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Public Wellness Rep. 2012 Jan-Feb; 127(one): 4–22.
A Review of Antibiotic Use in Nutrient Animals: Perspective, Policy, and Potential
Timothy F. Landers
aThe Ohio Land University, Higher of Nursing, Columbus, OH
Bevin Cohen
bCenter for Interdisciplinary Research to Reduce Antibiotic Resistance, Columbia University School of Nursing, New York, NY
Thomas E. Wittum
cThe Ohio Land Academy, Department of Veterinary Preventive Medicine, Columbus, OH
Elaine L. Larson
bMiddle for Interdisciplinary Research to Reduce Antibody Resistance, Columbia University School of Nursing, New York, NY
SYNOPSIS
Antibiotic utilise plays a major role in the emerging public wellness crisis of antibody resistance. Although the majority of antibiotic utilize occurs in agricultural settings, relatively little attention has been paid to how antibiotic use in farm animals contributes to the overall trouble of antibiotic resistance. The aim of this review is to summarize literature on the role of antibiotics in the evolution of resistance and its risk to human health. Nosotros searched multiple databases to identify major lines of argument supporting the role of agricultural antibiotic use in the development of resistance and to summarize existing regulatory and policy documents. Several lines of reasoning back up the conclusion that agronomical antibiotics are associated with resistance, even so most public policy is based on skilful opinion and consensus. Finally, we propose strategies to address current gaps in knowledge.
Antibiotic resistance is a looming public health crisis. While once believed to be the province of hospitals and other health-care facilities, a host of community factors are now known to promote antibody resistance, and community-associated resistant strains take now been implicated as the cause of many hospital-caused infections.1 , 2 An inherent consequence of exposure to antibiotic compounds, antibody resistance arises as a result of natural choice.iii Due to normal genetic variation in bacterial populations, individual organisms may carry mutations that render antibiotics ineffective, conveying a survival advantage to the mutated strain. In the presence of antibiotics, advantageous mutations can also be transferred via plasmid exchange within the bacterial colony, resulting in proliferation of the resistance trait.iv The emergence of drug resistance has been observed following the introduction of each new grade of antibiotics, and the threat is compounded past a slow drug development pipeline and limited investment in the discovery and development of new antibody agents.five – 7
International, national, and local antibody stewardship campaigns have been developed to encourage prudent utilize of and limit unnecessary exposure to antibiotics, with the ultimate goal of preserving their effectiveness for serious and life-threatening infections.viii , 9 In do, even so, clinicians must balance the commonsensical goal of preserving the effectiveness of antibiotics with ethical obligations to patients who present with conditions that are unlikely to be harmed and may benefit from antibiotic use. There is as well considerable debate in veterinary medicine regarding use of antibiotics in animals raised for human consumption (food animals). The potential threat to human health resulting from inappropriate antibody use in food animals is meaning, every bit pathogenic-resistant organisms propagated in these livestock are poised to enter the nutrient supply and could be widely disseminated in food products.x – 15 Commensal bacteria constitute in livestock are frequently present in fresh meat products and may serve every bit reservoirs for resistant genes that could potentially be transferred to pathogenic organisms in humans.16 , 17
While antibiotic employ in food animals may correspond a risk to human health, the degree and relative impact take not been well characterized. Given divergent stakeholder interests and inadequate research to date, public policy discussions of this upshot are often contentious and highly polarized. The aim of this review is to examine the telescopic and nature of antibiotic utilise in food animals and summarize its potential touch on human being health. Nosotros also review key national and international policies on use of antibiotics in food animals. Finally, we propose future directions for research and monitoring of the agricultural employ of antibiotics.
METHODS
Nosotros searched three online databases of medical and scientific literature citations—the National Library of Medicine's MEDLINE®, the U.S. Section of Agriculture's National Agricultural Library Catalog (known equally AGRICOLA), and Thomson Reuter's Spider web of Scientific discipline—for English-language documents from 1994–2009 containing the keywords "antibiotic," "antibiotic resistance," "antimicrobial," "antimicrobial resistance," "agriculture," "livestock," "nutrient creature," "farm creature," "hog," "swine," "cattle," "moo-cow," "poultry," and "craven." Two authors reviewed the references and selected exemplary original research articles examining the association between antibiotic use in food animals and antibody-resistant bacteria in humans. We too performed searches of the ROAR Commensal Literature Database (function of the Reservoirs of Antibody Resistance [ROAR] projection, coordinated past the Alliance for Prudent Use of Antibiotics and funded by a grant from the National Institute of Allergy and Infectious Diseases) and the Globe Health Organization (WHO) website to identify research articles and policy documents pertaining to antibiotic utilise in food animals. An online search engine was used to locate policy statements published past governmental agencies.
RESULTS
In our review, we establish that the use of antibiotics in food animals is widespread, yet poorly characterized. Furthermore, in existing studies, neither the risks to human health nor the benefits to animal production take been well studied. We likewise found a lack of consistency in national and international policies.
In the following sections, we review the current literature on the nature and scope of antibody use in food animals, and on the epidemiologic links between use of antibiotics in food animals and resistance in humans. Nosotros and so provide an overview of the complex hazard assay framework required to understand this problem. Finally, nosotros review key national and international policy and regulatory recommendations.
Literature on the nature and telescopic of antibiotic utilize in food animals
The high population density of modernistic intensively managed livestock operations results in sharing of both commensal flora and pathogens, which tin can be conducive to rapid dissemination of infectious agents. Every bit a result, livestock in these environments commonly require ambitious infection direction strategies, which often include the utilise of antibiotic therapy.
Antibiotics are used in food animals to care for clinical disease, to prevent and control common disease events, and to heighten animal growth.18 The different applications of antibiotics in food animals accept been described as therapeutic use, prophylactic use, and subtherapeutic use. Antibiotics can be used to treat a unmarried animal with clinical illness or a large group of animals. However, these various uses are frequently indistinct; definitions of each type of use vary, and the approaches are often practical concurrently in livestock populations.19 For example, 16% of all lactating dairy cows in the U.Due south. receive antibiotic therapy for clinical mastitis each twelvemonth, but well-nigh all dairy cows receive intramammary infusions of prophylactic doses of antibiotics following each lactation to prevent and command future mastitis—primarily with penicillins, cephalosporins, or other beta-lactam drugs.20 Similarly, 15% of beefiness calves that enter feedlots receive antibiotics for the treatment of clinical respiratory disease, but therapeutic antibiotic doses are also administered to ten% of evidently good for you calves to mitigate anticipated outbreaks of respiratory affliction.21 40-2 percent of beef calves in feedlots are fed tylosin—a veterinarian macrolide drug—to forbid liver abscesses that negatively bear on growth, and approximately 88% of growing swine in the U.S. receive antibiotics in their feed for disease prevention and growth promotion purposes, commonly tetracyclines or tylosin.22 Most antibiotic apply in livestock requires a veterinary prescription, although individual treatment decisions are oft made and administered past lay subcontract workers in accordance with guidelines provided by a veterinarian.23 , 24
Despite the widespread adoption of antibiotic use in food animals, reliable data about the quantity and patterns of utilise (east.thou., dose and frequency) are not available.25 Quantifying antibody use in nutrient animals is challenging due to variations in written report objectives—investigators may measure only therapeutic uses, simply nontherapeutic uses, or a combination thereof, depending on their outcome of interest—and lack of clarity surrounding the definitions of therapeutic vs. nontherapeutic uses.26 Although limited, the bachelor data suggest that food animal production is responsible for a significant proportion of antibiotic use. In 1989, the Establish of Medicine estimated that approximately one-half of the 31.9 one thousand thousand pounds of antimicrobials consumed in the U.S. were for nontherapeutic use in animals.27 More than contempo estimates past the Union of Concerned Scientists, an advocacy group that supports reduced agronomical antimicrobial apply, suggest that 24.6 million pounds of antimicrobials are used for nontherapeutic purposes in chickens, cattle, and swine, compared with just 3.0 1000000 pounds used for human medicine. Calculations by the pharmaceutical industry-sponsored Beast Wellness Establish are more conservative, suggesting that of 17.eight meg pounds of antimicrobials used for animals, just 3.1 million pounds are used nontherapeutically.26 Twelve classes of antimicrobials—arsenicals, polypeptides, glycolipids, tetracyclines, elfamycins, macrolides, lincosamides, polyethers, beta-lactams, quinoxalines, streptogramins, and sulfonamides—may be used at different times in the life wheel of poultry, cattle, and swine.25 While some of the antimicrobials used in animals are non currently used to treat human disease, many, such as tetracyclines, penicillins, and sulfonamides, are also used in the handling of infections in humans.26 The WHO has developed criteria for the classification of antibiotics as "critically important," "highly important," and "important" based on their importance in the handling of human disease.28 , 29
However, other classes of antimicrobials used in agriculture have not led to concerns nearly dissemination of resistance in humans. For case, some of the most frequently used antibiotics in ruminants are ionophores, a distinctive class of antibiotics that change intestinal flora to achieve increased free energy and amino acid availability and improved nutrient utilization. Most beefiness calves in feedlots and some dairy heifers receive this drug routinely in their feed. Considering of their specific mode of action, ionophores have never been used in humans or therapeutically in animals. While some bacteria are intrinsically resistant to these drugs, there is currently no prove to suggest that ionophore resistance is transferable or that co-selection for resistance to other classes of antimicrobials occurs.30
Literature suggesting epidemiologic bear witness of an association betwixt antibody utilize in nutrient animals and antibiotic resistance in humans
Evidence that antibody utilise in food animals can result in antibody-resistant infections in humans has existed for several decades. Associations between antibody use in food animals and the prevalence of antibiotic-resistant bacteria isolated from those animals take been detected in observational studies too equally in randomized trials. Antibiotic-resistant leaner of animal origin have been observed in the environment surrounding livestock farming operations, on meat products bachelor for purchase in retail food stores, and every bit the cause of clinical infections and subclinical colonization in humans. Effigy 1 outlines a sampling of prevalence studies, outbreak investigations, ecological studies, case-control studies, and randomized trials whose results advise a potential relationship between antibody employ in nutrient animals and antibiotic resistance in humans.
Literature on the risks and benefits of antibiotic use in food animals
To sympathize how antibiotic employ in agriculture might impact the emergence of antibiotic resistance, it is essential to consider the complex interaction of elements in the physical surround (e.thousand., air, soil, and water) with social exchanges (eastward.grand., between animals within a herd, farmers and animals, and domestic poultry and migratory birds), in processing steps (eastward.g., farming activities, transportation, and storage), and in human use patterns (e.g., food preparation, meat consumption, and susceptibility to infection) (Figure ii). Antibiotic apply in animals tin have direct and indirect effects on man health: direct effects are those that tin can be causally linked to contact with antibody-resistant leaner from nutrient animals, and indirect effects are those that event from contact with resistant organisms that have been spread to diverse components of the ecosystem (due east.g., water and soil) as a result of antibody use in food animals (Figure 3).
Figure iii.
Examples of direct and indirect furnishings of antibody use in food animals on homo health
Given the multitude of factors that contribute to the pathways by which antibiotic apply in food animals could pose risks to human health, it is non surprising that a broad variety of methods has been used past researchers in various disciplines to approach the problem. In full general, risk assessment models in veterinary medicine emphasize brute wellness and treatment of diseases in animals, nutrient scientists' studies focus on the safety of human food supplies and the presence of antibiotic-resistant bacteria on food products, clinicians and epidemiologists investigate homo outbreaks caused by resistant infections for which animals are identified as primary sources, and molecular biologists examine relationships between resistant strains and the prevalence of specific resistance genes in human and creature bacteria. It is unlikely that any single study will be able to fully and accurately quantify the relationship between antibiotic utilise in food animals and infections in humans. At all-time, but crude estimates of the etiologic fraction or "impact fraction" tin can be fabricated for specific links in the ecologic chain.31
Several mathematical models have been proposed to quantify the overall take a chance associated with antibody use in animals, typically past estimating the prevalence of infection with a specific organism and its associated morbidity, and then multiplying by the proportion of these infections believed to be attributable to antibiotic utilise in food animals. While models of this nature have been rightfully criticized for failing to include indirect chance and, consequently, underestimating full potential risk, felicitous risk assessment strategies must besides consider the potential benefits of antibiotic use in food animals. Even though agricultural antibody apply carries a demonstrated hazard, at that place are likely benefits to the agronomical use of antibiotics as well. For example, reducing animal microbial load and shedding could lead to safer, more affordable food. However, many of the claims of do good take not been fully demonstrated in large-scale trials, and other trials take shown that the overall impact of the brusk-term benefit is poorly described.
The U.South. Food and Drug Assistants (FDA) requires manufacturers of new antibiotics to perform risk assessments to demonstrate that new drugs are prophylactic and constructive for utilize in animals and that "there is reasonable certainty of no harm to man health from the proposed use of the drug in food-producing animals."32 To evaluate potential human wellness consequences, the FDA employs a qualitative framework to classify as "low," "medium," or "high" the probabilities that bacteria in the brute population will acquire resistance, that humans will ingest the resistant bacteria in food products, and that ingesting the bacteria will consequence in adverse health outcomes (Figure 4). Drug blessing decisions are based on these risk estimations, along with information well-nigh proposed marketing status (e.chiliad., prescription, over-the-counter, or veterinary feed additives), extent of limitations on extra-characterization use, and intended use patterns (e.g., duration of use and assistants to individual animals vs. select groups of animals vs. flocks or herds of animals). "High-risk" drugs may be canonical if the FDA determines that human health gamble tin be mitigated. "Medium-chance" drugs could be approved if appropriate label restrictions are required.
In improver to the direct adventure assessment model, the FDA has developed guidance to determine the risk of antibiotic residues remaining on food products.32 This guidance recommends determining the touch of antibiotic residues on normal human being intestinal flora and the presence of resistance in these strains, and it provides guidelines for the calculation of Acceptable Daily Intake (ADI) for antibiotic residues that pose an appreciable risk to human health.
Guidelines and recommendations on the use of antibiotics in food animals
Given the importance of antibiotic resistance as a public health problem, many governments and professional societies have reviewed existing scientific evidence and adult recommendations to limit all types of antibiotic utilize, including use in nutrient animals. Depending on the nature and jurisdiction of each group, the findings may provide all-time practice guidelines for antibiotic utilize, prioritized agendas for research on the emergence of antibiotic resistance, recommendations for legislative action to regulate drug approval and surveillance processes, or enforceable laws on the manufacture, distribution, and prescription of antibiotics. Figure 5 summarizes recommendations directly related to utilise of antibiotics in food animal product for a sample of national and international guidance and policy documents.
DISCUSSION
Despite increasingly widespread recognition that antibiotic employ in food animals is an important contributor to human infections with antibody-resistant leaner (Effigy ane), at that place remains a significant need for scientific testify of the antibiotic use practices that create the greatest human wellness chance. Our goal with this article was non to advise specific solutions to the problem—in part because we believe there are no easy, specific answers—only rather to reiterate and summarize the importance of this issue and to advise some general policy directions that are indicated. Equally the importance of the problem and complication of the issues are increasingly appreciated by the public, policy dialogue, focused inquiry, and informed regulatory activity tin be undertaken. To facilitate farther research and timely action in response to emerging knowledge on this issue, we propose the following measures, which are in concert with WHO's global strategy for the containment of antimicrobial resistance, the U.Due south. Interagency Task Forcefulness on Antibiotic Resistance's public health action plan to combat antimicrobial resistance, and the Infectious Diseases Gild of America'south call to action.33 – 35
Develop a scientific agenda to recommend appropriate study designs and specific aims related to antimicrobial use in nutrient animals
A coordinated plan is needed to identify missing scientific data and to specify research designs and methods to address these needs. Although rigorous studies have been conducted in some disciplines, at that place has been a lack of serious and harmonized interdisciplinary effort to aggrandize on the corpus of knowledge, which should be used to inform public policy. To result in a useful and complete list of enquiry priorities, the agenda must include contributions past experts in bones sciences (eastward.g., genetics and microbiology), clinical sciences (e.thou., veterinary medicine and human medicine), public health (e.yard., epidemiology and nursing), social sciences (east.g., anthropology and sociology), economics (e.k., wellness and agriculture), and public policy (e.g., legislative and regulatory). Inquiry goals put forth in the agenda should be cogitating of methodological weaknesses identified in the existing literature. For example, definitions of antibody uses in food animals (e.thou., therapeutic and subtherapeutic) should be standardized and designed to reflect specific goals (eastward.yard., improving production or preventing economical loss from unrestrained affliction); the terms should be recognized across disciplines and used to classify the potential effects of different types of antibody use on human health. Another potential focus could be whether to approach enquiry on the development of resistance narrowly (i.due east., the causes and effects of specific drug-organism combinations) or broadly (i.e., the causes and effects of all antibiotics used in animals on microbial flora) to develop public health recommendations.
Fund agricultural enquiry that reflects the priorities identified by the inquiry agenda
Inadequate funding for agricultural research has likely contributed to the lack of sufficient scientific evidence necessary for informing public wellness decisions. For case, in the United States, it was recently estimated that the $101 billion in combined governmental and biomedical industry research funding represents about v% of national health expenditures each twelvemonth.36 In 2007, the U.S. Department of Agriculture provided more than $32 million in external research funding, representing less than ane i-thousandth of 1% of annual U.Due south. livestock and poultry sales.37 In dissimilarity, one single Constitute inside the National Institutes of Health—the National Found of Allergy and Infectious Diseases—directed more than than 20 times this amount to antimicrobial resistance research (more than $800 1000000) in the same yr.38 Given the scale of the antibiotic resistance problem and the demonstrated role of agricultural antibiotic uses in this impending public health crisis, adequate support for research specific to the function of agronomical uses of antibiotics in the evolution of resistance must be a national priority. Because that the U.S. funds lxx% to 80% of biomedical enquiry worldwide, the demand for appropriate levels of funding is especially acute.36
Urgently address barriers to the collection and analysis of antimicrobial use data
Circuitous political, economical, and social barriers limit the quality of data on the utilise of antibiotics in food animals. Currently, such data are provided on a voluntary basis, and the methods used to collect and compile reports are not standardized or fully transparent. While voluntary industry compliance with antibiotic reporting is commendable, the long-term effectiveness of nonbinding auditing programs is unproven. Effective surveillance of veterinary antimicrobial production and administration to food animals is a key first step toward ascertaining realistic estimates of the full scope of antibiotic utilise. These data will exist useless, notwithstanding, unless an agency with adequate analytic, regulatory, and enforcement capabilities exists. Because the commercial interests of antibiotic manufacturers must be appropriately counterbalanced with the public wellness urgency for development of new antibiotics, any agency tasked with monitoring antibiotic resistance must operate independently of commercial influences when releasing data to the public and drafting evidence-based regulations to safeguard human wellness.
Conclusion
Information technology is evident that now, the resources devoted to studying the role of antibiotic utilize in food animals—both in terms of funding and scientific inquiry—are insufficient. It is now disquisitional that agricultural use of antibiotics be recognized as i of the major contributors to the development of resistant organisms that result in life-threatening human infections and included as function of the strategy to control the mounting public wellness crunch of antibiotic resistance.
Footnotes
During portions of this project, Dr. Landers was supported past a grooming grant from the National Plant of Nursing Research, National Institutes of Health (Training in Interdisciplinary Research to Reduce Antimicrobial Resistance; T90 NR010824).
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