Grass Fed Beef Reduced Risk for Anibiotic Resistant Bacteria
Public Health Rep. 2012 Jan-Feb; 127(1): 4–22.
A Review of Antibiotic Utilise in Food Animals: Perspective, Policy, and Potential
Timothy F. Landers
aThe Ohio Land Academy, College of Nursing, Columbus, OH
Bevin Cohen
bCenter for Interdisciplinary Research to Reduce Antibiotic Resistance, Columbia University School of Nursing, New York, NY
Thomas Eastward. Wittum
cThe Ohio State Academy, Section of Veterinary Preventive Medicine, Columbus, OH
Elaine L. Larson
bCenter for Interdisciplinary Research to Reduce Antibiotic Resistance, Columbia University School of Nursing, New York, NY
SYNOPSIS
Antibiotic use plays a major role in the emerging public health crisis of antibiotic resistance. Although the majority of antibiotic use occurs in agricultural settings, relatively picayune attention has been paid to how antibiotic use in farm animals contributes to the overall problem of antibiotic resistance. The aim of this review is to summarize literature on the role of antibiotics in the development of resistance and its risk to human health. Nosotros searched multiple databases to place major lines of statement supporting the part of agricultural antibiotic apply in the development of resistance and to summarize existing regulatory and policy documents. Several lines of reasoning support the conclusion that agronomical antibiotics are associated with resistance, yet near public policy is based on expert opinion and consensus. Finally, we propose strategies to address current gaps in knowledge.
Antibiotic resistance is a looming public wellness crisis. While once believed to be the province of hospitals and other wellness-care facilities, a host of community factors are now known to promote antibody resistance, and community-associated resistant strains have at present been implicated as the crusade of many hospital-acquired infections.one , 2 An inherent consequence of exposure to antibiotic compounds, antibiotic resistance arises as a result of natural selection.3 Due to normal genetic variation in bacterial populations, individual organisms may carry mutations that return antibiotics ineffective, conveying a survival reward to the mutated strain. In the presence of antibiotics, advantageous mutations can also be transferred via plasmid substitution within the bacterial colony, resulting in proliferation of the resistance trait.iv The emergence of drug resistance has been observed post-obit the introduction of each new class of antibiotics, and the threat is compounded by a slow drug development pipeline and limited investment in the discovery and development of new antibiotic agents.v – 7
International, national, and local antibiotic stewardship campaigns have been developed to encourage prudent use of and limit unnecessary exposure to antibiotics, with the ultimate goal of preserving their effectiveness for serious and life-threatening infections.8 , 9 In practice, however, clinicians must rest the commonsensical goal of preserving the effectiveness of antibiotics with ethical obligations to patients who nowadays with conditions that are unlikely to be harmed and may benefit from antibody use. There is also considerable debate in veterinary medicine regarding employ of antibiotics in animals raised for human consumption (nutrient animals). The potential threat to man wellness resulting from inappropriate antibiotic utilize in food animals is significant, as pathogenic-resistant organisms propagated in these livestock are poised to enter the food supply and could be widely disseminated in food products.10 – fifteen Commensal bacteria constitute in livestock are oft present in fresh meat products and may serve as reservoirs for resistant genes that could potentially be transferred to pathogenic organisms in humans.sixteen , 17
While antibiotic use in food animals may represent a gamble to human health, the degree and relative impact have not been well characterized. Given divergent stakeholder interests and inadequate research to date, public policy discussions of this issue are ofttimes contentious and highly polarized. The aim of this review is to examine the telescopic and nature of antibody use in food animals and summarize its potential bear upon on human health. We also review key national and international policies on utilize of antibiotics in food animals. Finally, we propose future directions for research and monitoring of the agronomical use of antibiotics.
METHODS
We searched 3 online databases of medical and scientific literature citations—the National Library of Medicine's MEDLINE®, the U.S. Section of Agronomics's National Agronomical Library Catalog (known equally AGRICOLA), and Thomson Reuter's Web of Science—for English-language documents from 1994–2009 containing the keywords "antibiotic," "antibiotic resistance," "antimicrobial," "antimicrobial resistance," "agriculture," "livestock," "nutrient creature," "farm animal," "pig," "swine," "cattle," "cow," "poultry," and "craven." Two authors reviewed the references and selected exemplary original research articles examining the clan between antibody use in food animals and antibiotic-resistant leaner in humans. We also performed searches of the ROAR Commensal Literature Database (office of the Reservoirs of Antibiotic Resistance [ROAR] project, coordinated past the Alliance for Prudent Use of Antibiotics and funded by a grant from the National Establish of Allergy and Infectious Diseases) and the World Health Organization (WHO) website to place research articles and policy documents pertaining to antibiotic utilize in food animals. An online search engine was used to locate policy statements published past governmental agencies.
RESULTS
In our review, we institute that the use of antibiotics in food animals is widespread, even so poorly characterized. Furthermore, in existing studies, neither the risks to homo health nor the benefits to animal production have been well studied. Nosotros also found a lack of consistency in national and international policies.
In the following sections, we review the electric current literature on the nature and scope of antibiotic utilize in nutrient animals, and on the epidemiologic links between employ of antibiotics in food animals and resistance in humans. We then provide an overview of the complex risk analysis framework required to sympathize this problem. Finally, nosotros review fundamental national and international policy and regulatory recommendations.
Literature on the nature and scope of antibody employ in food animals
The high population density of modern intensively managed livestock operations results in sharing of both commensal flora and pathogens, which tin be conducive to rapid dissemination of infectious agents. As a effect, livestock in these environments usually require aggressive infection management strategies, which often include the employ of antibody therapy.
Antibiotics are used in food animals to treat clinical disease, to prevent and control mutual disease events, and to enhance beast growth.18 The dissimilar applications of antibiotics in food animals have been described every bit therapeutic use, prophylactic utilize, and subtherapeutic utilize. Antibiotics tin can exist used to treat a single animal with clinical disease or a large grouping of animals. Even so, these various uses are ofttimes indistinct; definitions of each type of use vary, and the approaches are often applied concurrently in livestock populations.19 For example, xvi% of all lactating dairy cows in the U.Due south. receive antibiotic therapy for clinical mastitis each year, but nearly all dairy cows receive intramammary infusions of prophylactic doses of antibiotics following each lactation to prevent and control 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 illness, just therapeutic antibiotic doses are also administered to 10% of plainly healthy calves to mitigate anticipated outbreaks of respiratory disease.21 Twoscore-two percent of beef calves in feedlots are fed tylosin—a veterinary macrolide drug—to preclude liver abscesses that negatively impact growth, and approximately 88% of growing swine in the U.S. receive antibiotics in their feed for affliction prevention and growth promotion purposes, ordinarily tetracyclines or tylosin.22 Most antibody use in livestock requires a veterinary prescription, although individual treatment decisions are often made and administered by lay farm workers in accordance with guidelines provided by a veterinarian.23 , 24
Despite the widespread adoption of antibiotic employ in nutrient animals, reliable data about the quantity and patterns of use (e.1000., dose and frequency) are not available.25 Quantifying antibody utilise in food animals is challenging due to variations in study objectives—investigators may measure only therapeutic uses, only 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 available data suggest that food creature production is responsible for a significant proportion of antibiotic use. In 1989, the Institute of Medicine estimated that approximately half of the 31.9 million pounds of antimicrobials consumed in the U.S. were for nontherapeutic use in animals.27 More recent estimates by the Union of Concerned Scientists, an advocacy grouping that supports reduced agricultural antimicrobial use, suggest that 24.vi one thousand thousand pounds of antimicrobials are used for nontherapeutic purposes in chickens, cattle, and swine, compared with merely 3.0 million pounds used for human medicine. Calculations by the pharmaceutical industry-sponsored Fauna Wellness Found are more conservative, suggesting that of 17.eight million pounds of antimicrobials used for animals, merely 3.ane 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 bike of poultry, cattle, and swine.25 While some of the antimicrobials used in animals are not currently used to care for homo disease, many, such equally tetracyclines, penicillins, and sulfonamides, are also used in the treatment of infections in humans.26 The WHO has developed criteria for the classification of antibiotics as "critically important," "highly important," and "of import" based on their importance in the handling of human affliction.28 , 29
Yet, other classes of antimicrobials used in agronomics have not led to concerns almost dissemination of resistance in humans. For example, some of the about oft used antibiotics in ruminants are ionophores, a distinctive class of antibiotics that alter intestinal flora to reach increased free energy and amino acid availability and improved nutrient utilization. Nigh beef calves in feedlots and some dairy heifers receive this drug routinely in their feed. Because of their specific mode of activeness, ionophores have never been used in humans or therapeutically in animals. While some bacteria are intrinsically resistant to these drugs, there is currently no evidence to advise 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 antibiotic apply in food animals and antibody resistance in humans
Testify that antibiotic use in nutrient animals can result in antibiotic-resistant infections in humans has existed for several decades. Associations between antibody apply in nutrient animals and the prevalence of antibiotic-resistant bacteria isolated from those animals have been detected in observational studies every bit well as in randomized trials. Antibiotic-resistant leaner of animate being origin have been observed in the surround surrounding livestock farming operations, on meat products available for buy in retail food stores, and as the crusade of clinical infections and subclinical colonization in humans. Figure ane outlines a sampling of prevalence studies, outbreak investigations, ecological studies, case-control studies, and randomized trials whose results suggest a potential human relationship between antibody use in nutrient animals and antibody resistance in humans.
Literature on the risks and benefits of antibiotic use in food animals
To understand how antibiotic utilize in agronomics might impact the emergence of antibiotic resistance, it is essential to consider the circuitous interaction of elements in the physical environs (due east.grand., air, soil, and water) with social exchanges (e.g., between animals within a herd, farmers and animals, and domestic poultry and migratory birds), in processing steps (east.g., farming activities, transportation, and storage), and in human use patterns (e.g., food preparation, meat consumption, and susceptibility to infection) (Figure 2). Antibiotic use in animals can take direct and indirect furnishings on human being health: direct effects are those that can be causally linked to contact with antibody-resistant bacteria from food animals, and indirect effects are those that result from contact with resistant organisms that have been spread to various components of the ecosystem (eastward.g., h2o and soil) as a effect of antibiotic use in food animals (Figure 3).
Effigy 3.
Examples of direct and indirect furnishings of antibody apply in food animals on human health
Given the multitude of factors that contribute to the pathways by which antibiotic use in food animals could pose risks to man wellness, it is not surprising that a broad variety of methods has been used by researchers in various disciplines to approach the trouble. In general, chance assessment models in veterinary medicine emphasize brute health and treatment of diseases in animals, food scientists' studies focus on the rubber of man nutrient supplies and the presence of antibiotic-resistant leaner on nutrient products, clinicians and epidemiologists investigate human outbreaks acquired by resistant infections for which animals are identified as principal sources, and molecular biologists examine relationships betwixt resistant strains and the prevalence of specific resistance genes in human and fauna bacteria. Information technology is unlikely that whatsoever single study volition be able to fully and accurately quantify the relationship between antibiotic utilize in food animals and infections in humans. At best, only crude estimates of the etiologic fraction or "touch fraction" tin can be made for specific links in the ecologic chain.31
Several mathematical models have been proposed to quantify the overall run a risk associated with antibiotic use in animals, typically by estimating the prevalence of infection with a specific organism and its associated morbidity, and and so 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 declining to include indirect adventure and, consequently, underestimating total potential take a chance, felicitous risk assessment strategies must also consider the potential benefits of antibiotic utilise in nutrient animals. Even though agricultural antibiotic use carries a demonstrated risk, there are likely benefits to the agricultural utilise of antibiotics as well. For instance, reducing fauna microbial load and shedding could lead to safer, more than affordable food. Nonetheless, many of the claims of benefit accept not been fully demonstrated in large-scale trials, and other trials have shown that the overall impact of the short-term benefit is poorly described.
The U.Due south. Food and Drug Assistants (FDA) requires manufacturers of new antibiotics to perform risk assessments to demonstrate that new drugs are safe and constructive for utilise in animals and that "at that place is reasonable certainty of no damage to homo health from the proposed use of the drug in food-producing animals."32 To evaluate potential human health consequences, the FDA employs a qualitative framework to classify equally "depression," "medium," or "high" the probabilities that bacteria in the animal population will larn resistance, that humans will ingest the resistant leaner in food products, and that ingesting the bacteria will outcome in adverse health outcomes (Effigy 4). Drug approval decisions are based on these take a chance estimations, forth with information nigh proposed marketing status (e.m., prescription, over-the-counter, or veterinary feed additives), extent of limitations on extra-label employ, and intended use patterns (e.g., elapsing of apply and administration to individual animals vs. select groups of animals vs. flocks or herds of animals). "Loftier-risk" drugs may be approved if the FDA determines that human health gamble can be mitigated. "Medium-hazard" drugs could be approved if appropriate label restrictions are required.
In improver to the directly risk cess model, the FDA has developed guidance to decide the risk of antibody residues remaining on food products.32 This guidance recommends determining the impact of antibody residues on normal human being abdominal flora and the presence of resistance in these strains, and it provides guidelines for the calculation of Acceptable Daily Intake (ADI) for antibody residues that pose an appreciable gamble to human health.
Guidelines and recommendations on the utilise of antibiotics in food animals
Given the importance of antibiotic resistance as a public health problem, many governments and professional person societies have reviewed existing scientific evidence and developed recommendations to limit all types of antibiotic use, including use in food animals. Depending on the nature and jurisdiction of each grouping, the findings may provide best do guidelines for antibiotic employ, prioritized agendas for research on the emergence of antibiotic resistance, recommendations for legislative activity to regulate drug approval and surveillance processes, or enforceable laws on the manufacture, distribution, and prescription of antibiotics. Effigy 5 summarizes recommendations straight related to apply of antibiotics in food animal production for a sample of national and international guidance and policy documents.
Word
Despite increasingly widespread recognition that antibody use in food animals is an of import contributor to human being infections with antibiotic-resistant bacteria (Figure ane), there remains a significant need for scientific evidence of the antibody employ practices that create the greatest human being health hazard. Our goal with this article was non to advise specific solutions to the trouble—in role considering nosotros believe there are no like shooting fish in a barrel, specific answers—but rather to reiterate and summarize the importance of this issue and to propose some full general policy directions that are indicated. As the importance of the problem and complexity of the issues are increasingly appreciated by the public, policy dialogue, focused enquiry, and informed regulatory activity can be undertaken. To facilitate farther inquiry and timely activity in response to emerging cognition on this issue, nosotros propose the following measures, which are in concert with WHO's global strategy for the containment of antimicrobial resistance, the U.S. Interagency Task Force on Antibiotic Resistance'due south public health action plan to combat antimicrobial resistance, and the Infectious Diseases Society of America's call to action.33 – 35
Develop a scientific agenda to recommend appropriate study designs and specific aims related to antimicrobial utilise in food animals
A coordinated plan is needed to place missing scientific data and to specify research designs and methods to address these needs. Although rigorous studies have been conducted in some disciplines, there has been a lack of serious and harmonized interdisciplinary effort to expand 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 basic sciences (e.m., genetics and microbiology), clinical sciences (due east.g., veterinarian medicine and human being medicine), public health (e.g., epidemiology and nursing), social sciences (eastward.one thousand., anthropology and sociology), economics (due east.one thousand., wellness and agronomics), and public policy (east.m., legislative and regulatory). Research 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.grand., therapeutic and subtherapeutic) should be standardized and designed to reflect specific goals (eastward.g., improving production or preventing economic loss from unrestrained disease); the terms should be recognized across disciplines and used to classify the potential effects of different types of antibiotic utilize on homo health. Another potential focus could be whether to arroyo enquiry on the development of resistance narrowly (i.e., 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 agronomical research 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 example, in the United States, it was recently estimated that the $101 billion in combined governmental and biomedical industry research funding represents well-nigh v% of national health expenditures each year.36 In 2007, the U.Southward. Department of Agronomics provided more than $32 1000000 in external inquiry funding, representing less than one 1-thousandth of 1% of annual U.S. livestock and poultry sales.37 In contrast, one single Plant within the National Institutes of Health—the National Found of Allergy and Infectious Diseases—directed more than 20 times this amount to antimicrobial resistance enquiry (more than $800 million) in the same year.38 Given the scale of the antibiotic resistance trouble and the demonstrated part of agricultural antibody uses in this impending public health crisis, acceptable support for research specific to the role of agronomical uses of antibiotics in the development of resistance must exist a national priority. Considering that the U.S. funds seventy% to 80% of biomedical inquiry worldwide, the need for appropriate levels of funding is especially acute.36
Urgently address barriers to the collection and analysis of antimicrobial use data
Circuitous political, economic, and social barriers limit the quality of data on the use of antibiotics in nutrient 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 laudable, 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 use. These information will be useless, however, unless an bureau with acceptable analytic, regulatory, and enforcement capabilities exists. Because the commercial interests of antibiotic manufacturers must be appropriately balanced with the public health urgency for evolution of new antibiotics, any agency tasked with monitoring antibiotic resistance must operate independently of commercial influences when releasing information to the public and drafting evidence-based regulations to safeguard human health.
CONCLUSION
Information technology is evident that at nowadays, the resources devoted to studying the role of antibody use in food animals—both in terms of funding and scientific inquiry—are insufficient. Information technology is at present critical that agricultural use of antibiotics exist recognized equally one of the major contributors to the development of resistant organisms that result in life-threatening human infections and included as part of the strategy to control the mounting public health crisis of antibiotic resistance.
Footnotes
During portions of this projection, Dr. Landers was supported by a training grant from the National Institute of Nursing Research, National Institutes of Health (Preparation in Interdisciplinary Research to Reduce Antimicrobial Resistance; T90 NR010824).
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