Characterization of antimicrobial resistance and virulence genes in Enterococcus spp. isolated from retail meats in Alberta, Canada

International Journal of Food Microbiology

Volumn 156, Issue 3, 2012, Pages 222-230

  Aslam, Mueen ^a   Diarra, Moussa S ^b   Checkley, Sylvia ^c   Bohaychuk, Valerie ^d   Masson, Luke ^e  

^a LACOMBE RESEARCH CENTRE   (Canada)

^b SUMMERLAND RESEARCH AND DEVELOPMENT CENTRE   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

^d ALBERTA AGRICULTURE AND RURAL DEVELOPMENT   (Canada)

^e NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

Antimicrobial resistance; Enterococcus spp. retail meats; Resistance genes; Virulence genes

Indexed keywords

AMINOGLYCOSIDE; BACITRACIN; CHLORAMPHENICOL; CIPROFLOXACIN; CYTOLYSIN; DAPTOMYCIN; ERYTHROMYCIN; GENTAMICIN; KANAMYCIN; LINCOMYCIN; LINCOSAMIDE; LINEZOLID; MACROLIDE; NITROFURANTOIN; PENICILLIN G; QUINUPRISTIN; STREPTOGRAMIN; STREPTOMYCIN; TETRACYCLINE; TIGECYCLINE; TYLOSIN; VANCOMYCIN;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BEEF; CANADA; CHICKEN MEAT; CONTROLLED STUDY; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; GENE IDENTIFICATION; GENOTYPE; MEAT; NONHUMAN; PHENOTYPE; PORK; PREVALENCE;

ALBERTA; ANIMALS; ANTI-BACTERIAL AGENTS; CATTLE; CHICKENS; COMMERCE; DRUG RESISTANCE, BACTERIAL; ENTEROCOCCUS; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; GENES, BACTERIAL; MEAT; MICROBIAL SENSITIVITY TESTS; POULTRY; SWINE; TURKEYS; VIRULENCE; VIRULENCE FACTORS;

ENTEROCOCCUS; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM;

EID: 84861006573     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2012.03.026     Document Type: Article

References (42)

1. 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. Diagnostic Microbiology and Infectious Disease 2000, 37:127-137.
2. Aslam M., Diarra M.S., Service C, Rempel H. Antimicrobial resistance genes in Escherichia coli isolates recovered from a commercial beef processing plant. Journal of Food Protection 2009, 72:1089-1093.
3. Aslam M., Diarra M.S., Service C., Rempel H. Characterization of antimicrobial resistance in Enterococcus spp. recovered from a commercial beef processing plant. Foodborne Pathogens and Disease 2010, 7:235-241.
4. Boerlin P., Travis R., Gyles C.L., Reid-Smith R., Janecko N., Lim H., Nicholson V., McEwen S.C., Friendship R., Archambault M. Antimicrobial resistance and virulence genes of Escherichia coli isolates from swine in Ontario. Applied and Environmental Microbiology 2005, 71:6753-6761.
5. Borgen K., Sørum M., Wasteson Y., Kruse H. VanA-type vancomycin-resistant enterococci (VRE) remain prevalent in poultry carcasses 3years after avoparcin was banned. International Journal of Food Microbiology 2001, 64:89-94.
6. Cauwerts K., Decostere A., De Graef E.M., Haesebrouck F., Pasmans F. High prevalence of tetracycline resistance in Enterococcus isolates from broilers carrying the erm(B) gene. Avian Pathology 2007, 36:395-399.
7. Champagne J., Diarra M.S., Rempel H., Topp E., Greer C.W., Harel J., Masson L. Development of a DNA microarray for enterococcal species, virulence, and antibiotic resistance gene determinations among isolates from poultry. Applied and Environmental Microbiology 2011, 77:2625-2633.
8. CIPARS Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS) Annual Report 2007, Public Health Agency of Canada Guelph, Ontario, Canada.
9. CIPARS Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS) Preliminary Report 2009, Public Health Agency of Canada Guelph, Ontario, Canada.
10. CLSI Clinical and Laboratory Standards Institute. 20th Informational Supplement 2010, Vol 30. No.1. M100-S20. Wayne, PA. USA.
11. Coque M.T. Evolutionary biology of pathgogeinc enterococci. P501-521. Evolutionary Biology of Bacterial and Fungal Pathogens 2008, ASM press, Washington, DC. USA. F. Baquero, C. Nombela, G.H. Gassel, J.A. Guitierrez (Eds.).
12. DANMAP, DANMAP Use of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Bacteria from Food Animals, Foods and Humans in Denmark. Copenhagen. Denmark Accessed April 2011. http://www.danmap.org/pdfFiles/Danmap_2009.pdf.
13. Del Grosso M., Caprioli A., Chinzari P., Fontana M.C., Pezzotti G., Manfrin A., Giannatale E.D., Goffredo E., Pantosti A. Detection and characterization of vancomycin-resistant enterococci in farm animals and raw meat products in Italy. Microbiology and Drug Resistance 2000, 6:313-318.
14. Diarra M.S., Silversides F.G., Diarrassouba F., Pritchard J., Masson L., Brousseau R., Bonnet C., Delaquis P., Bach S., Skura B.J., Topp E. Impact of feed supplementation with antimicrobial agents on growth performance of broiler chickens, Clostridium perfringens and Enterococcus counts, and antibiotic resistance phenotypes and distribution of antimicrobial resistance determinants in Escherichia coli isolates. Applied and Environmental Microbiology 2007, 73:6566-6576.
15. 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 chicken. Applied and Environmental Microbiology 2010, 76:8033-8043.
16. Eaton T.J., Gasson M.J. Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Applied and Environmental Microbiology 2001, 67:1628-1635.
17. Gales A.C., Sader H.S., Fritsche T.R. Tigecycline activity tested against 11808 bacterial pathogens recently collected from US medical centers. Diagnostic Microbiology and Infectious Disease 2008, 60:421-427.
18. Garneau P., Labrecque O., Maynard C., Messier S., Masson L., Archambault M., Harel J. Use of a bacterial antimicrobial resistance gene microarray for the identification of resistant Staphylococcus aureus. Zoonoses and Public Health 2010, 57:94-99.
19. Gilmore M.S., Coburn P.S., Nallapareddy S.R., Murray B.E. Enterococcal virulence. The Enterococci: Pathogenesis, Molecular Biology, and Antibiotic Resistance 2002, 301-354. ASM Press, Washington, DC. M.S. Gilmore, D.B. Clewell, P. Courvalin, G.M. Dunny, B.E. Murray, L.S. Rice (Eds.).
20. Grossi P.A. Early appropriate therapy of Gram-positive bloodstream infections: the conservative use of new drugs. International Journal of Antimicrobial Agents 2009, 34:S31-S34.
21. Hamelin K., Bruant G., El-Shaarawi A., Hill S., Edge T.A., Fairbrother J., Harel J., Maynard C., Masson L., Brousseau R. Occurrence of virulence and antimicrobial resistance genes in Escherichia coli isolates from different aquatic ecosystems within the St. Clair River and Detroit River areas. Applied and Environmental Microbiology 2007, 73:477-484.
22. Hancock L.E., Gilmore M.S. Pathogenicity of enterococci. Gram Positive Pathogens 2006, 299-311. ASM press, Washington, D.C. 2nd Ed. V.A. Fischetti, R.P. Novick, D.A. Portnoy, J.I. Rood (Eds.).
23. Hawkey P.M. The growing burden of antimicrobial resistance. The Journal of Antimicrobial Chemotherapy 2008, 62(Suppl. 1):i1-i9.
24. Hayes J.R., English L.L., Carter P.J., Proescholdt T., Lee K.Y., Wagner D.D., White D.G. Prevalence and antimicrobial resistance of Enterococcus species isolated from retail meats. Applied and Environmental Microbiology 2003, 69:7153-7160.
25. 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. Applied and Environmental Microbiology 2004, 70:6005-6011.
26. Hegstad K., Mikalsen T., Coque T.M., Werner G., Sundsfjord A. Mobile genetic elements and their contribution to the emergence of antimicrobial resistant Enterococcus faecalis and Enterococcus faecium. Clinical Microbiology and Infection 2010, 16:541-554.
27. Hummel A., Holzapfel W.H., Franz C.M.A.P. Characterization and transfer of antibiotic resistance genes from enterococci isolated from food. Systematic and Applied Microbiology 2007, 30:1-7.
28. Jackson C.R., Fedorka-Cray P.J., Barrett J.B. Use of genus- and species-specific multiplex PCR for identification of enterococci. Journal of Clinical Microbiology 2004, 42:3558-3565.
29. Jackson C.R., Fedorka-Cray P.J., Barrett J.B., Hiott L.M., Woodley T.A. Prevalence of streptogramin resistance in enterococci from animals: identification of vatD from animal sources in the USA. International Journal of Antimicrobial Agents 2007, 30:60-66.
30. Johnson A.P., Livermore D.M. Quinupristin/dalfopristin, a new addition to the antimicrobial arsenal. Lancet 1999, 354:2012-2015.
31. Mannu L., Paba A., Daga E., Comunian R., Zanetti S., Duprè I., Sechi L.A. Comparison of the incidence of virulence determinants and antibiotic resistance between Enterococcus faecium strains of dairy, animal and clinical origin. International Journal of Food Microbiology 2003, 88:294-304.
32. Matos R. Study on the dissemination of the bcrABDR cluster in Enterococcus spp. reveals that the bcrAB transporter is sufficient to confer high-level bacitracin resistance. International Journal of Antimicrobial Agents 2009, 34:142-147.
33. McGowan-Spicer L.L., Fedorka-Cray P.J., Frye J.G., Meinersmann R.J., Barrett J.B., Jackson C.R.J. Antimicrobial resistance and virulence of Enterococcus faecalis isolated from retail food. Journal of Food Protection 2008, 71:760-769.
34. NARMS National Antimicrobial Resistance Monitoring System: Retail Meat Annual Report Accessed May 2011. http://www.fda.gov/AnimalVeterinary/SafetyHealth/AntimicrobialResistance/NationalAntimicrobialResistanceMonitoringSystem/ucm237109.htm.
35. Ogier J.-C., Serror P. Safety assessment of dairy microorganisms: The Enterococcus genus. International Journal of Food Microbiology 2008, 126:291-301.
36. Pierson M.D., Zink D.L., Smoot L.M. Indicator microorganisms and microbiological criteria. Food microbiology: Fundamentals and Frontiers 2007, 69-85. ASM Press, Washington, DC. 3rd ed. M.P. Doyle, L.R. Beuchat (Eds.).
37. Rizzotti L., Simeoni D., Cocconcelli P., Gazzola S., Dellaglio F., Torriani S. Contribution of enterococci to the spread of antibiotic resistance in the production chain of swine meat commodities. Journal of Food Protection 2005, 68:955-965.
38. Statistical Analysis System Release 8.02 2000, SAS Institute, Inc., Cary, NC.
39. Šustáková A., Nápravníková E., Schlegelová J. Antimicrobial resistance of Enterococcus spp. isolates from raw beef and meat products. Folia Microbiologica 2004, 49:411-417.
40. Valenzuela A.S., Omar N.B., Abriouel H., López R.L., Veljovic K., Cañamero M.M., Milan, Topisirovic M.K.L., Gálvez A. Virulence factors, antibiotic resistance, and bacteriocins in enterococci from artisan foods of animal origin. Food Control 2009, 20:381-385.
41. Veterinary Drugs Directorate Proposed categorization of antimicrobial drugs. Current Thinking on Risk Management Measures to Address Antimicrobial Resistance Associated with the Use of Antimicrobial Agents in Food-producing Animals 2005, http://www.hc-sc.gc.ca/dhp-mps/vet/antimicrob/amr-ram_rep-rap_06_05-eng.php Accessed July 2011.
42. Werner G., Hildebrandt B., Witte W. Aminoglycoside-Streptothricin resistance gene cluster aadE-sat4-aphA-3 disseminated among multiresistant isolates of Enterococcus faecium. Antimicrobial Agents and Chemotherapy 2001, 45:3267-3269.