Pet owners’ knowledge of and attitudes toward the judicious use of antimicrobials for companion animals

Laurel E. Redding Department of Clinical Sciences and Advanced Medicine, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104.

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 VMD, PhD
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Stephen D. Cole Department of Clinical Sciences and Advanced Medicine, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104.

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 VMD, MS

Abstract

OBJECTIVE To explore owners’ knowledge of and experiences with antimicrobial treatment of their pets and their perceptions of veterinarian-led antimicrobial stewardship initiatives.

DESIGN Cross-sectional study.

SAMPLE 25 pet owners visiting 1 of 3 clinic types (tertiary care, general practice, or low cost) in the greater Philadelphia area.

PROCEDURES Semistructured interviews were conducted with pet owners to gather responses related to the study objectives. Responses were transcribed and analyzed by means of conventional content analysis.

RESULTS Although participants were mostly unfamiliar with the mechanisms of antimicrobials and antimicrobial resistance, they generally understood what constituted the inappropriate use of antimicrobials. Few pet owners appeared concerned about the risk of antimicrobial resistance, and no owners were concerned that antimicrobials used for people were also used for pets. Overall, pet owners reported closely following veterinarians’ directions when administering antimicrobials at home, and the main reasons for not following directions included difficulty administering the medication and concern about overmedicating the pet. Most (21/25 [84%]) pet owners expressed trust in their veterinarian to meet their pets’ medical needs and prescribe antimicrobials appropriately. However, in situations when it was unclear whether antimicrobials would be effective, most owners nevertheless wanted their pet to receive them. Initiatives to promote the judicious use of antimicrobials, such as microbial culture and antimicrobial susceptibility testing and formal stewardship programs, were generally well received and appreciated by owners.

CONCLUSIONS AND CLINICAL RELEVANCE Considerable opportunity was identified to leverage the trust that exists between veterinarians and pet owners to promote the judicious use of antimicrobials for pets.

Abstract

OBJECTIVE To explore owners’ knowledge of and experiences with antimicrobial treatment of their pets and their perceptions of veterinarian-led antimicrobial stewardship initiatives.

DESIGN Cross-sectional study.

SAMPLE 25 pet owners visiting 1 of 3 clinic types (tertiary care, general practice, or low cost) in the greater Philadelphia area.

PROCEDURES Semistructured interviews were conducted with pet owners to gather responses related to the study objectives. Responses were transcribed and analyzed by means of conventional content analysis.

RESULTS Although participants were mostly unfamiliar with the mechanisms of antimicrobials and antimicrobial resistance, they generally understood what constituted the inappropriate use of antimicrobials. Few pet owners appeared concerned about the risk of antimicrobial resistance, and no owners were concerned that antimicrobials used for people were also used for pets. Overall, pet owners reported closely following veterinarians’ directions when administering antimicrobials at home, and the main reasons for not following directions included difficulty administering the medication and concern about overmedicating the pet. Most (21/25 [84%]) pet owners expressed trust in their veterinarian to meet their pets’ medical needs and prescribe antimicrobials appropriately. However, in situations when it was unclear whether antimicrobials would be effective, most owners nevertheless wanted their pet to receive them. Initiatives to promote the judicious use of antimicrobials, such as microbial culture and antimicrobial susceptibility testing and formal stewardship programs, were generally well received and appreciated by owners.

CONCLUSIONS AND CLINICAL RELEVANCE Considerable opportunity was identified to leverage the trust that exists between veterinarians and pet owners to promote the judicious use of antimicrobials for pets.

The widespread use of antimicrobials in human and veterinary medicine and resulting increase in antimicrobial resistance are associated with increased morbidity and mortality rates, increased treatment costs, treatment failures, and transmission of antimicrobial-resistant pathogens between humans and other animals.1–3 Whether appropriate or inappropriate, the use of antimicrobials contributes to the emergence and spread of antimicrobial resistance; however, the excessive and inappropriate use of these drugs compounds this problem.1 Consequently, concerns have been raised among the human and veterinary medical professions about the need to achieve more judicious use of antimicrobials.

The judicious use of antimicrobials is broadly defined as selection of the optimal type, dose, and duration of antimicrobial treatment coupled with a reduction in inappropriate and excessive use, with the goal of achieving the best clinical outcome possible and minimizing the emergence of antimicrobial resistance.4 In companion animal medicine, antimicrobials are used almost exclusively for therapeutic purposes and for indications similar to those in human medicine. Guidelines5 exist for this use, and yet studies6–8 have shown that such guidelines are frequently not followed.

In a qualitative UK study,8 certain extrinsic factors related to pets and their owners were identified as significant influencers of the prescribing patterns of veterinarians. Specifically, the perceived expectations and ability of pet owners to comply with treatments, likelihood of follow-up, and ability of owners to pay for treatment influenced the choice of antimicrobial treatment prescribed by veterinarians. This suggests that veterinarians may tailor their prescribing to the perceived expectations and abilities of clients, which could contribute to the inappropriate use of antimicrobials.

Administration of antimicrobials by pet owners at home could also contribute to the misuse of antimicrobials when recommended regimens are not followed. For example, owner compliance regarding short-term antimicrobial treatment of their dogs was high (median compliance rate, 97%; n = 90) in a previous study9; however, because recruitment of subjects for that study was reportedly difficult, selection bias could have existed. In addition, the results may have been influenced by the Hawthorne effect, by which a conscious change in behavior can occur when participants know they are being observed.

Inappropriate administration of antimicrobials by owners to pets can occur in various ways, such as early cessation of treatment because of perceived pet recovery, failure to follow administration instructions (eg, cutting pills in half to save money and make the pills last longer) or schedules, treatment abandonment when pets resist administration, use of leftover pills from previous prescriptions when their pets have flare-ups of a chronic condition, or use of personal medication for pets. Studies8,10 have shown that veterinarians can also sometimes feel pressured to prescribe antimicrobials in circumstances when their use is unnecessary, and this situation can also occur in human medicine11 (particularly pediatrics12). To the authors’ knowledge, only 1 other study8 has been conducted to examine the influence of veterinary clients on antimicrobial dispensing at the point of care, and no studies have been reported regarding the ways in which pet owners could contribute to more judicious use of antimicrobials for companion animals.

The purpose of the study reported here was to investigate the experiences and attitudes of pet owners concerning antimicrobial use and prescribing for their pets. The aim was to use an exploratory and open-ended, qualitative approach to capture participants’ perceptions and beliefs. More specifically, we sought to determine whether and how pet owners may be contributing to the inappropriate use of antimicrobials in companion animal medicine, assess owners’ knowledge of antimicrobials and antimicrobial resistance and their interest in promoting the judicious use of antimicrobials for their pets, and understand the relationship between veterinarians and clients when antimicrobials are prescribed.

Materials and Methods

Participant recruitment

A purposeful sampling approach was used to select pet owners for interviews in the study. This approach involved purposeful selection of individuals who met certain criteria (eg, certain demographic characteristics or experiences with the phenomenon of interest) to provide perspectives from people with a wide range of characteristics and experiences.13 For the present study, people of different socioeconomic statuses with different degrees of experience with antimicrobial use for their pets were sought for participation.

To recruit people of different socioeconomic statuses, pet owners were approached to participate while they were waiting in the lobby of 1 of 3 veterinary practices in the greater Philadelphia area: an urban tertiary care facility, where clients were expected to be of high socioeconomic status; a suburban general practice, where clients were expected to be of intermediate socioeconomic status; and a suburban low-cost clinic, where clients were expected to be of low socioeconomic status. To enroll owners with different degrees of experience with antimicrobial use for their pets, potential participants were asked if they had ever used antimicrobials for their pets and, if so, the frequency of that use. Pet owners who recalled administering only a single course of antimicrobials to their pets were characterized as single-experience users. Pet owners who recalled having given their pets 2 or more courses of antimicrobials were considered multiple-experience users.

Participants were enrolled over a 4-month period until interviews yielded no additional information (ie, thematic data saturation was achieved), which is a standard methodological approach in qualitative research.14 Such saturation was assessed by review of the content of specific codes from each interview transcript for redundancy.15 All participants provided informed consent. The study protocol, consent process, and interview guide were approved by the institutional review board of the University of Pennsylvania.

Before data collection began, a semistructured, open-ended interview guide was developed on the basis of information obtained from a literature review and discussions among the research team (Supplementary Appendix S1, available at avmajournals.avma.org/doi/suppl/10.2460/javma.254.5.626). The first section was designed to collect information from the owners on their pets, their pets’ health conditions, reasons for antimicrobial use, and adherence to prescribed regimens. The second section was designed to elicit owners’ knowledge and perception of antimicrobials and antimicrobial resistance. To simplify the discussion, the term antibiotic rather than antimicrobial was used throughout the interviews. The third section presented hypothetical scenarios related to antimicrobial use and stewardship initiatives (specifically, use of diagnostic tests such as MCAST, formal antimicrobial stewardship programs, and delayed antimicrobial prescribing) and asked owners to express and explain their preferences for different approaches. Finally, because veterinarians have reported experiencing pressure from pet owners to prescribe antimicrobials,8 a question was included to determine whether there was an expectation for antimicrobials among pet owners. The interview guide was preliminarily tested by 3 pet owners, and the wording was refined as necessary to resolve any ambiguities.

Interviews

All interviews were conducted in person at each participating clinic, typically in an empty examination room. All interviews were, with permission, recorded and conducted by both investigators, one of whom had previous experience conducting qualitative interviews. Each participant was asked the same set of questions from the interview guide, with the interviewer probing and redirecting the conversation to elicit more in-depth responses or clarify points as necessary.16

Data analysis

All audio files were transcribed by a professional transcribing service, and the resulting data were uploaded to qualitative data analysis softwarea for management and analysis. One investigator (LER) with experience in qualitative data analysis coded all interview transcripts using conventional content analysis, which involves the subjective interpretation of the content of text data through the systematic classification process of coding and identifying themes or patterns.17 First, all interview data were reviewed repeatedly to achieve immersion and obtain a sense of the entire dataset.18 Then, data were read word by word to derive an initial coding scheme by highlighting the exact words from the text that captured key concepts.19,20 Codes were then sorted into categories and defined on the basis of how they were related, and the categories were used to organize and group codes into meaningful clusters. The 2 investigators consulted with each other to discuss code definitions and refine the interpretation of emerging patterns in the data.

Results

Participants

Thirty pet owners at the 3 clinics were approached for participation. Three owners did not recall ever having given their pets antimicrobials, and 2 owners declined to participate. A total of 25 people (18 [72%] women and 7 [28%] men) were interviewed, with interviews ranging in duration from 9 to 29 minutes (mean duration, 13 minutes). Participants ranged in age from 27 to 85 years, and professions generally differed across clinic types (Supplementary Table S1, available at avmajournals.avma.org/doi/suppl/10.2460/javma.254.5.626). All enumerated education levels were represented, although no clustering of education level (an indicator of socioeconomic status21) by clinic type was obvious. Most (17/25 [68%]) participants had children.

Seven pet owners were interviewed at the urban tertiary care facility, 7 were interviewed at the suburban general practice, and 11 were interviewed at the suburban low-cost clinic. Twelve owners were considered single-experience users of antimicrobials for their pets, and 13 were considered multiple-experience users. In general, no consistent patterns were apparent in beliefs or perceptions about antimicrobial use by hospital type or user experience.

Knowledge of antimicrobials and antimicrobial resistance

When asked to define “antibiotics” in their own words, most (18/25 [72%]) pet owners responded with some variation of “a medicine to fight infection,” with 5 owners specifically identifying bacteria as the offending agent. One owner confused the term with antibodies, and the remaining 6 owners were unsure how to define the term.

Almost half (12/25 [48%]) of participants were aware that many of the same antimicrobials that are used for nonhuman animals are also used for people. When asked how this made them feel, no owners reported feeling concerned. Most (20/25 [80%]) expressed neutrality (“I don't have a feeling one way or the other. It's like I guess if it's good for me, it's good for them too.”), and a small number (3/25 [12%]) appeared comforted that their pets received the same antimicrobials as people (“I feel good [that pets receive the same antimicrobials as people]. I like to know that we're not giving them nothing crazy.”).

When asked to define the concept of “antibiotic resistance,” only a small number (5/25 [20%]) of participants explicitly stated that the offending bacteria had become resistant to the medication. Many (15/25 [60%]) participants believed that such resistance occurred when the person or animal became resistant to the drug. Two (8%) owners believed the term referred to allergic reactions or other adverse effects of the drugs, and the remaining 3 (12%) owners either did not know what “antibiotic resistance” was or simply defined it as the drug “not working well anymore” for unspecified reasons. No patterns were apparent in the ability to accurately define “antibiotic” (ie, specifically identifying bacteria as a target organism of the drug) or “antibiotic resistance” (ie, specifically ascribing the resistance to bacterial organisms rather than the pet or person) among clinic types, owner experience with antimicrobials, or owner characteristics.

When asked to describe factors that they suspected would result in antimicrobial resistance, most (21/25 [85%]) pet owners were able to cite at least 1 factor, including taking too much, using antimicrobials when they are not needed (eg, for a common cold), and not following the prescriber's directions. One owner believed that antimicrobial resistance was hereditary, and 3 owners did not know any factors that could contribute to resistance. For some (11/25 [44%]) participants, the conversation extended into concern about antimicrobial resistance and the development of so-called superbugs. Almost half (5/11) of those owners reported being very concerned, whereas the remainder were either mildly concerned (“I guess, relatively I am concerned, but not day-to-day.”) or not at all concerned. One person did not believe in antimicrobial resistance or superbugs.

Following directions when administering antimicrobials to pets

Most (20/25 [85%]) pet owners reported always administering the entire course of prescribed antimicrobial, always following the administration schedule, and always returning for follow-up visits as directed (“Whatever the instructions were, that's what was done.”). One dog owner reported giving less than the indicated dose and not following the entire course of treatment because her pet, like her, was “not a pill taker.” Another dog owner reported not administering the entire dose because of a preference for holistic treatments. Two cat owners reported not always following the entire course of treatment because of difficulties administering medications to the cats (“It's really hard to give cats medicine!”), and a third owner with a cat and a dog reported, “We have stopped [giving antimicrobials] a tiny bit earlier, but it's usually maybe a day or two before if we see that [the pet is] doing all right.” All but one (ie, 24/25 [96%]) of the owners reported always returning for follow-up visits, with the remaining person (a dog owner) stating, “If [my pet] got better, I just never came back for an appointment.” Three owners (2 with dogs and 1 with a dog and a cat) admitted to keeping unused antimicrobials on hand and administering them in the case of a flare-up of a chronic condition (eg, otitis externa or dermatitis). Of these 3 owners, 2 referred to topical medications that were left over after they had administered the medication for the recommended amount of time.

Expectations for antimicrobials

In response to a hypothetical scenario in which a pet was sick with an infection but the veterinarian told the owner that their pet did not need antimicrobials, almost all (21/25 [84%]) participants expressed acceptance of this opinion and complete trust in their veterinarian (Table 1). A small number (4/25 [16%]) stated that they would push for antimicrobials, either because they did not want their pet to suffer or because they did not think the veterinarian realized how sick their pet was.

Table 1—

Themes and illustrative quotations regarding antimicrobial use for pets elicited through semistructured interviews of pet owners visiting an urban tertiary care veterinary facility (n = 7), a suburban general veterinary practice (7), or a suburban low-cost veterinary clinic in the greater Philadelphia area (11).

ThemeSubtheme or opinionNo. (%) of ownersIllustrative quotations
Expectations for antimicrobialsNo pushback: trust that the veterinarian is prescribing appropriately21 (84)“I would trust in the vet. Obviously I would prefer to walk away with some form of medication, but I would have to trust, you know, what they're saying.”
   “You gotta trust that [veterinarians] are doing everything that they can possibly do that's going to care for your animal.”
   “I go by her [the veterinarian's] judgment. I mean, I don't ask her anything about driving a truck and she doesn't ask me about being a vet.”
   “I guess I would honestly just defer to their professional experience. If they said no antibiotic, I mean, I'm not going to fight somebody that went to vet school.”
   “I have to put faith in the fact that you went to school for this and I didn't.”
 Pushback because of a belief that antimicrobials would limit animal suffering2 (8)“I wouldn't be too happy…. I'd want [the pet] to have some type of medication rather than just fighting it himself.”
 Pushback because of a belief that the veterinarian does not see how sick the pet truly is2 (8)“But it's just like anything else, I don't know if you guys have children or not, but I mean, you don't want no one to tell you that your baby's not sick when you're the mom or dad and you know he's sick. You can't tell me he's not sick.”
   “I've challenged [the veterinarian over] an ear infection before because I think that. … just like children, if you're around your animal often enough, you kinda know their normal behavior and what their patterns are. And you can kind of just say, ‘Oh, well, I know how they've acted before with this and how they act normally daily, and they're sick, you know?’ So, I definitely would challenge it.”
Use of additional diagnostic tests such as MCASTFull-fledged support to obtain a better cure for the pet6 (24)“I think that I would [approve the MCAST] if that meant better treatment for my dog and a more robust antibiotic and minimize side effects.”
 Full-fledged support to limit the use of medication for the pet1 (4)“I'd rather not give my dogs something that they don't need. I don't take anything that I don't think that I need. If I'm sick, I don't even go to the doctors. By the time they get me on anything, it's already run its course, so why am I taking crap that I don't need? So for that reason, yeah, I would do the culture.”
 Conditional support13 (52)“Is it something major? Yeah, I want you guys to nail it. We're spot on first time. Get him what he needs and sure, instead of trial and error and say, ‘Hey doc, 7 days just isn't working. Try something else.’ Plus if he's in pain, vision, heart, breathing, something major? Yeah, I guess you couldn't really put a price on that. But, you know, a little skin rash or something maybe, I don't know if I'd wanna pay top dollar for something like that.”
   “Well, knowing I don't have all the money in the world, it would depend on how expensive it is. But honestly if my animal was very sick, I mean, I would rather treat it properly, because the amount of time you have to treat it before something goes very, very wrong, is very limited compared to a human being. And they can't communicate. So I think checking first and taking a culture would definitely be something I would do.”
   “That's a tough one. Only because you draw the blood and then you start a course of antibiotics and the culture and sensitivity testing basically comes back 3 or 4 days later and it may result in a change or it may not. It would really, to me, probably depend on how certain the vet was about the type of organism and the cost of the test. So if the vet was uncertain at all and was recommending it, you know, it's, like, ‘You know what? I don't think I've seen this before. I'm gonna try this but I'd really like to run the culture and sensitivity testing.’ In that case, I'd probably go for it depending on the cost.”
 Lack of support for financial reasons5 (20)“I wish I could say money was no [object] and I would love to know that [my pets] were treated for the right thing and … with the appropriate medicine to get rid of [the infection] as quickly as it could. But money is an [object].”
Importance of the veterinarian participating in antimicrobial stewardship initiativesInvolvement is a good thing and necessary8 (32)“I would like to know that they did participate in it. All the information that they have comes down to me. So the better learned they are, the more educated I am.”
   “I would be very happy if my vet did [participate in stewardship initiatives]. Now that I know about it, if I was to find out that a vet didn't, that would definitely raise some alarms to me and I would probably either inform them about it first and see where we go from there, and if not, then I'd be looking for another vet because I don't want my vet overusing medications and I very specifically go to a vet that does not overuse medications and promotes titering and, you know, doesn't jump to medication use.”
 Involvement is useful but not necessary4 (16)“Would I like it? Probably. But it wouldn't make me not want to see the vet if they didn't. I'm interested in a vet who is kind and knows cats well.”
   “Knowing of it now, I think it to be important. But would I change vets because of it? I don't think so because you build confidence in your doctor.”
   “It would make me believe my vet was on the cutting edge. So would it make me change vets? Probably not, but I guess I'd have more respect for that vet that they were really paying attention to something that is, you know, globally important for all living species.”
 Indifference to veterinarian's involvement6 (24)“It wouldn't make a difference. … I guess because I wouldn't have been aware of it. I guess if it was something that I was more aware of, I would think about it.”
   “Being honest, probably wouldn't matter too much.”
 Assumption that veterinarian is already responsible with antimicrobials2 (8)“I think [my veterinarian is] responsible enough that I wouldn't worry about something like that. I don't know. I wouldn't go to her in the first place if I didn't think she was, you know, capable of treating these guys.”
   “I would hope that my vet is monitoring their antibiotic prescription frequency, to try to be better, you know, for continuing learning and improving.”
Attitudes toward delayed prescribingPositive reaction8 (32)“It's a good idea because sometimes it's difficult to get into the vet's office to see the vet. So in the meantime if something goes terribly wrong overnight and you can't get in, then at least you have something they can treat it with because it could be that we don't find much at the vet's and then you get home and all hell breaks loose. So I like having my options.”
   “I probably am okay with [delayed prescribing], because, again, sometimes, like kids, they [the pets] make a liar out of me. You come in and what presents is not always what's happening the other 23 hours of the day. And so, in that respect, I would be fine with taking [the script] home and watching them a few more days and just make sure.”
 Negative reaction6 (24)“It seems a little strange. I mean, if you suspect that the pet's gonna need that antibiotic, I would think that you would probably administer it at that point.”
   “I wouldn't want to do that. In a couple of days, if I felt like she wasn't doing better, I would totally bring her back to have her reevaluated.”

Perceptions of initiatives for the judicious use of antimicrobials

Use of additional diagnostic tests—Some differences among clinic types were apparent in the desire of pet owners to pursue diagnostic tests such as MCAST to enhance the judicious use of antimicrobials. Six (24%) pet owners (4 from the tertiary care facility and 2 from the suburban general practice) said they would pursue the additional testing to achieve a better outcome for their pet. One dog owner said she would pursue the testing to avoid having her pet receive unnecessary medication. Three (12%) pet owners stated that they would pursue empirical treatment first and only pursue additional testing if treatment failed. Five (20%) owners (4 from the low-cost clinic and 1 from the general practice) said they would decline the additional diagnostic tests for financial reasons. The remaining owners (10/25 [40%]) stated that it would depend on the situation, citing the severity of the infection and the type of illness as important in deciding whether to pursue MCAST.

Antimicrobial stewardship programs—Only 1 pet owner who worked in the health-care setting knew about antimicrobial stewardship programs. When provided with an explanation of the term (“coordinated interventions designed to improve and measure the appropriate use of antimicrobial agents by promoting the selection of the optimal drug regimen including dosing, duration of therapy, and route of administration”22), owners were split on their opinions (Table 1). The most common theme (8/25 [32%]) was that owners would want their veterinarian involved in initiatives aimed at promoting the judicious use of antimicrobials, either to ensure prescribing was as appropriate as possible or to better educate the client.

Delayed prescribing—None of the participants were familiar with the concept of “delayed prescribing.” A definition was provided to participants (ie, “the provider provides an antibiotic prescription, but with advice to delay filling the prescription because he/she believes that antibiotics are not immediately required and that symptoms will resolve without antibiotics”23), and participants were asked to reflect on this practice. Eight (32%) owners responded positively, citing convenience and having a fallback option if they could not return their pet quickly for a recheck appointment. Six (24%) owners reacted negatively, citing an inability to closely monitor the pet or a desire to have the pet reexamined by a veterinarian if the pet did not improve. The remaining 11 (44%) owners had a neutral response. A few (4/25 [16%]) owners had had experience with delayed prescribing and appreciated the convenience of the option to take home a script.

Use of antimicrobials when their efficacy is ambiguous

In response to a hypothetical scenario in which it was unknown whether antimicrobials would be efficacious for treating an infection in their pet, most (23/25 [92%]) pet owners stated that they would nevertheless want to treat their pets with antimicrobials. In most situations, risk aversion was the main reason (“I would advocate for starting right away to prevent it from getting worse, to keep my dog from suffering if we could avoid it.”). However, if told that there was no strong evidence to suggest that treatment with antimicrobials would make a difference in long-term outcome for their pet, a small number (4/25 [16%]) of owners said that they would accept withholding treatment (“Why put your pet through [treatment] if there is no real, like, ‘Yes, it's going to be awesome,' or, ‘No, it's not.’ So, I think as long as they're comfortable and they're fine, then, yeah, maybe their body is handling it just fine.”).

Discussion

The present study was conducted to explore pet owners’ experiences with the use of antimicrobials for their pets and their perceptions of initiatives to promote the judicious use of antimicrobials in veterinary medicine. Although several studies8,10,24–26 have examined the drivers of antimicrobial prescribing by veterinarians, to our knowledge only 1 study8 has investigated the attitudes and role of pet owners in influencing the prescribing of antimicrobials. It is important to know whether the perceived barriers to appropriate prescribing associated with pet owners’ expectations and abilities are real and could be addressed by adequate education and communication. We enrolled pet owners with a wide range of demographic characteristics, professions, socioeconomic statuses, and levels of experience with antimicrobial use for their pets. In enrolling subjects with different backgrounds, we sought to obtain a range of perspectives that may be relevant to a broad spectrum of veterinary practitioners who practice in different environments.

Few pet owners in the present study expressed concern about antimicrobial resistance in general, and none appeared concerned that the same antimicrobials that are used for people are also used for pets. These findings may have been due to a general lack of knowledge of antimicrobial resistance and of the possibility of interspecies transmission of resistant organisms, as was found in a previous study.10 Veterinarians are well positioned to educate pet owners about such concerns and the need for antimicrobials to be used judiciously when treating pets. For example, many pet owners were aware that there were conditions in human medicine for which antimicrobials were not indicated (eg, a common cold or viral infection), and veterinarians could use these situations to explain analogously the reason a pet may not need antimicrobials. Similarly, transmission of microbes is known to occur between pets and owners and vice versa,27–29 and so veterinarians may find it useful to discuss the possibility of such transmission and the fact that judicious use of antimicrobials in humans and other animals might decrease the risk of acquiring antimicrobial-resistant infections.30,31 However, we acknowledge that educating each and every pet owner on the potential risks of antimicrobial use may be unrealistic given the time constraints of veterinary practice. As a solution, veterinarians could consider having educational stewardship materials on hand (eg, client-targeted posters developed by the AVMA32) that could be followed up with more in-depth conversations as needed. We expect that this type of information and education could be particularly useful in situations when pet owners challenge prescribing decisions or decline diagnostic tests.

Educational campaigns of patients and parents have been successful in achieving substantial reductions in antimicrobial use in human medicine.33–35 However, with such campaigns there is also the risk of a paradoxical increase in demand for antimicrobials by certain so-educated people. For example, information campaigns to reduce the prevalence of antimicrobial-resistant organisms in people can result in an increased demand for antimicrobials by patients who had poor awareness of antimicrobial resistance,36 and similar reactions to health campaigns designed to motivate through fear have been documented for vaccination-related educational campaigns.37 A great deal more research is needed on the types of messaging and message delivery systems that would be effective for different types of veterinary clients. It may be that pet owners with a poor understanding or awareness of antimicrobial resistance will require a different type of messaging than pet owners with a strong understanding, as has been suggested in human medicine.36

In both veterinary and human medicine (particularly pediatrics), dissonance has been documented between the expectations of clients, parents, or patients regarding antimicrobials and the perception of those expectations by prescribers.10,11,38 Veterinarians have reported feeling that pet owners pushed for inappropriate antimicrobials, whereas pet owners have reported feeling that veterinarians were overprescribing antimicrobials.10 Although participants in the present study were not asked whether they believed that veterinarians were overprescribing antimicrobials, we found that almost all participants trusted their veterinarian to prescribe antimicrobials appropriately. Only a small number of pet owners stated that they would push back if a veterinarian told them their pet did not need antimicrobials, and 2 of them said they would do so with reservations.

In seeking to decrease the unnecessary use of antimicrobials, veterinarians need to balance the abstract phenomenon of antimicrobial resistance with the immediate concerns of pet health and well-being and owners’ concerns for their pet. Prescribing of antimicrobials simply to keep owners happy or minimize risk (ie, prescribing “just in case”) was a key barrier to achieving effective antimicrobial stewardship in 1 study.26 We too found that risk aversion was an important driver of owner desire for antimicrobials for their pet, even in a clinical scenario in which antimicrobials may not be useful. Clients’ perceptions of risk need to be considered when prescribing antimicrobials.

In the situation of Lyme disease (the hypothetical scenario used in the present study), we suspect that the perception of risk was heightened by the fact that all participants lived in a Lyme disease–endemic area39; indeed, some pet owners even mentioned to us that they or their children had contracted Lyme disease. In similar situations, we recommend that veterinarians provide clients with as much information as possible about the potential lack of effectiveness of antimicrobials. For example, veterinarians could refer owners to the American College of Veterinary Internal Medicine consensus statement on borreliosis in dogs and cats,40 which does not recommend antimicrobial treatment for nonproteinuric dogs that are seropositive for Borrelia burgdorferi infection but have no clinical signs of Lyme disease. Veterinarians could also cite the guidelines of the Infectious Disease Society of America on the subject,41 which do not recommend the routine use of antimicrobial prophylaxis for or serologic testing of people after a recognized tick bite. When these nuances were explained to the participants in the present study, some changed their mind about wanting to treat their pet with antimicrobials. Therefore, for specific clinical scenarios, we believe that veterinarians could achieve a reduction in the use of antimicrobials for a subset of clients with the proper education and communication. We refer readers to pet owner–targeted educational material developed by the AVMA.32

We also assessed owners’ reactions to initiatives for promoting antimicrobial stewardship that have been successful in human medicine. Microbial culture and antimicrobial susceptibility testing plays an important role in antimicrobial stewardship,42,43 and its use is recommended to combat inappropriate antimicrobial use and antimicrobial resistance by the American College of Veterinary Internal Medicine.5 In veterinary medicine, the use of MCAST is fairly infrequent,44,45 and cost is cited as one of the most important barriers to pursuing such testing.45,46 In the present study, only a small subset of owners would have declined MCAST because of cost. Six participants stated that they would definitely pursue MCAST (even if the cost was between $150 and $200), and the remaining owners stated that it would depend upon the situation. Almost all of the owners stated that they would defer to the expertise of the veterinarian, which is consistent with findings of another study.10 Provided veterinarians have developed trusting relationships with their clients, we believe that there is more opportunity for the use of MCAST than veterinarians may believe, particularly when the reasons for pursuing such testing (including potential cost savings in the long term) are clearly explained.

Although formal antimicrobial stewardship programs of the type that exist in human hospitals may not be realistic for many companion animal practices, there are initiatives that can be pursued to improve prescribing practices of individual veterinarians. Resources on such initiatives include the 5R framework (responsibility, reduction, refinement, replacement, and review),47 other publications,4,5 and AVMA material on antimicrobial stewardship.48,49 In the study reported here, most pet owners appreciated having their veterinarian involved in initiatives geared at judicious antimicrobial use, although involvement in such initiatives was critical for only 1 owner. We suspect that the indifference noted in a subset of owners was related to a lack of awareness of such initiatives and of antimicrobial resistance in general, as has been previously reported.10 We therefore suspect that proactive engagement in the judicious use of antimicrobials coupled with owner education on antimicrobial resistance could be a selling point for veterinarians.

Delayed prescribing is a stewardship initiative by which a prescriber provides a prescription for an antimicrobial but with advice to delay filling the prescription because the prescriber assesses that antimicrobials are not immediately required and that symptoms (or clinical signs) will resolve without antimicrobial treatment.23 A systematic review23 of reported studies on this practice in human medicine revealed that delayed prescribing results in clinical outcomes and patient satisfaction similar to those when antimicrobials are provided immediately. Delayed prescribing is particularly well suited to respiratory tract infections and is recommended for both people23 and cats and dogs.50 Several pet owners in the present study indicated that they had experienced delayed prescribing, suggesting that some veterinarians already use this practice. Most participants had a positive or neutral reaction to the practice, and several owners expressed enthusiasm for the convenience of the option. We therefore believe that delayed prescribing is a viable strategy for decreasing antimicrobial use in situations when antimicrobials may not be necessary.

The present study had several limitations that warrant consideration. First, the study was conducted in a restricted geographic region, and so the generalizability of our findings may be limited. This is a well-known limitation of qualitative research, which we attempted to mitigate by approaching pet owners from a variety of clinic types. Another limitation was the small sample size. Although this is often seen as a considerable limitation in qualitative studies, there is a general consensus among researchers that data saturation is not about the numbers of interviews per se, but about the depth of the data.51 Achievement of thematic data saturation is the critical objective of qualitative studies,15 and although no universally recognized method exists for achieving data saturation, redundancy of data is one of the key recognized general principles.14 Such redundancy was achieved in our study, and what the study may have lacked in representativeness, it gained in depth given that pet owners were asked to elaborate on their experiences and responses to different scenarios. In general, the use of purposeful sampling to obtain perspectives from people with different experiences and characteristics can add to the depth of findings; however, because the characteristics of interest are selected by the researchers, bias can be introduced from the selection of subjects according to criteria perceived a priori to be relevant to the researcher.

Other study limitations were related to participant behavior. Because interviews took place in the clinic where owners brought their pet for care, owners may have overstated the trust that they had in their veterinarian. Indeed, the finding that so many owners reported still wanting antimicrobials in the hypothetical clinical scenarios in which their effectiveness was unclear contradicted their reported trust in the veterinarian. Potential owner biases associated with social desirability are an inevitable limitation of the recruitment strategy used, even though efforts were made when seeking informed consent to ensure participants were aware that the interviewers were not affiliated with their veterinarian and that none of their responses would affect the care they received from their veterinarian. Predicted future behavior in response to certain clinical scenarios may also differ from what would actually happen; however, during the interviews participants often discussed their past experiences to illustrate their opinions or reactions, bolstering our confidence in the findings.

Overall, findings of the present study suggested that the veterinarian-client relationship could be leveraged to improve antimicrobial stewardship in veterinary practice. Ideas for future research include evaluation of differences between owners of different animal species regarding attitudes toward antimicrobial stewardship and determination of whether targeted client-education efforts (eg, via educational handouts or video recordings) could be used to promote the benefits of appropriate antimicrobial use.

ABBREVIATIONS

MCAST

Microbial culture and antimicrobial susceptibility testing

Footnotes

a

NVivo software, version 11, QSR International, Melbourne, VIC, Australia.

References

  • 1. CDC. Antibiotic resistance threats in the United States. Available at: www.cdc.gov/drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf, ed, 2013. Accessed Dec 14, 2018.

    • Search Google Scholar
    • Export Citation
  • 2. Klevens RM, Edwards JR, Richards CL Jr, et al. Estimating health care-associated infections and deaths in US hospitals, 2002. Public Health Rep 2007;122:160166.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. Acar J, Rostel B. Antimicrobial resistance: an overview. Rev Sci Tech 2001;20:797810.

  • 4. Prescott JF, Boerlin P. Antimicrobial use in companion animals and Good Stewardship Practice. Vet Rec 2016;179:486488.

  • 5. Weese JS, Giguere S, Guardabassi L, et al. ACVIM consensus statement on therapeutic antimicrobial use in animals and antimicrobial resistance. J Vet Intern Med 2015;29:487498.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Wayne A, McCarthy R, Lindenmayer J. Therapeutic antibiotic use patterns in dogs: observations from a veterinary teaching hospital. J Small Anim Pract 2011;52:310318.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Escher M, Vanni M, Intorre L, et al. Use of antimicrobials in companion animal practice: a retrospective study in a veterinary teaching hospital in Italy. J Antimicrob Chemother 2011;66:920927.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Mateus AL, Brodbelt DC, Barber N, et al. Qualitative study of factors associated with antimicrobial usage in seven small animal veterinary practices in the UK. Prev Vet Med 2014;117:6878.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Adams VJ, Campbell JR, Waldner CL, et al. Evaluation of client compliance with short-term administration of antimicrobials to dogs. J Am Vet Med Assoc 2005;226:567574.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Smith M, King C, Davis M, et al. Pet owner and vet interactions: exploring the drivers of AMR. Antimicrob Resist Infect Control 2018;7:46.

  • 11. Henriksen K, Hansen EH. The threatened self: general practitioners’ self-perception in relation to prescribing medicine. Soc Sci Med 2004;59:4755.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Szymczak JE, Feemster KA, Zaoutis TE, et al. Pediatrician perceptions of an outpatient antimicrobial stewardship intervention. Infect Control Hosp Epidemiol 2014;35(suppl 3):S69S78.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Palinkas LA, Horwitz SM, Green CA, et al. Purposeful sampling for qualitative data collection and analysis in mixed method implementation research. Adm Policy Ment Health 2015;42:533544.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Guest G, Bunce A, Johnson L. How many interviews are enough?: an experiment with data saturation and variability. Field Methods 2006;18:5982.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Grady MP. Qualitative and action research: a practitioner handbook. Bloomington, Ind: Phi Delta Kappa, 1998.

  • 16. Weiss RS. Learning from strangers: the art and method of qualitative interview studies. New York: Free Press, 1994;6181.

  • 17. Hsieh HF, Shannon SE. Three approaches to qualitative content analysis. Qual Health Res 2005;15:12771288.

  • 18. Tesch R. Qualitative research: analysis types and software tools. Bristol, Pa: Falmer, 1990;115141.

  • 19. Miles M, Huberman A. Qualitative data analysis: an expanded sourcebook. 2nd ed. Thousand Oaks, Calif: Sage Publications, 1994;5469.

    • Search Google Scholar
    • Export Citation
  • 20. Morse JM, Field PA. Qualitative research methods for health professionals. Thousand Oaks, Calif: Sage, 1995;2131.

  • 21. Liberatos P, Link BG, Kelsey JL. The measurement of social class in epidemiology. Epidemiol Rev 1988;10:87121.

  • 22. Society for Healthcare Epidemiology of America. Infectious Diseases Society of America, Pediatric Infectious Diseases Society. Policy statement on antimicrobial stewardship by the Society for Healthcare Epidemiology of America (SHEA), the Infectious Diseases Society of America (IDSA), and the Pediatric Infectious Diseases Society (PIDS). Infect Control Hosp Epidemiol 2012;33:322327.

    • Search Google Scholar
    • Export Citation
  • 23. Spurling GK, Del Mar CB, Dooley L, et al. Delayed antibiotic prescriptions for respiratory infections. Cochrane Database Syst Rev 2017;9:CD004417.

    • Search Google Scholar
    • Export Citation
  • 24. Coyne LA, Latham SM, Williams NJ, et al. Understanding the culture of antimicrobial prescribing in agriculture: a qualitative study of UK pig veterinary surgeons. J Antimicrob Chemother 2016;71:33003312.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25. De Briyne N, Atkinson J, Pokludova L, et al. Factors influencing antibiotic prescribing habits and use of sensitivity testing amongst veterinarians in Europe. Vet Rec 2013;173:475.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26. Currie K, King C, Nuttall T, et al. Expert consensus regarding drivers of antimicrobial stewardship in companion animal veterinary practice: a Delphi study. Vet Rec 2018;182:691.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27. Song SJ, Lauber C, Costello EK, et al. Cohabiting family members share microbiota with one another and with their dogs. eLife 2013;2:e00458.

  • 28. van Duijkeren E, Wolfhagen MJ, Box AT, et al. Human-to-dog transmission of methicillin-resistant Staphylococcus aureus. Emerg Infect Dis 2004;10:22352237.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29. Cefai C, Ashurst S, Owens C. Human carriage of methicillin-resistant Staphylococcus aureus linked with pet dog. Lancet 1994;344:539540.

  • 30. van den Bogaard AE, Stobberingh EE. Epidemiology of resistance to antibiotics. Links between animals and humans. Int J Antimicrob Agents 2000;14:327335.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31. Wegener HC, Aarestrup FM, Gerner-Smidt P, et al. Transfer of antibiotic resistant bacteria from animals to man. Acta Vet Scand Suppl 1999;92:5157.

    • Search Google Scholar
    • Export Citation
  • 32. AVMA. Clinic posters: be careful with antibiotics, 2018. Available at: www.avma.org/PracticeManagement/ClientMaterials/Pages/clinic-posters-client-handouts.aspx. Accessed Dec 14, 2018.

    • Search Google Scholar
    • Export Citation
  • 33. Sabuncu E, David J, Bernede-Bauduin C, et al. Significant reduction of antibiotic use in the community after a nationwide campaign in France, 2002–2007. PLoS Med 2009;6:e1000084.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34. Goossens H, Guillemot D, Ferech M, et al. National campaigns to improve antibiotic use. Eur J Clin Pharmacol 2006;62:373379.

  • 35. Finkelstein JA, Davis RL, Dowell SF, et al. Reducing antibiotic use in children: a randomized trial in 12 practices. Pediatrics 2001;108:17.

  • 36. Roope LSJ, Tonkin-Crine S, Butler CC, et al. Reducing demand for antibiotic prescriptions: evidence from an online survey of the general public on the interaction between preferences, beliefs and information, United Kingdom, 2015. Euro Surveill 2018;23:1700424.

    • Search Google Scholar
    • Export Citation
  • 37. Nyhan B, Reifler J, Richey S, et al. Effective messages in vaccine promotion: a randomized trial. Pediatrics 2014;133:e835e842.

  • 38. Stivers T, Mangione-Smith R, Elliott MN, et al. Why do physicians think parents expect antibiotics? What parents report vs what physicians believe. J Fam Pract 2003;52:140148.

    • Search Google Scholar
    • Export Citation
  • 39. Aenishaenslin C, Ravel A, Michel P, et al. From Lyme disease emergence to endemicity: a cross sectional comparative study of risk perceptions in different populations. BMC Public Health 2014;14:1298.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40. Littman MP, Gerber B, Goldstein RE, et al. ACVIM consensus update on Lyme borreliosis in dogs and cats. J Vet Intern Med 2018;32:887903.

  • 41. Wormser GP, Dattwyler RJ, Shapiro ED, et al. The clinical assessment, treatment, and prevention of Lyme disease, human granulocytic anaplasmosis, and babesiosis: clinical practice guidelines by the Infectious Diseases Society of America. Clin Infect Dis 2006;43:10891134.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42. Dellit TH, Owens RC, McGowan JE Jr, et al. Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship. Clin Infect Dis 2007;44:159177.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 43. Morency-Potvin P, Schwartz DN, Weinstein RA. Antimicrobial stewardship: how the microbiology laboratory can right the ship. Clin Microbiol Rev 2016;30:381407.

    • Search Google Scholar
    • Export Citation
  • 44. Murphy CP, Reid-Smith RJ, Boerlin P, et al. Out-patient antimicrobial drug use in dogs and cats for new disease events from community companion animal practices in Ontario. Can Vet J 2012;53:291298.

    • Search Google Scholar
    • Export Citation
  • 45. AVMA Task Force for Antimicrobial Stewardship in Companion Animal Practice. Understanding companion animal practitioners’ attitudes toward antimicrobial stewardship. J Am Vet Med Assoc 2015;247:883884.

    • Search Google Scholar
    • Export Citation
  • 46. Fowler H, Davis MA, Perkins A, et al. A survey of veterinary antimicrobial prescribing practices, Washington State 2015. Vet Rec 2016;179:651.

  • 47. Page S, Prescott J, Weese S. The 5Rs approach to antimicrobial stewardship. Vet Rec 2014;175:207208.

  • 48. AVMA. Antimicrobial stewardship definition and core principles, 2018. Available at: www.avma.org/KB/Policies/Pages/Antimicrobial-Stewardship-Definition-and-Core-Principles.aspx. Accessed Dec 14, 2018.

    • Search Google Scholar
    • Export Citation
  • 49. AVMA. Antimicrobials: guidelines for judicious use, 2017. www.avma.org/KB/Resources/Reference/Pages/Antimicrobial-use.aspx. Accessed Dec 14, 2018.

    • Search Google Scholar
    • Export Citation
  • 50. Lappin MR, Blondeau J, Boothe D, et al. Antimicrobial use guidelines for treatment of respiratory tract disease in dogs and cats: Antimicrobial Guidelines Working Group of the International Society for Companion Animal Infectious Diseases. J Vet Intern Med 2017;31:279294.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 51. Burmeister E, Aitken LM. Sample size: how many is enough? Aust Crit Care 2012;25:271274.

Contributor Notes

Address correspondence to Dr. Redding (lredding@vet.upenn.edu).
  • 1. CDC. Antibiotic resistance threats in the United States. Available at: www.cdc.gov/drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf, ed, 2013. Accessed Dec 14, 2018.

    • Search Google Scholar
    • Export Citation
  • 2. Klevens RM, Edwards JR, Richards CL Jr, et al. Estimating health care-associated infections and deaths in US hospitals, 2002. Public Health Rep 2007;122:160166.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. Acar J, Rostel B. Antimicrobial resistance: an overview. Rev Sci Tech 2001;20:797810.

  • 4. Prescott JF, Boerlin P. Antimicrobial use in companion animals and Good Stewardship Practice. Vet Rec 2016;179:486488.

  • 5. Weese JS, Giguere S, Guardabassi L, et al. ACVIM consensus statement on therapeutic antimicrobial use in animals and antimicrobial resistance. J Vet Intern Med 2015;29:487498.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Wayne A, McCarthy R, Lindenmayer J. Therapeutic antibiotic use patterns in dogs: observations from a veterinary teaching hospital. J Small Anim Pract 2011;52:310318.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Escher M, Vanni M, Intorre L, et al. Use of antimicrobials in companion animal practice: a retrospective study in a veterinary teaching hospital in Italy. J Antimicrob Chemother 2011;66:920927.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Mateus AL, Brodbelt DC, Barber N, et al. Qualitative study of factors associated with antimicrobial usage in seven small animal veterinary practices in the UK. Prev Vet Med 2014;117:6878.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Adams VJ, Campbell JR, Waldner CL, et al. Evaluation of client compliance with short-term administration of antimicrobials to dogs. J Am Vet Med Assoc 2005;226:567574.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Smith M, King C, Davis M, et al. Pet owner and vet interactions: exploring the drivers of AMR. Antimicrob Resist Infect Control 2018;7:46.

  • 11. Henriksen K, Hansen EH. The threatened self: general practitioners’ self-perception in relation to prescribing medicine. Soc Sci Med 2004;59:4755.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Szymczak JE, Feemster KA, Zaoutis TE, et al. Pediatrician perceptions of an outpatient antimicrobial stewardship intervention. Infect Control Hosp Epidemiol 2014;35(suppl 3):S69S78.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Palinkas LA, Horwitz SM, Green CA, et al. Purposeful sampling for qualitative data collection and analysis in mixed method implementation research. Adm Policy Ment Health 2015;42:533544.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Guest G, Bunce A, Johnson L. How many interviews are enough?: an experiment with data saturation and variability. Field Methods 2006;18:5982.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Grady MP. Qualitative and action research: a practitioner handbook. Bloomington, Ind: Phi Delta Kappa, 1998.

  • 16. Weiss RS. Learning from strangers: the art and method of qualitative interview studies. New York: Free Press, 1994;6181.

  • 17. Hsieh HF, Shannon SE. Three approaches to qualitative content analysis. Qual Health Res 2005;15:12771288.

  • 18. Tesch R. Qualitative research: analysis types and software tools. Bristol, Pa: Falmer, 1990;115141.

  • 19. Miles M, Huberman A. Qualitative data analysis: an expanded sourcebook. 2nd ed. Thousand Oaks, Calif: Sage Publications, 1994;5469.

    • Search Google Scholar
    • Export Citation
  • 20. Morse JM, Field PA. Qualitative research methods for health professionals. Thousand Oaks, Calif: Sage, 1995;2131.

  • 21. Liberatos P, Link BG, Kelsey JL. The measurement of social class in epidemiology. Epidemiol Rev 1988;10:87121.

  • 22. Society for Healthcare Epidemiology of America. Infectious Diseases Society of America, Pediatric Infectious Diseases Society. Policy statement on antimicrobial stewardship by the Society for Healthcare Epidemiology of America (SHEA), the Infectious Diseases Society of America (IDSA), and the Pediatric Infectious Diseases Society (PIDS). Infect Control Hosp Epidemiol 2012;33:322327.

    • Search Google Scholar
    • Export Citation
  • 23. Spurling GK, Del Mar CB, Dooley L, et al. Delayed antibiotic prescriptions for respiratory infections. Cochrane Database Syst Rev 2017;9:CD004417.

    • Search Google Scholar
    • Export Citation
  • 24. Coyne LA, Latham SM, Williams NJ, et al. Understanding the culture of antimicrobial prescribing in agriculture: a qualitative study of UK pig veterinary surgeons. J Antimicrob Chemother 2016;71:33003312.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25. De Briyne N, Atkinson J, Pokludova L, et al. Factors influencing antibiotic prescribing habits and use of sensitivity testing amongst veterinarians in Europe. Vet Rec 2013;173:475.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26. Currie K, King C, Nuttall T, et al. Expert consensus regarding drivers of antimicrobial stewardship in companion animal veterinary practice: a Delphi study. Vet Rec 2018;182:691.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27. Song SJ, Lauber C, Costello EK, et al. Cohabiting family members share microbiota with one another and with their dogs. eLife 2013;2:e00458.

  • 28. van Duijkeren E, Wolfhagen MJ, Box AT, et al. Human-to-dog transmission of methicillin-resistant Staphylococcus aureus. Emerg Infect Dis 2004;10:22352237.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29. Cefai C, Ashurst S, Owens C. Human carriage of methicillin-resistant Staphylococcus aureus linked with pet dog. Lancet 1994;344:539540.

  • 30. van den Bogaard AE, Stobberingh EE. Epidemiology of resistance to antibiotics. Links between animals and humans. Int J Antimicrob Agents 2000;14:327335.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31. Wegener HC, Aarestrup FM, Gerner-Smidt P, et al. Transfer of antibiotic resistant bacteria from animals to man. Acta Vet Scand Suppl 1999;92:5157.

    • Search Google Scholar
    • Export Citation
  • 32. AVMA. Clinic posters: be careful with antibiotics, 2018. Available at: www.avma.org/PracticeManagement/ClientMaterials/Pages/clinic-posters-client-handouts.aspx. Accessed Dec 14, 2018.

    • Search Google Scholar
    • Export Citation
  • 33. Sabuncu E, David J, Bernede-Bauduin C, et al. Significant reduction of antibiotic use in the community after a nationwide campaign in France, 2002–2007. PLoS Med 2009;6:e1000084.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34. Goossens H, Guillemot D, Ferech M, et al. National campaigns to improve antibiotic use. Eur J Clin Pharmacol 2006;62:373379.

  • 35. Finkelstein JA, Davis RL, Dowell SF, et al. Reducing antibiotic use in children: a randomized trial in 12 practices. Pediatrics 2001;108:17.

  • 36. Roope LSJ, Tonkin-Crine S, Butler CC, et al. Reducing demand for antibiotic prescriptions: evidence from an online survey of the general public on the interaction between preferences, beliefs and information, United Kingdom, 2015. Euro Surveill 2018;23:1700424.

    • Search Google Scholar
    • Export Citation
  • 37. Nyhan B, Reifler J, Richey S, et al. Effective messages in vaccine promotion: a randomized trial. Pediatrics 2014;133:e835e842.

  • 38. Stivers T, Mangione-Smith R, Elliott MN, et al. Why do physicians think parents expect antibiotics? What parents report vs what physicians believe. J Fam Pract 2003;52:140148.

    • Search Google Scholar
    • Export Citation
  • 39. Aenishaenslin C, Ravel A, Michel P, et al. From Lyme disease emergence to endemicity: a cross sectional comparative study of risk perceptions in different populations. BMC Public Health 2014;14:1298.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40. Littman MP, Gerber B, Goldstein RE, et al. ACVIM consensus update on Lyme borreliosis in dogs and cats. J Vet Intern Med 2018;32:887903.

  • 41. Wormser GP, Dattwyler RJ, Shapiro ED, et al. The clinical assessment, treatment, and prevention of Lyme disease, human granulocytic anaplasmosis, and babesiosis: clinical practice guidelines by the Infectious Diseases Society of America. Clin Infect Dis 2006;43:10891134.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42. Dellit TH, Owens RC, McGowan JE Jr, et al. Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship. Clin Infect Dis 2007;44:159177.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 43. Morency-Potvin P, Schwartz DN, Weinstein RA. Antimicrobial stewardship: how the microbiology laboratory can right the ship. Clin Microbiol Rev 2016;30:381407.

    • Search Google Scholar
    • Export Citation
  • 44. Murphy CP, Reid-Smith RJ, Boerlin P, et al. Out-patient antimicrobial drug use in dogs and cats for new disease events from community companion animal practices in Ontario. Can Vet J 2012;53:291298.

    • Search Google Scholar
    • Export Citation
  • 45. AVMA Task Force for Antimicrobial Stewardship in Companion Animal Practice. Understanding companion animal practitioners’ attitudes toward antimicrobial stewardship. J Am Vet Med Assoc 2015;247:883884.

    • Search Google Scholar
    • Export Citation
  • 46. Fowler H, Davis MA, Perkins A, et al. A survey of veterinary antimicrobial prescribing practices, Washington State 2015. Vet Rec 2016;179:651.

  • 47. Page S, Prescott J, Weese S. The 5Rs approach to antimicrobial stewardship. Vet Rec 2014;175:207208.

  • 48. AVMA. Antimicrobial stewardship definition and core principles, 2018. Available at: www.avma.org/KB/Policies/Pages/Antimicrobial-Stewardship-Definition-and-Core-Principles.aspx. Accessed Dec 14, 2018.

    • Search Google Scholar
    • Export Citation
  • 49. AVMA. Antimicrobials: guidelines for judicious use, 2017. www.avma.org/KB/Resources/Reference/Pages/Antimicrobial-use.aspx. Accessed Dec 14, 2018.

    • Search Google Scholar
    • Export Citation
  • 50. Lappin MR, Blondeau J, Boothe D, et al. Antimicrobial use guidelines for treatment of respiratory tract disease in dogs and cats: Antimicrobial Guidelines Working Group of the International Society for Companion Animal Infectious Diseases. J Vet Intern Med 2017;31:279294.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 51. Burmeister E, Aitken LM. Sample size: how many is enough? Aust Crit Care 2012;25:271274.

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