Original Scientific Article
Understanding antimicrobial prescription practices: Insights from small animal veterinarians in North Macedonia
Ivana Shikoska * ,
Aleksandar Cvetkovikj ,
Martin Nikolovski ,
Iskra Cvetkovikj

Mac Vet Rev 2024; 47 (2): 103 - 114

10.2478/macvetrev-2024-0020

Received: 28 May 2024

Received in revised form: 20 June 2024

Accepted: 02 July 2024

Available Online First: 13 July 2024

Published on: 15 October 2024

Correspondence: Ivana Shikoska, ivana@fvm.ukim.edu.mk
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Abstract

Antimicrobial resistance (AMR) is an increasing global concern in small animal veterinary practices. The overuse and misuse of antimicrobials in companion animals can contribute to the spread of AMR between animals and humans. This study aimed to assess small animal veterinarians’ knowledge, attitudes, and behaviors towards antimicrobial use (AMU) and AMR in North Macedonia. A web-based questionnaire was developed, including questions addressing demographics, owner influence on antibiotic prescription and prescribing practices. The response rate of the small animal veterinarians was 47.50% (57/120), with most of them (84.20%) having 1-15 years of work experience. Pearson’s chi-square test of independence was used for contingency tables that met the chi-square assumption, and Fisher’s exact test was conducted for contingency tables that did not. Most veterinarians responded that they had perceived pressure and direct demands from pet owners to prescribe antimicrobials (35.09% frequently, 45.61% occasionally). In the survey, 50.77% of the veterinarians reported frequently administering antibiotics without conducting bacteriological or antimicrobial susceptibility testing. They typically resorted to these tests in cases with recurrent infections, such as skin infections (19.63%), or when empirical therapy is ineffective (14.72%). Based on the findings, it can be concluded that veterinarians play a crucial role in tackling the AMR in North Macedonia. The lack of stewardship programs or guidelines for responsible antimicrobial use in companion animals is a critical issue that requires urgent attention, emphasizing the vital role of veterinarians in combating AMR.

Keywords: stewardship, companion animals, guidelines, survey, awareness


References

1. Marco-Fuertes, A., Marin, C., Lorenzo-Rebenaque, L., Vega, S., Montoro-Dasi, L. (2022). Antimicrobial resistance in companion cnimals: a new challenge for the One Health approach in the European Union. Vet Sci. 9(5): 208. https://doi.org/10.3390/vetsci9050208 PMid:35622736 PMCid:PMC9146952
2. World Health Organization (2021). Global antimicrobial resistance and use surveillance system (GLASS) report: 2021.
3. Joosten, P., Ceccarelli, D., Odent, E., Sarrazin, S., Graveland, H., Van Gompel, L., Battisti, A., et al. (2020). Antimicrobial usage and resistance in companion animals: A cross-sectional study in three european countries. Antibiotics 9(2): 87. https://doi.org/10.3390/antibiotics9020087 PMid:32079072 PMCid:PMC7175148
4. Galarce, N., Arriagada, G., Sánchez, F., Venegas, V., Cornejo, J., Lapierre, L. (2021). Antimicrobial use in companion animals: assessing veterinarians’ prescription patterns through the first national survey in Chile. Animals (Basel). 11(2): 348. https://doi.org/10.3390/ani11020348 PMid:33573203 PMCid:PMC7912091
5. Jin, M., Osman, M., Green, B.A., Yang, Y., Ahuja, A., Lu, Z., Cazer, C.L. (2023). Evidence for the transmission of antimicrobial resistant bacteria between humans and companion animals: a scoping review. One Health 17, 100593. https://doi.org/10.1016/j.onehlt.2023.100593 PMid:37448771 PMCid:PMC10336692
6. Guardabassi, L., Prescott, J.F. (2015). Antimicrobial stewardship in small animal veterinary practice: from theory to practice. Vet Clin North Am Small Anim Pract. 45(2): 361-376. https://doi.org/10.1016/j.cvsm.2014.11.005 PMid:25721619
7. Allerton, F., Prior, C., Bagcigil, A.F., Broens, E., Callens, B., Damborg, P., Dewulf, J., et al. (2021). Overview and evaluation of existing guidelines for rational antimicrobial use in small-animal veterinary practice in europe. Antibiotics 10(4): 409. https://doi.org/10.3390/antibiotics10040409 PMid:33918617 PMCid:PMC8069046
8. Nielsen, S.S., Bicout, D.J., Calistri, P., Canali, E., Drewe, J.A., Garin-Bastuji, B., Gonzales Rojas, J.L., et al. (2021). Assessment of animal diseases caused by bacteria resistant to antimicrobials: dogs and cats. EFSA J. 19(6): e06680. https://doi.org/10.2903/j.efsa.2021.6680 PMid:34194578 PMCid:PMC8237238
9. Lhermie, G., La Ragione, R.M., Weese, J.S., Olsen, J.E., Christensen, J.P., Guardabassi, L. (2020). Indications for the use of highest priority critically important antimicrobials in the veterinary sector. J Antimicrob Chemother. 75(7): 1671-1680. https://doi.org/10.1093/jac/dkaa104 PMid:32240295
10. Pomba, C., Rantala, M., Greko, C., Baptiste, K.E., Catry, B., van Duijkeren, E., Mateus, A., et al. (2017). Public health risk of antimicrobial resistance transfer from companion animals. J Antimicrob Chemother. 72(4): 957-968. https://doi.org/10.1093/jac/dkw481 PMid:27999066
11. Tomanic, D., Stojanovic, D., Belić, B., Davidov, I., Novakov, N., Radinovic, M., Kladar, N., Kovacevic, Z. (2021). Off label use of human approved drugs in treatment of dogs in the Republic of Serbia. Pol J Vet Sci. 24(3): 399-407. https://doi.org/10.24425/pjvs.2021.138731 PMid:34730304
12. European Medicines Agency (EMA). (2017). Sales of veterinary antimicrobial agents in 30 European countries in 2015. Trends from 2010 to 2015. Seventh ESVAC Report. Oj L 135: 1-109.
13. Duarte, A.S.R., Høg, B.B., Korsgaard, H., Attauabi, M., Boel, J., Dalby, T., Hammerum, A.M., et al. (2021). DANMAP 2020 - Use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark. Statens Serum Institut og Technical University of Denmark. DANMAP.
14. EMA/CVMP/CHMP. (2019). Categorisation of antibiotics in the European Union. Eur Med Agence. 31, 1-73.
15. Frey, E., Costin, M., Granick, J., Kornya, M., Weese, J.S. (2022). 2022 AAFP/AAHA antimicrobial stewardship guidelines. J Am Anim Hosp Assoc. 58(4): 1-5. https://doi.org/10.5326/1547-3317-58.4.1 PMid:35793483
16. Mader, R., Muñoz Madero, C., Aasmäe, B., Bourély, C., Broens, E.M., Busani, L., et al. (2022). Review and analysis of national monitoring systems for antimicrobial resistance in animal bacterial pathogens in Europe: A basis for the development of the European antimicrobial resistance surveillance network in veterinary medicine (EARS-Vet). Front Microbiol. 13, 838490. https://doi.org/10.3389/fmicb.2022.838490 PMid:35464909 PMCid:PMC9023068
17. Cvetkovikj, I., Shikoska, I., Ratkova Manovska, M., Prodanov, M., Rashikj, L., Popova, Z., Djadjovski, I., Cvetkovikj, A. (2022). Antimicrobial resistance in Staphylococci isolated from dogs in the Republic of North Macedonia. Days of Vet Med. September, 22-25, (p. 48), Ohrid, North Macedonia.
18. Van Cleven, A., Sarrazin, S., de Rooster, H., Paepe, D., Van der Meeren, S., Dewulf, J. (2018). Antimicrobial prescribing behaviour in dogs and cats by Belgian veterinarians. Vet Rec. 182(11): 324. https://doi.org/10.1136/vr.104316 PMid:29196488
19. Chipangura, J.K., Eagar, H., Kgoete, M., Abernethy, D., Naidoo, V. (2017). An investigation of antimicrobial usage patterns by small animal veterinarians in South Africa. Prev Vet Med. 136, 29-38. https://doi.org/10.1016/j.prevetmed.2016.11.017 PMid:28010905
20. Hopman, N.E.M., Mughini-Gras, L., Speksnijder, D.C., Wagenaar, J.A., van Geijlswijk, I. M., Broens, E.M. (2019). Attitudes and perceptions of Dutch companion animal veterinarians towards antimicrobial use and antimicrobial resistance. Prev Vet Med. 170, 104717. https://doi.org/10.1016/j.prevetmed.2019.104717 PMid:31421495
21. De Briyne, N., Atkinson, J., Pokludová, L., Borriello, S.P., Price, S. (2013). Factors influencing antibiotic prescribing habits and use of sensitivity testing amongst veterinarians in Europe. Vet Rec. 173(19): 475. https://doi.org/10.1136/vr.101454 PMid:24068699 PMCid:PMC3841786
22. Hughes, L.A., Williams, N., Clegg, P., Callaby, R., Nuttall, T., Coyne, K., Pinchbeck, G., Dawson, S. (2012). Cross-sectional survey of antimicrobial prescribing patterns in UK small animal veterinary practice. Prev Vet Med. 104(3-4): 309-316. https://doi.org/10.1016/j.prevetmed.2011.12.003 PMid:22225772
23. Vandeweerd, J.M., Vandeweerd, S., Gustin, C., Keesemaecker, G., Cambier, C., Clegg, P., Saegerman, C., et al. (2012). Understanding veterinary practitioners’ decision-making process: Implications for veterinary medical education. J Vet Med Educ. 39(2): 142-151. https://doi.org/10.3138/jvme.0911.098R1 PMid:22718001
24. Frey, E., Kedrowicz, A., Hedgpeth, M.W. (2024). Decision making on antimicrobial use: cat and dog owners’ knowledge and preferences for veterinary communication. Vet Rec. 194(5): e3411. https://doi.org/10.1002/vetr.3411 PMid:37691448
25. Scarborough, R., Hardefeldt, L., Browning, G., Bailey, K. (2021). Pet owners and antibiotics: knowledge, opinions, expectations, and communication preferences. Antibiotics (Basel). 10(11): 1326. https://doi.org/10.3390/antibiotics10111326 PMid:34827264 PMCid:PMC8615269
26. Jessen, L.R., Damborg, P., Spohr, A. (2019). Antibiotic use guidelines for companion animal practice, 2nd ed. Danish Small Anim Vet Assoc. SvHKS.
27. Timofte, D., Broens, E.M., Guardabassi, L., Pomba, C., Allerton, F., Ikonomopoulos, J., Overesch, G., Damborg, P. (2021). Driving laboratory standardization of bacterial culture and antimicrobial susceptibility testing in veterinary clinical microbiology in Europe and beyond. J Clin Microbiol. 59(6): e02572-20. https://doi.org/10.1128/JCM.02572-20 PMid:33361339 PMCid:PMC8315970
28. Alcantara, G.L.C., Pinello, K.C., Severo, M., Niza-Ribeiro, J. (2021). Antimicrobial resistance in companion animals - Veterinarians’ attitudes and prescription drivers in Portugal. Comp Immunol Microbiol Infect Dis. 76, 101640. https://doi.org/10.1016/j.cimid.2021.101640 PMid:33684640
29. Weese, J.S., Blondeau, J., Boothe, D., Guardabassi, L.G., Gumley, N., Papich, M., Jessen, L.R., et al. (2019). International society for companion animal infectious diseases (ISCAID) guidelines for the diagnosis and management of bacterial urinary tract infections in dogs and cats. Vet J. 247, 8-25. https://doi.org/10.1016/j.tvjl.2019.02.008 PMid:30971357
30. Carmo, L.P., Nielsen, L.R., Alban, L., da Costa, P.M., Schüpbach-Regula, G., Magouras, I. (2018). Veterinary expert opinion on potential drivers and opportunities for changing antimicrobial usage practices in livestock in Denmark, Portugal, and Switzerland. Front Vet Sci. 5, 29. https://doi.org/10.3389/fvets.2018.00029 PMid:29546044 PMCid:PMC5837977
31. Chirollo, C., Nocera, F.P., Piantedosi, D., Fatone, G., Della Valle, G., De Martino, L., Cortese, L. (2021). Data on before and after the traceability system of veterinary antimicrobial prescriptions in small animals at the university veterinary teaching hospital of Naples. Animals 11(3): 913. https://doi.org/10.3390/ani11030913 PMid:33806745 PMCid:PMC8005210
32. Escher, M., Vanni, M., Intorre, L., Caprioli, A., Tognetti, R., Scavia, G. (2011). Use of antimicrobials in companion animal practice: A retrospective study in a veterinary teaching hospital in Italy. J Antimicrob Chemother. 66(4): 920-927. https://doi.org/10.1093/jac/dkq543 PMid:21393194
33. EMA. (2013). Reflection paper on the risk of antimicrobial resistance transfer from companion animals Summary. Ema/Cvmp/Awp/401740/2013. 44, 1-27.
34. Zhuo, A., Labbate, M., Norris, J.M., Gilbert, G.L., Ward, M.P., Bajorek, B.V., Degeling, C., et al. (2018). Opportunities and challenges to improving antibiotic prescribing practices through a One Health approach: results of a comparative survey of doctors, dentists and veterinarians in Australia. BMJ Open 8(3): e020439. https://doi.org/10.1136/bmjopen-2017-020439 PMid:29602857 PMCid:PMC5884343
35. Holloway, S., Trott, D., Shipstone, M., Barrs, V., Malik, R., Burrows, M., Norris, J., et al. (2022). AIDAP Antibiotic prescribing guidelines-companion animals. Aust Infect Dis Advis Painel. 2, 205.
36. Williams, J. (2018). Antimicrobial prophylaxis: the why and how of antimicrobial prophylaxis. BSAVA Companion 11, 4-7. https://doi.org/10.22233/20412495.1118.4 
37. Attauabi, M., Høg, B. B., Müller-Pebody, B. (2021). Summary Danmap 2020: use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark. Statens Serum Institut og Technical University of Denmark. DANMAP
38. Hillier, A., Lloyd, D.H., Weese, J.S., Blondeau, J.M., Boothe, D., Breitschwerdt, E., Guardabassi, L., et al. (2014). Guidelines for the diagnosis and antimicrobial therapy of canine superficial bacterial folliculitis (antimicrobial guidelines working group of the international society for companion animal infectious diseases). Vet Dermatol. 25(3): 163-e43.
39. Lappin, M.R., Blondeau, J., Boothe, D., Breitschwerdt, E.B., Guardabassi, L., Lloyd, D.H., Papich, M.G., et al. (2017). Antimicrobial use guidelines for treatment of respiratory tract disease in dogs and cats: antimicrobial guidelines working group of the international society for companion animal infectious diseases. J Vet Intern Med. 31(2): 279-294. https://doi.org/10.1111/jvim.14627 PMid:28185306 PMCid:PMC5354050
40. Hur, B.A., Hardefeldt, L.Y., Verspoor, K.M., Baldwin, T., Gilkerson, J.R. (2020). Describing the antimicrobial usage patterns of companion animal veterinary practices; free text analysis of more than 4.4 million consultation records. PLoS One 15(3): e0230049. https://doi.org/10.1371/journal.pone.0230049 PMid:32168354 PMCid:PMC7069610
41. Burke, S., Black, V., Sánchez-Vizcaíno, F., Radford, A., Hibbert, A., Tasker, S. (2017). Use of cefovecin in a UK population of cats attending first-opinion practices as recorded in electronic health records. J Feline Med Surg. 19(6): 687-692. https://doi.org/10.1177/1098612X16656706 PMid:27507842 PMCid:PMC11128814
42. Food and Veterinary Agency of Republic of North Macedonia. (2024). List of veterinary medicinal products that have a marketing authorization, i.e. for which the approval has been cancelled, i.e. for which a change has been made during the validity of the authorization. Official Gazette of Republic of North Macedonia No.111/2024 [in Macedonian].


Copyright

© 2024 Shikoska I. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Conflict of Interest Statement

The authors declared that they have no potential lict of interest with respect to the authorship and/or publication of this article.

Citation Information

Macedonian Veterinary Review. Volume 47, Issue 2, Pages 103-114, e-ISSN 1857-7415, p-ISSN 1409-7621, DOI: 10.2478/macvetrev-2024-0020