Preventive Veterinary Medicine 188 (2021) 105253

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Preventive Veterinary Medicine

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Survey of perceptions and attitudes of an international group of

veterinarians regarding antibiotic use and resistance on dairy cattle farms
Sebastian G. Llanos-Soto a, *, Neil Vezeau a, Michelle Wemette a, Ece Bulut a,
Amelia Greiner Safi a, b, Paolo Moroni a, c, Michael A. Shapiro b, Renata Ivanek a
a
Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY, 14853, USA
b
Department of Communication, College of Agriculture and Life Sciences, Ithaca, NY, 14853, USA
c
Università degli Studi di Milano, Dipartimento di Medicina Veterinaria, Milan, Italy

A R T I C L E I N F O A B S T R A C T

Keywords: Veterinarians are the main source of information for farmers regarding the responsible use of antibiotics in farm
Antibiotic resistance animals and how to reduce the risk of antibiotic resistance. Consequently, understanding how veterinarians
Perceptions perceive their clients’ and colleagues’ antibiotic use and their own beliefs about the development of antibiotic
Dairy farm
resistance is essential to determining areas in which antibiotic use practices can be improved to minimize the
Antibiotic prescribing
emergence of antibiotic resistance. An international cross-sectional study was carried out using a questionnaire
Thematic analysis
Veterinary medicine designed to elucidate perceptions, attitudes, and concerns of dairy veterinarians regarding antibiotic use and the
emergence of antibiotic resistance in dairy farming. The questionnaire was initially administered to veterinarians
attending the International Bovine Mastitis Conference in Milano, Italy, 2018, followed by veterinarian members
of the National Mastitis Council, and all conference registrants. A total of 71 participants from 21 countries
participated in the survey, the majority were from the United States and member countries of the European
Union. Logistic regression analysis was conducted to identify predictors of veterinarians’ level of concern about
the development of antibiotic resistance on their clients’ farms. Associations were described with odds ratios
(ORs) and the associated 95 % confidence intervals (95 % CIs). Free text responses where participants shared
their views on the reason for overprescribing antibiotics by veterinarians were analyzed using thematic analysis.
Participants perceived that nearly half of their clients overuse or inappropriately use antibiotics, and nearly half
of their colleagues overprescribe or inappropriately prescribe antibiotics. After controlling for other factors, the
odds of veterinarians being concerned about antibiotic resistance on dairy farms they served decreased by a
factor of 0.91 for each additional year of participants’ experience working with dairy cattle (OR = 0.91, 95 % CI
= 0.84− 0.99). Participants concerned about antibiotic resistance on clients’ dairy farms were also more likely to
consider better adherence to drug labelling as important for reducing farmers’ antibiotic use (OR = 6.86, 95 % CI
= 1.21–38.93). Thematic analysis revealed four themes surrounding the perceived reasons for veterinarians’
overprescribing of antibiotics: (i) knowledge, (ii) attitudes, (iii) barriers, and (iv) rules and regulations. The study
findings will aid in the development of strategies to improve antibiotic use in dairy farming and educational
initiatives looking to enhance the communication between veterinarians and farmers about judicious use of
antibiotics.

1. Introduction (Oliver et al., 2011; Prestinaci et al., 2015; Lhermie et al., 2017).
Resistant organisms spreading in the environment have been recognized
Overuse and inappropriate antibiotic use in livestock have the po­ for their role in human health risks (Manaia, 2017), while antibiotic
tential to influence the emergence of antibiotic resistant commensals residues promote the emergence of antibiotic resistant bacteria in the
and pathogens in animals (Stanton, 2013; Prestinaci et al., 2015). environment through selective pressure (Ben et al., 2019). Therefore, it
Emergence of antibiotic resistant pathogens can increase the morbidity is important that appropriate antibiotic use protocols are rigorously
and mortality of infections, limiting veterinary treatment options followed by farmers and veterinarians in order to prevent the

* Corresponding author at: College of Veterinary Medicine, Cornell University, 602 Tower Rd, Ithaca, NY, 14853, USA.
E-mail address: sgl67@[Link] (S.G. Llanos-Soto).

[Link]
Received 22 August 2020; Received in revised form 17 December 2020; Accepted 23 December 2020
Available online 15 January 2021
0167-5877/© 2021 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license
([Link]
S.G. Llanos-Soto et al. Preventive Veterinary Medicine 188 (2021) 105253

development of antibiotic resistant bacteria on dairy farms and, through 2. Materials and methods
that, protect animals, humans, and the environment in the context of
One Health (Robinson et al., 2016). This holds although the extent of 2.1. Survey design
adverse impacts on One Health from antibiotic use in dairy farming is
currently unknown (Oliver et al., 2011). A cross-sectional study of dairy veterinarians from different coun­
Numerous national and international efforts by government and non- tries was conducted using a questionnaire survey. The questionnaire was
governmental organizations are underway to establish guidelines and implemented using the online Qualtrics survey platform (Qualtrics,
recommendations aimed at preventing and reducing the occurrence of Provo, UT) and was also available in a paper-based format; Table 1
antibiotic resistant bacteria in animal production systems, including on shows the survey questions considered in statistical and thematic anal­
dairy cattle farms (FDA, 2012; 2013; EC, 2015; 2018a; 2018b; FDA, ysis (the whole survey is included in the Supplementary Material).
2015; WHO, 2017). Current regulations are not homogenous between Veterinarians who have been working with dairy cattle in clinical
countries. For example, antibiotic use regulations differ between two practice over the past year were eligible to participate. The survey was
large geopolitical entities and major dairy milk producers, the United piloted by two veterinarians in clinical dairy practice and revised based
States (US) and European Union (EU). For instance, in January 2017, the on their feedback. Considering the preliminary nature of the investiga­
US Food and Drug Administration (FDA) finished implementation of tion, power-based sample size calculation could not be conducted.
Guidance for Industry #213, bringing the use of medically important
antibiotics in feed or water for the treatment, control, and prevention of 2.2. Data collection and management
diseases under veterinary oversight and eliminating the use of medically
important antibiotics for growth promotion (FDA, 2013; 2015). Mean­ The study was approved by the Cornell University Institutional Re­
while, the EU has recently issued strict regulations to prohibit the view Board for Human Participants (IRB protocol #1805008010). Par­
administration of antibiotics as a preventive measure, limit their meta­ ticipants’ responses were anonymous and confidentiality was assured.
phylactic application, and establish a mandatory requirement for The survey was administered in three venues. First, veterinarians
member countries to gather data about the sale and use of antibiotics attending the International Bovine Mastitis Conference in Milano, Italy,
(Europe Commission (EC, 2018a; 2018b). The differences in regulations 2018 (which was organized by the University of Milan), were invited to
and their timing might influence or be a reflection of the prevailing complete either a paper-based survey at the conference (June 11 and 12,
culture and beliefs among farmers and veterinarians working in these 2018) or an online Qualtrics survey (from June 11 to July 12, 2018). As
two economies. Thus, it is of interest to determine whether veterinarians the second venue, a link to take the online version of the survey was
from different countries, including from the US and EU, have different distributed by the National Mastitis Council (NMC) via email to their
perceptions regarding the risk of antibiotic resistance emergence on 176 member veterinarians (from June 23 to July 20, 2018). The NMC is
dairy farms. a not-for-profit professional organization, with international member­
Veterinarians have a crucial role in promoting measures to reduce ship, devoted to reducing mastitis and enhancing milk quality. As the
the risk of antibiotic resistance from emerging on dairy farms, as well as third venue, the online version of the survey was distributed by the
educating their clients regarding the judicious use of antibiotics. In fact, University of Milan via email to 623 people who registered for the
success of antibiotic resistance reduction programs has mostly relied on conference and through this venue the survey was open from July 27 to
changing attitudes held by veterinarians and their clients about the September 6, 2018. Of those 623 registered, author P.M., who also
prescription and administration of antibiotics (Oliver et al., 2011). For served as a member of the conference organizing and scientific com­
this reason, understanding how veterinarians perceive their clients’ and mittees, approximated that two thirds (or roughly 400 participants)
colleagues’ antibiotic use and their own beliefs about the development were dairy veterinarians. In addition to dairy veterinarians, the at­
of antibiotic resistance is pivotal to identifying areas in which education tendees of this annual conference have typically been dairy producers,
and training efforts might improve antibiotic use and prescribing prac­ researchers, extension specialists, industry suppliers, dairy processor
tices. Nonetheless, there is limited research assessing dairy veterinar­ field representatives, regulatory officials, teachers, and students.
ians’ perceptions regarding antibiotic use and the risk of development of Though not possible to confirm, it is highly plausible that many of the
antibiotic resistance in animals and humans, including studies in Italy NMC member veterinarians were also among the 623 people registered
(Busani et al., 2004), New Zealand (McDougall et al., 2017), the for the conference. In both paper and online formats, the survey was
Netherlands (Speksnijder et al., 2015a, 2015b), the United Kingdom estimated to take 10− 15 min to complete. An incentive was offered in
(Higgins et al., 2017), and the US (Cattaneo et al., 2009); this is insuf­ the first administration venue; after completing the survey participants
ficient considering the continuous development of regulations and were offered to enter their e-mail address into a drawing to win one of 24
guidelines for the use of antibiotics. Knowledge is especially sparse Cornell University T-shirts.
regarding perceptions of dairy veterinarians in the US. The study by Information obtained from completed paper and online surveys, was
Cattaneo et al. (2009) was performed before the Veterinary Feed organized into a datasheet in Microsoft Excel (Microsoft, Seattle, WA).
Directive (VFD) final rule entered into effect in early 2017, introducing Non-numeric responses to questions asking for a numeric response (i.e.,
relevant changes in the way in which farmers access some antibiotics participant did not respond with a number) were not utilized. Responses
(FDA, 2015). Information is even more limited regarding veterinarians’ with numerical ranges in open-end questions were averaged, and an­
attitudes towards the application of diverse preventive and management swers “greater than” or “less than” were given as 1 integer above or
measures to reduce antibiotic resistance on dairy farms (Cattaneo et al., below the provided value, respectively. If no proper response to a
2009). Also, it is currently unknown how many veterinarians are even question was given, the corresponding response was left blank in the
concerned about development of antibiotic resistant organisms on their datasheet and considered as a missing observation. All surveys that were
dairy clients’ farms, which are within the circle of their direct awareness unfinished (i.e., participant did not finalize the questionnaire by sub­
and potential influence, and what distinguishes them from their col­ mitting her/his answers, n = 50) and those answered by non-
leagues. The objective of this study was to describe opinions and con­ veterinarians (n = 7) were disregarded. Similarly, responses from
cerns of an international group of dairy veterinarians regarding which significant information regarding the subject matter could not be
antibiotic use and resistance in dairy farming and determine the asso­ discerned were also excluded. For statistical analyses, all close-ended
ciated sources of variability with regards to the level of concern they questions with offered responses, and the open-ended question asking
have about antibiotic resistance on the dairy farms they serve. for a country where the participants has practiced over the past year,
were converted into categorical variables, while the remaining open-
ended questions (which asked for a numerical response) were

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Table 1 Table 1 (continued )

Survey questions and the associated variable names used in statistical and the­ Question Variable
matic analysis (answer choices for multiple choice questions are omitted for
brevity; full questionnaire can be found in the Supplementary Material). - Increased utilization of diagnostics available Importance-diagnostics
for various diseases
Question Variable - Improved communication between farm Importance-
1 In the past year, approximately what fraction of % of year in dairy owners, farm staff, and/or others communication
your time in clinical practice did you spend 15 In your opinion, considering all the farms you
working with dairy cows? have served over the past year, how easy would
2 In what country did you practice veterinary Country the following changes be to implement in order
medicine for most of the past year? to reduce farmers’ antibiotic use in dairy cattle?
3 Approximately how many years in total have you Years in dairy - Improved environmental conditions for cattle Difficulty-environment
worked with dairy cows in clinical practice as a (e.g. clean, well-ventilated, and adequately
veterinarian? sized facilities that promote cow comfort)
4 In a typical week over the past year, Time/week in dairy - Improved herd health management (e.g. Difficulty- management
approximately what percentage of your time in quality nutrition, vaccination, biosecurity, and
clinical practice do you spend working with dairy hoof care) NOT including the environmental
cattle? factors described in the first row
5 Over the past year, approximately how many No. farms served - Better utilization of and/or adherence to Difficulty-AB protocols
individual dairy farms have you personally antibiotic use protocols
provided veterinary services to? - Better adherence to labelling on drug Difficulty- drug packing/
6 Considering all the farms that you provided No. lact. cows served packaging in regard to treatment regimen labelling
veterinary services to over the past year, what is (dose, route, duration, and frequency)
the approximate total number of lactating dairy - Improved record keeping Difficulty-records
cows that you oversaw as a veterinarian? - Increased utilization of diagnostics available Difficulty-diagnostics
7 Approximately how many of the dairy farms you No. organic farms served for various diseases
provided veterinary services to over the past year - Improved communication between farm Difficulty-
were certified organic? owners, farm staff, and/or others communication
8 What is the smallest dairy farm size (in terms of Smallest farm served 16 In your opinion, approximately, what percentage % vets overprescribe AB
the number of lactating cows) you provided of veterinarians you know overprescribed or
veterinary services to over the past year? Please inappropriately prescribed antibiotics for use in
estimate if you are unsure. dairy cattle over the past year?
a,c
9 What is the largest dairy farm size (in terms of the Largest farm served A) If your answer in question 16 is not 0%: Vet overprescribing
number of lactating cows) you provided Why do you think these veterinarians reasons
veterinary services to over the past year? Please overprescribe or inappropriately prescribe
estimate if you are unsure. antibiotics to their clients?
10 Approximately what percentage of your current % clients use AB 17 Over the past year, how many times have you Times pressured to
dairy farmer clients have you ever assisted in protocol experienced pressure or influence from your prescribe AB
developing protocols for antibiotic use over the dairy farmer clients to prescribe antibiotics when
past year? they were unnecessary in your opinion?
11 Please state your level of agreement with the Give AB advice 18 Please complete the following statement with Discuss ABR
following statement: “I feel comfortable giving one of the choices below: “I __________ discuss
my dairy farmer clients advice about antibiotic antibiotic resistance with my clients.”
use, even if it conflicts with/differs from their 19b How concerned are you about antibiotic resistant Concern-ABR on farms
current practices.” organisms developing on your dairy clients’
12 Please state your level of agreement with the Clients take AB advice farms?
following statement: “Most of my dairy farmer 20c How concerned are you about antibiotic use on Concern-ABR in people
clients are (or would be) generally receptive to your clients’ dairy farms potentially causing on farms
advice I provide regarding antibiotic use.” antibiotic resistant infections in people working
13 In your opinion, approximately, what percentage % clients overuse AB on those farms?
of your dairy farmer clients overused or 21c How concerned are you about antibiotic use on Concern-ABR in general
inappropriately used antibiotics in their dairy your clients’ dairy farms potentially causing public
cattle over the past year? antibiotic resistant infections in the general
A) Of those farmers overusing or AB improvement area public?
inappropriately using antibiotics, in what 22 Please state your level of agreement with the AB overuse-ABR in dairy
treatment area do you think these dairy farmers following statement: “In your country, antibiotic
could improve their antibiotic use the most? You resistance due to antibiotic overuse and
may make multiple selections. inappropriate use in dairy farming contributes to
B) What might deter or prevent those farmers Barriers to AB reduction antibiotic resistant infections in dairy cattle.”
who are using more antibiotics than needed from 23 Please state your level of agreement with the AB overuse-ABR in
reducing antibiotic use? (Check all that apply.) following statement: “In your country, antibiotic humans
14 In your opinion, considering all the farms you resistance due to antibiotic overuse and
have served over the past year, how important are inappropriate use in dairy farming contributes to
the following changes in reducing farmers’ antibiotic resistant infections in the general
antibiotic use in dairy cattle? public.”
- Improved environmental conditions for cattle Importance- 24 Please state your level of agreement with the AB overuse-ABR in
(e.g. clean, well-ventilated, and adequately environment following statement: “In your country, antibiotic environment
sized facilities that promote cow comfort) overuse and inappropriate use in dairy farming
- Improved herd health management (e.g. Importance- negatively impacts the environment.”
quality nutrition, vaccination, biosecurity, and management 25 On a global scale, how do you rate antibiotic use ABR threat from AB in
hoof care) NOT including the environmental in dairy farming as a threat to human health in dairy
factors described in the first row terms of contribution to antibiotic resistant
- Better utilization of and/or adherence to Importance-AB infections in humans?
antibiotic use protocols protocols 26 On a global scale, how do you rate antibiotic use ABR threat from AB in
- Better adherence to labelling on drug Importance- drug in human medicine as a threat to human health in humans
packaging in regard to treatment regimen packing/labelling terms of contribution to antibiotic resistant
(dose, route, duration, and frequency) infections in humans?
- Improved record keeping Importance-records 27 Approximately what percentage of your income % income from AB sale
over the past year was generated by antibiotic
sales to your dairy farm clients?

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S.G. Llanos-Soto et al. Preventive Veterinary Medicine 188 (2021) 105253

Notations: AB = antibiotic; ABR: antibiotic resistance; Vet(s): veterinarian(s). as odds ratio (OR) and the associated 95 % confidence interval (95 %
a
This question was considered in qualitative (thematic) analysis. CI). Predictor variables displaying significant associations (p < 0.1) with
b
This question was considered as the outcome of interest in logistic regression the outcomes at the bivariable level were tested in multivariable logistic
analysis. regression models. For both bivariable and multivariable logistic
c
These variables were no included in the logistic regression analysis.
regression analyses, p-values and the associated OR 95 % CI were based
on the Wald test. Variables with more than 10 missing observations were
converted into continuous variables. evaluated at the bivariable level and were considered in multivariable
analysis initially but were eventually excluded due to data loss. When
2.3. Statistical analysis multiple continuous variables were found to be highly correlated (at r >
0.7), only one was considered at a time in the multivariable analysis.
All statistical analyses were performed in R Studio using R v. 3.5.1 (R Based on the Cramer’s Phi tests of association, responses to questions 20
Core Team, 2017). R packages "lme4", "exact2x2", "ggplot2", "rcom­ (“Concern-ABR in people on farms”) and 21 (“Concern-ABR in general
panion", and "epiDisplay" were employed for analysis. Responses ob­ public”) were very similar to those responded to question 19 (“Con­
tained for every question in Table 1 were summarized and organized in cern-ABR on farms”), which was used as the outcome of interest
tables (Tables 2 and 3) and/or visualized using plots. The outcome of (Cramer’s Phi = 0.5); thus, questions 20 and 21 were excluded from
interest was derived from the survey question “How concerned are you consideration in the multivariable logistic regression analysis. Question
about antibiotic resistant organisms developing on your dairy clients’ 16A (“Vet overprescribing reasons”) was considered in thematic anal­
farms?” (question 19, Table 1). This question was converted into a bi­ ysis. Other than questions 20, 21, and 16A, all other variables shown in
nary variable “Concern-ABR on farms” with levels “Unconcerned” Table 1 were considered as predictors in the bivariable logistic
(including original levels: “Not at all concerned”, “Slightly concerned”, regression.
and “Somewhat concerned”) and “Concerned” (including: “Moderately The final logistic regression model was selected through the stepwise
concerned” and “Extremely concerned”). The open-ended survey ques­ backward elimination process using likelihood ratio test and the Akaike
tion “In what country did you practice veterinary medicine for most of information criterion (AIC). Box-Tidwell test was used to determine if
the past year?” (question 2, Table 1) was converted into a categorical the assumption of linearity holds between the logit transformation of the
variable “Country” by grouping responses into “United States”, “Euro­ outcome and the continuous predictor variables in the final logistic
pean Union”, and “Other countries”. However, because of a small regression model (Box and Tidwell, 1962). Receiver operating charac­
number of responses under “Other countries” (n = 9), this level was teristic (ROC) curves were built to determine to which extent the final
dropped after initial descriptive analyses; the resulting binary variable model properly fitted the data. Confounding among variables was
was used as an explanatory variable (predictor) for the outcome of in­ identified by evaluating changes of ≥30 % in the ln(OR) between the
terest. Other predictor variables derived from the survey questions are estimate calculated in the bivariable logistic regression (crude estimate)
listed in Table 1. and estimate obtained after including the potential confounder in the
Potential associations between the outcome and categorical predic­ multivariable model (adjusted estimate) (Dohoo et al., 2003). Two and
tor variables were first visually assessed by generating balloon plots, three-way interactions between variables included in the final multi­
while boxplots were used to visually evaluate relationships between the variable model were also assessed for. Except when otherwise stated,
outcomes and continuous predictor variables. Logistic regression was statistical significance was established at p-value < 0.05.
used to evaluate associations between the outcome of interest and pre­ The “Country” variable was additionally evaluated as a dependent
dictors. Associations between two categorical predictors were assessed variable using logistic regression analysis to identify any systematic
by the Chi-square (or as applicable by the Blaker’s exact test (Fay, differences between study participants from the US and EU (this is
2010)) and associations between a categorical and continuous variable further described in the Supplementary Material).
were assessed using the Mann-Whitney test. Correlations between two
continuous predictor variables were tested using the Spearman’s test. All 2.4. Thematic analysis
categorical predictors were dichotomized (as explained in Table 3) to
reduce the number of levels included in the models to improve study Answers to the open-ended question “Why do you think … veteri­
power. Variables “No. farms served”, “No. lact. cows served”, “Smallest narians [you know] overprescribe or inappropriately prescribe antibi­
farm served”, and “Largest farm served” were highly skewed and so were otics to their clients?” (Question 16 A, Table 1) were analyzed using
log10-transformed for logistic regression analysis. An association be­ thematic analysis (Braun and Clarke, 2006). All participants’ responses
tween the outcome and a statistically significant predictor was expressed were read by S.L.-S. to develop a preliminary codebook based on

Table 2
Summary statistics for continuous variables describing the responses provided by dairy veterinarians (n = 71) enrolled in the context of the International Bovine
Mastitis Conference held in Italy in 2018.
Variable (unit)

Mean Median IQR Range Missing

% of year in dairy (%) 83.5 90 70− 100 20− 100 3

Years in dairy (year) 18.9 17 8− 27 1− 47 0
Time/week in dairy (%) 84.5 90 70− 100 20− 100 1
No. farms served (farm) 74.1 40 25− 100 1− 550 0
No. lact. cows served (cow) 19,273 5,000 2,500− 11,000 20− 350,000 0
No. organic farms served (farm) 2.6 1 0− 3 0− 25 0
Smallest farm served (cow) 120.6 30 20− 50 2− 2,600 0
Largest farm served (cow) 4,669 800 380− 1,500 120− 200,000 0
% clients use AB protocol (%) 59.3 60.5 30− 90 0− 100 1
% clients overuse AB (%) 47.1 40 30− 70.5 0− 100 3
% vets overprescribe AB (%) 42.9 47.5 17.5− 61 0− 100 3
Times pressured to prescribe AB (times pressured) 16.6 8.75 2.4− 20 0− 80 19
% income from AB sale (%) 13.2 6.5 0− 25 0− 65 17

Notation: IQR = Interquartile range; AB = antibiotic.

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S.G. Llanos-Soto et al. Preventive Veterinary Medicine 188 (2021) 105253

e
Table 3 Responses were dichotomized for logistic regression analysis: Levels
Summary statistics of categorical variables describing the responses provided by “Strongly disagree”, “Disagree”, and “Neither agree nor disagree” were grouped
dairy veterinarians (n = 71) enrolled in the context of the International Bovine into “Disagree”, while levels “Agree” and “Strongly agree” were grouped into
Mastitis Conference held in Italy in 2018. “Agree”.
f
Responses were dichotomized for logistic regression analysis: Levels “No
Variablea Response Number %b
threat” and “Low threat” were grouped into “No threat”, while levels “Moderate
European Union 45 64 threat” and “High threat” were grouped into “Threat”.
Country United States 16 23
Other countries 9 13
Never 0 0 emergent themes. Responses and the codebook were then also reviewed
Very rarely 0 0 by A.G.S., M.W., and R.I. The codebook was revised until an agreement
Rarely 4 6 was reached between S.L.-S., A.G.S., M.W., and R.I. Next, S.L.-S. applied
Discuss ABRc
Occasionally 23 32
the topic-level codes to the responses in consultation with A.G.S. This
Frequently 30 42
Very frequently 14 20 method of coding allowed the participants’ exact responses to be
Not at all concerned 1 1 captured and organized for qualitative analysis. All quotes within a topic
Slightly concerned 12 17 were then analyzed by S.L.-S. to identify higher-order trends and
Concern-ABR on farmsd Somewhat concerned 13 18 themes, which were then reviewed, discussed, refined accordingly, and
Moderately concerned 28 39
Extremely concerned 17 24
agreed on by A.G.S., M.W., and R.I.
Not at all concerned 4 6
Slightly concerned 22 31 3. Results
Concern-ABR in people on farmsd Somewhat concerned 19 27
Moderately concerned 15 21
Extremely concerned 11 16
The survey was completed by 71 dairy veterinarians. Of these, 34
Not at all concerned 9 13 were obtained through the administration venue 1 (offered on paper and
Slightly concerned 18 25 online at the International Bovine Mastitis Conference in Milano), 24
Concern-ABR in general publicd Somewhat concerned 17 24 through the administration venue 2 (online version distributed to NMC
Moderately concerned 18 25
member veterinarians), and 13 through the administration venue 3
Extremely concerned 9 13
Strongly disagree 2 3 (online version distributed to all conference attendees post conference).
Disagree 0 0 Therefore, the response rate was between (i) 9 % (71/(623 + 176)) and
Give AB advicee Neither agree nor disagree 6 9 (ii) 18 % (71/400) depending on how conservative or liberal denomi­
Agree 28 39 nator is used in calculation. In (i) the denominator is a sum of the 623
Strongly agree 35 49
Strongly disagree 2 3
people registered to attend the conference and 176 NMC member vet­
Disagree 0 0 erinarians assuming that all 623 registrants were dairy veterinarians and
Clients take AB advicee Neither agree nor disagree 4 6 that none of the NMC’s 176 member veterinarians was registered to
Agree 49 69 attend the conference. In (ii) the denominator is comprised of 400 dairy
Strongly agree 16 23
veterinarians (approximated by P.M. to have been among people
Strongly disagree 2 3
Disagree 13 18 registered to attend the conference) and it is assumed that this number
AB overuse-ABR in dairye Neither agree nor disagree 16 23 already includes the NMC’s member veterinarians. There was a total of
Agree 29 41 80 missing observations distributed among 14 questions (with the
Strongly agree 11 16 largest number of missing observations for the variables “Times pres­
Strongly disagree 7 10
Disagree 27 39
sured to prescribe AB” and “% income from AB sale”; Table 2).
AB overuse-ABR in humanse Neither agree nor disagree 26 37
Agree 8 11
3.1. Descriptive analysis
Strongly agree 2 3
Strongly disagree 3 4
Disagree 14 20 Responses to the questionnaire are summarized in Tables 2 and 3,
AB overuse-ABR in environmente Neither agree nor disagree 19 27 and in Figs. 1–4. Participants represented 21 countries from the conti­
Agree 26 37 nents of South America, North America, Europe, Asia, and Oceania:
Strongly agree 8 11
No threat 2 3
Australia (n = 1), Austria (n = 1), Belgium (n = 1), Canada (n = 2),
Low threat 40 57 China (n = 2), Denmark (n = 1), Finland (n = 1), France (n = 4), Ger­
ABR threat from AB in dairyf
Moderate threat 22 31 many (n = 7), Hungary (n = 2), Ireland (n = 2), Italy (n = 21), New
High threat 6 9 Zealand (n = 2), Portugal (n = 1), Spain (n = 1), the Netherlands (n = 2),
No threat 5 7
Ukraine (n = 1), United Kingdom (n = 1), Uruguay (n = 1), the US (n =
Low threat 12 17
ABR threat from AB in humansf 16), and there was a single veterinarian working in three countries
Moderate threat 51 73
High threat 2 3 (Canada, the US, and Mexico). Among these, 45 (64 %) veterinarians
were from countries members of the EU, 16 (23 %) from the US, and 9
Notations: ABR = antibiotic resistance; AB = antibiotic.
a
One observation is missing in each of the variables: “Country”, “AB overuse-
(13 %) came from other countries (counting in the veterinarian working
ABR in humans”, “AB overuse-ABR in environment”, “ABR threat from AB in in Canada, the US, and Mexico), while one participant did not specify
dairy”, and “ABR threat from AB in humans”. their country of work. Furthermore, veterinarians indicated that they
b
Percentages were rounded to two decimal places. This caused some numbers worked a median of 17 (interquartile range (IQR) = 8− 27) years with
to not add up to 100 %. dairy cows and spent a median of 90 % (IQR = 70 %–100 %) of their
c
Responses were dichotomized for logistic regression analysis: Levels time in a typical week over the past year working with dairy cattle in
“Never”, “Very rarely”, and “Rarely” were grouped into “Rarely”, while levels clinical practice. Additionally, participants served a median of about 40
“Occasionally”, “Frequently”, and “Very Frequently” were grouped into (IQR = 25− 100) individual farms and 5,000 (IQR = 2,500− 11,000)
“Frequently”.
d
lactating dairy cows in the past year, with the smallest and largest farms
Responses were dichotomized for logistic regression analysis: Levels “Not at
having a median size of 30 (IQR = 20− 50) and 800 (IQR = 380− 1,500)
all concerned”, “Slightly concerned”, and “Somewhat concerned” were grouped
lactating cows, respectively.
into “Unconcerned”, while levels “Moderately concerned” and “Extremely
concerned” were grouped into “Concerned”. Overall, veterinarians indicated that they have assisted a median of
61 % (IQR = 30 %–90 %) of their dairy farmer clients in developing

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Furthermore, participants perceived pressure from their clients to pre­

scribe antibiotics when they deemed it unnecessary a median of 9 (IQR
= 2–20) times over the past year (Fig. 1E).
Among proposed strategies to reduce dairy farmers’ antibiotic use,
most veterinarians categorized them as “Very important” or “Extremely
important”, with the exception of “Importance- drug packing/labelling”
which was mostly perceived as being “Moderately important” (Fig. 2A).
Veterinarians perceived that improved environmental conditions for
cattle and improved herd health management practices were the most
important strategies. Conversely, the opinions of veterinarians about
how difficult is to implement these same strategies were more centered
around the neutral response. Most of the answers were classified as

Fig. 1. Boxplots describing responses of participating dairy veterinarians

enrolled in the context of the International Bovine Mastitis Conference held in
Italy in 2018 regarding the (A) percentage of clients they assisted to in devel­
oping antibiotic use protocols, (B) perceived percentage of their dairy farmer
clients overusing or inappropriately using antibiotics in their dairy cattle over
the past year, (C) percentage of their income over the past year generated by
antibiotic sales to dairy farm clients, (D) perceived percentage of their veteri­
narian colleagues overprescribing or inappropriately prescribing antibiotics for
use in dairy cattle over the past year, and (E) number of times that they have
experienced pressure or influence from their dairy farmer clients to prescribe
antibiotics when they were considered unnecessary.

protocols for antibiotic use in the past year (Fig. 1A) and perceived that a
median of 40 % (IQR = 30 %–71 %) of their clients overused or inap­
propriately used antibiotics in their dairy cows over the past year
(Fig. 1B). Additionally, participants pointed out that a median of 7 %
(IQR = 0 %–25 %) of their income comes from the sale of antibiotics to Fig. 3. Responses of participating dairy veterinarians to the question “Of those
dairy farm clients (Fig. 1C). When asked about the use of antibiotics by farmers overusing or inappropriately using antibiotics, in what treatment area
do you think these dairy farmers could improve their antibiotic use the most?
their colleagues over the past year, participants responded that a median
You may make multiple selections.” x-axis indicates the percentage of veteri­
of 48 % (IQR = 18 %–61 %) of veterinarians they know are over­
narians out of 71 participants who selected each response (the number within
prescribing or inappropriately prescribing these drugs (Fig. 1D). each bar represents frequency).

Fig. 2. Heat map of the response frequencies for the perceived importance (panel A) and difficulty (panel B) of different strategies to reduce farmers’ use of an­
tibiotics in dairy cattle responded by the participating dairy veterinarians. Notation: AB = antibiotic.

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S.G. Llanos-Soto et al. Preventive Veterinary Medicine 188 (2021) 105253

and digestive problems in cows (14/71, 20 %) are relevant (Fig. 3). In

addition, veterinarians indicated that the main barriers to reducing
antibiotic use by dairy farmers who use antibiotics more than needed are
a lack of knowledge of how and when specific antibiotic should be used
to treat various diseases (42/71, 59 %), poor environmental conditions
for cattle (41/71, 58 %), poor herd management (40/71, 56 %), and lack
of knowledge of strategies to reduce antibiotic use (36/71, 51 %). Only
one of 71 (1 %) participating veterinarians perceived that dairy farmers
are not overusing antibiotics and 6 of 71 (8 %) believed that their use is
already minimal (Fig. 4).

3.2. Variables associated with veterinarians’ concern about the emergence

of antibiotic resistant infections on their clients’ dairy farms

Statistically significant associations (at the p-value = 10 % level)

between the outcome of interest, namely expressed concerns of
participating veterinarians about the emergence of antibiotic resistant
infections in dairy cattle on their clients’ farms, and several predictors
were identified (Table 4). Namely, the veterinarians’ concern about
antibiotic resistance on clients’ farms was weakly negatively associated
with the proportion of the last year spent in dairy cattle clinical practice,
veterinarians’ years of experience working with dairy cows in clinical
Fig. 4. Responses of participating dairy veterinarians to the question “What practice, the proportion of dairy farmers they assisted in the develop­
might deter or prevent those farmers who are using more antibiotics than ment of antibiotic protocols, and the proportion of veterinarians’ in­
needed from reducing antibiotic use? (Check all that apply.)” x-axis indicates come obtained from antibiotic sales. Also, concern about antibiotic
the percentage of veterinarians out of 71 participants who selected each resistance on clients’ farms was positively associated with the percep­
response (the number within or beside each bar represents frequency). tions that better adherence to labelling on drug packaging was an
important but difficult to implement strategy to reduce antibiotic
“Easy”, “Neither easy nor difficult”, or “Difficult” and only a few vet­ resistant infections in dairy cattle, the perceived importance of increased
erinarians perceiving these strategies as “Very easy” or “Extremely utilization of diagnostics for various diseases, the perceived difficulty of
difficult” (Fig. 2B). better utilization of and/or adherence to antibiotic use protocols, the
Regarding clinical treatment areas in which antibiotic use could be perception that overuse and inappropriate use of antibiotics in dairy
improved the most, the majority of veterinarians expressed that clinical farming contributes to antibiotic resistant infections in dairy cattle, and
mastitis (53/71, 75 %) and diarrhea and digestive problems in calves veterinarian’s concerns regarding antibiotic resistance emergence in
(43/71, 61 %) requires the most attention, followed by subclinical people working on the farms they serve and in the general public.
mastitis or high somatic cell count in cows (32/71, 45 %), while only a Results from the multivariable logistic regression model are shown in
few perceived that navel infection in calves (7/71, 10 %) and diarrhea Table 5. They indicated that participants thought that better adherence
to labelling on drug packaging is an important strategy to implement in

Table 4
Variables associateda with veterinarians’ expressed concern (Concerned vs. Unconcerned as the baseline level) about the development of antibiotic resistant organisms
on their dairy clients’ farms.
Variable Levels/Unit Unconcerned (%) Concerned (%) ORb 95 % CIc p-value

Importance-drug packing/labelling Unimportant 7 (54 %) 10 (18 %) 1.00

Important 6 (46 %) 47 (82 %) 5.48 1.51 – 19.85 0.01
Importance-diagnostics Unimportant 5 (38 %) 3 (5 %) 1.00
Important 8 (62 %) 54 (95 %) 10.63 2.07 – 60.56 0.004
Difficulty-AB protocols Easy 11 (85 %) 26 (45 %) 1.00
Difficult 2 (15 %) 32 (55 %) 6.60 1.34 – 44.00 0.01
Difficulty-drug packing/labelling Easy 9 (69 %) 23 (40 %) 1.00
Difficult 4 (31 %) 35 (60 %) 3.36 0.86 – 13.08 0.07
Concern-ABR in people on farms Unconcerned 12 (92 %) 14 (24 %) 1.00
Concerned 1 (8%) 44 (76 %) 35.60 5.10 – 811.36 <0.0001
Concern-ABR in general public Unconcerned 11 (85 %) 16 (28 %) 1.00
Concerned 2 (15 %) 42 (72 %) 13.83 2.71 – 95.90 <0.001
AB overuse-ABR in dairy Disagree 11 (85 %) 20 (34 %) 1.00
Agree 2 (15 %) 38 (66 %) 10.10 2.02 – 69.32 0.001
% of year in dairyd % NAe NA 0.96 0.91 – 1.01 0.08
Years in dairyd Year NA NA 0.95 0.91 – 1.00 0.04
% clients use AB protocold % NA NA 0.98 0.96 – 1.00 0.07
% income from AB saled % NA NA 0.96 0.93 – 1.00 0.05
a
Variables associated with the outcome at the p-value = 10 % level are shown.
b
OR: Odds ratio.
c
95 % CI: 95 % confidence interval.
d
Among participants who were Unconcerned and Concerned about the development of antibiotic resistant organisms on their dairy clients’ farms the median and
interquartile range (IQR) were respectively: for “% of year in dairy” 98 % (90%–100%) and 90 % (70%–100%); for “Years in dairy” 26 (18–30) and 15 (6–25) years; for
“% clients use AB protocol” 90 % (80%–90%) and 58 % (30 %–90 %); and for “% income from AB sale” 20 % (5%–41%) and 0% (0%–20%).
e
NA: not applicable for a continuous variable.

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Table 5 about pathologies in dairy cattle (e.g., mastitis), and poor understanding
Final multivariable logistic regression model for veterinarians’ expressed of diagnostics. Less commonly mentioned motives were insufficient
concern (Concerned vs. Unconcerned as the baseline level) about the develop­ knowledge about alternative treatments or unawareness of the issue of
ment of antibiotic resistant organisms on their dairy clients’ farms. antibiotic resistance emergence. Nonetheless, most participants pro­
Variable Levels/Unit ORa 95 % CIb p- vided a much more general answer by only stating that lack of knowl­
value edge was the main reason for antibiotic overprescription, without
Importance-drug packing/ Unimportant 1.00 providing specific reasons.
labelling In most responses, veterinarians described their colleagues’ attitudes
Important 6.86 1.21 – 0.03 towards prescribing antibiotics. Reported motives that contributed to
38.93
AB overuse-ABR in dairy Disagree 1.00
the overprescription of antibiotics included: profit (mentioned by
Agree 11.70 1.76 – 0.01 approximately one in every six participants) and bad habit or tradition
77.76 (mentioned by approximately one in every three participants), as well as
Years in dairy Year 0.91 0.84 – 0.99 0.03 less commonly mentioned: lack of concern, easiness on the veterinarian
% clients use AB protocol % 0.97 0.94 – 1.00 0.03
to continue their current practices, and fear of conflict with farmer or
a
OR: Odds ratio. losing business. Among farmer attitudes, participants also indicated that
b
95 % CI: 95 % confidence interval. antibiotic overprescription might result from increased pressure on
veterinarians to comply with their client’s demands (mentioned by
order to reduce client’s antibiotic use (OR = 6.86, 95 % CI = approximately one in every five participants) and several participants
1.21–38.93) and agreed that overuse of antibiotics contributes to the mentioned farmers’ unwillingness to change their own incorrect beliefs
emergence of antibiotic resistance on farms (OR = 11.70, 95 % CI = about the proper use of antibiotics.
1.76–77.76). For every one-unit increase in participants’ years of Veterinarians’ barriers were mentioned by several participants and
experience and the proportion of clients being assisted by veterinarians they included problems with diagnosis and availability of diagnostic
in the development of antibiotic protocols, the odds of veterinarians tests, and lack of time. Similarly, only a few mentioned farmers’ barriers,
being concerned about the emergence of antibiotic resistant infections which were related with the lack of infection prevention or good envi­
on the dairy farms they served decreased by a factor of 0.91 (OR = 0.91, ronmental conditions. Finally, a few participants expressed concern
95 % CI = 0.84− 0.99) and 0.97 (OR = 0.97, 95 % CI = 0.94–1.00; about the lack of oversight and regulation of antibiotic use.
Table 5), respectively. The Box-Tidwell test indicated that the assump­
tion of linearity held for both continuous predictors included in the 4. Discussion
model (i.e., “Years in dairy” and “% clients use AB protocol”). This
model presented an AIC of 50.76 and a residual standard deviation of Elucidating whether and how veterinarians’ antibiotic prescribing
40.76 on 64 degrees of freedom, while the null model had an AIC of practices need to improve and whether veterinarians are concerned
68.78 and a residual standard deviation of 66.78 on 68 degrees of about antibiotic resistance emergence is a crucial step for developing
freedom. Results from the likelihood ratio test indicated that models solutions to these challenges. Furthermore, understanding the reasons
differed significantly (p-value < 3.13 × 10− 5) and diagnostics with ROC behind veterinarians’ and farmers’ attitudes and behaviors towards
(area under curve [AUC] = 0.91) also suggested a good fit. No in­ antibiotic use helps to put these practices into context, which is
teractions nor meaningful confounding were identified. important to consider when planning and implementing strategies to
reduce antibiotic use. Veterinarians’ knowledge, behavior, and attitudes
regarding antibiotic use greatly influences those of their farmer clients
3.3. Thematic analysis (Sawant et al., 2005; Jones et al., 2015; McDougall et al., 2017). For
example, veterinarians are frequently tasked with developing antibiotic
Among the 71 study participants, 52 responded to the open-ended use protocols to reduce their clients’ antibiotic use. In fact, a little more
question about reasons why veterinarians overprescribe or inappropri­ than half of veterinarians participating in this study assisted their clients
ately prescribe antibiotics to their dairy farmer clients. Their responses with developing antibiotic use protocols. Similarly, a study by Habing
were classified into four key themes: 1) knowledge, 2) attitudes, 3) et al. (2016) found that close to 43 % (176/419) of surveyed dairy
barriers, and 4) rules and regulations (Table 6). Themes “attitudes” and farmers from Ohio and Michigan, US, had written protocols to treat
“barriers” were further classified into groups concerning veterinarians cattle against common pathologies in dairy provided to them by veter­
and farmers, while the theme “knowledge” only concerned veterinar­ inarians. Contrary to that, a study assessing a similar question among
ians. The distinction between attitudes and barriers for this is as follows. veterinarians from Ohio State, reported that only 23 % of veterinarians
Attitudes refer to overprescription or inappropriate prescription by (10/43) always assisted farmers with antibiotic protocols (Cattaneo
veterinarians’ colleagues based on their experiences, beliefs, interests, et al., 2009). The difference in findings between Cattaneo et al. (2009)
and traditions or those imposed by their farmer clients, whereas barriers and our study may be due to the question wording. In Cattaneo et al.
were understood as limitations of veterinarians or farmers that were (2009), the question asked if veterinarians supply their clients with
caused by a lack of appropriate tools or opportunities to reduce/avoid antibiotic use protocols 100 % of the time. Thus, the participants’
injudicious antibiotic prescription. Finally, the rules and regulations negative response to that question might have meant that they did assist
theme included veterinarian’s perception of limitations in the way their clients, just not 100 % of the times. Another potential explanation
proper antibiotic use is enforced or overseen by responsible organiza­ for the higher proportion in our study may be a trend for veterinarians to
tions. Participants were not provided with a definition of “inappro­ become more involved in the antibiotic use protocol development in
priate” antibiotic use, so their responses reflected their own recent years. Associated with this, we found that dairy veterinarians
understanding of this concept. who assist their farmers in developing antibiotic use protocols are less
Approximately one in every three participants mentioned lack of likely to be concerned about antibiotic resistance emergence on their
knowledge to explain veterinarian’s overprescription of antibiotics. clients’ dairy farms. This finding could be a consequence of veterinar­
According to the participants, there were different reasons why insuf­ ians’ confidence that their clients’ will follow their instructions in
ficient knowledge was relevant, with the most mentioned reason being antibiotic use, therefore limiting opportunities for antibiotic resistance
the lack of understanding about the way in which particular antibiotics emergence.
work (i.e., duration, dose). Other common reasons were insufficient Participants perceived that nearly half of their clients use antibiotics
knowledge about the appropriate antibiotic treatment, lack of education injudiciously, and that nearly half of their colleagues overprescribe/

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Table 6
Themes identified in responses given by veterinarians to the question “Why do you think … veterinarians [you know] overprescribe or inappropriately prescribe
antibiotics to their clients?” (52 participants provided responses for analysis).
Theme Category Subtheme Country, Participant’s Quote
experiencea ID

Knowledge Veterinarians Lack of knowledge United States, 45 “They [veterinarians] do not think it is causing a problem and are
6 years unwilling to do what needs to be done to change it. In many cases, I see
veterinarians that are not even aware or involved in how drugs are
actually used on a day-to-day basis. Taking a stand would necessitate
becoming more integrally involved in day-to-day operations and actually
training on diagnosis and prognosis”
China, 3 years 15 “In China, each dairy [farm] has its own vets, who are normally not well-
educated and don’t have enough knowledge to understand how to
scientifically use antibiotics”
Germany, 18 40 “Lack of knowledge: duration, dose, alternative treatment protocols”
years
Attitudes Veterinarians Profit motive Ireland, 3 years 27 “In one case, fluoroquinolones were prescribed repeatedly as they are
more profitable”
Germany, 20 18 “The fact that Ab [antibiotics] are responsible for a considerable part of
years the income”
Portugal, 15 24 “Market pressure on veterinarians”
years
Bad habit/tradition United States, 45 “They [veterinarians] do not think [overprescription of antibiotics] is
6 years causing a problem and are unwilling to do what needs to be done to
change it”
United States, 25 “Old school mentality of treating animals”
1 year
Lack of concern Italy, 35 years 1 “Lack of sensibility to the problem (AMR) [antibiotic resistance]”
Italy, 4 years 33 “[Veterinarians] are not interested in preventing in the right way the
disease”
Easier on the veterinarian Italy, 7 years 8 “They just follow the needs of the farm”
Italy, 15 years 20 “Because the use of lot of antibiotics in a therapy procedure helps the vet
mental peace and keeps the farmer quiet”
Fear of conflict/losing Uruguay 10 22 “Farmers want to use atb [antibiotics], so they [veterinarians] prefer to
business years not fight”b
Farmers Unwillingness to change/ Germany, 20 18 “There are certain habits that are very difficult to change (both vets and
habit and autonomy years farmers)”c
Australia, 12 35 “It’s more because the client refuses to change their treatment practices”
years
Pressure on veterinarians to France, 5 years 6 “The producer did not perceive a clinical result, so they [veterinarians]
meet client’s demands have to make longer treatments or provide bigger doses”
Barriers Veterinarians Problems with diagnosis and Ireland, 26 2 “Limitations in diagnostics”
availability of diagnostic tests years
Lack of time Finland, 8 66 “Lack of time and knowledge of the current protocols and needs for
years antimicrobials. No knowledge nor time for appropriate consulting”d
Farmers Lack of infection prevention/ Italy, 8 years 32 “Lack of prevention resources”
good environmental
conditions
Germany, 21 23 “Lack of appropriate environmental conditions, farmer is not willing to
years change that (or able)”
Rules and Lack of regulations/oversight Portugal, 15 24 “Absence of mandatory regulation and supervision by local authorities”
regulations years
United States, 49 “Not enough oversight”
47 years
a
Years of clinical experience working with dairy cattle.
b
Considered as both the “Easier on the veterinarian” and “Fear of conflict/losing business” subthemes.
c
Considered as both the farmers’ and veterinarians’ attitudes.
d
Considered in both the “Knowledge” and “Attitude” themes.

inappropriately prescribe antibiotics (Table 2; Fig. 1B, D). Over­ digestive problems in calves as their primary targets for optimization of
prescribing of antibiotics by veterinarians may be the result of the antibiotic use. These findings are consistent with a previous study
pressure being exerted by their clients, as participants expressed being assessing veterinarians’ perceptions in Ohio, US (Cattaneo et al., 2009),
pressured to prescribe an antibiotic when they deemed it unnecessary a antibiotic use information published by the USDA (2008) and Walker
median of 9 times during the past year (Table 2, Fig. 1E). These results et al. (2012), and even perceptions of dairy farmers (Wemette et al.,
are similar to those in other studies, indicating that veterinarians might 2020). Consequently, it is more than likely that the importance of
feel the need to comply with the request of their clients to avoid dete­ mastitis, diarrhea and digestive problems for dairy cattle production is a
riorating their business relationship (McIntosh et al., 2009; Speksnijder major factor influencing the perceptions of veterinarians regarding
et al., 2015b; Coyne et al., 2016). However, research has shown that clinical treatment areas for antibiotic use improvement. Despite the
more experienced veterinarians might be less concerned about the widespread use of antibiotics to treat mastitis in dairy cattle, there is no
consequences of declining their clients’ requests for an antibiotic pre­ compelling evidence that antibiotic resistance is currently emerging in
scription (Speksnijder et al., 2015b). mastitis-associated pathogens in dairy cattle (Oliver et al., 2011).
Veterinarians in this study believed that there is room for improve­ Nonetheless, a judicious use of antibiotics by veterinarians in the
ment of antibiotic use in several clinical domains. Among treatment treatment of clinical mastitis could assist in reducing the risk of anti­
areas, veterinarians pointed out clinical mastitis as well as diarrhea and biotic residues in milk (and the associated fines for farmers) and reduce

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the cost of mastitis treatment. antibiotics and for them to receive training on how to properly advise
Veterinarians’ perceptions about their clients’ behavior can provide their clients’ and deal with potential conflicts regarding antibiotic use
valuable insight into barriers that prevent dairy farmers from reducing that veterinarians might come across during their clinical practice.
antibiotic use. Veterinarians are in an excellent position to identify Interestingly, veterinarians worried about the risk of antibiotic
barriers and attitudes of their clients in regards to antibiotic treatment resistance emergence on dairy farms they serve believed that better
and can provide valuable information that might not be obtained by adherence to drug labeling was important for reducing farmers’ anti­
surveying farmers. In our study, veterinarians expressed the belief that biotic use; though this variable (“Importance- drug packing/labelling”)
their clients are lacking in knowledge about the proper use of antibiotics displayed a wide confidence interval (95 % CI: 1.21–38.93), indicating
and awareness regarding strategies for antibiotic use reduction, sup­ the uncertainty of how relevant this measure really is for veterinarians.
porting the possibility that antibiotic use by farmers should be further Although not directly related to our findings, a study by Cattaneo et al.
optimized. Additionally, nearly half of veterinarians indicated that (2009) on dairy veterinarians from the US indicates that hand-outs with
deficient environmental conditions and poor herd management pre­ good management practices, diagnosis descriptions, and appropriate
vented farmers from reducing their antibiotic use (Fig. 4). These per­ dosages are effective ways to assist farmers in improving their knowl­
ceptions could be related to the understanding that dairy farm edge of antibiotic resistance (Cattaneo et al., 2009). It is important to
environments can host opportunistic and pathogenic bacteria that can consider that the study by Cattaneo et al. (2009) represents the beliefs
be transmitted through contaminated milk equipment and pens, and opinions of veterinarians from a decade ago, something that may be
particularly when established hygiene practices are precarious or outdated given the rapidly growing attention that antibiotic resistance
insufficient (Munoz et al., 2007). Meanwhile, inappropriate herd man­ and antibiotic use are receiving and how the legislations have changed
agement practices might increase dairy cattle susceptibility to bacterial in the US. Further research is necessary to determine if education of
infections and disease (Vasseur et al., 2010). In this sense, veterinarians farmers on good management practices and antibiotic use would
believe that improving key elements involved in dairy farm herd and improve their compliance with instructions in drug labels.
environmental management, such as farm infrastructure, cleaning of When asked about the possible reasons why their colleagues might
equipment and sheds, vaccination and feeding protocols, and animal overprescribe or inappropriately prescribe antibiotics in dairy farms,
care, could contribute to minimizing the need for antibiotic treatment veterinarians provided answers that were grouped into themes associ­
through disease prevention (Fig. 4). This finding matches those reported ated with veterinarians’ and farmers’ attitudes. In addition, they
by other veterinarians working in agricultural settings (Coyne et al., mentioned barriers and lack of regulation and oversight regarding
2016). antibiotic prescription in dairy farms (Table 6). Limitations in knowl­
We found that veterinarians with fewer years in clinical practice edge about antibiotic treatment, pathologies in dairy cattle, diagnostics,
were more concerned about antibiotic resistant infections on the dairy alternative treatments, and the consequences of antibiotic misuse were
farms they serve. These findings are consistent with studies conducted pointed out as important factors preventing judicious antibiotic use by
both in the Netherlands (Speksnijder et al., 2015b) and US (Cattaneo veterinarians. This is of no surprise, as insufficient knowledge regarding
et al., 2009). Increased concern about antibiotic resistance among vet­ the use of antibiotics is considered one of the main drivers of antibiotic
erinarians with fewer years of experience could be a consequence of resistance and can have an effect in how antibiotics are prescribed (e.g.,
their training and education or the continuous increase in information preference for prescription of broad-spectrum antibiotics) (Lee et al.,
regarding the adequate use of antibiotics made available by govern­ 2013, 2015). Logically, understanding antibiotic pharmacokinetics,
mental and non-governmental institutions to communicate this issue to pharmacodynamics, toxicity, alternative treatments, and the circum­
human and animal health professional students (Minen et al., 2010; stances in which they are required is essential for antibiotic use reduc­
Gordoncillo et al., 2011; World Health Organization (WHO, 2017). The tion in veterinary practice. Furthermore, New Zealand dairy
finding that longer serving veterinarians are less concerned about anti­ veterinarians indicated the main source of information they took into
biotic resistance emergence in dairy farming is worrisome because they account when prescribing antibiotics for mastitis or dry off treatment
are likely less willing to change their already adopted behaviors and was their own veterinary training (McDougall et al., 2017). This high­
attitudes regarding antibiotic use. For example, others have reported lights what should be the obvious that knowledge is crucial for decision
that changing veterinarians’ behavior is challenging when veterinarians making in antibiotic use. Similarly, knowledge about availability and
are unaware of the consequences of overusing antibiotics, they feel no suitability of diagnostic methods is also a major factor for veterinarians
responsibility for contributing to the antibiotic resistance issue, show no in identifying pathogenic agents and applying an adequate antibiotic
interest in improving their practices, or their practices have become treatment for a particular disease.
routine (Speksnijder and Wagenaar, 2018). Veterinarians’ time limitations and farmers’ lack of interest in
Additionally, more recently trained veterinarians might be more improving behaviors were also factors considered relevant by partici­
receptive to new ideas and regulations regarding judicious antibiotic pating veterinarians. This corroborates previous findings (Friedman
use. Research in the United Kingdom has shown that health students, et al., 2007), where authors noted that lack of time dedicated to seeking
including veterinarians, recognize antibiotic resistance as a matter of out information from veterinarians was a contributing factor driving
upmost importance for their future (Castro-Sánchez et al., 2016; Dyar farmers’ to inappropriately use antibiotics. In other study, veterinarians
et al., 2018). Veterinary students from Australian universities were have experienced resistance from their clients in regards to responsible
knowledgeable about antibiotic resistance and how to properly combat antibiotic practices (Higgins et al., 2017). The combined effects of vet­
it (Hardefeldt et al., 2018a). There is still a perceived need for erinarians’ reluctance or inability to dedicate time to advise their
improvement as 61 % (38/62) of veterinarians working in a veterinary farmers and farmers’ interest in receiving such advice might be leading
teaching hospital in the US perceived that students are not receiving to ineffective communication between veterinarians and their clients. In
appropriate education about the rational use of antibiotics, or that the addition, convincing farmers about the importance of antibiotic use
amount of training is too little or moderate (Ekakoro and Okafor, 2019). reduction in dairy farms might be a time-consuming activity for veter­
However, the scenario could be different for developing countries, as a inarians, even more in cases where farmers are stiff defenders of their
survey in Nigeria found that more than a half of the surveyed students own incorrect beliefs.
showed lower than average knowledge scores in this matter, indicating Opinions regarding the influence of profit in veterinarians’ antibiotic
an urgent need for improved training of veterinarians on antibiotic use prescription behavior are conflicting, with some reports indicating it as a
(Odetokun et al., 2019). As veterinarians have a fundamental role in relevant factor (World Health Organization (WHO, 2001; Grave and
preventing antibiotic resistance development in animals, it is important Wegener, 2006), while most recent evidence support the opposite (De
for veterinary students to be educated in the responsible use of Briyne et al., 2013; Coyne et al., 2014, 2016). Veterinarians are an

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important source of antibiotics for farmers and therefore have an ethical dairy cattle clinics, especially for problematic treatment areas, such as
responsibility to appropriately prescribe these drugs to their clients and mastitis and diarrhea and digestive problems in cows and calves,
advise them on their correct administration. Opportunity to make a respectively. In addition, veterinary students should receive training in
profit from antibiotic sale could therefore create a conflict of interest communication strategies to effectively discuss antibiotic use. Although
and a potential for overuse or overprescription of antibiotics (as also some countries provide training to veterinary students aimed to improve
suggested by our results in Table 6). Whether or not this was the case communication skills (Castro-Sánchez et al., 2016; Ritter et al., 2018),
among veterinarians in our study could not be determined since our this is not the rule for most countries, even in the developed world
study was not designed to compare the income from antibiotics sale and (Cipolla and Zecconi, 2015). Most notably, continuous educational
the actual antibiotic use by a veterinarian. programs focused in improving veterinarians’ communication with their
Participants expressed that their clients exerted pressure on them to dairy clients are almost non-existent (Moore et al., 2016). These pro­
prescribe antibiotics when deemed unnecessary. Farmers often expect grams could not only provide a mechanism for improvement of
veterinarians to include antibiotics in the treatment given to their ani­ communication skills in previously untrained veterinarians, but also
mals, a factor that has been frequently mentioned to influence veteri­ serve as a review and/or update for those who received this kind of
narians to take the inappropriate decision to overprescribe antibiotics instruction before (Cipolla and Zecconi, 2015). Better communication
(McIntosh et al., 2009; Speksnijder et al., 2015a, 2015b; Higgins et al., between veterinarians and farmers could also serve to improve dairy
2017; Hardefeldt et al., 2018b). Indeed, dairy veterinarians from the farmers’ antibiotic use and promote certain attitudes that might factor
Netherlands have expressed the importance of satisfying their clients in into veterinarians’ decision-making on antibiotic treatment (i.e., pres­
maintaining their business and that actions to dissuade farmers from sure to prescribe antibiotics). It is important for veterinarians and
inappropriately using antibiotics could be detrimental in this regard farmers to share a similar idea about antibiotic use practices to better
(Speksnijder et al., 2015b). Additionally, veterinarians also believe that prevent antibiotic resistance emergence in dairy farms and achieve the
some farmers display a lack of interest in changing their beliefs about appropriate antibiotic treatment (Reyher et al., 2017).
antibiotic use, which might create a situation in which veterinarians’
and farmers’ views do not align, thus leading veterinarians to feel the 4.1. Study limitations
need to meet clients’ expectations. In these cases, it is much easier for
the veterinarians to prevent conflict with their clients and avoid the risk It is important to consider that the number of participants included in
of losing their business. this study was limited to veterinarians that are active members of the
Some veterinarians also perceived that there are missed opportu­ NMC and those attending the International Bovine Mastitis Conference
nities for antibiotic use reduction due to limitations in availability and in Milano, Italy, 2018. Therefore, it is possible that bias was introduced
training for current diagnostic techniques (Table 6). Although this by selecting a non-random sample of veterinarians. The study partici­
perception is shared by small animal veterinarians (King et al., 2018), pants may represent a more affluent and educated subgroup of veteri­
the existence of such barrier in the context of large animal medicine narians, given their interest in continuing education through the
needs to be further addressed in future studies. Moreover, farmers’ lack conference and their ability to travel to Italy. Also, the study population
of adoption of preventive measures to reduce the occurrence of disease had an overrepresentation of dairy veterinarians from Italy. Selection
and poor environmental conditions in dairy farms were identified as bias might have been further compounded through the relatively low
important factors leading to overprescription of antibiotics by veteri­ response rate. The direction in which the selection bias could have
narians. The reason for lack of adoption of such preventative measures influenced the results is difficult to predict. However, considering the
could be related to farmers’ budget constraints. Non-dairy farm animal participation by veterinarians from 21 countries with a wide range of
veterinarians from the Netherlands have agreed that economic consid­ years of experience and who served diverse dairy farms, the study is
erations are a major factor in adopting preventive measures to reduce expected to provide useful information about dairy veterinarians,
disease occurrence in livestock animals (Speksnijder et al., 2015a). In particularly in countries/regions with the largest representation (the US,
this study, veterinarians indicated certain situations in which farmers Italy, and the EU as a whole). The study relied on participants’ self-
might be unwilling to reduce antibiotic use through investment in reporting of practices and perceptions, which could have introduced
alternative preventive measures (i.e., vaccination), therefore forcing information bias if participants under or over-reported certain percep­
veterinarians to increase antibiotic prescription in order to control dis­ tions, due to social desirability bias. However, we do not expect that self-
ease outbreaks on farms. reporting would have systematically affected some groups of partici­
Participants from the US and EU also mentioned the absence of pants more than others (e.g., those who are concerned about the
mandatory regulations and oversight by local authorities as a relevant emergence of antibiotic resistance and believe that better labeling of
factor contributing to the overprescribing of antibiotics (Table 6). This is drugs is important to reduce antibiotic use). Therefore, if present, the
somewhat surprising considering that the majority of participants were information bias would be expected to be non-differential and so would
from the US and EU where more strict regulations have recently taken underestimate the strengths of associations. Participants were not pro­
place. The EU member countries, for instance, have strict regulations to vided with a definition of “overprescription” during the survey, meaning
eliminate the use of antibiotics for prevention and restrict their meta­ that their answers include their own understanding of this concept. For
phylactic application (Europe Commission (EC, 2018a; 2018b). This also instance, some veterinarians might understand “overprescription” as
suggests that there is still room for tighter regulatory framework. prescribing larger doses than those indicated on the drug label, pre­
In summary, veterinarians participating in this study believed that scription of antibiotics when infection may not be bacterial, unnecessary
injudicious antibiotic prescription is a prevalent behavior among their prolongation of antibiotic treatment, and/or antibiotic prescription
colleagues, with many reasons being centered around veterinarian- based entirely on farmers’ demand. As this term might be understood
client interactions, as revealed by the thematic analysis. This study did differently by different people, we strongly believe that reaching a
not assess the thought process behind veterinarians’ judgement about consensus on the definition of the term would assist in addressing the
their colleagues (i.e., what factors contributed to their perceptions of issue of antibiotic resistance in the context of large animal medicine.
overprescribing behavior), something that would be interesting to know Confounding bias was controlled through multivariable modeling,
to better understand what veterinarians deem as “injudicious”. These however, potential confounding from unmeasured variables could not
findings also highlight the need for actions to improve antibiotic pre­ be controlled. One such unmeasured variable was the participant’s
scription practices by dairy cattle veterinarians, which can be achieved gender, which unfortunately was not inquired about in the question­
through strategic educational efforts. For instance, opportunities for naire. There was no evidence of participants from the US and EU being
continuing education should be provided for veterinarians working in different with respect to the concern for the emergence of antibiotic

11
S.G. Llanos-Soto et al. Preventive Veterinary Medicine 188 (2021) 105253

resistance on their clients’ farms (the outcome of interest in logistic for their help in distributing the survey.
regression). Having said that, we acknowledge that grouping partici­
pants from the EU countries into a single category in this study may have Appendix A. Supplementary data
oversimplified the diversity among the EU member countries and this
diversity should be subject of future research. Interestingly, further Supplementary material related to this article can be found, in the
comparison of the US and EU participants indicated that the US par­ online version, at doi:[Link]
ticipants had an overrepresentation of senior veterinarians and veteri­ 5253.
narians serving larger dairy farms compared to their EU counterparts
(Supplementary Material, Tables S1 and S2). These discrepancies may References
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