• O. E. OJO
  • O. O. ONI
Keywords: Antimicrobial resistance, apparently healthy chickens, diseased chickens, diseased turkeys, enterobacteriaceae


The emergence and wide-spread dissemination of antimicrobial resistant bacteria strains is a global phenomenon of great public health and economic implications. Antimicrobial resistance was investigated in enterobacteriaceae isolated from apparently healthy and diseased poultry birds using the broth micro-dilution method to determine antimicrobial minimum inhibitory concentration (MIC). In all, 504 bacterial isolates including Escherichia coli (471), Klebsiella spp (28) and Salmonella enterica isolates (5) were studied. The isolates were resistant to ampicillin (88.5%), chloramphenicol (62.3%), ciprofloxacin (74.8%), enrofloxacin (81.0%), neomycin (83.9%), norfloxacin (78.8%), streptomycin (91.3%) and tetracycline (83.3%). The geometric mean MIC (µg/µL) of tested antimicrobials for enterobacteriaceae is as follows: ampicillin (102.5), chloramphenicol (48.4), ciprofloxacin (19.1), enrofloxacin (34.5), neomycin (47.7), norfloxacin (24.5), streptomycin (142.2) and tetracycline (62.5). Although rates of resistance to ampillin, streptomycin and tetracycline were similar among isolates from apparently healthy and diseases birds, resistance to chloramphenicol, ciprofloxacin, enrofloxacin, neomycin and norfloxacin were significantly higher (p<0.05) in isolates from diseased chickens than in those from apparently healthy chickens. The high rates of antimicrobial resistance in bacteria may contribute to the persistence of pathogens in poultry flock and ineffectiveness of antimicrobial chemotherapy during disease outbreaks.



Agbaje, M., Davies, R., Oyekunle, M.A., Ojo, O.E., Fasina, F.O., Akinduti, P.A. 2010. Observation on the occurrence and transmission pattern of Salmonella gallinarum in commercial poultry farms in Ogun State, South Western Nigeria. African Journal of Microbiology Research, 4 (9): 796–800.
Balis, E., Vatopoulos, A.C., Kanelopoulou, M., Mainas, E., Hatzoudis, G., Kontogianni, V., Malamou-Lada, H., Kitsou-Kiriakopoulou, S., Kalapothaki, V., 1996. Indications of in vivo transfer of an epidemic R plasmid from Salmonella enteritidis to Escherichia coli of the normal human gut flora. Journal of Clinical Microbiology, 34: 977–979.

Barbosa, T.M., Levy, S.B. 2000. The impact of antibiotic use on resistance development and persistence. Drug Resistance Updates, 3: 303–311.

Bergeron, C.R., Prussing, C., Boerlin, P., Daignault, D., Dutil, L., Reid-Smith, R.J., Zhanel, G.G., Manges, A.R. 2012. Chicken as reservoir for extraintestinal pathogenic Escherichia coli in humans, Canada. Emerging Infectious Diseases, 18 (3): 415-521.

Boothe, D.M., Debavalya, N. 2011. Impact of routine antimicrobial therapy on canine fecal Escherichia coli antimicrobial resistance: A pilot study. International Journal of Applied Research in Veterinary Medicine, 9 (4): 396-406.

Carrique-Mas J.J. and Davies R.H. 2008. Sampling and bacteriological detection of Salmonella in poultry and poultry premises: a review. Revue Scientifique et Technique de Office International des Epizooties 27 (3): 665 – 677.

Chen, X., Pan, W., Zhang, W., Pan, Z., Gao, S., Jiao, X. 2011. Quinolone resistance in Escherichia coli and Salmonella spp. isolates from diseased chickens during 1993-2008 in China. African Journal of Microbiology Research, 5 (19): 3078-3083.

Cheng, A.C., Turnidge, J., Collignon, P., Looke, D., Barton, M., Gottlieb, T. 2012. Control of Fluoroquinolone Resistance through Successful Regulation, Australia. Emerging Infectious Diseases, 18 (9): 1453-1460.

CLSI, 2008. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals; Approved standard-Third edition Vol 28 (8), CLSI document M31-A3, 1 – 99. Clinical and Laboratory Standards Institute, 940 West Valley Road, Wayne Pennsylvania, USA.

DANMAP 2011. The Danish Integrated Antimicrobial Resistance Monitoring and Research Programme. Use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark. ISSN 1600-2032. Available from Accessed 19th September, 2012.

Guerrant, R.L., Van Gilder, T., Steiner, T.S., Thielman, N.M., Slutsker, L., Tauxe, R.V., Hennessy, T., Griffin, P.M., DuPont, H., Sack. R.S., Tarr, P., Neill, M., Nachamkin, I., Reller, L.B., Osterholm, M.T., Bennish, M.L., Pickering, L.K. 2001. Practice guidelines for the management of infectious diarrhea. Clinical Infectious Diseases, 32: 331–351.

Harbarth, S., Samore, M.H. 2005. Antimicrobial Resistance Determinants and Future Control. Emerging Infectious Diseases, 11 (6): 794-801.

Helms, M., Simonsen, J., Molbak, K. 2004. Quinolone resistance is associated with increased risk of invasive illness or death during infection with Salmonella serotype Typhimurium. Journal of Infectious Diseases, 190: 1652–1654.

Kabir, S.M.L. 2010. Avian colibacillosis and Salmonellosis: A closer look at epidemiology, pathogenesis, diagnosis, control and public health concerns. International Journal of Environmental Research and Public Health, 7: 89–114.

Kijima-Tanaka, M., Ishihara, K., Morioka, A., Kojima, A., Ohzono, T., Ogikubo, K., Takahashi, T., Tamura, Y. 2003. A national surveillance of antimicrobial resistance in Escherichia coli isolated from food-producing animals in Japan. Journal of Antimicrobial Chemotherapy, 51: 447–451.
Kilonzo-Nthenge, A., Nahashon, S.N., Chen, F., Adefope, N. 2008. Prevalence and Antimicrobial Resistance of Pathogenic Bacteria in Chicken and Guinea Fowl. Poultry Science 87: 1841-1848.

MacPherson, D.W., Gushulak, B.D., Baine, W.B., Bala, S., Gubbins, P.O., Holtom, P., Segarra-Newnham, M. 2009. Population mobility, globalization, and antimicrobial drug resistance. Emerging Infectious Diseases, 15 (11): 1727–1732.

Momtaz, H., Rahimi, E., Moshkelani, S. 2012. Molecular detection of antimicrobial resistance genes in E. coli isolated from slaughtered commercial chickens in Iran. Veterinarni Medicina, 57 (4): 193–197.

Nataro. P., Kaper, J.B., 1998. Diarrhoeagenic Escherichia coli. Clinical Microbiology Reviews, 11(1): 142-201.

Ogunleye, A.O., Oyekunle, M.A., Sonibare, A.O. 2008. Multidrug resistant Escherichia coli isolates of poultry origin in Abeokuta, South Western Nigeria. Veterinarski Arhiv 78 (6): 501–509.

Osterloh, M. 2004. Transfer of antibiotic resistant genes between Escherichia coli and Salmonella typhimurum. Cantaurus, 12: 13-14.
Schwarz, S., Chaslus-Dancla, E. 2001. Use of antimicrobials in veterinary medicine and mechanisms of resistance. Veterinary Research 32: 201–225.

Silbergeld, E.K., Graham, J., Price, L.B., 2008. Industrial Food Animal Production, Antimicrobial Resistance, and Human Health. Annual Review of Public Health 29: 151-169.

Soulsby, L. 2007. Antimicrobials and animal health: a fascinating nexus. Journal of Antimicrobial Chemotherapy 60, Suppl. 1: i77–i78.

Statistical Package for Social Sciences (SPSS) version 16, 2007. SPSS Inc. 233 South Wacker Drive, 11th floor Chicago, Illinois 60606.

Stordeur, P., Marlier, D., Blanco, J., Oswald, E., Biet, F., Dho-Moulin, M., Mainil, J., 2002. Examination of Escherichia coli from poultry for selected adhesion genes important in disease caused by mammalian pathogenic E. coli. Veterinary Microbiology, 84: 231-241.

Sunde, M., Norström, M. 2006. The prevalence of, associations between and conjugal transfer of antibiotic resistance genes in Escherichia coli isolated from Norwegian meat and meat products. Journal of Antimicrobial Chemotherapy, 58 (4): 741-747.

Thorsteinsdottir, T.R., Haraldsson, G., Fridriksdottir, V., Kristinsson, K.G., Gunnarsson, E. 2010. Broiler Chickens as Source of Human Fluoroquinolone-Resistant
Escherichia coli, Iceland. Emerging Infectious Diseases, 16 (1): 133-135.

Van den Bograad, A.E., London, N., Driessen, C., Stobberingh, E.E., 2001. Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterers. Journal of Antimicrobial Chemotherapy, 47: 763-771.

Varga C., Rajić A., McFall M.E., Avery B.P., Reid-Smith R.J., Deckert A., Checkley S.L., McEwen S.A. 2008. Antimicrobial resistance in generic Escherichia coli isolated from swine faecal samples in 90 Alberta finishing farms. The Canadian Journal of Veterinary Research 72:175–180.

Warren, R.E., Ensor, V.M., O’Neill, P., Butler, V., Taylor, J., Nye, K., Harvey, M., Livermore, D.M., Woodford, N., Hawkey, P.M. 2008. Imported chicken meat as a potential source of quinolone-resistant Escherichia coli producing extended-spectrum β-lactamases in the UK. Journal of Antimicrobial Chemotherapy 61: 504–508.

White, D.G., Piddock, L.J.V., Maurer, J.J., Zhao, S., Ricci, V., Thayer, S.G. 2000. Characterization of Fluoroquinolone Resistance among Veterinary Isolates of Avian. Antimicrobial agents and Chemotherapy, 44 (10): 2897–2899.

WHO (World Health Organisation), 2001. WHO global strategy for containment of antimicrobial resistance. WHO/CDS/CSR/DRS/2001.2. Accessed 19th September, 2012.

WHO (World Health Organisation), 2007. Critically important antimicrobials for human medicine: categorization for the development of risk management strategies to contain antimicrobial resistance due to non-human antimicrobial use : report of the second WHO Expert Meeting, Copenhagen, 29-31 May 2007. Accessed 19th September, 2012.

Yaron, S., Kolling, G.L., Simon, L., Matthews, K.R. 2000. Vesicle-mediated transfer of virulence genes from Escherichia coli O157:H7 to other enteric bacteria. Applied and Environmental Microbiology, 66 (10): 4414–4420.

Zhao S., White D.G., Ge B. Ayers S., Friedman S., English L., Wagner D., Gaines S. and Meng J. 2001. Identification and characterization of integron-mediated antibiotic resistance among shiga toxin-producing Escherichia coli isolates. Applied and Environmental Microbiology 67 (4): 1558 – 1564.