Consumer perceptions of antimicrobial use in animal husbandry: A scoping review

Antimicrobial use in animal agriculture is often perceived to play a role in the emerging threat of antimicrobial resistance. Increased consumer awareness of this issue places pressure on animal husbandry to adopt policies to reduce or eliminate antimicrobial use. We use a scoping review methodology to assess research on consumer perceptions of antimicrobial drugs in meat products in the United States, Canada, or the European Union. Evaluating peer-reviewed and grey literature, we included studies for assessment if they met these topical and geographic requirements, involved primary data collection, and were originally published in English. Our screening process identified 124 relevant studies. Three reviewers jointly developed a data charting form and independently charted the contents of the studies. Of the 105 studies that measured consumer concern, 77.1% found that consumers were concerned about antimicrobial use in meat production. A minority of studies (29.8% of all studies) queried why consumers hold these views. These studies found human health and animal welfare were the main reasons for concern. Antimicrobial resistance rarely registered as an explicit reason for concern. A smaller group of studies (23.3%) measured the personal characteristics of consumers that expressed concern about antimicrobials. Among these studies, the most common and consistent features of these consumers were gender, age, income, and education. Regarding the methodology used, studies tended to be dominated by either willingness-to-pay studies or Likert scale questionnaires (73.64% of all studies). We recommend consideration of qualitative research into consumer views on this topic, which may provide new perspectives that explain consumer decision-making and mentality that are lacking in the literature. In addition, more research into the difference between what consumers claim is of concern and their ultimate purchasing decisions would be especially valuable.

Enter a financial disclosure statement that   Yes -all data are fully available without restriction Antimicrobial use in animal agriculture is often perceived to play a role in the emerging threat of 54 antimicrobial resistance. Increased consumer awareness of this issue places pressure on animal 55 agriculture to adopt policies to reduce or eliminate antimicrobial use. We use a scoping review 56 methodology to assess research on consumer perceptions of antimicrobial drugs in meat products 57 in the United States, Canada, or the European Union. Evaluating peer reviewed and grey 58 literature, we included studies for assessment if they met these topical and geographic 59 requirements, involved primary data collection, and were originally published in English. Our 60 screening process identified 125 relevant studies. Three reviewers jointly developed a data 61 charting form and independently charted the contents of the studies. Of the 106 studies that 62 directly measured consumer concern, 77.4% found that consumers were concerned about 63 antimicrobial use in meat production. A minority of studies (29.6% of all studies) queried why 64 consumers hold these views. These studies found human health and animal welfare were the 65 main reasons for concern. Antimicrobial resistance rarely registered as an explicit reason for 66 concern. A smaller group of studies (23.2%) measured the personal characteristics of consumers 67 that expressed concerned about antimicrobials. The most common and consistent features of 68 these consumers were gender, age, income, and education. Overall, studies tended to be 69 dominated by either willingness-to-pay studies or likert scale questionnaires (73.6% of all 70 studies). The popularity of these methods may have contributed to the relative lack of studies that 71 characterized worried consumer demographics or reasons for their perspectives. We recommend 72 more qualitative research into consumer views on this topic, which may better elucidate 73 consumer decision-making and mentality. In addition, more research into the difference between 74 what consumers claim is of concern and their ultimate purchasing decisions would be especially  infections in humans (Innes, et al. 2020). To address public concern about antimicrobial 84 resistance, regulation has been promulgated to limit the use of certain drugs in animal agriculture   prevalence of "antibiotic free" labels on food, and emerging evidence that consumers will pay 122 more for meat with this label, mean that the consumers influence the governance of wider food 123 systems.        The extracted data were coded in anticipation of statistical analysis.

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When developing the protocol for this review, we limited our scope to studies about the U.S., 235 Canada, and the European Union (including the United Kingdom). We made this decision 236 because these countries have similar regulatory environments and close trade associations. We 237 also excluded texts written in non-English languages due a lack of reading proficiency among 238 authors. Therefore, some otherwise relevant Canadian and European studies were excluded.

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Between the title and abstract stage and full text screening stage of this review, we further 240 decided to exclude any texts that did not contain primary data collection (reflected in the 241 amended protocol). As a result, most of the originally included news articles and opinion pieces 242 became excluded. This decision was made in an effort to avoid bias as we could not ensure that 243 all non-academic texts about this topic were captured. Several news articles with extractable data 244 were included in the final analysis because they cited studies that were not otherwise captured 245 through database and grey literature searches. Although our search strategy was comprehensive 246 in its use of "antimicrobial" and the other associated terms listed above, extracted studies about 247 consumer concern all focused on antibiotic use as opposed to antimicrobial use; and the term 248 "antibiotic" was overwhelmingly used in these studies. For this reason, we use the more specific 249 term "antibiotics" for the results and discussion sections.

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To answer our proposed question we performed additional analysis on the studies that measured 251 consumer concern. For manuscripts which utilized Likert scale surveys, studies were classified 252 as finding that consumers were "concerned" if there was, on average, a higher than neutral level 253 of agreement with a statement that expressed concern about antibiotic use. Conversely, Likert 254 surveys that discovered a lower than neutral level of agreement for similar statements were 255 coded as finding that consumers were "not concerned." Willingness-to-pay studies that showed 256 consumers were willing to pay more for food with antibiotic-free traits (at a statistically 257 significant level) were labeled as studies that showed consumers are "concerned." Similarly, 258 willingness-to-pay studies that failed to find consumers would pay more for antibiotic-free food 259 were coded as having found consumers to be "not concerned." Some studies found that 260 consumers agreed with some concern-type statements while disagreeing with others; such studies 261 were labeled as "mixed concern." 262 Reasons for consumer concern were identified and each reason was given a unique identifier for   Studies often had multiple themes but those tallied in Table 2 were identified by reviewers as the 298 primary focus of each study. We found 18 distinct research themes among which antibiotic 299 perception data could be assessed. Few publications (12.8%) had a central focus on consumer 300 perceptions of antibiotics. More commonly, antibiotics were one of several consumer concerns 301 that were measured in a study. Of the studies with a main focus on antibiotic use, dairy (n = 6) 302 and beef (n = 4) were the most common, followed by pork (n = 2) (See Figure 2). Other core 303 topics for studies include production characteristics (23.2%), food safety (16%), and credence 304 claims/product attributes (10.4%). The production characteristics category includes any 305 publication that focuses on agricultural practices and other aspects of production, e.g.,. rearing  The publications under review were dominated by quantitative methods (82.4%; see Table 3).

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Qualitative methods-including interviews, focus groups, and document analysis-were used in 313 11.2% of the studies, and mixed quantitative/qualitative techniques were used in 6.4% of studies.   Research on consumer perceptions of antibiotic use in animal agriculture encompasses a wide 344 variety of subjects, and researchers utilized several measurement techniques, which challenges 345 the ability to summarize findings among studies. Nevertheless, most studies found that consumer 346 perceptions of antibiotic use exist along a spectrum. As described in the methods section, studies 347 that gauged a level of concern about antibiotic use were coded as finding that consumers were 348 "concerned about antibiotic use," "not concerned about antibiotic use," or had "mixed concern 349 about antibiotic use." A total of 84.8% of studies were able to be classified in this way. The  Among the literature investigated, 65.6% of studies concluded that consumers were concerned 354 with antibiotic use in food production, 8% were not concerned, and 11.2% showed mixed 355 concern (see Table 4). Figure 2 summarizes the findings of studies that gauged consumer 356 concern by tallying the number of studies by product type, method used and level of concern. 357 Likert scale surveys and willingness-to-pay studies dominate this research (73.6%). Consumers 358 tended to demonstrate concern regardless of product type. The only exception was beef, a 359 product in which consumer concern was mixed. next most commonly cited reason for concern was animal welfare, comprising 32.4% of studies 367 where perspectives were evaluated. It is notable that the evolutionary consequences of antibiotic 368 use-the emergence of antibiotic resistant bacteria in the world-is mentioned in only four 369 studies (10.8% of those that examined reasoning) and this concern was always in combination 370 with others. However, it is possible that concerns about antibiotic resistance were an 371 unmentioned or implied aspect of human health and safety concerns.  The most common descriptors across studies are gender (n=13), income (n=10), age (n=9), and 376 education (n=6). In general, female, older, highly educated, and high-income were the 377 demographic characteristics most consistently associated with consumer concern about 378 antibiotics (see Table 5). While the findings for each of these features were consistent, there was 379 at least one contradictory finding for each of these characteristics (e.g., one study found that men 380 are more concerned about antibiotic use while all the others found more concern among women 381 participants). Other personal identifiers included eating and shopping habits, level of trust, type  of consumers which found that two-thirds would vote hypothetically to restrict antibiotic use to 389 medical treatment only, and men were more likely to reject such a policy. Conversely, 390 individuals with higher incomes and those exposed to animal welfare media were more likely to  Research that investigates consumer concern about antibiotic use in animal agriculture 403 production is gaining traction. Two-thirds of studies that met our inclusion criteria were 404 published within the past ten years. This trend may relate to an increased public awareness and 405 popularization of antibiotic-free and organic products, but longitudinal analysis was not 406 conducted to confirm this theory.

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Overall, consumer perceptions of antibiotic use in animal agriculture is overwhelmingly 409 negative. Out of the studies that measured a degree of consumer concern (n=106), 77.4% found 410 that there is some level of concern. This is unsurprising, given the number of studies that show 411 consumer concern about potential practices that can be conceived as "contamination" (Brewer 412 and Rojas 2008). While we have not completed reviews outside the ambit of antibiotics, several 413 studies found that genetically modified foods (Wunderlich and Gatto 2015), pesticides, 414 (Boccaletti et al. 2000), and hormones (Lusk et al. 2003) are also of great concern to consumers.

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Most studies indirectly measured antibiotic concern through credence labels (e.g., "raised 417 without antibiotics" and "USDA Organic"), rearing practices, and food safety research in which 418 antibiotic use is one of several related practices that were studied. Thus, in many cases, we had to 419 extract the antibiotic-related findings from a study that was exploring a wider issue. This Consumers who expressed reasons for concern may be ill-informed about animal agriculture 433 production processes and antimicrobial uses. For example, consumers cited concerns that 434 administration of antimicrobials in animals may present health and safety hazards to consumers.

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Although without further investigation, we cannot say what exactly those concerns are, one 436 20 conjecture is that consumers believe that drug administration leads to antibiotic residues on or in 437 animal products that could contribute to consumer exposure to active antimicrobial agents System. This ensures the risk of exposure to antimicrobial residues in meat is low (NRC 1999).

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Similar regulatory efforts exist for non-meat animal products. It is possible that consumer's 444 concern for human health is, in fact, expressing an unstated concern around antimicrobial 445 resistance, however, none of the papers explored this potential conflation of these two terms.   Typically, when discordance is found between consumer perceptions and producer realities, it is 478 often accompanied by a call to "better educate" the consumer. We reject that "better education" 479 will lead to different results. Instead, we posit that consumers are not ignorant or irrational, but,   consumer concern. The most common variables found to be significant were gender, age, 507 education, and income. Collectively, these studies illustrate that older, highly educated, high 508 income females are most concerned about antibiotics. This picture of the "concerned consumer" 509 is not a surprising one, and indeed, seems to play into the stereotype that organic food often 510 serves as a luxury item for upper-class consumers. Nevertheless, these findings were not 511 consistent across studies, and other, less explored variables were implicated in these papers that 512 paint a potentially more complex picture of the concerned consumer.

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There were a host of other characteristics found to be of significance, but they were limited to 515 just a few studies, with little consistency in findings. Both "high trust" and "low trust" 516 individuals were found to be concerned along with "altruistic people" and those with 517 "individualizing moral foundations." Both "Protestants" and "atheists" were also found to be 518 concerned. These differences could be the result of different methods and/or the differences in 519 study populations that researchers utilized. Perhaps with more research more stable typologies 520 will emerge as we have seen with gender, income, education, and age. One small (three studies) but consistent finding is that a consumer with a high level of 523 knowledge and awareness tends to be concerned about antibiotics. Those with more knowledge 524 seem to be more concerned, but as we discussed above, the kind of knowledge one has could 525 greatly impact their stance on antibiotic use in animal industries. A high-knowledge consumer 526 does not necessarily know specific information about antibiotic regimes and their role in animal 527 production. Instead, "knowledge" often means a consumer understands the rules of thumb that 528 24 labels provide, or has a general understanding of how our food system works. We suggest here 529 that the relationship between "high knowledge" consumers and concern about antibiotics further 530 strengthens our contention to be wary of calls for further education of consumers. Such 531 education is already being provided through labels, but it does not necessarily translate into a 532 nuanced understanding of the role of antibiotic use in agriculture. Consumers have different 533 ways of evaluating agricultural production than producers, and the evidence so far suggests that 534 is unlikely to change. what 'social license' (e.g., freedom to operate) producers will maintain and what production 552 practices will be accepted in the future" (pg. 102).  and systematic screening process, we identified 125 texts that fulfilled our inclusion criteria. We 575 extracted relevant data from these texts for analysis, including the available data on consumer 576 concern. The majority of studies used quantitative methods, willingness-to-pay studies and 577 Likert surveys prominent among them, and were conducted by university researchers on U.S.

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populations. The studied products and themes varied.

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Not every text measured consumer concern, and fewer assessed reasons for concern or identified 581 characteristics of concerned people. Those that measured concern focused on antibiotic use, a 582 priority to reduce antimicrobial resistance. The different topics of interest and methods used 583 made synthesis of findings about consumer concern difficult. We developed a rubric to 584 categorize each study's population into "concern," "mixed concern," or "no concern" regarding 585 antibiotic use in animal agriculture. Most studies found some level of concern or mixed concern. 586 Concern for human and animal welfare were the most common reasons cited. The animal 587 welfare concern may derive from the consistent associations that consumers construe between 588 antimicrobial use and industrial agriculture practices that they perceive as having negative 589 consequences for the produced animals. It is notable that the emergence of resistant bacteria, 590 which is a consequence of antibiotic use, is only mentioned in four studies and never as a study's 591 explicit focus.

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Consumers may not understand the nuances of antimicrobial use in animal agriculture or 594 specifics about disease treatment, metaphylaxis, prophylaxis, and growth promotion/feed 595 efficiency uses. However, we do not recommend the typical tactic to educate consumers given 596 that consumers may already be well informed about some aspects of animal production. We do 597 27 propose that more research should focus on consumer concern about antimicrobial use rather 598 than appending a few questions about antimicrobial use to a study that has a broader focus. 599 Similarly, more in-depth qualitative research is also needed on this topic because the The dominance of university researchers and U.S. studies likely resulted from inclusion criteria 606 that required texts be in English and have primary data collection. We cannot say if a more 607 expansive criteria would lead to others results, but there were several seemingly relevant studies 608 that could be incorporated into a future review. We also recognize that our criteria was limiting 609 in the sense that non-academic types of literature (e.g. opinion pieces) were, with few exceptions,   Tally of studies by food studied, method used, and level of concern about antibiotics that the 788 study found. Excludes studies that did not explicitly gauge a level of concern about antibiotics and 789 studies that did not specify the product. Each dot is one study. 790 791 792