Introduction
Antimicrobial resistance (AMR) is a growing One Health problem and impacts human, animal, and environmental health. The use of antimicrobial drugs (AMDs) in any setting exerts pressure on bacterial populations to develop AMR, with extra-label or unsupported use of AMDs exacerbating this public health threat.1 AMD use in companion animal medicine (ie, dogs and cats) is often overshadowed by AMD use in human medicine and food animal production.2 However, AMR in companion animal medicine is a growing concern and one of the greatest challenges that veterinary practitioners encounter.2–4
Multidrug-resistant (MDR) bacteria have emerged and spread among companion animals, resulting in animal welfare concerns because of treatment failures and hospital-acquired infections.3 These complications pose economic and emotional hardships for pet owners due to expensive diagnostic testing, longer hospitalizations, and euthanasia due to treatment failure, while veterinary practices that struggle with AMR infections may grapple with economic consequences from reputation decline.2 In addition to the animal health risks, AMR infections in companion animals may also pose a threat to human health through zoonotic disease transmission from animals to humans.5–13 Moreover, some AMDs used in companion animal medicine are also critical to the treatment of infections in human medicine.5,10
Combating antimicrobial resistance in companion animal clinical settings requires antimicrobial stewardship (AMS) practices to optimize the use of antimicrobials.4 The term AMS is used to describe the coordinated efforts and programs required to sustain the clinical efficacy of AMDs, slow the development of AMR, and prevent hospital-acquired infections and adverse effects associated with AMDs in patients.4 The AVMA, International Society of Companion Animal Infectious Disease (ISCAID), and the Centers for Disease Control and Prevention (CDC) have complied general guidelines on AMS. However, companion animal veterinarians are provided with few “cage-side” resources to achieve these goals. Research investigating AMD use in companion animal medicine shows low adherence to prescribing guidelines.14–16 Few programs and studies have been designed to advance AMS in companion animal medicine.17–23
In human medicine, technology is often incorporated into AMS programs through electronic medical records, clinical decision support systems, mobile applications, and social media.24 Integration of these technologies results in interventions, such as dose checking and best practice alerts, antimicrobial time outs, restriction processes, and intravenous to oral dosing monitoring. Additionally, mobile applications and social media promote knowledge-sharing and opportunities to connect with other stakeholders, including patients, specialists, and pharmacists. The advantages of these technologies to promote AMS include opportunities for training, continuing education, colleagues’ support, integration into the workflow, and identifying medical or decision errors. However, the adoption of these technology-based tools requires overcoming barriers such as loss of physician autonomy, alert fatigue, desensitization, workarounds, cost, and IT support.24
This study aimed to qualitatively understand veterinarians’ attitudes, perceptions, and knowledge of AMS programs, explore barriers to AMS resource implementation, and source technological solutions to enhance AMS in practice and overcome barriers to judicious AMD use.
Materials and Methods
Study design and participant recruitment
Focus groups of companion animal veterinarians were formed and conducted in February and March 2021. Veterinarians were initially recruited to participate in the study through the authors’ professional networks and recruitment expanded with a snowball sampling approach and social media outreach. Those who expressed interest in participating were presented various dates and time options to attend a focus group, and the 6 focus groups were formed based on this availability. The study protocol was found to be exempt by the Colorado Multiple Institutional Review Board (COMIRB-Protocol number 21-2721)
Focus group question guide
A semi-structured focus group question guide was developed by the study team based on a scoping literature review of 3 areas: 1) AMD use and stewardship in companion animal medicine, 2) the use of technology in AMS in human medicine, and 3) qualitative research describing AMS in human medicine. The question guide (Supplementary Appendix S1) included open-ended questions with prompts addressing 2 broad categories: 1) experience with AMS and barriers to judicious AMD use and 2) technological solutions that promote stewardship in companion animal medicine. The question guide also included questions about tracking and reporting antimicrobial drug use (AMU) as perceptions of this practice have not been explored among companion animal veterinarians in US. The question guide was piloted with 2 veterinarians (a general practitioner and a board-certified veterinary surgeon) and revised to clarify any areas of confusion.
Conducting focus groups
Before each focus group, informed consent was obtained from each participant. Focus groups were hosted and recorded through Zoom video conferencing software (Zoom Video Communications Inc) and were scheduled for 1 hour. Participants were informed of the purpose of the study and that the session was being recorded. Prior to recording, participants were offered the opportunity to turn off their video function and edit any identifying information. Participants were free to leave the group at any time, however, there was no refusal to participate or early drop-out in any of the groups. Two authors, both companion animal veterinarians with training in qualitative methods (DL and DT) started the focus group session by first introducing themselves and describing their clinical and research backgrounds. Next, they facilitated discussions by asking open-ended questions and stimulating group discussions with subsequent prompt questions. Following each focus group, the research team held debriefing sessions and revised questions as needed. The recorded sessions were downloaded and maintained on a secure server before being transcribed by a third-party transcription service.
Data analysis
Identifying information was removed from the transcriptions prior to data analysis. Transcriptions were analyzed thematically using a grounded theory approach, which allowed theories to emerge through inductive analysis of the data collected during the focus groups.25–27 Two researchers (DL and DT) independently applied initial open codes to the first focus group transcript. These open codes represented concepts related to AMS and aspects of technology that could enhance AMD prescribing. Codes from this initial review were rectified and consensus was reached to create a final codebook, which was applied to the remaining 5 transcripts. After applying these first-level codes to key phrases, codes with overlapping meanings were grouped into higher-level categories and themes. Emphasis was placed on developing themes that could drive sustainable change in the way antimicrobials are used in veterinary medicine. Data collection and analysis continued until no new themes emerged (i.e., Data saturation). Analysis was conducted in NVivo qualitative data analysis software (QSR International). Participants were able to review the draft manuscript and provide feedback prior to submission for peer review.
Results
Twenty-five veterinarians from 11 different states participated in 6 focus groups, with 2 to 6 participants per groups (mean, 4.2). Most veterinarians (64%) currently worked in general practice, followed by emergency medicine (16%), humane organizations (8%), and specialty/referral hospitals (8%). One participant had military veterinary medical experience. Most (64%) participants had 5 or more years of experience (Table 1).
The demographic information from the focus group participants (n = 25) with comparison to the US veterinary workforce in 2018.28
| Characteristic | Participants (n) % | US veterinary workforce (n) % |
|---|---|---|
| Year of graduation from veterinary college | ||
| 1990–1999 | 1 (4.0) | 23,444 (20.7) |
| 2000–2009 | 5 (20.0) | 28,245 (24.9) |
| 2010–2019 | 18 (72.0) | 31,344 (27.6) |
| 2020–2021 | 1 (4.0) | NA |
| Practice type | ||
| General medicine/surgery | 16 (64.0) | 70,526 (70.7) |
| Specialty/referral | 2 (8.0) | 4,988 (5.0) |
| Army | 1 (4.0) | 682 (0.7) |
| Critical care/emergency | 4 (16.0) | 3,636 (3.6) |
| Humane organization | 2 (8.0) | 963 (1.0) |
| Geographic location | ||
| Pacific | 2 (8.0) | 16,921 (14.9) |
| Mountain | 12 (48.0) | 9,919 (8.7) |
| East north central | 5 (20.0) | 16,185 (14.3) |
| East south central | 0 (0) | 6,811 (6.0) |
| West north central | 1 (4.0) | 10,197 (9.0) |
| West south central | 0 (0) | 11,757 (10.4) |
| South Atlantic | 2 (8.0) | 22,939 (20.2) |
| Middle Atlantic | 3 (12.0) | 12,113 (10.7) |
| New England | 0 (0) | 6,002 (5.3) |
| Other territories | 0 (0) | 542 (0.5) |
| Type of position | ||
| Relief | 2 (8.0) | NA |
| Associate | 9 (36.0) | 33,207 (29.3) |
| Owner | 3 (12.0) | 24,159 (21.3) |
| Chief of staff/medical director | 6 (24.0) | NA |
| Intern | 1 (4.0) | NA |
| Unspecified | 4 (16.0) | NA |
Overall, analysis revealed 2 distinct themes: (1) Veterinarians expressed that AMS was important and understood the principles of AMS, but experienced barriers to practicing judicious AMD use principles (Figure 1); (2) Veterinarians felt that technology can promote AMS, but that technology would need to support their prescribing decisions, provide accurate and concise stewardship information, and be integrated into the existing workflow (Table 2).
Conceptual model of factors influencing antimicrobial prescribing behavior of small animal veterinary focus group participants (n = 25) during 6 focus groups.
Citation: Journal of the American Veterinary Medical Association 261, 8; 10.2460/javma.23.02.0100
Summary of the recommendations for an antimicrobial stewardship (AMS) clinical decision support technology from small animal veterinary focus group participants (n = 25) during 6 focus groups with example quotes.
| Theme: Quickly and easily provides information to enhance knowledge | |
|---|---|
| Recommendation | Example participant quote |
| Central database of up-to-date AMS information organized by organ system Integrated into medical records software Provides prompts on correct dose, duration, and route of antimicrobial Flags inappropriate use of an antimicrobial Guidance on antimicrobial choice based on AMR profiles of geographic region Suggests nonantimicrobial treatment options for specific conditions |
“Going back to having a list of specific types of antibiotics for specific body systems, I would love to see that incorporated…it would make their—the arguments go away, arguing with specialists or fellow ER doctors about what’s the best choice for a pet, especially when they’re hopping from doctor to doctor, from day to day during hospitalization. Then there’s not an argument. It’s just fact-based. It’s not emotion-based.” |
| Theme: Supports stewardship decisions | |
|---|---|
| Recommendation | Example participant quote |
| Promotes knowledge sharing amongst hospital stakeholders Improved turn-around time for diagnostic testing results Reduced cost of diagnostic testing Client integration that educates about disease process, AMS, AMR Telehealth to reduce barriers to delayed prescribing |
“I’m a big fan of handouts…if there were handouts that were on the specific conditions that clients oftentimes expect antibiotics for, then I can show them, “Here is another resource that explains why I’m making this decision,” so it backs me up. If there’s some kind of resource that we can easily give to them that uses terminology that they understand, that feels specific enough to their situation, I think that may be helpful.” |
AMR = Antimicrobial resistance.
Antimicrobial stewardship and barriers
Importance of AMS—When asked how they practiced AMS, participants primarily discussed the following: (1) delayed prescribing or withholding antimicrobials, (2) diagnostics to guide the use of antimicrobials, (3) resources such as Plumbs29 and the Bayer Target App,30 and (4) published consensus guidelines to support correct antimicrobial drug use. Few participants discussed having a personal experience with an MDR infection or fearing treatment failure in a patient. Most participants felt a responsibility to safeguard the effectiveness of antimicrobials for humans and future use in their animal patients. All participants reported currently working in a hospital environment without a formal AMS program.
Information and the clinic environment—The participants discussed the difficulty of locating AMS information in the practice environment. Many of the veterinarians discussed asking colleagues for advice on treatment plans because they lacked time to conduct their own research. For example, one veterinarian described receiving advice such as,
“… you ask a peer and they say, ‘Well, I’ve done this in the past and it worked okay,’ and then you just do that because it’s fast-paced and the owner doesn’t want to pay for a culture and you don’t have the time to explain it to them if they aren’t willing to listen or whatever the case may be.”
Participants with fewer years of practice experience discussed a lack of confidence, education, or mentorship on AMS. When presented with a difficult decision to prescribe or withhold antimicrobials, they sought advice from more experienced colleagues. However, the participants worried that colleagues might not provide advice that followed AMS guidelines and feared a lack of support from colleagues in delayed prescribing of an antimicrobial. For example, one veterinarian described confusion caused by conflicting advice, “Our younger doctors will be instructed by some of the doctors that aren’t good at antibiotic stewardship to use things that maybe we shouldn’t.”
The participants discussed that the hospital inventory of medication options influences their ability to practice stewardship. Lack of non-antimicrobial options or lack of first-line antimicrobials prohibited participants from following prescribing guidelines. Practice type also influenced antimicrobial prescribing practices. A veterinarian working in an emergency and specialty hospital stated,
“We are very conscious of our antibiotic use, specifically because our practice tends to be a bit of a fishbowl and all of the other practices in the area will emulate our medicine and model after us. Our medical director thinks it’s very important and we’re constantly rounding cases back and forth to each other.”
Participants discussed that AMS was more prominent when working in a specialty hospital, corporate hospital, or hospital accredited by the American Animal Hospital Association (AAHA).
The veterinary-client relationship—Most veterinarians perceived client behaviors as barriers to antimicrobial stewardship. They felt that costs prohibited owners from approving diagnostic and treatment plans that promoted AMS. One veterinarian discussed,
“You do have so many people that just are not going to pay for the culture. I look up the guidelines then think, “Well, I can’t possibly achieve that, so I’ll just do the best that I can.”
The discussions throughout the 6 focus groups all turned to clients declining important diagnostics such as bacterial culture.
The participants worried about perceived pressure from clients to prescribe an antimicrobial in 2 situations: (1) when diagnostic testing does not show a need for antibiotics or (2) when clients decline diagnostic testing. They felt that clients lacked knowledge and understanding of disease processes, AMR, and AMS. Some participants recalled that clients ask for antibiotics directly. When withholding antibiotics or practicing delayed prescribing, participants feared losing clients to another practice or possible litigation. One veterinarian detailed their fears of withholding antibiotics,
“Let’s say we’ve got a young cat and you know that it’s very unlikely that it’s a bacterial infection and you try to explain that to [the client], that we need to culture and that you’re not going to send them home with antibiotics… then they go down the road, four or five days later because they’re still seeing signs.”
Shelter veterinarians also expressed concern about pressure to prescribe antimicrobials without diagnostic testing, as clients in these settings might be animal rescues or shelter administrators who make decisions about shelter protocols.
Veterinarians felt empowered to withhold antibiotics when they could provide supportive care for the patient’s symptoms. Treatment options such as cough suppressants, probiotics, and anti-diarrheal medications enabled the participants to practice AMS. Experience in practice and confidence in client communication positively contributed to AMS. One participant stated, “I’m going to address the reason why they came in. Oftentimes, the antibiotic is brought up by the doctor as an option, and so I don’t give them that option.” Many participants discussed that their confidence in withholding antibiotics depended on their ability to communicate with the client and their knowledge of nonantimicrobial treatment options.
Solutions using technology to promote antimicrobial stewardship
Quickly and easily provide solutions that enhance their knowledge—When asked about characteristics of a decision support technology, veterinarians wanted a technology that: (1) provides a central database of up-to-date AMS information organized by organ system, (2) is integrated into their medical records software, (3) prompts them on the correct dose, duration, and route for an antimicrobial, (4) flags inappropriate use of an antimicrobial, (5) helps them choose antimicrobials based on the AMR profiles of their geographic location, and (6) suggests nonantimicrobial treatment options for specific conditions (Table 2).
Participants said that software integration was the ideal solution; however, the multitude of programs for medical records makes integration difficult. Additionally, unreliable internet in mobile practice poses a problem for certain practices to use medical records software. Participants suggested mobile applications that update with new information and download to mobile devices. A dynamic technology that could be integrated into the software, accessed from a website, and downloaded on a mobile device would meet the study participants’ needs.
Support stewardship decisions—Technology should aid in forming a hospital culture committed to AMS by allowing for knowledge sharing between colleagues, staff, and animal rescue organizations (Table 2). The participants discussed that technicians communicate with clients about antimicrobials and play a role in their workflow. Paraprofessional staff and animal rescue personnel need to have information written in understandable language. A technology that includes these stakeholders by providing up-to-date information on antimicrobial resistance and prescribing guidelines in lay language will help veterinarians practice antimicrobial stewardship.
Participants hoped for a technology that could enhance their use of diagnostic testing by decreasing the turn-around time for results and reducing costs for owners. Shortening the time frame between seeing a patient and receiving test results would allow the participant to withhold an antimicrobial until the infection is confirmed. Improving client compliance with guidelines through reduced cost of diagnostic testing was important to the participants. Participants also discussed a technology that can support interpreting in-house diagnostic testing.
Participants emphasized the need for technology to support their AMS decisions through client integration. They discussed using handouts to help them communicate with owners. The participants proposed a technology that educates clients about disease processes, AMS, and AMR, and prompts the client to comply with veterinarian recommendations. The participants felt client informational handouts created by a reputable organization and written in accessible language reinforced their decision to withhold antimicrobials (Table 2). Ideally, these education materials and alerts would populate automatically based on the medical record through integration into the technology that aids clinical decision-making.
Two focus groups discussed telehealth as a potential technology solution to overcome barriers to the veterinarian-client relationship. Participants felt telemedicine allows more time to educate the client about AMS. They felt telemedicine reduces the cost of follow-up care for clients, prevents unnecessary appointments through reduced-cost consultations, and improves confidence in delayed antimicrobial prescribing.
Technology that tracks antimicrobial prescribing—Veterinarians supported a technology that tracked their antimicrobial use and compared prescribing between veterinarians. However, participants wanted tracking to support their AMS decision-making (Table 3). The participants felt that tracking and comparing their antimicrobial use data could drive behavior change and promote AMS through supporting their decisions to withhold antimicrobials or use certain first-line antimicrobials more frequently and second-line antimicrobials less frequently. Fears concerning criticism were perceived barriers to adopting a stewardship program that tracked antimicrobial use.
Summary of perceived benefits and barriers to an antimicrobial tracking and reporting program from small animal veterinary focus group participants (n = 25) during 6 focus groups with example quotes.
| Perceived benefits and barriers | Example participant comment |
|---|---|
| Benefit: Provides hospital level AMU and AMR data Barrier: Inappropriate comparisons across regions and practice types |
“I think one of the things that would have to be really, really clear is that we’re comparing apples to apples. We all deal with different populations that have different requirements and different diseases. I think that that would be something that would have to be clear, that there was a way to actually appropriately compare.” |
| Benefit: Learning tool through self-evaluation Barrier: Criticism/judgement |
“I don’t like to be told that I’m doing a ton of things wrong—I don’t think anybody does—but as far comparing and learning, I can push my ego to the side and learn, always.” “I’m thinking of coming from the perspective of constantly having impostor complex, and so I’m always doing everything wrong regardless, so that could be a little bit challenging.” |
| Benefit: Peer influence to support AMS Barrier: Induce fear of prescribing antimicrobials |
“I think potentially, it could change individual behaviors as far as prescribing certain antibiotics if we were to actually see what our peers are doing and what other hospitals are doing.” “You wouldn’t want to discourage someone like a new grad from using antibiotics in a case that needed it.” |
| Benefit: Automated, voluntary, and incentivized Barrier: Extra work/time |
“Being a leader of different vet clinics, getting buy-in from people can be so hard, even if it’s the simplest idea… I think that making something like that as easy to use as possible will improve people using it.” “There needs to be some kind of carrot or guidance or something instead of just seeing where you are on the ranking.” |
AMR = Antimicrobial resistance. AMU = Antimicrobial drug use.
The participants wanted a tracking technology to make appropriate location and practice type comparisons. Concerns about comparing specialty hospitals to general practice emerged because veterinarians felt that their practice environment impacted their ability to practice AMS. Many participants expressed doubts that reports could accurately compare prescribing between similar practice types and that a tracking program would need to be voluntary and incentivized. Suggested incentives included learning opportunities, improving clinical decision-making, or demonstrating the economic importance of stewardship. The program would need to be easy to use and require no effort from the participating veterinarians to collect the data. Participants expressed fears about the time commitment of participating in a tracking program. Practice owner and hospital leadership participants emphasized this barrier to adopting a tracking program (Table 3).
Participants discussed that tracking technology may help to identify emerging AMR threats in their specific area or identify reoccurring infections within their hospital. For tracking to be useful, veterinarians in this study wanted information on regional differences in AMR profiles. They also hoped that tracking antimicrobial use could be accompanied by data on AMR, specifically in the pet population.
Discussion
Companion animal veterinary medicine lacks practical tools to achieve and measure AMS. The multiple stakeholders involved in companion animal veterinary medicine create complex prescribing behaviors that require unique, collaborative solutions. Technology through clinical decision support systems, education for hospital teams and clients, and antimicrobial use tracking can promote initiating, committing, and assessing antimicrobial stewardship activities.
AMS programs would benefit from a method to measure the success of stewardship efforts.3 Tracking antimicrobial prescribing is a potential option for measuring the success of stewardship efforts. Veterinarians in this study accepted having their antimicrobial prescribing tracked but were concerned about comparisons with other doctors. These findings are consistent with previous research, which found that veterinarians at a US veterinary teaching hospital were concerned about compatibility and desired an institution-wide discussion of AMS. However, findings from our study and previous research reveal that communicating data on prescribing behavior to veterinarians could drive changes in prescribing behavior.20
Additionally, providing a report to hospitals or individual veterinarians on their antimicrobial use in a supportive manner and through equal comparisons by geography and practice type may positively advance stewardship goals by providing a social incentive to prescribe judiciously. Throughout the focus groups, participants discussed pressure from colleagues and clients to prescribe antimicrobials. Providing veterinarians with data that supports withholding antimicrobials may serve to dismantle the fear and uncertainty surrounding withholding antimicrobials.
Consensus statements, prescribing guidelines, and pharmacology applications such as the Bayer Target App30 and Plumbs29 provide resources for veterinarians to practice antimicrobial stewardship. However, the participants in this study discuss that integrating these resources, as well as peer-reviewed journal articles, into a clinical decision support system would improve their workflow and help them create a culture of stewardship in their hospital. A real-time technology that allows veterinarians to gain knowledge while working through clinical reasoning will promote behavior change in prescribing habits by reducing barriers due to lack of time, training, and resources. Ekakoro and Okafor14 found that lack of training and fear of litigation were barriers to prescribing judiciously and that continuing education and reading peer-reviewed journals promoted judicious prescribing habits. Participants in the current study echo these challenges and feel that improved access to guidelines through concise, straightforward information will promote their antimicrobial stewardship practice.
Integrating the client’s needs into an AMS technology will allow veterinarians to better partner with their clients and achieve compliance with prescribing guidelines. Previous research has shown that communication skills enable veterinarians to practice delayed prescribing. In a survey of pet owners, Cole and Redding22 found that few pet owners appeared concerned about the risk of AMR, and no owners were concerned that antimicrobials used for people were also used for pets. They also found that owners still wanted their veterinarian to prescribe an antimicrobial when it was unclear whether antimicrobials would be effective. These findings align with the client-related barriers reported in this study. Participants in this study report that time to spend communicating with owners about AMR is limited and strongly indicate that educational tools for clients before, during, and after an appointment will help them prescribe judiciously by enhancing their abilities to communicate their decisions with clients, thereby reducing barriers involving misunderstanding follow-up instructions.
Telehealth may also provide an opportunity for continued care once a client leaves the hospital. Participants in this study perceived client’s understanding of their pet’s illness as a barrier. A study on the impacts of telemedicine in veterinary care found that owners feel more informed about their pets’ illness after consultation with a telemedicine expert.31 Additionally, veterinarians in this study feared client dissatisfaction with delayed prescribing in the absence of an infection. Participants feared not only that clients fail to schedule a follow-up appointment when symptoms persist or worsen but also that clients would resent needing to return for an appointment to re-evaluate their pet. Telemedicine can provide access to medical care after a hospital appointment, reducing these barriers. In a survey of veterinarians during the COVID-19 pandemic, Bishop et al.32 found that veterinarians were dissatisfied with their ability to communicate with clients via telemedicine. However, recent research shows that clients are satisfied with telemedicine appointments and willing to pay for them.31,32 These findings suggest a disconnect between client needs and veterinarian perceptions, indicating room for improvement in the economic viability of telemedicine from the veterinarian’s perspective.
Veterinary medicine should consider the need for lower-cost diagnostics to support veterinarians following AMU guidelines. In a survey of 1,088 veterinarians, 57% reported that the economic limitations of clients impacted their ability to provide quality medical care.33 Improving adherence to consensus guidelines that recommend expensive diagnostic testing, such as cultures and sensitivities, will require addressing the economic limitations of clients in addition to the veterinarian’s education on AMU.
A limitation of our study was the snowball recruitment approach. This approach attracted veterinarians who were aware of AMR in companion animal medicine. This selection bias might have created discussions around valuing AMS and a willingness to participate in AMS. The qualitative nature of the study may limit the generalizability of our results to the larger veterinary population. Further research on veterinarians’ perceived barriers and enablers of AMS among a wider audience may generate additional insights.
Human hospitals employ many different technologies to achieve antimicrobial stewardship, including clinical decision support systems, dose-checking alerts, prescribing restrictions, telemedicine and teleconsultation with specialists, and social media apps for education.24 Participants in this study discuss the utility of these technology interventions to aid in their AMS decision-making. Additionally, human hospitals leverage electronic medication administration records to automate antimicrobial use data submissions to the National Healthcare Safety Network. The National Healthcare Safety Network aggregates, analyzes, and produces reports on antimicrobial use. These reports enable hospitals to measure the success of their antimicrobial stewardship programs. The veterinary medical industry lacks tools to advance antimicrobial stewardship and track antimicrobial use, despite the mounting evidence that AMR infections are a risk to companion animal patients, veterinary hospital staff, and the public.
If left unchecked, companion animal veterinary medical providers may continue to misuse antimicrobials due to barriers and knowledge gaps, jeopardizing human and animal health and compromising the reputation of companion animal medicine. Companion animal veterinary medicine urgently needs tools to initiate, commit, and measure antimicrobial stewardship. This study describes areas where veterinarians face barriers to prescribing judiciously and suggests solutions to these barriers. As in human medicine, veterinarians need centralized information on antimicrobial use, improved access to geographical AMR patterns, and communication support with clients and their hospital teams.
Supplementary Materials
Supplementary materials are posted online at the journal website: avmajournals.avma.org
Acknowledgments
The authors have no conflicts of interest to declare.
We would like to thank all focus group participants for their time and valuable contributions.
References
- 1.↑
Collignon PJ, McEwen SA. One Health—its importance in helping to better control antimicrobial resistance. Trop Med Infect Dis. 2019;4(1):22. doi:10.3390/tropicalmed4010022
- 2.↑
Bengtsson B, Greko C. Antibiotic resistance—consequences for animal health, welfare, and food production. Ups J Med Sci. 2014;119(2):96-102. doi:10.3109/03009734.2014.901445
- 3.↑
Guardabassi L, Prescott JF. Antimicrobial stewardship in small animal veterinary practice: from theory to practice. Vet Clin North Am Small Anim Pract. 2015;45(2):361-376, vii. doi:10.1016/j.cvsm.2014.11.005
- 4.↑
AVMA Committee on Antimicrobials. Antimicrobial resistant pathogens affecting animal health in the United States; 2020. AVMA. Accessed February 3, 2023. https://www.avma.org/sites/default/files/2020-10/AntimicrobialResistanceFullReport.pdf
- 5.↑
Abraham S, Wong HS, Turnidge J, Johnson JR, Trott DJ. Carbapenemase-producing bacteria in companion animals: a public health concern on the horizon. J Antimicrob Chemother. 2014;69(5):1155-1157. doi:10.1093/jac/dkt518
- 6.
Wendlandt S, Shen J, Kadlec K, et al. Multidrug resistance genes in staphylococci from animals that confer resistance to critically and highly important antimicrobial agents in human medicine. Trends Microbiol. 2015;23(1):44-54. doi:10.1016/j.tim.2014.10.002
- 7.
Walther B, Tedin K, Lübke-Becker A. Multidrug-resistant opportunistic pathogens challenging veterinary infection control. Vet Microbiol. 2017;200:71-78. doi:10.1016/j.vetmic.2016.05.017
- 8.
Perreten V, Kadlec K, Schwarz S, et al. Clonal spread of methicillin-resistant Staphylococcus pseudintermedius in Europe and North America: an international multicentre study. J Antimicrob Chemother. 2010;65(6):1145-1154. doi:10.1093/jac/dkq078
- 9.
Rubin J, Walker RD, Blickenstaff K, Bodeis-Jones S, Zhao S. Antimicrobial resistance and genetic characterization of fluoroquinolone resistance of Pseudomonas aeruginosa isolated from canine infections. Vet Microbiol. 2008;131(1-2):164-172. doi:10.1016/j.vetmic.2008.02.018
- 10.↑
Papich MG. Antibiotic treatment of resistant infections in small animals. Vet Clin North Am Small Anim Pract. 2013;43(5):1091-1107. doi:10.1016/j.cvsm.2013.04.006
- 11.
Scott A, Pottenger S, Timofte D, et al. Reservoirs of resistance: polymyxin resistance in veterinary-associated companion animal isolates of Pseudomonas aeruginosa. Vet Rec. 2019;185(7):206. doi:10.1136/vr.105075
- 12.
Vincze S, Stamm I, Kopp PA, et al. Alarming proportions of methicillin-resistant Staphylococcus aureus (MRSA) in wound samples from companion animals, Germany 2010-2012. PLoS One. 2014;9(1):e85656. doi:10.1371/journal.pone.0085656
- 13.↑
Pomba C, Rantala M, Greko C, et al. Public health risk of antimicrobial resistance transfer from companion animals. J Antimicrob Chemother. 2017;72(4):957-968. doi:10.1093/jac/dkw481
- 14.↑
Ekakoro JE, Okafor CC. Antimicrobial use practices of veterinary clinicians at a veterinary teaching hospital in the United States. Vet Anim Sci. 2018;7:100038. doi:10.1016/j.vas.2018.09.002
- 15.
Fowler H, Davis MA, Perkins A, et al. A survey of veterinary antimicrobial prescribing practices, Washington State 2015. Vet Rec. 2016;179(25):651. doi:10.1136/vr.103916
- 16.↑
Taylor DD, Martin JN, Scallan Walter EJ. Survey of companion animal veterinarians’ antimicrobial drug prescription practices and awareness of antimicrobial drug use guidelines in the United States. Zoonoses Public Health. 2022;69(4):277-285. doi:10.1111/zph.12915
- 17.↑
Hardefeldt LY, Gilkerson JR, Billman-Jacobe H, et al. Barriers to and enablers of implementing antimicrobial stewardship programs in veterinary practices. J Vet Intern Med. 2018;32(3):1092-1099. doi:10.1111/jvim.15083
- 18.
Hopman NEM, Portengen L, Hulscher MEJL, et al. Implementation and evaluation of an antimicrobial stewardship programme in companion animal clinics: a stepped-wedge design intervention study. PLoS One. 2019;14(11):e0225124. doi:10.1371/journal.pone.0225124
- 19.
Radford AD, Noble PJ, Coyne KP, et al. Antibacterial prescribing patterns in small animal veterinary practice identified via SAVSNET: the small animal veterinary surveillance network. Vet Rec. 2011;169(12):310. doi:10.1136/vr.d5062
- 20.↑
Redding LE, Muller BM, Szymczak JE. Small and large animal veterinarian perceptions of antimicrobial use metrics for hospital-based stewardship in the United States. Front Vet Sci. 2020;7:582. doi:10.3389/fvets.2020.00582
- 21.
Redding LE, Cole SD. Posters have limited utility in conveying a message of antimicrobial stewardship to pet owners. Front Vet Sci. 2019;6:421. doi:10.3389/fvets.2019.00421
- 22.↑
Redding LE, Cole SD. Pet owners’ knowledge of and attitudes toward the judicious use of antimicrobials for companion animals. J Am Vet Med Assoc. 2019;254(5):626-635. doi:10.2460/javma.254.5.626
- 23.↑
Robbins SN, Goggs R, Lhermie G, Lalonde-Paul DF, Menard J. Antimicrobial prescribing practices in small animal emergency and critical care. Front Vet Sci. 2020;7:110. doi:10.3389/fvets.2020.00110
- 24.↑
Bremmer DN, Trienski TL, Walsh TL, Moffa MA. Role of technology in antimicrobial stewardship. Med Clin North Am. 2018;102(5):955-963. doi:10.1016/j.mcna.2018.05.007
- 26.
Starks H, Trinidad SB. Choose your method: a comparison of phenomenology, discourse analysis, and grounded theory. Qual Health Res. 2007;17(10):1372-1380. doi:10.1177/1049732307307031
- 27.↑
Jeon YH. The application of grounded theory and symbolic interactionism. Scand J Caring Sci. 2004;18(3):249-256. doi:10.1111/j.1471-6712.2004.00287.x
- 28.↑
Ouedraogo FB, Bain B, Hansen C, Salois M. A census of veterinarians in the United States. J Am Vet Med Assoc. 2019;255(2):183-191. doi:10.2460/javma.255.2.183
- 29.↑
Plumb DC. Misoprostol. Plumb’s Veterinary Drugs. Accessed August 15, 2020. https://app.plumbs.com/drug-monograph/vTu5mODx1yPROD
- 31.↑
Roca RY, McCarthy RJ. Impact of telemedicine on the traditional veterinarian-client-patient relationship. Top Companion Anim Med. 2019;37:100359. doi:10.1016/j.tcam.2019.100359
- 32.↑
Bishop GT, Rishniw M, Kogan LR. Small animal general practice veterinarians’ use and perceptions of synchronous video-based telemedicine in North America during the COVID-19 pandemic. J Am Vet Med Assoc. 2021;258(12):1372-1377. doi:10.2460/javma.258.12.1372
- 33.↑
Kipperman BS, Kass PH, Rishniw M. Factors that influence small animal veterinarians’ opinions and actions regarding cost of care and effects of economic limitations on patient care and outcome and professional career satisfaction and burnout. J Am Vet Med Assoc. 2017;250(7):785-794. doi:10.2460/javma.250.7.785
