Challenges to appropriate antimicrobial use in horses

This is the authors' abstract. We don't add key points for this paper.

Antimicrobial resistance (AMR) is a wicked one health challenge that has been comprehensively described by Scott Weese in this issue with a compelling call to action (Weese, 2023). Antimicrobial use is the primary driver of AMR. Any antimicrobial use can lead to AMR but the risk of AMR can change depending on the dose, duration and agent used. For this reason, antimicrobial stewardship (AMS) was developed as a way of optimising antimicrobial use to reduce the impact on AMR (World Health Organization, 2015). Antimicrobial stewardship has been an effective means of reducing AMR in tertiary human hospitals in the face of nosocomial outbreaks of resistant infections (Baur et al., 2017). Antimicrobial stewardship programmes are now widely implemented in small animal hospitals (Hardefeldt et al., 2022; Hopman et al., 2019; Singleton et al., 2021), however, the impact on AMR in this environment is very difficult to measure since culture and susceptibility are less frequently performed, caseloads are lower and clinical records are difficult to interrogate. The impact of AMS programmes on antimicrobial use is much easier to evaluate and several AMS programmes with different interventions have now been shown to have a positive influence on AMU in small animal practice (Hardefeldt et al., 2022; Hopman et al., 2019; Singleton et al., 2021). Recently a behaviour change framework called the behaviour change wheel has been used in healthcare (Michie et al., 2011). This framework is centred on three essential conditions: capability, opportunity and motivation (Figure 1). In addition, culture and context are also important factors that need to be considered (Charani & Holmes, 2019). While education is very important (as outlined below), there is strong evidence that educational interventions alone do not lead to behaviour change (Giguère et al., 2012). Capability includes physical (skills, ability and proficiencies) and psychological (knowledge, memory, decision processes) capability. This is perhaps the most obvious and most frequently targeted wedge of the behaviour change wheel—education. There has been a rapid increase in the production of educational resources about veterinary antimicrobial use and antimicrobial resistance over the past decade. Antimicrobial use guidelines are common in many countries (Asia Pacific Centre for Animal Health, 2017; British Equine Veterinary Association, 2016) and institutions such as the Fleming Fund are spearheading the development of these resources for low- and middle-income countries. Further work is needed to update product labels to reflect contemporary dosing regimens as many promote practices that are not supported by the literature (i.e. procaine penicillin) (Hardefeldt et al., 2018). Also, the interpretation of susceptibility testing is another area where capability could be targeted and increased research could address deficiencies. The difference between acquired and innate resistance is critically important, but there is poor awareness of innate resistance for specific pathogens and laboratories frequently report susceptibility for these antimicrobials. An accessible reference for the innate resistance profiles of pathogens would assist laboratories and clinicians but is currently not available. Clinicians should develop relationships with their laboratories. Improved communication, especially when unusual or unlikely resistance patterns occur (such as penicillin resistance in beta-haemolytic Streptococci), can lead to improved stewardship through repeated testing, to confirm unlikely resistances and appropriate interpretation of results especially when topical antimicrobials are being considered (e.g. in guttural pouches or intrauterine therapies) or when cut-offs have not been determined for horse pathogens, which is the case for many antimicrobials. Education and resources that target antimicrobial pharmacology have also been developed in Australia (Hardefeldt & Bailey, 2021) with wide usage in the equine veterinary community. Opportunity comprises physical (environmental context and resources) and social (social norms, comparisons and other social pressures) opportunity. Resources, like education, are commonplace with organisations such as BEVA (2016), AAEP (2022), AMR Vet Collective and University of Melbourne (2017) creating downloadable resources that aim to address the physical opportunity. Interventions such as the traffic light system that indicate the importance of antimicrobials are easy to implement and provide a visual reminder every time veterinarians reach for an antimicrobial. Similarly, waiting room posters can create an environmental context where antimicrobial stewardship is promoted. Understanding the social norms that drive and determine antimicrobial decision-making is critical for behaviour change (Mateus et al., 2014). We are social beings who interact and moderate our behaviours because of the response we get from our peers. Previous research highlighted the existence of professional hierarchies and etiquette as key determinants of prescribing decision-making in medical (Charani et al., 2011) and veterinary hospitals (Hardefeldt et al., 2018). In this context, having “buy-in” from leaders within a clinic and within the profession can alter the social norm of prescribing liberally to that of prescribing conservatively and in concordance with guidelines and protocols. This is difficult to “implement” as changing leadership is not an intervention that is often an option, however generational change and changing social norms within our profession seem to be having an impact. Social pressures from clients, especially when those clients contribute significantly to business prosperity, such as large stud farms to training yards, are also commonly identified as a barrier to AMS (Hardefeldt et al., 2018). Despite reducing rates of susceptibility to highly important antimicrobials (Flood et al., 2023), antimicrobial use on equine farms in many regions could reasonably be described as excessive (Alvarez-Narvaez et al., 2020; Hardefeldt et al., 2017; Ross et al., 2016). Prophylactic use of antimicrobials in neonatal foals in the first days of life, in older foals for R. equi, in yearlings during preparation for sales and in adults travelling to sales are all examples of use for which there is no evidence of benefit and, in some cases, evidence of harm. While the cost associated with antimicrobials is a driver for reducing use in farm animals, this is not the case in many equine operations. It is likely that regulation will be required to adequately address this issue, and this comes with the risk of additional restrictions on veterinary prescribing. Veterinarians and veterinary organisations should consider what steps they can take to reduce unnecessary antimicrobial use to mitigate the threat of regulation. Motivation incorporates reflective (beliefs about capabilities and consequences, roles, identity and optimism) and automatic (rewards, incentives and punishment) motivations. Lack of reflective motivation has contributed to inappropriate prescribing in the past, with prescribers often relaying beliefs about the low risk of antimicrobial use in horses on AMR in humans and the low contribution of individual prescribers' antimicrobial use on the risk of AMR development. This has probably led to a culture where prescribing for conditions such as equine asthma (Weese & Sabino, 2005) is widespread despite the common knowledge of the non-infectious nature of this syndrome. Lack of evidence for change, such as shortening duration of therapy, may also be negatively impacting reflective motivation and fear of deterioration is often cited as a barrier to AMS. However, antimicrobial use is not all or nothing and AMS is not withholding all antimicrobials. There is an in-between and a stepwise approach (reducing durations from 7 days to 5 days to 3 days, for example) that can substantially reduce antimicrobial use while allaying the fears of clinicians. It is unlikely that a “one size fits all” approach will work for AMS and the implementation of evidence-based interventions from one setting into another is greatly strengthened by taking time to tailor them to the relevant sociocultural context, which influences prescribers', patients' and even the professions' attitudes to antimicrobials. Veterinarians are critical to the process of designing antimicrobial stewardship programmes for veterinary practice if the outcome is to change our behaviour. This co-design of AMS programmes is a means of addressing reflective motivation. Co-design of interventions can improve individuals' beliefs about individual capabilities and roles and gives ownership to prescribers which increases accountability for adherence to the agreed interventions (Ward et al., 2018). Rewards or punishment are generally not part of veterinary AMS programmes although in the equine context racing exclusion times and other restrictions on drug use in performance horses may influence antimicrobial prescribing decisions. In addition, the financial reward that many veterinary businesses gain from the sales of antimicrobials may be a disincentive, real or perceived, for curbing antimicrobial sales. Culture and context also play a role in the success of AMS programmes. Research into how medical general practitioner's use evidence-based guidelines has revealed that, rather than referring to evidence-based guidelines, clinicians use inarticulate sources of knowledge which the authors called “mindlines” (Gabbay & le May, 2004). These mindlines consisted chiefly of factors of culture—interactions with opinion leaders, patients and their own and their colleagues' experiences. AMS programmes that are designed with culture and context in mind are likely to be more implementable. In conclusion, while there are numerous challenges to appropriate antimicrobial use in equine practice, it is incumbent upon us, as a profession, to take a proactive approach. Small changes can make a difference and numerous small changes can change the culture of prescribing within our profession. We need to take responsibility or we face a situation where regulators will make changes for us. Perhaps of greater concern, we are already facing a situation where AMR is impacting our patient outcomes and cost of therapy, and where culture and susceptibility testing will be required for every case we examine, as susceptibility becomes unpredictable. Both authors contributed to this editorial. No conflicts of interest have been declared. LYH is funded by the Australian Research Council Discovery Early Career Grant Award program (DE200100030). Not applicable to this editorial.