Restricting the use of antibiotics in food-producing animals and its associations with antibiotic resistance in food-producing animals and human beings: a systematic review and meta-analysis

Abstract

SummaryBackgroundAntibiotic use in human medicine, veterinary medicine, and agriculture has been linked to the rise of antibiotic resistance globally. We did a systematic review and meta-analysis to summarise the effect that interventions to reduce antibiotic use in food-producing animals have on the presence of antibiotic-resistant bacteria in animals and in humans.MethodsOn July 14, 2016, we searched electronic databases (Agricola, AGRIS, BIOSIS Previews, CAB Abstracts, MEDLINE, Embase, Global Index Medicus, ProQuest Dissertations, Science Citation Index) and the grey literature. The search was updated on Jan 27, 2017. Inclusion criteria were original studies that reported on interventions to reduce antibiotic use in food-producing animals and compared presence of antibiotic-resistant bacteria between intervention and comparator groups in animals or in human beings. We extracted data from included studies and did meta-analyses using random effects models. The main outcome assessed was the risk difference in the proportion of antibiotic-resistant bacteria.FindingsA total of 181 studies met inclusion criteria. Of these, 179 (99%) described antibiotic resistance outcomes in animals, and 81 (45%) of these studies were included in the meta-analysis. 21 studies described antibiotic resistance outcomes in humans, and 13 (62%) of these studies were included in the meta-analysis. The pooled absolute risk reduction of the prevalence of antibiotic resistance in animals with interventions that restricted antibiotic use commonly ranged between 10 and 15% (total range 0–39), depending on the antibiotic class, sample type, and bacteria under assessment. Similarly, in the human studies, the pooled prevalence of antibiotic resistance reported was 24% lower in the intervention groups compared with control groups, with a stronger association seen for humans with direct contact with food-producing animals.InterpretationInterventions that restrict antibiotic use in food-producing animals are associated with a reduction in the presence of antibiotic-resistant bacteria in these animals. A smaller body of evidence suggests a similar association in the studied human populations, particularly those with direct exposure to food-producing animals. The implications for the general human population are less clear, given the low number of studies. The overall findings have directly informed the development of WHO guidelines on the use of antibiotics in food-producing animals.FundingWorld Health Organization.

End non-essential use of antimicrobials in livestock

“…This work reinforced the established understanding that reducing antimicrobial use in agriculture is associated with reductions in antimicrobial resistance in food producing animals, as well as the idea that, at minimum, the benefit appears to extend to farmers and those in direct contact with food producing animals 9. The authors clearly acknowledge the limitations in these reviews, and although there are few studies showing a direct effect on human health of antimicrobial use in animals, the overall body of evidence provided enough evidence to support WHO’s recommendations.…”

“…The new guidelines were shaped by published reviews commissioned by the WHO Advisory Group on Integrated Surveillance of AMR 89. This work reinforced the established understanding that reducing antimicrobial use in agriculture is associated with reductions in antimicrobial resistance in food producing animals, as well as the idea that, at minimum, the benefit appears to extend to farmers and those in direct contact with food producing animals 9.…”

What are the effective solutions to control the dissemination of antibiotic resistance in the environment? A systematic review protocol

“…1). Moreover, according to [30], the decrease of the antibiotic resistance in animal matrices has already be linked to the reduction of antibiotic use in livestock.…”

“…Several management options can be proposed to reduce the antibiotic use and to treat the organic wastes before their release in the natural compartments [13,29]. Recently, a systematic review showed that the restriction of antibiotic use in livestock can be associated with a decrease of antibiotic resistance in the animals and in farmers in contact with them [30].…”

Critically important antibiotics: criteria and approaches for measuring and reducing their use in food animal agriculture

“…In recent years, there have been increasing concerns that the widespread use of antibiotics in food animal agriculture could lead to the emergence, spread, and propagation of bacteria that are antibiotic resistant. If these bacteria spread to human populations through food products, direct contact with animals, or via the environment, the resulting infections could be more difficult to treat if antibiotics of the same class or different classes of antimicrobials are used in both animals and in human medicine, leading to increased burdens of morbidity and mortality, and increased costs for care . To help navigate the complex set of medications involved and to ensure that the most essential drugs are used judiciously in both human and veterinary medicine, public and animal health organizations have created competing lists of “critically important antimicrobials” (CIAs) that rank these compounds according to their importance in human and veterinary medicine, respectively…”