Introduction

Antimicrobials play a critical role in the health and welfare of humans and animals. The advent and subsequent widespread availability of antimicrobial agents was one of the most transformative milestones in modern medicine. Without effective antimicrobials for treatment and prophylaxis, major medical and surgical advances would have been impossible, and infectious diseases would account for a much greater health and economic burden. Modern medicine is built on antimicrobials. The rapidly rising problem of resistance requires vigorous multipronged counteraction across a broad field (World Health Organization, 2016).

The optimism that accompanied entry into the “antibiotic era” was quickly tempered by the recognition that microorganisms would not simply surrender to these new therapeutic agents. In addition to discovering penicillin, Sir Alexander Fleming may also be one of the forefathers of antimicrobial stewardship (AMS), as he warned of the dangers of antimicrobial misuse, the selection and dissemination of resistant pathogens, and the consequences of untreatable infections in his Nobel Prize acceptance speech (Fleming, 1945). Clearly, the reality of Fleming’s concerns has been repeatedly validated through successive waves of antimicrobial resistance (AMR) that now threaten human and animal health.

While the concept of antimicrobial resistance and prudent use originated early in the antibiotic era, concern about antimicrobial resistance was largely tempered by continued development of new drugs. Whereas development of new antimicrobials and antimicrobial classes outpaced development of resistance in the 1950s to early 1970s, the trend has now reversed, and emergence and dissemination of resistant bacteria are a problem worldwide. Antimicrobial resistance is a major threat in medicine, associated with increased morbidity, mortality, and treatment costs (Morel et al., 2020). Achieving good stewardship of antimicrobials is now one of the major challenges facing veterinary and human medicine.

Based on the increasing prevalence of antimicrobial resistance and the negative effect on patient outcomes, it is not surprising that factors promoting the development and spread of resistance have come under increasing scrutiny. Antimicrobial misuse and overuse are common in human medicine, where as much as 50% of antimicrobial use continues to be inappropriate in some subspecialties, especially for surgical prophylaxis, despite continued efforts to improve use (ACSQHC, 2019; Velasco‐Arnaiz et al., 2020; Magill et al., 2021); over‐the‐counter antimicrobials are widely available in many low‐ and middle‐income countries, and ready access to antimicrobials via online pharmacies is increasing worldwide. The emergence and dissemination of multidrug‐resistant pathogens have gathered attention well beyond the medical fields, as evidenced by the heightened political and public concern raised by pathogens such as methicillin‐resistant Staphylococcus aureus (MRSA) and carbapenemase‐producing Enterobacterales.

Although there is less information in veterinary medicine, excessive and inappropriate use of antimicrobials can be an important problem in food animals and companion animals (Weese, 2006; Wayne et al., 2011; Hardefeldt et al., 2017, 2020; Singleton et al., 2017; Malijan et al., 2022). Additionally, increased awareness of antimicrobial use in animals and antimicrobial resistance in zoonotic pathogens has increased awareness of veterinary antimicrobial use as a public health concern.

Antimicrobial Resistance is a Wicked, One Health Problem

One Health is the collaborative effort of multiple disciplines working locally, nationally, and globally to attain optimal health for people, animals, and the environment (One Health Initiative Task Force, 2008). Antimicrobial resistance is a quintessential One Health challenge; microbes (and their resistance determinants) in one discipline can be, and are, exchanged with microbes from other disciplines (people or the environment to animals, animals or the environment to people, and animals or people to the environment) so resistance in any of these “reservoirs” can impact the health of others, especially if that resistance develops in zoonotic or anthroponotic microbial species.

In addition, antimicrobial resistance is a wicked problem. A wicked problem is a social or cultural problem that is difficult or impossible to solve for as many as four reasons: incomplete or contradictory knowledge, the number of people and opinions involved, the large economic burden, and the interconnected nature of these problems with other problems. Wicked problems are difficult to resolve, often because they are difficult to define, arise from interdependent and multicausal factors, and are socially complex (Figure 20.1).

Misuse of antimicrobials is driven not only by prescribers but also by consumers. Both prescribers and consumers often do not use antimicrobials appropriately despite being aware of the potential consequences of their actions. Challenges include managing risk, both immediate (patient safety and personal reputation and legal) and delayed (AMR), organizational structure and culture, individualizing core messages according to communication preferences of clients (Frey et al., 2023), as well as financial incentives where prescribing and dispensing are performed by a single business. Effective policy will require experts including clinicians, veterinarians, microbiologists, pharmacists, pharmacologists, epidemiologists, lawyers, economists, and public health professionals to work together for the good of all sectors, not just for human health.

This challenge is further compounded by the global scale of numerous drivers. Resistance is perpetuated by international travel, tourism, and trade and as such, while national policies impact on the prevalence of drug‐resistant infections, these efforts cannot be effective with the global dissemination of resistant bacteria.

Antimicrobial resistance also raises distinctive ethical issues, which must be considered in policy and response activities, and play an important role in supporting the numerous difficult choices involved in balancing the need for antimicrobials to treat disease with protecting antibiotic effectiveness and reducing the spread of drug‐resistant infections (Littmann et al., 2020).

Antimicrobial resistance has additional challenges to those discussed above. Multidrug‐resistant pathogens are already observed in human medicine with increasing frequency and research predicts that, with no intervention, antimicrobial resistance may become the largest health threat to humans by 2050. Time is not on our side. However, those seeking to solve the problem may also be part of the cause. Antimicrobials are often prescribed more than necessary by medical and veterinary professionals, which leads to higher prevalence of drug‐resistant infections. In addition, pharmaceutical companies have steadily reduced research efforts into commercializing new antimicrobial drugs due to lack of financial incentive. Finally, there is currently a lack of institutional structures that can meet the global challenge of antimicrobial resistance effectively (see Chapter 22).

In veterinary medicine, antimicrobials are critical for preventing and treating disease, improving animal welfare, and potentially increasing the safety of food. Veterinarians have an ethical responsibility to use antimicrobials when indicated. They also have a responsibility to ensure the wise use of antimicrobials that is not a replacement for good management or infection control practices nor used at clients’ request nor purely to gain profit. Failure to recognize these responsibilities, and to proactively engage in stewardship, leaves the veterinary profession at risk of having antimicrobial prescribing restrictions imposed. Restrictions on when Critically Important Antimicrobials (see below) can be prescribed is already a reality in some countries, with others restricting the profit veterinarians can make from selling antimicrobials.

Accordingly, the focus must be on the appropriate use of antimicrobials to balance concerns regarding antimicrobial resistance and positive effects of antimicrobial use. In addition, the profession globally must demonstrate its commitment to appropriate use and stewardship to ensure that access to antimicrobials is maintained. Even small actions can have a cumulative effect in reducing the burden of future antimicrobial resistance.

What is Antimicrobial Stewardship?

Antimicrobial stewardship (AMS) is the term increasingly used to describe the multifaceted approaches required to sustain the efficacy of antibiotics and minimize the emergence of resistance. Previously, terms such as prudent use or judicious use were used but these have now largely become elements within the broader term AMS.

The complexity of factors affecting the effectiveness of antibiotic use (Chapters 1, 4–6), and of resistance and its epidemiology (Chapter 3), means that effective stewardship requires multiple approaches. In large human hospitals, this often encompasses multidisciplinary teams, including clinicians, clinical microbiologists, pharmacists, epidemiologists, and infection control practitioners. The term stewardship resonates with a sense of dedicated obligation, as in its use in the concept of “environmental stewardship.” Stewardship in the context of AMS takes on the original (Middle English) meaning, which refers to the higher order of management of a situation that is necessary when the steward takes personal responsibility for the management of a valuable resource entrusted to their care. In human hospital practice, a key strategy of stewardship has been drug restriction and preauthorization of use of certain antibiotics, but the concept of stewardship must go beyond its use as simply a euphemism for restriction. Antimicrobial stewardship programs have been mandatory for human healthcare (ACSQHC, 2017; Joint Commission International Accreditation Standards for Hospitals, 2017), and it is difficult to justify any lesser expectation in veterinary medicine.

In human medicine, successful AMS programs, like broader infection control programs, tend to be multimodal interventions incorporating different actions as well as structures to support the program. Structural elements include governance or leadership, policies or rules, resources such as staff time and access to experts and tools and mechanisms for tracking and reporting antimicrobial use. Actions may include a combination of educational initiatives, prescription interventions such as traffic light systems, restriction or approval and postprescription review, and antimicrobial use audits and similar measures (CDC, 2014). The complexity of antimicrobial resistance requires multiple interventions targeting variations of disease prevention, management improvement, and refined antimicrobial use practices, all elements encompassed within the framework of AMS.

The need for veterinary medicine to embrace AMS, in its multifaceted dimensions, is recognized by the WHO global action plan on antimicrobial resistance (WHO, 2016) and various national action plans. Antimicrobial stewardship takes a continuous improvement and dynamic approach to addressing resistance and sustaining the future of antimicrobial therapy. Numerous small actions that will have large cumulative effects are required to address a problem of such multidimensional complexity. Each action on its own may seem minor or insignificant but cumulatively has a significant effect.

Stewardship addresses the entire dimensions of antimicrobial use as well as approaches to prevent and control infection. Everyone associated with antibiotic use, whether government regulators, individual veterinarians, or animal owners, needs to be involved in a stewardship approach. At the “front‐line” veterinary practitioner level, embracing stewardship will involve moving beyond concepts into generally accepted practice standards and implementing interventions to effect behavior change. Included is the need to find ways to measure outcomes of implementation, to promote continuing education, and to ensure that guidelines are dynamic and able to change as needed. The general principles of antimicrobial use, which underlie stewardship, are outlined in Table 20.1. The elements of stewardship are illustrated in Figure 20.2.

Considerations in Facilitating Antimicrobial Stewardship

Antimicrobial stewardship has multidimensional components encompassing the effective use of antimicrobials while minimizing the development and spread of resistance. It needs to involve everyone, but particularly those involved in antibiotic use. Only a stewardship mindset will ensure the long‐term sustainability of antimicrobial medicines. Although the veterinary practitioner is on the front line of stewardship, the evolving concept of stewardship involves many other elements and actors (Figure 20.2). A summary of the different elements of AMS discussed in this chapter is given in Table 20.2.

Implementation science

Behavior change

Leadership

Measurement of effectiveness

Measurement of use

Benchmarking

Reduction of use

Big data to monitor use

Antimicrobial guidelines

Antimicrobial selection

Diagnostic testing

Regulation of AMS

Alternatives to antimicrobial use

Infection control

Vaccination

Implementation Science

Even when effectively implemented, interventions and practice changes still might not produce expected outcomes if effectiveness is lost during implementation, or if the intervention or practice was not even effective in the first place. Implementation science is the scientific study of methods and strategies that facilitate the uptake of evidence‐based practice and research into regular use by practitioners and policy makers. The field of implementation science seeks to fill the gap between what we know and what we do by identifying and addressing the barriers that slow or halt the uptake of proven interventions and evidence‐based practices. These considerations are critical in implementing AMS interventions. Without addressing factors such as behavioral change and leadership, AMS programs are unlikely to impact prescribing in veterinary medicine.

Behavioral Change

Regardless of the components of AMS, an important outcome is a change of behavior by prescribers which is often not easy to achieve. Behavior change science should be an integral part of designing AMS programs to maximize the likelihood that interventions will improve the quality of use of antimicrobials. It is unlikely that the “one size fits all” approach will work and the implementation of evidence‐based interventions from one setting into another is greatly strengthened by taking time to tailor them to the relevant sociocultural context, which influences the attitude to antimicrobials of prescribers, patients, and even the professions. Veterinarians are critical to the process of designing AMS programs for veterinary practice if the outcome is to change our behavior.

In addition to involving practitioners in the process of program design, an understanding of the drivers of behavior is beneficial in both implementation and as a prescriber whose habits must change. Numerous frameworks have been described and the COM‐B (Capability, Opportunity, Motivation‐Behavior) is a useful way of understanding what drives others and our behavior. COM‐B is a model of behavior which postulates that for a behavior to occur, individuals must have the physical and psychological capability, physical and social opportunity, and reflective and automatic motivation (Michie et al., 2011). By understanding the relative importance of the different COM‐B domains, potential interventions can be identified to improve the stewardship of antimicrobials.

All veterinarians have the physical skills needed to prescribe antimicrobial medicines appropriately; however, psychological capability entails knowledge, behavioral regulation and memory, attention, and decision processes. For example, awareness of prescribing rate, in comparison to peers, allows veterinarians who are high prescribers to reflect on why they prescribe more than others and to consider how to reduce the rate accordingly. Therefore, benchmarking is an important part of behavioral change. Stewardship components that intervene at important decision points present opportunities for affecting psychological capability. As an example, reorganizing antimicrobials in the pharmacy so that Critically Important Antimicrobial medicines are marked in red and located high on the shelf, out of immediate view, may prompt veterinarians to recall the importance of these drugs at a critical point in the prescribing/dispensing process.

Physical opportunity requires an environment that is conducive and has adequate resources. The environment should be organized in such a way that it is appropriate not to prescribe antimicrobials if they are not indicated. This is not the case in many veterinary clinics, where the hierarchical practice structure and time pressures often mean it is easier to prescribe even when it is known that antimicrobials are not indicated. The role of nurses and technicians is often undervalued in this context. Nurses and technicians often have first contact with clients and ensuring they are not promoting the case for antimicrobials with clients is critical. Nurses can and should act as stewards by educating clients on infection control, administering medications, nursing care, and alternatives to antimicrobials. Pharmacies should be stocked with antimicrobials with lesser importance to human medicine (e.g., amoxicillin, doxycycline) and veterinarians should have resources available to support decisions of no antimicrobials for patients.

The social opportunity or social influences are also important. The belief that antimicrobial resistance is caused by “other prescribers” and that the responsibility lies with others within the veterinary profession is a common attitude. Veterinarians need to see other prescribers (all sectors of the veterinary profession, doctors, dentists, etc.) also aiming to reduce the threat of antimicrobial resistance to improve the belief that their own actions can impact collectively on the rate of antimicrobial resistance.

Reflective motivation is the belief about the consequences of one’s actions, optimism, and capabilities. Clinicians are trained based on improving the health of the animal in front of them and an active awareness of the consequences of inappropriate use of antimicrobials is required. One of the most identified factors associated with inappropriate prescribing in human and veterinary medicine is complacency (Teixeira Rodrigues et al., 2013; Hardefeldt et al., 2018a). Veterinarians need to change a common attitude that prescribing antimicrobials to animals that don’t need them “won’t do any harm” and will appease the client. On the other hand, when rare events do occur, veterinarians should feel supported in their decision making.

Automatic motivation is the reinforcement and emotion surrounding prescribing. Fear is another common driver for inappropriate prescribing of antimicrobials. There is often fear not only of the risk of disease progression but also of losing patients to competitors (Hardefeldt et al., 2018a; Scarborough et al., 2023). Fear because of diagnostic uncertainty should be rationally evaluated and “just‐in‐case” prescribing avoided. The profession‐wide approach to AMS should mitigate the risks of losing clients. In the absence of this, strong support from practice leadership is required. A participatory approach has been effective in changing antimicrobial use practices by farmers (Morgans et al., 2021) and may also be effective with veterinarians.

Leadership

Leadership is required at multiple levels to achieve AMS. International, national, and professional leaders are important for profession‐wide change but since this chapter is practitioner focused, only clinic‐level leadership is considered here.

The AMS leader or team, sometimes called champions, can develop a clear vision and successfully convey this to their peers. They inspire staff and focus on finding solutions to barriers and think strategically by working with all practitioners within a practice to achieve change. Change at a practice level requires four conditions: a belief in a shared purpose, reinforcement systems, consistent role models, and skills and resources to support change. Champions can provide all of these if sufficiently trained and empowered but require backing from practice owners or corporations. This model is widely used in medical practice and has been reported in veterinary practice in Wales (Rees et al., 2021). A novel One Health model which developed from a collaboration of the Tufts Medical Center and nearby Foster Hospital for Small Animals shares interdisciplinary experiences in infection control and antimicrobial stewardship with the potential of multiple benefits for animal and human health and welfare, providing a model for wider adaptation and adoption (Sjoberg et al., 2023).

Measuring Stewardship and Its Effectiveness

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2. Regulation of Antimicrobial Use in Animals
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