Antimicrobial use (AMU) in livestock production has beneficial impacts on animal health and welfare, and on household livelihoods, food security, and food safety (1, 2). However, there is increasing concern about the role of livestock production in the emergence of antimicrobial resistance (AMR) and consequent human exposure to resistant pathogens and/or antibiotic residues through the food chain, direct contact with livestock, or indirectly, via a contaminated environment (3–6). The loss of antibiotic efficacy due to AMR is a global public health challenge and a complex problem driven by many interconnected biological and socio-economic factors. Consequently, isolated interventions and non-coordinated actions may have limited impact on its management. Instead, effective mitigation of AMR risks requires dialogue and coordinated engagement between stakeholders from public and private sectors along the animal and antibiotics (ABX) value chains, implicating veterinarians, public health scientists, microbiologists, environmental scientists (ecologists), agricultural/forestry scientists, and epidemiologists (2, 7–9). Broader regulatory oversight is required, including of importation, distribution, sale, and use (7, 10). This regulatory complexity is part of a quintessential One Health (OH) approach implying the need to coordinate action across human, animal and environmental settings.

In the animal setting, veterinarians are key stakeholders in terms of diagnosis and treatment decisions for livestock. Yet, the international evidence on veterinary antimicrobial stewardship (AMS) is conflicting. Even in developed countries like Australia, small companion animal veterinarians reported prescribing broad-spectrum ABX of higher importance to human health more frequently than was the case for livestock veterinarians (11). The same study observed that the cost of bacterial culture to identify the causative agent, antimicrobial susceptibility testing (AST), and the lack of access to rapid and affordable diagnostics were barriers to appropriate ABX prescribing. A systematic review for non-clinical factors influencing veterinarians' prescribing behavior of ABX (12) indicated that fear of possible complications or losing customers if ABX were not prescribed (identified in 19 out of 34 studies), self-confidence (19/34), business factors (19/34), and complacency (16/34) are influencing veterinarians' decisions. Other influencing factors were; lack of awareness of animal owners regarding AMS (16/34) and demand for ABX (12/34), lack of appropriate regulations (10/34), cost and time for culture and AST (10/34), and inadequate farm hygiene (8/34) (12) with AMU as a “quick fix” to cover for poor hygiene and biosecurity practices (13).

There are conspicuous evidence gaps in low and middle-income countries (LMICs), where pharmaceutical regulation continues to be weak and diagnosis hampered by poor access to laboratory tests, poor training, negligible awareness, and lack of biosecurity measures (12, 14). Other factors influencing AMU are a higher burden of animal diseases such as mastitis in dairy cattle (15, 16). Identifying and understanding these barriers and drivers is important for designing strategies for rationalizing AMU in livestock production (12). A survey of Nigerian veterinarians revealed that only 21% were able to define the term “antimicrobial stewardship,” and 60% were unaware of the National Action Plan guidelines for AMR. More than half perceived prophylactic AMU as appropriate under poor farm biosecurity, and only 20% frequently conducted AST before deciding to administer ABX for treatment (17). A similar situation pertains in known global AMR hotspots, such as China and India, where livestock production is projected to grow in line with income growth and consumption preferences (18), and where there is an urgent need to evaluate the feasibility and acceptability of veterinary AMU control measures.

Accordingly, this study aimed to assess factors influencing antimicrobial prescribing behavior of a sample of veterinarians in Assam, India, where access to medicines is poorly regulated (19–21). The output of this study would inform the design of potential AMR control interventions, and to bridge the gap between prescribing guidelines and clinical usage. The research builds on evidence indicating that Indian veterinarians liberally prescribed ABX for animal cases based on the initial diagnosis, and that there is no strong relationship with farmers to ensure active involvement of stakeholders in more rational AMU (7, 9, 19, 22).

The survey results indicate a lack of awareness of the national and/or state policy/plan, despite the existence of a national action plan for AMR (NAP-AMR 2017–2021),¹ which among other aims seeks to improve “awareness and understanding of AMR through effective communication, education and training.” In Assam, the AHVD has a Professional Efficiency Development scheme to regulate veterinary practices according to the Indian Veterinary Council Act, 1984. The Council is also responsible for the development of training modules and continued training of field veterinarians. Another project, “Assistance to States for Control of Animal Diseases,” is also supporting the training needs of veterinarians, para-veterinarians as well as laboratory persons. However, the extent of AMU training and awareness in these is unclear and there is a need to improve collaboration between different organizations such as veterinary colleges and the AHVD (15, 19, 25), and for them to be aligned with the objectives of the NAP. Despite this, only 26% of the survey respondents reported having attended at least one training/awareness seminar since graduating however, suggesting that opportunities for continued professional development (CDP) are limited. Less than two thirds (64%) of participants were aware of the government ban for Colistin and the reasons for this decision in their opinions were varied. The verbatim responses (Table 4) showed a potential confusion or lack of understanding over whether it is human/animals who developed resistance to the antibiotics or the pathogens. Veterinarians might have used “animal/humans resistance” as a proxy or indicator for not responding to treatment with ABX. Core competencies among veterinarians have been found to be lacking or inefficient and it has been suggested that training and attending national and international seminars/workshops are appropriate ways to acquire competencies (26). There is a continuing education and training needs for veterinary students, working veterinarians, para-veterinarians and other stakeholders for which online and open and distance learning programmes in animal welfare need to be developed (27). In India and other LMICs with limited resources, private sector and non-governmental organizations (NGOs) could play an important role to support continuous education and training of veterinarians. “Vet Sustain” is an example of a UK-based social enterprise working to enable and inspire veterinary professionals to continually improve the health and wellbeing of animals, people and the environment. It is also supporting veterinary professionals to drive change toward a more sustainable future and to become leading forces for sustainability.² Guidelines, provided by NGOs such as the British Veterinary Association, the British Small Animal Veterinary Association, and the British Cattle Veterinary Associations, have been considered a key step for appropriate AMU (28, 29). Such activities provide opportunities for keeping stakeholders up to date with the latest government advice and regulation, better ways to support training and CPD in India using a similar model could be investigated.

As found in previous studies (11, 30–32), low levels of laboratory diagnosis for animal diseases continues to be a factor in speculative AMU, and arises due to a lack of onsite diagnostic facilities. In this study, 58% of veterinary clinics have no diagnostic laboratories and 70% of veterinarians never use AST before AMU. The AHVD has a scheme for assisting states to set up infrastructure for new veterinary hospitals and dispensaries and to strengthen/equip the existing ones.³ However, coverage and access are still not universal for all states. In 2015–16, the contribution by the central government was increased from 60 to 90% for 11 states (8 North-East and 3 Himalayan states) which may improve the veterinary services in Assam. There are disease diagnostic laboratories only at the state and district level. A field veterinarian who wants to conduct basic tests has to send samples to these laboratories, which is time consuming. Hence, equipping the veterinary clinics and dispensaries with basic equipment including microscopes, on-farm diagnostic kits and other tools for screening some of the diseases will help field veterinarians to diagnose quickly and to prescribe appropriate ABX based on confirmed infection instead of depending on clinical signs alone. A survey of animal health professionals in 20 sub-Saharan African countries concluded that the development of on-farm diagnostics and management tools for animal diseases are essential to considerably improve AMU (32).

Respondents in this study reported that farmers often call and/or consult them only after trying other options. This can lead to the progression of health problems that are less likely to respond to medications and more likely to develop resistance. Non-responsive cases also drives a lack of confidence between farmers and veterinarians (15). This behavior might be due to the shortage of veterinarians in Assam; there are around 1,000 veterinarians but the required number is estimated at 2,529 (one veterinarian per 5,000 cattle head) according to the National Commission of Agriculture.⁴ Ethnographic work with farmers in Assam (conducted under this project but yet to be published) identified lack of access to veterinarians and veterinary services as a major barrier to proper management of animal health; farmers in peri-urban villages such as Garchuk and Nagaom around Guwahati reported that veterinarians were reluctant to make in-person diagnoses due the time taken to travel to and from remote farms. This suggests that access—to veterinarians in general and, when veterinarians are available to their access to laboratories—is a serious issue that needs to be further addressed. A shortage of veterinarians results in over prescription and/or irrational AMU by untrained caregivers or informal prescribers, known as “private doctors” among Indian dairy farmers (19). In India, like many other LMICs, veterinarians are not the only prescribers of ABX for animal use. Para-veterinarians and other untrained community members might be more accessible, charging less for consultations compared to veterinarians. Over-the-counter access of ABX, without prescriptions, and direct marketing of drugs to farmers are also common practices in India (15).

In Assam, the most frequently observed diseases in cattle, goats, and poultry are potentially associated with the lack of hygiene, biosecurity, and non-adherence to the vaccination schedule for endemic diseases. A high proportion of veterinarians reported AMU for cattle with respiratory health problems, mostly caused by viral infections, followed by mastitis. This was also reported in a previous study that identified AMU mostly for mastitis cases (15). This could be prevented by improving environment and animal hygiene, prober nutrition and dry cow therapy (33). Veterinarians are prescribing ABX listed as highest priority, critically important antimicrobials (HPCIA) by the World Health Organization (WHO). This confirms the results of previous studies, in India and other LMICs, in which veterinarians used Quinolones and 3rd generation Cephalosporins for animal treatment (9, 10). In India, 76.8 and 47.8% of veterinarians were found to prescribe Quinolones and 3rd generation Cephalosporins for dairy farms (9).

Among many factors influencing veterinarians' decisions for AMU, the economic status of livestock owners was a significant determinant, with veterinarians assessing the ability of farmers to pay before prescribing ABX. In Bangladesh, it was found that the farmer's economic condition highly influenced the selection of ABX for treatment of livestock and poultry (31). Such subjective assessments are common in veterinary practice where prescription has been shown to be determined by perceived ease of administration and compliance, willingness of pet owners to give ABX, as well as animal characteristics (24). Cost of ABX was typically a factor in areas of varying socioeconomic status (24). We also found that the manufacturer's instructions were ranked as “very important” in calculating the dose of ABX by only 6% of respondent veterinarians. Other studies have also identified non-adherence to manufacturers' instructions as a reason for indiscriminate AMU in the agriculture sector (34). These findings contradict the observations in Bangladesh where drug instructions had a high-to-moderate influence on AMU (31).

Our results indicated that all respondents agreed that AMR is a major human and animal health problem caused by over use and/or improper AMU. However, in practice veterinarians are still prescribing ABX without prober laboratory diagnosis or AST. As discussed above this is due to the lack of on-site diagnostic facilities. These findings are similar to those from other LMICs such as Bangladesh (31) but contradict observations in developed countries where the majority of veterinarians followed AST before AMU (30, 35). However, availability and affordability of diagnostic tools and other facilities are different in developed and LMICs. Veterinarians suggested a wide range of preventive measures like proper animal nutrition, hygiene, and vaccination for the most frequently occurring animal diseases in the study area. This would result in reducing AMU and AMR in livestock production. They also identified key stakeholders responsible for implementing these prophylactic measures. However, they were not willing to participate in future work aiming to collect qualitative and quantitative data for AMU in animals. This is due to the lack of strict guidelines and regulations of AMU and having no time to keep records. As indicated in the results, in addition to the treatment of diseased animals, veterinarians are burdened with many other tasks as conducting extension services on animal production and health, implementing various government schemes, and running surveillance. Veterinarians' negative attitude toward keeping records for AMU may be due to the difficulties of being able to adhere to recommendations and guidelines if they did; they are not unaware of the dangers of inappropriate AMU but face very real barriers to improving practice. Further studies are required to understand the reasons behind veterinarians' negative attitudes toward keeping medical records and how better AMU can be supported. Unfortunately, it was impossible to do so due to COVID-19 restrictions but future research should use ethnographic assessments and qualitative research methods such as focus group discussions and in-depth interviews with veterinarians and farmers to properly address the problem and co-design solutions. Mixed methods provide deep understanding of the pattern and reasons of AMU that would not be identified using quantitative surveys alone (36, 37).

This study sought to provide insights on prescribing behavior and opinions of veterinarians regarding AMU and AMR. Although veterinarians are aware of AMR risks, the lack of diagnostic facilities in most veterinary clinics means that most prescribe ABX based on clinical symptoms. They are unaware of the existing national and state level regulations, guidelines, and strategies for AMR. Furthermore, there is a need for improved communication between policy makers and field veterinarians to bridge a gap between prescribing guidelines and clinical usage. Future initiatives should explore ways of better connecting all stakeholders with policy makers to drive the uptake and evaluation of key regulatory messages associated with key policies. To moderate AMU in livestock production in India and other LMICs with similar production systems, strategies should focus on: (1) enhancing communication and regular dissemination of updated AMU guidelines between relevant stakeholders; (2) CPD for veterinarians and other key stakeholders; and (3) provision of affordable and accessible veterinary services. In designing interventions to meet these objectives, attention need to be paid to the evaluation of their effectiveness. There is currently a conspicuous gap in the evidence on what works in different animal health systems including the role of veterinarians in the diagnostic, prescribing and treatment process. This is a significant challenge in under regulated dispensary settings in LMICs.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

This study was approved by the Human Ethical Review Committee (HERC), Royal (Dick), School of Veterinary Studies, The University of Edinburgh (Ref No. HERC_673_21). Local ethical approval was not acquired as there was no Ethical Committee for social science research in our partner's institute. However, a permission from the head of the Animal Husbandry and Veterinary Department (AHVD) in Assam to interview veterinarians. As interviews were conducted via telephone calls, oral consents were obtained after assurance of confidentiality and anonymity of respondents (University of Edinburgh).

ME contributed to the concept, survey design, data analysis, and writing up. JC, GG, and AT contributed to the research design and editing of article. BS and HS participated in preparing questionnaires and editing the article. BD piloted the questionnaires and collected the necessary data from the respondents. MH and BS provided the necessary logistics and overall supervision for executing the work. DM contributed to the concept and proof reading. All authors contributed to manuscript revision, read, and approved the submitted version.

This work was funded by the UK Newton Fund awards co-funded by the Economic and Social Research Council grant numbers ES/S000186/1 and the Department of Biotechnology (DBT), Government of India (BT/IN/Indo-UK/AMR/06/BRS/2018-19). For the purpose of open access, the author has applied a Creative Commons Attribution (CC BY) licence to any Author Accepted Manuscript version arising from this submission.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The reviewer SK declared a shared affiliation, though no other collaboration, with one of the author MH to the handling Editor.

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