Challenges to exotic disease preparedness in Great Britain: The frontline veterinarian's perspective

Background: Exotic diseases pose a significant risk to horse health and welfare. Several stakeholder groups, including primary care veterinarians, share responsibility for maintaining freedom from pathogens that cause exotic diseases. However, little is known about the current state of exotic disease preparedness within the British horse industry. Objectives: The aim of this study was to explore equine veterinarians' experiences of, and attitudes towards, exotic disease preparedness in Great Britain. Study design: This is a qualitative interview- based study. Methods: Semistructured interviews were conducted with 14 primary care equine veterinarians in Great Britain. Participants were purposively selected to include perspectives across varying levels of experience, clientele and location. All interviews were recorded, transcribed verbatim and analysed using thematic analysis. Results: Three themes were developed: (a) the reactive generalist , relating to participants' self- concept of their role as primary care practitioners; (b) working within the bounds of influence , encompassing participants' perceived inability to influence their clients' knowledge and behaviours and (c) a fragmented horse industry , illustrating the wider culture in which participants worked, characterised by a lack of cohesion amongst its members.


| INTRODUC TI ON
Outbreaks of exotic diseases, defined in the United Kingdom as those not normally present in the country, occur infrequently but can cause significant health and economic consequences. In preparation for an exotic disease outbreak, each constituent country in the United Kingdom produces a contingency plan that outlines stakeholders' roles and responsibilities for animal disease emergencies. 1 During past significant exotic animal disease outbreaks, including foot-and-mouth disease in the United Kingdom (2001) and equine influenza in Australia (2007), primary care veterinarians were critical in mobilising an effective outbreak response alongside government authorities. [2][3][4] Given their training, expertise and established relationships with animal owners, primary care veterinarians are well placed to advise both their clients and other stakeholders in the event of a disease emergency. 5 The British horse industry has experienced sporadic outbreaks of exotic diseases in the past several years, including equine infectious anaemia (EIA) in 2012 and equine viral arteritis (EVA) in 2019. 6,7 In each instance, the investigation was prompted after primary care veterinarians performed diagnostic testing on horses that had been imported into the country or had gathered with international horses several years earlier. 6,7 A systematic review of pathogen incursions following international horse movements identified that the majority of transmission events involved horses that had not shown any clinical signs at the time of import, allowing them to enter the general population and subsequently spread infection. 8 In the event that exotic diseases escape border control, primary care veterinarians are likely to be the first line of defence to detect and report these pathogens.
While contingency planning focuses on coordinating the response to an exotic disease, preventing pathogen incursions in the first instance is central to effective preparedness. Primary care veterinarians have a multitude of roles and responsibilities when responding to an exotic disease outbreak; however, guidance on how to improve preparedness is less clear. There is a wide range of recommendations for veterinarians to improve their skills, including specialised training on recognising exotic diseases, 9,10 additional biosecurity training [11][12][13] or taking an active role in improving their clients' biosecurity. [14][15][16][17] Despite these recommendations, there is no prior research exploring what primary care veterinarians need for succeeding in this role and a lack of guidance on how they should follow current preparedness advice. A better understanding of the current state of exotic disease preparedness, and any challenges to actioning an effective response plan, would provide insights into opportunities for improvement. Therefore, the aim of this study was to explore experiences of, and attitudes towards, equine exotic disease preparedness amongst primary care veterinarians in Great Britain.

| MATERIAL S AND ME THODS
This was a qualitative interview study conducted from a critical realist stance, which considers that individuals' interpretation of reality is grounded in their experiences, beliefs and perceptions. 18 The study protocol was reviewed and approved by the Royal Veterinary

| Participants
Equine veterinarians working in primary care practice in Great Britain were invited to participate. Potential participants were identified through a combination of (a) contacts nominated by members of the RVC equine veterinarian community and (b) snowball sampling (ie, participant referrals of other participants). Based on prior understanding of factors that might impact experiences, perspectives and attitudes amongst veterinarians, potential participants were purposively selected to include several demographic characteristics, including gender, length of experience in practice, clientele (racing or nonracing) and geographic location. The research team made initial contact with potential participants by email, describing the study and inviting voluntary participation in an interview. Participant recruitment ended when individuals representing an array of the demographic characteristics of interest had been included in the sample.

| Interviews
Semistructured interviews were conducted between December 2018 and May 2019 by the first author, an epidemiologist with qualitative research training. The interviewer's background as a nonveterinarian was disclosed to participants prior to the start of the interview. All interviews were conducted face to face at a location of the participant's choosing, such as a quiet area at their practice.
Participants were presented with a consent form, and written consent to participate was obtained prior to the start of the interview.
All interviews were audio recorded.
An interview guide, previously piloted with two veterinarians, was used to encourage conversation about exotic disease preparedness (Item S1). The interview guide was structured around three broad topic areas: general infectious disease prevention (ie, biosecurity), detecting and reporting exotic diseases and the response to exotic disease incursions. The topic areas acted as a starting point for the interviewer to ask open-ended questions and follow-up questions based on the participant's responses.

| Analysis
Audio recordings from the interviews were transcribed verbatim by an external service and checked for accuracy against the original recordings by the first author. Inductive thematic analysis was conducted by the first author, based on the method described by Braun and Clarke. 19 Thematic analysis was chosen due to its theoretical flexibility (eg, could be applied from a critical realist stance) and appropriateness for identifying patterns of meaning across data. 19 An inductive approach was used to avoid imposing a priori assumptions on the data and resulting themes. First, the transcripts were read several times to gain familiarity with the data, followed by initial semantic-level coding to label topics or concepts expressed by participants. All data, and their initial codes, were then imported into NVivo version 12.2.0 for data management. Codes were refined through a comparison with different levels of data (other codes, data extracts, and the original dataset). Preliminary themes were developed through an iterative process of grouping codes with similar meaning together followed by discussion amongst the research team. The final themes reflected patterns identified across the dataset, and subthemes reflected specific elements within each theme.

| RE SULTS
Fourteen veterinarians agreed to participate in the study (Table 1).
Interviews were a median of 53 min in length (range 33 to 87 min).
Three themes relating to veterinarians' experiences of, and attitudes towards, exotic disease preparedness were developed from the interview data: (a) the reactive generalist, (b) working within the bounds of influence and (c) a fragmented horse industry. An overview of the themes and subthemes is presented in Figure 1.

| Theme 1: The reactive generalist
Participants' self-concepts of their role in primary care practice shaped how they approached exotic disease preparedness.
Participants often found themselves working to the 'firefighter' model of medicine, responding to ill-health instead of proactively providing wellness services. This ingrained reactive approach meant that participants struggled to shift into a preventive mindset in the absence of an imminent threat. By identifying as generalists, participants acknowledged they could not reasonably be an expert in all areas of veterinary medicine. Over time, their expertise became targeted towards common conditions, moving them further away from specialist topics like exotic diseases.
3.1.1 | Subtheme 1.1: Firefighting approach to medicine The 'firefighter' model of veterinary medicine underpinned participants' approach to preparedness; responding to illness (ie, curing disease) was generally prioritised over preventive medicine.
Consultations with clients were reserved for resolving health problems and initiating discussions beyond the remit of the situation seemed inappropriate: On a day-to-day basis, I'm being paid to go and fix the eye or the heart or something and you can't just spiral off into worrying [the client] about West Nile virus.

(Vet 14)
With consultations dedicated to the health problem at hand, participants had to find time outside of their client contact hours to focus on preventive medicine. However, this required effort from both the participant and the client. Some veterinary practices set up initiatives Working in an environment that fostered collaboration between colleagues led to increased confidence in asking for help when needed.

| Theme 2: Working within the bounds of influence
Participants struggled with a perceived inability to influence their clients' knowledge and behaviours in relation to improving biosecurity. Within the veterinarian-client relationship, some participants viewed their role as information providers, or educators, and experienced frustration when clients did not follow their advice. The need to be influential stemmed from an assumption that the client lacked sufficient knowledge. By acting as an educator, participants aimed to change their clients' behaviours through providing more knowledge.
Participants perceived a greater level of influence when a positive client relationship was established; however, good veterinarianclient relationships were sometimes undermined by more accessible and preferable information sources, such as other horse owners on social media. The increased availability and accessibility of competing influences was an added challenge to the veterinarian's ability to influence positive change.

| Subtheme 2.1: Educators, not enforcers
There was a tendency for participants to take an 'educator' approach to the veterinarian-client relationship. Some used a traditional directive communication style, which attempted to impart the veterinarian's knowledge to the client. For example, one participant described his approach for asking clients to follow disease management guidelines: I will repeat myself until they're bored of me saying it … and get them almost to repeat it back to me, so that they're at the point where they're so bored of you telling them the rules and regulations, that they're going, 'Yeah, that one, yeah, that one'. (Vet 12) Participants often observed dissonance between their own training in preventing and managing disease and how clients were approaching disease management. The difference in management styles was assumed, by participants, to stem from clients' lack of knowledge about biosecurity. To counteract this assumed lack of knowledge, participants suggested that the best approach to improve biosecurity uptake was to provide more education:

| Theme 3: A fragmented horse industry
An effective response to an equine infectious disease outbreak would rely on action at the population level. However, the culture of the wider horse industry in which participants worked was characterised by a lack of cohesion amongst its members.
Overarching issues with coordination across sectors, and unbalanced resources between racing and nonracing horses, reflected a siloed industry structure. Participants perceived that owners, in general, did not have a sense of their horse belonging to a national herd.

| Subtheme 3.1: An industry of two halves
The overarching structure of the horse industry was described as 'disparate' and 'disjointed', with different sectors (ie, racing and nonracing) operating by their own rules within their own contexts. In particular, the racing sector had more resources and support than other sectors and could therefore prepare and facilitate a more coherent response to outbreaks. This was largely driven by the eco- This tendency for horse owners to ostracise those with horses affected by disease made it challenging for participants to promote preparedness, a practice that relies on altruism. Preventing the spread of infectious diseases requires clients to make sacrifices (eg, restricting horse movements). When horse ownership was tied to clients' livelihood, such as for those in the racing industry, it was more difficult for participants to convince them to be altruistic:

| D ISCUSS I ON
This study provides insights into British equine veterinarians' perceptions of their role in exotic disease preparedness. The findings highlight several challenges to preparedness, including the mismatch between the nature of primary care practice and the required awareness of exotic diseases, the lack of influence on clients' general horse management behaviours and the fragmented nature of the equine industry.
As primary care practitioners, participants shared a strong identity as generalists. An increased recognition of the value of primary care practitioners as 'expert generalists' has highlighted their unique skillset in recognising familiar patterns and applying clinical reasoning. 20,21 Both generalists and specialists play integral roles in medicine, and by acknowledging the expertise needed to be a successful general practitioner, veterinarians can be better supported in that role. 20 Differential diagnoses, in the first instance, often rely on the ability of a veterinarian to recognise and categorise a disease based on its clinical presentation. 22,23 Therefore, training focused on strengthening clinical reasoning skills, rather than specific diagnostic aspects for particular exotic diseases, is better suited to support primary care veterinarians in all aspects of their role as expert generalists. The potential for delays in diagnosis because of lack of specificity of clinical signs highlights the importance of developing good, baseline biosecurity practices as routine, as well as the need to improve understanding and perception of individual risk.
Participants described a pragmatic approach to preparedness, which relied on effective support systems. Unsurprisingly, the first ports of call were colleagues and other familiar sources. Trusted colleagues and specialists are frequently used by veterinarians to guide their clinical decision making, 24 with most experienced colleagues acting as key individuals for advice. 25 In contrast, distrust and unfamiliarity might dissuade participants from following an organisation's advice. 26 In 2010, local veterinarians in the county of Devon, UK, criticised the lack of communication from the government about a confirmed case of EIA in their region. 27 A previous study of horse owners in the United Kingdom described a sense of distrust in whether the government would engage in equine disease outbreaks given that they were not farm animals. 28 Furthermore, several studies have reported that distrust in authorities was a barrier to veterinarians reporting notifiable diseases, even when it was mandated. 29,30 Despite the usefulness of veterinarians using personal support networks when presented with clinical uncertainty, developing and strengthening trust between veterinarians and the government is needed to ensure that suspected exotic diseases are actually reported, as mandated.
In the absence of an imminent threat, participants did not prioritise exotic disease preparedness because of more immediate concerns. The lack of prioritisation of nonimmediate threats has been described for other emerging issues, such as antimicrobial resistance, where veterinarians felt it was difficult to change their current behaviours when antimicrobial resistance was regarded as something that was not currently affecting them. 31 Instead, participants continued to default to the 'firefighter' model of responding to threats, as and when they arrived. The veterinary profession has experienced longstanding difficulties in moving into a preventive advisory role, often due to a complex relationship between the veterinary and agricultural industries, as well as political environments and pressures. 32 In the farming industry, veterinarians have struggled to market their preventive services, citing difficulties in putting their knowledge into action on farms. [33][34][35] This is further complicated by the fact that most preventive care is being administered by other professionals or by the owner themselves, rather than the veterinarian. 36 As the demand for 'firefighter' services remains high (eg, over 60% of small animal consultations), 37 equine veterinarians might struggle to shift effectively into a preventive advisory role for distant risks, such as exotic diseases.
Arguably, there is a tendency in veterinary training to view knowledge as something that can be passed from one person to another. 38 Some of the participants relied on this didactic style of communication, tending to assume that providing more education to clients would result in them changing their behaviours. Moving towards a relationship-centred communication approach would increase the likelihood of achieving any desired behaviour change. [38][39][40] The competition between veterinarians and other influential sources can conflict with an individual's professional identity, because it positions clients as 'frustrating obstacles' to transferring their veterinary knowledge. 41 Communication strategies tailored to specific clients might allow veterinarians to reach an agreed solution with those who are initially less receptive. 42 Owners who trust their veterinarian are more likely to prefer them to other available information sources, 43 so strategies aiming to strengthen the veterinarian-client relationship could mitigate veterinarians' perceived lack of influence and lead to positive change.
An individualistic culture within the British horse industry appears to pose a key threat to effective exotic disease preparedness overall. Study participants perceived that owners would not act against their self-interests in order to protect the health of the wider horse population. In the UK cattle and sheep farming community, barriers to collective action during a disease outbreak were linked to distrust within the community itself. 44 Community distrust can be a product of 'in-group' formation, where individuals naturally form groups with those that are similar to each other. 45 A study of livestock keepers identified a strong separation between commercial and hobby farmers, in which commercial farmers perceived themselves as 'good' and perceived hobby farmers as 'poor'. 46 This is similar to the distinction between the racing and nonracing sectors observed in this study. The lack of collective identity across the British horse industry, and the individualistic culture of its members, has implications for the type of preparedness measures that would be effective and feasible to implement. Individualistic cultures tend to benefit from the adoption of passive measures (ie, those instituted by an overarching body) instead of those that require substantial action from the individual. 47 However, given the fragmented culture of this industry, a reliance on an overarching body to institute change might introduce further challenges. The British horse industry is an amalgamation of several overarching bodies that regulate and advise on several interest groups (eg, racing, breeding and equestrian competition). In 2010, a structural review of the British horse industry concluded that relationships between the large number of interest groups were unstable. 48 Furthermore, the review found that a differential allocation of resources across the groups created an unequal distribution of power and the potential for conflict amongst the members. 48 While the structure of the industry has likely changed since 2010, the mirrored experiences of the participants suggest further improvements are required to achieve unison. Continued lack of cohesiveness would be detrimental to any outbreak response that relies on effective partnerships across multiple agencies, organisations and stakeholders. 49 As this was a qualitative study, the findings are not intended to be statistically representative of the wider population of veterinarians, but rather representative of a variety of experiences, attitudes and perceptions held by veterinarians within a specified context. Criteria used to evaluate quantitative research, such as statistical power and generalisability, are not directly transferable to qualitative research due to differences in epistemological assumptions. In fact, small and purposively chosen samples are a benefit of qualitative research because they allow for the collection of rich, in-depth accounts from participants. 50 The purposive selection of participants across different demographic characteristics, including gender, length of experience, type of clientele, and geographic location, allowed for the inclusion of diverse viewpoints, but the consistencies across participants' accounts support the reliability of the key findings. 51 Qualitative research is inherently influenced by the research team, because the researcher is actively engaged in conceptualisation, interpretation and reporting. 52 As an infectious disease epidemiologist, the first author was aware of general issues surrounding disease preparedness in the equine industry; however, they had not trained as a veterinarian and therefore could approach topics with participants without prejudgement or assumed knowledge. The experiences and positionality of the wider research team, which included equine veterinarians, brought a richer understanding of the data through team discussions. It is important to note that this study does not capture the views of clients, government officials or infectious disease specialists, and therefore, further research is needed to explore other stakeholders' experiences and perceptions of exotic disease preparedness.

| CON CLUS IONS
This study sought to explore primary care veterinarians' experiences of, and attitudes to wards, exotic disease preparedness in Great Britain. The findings suggest that improvements are required before an optimal level of preparedness can be achieved. There are several areas where veterinarians can be better supported at the frontline of disease emergencies: (a) strengthening the development of clinical reasoning skills and fostering collaborative client relationships; (b) ensuring that primary care veterinarians have access to support networks during an emergency, such as trusted senior colleagues or infectious disease specialists; and (c) clarification of the role of the primary care veterinarian in disease preparedness, particularly in engaging in biosecurity implementation with their clients.
Further research into the culture of the horse industry and how the overarching structure might facilitate or prevent effective disease preparedness is required.

ACK N OWLED G EM ENTS
The authors gratefully acknowledge the veterinarians who participated in this study.

CO N FLI C T O F I NTE R E S T S
The authors have declared no competing interests.

AUTH O R CO NTR I B UTI O N S
K. Spence, S. Rosanowski, J. Slater and J. Cardwell contributed to study conception and design. K. Spence collected and analysed the data, with guidance from J. Cardwell. K. Spence, S. Rosanowski, J.
Slater and J. Cardwell contributed to data interpretation and manuscript preparation. All authors approved the final manuscript.

E TH I C A L A N I M A L R E S E A RCH
This study was granted institutional ethical approval from the Royal Veterinary College (URN 2018-1664).

I N FO R M E D CO N S E NT
All participants provided written informed consent.

DATA ACCE SS I B I LIT Y S TATE M E NT
The data that support the findings of this study are not publicly available due to privacy or ethical restrictions.

PE E R R E V I E W
The peer review history for this article is available at https://publo ns.com/publo n/10.1111/evj.13469.