Prevalence of Antimicrobial Resistance in Enterococci and Escherichia coli in Meat Chicken Flocks During a Production Cycle and Egg Layer Pullets During Rearing
DOI:
https://doi.org/10.3923/ijps.2014.489.503Keywords:
E. coli, enterococcal isolates, enterococci, free-range meat chickens, resistance genes, shed raised egg layer pulletsAbstract
Avian Pathogenic Escherichia coli (APEC) and some enterococci are important zoonotic pathogens associated with poultry and some human illnesses. This study was conducted to evaluate the phenotypic antibiotic resistance and resistance genes during the production cycle of healthy free-range meat chickens and egg layer pullets raised in two different controlled farms in South Australia, in particular to determine at which point in the production cycle birds become colonized with antibiotic resistant bacteria. Antibiotic resistance was investigated in faecal E. coli (206) and enterococcal (252) isolates by agar dilution and polymerase chain reaction. Southern hybridization was carried on plasmids from selected multi-resistant E. coli isolates to determine the location of resistance genes. Our results revealed that birds are colonized with resistant bacteria encoding various resistance genes from a very early age. Resistance to ampicillin and tetracycline (and associated resistance genes) were the most frequently detected resistances in E. coli isolates from egg layer pullets and free-range meat chickens. Phenotypically resistant enterococcal isolates from 3-5 days old chickens carried genetic determinants for resistance to tetracycline, bacitracin and tylosin. Whilst statistical analysis revealed there was no significant differences (p<0.05) with the phenotypic resistance observed in the E. coli and enterococcal isolates from meat chickens and egg layer pullets, a significant difference was observed in resistant E. coli isolates containing blaTEM and tet genes. This study demonstrates that newly hatched chicks are already colonized with resistant bacteria which persist through the production cycle and can potentially contaminate eggs and chicken carcasses. This study also confirms that poultry are a potential source of pathogenic E. coli strains.
References
Aarestrup, F.M., Y. Agerso, P.Gerner-Smith, M. Madsen and L.B. Jensen, 2000. Comparison of antimicrobial resistance phenotypes and resistance genes in Enterococcus faecalis and Enterococcus faecium from humans in the community, broilers and pigs in Denmark. Diagnostic Microbiol. Infect. Dis., 37: 127-137.
ACMF., 2010. Report of Australia meat federation-growing meat chickens. Australian Chicken Meat Federation Inc., Australia.
Aminov, R.I., N. Garrigues Jeanjean and R.I. Mackie, 2001. Molecular ecology of tetracycline resistance: Development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins. Applied Environ. Microbiol., 67: 22-32.
Barton, M.D., 2004. Antibiotic Susceptibility of Veterinary Isolates. In: Antimicrobial Susceptibility Testing: Methods and Practices with an Australian Perspective, Merlino, J. and M.D. Barton (Eds.). Australian Society for Microbiology, Syndey, Australia, pp: 231-240.
Bergenholtz, R.D., M.S. Jorgensen, L.H. Hansen, L.B. Jensen and H. Hasman, 2009. Characterization of genetic determinants of Extended-Spectrum Cephalosporinases (ESCs) in Escherichia coli isolates from Danish and imported poultry meat. J. Antimicrobial. Chemother., 64: 207-209.
CIPAS., 2005. Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS) 2005 annual report. Public Health Agency of Canada.
Clermont, O., S. Bonacorsi and E. Bingen, 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Applied Environ. Microbiol., 66: 4555-4558.
CLSI., 2008. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals; Approved Standard: Document M31-A3. 3rd Edn., Clinical and Laboratory Standards Institute, Wayne, PA pp: 1-95.
Crandall, P.G., S. Seideman, S.C. Ricke, C.A. O'Bryan, A.F. Fanatico and R. Rainey, 2009. Organic poultry: Consumer perceptions, opportunities and regulatory issues. J. Applied Poult. Res., 18: 795-802.
DANMAP., 2008. Use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, foods and humans in Denmark. http://www.danmap.org/~/media/Projekt%20sites/Danmap/DANMAP%20reports/Danmap_2008.ashx.
Deasy, B.M., M.C. Rea, G.F. Fitzgerald, T.M. Cogan and T.P. Beresford, 2000. A rapid PCR based method to distinguish between Lactococcus and Enterococcus. Syst. Applied Microbiol., 23: 510-522.
EUROPA., 2009. Effects of biocides on antibiotic resistance. http://ec.europa.eu/health/opinions/en/biocides-antibiotic-resistance/index.htm#il1.
Fertner, M.E., R.H. Olsen, M. Bisgaard and H. Christensen, 2011. Transmission and genetic diversity of Enterococcus faecalis among layer chickens during hatch. Acta Veterinaria Scandinavica, Vol. 53.
Fluit, A.C. and F.J. Schmitz, 2004. Resistance integrons and super-integrons. Clin. Microbiol. Infect., 10: 272-288.
Ginns, C.A., G.F. Browning, M.L. Benham, G.A. Anderson and K.G. Whithear, 1996. Antimicrobial resistance and epidemiology of Escherichia coli in broiler breeder chickens. Avian Pathol., 25: 591-605.
Hammerum, A.M. and O.E. Heuer, 2009. Human health hazards from antimicrobial-resistant Escherichia coli of animal origin. Clin. Infect. Dis., 48: 916-921.
Harisberger, M., S. Gobeli, R. Hoop, J. Dewulf, V. Perreten and G. Regula, 2011. Antimicrobial resistance in swiss laying hens, prevalence and risk factors. Zoonoses Public Health, 58: 377-387.
Higgins, J., C. Hohn, S. Hornor, M. Frana, M. Denver and R. Joerger, 2007. Genotyping of Escherichia coli from environmental and animal samples. J. Microbiol. Meth., 70: 227-235.
Ho, P.L., R.H.L. Shek, K.H. Chow, R.S. Duan and G.C. Mak et al., 2005. Detection and characterization of extended-spectrum β-lactamases among bloodstream isolates of Enterobacter spp. in Hong Kong, 2000-2002. J. Antimicrobial. Chemother., 55: 326-332.
Jackson, C.R., P.J. Fedorka Cray and J.B. Barrett, 2004. Use of a genus and species specific multiplex PCR for identification of Enterococci. J. Clin. Microbiol., 42: 3558-3565.
Jakobsen, L., P. Garneau, A. Kurbasic, G. Bruant and M. Stegger et al., 2011. Microarray-based detection of extended virulence and antimicrobial resistance gene profiles in phylogroup B2 Escherichia coli of human, meat and animal origin. J. Med. Microbiol., 60: 1502-1511.
Johnson, J.R. and A.L. Stell, 2001. Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J. Infect. Dis., 181: 216-272.
Lapierre, L., J. Cornejo, C. Borie, C. Toro and B.S. Martin, 2000. Genetic characterization of antibiotic resistance genes linked to class 1 and class 2 integrons in commensal strains of Escherichia coli isolated from poultry and swine. Microbial. Drug Resist., 14: 265-272.
Michel, L.M., S. Anders and W.V. Wismer, 2011. Consumer preferences and willingness to pay for value-added chicken product attributes. J. Food Sci., 76: S469-S477.
Maturana, V.G., F. de Pace, C. Carlos, M.M. Pires and T.A. de Campos et al., 2011. Subpathotypes of avian pathogenic Escherichia coli (APEC) exist as defined by their syndromes and virulence traits. Open Microbiol. J., 5: 55-64.
Maynard, C., S. Bekal, F. Sanschagrin, R.C. Levesque and R. Brousseau et al., 2004. Heterogeneity among virulence and antimicrobial resistance gene profiles of extraintestinal Escherichia coli isolates of animal and human origin. J. Clin. Microbiol., 42: 5444-5452.
Obeng, A.S., H. Rickard, O. Ndi, M. Sexton and M. Barton, 2012. Antibiotic resistance, phylogenetic grouping and virulence potential of Escherichia coli isolated from the faeces of intensively farmed and free range poultry. Vet. Microbiol., 154: 305-315.
Obeng, A.S., H. Rickard, O. Ndi, M. Sexton and M. Barton, 2012. Comparison of antimicrobial resistance patterns in enterococci from intensive and free range chickens in Australia. Avian Pathol., 42: 45-54.
Oberholtzer, L., C. Greene and E. Lopez, 2006. Organic poultry and eggs capture high price premiums and growing share of specialty markets. USDA Outlook Report from the Economic Research Service. http://www.ers.usda.gov/media/866670/ldpm15001_002.pdf.
Ozaki, H., H. Esaki, K. Takemoto, A. Ikeda and Y. Nakatani et al., 2011. Antimicrobial resistance in fecal Escherichia coli isolated from growing chickens on commercial broiler farms. Vet. Microbiol., 150: 132-139.
Pitout, J.D.D., K.S. Thompson, N.D. Hanson, A.F. Ehrhardt, E.S. Moland and C.C. Sander, 1998. β-lactamases responsible for resistance to expanded-spectrum cephalosporins in Klebsiella pneumoniae, Escherichia coli and Proteus mirabilis isolates recovered in South Africa. Antimicrob. Agents Chemother., 42: 1350-1354.
Sapkota, A.R., R.M. Hulet, G. Zhang, P. McDermott, E.L. Kinney, K.J. Schwab and S.W. Joseph, 2011. Lower prevalence of antibiotic-resistant Enterococci on U.S. conventional poultry farms that transitioned to organic practices. Environ. Health Perspect., 119: 1622-1628.
Schwaiger, K., E.M.V. Schmied and J. Bauer, 2010. Comparative analysis on antibiotic resistance characteristics of Listeria spp. and Enterococcus spp. isolated from laying hens and eggs in conventional and organic keeping systems in Bavaria, Germany. Zoonoses Public Health, 57: 171-180.
Silva, N., G. Igrejas, A. Goncalves and P. Poeta, 2012. Commensal gut bacteria: distribution of enterococcus species and prevalence of escherichia coli phylogenetic groups in animals and humans in portugal. Annal. Microbiol, 62: 449-459.
Thibodeau, A., S. Quessy, E. Guevremont, A. Houde, E. Topp, M.S. Diarra and A. Letellier, 2008. Antibiotic resistance in Escherichia coli and Enterococcus spp. isolates from commercial broiler chickens receiving growth-promoting doses of bacitracin or virginiamycin. Can. J. Vet. Res., 72: 129-136.
Vahaboglu, H., R. Ozturk, H. Akbal, S. Saribas, O. Tansel and F. Coskunkan, 1998. Practical approach for detection and identification of OXA 10 derived ceftazidime hydrolyzing extended spectrum β lactamases. J. Clin. Microbiol., 36: 827-829.
Van den Bogaard, A.E., N. London, C. Driessen and E.E. Stobberingh, 2001. Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterers. J. Antimicrob. Chemother., 47: 763-771.
Van Hoorebeke, S., F. Van Immerseel, A.C. Berge, D. Persoons and J. Schulz et al., 2012. Antimicrobial resistance of Escherichia coli and Enterococcus faecalis in housed laying-hen flocks in Europe. Epidemiol. Infect., 139: 1610-1620.
Xia, X., J. Meng, S. Zhao, S. Bodeis-Jones, S.A. Gaines, S.L. Ayers and P.F. McDermott, 2011. Identification and antimicrobial resistance of extraintestinal pathogenic Escherichia coli from retail meats. J. Food Protect., 74: 38-44.
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