Effect of subtherapeutic vs. therapeutic administration of macrolides on antimicrobial resistance in Mannheimia haemolytica and enterococci isolated from beef cattle

Frontiers in Microbiology

Volumn 4, Issue MAY, 2013, Pages

  Zaheer, Rahat ^a   Cook, Shaun R ^a   Klima, Cassidy L ^a   Stanford, Kim ^b   Alexander, Trevor ^a   Topp, Edward ^c   Read, Ron R ^d   McAllister, Tim A ^a  

^a LETHBRIDGE RESEARCH CENTRE   (Canada)

^b ALBERTA AGRICULTURE AND RURAL DEVELOPMENT   (Canada)

^c AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^d UNIVERSITY OF CALGARY   (Canada)

Author keywords

Antimicrobial resistance; Beef cattle; Enterococci; Macrolides; Mannheimia haemolytica

Indexed keywords

AMOXICILLIN; AMOXICILLIN PLUS CLAVULANIC ACID; CEFTIOFUR; COTRIMOXAZOLE; DANOFLOXACIN; DNA 16S; ERYTHROMYCIN; FLORFENICOL; GENTAMICIN; MACROLIDE; OXYTETRACYCLINE; SPECTINOMYCIN; TILMICOSIN; TULATHROMYCIN; TYLOSIN; TYLOSIN PHOSPHATE; UNCLASSIFIED DRUG;

ACINETOBACTER; ANIMAL EXPERIMENT; ANTIBIOTIC RESISTANCE; ARTICLE; BACILLUS; BACTERIUM ISOLATION; BEEF CATTLE; BULLOCK; CONTROLLED STUDY; DNA SEQUENCE; ENTEROCOCCUS; ENTEROCOCCUS HIRAE; ESCHERICHIA COLI; FECES ANALYSIS; MALE; MANNHEIMIA HAEMOLYTICA; NASOPHARYNX; NONHUMAN; PASTEURELLA MULTOCIDA; PNEUMONIC PASTEURELLOSIS; POLYMERASE CHAIN REACTION; SAMPLING; SEROTYPING; STAPHYLOCOCCUS;

ACINETOBACTER; ANIMALIA; BOS; BOVINAE; ENTEROBACTERIACEAE; ENTEROCOCCUS; ENTEROCOCCUS HIRAE; ESCHERICHIA COLI; MANNHEIMIA HAEMOLYTICA; PASTEURELLA MULTOCIDA; STAPHYLOCOCCUS;

EID: 84884237997     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2013.00133     Document Type: Article

References (67)

1. Aarestrup, F. M., Agersl, Y., Ahrens, P., Jlrgensen, J. C., Madsen, M., and Jensen, L. B. (2000a). Antimicrobial susceptibility and presence of resistance genes in staphylococci from poultry. Vet. Microbiol. 74, 353-364.
2. Aarestrup, F. M., Kruse, H., Tast, E., Hammerum, A. M., and Jensen, L. B. (2000b). Associations between the use of antimicrobial agents for growth promotion and the occurrence of resistance among Enterococcus faecium from broilers and pigs in Denmark, Finland, and Norway. Microb. Drug Resist. 6, 63-70.
3. Aarestrup, F. M., and Wegener, H. C. (1999). The effects of antibiotic usage in food animals on the development of antimicrobial resistance of importance for humans in Campylobacter and Escherichia coli. Microbes. Infect. 1, 639-644.
4. Aarestrup, F. M. A., Seyfarth, M., Emborg, H. D., Pedersen, K., Hendriksen, R. S., and Bager, F. (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.
5. Addah, W., Baah, J., Groenewegen, P., Okine, E. K., and McAllister, T. A. (2011). Comparison of the fermentation characteristics, aerobic stability and nutritive value of barley and corn silages ensiled with or without a mixed bacterial inoculant. Can. J. Anim. Sci. 91, 133-146.
6. Alexander, T. W., Cook, S. R., Yanke, L. J., Booker, C. W., Morley, P. S., Read, R. R., et al. (2008). A multiplex polymerase chain reaction assay for the identification of Mannheimia haemolytica, Mannheimia glucosida and Mannheimia ruminalis. Vet. Microbiol. 130, 165-175.
7. Allison, M. J., Robinson, I. M., Bucklin, J. A., and Booth, G. D. (1979). Comparison of bacterial populations of the pig cecum and colon based upon enumeration with specific energy sources. Appl. Environ. Microbiol. 37, 1142-1151.
8. Andersen, N. M., Poehlsgaard, J., Warrass, R., and Douthwaite, S. (2012). Inhibition of protein synthesis on the ribosome comparing tildipirosin with other veterinary macrolides. Antimicrob. Agents Chemother. 56, 6033-6036.
9. Bozdogan, B., Galopin, S., and Leclercq, R. (2004). Characterization of a new erm-related macrolide resistance gene present in probiotic strains of Bacillus clausii. Appl. Environ. Microbiol. 70, 280-284.
10. Canh, T. T., Verstegen, M. W. A., Aarnink, A. J. A., and Schrama, J. W. (1997). Influence of dietary factors on nitrogen partitioning and composition of urine and feces of fattening pigs. J. Anim. Sci. 75, 700-706.
11. Checkley, S. L., Campbell, J. R., Chirino-Trejo, M., Janzen, E. D., and Waldner, C. L. (2010). Associations between antimicrobial use and the prevalence of antimicrobial resistance in fecal Escherichia coli from feedlot cattle in western Canada. Can. Vet. J. 51, 853-861.
12. Chen, J., Fluharty, F. L., 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. J. Anim. Sci. 86, 2385-2391.
13. Chen, J., Yu, Z., Michel, F. C. Jr., Wittum, T., and Morrison, M. (2007). Development and application of real-time PCR assays for quantification of erm genes conferring resistance to macrolides-lincosamides-streptogramin B in livestock manure and manure management systems. Appl. Environ. Microbiol. 73, 4407-4416.
14. CIPARS. (2013). Canadian Integrated Program for Antimicrobial Resistance Surveillance Report. Available online at: http://www.phac-aspc.gc.ca/ciparspicra/ pubs-eng.php#ar (last accessed date: 8 March 2013).
15. Clinical Laboratory Standards Institute (2008a). Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals; Approved Standard - 3rd Edn. Document M31-A3. Wayne, PA: Clinical and Laboratory Standards Institute.
16. Clinical Laboratory Standards Institute (2008b). Methods for Antimicrobial Dilution and Disk Susceptibility Testing of Infrequently Isolated or Fastidious Bacteria; Approved Guideline. Document M45-A. Wayne, PA: Clinical and Laboratory Standards Institute.
17. Confer, A. W. (2009). Update on bacterial pathogenesis in BRD. Anim. Health Res. Rev. 10, 145-148.
18. Cox, S. R., McLaughlin, C., Fielder, A. E., Yancey, M. F., Bowersock, T. L., Garcia-Tapia, D., et al. (2010). Rapid and prolonged distribution of tulathromycin into lung homogenate and pulmonary epithelial lining fluid of Holstein calves following a single subcutaneous administration of 2.5 mg/kg body weight. Int. J. Appl. Res. Vet. Med. 8, 129-137.
19. Dabo, S. M., Taylor, J. D., and Confer, A. W. (2007). Pasteurella multocida and bovine respiratory disease. Anim. Health Res. Rev. 8, 129-150.
20. Desmolaize, B., Rose, S., Warrass, R., and Douthwaite, S. (2011). A novel Erm monomethyltransferase in antibiotic-resistant isolates of Mannheimia haemolytica and Pasteurella multocida. Mol. Microbiol. 80, 184-194.
21. DiPersio, L. P., and DiPersio, J. R. (2006). High rates of erythromycin and clindamycin resistance among OBGYN isolates of group B Streptococcus. Diagn. Microbiol. Infect. Dis. 54, 79-82.
22. Fisher, K., and Phillips, C. (2009). The ecology, epidemiology and virulence of Enterococcus. Microbiol. 55, 1749-1757.
23. Food Drug Administration's Center for Veterinary Medicine (FDA/CVM). (2013). Tulathromycin solution for parenteral injection for treatment of bovine and swine respiratory diseases: microbiological effects on bacteria of human health concern, a qualitative risk estimation. Available online at: www.fda.gov/downloads/AdvisoryCommittees/CommitteesMeetingMaterials/VeterinaryMedicineAdvisoryCommittee/UCM127196.pdf (last accessed date: 8 March 2013).
24. Frank, G. H., Briggs, R. E., Loan, R. W., Purdy, C. W., and Zehr, E. S. (2000). Effect of tilmicosin treatment on Pasteurella haemolytica organisms in nasal secretion specimens of calves with respiratory tract disease. Am. J.Vet. Res. 61, 525-529.
25. Fulton, R. W. (2009). Bovine respiratory disease research (1983-2009). Anim. Health Res. Rev. 10, 131-139.
26. Giraffa, G. (2002). Enterococci from foods. FEMS Microbiol. Rev. 26, 163-171.
27. Gow, S. (2005). Antimicrobial resistance, prudent use, and the Canadian integrated program for antimicrobial resistance surveillance (CIPARS). Large Anim. Vet Rounds 5, 1-6.
28. Heuer, O. E., Hammerum, A. M., Collignon, P., Collignon, P., and Wegener, H. C. (2006). Human health hazard from antimicrobial-resistant enterococci in animals and food. Clin. Infect. Dis. 43, 911-916.
29. Inglis, G. D., McAllister, T. A., Busz, H. W., Yanke, L. J., Morck, D. W., Olson, M. E., et al. (2005). Effects of subtherapeutic administration of antimicrobial agents to beef cattle on the prevalence of antimicrobial resistance in Campylobacter jejuni and Campylobacter hyointestinalis. Appl. Environ. Microbiol. 71, 3872-3881.
30. Israeli-Reches, M., Weinrauch, Y., and Dubnau, D. (1984). Evolutionary relationships of the Bacillus licheniformis macrolide-lincosamide-streptogramin B resistance elements. Mol. Gen. Genet. 194, 362-367.
31. Jackson, C. R., Fedorka-Cray, P. J., Barrett, J. B., and Ladely, S. R. (2004). Effects of tylosin use on erythromycin resistance in enterococci isolated from swine. Appl. Environ. Microbiol. 70, 4205-4210.
32. Jensen, L. B., Frimodt-Moller, N., and Aarestrup, F. M. (1999). Presence of erm gene classes in gram-positive bacteria of animal and human origin in Denmark. FEMS Microbiol. Lett. 170, 151-158.
33. Jensen, L. B., Hammerum, A. M., Bager, F., and Aarestrup, F. M. (2002). Streptogramin resistance among Enterococcus faecium isolated from production animals in Denmark in 1997. Microb. Drug Resist. 8, 369-374.
34. Katsuda, K., Kohmoto, M., Mikami, O., and Uchida, I. (2009). Antimicrobial resistance and genetic characterization of fluoroquinolone-resistant Mannheimia haemolytica isolates from cattle with bovine pneumonia. Vet. Microbiol. 139, 74-79.
35. Klima, C. L., Alexander, T. W., Read, R. R., Gow, S. P., Booker, C. W., Hannon, S., et al. (2011). Genetic characterization and antimicrobial susceptibility of Mannheimia haemolytica isolated from the nasopharynx of feedlot cattle. Vet. Microbiol. 149, 390-398.
36. Kloos, W., and Bannerman, T. L. (1994). Update on clinical significance of coagulase-negative staphylococci. Clin. Microbiol. Rev. 7, 117-140.
37. Kobland, J. D., Gale, G. O., Gustafson, R. H., and Simkins, K. L. (1987). Comparison of therapeutic versus subtherapeutic levels of chlortetracycline in the diet for selection of resistant salmonella in experimentally challenged chickens. Poult. Sci. 66, 1129-1137.
38. Ladely, S. R., Harrison, M. A., Fedorka-Cray, P. J., Berrang, M. E., Englen, M. D., and Meinersmann, R. J. (2007). Development of macrolide-resistant Campylobacter in broilers administered subtherapeutic or therapeutic concentrations of tylosin. J. Food Prot. 70, 1945-1951.
39. Lewicki, J. (2006). Tylosin. A review of pharmacokinetics, residues in food animals and analytical methods. FAO website: ftp://ftp.fao.org/ag/agn/food/tylosin_2006.pdf (last accessed date: 8 March 2013).
40. Lim, J. A., Kwon, A. R., Kim, S. K., Chong, Y., Lee, K., and Choi, E. C. (2002). Prevalence of resistance to macrolide, lincosamide and streptogramin antibiotics in Gram-positive cocci isolated in a Korean hospital. J. Antimicrob. Chemother. 49, 489-495.
41. Loy, T., Wilson, C., Bailey, D., Klopfenstein, T. J., and Moxley, R. A. (2001). Influence of restricted intake and reduced dietary starch on colonic pH and E. coli prevalence. Nebraska Beef Report MP76-A, 86-88.
42. Marshall, B. M., and Levy, S. B. (2011). Food animals and antimicrobials: impacts on human health. Clin. Microbiol. Rev. 24, 718-733.
43. Mao, J. C., and Putterman, M. (1968). Accumulation in gram-postive and gram-negative bacteria as a mechanism of resistance to erythromycin. J. Bacteriol. 95, 1111 -1117.
44. McEwen, S. A., and Fedorka-Cray, P. J. (2002). Antimicrobial use and resistance in animals. Clin. Infect. Dis. 34, S93-S106.
45. Michael, G. B., Kadlec, K., Sweeney, M. T., Brzuszkiewicz, E., Liesegang, H., Daniel, R., et al. (2012). ICEPmu1, an integrative conjugative element (ICE) of Pasteurella multocida: analysis of the regions that comprise 12 antimicrobial resistance genes. J. Antimicrob. Chemother. 67, 84-90.
46. Pardon, B., De Bleecker, K., Dewulf, J., Callens, J., Boyen, F., Catry, B., et al. (2011). Prevalence of respiratory pathogens in diseased, non-vaccinated, routinely medicated veal calves. Vet. Rec. 169, 278.
47. Piette, A., and Verschraegen, G. (2008). Role of coagulase-negative staphylococci in human disease. Vet. Microbiol. 134, 45-54.
48. Portis, E., Lindeman, C., Johansen, L., and Stoltman, G. (2012). A ten-year (2000-2009) study of antimicrobial susceptibility of bacteria that cause bovine respiratory disease complex-Mannheimia haemolytica, Pasteurella multocida, and Histophilus somni-in the United States and Canada. J. Vet. Diagn. Invest. 24, 932-944.
49. Roberts, M. C. (2008). Update on macrolide-lincosamide-streptogramin, ketolide, and oxazolidinone resistance genes. FEMS Microbiol. Lett. 282, 147-159
50. Roberts, M. C., Sutcliffe, J., Courvalin, P., Jensen, L. B., Rood, J., and Seppala, H. (1999). Nomenclature for macrolide and macrolide-lincosamide-streptogramin B resistance determinants. Antimicrob. Agents Chemother. 43, 2823-2830.
51. Savini, V., Catavitello, C., Carlino, D., Bianco, A., Pompilio, A., Balbinot, A., et al. (2009). Staphylococcus pasteuri bacteraemia in a patient with leukaemia. J. Clin.Pathol. 62, 957-958.
52. Schjørring, S., and Krogfelt, K. A. (2011). Assessment of bacterial antibiotic resistance transfer in the gut. Int. J. Microbiol. 2011, ID 312956. doi: 10.1155/2011/312956
53. Schlünzen, F., Zarivach, R., Harms, J., Bashan, A., Tocilj, A., Albrecht, R., et al. (2001). Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria. Nature 413, 814-821.
54. Scott, T., Wilson, C., Bailey, D., Klopfendtein, T. J., and Milton, T. (2000). Influence of diet on total and acid resistant E. coli and colonic pH. Nebraska Beef Report MP73-A, 39-43.
55. Siegel, T. W., Earley, D. L., Smothers, C. D., Sun, F., and Ricketts, A. P. (2004). Cellular uptake of the triamilide tulathromycin by bovine and porcine phagocytic cells in vitro. J. Anim. Sci. 82, 186.
56. Simeoni, D., Rizzotti, L., Cocconcelli, P., Gazzola, S., Dellaglio, F., and Torriani, S. (2008). Antibiotic resistance genes and identification of staphylococci collected from the production chain of swine meat commodities. Food Microbiol. 25, 196-201.
57. Skinner, R., Cundliffe, E., and Schmidt, F. J. (1983). Site of action of a ribosomal RNA methylase responsible for resistance to erythromycin and other antibiotics. J. Biol. Chem. 258, 12702-12706.
58. Szczepanowski, R., Linke, B., Krahn, I., Gartemann, K. H., Gützkow, T., Eichler, W., et al. (2009). Detection of 140 clinically relevant antibiotic-resistance genes in the plasmid metagenome of wastewater treatment plant bacteria showing reduced susceptibility to selected antibiotics. Microbiol. 155, 2306-2319.
59. Turabelidze, D., Kotetishvili, M., Kreger, A., Morris, J. G. Jr., and Sulakvelidze, A. (2000). Improved pulsed-field gel electrophoresis for typing vancomycin-resistant enterococci. J. Clin. Microbiol. 38, 4242-4245.
60. USDA. (1999). Report part III, health management and biosecurity in U.S. feedlots 1999. Available online at, http, //www.aphis.usda.gov/animal_health/nahms/feedlot/downloads/feedlot99/Feedlot99_dr_PartIII.pdf (last accessed date, 8 March 2013).
61. van Schaik, W., and Willems, R. J. (2010). Genome-based insights into the evolution of enterococci. Clin. Microbiol. Infect. 16, 527-532.
62. Watts, J. L., and Sweeney, M. T. (2010). Antimicrobial resistance in bovine respiratory disease pathogens, measures, trends, and impact on efficacy. Vet. Clin. North Am. Food Anim. Pract. 26, 79-88.
63. Wegener, H. C., Aarestrup, F. M., Jensen, L. B., Hammerum, A. M., and Bager, F. (1999). Use of antimicrobial growth promoters in food animals and Enterococcus faecium resistance to therapeutic antimicrobial drugs in Europe. Emerg. Infect. Dis. 5, 329-335.
64. Werner, G., Hildebrandt, B., Klare, I., and Witte, W. (2000). Linkage of determinants for streptogramin A, macrolide-lincosamide-streptogramin B, and chloramphenicol resistance on a conjugative plasmid in Enterococcus faecium and dissemination of this cluster among streptogramin-resistant enterococci. Int. J. Med. Microbiol. 290, 543-548.
65. Yost, C. K., Diarra, M. S., and Topp, E. (2011). "Animals and humans as sources of fecal indicator bacteria," in The Fecal Bacteria, eds M. J. Sadowsky and R. L. Whitman (Washington DC, ASM Press), 67-91.
66. Zaheer, R., Yanke, L. J., Church, D., Topp, E., Read, R. R., and McAllister, T. A. (2012). High-throughput species identification of enterococci using pyrosequencing. J. Microbiol. Methods 89, 174-178.
67. Zecchinon, L., Fett, T., and Desmecht, D. (2005). How Mannheimia haemolytica defeats host defence through a kiss of death mechanism. Vet. Res. 36, 133-156.