Implementation and evaluation of an antimicrobial stewardship programme in companion animal clinics: A stepped-wedge design intervention study

Autoři: Nonke E. M. Hopman aff001;  Lützen Portengen aff002;  Marlies E. J. L. Hulscher aff003;  Dick J. J. Heederik aff002;  T. J. M. Verheij aff004;  Jaap A. Wagenaar aff001;  Jan M. Prins aff006;  Tjerk Bosje aff007;  Louska Schipper aff002;  Ingeborg M. van Geijlswijk aff002;  Els M. Broens aff001
Působiště autorů: Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, the Netherlands aff001;  Institute for Risk Assessment Sciences, Utrecht University, Utrecht, the Netherlands aff002;  Scientific Center for Quality of Healthcare (IQ healthcare), Radboud Institute for Health Sciences, Radboud University Medical Center, Nijmegen, the Netherlands aff003;  Julius Center for Health Sciences and Primary care, University Medical Center, Utrecht, the Netherlands aff004;  Wageningen Bioveterinary Research, Lelystad, the Netherlands aff005;  Department of Internal Medicine, Amsterdam University Medical Center, University of Amsterdam, Amsterdam, the Netherlands aff006;  Medical Center for Animals, Amsterdam, the Netherlands aff007;  Pharmacy Department, Faculty of Veterinary Medicine, Utrecht University, Utrecht, the Netherlands aff008
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0225124



To curb increasing resistance rates, responsible antimicrobial use (AMU) is needed, both in human and veterinary medicine. In human healthcare, antimicrobial stewardship programmes (ASPs) have been implemented worldwide to improve appropriate AMU. No ASPs have been developed for and implemented in companion animal clinics yet.


The objective of the present study was to implement and evaluate the effectiveness of an ASP in 44 Dutch companion animal clinics. The objectives of the ASP were to increase awareness on AMU, to decrease total AMU whenever possible and to shift AMU towards 1st choice antimicrobials, according to Dutch guidelines on veterinary AMU.


The study was designed as a prospective, stepped-wedge, intervention study, which was performed from March 2016 until March 2018. The multifaceted intervention was developed using previous qualitative and quantitative research on current prescribing behaviour in Dutch companion animal clinics. The number of Defined Daily Doses for Animal (DDDAs) per clinic (total, 1st, 2nd and 3rd choice AMU) was used to quantify systemic AMU. Monthly AMU data were described using a mixed effect time series model with auto-regression. The effect of the ASP was modelled using a step function and a change in the (linear) time trend.


A statistically significant decrease of 15% (7%-22%) in total AMU, 15% (5%-24%) in 1st choice AMU and 26% (17%-34%) in 2nd choice AMU was attributed to participation in the ASP, on top of the already ongoing time trends. Use of 3rd choice AMs did not significantly decrease by participation in the ASP. The change in total AMU became more prominent over time, with a 16% (4%-26%) decrease in (linear) time trend per year.


This study shows that, although AMU in Dutch companion animal clinics was already decreasing and changing, AMU could be further optimised by participation in an antimicrobial stewardship programme.

Klíčová slova:

Antimicrobial resistance – Antimicrobials – Behavior – Decision making – Pets and companion animals – Veterinarians – Veterinary medicine – Small animal care


1. World Health Organisation (WHO). Global action plan on antimicrobial resistance; 2015. Last accessed: 1 July 2019.

2. Collignon PC, Conly JM, Andremont A, McEwen SA, Aidara-Kane A, World Health Organization Advisory Group, Bogota Meeting on Integrated Surveillance of Antimicrobial Resistance (WHO-AGISAR), et al. World Health Organisation Ranking of Antimicrobials According to Their Importance in Human Medicine: A Critical Step for Developing Risk Management Strategies to Control Antimicrobial Resistance From Food Animal Production. Clin Infect Dis. 2016;63: 1087–1093. doi: 10.1093/cid/ciw475 27439526

3. AVMA Task Force for Antimicrobial Stewardship in Companion Animal Practice. Antimicrobial stewardship in companion animal practice. J Am Vet Med Assoc. 2015;246: 287–288. doi: 10.2460/javma.246.3.287 25587725

4. Schuts EC, Hulscher MEJL, Mouton JW, Verduin CM, Stuart JWTC, Overdiek HWPM, et al. Current evidence on hospital antimicrobial stewardship objectives: a systematic review and meta-analysis. The Lancet Infectious Diseases. 2016;16: 847–856. doi: 10.1016/S1473-3099(16)00065-7 26947617

5. Dyar OJ, Huttner B, Schouten J, Pulcini C, ESGAP (ESCMID Study Group for Antimicrobial stewardship). What is antimicrobial stewardship? Clin Microbiol Infect. 2017;23: 793–798. doi: 10.1016/j.cmi.2017.08.026 28882725

6. Sikkens JJ, van Agtmael MA, Peters EJG, Lettinga KD, van der Kuip M, Vandenbroucke-Grauls CMJE, et al. Behavioral Approach to Appropriate Antimicrobial Prescribing in Hospitals: The Dutch Unique Method for Antimicrobial Stewardship (DUMAS) Participatory Intervention Study. JAMA Intern Med. 2017;177: 1130–1138. doi: 10.1001/jamainternmed.2017.0946 28459929

7. Kallen MC, Ten Oever J, Prins JM, Kullberg BJ, Schouten JA, Hulscher MEJL. A survey on antimicrobial stewardship prerequisites, objectives and improvement strategies: systematic development and nationwide assessment in Dutch acute care hospitals. J Antimicrob Chemother. 2018;73: 3496–3504. doi: 10.1093/jac/dky367 30252063

8. Guardabassi L, Prescott JF. Antimicrobial stewardship in small animal veterinary practice: from theory to practice. Vet Clin North Am Small Anim Pract. 2015;45: 361–76, vii. doi: 10.1016/j.cvsm.2014.11.005 25721619

9. NethMap/MARAN. NethMap: Consumption of antimicrobial agents and antimicrobial resistance among medically important bacteria in the Netherlands/MARAN: Monitoring of antimicrobial resistance and antibiotic usage in animals in the Netherlands in 2017. 2018.

10. Speksnijder DC, Mevius DJ, Bruschke CJ, Wagenaar JA. Reduction of veterinary antimicrobial use in the Netherlands. The Dutch success model. Zoonoses Public Health. 2015;62 Suppl 1: 79–87. doi: 10.1111/zph.12167 25421382

11. Dorado-Garcia A, Mevius DJ, Jacobs JJ, Van Geijlswijk IM, Mouton JW, Wagenaar JA, et al. Quantitative assessment of antimicrobial resistance in livestock during the course of a nationwide antimicrobial use reduction in the Netherlands. J Antimicrob Chemother. 2016;71: 3607–3619. dkw308. doi: 10.1093/jac/dkw308 27585970

12. Hesp A, Veldman K, van der Goot J, Mevius D, van Schaik G. Monitoring antimicrobial resistance trends in commensal Escherichia coli from livestock, the Netherlands, 1998 to 2016. Euro Surveill. 2019;24: doi: 10.2807/1560-7917.ES.2019.24.25.1800438 31241037

13. Staatscourant. Regeling van de Staatssecretaris van Economische Zaken van 14 januari 2013, nr. WJZ / 13002270, houdende wijziging van de Regeling diergeneesmiddelen in verband met het uitvoeren van een gevoeligheidsbepaling bij toepassing of aflevering van bepaalde diergeneesmiddelen (Regulation of the State Secretary of Economic Affairs, 4 January 2013, nr WJZ / 13002270, considering amendement of the Regulation on veterinary medicines, with reference to performance of sensitivity testing when applying or delivering certain veterinary medicines). 2013. Last accessed: 26 August 2019.

14. WHO. Critically important antimicrobials for human medicine. 2019; 6th revision. Last accessed: 1 July 2019.

15. Van Geijlswijk I, Alsters S, Schipper L. Prescription of antimicrobial agents in companion animal practices. Tijdschr Diergeneeskd. 2013;138: 26–29.

16. Hopman NEM, van Dijk MAM, Broens EM, Wagenaar JA, Heederik DJJ, van Geijlswijk IM. Quantifying Antimicrobial Use in Dutch Companion Animals. Front Vet Sci. 2019;6: 158. doi: 10.3389/fvets.2019.00158 31192236

17. Hulscher ME, Grol RP, van der Meer JW. Antibiotic prescribing in hospitals: a social and behavioural scientific approach. The Lancet infectious diseases. 2010;10: 167–75. doi: 10.1016/S1473-3099(10)70027-X 20185095

18. Hulscher ME, van der Meer JW, Grol RP. Antibiotic use: how to improve it? Int J Med Microbiol. 2010;300: 351–356. doi: 10.1016/j.ijmm.2010.04.003 20434950

19. Hopman NEM, Hulscher MEJL, Graveland H, Speksnijder DC, Wagenaar JA, Broens EM. Factors influencing antimicrobial prescribing by Dutch companion animal veterinarians: A qualitative study. Prev Vet Med. 2018;158: 106–113. doi: 10.1016/j.prevetmed.2018.07.013 30220383

20. Lam TJGM, Jansen J, Wessels RJ. The RESET Mindset Model applied on decreasing antibiotic usage in dairy cattle in the Netherlands. Ir Vet J. 2017;70: 5-017-0085-x. eCollection 2017. doi: 10.1186/s13620-017-0085-x 28250915

21. Wessels RJ, Lam TJGM, Jansen J. Communication in Practice. The vet's manual on clienthusiasm: CIP: ISBN 978-90-822321-0-3; 2014.

22. SWAB. A-teams (Antibiotic Team): Last accessed: 1 July 2019.

23. SWAB. Stichting Werkgroep Antibioticabeleid (Dutch Working Party on Antibiotic Policy), Last accessed: 1 July 2019.

24. WVAB (Dutch Working Party on Veterinary Antibiotic Policy). Formularium: Formulary companion animals: dog, cat and rabbit. 2018. Last accessed: 1 July 2019.

25. KNMvD (Royal Dutch Veterinary Association). Richtijnen (guidelines): Last accessed: 1 July 2019.

26. WVAB (Dutch Working Party on Veterinary Antibiotic Policy). WVAB-richtlijn classificatie van veterinaire antimicrobiële middelen: Last accessed 1 July 2019.

27. European Medicines Agency (EMA). Principles on assignment of defined daily dose for animals (DDDvet) and defined course dose for animals (DCDvet). 2015;EMA/710019/2014.

28. EMA. Defined daily doses for animals (DDDvet) and defined course doses for animals (DCDvet). European Surveillance of Veterinary Antimicrobial Consumption (ESVAC). 2016;EMA/224954/2016.

29. Dodds Ashley ES, Kaye KS, DePestel DD, Hermsen ED. Antimicrobial stewardship: philosophy versus practice. Clin Infect Dis. 2014;59 Suppl 3: S112–21. doi: 10.1093/cid/ciu546 25261538

30. Schouten JA, Berrevoets MAH, Hulscher ME. Quality Indicators to Measure Appropriate Antibiotic Use: Some Thoughts on the Black Box. Clin Infect Dis. 2017;64: 1295. doi: 10.1093/cid/cix172 28329185

31. Spivak ES, Cosgrove SE, Srinivasan A. Measuring Appropriate Antimicrobial Use: Attempts at Opening the Black Box. Clin Infect Dis. 2016;63: 1639–1644. ciw658. doi: 10.1093/cid/ciw658 27682070

32. Van den Bosch CM, Geerlings SE, Natsch S, Prins JM, Hulscher ME. Quality indicators to measure appropriate antibiotic use in hospitalized adults. Clin Infect Dis. 2015;60: 281–291. doi: 10.1093/cid/ciu747 25266285

33. Kallen MC, Roos-Blom MJ, Dongelmans DA, Schouten JA, Gude WT, de Jonge E, et al. Development of actionable quality indicators and an action implementation toolbox for appropriate antibiotic use at intensive care units: A modified-RAND Delphi study. PLoS One. 2018;13: e0207991. doi: 10.1371/journal.pone.0207991 30496227

34. McCarney R, Warner J, Iliffe S, van Haselen R, Griffin M, Fisher P. The Hawthorne Effect: a randomised, controlled trial. BMC Med Res Methodol. 2007;7: 30-2288-7-30. 1471-2288-7-30.

35. Ajzen I. The theory of planned behavior. Organizational Behavior and Human Decision Processes. 1991;50: 179–211.

36. King C, Smith M, Currie K, Dickson A, Smith F, Davis M, et al. Exploring the behavioural drivers of veterinary surgeon antibiotic prescribing: a qualitative study of companion animal veterinary surgeons in the UK. BMC Vet Res. 2018;14: 332-018-1646-2. doi: 10.1186/s12917-018-1646-2 30404649

37. Smith M, King C, Davis M, Dickson A, Park J, Smith F, et al. Pet owner and vet interactions: exploring the drivers of AMR. Antimicrob Resist Infect Control. 2018;7: 46-018-0341-1. eCollection 2018. doi: 10.1186/s13756-018-0341-1 29619213

38. Mateus AL, Brodbelt DC, Barber N, Stark KD. Qualitative study of factors associated with antimicrobial usage in seven small animal veterinary practices in the UK. Prev Vet Med. 2014;117: 68–78. doi: 10.1016/j.prevetmed.2014.05.007 25091861

39. Hulscher M, Laurant M, Grol R. Process evaluation of implementation strategies. In: Grol R, Wensing M, Eccles M, Davis D, editors. Improving patient care: the implementation of change in health care. Chichester, West Sussex: Wiley-Blackwell/BMJ Books; 2013. pp. 333–349.

Článek vyšel v časopise


2019 Číslo 11