Preventive Veterinary Medicine 117 (2014) 68–78

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Preventive Veterinary Medicine

journal homepage: www.elsevier.com/locate/prevetmed

Qualitative study of factors associated with antimicrobial

usage in seven small animal veterinary practices in the UK
Ana L.P. Mateus a,∗ , David C. Brodbelt a , Nick Barber b , Katharina D.C. Stärk a
a
Royal Veterinary College, Veterinary Clinical Sciences Department, Hawkshead Campus, Hawkshead Lane, North Mymms,
Hatfield AL9 7TA, UK
b
UCL School of Pharmacy, Department of Practice and Policy, Centre for Medication Safety and Service Quality, Tavistock (BMA) House,
Tavistock Square, London WC1H 9JP, UK

a r t i c l e i n f o a b s t r a c t

Article history: Responsible use of antimicrobials by veterinarians is essential to contain antimicrobial

Received 12 January 2013 resistance in pathogens relevant to public health. Inappropriate antimicrobial use has been
Received in revised form 17 May 2014 previously described in practice. However, there is scarce information on factors influenc-
Accepted 20 May 2014
ing antimicrobial usage in dogs and cats. We investigated intrinsic and extrinsic factors
influencing decision-making of antimicrobial usage in first opinion small animal practices
Keywords: in the UK through the application of qualitative research methods.
Antimicrobials
Semi-structured interviews were conducted with 21 veterinarians from seven veteri-
Antibiotics
nary first opinion practices in the UK in 2010. Topics investigated included: a) criteria
Small animals
Decision-making used for selection of antimicrobials, b) influences by colleagues, c) influences by clients,
Qualitative d) pet characteristics, e) sources of knowledge, f) awareness of guidelines and g) protocols
Veterinary implemented in practice that may affect antimicrobial usage by veterinarians. Hypothetical
scenarios selected to assess appropriateness of antimicrobial usage were: a) vomiting in a
Yorkshire Terrier due to dietary indiscretion, b) deep pyoderma in a Shar-Pei, c) Feline Lower
Urinary Tract disease in an 7 year-old male neutered cat and d) neutering of a 6-months dog.
Interviews were recorded and transcribed by the interviewer. Thematic analysis was used
to analyse content of transcribed interviews. Data management and analysis was conducted
with qualitative analysis software NVivo8 (QSR International Pty Ltd).
Antimicrobial usage by participants was influenced by factors other than clinical evi-
dence and scientific knowledge. Intrinsic factors included veterinarian’s preference of
substances and previous experience. Extrinsic factors influencing antimicrobial selection
were; perceived efficacy, ease of administration of formulations, perceived compliance,
willingness and ability to treat by pet owners, and animal characteristics. Cost of therapy
was only perceived as an influential factor in low, mixed socioeconomic areas. Veterinari-
ans had limited awareness of current recommendations for responsible use in small animal
practice. Social norms, particularly verbally agreed protocols influenced veterinarians. Inap-
propriate antimicrobial usage was identified in the therapy of non-infectious diseases and
prophylaxis of routine clean surgical procedures.

∗ Corresponding author. Tel.: +44 01707 666528; fax: +44 01707 652090.
E-mail addresses: amateus@rvc.ac.uk (A.L.P. Mateus), dbrodbelt@rvc.ac.uk (D.C. Brodbelt), n.barber@pharmacy.ac.uk (N. Barber), kstaerk@rvc.ac.uk
(K.D.C. Stärk).

http://dx.doi.org/10.1016/j.prevetmed.2014.05.007
0167-5877/© 2014 Elsevier B.V. All rights reserved.
 A.L.P. Mateus et al. / Preventive Veterinary Medicine 117 (2014) 68–78 69

Discussion of clinical cases with peers and effectiveness meetings in the workplace were
useful to veterinarians to share scientific knowledge. Effectiveness meetings can be a com-
mon ground for veterinarians to discuss and agree protocols for clinical conditions and
surgical procedures. Protocols should be evidence-based, follow current recommenda-
tions and take into account the resources available in the workplace. Targeted training
of veterinarians in the workplace with peer support should be used to promote responsible
antimicrobial usage.
© 2014 Elsevier B.V. All rights reserved.

1. Introduction through practice managers and senior partners. One to

Inappropriate and excessive antimicrobial use (AMU)
has been reported in small animal practice (Watson and
Maddison, 2001; Hill et al., 2006; German et al., 2010).
It can cause antimicrobial resistance (AMR) in bacterial
populations with serious implications for both animal and
public health (Guardabassi et al., 2004; Rantala et al., 2004;
Morley et al., 2005). Recent qualitative research studies
show that factors other than scientific knowledge and rec-
ommended guidelines influence practitioners resulting in
inappropriate AMU in humans (Paredes et al., 1996; Carthy
et al., 2000; Coenen et al., 2000; Cantrell et al., 2002;
Trémolières, 2003; de Souza et al., 2006; Barlow et al.,
2008; Cortoos et al., 2008; Altiner et al., 2010; Charani et al.,
2011).
Investigation of decision-making processes in veteri-
nary settings with qualitative methodologies is not novel.
However, research has been focused on the investigation of
attitudes and beliefs towards food safety, biosecurity and
AMU in food-producing animals (Vaarst et al., 2002; Jansen
et al., 2009; Lastein et al., 2009; Ellis-Iversen et al., 2010;
Young et al., 2010). There is an extensive body of qualita-
tive research literature in relation to AMU in humans but to
our knowledge this is limited in small animals (Sahoo et al.,
2010). The majority of the studies currently available use
quantitative methods to assess attitudes of small animal
veterinarians towards AMU (Knights et al., 2012; Pleydell
et al., 2012).
The objective of this study was to identify intrinsic
and extrinsic factors that influence the decision-making
process involved in the selection of AMs by small animal
veterinarians through qualitative methods. Awareness of
current guidelines and appropriateness of AMU in veteri-
nary practice was also investigated.
2. Materials and methods
Approval from the Ethics and Welfare Committee of
the Royal Veterinary College (RVC) was obtained. A conve-
nience sample of veterinarians was recruited from British
practices that had participated in a related RVC project
investigating extent and patterns of AMU (Mateus et al.,
2011). These practices were selected through the Royal
College of Veterinary Surgeons (RCVS) directorate. Crite-
ria for selection were; (a) use of a specific electronic
patient management system (i.e. RxWorks Inc, UK) with a
built-in query for data extraction and (b) provision of vet-
erinary care to small animals. Veterinarians were recruited
six veterinarians were recruited per practice depending
on staff availability. A semi-structured questionnaire was
developed based on the topics described above (see supple-
mentary material). Questions were re-defined throughout
the research process. Four hypothetical case scenarios were
included to investigate appropriateness of AMU (Table 1).
Pilot interviews were conducted in a referral practice
(data not shown) for validation purposes. Ambiguous and
leading questions were modified accordingly based on
the feedback provided. One of the scenarios (i.e. cysti-
tis in a cat) was replaced by Feline Lower Urinary Tract
Disease (FLUTD) and another one was redefined from ‘pyo-
derma’ to ‘deep pyoderma’ in dogs to exclude superficial
pyoderma.
Written consent was obtained from interviewees. Inter-
views were recorded with a digital device (Olympus
DS-2400, UK) and transcribed into Word (Microsoft Office
2007, Microsoft Corporation, USA) by the first author.
Veterinarians were identified during analysis as Fn (where
n ranged between 1 and 21). Veterinary practices were
coded as ‘Pn’ (where n ranged between 1 and 7). Trans-
cripts and memos were transferred into NVivo8 (QSR
International Pty Ltd., UK) for data management and
analysis.
Thematic analysis was used for the purpose of this
study, as it allows both inductive and deductive reasoning
(Boyatzis, 1998; Braun and Clarke, 2006; Pope and Mays,
2006). A “rich thematic description” and interpretation of
the overall data collected to explain the phenomena of
interest through analytical narrative was performed by the
first author (Braun and Clarke, 2006). Themes (e.g. non-
compliance by pet owners, client’s expectations for AM
prescriptions, peer pressure, cost of therapy) were pre-
defined based on current scientific evidence on factors
influencing AMU in humans and food-producing animals
and, to a lesser extent, on small animal’s AMU quantita-
tive studies. This a priori knowledge was used to identify
common themes and patterns across participants (Table 2).
Table 1
Hypothetical case studies used to assess appropriateness of AMU in small
animals by participating veterinarians (n = 21).
1. Acute vomiting in a 14 year-old Yorkshire Terrier caused by diet
indiscretion (i.e. garbage scavenging)
2. Feline Lower Urinary Tract Disease (FLUTD) in a 7 year-old male,
neutered, overweight, indoor cat
3. Deep pyoderma in a male 3 year-old Shar-Pei dog
4. Neutering of a 6 months-old healthy, male dog
70 A.L.P. Mateus et al. / Preventive Veterinary Medicine 117 (2014) 68–78

Table 2
Research topics and factors explored included in the qualitative semi-
structured questionnaire to small animal veterinarians (n = 21).

Research topics and associated factorsa

Selection of antimicrobial (AM) therapy in everyday practice
1. Selection criteria for AMU
a. Previous knowledge
b. Work experience
c. Antimicrobial susceptibility tests (ASTs)
d. Organ affected
e. Potential pathogen involved
f. Animal’s clinical history
g. Clinical signs
h. Licensed for veterinary use
2. Duration of consultations
3. Protocols for AMU in the workplace Fig. 1. Distribution of participating small animal veterinarians by sex and
4. Colleagues at work age group (n = 21).
a. Senior and peer pressure
b. Hierarchical structure of the practice
5. Cost of AM treatment
a. Proportion of clients with pet insurance 3. Results
b. Socioeconomic status of clients
c. Willingness and/or ability to pay AM therapy 3.1. Demographic data
d. Demographic area

Veterinarian-animal-owner relationship- role in the selection of AM Twenty-one veterinarians from seven practices partici-
therapy
pated in this project between January and July 2010. Length
1. Attitudes of pet owners
a. Impact of client compliance in AM selection
of interviews varied between 20 and 55 minutes. Most
b. Importance of communication veterinarians were male (71%) and of British nationality
c. Importance of veterinary-owner relationship (81.0%). Median age of participants was 33 years-old (yo)
d. Previous knowledge of the pet and the owner (range = 25–57 yo) (Fig. 1). Two thirds of the interviewees
Importance of current AM guidelines and recommendations worked in practices located in the West Midlands (n = 7)
1. Knowledge of any recommendations relevant to the veterinarian and in the Greater London areas (n = 7); the remaining
a. Use of BSAVA recommendations in practice worked in the East of England (n = 4), Scotland (n = 2) and
Appropriateness of AMU in hypothetical case scenarios East Anglia (n = 1). Median period since graduation was 10
1. For each case scenario these aspects were explored years (range = 1–34). Most veterinarians were graduates
a. Knowledge of (non) infectious diseases
from British universities (86%). Less than a quarter of the
b. Criteria applied to support or not AM use
c. AM most commonly used per condition participants possessed postgraduate qualifications.
d. Duration of therapy
e. Prophylactic use 3.2. Qualitative analysis
Knowledge of antimicrobials
1. Sources of knowledge Several factors were identified associated with the
a. Pharmaceutical drug companies decision-making process involved in AM selection by veter-
b. Colleagues
c. CPDs
inarians (Fig. 2). This paper focuses on the most relevant
d. Scientific journals factors. Factors were organised in three groups; (a) intrin-
e. Textbooks sic factors (linked to the veterinarian), (b) extrinsic factors
f. Empirical knowledge I (AM characteristics, workplace and colleagues at work)
a
This is not an exhaustive list of factors that were covered during the and (c) extrinsic factors II (characteristics of pet owners
research process. and animals), as described below.

3.2.1. Factors influencing selection of AM for animal

After familiarisation with the content of the transcripts and
memos produced, data were labelled within and between
cases against the pre-established hierarchical nodes (i.e.
themes and associated categories). Relationships between
factors and the development of theories associated with
the decision-making process of interest were investigated
through diagram representation of identified themes and
associated categories. A random sample of four transcribed
interviews, emerging codes and preliminary theoretical
models were revised by one of the authors (Prof Nick
Barber) for validation purposes. Discrepancies in coding,
interpretation of findings and emerging theories were dis-
cussed and adjusted accordingly.
therapy
3.2.1.1. Intrinsic factors.
3.2.1.1.1. Knowledge of (non-)infectious diseases.
Knowledge of infectious diseases influenced veterinarians
assessing clinical conditions and subsequently their AM
selection, as reported by a third of the participants. Seven
interviewees considered selecting AMs for therapy of
non-infectious gastritis if they were in presence of an
elderly animal (e.g. compromised immune system) or if
the owners were “particularly worried”. The most com-
mon AMs selected by participants were amoxicillin and
potentiated amoxicillin. Short-term AM therapies were
frequently administered (i.e. 2–3 days) using long-acting
injectable preparations. Nine interviewees believed FLUTD
 A.L.P. Mateus et al. / Preventive Veterinary Medicine 117 (2014) 68–78
Fig. 2. Intrinsic and extrinsic factors associated with decision-making processes involved in the selection of AM therapy by participants veterinarians
(n = 21) in everyday small animal practice (PK – pharmacokynetics; PD – pharmacodynamics) (NVivo 8, QSR International Pty Ltd., UK).
was of infectious origin and selected AMs accordingly.
Over half of the participants were aware that FLUTD is a
non-infectious condition, associated with environmental
stressors (Westropp et al., 2005; Grauer, 2009). From
these, three supported prophylactic AMU. One of the latter
believed that current scientific evidence was contradic-
tory (Westropp et al., 2005; Eggertsdóttir et al., 2007;
Forrester and Roudebush, 2007; Grauer, 2009) and could
not make an informed decision against AMU. Systemic
use of cephalexin for deep pyoderma was referred by
all veterinarians, according to current recommendations
(Guardabassi et al., 2008). Only one veterinarian con-
sidered use of fluoroquinolones (i.e. marbofloxacin) as
alternative first choice AM. Over half of the veterinarians
referred that they would not consider prophylactic AMU
in routine clean surgeries, in accordance with current
recommendations (BSAVA, 2013). Nine veterinarians
stated using routinely one shot long-acting AM injections
(e.g. amoxicillin and potentiated amoxicillin) in surgery.
Among these, five used AMs without clinical justification.
The remaining four selected AMs in neutering procedures
if a “breach of sterility” was suspected, surgical technique
was poor or if the procedure was prolonged (i.e. >90 min).
Perceived bias of research supported by pharmaceutical
companies, lack of clinical relevance and scarce time to read
scientific journals were perceived by participants as extrin-
sic barriers to knowledge. Lack of time has been previously
reported by practitioners in human medicine as a barrier
to acquire knowledge on AMs (Carthy et al., 2000). Own
intellectual capacity to process information and inability to
critically review scientific papers were identified by inter-
viewees as intrinsic barriers.
71
3.2.1.1.2. Personal preference of AM. Personal prefer-
ence was influential in the selection of first line therapy of
common conditions, as reported by over half of the inter-
viewees: “I always use the same sort of things for the same
type of problems. For skin, I always use a second generation
cephalosporin [cephalexin]. First choice for pulmonary prob-
lems I always use doxycycline (. . .). For dental issues, I tend
to use (. . .) clavulanic acid, potentiated amoxicillin. So I have
nearly protocols just based on the types of bacteria that I might
think are causing the problem” (F10, P5, 33 yo). In a study in
Sweden, selection of commercial versus generic prepara-
tions by healthcare professionals was also influenced by
personal preference and cost (Lundin, 2000).
3.2.1.1.3. Work experience. Veterinarians reported
selecting AMs based on past positive experiences (e.g.
resolution of clinical condition). Participants were risk-
adverse when considering negative aspects of substances
(e.g. adverse effects): “Well, it is easier to prescribe quickly
an antibiotic that I have used thousands of times before and
so I usually get into just dolling out the one that I know it is
easy. (. . .) I think if I have used a drug many times without
having problems associated with it, then I would tend to
stick with it” (F13, P6, 33 yo). Often veterinarians stated
that they were less likely to use AMs that were outside
their “comfort zone” (i.e. no previous experience using the
substance or lack of knowledge of).
One of the veterinarians observed that cats with FLUTD
treated empirically with AMs appeared to improve faster
than cats on symptomatic therapy, based on his work
experience. This was despite his awareness that current
scientific knowledge and practice protocols were against
AMU, resulting in unnecessary use.
72 A.L.P. Mateus et al. / Preventive Veterinary Medicine 117 (2014) 68–78
3.2.1.1.4. “Business” perception. Only three of the par-
ticipants had a strong perception of provision of veterinary
services as a “business”. They felt the need to meet
the client’s expectations (“client satisfaction”), due to the
perceived risk of losing them to other practices. The act of
prescription as a source of income was raised by two veter-
inarians; however, this was not considered a major driver
for AM selection in this study.
3.2.2. Extrinsic factors I
3.2.2.1. AM substances.
3.2.2.1.1. Perceived efficacy. Veterinarians stated that
their AM selection was influenced by the tissue, organ or
body system affected. Whenever possible, the substance
perceived to be the most efficacious against the most likely
microorganism involved was selected as stated by eleven
of the interviewees.
3.2.2.1.2. Spectrum of action. Most of the interviewees
preferred broad-spectrum over narrow AMs: “Every case
that I have to look at I try and head on that direction if anything
else I don’t often reach for it as a first port of call because often
if they [the animals] come in, they have got an infection and
it needs treatment, you know, realistically, you can’t wait for
culture and [antimicrobial] sensitivity [testing] [AST] results,
you need to put them on something broad spectrum any-
way” (F14, P6, 25 yo). This was also supported by F1 (P1,
46 yo): “On the back of that we tend to use broad spectrum
antibiotics because we don’t know exactly which bacteria
we are treating”. Perceived higher efficacy and uncertainty
of diagnosis were the reasons most frequently mentioned
by veterinarians for the selection of broad spectrum sub-
stances. Over half of the interviewees stated they often
selected AMs without a confirmed diagnosis, based only on
clinical examination findings. Uncertainty was also exac-
erbated when veterinarians were not able to rule out the
presence of infection. In these situations, participants men-
tioned they were likely to select AM as a “trial and error”
strategy: “But if they said either ‘No, I cannot afford the bloods’
or ‘I can’t bring it back until a week on Thursday’ then actu-
ally I probably would put it in antibiotics because that would
be me thinking ‘Well, I have got to do something’, to some
extent, you know, is not going to make the problem worst and
it might just make things better” (F3, P2, 40 yo). Similarly,
in human medicine when practitioners cannot differenti-
ate between conditions (e.g. bronchitis and pneumonia),
diagnosis uncertainty has resulted in unnecessary AMU
(Coenen et al., 2000).
3.2.2.1.3. Type of preparation and ease of administration.
Selection of a particular formulation was influenced often
by ease and route of administration: “Well, I suppose method
of [route of] administration (. . .) and ease of administration.
To ensure compliance. I mean, I obviously want to pick the
antibiotic for what I’m treating but I also have to pick one that
I think I’m going to get a big compliance. I think it is a balance
between the two” (F15, P5, 26 yo). The formulations pre-
ferred by veterinarians were injectable, as these ensured
that the animal received the complete course of treatment.
Use of long-acting preparations (e.g. 14 days duration) con-
taining third-generation cephalosporins (e.g. cefovecin)
was frequently mentioned by participants. Their use was
extended to the therapy of non-infectious (e.g. FLUTD)
and infectious diseases (e.g. urinary tract infections or
UTIs) for which long-term therapy is currently not recom-
mended (BSAVA, 2013). Third-generation cephalosporins
are deemed as critically important in human medicine
and are used as last resort treatment of life-threatening
conditions caused by multi-resistant pathogens (WHO,
2012). Excessively prolonged AMU could lead to selec-
tive pressure in bacterial populations and to increased
risk of carriage of resistant bacteria. Carriage of penicillin-
resistant Streptococcus pneumoniae has been observed in
children treated for prolonged periods with beta-lactams
(Guillemot et al., 1998; Niederman, 2005). Tablet size was
also discussed by veterinarians, as appropriate dosing for
the weight of the animal may not always be possible for
the substance initially selected consequently affecting AM
selection.
3.2.2.1.4. Drug availability. Veterinarians were often
restricted to AM formulations available in their work-
place. This could lead to the selection of substances that
would not have been their first choice. In some prac-
tices, veterinarians were able to order other AM substances
or formulations in a case-by-case basis if animal welfare
was compromised after approval by partners and practice
managers.
3.2.2.1.5. Duration of AM therapy. Length of AM therapy
was variable; it was decided by the veterinarian accord-
ing to the condition and its progression over time. Cost
of check-up consultations was a barrier to the decision-
making process as it affected the assessment of therapeutic
success. Veterinarians stated that often pet owners did
not return for follow-up consultations. This occurred if the
animal was perceived to be recovering by the client or if
he/she was not willing or able to pay for the cost of the
consultation.
3.2.2.1.6. Cost of therapy. Selection of AM substances
was markedly influenced by cost of therapy as stated by
seven of the interviewees that worked in areas where
clients of low (n = 1) and mixed socioeconomic status pre-
dominated (n = 16). These clinicians reported that a large
number of pet owners received benefits or were pension-
ers; only a small proportion of owners (6–8%) had pet
insurance, in contrast with veterinarians working in afflu-
ent areas (approximately 75% insurance coverage) (data
not shown). For the latter (n = 4), therapy cost was not
an influential factor in AM selection. Nevertheless, most
veterinarians stated that they offered the same therapeutic
options to all pet owners independently of their socio-
economic background. Discussion of cost of therapeutic
options should be included as part of the consultation as
lack of communication on this subject has been an issue
previously reported by pet owners in a study by Coe et al.
assessing communication of monetary aspects of veteri-
nary care (Coe et al., 2007).
3.2.2.2. Workplace.
3.2.2.2.1. Hierarchical structure and professional rela-
tionships. In human medicine, formal hierarchy between
practitioners is often observed. Junior practitioners tend to
follow instructions from senior colleagues when selecting
AMs, even when aware that these are not in accor-
dance with current recommendations (de Souza et al.,
 A.L.P. Mateus et al. / Preventive Veterinary Medicine 117 (2014) 68–78 73

2006). Relationships between veterinarians as reported by Table 3

Common conditions for which veterinarians stated they would consider
interviewees tended to be more informal. Support and
using ASTs to guide AM selection for therapy of small animal (n = 21).
mentoring by senior colleagues was provided and appeared
to be particularly important to recent graduates. This Common conditions Common situations
has also been described in a recent survey in Australia All species Non healing wounds Treatment failure
where 82% of young graduates working in practice affirmed Infected surgical Assessment of
receiving good support in their workplaces (Heath, 2008). wounds treatment efficacy
Purulent joint Selection of AM in the
Veterinarians did not feel influenced by colleagues dur-
infections presence of adverse
ing AM selection. Nevertheless, indirect influences were reactions to first choice
observed when advice was sought during discussion of substances
clinical cases. Veterinarians also mentioned that they often Non-healing corneal
checked therapy previously prescribed by colleagues when ulcerations
Conjuntivitis
dealing with complex clinical cases or when revising ani- Abnormal nasal
mal history during consultation in order to guide their discharges
decision-making. Haemorrhagic and
3.2.2.2.2. Attitudes of senior and junior veterinarians chronic diarrhoea
towards AMU. Most of the older participants were aware Dogs Otitis externa
of using AMs more frequently than recent graduates. This “nasty” or unusual skin
was associated by the former with differences in the under- conditions
UTIs
graduate training received and with accumulated work
experience: “Because I think that now they are taught more Cats FLUTD
Blocked bladder
in college now and it [AMR] is more in the public eye and in
the veterinary press to avoid using antibacterials in circum-
stances where I would use them and that has to be training the relationships between veterinarians and agreed non-
and experience that probably make me approach cases like verbal protocols with colleagues. Effectiveness meetings
that. Their training and I would say their experience or what- can be used to monitor inappropriate AMU and to imple-
ever is probably less than mine because they are younger ment corrective actions accordingly, to identify training
and, you know, pushes them away from AMU” (F4, P3, 38 yo) needs and raise awareness for AMR and responsible AMU
and “I know particularly how in young graduates working in a supportive environment.
in the practice, the emphasis appears in the education now 3.2.2.2.4. Diagnostic tests. The most frequently used
is more on problem-solving than is necessarily on experience tests by participants to support diagnosis and AM selection
because again your experience can foul you sometimes, but, were; urinalysis, cytology and gram-staining for micro-
yeah, given that I’m a little bit older now, I think experience scopic examination. These tests had the advantage of
is quite an important thing” (F9, P5, 44 yo). Younger veter- being readily available in the workplace and were of low
inarians resorted to the knowledge acquired during their cost to pet owners compared to ASTs. ASTs were recom-
undergraduate training to support their decision-making: mended only when in the presence of specific conditions
“Most of it is from knowledge from vet school, because we and situations (Table 3). However, cytology and ASTs were
can look back at our notes, our clinical notes, discussing with rarely performed (‘fail to action’) due to extrinsic barriers
the other vets, I’ll probably have experience from other cases (Table 4). Most of the veterinarians stated they prescribed
that I had as well, how the animals have responded and just AMs while waiting for AST results which made it difficult
chatting to the colleagues” (F7, P4, 26 yo). Some of the inter- to justify the additional cost to pet owners: “It is difficult to
viewees reported changing their prescribing behaviour persuade owners to take samples at the onset (. . .). Because I
over the years. They associated this with acquired scien- think they want a fix quickly rather than, you know, fiddling
tific knowledge and with the discussion of clinical cases around, doing more diagnostics and more sort of time (. . .).
and therapeutic protocols with younger colleagues in the They rather take the antibiotics and go home than to have
workplace. to come in, wait for samples” (F11, P6, 25 yo). Pet owners
3.2.2.2.3. Influence of staff effectiveness meetings. Par- may not want to pay for diagnostic tests if they are not
ticipants mentioned being influenced by issues discussed aware of its relevance in the selection of AMs (‘perceived
during staff meetings: “Otherwise, we have regular clinical value’). On the other hand, pet owners may be aware of
effectiveness meetings (. . .) and if anyone has new informa- it, but may not be able to afford these due to financial
tion or anything that they want to discuss about antibiotics or constraints. Gram-staining can be used as a quicker and
about protocols, that’s where they would come up and, yeah,
I would be highly influenced in that kind of environment if
Table 4
somebody came with papers and evidence and we would dis- Extrinsic barriers identified to use of ASTs to support decision-making in
cuss it, then yeah, that would often change what I do” (F15, P5, practice reported by participants in this study (n = 21).
26 yo). During these, veterinarians agreed upon and revised
Barriers to ASTs
non-written protocols for first line AM therapy of common 1. Willingness or ability of clients to pay
conditions and surgical prophylaxis (“social norms”). Social 2. Duration of consultation
norms are “rules that govern ordinary or non-contractual 3. Difficult access to infection site for sample collection
interactions among members of a community” (McDonnell, 4. Time delay for diagnostic results
5. Attitudes of clients towards diagnostic tests
2008). In this study, “social norms” were represented by
74 A.L.P. Mateus et al. / Preventive Veterinary Medicine 117 (2014) 68–78
cheaper alternative to ASTs in small animal practice. In
Japan, gram-staining was used to guide empirical AMU of
patients with suspect bacteraemia, improving responsible
use (Uehara et al., 2009). However, gram-staining requires
that the practitioner is trained properly in its use and in the
identification of microorganisms; incorrect diagnosis may
result in inadequate AM selection.
3.2.2.2.5. Length of consultation. Consultations report-
edly varied between 10 and 20 min. This is similar to a
recent study in England where mean duration time of con-
sultations was 14 min (Everitt et al., 2013). Lack of time
during consultation was commonly described as a barrier
to conduct further clinical investigations even when lab-
oratorial facilities and equipment were available: “Yes, we
do have a lab here, yes, with a microscope and we have a
Dif-Quick stain and some things. So that can be used for ears
[diagnostic of ear bacterial and fungal infections] but in
reality we only have 15 minutes to see an animal, make your
decisions and send it out the door, you don’t have time to
do a lot of cytology and things and it is something that I did
more perhaps when I started, here. (. . .) I don’t really have the
time and we end up putting them on the same thing anyway”
(F14, P6, 25 yo). This has also been associated in healthcare
systems with the overuse of AMs by practitioners treat-
ing patients with upper respiratory tract infections (Linder
et al., 2003). Allocation of longer consultation times for
new clinical conditions should be considered (Everitt et al.,
2013), to allow the veterinarian to collect sufficient evi-
dence to support their decision-making on the therapeutic
plan to follow.
3.2.2.2.6. Awareness of recommendations for responsible
usage of AMs. Many of the interviewees were unaware of
current recommendations in the UK (e.g. BSAVA and British
Veterinary Association or BVA). Recommendations – if
known – were considered to be difficult to implement and
of limited use in everyday practice. Only a small number of
veterinarians perceived current guidelines as a reminder
of best practice. This has also been previously described
in human practitioners, where poor knowledge of imple-
mented formularies and other strategies in the workplace
led to inappropriate AMU (Woodford et al., 2004). Fear of
losing clinical autonomy could act as a barrier for the imple-
mentation of protocols and recommendations as stated by
some of the interviewees. In a survey of Dutch dentists,
approximately half of the respondents (n = 1774) found that
recommendations were a useful tool to support decision-
making when dealing with complex clinical cases (van der
Sanden et al., 2003). However, the same practitioners did
not perceive the need for recommendations in everyday
practice (van der Sanden et al., 2003). Specific guidelines for
the responsible use of medicines in small animals are cur-
rently available to veterinarians in the UK (BSAVA, 2013).
However, there are presently no data on the level of imple-
mentation and effectiveness of existing guidelines.
3.2.2.2.7. Effectiveness of AMU written protocols.
Approximately half of the interviewees worked in prac-
tices with written protocols. However from these, half
were unaware of the protocols implemented in their
workplaces. It emerged protocols were not properly
implemented or introduced to new staff during induction.
Generally, veterinarians felt that they were given freedom
of choice in their workplaces when selecting AMs: “We
have free rein in what we do clinically, generally speaking
(. . .). I can do what I choose and there is no set policy on
AMU” (F13, P6, 32 yo). Veterinarians valued their autonomy
when selecting AM therapy. Many of the veterinarians did
not acknowledge a need for protocols.
3.2.3. Extrinsic factors II
3.2.3.1. Owner characteristics.
3.2.3.1.1. Perceived compliance. Compliance is defined
as “the extent to which the patient’s behaviour matches the
prescriber’s recommendations” (Horne et al., 2005). Poor
compliance was reported in the administration of tablets
to cats and aggressive animals, topical otic preparations
in dogs and long-term therapies (e.g. deep pyoderma in
dogs). The latter is supported by a study in Canada with
dog owners, where compliance was estimated to be higher
for short-term oral AM therapies with dosing frequencies
of one to two times a day compared to long-term thera-
pies and higher dosing frequencies (Adams et al., 2005). For
the participants, it was essential to have owners “on-board”
to avoid therapeutic failure. To deal with non-compliance,
veterinarians either, recurred to advice, trained owners in
the administration of therapy or changed their first choice
AM. Most of the veterinarians mentioned that they were
more likely to use long-acting injectable preparations with
owners that were not able to administer tablets to ensure
that animals would receive the complete therapy course.
All but one of the veterinarians interviewed used long-
acting third-generation cephalosporins to treat empirically
common conditions in cats: “One injection [of cefovecin] in
the consulting room, two weeks cover antibiotics, the owners
don’t have to tablet their cats, we are ensured that the cats got
the treatment, it is just so. . . And when we are down to the size
of the cat, it is not costly either. So I think that is compliance
and convenience is a major decision as well” (F1, P1, 46 yo).
The same veterinarian referred to a change of pattern of
AMU in cats since cefovecin was licensed for veterinary use:
“I would say it [dispensation of oral formulations] has proba-
bly halved, if not more. We used to sell, on average, well, 2,500
tablets [of amoxicillin plus clavulanic acid] (. . .). In 2006
we sold 1,700, in 2007 1,000, and presumably [cefovecin] X
was to come out in 2007 and in 2008, 560 [tablets]”. The use
of these preparations also satisfied the perceived expec-
tations of the pet owners. However, two veterinarians
reported “downsides” to the use of long-acting prepara-
tions. Difficulty to control occurrence of adverse reactions
and risk of AMR were mentioned. In medium and large size
dogs, cefovecin was not commonly selected due to its high
cost and the availability of cheaper substances.
3.2.3.1.2. Willingness or ability to pay AM therapy.
Perceived ability or willingness to administer AM ther-
apy by pet owners influenced veterinarians when selecting
type of formulation and therefore, of the substance. If the
owner expressed that they could not afford or were not
willing to pay, veterinarians stated they would consider
changing their first choice of substance to a cheaper option
that might not have been as effective. Willingness to pay or
treat was associated by the veterinarians with the strength
of the bond between the client and their animal. Many
owners consider their animals as family members and this
 A.L.P. Mateus et al. / Preventive Veterinary Medicine 117 (2014) 68–78
often is reflected in the level of veterinary care that they
are willing to provide (Lund et al., 2009). In a qualitative
research study by Coe et al. (2007), pet owners prioritised
veterinary care over monetary costs. The strength of the
bond between the animal and its owner will dictate to some
extent the expectations and pressure imposed upon the
veterinarian.
3.2.3.1.3. Pressure and expectations. In our study, a con-
flict was identified between the perceived expectations of
pet owners (e.g. cheap veterinary care and “quick fix” of
the animal’s condition) and what veterinarians perceived
they should be doing (‘intent of action’ and ‘professional
role’). These may lead the veterinarian to behave in some
circumstances against his/her intent of action based on
beliefs, scientific knowledge, training or current recom-
mendations. In Denmark, general practitioners stated that
they were sensitive to pressure by patients and how
they reacted to their prescriptions (Henriksen and Hansen,
2004). Perception of client expectations may have an effect
in the act of prescribing particularly if the individual has
low levels of confidence and limited clinical experience
(‘perception of self ’) (Henriksen and Hansen, 2004). Ethi-
cal issues may rise if the veterinarian is aware of the risk of
therapeutic failure and its negative impact on the animal’s
health and welfare. Two thirds of the interviewees affirmed
suffering pressure from pet owners to prescribe AMs dur-
ing consultation. However, most veterinarians stated they
did not yield to owner’s expectations. Participants felt con-
fident of their clinical expertise to convoy their findings and
therapeutic plan to clients. This was linked to the relation-
ship and degree of trust established. Three veterinarians
stated that they occasionally bent to client’s expectations.
This could lead to the prescription of less suitable formu-
lations or less effective substances. Veterinarians indicated
that sometimes they dealt with owner’s expectations by
prescribing non-AM drugs that were beneficial to the ani-
mal and involved actively the client in the care of their pet:
“When you say prescribing, I think things like, other therapies,
for example, sending a dog with diarrhoea instead of giving it
metronidazole sending it home with on a probiotic and binder
(. . .). The owner feels like they are giving it, a medication in
commas but it is nothing that will cause any negative effects
on the animal or on the general population. Likewise, with
simple wounds, getting the client to bath him, again I’m not
really prescribing anything but I’m telling them to be actively
involved in the welfare of their pet which tends to do the job,
I think” (F15, P5, 26 yo).
3.2.3.1.4. Owner’s experience with AMs. If pet owners
reported previous negative experiences with AMs, the
veterinarian was less likely to select the same substance,
as was stated by five of the participants: “Obviously if there
has been a dog there that had that tablet before and it has
been sick on that tablet, then owners will not want back that
tablet, you will have to use something else, so . . . it depends
how the animals have reacted in the past as well to what
you use as well” (F2, P1, 27 yo) and: “You know, you have
got to consult them and say “Well, he might have an allergic
reaction, the itching like you had but it is not always going to
be like that. Sometimes, some people can be adamant and say
‘Well, no penicillins can be given to my dog because it nearly
killed me”’ (F16, P4, 32 yo).
75
3.2.4. Animal characteristics
3.2.4.1. Previous clinical history. When dealing with recur-
rent infections, most participants referred that if a therapy
had been effective in the past they were more likely to
select it again, without further diagnostic tests unless treat-
ment failure was observed: “I wouldn’t suddenly change it
to another drug certainly, if it has worked previously. I mean,
obviously, there is a chance that its former flora has changed,
so it might not work this time. But, you know, I would go on
that, yes. Similarly, ear [otitis media] are another one that
tend to recur a lot and if it is a suitable time period, once
a year, twice a year, three times a year I might think ‘Well,
we can repeat it’ but if it is just been last week and it is not
working then I would, based on the history, I would think to
start doing a swab for instance rather than just giving antibi-
otics again and again and again. So, previous history of the
patient, know the patient, yes” (F20, P7, 35 yo). In recurrent
FLUTD cases, some veterinarians stated that they were less
likely to use AMs, if previous history was known. If this
was not the case, AMU would be considered due to the lack
of evidence against presence of infection, as stated by one
veterinarian.
3.2.4.2. Animal species and associated behaviour. Inability
to give tablets and oral preparations in cats was mainly
associated with behavioural issues but it was not found
to be a major issue in dogs, unless when dealing with
aggressive animals. This could result in non-compliance
and often led to a change of oral to injectable preparations,
as described above.
3.2.4.3. Weight. In large dogs, selection of AM was influ-
enced by cost, particularly when considering long-term
therapies: “(. . .) I mean, there might be a big dog with a
skin infection where maybe you want to use cephalexin but
it is a really big dog it might be an issue, it may be cheaper
to try them on trimethoprim-sulphonamides or amoxicillin
and then, if that doesn’t work obviously change the antibiotic.
So, for bigger dogs it will be cheaper to use something else”
(F7, P4, 26 yo). For heavier, large breed dogs, there could be
the risk of therapeutic failure and adverse reactions, if the
cheaper therapy was less efficacious and less safe than the
first choice substance initially selected by the veterinarian.
3.2.4.4. Age. Animal age influenced veterinarians when
evaluating the risk of adverse reactions. This was linked
to the a priori knowledge of the substance by the clinician:
“I mean, age kind of affect which antibiotic you use, you will
not give puppies any X [oxytetracycline] if you can avoid it
or Y [enrofloxacin] (. . .). X [oxytetracycline] they get yellow
teeth and Y [enrofloxacin] because it knackers the growth
plates” (F6, P4, 28 yo). However, if the implied benefits to
the animal were considered to be more important than the
perceived risk of adverse reactions, substances not usually
recommended would be selected, as referred by F21 (P7,
34 yo): “(. . .) because of its age [a puppy] I wouldn’t nor-
mally use doxycycline because of the (. . .) side effects [on teeth
growth] and stuff but we have learned from experience using
something like, trimethoprim-sulfa or amoxicillin-clavulanic
acid just doesn’t seem to work (. . .) [against] that [particular]
strain [of Bordetella bronchiseptica], it is pretty nasty”. In this
76 A.L.P. Mateus et al. / Preventive Veterinary Medicine 117 (2014) 68–78
particular case, previous work experience and potential
health benefits had a higher impact in the decision-making
process than scientific knowledge of potential adverse
effects of the substance.
3.2.4.5. Clinical signs. Presence of pyrexia was perceived
as an indicator of infection and influenced AM selection.
AMs were believed to have an anti-inflammatory effect by
at least one of the participants (F6, P4, 28 yo). However,
only a few AMs (i.e. tetracyclines) have anti-inflammatory
properties (Giguere, 2007). Pyrexia has been identified in
previous studies as a influencing factor for AM prescrip-
tion in humans (Altiner et al., 2010). However, pyrexia
can be non-bacterial in origin and observed in animals
with haemoparasitosis, mycotic, immune-mediated, neo-
plasic, metabolic conditions, be of idiopathic nature or
occur due AMU itself (Couto, 2008). Other clinical signs
reported by interviewees included; haematochezia, hae-
matemesis, haematuria, reactive lymph nodes, toxic shock,
vomiting and diarrhoea, blocked bladder and depression.
These could result in unnecessary AMU if incorrect diag-
nosis or a bacterial component cannot be ruled out by the
veterinarian.
4. Discussion
This was the first study applying qualitative research
that investigated influences and barriers faced by veter-
inarians related to AMU in small animal therapy in the
UK. Although this study only included 21 veterinarians, it
produced a substantial amount of data regarding factors
involved in the decision-making process of AMU that had
not been previously investigated. Caution in the general-
isation of findings of this study to the overall veterinary
profession in the UK should be taken, as situations and
dynamics of decision-making processes can vary across
practices. Nevertheless, this study offers a first insight
into attitudes and behaviours of participating veterinarians
towards AMU that should not be overlooked.
Thematic analysis is frequently used as a descrip-
tive qualitative tool in conjunction with other qualitative
research methods but not as a qualitative research method
per se (Boyatzis, 1998). We adopted Braun and Clarke’s
approach (Braun and Clarke, 2006) and used thematic anal-
ysis as a research method in this study. We focused on
the overall descriptive analysis of the process of inter-
est and provide an interpretation of the findings in the
context of current scientific evidence (Braun and Clarke,
2006). The findings of this research supported most of the
pre-defined themes based on current scientific literature
(Fig. 2). Furthermore, analysis of the raw data also allowed
the identification of new themes and sub-themes inherent
to the decision-making process of interest in an inductive
process, somewhat similar to grounded theory (Braun and
Clarke, 2006; Corbin and Strauss, 2008).
The decision-making process involved in the selection
of AM in small animal practice is complex. In human
healthcare systems, beliefs and attitudes not associated
with scientific knowledge and guidelines influence the
decision-making involved in AM selection (Paredes et al.,
1996; Coenen et al., 2000; Cantrell et al., 2002; de Souza
et al., 2006; Hancock and Easen, 2006). Similar results were
observed in our study. Extrinsic factors, such as willing-
ness and ability of pet owners to pay and/or to administer
AM (compliance) were found to influence greatly substance
selection. Cost of therapy was found to be highly influen-
tial in the decision-making process but only in practices
located in areas with low, mixed socioeconomic status,
with large, heavy dogs and long-term therapies. Interest-
ingly, peer pressure was not a key factor in AM selection,
as observed in human medicine (de Souza et al., 2006). Par-
ticipants were influenced by social norms such as agreed
verbal protocols for AMU in common conditions.
Perception of veterinary practice as a “business” was
only raised by a few participants. Nevertheless, this could
have an impact on the decision to prescribe or administer
AM to satisfy client’s expectations and result in exces-
sive AMU. Profit of AM sales was not assessed in this
study and it is one of its limitations. Grave et al. reported
that this factor may also influence AMU by veterinarians
and therefore should be further investigated (Grave and
Wegener, 2006). Conflict between best practice and AM
selection by veterinarians was observed. Personal beliefs,
based on work experience may influence AMU behaviour
against social norms, scientific knowledge, protocols or
current recommendations for responsible AMU. Causes for
non-compliance by pet owners were assessed indirectly
through the beliefs of the participants. It was not possi-
ble to discuss these findings with pet owners as this was
not the scope of this study.
Discussion of hypothetical scenarios with the partici-
pants was useful to identify factors influencing selection
of animal therapy and inadequate AMU. Action should
be taken to raise awareness of veterinarians for the
potential risk for society resultant from AMU in everyday
practice. Targeted training of veterinarians in the work-
place through CPDs, effectiveness meetings, seminars or
mentoring schemes in the workplace could also be used
to promote responsible AMU and raise AMR awareness.
Protocols ought to be evidence-based but should also
take into account resources available in the workplace
(Morley et al., 2005). Furthermore, we recommend that
veterinarians take a more active role in educating pet
owners to comply with prescribed therapy in order to
reduce the occurrence of therapeutic failure and AMR.
The findings in this study were novel its kind and
supported the feasibility of qualitative methods in small
animal research. Findings of qualitative research can be
used to inform policy makers upon factors that influence
prescribing behaviour of veterinarians and help to improve
effectiveness of current guidelines for responsible AMU.
Funding
This research project was funded partially by a grant of
the Central Research Fund of the University of London (Ref:
AR/CRF/B). This funding body did not have any influence
at any stage of this research project. Ana L. P. Mateus was
funded by a joint internal PhD scholarship from the Royal
Veterinary College and the School of Pharmacy (University
of London).
 A.L.P. Mateus et al. / Preventive Veterinary Medicine 117 (2014) 68–78
Submission declaration
This research study has not been published previously
elsewhere.
Conflicts of interest
None to declare.
Acknowledgements
The authors would wish to thank all of the veterinarians
and veterinary practices that participated in this study and
the Central Research Fund of the University of London for
supporting the project.
Appendix A. Supplementary data
Supplementary data associated with this article can be
found, in the online version, at http://dx.doi.org/10.1016/
j.prevetmed.2014.05.007.
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