Effects of chlortetracycline and copper supplementation on the prevalence, distribution, and quantity of antimicrobial resistance genes in the fecal metagenome of weaned pigs

Preventive Veterinary Medicine

Volumn 119, Issue 3-4, 2015, Pages 179-189

  Agga, Getahun E ^a,c   Scott, H Morgan ^a   Vinasco, Javier ^a   Nagaraja, T G ^a   Amachawadi, Raghavendra G ^a   Bai, Jianfa ^a   Norby, Bo ^b   Renter, David G ^a   Dritz, Steve S ^a   Nelssen, Jim L ^a   Tokach, Mike D ^a  

^a KANSAS STATE UNIVERSITY   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c U S MEAT ANIMAL RESEARCH CENTER   (United States)

Author keywords

Antimicrobial resistance; Antimicrobial resistance gene quantification; Chlortetracycline; Copper; Pigs; Total community DNA

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS); SUIDAE;

ANTIINFECTIVE AGENT; CEPHALOSPORIN DERIVATIVE; CHLORTETRACYCLINE; COPPER;

ANALYSIS; ANIMAL; ANIMAL FOOD; ANTIBIOTIC RESISTANCE; DIET; DIETARY SUPPLEMENT; DRUG EFFECTS; GENETIC SELECTION; INTESTINE FLORA; MALE; MICROBIOLOGY; PIG; POLYMERASE CHAIN REACTION; RANDOMIZATION; VETERINARY;

ANIMAL FEED; ANIMALS; ANTI-BACTERIAL AGENTS; CEPHALOSPORINS; CHLORTETRACYCLINE; COPPER; DIET; DIETARY SUPPLEMENTS; DRUG RESISTANCE, BACTERIAL; GASTROINTESTINAL MICROBIOME; MALE; POLYMERASE CHAIN REACTION; RANDOM ALLOCATION; SELECTION, GENETIC; SUS SCROFA;

EID: 84926983914     PISSN: 01675877     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.prevetmed.2015.02.008     Document Type: Article

References (46)

1. Abley M.J., Wittum T.E., Funk J.A., Gebreyes W.A. Antimicrobial susceptibility, pulsed-field gel electrophoresis, and multi-locus sequence typing of Campylobacter coli in swine before, during, and after the slaughter process. Foodborne Pathog. Dis. 2012, 9:506-512.
2. Agga G.E., Scott H.M., Amachawadi R.G., Nagaraja T.G., Vinasco J., Bai J., Norby B., Renter D.G., Dritz S.S., Nelssen J.L., Tokach M.D. Effects of chlortetracycline and copper supplementation on antimicrobial resistance of fecal Escherichia coli from weaned pigs. Prev. Vet. Med. 2014, 114:231-246.
3. Alali W.Q., Scott H.M., Harvey R.B., Norby B., Lawhorn D.B., Pillai S.D. Longitudinal study of antimicrobial resistance among Escherichia coli isolates from integrated multisite cohorts of humans and swine. Appl. Environ. Microbiol. 2008, 74:3672-3681.
4. Alali W.Q., Scott H.M., Norby B., Gebreyes W., Loneragan G.H. Quantification of the bla(CMY-2) in feces from beef feedlot cattle administered three different doses of ceftiofur in a longitudinal controlled field trial. Foodborne Pathog. Dis. 2009, 6:917-924.
5. Amachawadi R.G., Scott H.M., Alvarado C.A., Mainini T.R., Vinasco J., Drouillard J.S., Nagaraja T.G. Occurrence of the transferable copper resistance gene tcrB among fecal enterococci of U.S. feedlot cattle fed copper-supplemented diets. Appl. Environ. Microbiol. 2013, 79:4369-4375.
6. Amachawadi R.G., Shelton N.W., Shi X., Vinasco J., Dritz S.S., Tokach M.D., Nelssen J.L., Scott H.M., Nagaraja T.G. Selection of fecal enterococci exhibiting tcrB-mediated copper resistance in pigs fed diets supplemented with copper. Appl. Environ. Microbiol. 2011, 77:5597-5603.
7. Aminov R.I., Garrigues-Jeanjean N., Mackie R.I. Molecular ecology of tetracycline resistance: development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins. Appl. Environ. Microbiol. 2001, 67:22-32.
8. Apley M.D., Bush E.J., Morrison R.B., Singer R.S., Snelson H. Use estimates of in-feed antimicrobials in swine production in the United States. Foodborne Pathog. Dis. 2012, 9:272-279.
9. Barbosa T.M., Levy S.B. The impact of antibiotic use on resistance development and persistence. Drug Resist. Updat. 2000, 3:303-311.
10. Barkovskii A.L., Bridges C. Persistence and profiles of tetracycline resistance genes in swine farms and impact of operational practices on their occurrence in farms' vicinities. Water Air Soil Pollut. 2012, 223:49-62.
11. Berge A.C., Hancock D.D., Sischo W.M., Besser T.E. Geographic, farm, and animal factors associated with multiple antimicrobial resistance in fecal Escherichia coli isolates from cattle in the western United States. J. Am. Vet. Med. Assoc. 2010, 236:1338-1344.
12. Borjesson S., Dienues O., Jarnheimer P.A., Olsen B., Matussek A., Lindgren P.E. Quantification of genes encoding resistance to aminoglycosides, beta-lactams and tetracyclines in wastewater environments by real-time PCR. Int. J. Environ. Health Res. 2009, 19:219-230.
13. Boyer T.C., Hanson T., Singer R.S. Estimation of low quantity genes: a hierarchical model for analyzing censored quantitative real-time PCR data. PLOS ONE 2013, 8:e64900.
14. Brown N.L., Rouch D.A., Lee B.T. Copper resistance determinants in bacteria. Plasmid 1992, 27:41-51.
15. Call D.R., Singer R.S., Meng D., Broschat S.L., Orfe L.H., Anderson J.M., Herndon D.R., Kappmeyer L.S., Daniels J.B., Besser T.E. blaCMY-2-positive IncA/C plasmids from Escherichia coli and Salmonella enterica are a distinct component of a larger lineage of plasmids. Antimicrob. Agents Chemother. 2010, 54:590-596.
16. Chopra I., Roberts M. Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol. Mol. Biol. Rev. 2001, 65:232-260.
17. Dewey C.E., Cox B.D., Straw B.E., Bush E.J., Hurd S. Use of antimicrobials in swine feeds in the United States. J. Swine Health Prod. 1999, 7:19-25.
18. Doyle M.P., Loneragan G.H., Scott H.M., Singer R.S. Antimicrobial resistance: challenges and perspectives. Compr. Rev. Food Sci. Food Saf. 2013, 12:234-248.
19. G8 2013 G8 Science Ministers Statement, London, United Kingdom 2013 June.
20. Giguère S. Tetracyclines and glycyclines. Antimicrobial Therapy in Veterinary Medicine 2006, 231-240. Blackwell Publishing, Ames, IA. S. Giguère, J.F. Prescott, J.D. Baggot, R.D. Walker, P.M. Dowling (Eds.).
21. Guillaume G., Verbrugge D., Chasseur-Libotte M., Moens W., Collard J. PCR typing of tetracycline resistance determinants (TetA-E) in Salmonella enterica serotype Hadar and in the microbial community of activated sludges from hospital and urban wastewater treatment facilities in Belgium. FEMS Microbiol. Ecol. 2000, 32:77-85.
22. Hasman H., Aarestrup F.M. tcrB, a gene conferring transferable copper resistance in Enterococcus faecium: occurrence, transferability, and linkage to macrolide and glycopeptide resistance. Antimicrob. Agents Chemother. 2002, 46:1410-1416.
23. Hasman H., Franke S., Rensing C. Resistance to metals used in agricultural production. Antimicrobial Resistance in Bacteria of Animal Origin 2006, 99-114. ASM Press, Washington, DC. F.M. Aarestrup (Ed.).
24. Holman D.B., Chenier M.R. Impact of subtherapeutic administration of tylosin and chlortetracycline on antimicrobial resistance in farrow-to-finish swine. FEMS Microbiol. Ecol. 2013, 85:1-13.
25. Kazimierczak K.A., Scott K.P., Kelly D., Aminov R.I. Tetracycline resistome of the organic pig gut. Appl. Environ. Microbiol. 2009, 75:1717-1722.
26. Kim H.B., Borewicz K., White B.A., Singer R.S., Sreevatsan S., Tu Z.J., Isaacson R.E. Longitudinal investigation of the age-related bacterial diversity in the feces of commercial pigs. Vet. Microbiol. 2011, 153:124-133.
27. Langlois B.E., Dawson K.A., Leak I., Aaron D.K. Effect of age and housing location on antibiotic resistance of fecal coliforms from pigs in a non-antibiotic-exposed herd. Appl. Environ. Microbiol. 1988, 54:1341-1344.
28. Looft T., Johnson T.A., Allen H.K., Bayles D.O., Alt D.P., Stedtfeld R.D., Sul W.J., Stedtfeld T.M., Chai B., Cole J.R., Hashsham S.A., Tiedje J.M., Stanton T.B. In-feed antibiotic effects on the swine intestinal microbiome. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:1691-1696.
29. Lowrance T.C., Loneragan G.H., Kunze D.J., Platt T.M., Ives S.E., Scott H.M., Norby B., Echeverry A., Brashears M.M. Changes in antimicrobial susceptibility in a population of Escherichia coli isolated from feedlot cattle administered ceftiofur crystalline-free acid. Am. J. Vet. Res. 2007, 68:501-507.
30. Marshall B.M., Levy S.B. Food animals and antimicrobials: impacts on human health. Rev. Clin. Microbiol. Rev. 2011, 24:718-733.
31. Marshall B.M., Ochieng D.J., Levy S.B. Commensals: underappreciated reservoir of antibiotic resistance. Microbe 2009, 3:231-238.
32. Mathew A.G., Upchurch W.G., Chattin S.E. Incidence of antibiotic resistance in fecal Escherichia coli isolated from commercial swine farms. J. Anim. Sci. 1998, 76:429-434.
33. Ng L.K., Martin I., Alfa M., Mulvey M. Multiplex PCR for the detection of tetracycline resistant genes. Mol. Cell. Probes 2001, 15:209-215.
34. Norman K.N., Harvey R.B., Scott H.M., Hume M.E., Andrews K., Brawley A.D. Varied prevalence of Clostridium difficile in an integrated swine operation. Anaerobe 2009, 15:256-260.
35. Odeh R., Kelkar S., Hujer A.M., Bonomo R.A., Schreckenberger P.C., Quinn J.P. Broad resistance due to plasmid-mediated AmpC beta-lactamases in clinical isolates of Escherichia coli. Clin. Infect. Dis. 2002, 35:140-145.
36. Pakpour S., Jabaji S., Chenier M.R. Frequency of antibiotic resistance in a swine facility 2.5 years after a ban on antibiotics. Microb. Ecol. 2012, 63:41-50.
37. Patterson S.K., Singer R.S. Development of a polymerase chain reaction assay for the detection of antibiotic resistance genes in community DNA. J. Vet. Diagn. Invest. 2006, 18:172-181.
38. Rensing C., Grass G. Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol. Rev. 2003, 27:197-213.
39. Roberts M.C. Environmental macrolide-lincosamide-streptogramin and tetracycline resistant bacteria. Front. Microbiol. 2011, 2:40.
40. Rouch D.A., Brown N.L. Copper-inducible transcriptional regulation at two promoters in the Escherichia coli copper resistance determinant pco. Microbiology 1997, 143:1191-1202.
41. TATFAR Recommendations for future collaboration between the U.S. and EU. Transatlantic Taskforce on Antimicrobial Resistance (TATFAR) 2011, Available at http://ecdc.europa.eu/en/activities/diseaseprogrammes/tatfar/documents/210911_tatfar_report.pdf (accessed 30.12.13).
42. Verstegen M.W., Williams B.A. Alternatives to the use of antibiotics as growth promoters for monogastric animals. Anim. Biotechnol. 2002, 13:113-127.
43. WHO The Medical Impact of the Use of Antimicrobials in Food Animals: Report and Proceedings of a WHO Meeting. Berlin, Germany, 13-17 October 1997 1997, World Health Organization (WHO), Geneva, Available at http://whqlibdoc.who.int/hq/1997/WHO_EMC_ZOO_97.4.pdf (accessed 30.12.13).
44. WHO WHO Global Strategy for Containment of Antimicrobial Resistance 2001, World Health Organization (WHO), Geneva, Switzerland, Available at http://whqlibdoc.who.int/hq/2001/WHO_CDS_CSR_DRS_2001.2.pdf (accessed 30.12.13).
45. Yu Z., Michel F.C., Hansen G., Wittum T., Morrison M. Development and application of real-time PCR assays for quantification of genes encoding tetracycline resistance. Appl. Environ. Microbiol. 2005, 71:6926-6933.
46. Zimmermann M., Udagedara S.R., Sze C.M., Ryan T.M., Howlett G.J., Xiao Z., Wedd A.G. PcoE - a metal sponge expressed to the periplasm of copper resistance Escherichia coli. Implication of its function role in copper resistance. J. Inorg. Biochem. 2012, 115:186-197.