Antimicrobial resistance in Enterococcus spp. isolated from environmental samples in an area of intensive poultry production

International Journal of Environmental Research and Public Health

Volumn 10, Issue 3, 2013, Pages 1020-1036

  Furtula, Vesna ^a   Jackson, Charlene R ^b   Farrell, Erin Gwenn ^a   Barrett, John B ^b   Hiott, Lari M ^b   Chambers, Patricia A ^a  

^a ENVIRONMENT CANADA   (Canada)

^b RUSSELL RESEARCH CENTER   (United States)

Author keywords

Antimicrobial; Contamination; Enterococci; Ground water; Poultry litter; Resistance; Surface water

Indexed keywords

ANTIINFECTIVE AGENT; CHLORAMPHENICOL; CIPROFLOXACIN; DALFOPRISTIN PLUS QUINUPRISTIN; DAPTOMYCIN; GENTAMICIN; GROUND WATER; KANAMYCIN; LINCOMYCIN; LINEZOLID; NITROFURANTOIN; PENICILLIN DERIVATIVE; SURFACE WATER; TETRACYCLINE; TIGECYCLINE; TYLOSIN;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; BACTERIUM; GROUNDWATER POLLUTION; HEALTH RISK; POULTRY;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COUNT; BACTERIUM DETECTION; BACTERIUM ISOLATE; BROILER; COLONY FORMING UNIT; CONTROLLED STUDY; ENTEROCOCCUS; ENTEROCOCCUS CASSELIFLAVUS; ENTEROCOCCUS DURANS; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ENTEROCOCCUS GALLINARUM; ENTEROCOCCUS HIRAE; ENTEROCOCCUS MUNDTII; ENTEROCOCCUS RAFFINOSUS; ENVIRONMENTAL MONITORING; GEOGRAPHIC DISTRIBUTION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; POULTRY FARMING; WATER SAMPLING;

EID: 84875247255     PISSN: 16617827     EISSN: 16604601     Source Type: Journal    
DOI: 10.3390/ijerph10031020     Document Type: Article

References (45)

1. Araujo, C.; Torres, C.; Silva, N.; Carneiro, C.; Goncalves, A.; Radhouani, H.; Correia, S.; da Costa, P.M.; Paccheco, R.; Zarazaga, M.; Ruiz-Larrea, F.; Poeta, P.; Igrejas, G. Vancomycin-resistant enterococci from Portuguese wastewater treatment plants. J. Basic Microbiol. 2010, 50, 605-609.
2. Lanthier, M.; Scott, A.; Zhang, Y.; Cloutier, M.; Durie, D.; Henderson, V.C.; Wilkes, G.; Lapen, D.R.; Topp, E. Distribution of selected virulence genes and antibiotic resistance in Enterococcus species isolated from the South Nation River drainage basin, Ontario, Canada. J. Appl. Microbiol. 2011, 110, 407-421.
3. Novo, A.; Manaia, C.M. Factors influencing antibiotic resistance burden in municipal wastewater treatment plants. Appl. Microbiol. Biotechnol. 2010, 87, 1157-1166.
4. Kotzamanidis, C.; Zdragas, A.; Kourelis, A.; Moraitou, E.; Papa, A.; Yiantzi, V.; Pantelidou, C.; Yiangou, M. Characterization of vanA-type Enterococcus faecium isolates from urban and hospital wastewater and pigs. J. Appl. Microbiol. 2009, 107, 997-1005.
5. Jackson, C.R.; Furtula, V.; Farrell, E.G.; Barrett, J.B.; Hiott, L.M.; Chambers, P. A comparison of BOX-PCR and pulsed-field gel electrophoresis to determine genetic relatedness of enterococci from different environments. Microb. Ecol. 2012, 64, 378-387.
6. Facklam, R.R.; Sahm, D.F.; Teixeiram, L.M. Enterococcus. In Manual of Clinical Microbiology, 7th ed.; Murray, P.R., Baron, E.J., Pfaller, M.A., Tenover, F.C., Yolken, R.H., Eds.; ASM Press: Washington, DC, USA, 1999; pp. 297-305.
7. Malani, P.N.; Kauffman, C.A.; Zervos, M.J. Enterococcal disease, epidemiology, and treatment. In The Enterococci: Pathogenesis, Molecular Biology, and Antibiotic Resistance; Gilmore, M.S., Clewell, D.B., Courvalin, P., Dunny, G.M., Murray, B.E., Rice, L.B., Eds.; ASM Press: Washington, DC, USA, 2002; pp. 385-408.
8. Cetinkaya, Y.; Falk, P.; Mayhall, C.G. Vancomycin-resistant enterococci. Clin. Microbiol. Rev. 2000, 13, 686-707.
9. Macedo, A.S.; Freitas, A.R.; Abreu, C.; Machado, E.; Peixe, L.; Sousa, J.C.; Novais, C. Characterization of antibiotic resistant enterococci isolated from untreated waters for human consumption in Portugal. Int. J. Food Microbiol. 2011, 145, 315-319.
10. McGowan, L.L.; Jackson, C.R.; Barrett, J.B.; Hiott, L.M.; Fedorka-Cray, P.J. Prevalence and antimicrobial resistance of enterococci isolated from retail fruits, vegetables, and meats. J. Food Prot. 2006, 69, 2976-2982.
11. Panda, S.K.; Patra, A.K.; Kar, R.N. Monitoring of multiple drug-resistant pathogens in a selected stretch of Bay of Bengal, India. Environ. Monit. Assess. 2011, 5, 83-98.
12. Murray, B.E. Diversity among multidrug-resistant enterococci. Emerg. Infect. Dis. 1998,4, 37-47.
13. Brooks, J.P.; Adeli, A.; Read, J.J.; McLaughlin, M.R. Rainfall simulation in greenhouse microcosms to assess bacterial-associated runoff from land-applied poultry litter. J. Environ. Qual. 2009, 38, 218-229.
14. Diarrassouba, F.; Diarra, M.S.; Bach, S.; Delaquis, P.; Pritchard, J.; Topp, E.; Skura, B.J. Antibiotic resistance and virulence genes in commensal Escherichia coli and Salmonella isolates from commercial broiler chicken farms. J. Food Prot. 2007, 70, 1316-1327.
15. Furtula, V.; Farrell, E.G.; Diarrassouba, F.; Rempel, H.; Pritchard, J.; Diarra, M.S. Veterinary pharmaceuticals and antibiotic resistance of Escherichia coli isolates in poultry litter from commercial farms and controlled feeding trials. Poult. Sci. 2010, 89, 180-188.
16. Kelley, T.R.; Pancorbo, O.C.; Merka, W.C.; Thompson, S.A.; Cabrera, M.L.; Barnhart, H.M. Bacterial pathogens and indicators in poultry litter during re-utilization. J. Appl. Poultry Res. 1995, 4, 366-373.
17. Graham, J.P.; Evans, S.L.; Price, L.B.; Silbergeld, E.K. Fate of antimicrobial-resistant enterococci and staphylococci and resistance determinants in stored poultry litter. Environ. Res. 2009, 109, 682-689.
18. Jenkins, M.B.; Truman, C.C.; Siragusa, G.; Line, E.; Bailey, J.S.; Frye, J.; Endale, D.M.; Franklin, D.H.; Schomberg, H.H.; Fisher, D.S.; Sharpe, R.R. Rainfall and tillage effects on transport of fecal bacteria and sex hormones 17beta-estradiol and testosterone from broiler litter applications to a Georgia Piedmont Ultisol. Sci. Total Environ. 2008, 403, 154-163.
19. Servais, P.; Passerat, J. Antimicrobial resistance of fecal bacteria in waters of the Seine river watershed (France). Sci. Total Environ. 2009, 408, 365-372.
20. Lata, P.; Ram, S.; Agrawal, M.; Shanker, R. Enterococci in river Ganga surface waters: Propensity of species distribution, dissemination of antimicrobial-resistance and virulence-markers among species along landscape. BMC Microbiol. 2009, 9, 140-149.
21. Moore, D.F.; Guzman, J.A.; McGee, C. Species distribution and antimicrobial resistance of enterococci isolated from surface and ocean water. J. Appl. Microbiol. 2008, 105, 1017-1025.
22. Furtula, V.; Jackson, C.R.; Osman, R.; Chambers, P.A. Use of Enterococcus, BST and sterols for poultry pollution source tracking in surface and groundwater. In Environmental Health-Emerging Issues and Practice; Oosthuizen, J., Ed.; InTech Open Access: Rijeka, Croatia, 2012; pp. 57-78.
23. Improved Enumeration Methods for the Recreational Water Quality Indicators: Enterococci and Escherichia coli; USEPA: Washington, DC, USA, 2000; pp. 1-49.
24. Jackson, C.R.; Fedorka-Cray, P.J.; Barrett, J.B. Use of a genus- and species-specific multiplex PCR for identification of enterococci. J. Clin. Microbiol. 2004, 42, 3558-3565.
25. Bacterial Epidemiology and Antimicrobial Resistance: NARMS-National Antimicrobial Resistance Monitoring System Animal Isolates. Available online: http://www.ars.usda.gov/Main/docs.htm?docid=6750&page=3 (accessed on 7 March 2013).
26. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically, 7th ed.; Clinical and Laboratory Standards Institute (CLSI): Villanova, PA, USA, 2006.
27. Performance Standards for Antimicrobial Susceptibility Testing, Seventh Informational Supplement; Clinical and Laboratory Standards Institute (CLSI): Wayne, PA, USA, 2007.
28. Krumperman, P.H. Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Appl. Environ. Microbiol. 1983, 46, 165-170.
29. The European Parliament and the Council of the European Union Directive. Available online: http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2006:064:0037:0051:EN:PDF (accessed on 29 October 2012).
30. Luczkiewicz, A.; Jankowska, K.; Kurlenda, J.; Olanczuk-Neyman, K. Identification and antimicrobial resistance of Enterococcus spp.isolated from surface water. Water Sci. Technol. 2010, 62, 466-473.
31. Thal, L.A.; Chow, J.W.; Mahayni, R.; Bonilla, H.; Perri, M.B.; Donabedian, S.A.; Silverman, J.; Taber, S.; Zervos, M.J. Characterization of antimicrobial resistance in enterococci of animal origin. Antimicrob. Agents Chemother. 1995, 39, 2112-2115.
32. Simjee, S.; White, D.G.; McDermott, P.F.; Wagner, D.D.; Zervos, M.J.; Donabedian, S.M.; English, L.L.; Hayes, J.R.; Walker, R.D. Characterization of Tn1546 in vancomycin-resistant Enterococcus faecium isolated from canine urinary tract infections: Evidence of gene exchange between human and animal enterococci. J. Clin. Microbiol. 2002, 40, 4659-4665.
33. Fedorka-Cray, P.J.; Englen, M.D.; Gray, J.T.; Hudson, C.; Headrick, M.L. Programs for monitoring antimicrobial resistance. Animal Biotech. 2002, 13, 43-55.
34. Fluit, A.C.; van der Bruggen, J.T.; Aarestrup, F.M.; Verhoef, J.; Jansen, W.T. Priorities for antibiotic resistance surveillance in Europe. Clin. Microbiol. Infect. 2006, 12, 410-417.
35. Butaye, P.; Devriese, L.A.; Haesebrouck, F. Differences in antibiotic resistance patterns of Enterococcus faecalis and Enterococcus faecium strains isolated from farm and pet animals. Antimicrob. Agents Chemother. 2001, 45, 1374-1378.
36. Petsaris, O.; Miszczak, F.; Gicquel-Bruneau, M.; Perrin-Guyomard, A.; Humbert, F.; Sanders, P.; Leclercq, R. Combined antimicrobial resistance in Enterococcus faecium isolated from chickens. Appl. Environ. Microbiol. 2005, 71, 2796-2799.
37. Butaye, P.; Baele, M.; Devriese, L.A.; Haesebrouck, F. Comparison of susceptibility to antimicrobials of the enterococcal species isolated from pigeons (Columba livia). Microb. Drug Resist. 2002, 8, 215-218.
38. Yoshimura, H.; Ishimaru, M.; Endoh, Y.S.; Kojima, A. Antimicrobial susceptibilities of enterococci isolated from faeces of broiler and layer chickens. Lett. Appl. Microbiol. 2000, 31, 427-432.
39. Ruzauskas, M.; Siugzdiniene, R.; Spakauskas, V.; Povilonis, J.; Seputiene, V.; Suziedeliene, E.; Daugelavicius, R.; Pavilonis, A. Susceptibility of bacteria of the Enterococcus genus isolated from Lithuanian poultry farms. Vet. Med. 2009, 54, 583-588.
40. Da Costa, P.M.; Belo, A.; Goncalves, J.; Bernardo, F. Field trial evaluating changes in prevalence and patterns of antimicrobial resistance among Escherichia coli and Enterococcus spp.isolated from growing broilers medicated with enrofloxacin, apramycin and amoxicillin. Vet. Microbiol. 2009, 139, 284-292.
41. Aslam, M.; Diarra, M.S.; Service, C.; Rempel, H. Characterization of antimicrobial resistance in Enterococcus spp. recovered from a commercial beef processing plant. Foodborne. Pathog. Dis. 2010, 7, 235-241.
42. Jacob, M.E.; Fox, J.T.; Narayanan, S.K.; Drouillard, J.S.; Renter, D.G.; Nagaraja, T.G. Effects of feeding wet corn distillers grains with solubles with or without monensin and tylosin on the prevalence and antimicrobial susceptibilities of fecal foodborne pathogenic and commensal bacteria in feedlot cattle. J. Anim. Sci. 2008, 86, 1182-1190.
43. Diarra, M.S.; Rempel, H.; Champagne, J.; Masson, L.; Pritchard, J.; Topp, E. Distribution of antimicrobial resistance and virulence genes in Enterococcus spp. and characterization of isolates from broiler chickens. Appl. Environ. Microbiol. 2010, 76, 8033-8043.
44. Hayes, J.R.; English, L.L.; Carr, L.E.; Wagner, D.D.; Joseph, S.W. Multiple-antibiotic resistance of Enterococcus spp. isolated from commercial poultry production environments. Appl. Environ. Microbiol. 2004, 70, 6005-6011.
45. Aarestrup, F.M.; Agerso, Y.; Gerner-Smidt, P.; Madsen, M.; Jensen, L.B. Comparison of antimicrobial resistance phenotypes and resistance genes in Enterococcus faecalis and Enterococcus faecium from humans in the community, broilers, and pigs in Denmark. Diagn. Microbiol. Infect. Dis. 2000, 37, 127-137.