Pathways to sustainable antimicrobial use in cats

Casey L. Cazer Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY
Department of Public and Ecosystem Health, College of Veterinary Medicine, Cornell University, Ithaca, NY

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Amelia Frye Department of Public and Ecosystem Health, College of Veterinary Medicine, Cornell University, Ithaca, NY

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Jeanne W. Lawless Department of Public and Ecosystem Health, College of Veterinary Medicine, Cornell University, Ithaca, NY

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Lecsy Gonzalez Department of Public and Ecosystem Health, College of Veterinary Medicine, Cornell University, Ithaca, NY

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Claudia Cobo-Angel Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY

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Amelia Greiner Safi Department of Public and Ecosystem Health, College of Veterinary Medicine, Cornell University, Ithaca, NY

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Abstract

Antimicrobial stewardship encompasses all the individual and collective actions that medical professionals take to preserve the efficacy of antimicrobials. It is a one-health problem, affecting animals and humans. The current state of antimicrobial use in cats, particularly (1) the overuse and improper use of cefovecin, which belongs to the third-generation cephalosporin class that is critically important to human health, and (2) use of antimicrobials when they are not needed, poses unsustainable risks of antimicrobial resistance. This paper describes the principles of antimicrobial stewardship and stewardship challenges faced by feline veterinarians, including (1) poor adherence to or awareness of antimicrobial use guidelines, (2) lack of access to affordable diagnostic tests and antibiograms, (3) lack of access to materials and tools for clients that may facilitate more sustainable antimicrobial use and help cat owners understand resistance risks, (4) underestimating the ability of cat owners to administer oral antimicrobials, and (5) limited time and resources to support stewardship efforts. Based on research described in this paper; an original research article by Cazer et al, JAVMA, December 2023; and a Currents in One Health article by Cobo-Angel et al, AJVR, December 2023, several solutions are proposed to advance antimicrobial stewardship in feline medicine. Many of these proposals were expressly requested by veterinarians interviewed in Cazer et al, JAVMA, December 2023. Education and training of veterinarians and cat owners is an essential step toward sustainable antimicrobial use, but it must be complemented with innovations in diagnostic testing, antimicrobial drug development, structural changes, and technological supports.

Abstract

Antimicrobial stewardship encompasses all the individual and collective actions that medical professionals take to preserve the efficacy of antimicrobials. It is a one-health problem, affecting animals and humans. The current state of antimicrobial use in cats, particularly (1) the overuse and improper use of cefovecin, which belongs to the third-generation cephalosporin class that is critically important to human health, and (2) use of antimicrobials when they are not needed, poses unsustainable risks of antimicrobial resistance. This paper describes the principles of antimicrobial stewardship and stewardship challenges faced by feline veterinarians, including (1) poor adherence to or awareness of antimicrobial use guidelines, (2) lack of access to affordable diagnostic tests and antibiograms, (3) lack of access to materials and tools for clients that may facilitate more sustainable antimicrobial use and help cat owners understand resistance risks, (4) underestimating the ability of cat owners to administer oral antimicrobials, and (5) limited time and resources to support stewardship efforts. Based on research described in this paper; an original research article by Cazer et al, JAVMA, December 2023; and a Currents in One Health article by Cobo-Angel et al, AJVR, December 2023, several solutions are proposed to advance antimicrobial stewardship in feline medicine. Many of these proposals were expressly requested by veterinarians interviewed in Cazer et al, JAVMA, December 2023. Education and training of veterinarians and cat owners is an essential step toward sustainable antimicrobial use, but it must be complemented with innovations in diagnostic testing, antimicrobial drug development, structural changes, and technological supports.

Introduction

Antimicrobials improve the lives of humans and animals, but antimicrobial resistance (AMR) threatens to claim up to 10 million human lives a year and cost the global economy trillions of dollars.1 Resistant pathogens and resistance genes do not discriminate between hosts; they can move between humans, pets, domesticated livestock, wildlife, and environmental reservoirs.2 Thus, a one-health approach that considers the interplay between humans, animals, and the environment is essential to combat AMR.

Any use of an antimicrobial, whether it is taken orally by a person, injected into a cat, or sprayed on crops, is an opportunity for the development and selection of AMR in pathogens and commensal bacteria.3 Therefore, all antimicrobial prescribers and end-users must practice antimicrobial stewardship and use antimicrobials carefully to minimize the risk of AMR. Although the volume of antimicrobials used in companion animals is small,4 judicious antimicrobial use (AMU) in dogs and cats is essential not only for their own health but also for human health, as zoonotic transmission of resistant pathogens from companion animals to people is a growing concern.5 For example, pet store puppies treated with antimicrobials caused an outbreak of multidrug-resistant Campylobacter jejuni infections, sickening at least 168 people and hospitalizing one-quarter of them.6

Approximately 10% to 25% of feline veterinary visits in the US include the prescription of an antimicrobial,79 most often to treat urinary, skin, and respiratory diseases.7,9 Unfortunately, many of these prescriptions are for an inappropriate—or less-than-ideal—drug, dosage, and/or duration.10 The most common antimicrobials used in cats are cephalosporins, penicillins, and fluoroquinolones.710 Third-generation cephalosporins (ie, cefovecin) and fluoroquinolones are highest priority antimicrobials that are critically important to human health11; therefore, their use in other species should be minimized whenever possible.3

This article lays out the challenges to sustainable AMU in cats and potential solutions. Addressing these problems will improve feline health and reduce the one-health risk of AMR. The tenets of antimicrobial stewardship, which can be applied to any species, are reviewed as well as potential solutions to stewardship challenges specific to feline practice. These pathways to sustainable AMU draw upon recent research with cat owners and veterinarians; results from this research are presented here to support the identified challenges and potential solutions. A complete description of the surveys of cat owners and interviews of veterinarians can be found in the related article by Cazer et al, JAVMA, December 2023.12

Although antimicrobial stewardship is a global issue, the focus of this article is sustainable feline AMU in the US. Many of the identified barriers and proposed solutions are applicable in other countries and geographical regions. Some aspects of antimicrobial stewardship will vary, such as antimicrobial availability and regulations, AMR surveillance structures, diagnostic testing availability and cost, veterinary education, and cultural practices and beliefs of both cat owners and veterinarians.2

Antimicrobial Stewardship

The fundamental principle of antimicrobial stewardship is that antimicrobial efficacy should be conserved by using antimicrobials only when they are needed to prevent, control, or treat disease.13 Stewardship extends beyond AMU to include disease prevention (eg, vaccination and hygiene), disease diagnosis, nonantimicrobial therapeutics, and evidence-based medicine.13 Once prescribers decide to use antimicrobials, they should seek to optimize the antimicrobial drug (ie, spectrum, generation, and importance to human health), dosage, and duration to balance individual patient health and future antimicrobial efficacy. The US CDC and AVMA outline similar key elements for antimicrobial stewardship, including a commitment to stewardship principles, selecting antimicrobials in accordance with evidence-based guidelines, assessing AMU and reflecting on trends or improvements, and seeking out educational opportunities to improve one’s antimicrobial prescribing.13,14 Antimicrobial stewardship has also been framed as 5 Rs: responsibility (of the prescriber), reduction (in AMU when possible), refinement (of the dosage regimen to minimize resistance), replacement (of antimicrobials by alternative therapeutics when possible), and review (of stewardship initiatives to reflect best practices).3

Specialty medical and veterinary organizations have built upon this framework to make antimicrobial stewardship recommendations and policies specific to their prescribers.15 Antimicrobial stewardship guidelines relevant to small animal veterinarians include the AVMA Antimicrobial Stewardship Definition and Core Principles,13 the American College of Veterinary Internal Medicine Consensus Statement on Therapeutic Antimicrobial Use in Animals and Antimicrobial Resistance,16 and the American Association of Feline Practitioners (AAFP)/American Animal Hospital Association (AAHA) Antimicrobial Stewardship Guidelines.17 Importantly, the AAFP/AAHA guidelines note specific clinical conditions for which antimicrobials are generally not necessary (eg, upper respiratory infections, pancreatitis, lower urinary tract disease, dental prophylaxis and tooth extractions, and acute diarrhea).17

Several challenges persist in implementing antimicrobial stewardship policies for feline medicine. First, veterinarians and veterinary students have limited knowledge of antimicrobial stewardship guidelines.18,19 Lack of knowledge of antimicrobial stewardship, AMU, and AMR has been repeatedly identified as a barrier to stewardship in veterinary medicine.2022

Second, diagnostic testing is underutilized, which can result in “just-in-case” antimicrobial prescribing. Cost, particularly of culture and susceptibility (C&S) testing, is frequently cited as the primary barrier to diagnostic testing in small animal practice.10,21,2325 A downstream effect of high-cost cultures is that antibiograms (ie, summaries of bacterial susceptibilities) may be biased and result in inappropriate empiric antimicrobial choices.

Third, cat owners play an important role in antimicrobial stewardship because they are responsible for antimicrobial administration in outpatient settings, and they play a decision-making role in diagnostics and treatments for their cats. The AAFP/AAHA guidelines and AVMA stewardship definition emphasize that engaging with and educating clients is an essential component of antimicrobial stewardship. Yet in a study26 of pet owners’ overall attitudes toward veterinary care, half of cat owners did not think it was necessary to follow their veterinarian’s recommendations. This disregard suggests substantial room for improvement in veterinary-client communication to enhance antimicrobial stewardship, including better attention to what motivates cat owners to follow recommendations, providing materials for clients about AMR and its relevance to them, suggesting alternatives to antimicrobials, identifying conditions that do not need antimicrobial treatment, and highlighting zoonotic transmission risks.

Finally, antimicrobial stewardship programs require substantial time, expertise, and funds. For example, tracking AMU and AMR is necessary to observe the impact of stewardship interventions, yet it is time and cost-intensive.8,2729 Lack of time and resources were the primary barriers to stewardship activities at US veterinary teaching hospitals.30 Most small animal practices outside of academia do not have the necessary resources or expertise to assess their AMU and compare it to best practices. New investments and approaches in these areas are particularly important to counter time and resource constraints.

Antimicrobial Stewardship Challenges in Feline Medicine

Following AMU guidelines

Whereas antimicrobial stewardship policies lay out the principles veterinarians should consider to preserve antimicrobial efficacy, AMU guidelines offer practical diagnostic and treatment recommendations for common bacterial infections and disease processes. Veterinarians who are aware of AMU guidelines are more likely to recommend antimicrobials appropriately in hypothetical clinical scenarios.19 Unfortunately, many veterinary students and veterinarians have limited knowledge and use of both stewardship policies and AMU guidelines.18,19,22 Several countries and international professional organizations have AMU guidelines for small animal veterinarians that are freely available.3134 The AVMA has summarized the International Society for Companion Animal Infectious Diseases AMU guidelines3537 and Clinical Laboratory Standards Institute antimicrobial stewardship resources into a chart for feline AMU decisions.38 However, there are no US national guidelines. Compared to international guidelines, national-level guidelines can account for national antimicrobial regulation and availability, national or regional infectious disease prevalence, and AMR trends. Veterinary colleges have created college-specific AMU guidelines, which are likely broadly applicable to veterinarians in the US.3941 Veterinarians can find web links for these guidelines in the References list; some guidelines are or include posters that can be posted in veterinary clinics for quick reference,3234,38,41 and one is a phone application.40

These guidelines generally agree that veterinarians should use the most narrow-spectrum antimicrobial that will be effective, use topical over systemic antimicrobials when appropriate, and avoid using antimicrobials that are critically important for human medicine.31 They also list disease processes and diagnoses that typically do not require antimicrobials.31 For cats, this includes 5 areas in which antimicrobials are often wrongly prescribed10,22: (1) lower urinary tract signs without evidence of bacterial infection on urinalysis and/or culture,17,36 (2) upper respiratory signs,17,37 (3) acute diarrhea,17,32,33 (4) clean surgery,32 and (5) periodontal disease.17,33 For example, among feline urinary tract infections treated with antimicrobials at hospitals of 1 veterinary company in 2016, 40% did not have a urinalysis performed or had negative urinalysis results,10 suggesting that antimicrobials were not or may not have been indicated. Besides prescribing an antimicrobial when it was not indicated, veterinarians also picked inappropriate antimicrobial drugs. Only 41% of the antimicrobial prescriptions were for recommended first-line antimicrobials, and most were not for the recommended dosage, duration, and frequency.10 Similar diagnostic test and AMU patterns have been reported in other studies.7,9,42 Most veterinarians and veterinary practices do not have the time or resources to analyze their AMU data and assess guideline compliance,43 which is a hurdle in the path toward antimicrobial stewardship.

Using diagnostic tests to guide antimicrobial choices

AMU guidelines3537 and antimicrobial labels44,45 recommend C&S testing when bacterial infection is suspected, particularly for refractory or recurrent infections. Yet only 14% of recurrent feline urinary tract infections were cultured at practices of 1 veterinary company operating throughout the US in 2016.10 Nearly a quarter of small animal veterinarians in 1 statewide survey reported never ordering C&S.24 The cost, wait time, inability to collect samples, and veterinarians’ lack of knowledge and limited confidence in interpreting C&S test results reduce veterinarians’ abilities to use diagnostic tests to support judicious AMU.

Cost has repeatedly been identified as the primary barrier to C&S testing in small animal practice,10,12,21,2325 and veterinarians think that clients’ limited willingness or inability to pay for diagnostic testing hinders appropriate antimicrobial prescribing.23 According to the AAHA, C&S testing costs pet owners $158 on average, with 25% of clients paying over $200.46 Veterinary practices are paying the laboratory $77 on average for the test,46 indicating a potential for price reduction. The veterinarians interviewed in a related original research article were asked how much they charge for a C&S test12; they typically charged $200 (median; range, $90 to $325). However, when surveyed cat owners were asked how much they would pay for a diagnostic test that would help a veterinarian choose the best antibiotic,12 the median amount cat owners were willing to pay was only $50 (Figure 1). Only 10% of cat owners were willing to pay $200 or more.

Figure 1
Figure 1

Cat owner willingness to pay for a diagnostic test to guide antimicrobial use decisions. Cat owners were asked the following: “Imagine a scenario where your cat may have a bacterial infection, such as a urinary tract infection or skin infection. There is a diagnostic test that will help your veterinarian select the best antibiotic treatment for your cat. This test is beneficial because it will determine whether a particular antibiotic will be able to kill the bacteria causing the infection. Without the diagnostic test, the veterinarian will use their best judgment for selecting an antibiotic, but there is a risk that the treatment will not cure the infection. What is the most that you would be willing to pay for this test?”

Citation: Journal of the American Veterinary Medical Association 261, 12; 10.2460/javma.23.08.0481

A second barrier to C&S utilization is turnaround time,21 which includes shipping to the lab and time for bacterial growth on the initial culture and subsequent susceptibility test. A veterinarian may not receive complete C&S results for 3 or more days after sample collection; thus, results are not available to guide initial antimicrobial decisions. The challenge of turnaround time for C&S was emphasized by one of the interviewed veterinarians in a related original research article12: “cultures are hard because we have to wait 3 days to get those back” (Veterinarian #12).

Feline veterinarians face an additional challenge of collecting a diagnostic sample, particularly with fractious cats, and this may lead to inappropriate or “just-in-case” antimicrobial prescribing. The alternatives that the interviewees mentioned, such as having the owner bring the cat back on another day, possibly with sedatives, require additional cat owner time and effort.

Veterinarian and diagnostic laboratory collaboration

Extensive knowledge is required to select an antimicrobial that will be effective while minimizing the potential for AMR; improved veterinarian-laboratory communication could facilitate better decision-making. Veterinarians should interpret the C&S results with attention to information provided in the laboratory C&S report, susceptibility testing methods, breakpoints, and patient-specific and client-specific factors.47 Breakpoints, used to classify bacteria as susceptible or resistant to an antimicrobial, depend on the antimicrobial clinical pharmacology and are generally specific for bacterial-antimicrobial-host-tissue combinations47; thus, applying breakpoints incorrectly may cause misclassifications of resistance. There are only 43 feline-specific breakpoints for a small subset of pathogens and antimicrobials.48 Breakpoints can be extrapolated from other species (eg, dog or human), but extrapolation may result in inaccurate estimates of in vivo antimicrobial efficacy because of antimicrobial pharmacokinetic differences between host species.47

To improve antimicrobial selection and reduce error, veterinary diagnostic laboratories should indicate when extrapolated breakpoints are used in an antimicrobial susceptibility test report so that veterinarians can consider the extrapolation in their clinical decisions.47 Veterinary laboratories also should ensure they are applying current and correct breakpoints. A survey of veterinary laboratories in the US and Canada found that half of the laboratories applied incorrect breakpoints for pyelonephritis submissions.49 Finally, breakpoints are developed using pharmacokinetic data from a specific antimicrobial dose, frequency, and duration.47 Therefore, veterinarians should prescribe the same regimen used in breakpoint development to ensure that antimicrobial concentrations will be above the minimum inhibitory concentration (MIC) for susceptible bacteria. Breakpoint dosage regimens can be found in breakpoint documents.47,48

Understanding antimicrobial resistance trends, surveillance data, and antibiograms

Ideally, empiric antimicrobial decisions are informed by local or regional antibiograms that summarize pathogen susceptibility to antimicrobials.50 Unfortunately, very few veterinarians have or use an antibiogram.24 Challenges to making antibiograms include the time required to extract data from laboratory or clinical information systems and the expertise needed to analyze susceptibility data.

Antibiograms are created from C&S test results and require representative data. Given the costs to pet owners and long turnaround time, C&S testing is not performed systematically. Testing may be more frequent with chronic cases with poor response to empirical drug therapy, resulting in antibiograms that overestimate AMR and may mislead empiric antimicrobial choices. Additionally, AMR results are often not linked to demographic information or data on prior antimicrobial exposure, which is important to understand AMR trends and their generalizability to other patient populations.50 If veterinarians do use an antibiogram, they should consider the context of C&S test frequency, bias toward resistance, and limited demographic data before changing their empiric antimicrobial strategies. A related AJVR Currents in One Health article addresses these challenges and provides guidance on how veterinarians should use antibiograms.50

Limited collaboration with cat owners on AMU

Similar to other studies, the survey of cat owners in the related article by Cazer et al, JAVMA, December 2023,12 found that owners and cats often find oral administration of medications challenging12,51; they prefer to use antimicrobials with lower cost and greater ease of administration.52 The surveyed cat owners were asked about their experiences requesting antibiotics from their veterinarians.12 Owners requested specific antimicrobial formulations, most often liquid, on the basis of their ability to administer it; if they struggled to administer medications, they seldom asked veterinarians for help. In addition, nearly half of the surveyed cat owners had requested an antimicrobial from their veterinarian in the past and they reported that veterinarians gave them antimicrobials three-quarters of the time.12 These findings reveal an opportunity for improved stewardship and communication among veterinarians and cat owners.

Structural barriers impede cat owner and veterinarian collaboration on sustainable AMU. Veterinarians often feel time pressure in their interactions with clients, which limits their ability to guide cat owners on antimicrobial choices and demonstrate oral antimicrobial administration.20 Veterinarians stock a limited number of antimicrobial drugs and formulations,23 constraining cat owners’ options for palatable and easy-to-administer oral antimicrobials.

The cost of convenience: cefovecin in cats

Veterinarians perceive the difficulty of cat owners administering oral medications to be substantially greater than cat owners report.12 This perception may contribute to the overuse of cefovecin because it is the only parenteral antimicrobial designed for outpatient use in cats and avoids owners having to administer oral antimicrobials. Veterinarians frequently administer cefovecin to cats instead of the recommended first-line oral antimicrobials.7,8,10,42,53,54 Cefovecin is a long-acting third-generation cephalosporin, which is a critically important class of antimicrobials for human health; its overuse poses significant risks for AMR.

Since cefovecin was introduced, resistance to cefovecin in bacteria isolated from dogs and cats has increased.5557 Cefovecin can also select for resistance to related antimicrobials58 and other antimicrobial classes.59 The pharmacokinetics of cefovecin favor the selection of AMR. Cefovecin has a half-life of 6.9 days, so it takes 9 weeks to eliminate 97% of the dose.44 Therefore, subinhibitory concentrations of cefovecin persist for 7 to 8 weeks after the therapeutic duration of 1 to 2 weeks postinjection,44 which can lead to resistance. Susceptible Escherichia coli exposed in vitro to subinhibitory cefovecin concentrations had 8-fold increases in cefovecin MICs, which persisted for at least 6 days after exposure.58 Similar trends have been observed in vivo; healthy dogs treated with cefovecin have an increased prevalence of β-lactam–resistant and tetracycline-resistant gastrointestinal E coli for at least 28 days postinjection.59 Treatment with aminopenicillins or first-generation cephalosporins results in less persistent AMR in dogs,60,61 suggesting that switching to alternative, narrower-spectrum antimicrobials in cats could reduce AMR selection pressure. Cat owners’ varying ability to administer oral medications, veterinarians’ willingness to coach and demonstrate how to medicate cats, veterinarians’ (mis)perception of cat owners’ abilities, and veterinarians’ beliefs about limited drawbacks of cefovecin are hurdles of switching from cefovecin to more appropriate antimicrobials.12

Antimicrobial Stewardship Solutions

Educational interventions

Insufficient education, training, and resources, for both clients and veterinarians, have been repeatedly identified as a barrier to antimicrobial stewardship in veterinary medicine.2022 A variety of strategic, context-aware educational interventions can be implemented to build feline veterinarians’ competency and confidence in antimicrobial stewardship.12 While such interventions hold promise,62,63 there are several challenges in changing veterinarians’ prescribing behavior that require attention to successfully develop and implement impactful training (Table 1). These challenges were drawn from interviews with veterinarians about their AMU practices, as described in the related original research article by Cazer et al, JAVMA, December 2023.12

Table 1

Challenges anticipated in changing veterinarians’ antimicrobial prescribing behaviors. The number following the quotation refers to the individual veterinarian interviewed in the related original research article by Cazer et al, JAVMA, December 2023.12 Quotes have been edited for clarity.

Challenge anticipated Quote
Veterinarians do not view antimicrobial resistance as a problem in companion animals “I think [antimicrobial resistance] is important. As I said, I think [it is important] much more for large animal veterinarians than the small animal veterinarians. But I think there’s also a lot. of resistance. It probably started from human medicine with the overprescription [of] antibiotics also. So, I think [human medicine antibiotic use is] more of a concern than veterinary medicine” (Veterinarian #4).
Antimicrobial prescribing habits are ingrained “I generally don’t ask owners to try to put a pill down the cat’s mouth unless they volunteer that it’s easy for them to do and they’ve done it before” (Veterinarian #5).

“Convenia was a huge thing. If I offer [owners] that antibiotic, almost 90% take that option even though it’s more expensive. ‘I’m not giving that cat a pill, or a capsule, or liquid twice a day. Give them the shot’” (Veterinarian #13).
Educating cat owners takes time, but it can be effective “It took a lot of educating for us to have the owner understand that what they were asking for was not actually going to fix their cat” (Veterinarian #2).

“We had 1 [cat] recently that was getting medication once a day and [the owners would] bring him in, I’d pop the pill down in about 3 seconds and walk away, and they’re [wondering], ‘How did she do that?’

Every family member came in and after a week started giving the cat his meds at home I think after seeing it [done successfully],they learned that [the cat] wasn’t going to hurt them” (Veterinarian #21).
Regulation of antimicrobial use in companion animals is not likely and is not preferred; education is more acceptable “Continuing education [is preferred]. I’m not for the development of any regulations. or laws because those can still be worked around. People have to want to do better” (Veterinarian #17).

“I think it would be hard to do on like a broader level, like FDA changes taking away veterinarians’ right to prescribe certain medications. That’s not going to happen anytime soon. I think having conversations within hospitals, between doctors is very helpful. I think webinars and continuing education is helpful, and also [education in] vet schools; I think a lot of younger vets are more judicious in their antibiotic use” (Veterinarian #3).

First, some interviewed veterinarians expressed the belief that AMR and inappropriate AMU are more of an issue in human medicine and therefore not important in veterinary practice (a conclusion that is incorrect, as AMR and inappropriate AMU are present in veterinary medicine). This mistaken belief has also been observed in veterinary students.18 Second, changing beliefs and habits is hard64,65; AMU is no different. Even when veterinarians know the theoretical best-choice antimicrobial, they do not necessarily make that choice in their daily practice.7 Multilevel interventions need to address risk perception and motivation (ie, answer why a change is worth it), model skills (ie, conversations with clients), and provide structural support to increase the likelihood of a change in AMU.

The ingrained nature of antimicrobial prescribing was evident in the interviews described in Cazer et al, JAVMA, December 2023.12 For example, 1 veterinarian said that they do not ask if cat owners can administer oral medication to their cats, as they assume no one wants to pill a cat (Table 1). Another mentioned that they offer cat owners a choice of cefovecin or oral antimicrobials without context; unsurprisingly, cat owners prefer the convenience of a cefovecin injection. Third, education and training take time. Small animal veterinarians are busy, and time pressures contribute to inappropriate antimicrobial prescribing; such pressures also often preclude continuing education or proactive efforts to educate pet owners.20 Any educational interventions for antimicrobial stewardship must work within this time-pressure constraint and the possibility of veterinarians’ limited perceived need to change behaviors.

Capacity building with veterinarians

In the interviews described in Cazer et al, JAVMA, December 2023,12 veterinarians repeatedly requested training in antimicrobial stewardship rather than new laws or regulations on AMU in small animals (Table 1). However, regulations can be effective at reducing AMU. In some European countries, third-generation cephalosporins (eg, cefovecin) and fluoroquinolones can only be used when a C&S test shows that no lower tier antimicrobials will be effective; this policy reduced the prescription of these drugs by over 90%.66 While continuing education is unlikely to be as impactful as regulation, it is a necessary component of antimicrobial stewardship.

The veterinarians interviewed in Cazer et al, JAVMA, December 2023,12 were asked what the profession can do to impact antimicrobial resistance. When answering this question and others, interviewed veterinarians requested continuing education on several topics, as follows (Table 2): (1) properties and use of cefovecin, including potential harms; (2) AMR in general in veterinary medicine; and (3) alternative treatments (other than antimicrobials). When asked about desired format, the veterinarians preferred in-person continuing education, webinars, or written resources. Fortunately, many written AMU guidelines exist and several are fact sheets or infographics.32,33,41

Table 2

Trainings on antimicrobial use and resistance requested by New York veterinarians or emerging during interviews about antimicrobial administration to cats. Veterinarians’ comments on continuing education arose from multiple interview questions and discussion topics. The number following the quotation refers to the individual veterinarian interviewed in the related original research article by Cazer et al, JAVMA, December 2023.12 Quotes have been edited for clarity.

Training requested Quote
Cefovecin-specific education “We’re left to do our continuing education on our own …
I don’t know that I have really great information [on cefovecin] other than it’s a cephalosporin and I think it lasts 1 to 2 weeks. You can redose after a week if you need to.
It’s the only long-acting injectable antibiotic available for me. I don’t think I have tons of information about it” (Veterinarian #10).
“I think some continuing education would probably be really good. Something titled ‘when should you and should you not use Convenia’… I personally would love to hear something like ‘even though it’s easy to give, you should never use it for this type of infection’ or ‘it’s very unlikely to help here’…
Having a webinar on something like that would be very good … as well as a written source of [information]” (Veterinarian #15).
“I think education about how just blindly using Convenia could be deleterious to patients would be good” (Veterinarian #11).
Antimicrobial resistance “When we have to get our license renewed, maybe having some type of continuing education, or some type of mandatory program that teaches us or reinforces this concept of resistance and what we should be aware of and how we should be speaking to clients.
Especially for the older veterinarians that are more set in their ways … [they] have been practicing a certain way for so long. Something that gets them thinking, ‘Maybe I won’t reach for an antibiotic this time because of just what I heard’” (Veterinarian #18).
Antimicrobial alternatives “I try to give [owners] something else to do … like FortiFlora or a supplement, like lysine … whether or not I think it will actually make a huge difference in the animals’ outcome.
I’m treating the people more than the cat sometimes” (Veterinarian #3).
Antimicrobials are not benign (even though some veterinarians mentioned no potential for harm) “My clients are not generally demanding … if they ask me for an antibiotic, fine, I really don’t think that it could hurt much” (Veterinarian #1).
“[If it is a client that I have a good] relationship with, [I] would tell her maybe you can try [an antibiotic] and see if it works, but it’s unlikely [that the antibiotic will work].
As long as you’re honest with a client, there’s nothing wrong with trying a course of antibiotics as long as it’s not contraindicated” (Veterinarian #16).

Engaging with cat owners

Veterinarians are a trusted source of information for pet owners.25 The cat owners surveyed in the related original research article12 were asked which sources of information they trust about cat health; most selected veterinarians (96% of owners) and veterinary technicians (68%) in their top 3 trusted sources. Veterinarians could significantly impact cat owner AMU through owner education.12 Cat owners have limited knowledge of antimicrobials and AMR,25,52 but when the relationship between AMU and resistance is put in plain language, cat owners consider AMR in their cat care decisions.12 In the survey of cat owners reported in Cazer et al, JAVMA, December 2023,12 cat owners were asked about their AMU preferences. Cat owners overwhelming preferred cefovecin to treat a urinary tract infection when given a choice between different antimicrobial formulations and costs (Figure 2). After reading about cefovecin and amoxicillin and their relative risks of resistance, most cat owners reverse their preferences and are willing to give their cat oral amoxicillin. Cat owners who changed their preference from cefovecin to amoxicillin were concerned about AMR (73%) and willing to give up the “convenience” of cefovecin (23%).

Figure 2
Figure 2
Figure 2

Cat owner preferences for antibiotics to treat a feline urinary tract infection. A—Cat owner preferences on type of medication before antimicrobial resistance information was provided. Cat owners could select from 1 Convenia injection for $25, 1 week of tablets given twice a day for $10 (amoxicillin–clavulanic acid tablets), 1 week of liquid antibiotic given twice a day for $25 (amoxicillin–clavulanic acid oral suspension), and 1 week of liquid antibiotic given once a day for $35 (pradofloxacin oral suspension). No additional information was provided. Count of cat owners is shown on the y-axis. B—Cat owner preference for Convenia or amoxicillin after reading the following information: “Convenia is an antibiotic given as a 1-time injection to a cat by a veterinarian. Use of Convenia in cats may lead to resistant bacteria. These resistant bacteria can cause infections in cats that are very hard to treat and may lead to infections in humans that are hard to treat. Amoxicillin is a different antibiotic. Use of this antibiotic is less likely to cause resistant bacterial infections that are hard to treat. Cat owners must give amoxicillin to their cats orally (by mouth) twice a day as a liquid or tablet, typically for 7 to 10 days.” Earlier in the survey, cat owners were given this definition of AMR: “Antibiotic resistance is when bacteria are no longer effectively killed by antibiotics.” Count of cat owners is shown on the y-axis.

Citation: Journal of the American Veterinary Medical Association 261, 12; 10.2460/javma.23.08.0481

Communication is the most important component of a strong veterinarian–pet owner bond; clear, situationally aware communication results in pet owners following their veterinarian’s recommendations.26 To facilitate effective communication about antimicrobial stewardship between the veterinary team and cat owners, the veterinary team should focus on in-person demonstrations of AMU and provide written or audiovisual materials to clients rather than the verbal advice that was commonly reported by both cat owners and veterinarians.12 Observational learning is a core component of behavior change interventions,67 and demonstrations increase the likelihood of pet owners administering all medication doses.68 In the interviews described in the original research article by Cazer et al, JAVMA, December 2023,12 veterinarians reflected on the importance of demonstrating that the cats could be “pilled” to counter a belief among some owners that it was impossible; 1 veterinarian found that in-person demonstrations build cat owner confidence in oral antimicrobial administration (Table 1).

Veterinarians often need to respond to “just-in-case” requests and pressure for antimicrobials. Over 90% of pet owners want to give their pet an antimicrobial “just in case.”25 Providing information to cat owners on other factors contributing to a cat’s symptoms is important for responding to client pressure for antimicrobials, particularly when there is not a confirmed diagnosis and the efficacy of an antimicrobial for a cat’s problem is uncertain. Veterinarians may find the British Small Animal Veterinary Association “no antibiotic prescription required” handout useful for educating clients in these scenarios and providing nonantimicrobial recommendations.32 In the interviews with veterinarians described in Cazer et al, JAVMA, December 2023,12 several effective strategies emerged for responding to client pressure for antimicrobials (Table 3). One veterinarian mentioned delayed prescribing, in which the veterinarian will prescribe antimicrobials if there is no improvement after a few days; this can be an effective approach to pressure to prescribe antimicrobials17 and has reduced AMU in human health care.69

Table 3

Communication strategies for discussing antimicrobial use with cat owners that emerged from interviews with New York veterinarians. The number following the quotation refers to the individual veterinarian interviewed in the related original research article by Cazer et al, JAVMA, December 2023.12 Quotes have been edited for clarity.

Strategy Quote
Anticipate cat owner concerns “I’ve usually explained to [the owner] why I’m not giving [antibiotics] before they have a chance to say that they were expecting to get one. I’m anticipating what’s going to happen and getting right into [explaining that] these are viral [infections], [there is] nothing we can do to make [it] go away. We can do supportive care” (Veterinarian #15).
Be prepared for “frequent flyers” “If it’s a client coming in several times a year, I impress upon the client that type of discussion [about antibiotic overuse] ... If they’ve come in once in 5 years with a sick cat looking for an antibiotic, I might not be as quick to jump to that discussion as I might with a frequent flyer” (Veterinarian #1).
Explain why antimicrobials are not indicated and offer alternative treatment if appropriate “I think it really is helpful for the clients to understand why we’re saying no … there are other things in that scenario that we are often offering the patient and the client as treatments that are not antibiotics. I think both of those really help the client get off of the antibiotic train if you can offer them something different that will be appropriate and will help the patient and explaining to them why we’re not using antibiotics” (Veterinarian #2).
“A lot of times when a cat comes in with some kind of symptom, [the owners] want something, they don’t want to [be told] ‘just go home and watch and wait.’ I can say … ‘it’s not a bacterial infection in the bladder, it’s inflammatory, here’s some anti-inflammatories because an antibiotic’s not going to work.’ As long as you explain things, I think the owners are accepting it” (Veterinarian #6).
Explain the benefits of diagnostic testing “Hopefully we’ve been able to do some diagnostic, even just basic urinalysis to see if that supports [antibiotic use]. I try to explain to [owners] our diagnostic options and whether that supports use of an antibiotic” (Veterinarian #1).
Explain differential diagnoses and which ones do not need antibiotics “[Owners] want the antibiotics, but there’s no infection, and then we discuss lifestyle management and what [feline lower urinary tract disease] actually means and how it’s not a urinary tract infection” (Veterinarian #3).
“If it’s not likely infectious, then we probably shouldn’t [use antibiotics]. [I] try to explain that to the owners and explain all the other possible things that might be going on causing the symptoms” (Veterinarian #5).
Delayed prescribing “I try to say to my clients, ‘You don’t necessarily have to come back if you end up needing an antibiotic, you can call me.’ I’m not going to demand you come for an in-person recheck and make your cat go in the car again and puke in the carrier and you take off time from work just to get to the antibiotic. If you need it in 2 days, 3 days, 5 days, whenever this infection shows up, you can call me” (Veterinarian #10).

In addition to verbally responding to client pressure, other materials can be useful to build client understanding, especially when time is limited. Resources for clients should cover the following topics, written at a sixth-grade reading level and with audio and/or visuals wherever possible to increase understanding and effectiveness: (1) the basic principles of AMR and how it relates to their cat’s well-being, as this was a primary concern from the cat owner surveys; (2) potential transmission routes of resistant bacteria between humans and cats; (3) antimicrobial and nonantimicrobial therapeutics for common diseases; (4) situations when antimicrobials are not needed; (5) risks of long-duration injectable antimicrobials; (6) tips for administering oral antimicrobials to cats; and (7) diagnostics, including the purpose, benefit, and cost of each test.

Structural approaches to veterinary-client interactions for stewardship

Having longer appointment times, a wider array of antimicrobial formulations, and stocking tools for clients (ie, pill pockets) can increase the likelihood that owners can successfully medicate their cat. Veterinarians want at least 20 minutes for sick pet appointments, and nearly 20% prefer at least 30 minutes.70 Having sufficient time available for diagnostic and treatment discussions is essential for antimicrobial stewardship; veterinary practices should strive to schedule appointment times accordingly and charge appropriately for the veterinary team’s time.

Effectively using available resources is another component of stewardship. The role of veterinary technicians in antimicrobial stewardship has not been sufficiently studied. Although the AVMA recommends engaging all practice members in stewardship, it does not identify specific roles or responsibilities for veterinary technicians or speak to their stewardship training.13 Veterinary technicians could have a significant impact on antimicrobial stewardship in feline medicine through their work as pharmacists, diagnosticians, pet advocates, and pet owner educators. Veterinary technicians can collaborate with veterinarians to ensure antimicrobials are dispensed with dosages and durations that align with breakpoint dosage regimens and AMU guidelines. Technicians collect diagnostic samples and conduct in-house diagnostic testing, including cytology and urinalysis, to inform AMU decisions. Importantly, veterinary technicians can spend time educating clients and showing them how to give oral antimicrobials to cats. Previous research has found that clients are more engaged when pet care decisions include both veterinary technicians and veterinarians.71

Finally, veterinary practices should stock and sell tools to make oral antimicrobial administration easy for cat owners. This minor environmental change will make it easy to engage cat owners in demonstrations of oral antimicrobial administration. This practice eliminates a step to cat owners actually buying and using that support. One of the interviewees from the study described in Cazer et al, JAVMA, December 2023,12 described how their practice empowers cat owners to medicate their cats: “We sell every variety of pill pockets. I show [cat owners] how you can hide [medications] in those. Our techs are really good; they’ll demonstrate pill shooters and syringes” (Veterinarian #12).

Diagnostic test innovations

C&S testing costs to pet owners need to be reduced for veterinarians to fully use C&S testing as a diagnostic tool in antimicrobial decision-making. This reduction could take the form of subsidies (eg, governmental, institutional, company, or practice level), more efficient microbiologic methods, or increased uptake of pet insurance. Cheaper, faster, and accessible diagnostic tests can increase test utilization and, in turn, reduce clinical uncertainty and “just-in-case” prescribing, which was often associated with prescribing cefovecin in the interviews.12 More widespread benefits exist, too: if C&S is cheaper and veterinarians submit cultures more frequently, antibiograms will be more representative of all feline bacterial infections, which will improve empiric antimicrobial choices.

Veterinarians also want rapid or point-of-care tests. These tests would need to be inexpensive or they will present the same cost-related uptake barriers as laboratory C&S testing. One of the veterinarians interviewed in Cazer et al, JAVMA, December 2023,12 noted the following:

There’s a lot of new PCR panels now too for different infectious diseases, which don’t take quite as long as the typical culture, which is nice. But a lot of the time it can be cost prohibitive … [owners] want to know if they should have antibiotics right now and not have to come back (Veterinarian #5).

A point-of-care C&S test exists in Europe, although research indicates that clinical veterinary staff make more errors in interpreting the results than expert microbiologists.72 Genomic sequencing advances may enable rapid, point-of-care tests for bacterial identification and susceptibility prediction. However, sequencing methods raise additional uncertainties in interpreting test results because the presence of bacterial genomic material is not equivalent to a bacterial infection; similarly, the presence of resistance genes does not necessarily mean the bacteria will be phenotypically resistant in vivo or that the gene is from a clinically relevant pathogen.50

Collaborating with veterinary microbiologists

Given the complexities of antimicrobial decision-making, veterinarians should collaborate with veterinary microbiology experts at diagnostic laboratories, who can help veterinarians understand breakpoints and select diagnostic tests and antimicrobials.47 Veterinarians should tell the laboratory about patient clinical signs, suspected diagnosis, and the reason for C&S testing so that the correct breakpoints are applied. For example, bacteria isolated from urine will be classified with urinary-specific breakpoints. However, if the patient has signs of pyelonephritis, tissue-specific breakpoints should be applied to account for differences in antimicrobial tissue versus urine penetration. Pharmacokinetic-pharmacodynamic studies and clinical trials are needed to support feline breakpoint development50 and optimize antimicrobial dosages and durations for clinical efficacy with minimal AMR selection.73

New antimicrobial formulations

The development of more palatable oral antimicrobials in appropriate sizes for feline patients will improve antimicrobial stewardship by making administration easier and minimizing the need for compounded formulations, which may have reduced efficacy.73 Creating appropriate-duration, injectable, lower tier antimicrobials with pharmacokinetics that minimize the selection of AMR, or injection aids that would allow pet owners to give lower tier parenteral antimicrobials at home, will also help minimize the use of cefovecin and subsequent AMR. Since 40% of cat owners find insulin injections easy to give,51 low-tier parenteral antimicrobials given at home could be a reasonable stewardship approach. Funding and resources need to be allocated to these areas and to training the veterinary pharmacologists, veterinary microbiologists, and researchers needed to advance feline antimicrobial therapy.50

Leveraging technology

New technologies can support sustainable AMU. Electronic veterinary records can supply AMU and AMR data, although there are still significant barriers of interoperability, data entry consistency, and data management and epidemiologic expertise is needed.43 In the UK, veterinary practices participating in the Small Animal Veterinary Surveillance Network can compare their AMU data to their peers,53 which is effective at reducing AMU in human medicine.74 VetCompass software extracts data from veterinary records and has been used to investigate AMU in dogs and cats in Australia.54 US veterinarians support the creation of AMU tracking systems, although they have some reservations about peer criticism, time constraints, and comparability across practice types.21 Given that clinical decision support systems are supported by veterinarians and that they have improved judicious AMU in human medicine,75 such technology should be integrated into the electronic veterinary record and help veterinarians select diagnostics, nonantimicrobial treatments, and the optimal antimicrobial drug, duration, and dose.21 Veterinary corporations, medical record software creators, and academic institutions should collaborate to create and implement these technologies that have been proven to improve antimicrobial stewardship.

Conclusion

Antimicrobial stewardship and resistance are a one-health challenge; all antimicrobial prescribers are responsible for preserving the effectiveness of antimicrobials. Feline veterinarians encounter unique challenges in antimicrobial stewardship, including cat and cat owner preferences for oral versus injectable antimicrobials, the convenience of a long-duration injectable antimicrobial from a class that is critically important in human medicine, pressure from clients for antimicrobials, limited knowledge of antimicrobial pharmacokinetics and pharmacodynamics in cats, and common diseases that resemble bacterial infections but do not need treatment with antimicrobials (eg, feline idiopathic cystitis). Other challenges are common to all areas of veterinary medicine, such as the cost of diagnostics, awareness and use of AMU guidelines, time constraints, and lack of information on AMR. Here, multilevel interventions to improve antimicrobial stewardship in cats are proposed. Tailored, theory-informed educational engagement with veterinarians and cat owners is important; it must be accompanied with structural-level innovations in diagnostic testing, antimicrobial formulations, medical records technology, and veterinary practice structures to make change and impact possible. Veterinary practices, pharmaceutical and diagnostic companies, academic institutions, feline-oriented nonprofits, and government agencies need to invest resources in these areas and collaborate to understand the specific barriers and create effective and sustainable antimicrobial stewardship solutions.

Acknowledgments

The authors would like to thank the cat owners and veterinarians who participated in their research into the use of cefovecin and oral antimicrobials in cats.

Disclosures

The authors have nothing to disclose. No AI-assisted technologies were used in the generation of this manuscript.

Funding

The survey of cat owners and interviews with New York veterinarians were funded by a Cornell University Department of Public and Ecosystem Health Impact Award. This material is based on work supported by the Cornell Feline Health Center Research Grants Program, a grant made available to the Cornell University College of Veterinary Medicine.

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