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Dairy veterinarians' perceptions and experts' opinions regarding implementation of antimicrobial stewardship on dairy farms in the western United States

Dale A. MooreDepartment of Veterinary Clinical Sciences, College of Veterinary Medicine, Washington State University, Pullman, WA 99164.

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Craig S. McConnelDepartment of Veterinary Clinical Sciences, College of Veterinary Medicine, Washington State University, Pullman, WA 99164.

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Roselle BuschAntimicrobial Use and Stewardship Program, California Department of Food and Agriculture, Sacramento, CA 95814.

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William M. SischoDepartment of Veterinary Clinical Sciences, College of Veterinary Medicine, Washington State University, Pullman, WA 99164.

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OBJECTIVE

To explore veterinarians' perceptions and veterinary experts' opinions regarding antimicrobial stewardship (AMS) on dairy farms in the western United States.

SAMPLE

20 dairy veterinarians and 9 AMS experts.

PROCEDURES

3 focus group discussions involving 20 dairy veterinarians from California, Idaho, and Washington and an expert opinion study involving 9 North American AMS experts were conducted. During focus group discussions, participants were asked open-ended questions regarding implementation of AMS programs on dairy farms. Discussions were recorded and transcribed for thematic analysis. An asynchronous nominal group process was used for the expert opinion study. Participants were asked to complete a series of 3 online surveys consisting of open-ended questions. Expert opinion data underwent thematic analysis and were compared with results obtained from focus group discussions.

RESULTS

Veterinarian-perceived barriers to implementation of AMS on dairy farms included variable relationships with clients and farm employees, ensuring AMS provided value to the farm, and uncertainty about regulations for monitoring on-farm antimicrobial use (AMU). Veterinarians were willing to accept additional responsibility for AMU provided that protocols were adopted to ensure them more complete control of on-farm AMU and they were compensated. The AMS experts indicated that effective implementation of AMS on dairy farms requires producer buy-in and tools to facilitate treatment protocol development and monitoring.

CONCLUSIONS AND CLINICAL RELEVANCE

Additional veterinary oversight of AMU on dairy farms will require engagement by both veterinarians and producers and practical value-added methods for AMS. Continuing education programs should address treatment protocol development, AMU monitoring strategies, and employee training.

OBJECTIVE

To explore veterinarians' perceptions and veterinary experts' opinions regarding antimicrobial stewardship (AMS) on dairy farms in the western United States.

SAMPLE

20 dairy veterinarians and 9 AMS experts.

PROCEDURES

3 focus group discussions involving 20 dairy veterinarians from California, Idaho, and Washington and an expert opinion study involving 9 North American AMS experts were conducted. During focus group discussions, participants were asked open-ended questions regarding implementation of AMS programs on dairy farms. Discussions were recorded and transcribed for thematic analysis. An asynchronous nominal group process was used for the expert opinion study. Participants were asked to complete a series of 3 online surveys consisting of open-ended questions. Expert opinion data underwent thematic analysis and were compared with results obtained from focus group discussions.

RESULTS

Veterinarian-perceived barriers to implementation of AMS on dairy farms included variable relationships with clients and farm employees, ensuring AMS provided value to the farm, and uncertainty about regulations for monitoring on-farm antimicrobial use (AMU). Veterinarians were willing to accept additional responsibility for AMU provided that protocols were adopted to ensure them more complete control of on-farm AMU and they were compensated. The AMS experts indicated that effective implementation of AMS on dairy farms requires producer buy-in and tools to facilitate treatment protocol development and monitoring.

CONCLUSIONS AND CLINICAL RELEVANCE

Additional veterinary oversight of AMU on dairy farms will require engagement by both veterinarians and producers and practical value-added methods for AMS. Continuing education programs should address treatment protocol development, AMU monitoring strategies, and employee training.

Introduction

In the United States, veterinary oversight of AMU has increased with the implementation of the FDA Veterinary Feed Directive Rule in 2017 and various state initiatives that restrict use of antimicrobials in food-producing animals to therapeutic purposes by prescription only.1 However, substantial gaps in both availability and delivery of AMS education to current and future veterinarians working with food-producing species remain. Antimicrobial stewardship is touted as an important component for reducing the risk of AMR in both human and veterinary medical practice. The Association of Professionals in Infection Control and Epidemiology defines AMS as “a coordinated program that promotes the appropriate use of antimicrobials (including antibiotics), improves patient outcomes, reduces microbial resistance, and decreases the spread of infections caused by multidrug-resistant organisms.”2

Veterinary organizations are developing or have developed AMS guidelines. One such set of guidelines was developed by the AABP and is available to members on their website. The AABP, in consultation with the AVMA and CDC, created bovine-specific practice guidelines based on the cycle of bacterial disease management. The 5 key elements for AMS outlined in the AABP's guidelines include a commitment to AMS by practice leadership, drug expertise, the tracking of drug use in the practice and on client farms, reporting to clients, and follow-up action after monitoring, which may include review of disease prevention programs, diagnosis and treatment protocols, and drug efficacy. Those guidelines were made available online in July 2017 and have been widely circulated to members, but to date there is no information on the implementation rates or impact of the 5 key elements, no specific continuing veterinary medical educational programs available to inform a broader audience, and no insights into the motivations for and barriers to implementation of AMS by practitioners.

Although published information regarding the motivations for and barriers to implementation of AMS specific to cattle practices in the United States is lacking, a recent survey3 of all veterinary practice types in Australia identified the following key barriers to implementation of AMS programs: “a lack of AMS governance structures, client expectations and competition between practices, cost of microbiological testing, and lack of access to education, training and AMS resources.” Key enablers of AMS programs identified in that survey3 were “concern for the role of veterinary antimicrobial use in development of AMR in humans, a sense of pride in the service provided, and preparedness to change prescribing practices.” In a survey4 of companion animal practitioners in the United Kingdom, a Delphi method was used to explore enablers for implementation of AMS practices, and national guidelines, practice-level policies, clinical audits, free continuing education or training programs on AMS, and use of antimicrobial susceptibility test results were the highest weighted factors. In an expert opinion survey5 regarding potential drivers for changing AMU in livestock conducted in Denmark, Portugal, and Switzerland, the 6 key areas identified as enablers of AMS included use of antimicrobial susceptibility test results, identification of treatment failures, knowledge of common diseases that require antimicrobial treatment, on-farm protocol changes focused on AMS, improved farm biosecurity, and additional veterinary education focused on AMS. Even though the results of those surveys3,4,5 make it clear that continuing education programs to address practice-based enablers and barriers are necessary to promote adoption of AMS, there are specific challenges to AMS for dairy practitioners in the western United States, owing to large herd sizes and the multiple levels of employees on those operations, that need to be understood and articulated.6

The purpose of the project described here was to explore dairy veterinarians' perceptions and veterinary experts' opinions regarding implementation of the AABP AMS Guidelines on dairy herds in the western United States. The goal of the project was to take lessons learned from veterinary practitioners and AMS experts and create a continuing education program to promote adoption of AMS principles and practices in the dairy industry.

Materials and Methods

The project consisted of 3 dairy veterinarian focus groups and an expert opinion study. The project was reviewed and provided exempt status by the Washington State University Office of Research Assurances Institutional Review Board (IRB No. 17059).

Practitioner focus groups

Participants—Three focus groups of dairy veterinarians (5 to 9 veterinarians/group) were gathered to explore possible barriers to and enablers of implementation of AMS guidelines on dairy farms in the western United States. In each of 3 western states (California, Idaho, and Washington), a dairy region was chosen as a study site, and dairy veterinarians within the region who were members of the AABP were invited to participate in a focus group. In California, 1 to 2 practitioners from each veterinary practice in the southern portion of the Central Valley that had at least a 70% dairy workload (n = 20) were invited to participate. Fifteen dairy practitioners from a 3-county area in Idaho and all dairy practitioners from 1 county (n = 13) in Washington were invited to participate in the focus groups for their respective states. For each of those 3 states, the mean dairy herd size exceeded 675 cows/herd as of 2018.7 Invitees were recruited by email or telephone communication until at least 5 agreed to a set date and time. Focus group participants were provided a meal and continuing education credit through the Washington State University Continuing Veterinary Medical Education Program Office.

The focus groups were planned discussions designed to promote interaction of similar individuals and obtain their perceptions on AMS in a nonthreatening environment. The methods used to conduct the focus groups were consistent with those previously described.8 Participants were provided the AABP AMS Guidelines document at the beginning of the discussion. An experienced facilitator was employed to ask the research questions, guide the flow of the conversations, and ensure that all participants had the opportunity to contribute. A script of questions that focused on the AABP AMS Guidelines was followed (Supplementary Appendix S1, available at: avmajournals.avma.org/doi/supp/10.2460/javma.258.5.515). Notes were taken by the facilitator and study personnel. At the end of each focus group, participants were surveyed about the experience and whether they had learned anything new during the discussion. Group conversations were recorded, and audio files were transcribed with all identifying information removed.

Analysis of focus group data—The primary investigator (DAM) reviewed the audio recording of each focus group discussion to ensure accuracy and edit the transcript when necessary. Then, the transcripts were read in their entirety, and thematic analysis was used to understand and examine the data and design a code book. The primary investigator coded each transcript line by line to identify data segments for themes and subthemes as described.9 The focus group questions did not guide the thematic analysis. Instead, all transcripts were evaluated for themes or patterns of interest.10 A theme referred to a specific pattern of meaning in the data. Themes could be obvious or implied. Specific criteria about what was and was not coded were the foci of barriers and enablers to adoption of AMS guidelines. An inductive approach was used, whereby themes were derived from the raw data. A qualitative data analysis software programa was used to organize and analyze qualitative data, create a codebook, and apply codes to transcript segments. The transcripts and codebook were then provided to 2 coinvestigators (CSM and RB), who independently reviewed the information to establish reliability of the coding and identify themes. They reviewed each transcript without codes and then with the initial codes. The primary investigator added new codes recommended by the coinvestigators to the codebook and reviewed and recoded the transcripts. Coded sections of text were rereviewed for relevance and placed under agreed-upon overarching themes.

Data from the 3 focus groups were combined into a single data set for analysis. The analysis was designed to describe and quantify coded overarching themes and subthemes that described participants' perspectives and experiences, both common and unique. The importance of coded themes was determined on the basis of the number of references to specific codes, which were summarized to indicate the frequency of discussion about a topic. Specific sections of text were used to represent perspectives and themes.

Expert opinion study

The expert opinion study used a modified, asynchronous nominal group technique.11,12 Materials and presentations provided by the AABP were used to select 25 experts from veterinary academia or otherwise associated with cattle medicine who had spoken at a veterinary conference or published on the topic of AMS or AMU in bovine practice within the previous 5 years. The selected experts were emailed an invitation to participate in the study and offered a $100 honorarium. Invitees who were willing to participate in the study were sent a second email that contained a link to an online surveyb (round 1 survey) that provided a list of the 5 key elements for AMS (key elements) as identified in the AABP AMS Guidelines and asked general open-ended questions about the completeness of that list and for ideas on how to create a continuing education program on AMS that was attractive to veterinary practitioners. Five days later, participants were sent a third email that contained an anonymized summary of responses to the round 1 survey and a link to a second online survey (round 2 survey) that asked open-ended questions regarding potential enablers and barriers to each of the 5 key elements and ideas for how veterinarians might be best able to implement each key element. All responses were evaluated for themes by 2 investigators (DAM and WMS). Each response was then reread and coded for theme. One week later, participants were sent a fourth email that contained a summary of the responses to the round 2 survey and a link to a third survey (round 3 survey) that asked participants to rank each enabler, barrier, and implementation idea for each key element in order from highest (1) to lowest (N). One week later, participants were sent a fifth email that provided an overall summary of the rankings with key learning points gleaned from the survey responses that would be considered for curriculum development. Participants were thanked for their participation and asked to provide feedback on the asynchronous nominal group process. A qualitative data analysis software programa was used to organize data from survey responses. Then, each response was recoded with codes developed for the focus group data in addition to codes created for any newly identified themes.

Comparisons of data obtained from the practitioner focus groups and expert opinion study

The most common ideas and themes identified during the dairy practitioner focus groups and expert opinion study were compared by means of content analysis13 to evaluate congruence or incongruence in the quantity and quality of ideas generated by each method. We hypothesized that both the quantity (number of unique ideas generated) and quality of ideas generated by dairy practitioners during the focus group discussions would be greater than those generated by the experts during the expert opinion study.

Results

Practitioner focus groups

A total of 20 dairy practitioners (15 males and 5 females) participated in the 3 focus groups, which ranged in size from 5 to 9 participants. The duration of the focus group discussions ranged from 65 to 110 minutes. Nine of the 20 (45%) participants had seen or heard about the AABP AMS Guidelines document before the focus group discussion.

Although the focus group discussions were initiated by barrier and enabler questions about each key element, the conversations often diverged and reflected practitioners' concerns about AMU. In general, the participants were willing to provide additional oversight of AMU on dairy farms but perceived some barriers to implementing AMS. Thematic analysis revealed 3 overarching themes among the 517 total references to coded themes identified from the transcripts.

Overarching theme 1—relationships with clients and employees—The first overarching theme was that successful implementation of AMS on client dairy farms was tied to relationships veterinarians had with clients and farm employees. This theme was linked to 4 common subthemes including the strength of relationships and communication, providing value to the client, assuming responsibility for and oversight of on-farm AMU, and being compensated for that work (Table 1). The participants perceived that effective implementation of AMS on dairy farms involving additional veterinary oversight and responsibility would require buy-in from all stakeholders, particularly dairy farm owners and employees, as well as pharmaceutical companies and drug distributors.

Table 1

Summary of overarching themes, associated subthemes, and the frequency with which those subthemes were mentioned in 517 transcribed responses from 3 focus group discussions regarding AMS on dairy farms in the western United States as determined by thematic analysis.

Overarching theme Subtheme Representative comment for subtheme No. (%) of responses related to the subtheme
Relationships with clients and farm employees Strength of relationships and communication These farms are complex. There's a lot of layers. And oftentimes as you get through the layers, you realize that you're talking to managers, middle managers, and employees. 48 (9.3)
Providing value to clients You have to show success or failure of these protocols. 40 (7.7)
Assuming responsibility and oversight for all AMU I can't control the dispensing or the administration of antimicrobials. 49 (9.5)
Getting paid One of the biggest barriers to doing this is getting paid for your time. 17 (3.3)
Tracking and monitoring AMU What to track and how I think the tracking part is going to be one of the hardest things to get producer compliance with. Tracking what they actually used. 73 (14.1)
Treatment protocols I don't get involved as much as I should as far as making protocols and then reevaluating on a regular basis with what they're doing. 45 (8.7)
Use of diagnostic testing (eg, microbiological culture and susceptibility testing) Monitoring pathogens and susceptibility is not commonly done because the pathogen is usually the same. I am surprised they mentioned susceptibility because lab susceptibility is different than field susceptibility. 30 (5.8)
Improving AABP AMS Guidelines Disease prevention They talk … about the entire cycle associated with bacterial disease management, but they really don't talk much about disease management without antimicrobials being involved. The point is, there's a lot of it that takes place before you ever need to pick up a drug. 11 (2.1)
Animal welfare Focus only on reducing AMU ignores that when an animal needs to be treated with an antimicrobial, it should be treated appropriately, quickly and monitored for treatment success. 16 (3.1)
Continuing education Doing trainings in conjunction with producers would be helpful. That would bring the conversations to all the parties involved. 25 (4.8)

A total of 20 dairy veterinarians from California, Idaho, and Washington participated in the 3 focus group discussions (5 to 9 veterinarians/group).

Regarding the subtheme of strength of relationships and communication, focus group participants indicated that their primary role in on-farm AMU was the development of treatment protocols. Participants were not, or only infrequently, involved with treatment decisions for and drug administration to individual cows and calves, and they perceived that as a barrier to AMS. On large dairy farms, farm employees are generally responsible for detecting disease in individual animals and administering drugs on a daily basis. Participants reported that protocol drift on farms was common, and the communication structure on client farms was often multilayered and sometimes ineffective, which made AMS challenging.

Focus group participants had many ideas for improving their on-farm involvement with AMS and providing value to the farm. Those ideas involved reducing a farm's risk for drug residues in milk and cows sent to slaughter, providing drug inventory management services, reducing drug costs, developing treatment protocols, assessing treatment efficacy, training employees, and helping clients maintain product markets. Some participants reported that they were providing drug inventory management services for their clients and developing and tracking treatment protocols, which often provided value to the farm in the form of a decrease in drug use and costs.

Focus group participants perceived that the greatest barrier to the implementation of AMS on dairy farms was their hesitancy to accept complete oversight and responsibility for AMU on those farms owing to the fact that they do not always have knowledge of the drugs being used because they do not dispense or sell those drugs. Many large dairy farms obtain veterinary prescriptions and purchase pharmaceuticals through drug distributors. Although drug distributors are required to report all transactions with farms to the prescribing veterinarian, participants uniformly reported that they do not receive such reports. They also reported variable relationships with pharmaceutical companies and drug distributors. Participants indicated that, although they appreciated the knowledge and benefits that pharmaceutical company personnel provided to their practices, they became frustrated when those individuals provided veterinary advice and treatment recommendations to their clients without an established VCPR or without including them in the conversation. Some participants alluded to frustration with other practitioners in their practice areas in addition to pharmaceutical company personnel. Consequently, some participants were unwilling to accept complete responsibility for AMU on their clients' farms because they perceived that they did not have sufficient control of the antimicrobials available to those farms. Several participants believed that AMU on dairy farms could be reduced if VCPR guidelines were adhered to more closely. Participants also identified compensation for their time and effort as another barrier to the implementation of AMS on dairy farms.

Overarching theme 2—tracking and monitoring AMU—The second overarching theme regarding successful implementation of AMS on dairy farms was associated with tracking and monitoring AMU. This theme was linked to 3 common subthemes including how and what to track in regard to AMU, the need for standardized treatment protocols, and availability of data from diagnostic laboratories (Table 1). Some focus group participants were frustrated with ambiguities associated with potential regulatory requirements for tracking or monitoring on-farm AMU. They wanted clarification regarding what to monitor, how to collect data, and how the information would be used. Participants believed data that focused only on meeting regulatory requirements and that were not useful to farm management would be difficult to obtain and validate. Additionally, participants indicated that data summaries would not accurately reflect the effectiveness of AMS unless they included useful summary metrics focused on animal health outcomes rather than on the amounts of antimicrobials administered. Some participants reported that they did some form of monitoring drug use on farms, such as tracking farm-specific drug inventories, developing computerized treatment protocols and records, and implementing technology to match a treatment protocol to a particular treatment record for an animal.

Although treatment protocols were mentioned in the overarching theme of relationships with clients and farm employees and subtheme of assuming responsibility for AMU, the main context of the discussion surrounding treatment protocols was as a subtheme within the overarching theme of tracking and monitoring. Participants recognized opportunities for and associations between developing treatment protocols and training employees to use, assessing the compliance with, and monitoring the success of those protocols. Most of the participants had clients with whom they had valid VCPRs and for whom they made regular herd visits, developed treatment protocols, and wrote prescriptions for antimicrobials. Once treatment protocols were developed and made available to farm personnel, the extent to which they were assessed for use and compliance varied. Compliance with treatment protocols was dependent on the client. Participants indicated that they had regular conversations about treatment protocols and drug use and reestablished a VCPR contract with some clients on an annual basis. However, they also reported that adjustments or changes to treatment protocols by farm personnel without veterinary input (protocol shift) were not uncommon.

The extent of diagnostic testing performed on farms varied among the focus group participants. Some confessed that they could perform more necropsies and often did not obtain a definitive diagnosis for individual animals. Other participants commented that when they did pursue diagnostic testing (eg, microbiological culture and susceptibility testing), the pathogens isolated were always the same. Several participants described problems with interpreting antimicrobial susceptibility test results, such as the lack of adequate breakpoint information for some drugs and unclear or confusing information provided by the diagnostic laboratory. Diagnostic test results were rarely used to guide changes to treatment protocols.

Overarching theme 3—items not included in the AABP AMS Guidelines—The third overarching theme that arose during the focus group discussions was deficiencies in the AABP AMS Guidelines, which was linked to 3 subthemes including disease prevention, animal welfare, and continuing education (Table 1). Participants believed that the guidelines placed too much emphasis on drug management and not enough emphasis on disease prevention strategies. There was strong support to update the AABP AMS Guidelines to promote the importance of disease prevention strategies and decrease the need for AMU. Participants perceived that the goal of AMS should be to lower morbidity and mortality rates and that disease prevention was more important than treatment in achieving that goal.

Animal welfare and the need for AMU in some animals were also discussed. The idea that less AMU was not the same as judicious AMU came up in multiple discussions. Some participants remarked that the requirements for veterinary oversight of AMU and AMS were focused only on decreasing AMU. However, there are times when animals need to be treated with antimicrobials, and in those instances, animals should receive appropriate antimicrobials promptly and be monitored for response so that the treatment regimen can be modified as necessary.

Continuing education was frequently mentioned as an important aspect for implementation of AMS on dairy farms. Participants believed continuing education programs that brought veterinarians and clients together would facilitate a shared understanding of AMS. Other topics cited for continuing education specific for veterinarians included improving skills for client communication and developing, monitoring, and evaluating the efficacy of treatment protocols.

At the end of each focus group discussion, participants were asked to provide their opinions about the discussion process and list things they had learned from participating. All but 1 participant noted that, as a result of the discussions, they had learned new things that they could apply in their practices. Fifteen of the 20 participants listed 1 or 2 new things they had learned during the discussion (Supplementary Table S1, available at: avmajournals.avma.org/doi/suppl/10.2460/javma.258.5.515); however, there was no common theme identified among the items listed.

Expert opinion study

Twenty-five individuals from across North America with expertise in AMS were invited to participate in the expert opinion study. Sixteen agreed to participate, 14 completed the round 1 survey, and 9 completed the round 2 and 3 surveys. The general geographic location of residence was known for 12 of the 14 experts who participated in the round 1 survey. Five experts resided in the western United States, 3 resided in the southern United States, 2 resided in the upper Midwest, 1 resided in Washington, DC, and 1 resided in Canada.

At the beginning of the nominal group process, participants were asked the following 3 questions that were not included in the focus group process: “Did the AABP AMS Guidelines meet the definition and goals outlined in the document?”; “Are there missing AMS elements in the guidelines?”; and “How should AMS be presented to practitioners to make the topic attractive?” Of the 14 participants who responded to the round 1 survey, 11 agreed that the AABP AMS Guidelines met the definition and goals of AMS as described in the document and 3 disagreed. Six of the 14 respondents noted that a focus on disease prevention to reduce AMU was missing from the document. Many participants indicated that the guidelines should include a statement that veterinarians should provide guidance on practices that will decrease the need for antimicrobials, such as vaccination and good nutritional management. Other suggestions for improving the AMS guidelines were inclusion of recommendations for client and employee education and training on AMU and better use of microbiological culture and susceptibility test results. The most common theme that arose from the nominal group process in regard to making AMS attractive to veterinarians was to demonstrate how it would be of benefit or provide economic value to clients (noted by 5 of 13 participants who responded to this question).

Nominal group responses for each question were coded and summarized after the round 2 survey and a summary set of responses were provided to the participants. The participants were asked to rank the responses by importance as a barrier or enabler for each key element of the AABP AMS Guidelines. The returned rankings were summed, and for each key element, the 4 barriers and 4 enablers with the lowest sums (ie, highest ranked items) were summarized (Table 2) and provided to the participants for further comment. Some participants commented that, although the ranked items were important, AMS was not a priority for most dairy producers. Thus, measures to facilitate AMS on dairy farms were unlikely to be implemented regardless of how reasonable they might appear. Further, participants suggested that incentives would need to be provided by milk purchasers or health department inspectors for dairy producers to invest in and implement AMS. Likewise, adoption of AMS by veterinarians would be facilitated by adequate compensation for their time.

Table 2

Summary of the 4 highest ranked responses to questions about the barriers and enablers to implementation of the 5 key elements outlined in the AABP AMS Guidelines on US dairy farms as rated by 9 experts on AMS who participated in an expert opinion study.

Key element Barriers Enablers
Commitment to AMS by practice leadership
  1. Inertia to change

  2. Time

  3. Lack of rewards, incentives, and compensation

  4. Poor attitude or lack of compliance or buy-in by the client

  1. Review existing client herd health programs

  2. Assign roles within the practice

  3. Collaboration with quality assurance commodity programs to reinforce AMS

  4. Continuous, consistent messages across the industries

Drug expertise
  1. Time

  2. Attitude and practitioner confidence in personal clinical experience

  3. Ease of access to information

  4. Availability of educational resources for some practice areas

  1. Incorporation of AMS in veterinary school curricula

  2. Continuing education opportunities at AABP

  3. Ability to distill information into something practical

  4. Scheduling a practice review every few months (eg, assign an associate to review new information)

Tracking AMU
  1. Data are hard to access or compile

  2. Time

  3. Lack of practitioner expertise in data extraction or manipulation

  4. Recording and summarizing data accurately

  1. Provide veterinarians with a record-keeping system and guideline for approaching clients

  2. Annual publishing and use of data on susceptibility testing and antibiograms from local diagnostic laboratories

  3. Templates for consistent record keeping

  4. Work with clients to implement software programs

Reporting drug use to clients
  1. Accuracy of data

  2. Data are reported in different formats

  3. Variation in case definitions among operations with too much variability in the data for benchmarking

  4. Uncompensated practitioner time

  1. Some type of standardized form (online and mobile) that collects information and ensures privacy

  2. Ensure confidentiality

  3. Be clear that data will benefit everyone

  4. Use similar software platforms across farms

Follow-up action after monitoring
  1. Time

  2. Commitment or buy-in by farm managers and producers

  3. Data inaccuracies

  4. Cost of changes to production practices

  1. Regularly scheduled meetings with clients dedicated to data presentation with solutions to problems identified and praise for progress

  2. Show the economic and animal health benefits of AMS changes

  3. Provide stewardship leaders with program or materials and ideas on a regular basis (eg, the AABP could provide client-friendly AMS materials that practitioners can discuss with clients)

  4. Working with clients to determine reasonable circumstances that should trigger an alarm about AMS

The study used a modified, asynchronous, nominal group technique. Participants completed a series of 3 online surveys 5 to 7 days apart and were provided an anonymized summary of the responses to the preceding survey prior to completing the second and third surveys.

All nominal group responses (n = 104) were reviewed and coded by use of the same codes used for the focus groups transcripts. An additional 8 unique codes were identified. Thematic analysis revealed 3 overarching themes. Interestingly, the 3 overarching themes were the same as those identified in the focus group discussions, but the content differed.

Overarching theme 1—relationships with clients and employees—The first overarching theme identified was that successful implementation of AMS on dairy farms was dependent on the relationship veterinarians had with farm owners and employees. This theme was linked to 2 subthemes including improving relationships through client education and providing value to clients (Table 3). The AMS experts emphasized the importance of positive relationships between veterinarians and clients to facilitate client education. It is critical for veterinarians to interact with clients in a positive manner to gain an understanding of what motivates them to implement new procedures. Also, it is essential that dairy producers buy in to the principles of AMS, otherwise attempts to implement AMS on dairy farms will fail. The experts further noted that continuous open dialogue among veterinarians and all parties on the farm was necessary so that the commitment to AMS is a shared experience. The experts recognized that some dairy clients may expect their herd veterinarian to bend the rules for them and that some veterinary practices might poach dairy clients from other practices by providing the farms prescriptions for various drugs including antimicrobials. The responses provided by the AMS experts did not address the relationships between veterinarians and farm employees beyond the fact that farm employees need training on AMS.

Table 3

Summary of overarching themes, associated subthemes, and the frequency with which those subthemes were mentioned in 104 transcribed responses to open-ended questions provided by the 9 experts on AMS described in Table 2.

Overarching theme Subtheme Representative comment for subtheme No. (%) of responses related to the subtheme
Relationships with clients and farm employees Improving relationships through client education The practitioner needs to be placed in a positive position relative to the client. 14 (13.5)
Providing value to clients The VCPR should result in management meetings with the veterinarian, dairy ownership, and other stakeholders. 17 (16.3)
Tracking and monitoring Templates for records Records vary from farm to farm. There must be an informational technology solution to link all these data. 32 (30.8)
Treatment protocols Need for standardization of protocols, data collection, and evaluation. 21 (20.2)
Diagnostic testing (eg, microbiological culture and susceptibility testing) Data from diagnostic laboratories should be published regularly. 13 (12.5)
Improving AABP AMS Guidelines Continuing education Drug expertise, in my experience, is one of the very weakest links in veterinary education for a variety of reasons. 12 (11.5)
Lack of knowledge or understanding of how to interpret trials.
Disease prevention Bring up how preventive measures, as well as an effective approach for each diagnosis, could reduce drug costs. 10 (9.6)

The expert responses related to providing value to clients focused on economics. On-farm implementation of AMS must provide value to the client and a return for the veterinarian. Experts suggested that economic analyses should be performed to demonstrate how AMS promotes animal and public health as well as economic benefits to both the farm and veterinarian owing to improved animal health and a decrease in drug use. It was also noted that the VCPR between a veterinarian and dairy producer should include regular meetings of stakeholders on the farm. Most experts remarked that direction on disease prevention was lacking in the AABP AMS Guidelines.

Overarching theme 2—tracking and monitoring AMU—Three subthemes were linked to the overarching theme of tracking and monitoring AMU on dairy farms, including the development of templates for records, treatment protocols, and the use of microbiological culture and susceptibility test results (Table 3). The AMS experts suggested there was a need to bridge data collection platforms within and between farms and provide veterinarians and dairy producers with decision-support tools. One expert suggested that because veterinarians have to rely on farm personnel for AMU data, it might be beneficial for a specific software program or method to be designated for collection and storing that data as part of the VCPR contract.

The AMS experts also indicated that the use of templates for treatment protocols and development of tools and approaches for collecting and analyzing treatment information would be beneficial for understanding health outcomes associated with treatment protocols and support AMS. Many experts advocated the use of microbiological culture and susceptibility test results and antibiograms generated by local veterinary diagnostic laboratories for tracking AMR. One expert noted that veterinary diagnostic laboratories should publish antimicrobial susceptibility test data on an annual basis to help inform veterinary practitioners on emerging AMR among pathogens so they can modify empirical AMU and support AMS.

Overarching theme 3—items not included in the AABP AMS Guidelines—Similar to the dairy practitioners who participated in the focus group discussions, the AMS experts indicated that information regarding disease prevention and continuing education efforts was lacking in the AABP AMS Guidelines. Some experts believed that training related to understanding drugs commonly used in clinical practice and interpretation of clinical trials was lacking in most veterinary school curricula and that many veterinarians required continuing education on those topics.

Comparisons between practitioner focus groups and the expert opinion study

Coded responses were compared between the practitioner focus groups (Table 1) and the expert (nominal group) opinion study (Table 3). The most frequent responses for the participants of the focus groups were associated with tracking, assuming AMU responsibility, strength of client relationships, and treatment protocols. The most common responses for the nominal group were associated with tracking, creating templates for records, client value, relationships with clients, drug expertise, continuing education, and a focus on disease prevention. Contrary to the practitioner focus group discussions, the nominal group did not have any discussion about veterinarians' assumption of responsibility for all on-farm AMU. Approximately half of the nominal group noted that producers and veterinarians were jointly responsible for on-farm AMU. The nominal group infrequently mentioned the role of pharmaceutical companies in AMS and the variable relationships that veterinarians have with pharmaceutical companies and did not mention animal welfare or the need to treat diseased animals. Despite the differences noted, the quantity (number of unique ideas generated) and quality of ideas generated by practitioners during the focus group discussions and by experts during the nominal group process were similar albeit with different emphases.

Discussion

A gap addressed in the present report was to define the specific concerns of veterinarians when implementing new guidelines for AMU and identify educational needs of veterinarians necessary to provide additional AMU oversight. The goal of the project was to take lessons learned from veterinary practitioners and experts and create a continuing education program to promote adoption of AMS principles and practices in the dairy industry. In the presence of programs that have established learning outcomes for AMR Core Competencies14 and set criteria for veterinary AMS, government regulators, extension specialists, and veterinary educators wrestle with the development and implementation of AMS education programs. A gap addressed by this report was the identification of specific concerns and education needs of veterinarians who are being asked to implement new guidelines that require them to provide additional AMU oversight on farms. In this project, we invited dairy practitioners in California, Idaho, and Washington to participate in focus group discussions to better understand issues they are dealing with in regard to AMU oversight and challenges associated with implementation of AMS guidelines on dairy farms and determine what they need to support AMS efforts. The dairy practitioners who participated in the focus group discussions indicated that they were willing to take on additional oversight of AMU on client farms but noted some barriers to implementation of AMS. Specifically, those barriers included compensation for time spent on AMS activities, variable relationships with clients and farm employees, the extent of their responsibility for tracking on-farm drug use given that they do not have absolute control of the drugs available and administered to the animals, and insufficient guidelines for on-farm implementation of AMS.

The dairy veterinarians who participated in the focus group discussions as well as the AMS experts who participated in the expert opinion study recognized the importance of buy-in from dairy producers and employees for successful implementation of AMS, but veterinarians believed that they did not have a sufficient relationship or involvement with every client to successfully implement AMS on every client farm. The veterinary literature indicates that veterinarians' relationships with clients and dairy farm employees is critical for implementation of AMS guidelines. In the United Kingdom, farmers who were very aware of AMR were more likely to have regular contact with a veterinarian than were farmers who were less aware of AMR and indicated that they preferred training and education with follow-up by their veterinarian to improve herd health and AMU.15 The farmers of that survey15 also suggested that financial incentives were needed to reduce AMU. In a survey16 of Canadian dairy farmers' satisfaction with and preparedness to adopt veterinarian recommendations after herd health visits, the investigators concluded that veterinarians need to make sure they communicate advice to dairy producers in a way that creates understanding and is within the implementation capabilities of the producers or farm employees on that particular farm. Investigators of a survey17 conducted to investigate relational factors that influence the implementation of veterinary advice by farmers in the United Kingdom concluded that the advice must be meaningful to the farm or farmer in question, the veterinarian must be considered trustworthy, a perceived shared understanding is accurate, and the goals and priorities are explicit and shared. The investigators of that survey17 also noted that, to successfully achieve implementation of their advice, veterinarians should understand a farmer's priorities, motivations, and goals and work in a collaborative way. Although the results of those surveys16,17 were instructive, the mean dairy herd size in Canada18 and the United Kingdom19 (100 to 150 cows/herd) is much smaller than that in the western United States20 (> 1,000 cows/herd), and herd size is an important consideration when interpreting and trying to extrapolate the results of those surveys. For dairy farms in the western United States, the relationship between veterinarian and herd owner remains important but elements of trust, understanding, and collaboration need to extend to the workforce tasked with making health care decisions and implementing AMS.

The veterinarians who participated in the focus group discussions described in the present report noted that, to foster AMS on large dairy farms with multiple layers of employees and consultants, there needs to be communication and agreement among all those who are responsible for AMU on the farm. Results of a survey21 in which semi-structured interviews of farm animal veterinarians in the Netherlands were analyzed revealed themes similar to those identified during the focus group discussions of the present report in regard to conflicting interests related to the prescription of antimicrobials. Veterinarian-perceived barriers to decreasing AMU on farms include pressure from clients, financial reliance on clients, farmers failing to comply with veterinarians' advice, and the professional obligation of veterinarians to relieve animal discomfort.22 During the focus group discussions of the present report, dairy veterinarians remarked on the challenges and complexity of developing treatment protocols for large dairy farms because of the difficulty associated with assessing compliance with those protocols. The multiple layers of employees on large dairy farms makes ensuring protocol compliance challenging.6 Interestingly, these challenges associated with AMS implementation were not specifically noted by the AMS experts during the nominal group process.

Another barrier to adoption of AMS principles by dairy farms and veterinarians assuming more oversight for AMU is that dairy producers and their employees have access to treatment advice from pharmaceutical company representatives and other veterinarians. Those interactions can result in prescriptions and new or modified treatment protocols on a farm without the knowledge of the veterinarian of record who has established a VCPR with that farm. This was a source of frustration for the veterinarians involved in the focus group discussions and identified as an impediment to their having control of AMU on farms. Complete veterinary oversight of on-farm AMU will not be possible unless the requirement for an established VCPR to dispense drugs is enforced. In short, AMS will not work without collaboration across the dairy industry.

During the present project, the participants of both the focus group discussions and expert opinion study indicated that successful implementation of AMS was dependent on the involvement of all stakeholders of a dairy farm. Investigators of a survey22 involving New York dairy producers concluded that the opinions or approval of family, peers, veterinarians, and milk processors were important to a producer's perceived control of prudent AMU. In the Netherlands, the government involved all dairy industry stakeholders when reevaluating its approach to AMS and developed a plan to reduce AMU on dairy farms in the country by use of the RESET Mindset Model.23 The RESET Mindset Model is a behavioral change model that summarizes information from the existing scientific literature to identify action cues to modify human behavior in the following 5 areas: rules and regulations, education and information, social pressure, economics, and tools.23 In accordance with the Dutch RESET Mindset Model for reducing AMU on dairy farms, the government mandated that farmers have a valid relationship with a veterinarian and a herd health plan in place and follow very specific rules regarding AMU.23 The model was applied across the country but was flexible in regard to preferred learning styles and communication and used a mix of stimuli to effect change.23 Antimicrobial use on dairy farms in the Netherlands decreased substantially following implementation of RESET Mindset Model; however, it is likely that the government's ban on the administration of antimicrobials to all dairy cows immediately after the last milking before the dry period (ie, period before parturition during which dairy cows are not milked; blanket dry cow therapy) had the greatest effect on decreasing AMU.23 Although selective dry cow therapy (ie, administration of antimicrobials immediately prior to the dry period only to cows with evidence of an intramammary infection) is an option for all dairy producers, it has not been widely adopted by US dairy producers24 and is not widely recommended by dairy practitioners in the western United States.25 Congruent with the Dutch approach, the findings of the present project suggested that a combination of regulation, education, and new tools was necessary to decrease AMU on dairy farms in the western United States.

Tools for the promotion of AMS on dairy farms mentioned by the experts who participated in the opinion study included the use of microbiological culture and susceptibility test results and antibiograms from local diagnostic laboratories to inform veterinarians on emerging AMR and guide empirical treatments. Suggestions included requiring diagnostic laboratories to regularly report, perhaps on an annual basis, antimicrobial susceptibility test data to monitor for trends in AMR. However, a 2017 survey26 of US veterinary diagnostic laboratories indicated that only about 25% of them reported such summary data on a regular basis. Results of another study27 indicate that use of clinical breakpoints to interpret antimicrobial susceptibility data facilitates prediction of treatment outcomes for individual animals. In contrast, use of epidemiological cutoff values to interpret antimicrobial susceptibility data is useful for surveillance purposes and detection of AMR.27 Clinical breakpoints are not necessarily the same as epidemiological cutoff values; therefore, it is important to understand the purpose of the analysis so that erroneous interpretations can be avoided.27 Although the use of antibiograms for making treatment decisions is becoming increasingly common in human medicine, it is not common in veterinary medicine and may not be applicable in bovine practice unless it is focused on only 1 herd at a time to account for differences in herd management and animal populations among herds.

In the present project, the most frequent criticisms of the AABP AMS Guidelines were that they did not adequately address preventive measures to reduce the necessity for AMU, animal welfare challenges, and the need to engage clients and farm employees in AMS. In a consensus statement on therapeutic AMU, the American College of Veterinary Internal Medicine noted that disease prevention is the first general method to reduce AMR.28 Although the purpose of the present project was not to rewrite the AMS guidelines for cattle practice, the criticisms of currently available guidelines should be used to inform continuing education programs on the topic.

Qualitative research methods are designed to facilitate understanding of a phenomenon from the perspective of individuals who are experiencing it. Qualitative research methods are useful when possible responses to research questions are unknown and when detection of nuances in participants' perspectives is important. Investigators decide which approach will best answer their research questions. The nominal group technique used in the expert opinion study of the present project has also been used for curriculum development and strategic planning.29 Focus groups can explore the depth and breadth of participants' opinions.7 The use of focus groups and thematic analysis in the present project allowed us to explore the barriers to and motivations for implementation of AMS, a topic on which little was known. Qualitative analysis involves immersion into the data and detailed interpretations of the meaning behind the responses. The objective of thematic analysis is to provide a balanced view of the data and its meaning within a particular context of thoughts rather than attaching too much importance to the frequency of coded responses that have been abstracted from their original context.30 Given the nature of the veterinary practices in which the focus group participants worked, we believed that their individual perspectives would reflect the social thinking in their environments. The results of the focus group discussions described here represented the perspectives of the participants, all of whom practiced in California, Idaho, and Washington, and may not be generalizable to dairy practitioners throughout the United States. Additionally, the focus group participants were not randomly selected and were volunteers from regional practices who were willing to spend time discussing AMS. Thus, they may have had stronger opinions regarding AMS than other practitioners, but we believe that addressing the concerns of the focus group participants will likely address the concerns of many other dairy practitioners. The third focus group did not yield any ideas that had not already been discussed in the first 2 focus groups; therefore, we believed we achieved data saturation.

In the field of continuing medical education, program development is often informed by focus groups.31 On the basis of the results of the present project, continuing education on AMS should elaborate overall expectations for on-farm programs and provide specific tools to create value for clients and make it easier to create, provide training on, and implement treatment protocols. Continuing education programs should also include discussion on how to monitor compliance with treatment protocols and track treatments and treatment outcomes and provide guidance on the use of microbiological culture and susceptibility data. Participants of the present project indicated that continuing education programs that involved both veterinarians and their clients was important for delivery of a coherent message on the importance of AMS and the key elements necessary for its successful implementation.

A positive outcome for both the veterinarians who participated in the focus group discussions and AMS experts who participated in the nominal group process was the sharing of ideas within the respective groups. The practitioners who participated in the focus group discussions listed the things they learned and could implement in their practices. The various items listed by the practitioners reflected diverse learning needs and take-home messages identified as important within each group. Ideas were likewise shared, albeit asynchronously, among the participants of the expert opinion study.

Similar themes and concerns emerged from the focus group discussions and expert opinion study despite differences in the volume and nature of the discussions and the regional selection of focus group participants and purposeful section of AMS experts. However, the 2 groups occasionally differed in regard to perceived areas of emphasis for implementation of AMS, and some portion of those differences might be attributed to the regional makeup of the groups. The focus group participants were dairy veterinarians who practiced in California, Idaho, and Washington, whereas the AMS experts were recruited from across the United States and included 1 individual from Canada. Regional differences in the dairy industry and farm characteristics may have contributed to the varying opinions regarding barriers to AMS. However, it is more likely that the difference in survey methods contributed to the differences between groups. Data from the focus groups were collected synchronously and in person, whereas data from the AMS experts were collected asynchronously and anonymously. Thus, at the time the AMS experts were submitting their comments, they remained unaware of the responses from the other participants, which limited comments in real time. The nominal group process was modified to be asynchronous and was very structured. Only 9 of the 25 individuals invited to participate in the expert opinion study completed each stage of the study. A traditional nominal group process reportedly works best with < 12 but > 5 individuals.11 Although less than half of the invitees participated in and completed the expert opinion study, the responses collected during the asynchronous process resulted in very specific comments on how to engage veterinarians in implementing each of the 5 key elements outlined in the AABP AMS Guidelines. Also, the comments generated during the expert opinion study were generally more focused on the questions asked than were the comments generated during the focus group discussions.

On the basis of the information gleaned during the project reported here, we concluded that getting dairy veterinarians in the western United States to provide additional oversight of on-farm AMU will require engaging those veterinarians, their clients, and farm employees in discussions on the importance of AMS and providing them with practical ideas for implementing AMS that will provide value to both the veterinarian and client and help them create and monitor treatment protocols. New tools, such as templates for record keeping, cell phone applications for easy data capture and analysis, and regular updates on evidence-based treatment options, could be developed to help with this effort. All stakeholders, especially dairy producers, need to be engaged in this effort if AMS is perceived as critical and antimicrobials are to continue to be effective for treatment of veterinary patients.

Acknowledgments

Supported by the Washington State University College of Veterinary Medicine Intramural Research Fund and USDA National Institute of Food and Agriculture, Animal Health and Disease Research Capacity Grant (project 1014680).

The authors declare that there were no conflicts of interest.

The authors thank Donald J. Klingborg for facilitating the 3 focus group discussions and Katy Heaton for data management.

Abbreviations

AABP

American Association of Bovine Practitioners

AMR

Antimicrobial resistance

AMS

Antimicrobial stewardship

AMU

Antimicrobial use

VCPR

Veterinary-client-patient relationship

Footnotes

a.

Nvivo 12, QSR International Pty Ltd, Doncaster, Australia. Available at: www.qsrinternational.com/nvivo-qualitative-data-analysis-software/about/nvivo. Accessed Jun 10, 2018.

b.

Qualtrics, Provo, Utah. Available at: www.qualtrics.com. Accessed Jul 18, 2018.

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Contributor Notes

Dr. Busch's present address is the Department of Population Health and Reproduction, School of Veterinary Medicine, University of California-Davis, Davis, CA 95616.

Address correspondence to Dr. Moore (damoore@wsu.edu).