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Scientific reports2020; 10(1); 911; doi: 10.1038/s41598-020-57479-9

A Common Practice of Widespread Antimicrobial Use in Horse Production Promotes Multi-Drug Resistance.

Abstract: The practice of prophylactic administration of a macrolide antimicrobial with rifampin (MaR) to apparently healthy foals with pulmonary lesions identified by thoracic ultrasonography (i.e., subclinically pneumonic foals) is common in the United States. The practice has been associated epidemiologically with emergence of R. equi resistant to MaR. Here, we report direct evidence of multi-drug resistance among foals treated with MaR. In silico and in vitro analysis of the fecal microbiome and resistome of 38 subclinically pneumonic foals treated with either MaR (n = 19) or gallium maltolate (GaM; n = 19) and 19 untreated controls was performed. Treatment with MaR, but not GaM, significantly decreased fecal microbiota abundance and diversity, and expanded the abundance and diversity of antimicrobial resistance genes in feces. Soil plots experimentally infected with Rhodococcus equi (R. equi) and treated with MaR selected for MaR-resistant R. equi, whereas MaR-susceptible R. equi out-competed resistant isolates in GaM-treated or untreated plots. Our results indicate that MaR use promotes multi-drug resistance in R. equi and commensals that are shed into their environment where they can persist and potentially infect or colonize horses and other animals.
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Publication Date: 2020-01-22 PubMed ID: 31969575PubMed Central: PMC6976650DOI: 10.1038/s41598-020-57479-9Google Scholar: Lookup
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  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research investigates the effect of a common horse care practice in the U.S.—the administration of a macrolide antimicrobial and rifampin—to foals that appear healthy but show signs of pneumonia on an ultrasound. The results indicate that this practice leads to multiple drug resistance among foals and negatively impacts the fecal microbiome.

Research Background and Methods

  • This study focused on the practice common in the U.S horse production of administering a combination of a macrolide antimicrobial and rifampin (abbreviated as MaR) to foals that seem healthy but have pulmonary lesions detectable by thoracic ultrasonography, indicating that they are subclinically pneumonic.
  • The research team used in vitro analysis (performed in a controlled environment, such as a petri dish) and in silico analysis (performed through computer simulation) of the fecal microbiome and resistome of 38 similar foals.
  • Of the total foals, 19 were treated with MaR, 19 with gallium maltolate (GaM, another antimicrobial), and 19 were left untreated as control subjects.

Results of the Study

  • Treatment with MaR resulted in a significant decrease in the variety and quantity of bacterial species in the feces of the foals, but treatment with GaM did not show this effect.
  • Moreover, MaR treatment resulted in an increased abundance and diversity of antimicrobial resistance genes present in feces.
  • The researchers used soil plots infected experimentally with Rhodococcus equi (R. equi – a bacteria that generally causes pneumonia in foals). They found that the soil treated with MaR showed a selection for MaR-resistant R. equi.
  • In contrast, soil plots treated with GaM or left untreated showed a predominance of MaR-susceptible R. equi, which out-competed the resistant strains.

Conclusion

  • The results led to the conclusion that using MaR promotes multi-drug resistance in R. equi and other naturally occurring commensals in horses.
  • These drug-resistant bacteria can then be shed into the environment where they can persist, and potentially expose or colonize other horses and animals, thereby escalating the problem of antimicrobial resistance.

Overall, these findings suggest a need to re-examine common antibiotic use practices in horse care, particularly those involving MaR, as such practices seem to contribute significantly to environmental and biomedical issues related to antibiotic resistance.

Cite This Article

APA
Álvarez-Narváez S, Berghaus LJ, Morris ERA, Willingham-Lane JM, Slovis NM, Giguere S, Cohen ND. (2020). A Common Practice of Widespread Antimicrobial Use in Horse Production Promotes Multi-Drug Resistance. Sci Rep, 10(1), 911. https://doi.org/10.1038/s41598-020-57479-9

Publication

Scientific reports
ISSN: 2045-2322
NlmUniqueID: 101563288
Country: England
Language: English
Volume: 10
Issue: 1
Pages: 911
PII: 911

Researcher Affiliations

Álvarez-Narváez, S
  • Department of Large Animal Medicine, College of Veterinary Medicine, University of Georgia, Athens, Ga, USA.
Berghaus, L J
  • Department of Large Animal Medicine, College of Veterinary Medicine, University of Georgia, Athens, Ga, USA.
Morris, E R A
  • Department of Large Animal Clinical Sciences, College of Veterinary Medicine & Biomedical Sciences, Texas A&M University, College Station, TX, USA.
Willingham-Lane, J M
  • Department of Large Animal Medicine, College of Veterinary Medicine, University of Georgia, Athens, Ga, USA.
Slovis, N M
  • Hagyard Equine Medical Institute, Lexington, KY, USA.
Giguere, S
  • Department of Large Animal Medicine, College of Veterinary Medicine, University of Georgia, Athens, Ga, USA.
Cohen, N D
  • Department of Large Animal Clinical Sciences, College of Veterinary Medicine & Biomedical Sciences, Texas A&M University, College Station, TX, USA. ncohen@cvm.tamu.edu.

MeSH Terms

  • Animals
  • Anti-Bacterial Agents / adverse effects
  • Anti-Bacterial Agents / pharmacology
  • Anti-Bacterial Agents / therapeutic use
  • Antibiotic Prophylaxis
  • Drug Resistance, Multiple / drug effects
  • Drug Resistance, Multiple / genetics
  • Feces / microbiology
  • Horse Diseases / prevention & control
  • Horses
  • Macrolides / adverse effects
  • Macrolides / pharmacology
  • Macrolides / therapeutic use
  • Microbial Sensitivity Tests
  • Organometallic Compounds / adverse effects
  • Organometallic Compounds / pharmacology
  • Organometallic Compounds / therapeutic use
  • Pneumonia, Bacterial / microbiology
  • Pneumonia, Bacterial / prevention & control
  • Pneumonia, Bacterial / veterinary
  • Pyrones / adverse effects
  • Pyrones / pharmacology
  • Pyrones / therapeutic use
  • Rhodococcus equi / drug effects
  • Rhodococcus equi / genetics
  • Rifampin / adverse effects
  • Rifampin / pharmacology
  • Rifampin / therapeutic use

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 84 references
  1. Bengtsson B, Greko C. Antibiotic resistance--consequences for animal health, welfare, and food production.. Ups J Med Sci 2014 May;119(2):96-102.
    doi: 10.3109/03009734.2014.901445pmc: PMC4034566pubmed: 24678738google scholar: lookup
  2. Ashbolt NJ, Amézquita A, Backhaus T, Borriello P, Brandt KK, Collignon P, Coors A, Finley R, Gaze WH, Heberer T, Lawrence JR, Larsson DG, McEwen SA, Ryan JJ, Schönfeld J, Silley P, Snape JR, Van den Eede C, Topp E. Human Health Risk Assessment (HHRA) for environmental development and transfer of antibiotic resistance.. Environ Health Perspect 2013 Sep;121(9):993-1001.
    doi: 10.1289/ehp.1206316pmc: PMC3764079pubmed: 23838256google scholar: lookup
  3. Yang P, Chen Y, Jiang S, Shen P, Lu X, Xiao Y. Association between antibiotic consumption and the rate of carbapenem-resistant Gram-negative bacteria from China based on 153 tertiary hospitals data in 2014.. Antimicrob Resist Infect Control 2018;7:137.
    doi: 10.1186/s13756-018-0430-1pmc: PMC6245771pubmed: 30479750google scholar: lookup
  4. Goossens H. Antibiotic consumption and link to resistance.. Clin Microbiol Infect 2009 Apr;15 Suppl 3:12-5.
    doi: 10.1111/j.1469-0691.2009.02725.xpubmed: 19366364google scholar: lookup
  5. Hoelzer K, Wong N, Thomas J, Talkington K, Jungman E, Coukell A. Antimicrobial drug use in food-producing animals and associated human health risks: what, and how strong, is the evidence?. BMC Vet Res 2017 Jul 4;13(1):211.
    doi: 10.1186/s12917-017-1131-3pmc: PMC5496648pubmed: 28676125google scholar: lookup
  6. Hu Y, Yang X, Qin J, Lu N, Cheng G, Wu N, Pan Y, Li J, Zhu L, Wang X, Meng Z, Zhao F, Liu D, Ma J, Qin N, Xiang C, Xiao Y, Li L, Yang H, Wang J, Yang R, Gao GF, Wang J, Zhu B. Metagenome-wide analysis of antibiotic resistance genes in a large cohort of human gut microbiota.. Nat Commun 2013;4:2151.
    doi: 10.1038/ncomms3151pubmed: 23877117google scholar: lookup
  7. Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, Teillant A, Laxminarayan R. Global trends in antimicrobial use in food animals.. Proc Natl Acad Sci U S A 2015 May 5;112(18):5649-54.
    doi: 10.1073/pnas.1503141112pmc: PMC4426470pubmed: 25792457google scholar: lookup
  8. Zhao Y, Su JQ, An XL, Huang FY, Rensing C, Brandt KK, Zhu YG. Feed additives shift gut microbiota and enrich antibiotic resistance in swine gut.. Sci Total Environ 2018 Apr 15;621:1224-1232.
    doi: 10.1016/j.scitotenv.2017.10.106pubmed: 29054657google scholar: lookup
  9. Thomas M, Webb M, Ghimire S, Blair A, Olson K, Fenske GJ, Fonder AT, Christopher-Hennings J, Brake D, Scaria J. Metagenomic characterization of the effect of feed additives on the gut microbiome and antibiotic resistome of feedlot cattle.. Sci Rep 2017 Sep 25;7(1):12257.
    doi: 10.1038/s41598-017-12481-6pmc: PMC5612972pubmed: 28947833google scholar: lookup
  10. Taylor EA, Jordan ER, Garcia JA, Hagevoort GR, Norman KN, Lawhon SD, Piñeiro JM, Scott HM. Effects of two-dose ceftiofur treatment for metritis on the temporal dynamics of antimicrobial resistance among fecal Escherichia coli in Holstein-Friesian dairy cows.. PLoS One 2019;14(7):e0220068.
    doi: 10.1371/journal.pone.0220068pmc: PMC6645674pubmed: 31329639google scholar: lookup
  11. Weinroth MD, Scott HM, Norby B, Loneragan GH, Noyes NR, Rovira P, Doster E, Yang X, Woerner DR, Morley PS, Belk KE. Effects of Ceftiofur and Chlortetracycline on the Resistomes of Feedlot Cattle.. Appl Environ Microbiol 2018 Jul 1;84(13).
    pmc: PMC6007121pubmed: 29728379doi: 10.1128/aem.00610-18google scholar: lookup
  12. Ohta N, Norman KN, Norby B, Lawhon SD, Vinasco J, den Bakker H, Loneragan GH, Scott HM. Population dynamics of enteric Salmonella in response to antimicrobial use in beef feedlot cattle.. Sci Rep 2017 Oct 30;7(1):14310.
    doi: 10.1038/s41598-017-14751-9pmc: PMC5662634pubmed: 29085049google scholar: lookup
  13. Beukers AG, Zaheer R, Cook SR, Stanford K, Chaves AV, Ward MP, McAllister TA. Effect of in-feed administration and withdrawal of tylosin phosphate on antibiotic resistance in enterococci isolated from feedlot steers.. Front Microbiol 2015;6:483.
    doi: 10.3389/fmicb.2015.00483pmc: PMC4444845pubmed: 26074889google scholar: lookup
  14. Kanwar N, Scott HM, Norby B, Loneragan GH, Vinasco J, McGowan M, Cottell JL, Chengappa MM, Bai J, Boerlin P. Effects of ceftiofur and chlortetracycline treatment strategies on antimicrobial susceptibility and on tet(A), tet(B), and bla CMY-2 resistance genes among E. coli isolated from the feces of feedlot cattle.. PLoS One 2013;8(11):e80575.
    doi: 10.1371/journal.pone.0080575pmc: PMC3834275pubmed: 24260423google scholar: lookup
  15. Coleman MC, Blodgett GP, Bevevino KE, Ivanek R, Cummings KJ, Carter GK, Cohen ND. Foal-Level Risk Factors Associated With Development of Rhodococcus equi Pneumonia at a Quarter Horse Breeding Farm.. J Equine Vet Sci 2019 Jan;72:89-96.
    doi: 10.1016/j.jevs.2018.10.023pubmed: 30929790google scholar: lookup
  16. Chaffin MK, Cohen ND, Martens RJ. Evaluation of equine breeding farm characteristics as risk factors for development of Rhodococcus equi pneumonia in foals.. J Am Vet Med Assoc 2003 Feb 15;222(4):467-75.
    doi: 10.2460/javma.2003.222.467pubmed: 12597420google scholar: lookup
  17. Huber L, Giguère S, Cohen ND, Slovis NM, Hanafi A, Schuckert A, Berghaus L, Greiter M, Hart KA. Prevalence and risk factors associated with emergence of Rhodococcus equi resistance to macrolides and rifampicin in horse-breeding farms in Kentucky, USA.. Vet Microbiol 2019 Aug;235:243-247.
    doi: 10.1016/j.vetmic.2019.07.010pubmed: 31383308google scholar: lookup
  18. Chaffin MK, Cohen ND, Martens RJ, Edwards RF, Nevill M. Foal-related risk factors associated with development of Rhodococcus equi pneumonia on farms with endemic infection.. J Am Vet Med Assoc 2003 Dec 15;223(12):1791-9.
    doi: 10.2460/javma.2003.223.1791pubmed: 14690209google scholar: lookup
  19. Cohen ND, Chaffin MK, Kuskie KR, Syndergaard MK, Blodgett GP, Takai S. Association of perinatal exposure to airborne Rhodococcus equi with risk of pneumonia caused by R equi in foals.. Am J Vet Res 2013 Jan;74(1):102-9.
    doi: 10.2460/ajvr.74.1.102pubmed: 23270353google scholar: lookup
  20. Kuskie KS. Associations between the exposure to airborne virulent Rhodococcus equi ane the Incidence of R. equi Pneumonia among Individual Foals. Journal of Equine Veterinary Science 2011;31:463–469.
    doi: 10.1016/j.jevs.2011.03.002google scholar: lookup
  21. Giguère S, Cohen ND, Chaffin MK, Slovis NM, Hondalus MK, Hines SA, Prescott JF. Diagnosis, treatment, control, and prevention of infections caused by Rhodococcus equi in foals.. J Vet Intern Med 2011 Nov-Dec;25(6):1209-20.
    doi: 10.1111/j.1939-1676.2011.00835.xpubmed: 22092608google scholar: lookup
  22. Ramirez S, Lester GD, Roberts GR. Diagnostic contribution of thoracic ultrasonography in 17 foals with Rhodococcus equi pneumonia.. Vet Radiol Ultrasound 2004 Mar-Apr;45(2):172-6.
    doi: 10.1111/j.1740-8261.2004.04028.xpubmed: 15072151google scholar: lookup
  23. Muscatello G. Rhodococcus equi pneumonia in the foal--part 2: diagnostics, treatment and disease management.. Vet J 2012 Apr;192(1):27-33.
    doi: 10.1016/j.tvjl.2011.08.009pubmed: 22036870google scholar: lookup
  24. Venner M, Astheimer K, Lämmer M, Giguère S. Efficacy of mass antimicrobial treatment of foals with subclinical pulmonary abscesses associated with Rhodococcus equi.. J Vet Intern Med 2013 Jan-Feb;27(1):171-6.
    doi: 10.1111/jvim.12030pubmed: 23278131google scholar: lookup
  25. Venner M, Rödiger A, Laemmer M, Giguère S. Failure of antimicrobial therapy to accelerate spontaneous healing of subclinical pulmonary abscesses on a farm with endemic infections caused by Rhodococcus equi.. Vet J 2012 Jun;192(3):293-8.
    doi: 10.1016/j.tvjl.2011.07.004pubmed: 21924651google scholar: lookup
  26. Giguère S, Lee E, Williams E, Cohen ND, Chaffin MK, Halbert N, Martens RJ, Franklin RP, Clark CC, Slovis NM. Determination of the prevalence of antimicrobial resistance to macrolide antimicrobials or rifampin in Rhodococcus equi isolates and treatment outcome in foals infected with antimicrobial-resistant isolates of R equi.. J Am Vet Med Assoc 2010 Jul 1;237(1):74-81.
    doi: 10.2460/javma.237.1.74pubmed: 20590498google scholar: lookup
  27. Huber L, Giguère S, Slovis NM, Carter CN, Barr BS, Cohen ND, Elam J, Erol E, Locke SJ, Phillips ED, Smith JL. Emergence of Resistance to Macrolides and Rifampin in Clinical Isolates of Rhodococcus equi from Foals in Central Kentucky, 1995 to 2017.. Antimicrob Agents Chemother 2019 Jan;63(1).
    pmc: PMC6325176pubmed: 30373803doi: 10.1128/aac.01714-18google scholar: lookup
  28. Anastasi E, Giguère S, Berghaus LJ, Hondalus MK, Willingham-Lane JM, MacArthur I, Cohen ND, Roberts MC, Vazquez-Boland JA. Novel transferable erm(46) determinant responsible for emerging macrolide resistance in Rhodococcus equi.. J Antimicrob Chemother 2015 Dec;70(12):3184-90.
    doi: 10.1093/jac/dkv279pubmed: 26377866google scholar: lookup
  29. Álvarez-Narváez S, Giguère S, Anastasi E, Hearn J, Scortti M, Vázquez-Boland JA. Clonal Confinement of a Highly Mobile Resistance Element Driven by Combination Therapy in Rhodococcus equi.. mBio 2019 Oct 15;10(5).
    doi: 10.1128/mBio.02260-19pmc: PMC6794481pubmed: 31615959google scholar: lookup
  30. Burton AJ, Giguère S, Sturgill TL, Berghaus LJ, Slovis NM, Whitman JL, Levering C, Kuskie KR, Cohen ND. Macrolide- and rifampin-resistant Rhodococcus equi on a horse breeding farm, Kentucky, USA.. Emerg Infect Dis 2013 Feb;19(2):282-5.
    doi: 10.3201/eid1902.121210pmc: PMC3559061pubmed: 23347878google scholar: lookup
  31. Haggett EF. Antimicrobial use in foals: Do we need to change how we think?. Equine Vet J 2014 Mar;46(2):137-8.
    doi: 10.1111/evj.12178pubmed: 24548374google scholar: lookup
  32. Dunkel B, Johns IC. Antimicrobial use in critically ill horses.. J Vet Emerg Crit Care (San Antonio) 2015 Jan-Feb;25(1):89-100.
    doi: 10.1111/vec.12275pubmed: 25582245google scholar: lookup
  33. Orsini JA, Snooks-Parsons C, Stine L, Haddock M, Ramberg CF, Benson CE, Nunamaker DM. Vancomycin for the treatment of methicillin-resistant staphylococcal and enterococcal infections in 15 horses.. Can J Vet Res 2005 Oct;69(4):278-86.
    pmc: PMC1250240pubmed: 16479726
  34. Giguère S, Berghaus LJ, Lee EA. Activity of 10 antimicrobial agents against intracellular Rhodococcus equi.. Vet Microbiol 2015 Aug 5;178(3-4):275-8.
    doi: 10.1016/j.vetmic.2015.05.019pubmed: 26051479google scholar: lookup
  35. Magdesian KG. Antimicrobial Pharmacology for the Neonatal Foal.. Vet Clin North Am Equine Pract 2017 Apr;33(1):47-65.
    doi: 10.1016/j.cveq.2016.12.004pubmed: 28325182google scholar: lookup
  36. Coleman M, Kuskie K, Liu M, Chaffin K, Libal M, Giguère S, Bernstein L, Cohen N. In vitro antimicrobial activity of gallium maltolate against virulent Rhodococcus equi.. Vet Microbiol 2010 Nov 20;146(1-2):175-8.
    doi: 10.1016/j.vetmic.2010.05.027pubmed: 20554401google scholar: lookup
  37. Harrington JR, Martens RJ, Cohen ND, Bernstein LR. Antimicrobial activity of gallium against virulent Rhodococcus equiin vitro and in vivo.. J Vet Pharmacol Ther 2006 Apr;29(2):121-7.
    doi: 10.1111/j.1365-2885.2006.00723.xpubmed: 16515666google scholar: lookup
  38. Cohen ND, Slovis NM, Giguère S, Baker S, Chaffin MK, Bernstein LR. Gallium maltolate as an alternative to macrolides for treatment of presumed Rhodococcus equi pneumonia in foals.. J Vet Intern Med 2015 May-Jun;29(3):932-9.
    doi: 10.1111/jvim.12595pmc: PMC4895420pubmed: 25868480google scholar: lookup
  39. Chaffin MK, Fajt V, Martens RJ, Arnold CE, Cohen ND, O'Conor M, Taylor RJ, Bernstein LR. Pharmacokinetics of an orally administered methylcellulose formulation of gallium maltolate in neonatal foals.. J Vet Pharmacol Ther 2010 Aug;33(4):376-82.
    doi: 10.1111/j.1365-2885.2009.01150.xpubmed: 20646200google scholar: lookup
  40. Martens RJ, Cohen ND, Fajt VR, Nerren JR, Chaffin MK, Taylor RJ, Bernstein LR. Gallium maltolate: safety in neonatal foals following multiple enteral administrations.. J Vet Pharmacol Ther 2010 Apr;33(2):208-12.
    doi: 10.1111/j.1365-2885.2009.01121.xpubmed: 20444048google scholar: lookup
  41. Giguère S. Treatment of Infections Caused by Rhodococcus equi.. Vet Clin North Am Equine Pract 2017 Apr;33(1):67-85.
    doi: 10.1016/j.cveq.2016.11.002pubmed: 28161038google scholar: lookup
  42. Båverud V, Franklin A, Gunnarsson A, Gustafsson A, Hellander-Edman A. Clostridium difficile associated with acute colitis in mares when their foals are treated with erythromycin and rifampicin for Rhodococcus equi pneumonia.. Equine Vet J 1998 Nov;30(6):482-8.
    doi: 10.1111/j.2042-3306.1998.tb04523.xpubmed: 9844966google scholar: lookup
  43. Villarino N, Martín-Jiménez T. Pharmacokinetics of macrolides in foals.. J Vet Pharmacol Ther 2013 Feb;36(1):1-13.
    doi: 10.1111/jvp.12010pubmed: 23082900google scholar: lookup
  44. Chaffin MK, Cohen ND, Blodgett GP, Syndergaard M. Evaluation of ultrasonographic screening methods for early detection of Rhodococcus equi pneumonia in foals. J. Equine Vet. Sci 32 (2012).
  45. Morrison PK, Newbold CJ, Jones E, Worgan HJ, Grove-White DH, Dugdale AH, Barfoot C, Harris PA, Argo CM. The Equine Gastrointestinal Microbiome: Impacts of Age and Obesity.. Front Microbiol 2018;9:3017.
    doi: 10.3389/fmicb.2018.03017pmc: PMC6293011pubmed: 30581426google scholar: lookup
  46. Jacquay E, Jones E, Kouba J, Lillich J, Zeglin L. 63 Characterization of Foal Fecal Microbiome from Birth to Weaning and the Relationship to Mare Milk and Mare Feces. Journal of Animal Science 2018;96:33–33.
    doi: 10.1093/jas/sky073.061google scholar: lookup
  47. Salem SE, Maddox TW, Berg A, Antczak P, Ketley JM, Williams NJ, Archer DC. Variation in faecal microbiota in a group of horses managed at pasture over a 12-month period.. Sci Rep 2018 May 31;8(1):8510.
    doi: 10.1038/s41598-018-26930-3pmc: PMC5981443pubmed: 29855517google scholar: lookup
  48. Bordin AI, Suchodolski JS, Markel ME, Weaver KB, Steiner JM, Dowd SE, Pillai S, Cohen ND. Effects of administration of live or inactivated virulent Rhodococccus equi and age on the fecal microbiome of neonatal foals.. PLoS One 2013;8(6):e66640.
    doi: 10.1371/journal.pone.0066640pmc: PMC3681940pubmed: 23785508google scholar: lookup
  49. Parker EPK, Praharaj I, John J, Kaliappan SP, Kampmann B, Kang G, Grassly NC. Changes in the intestinal microbiota following the administration of azithromycin in a randomised placebo-controlled trial among infants in south India.. Sci Rep 2017 Aug 23;7(1):9168.
    doi: 10.1038/s41598-017-06862-0pmc: PMC5569098pubmed: 28835659google scholar: lookup
  50. Korpela K, Salonen A, Virta LJ, Kekkonen RA, Forslund K, Bork P, de Vos WM. Intestinal microbiome is related to lifetime antibiotic use in Finnish pre-school children.. Nat Commun 2016 Jan 26;7:10410.
    doi: 10.1038/ncomms10410pmc: PMC4737757pubmed: 26811868google scholar: lookup
  51. Rosas T, García-Ferris C, Domínguez-Santos R, Llop P, Latorre A, Moya A. Rifampicin treatment of Blattella germanica evidences a fecal transmission route of their gut microbiota.. FEMS Microbiol Ecol 2018 Feb 1;94(2).
    pubmed: 29325007doi: 10.1093/femsec/fiy002google scholar: lookup
  52. Dinos GP. The macrolide antibiotic renaissance.. Br J Pharmacol 2017 Sep;174(18):2967-2983.
    doi: 10.1111/bph.13936pmc: PMC5573421pubmed: 28664582google scholar: lookup
  53. Zhu JH, Wang BW, Pan M, Zeng YN, Rego H, Javid B. Rifampicin can induce antibiotic tolerance in mycobacteria via paradoxical changes in rpoB transcription.. Nat Commun 2018 Oct 11;9(1):4218.
    doi: 10.1038/s41467-018-06667-3pmc: PMC6181997pubmed: 30310059google scholar: lookup
  54. Iredell J, Brown J, Tagg K. Antibiotic resistance in Enterobacteriaceae: mechanisms and clinical implications.. BMJ 2016 Feb 8;352:h6420.
    doi: 10.1136/bmj.h6420pubmed: 26858245google scholar: lookup
  55. Langdon A, Crook N, Dantas G. The effects of antibiotics on the microbiome throughout development and alternative approaches for therapeutic modulation.. Genome Med 2016 Apr 13;8(1):39.
    doi: 10.1186/s13073-016-0294-zpmc: PMC4831151pubmed: 27074706google scholar: lookup
  56. Costa MC, Stämpfli HR, Arroyo LG, Allen-Vercoe E, Gomes RG, Weese JS. Changes in the equine fecal microbiota associated with the use of systemic antimicrobial drugs.. BMC Vet Res 2015 Feb 3;11:19.
    doi: 10.1186/s12917-015-0335-7pmc: PMC4323147pubmed: 25644524google scholar: lookup
  57. Chaffin MK, Cohen ND, Martens RJ. Chemoprophylactic effects of azithromycin against Rhodococcus equi-induced pneumonia among foals at equine breeding farms with endemic infections.. J Am Vet Med Assoc 2008 Apr 1;232(7):1035-47.
    doi: 10.2460/javma.232.7.1035pubmed: 18380623google scholar: lookup
  58. Walsh F, Duffy B. The culturable soil antibiotic resistome: a community of multi-drug resistant bacteria.. PLoS One 2013;8(6):e65567.
    doi: 10.1371/journal.pone.0065567pmc: PMC3680443pubmed: 23776501google scholar: lookup
  59. Li J, Rettedal EA, van der Helm E, Ellabaan M, Panagiotou G, Sommer MOA. Antibiotic Treatment Drives the Diversification of the Human Gut Resistome.. Genomics Proteomics Bioinformatics 2019 Feb;17(1):39-51.
    doi: 10.1016/j.gpb.2018.12.003pmc: PMC6520913pubmed: 31026582google scholar: lookup
  60. Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, Stedtfeld RD, Hashsham SA, Tiedje JM. Diverse and abundant antibiotic resistance genes in Chinese swine farms.. Proc Natl Acad Sci U S A 2013 Feb 26;110(9):3435-40.
    doi: 10.1073/pnas.1222743110pmc: PMC3587239pubmed: 23401528google scholar: lookup
  61. Kirst HA. Macrolide antibiotics in food-animal health.. Expert Opin Investig Drugs 1997 Feb;6(2):103-18.
    doi: 10.1517/13543784.6.2.103pubmed: 15989594google scholar: lookup
  62. Palmer KL, Kos VN, Gilmore MS. Horizontal gene transfer and the genomics of enterococcal antibiotic resistance.. Curr Opin Microbiol 2010 Oct;13(5):632-9.
    doi: 10.1016/j.mib.2010.08.004pmc: PMC2955785pubmed: 20837397google scholar: lookup
  63. Nolivos S, Cayron J, Dedieu A, Page A, Delolme F, Lesterlin C. Role of AcrAB-TolC multidrug efflux pump in drug-resistance acquisition by plasmid transfer.. Science 2019 May 24;364(6442):778-782.
    doi: 10.1126/science.aav6390pubmed: 31123134google scholar: lookup
  64. Willingham-Lane JM, Berghaus LJ, Berghaus RD, Hart KA, Giguère S. Effect of Macrolide and Rifampin Resistance on the Fitness of Rhodococcus equi.. Appl Environ Microbiol 2019 Apr 1;85(7).
    pmc: PMC6585491pubmed: 30683740doi: 10.1128/aem.02665-18google scholar: lookup
  65. Bernstein LR. Mechanisms of therapeutic activity for gallium.. Pharmacol Rev 1998 Dec;50(4):665-82.
    pubmed: 9860806
  66. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample.. Proc Natl Acad Sci U S A 2011 Mar 15;108 Suppl 1(Suppl 1):4516-22.
    doi: 10.1073/pnas.1000080107pmc: PMC3063599pubmed: 20534432google scholar: lookup
  67. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data.. Nat Methods 2016 Jul;13(7):581-3.
    doi: 10.1038/nmeth.3869pmc: PMC4927377pubmed: 27214047google scholar: lookup
  68. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data.. PLoS One 2013;8(4):e61217.
    doi: 10.1371/journal.pone.0061217pmc: PMC3632530pubmed: 23630581google scholar: lookup
  69. Wickham H. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York (2016).
  70. Pinheiro J, Bates D, DebRoy S, Sarka D, Team RC. nlme: Linear and Nonlinear Mixed Effects Models. (2019).
  71. Dixon P. VEGAN, a package of R functions for community ecology. Journal of Vegetation Science 2003;14:4.
    doi: 10.1111/j.1654-1103.2003.tb02228.xgoogle scholar: lookup
  72. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data.. Bioinformatics 2014 Aug 1;30(15):2114-20.
    doi: 10.1093/bioinformatics/btu170pmc: PMC4103590pubmed: 24695404google scholar: lookup
  73. Zhang J, Kobert K, Flouri T, Stamatakis A. PEAR: a fast and accurate Illumina Paired-End reAd mergeR.. Bioinformatics 2014 Mar 1;30(5):614-20.
    doi: 10.1093/bioinformatics/btt593pmc: PMC3933873pubmed: 24142950google scholar: lookup
  74. Lakin SM, Dean C, Noyes NR, Dettenwanger A, Ross AS, Doster E, Rovira P, Abdo Z, Jones KL, Ruiz J, Belk KE, Morley PS, Boucher C. MEGARes: an antimicrobial resistance database for high throughput sequencing.. Nucleic Acids Res 2017 Jan 4;45(D1):D574-D580.
    doi: 10.1093/nar/gkw1009pmc: PMC5210519pubmed: 27899569google scholar: lookup
  75. McArthur AG, Waglechner N, Nizam F, Yan A, Azad MA, Baylay AJ, Bhullar K, Canova MJ, De Pascale G, Ejim L, Kalan L, King AM, Koteva K, Morar M, Mulvey MR, O'Brien JS, Pawlowski AC, Piddock LJ, Spanogiannopoulos P, Sutherland AD, Tang I, Taylor PL, Thaker M, Wang W, Yan M, Yu T, Wright GD. The comprehensive antibiotic resistance database.. Antimicrob Agents Chemother 2013 Jul;57(7):3348-57.
    doi: 10.1128/AAC.00419-13pmc: PMC3697360pubmed: 23650175google scholar: lookup
  76. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND.. Nat Methods 2015 Jan;12(1):59-60.
    pubmed: 25402007doi: 10.1038/nmeth.3176google scholar: lookup
  77. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences.. Bioinformatics 2006 Jul 1;22(13):1658-9.
    doi: 10.1093/bioinformatics/btl158pubmed: 16731699google scholar: lookup
  78. Woolcock JB, Farmer AM, Mutimer MD. Selective medium for Corynebacterium equi isolation.. J Clin Microbiol 1979 May;9(5):640-2.
    pmc: PMC275365pubmed: 479362doi: 10.1128/jcm.9.5.640-642.1979google scholar: lookup
  79. Grimm MB, Cohen ND, Slovis NM, Mundy GD, Harrington JR, Libal MC, Takai S, Martens RJ. Evaluation of fecal samples from mares as a source of Rhodococcus equi for their foals by use of quantitative bacteriologic culture and colony immunoblot analyses.. Am J Vet Res 2007 Jan;68(1):63-71.
    doi: 10.2460/ajvr.68.1.63pubmed: 17199420google scholar: lookup
  80. Halbert ND, Reitzel RA, Martens RJ, Cohen ND. Evaluation of a multiplex polymerase chain reaction assay for simultaneous detection of Rhodococcus equi and the vapA gene.. Am J Vet Res 2005 Aug;66(8):1380-5.
    doi: 10.2460/ajvr.2005.66.1380pubmed: 16173481google scholar: lookup
  81. Zaheer R, Cook SR, Klima CL, Stanford K, Alexander T, Topp E, Read RR, McAllister TA. Effect of subtherapeutic vs. therapeutic administration of macrolides on antimicrobial resistance in Mannheimia haemolytica and enterococci isolated from beef cattle.. Front Microbiol 2013;4:133.
    doi: 10.3389/fmicb.2013.00133pmc: PMC3664329pubmed: 23750157google scholar: lookup
  82. Huber L, Giguère S, Cohen ND, Slovis NM, Berghaus L, Greiter M, Hart KA. Identification of macrolide- and rifampicin-resistant Rhodococcus equi in environmental samples from equine breeding farms in central Kentucky during 2018.. Vet Microbiol 2019 May;232:74-78.
    doi: 10.1016/j.vetmic.2019.04.008pubmed: 31030848google scholar: lookup
  83. Šidák ZK. Rectangular confidence regions for the means of multivariable normal distributions. J Am Stat Assoc 1967;62:626–633.
  84. Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P, Tsang KK, Lago BA, Dave BM, Pereira S, Sharma AN, Doshi S, Courtot M, Lo R, Williams LE, Frye JG, Elsayegh T, Sardar D, Westman EL, Pawlowski AC, Johnson TA, Brinkman FS, Wright GD, McArthur AG. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database.. Nucleic Acids Res 2017 Jan 4;45(D1):D566-D573.
    doi: 10.1093/nar/gkw1004pmc: PMC5210516pubmed: 27789705google scholar: lookup

Citations

This article has been cited 22 times.
  1. Pimenta J, Pinto AR, Saavedra MJ, Cotovio M. Equine Gram-Negative Oral Microbiota: An Antimicrobial Resistances Watcher?. Antibiotics (Basel) 2023 Apr 21;12(4).
    doi: 10.3390/antibiotics12040792pubmed: 37107153google scholar: lookup
  2. Theelen MJP, Luiken REC, Wagenaar JA, Sloet van Oldruitenborgh-Oosterbaan MM, Rossen JWA, Schaafstra FJWC, van Doorn DA, Zomer AL. Longitudinal study of the short- and long-term effects of hospitalisation and oral trimethoprim-sulfadiazine administration on the equine faecal microbiome and resistome. Microbiome 2023 Feb 27;11(1):33.
    doi: 10.1186/s40168-023-01465-6pubmed: 36850017google scholar: lookup
  3. Nwobi OC, Anyanwu MU, Jaja IF, Nwankwo IO, Okolo CC, Nwobi CA, Ezenduka EV, Oguttu JW. Staphylococcus aureus in Horses in Nigeria: Occurrence, Antimicrobial, Methicillin and Heavy Metal Resistance and Virulence Potentials. Antibiotics (Basel) 2023 Jan 24;12(2).
    doi: 10.3390/antibiotics12020242pubmed: 36830153google scholar: lookup
  4. Wongtawan T, Narinthorn R, Sontigun N, Sansamur C, Petcharat Y, Fungwithaya P, Saengsawang P, Blackall PJ, Thomrongsuwannakij T. Characterizing the antimicrobial resistance profile of Escherichia coli found in sport animals (fighting cocks, fighting bulls, and sport horses) and soils from their environment. Vet World 2022 Nov;15(11):2673-2680.
    doi: 10.14202/vetworld.2022.2673-2680pubmed: 36590125google scholar: lookup
  5. Lord J, Carter C, Smith J, Locke S, Phillips E, Odoi A. Antimicrobial resistance among Streptococcus equi subspecies zooepidemicus and Rhodococcus equi isolated from equine specimens submitted to a diagnostic laboratory in Kentucky, USA. PeerJ 2022;10:e13682.
    doi: 10.7717/peerj.13682pubmed: 36164606google scholar: lookup
  6. Anyanwu MU, Jaja IF, Nwobi OC, Mgbeahuruike AC, Ikpendu CN, Okafor NA, Oguttu JW. Epidemiology and Traits of Mobile Colistin Resistance (mcr) Gene-Bearing Organisms from Horses. Microorganisms 2022 Jul 25;10(8).
    doi: 10.3390/microorganisms10081499pubmed: 35893557google scholar: lookup
  7. Sting R, Schwabe I, Kieferle M, Münch M, Rau J. Fatal Infection in an Alpaca (Vicugna pacos) Caused by Pathogenic Rhodococcus equi. Animals (Basel) 2022 May 19;12(10).
    doi: 10.3390/ani12101303pubmed: 35625149google scholar: lookup
  8. Fungwithaya P, Boonchuay K, Narinthorn R, Sontigun N, Sansamur C, Petcharat Y, Thomrongsuwannakij T, Wongtawan T. First study on diversity and antimicrobial-resistant profile of staphylococci in sports animals of Southern Thailand. Vet World 2022 Mar;15(3):765-774.
    doi: 10.14202/vetworld.2022.765-774pubmed: 35497942google scholar: lookup
  9. Ang L, Vinderola G, Endo A, Kantanen J, Jingfeng C, Binetti A, Burns P, Qingmiao S, Suying D, Zujiang Y, Rios-Covian D, Mantziari A, Beasley S, Gomez-Gallego C, Gueimonde M, Salminen S. Gut Microbiome Characteristics in feral and domesticated horses from different geographic locations. Commun Biol 2022 Feb 25;5(1):172.
    doi: 10.1038/s42003-022-03116-2pubmed: 35217713google scholar: lookup
  10. Rochegüe T, Haenni M, Mondot S, Astruc C, Cazeau G, Ferry T, Madec JY, Lupo A. Impact of Antibiotic Therapies on Resistance Genes Dynamic and Composition of the Animal Gut Microbiota. Animals (Basel) 2021 Nov 16;11(11).
    doi: 10.3390/ani11113280pubmed: 34828011google scholar: lookup
  11. Ma T, McAllister TA, Guan LL. A review of the resistome within the digestive tract of livestock. J Anim Sci Biotechnol 2021 Nov 11;12(1):121.
    doi: 10.1186/s40104-021-00643-6pubmed: 34763729google scholar: lookup
  12. Freccero F, Lanci A, Mariella J, Viciani E, Quercia S, Castagnetti A, Castagnetti C. Changes in the Fecal Microbiota Associated with a Broad-Spectrum Antimicrobial Administration in Hospitalized Neonatal Foals with Probiotics Supplementation. Animals (Basel) 2021 Aug 2;11(8).
    doi: 10.3390/ani11082283pubmed: 34438741google scholar: lookup
  13. Cohen ND, Kahn SK, Cywes-Bentley C, Ramirez-Cortez S, Schuckert AE, Vinacur M, Bordin AI, Pier GB. Serum Antibody Activity against Poly-N-Acetyl Glucosamine (PNAG), but Not PNAG Vaccination Status, Is Associated with Protecting Newborn Foals against Intrabronchial Infection with Rhodococcus equi. Microbiol Spectr 2021 Sep 3;9(1):e0063821.
    doi: 10.1128/Spectrum.00638-21pubmed: 34319137google scholar: lookup
  14. Álvarez-Narváez S, Huber L, Giguère S, Hart KA, Berghaus RD, Sanchez S, Cohen ND. Epidemiology and Molecular Basis of Multidrug Resistance in Rhodococcus equi. Microbiol Mol Biol Rev 2021 May 19;85(2).
    doi: 10.1128/MMBR.00011-21pubmed: 33853933google scholar: lookup
  15. Bordin AI, Cohen ND, Giguère S, Bray JM, Berghaus LJ, Scott B, Johnson R, Hook M. Host-directed therapy in foals can enhance functional innate immunity and reduce severity of Rhodococcus equi pneumonia. Sci Rep 2021 Jan 28;11(1):2483.
    doi: 10.1038/s41598-021-82049-ypubmed: 33510265google scholar: lookup
  16. Álvarez-Narváez S, Giguère S, Cohen N, Slovis N, Vázquez-Boland JA. Spread of Multidrug-Resistant Rhodococcus equi, United States. Emerg Infect Dis 2021 Feb;27(2):529-537.
    doi: 10.3201/eid2702.203030pubmed: 33496218google scholar: lookup
  17. Sato W, Sukmawinata E, Uemura R, Kanda T, Kusano K, Kambayashi Y, Sato T, Ishikawa Y, Toya R, Sueyoshi M. Antimicrobial resistance profiles and phylogenetic groups of Escherichia coli isolated from healthy Thoroughbred racehorses in Japan. J Equine Sci 2020;31(4):85-91.
    doi: 10.1294/jes.31.85pubmed: 33376444google scholar: lookup
  18. Steinman A, Navon-Venezia S. Antimicrobial Resistance in Horses. Animals (Basel) 2020 Jul 9;10(7).
    doi: 10.3390/ani10071161pubmed: 32659916google scholar: lookup
  19. Baptiste KE, Kyvsgaard NC, Ahmed MO, Damborg P, Dowling PM. Is Rifampin (Rifampicin) Essential for the Treatment of Rhodococcus equi Infections in Foals? A Critical Review of the Role of Rifampin. J Vet Pharmacol Ther 2025 Sep;48(5):345-358.
    doi: 10.1111/jvp.70007pubmed: 40552784google scholar: lookup
  20. Kabir A, Lamichhane B, Habib T, Adams A, El-Sheikh Ali H, Slovis NM, Troedsson MHT, Helmy YA. Antimicrobial Resistance in Equines: A Growing Threat to Horse Health and Beyond-A Comprehensive Review. Antibiotics (Basel) 2024 Jul 29;13(8).
    doi: 10.3390/antibiotics13080713pubmed: 39200013google scholar: lookup
  21. Álvarez Narváez S, Beaudry MS, Norris CG, Bartlett PB, Glenn TC, Sanchez S. Improved Equine Fecal Microbiome Characterization Using Target Enrichment by Hybridization Capture. Animals (Basel) 2024 Jan 29;14(3).
    doi: 10.3390/ani14030445pubmed: 38338088google scholar: lookup
  22. Alvarez Narvaez S, Sanchez S. Exploring the Accessory Genome of Multidrug-Resistant Rhodococcus equi Clone 2287. Antibiotics (Basel) 2023 Nov 17;12(11).
    doi: 10.3390/antibiotics12111631pubmed: 37998833google scholar: lookup
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