Evaluation of drug-resistant Enterobacteriaceae in retail poultry and beef

Poultry Science

Volumn 92, Issue 4, 2013, Pages 1098-1107

  Kilonzo Nthenge, A ^a   Rotich, E ^a   Nahashon, S N ^a  

^a TENNESSEE STATE UNIVERSITY   (United States)

Author keywords

Antibiotic resistance; Beef; Enterobacteriaceae; Poultry

Indexed keywords

EID: 84875025814     PISSN: 00325791     EISSN: 15253171     Source Type: Journal    
DOI: 10.3382/ps.2012-02581     Document Type: Article

References (65)

1. Aarestrup, F. M., A. M. Seyfarth, H. D. Emborg, K. Pedersen, R. S. Hendriksen, and F. Bager. 2001. Effect of abolishment of the use of antimicrobial agents for growth promotion on occurrence of antimicrobial resistance in fecal enterococci from food animals in Denmark. Antimicrob. Agents Chemother. 45:2054-2059.
2. Andersson, D. I. 2003. Persistence of antibiotic resistant bacteria. Curr. Opin. Microbiol. 6:452-456.
3. Barham, A. R., B. L. Barham, A. K. Johnson, D. M. Allen, J. R. Blanton, and F. M. Miller. 2002. Effects of the transportation of beef cattle from the feed yard to the packaging plant on prevalence levels of Escherichia coli O157 and Salmonella spp. J. Food Prot. 65:280-283.
4. Belanger, A. E., and T. R. Shryock. 2007. Macrolide-resistant Campylobacter: The meat of the matter. J. Antimicrob. Chemother. 60:715-723.
5. Berrang, M. E., S. R. Ladely, R. J. Meinersmann, and P. J. Fedorka-Cray. 2007. Sub therapeutic tylosin phosphate in broiler feed affects Campylobacter on carcasses during processing. Poult. Sci. 86:1229-1233.
6. Carattoli, A. 2009. Resistance plasmid families in Enterobacteriaceae. Antimicrob. Agents Chemother. 53:2227-2238.
7. Castanon, J. I. R. 2007. History of the use of antibiotic as growth promoters in European poultry feeds. Poult. Sci. 86:2466-2471.
8. Catry, B., H. Laevens, L. A. Devriese, G. Opsomer, and A. De Kruif. 2003. Antimicrobial resistance in livestock. J. Vet. Pharmacol. Ther. 26:81-93.
9. Chen, J., L. Zhang, G. C. Paoli, C. Shi, S. Tu, and X. Shi. 2010. A real-time PCR method for the detection of Salmonella enterica from food using a target sequence identified by comparative genomic analysis. Int. J. Food Microbiol. 137:168-174.
10. Chikwendu, C. I., R. N. Nwabueze, and B. N. Anyanwu. 2008. Antibiotic resistance profile of Escherichia coli from clinically healthy pigs and their commercial farm environments. African. J. Microbiol. Res. 2:012-017.
11. Clinical Laboratory Standards Institute (CLSI). 2009. Performance Standards for Antimicrobial Disk Susceptibility Test approved standard, 10th ed. Clinical and Laboratory Standards Institute, Wayne, PA.
12. Cogan, T. A., S. F. Bloomfield, and T. J. Humphrey. 1999. The effectiveness of hygiene procedures for prevention of cross contamination from chicken carcasses in the domestic kitchen. Lett. Appl. Microbiol. 29:354-358.
13. Doyle, M. P., and M. C. Erickson. 2006. Reducing the carnage of foodborne pathogens in livestock and poultry. Poult. Sci. 85:960-973.
14. Doyle, M. P., and J. L. Schoeni. 1987. Isolation of Escherichia coli0157:H7 from retail fresh meats and poultry. Appl. Environ. Microbiol. 53:2394-2396.
15. Dunowska, M., P. S. Morley, J. L. Traub-Dargatz, D. R. Hyatt, and D. A. Dargatz. 2006. Impact of hospitalization and antimicrobial drug administration on antimicrobial susceptibility patterns of commensal Escherichia coli isolated from the feces of horses. J. Am. Vet. Med. Assoc. 228:1909-1917.
16. Fernandes, R., A. Gestoso, J. M. Freitas, P. Santos, and C. Prudêncio. 2009. High resistance to fourth-generation cephalosporins among clinical isolates of Enterobacteriaceae producing extendedspectrum beta-lactamases isolated in Portugal. Int. J. Antimicrob. Agents 33:184-185.
17. Fluckey, W. M., G. H. Loneragan, R. Warner, and M. M. Brashears. 2007. Antimicrobial drug resistance of Salmonella and Escherichia coli isolates from cattle feces, hides, and carcasses. J. Food Prot. 70:551-556.
18. Foley, S. L., A. M. Lynne, and R. Nayak. 2008. Salmonella challenges: Prevalence in swine and poultry and potential pathogenicity of such isolates. J. Anim. Sci. 86(E. Suppl.):E149-E162.
19. Gomez-Lus, R. 1998. Evolution of bacterial resistance to antibiotics during the last three decades. Int. Microbiol. 1:279-284.
20. Gorman, R., S. F. Bloomfield, and C. Adley. 2002. A study of crosscontamination of foodborne pathogens in the domestic kitchen in the Republic of Ireland. Int. J. Food Microbiol. 76:143-150.
21. Harrison, W.A., C. J. Griffith, T. D. Tennan, and A. C. Peters. 2001. Incidence of Campylobacter and Salmonella isolated from retail chicken and associated packaging in South Wales. Lett. Appl. Microbiol. 33:450-454.
22. Hayes, J. R., L. L. English, L. E. Carr, D. D. Wagner, and S. W. Joseph. 2004. Multiple-antibiotic resistance of Enterococcus spp. isolated from commercial poultry production environments. Appl. Environ. Microbiol. 70:6005-6011.
23. Holmberg, S. D., M. T. Osterholm, K. A. Senger, and M. L. Cohen. 1984. Drug-resistant Salmonella from animals fed antimicrobials. N. Engl. J. Med. 311:617-622.
24. Iwabuchi, E., S. Yamamoto, Y. Endo, T. Ochiai, and K. Hirai. 2011. Prevalence of Salmonella isolates and antimicrobial resistance patterns in chicken meat throughout Japan. J. Food Prot. 74:270-273.
25. Karlowsky, J. A., M. E. Jones, C. Thornsberry, I. R. Friedland, and D. F. Sahm. 2003. Trends in antimicrobial susceptibilities among Enterobacteriaceae isolated from hospitalized patients in the United States from 1998 to 2001. J. Antimicrob. Agents Chemother. 47:1672-1680.
26. Kegode, R. B., D. K. Doetkott, M. L. Khaitsa, and I. V. Wesley. 2008. Occurrence of Campylobacter species, Salmonella species and generic Escherichia coli in meat products from retail outlets in the Fargo metropolitan area. J. Food Saf. 28:111-125.
27. Kennedy, J., I. S. Blair, D. A. McDowell, and D. J. Bolton. 2005. The microbial status of nonfood contact surfaces in domestic kitchens and the growth of Staphylococcus aureus in domestic refrigerators. Food Prot. Trends 25:974-980.
28. Kim, J.-S., D. K. Carver, and S. Kathariou. 2006. Natural transformation-mediated transfer of erythromycin resistance in Cam-pylobacter coli strains from turkeys and swine. Appl. Environ. Microbiol. 72:1316-1321.
29. Kim, S. H., C. I. Wei, and H. An. 2005. Multidrug-resistant Klebsiella pneumonia isolated from farm environments and retail products in Oklahoma. J. Food Prot. 10:2022-2029.
30. Knezevic, P., and O. Petrovic. 2008. Antibiotic resistance of commensal Escherichia coli of food-producing animals from three Vojvodinian farms. Serbia. Int. J. Antimicrob. Agents 31:360-363.
31. Kolpin, D. W., E. Furlong, M. Meyer, E. M. Thurman, and S. Zaugg. 2002. Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999-2000: A national reconnaissance. Environ. Sci. Technol. 36:1202-1211.
32. LeJeune, J. T., and N. P. Christie. 2004. Microbiological quality of ground beef from conventionally-reared cattle and 'Raised without antibiotics' label claims. J. Food Prot. 67:1433-1437.
33. Li, X., and H. H. Wang. 2010. Tetracycline resistance associated with commensal bacteria from representative ready-to-consume deli and restaurant foods. J. Food Prot. 73:1841-1848.
34. Lundeen, T., ed. 2008. Erythromycin. Page 251 in Feed Additive Compendium. The Miller Publishing Company, Minnetonka, MN, and The Animal Health Institute, Washington, DC.
35. Madden, R. H., K. A. Murray, and A. Gilmore. 2004. Determination of principal points of product contamination during beef carcass dressing process in Northern Ireland. J. Food Prot. 67:1494-1496.
36. Mainali, C., G. Gensler, M. McFall, R. King, R. Irwin, and A. Senthilselvan. 2009. Evaluation of association between feed withdrawal and other management factors with Salmonella contamination of broiler chickens at slaughter in Alberta. J. Food Prot. 72:2202-2207.
37. Massé, D. I., D. Lu, L. Masse, and R. L. Droste. 2000. Effect of antibiotics on psychrophilic anaerobic digestion of swine manure slurry in sequencing batch reactors. Bioresour. Technol. 75:205-211.
38. Mattick, K., K. Durham, G. Domingue, F. Jorgensen, M. Sen, D. W. Schaffner, and T. Humphrey. 2003. The survival of foodborne pathogens during domestic washing-up and subsequent transfer onto washing-up sponges, kitchen surfaces and food. Int. J. Food Microbiol. 85:213-226.
39. McEwen, S. A., and P. J. Fedorka-Cray. 2002. Antimicrobial use and resistance in animals. Clin. Infect. Dis. 34:S93-S106.
40. McGowan, J. E., Jr. 2001. Economic impact of antimicrobial resistance. Emerging Infect. Dis. 7:286-292.
41. Mead, P. S., L. Slutsker, V. Dietz, L. F. McCaig, J. S. Bresee, C. Shapiro, P. M. Griffin, and R. V. Tauxe. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5:607-625.
42. Meldrum, R. J., D. Tucker, R. M. Smith, and C. Edwards. 2005. Survey of Salmonella and Campylobacter contamination of whole, raw poultry on retail sales in Wales in 2003. J. Food Prot. 70:1447-1449.
43. National Academy of Sciences Committee on Drug Use in Food Animals. 1999. The Use of Drugs in Food Animals: Benefits and Risks. Natl. Acad. Press, Washington, DC.
44. Poppe, C., L. Martin, A. Muckle, M. Archambault, S. Mcewen, and E. Weir. 2006. Characterization of antimicrobial resistance of Salmonella Newport isolated from animals, the environment, and animal food products in Canada. Can. J. Vet. Res. 70:105-114.
45. Pothuluri, J. V., M. Nawaz, and C. E. Cerniglia. 1998. Environmental fate of antibiotics used in aquaculture. Pages 221-248 in Bioremediation: Principles and Practice, Biodegradation Technology Developments, Volume 2. S. K. Sikdar and R. L. Irvine, ed. Technomic Publ. Co., Lancaster, PA.
46. Price, L. B., J. P. Graham, L. G. Lackey, A. Roess, R. Vailes, and E. Silbergeld. 2007. The persistence of fluoroquinolone-resistant Campylobacter in poultry production. Environ. Health Perspect. 115:1035-1039.
47. Rasschaert, G., K. Houf, and L. De Zutter. 2007. Impact of slaughter line contamination on the presence of Salmonella on broiler carcasses. J. Appl. Microbiol. 103:333-341.
48. Schroeder, C. M., D. G. White, B. Ge, Y. Zhang, P. F. McDermott, S. Ayers, S. Zhao, and J. Meng. 2003. Isolation of antimicrobialresistant Escherichia coli from retail meats purchased in Greater Washington, DC, USA. Int. J. Food Microbiol. 85:197-202.
49. Schroeder, C. M., D. G. White, and J. Meng. 2004. Retail meat and poultry as a reservoir of antimicrobial-resistant Escherichia coli. Food Microbiol. 21:249-255.
50. Scott, E., S. F. Bloomfield, and C. G. Barlow. 1982. An investigation of microbial contamination in the home. J. Hyg. Camb. 89:279-293.
51. Shea, K. M. 2004. Nontherapeutic use of antimicrobial agents in animal agriculture: Implications for pediatrics. Pediatrics 114:862-868.
52. Simeoni, D., L. Rizzotti, P. Cocconcelli, S. Gazzola, F. Dellaglio, and S. Torriani. 2008. Antibiotic resistance genes and identification of staphylococci collected from the production chain of swine meat commodities. Food Microbiol. 25:196-201.
53. Singer, R. S., and C. L. Hofacre. 2006. Potential impacts of antibiotic use in poultry production. Avian Dis. 50:161-172.
54. Sorum, H., and M. Sunde. 2001. Resistance to antibiotics in the normal flora of animals. Vet. Res. 32:227-241.
55. Spiers, J. P., A. Anderson, and J. G. Anderson. 1995. A study of the microbial content of the domestic kitchen. Int. J. Environ. Health Res. 5:109-122.
56. Stiles, M. E., and L. Ng. 1981a. Biochemical characteristics and identification of Enterobacteriaceae isolated from meats. Appl. Environ. Microbiol. 41:639-645.
57. Stiles, M. E., and L. Ng. 1981b. Enterobacteriaceae associated with meats and meat handling. Appl. Environ. Microbiol. 41:867-872.
58. Troutt, H. F., and B. I. Osburn. 1997. Meat from dairy cows: Possible microbiological hazards and risks. Rev. Sci. Tech. 16:405-414.
59. Van, T. T., G. Moutafis, T. Istivan, T. L. Tran, and P. J. Coloe. 2007. Detection of Salmonella spp. in retail raw food samples from Vietnam and characterization of their antibiotic resistance. Appl. Environ. Microbiol. 73:6885-6890.
60. Welton, L. A., L. A. Thal, M. B. Perri, S. Donabedian, J. McMahon, J. W. Chow, and M. J. Ervos. 1998. Antimicrobial resistance in enterococci isolated from turkey flocks fed virginiamycin. Antimicrob. Agents Chemother. 42:705-708.
61. White, D. G, S. Zhao, R. Sudler, S. Ayers, S. Friedman, S. Chen, P. F. Mcdermott, D. D. Wagner, and J. Meng. 2001. The isolation of antibiotic-resistant Salmonella from retail ground meats. N. Engl. J. Med. 345:1147-1154.
62. Witte, W. 1998. Medical consequences of antibiotic use in agriculture. Science 279:996-997.
63. Wong, T., R. J. Whyte, A. J. Cornelius, and J. A. Hudson. 2004. Enumeration of Campylobacter and Salmonella on chicken packs. Br. Food J. 9:651-662.
64. Wong, T. L., L. Hollis, A. Cornelius, C. Nicol, R. Cook, and J. A. Hudson. 2007. Prevalence, numbers and subtypes of Campylobacter coli in uncooked retail meat samples. J. Food Prot. 70:566-573.
65. Zhao, T., M. P. Doyle, P. J. Fedorka-Cray, P. Zhao, and S. Ladel. 2002. Occurrence of Salmonella enterica serotype Typhimurium DT104A in retail ground beef. J. Food Prot. 65:403-407.