015). Global Action Plan on Antimicrobial Resistance. https://www.who.int/publications/i/item/9789241509763. (Accessed Oct., 11th, 2021).
References
Abdissa, R., Haile W., Fite, A. T., Beyi, A. F., Agga, G. E., Edao, B. M., Tadesse, F., Korsa, M.G., Beyene, T., Beyene, T. J. and De Zutter, L.(2017). Prevalence of Escherichia coli O157:H7 in beef cattle at slaughter and beef carcasses at retail shops in Ethiopia. BMC Infect Dis., 17: 1-6. https://doi.org/10.1186/s12879-017-2372-2
Adzitey, F., Teye, G. A, Kutah, W. N. and Adday, S. (2011). Microbial Quality of Beef Sold on Selected Markets in the Tamale Metropolis in the Northern Region of Ghana. Livestock Res. Rural Dev., 23(1): 5. http://hdl.handle.net/123456789/953
Agerso, Y., Jensen, J. D., Hasman, H., and Pedersen, K. (2014). Spread of extended spectrum cephalosporinase-producing Escherichia coli clones and plasmids from parent animals to broilers and to broiler meat in a production without use of cephalosporins. Foodborne Path. Dis., 11, 740–746. doi: 10.1089/fpd.2014.1742.
Bennett, S. D, Walsh, K. A. and Gould, L. H. (2013). Foodborne disease outbreaks caused by Bacillus cereus, Clostridium perfringens, and Staphylococcus aureus—United States, 1998–2008. Clin. Infect. Dis., 57: 425–433.
Berkel, B. M., Boogaard B. V. and Heijnen, C. (2004). Preservation of fish and meat. Agromisa Foundation, Wageningen. The Netherlands, 8: 78-80.
Blodgett, R. (2008). Mathematical treatment of plates with colony counts outside the acceptable range. Food microbiol., 25: 92-8.
Börjesson, S., Ny, S., Egervarn, M., Bergstrom, J., Rosengren, A., Englund, S., et al. (2016). Limited Dissemination of Extended-Spectrum beta-Lactamase-and Plasmid-Encoded AmpC-Producing Escherichia coli from Food and Farm Animals, Sweden. Emerg. Infect. Dis., 22(4): 634–40. pmid:26982890.
Bortolaia, L. G., Bisgaard, M., Larsen, J. and Bojesen, A. M. (2010). Escherichia coli producing CTX-M-1, -2, and -9 group β-lactamases in organic chicken egg production. Antimicrobial Agents Chem., 54(8): 3527–3528.
Briñas, L., Moreno, M. A. and Zarazaga, M. (2003). Detection of CMY-2, CTX-M-14, and SHV-12β-lactamases in Escherichia coli fecal-sample isolates from healthy chickens. Antimicrobial Agents and Chem., 47(6): 2056–2058.
Bunning, V. K., Lindsay, J. A. and Archer, D. L. (1997). Chronic health effects of microbial foodborne disease. World Health Stat., Quarterly, 50(1-2): 51–56.
Carattoli, A. (2013). Plasmids and the spread of resistance. Intl. J. Med. Microbiol. 303: 298–304. doi: 10.1016/j.ijmm.2013.02.001.
Clark, W. M. and Lubs, A. H. (1978). Oyo State Government of Nigeria (OYSGN), Oyo State of Nigeria Gazette. The Meat Edict. 23 (31): June 1978-Part A.
Codex Alimentarius Commission, FAO/WHO (2011). Joint FAO/WHO Food Standards Programme Codex Committee on Contaminants in Foods. Fifth Session, 21-25 March 2011.
Cohen, N., Ennaji, H., Bouchrif, B., Hassar, M. and Karib, H. (2007). Comparative Study of Microbiological Quality of Raw Poultry Meat at Various Seasons and Different Slaughter Process in Casablanca. Morocco J. Appl. Poult. Res., 16(4): 502-508.
Goksoy, E. O., Kirkan, S. and Kok, F. (2004). Microbiological Quality of broiler carcasses during processing in two slaughterhouses in Turkey. Poult Sci., 83(8): 1427-32.
Henry, C. J. K. and Xin, J. L. W. (2014). Application of Hazard Analysis Critical Control Point in the Local Manufacture of Ready-to-Use Therapeutic Foods (RUTFs). Food and Nutr. Bull., 35(2): S57–S63.
Iramiot, J., Kajumbula, H., Bazira, J., Kansiime, C. and Asiimwe, B. B. (2020). Antimicrobial resistance at the human-animal interface in the communities of Kasese District, South Western Uganda. Sci. Rep., 10, 14737
Karmali, A. M., Gannon, V. and Sargeant, M. J. (2010). Verocytotoxin-producing Escherichia coli (VTEC), Vet. Microbiol., 140(3-4): 360-370.
Katakweba, A. A. S., Mtambo, M. M. A., Olsen, J. E. and Muhairwa, A. P. (2012). Awareness of human health risks associated with the use of antibiotics among livestock keepers and factors that contribute to selection of antibiotic resistance bacteria within livestock in Tanzania. Livestock Res. Rural Dev., 24(10): 170. Retrieved March 27, 2022, from http://www.lrrd.org/lrrd24/10/kata24170.htm
Kwoji, I. D., Musa, J. A., Daniel, N., Mohzo, D. L., Bitrus, A. A., Ojo, A. A. and Ezema, K. U. (2019). Extended-spectrum beta-lactamase-producing Escherichia coli in chickens from small-scale (backyard) poultry farms in Maiduguri, Nigeria. Intl. J. One Health, 5: 26-30. www.onehealthjournal.org/vol.5/4.pdf
McGaugh, S. E. and Noor, M. A. (2012). Genomic impacts of chromosomal inversions in parapatric Drosophila species. Philosophical transactions of the Royal Society of London. Series B, Biol. Sci., 367(1587): 422–429.
Miller, R. K. (2002). Factors affecting the quality of raw meat. Meat Process., 27–63. https://doi.org/10.1533/9781855736665.1.27.
Mohammed, Y., Gadzama, G. B., Zailani, S. B. and Aboderin, A. O. (2016). Characterization of extended-spectrum beta-lactamase from Escherichia coli and Klebsiella species from North Eastern Nigeria. J. Cli. Diagn. Res, JCDR, 10(2), DC07.
Mohamed-Noor, S. E., Shuaib, Y.A., Suliman, S. E. and Aballa, M. A. (2012). Study of Microbial Contamination of Broilers in Modern Abattoirs in Khartoum State. Food Tech., 36(1): 74-80.
Nafarnda, W. D., Ajayi, I. E., Shawulu, J. C., Kawe, M. S., Omeiza, G. K., Sani, N. A., Tenuche, O. Z. and Dantong, D. D. (2012). Bacteriological Quality of Abattoir Effluents Discharged into Water Bodies in Abuja, Nigeria. ISRN Vet. Sci. pp.15.
National Action Plan for Antimicrobial Resistance (2017). https://ncdc.gov.ng/themes/common/docs/ protocols/77_1511368219.pdf. Accessed 25/03/2022.
Nordmann, P., Naas, T. and Poirel, L. (2011). Global spread of carbapenemase-producing Enterobacteriaceae. Emerg. Infect. Dis., 17: 1791–1798.
Nsofor, C.A. and Iroegbu, C. U. (2013). Antibiotic resistance profile of Eschetichia coli isolated from five major geopolitical zones of Nigeria. J. Bacteriol. Res., 5(3): 29-34.
Okorie-Kanu, O. J., Madubuike, U. A. Ezenduka, E. V., Mgbeahuruike, A. C., Okorie-Kanu, C. O., Ugwuijem, E. E., Okorie-Kanu, C.O., Agbowo, P., Olorunleke, S. and Nwanta, J.A. (2020). Occurrence and antibiogram of Listeria species in raw pork, beef and chicken meats marketed in Enugu State, Southern Nigeria. Vet. World, 13(2): 317-325. https://doi.org/10.1371/journal.pone.0232913
Onuoha, S. C., S.C. Eluu and Okata, M.O. 2016. In-vitro Antimicrobial Resistance of Shigella and Salmonella species Recovered from Abattoir effluent in Afikpo, South Eastern Nigeria. Int. J. Curr. Microbiol. App. Sci., 5(4): 488_497. doi:http://dx.doi.org/10.20546/ijcmas.2016.504.05
Projan, S. J. (2010). Francis Tally and the discovery and development of tigecycline: a personal reminiscence. Clinical infectious diseases: an official publication of the Infect. Dis. Soc. Am., 50 (1): S24–S25. https://doi.org/10.1086/647941
Randall, L. P., Clouting, C., Horton, R. A., Coldham, N. G., Wu, G., Clifton-Hadley, F. A., Davies, R.H. and Teale, C. J. (2011). Prevalence of Escherichia coli carrying extended-spectrum β-lactamases (CTX-M and TEM-52) from broiler chickens and turkeys in Great Britain between 2006 and 2009. The J. Antimicrobial Chem., 66(1): 86–95.
https://doi.org/10.1093/jac/dkq396
Rasheed, M. U., Thajuddin, N., Ahamed, P., Teklemariam, Z. and Jamil, K. (2014). Antimicrobial drug resistance in strains of Escherichia coli isolated from food sources. Rev. Instituto de Med. Trop. São Paulo, 56(4): 341–346.
Rottier, W. C., Ammerlaan, H. S. M. and Bonten, M. J. M. (2012). Effects of confounders and intermediates on the association of bacteraemia caused by extended-spectrum β lactamase producing Enterobacteriaceae and patient outcome: a meta-analysis, J. Antimicrobial Chem., 67(6): 1311–1320.
Schrijver, R., Stijntjes, M., Rodríguez-Baño, J., Tacconelli, E., Babu-Rajendran N. and Voss A. (2018). Review of antimicrobial resistance surveillance programmes in livestock and meat in EU with focus on humans. Clin. Microbiol. Infect. 24, 577–590. 10.1016/j.cmi.2017.09.013.
Shaikh, S., Fatima, J., Shakil, S., Rizvi, S. M., Kamal, M. A. (2015). Antibiotic resistance and extended spectrum beta-lactamases: types, epidemiology and treatment. Saudi J. Biol. Sci., 22: 90–101.
Sharma, K. P. and Chattopadhyay, U. K. (2015). Assessment of microbial load of raw meat samples sold in open markets of city of Kolkata. J. Agric. Vet. Sci., 8: 24–7.
Silvia, L. M. and Jacoby, A. G. (2014). Extended Spectrum Beta-Lactamases. Up-to-date. Antimicrobial Agents Chem., 58: 833.
Steve, P. (2017). Antibodies for the Prevention Treatment, and Preemption of Infectious Diseases. Pp. 611–20. https://doi.org/10.1002/9783527699124.ch18.
Thrushfield, M. (2013). Veterinary Epidemiology. (6th Edition). Elsevier Science. Available at: https://www.perlego.com/book/1898785/veterinary-epidemiology-pdf (Accessed Oct., 12th, 2021).
Tille, P.M. (2014). Bailey and Scott’s diagnostic microbiology, Thirteen edition, Mosby, Inc., an affiliate of Elsevier Inc., 3251 Riverport Lane, St. Louis, Missouri, 63043.
WHO, World Health Organization (1982). World Health Organisation, Geneva. Guidelines for organization and management of surveillance of food-borne disease. WHO monograph No. VPH/82. 39.
WHO, World Health Organization (2015). Global Action Plan on Antimicrobial Resistance. https://www.who.int/publications/i/item/9789241509763. (Accessed Oct., 11th, 2021).