Introduction
Antimicrobial resistance (AMR) is a critical threat to animal and public health. Global estimates suggest that up to 10 million people will die annually from resistant infections by the year 2050 if antimicrobial-prescribing behaviors do not change.1 Of the pathogens identified to be “urgent” or “significant” threats to human health by the CDC, over half have zoonotic potential and some are considered commensal in companion animal species.2 Many of the same or similar antimicrobials are used in human and veterinary medicine, and close contact within households, including behaviors such as sharing food and cleaning up feces, increases the risk of zoonotic infections and may facilitate the transfer of multidrug-resistant bacteria between companion animals and people.3–6 Multiple studies7–11 have documented sharing of antimicrobial-resistant organisms, including extended-spectrum beta-lactamase–producing Escherichia coli and methicillin-resistant staphylococci, between pets and their owners. Given the similarity of pathogens, shared resistance elements, and evidence for interspecies transmission, antimicrobial stewardship (AS) interventions and improved antimicrobial use in companion animal veterinary medicine are critical for the global success of AS.
The AVMA defines AS as “the actions veterinarians take individually and as a profession to preserve the effectiveness and availability of antimicrobial drugs through conscientious oversight and responsible medical decision-making while safeguarding animal, public, and environmental health.”12 The AVMA has also outlined core principles of AS to guide veterinary actions toward this goal.12 However, development of AS programs (ASPs) remains a challenge in veterinary medicine. In human hospitals, ASPs have become the standard of care, as the link between antimicrobial use and the development of resistance is well established, both on a patient and population level.13 Well-designed, evidence-based clinical practice guidelines outlining stewardship activities have been effectively deployed,13 overseen by federal regulations mandating proof of implementation.14 Importantly, human ASPs significantly improve patient outcomes, including reduced healthcare costs, patient morbidity, and mortality.15
In 2015, the AVMA Task Force on Antimicrobial Stewardship in Companion Animal Practice published a commentary describing the importance of AS in veterinary medicine and encouraging veterinarians to adopt strategic principles to slow the progression of AMR.16 However, previous AS efforts in veterinary medicine have largely focused on production animal medicine and potential transfer of resistant bacteria to farm workers and the food supply.17 Recently, the Presidential Advisory Council on Combating Antibiotic-Resistant Bacteria included improved AS within small animals as a priority area for education and intervention.18,19 There is an urgent need to engage the small animal veterinary community in practicing AS. Most veterinary schools actively incorporate AS concepts into courses20; however, the authors’ experience has identified that reinforcement of these concepts during the clinical portion of the curriculum is lacking, and carrying forward these concepts from veterinary professional education to clinical practice after graduation poses additional challenges.
Problem Statement
Small animal AS is increasingly acknowledged as a critical need, but there is little support for ASP implementation within veterinary hospitals, including academic teaching hospitals. There is also a need for research to guide development of evidence-based AS and infection prevention and control (IPC) guidelines. Veterinary students receive variable training in the principles of AS and IPC and are often insufficiently prepared for the day-one reality of AMR in veterinary practice. Despite the presence of expert knowledge in pharmacology, infectious disease, and microbiology within veterinary schools, not all veterinary teaching hospitals have ASPs. Against this backdrop, it is unsurprising that many primary care and specialty practices consider implementing AS practices within their hospitals out of reach. This must change. Veterinary schools must embrace the opportunity to lead by performing research, providing appropriate training for new graduates, and modeling AS principles during clinical training. To accomplish this, increased collaboration is needed to unify AS efforts, promote the establishment and expansion of AS and IPC committees, support professional curriculum and outreach regarding AS, and identify priorities for continued research.
Proposed Solutions
To engage discussion and spark collaboration between veterinary schools, from August 24 to 25, 2023, the University of Minnesota, The Ohio State University, and Tufts University hosted a 2-day in-person small animal AS workshop in Minneapolis, Minnesota. Representatives, including faculty, administrators, pharmacists, and veterinary nurses from 23 US veterinary schools and delegates from government and industry gathered to focus on questions in 3 domains: implementation of clinical ASPs, research opportunities and needs, and education. A half day was devoted to each domain, which included short presentations from invited speakers and small group discussions prompted by key questions to define top-priority issues and concluded with large group discussions to obtain consensus on critical needs and next steps.
This white paper presents findings, recommendations, and plans from the workshop to heighten awareness and promote implementation of AS and IPC practices in academic, specialty, and primary care settings.
Domain 1: implementation of clinical AS and IPC programs
Workshop participants focused on 2 key areas surrounding hospital ASPs: (1) identifying and addressing common barriers to establishment and development of AS and IPC programs in teaching institutions and (2) envisioning how the network established by this workshop would support and expand each institution’s AS and IPC programs. Several consistent themes emerged from group discussions.
The most common barriers identified by groups for the implementation of AS and IPC programs were a lack of resources and limited buy-in from clinicians and staff. A desire for formalized commitment to AS and IPC from institutional leaders was identified by every small group and advanced during the large group discussion as a primary concern. Identified areas of need included dedicated funding, faculty and staff time allocation to manage and implement AS and IPC programs, and establishment of institutional AS policies. Congruent to leadership commitment, the need to garner support from hospital faculty and staff was emphasized. Common phrases identified during the discussion included, “difficult to get clinician buy-in from the entire hospital,” “how do you get everyone on board?” and “I don’t have time to evaluate [AS].” These comments showed the interconnectedness between a lack of leadership and employee engagement. Participants expressed the frustration of grassroots and volunteer-based efforts and the unequivocal need for prioritization of AS activities by hospital leadership and empowerment of a champion and/or committee to facilitate meaningful change. Discussion group recommendations included generating funding through new fees to support hospital AS and IPC and reporting individual antimicrobial use to provide clinicians with evidence-based information regarding their own antimicrobial prescribing.
Another barrier identified was a lack of awareness of AMR and urgency around this topic among the public, prescribing clinicians, and hospital leadership. This undermines the willingness to devote financial and staff resources for AS and reduces clinician engagement with AS efforts. Additional gaps for clinical ASPs included limited evidence-based studies to demonstrate the effectiveness of AS interventions and a desire for standardized procedures, policies, and guidance to be shared across institutions. It was noted that creation of collaborative resources can conflict with many universities’ approaches to faculty promotion and institutional identity (eg, who owns the intellectual property, who should be credited). There were also concerns about providing a consistent AS approach across training sites for institutions employing a distributive model in the clinical year of education (ie, lacking a teaching hospital).
Participants were enthusiastic about networking with colleagues and sharing resources and protocols for improving AS and IPC programs. A cohesive network of AS and IPC champions will help those without programs advocate for the creation of AS and IPC programs and those with established programs advocate for needed resources to further their missions. The groups identified that the first steps to reach this vision include standardized terminology, definitions, and guidelines for minimum standards for AS and IPC programs. Discussion also focused on the potential for an accrediting body to set and maintain these common standards and develop an AS certification program, which might generate enthusiasm and value among veterinary hospitals.
In summary, the workshop participants’ proposed solutions for improved AS and IPC in small animal veterinary settings must include support from institutional leadership, creation of a common set of standards for AS and IPC programs, and collaboration across institutions.
Domain 2: research opportunities and needs
Participants were asked to (1) identify research needs to further AS in small animal medicine and (2) prioritize research needed to support evidence-based prescribing for common infectious diseases. Discussions for both questions overlapped and included a variety of themes.
Research needs most commonly identified by the small groups included evidence-based research to support development of antimicrobial use guidelines intended for animals in multiple care settings, such as primary care, breeding operations, and shelters. Participants highlighted a need for resources (eg, clinical algorithms) to outline when antimicrobials are and might not be necessary. This would support the decision not to treat in situations where veterinarians suspect an antimicrobial is not needed but hesitate to withhold antimicrobials in the absence of evidence-based or consensus-driven resources.
The groups identified that both short-term and long-term clinical outcomes data surrounding antimicrobial use are lacking in small animal practice. Data are needed to understand the impact of prophylactic and therapeutic antimicrobial use and AS interventions, such as watchful waiting (not immediately prescribing antimicrobials for conditions in which the infection may resolve on its own or with supportive care). Optimal outcome data (eg, from noninferiority clinical trials) would inform treatment and prophylaxis duration, especially for common conditions. Use of evidence-based recommendations to shorten treatment durations is an important part of patient care and AS in human healthcare.21 Discussion themes also included the need to develop new antimicrobials, additional drug formulations, and nonantimicrobial alternatives. The group underscored the importance of qualitative behavioral research to support practice change and explore real-world feasibility and impact of AS interventions.
Participants also prioritized pharmacokinetic and pharmacodynamic studies to generate data to improve antimicrobial susceptibility testing, including species- and body site–specific interpretative categories. This will improve laboratory reporting and clinician understanding when selecting antimicrobials on the basis of laboratory results. Gaps in this type of data impede veterinary diagnostic laboratories’ ability to provide interpretation of bacterial culture and susceptibility data with high confidence. In contrast, many expressed that the cost of bacterial culture and susceptibility testing can make this diagnostic test inaccessible to pet owners. Tests that quickly and affordably identify the presence of infection or help to characterize pathogens can support AS initiatives by curtailing just-in-case prescribing and informing empiric drug selection.
Participants identified several barriers to conducting needed research. Funding for small animal studies is limited. No government agency has a mission that primarily focuses on small animal health outcomes and veterinary practice. Intramural and foundation grants are limited and often do not support faculty salaries and indirect costs, making it difficult to pursue small animal research, despite the impact that such research may have on both animals and public health. Beyond funding, additional barriers include a waning pipeline of clinician scientists, given the high cost of veterinary medical education and the relatively low return on investment for additional graduate training. The lack of interoperability of small animal medical health records systems also presents a barrier to large-scale epidemiologic research.
In summary, proposed solutions for research that addresses the gaps in knowledge needed to advance small animal AS include performing collaborative and multi-institutional research to provide evidence for antimicrobial prescribing guidelines and bacterial culture and susceptibility interpretation. Other priorities include supporting the development of new antimicrobials and the assessment of nonantimicrobial therapies. Agencies funding One Health research should include small animals as well as meaningful financial support for the next generation of clinician scientists (eg, fellowships, training grants).
Domain 3: education
Participants discussed efforts to integrate and effectively teach AS within the preclinical and clinical veterinary curricula. Groups were asked to identify (1) barriers and needs to incorporate AS into the preclinical curriculum, (2) strategies to create uniform messaging of AS concepts in the clinical setting, and (3) methods to measure the impact of curriculum or clinical education AS initiatives.
Early introduction of AS concepts into the preclinical curriculum was recommended to provide foundational context for prescribing information taught in later courses. Participants suggested incorporating AS concepts when teaching about common clinical conditions to support student learning and garner enthusiasm for AS from faculty and students alike. Creating elective or extracurricular options, such as microbiology or pharmacy/pharmacology rotations, could augment baseline instruction within the curriculum. There is risk of inconsistent or contradictory messaging when AS concepts are taught in various disciplines within the veterinary curriculum (eg, microbiology, pharmacology, clinical lectures). Emphasis was placed on the need to reinforce AS concepts consistently, meaningfully, and intentionally throughout the curriculum to promote student understanding and retention of best practices. Collaboration between clinicians and basic scientists teaching AMR in the preclinical curriculum is desired, and importantly this interdisciplinary teaching should be continued in clinical training by including microbiologists and clinical pharmacologists/pharmacists in patient rounds.
Presentation of AMR data and prescribing patterns in a large group format, such as hospital grand rounds, is an opportunity to support AS teaching during clinical training. Providing access to tangible resources to support judicious prescribing (eg, posters for student and clinician reference, handouts or videos shown in teaching hospital lobbies for clients) was identified as another opportunity. Participants expressed that students receive widely variable recommendations about antimicrobial use in their clinical training and that reinforcement of concepts taught in the preclinical training is inconsistent. Antimicrobial stewardship programs could serve as support for all aspects of AS education and application to aid in aligning messaging between preclinical and clinical experiences.
Proposed solutions included using resources currently designed for veterinary students (eg, “Antimicrobial Stewardship” modules developed by Cornell University, Texas A&M University, and Oklahoma State University22) across all veterinary curricula to standardize the messaging of AS principles more broadly. Uniform onboarding of individuals entering the clinical space (eg, faculty, staff, students, house officers) to introduce AS principles and resources within the teaching hospital will allow for harmonization between preclinical AS teaching and reinforcement in clinical rotations. Ultimately, there was consensus that clinical veterinary students should observe best empirical prescribing practices in the teaching hospital. Many new graduates will work in private practices without an ASP, and this foundation will support their confidence in continuing and fostering AS-guided prescribing after graduation.
Measurable outcomes are needed to establish the effectiveness of AS education efforts and justify their inclusion within veterinary curricula. Suggestions included standardized postgraduation surveys across academic institutions to assess understanding of antimicrobial selection and AS concepts and longitudinal prescription monitoring after graduation using methods like point-prevalence surveys to document effects on antimicrobial use. Other ideas to estimate success of increasing AS awareness centered around uptake of AS concepts more broadly, such as traffic on websites, downloads of resources, and evaluation of the number of practices expressing a commitment to AS.
Antimicrobial stewardship education must also extend to primary care and specialty private practices. Discussion focused on how practices welcoming veterinary student externships could support AS education. Proposed solutions included providing information outlines to clinics on the veterinary program’s AS curriculum and providing resources on AS. The question was raised whether externship sites should have minimum requirements around AS to reinforce curricular concepts. Other ideas shifted the onus to students by suggesting written reflections on AS practices during externships and encouraging students to ask questions about antimicrobial selection. While the initial focus for AS education will likely occur within the preclinical curriculum, reinforcing learning through clinical teaching and at externship locations is an important goal.
In summary, the group’s proposed solutions to enhance AS education in veterinary schools is the intentional incorporation of AS into all years of the curriculum, including clinical experiences in and outside of the teaching hospital, with collaborative teaching between basic science and clinical faculty. The creation and use of shared resources is recommended to decrease the burden and standardize AS messaging across all veterinary schools.
Future Directions
The network created by this workshop will facilitate progress in developing and implementing AS principles in small animal medicine. With coordination and collaboration, veterinary hospitals can be empowered to overcome barriers and advocate together. This collaboration can also reduce duplicative efforts. Workshop attendees were motivated to create 4 working groups to further key action items regarding veterinary AS: sharing and creating AS resources, antimicrobial use and outcomes research, AS education and outreach, and road maps to creating hospital ASPs. The mission and goals of the working groups are described in Table 1, with agreed-upon priority domains for the 3 focus areas shown in Figure 1.
Working groups created after the inaugural Veterinary School Small Animal Antimicrobial Stewardship Workshop, August 24 to 25, 2023, Minneapolis, Minnesota.
| Working groups and mission | Initial goals |
|---|---|
| Sharing and creating AS resources: to foster a collaborative environment to develop and share resources for the advancement of AS in small animal veterinary medicine |
|
| AU and outcomes research: to advance veterinary AS through multi-institutional collaboration, focusing on innovative research, knowledge sharing, and the development of evidence-based practices to enhance the effectiveness, sustainability, and ethical use of antimicrobials |
|
| AS education and outreach: to advance learning on AS, AU, and IPC through an interinstitutional strategy focused on enhancing veterinary core curriculum and elevating the training of clinicians in teaching hospitals and external veterinary practitioners |
|
| Road maps to creating hospital ASPs: to advance the implementation, development, and improvement of ASPs in veterinary schools, primary care practices, and specialty hospitals |
|
AMR = Antimicrobial resistance. AS = Antimicrobial stewardship. ASPs = Antimicrobial stewardship programs. AU = Antimicrobial use. IPC = Infection prevention and control.
Priorities and urgent needs for domains discussed in the inaugural Veterinary School Small Animal Antimicrobial Stewardship Workshop, August 24 to 25, 2023, Minneapolis, Minnesota. AS = Antimicrobial stewardship. IPC = Infection prevention and control. PK/PD = Pharmacokinetics/pharmacodynamics.
Citation: Journal of the American Veterinary Medical Association 262, 11; 10.2460/javma.24.07.0478
Presently, working groups are independently structured, with each group meeting according to an internally established schedule. A common goal for all working groups is to advance the ideas stemming from the inaugural workshop and sustain working group momentum to the next large meeting. In addition to the working groups, deliverables from the inaugural workshop include the incorporation of an AS day at the 2024 International Society for Companion Animal Infectious Diseases Symposium and the organization of a second AS workshop in 2025.
Future directions include sharing resources and findings from working groups with the broader veterinary community. Engagement with colleagues will be needed to tailor strategies to primary care and specialty veterinary hospitals and veterinary corporate networks. It will also be important to foster relationships and collaborate with individuals working in AS in equine medicine and animal agriculture, in addition to leveraging the expertise and knowledge of physicians and infectious disease pharmacists with established ASPs. A One Health approach is key to maximizing the consistency of veterinary efforts and the success of global AS.
Recommendations
The CDC has identified AMR as 1 of the 4 priority topics of One Health, which also include zoonotic diseases, food safety, and vector-borne infections.23 The working groups aim to further AS progress in veterinary schools and ultimately the larger veterinary community. This progress can advance more quickly with appropriate support. Antimicrobial stewardship and IPC are multidisciplinary fields that require input and expertise in pharmacology, microbiology, infectious disease, and clinical medicine. These efforts benefit from inclusion of all members of veterinary practices from clinicians and nursing staff to administration. We call on funding agencies and the AVMA to enhance support of this mission and prioritize the development of ASPs within small animal hospitals. We call on small animal hospitals to begin AS efforts using resources currently available, including the AVMA handouts, posters, and checklists24; the International Society for Companion Animal Infectious Diseases antimicrobial use guidelines25; the University of Minnesota Handbook of Antimicrobial Stewardship26; and others. Finally, we call on our colleagues and leaders in academia to prioritize AS. We can all contribute to improving antimicrobial use and preserving these life-saving medications for our patients, our families, and future generations.
Acknowledgments
The authors sincerely thank the attendees of the workshop for their active involvement and commitment to antimicrobial stewardship and infection prevention and control. The authors thank the Clinical and Translational Science Award One Health Alliance, Mars Veterinary Health, Zoetis Animal Health, and Merck Animal Health for funding the workshop.
Disclosures
The authors have nothing to disclose. No AI-assisted technologies were used in the generation of this manuscript.
Funding
The workshop was funded by the Clinical and Translational Science Award One Health Alliance, Mars Veterinary Health, Zoetis Animal Health, and Merck Animal Health.
ORCID
C. L. Fellman https://orcid.org/0000-0003-4799-3372
J. L. Granick https://orcid.org/0000-0001-8330-3848
E. R. Bollig https://orcid.org/0000-0002-5997-3208
I. M. DeStefano https://orcid.org/0000-0002-3634-9971
D. Diaz-Campos https://orcid.org/0000-0001-6749-4218
References
- 1.↑
Interagency Coordination Group on Antimicrobial Resistance. No Time to Wait: Securing the Future From Drug-Resistant Infections. WHO; 2019.
- 2.↑
CDC. Antibiotic Resistance Threats in the United States, 2019. US Department of Health and Human Services, CDC; 2019.
- 3.↑
Oh C, Lee K, Cheong Y, et al. Comparison of the oral microbiomes of canines and their owners using next-generation sequencing. PLoS One. 2015;10(7):e0131468. doi:10.1371/journal.pone.0131468
- 4.
Wang MG, Fang C, Liu KD, et al. Transmission and molecular characteristics of blaNDM-producing Escherichia coli between companion animals and their healthcare providers in Guangzhou, China. J Antimicrob Chemother. 2022;77(2):351-355. doi:10.1093/jac/dkab382
- 5.
Jin M, Osman M, Green BA, et al. Evidence for the transmission of antimicrobial resistant bacteria between humans and companion animals: a scoping review. One Health. 2023;17:100593. doi:10.1016/j.onehlt.2023.100593
- 6.↑
Joosten P, Van Cleven A, Sarrazin S, Paepe D, De Sutter A, Dewulf J. Dogs and their owners have frequent and intensive contact. Int J Environ Res Public Health. 2020;17(12):4300. doi:10.3390/ijerph17124300
- 7.↑
Damborg P, Pirolo M, Schøn Poulsen L, Frimodt-Møller N, Guardabassi L. Dogs can be reservoirs of Escherichia coli strains causing urinary tract infection in human household contacts. Antibiotics (Basel). 2023;12(8):1269. doi:10.3390/antibiotics12081269
- 8.
Toombs-Ruane LJ, Benschop J, French NP, et al. Carriage of extended-spectrum-beta-lactamase- and AmpC beta-lactamase-producing Escherichia coli strains from humans and pets in the same households. Appl Environ Microbiol. 2020;86(24):e01613-20. doi:10.1128/AEM.01613-20
- 9.
Chai MH, Sukiman MZ, Liew YW, et al. Detection, molecular characterization, and antibiogram of multi-drug resistant and methicillin-resistant Staphylococcus aureus (MRSA) isolated from pets and pet owners in Malaysia. Iran J Vet Res. 2021;22(4):277-287.
- 10.
Beaulac K, Fellman CL, Wayne AS, McDermott LA, Snydman DR, Doron S. Impact of antimicrobial use in dogs on antimicrobial resistance and shared flora with human owners. Antimicrob Steward Healthc Epidemiol. 2023;3(1):e1. doi:10.1017/ash.2022.323
- 11.↑
Gómez-Sanz E, Ceballos S, Ruiz-Ripa L, Zarazaga M, Torres C. Clonally diverse methicillin and multidrug resistant coagulase negative staphylococci are ubiquitous and pose transfer ability between pets and their owners. Front Microbiol. 2019;10:485. doi:10.3389/fmicb.2019.00485
- 12.↑
AVMA. Antimicrobial stewardship definition and core principles. Accessed June 13, 2024. https://www.avma.org/policies/antimicrobial-stewardship-definition-and-core-principles
- 13.↑
Barlam TF, Cosgrove SE, Abbo LM, et al. Implementing an antibiotic stewardship program: guidelines by the Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America. Clin Infect Dis. 2016;62(10):e51-e77. doi:10.1093/cid/ciw118
- 14.↑
Condition of Participation: Infection Prevention and Control and Antibiotic Stewardship Programs. 42 CFR 482.42 (2023).
- 15.↑
Ohl CA, Luther VP. Antimicrobial stewardship for inpatient facilities. J Hosp Med. 2011;6(suppl 1):S4-S15. doi:10.1002/jhm.881
- 16.↑
AVMA Task Force for Antimicrobial Stewardship in Companion Animal Practice. Antimicrobial stewardship in companion animal practice. J Am Vet Med Assoc. 2015;246(3):287-288. doi:10.2460/javma.246.3.287
- 17.↑
Tang KL, Caffrey NP, Nóbrega DB, et al. Restricting the use of antibiotics in food-producing animals and its associations with antibiotic resistance in food-producing animals and human beings: a systematic review and meta-analysis. Lancet Planet Health. 2017;1(8):e316-e327. doi:10.1016/S2542-5196(17)30141-9
- 18.↑
Presidential Advisory Council on Combating Antibiotic-Resistant Bacteria. Advancing Interprofessional Education and Practice to Combat Antimicrobial Resistance. A Report With Recommendations. US Department of Health and Human Services; 2021.
- 19.↑
Presidential Advisory Council on Combating Antibiotic-Resistant Bacteria. Bridging the Gap: Improving Antimicrobial Access and Use Across One Health. A Report With Recommendations. US Department of Health and Human Services; 2021.
- 20.↑
Beaudoin AL, Bollig ER, Burgess BA, et al. Prevalence of antibiotic use for dogs and cats in United States veterinary teaching hospitals, August 2020. J Vet Intern Med. 2023;37(5):1864-1875. doi:10.1111/jvim.16814
- 21.↑
Spellberg B, Rice LB. Duration of antibiotic therapy: shorter is better. Ann Intern Med. 2019;171(3):210-211. doi:10.7326/M19-1509
- 22.↑
Antimicrobial stewardship: building competencies in judicious use to combat antimicrobial resistance. The Center for Educational Technologies at Texas A&M University. Accessed June 13, 2024. https://www.tamucet.org/curriculum/amr/
- 23.↑
Miao L, Li H, Ding W, et al. Research priorities on One Health: a bibliometric analysis. Front Public Health. 2022;10:889854. doi:10.3389/fpubh.2022.889854
- 24.↑
Antimicrobial use in veterinary practice. AVMA. Accessed June 13, 2024. https://www.avma.org/resources-tools/one-health/antimicrobial-use-and-antimicrobial-resistance/antimicrobial-use-veterinary-practice
- 25.↑
Guidelines and consensus statements. International Society for Companion Animal Infectious Diseases. Accessed June 13, 2024. https://www.iscaid.org/guidelines
- 26.↑
University of Minnesota. Handbook of Antimicrobial Stewardship in Companion Animal Veterinary Settings. University of Minnesota; 2020.
