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Antimicrobial resistance in beef and dairy cattle production

Published online by Cambridge University Press:  05 November 2008

Douglas R. Call ,
Margaret A. Davis  and
Ashish A. Sawant
Douglas R. Call*
Affiliation:
Department of Veterinary Microbiology and Pathology, College of Veterinary Medicine, Washington State University, Pullman, WA 99164-7040, USA
Margaret A. Davis
Affiliation:
Department of Veterinary Microbiology and Pathology, College of Veterinary Medicine, Washington State University, Pullman, WA 99164-7040, USA
Ashish A. Sawant
Affiliation:
Department of Veterinary Microbiology and Pathology, College of Veterinary Medicine, Washington State University, Pullman, WA 99164-7040, USA
*
*Corresponding author. E-mail: drcall@wsu.edu
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Abstract

Observational studies of cattle production systems usually find that cattle from conventional dairies harbor a higher prevalence of antimicrobial resistant (AMR) enteric bacteria compared to organic dairies or beef-cow operations; given that dairies usually use more antimicrobials, this result is not unexpected. Experimental studies have usually verified that application of antimicrobials leads to at least a transient expansion of AMR bacterial populations in treated cattle. Nevertheless, on dairy farms the majority of antibiotics are used to treat mastitis and yet AMR remains relatively low in mastitis pathogens. Other studies have shown no correlation between antimicrobial use and prevalence of AMR bacteria including documented cases where the prevalence of AMR bacteria is non-responsive to antimicrobial applications or remains relatively high in the absence of antimicrobial use or any other obvious selective pressures. Thus, there are multi-factorial events and pressures that influence AMR bacterial populations in cattle production systems. We introduce a heuristic model that illustrates how repeated antimicrobial selection pressure can increase the probability of genetic linkage between AMR genes and niche- or growth-specific fitness traits. This linkage allows persistence of AMR bacteria at the herd level because subpopulations of AMR bacteria are able to reside long-term within the host animals even in the absence of antimicrobial selection pressure. This model highlights the need for multiple approaches to manage herd health so that the total amount of antimicrobials is limited in a manner that meets animal welfare and public health needs while reducing costs for producers and consumers over the long-term.

Keywords

genetic linkageselective pressureconventional dairyorganicfeedlotmastitis
Type
Review Article
Information
Animal Health Research Reviews , Volume 9 , Issue 2: Symposium on Antimicrobial Resistance in Bacteria from Animals , December 2008 , pp. 159 - 167
Copyright
Copyright © Cambridge University Press 2008

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References

Alexander, TW, Yanke, LJ, Topp, E, Olson, ME, Read, RR, Morck, DW and McAllister, TA (2008). Effect of subtherapeutic administration of antibiotics on the prevalence of antibiotic-resistant Escherichia coli bacteria in feedlot cattle. Applied and Environmental Microbiology 74: 4405–4416.CrossRefGoogle ScholarPubMed
Barber, DA, Miller, GY and McNamara, PE (2003). Models of antimicrobial resistance and foodborne illness: examining assumptions and practical applications. Journal of Food Protection 66: 700–709.CrossRefGoogle ScholarPubMed
Berge, AC, Epperson, WB and Pritchard, RH (2005a). Assessing the effect of a single dose florfenicol treatment in feedlot cattle on the antimicrobial resistance patterns in faecal Escherichia coli. Veterinary Research 36: 723–734.CrossRefGoogle ScholarPubMed
Berge, AC, Lindeque, P, Moore, DA and Sischo, WM (2005b). A clinical trial evaluating prophylactic and therapeutic antibiotic use on health and performance of preweaned calves. Journal of Dairy Science 88: 2166–2177.CrossRefGoogle ScholarPubMed
Borgen, K, Sorum, M, Wasteson, Y, Kruse, H and Oppegaard, H (2002). Genetic linkage between erm(B) and vanA in Enterococcus hirae of poultry origin. Microbial Drug Resistance 8: 363–368.CrossRefGoogle ScholarPubMed
Bryan, CS (1947). Penicillin in the treatment of infectious bovine mastitis. American Journal of Public Health and the Nation's Health 37: 1147–1150.CrossRefGoogle ScholarPubMed
Carson, CA, Reid-Smith, R, Irwin, RJ, Martin, WS and McEwen, SA (2008). Antimicrobial resistance in generic fecal Escherichia coli from 29 beef farms in Ontario. Canadian Journal of Veterinary Research 72: 119–128.Google ScholarPubMed
Catry, B, Dewulf, J, Goffin, T, Decostere, A, Haesebrouck, F and De Kruif, A (2007). Antimicrobial resistance patterns of Escherichia coli through the digestive tract of veal calves. Microbial Drug Resistance 13: 147–150.CrossRefGoogle ScholarPubMed
Checkley, SL, Campbell, JR, Chirino-Trejo, M, Janzen, ED and McKinnon, JJ (2008). Antimicrobial resistance in generic fecal Escherichia coil obtained from beef cattle on arrival at the feedlot and prior to slaughter, and associations with volume of total individual cattle antimicrobial treatments in one western Canadian feedlot. Canadian Journal of Veterinary Research 72: 101–108.Google ScholarPubMed
Chen, J, Fluharty, FL, St-Pierre, N, Morrison, M and Yu, Z (2008). Technical note: occurrence in fecal microbiota of genes conferring resistance to both macrolide-lincosamide-streptogramin B and tetracyclines concomitant with feeding of beef cattle with tylosin. Journal of Animal Science. doi:10.1016/j.ijantimicag.2008.05.013CrossRefGoogle ScholarPubMed
Cho, S, Fossler, CP, Diez-Gonzalez, F, Wells, SJ, Hedberg, CW, Kaneene, JB, Ruegg, PL, Warnick, LD and Bender, JB (2007). Antimicrobial susceptibility of Shiga toxin-producing Escherichia coli isolated from organic dairy farms, conventional dairy farms, and county fairs in Minnesota. Foodborne Pathogens and Disease 4: 178–186.CrossRefGoogle ScholarPubMed
Claycamp, HG (2006). Rapid benefit-risk assessments: no escape from expert judgments in risk management. Risk Analysis 26:147–156; discussion 157–161.CrossRefGoogle ScholarPubMed
Cox Jr, LA and Popken, DA (2006). Quantifying potential human health impacts of animal antibiotic use: enrofloxacin and macrolides in chickens. Risk Analysis 26: 135–146.CrossRefGoogle ScholarPubMed
Dargatz, DA, Fedorka-Cray, PJ, Ladely, SR, Ferris, KE, Green, AL and Headrick, ML (2002). Antimicrobial susceptibility patterns of Salmonella isolates from cattle in feedlots. Journal of the American Veterinary Medical Association 221: 268–272.CrossRefGoogle ScholarPubMed
Dargatz, DA, Fedorka-Cray, PJ, Ladely, SR, Kopral, CA, Ferris, KE and Headrick, ML (2003). Prevalence and antimicrobial susceptibility of Salmonella spp. isolates from US cattle in feedlots in 1999 and 2000. Journal of Applied Microbiology 95: 753–761.CrossRefGoogle ScholarPubMed
Davis, MA, Hancock, DD, Besser, TE, Daniels, JB, Baker, KN and Call, DR (2007). Antimicrobial resistance in Salmonella enterica serovar Dublin isolates from beef and dairy sources. Veterinary Microbiology 119: 221–230.CrossRefGoogle ScholarPubMed
Erskine, RJ, Walker, RD, Bolin, CA, Bartlett, PC and White, DG (2002). Trends in antibacterial susceptibility of mastitis pathogens during a seven-year period. Journal of Dairy Science 85: 1111–1118.CrossRefGoogle ScholarPubMed
Gow, SP, Waldner, CL, Rajic, A, McFall, ME and Reid-Smith, R (2008a). Prevalence of antimicrobial resistance in fecal generic Escherichia coli isolated in western Canadian beef herds. Part II – cows and cow–calf pairs. Canadian Journal of Veterinary Research 72: 91–100.Google ScholarPubMed
Gow, SP, Waldner, CL, Rajic, A, McFall, ME and Reid-Smith, R (2008b). Prevalence of antimicrobial resistance in fecal generic Escherichia coli isolated in western Canadian cow-calf herds. Part I – beef calves. Canadian Journal of Veterinary Research 72: 82–90.Google ScholarPubMed
Grave, K, Jensen, VF, Odensvik, K, Wierup, M and Bangen, M (2006). Usage of veterinary therapeutic antimicrobials in Denmark, Norway and Sweden following termination of antimicrobial growth promoter use. Preventative Veterinary Medicine 75: 123–132.CrossRefGoogle ScholarPubMed
Halbert, LW, Kaneene, JB, Ruegg, PL, Warnick, LD, Wells, SJ, Mansfield, LS, Fossler, CP, Campbell, AM and Geiger-Zwald, AM (2006). Evaluation of antimicrobial susceptibility patterns in Campylobacter spp isolated from dairy cattle and farms managed organically and conventionally in the midwestern and northeastern United States. Journal of the American Veterinary Medical Association 228: 1074–1081.CrossRefGoogle ScholarPubMed
Hasman, H and Aarestrup, FM (2002). TcrB, a gene conferring transferable copper resistance in Enterococcus faecium: occurrence, transferability, and linkage to macrolide and glycopeptide resistance. Antimicrobial Agents and Chemotherapy 46: 1410–1416.CrossRefGoogle ScholarPubMed
Hasman, H, Kempf, I, Chidaine, B, Cariolet, R, Ersboll, AK, Houe, H, Bruun Hansen, HC and Aarestrup, FM (2006). Copper resistance in Enterococcus faecium, mediated by the tcrB gene, is selected by supplementation of pig feed with copper sulfate. Applied and Environmental Microbiology 72: 5784–5789.CrossRefGoogle ScholarPubMed
Hendriksen, RS, Mevius, DJ, Schroeter, A, Teale, C, Meunier, D, Butaye, P, Franco, A, Utinane, A, Amado, A, Moreno, M, Greko, C, Stark, K, Berghold, C, Myllyniemi, AL, Wasyl, D, Sunde, M and Aarestrup, FM (2008). Prevalence of antimicrobial resistance among bacterial pathogens isolated from cattle in different European countries: 2002–2004. Acta Veterinaria Scandinavica 50: 28.CrossRefGoogle ScholarPubMed
Heuer, OE, Hammerum, AM, Collignon, P and Wegener, HC (2006). Human health hazard from antimicrobial-resistant enterococci in animals and food. Clinical Infectious Diseases 43: 911–916.CrossRefGoogle ScholarPubMed
Hoe, FG and Ruegg, PL (2005). Relationship between antimicrobial susceptibility of clinical mastitis pathogens and treatment outcome in cows. Journal of the American Veterinary Medical Association 227: 1461–1468.CrossRefGoogle ScholarPubMed
Hoyle, DV, Shaw, DJ, Knight, HI, Davison, HC, Pearce, MC, Low, JC, Gunn, GJ and Woolhouse, ME (2004). Age-related decline in carriage of ampicillin-resistant Escherichia coli in young calves. Applied and Environmental Microbiology 70: 6927–6930.CrossRefGoogle ScholarPubMed
Hurd, HS and Malladi, S (2008). A stochastic assessment of the public health risks of the use of macrolide antibiotics in food animals. Risk Analysis 28: 695–710.CrossRefGoogle ScholarPubMed
Jenkins, MB, Hartel, PG, Olexa, TJ and Stuedemann, JA (2003). Putative temporal variability of Escherichia coli ribotypes from yearling steers. Journal of Environmental Quality 32: 305–309.CrossRefGoogle ScholarPubMed
Khachatryan, AR, Besser, TE and Call, DR (2008). The streptomycin-sulfadiazine-tetracycline antimicrobial resistance element of calf-adapted Escherichia coli is widely distributed among isolates from Washington state cattle. Applied and Environmental Microbiology 74: 391–395.CrossRefGoogle ScholarPubMed
Khachatryan, AR, Besser, TE, Hancock, DD and Call, DR (2006a). Use of a nonmedicated dietary supplement correlates with increased prevalence of streptomycin-sulfa-tetracycline-resistant Escherichia coli on a dairy farm. Applied and Environmental Microbiology 72: 4583–4588.CrossRefGoogle ScholarPubMed
Khachatryan, AR, Hancock, DD, Besser, TE and Call, DR (2004). Role of calf-adapted Escherichia coli in maintenance of antimicrobial drug resistance in dairy calves. Applied and Environmental Microbiology 70: 752–757.CrossRefGoogle ScholarPubMed
Khachatryan, AR, Hancock, DD, Besser, TE and Call, DR (2006b). Antimicrobial drug resistance genes do not convey a secondary fitness advantage to calf-adapted Escherichia coli. Applied and Environmental Microbiology 72: 443–448.CrossRefGoogle ScholarPubMed
Khaitsa, ML, Kegode, RB, Bauer, ML, Gibbs, PS, Lardy, GP and Doetkott, DK (2007). A longitudinal study of Salmonella shedding and antimicrobial resistance patterns in North Dakota feedlot cattle. Journal of Food Protection 70: 476–481.CrossRefGoogle ScholarPubMed
Klement, E, Chaffer, M, Leitner, G, Shwimmer, A, Friedman, S, Saran, A and Shpigel, N (2005). Assessment of accuracy of disk diffusion tests for the determination of antimicrobial susceptibility of common bovine mastitis pathogens: a novel approach. Microbial Drug Resistance 11: 342–350.CrossRefGoogle ScholarPubMed
Langford, FM, Weary, DM and Fisher, L (2003). Antibiotic resistance in gut bacteria from dairy calves: a dose response to the level of antibiotics fed in milk. Journal of Dairy Science 86: 3963–3966.CrossRefGoogle Scholar
Langlois, BE and Dawson, KA (1999). Antimicrobial resistance of gram-negative enteric bacteria from pigs in a nonantimicrobial-exposed herd before and after transportation. Journal of Food Protection 62: 797–799.CrossRefGoogle Scholar
LeJeune, JT and Christie, NP (2004). Microbiological quality of ground beef from conventionally-reared cattle and “raised without antibiotics” label claims. Journal of Food Protection 67: 1433–1437.CrossRefGoogle ScholarPubMed
Liebert, CA, Hall, RM and Summers, AO (1999). Transposon Tn21, flagship of the floating genome. Microbiology and Molecular Biology Reviews 63: 507–522.CrossRefGoogle ScholarPubMed
Lowrance, TC, Loneragan, GH, Kunze, DJ, Platt, TM, Ives, SE, Scott, HM, Norby, B, Echeverry, A and Brashears, MM (2007). Changes in antimicrobial susceptibility in a population of Escherichia coli isolated from feedlot cattle administered ceftiofur crystalline-free acid. American Journal of Veterinary Research 68: 501–507.CrossRefGoogle Scholar
Lundin, JI, Dargatz, DA, Wagner, BA, Lombard, JE, Hill, AE, Ladely, SR and Fedorka-Cray, PJ (2008). Antimicrobial drug resistance of fecal Escherichia coli and Salmonella spp. isolates from United States dairy cows. Foodborne Pathogens and Disease 5: 7–19.CrossRefGoogle ScholarPubMed
Makovec, JA and Ruegg, PL (2003). Antimicrobial resistance of bacteria isolated from dairy cow milk samples submitted for bacterial culture: 8,905 samples (1994–2001). Journal of the American Veterinary Medical Association 222: 1582–1589.CrossRefGoogle ScholarPubMed
Mathew, AG, Arnett, DB, Cullen, P and Ebner, PD (2003). Characterization of resistance patterns and detection of apramycin resistance genes in Escherichia coli isolated from swine exposed to various environmental conditions. International Journal of Food Microbiology 89: 11–20.CrossRefGoogle ScholarPubMed
Mathew, AG, Cissell, R and Liamthong, S (2007). Antibiotic resistance in bacteria associated with food animals: a United States perspective of livestock production. Foodborne Pathogens and Disease 4: 115–133.CrossRefGoogle ScholarPubMed
McEwen, SA (2006). Antibiotic use in animal agriculture: what have we learned and where are we going? Animal Biotechnology 17: 239–250.CrossRefGoogle ScholarPubMed
McEwen, SA and Fedorka-Cray, PJ (2002). Antimicrobial use and resistance in animals. Clinical Infectious Diseases 34 (Suppl. 3): S93–S106.CrossRefGoogle ScholarPubMed
Moro, MH, Beran, GW, Griffith, RW and Hoffman, LJ (2000). Effects of heat stress on the antimicrobial drug resistance of Escherichia coli of the intestinal flora of swine. Journal of Applied Microbiology 88: 836–844.CrossRefGoogle ScholarPubMed
Moro, MH, Beran, GW, Hoffman, LJ and Griffith, RW (1998). Effects of cold stress on the antimicrobial drug resistance of Escherichia coli of the intestinal flora of swine. Letters in Applied Microbiology 27: 251–254.CrossRefGoogle ScholarPubMed
Netherthrope Committee (1962). Report of the Joint Committee on Antibiotics in Animal Feeding. London, UK: Agricultural Research Council and Medical Research Council.Google Scholar
Parveen, S, Lukasik, J, Scott, TM, Tamplin, ML, Portier, KM, Sheperd, S, Braun, K and Farrah, SR (2006). Geographical variation in antibiotic resistance profiles of Escherichia coli isolated from swine, poultry, beef and dairy cattle farm water retention ponds in Florida. Journal of Applied Microbiology 100: 50–57.CrossRefGoogle ScholarPubMed
Peak, N, Knapp, CW, Yang, RK, Hanfelt, MM, Smith, MS, Aga, DS and Graham, DW (2007). Abundance of six tetracycline resistance genes in wastewater lagoons at cattle feedlots with different antibiotic use strategies. Environmental Microbiology 9: 143–151.CrossRefGoogle ScholarPubMed
Pol, M and Ruegg, PL (2007a). Relationship between antimicrobial drug usage and antimicrobial susceptibility of gram-positive mastitis pathogens. Journal of Dairy Science 90: 262–273.CrossRefGoogle ScholarPubMed
Pol, M and Ruegg, PL (2007b). Treatment practices and quantification of antimicrobial drug usage in conventional and organic dairy farms in Wisconsin. Journal of Dairy Science 90: 249–261.CrossRefGoogle ScholarPubMed
Price, LB, Graham, JP, Lackey, LG, Roess, A, Vailes, R and Silbergeld, E (2007). Elevated risk of carrying gentamicin-resistant Escherichia coli among U.S. poultry workers. Environmental Health Perspectives 115: 1738–1742.CrossRefGoogle ScholarPubMed
Ray, KA, Warnick, LD, Mitchell, RM, Kaneene, JB, Ruegg, PL, Wells, SJ, Fossler, CP, Halbert, LW and May, K (2006). Antimicrobial susceptibility of Salmonella from organic and conventional dairy farms. Journal of Dairy Science 89: 2038–2050.CrossRefGoogle ScholarPubMed
Raymond, MJ, Wohrle, RD and Call, DR (2006). Assessment and promotion of judicious antibiotic use on dairy farms in Washington State. Journal of Dairy Science 89: 3228–3240.CrossRefGoogle ScholarPubMed
Rossitto, PV, Ruiz, L, Kikuchi, Y, Glenn, K, Luiz, K, Watts, JL and Cullor, JS (2002). Antibiotic susceptibility patterns for environmental streptococci isolated from bovine mastitis in central California dairies. Journal of Dairy Science 85: 132–138.CrossRefGoogle ScholarPubMed
Sato, K, Bartlett, PC, Kaneene, JB and Downes, FP (2004). Comparison of prevalence and antimicrobial susceptibilities of Campylobacter spp. isolates from organic and conventional dairy herds in Wisconsin. Applied and Environmental Microbiology 70: 1442–1447.CrossRefGoogle ScholarPubMed
Sato, K, Bartlett, PC and Saeed, MA (2005). Antimicrobial susceptibility of Escherichia coli isolates from dairy farms using organic versus conventional production methods. Journal of the American Veterinary Medical Association 226: 589–594.CrossRefGoogle ScholarPubMed
Sawant, AA, Sordillo, LM and Jayarao, BM (2005). A survey on antibiotic usage in dairy herds in Pennsylvania. Journal of Dairy Science 88: 2991–2999.CrossRefGoogle ScholarPubMed
Sears, PM and McCarthy, KK (2003). Diagnosis of mastitis for therapy decisions. Veterinary Clinics of North America. Food Animal Practice 19: 93–108, vi.CrossRefGoogle ScholarPubMed
Settepani, JA (1984). The hazard of using chloramphenicol in food animals. Journal of the American Veterinary Medical Association 184: 930–931.Google ScholarPubMed
Shriram, V, Jahagirdar, S, Latha, C, Kumar, V, Puranik, V, Rojatkar, S, Dhakephalkar, PK and Shitole, MG (2008). A potential plasmid-curing agent, 8-epidiosbulbin E acetate, from Dioscorea bulbifera L. against multidrug-resistant bacteria. International Journal of Antimicrobial Agents Chen et al. 86: 2385–2391; Shriram et al. 32: 405–410.Google Scholar
Silbergeld, EK, Graham, J and Price, LB (2008). Industrial food animal production, antimicrobial resistance, and human health. Annual Review of Public Health 29: 151–169.CrossRefGoogle ScholarPubMed
Singer, RS, Ward, MP and Maldonado, G (2006). Can landscape ecology untangle the complexity of antibiotic resistance? Nature Reviews Microbiology 4: 943–952.CrossRefGoogle ScholarPubMed
Stabler, SL, Fagerberg, DJ and Quarles, CL (1982). Effects of oral and injectable tetracyclines on bacterial drug resistance in feedlot cattle. American Journal of Veterinary Research 43: 1763–1766.Google ScholarPubMed
Stokes, DJ, Kelly, AF, Gould, SW, Cassar, CA and Fielder, MD (2008). The withdrawal of antimicrobial treatment as a mechanism for defeating resistant microorganisms. FEMS Immunology and Medical Microbiology 53: 300–305.CrossRefGoogle ScholarPubMed
Swann, M (1969). Joint Committee on the Use of Antibiotics in Animal Husbandry and Veterinary Medicine. London, UK: HMSO.Google Scholar
van den Bogaard, AE and Stobberingh, EE (2000). Epidemiology of resistance to antibiotics. Links between animals and humans. International Journal of Antimicrobial Agents 14: 327–335.CrossRefGoogle Scholar
Walk, ST, Mladonicky, JM, Middleton, JA, Heidt, AJ, Cunningham, JR, Bartlett, P, Sato, K and Whittam, TS (2007). Influence of antibiotic selection on genetic composition of Escherichia coli populations from conventional and organic dairy farms. Applied and Environmental Microbiology 73: 5982–5989.CrossRefGoogle ScholarPubMed
Wassenaar, TM, Kist, M and de Jong, A (2007). Re-analysis of the risks attributed to ciprofloxacin-resistant Campylobacter jejuni infections. International Journal of Antimicrobial Agents 30: 195–201.CrossRefGoogle ScholarPubMed
Zwald, AG, Ruegg, PL, Kaneene, JB, Warnick, LD, Wells, SJ, Fossler, C and Halbert, LW (2004). Management practices and reported antimicrobial usage on conventional and organic dairy farms. Journal of Dairy Science 87: 191–201.CrossRefGoogle ScholarPubMed