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Veterinary research2024; 55(1); 108; doi: 10.1186/s13567-024-01364-0

Prevalence and risk factors associated with nasal carriage of methicillin-resistant staphylococci in horses and their caregivers.

Abstract: Antimicrobial resistance is a global threat, and pet-associated strains may pose a risk to human health. Equine veterinarians are at high risk of carrying methicillin-resistant staphylococci (MRS), but specific risk factors remain elusive, and few data are available for other personnel involved in the horse industry. The prevalence, characteristics, and risk factors for nasal carriage of MRS in horses and their caregivers were studied in northwestern Italy. Nasal swabs from 110 asymptomatic horses housed at 21 barns and 34 human caregivers were collected. Data on barns, horses, and personnel were acquired through questionnaires. The samples were incubated in selective media, and the bacterial isolates were identified by mass spectrometry. Risk factors were investigated by Poisson regression. MRS were isolated from 33 horses (30%), 11 humans (32.4%) and 3 environmental samples (14.2%). Most isolates were multidrug resistant (MDRS). The prevalence of MRS and MDRS was greater in racehorses and their personnel than in pleasurable and jumping/dressing horses. MRS carriage in caregivers was associated with an increased prevalence of MRS carriage in horses. The frequency of antimicrobial treatments administered in the barn during the last 12 months was a risk factor for MRS carriage in horses [prevalence ratio (PR) 3.97, 95% CI 1.11, 14.13] and caregivers (PR 2.00, 95% CI 1.05, 3.82), whereas a good ventilation index of the horse tabling environment was a protective factor (PR 0.43, 95% CI 0.20, 0.92). Our data reveal relevant interactions occurring between bacterial communities of horses and humans that share the same environment, suggesting that One Health surveillance programs should be implemented.
Publication Date: 2024-09-09 PubMed ID: 39252070PubMed Central: PMC11386249DOI: 10.1186/s13567-024-01364-0Google Scholar: Lookup
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  • Journal Article

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.

Overview

  • This study investigates the prevalence and risk factors for nasal carriage of methicillin-resistant staphylococci (MRS) in horses and their human caregivers in northwestern Italy.
  • It highlights multidrug resistance in these bacteria and identifies key environmental and management factors associated with MRS carriage in both animals and humans sharing the same environment.

Background and Importance

  • Antimicrobial resistance (AMR) is a critical global health threat affecting both humans and animals.
  • Staphylococci resistant to methicillin (MRS) are significant because they are difficult to treat and can spread between animals and humans.
  • Equine veterinarians and other personnel working closely with horses may be at higher risk of carrying these resistant bacteria.
  • Understanding the prevalence of MRS in horses and their caregivers, and identifying risk factors for nasal carriage, is essential to improve infection control and limit transmission.

Study Design and Methods

  • The study was conducted in northwestern Italy and involved:
    • 110 asymptomatic horses housed at 21 different barns
    • 34 human caregivers working with these horses
    • Environmental samples from the barns
  • Data collection involved:
    • Nasal swabs taken from horses and humans for bacterial culture
    • Questionnaires gathering information on barn conditions, horse management, and personnel practices
  • Laboratory analysis:
    • Samples incubated in selective media to isolate methicillin-resistant staphylococci
    • Bacterial identification carried out using mass spectrometry
  • Statistical analysis used Poisson regression to identify significant risk factors for MRS nasal carriage.

Key Findings

  • Prevalence of MRS carriage:
    • 33 out of 110 horses (30%) were carriers of methicillin-resistant staphylococci
    • 11 out of 34 human caregivers (32.4%) were carriers
    • 3 environmental samples (14.2%) tested positive for MRS
  • Resistance profile:
    • Most bacterial isolates were multidrug-resistant staphylococci (MDRS), indicating resistance to multiple antibiotics
  • Differences by horse type:
    • Racehorses and their caregivers had higher prevalence of MRS and MDRS compared to pleasurable riding and jumping/dressing horses
  • Association between humans and horses:
    • MRS carriage in caregivers was linked to increased risk of MRS carriage in the horses they handled, indicating possible transmission or shared exposure
  • Significant risk and protective factors identified:
    • Frequency of antimicrobial treatments in the barn over the prior 12 months increased the prevalence of MRS carriage:
      • For horses, prevalence ratio (PR) was 3.97 (95% CI: 1.11 to 14.13)
      • For caregivers, PR was 2.00 (95% CI: 1.05 to 3.82)
    • Good ventilation in horse housing was protective against MRS carriage:
      • PR 0.43 (95% CI: 0.20 to 0.92)

Implications and Recommendations

  • The study highlights important interactions between bacterial communities of horses and their human caregivers sharing the same environment.
  • This indicates potential zoonotic transmission routes and suggests the need for integrated surveillance approaches targeting both animal and human health sectors.
  • The findings support implementing “One Health” programs that monitor antimicrobial resistance across humans, animals, and their shared environments.
  • Emphasis on proper antimicrobial stewardship in horse barns is critical to reduce selective pressure favoring resistant strains.
  • Improving barn ventilation and environmental management may be effective in lowering the risk of nasal carriage of MRS.

Concluding Summary

  • Methicillin-resistant and multidrug-resistant staphylococci were commonly found in horses and caregivers within the studied barns.
  • Caregivers and horses influence each other’s carriage status, highlighting bidirectional or shared risks.
  • Antimicrobial use practices and environmental conditions like ventilation are modifiable factors that affect MRS prevalence.
  • These findings underline the importance of coordinated efforts spanning veterinary and human healthcare to control antimicrobial resistance.

Cite This Article

APA
Bullone M, Bellato A, Robino P, Nebbia P, Morello S, Marchis D, Tarducci A, Ru G. (2024). Prevalence and risk factors associated with nasal carriage of methicillin-resistant staphylococci in horses and their caregivers. Vet Res, 55(1), 108. https://doi.org/10.1186/s13567-024-01364-0

Publication

ISSN: 1297-9716
NlmUniqueID: 9309551
Country: England
Language: English
Volume: 55
Issue: 1
Pages: 108
PII: 108

Researcher Affiliations

Bullone, Michela
  • Department of Veterinary Sciences, University of Torino, Largo Paolo Braccini 2, 10095, Grugliasco, Italy. michela.bullone@unito.it.
Bellato, Alessandro
  • Department of Veterinary Sciences, University of Torino, Largo Paolo Braccini 2, 10095, Grugliasco, Italy.
Robino, Patrizia
  • Department of Veterinary Sciences, University of Torino, Largo Paolo Braccini 2, 10095, Grugliasco, Italy.
Nebbia, Patrizia
  • Department of Veterinary Sciences, University of Torino, Largo Paolo Braccini 2, 10095, Grugliasco, Italy.
Morello, Sara
  • Feed Hygiene Laboratory, Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d'Aosta, via Bologna 148, 10154, Torino, Italy.
Marchis, Daniela
  • Feed Hygiene Laboratory, Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d'Aosta, via Bologna 148, 10154, Torino, Italy.
Tarducci, Alberto
  • Department of Veterinary Sciences, University of Torino, Largo Paolo Braccini 2, 10095, Grugliasco, Italy.
Ru, Giuseppe
  • Biostatistics, Epidemiology and Risk Analysis Unit, Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d'Aosta, via Bologna 220, 10154, Torino, Italy.

MeSH Terms

  • Animals
  • Horses
  • Risk Factors
  • Horse Diseases / microbiology
  • Horse Diseases / epidemiology
  • Prevalence
  • Staphylococcal Infections / veterinary
  • Staphylococcal Infections / epidemiology
  • Staphylococcal Infections / microbiology
  • Carrier State / veterinary
  • Carrier State / epidemiology
  • Carrier State / microbiology
  • Methicillin-Resistant Staphylococcus aureus / drug effects
  • Methicillin-Resistant Staphylococcus aureus / isolation & purification
  • Italy / epidemiology
  • Humans
  • Female
  • Male
  • Caregivers

Grant Funding

  • Erogazioni Ordinarie (RF #2018.0587). / Fondazione CRT

Conflict of Interest Statement

The authors declare that they have no competing interests.

References

This article includes 54 references
  1. Hogan PG, Mork RL, Boyle MG, Muenks CE, Morelli JJ, Thompson RM, Sullivan ML, Gehlert SJ, Merlo JR, McKenzie MG, Wardenburg JB, Rzhetsky A, Burnham CD, Fritz SA. Interplay of personal, pet, and environmental colonization in households affected by community-associated methicillin-resistant. J Infect 78:200–207.
    doi: 10.1016/j.jinf.2018.11.006pmc: PMC6408279pubmed: 30503843google scholar: lookup
  2. Zainab SM, Junaid M, Xu N, Malik RN. Antibiotics and antibiotic resistant genes (ARGs) in groundwater: a global review on dissemination, sources, interactions, environmental and human health risks. Water Res 187:116455.
    doi: 10.1016/j.watres.2020.116455pubmed: 33032106google scholar: lookup
  3. Grundmann H, Aires-de-Sousa M, Boyce J, Tiemersma E. Emergence and resurgence of meticillin-resistant as a public-health threat. Lancet 368:874–885.
    doi: 10.1016/S0140-6736(06)68853-3pubmed: 16950365google scholar: lookup
  4. Bollig ER, Granick JL, Webb TL, Ward C, Beaudoin AL. A quarterly survey of antibiotic prescribing in small animal and equine practices-Minnesota and North Dakota, 2020. Zoonoses Public Health 69:864–874.
    doi: 10.1111/zph.12979pmc: PMC9796041pubmed: 35643964google scholar: lookup
  5. Fitzgerald JR. Livestock-associated : origin, evolution and public health threat. Trends Microbiol 20:192–198.
    doi: 10.1016/j.tim.2012.01.006pubmed: 22386364google scholar: lookup
  6. Mehta A, Rodrigues C, Kumar R, Rattan A, Sridhar H, Mattoo V, Ginde V. A pilot programme of MRSA surveillance in India. J Postgrad Med 42:1–3.
    pubmed: 9715287
  7. Van Embden JD, Van Soolingen D, Heersma HF, De Neeling AJ, Jones ME, Steiert M, Grek V, Mooi FR, Verhoef J. Establishment of a European network for the surveillance of , MRSA and penicillin-resistant pneumococci. J Antimicrob Chemother 38:905–907.
    doi: 10.1093/jac/38.5.905pubmed: 8961063google scholar: lookup
  8. Johnson AP, Davies J, Guy R, Abernethy J, Sheridan E, Pearson A, Duckworth G. Mandatory surveillance of methicillin-resistant (MRSA) bacteraemia in England: the first 10 years. J Antimicrob Chemother 67:802–809.
    doi: 10.1093/jac/dkr561pubmed: 22223229google scholar: lookup
  9. Schonfeld V, Diercke M, Gilsdorf A, Eckmanns T, Walter J. Evaluation of the statutory surveillance system for invasive MRSA infections in Germany, 2016–2017. BMC Public Health 18:1063.
    doi: 10.1186/s12889-018-5971-ypmc: PMC6109305pubmed: 30143016google scholar: lookup
  10. Jordan D, Simon J, Fury S, Moss S, Giffard P, Maiwald M, Southwell P, Barton MD, Axon JE, Morris SG, Trott DJ. Carriage of methicillin-resistant by veterinarians in Australia. Aust Vet J 89:152–159.
  11. Becker K, Both A, Weisselberg S, Heilmann C, Rohde H. Emergence of coagulase-negative staphylococci. Expert Rev Anti Infect Ther 18:349–366.
    doi: 10.1080/14787210.2020.1730813pubmed: 32056452google scholar: lookup
  12. Becker K, Heilmann C, Peters G. Coagulase-negative staphylococci. Clin Microbiol Rev 27:870–926.
    doi: 10.1128/CMR.00109-13pmc: PMC4187637pubmed: 25278577google scholar: lookup
  13. Catry B, Van Duijkeren E, Pomba MC, Greko C, Moreno MA, Pyörälä S, Ruzauskas M, Sanders P, Threlfall EJ, Ungemach F, Törneke K, Munoz-Madero C, Torren-Edo J. Reflection paper on MRSA in food-producing and companion animals: epidemiology and control options for human and animal health. Epidemiol Infect 138:626–644.
    doi: 10.1017/S0950268810000014pubmed: 20141646google scholar: lookup
  14. Loeffler A, Pfeiffer DU, Lindsay JA, Soares Magalhaes RJ, Lloyd DH. Prevalence of and risk factors for MRSA carriage in companion animals: a survey of dogs, cats and horses. Epidemiol Infect 139:1019–1028.
    doi: 10.1017/S095026881000227Xpubmed: 20943000google scholar: lookup
  15. Weese JS, Lefebvre SL. Risk factors for methicillin-resistant colonization in horses admitted to a veterinary teaching hospital. Can Vet J 48:921–926.
    pmc: PMC1950112pubmed: 17966332
  16. Weese JS, Rousseau J, Traub-Dargatz JL, Willey BM, McGeer AJ, Low DE. Community-associated methicillin-resistant in horses and humans who work with horses. J Am Vet Med Assoc 226:580–583.
    doi: 10.2460/javma.2005.226.580pubmed: 15742700google scholar: lookup
  17. Adams R, Smith J, Locke S, Phillips E, Erol E, Carter C, Odoi A. An epidemiologic study of antimicrobial resistance of species isolated from equine samples submitted to a diagnostic laboratory. BMC Vet Res 14:42.
    doi: 10.1186/s12917-018-1367-6pmc: PMC5800099pubmed: 29402294google scholar: lookup
  18. EFSA Panel on Animal Health and Welfare (AHAW), Nielsen SS, Bicout DJ, Calistri P, Canali E, Drewe JA, Garin-Bastuji B, Gonzales Rojas JL, Gortazar Schmidt C, Herskin M, Michel V, Miranda Chueca MA, Padalino B, Pasquali P, Roberts HC, Sihvonen LH, Spoolder H, Stahl K, Velarde A, Viltrop A, Winckler C, Dewulf J, Guardabassi L, Hilbert F, Mader R, Baldinelli F, Alvarez J. Assessment of animal diseases caused by bacteria resistant to antimicrobials: horses. EFSA J 19:e07112.
  19. Roudaud M, Allano M, Fairbrother JH, Sauve F. A retrospective study on methicillin-resistant Staphylococcus spp. isolated from horses admitted to a Canadian veterinary teaching hospital between 2008 and 2018. Can Vet J 61:1197–1202.
    pmc: PMC7560767pubmed: 33149358
  20. Tirosh-Levy S, Steinman A, Carmeli Y, Klement E, Navon-Venezia S. Prevalence and risk factors for colonization with methicillin resistant and other Staphylococci species in hospitalized and farm horses in Israel. Prev Vet Med 122:135–144.
  21. Mallardo K, Nizza S, Fiorito F, Pagnini U, De Martino L. A comparative evaluation of methicillin-resistant staphylococci isolated from harness racing-horses, breeding mares and riding-horses in Italy. Asian Pac J Trop Biomed 3:169–173.
  22. Peterson AE, Davis MF, Awantang G, Limbago B, Fosheim GE, Silbergeld EK. Correlation between animal nasal carriage and environmental methicillin-resistant isolates at U.S. horse and cattle farms. Vet Microbiol 160:539–543.
    doi: 10.1016/j.vetmic.2012.06.032pubmed: 22795260google scholar: lookup
  23. Van den Eede A, Martens A, Feryn I, Vanderhaeghen W, Lipinska U, Gasthuys F, Butaye P, Haesebrouck F, Hermans K. Low MRSA prevalence in horses at farm level. BMC Vet Res 8:213.
    doi: 10.1186/1746-6148-8-213pmc: PMC3536571pubmed: 23134703google scholar: lookup
  24. Groves MD, Crouch B, Coombs GW, Jordan D, Pang S, Barton MD, Giffard P, Abraham S, Trott DJ. Molecular epidemiology of methicillin-resistant isolated from Australian veterinarians. PLoS One 11:e0146034.
  25. Moodley A, Nightingale EC, Stegger M, Nielsen SS, Skov RL, Guardabassi L. High risk for nasal carriage of methicillin-resistant among Danish veterinary practitioners. Scand J Work Environ Health 34:151–157.
    doi: 10.5271/sjweh.1219pubmed: 18470441google scholar: lookup
  26. Maddox TW, Pinchbeck GL, Clegg PD, Wedley AL, Dawson S, Williams NJ. Cross-sectional study of antimicrobial-resistant bacteria in horses. Part 2: risk factors for faecal carriage of antimicrobial-resistant in horses. Equine Vet J 44:297–303.
  27. Van den Eede A, Hermans K, Van den Abeele A, Flore K, Dewulf J, Vanderhaeghen W, Némeghaire S, Butaye P, Gasthuys F, Haesebrouck F, Martens A. The nasal vestibulum is the optimal sampling site for MRSA screening in hospitalised horses. Vet J 197:415–419.
    doi: 10.1016/j.tvjl.2013.01.031pubmed: 23465751google scholar: lookup
  28. Bocher S, Smyth R, Kahlmeter G, Kerremans J, Vos MC, Skov R. Evaluation of four selective agars and two enrichment broths in screening for methicillin-resistant . J Clin Microbiol 46:3136–3138.
    doi: 10.1128/JCM.00478-08pmc: PMC2546728pubmed: 18632905google scholar: lookup
  29. Smyth RW, Kahlmeter G. Mannitol salt agar-cefoxitin combination as a screening medium for methicillin-resistant . J Clin Microbiol 43:3797–3799.
  30. Stegger M, Andersen PS, Kearns A, Pichon B, Holmes MA, Edwards G, Laurent F, Teale C, Skov R, Larsen AR. Rapid detection, differentiation and typing of methicillin-resistant harbouring either mecA or the new mecA homologue mecA(LGA251). Clin Microbiol Infect 18:395–400.
  31. Johnston R, Jones K, Manley D. Confounding and collinearity in regression analysis: a cautionary tale and an alternative procedure, illustrated by studies of British voting behaviour. Qual Quant 52:1957–1976.
    doi: 10.1007/s11135-017-0584-6pmc: PMC5993839pubmed: 29937587google scholar: lookup
  32. Boyle AG, Timoney JF, Newton JR, Hines MT, Waller AS, Buchanan BR. infections in horses: guidelines for treatment, control, and prevention of strangles-revised consensus statement. J Vet Intern Med 32:633–647.
    doi: 10.1111/jvim.15043pmc: PMC5867011pubmed: 29424487google scholar: lookup
  33. Dayaram A, Seeber PA, Greenwood AD. Environmental detection and potential transmission of equine herpesviruses. Pathogens 10:423.
    doi: 10.3390/pathogens10040423pmc: PMC8066653pubmed: 33916280google scholar: lookup
  34. Busscher JF, van Duijkeren E, van Sloet MM. The prevalence of methicillin-resistant staphylococci in healthy horses in the Netherlands. Vet Microbiol 113:131–136.
    doi: 10.1016/j.vetmic.2005.10.028pubmed: 16303264google scholar: lookup
  35. Maddox TW, Clegg PD, Diggle PJ, Wedley AL, Dawson S, Pinchbeck GL, Williams NJ. Cross-sectional study of antimicrobial-resistant bacteria in horses. Part 1: prevalence of antimicrobial-resistant and methicillin-resistant . Equine Vet J 44:289–296.
  36. Bortolami A, Williams NJ, McGowan CM, Kelly PG, Archer DC, Corro M, Pinchbeck G, Saunders CJ, Timofte D. Environmental surveillance identifies multiple introductions of MRSA CC398 in an Equine Veterinary Hospital in the UK, 2011–2016. Sci Rep 7:5499.
    doi: 10.1038/s41598-017-05559-8pmc: PMC5511188pubmed: 28710350google scholar: lookup
  37. Carfora V, Caprioli A, Grossi I, Pepe M, Alba P, Lorenzetti S, Amoruso R, Sorbara L, Franco A, Battisti A. A methicillin-resistant (MRSA) sequence type 8, spa type t11469 causing infection and colonizing horses in Italy. Pathog Dis 74:ftw025.
    doi: 10.1093/femspd/ftw025pubmed: 27052029google scholar: lookup
  38. Cuny C, Abdelbary MMH, Kock R, Layer F, Scheidemann W, Werner G, Witte W. Methicillin-resistant from infections in horses in Germany are frequent colonizers of veterinarians but rare among MRSA from infections in humans. One Health 2:11–17.
  39. Van den Eede A, Martens A, Flore K, Denis O, Gasthuys F, Haesebrouck F, Van den Abeele A, Hermans K. MRSA carriage in the equine community: an investigation of horse-caretaker couples. Vet Microbiol 163:313–318.
    doi: 10.1016/j.vetmic.2012.12.038pubmed: 23434186google scholar: lookup
  40. Loncaric I, Tichy A, Handler S, Szostak MP, Tickert M, Diab-Elschahawi M, Spergser J, Künzel F. Prevalence of methicillin-resistant sp. (MRS) in different companion animals and determination of risk factors for colonization with MRS. Antibiotics 8:36.
    doi: 10.3390/antibiotics8020036pmc: PMC6627599pubmed: 30959767google scholar: lookup
  41. Rossi TM, Moore A, O’Sullivan TL, Greer AL. Equine rhinitis a virus infection at a standardbred training facility: incidence, clinical signs, and risk factors for clinical disease. Front Vet Sci 6:71.
    doi: 10.3389/fvets.2019.00071pmc: PMC6424864pubmed: 30918893google scholar: lookup
  42. Weese JS, Sabino C. Scrutiny of antimicrobial use in racing horses with allergic small airway inflammatory disease. Can Vet J 46:438–489.
    pmc: PMC1090451pubmed: 16018565
  43. Hobday RA, Dancer SJ. Roles of sunlight and natural ventilation for controlling infection: historical and current perspectives. J Hosp Infect 84:271–282.
    doi: 10.1016/j.jhin.2013.04.011pmc: PMC7132476pubmed: 23790506google scholar: lookup
  44. Angen O, Nielsen MW, Lofstrom P, Larsen AR, Hendriksen NB. Airborne spread of methicillin resistant from a swine farm. Front Vet Sci 8:644729.
    doi: 10.3389/fvets.2021.644729pmc: PMC8211894pubmed: 34150881google scholar: lookup
  45. Bai H, He LY, Wu DL, Gao FZ, Zhang M, Zou HY, Yao MS, Ying GG. Spread of airborne antibiotic resistance from animal farms to the environment: dispersal pattern and exposure risk. Environ Int 158:106927.
    doi: 10.1016/j.envint.2021.106927pubmed: 34673316google scholar: lookup
  46. Bos ME, Verstappen KM, van Cleef BA, Dohmen W, Dorado-Garcia A, Graveland H, Duim B, Wagenaar JA, Kluytmans JA, Heederik DJ. Transmission through air as a possible route of exposure for MRSA. J Expo Sci Environ Epidemiol 26:263–269.
    doi: 10.1038/jes.2014.85pubmed: 25515375google scholar: lookup
  47. Kaiser-Thom S, Gerber V, Collaud A, Hurni J, Perreten V. Prevalence and WGS-based characteristics of in the nasal mucosa and pastern of horses with equine pastern dermatitis. BMC Vet Res 18:79.
    doi: 10.1186/s12917-021-03053-ypmc: PMC8867626pubmed: 35209904google scholar: lookup
  48. Congdon ST, Guaglione JA, Ricketts OMA, Murphy KV, Anderson MG, Trowbridge DA, Al-Abduladheem Y, Phillips AM, Beausoleil AM, Stanley AJ, Becker TJ, Silver AC. Prevalence and antibiotic resistance of associated with a college-aged cohort: life-style factors that contribute to nasal carriage. Front Cell Infect Microbiol 13:1195758.
    doi: 10.3389/fcimb.2023.1195758pmc: PMC10333693pubmed: 37441241google scholar: lookup
  49. Liu G, Thomsen LE, Olsen JE. Antimicrobial-induced horizontal transfer of antimicrobial resistance genes in bacteria: a mini-review. J Antimicrob Chemother 77:556–567.
    doi: 10.1093/jac/dkab450pubmed: 34894259google scholar: lookup
  50. Martins A, Cunha Mde L. Methicillin resistance in and coagulase-negative staphylococci: epidemiological and molecular aspects. Microbiol Immunol 51:787–795.
  51. EFSA Panel on Biological Hazards (BIOHAZ), Koutsoumanis K, Allende A, Alvarez-Ordóñez A, Bolton D, Bover-Cid S, Chemaly M, Davies R, De Cesare A, Herman L, Hilbert F, Lindqvist R, Nauta M, Ru G, Simmons M, Skandamis P, Suffredini E, Andersson DI, Bampidis V, Bengtsson-Palme J, Bouchard D, Ferran A, Kouba M, López Puente S, López-Alonso M, Nielsen SS, Pechová A, Petkova M, Girault S, Broglia A, Guerra B, Innocenti ML, Liébana E, López-Gálvez G, Manini P, Stella P, Peixe L. Maximum levels of cross-contamination for 24 antimicrobial active substances in non-target feed Part 13: Diaminopyrimidines: trimethoprim. EFSA J 19:e06865.
    pmc: PMC8546793pubmed: 34729093
  52. EFSA Panel on Biological Hazards (BIOHAZ), Koutsoumanis K, Allende A, Alvarez-Ordóñez A, Bolton D, Bover-Cid S, Chemaly M, Davies R, De Cesare A, Herman L, Hilbert F, Lindqvist R, Nauta M, Ru G, Simmons M, Skandamis P, Suffredini E, Andersson DI, Bampidis V, Bengtsson-Palme J, Bouchard D, Ferran A, Kouba M, López Puente S, López-Alonso M, Nielsen SS, Pechová A, Petkova M, Girault S, Broglia A, Guerra B, Innocenti ML, Liébana E, López-Gálvez G, Manini P, Stella P, Peixe L. Maximum levels of cross-contamination for 24 antimicrobial active substances in non-target feed. Part 4: beta-lactams: Amoxicillin and penicillin V. EFSA J 19:e06855.
  53. Avolio R, Pederiva S, Morello S, Crescio MI, Ru G, Grifoni F, Abete MC, Marchis D. Official controls on carry-over of antibiotics in feed: a useful tool to contain the development of antibiotic resistance. Anim Husb Dairy Vet Sci 5:1–3.
    doi: 10.15761/AHDVS.1000185google scholar: lookup
  54. European Medicines Agency ESoVAC. Sales of veterinary antimicrobial agents in 31 European countries in 2022. .

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    doi: 10.1038/s41598-025-13369-6pubmed: 40750650google scholar: lookup
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