Peter Damborg, J. Scott Weese, and John F. Prescott Good antimicrobial stewardship (AMS) is critical because it is unlikely that any new classes of antimicrobial drugs will be approved in companion animals for many years. We need to preserve the efficacy of the drugs that we have for as long as we can. There is now considerable and constantly expanding global literature examining different aspects of AMS in companion animals, driven by increasing resistance and the spread of resistant pathogens in companion animals, as well as the sharing of multidrug‐resistant pathogens between companion animals and their owners. The general concepts of AMS are discussed in Chapter 20; the current chapter elaborates on these in relation to companion animals, specifically dogs and cats, although they can be applied to other companion animals. Antimicrobial stewardship is an emerging field that is still to some extent at the descriptive rather than mature stage. We understand the problem but the solutions are still being developed. A basic concept is that, because antimicrobial resistance (AMR) is a “wicked problem” (see Figure 20.1), AMS requires multiple approaches to address it (see Figure 20.2). It is the cumulative effect of many different actions that will effectively reduce AMR (Chapter 20). Following a brief review of some important aspects, this chapter discusses in detail the concepts and application of clinical antimicrobial stewardship within the context of companion animals, including the use of clinical microbiological diagnostics. The 5Rs approach developed by Page et al. (2014) is a rich “mindset” approach to AMS, which starts with accepting responsibility for addressing AMR. Reduction is not only a general reduction in use, wherever possible to where the benefits are clear and substantial, but also a reduction of the need for antimicrobial treatment by infection prevention and control measures. Replacement is the use of nonantimicrobial alternatives where appropriate, or replacement of systemic antimicrobial administration by local or topical treatments. Refinement is improvement in all aspects of the use of antimicrobial drugs, including the way in which diseases are diagnosed, the improvement in antimicrobial susceptibility testing, the choice and basis of choice of drugs for treatment, and the choice of dose and duration, among other considerations. Finally, review of the AMS program is fundamental, since AMS is a process of continuous improvement, which includes measurement of progress towards each objective which can involve measuring quantity of drugs use, the quality of their use, or the impact of interventions on these parameters. This topic is discussed further by Lloyd and Page (2018). Antimicrobial therapy is not a static field. Advances in understanding of dosing, species differences, interactions, safety and efficacy, clinical guidelines, and antimicrobial susceptibility clinical breakpoints, along with the release of new antimicrobials within an existing class, result in ongoing changes in antimicrobial use recommendations. Lack of antimicrobial availability, including national restrictions in antimicrobial access, may also impact necessary approaches. Education on antimicrobial use and stewardship needs to start early (veterinary medicine programs) and continue throughout a clinician’s career, since it is a dynamic field. Continuing education is an important component for understanding changes and, often overlooked, the reasons for those changes, which may encompass areas of microbiology, pharmacology, clinical medicine, and public health. Education can be effective. For example, a recent randomized controlled trial in the United Kingdom of two interventions to reduce the use of the WHO classified Highest Priority Critically Important Antimicrobials (HP‐CIAs) (e.g., third‐generation cephalosporins, fluoroquinolones) in companion animals in overprescribing practices showed a reduction of their use in dogs (24%) and cats (39%) in “heavy intervention” clinics and 17% in cats in “light intervention” clinics compared to controls clinics (Singleton et al., 2021). Results from this study are being used in development of a national AMS scheme promoted by the national veterinary regulatory agency. A Dutch study of the implementation of an AMS intervention in 44 companion animal clinics showed a significant 15% reduction of total antimicrobial use in companion animals, with a 15% reduction in first‐choice drugs and a 26% reduction in second‐choice drugs, but no reduction in third‐choice drug use. Importantly, given the tendency for behavioral changes to decline over time, the reduction in use unexpectedly actually increased over time (Hopman et al., 2019). The control of AMR is essentially a problem of infection control. There are now numerous examples of the remarkable clonal spread of multidrug‐resistant pathogens in companion animals, many of which are zoonotic. A considerable diversity of extended‐spectrum beta‐lactamase (ESBL) genes is increasingly prevalent and problematic in Escherichia coli in dogs and cats globally, commonly associated with hospital environments (reviewed in Chapters 8, 9) (Salgado‐Caxito et al., 2021). The ESBL‐E. coli encoded by CTX‐M‐15 and SHV‐12, along with the resistant epidemic strains ST38 and ST131, are widespread in dogs and cats and found on all continents (Salgado‐Caxito et al., 2021). These sequence types are also highly prevalent human extraintestinal pathogenic E. coli, and potentially a minor fraction of human strains originate from companion animals. Apart from ESBL and other extended‐spectrum cephalosporinase‐producing Enterobacterales, the emergence and spread of methicillin‐resistant Staphylococcus pseudintermedius (MRSP) in Europe and North America (Perreten et al., 2010) and the global dissemination of epidemic clones (Pires dos Santos et al., 2016) are well documented. In a study of the epidemiology of this infection, dogs and cats that had been hospitalised were over 100 times more likely to be infected with MRSP. If they had visited a veterinary clinic 6–10 or over 10 times, they were 1.6 and 7.3 times as likely, respectively (Lehner et al., 2014). Although humans are rarely infected by S. pseudintermedius, which is largely adapted to the canine host, being a veterinary professional has been proven as a risk factor for carriage of MRSP and other methicillin‐resistant coagulase‐positive staphylococci (Rodrigues et al., 2018). To prevent dissemination of these and other pathogens within hospitals, veterinary personnel should be properly trained in hospital infection control, including personal hygiene. Unfortunately, hand hygiene practices often leave a lot to be desired. In a video observational study in Canada, median contact time for soap and water handwashing in companion animal practice was just two seconds (Anderson et al., 2014). Hand hygiene rubs may constitute a convenient alternative or supplement to handwashing, but users should note that the efficacy of various products varies and the residual (long‐term) effect can be poor (Espadale et al., 2018). Implementing the highest standards of infection control in companion animals is important, not only for good AMS in animals but also for human health. In recent years, many studies have assessed the variety of antimicrobial use practices in companion animals and identified areas where use could be improved or where there are unmet needs (e.g., Murphy et al., 2012; Jacob et al., 2015; Hardefeldt et al., 2017; Goggs et al., 2021). Although it is beyond the scope of this chapter to critically review these, areas for improvement from an AMS perspective are listed in Table 22.1. Table 22.1 Areas where current antimicrobial use and stewardship practices could be improved in companion animal medicine. An antimicrobial stewardship program (ASP) consists of a bundle of different stewardship approaches. There is no standard approach and not all components apply equally to all veterinary situations or are of equal value. Practice type (e.g., type of companion animals, referral vs primary care), size, geographic location, and various other factors influence the relevance of different components. Examples of clinical stewardship components are outlined below. Diagnostic approaches fall under the umbrella of antimicrobial stewardship and will be covered in this chapter. The different elements and possible approaches discussed here are summarized in Table 22.2. Further research is needed to confirm the value and priority of these approaches in reducing AMR in companion animals. While the relative risks of the use of different antimicrobials or antimicrobial classes for the development of resistance in animal and human pathogens are only superficially understood, concerns are higher for certain drug classes, where the same drug is used in humans and animals, when the antimicrobial is particularly important for treatment of serious infections in people, and where antimicrobial use in animals is known to lead to resistance in human pathogens, and to illness in people. Table 22.2 Different approaches to antimicrobial stewardship of value or potential value in companion animals. These concerns have led to classification (tiering) of antimicrobials that are used in animals and to understanding that the different tiers are a basic awareness tool to indicate drugs that are of greater concern for specific reasons, particularly from a human health perspective. Various classification systems have been used internationally, such as those described by the World Health Organization (WHO, 2019) or European Medicines Agency (2019), as well as various national systems, differences in which can cause confusion. However, of particular concern are the third‐generation cephalosporins and fluoroquinolones, two drug classes that are commonly used in veterinary medicine and important in human medicine. Efforts to reduce the use of these drugs in animals, particularly for empirical therapy, are common (Chapter 24). Tiering is an awareness and educational approach that aims to influence clinician prescribing by having them consider the tier of potential drug options. Use of drugs in higher tier categories may be appropriate, even for empirical use, but when options are available, the important concept is that the lowest appropriate tier should be used. In general, it is clear that third‐generation cephalosporins and fluoroquinolones are extensively used in companion animals and that stewardship efforts should focus on reducing such use (Goggs et al., 2021). Measures such as infographics, lists of drugs and their categories or “traffic light” labeling of drug containers (e.g., a red sticker on fluoroquinolone bottles, an orange sticker on potentiated penicillins, and a green sticker on tetracyclines) are simple and cost‐free approaches to provide basic education and awareness. In addition to restricting antimicrobials that are stocked in a clinic, restrictions can be placed on how certain antimicrobials are used. This requires balancing a variety of factors, such as patient care, clinical efficiency, a clinician’s freedom to manage cases, and antimicrobial stewardship. A restriction or approval approach is most often used for the highest tier antimicrobials such as vancomycin or carbapenems. A restriction policy can outline when the drug can be used (e.g., culture is required, the isolate must be susceptible to the drug, no lower tier drugs are viable options, the patient must have a reasonable chance of survival with treatment, owners will commit to any other required treatments such as surgery) and the process to obtain it (e.g., completion of a form or checklist, sign‐off by a designated individual). This type of approach can ensure that rare but indicated use is permitted and also prevents unnecessary use and acts as an engagement point for stewardship discussions. Requests for a restricted drug may lead to discussion of other approaches to management of the patient and reducing the spread of antimicrobial resistance through isolation. While most often used in academic referral settings, this type of approach can be implemented in any veterinary setting.
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Antimicrobial Stewardship in Companion Animals
Introduction
Important Aspects of Antimicrobial Stewardship in Companion Animals
Responsibility, Reduction, Replacement, Refinement, Review: 5Rs Approach
Stewardship Education
Infection Control is Critically Important
Clinical Antimicrobial Stewardship Approaches
Drug Categorization
Drug Restrictions
Deescalation
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