Zoonoses and Public Health
ORIGINAL ARTICLE
Factors Associated with the Inappropriate Use of Antimicrobials W. McIntosh and W. Dean Texas A&M University – Sociology, College Station, TX, USA
Impacts
• The inappropriate use of antimicrobials in human patients and food • •
animals hastens the time at which these drugs lose their ability to combat infections. We review the characteristics of those who tend to misuse these drugs and introduce the Theory of Planned Behavior (TPB) as a means of further understanding this problem. We then recommend that the TPB be used in wide-spread efforts to identify and change the beliefs about the use of antimicrobials by those who have considerable influence over the use of antimicrobials in animal agriculture.
Keywords: Antimicrobial resistance; epidemiology; public health; social science; theory of planned behavior Correspondence W. McIntosh. Texas A&M University – Sociology, 4351 TAMU College Station, TX 77843-4351, USA. Tel.: 979-845-8522; Fax: 979-862-4057; E-mail: w-mcintosh@ tamu.edu Received for publication September 30, 2013 doi: 10.1111/zph.12169
Summary Antimicrobial resistance continues to grow and antimicrobial use in food animal production and to a lesser extent in human patients is under fire. Much of the criticism has to do with the misapplication of these drugs in both settings. Research indicates that patients, food animal producers, physicians and veterinarians have all played a part in misusing antimicrobials, often because of mistaken beliefs. This paper reviews this research and introduces a theoretical perspective, the Theory of Planned Behavior (TPB), which broadens our understanding of the motivations for misuse. In particular this approach shows that individuals making decisions about antimicrobial use take into account social pressures from and a sense of obligation to significant others in their social networks. Our own work summarized in this paper indicates that both feedlot veterinarians and feedlot managers’ antimicrobial decisions are influenced by both expectations from and obligations to a variety of actors in the feedlot network (other veterinarians, feedlot clients, consumers, pharmaceutical companies, and regulatory bodies). Generally across 4 circumstances of antimicrobial use (for acutely sick cattle, chronically-sick cattle, at-risk cattle, high-risk cattle), it is largely the perception that peers and clients expect feedlot veterinarians to use antimicrobials and feedlot veterinarians sense of obligation to these groups that have the most influence on their decisions to recommend antimicrobials. Based on these findings, the question of engaging in changing the choices made by those working with food animals must start with those who influence the decision to proscribe or use antimicrobials. As our data come from the United States and may be unique relative to other countries, these efforts should begin by ascertaining who influences these decisions. The next step is to then change the beliefs of these significant others.
Introduction Antimicrobials play an important role in human and foodanimal health. As antimicrobials are used over time, the probability increases that the microbes that are designed to 22
kill will develop resistance to these drugs. Thus, inappropriate use of antimicrobials hastens the point at which they lose their effectiveness (Meyer et al., 2013). Among human patients, inappropriate use of antimicrobials is in part due to patients who harbour the mistaken belief that
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antimicrobials are an effective treatment for viral infections. Inappropriate use in animal industry may be motivated by the economic benefits, which accrue from using antimicrobials to improve the efficiency of feeds in promoting growth (Allen et al., 2013). In addition, physicians and patients are notorious for failing to follow usage directions associated with prescribed and over-the-counter medications (Pulcini and Gyssens, 2013), a behaviour which also occurs to some degree in the treatment of food animals (Hughes et al., 2012). The purpose of this paper is to describe the factors we have identified that have been determined to predict the misuse of antimicrobials in the U.S. cattle-feeding industry. To identify these, a variety of terms was used to search the literature for any scholarly work on the determinants of antimicrobial use among both animal and human populations. We identified many studies that were a-theoretical and overlooked the attitude, belief, moral and normative determinants of use and misuse. The only theoretical approaches found in these studies were the expectancy value models known as the theory of planned behaviour (TPB) and its progenitor, the theory of reasoned action (TRA). We thus briefly describe these a-theoretical studies followed by an examination of the TPB and TRA-driven works. The paper then presents previously published findings from our study of feedlot managers and feedlot veterinarians, which used a modified version of the TPB to predict attitudes towards and uses of antimicrobials in feedlot cattle. The paper concludes with how the TPB might be applied to reduce inappropriate use.
Antimicrobial Use and Resistance Patients and physicians In a nine-country study, patients reported they often demanded antimicrobials from their physicians for upper tract respiratory infections (UTRI) and a few exaggerated symptoms to obtain these drugs (Pechere, 2001). The same study found that 20% of the patients admitted to misusing antimicrobials by saving them for future consumption rather than following the prescribed course. While evidence exists that patients demand antimicrobials for viruses, some researchers have noted that physicians often perceive their patients wish to receive these drugs when in fact those patients do not (Altiner, 2004). Others have found some physicians associate antimicrobial prescriptions to patient satisfaction with their treatment (Tonkin-Crine et al., 2011), but still others have found that patient satisfaction is more closely associated with whether their doctor spends enough time ‘to explain their illness and the choice of treatment’ (Terry, 2001:73). However, some studies found that antimicrobials were prescribed when the diagnosis was
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unclear or after receiving pressure from drug company representatives (Kotwani et al., 2010). Some Swedish GPs were found to perceive that drug resistance was not a problem in their practice or perceived that all physicians potentially contributed to the problem (Rkman et al., 2013). A number of those in the latter category followed all of the recommended treatment guidelines for UTRI. Others understood the issues but had not yet altered their behaviour. When a regimen of antimicrobials failed to alleviate an infection, a few physicians have blamed ‘viral aetiology’ rather than possible antimicrobial resistance (Wood et al., 2012:237). Finally, Wood et al. (2007) reported on the effect of social responsibility associated with prescribing broad spectrum antimicrobials, with some physicians justifying their use as a responsibility to the patient while others saw withholding these as their obligation to society. Food animals, animal producers and veterinarians Some studies strongly suggest that those caring for food animals either over- or underuse antimicrobials under a variety of circumstances. In one such study, a few Belgian broiler raisers failed to follow prescribed dosage requirements of antimicrobial administration (Pesoons et al., 2012). Wisconsin dairy farmers believed they utilized the ‘right’ amount of antimicrobials, but not all had a written protocol for the use of these drugs (Hoe and Ruegg, 2006). Other studies have reported the lack of such protocols (Friedman et al., 2007), but one nation-wide US study found that 51% of dairies had such a plan (Walker et al., 2012). An additional issue is that the presence of an antimicrobial plan does not guarantee that it is carefully followed. Furthermore, not all veterinarians have agreed that antimicrobials can lose their effectiveness over time and thus have not initiated discussions of antimicrobial resistance with their dairy farmer clients (Cattaneo et al., 2009). One study of small animal veterinarians in the UK found that 5% of their drug prescriptions were under the recommended dosage and 20% were over the recommended level. Incorrect dosage prescriptions were associated with their use of pharmaceutical companies as a source of information (Hughes et al., 2012). Missing from this research is a systematic examination of the influence of others on physicians, veterinarians and their clients’ antimicrobial use. None of the studies spoke of moral obligations to either use or not use antimicrobials in food animals. The Theory of Planned Behaviour Researchers have long-sought models that predict and explain behaviour. One class of models is based on attitudes and assumes that deciding to behave in a particular
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way results from a rational decision-making process that involves beliefs, attitudes and intentions. One of the more successful of these models is the theory of planned behaviour (TPB), which has largely superseded its progenitor, the theory of reasoned action (TRA). Both the TRA and the TPB begin with the assumption that most behaviour is under a person’s control and thus view a person’s intention to perform (or not perform) a behaviour as the chief motivating factor of behaviour (Ajzen, 1991). Furthermore, to understand behaviour, we have to understand the causes of intentions. Two factors prevail: one is personal and the other social. Personal factors involve (i) attitudes or the positive or negative evaluation of performing the behaviour or/and (ii) the belief that one has the ability to perform the behaviour. Social factors include perceived social pressures from significant others and moral obligations to these significant others to either perform or not perform the behaviour. Social pressures are referred to as subjective norms. Attitudes are based on beliefs, which involve the perception that the outcomes of the behaviour are either positive or negative, and are referred to as behavioural beliefs. However, some perceived outcomes seem more important than others. The perceptions of whether other people who are important to the individual would want him or her to engage in the behaviour (subjective norms) vary as well. Similar to outcomes, not all of these people’s judgments are equally important when it comes to a particular behaviour. Finally, perceived behavioural control (PBC) has to do with the perception the individual has regarding her or his ability to successfully perform the behaviour. PBC is the concept that was added to the TRA, transforming that model into the TPB. Applications of the TPB and TRA to antimicrobial use Most of this work has focused on physicians’ prescription of antimicrobials to patients, often in hospital settings. Beginning with findings regarding attitudes and beliefs, those clinicians who believed in the efficacy of prescribing drugs for infections such as UTRI tended to have a greater intention to continue this practice (Walker et al., 2001, 2004). Others reported that having a positive attitude about hospital protocols or beliefs in their efficacy was more likely to follow those protocols or to fill prescriptions (Limbert and Lamb, 2002; Saengcharoen et al., 2008). Others who believed the use of antimicrobials for UTRI increased the risk of antimicrobial resistance were less likely to prescribe these drugs for such infections, but were more likely to prescribe antimicrobials if they believed their patients would seek out another physician when denied these drugs (Walker et al., 2001). Several studies found behavioural control to be important, in that physicians were more likely 24
to follow hospital protocols regarding antimicrobial use if they perceived they had complete control over the prescribing of drugs (Limbert and Lamb, 2002; Cortoos et al., 2012). Finally, subjective norms were found to be important in several studies in that physicians and pharmacists were willing to follow protocols or avoid inappropriate prescription of antimicrobials if this was expected by colleagues or senior hospital staff (Walker et al., 2001; Limbert and Lamb, 2002; Liabsuetrakul et al., 2003; Saengcharoen et al., 2008). This set of studies found that subjective norms played a major role in the prescription of antimicrobials, and they played a major role in our own research. However, we discovered feedlot managers and veterinarians often not only feel pressure from particular significant others but also feel a sense of moral obligation to those significant others when it comes to prescribing antimicrobials. Our Feedlot Study Research on human and animal patients found that subjective norms play a major role in the prescription of antimicrobials, but this research has not explored the role of moral obligation to significant others in the prescription of antimicrobials. We addressed this issue in our study of the ‘Moral Economy of Antimicrobials in Animal Agriculture: Advancing Policy and Practice in an Era of Antimicrobial Resistance’, which examined the use of antimicrobials in the cattle-feeding industry. We consider the business of raising and slaughtering cattle to consist of an interdependent network of actors: the production–consumption chain which includes cow–calf operators, feedlot operators, meat processors, retailers, and consumers, other influential actors such as veterinarians, nutritionists, pharmaceutical companies, professional and business groups associated with cattle (e.g. Texas Cattlemen’s Association), and regulatory and advisory bodies of governments (i.e. the Food and Drug Administration (FDA), State Licensing Boards that license veterinarians and the Centers for Disease Control (CDC). Our study focused on feedlot operators and feedlot veterinarians, but included the relationships that these two groups had with others in the feedlot network. We measured the frequency with which feedlot operators used antimicrobials and feedlot veterinarians’ recommended use of antimicrobials in acutely sick cattle, chronically sick cattle, at-risk cattle (young age) and high-risk cattle (exposure to stress). We asked respondents about their beliefs regarding the efficacy of antimicrobial use (i.e. improves health, improves well-being and makes cattle more profitable) in each of the four circumstances; attitudes towards using antimicrobials (importance in improving health, well-being and profitability) and perceived behavioural control (use of antimicrobials is an economic
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necessity) under each of the four circumstances. In order to capture subjective norms, we asked the degree to which of the actors described above expected the feedlot managers to use, or feedlot veterinarians to recommend the use of antimicrobials, in each of the four circumstances. We also asked how important it was to meet the expectations of each of these persons or institutions. We then asked whether there was a moral obligation to each of these types of individuals or institutions to use antimicrobials under each of the four circumstances and the importance of each of those obligations. Greater detail regarding our methodological procedures is provided in Dean and Scott (2005), Dean et al. (2011), McIntosh et al. (2009a,b), Jan et al. (2010, 2012). Perceptions of feedlot owners and managers The perceptions of feedlot owners and managers of the degree of agreement among key groups and individuals in the feedlot network that antimicrobials should be used to treat feedlot cattle varied significantly across circumstance of treatment. Perceived agreement was highest for acutely sick cattle, followed by high-risk cattle, then at-risk cattle and last chronically sick cattle. Those in the consumer segment (i.e. packers, retailers, consumers) of the network were less likely to be perceived as believing that antimicrobials were necessary under any of the four circumstances. With the exception of acutely sick cattle, the FDA was perceived as less in agreement about the need to use antimicrobials under the remaining circumstances. However, despite these differences, it is clear that these owners and managers perceived these expectations of many other members of the feedlot network to be an important consideration in their own decision-making. Only the expectations of other feedlot operators and pharmaceutical companies were considered of little importance. Somewhat fewer feedlot operators perceived they had a moral obligation to network members to use antimicrobials in their cattle. Several profound differences between perceived obligations and expectations occurred in the cases of other feedlot operators, feedlot nutritionists and pharmaceutical companies. The feedlot operators believed these three members of the network expected them to use antimicrobials, but far fewer believed they had an obligation to those members to do so. By contrast, the operators believed that beef consumers were less likely to expect them to use antimicrobials in each of the four circumstances, but greater percentages of operators tended to believe they had an obligation to consumers to do so. A majority of feedlot operators considered that they had a moral obligation to the cattle themselves to treat those cattle with antimicrobials, but the degree of this perceived obligation varied by circumstance.
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Perceptions of feedlot veterinarians Feedlot veterinarians reported varied perceptions of feedlot network members’ antimicrobial use expectation and their moral obligations to those members. Pharmaceutical companies were perceived by a higher percentage than other significant others to expect feedlot veterinarians to recommend the use of antimicrobials regardless of the circumstance. The next highest level of social pressure came from clients (i.e. feedlot operators and retained owners of cattle); however, there was considerable difference in these percentages by treatment circumstance. Perceived pressures from regulatory and professional organizations (norm setting bodies), while high in the case of acutely sick cattle, dropped off considerably for the remaining three circumstances. Perceived pressures from colleagues (i.e. other veterinarians and feedlot nutritionists) tended to be as high as those from clients. There was less strong agreement on perceived moral obligations to many of these members. Thus, for example, while the perception that colleagues, some members of the consumer sector, and pharmaceutical companies held strong expectations that the feedlot veterinarians should use these drugs, particularly in the cases of acutely sick and chronically sick animals, feedlot veterinarians were less likely to agree they had an obligation to these network members to prescribe these treatments. Subjective norms and moral obligations influenced both attitudes about using antimicrobials across the four treatment circumstances and the recommendations about their use under these circumstances. Perceptions that colleagues expected them to use antimicrobials in the case of acutely sick and high-risk cattle tended to lead to a more favourable attitude towards using antimicrobials under these circumstances. A second generalization concerns the expectations of clients: the greater the clients’ expectation that antimicrobials be used in chronically ill and at-risk cattle, the more favourable the veterinarians’ attitude that using antimicrobials under these circumstances was important. High client expectations regarding the use of antimicrobials in at-risk cattle were associated with more frequent recommendations for the use of antimicrobials under this circumstance. Perception of a moral obligation to the public also was associated with a negative attitude about recommending antimicrobials for at-risk cattle (Jan et al., 2010). Finally, when perceived expectations of regulatory bodies regarding the use of antimicrobials in high-risk cattle were low, feedlot veterinarians tended to recommend this use in high-risk cattle, but veterinarians’ sense of obligation to clients to recommend antimicrobials for such cattle increased the likelihood they made such recommendations. Perceptions of antimicrobial risk under a given circumstance tended to be less when there was a strong subjective
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norm and strong moral obligation to use antimicrobials in that circumstance. A limited number of feedlot network members played a role here. The most common set of network members whose expectations and obligations supported the use of antimicrobials were colleagues and clients (see Jan et al., 2012). Changing Behaviour The use of TPB in interventions A review of 45 studies that examined the success and failure of efforts to improve the use of pharmaceuticals found that the behaviour of governments, pharmaceutical companies, health professionals, retailers and consumers would need to be changed (Homedes and Ugalde, 2001). We believe a more important lesson we learned from our research on the feedlot industry is that salient others exhibit regular patterns of influence on those who use antimicrobials. This suggests an avenue for changing antimicrobial behaviours and one that might allow changes in a widespread basis. Efforts to change hospital physicians’ use of antimicrobials, while showing some success, are usually confined to single hospitals. To take advantage of the TPB in wider change efforts, Fishbein and Ajzen (2010) recommend formative research before embarking on an intensive effort to change behaviour among a large number of people. Meetings with key informants in groups would provide a means of informing an evaluation of the issues surrounding the misuse of antimicrobials, the risk of antimicrobial resistance and the means to alleviate both. Interviews of the informants would include an assessment of current behaviour as well as perceptions of the efficacy of their current behaviour, an indication of the people and groups that influence their current behaviour and who might object to changing their behaviour, and constraints that would make it difficult to change their behaviour. Once these salient others are identified, they would become the target of the first effort to reduce antimicrobial use. After persuading these individuals and groups, they would then become part of the vanguard to change the behaviour of antimicrobial users. One issue neglected in this literature is that of mistrust. In the United States, for example, mistrust exists among feedlot veterinarians of government antimicrobial recommendations (Dean et al., 2011), and the belief among cow– calf operators (McIntosh et al., 2009a,b) and dairy farmers that some federal agencies do not have their best interest in mind when making policy (McIntosh et al., 2010). The lesson here is that the choice of salient others for employment as change agents in the effort to reduce the use of antimicrobials must take trust issues into account. We can learn from what appears to be successful efforts in more widespread efforts to reduce antimicrobial 26
use that involve those who influence antimicrobial use. An NGO and several universities have introduced greater control over antimicrobial use in selected hospitals located in a number of provinces in Vietnam by identifying key individuals who serve as sources of subjective norm and involving them in the intervention (Wertheim et al., 2013). In Sweden, a national effort was begun by bringing together key actors in the health field including the Swedish Institute for Infectious Disease Control, Medical Products Agency, National Corporation of Swedish Pharmacies, the Swedish Board of Agriculture and others. Regional subgroups were also brought into the mix (M€ olstad et al., 2008). Perhaps one of the most notable conceptual frameworks for intervening in agricultural and health practices is the widely employed adoption of innovations theory. This framework has not been used in prior research to either understand or intervene in human health or veterinary antimicrobial practices. Work using this theory finds that changing attitudes and beliefs are necessary before behaviour can be changed. These changes require more than information provision; instead, this literature emphasizes the importance of contact with persuasive change agents. One aspect of this contact is the frequency of interaction (Monge et al., 2008). At the same time, the stronger the social connections with peers, the more difficult it is to change a given individual’s behaviour. However, the more people identify with innovators in their organization or community, the more likely they will embrace those innovations recommended by these influential members of the community. Acknowledgements Our research was funded by the United States Department of Agriculture-CRSEES (Grant #2002-51110-01959). Support for the presentation of this paper was provided by the Organization for Economic Cooperation and Development. Conflict of Interest The authors have no conflicts of interest to declare. References Ajzen, I., 1991: The theory of planned behavior. Organ Behav Hum Decis 50, 179–211. Allen, H. K., U. Y. Levine, T. Looft, M. Bandrick, and T. A. Casey, 2013: Treatment, promotion, commotion: antibiotic alternatives in food-producing animals. Trends Microbiol. 21, 114–119. Altiner, A., 2004: Acute cough: a qualitative analysis of how GPs manage the consultation when patients explicitly or
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McIntosh, W. A., S. Schulz, W. Dean, H. M. Scott, K. S. Barling, and I. Takei, 2009a: Feedlot veterinarians’ moral beliefs and instrumental beliefs regarding antimicrobial use in feedlot cattle. J. Community Appl. Soc. 19, 51–67. McIntosh, W. A., W. Dean, B. Norby, H M. Scott, A. Delgado, and J. Davis, 2009b: Trust, risk, and moral obligations in the beef cattle industry. Presented at the annual meeting of the Association for the Study of Food and Society, May 31, State College, Pennsylvania. McIntosh, W.A., B. Norby, W.R. Dean, H.M. Scott, A. Delgado, J. Davis, and J-s. Jan, 2010: Risk, trust, and moral obligations and attitudes in the Texas dairy industry. Presented at the annual meeting of the Rural Sociological Society August 13, Boise, Idaho. Meyer, E., P. Gastmeirer, M. Deja, and F. Schwab, 2013: Antibiotic consumption and resistance: data from Europe and Germany. Int. J. Med. Microbiol. 303, 388–395. M€ olstad, S., M. Erntell, H. Hanberger, E. Meander, C. Norman, G. Skoog, C. Stalsby Lundborg, A S€ oderstr€ om, E. Tarell, and O. Cars, 2008: Sustained reduction of antibiotic use and low bacterial resistance: 10-year follow-up of the Swedish Strama programme. Lancet Infect. Dis. 8, 125–132. Monge, M., F. Harwich, and D. Halgin, 2008: How Change Agents and Social Capital Influence the Adoption of Innovations Among Small Farmers: Evidence From Social Networks in Bolivia. IFPRI Discussion Paper 00761. International Food Policy Research Institute, Washington, DC. Pechere, J. C., 2001: Patients’ interviews and misuse of antibiotics. Clin. Infect. Dis. 33, S170–S173. Pesoons, D., J. Dewulf, A. Smet, L. Herman, M. Heyndricks, a. Martel, B. Catry, P. Buataye, and F. Haesebrouck, 2012: Antimicrobial use in Belgian broiler production. Prev. Vet. Med. 105, 320–325. Pulcini, C., and I. C. Gyssens, 2013: How to educate prescribes in antimicrobial stewardship practices. Virulence 4, 192–202. Rkman, I. B.J., J. Berg, N. Viber, and C. St. L. Lundborg, 2013: Awareness of antibiotic resistance and antibiotic prescribing in UTI treatment: a qualitative study among primary care physicians in Sweden. Scand. J. Prim. Health 31, 50–55. Saengcharoen, W., V. Chongsuvivatwong, S. Lerkiatbundit, and P. Wongpoowarak, 2008: Factors influencing dispensing of antibiotics for upper respiratory infections among southern Thai community pharmacists. J. Clin. Pharm. Ther. 33, 123– 129. Tonkin-Crine, S., L. Yardley, and P. Little, 2011: Antibiotic prescribing for acute respiratory tract infections in promary care: a systematic review and meta-ethenography. J. Antimicrob. Chemither. 66, 2215–2223. Terry, K., 2001: How to say no when antibiotics won’t help. Med. Econ. 78, 73, 76, 79-80. Walker, A. E., J. M. Grimshaw, and E.M. Armstrong, 2001: Salient beliefs and intentions to prescribe antibiotics for patients with a sore throat. Br. J. Health Psychol. 6, 347– 360.
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ORIGINAL ARTICLE
Factors Associated with the Inappropriate Use of Antimicrobials W. McIntosh and W. Dean Texas A&M University – Sociology, College Station, TX, USA
Impacts
• The inappropriate use of antimicrobials in human patients and food • •
animals hastens the time at which these drugs lose their ability to combat infections. We review the characteristics of those who tend to misuse these drugs and introduce the Theory of Planned Behavior (TPB) as a means of further understanding this problem. We then recommend that the TPB be used in wide-spread efforts to identify and change the beliefs about the use of antimicrobials by those who have considerable influence over the use of antimicrobials in animal agriculture.
Keywords: Antimicrobial resistance; epidemiology; public health; social science; theory of planned behavior Correspondence W. McIntosh. Texas A&M University – Sociology, 4351 TAMU College Station, TX 77843-4351, USA. Tel.: 979-845-8522; Fax: 979-862-4057; E-mail: w-mcintosh@ tamu.edu Received for publication September 30, 2013 doi: 10.1111/zph.12169
Summary Antimicrobial resistance continues to grow and antimicrobial use in food animal production and to a lesser extent in human patients is under fire. Much of the criticism has to do with the misapplication of these drugs in both settings. Research indicates that patients, food animal producers, physicians and veterinarians have all played a part in misusing antimicrobials, often because of mistaken beliefs. This paper reviews this research and introduces a theoretical perspective, the Theory of Planned Behavior (TPB), which broadens our understanding of the motivations for misuse. In particular this approach shows that individuals making decisions about antimicrobial use take into account social pressures from and a sense of obligation to significant others in their social networks. Our own work summarized in this paper indicates that both feedlot veterinarians and feedlot managers’ antimicrobial decisions are influenced by both expectations from and obligations to a variety of actors in the feedlot network (other veterinarians, feedlot clients, consumers, pharmaceutical companies, and regulatory bodies). Generally across 4 circumstances of antimicrobial use (for acutely sick cattle, chronically-sick cattle, at-risk cattle, high-risk cattle), it is largely the perception that peers and clients expect feedlot veterinarians to use antimicrobials and feedlot veterinarians sense of obligation to these groups that have the most influence on their decisions to recommend antimicrobials. Based on these findings, the question of engaging in changing the choices made by those working with food animals must start with those who influence the decision to proscribe or use antimicrobials. As our data come from the United States and may be unique relative to other countries, these efforts should begin by ascertaining who influences these decisions. The next step is to then change the beliefs of these significant others.
Introduction Antimicrobials play an important role in human and foodanimal health. As antimicrobials are used over time, the probability increases that the microbes that are designed to 22
kill will develop resistance to these drugs. Thus, inappropriate use of antimicrobials hastens the point at which they lose their effectiveness (Meyer et al., 2013). Among human patients, inappropriate use of antimicrobials is in part due to patients who harbour the mistaken belief that
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antimicrobials are an effective treatment for viral infections. Inappropriate use in animal industry may be motivated by the economic benefits, which accrue from using antimicrobials to improve the efficiency of feeds in promoting growth (Allen et al., 2013). In addition, physicians and patients are notorious for failing to follow usage directions associated with prescribed and over-the-counter medications (Pulcini and Gyssens, 2013), a behaviour which also occurs to some degree in the treatment of food animals (Hughes et al., 2012). The purpose of this paper is to describe the factors we have identified that have been determined to predict the misuse of antimicrobials in the U.S. cattle-feeding industry. To identify these, a variety of terms was used to search the literature for any scholarly work on the determinants of antimicrobial use among both animal and human populations. We identified many studies that were a-theoretical and overlooked the attitude, belief, moral and normative determinants of use and misuse. The only theoretical approaches found in these studies were the expectancy value models known as the theory of planned behaviour (TPB) and its progenitor, the theory of reasoned action (TRA). We thus briefly describe these a-theoretical studies followed by an examination of the TPB and TRA-driven works. The paper then presents previously published findings from our study of feedlot managers and feedlot veterinarians, which used a modified version of the TPB to predict attitudes towards and uses of antimicrobials in feedlot cattle. The paper concludes with how the TPB might be applied to reduce inappropriate use.
Antimicrobial Use and Resistance Patients and physicians In a nine-country study, patients reported they often demanded antimicrobials from their physicians for upper tract respiratory infections (UTRI) and a few exaggerated symptoms to obtain these drugs (Pechere, 2001). The same study found that 20% of the patients admitted to misusing antimicrobials by saving them for future consumption rather than following the prescribed course. While evidence exists that patients demand antimicrobials for viruses, some researchers have noted that physicians often perceive their patients wish to receive these drugs when in fact those patients do not (Altiner, 2004). Others have found some physicians associate antimicrobial prescriptions to patient satisfaction with their treatment (Tonkin-Crine et al., 2011), but still others have found that patient satisfaction is more closely associated with whether their doctor spends enough time ‘to explain their illness and the choice of treatment’ (Terry, 2001:73). However, some studies found that antimicrobials were prescribed when the diagnosis was
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unclear or after receiving pressure from drug company representatives (Kotwani et al., 2010). Some Swedish GPs were found to perceive that drug resistance was not a problem in their practice or perceived that all physicians potentially contributed to the problem (Rkman et al., 2013). A number of those in the latter category followed all of the recommended treatment guidelines for UTRI. Others understood the issues but had not yet altered their behaviour. When a regimen of antimicrobials failed to alleviate an infection, a few physicians have blamed ‘viral aetiology’ rather than possible antimicrobial resistance (Wood et al., 2012:237). Finally, Wood et al. (2007) reported on the effect of social responsibility associated with prescribing broad spectrum antimicrobials, with some physicians justifying their use as a responsibility to the patient while others saw withholding these as their obligation to society. Food animals, animal producers and veterinarians Some studies strongly suggest that those caring for food animals either over- or underuse antimicrobials under a variety of circumstances. In one such study, a few Belgian broiler raisers failed to follow prescribed dosage requirements of antimicrobial administration (Pesoons et al., 2012). Wisconsin dairy farmers believed they utilized the ‘right’ amount of antimicrobials, but not all had a written protocol for the use of these drugs (Hoe and Ruegg, 2006). Other studies have reported the lack of such protocols (Friedman et al., 2007), but one nation-wide US study found that 51% of dairies had such a plan (Walker et al., 2012). An additional issue is that the presence of an antimicrobial plan does not guarantee that it is carefully followed. Furthermore, not all veterinarians have agreed that antimicrobials can lose their effectiveness over time and thus have not initiated discussions of antimicrobial resistance with their dairy farmer clients (Cattaneo et al., 2009). One study of small animal veterinarians in the UK found that 5% of their drug prescriptions were under the recommended dosage and 20% were over the recommended level. Incorrect dosage prescriptions were associated with their use of pharmaceutical companies as a source of information (Hughes et al., 2012). Missing from this research is a systematic examination of the influence of others on physicians, veterinarians and their clients’ antimicrobial use. None of the studies spoke of moral obligations to either use or not use antimicrobials in food animals. The Theory of Planned Behaviour Researchers have long-sought models that predict and explain behaviour. One class of models is based on attitudes and assumes that deciding to behave in a particular
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way results from a rational decision-making process that involves beliefs, attitudes and intentions. One of the more successful of these models is the theory of planned behaviour (TPB), which has largely superseded its progenitor, the theory of reasoned action (TRA). Both the TRA and the TPB begin with the assumption that most behaviour is under a person’s control and thus view a person’s intention to perform (or not perform) a behaviour as the chief motivating factor of behaviour (Ajzen, 1991). Furthermore, to understand behaviour, we have to understand the causes of intentions. Two factors prevail: one is personal and the other social. Personal factors involve (i) attitudes or the positive or negative evaluation of performing the behaviour or/and (ii) the belief that one has the ability to perform the behaviour. Social factors include perceived social pressures from significant others and moral obligations to these significant others to either perform or not perform the behaviour. Social pressures are referred to as subjective norms. Attitudes are based on beliefs, which involve the perception that the outcomes of the behaviour are either positive or negative, and are referred to as behavioural beliefs. However, some perceived outcomes seem more important than others. The perceptions of whether other people who are important to the individual would want him or her to engage in the behaviour (subjective norms) vary as well. Similar to outcomes, not all of these people’s judgments are equally important when it comes to a particular behaviour. Finally, perceived behavioural control (PBC) has to do with the perception the individual has regarding her or his ability to successfully perform the behaviour. PBC is the concept that was added to the TRA, transforming that model into the TPB. Applications of the TPB and TRA to antimicrobial use Most of this work has focused on physicians’ prescription of antimicrobials to patients, often in hospital settings. Beginning with findings regarding attitudes and beliefs, those clinicians who believed in the efficacy of prescribing drugs for infections such as UTRI tended to have a greater intention to continue this practice (Walker et al., 2001, 2004). Others reported that having a positive attitude about hospital protocols or beliefs in their efficacy was more likely to follow those protocols or to fill prescriptions (Limbert and Lamb, 2002; Saengcharoen et al., 2008). Others who believed the use of antimicrobials for UTRI increased the risk of antimicrobial resistance were less likely to prescribe these drugs for such infections, but were more likely to prescribe antimicrobials if they believed their patients would seek out another physician when denied these drugs (Walker et al., 2001). Several studies found behavioural control to be important, in that physicians were more likely 24
to follow hospital protocols regarding antimicrobial use if they perceived they had complete control over the prescribing of drugs (Limbert and Lamb, 2002; Cortoos et al., 2012). Finally, subjective norms were found to be important in several studies in that physicians and pharmacists were willing to follow protocols or avoid inappropriate prescription of antimicrobials if this was expected by colleagues or senior hospital staff (Walker et al., 2001; Limbert and Lamb, 2002; Liabsuetrakul et al., 2003; Saengcharoen et al., 2008). This set of studies found that subjective norms played a major role in the prescription of antimicrobials, and they played a major role in our own research. However, we discovered feedlot managers and veterinarians often not only feel pressure from particular significant others but also feel a sense of moral obligation to those significant others when it comes to prescribing antimicrobials. Our Feedlot Study Research on human and animal patients found that subjective norms play a major role in the prescription of antimicrobials, but this research has not explored the role of moral obligation to significant others in the prescription of antimicrobials. We addressed this issue in our study of the ‘Moral Economy of Antimicrobials in Animal Agriculture: Advancing Policy and Practice in an Era of Antimicrobial Resistance’, which examined the use of antimicrobials in the cattle-feeding industry. We consider the business of raising and slaughtering cattle to consist of an interdependent network of actors: the production–consumption chain which includes cow–calf operators, feedlot operators, meat processors, retailers, and consumers, other influential actors such as veterinarians, nutritionists, pharmaceutical companies, professional and business groups associated with cattle (e.g. Texas Cattlemen’s Association), and regulatory and advisory bodies of governments (i.e. the Food and Drug Administration (FDA), State Licensing Boards that license veterinarians and the Centers for Disease Control (CDC). Our study focused on feedlot operators and feedlot veterinarians, but included the relationships that these two groups had with others in the feedlot network. We measured the frequency with which feedlot operators used antimicrobials and feedlot veterinarians’ recommended use of antimicrobials in acutely sick cattle, chronically sick cattle, at-risk cattle (young age) and high-risk cattle (exposure to stress). We asked respondents about their beliefs regarding the efficacy of antimicrobial use (i.e. improves health, improves well-being and makes cattle more profitable) in each of the four circumstances; attitudes towards using antimicrobials (importance in improving health, well-being and profitability) and perceived behavioural control (use of antimicrobials is an economic
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necessity) under each of the four circumstances. In order to capture subjective norms, we asked the degree to which of the actors described above expected the feedlot managers to use, or feedlot veterinarians to recommend the use of antimicrobials, in each of the four circumstances. We also asked how important it was to meet the expectations of each of these persons or institutions. We then asked whether there was a moral obligation to each of these types of individuals or institutions to use antimicrobials under each of the four circumstances and the importance of each of those obligations. Greater detail regarding our methodological procedures is provided in Dean and Scott (2005), Dean et al. (2011), McIntosh et al. (2009a,b), Jan et al. (2010, 2012). Perceptions of feedlot owners and managers The perceptions of feedlot owners and managers of the degree of agreement among key groups and individuals in the feedlot network that antimicrobials should be used to treat feedlot cattle varied significantly across circumstance of treatment. Perceived agreement was highest for acutely sick cattle, followed by high-risk cattle, then at-risk cattle and last chronically sick cattle. Those in the consumer segment (i.e. packers, retailers, consumers) of the network were less likely to be perceived as believing that antimicrobials were necessary under any of the four circumstances. With the exception of acutely sick cattle, the FDA was perceived as less in agreement about the need to use antimicrobials under the remaining circumstances. However, despite these differences, it is clear that these owners and managers perceived these expectations of many other members of the feedlot network to be an important consideration in their own decision-making. Only the expectations of other feedlot operators and pharmaceutical companies were considered of little importance. Somewhat fewer feedlot operators perceived they had a moral obligation to network members to use antimicrobials in their cattle. Several profound differences between perceived obligations and expectations occurred in the cases of other feedlot operators, feedlot nutritionists and pharmaceutical companies. The feedlot operators believed these three members of the network expected them to use antimicrobials, but far fewer believed they had an obligation to those members to do so. By contrast, the operators believed that beef consumers were less likely to expect them to use antimicrobials in each of the four circumstances, but greater percentages of operators tended to believe they had an obligation to consumers to do so. A majority of feedlot operators considered that they had a moral obligation to the cattle themselves to treat those cattle with antimicrobials, but the degree of this perceived obligation varied by circumstance.
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Perceptions of feedlot veterinarians Feedlot veterinarians reported varied perceptions of feedlot network members’ antimicrobial use expectation and their moral obligations to those members. Pharmaceutical companies were perceived by a higher percentage than other significant others to expect feedlot veterinarians to recommend the use of antimicrobials regardless of the circumstance. The next highest level of social pressure came from clients (i.e. feedlot operators and retained owners of cattle); however, there was considerable difference in these percentages by treatment circumstance. Perceived pressures from regulatory and professional organizations (norm setting bodies), while high in the case of acutely sick cattle, dropped off considerably for the remaining three circumstances. Perceived pressures from colleagues (i.e. other veterinarians and feedlot nutritionists) tended to be as high as those from clients. There was less strong agreement on perceived moral obligations to many of these members. Thus, for example, while the perception that colleagues, some members of the consumer sector, and pharmaceutical companies held strong expectations that the feedlot veterinarians should use these drugs, particularly in the cases of acutely sick and chronically sick animals, feedlot veterinarians were less likely to agree they had an obligation to these network members to prescribe these treatments. Subjective norms and moral obligations influenced both attitudes about using antimicrobials across the four treatment circumstances and the recommendations about their use under these circumstances. Perceptions that colleagues expected them to use antimicrobials in the case of acutely sick and high-risk cattle tended to lead to a more favourable attitude towards using antimicrobials under these circumstances. A second generalization concerns the expectations of clients: the greater the clients’ expectation that antimicrobials be used in chronically ill and at-risk cattle, the more favourable the veterinarians’ attitude that using antimicrobials under these circumstances was important. High client expectations regarding the use of antimicrobials in at-risk cattle were associated with more frequent recommendations for the use of antimicrobials under this circumstance. Perception of a moral obligation to the public also was associated with a negative attitude about recommending antimicrobials for at-risk cattle (Jan et al., 2010). Finally, when perceived expectations of regulatory bodies regarding the use of antimicrobials in high-risk cattle were low, feedlot veterinarians tended to recommend this use in high-risk cattle, but veterinarians’ sense of obligation to clients to recommend antimicrobials for such cattle increased the likelihood they made such recommendations. Perceptions of antimicrobial risk under a given circumstance tended to be less when there was a strong subjective
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norm and strong moral obligation to use antimicrobials in that circumstance. A limited number of feedlot network members played a role here. The most common set of network members whose expectations and obligations supported the use of antimicrobials were colleagues and clients (see Jan et al., 2012). Changing Behaviour The use of TPB in interventions A review of 45 studies that examined the success and failure of efforts to improve the use of pharmaceuticals found that the behaviour of governments, pharmaceutical companies, health professionals, retailers and consumers would need to be changed (Homedes and Ugalde, 2001). We believe a more important lesson we learned from our research on the feedlot industry is that salient others exhibit regular patterns of influence on those who use antimicrobials. This suggests an avenue for changing antimicrobial behaviours and one that might allow changes in a widespread basis. Efforts to change hospital physicians’ use of antimicrobials, while showing some success, are usually confined to single hospitals. To take advantage of the TPB in wider change efforts, Fishbein and Ajzen (2010) recommend formative research before embarking on an intensive effort to change behaviour among a large number of people. Meetings with key informants in groups would provide a means of informing an evaluation of the issues surrounding the misuse of antimicrobials, the risk of antimicrobial resistance and the means to alleviate both. Interviews of the informants would include an assessment of current behaviour as well as perceptions of the efficacy of their current behaviour, an indication of the people and groups that influence their current behaviour and who might object to changing their behaviour, and constraints that would make it difficult to change their behaviour. Once these salient others are identified, they would become the target of the first effort to reduce antimicrobial use. After persuading these individuals and groups, they would then become part of the vanguard to change the behaviour of antimicrobial users. One issue neglected in this literature is that of mistrust. In the United States, for example, mistrust exists among feedlot veterinarians of government antimicrobial recommendations (Dean et al., 2011), and the belief among cow– calf operators (McIntosh et al., 2009a,b) and dairy farmers that some federal agencies do not have their best interest in mind when making policy (McIntosh et al., 2010). The lesson here is that the choice of salient others for employment as change agents in the effort to reduce the use of antimicrobials must take trust issues into account. We can learn from what appears to be successful efforts in more widespread efforts to reduce antimicrobial 26
use that involve those who influence antimicrobial use. An NGO and several universities have introduced greater control over antimicrobial use in selected hospitals located in a number of provinces in Vietnam by identifying key individuals who serve as sources of subjective norm and involving them in the intervention (Wertheim et al., 2013). In Sweden, a national effort was begun by bringing together key actors in the health field including the Swedish Institute for Infectious Disease Control, Medical Products Agency, National Corporation of Swedish Pharmacies, the Swedish Board of Agriculture and others. Regional subgroups were also brought into the mix (M€ olstad et al., 2008). Perhaps one of the most notable conceptual frameworks for intervening in agricultural and health practices is the widely employed adoption of innovations theory. This framework has not been used in prior research to either understand or intervene in human health or veterinary antimicrobial practices. Work using this theory finds that changing attitudes and beliefs are necessary before behaviour can be changed. These changes require more than information provision; instead, this literature emphasizes the importance of contact with persuasive change agents. One aspect of this contact is the frequency of interaction (Monge et al., 2008). At the same time, the stronger the social connections with peers, the more difficult it is to change a given individual’s behaviour. However, the more people identify with innovators in their organization or community, the more likely they will embrace those innovations recommended by these influential members of the community. Acknowledgements Our research was funded by the United States Department of Agriculture-CRSEES (Grant #2002-51110-01959). Support for the presentation of this paper was provided by the Organization for Economic Cooperation and Development. Conflict of Interest The authors have no conflicts of interest to declare. References Ajzen, I., 1991: The theory of planned behavior. Organ Behav Hum Decis 50, 179–211. Allen, H. K., U. Y. Levine, T. Looft, M. Bandrick, and T. A. Casey, 2013: Treatment, promotion, commotion: antibiotic alternatives in food-producing animals. Trends Microbiol. 21, 114–119. Altiner, A., 2004: Acute cough: a qualitative analysis of how GPs manage the consultation when patients explicitly or
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