Increasing awareness of bacterial antimicrobial resistance in human beings and veterinary medicine has raised concerns over the issue of overprescribing and the indiscriminate use of antimicrobials. Their use in food-producing animals is under scrutiny due to the perceived risk from the zoonotic transfer of resistant pathogens from animals to human beings. This study used focus groups to explore the drivers and motivators behind antimicrobial use and prescribing by veterinary surgeons and farmers in the pig industry in the UK. Studies of two veterinary and four farmer focus groups were undertaken, each with between three and six participants, in three geographically distinct regions of low, moderate and high pig density in England. Thematic analysis of the focus group transcriptions revealed convergent themes, both within and across, the veterinary and farmer focus groups. Veterinary opinion was such that ‘external pressures’, such as pressure from clients, legislation and public perception, were considered to strongly influence prescribing behaviour, whereas, farmers considered issues surrounding farming systems and management to be greater drivers towards antimicrobial use. Acquiring such in-depth insight into the antimicrobial prescribing behaviours in veterinary medicine provides more detailed understanding of prescribing practice and will aid the development of interventions to promote the responsible use of antimicrobials.
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The use of antimicrobials in food-producing animals is an emotive subject which has sparked much debate. Pigs currently contribute the largest proportion towards the sale of single-species antimicrobial products in food-producing animals in the UK (Anon 2013d). This high usage, alongside the common administration of antimicrobials through medicated feedstuffs, has highlighted their use in pigs as an area of concern (Levitt 2011b, Anon 2012b). The media has implicated the overuse of antimicrobials in pigs as being responsible for antimicrobial resistance in human beings (Levitt 2011a, Harvey 2013) through the zoonotic transfer of resistant pathogens from animals to human beings. However, others contend that there is little evidence to support such transfer being anything but an infrequent event (Bailar and Travers 2002, McEwen 2012, Guardabassi 2013).
The prudent use of antimicrobials is essential to reduce selection pressure and maintain the efficacy of such drugs. Guidelines on their responsible use in animals have been advocated by various UK organisations including the Responsible Use of Medicines in Agriculture, the British Veterinary Association (Andrews 2009, Anon 2013a, c), and more recently the Pig Veterinary Society (Anon 2014). Alongside the judicious use of antimicrobials, improvements in the management practices and housing of pigs have been shown to reduce the reliance of some farms on antimicrobials (Dunlop and others 1998, Stevens and others 2007, Fels-Klerx and others 2011). While existing quantitative studies have attempted to investigate and quantify antimicrobial use and the associations with particular practices (Dunlop and others 1998, Stevens and others 2007, Gibbons and others 2013), there has been little research investigating prescribing behaviours in the UK pig industry.
In this study, the motivations behind the use and prescribing patterns of antimicrobials in the pig industry are investigated using qualitative methods that have previously been used to explore human prescribing behaviours (Rodrigues and others 2013). The approach in this study was based on focus groups (Barden and others 1998, Coenen and others 2000, Walker and others 2000, Kotwani and others 2010, Kuehlein and others 2011, Vazquez-Lago and others 2012). The group discussion setting enabled the comparison of the different opinions that are exchanged between participants during sessions (Morgan 1993, Kitzinger and Barbour 1999, Bryman 2012). These methods are emerging as useful tools in assessing behaviours in veterinary medicine (Coe and others 2007, Gunn and others 2008, Kaler and Green 2013, Robinson and Epperson 2013, Sheehan 2013).
Through the medium of focus groups, this study aimed to investigate the motivations behind the use and prescribing patterns of antimicrobials in the pig industry.
Materials and methods
Focus group design and structure
In total, six focus groups, each containing between three and six participants were held to explore open-ended themes surrounding antimicrobial use and prescribing behaviours in pigs. These were conducted over three meetings in three geographically distinct regions; one in an area of moderate pig density and two in areas of high pig density. These regions were chosen based on the demographic density of the UK pig population, the convenience of using existing contacts in the pig industry and the ability to organise a focus group at the convenience of participants. Within most of the meetings, farmer-only and veterinary surgeon (vet)-only focus groups were conducted as there was concern that the presence of a vet in the farmer group and conversely a farmer in the vet group, may not allow for free discussion of opinions. At the end of each meeting, time was allowed for discussion and comparison between the groups.
A purposive sampling technique was used in order to identify a sample population, whereby individuals were chosen with characteristics relevant to the study (Bryman 2012). The characteristics for inclusion in the sample population were determined by the authors but aimed to include vets and farmers with experience of different pig rearing systems, with differing levels of job responsibility and experience, and from different geographical areas, in an attempt to represent a range of vets and farmers involved in commercial pig production in the UK. The only incentive provided was refreshments.
Approval for the study was granted by the University of Liverpool Research Ethics committee, and an information sheet giving an overview of the project was provided for all participants before their attendance at a focus group. Signed consent to participate in the focus groups was gained before discussion, with participants being given the option to opt out of having the discussion recorded.
The focus groups were conducted using Kreuger's guidelines on ‘Designing and Conducting Focus Group Interviews’, which use a set of open-ended questions to spark discussion (Krueger 2002). A topic guide was developed by the authors based on these guidelines; questions were clustered under the following topic headings (Table 1):
perceptions of antimicrobials and their usage
current antimicrobial use
All participants were provided with a copy of the question set and each focus group was moderated by one of the authors. The moderator's role was to guide the discussion and ensure all areas in the topic guide were covered while allowing free conversation to develop. The moderator took notes of any key points or body language of participants.
Focus group audio recordings were transcribed verbatim and anonymised. Thematic analyses techniques were used to analyse transcripts (Braun and Clarke 2006). The process of coding was assisted through the use of the qualitative data management tool Atlas.ti V.7.7.1. (ATLAS.ti Scientific Software Development). This involved identifying codes that summarised the meaning of text fragments and the iterative reading and re-reading of transcripts, such that codes were reviewed and re-evaluated. Constant comparison methods were used in order to ensure that less common attitudes and opinions were exposed as well as more dominant themes (Braun and Clarke 2006). Coded sections of the transcripts revealed recurring opinions and subject areas which were considered to be minor themes across the focus groups. These minor themes were found to link and common subject areas were exposed and were categorised as major themes.
Focus group participants
Six focus groups with a total of nine vets and seventeen farmers were completed. These focus groups encompassed a range of different individuals within the pig industry including vets working as assistants and partners, from both private practices and pig production companies, farmers from large companies and independent farms, and representatives from the British Pig Executive, the Pig Veterinary Society and the pharmaceutical industry (Tables 2 and 3). There was a wide age distribution among the vets and farmers ranging from approximately early twenties to mid-sixties.
Eight major themes emerged which were considered to influence antimicrobial prescribing behaviours. These major themes included ‘Agricultural Factors’, ‘External Pressures’, ‘Vet–Client Relationship’, ‘Drug-related Factors’, ‘Disease Epidemiology and Outcomes’, ‘Responsibility’, ‘Economic Factors’ and ‘Knowledge Base’.
‘Agricultural factors’ were a commonly recurring theme in the farmer focus groups and were often raised by the vet focus groups. There was a spectrum of opinion as to which rearing systems, be they indoor or outdoor, slatted or straw-based, were beneficial to reducing antimicrobial use by vet and farmer participants. There was, however, agreement between the vet and farmer focus groups that an all-in-all-out pig flow was beneficial to minimising the requirement for antimicrobials over continuous pig flow systems. In the following quote, a vet describes a farm that employs a pig flow system whereby pigs are continuously added to pens, and are mixed from different sources or farms, and uses this as an example of a farm with a high antimicrobial requirement.
…anything that's continuous… anything that mixes pigs… … (Vet)
There was some conflict of opinion on the relationship between management practices and antimicrobial usage. The subsequent quote, from a vet, reflects the opinion of the majority of vet and farmer participants, that management practices could be employed that would reduce the reliance on antimicrobials, but that may have negative economic consequences:
…my view is probably we do use too much mass medication… there could be management practices that a lot of clients could put in place to reduce antibiotics that are economically less viable than using the antibiotics… (Vet)
Conversely, the opinions of a minority of the farmer participants considered that antimicrobial use would not compensate for poor management.
…antibiotics are not going to cover bad management… (Farmer)
Both the vet and farmer focus groups considered the health status of a herd to be a key factor in the amount of antimicrobials used on farms. A high health status was correlated with the ability to reduce the reliance on antimicrobials when compared with a lower health status.
We're a high health herd, we get very good performance, we put nothing [no antimicrobials] in-feed… (Farmer)
A pressure was considered to be any factor that placed a demand on participants and resulted in some level of stress, or a feeling of coercion, into a particular behaviour. Pressures were identified by participants whenever they considered that a request or issue caused them to question and reflect on their personal morals. ‘External pressures’ considered pressure from politics and legislation, public perception, importation of pig products and pressure from retailers. In the vet focus groups, this was a very commonly recurring theme, but was less common in the farmer focus groups.
Pressures from politics and legislation were considered to be a major stressor by vets within the focus groups. Vets reflected that legislative decisions are driven by political pressure and are not always supported by scientific evidence; as one participant expressed on the subject of the Europe-wide Antimicrobial Growth Promoter ban:
…it was a political decision, it wasn't being driven by the farming community or by the veterinary community… (Vet)
Client pressure was considered to be a major influencer towards antimicrobial prescribing by the vet participants. Vets felt a strong burden of responsibility to ensure that the correct antimicrobial was prescribed as pressure arose from clients when a treatment was unsuccessful.
And the client won't accept well, why have you tried three products? They want you to come up with the right answer straight away … (Vet)
The farmer focus groups did not observe this pressure and considered their interactions with their vet to be more of a mutual relationship. Farmers considered that prescribing decisions by the vet were made following consultation and discussion with themselves.
I rely on them [the vet]… and you build a working relationship… over the years…. (Farmer)
By contrast, this theme did not appear in the vet focus groups.
‘Drug-related factors’ considered the characteristics of drugs chosen, such as efficacy, formulation, inherent sensitivity patterns, drug availability and the withdrawal periods of products. Across the vet and farmer focus groups, the majority of participants did not consider that antimicrobial resistance had affected the health and welfare of their livestock and considered this to be more problematic for others, while a minority acknowledged that the issue had arisen.
…there are locations in the UK that have multi-resistance dysentery but… we don't have it… (Vet)
This viewpoint was echoed in the farmer focus groups and linked closely with the theme of ‘Responsibility’; the sense that participants perceived that some vets and farmers are not using antimicrobials as judiciously as they perhaps should be, but that they were not themselves in this category.
The potential banning or restriction of the ‘critical antimicrobials’ (Collignon and others 2009) was a point for discussion within the focus groups. Vet and farmer participants generally considered that increased restrictions on the fluoroquinolones and third-generation and fourth-generation cephalosporins would restrict antimicrobial options. Independently, both vet focus groups felt that there had been an increased requirement to use the aforementioned classes of antimicrobials due to the ‘loss of products’:
Naxcel (Ceftiofur; Naxcel; Zoetis UK) and Baytril (Enrofloxacin; Baytril; Bayer) are being used because other products have been taken off the market… (Vet)
There was greater concern across the focus groups over the potential restriction of macrolide use; with the utmost concern over tylosin. Vets cited it as being the only authorised antimicrobial available as an in-feed formulation for use in pigs near slaughter weight as it has a zero withdrawal period. Farmers were concerned over whether alternative antimicrobials were available for use in these pigs, but considered the task of finding an alternative to be the responsibility of the vet.
Antimicrobial use for prophylaxis in pigs not exhibiting clinical signs of disease was considered justifiable and prudent by the vet and farmer focus groups, for conditions which cannot be controlled by other means. It sparked a rather emotive response among participants.
…you cannot argue welfare and ban antibiotic usage in a preventive way. (Vet)
All focus groups considered how difficult the decision can be to withdraw prophylactic antimicrobials once they are perceived to have a benefit. Participants also considered that the formulation of the drug played a role in this decision; should in-water medication require re-starting, following its withdrawal, there is no time delay in comparison with in-feed formulations where there is often a delay obtaining a feed order.
The difficulty is though if you put it [an antimicrobial] in feed, ‘it works’ in inverted commas, there is a perceived benefit, sometimes you're a bit reluctant to take it out… If you take it out, it goes wrong and it's in feed then there is quite a bit of a lag before it goes in again than with water… (Farmer)
Disease epidemiology and outcomes
Disease was not considered as a static state in which a pig is either infected or not, it was considered as a dynamic state in which different diseases interact to form a ‘stew pot of disease’ and where disease may be sporadic, subclinical or a persistent problem. This opinion was shared by the vet and farmer focus groups.
I think you've got to differentiate between whether you're dealing with an endemic, chronic, grumbling disease versus an acute outbreak of a disease and the usages of the two are completely different… (Vet)
This unpredictability led participants to consider disease prevention strategies to be essential with vets and farmers citing vaccination as a possible solution to reduce a farm's reliance on antimicrobials. Diagnostic testing, both in emerging diseases and in endemic infections was considered by all focus groups to influence antimicrobial prescription. Antimicrobial susceptibility testing for bacterial pathogens was considered to influence the decision of which class and formulation of antimicrobial to prescribe.
The theme, ‘Responsibility’, considered the concept of the prudent use of antimicrobials and explored where this responsibility was perceived to lie. There was an overwhelming opinion among vets and farmers that they considered themselves to use antimicrobials responsibly, and in the case of the farmers, they considered their respective vets to also be responsible. However, concern was present with some participants that other vets and farmers may be less judicious. In the following quote, the vet expresses concern that a neighbouring vet may overprescribe antimicrobials for a particular farm.
I can think of lots of names… of people [vets] … who've used antibiotics a lot more liberally than we'd ever dream of and in ways we'd want to avoid (Vet)
Commonly, both vet and farmer focus groups placed the main burden of responsibility for the prudent use of antimicrobials on the vet.
Vets considered compliance to be a factor that drove them to choose a particular formulation of an antimicrobial on a particular farm.
…if you know they're not going to jab something for five days then… you can water medicate… (Vet)
A shared belief among all focus groups was that irresponsible use in human medicine was contributing to the antimicrobial resistance problems in human medicine. A number of participants from the farmer and vet focus groups felt that poor compliance is an issue in human medicine.
the pigs actually finish the course whereas the humans don't. (Vet)
The theme of ‘Economic Factors’ emerged equally commonly in the farmer and vet focus groups. The shared opinion of the majority of vets and farmers was that cost influenced prescribing patterns in some situations.
[farmers] can't afford to put any antibiotics in without any good reason… (Farmer)
A small number of vets in Focus Group 1A showed dynamic views on this issue. Initially, one participant took a defensive stance that cost would never drive antimicrobial use:
what influences choice… not cost? (Vet)
However, later acknowledged that in some circumstances it may influence prescribing behaviours:
…responsible use and cost effectiveness…. (Vet)
Production costs were cited by both the farmer and vet focus groups as being a major factor in antimicrobial usage. Issues such as the high cost of management and an inability to reinvest in buildings were considered to be major hurdles in reducing antimicrobial usage.
If farmers could re-invest in new and better buildings. That would drive down antibiotic dependency… there isn't enough profitability to re-invest… (Farmer)
Farmers considered their vet to be the most trusted source of information on antimicrobials; while being sceptical and non-trusting of information gained from advertisements.
…farmers would be the least trusting of any advert… (Farmer)
Vets and farmers did not believe that the 2013 ban on such advertisement would have any impact on antimicrobial usage in the pig sector. Vets cited the National Office for Animal Health (NOAH) Compendium, alongside other academic and scientific literature, as the information they trusted most on antimicrobials.
The qualitative approach used in this study offered an interactive forum for participants to share and discuss their experiences and opinions on what drives and motivates antimicrobial use in pig production. Many of the themes that emerged were shared between vets and farmers showing common attitudes and concerns.
The focus group environment enabled participants to clarify their individual opinions on the subject through discussion and knowledge exchange between participants; a method called the ‘sharing and comparing process’ (Morgan 1997). This allowed a complex understanding of the subject without the moderator being required to give detailed information or definitions which may have influenced opinion. An inevitable limitation of the focus group setting is that the presence of one or two more dominant participants may result in data reflecting the opinions of these individuals, rather than the group as a whole, this was minimised by the presence of a moderator to encourage the expression of opinions by all participants (Fern 1982).
The literature suggests that antimicrobial usage may differ more on an individual farm basis than between different rearing systems as a whole (indoor v outdoor, slatted v straw-based systems) (Scott and others 2006, 2007, Stevens and others 2007). This trend is mirrored in the diverse opinions elicited from the focus groups with regards to which rearing systems would lead to lower or higher antimicrobial use, and may reflect the inclusion of participants experienced in a range of rearing systems and from a variety of geographical locations.
An inadequate farm environment and a lack of ability to reinvest in the farm infrastructure were a transparent concern in the vet and farmer focus groups. Similarly, Stevens and others (2007) found that 79 per cent of UK pig farmers considered ‘improved housing’ as an alternative to antimicrobial use. Participants considered the lack of profitability in the pig industry to limit their ability to improve housing, however, previous work shows that farms, where the farmer felt there was room for improvement in the farm environment, used more in-feed antimicrobials than those who did not (Scott and others 2006, 2007, Stevens and others 2007). This would inevitably increase drug costs on these farms. This shows the difficult balance between the relatively short-term cost of antimicrobials and the more long-term cost of environment improvements that were discussed at length by vets and farmers in these discussion groups.
Cost was considered to influence antimicrobial use by the vet and farmer focus groups. Previous work has found that cost motivates antimicrobial prescribing in human medicine (Buusman and others 2007), cattle practice (Gibbons and others 2013) and in the pig sector (Sheehan 2013). It has been proposed that there is a conflict of interest in that the vets' ability to profit from the sale of antimicrobials may be seen to influence prescribing decisions (Anon 2001, Rollin 2006). However, this study and previous work by the Veterinary Medicines Directorate (VMD) revealed that pig vets felt strongly that this did not drive their prescribing decisions (Sheehan 2013). The strength of opinion on this issue may reflect the pressure on vets from the media's negative portrayal of antimicrobial use in animals (Levitt 2011a, Harvey 2013) and WHO's proposal to ‘decouple’ antimicrobial sales, which would separate the right to prescribe from the vets' ability to supply antimicrobials (Anon 2012a).
Vets identified that pressure from clients can be a driver for antimicrobial prescribing, while farmers seldom considered this to be the case. Similar pressure has been shown to drive antimicrobial prescribing in human medicine (Cockburn and Pit 1997, Macfarlane and others 1997, Coenen and others 2000, Kumar and others 2003), and Gibbons and others (2013) identified that cattle practitioners in Ireland were more likely to prescribe antimicrobials if they perceived that farmers expected them. Conversely, farmers considered the mutual relationship between the farmer and the vet to have a greater influence on antimicrobial usage. Such interaction has been shown to influence prescribing practice in human medicine, where maintaining the doctor–patient relationship was considered to influence prescribing behaviours (Butler and others 1998). The vets in this study did not identify the theme ‘Vet–Client Relationship’ as influencing antimicrobial usage, possibly reflecting a difference in perceptions. By contrast, ‘veterinarian attitude/customer relationship’ was identified by the VMD focus groups as driving antimicrobial use in the pig sector (Sheehan 2013). This discrepancy may reflect differences in the participants purposively sampled for each study.
Despite this perceived close working relationship between the vet and farmer, farmers perceived the responsibility for the prudent use of antimicrobials to lie with vets. This opinion was echoed in work by Stevens and others (2007) who showed that 96 per cent of pig farmers considered responsibility for ‘good practice in the use of antimicrobials’ to lie with vets. Busani and others (2004) defined a ‘judicious user’ of antimicrobials to be a cattle practitioner who showed an awareness of the problem of antimicrobial resistance and the importance of responsible use; three-quarters of cattle vets conformed to this description (Busani and others 2004). In parallel, the majority of vets and farmers considered that they were prudent antimicrobial users and showed the appropriate awareness to fit Busani and other's model of a ‘judicious user’.
The importance of the prudent use of antimicrobials in livestock, which are considered by WHO to be ‘critical to human health’ (Anon 2011), was widely acknowledged by the vet focus groups. A high level of awareness of the importance of only using fluoroquinolones and third-generation and fourth-generation cephalosporins, when absolutely necessary, was shown by vets. This consciousness and sparing usage is widely quoted in various publications as being commonplace among companion and food-producing animal vets (Rantala and others 2004, Weese 2006, Williams and others 2012, De Briyne and others 2013). There was concern among vets and farmers that restrictions on these classes would put increased pressure on themselves and the health and economics of the UK pig herd. However, it was the possibility of increasing restrictions on the macrolide class of antimicrobials that provoked greater concern among vets and farmers. This may reflect the frequency of the use of macrolides in pig production globally (Dunlop and others 1998, Anon 2007, Jordan and others 2009).
Antimicrobial use for disease prophylaxis is a recognised practice within the pig industry and was considered by vets and farmers to be a common and justifiable use. This opinion is mirrored in work by Stevens and others (2007) who found that 62.6 per cent of pig farmers in the UK considered that disease prophylaxis warranted antimicrobial usage. Antimicrobial use for disease prevention was quoted by vets and farmers as being administered most often through an in-feed formulation, which accounts for this being the most common route of administration for antimicrobials in pigs in the UK (Stevens and others 2007).
The role of vaccination as an alternative to antimicrobials in disease prevention on pig farms was identified by vets and farmers. Such conclusions are reflected in the findings of Stevens and others (2007) that 80 per cent of pig farmers considered vaccination to be an alternative to antimicrobial usage. Once disease was identified, the vet and farmer groups recognised that diagnostic testing influenced prescribing behaviour in both routine disease surveillance as well as emerging infections. The VMD focus groups did not consider that ‘routine diagnostic testing’ influenced prescribing habits in the pig sector, however, it was acknowledged to be used to investigate novel infections on farms (Sheehan 2013).
The vet focus groups quoted the NOAH Compendium as being their most trusted source of information on antimicrobials to aid prescribing decisions. This agrees with previous research from across the veterinary sector (Hughes and others 2012, 2013, Williams and others 2012). Farmers considered their vet to be the most trustworthy source of information on antimicrobials as is shown by previous research which confirmed the strong reliance that farmers place on vets for information (Lathers 2001, Ruegg 2006, Friedman and others 2007). Advertising by pharmaceutical companies was not considered to influence prescribing behaviour by either the vet or farmer focus groups. This contradicted with the VMD prescribing pressures focus groups with vets, where participants within the pig sector felt that it may influence prescribing (Sheehan 2013).
Overall, vets and farmers felt there was insufficient evidence to prove a decisive link between antimicrobial use in food-producing animals and the development of resistance in human beings. This contrasted with the findings of Stevens and others (2007) that 50 per cent of pig farmers considered that resistance in human beings could be a consequence of antimicrobial use in farm animals. The apparent change to a more defensive stance shown by vets and farmers in this study could reflect increasing media interest, which has attributed blame for antimicrobial resistance in human beings on the intensive livestock sector (Levitt 2011a, Anon 2013b, Harvey 2013), or could be a consequence of the participants selected in this study.
Focus groups are considered to be most useful when they are composed of a balance of different individuals, whereby participants share similar cultural, societal and hierarchical roles, yet are dissimilar enough to elicit a variety of opinions (Krueger 1994, Greenbaum 1998). The purposive sampling employed in this study aimed to achieve this desired diversity by the inclusion of vets and farmers with experience of different pig-rearing systems, with differing levels of job responsibility and from different geographical areas, in an attempt to represent the range and extremes of vets and farmers in the UK pig industry. However, bias in selection may result in participants sitting to the extremities of antimicrobial prescribing patterns and may exclude the majority opinion of pig vets and farmers.
In conclusion, this study was able to elicit the motivations and behaviours behind antimicrobial prescribing practices in pig vets and farmers, providing a degree of complexity that is difficult to achieve through quantitative research methods. Convergent themes were generated both within and across the vet and farmer focus groups, although further exploration of these themes is required over a wider population of pig vets and farmers to provide more detailed evaluation of prescribing behaviours. Such studies are important to help provide the evidence and social context on which to build future policy and education and to develop effective interventions against the overuse or inappropriate use of antimicrobials in pigs.
This study was funded by the Veterinary Medicines Directorate, UK Department for Environment, Food and Rural Affairs (DEFRA). The authors thank the British Pig Executive and Pig Veterinary Society for their assistance in organising the focus groups and all participants contributing to the study.
Provenance: not commissioned; externally peer reviewed
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