Factors influencing antimicrobial prescribing behavior of Veterinarians in large animal practice in Kerala, India

Introduction

Antimicrobial resistance (AMR) is becoming more of a problem in both human and veterinary medicine. Antibiotic use in human and veterinary medicine particularly misuse has been linked to the selection and dissemination of antibiotic resistance strains in humans and animals. Monitoring antibiotic use and antibiotic resistance levels is critical for evaluating efforts to reduce selective pressure and the selection of resistant strains in animal health. The global desire to limit antibiotic use and hence selective pressures on microbes is pushing study into the factors influencing health professional's antimicrobial prescribing behaviors (Zhuo et al. 2018) [19] . A number of factors influence veterinary prescribing behavior. Surveys of veterinary prescribing in Europe identified that antimicrobial susceptibility testing results were the primary driver of veterinarian's prescribing behavior followed by their own experience. The perceived risk of antibiotic resistance development and the ease of administering the drug were also important factors influencing veterinarian's antibiotic selection decisions (De Briyne et al. 2013) [2] . Non-clinical factors influencing veterinary prescribing include farmer's demands and expectations, the veterinarian's experience and drug cost (Gibbons et al. 2013) [5] . According to a Dutch study, veterinarians face several competing interests when prescribing antimicrobials including an obligation to alleviate animal suffering, financial reliance on clients, risk avoidance, public health concerns and personal convictions (Speksnijder et al. 2015) [15] . According to their significance for human medicine, antimicrobials have been categorized by the World Health Organization (WHO) and it is advised that some antimicrobial classes only be used in certain circumstances. A number of classes of antimicrobials that are registered for veterinary use including the third and fourth generation cephalosporins, fluoroquinolones and macrolides have been categorised as critically important antimicrobials (WHO, 2019) [18] . However, investigations carried out in Europe have shown that these antibiotics are frequently used by veterinarians to treat mastitis and respiratory conditions (De Briyne et al. 2014) [3] . Numerous strategies, recommendations and treatment guidelines on responsible use of antibiotics have been developed by a variety of national, European and international bodies (OIE, 2012) [10] . Prescribing guidelines to reduce the risk of emergence of AMR have been developed by most of the countries including India. These guidelines emphasise good stewardship of prescribing as a means to reduce the development of resistance. The aim of these strategies is to encourage veterinarians to prescribe responsibly and prudently as well as to reduce antibiotic use. For any such strategy to be effective it is necessary to understand the factors influencing antibiotic prescribing behavior of veterinarians and the association between these factors with the perception of veterinarians regarding antimicrobial use and resistance. There were lack of data on the factors influencing antibiotic prescribing behavior of veterinarians across India, specifically in Kerala. In order to fill these evidence gaps, a study was conducted among the veterinarians engaged in large animal practice of Kerala state.

Materials and Methods

The questionnaire based cross-sectional analysis for the descriptive study was planned to be conducted among veterinarians of Kerala. The survey questionnaire was developed to explore the factors influencing veterinarian's antimicrobial prescribing behavior as well as to provide insight into antimicrobial use and resistance perceptions. The factors influencing prescribing behavior was studied in two categories in the present study. The first was that variables affecting a veterinarian's choice to prescribe or administer an antibiotic to an animal or not, which was operationally defined as those factors influencing a veterinarian's decision to prescribe or administer an antibiotic to an animal or not in large animal practice. The relevant factors that were likely to influence veterinarian's decisions on whether to prescribe an antibiotic to an animal or not were chosen based on an extensive literature review, the themes emerging from focus group discussions among veterinarians in large animal practice working in the Animal Husbandry Department, Kerala and consultation with experts as well as field practitioners. A total of 15 factors, four clinical and eleven non-clinical, were identified and included in the final questionnaire. Respondents were then asked to rate each factor's potential influence on their choice to prescribe or not an antimicrobial on a three-point scale: strong influence, moderate influence and no influence. Based on the responses, the factors with the greatest influence and those with the least influence have been identified and rated and interpretations were made. The second category was that the factors influencing a veterinarian's decision to prescribe an antibiotic choice were operationally defined as those factors that influenced the veterinarian's decision to prescribe a specific antibiotic for use in large animal practice. The key factors that were likely to affect a veterinarian's decision to choose a specific antibiotic to be administered to a large animal were chosen based on a comprehensive literature review, focus group discussions and consultation with specialists as well as field veterinarians. A total of 14 criteria were identified and incorporated into the final questionnaire. Respondents were then asked to rate the influence of each factor on their choice of an antibiotic on a three-point scale: strong influence, moderate influence and no influence. Based on the responses, the most and least influential factors were identified, ranked and interpreted. The survey questionnaire containing Google forms were sent to the list of veterinarians working in the Animal Husbandry Department in all the fourteen districts of Kerala state through mail and Whatsapp messenger and were requested to complete the survey. Numerous strategies, recommendations and treatment guidelines on responsible use of antibiotics have been developed by a variety of national, European and international bodies (OIE, 2012) [10] . Prescribing guidelines to reduce the risk of emergence of AMR have been developed by most of the countries including India. These guidelines emphasise good stewardship of prescribing as a means to reduce the development of resistance. The aim of these strategies is to encourage veterinarians to prescribe responsibly and prudently as well as to reduce antibiotic use. For any such strategy to be effective it is necessary to understand the factors influencing antibiotic prescribing behavior of veterinarians and the association between these factors with the perception of veterinarians regarding antimicrobial use and resistance. There were lack of data on the factors influencing antibiotic prescribing behavior of veterinarians across India, specifically in Kerala. In order to fill these evidence gaps, a study was conducted among the veterinarians engaged in large animal practice of Kerala state.

Materials and Methods

The questionnaire based cross-sectional analysis for the descriptive study was planned to be conducted among veterinarians of Kerala. The survey questionnaire was developed to explore the factors influencing veterinarian's antimicrobial prescribing behavior as well as to provide insight into antimicrobial use and resistance perceptions. The factors influencing prescribing behavior was studied in two categories in the present study. The first was that variables affecting a veterinarian's choice to prescribe or administer an antibiotic to an animal or not, which was operationally defined as those factors influencing a veterinarian's decision to prescribe or administer an antibiotic to an animal or not in large animal practice. The relevant factors that were likely to influence veterinarian's decisions on whether to prescribe an antibiotic to an animal or not were chosen based on an extensive literature review, the themes emerging from focus group discussions among veterinarians in large animal practice working in the Animal Husbandry Department, Kerala and consultation with experts as well as field practitioners. A total of 15 factors, four clinical and eleven non-clinical, were identified and included in the final questionnaire. Respondents were then asked to rate each factor's potential influence on their choice to prescribe or not an antimicrobial on a three-point scale: strong influence, moderate influence and no influence. Based on the responses, the factors with the greatest influence and those with the least influence have been identified and rated and interpretations were made. The second category was that the factors influencing a veterinarian's decision to prescribe an antibiotic choice were operationally defined as those factors that influenced the veterinarian's decision to prescribe a specific antibiotic for use in large animal practice. The key factors that were likely to affect a veterinarian's decision to choose a specific antibiotic to be administered to a large animal were chosen based on a comprehensive literature review, focus group discussions and consultation with specialists as well as field veterinarians. A total of 14 criteria were identified and incorporated into the final questionnaire. Respondents were then asked to rate the influence of each factor on their choice of an antibiotic on a three-point scale: strong influence, moderate influence and no influence. Based on the responses, the most and least influential factors were identified, ranked and interpreted. The survey questionnaire containing Google forms were sent to the list of veterinarians working in the Animal Husbandry Department in all the fourteen districts of Kerala state through mail and Whatsapp messenger and were requested to complete the survey.

Sampling procedure

The current study's source population included veterinarians working in Animal Husbandry Department, Kerala and the study population included veterinarians who fulfilled the inclusion criteria of being field veterinarians. i.e., those veterinarians working in Veterinary Dispensaries (VD), Veterinary Hospitals (VH), Veterinary Polyclinics (VPC) and District Veterinary Centres (DVC) of the Animal Husbandry Department, Kerala. The questionnaire was sent with the request that it be completed only by veterinarians who were engaged in clinical large animal practice. The sample size was calculated using the 'Raosoft calculator' (Raosoft: http://www.raosoft.com/samplesize.html?nosurvey). The sample size of 336 was estimated based on 50% response distribution, a 5% margin of error and a 95% confidence interval. The expected response proportion of 50% was assumed based on the fact that both responses and response rates were completely unknown, since there are no previously published similar studies from Kerala. Thereby, a total of 1580 questionnaires were sent to the veterinarians selected through registered emails and/or personal contacts from Indian Veterinary Association (IVA) mailing list, 2021. The questionnaire was administrated by using the online interface of Google Forms (Google LLC, Mountain View, CA, USA) to the target population and the survey remained open from April to June 2022.

Results

Factors influencing the decision on whether to prescribe an antimicrobial or not

Results indicated that clinical factors (mean of mean scores-2.67) were more influential in affecting the decision of veterinarians to prescribe or not when compared to nonclinical factor (mean of mean scores-2.1). Among clinical factors, a decision to prescribe an antimicrobial was most often taken based on clinical signs or symptoms (2.95) and the critical nature of illness (2.88). The decision to prescribe an antimicrobial was also influenced to a lesser extent by consideration of the risk of promoting antimicrobial resistance in the animal (2.48). It was notable that the results of cultural and sensitivity tests (2.38) was the factor that had the least influence on the decision of the respondents to prescribe an antimicrobial. The non-clinical factors that influenced the respondent's decision to prescribe an antimicrobial was their prior experience in managing similar problems (2.76) which of course would have contributed to a personal confidence in their diagnosis (2.69). Demand of the farmer for immediate relief (2.26), the lack of enough time to consider another option (2.09) and the care that the respondent took to avoid a mistake in diagnosis (2.08) were the other nonclinical factors that influenced respondent decision. Other non-clinical factors that exerted lesser influence on the respondent decision to prescribe a antimicrobial included not being confident about the diagnosis (2.06), situations in which the farmer had already initiated administering an antimicrobial (2.05), longstanding acquaintance with the farmer (2.00), guideline recommendations (1.81), perception that if the condition of the animal did not improve, the respondent would be called again (1.80) and the need to ensure an impression in cases where the farmer was a new client (1.57).

Factors influencing the decision to choose a particular antimicrobial

Results indicated that the predominance of pharmacological criteria (mean of mean scores-2.65) over nonpharmacological factors (mean of mean scores-2.41) in the respondent decision making process with respect to the choice of a particular antimicrobial to prescribe. Influential pharmacological considerations in this regard included consideration of the spectrum of activity of the antimicrobial (2.88), as well as the duration of therapy (2.82) and the route as well as frequency of administration (2.75). It is worth deliberating upon the fact that factor on the withdrawal period of an antimicrobial was the least considered pharmacological factor while arriving at a decision on the antimicrobial to prescribed. Among the non-pharmacological factors that exerted greater influence on the decision of the veterinarian to choose an antibiotic were the clinical signs/disease condition (2.95) followed by previous experience of using a drug to treat a particular condition (2.82), availability of the antibiotic (2.60), cost of the antibiotic treatment protocol (2.56) and the results of culture and sensitivity test (2.40). Non-pharmacological factors of relatively lesser influence included consideration of the local resistant pattern (2.36), ease of administration (2.34), guideline recommendations (2.28) and marketing offers coming along with an antibiotic (1.46).

Discussion

Factors influencing the decision on whether to prescribe an antimicrobial or not

The results of this study pointed to the predominant role of clinical factors such as clinical signs/symptoms, critical nature of the illness and risk of promoting antimicrobial resistance in the animal in exerting the influence over veterinarian decision on whether to prescribe an antimicrobial or not. The findings are in concordance with those of Norris et al. (2019) [8] , Odoi et al. (2021) [9] , Samuels et al. (2021) [13] and Kalam et al.

(2022) [6] who reported that clinical signs and symptoms were the factors that exerted the most influence on the decision of veterinarians to prescribe an antimicrobial or not. The respondents did not rely on culture and sensitivity test results as this factor was considered to be the factor of least influence among other clinical factors. This finding is not in accordance with that of De Briyne et al. (2013) [2] , Ekakoro and Okafor (2019) [4] and Odoi et al. (2021) [9] who reported that the majority of veterinarians relied on laboratory results which deciding whether or not to prescribe an antimicrobial. The possible reason for the lesser perceived influence of sensitivity test results on veterinarian antimicrobial prescribing could be due to lack of quick and efficient laboratory facilities to conduct culture and sensitivity tests at the field level in Kerala.

It was also evident from this study that non-clinical factors such as the veterinarian's prior experience in managing similar problems and personal confidence in disease diagnosis were important non-clinical factors influencing veterinarian prescribing decision. These findings are in line with those of McDougall et al. (2016) [7] , Coyne et al. (2018) [1] and Patnaik et al. (2019) [11] who reported that a veterinarian's previous experience with the response of a therapy was a significant factor influencing prescribing decisions and in line with Servia-Dopazo et al. (2021) [14] who reported that personal confidence of the veterinarian in his/her diagnosis was the major non-clinical factor that exerted influence on the veterinarian prescription behaviour. Veterinarian decision to prescribe was influenced by a perceived demand from the farmer for immediate relief putting the veterinarian under pressure to prescribe in cases where antibiotics were not required. This findings was contrary to that reported from Australia where client expectations had only a marginal effect on veterinarian decision to prescribe (Norris et al., 2019) [8] . Item wise analysis of the statement relating to non-clinical factors influencing veterinarian prescribing decision indicated that in certain cases there was not enough time to consider another option and the veterinarian had to prescribe antimicrobial. It was also evident from this study that certain non-clinical factors viz., not being confident about the diagnosis and the perception that if the condition of the animal did not improve, the veterinarian would be called again for treatment were the least factors that influenced prescribing decision to the least extent. These findings are contrary to the findings of Gibbons et al. (2013) [5] who reported that these factors exerted a major influence on the antimicrobial prescribing decision of the majority of the cattle practitioners in Ireland. Analysis of the various factors that influenced the prescribing decision of veterinarians indicated that guideline recommendation did not have much influence on the prescribing decision of veterinarians. This finding is contrary to the findings of Spernovasilis et al. (2020) [16] who reported in a study conducted among junior doctors in Greece that the use of guidelines was the most important factor influencing antimicrobial prescribing practices. The least influence of guideline recommendations could be due to lesser importance given by studied veterinarians for guidelines or unaware / unavailability of such guideline recommendations in the Kerala.

Factors influencing the decision to choose a particular antimicrobial

While choosing the antimicrobials, among pharmacological factors, spectrum of activity of the antibiotic remained the topmost criteria which is in accordance with the previous studies where spectrum of activity was the decisive for antibiotic selection among veterinarians of New Zealand (McDougall et al. (2016) [7] . The other pharmacological criteria for choosing the antimicrobial were the duration of therapy, route and frequency of administration, possibility of antibiotic resistance development and withdrawal period which is in line with findings of Odoi et al. (2021) [9] who reported in a study among veterinarians in United States of America that the factors that influenced the decision to choose an antibiotic were the route of administration, the expenses associated with the drug and the possible untoward reactions that could occur on administration of the drug. The present study also indicated that the choice of antimicrobial to prescribe by veterinarians were influenced by several factors that were not related to the pharmacology of the drug. The non-pharmacological factors that had the most influence on the decision of veterinarians to choose an antibiotic were the clinical signs/disease condition which is in line with the findings of Kalam et al. (2022) [6] who reported that the selection of appropriate antimicrobials by veterinarians in Bangladesh was influenced to a great extent by disease type or organism. The other non-pharmacological factors were the previous experience of using the drug to treat a particular condition, the availability of the antibiotic, the cost of the antibiotic treatment protocol and the results of the culture and susceptibility test results. These findings are in line with the findings of Vijay et al. (2021) [17] who in a study among veterinarians in India reported that for majority of the veterinarians, their own personal experience with the drug was the most influential factor in deciding on the choice of an antibiotic followed by availability of antimicrobial in the market, cost of the drug and the cost of culture and sensitivity test results. Similarly in a study among cattle practitioners in Ireland, Gibbons et al. (2013) [5] reported that more than half of the veterinarians always considered the nonpharmacological factor i.e., the prior experience of using a drug to treat a particular condition when choosing an antimicrobial to prescribe. The lower use of antimicrobial culture and sensitivity test results in choosing antimicrobials was in accordance with the study on New Zealand veterinarians (McDougall et al., 2016) [7] as well as with the study among veterinarians in Bangladesh (Kalam et al. 2022) [6] and contrary with the study among veterinarians in Europe (De Briyne et al. 2013) [2] . This least influence of culture test results on choosing antimicrobials indicated the practice of less culture and sensitivity tests being done at field level among the veterinarians of Kerala. This could be due to lack of awareness among veterinarians and farmers about culture and sensitivity testing and lack of such facilities at field level in Kerala. The non-pharmacological factors of least importance were the local resistant pattern and guideline recommendations.

The marketing offers and recommendations from the pharmaceutical companies also had the least influence on the veterinarian decision to choose a particular antibiotic which is in line with findings of Vijay et al. (2021) [17] who reported in a study among veterinarians in India that recommendations of pharmaceutical companies were criteria of least importance while making a choice of an antibiotic to prescribe. This finding is in contrast to those of previous studies where it was reported that half of the veterinarians studied reported that pharmaceutical companies did influence their antimicrobial prescribing choices (Postma et al., 2016) [12] .

Conclusion

This study highlighted the multifactorial nature of the veterinarian's decision to prescribe antimicrobials and the choice of antimicrobial prescribed. While further investigation of these issues is necessary, it is important that the role played by non-clinical and non-pharmacologicalrelated factors be recognised by regulatory authorities, veterinary surgeons and their clients, and that these issues are addressed when guidelines for antimicrobial use and intervention strategies to reduce antimicrobial consumption are being formulated.

Our results suggest non-clinical factors which are associated with veterinary antibiotic prescribing (e.g., prior experience, personal confidence in their diagnosis, demand of the farmer for immediate relief and the lack of enough time to consider another option etc.) which are potentially modifiable, and could thus be the target of future interventions designed to optimize antimicrobial use in this sector and decrease the prevalence of resistant development in animals and human beings alike. This study has identified a number of common factors that influence veterinarian prescribing practices across Kerala which could help inform optimum information channels and areas for interventions and investment to maximise appropriate prescribing and minimise risk of resistance emergence.

References

1. Coyne LA, Latham SM, Dawson S, Donald IJ, Pearson RB, Smith RF, et al. Antimicrobial use practices, attitudes and responsibilities in UK farm animal veterinary surgeons. Prev Vet Med. 2018;161:115-126.
2. Briyne DN, Atkinson J, Pokludova L, Borriello SP, Price S. Factors influencing antibiotic prescribing habits and use of sensitivity testing amongst veterinarians in Europe. Vet Rec. 2013;173:475-481.
3. Briyne DN, Atkinson J, Borriello SP, Pokludova L. Antibiotics used most commonly to treat animals in Europe. Vet Rec. 2014;175:325-332.
4. Ekakoro JE, Okafor CC. Antimicrobial use practices of veterinary clinicians at a veterinary teaching hospital in the United States. Vet Anim Sci. 2019;7:1-10.
5. Gibbons JF, Boland F, Buckley JF, Butler F, Egan J, Fanning S, et al. Influences on antimicrobial prescribing behaviour of veterinary practitioners in cattle practice in Ireland. Vet Rec. 2013;172:14-19.
6. Kalam M, Rahman M, Alim M, Shano S, Afrose S, Jalal FA, et al. Knowledge, attitudes, and common practices of livestock and poultry veterinary practitioners regarding AMU and AMR in Bangladesh. Antibiotics. 2022;11:8095.
7. McDougall S, Compton CWR, Botha N. Factors influencing antimicrobial prescribing by veterinarians and usage by dairy farmers in New Zealand. N Z Vet J. 2016;65:84-92.