Abstract
Antibiotic-resistant pathogens increasingly threaten human health. Widespread application of antibiotics to animal populations raised for food, including chickens, cattle, and pigs, selects for resistance and contributes to the evolution of those pathogens. Despite a half century of research establishing the mechanisms and pathways by which antibiotic-resistant bacteria spread from food animals to people, scientists lack the appropriate data and models to estimate the public health burden of antibiotic-resistant human infections attributable to antibiotic use in food-animal production. Genomic technologies are enabling researchers to track the bidirectional transmissions of specific bacterial strains from livestock to people – and from people to livestock – that can amplify resistance traits. Concepts in ecology, which were developed to understand resource subsidies, metapopulations, and biological invasions, provide insight into the epidemiology of antibiotic resistance from genomic data. By applying ecological principles to highly resolved phylogenetic data, researchers can improve strategies for controlling antibiotic resistance.
Generated Summary
This review article explores the role of ecology in understanding the spread of antibiotic resistance, focusing on the food-animal production industry. The study integrates genomic data with ecological principles to examine the transmission dynamics of antibiotic-resistant bacteria. The researchers utilize concepts from ecology, such as resource subsidies, metapopulations, and species invasions, to analyze the spread of resistance. The research examines various pathways of transmission, including those related to food production, human health sectors, and environmental contamination. The primary method involves applying ecological principles to genomic data to identify and track the movement of specific bacterial strains between food animals and humans. The scope of the study encompasses the entire food production chain, from animal farms to human populations, and it aims to improve strategies for controlling antibiotic resistance. The study also highlights the challenges in quantifying the public health burden of antibiotic-resistant human infections linked to antibiotic use in food-animal production.
Key Findings & Statistics
- Globally, more than 57 million kilograms of antibiotics are used annually on food animals (Van Boeckel et al. 2015).
- Food-animal production accounts for an estimated 80% of annual antibiotic purchases in the US (FDA 2012, 2014).
- On the basis of retail poultry sales, we estimate that there were at least 15 billion potential foodborne exposures to food-animal bacteria in 2012 (assuming an average exposure portion of 2 pounds [0.9 kg] for the 34.9 billion pounds [15.8 billion kilograms] of poultry sold in the US in 2012; USDA 2014a).
- At least 89% of retail poultry harbors bacterial strains resistant to at least one type of antibiotic (We estimated the proportion of retail poultry with antibiotic-resistant bacteria by multiplying the reported prevalence of bacteria in meat by the proportion of bacteria isolated from meat that was resistant to at least one antibiotic).
- If only 1% of the potential exposure events involving antibiotic-resistant bacteria resulted in successful transmission to people, then there are roughly 130 million instances of resistant strains moving from poultry to people via food annually in the US.
- An estimated 94,000 US workers come into contact with birds in poultry houses annually (assuming an average of two full-time workers at each poultry operation; USDA 2014b).
- If each of those workers transmits novel human bacteria to their flocks 10 times each year, then the flux of bacteria from humans to food animals is approximately 1% of the flux of resistant strains in the opposite direction.
- In recent years, human infections caused by CC398 have accounted for up to 40% of MRSA infections in parts of Europe, where they are strongly correlated with a high frequency of human-livestock contact (Graveland et al. 2011).
Other Important Findings
- Antibiotic-resistant pathogens increasingly threaten human health, and the widespread application of antibiotics to animal populations selects for resistance and contributes to the evolution of those pathogens.
- Genomic technologies enable the tracking of bidirectional transmissions of specific bacterial strains from livestock to people – and from people to livestock – that can amplify resistance traits.
- Concepts in ecology, such as resource subsidies, metapopulations, and biological invasions, provide insight into the epidemiology of antibiotic resistance from genomic data.
- Food-animal production is an important source of new antibiotic-resistant bacterial pathogens and a control point for decreasing resistance in the human population.
- Advances in genomic technologies enable new insights into the ecological dynamics and evolutionary relationships of zoonotic pathogens.
- Through genetic sequencing, it is possible to identify and track the movements of specific strains between food animals and people.
- Applying basic ecological principles can help organize new knowledge to better monitor, understand, and manage the spread of antibiotic resistance.
- The food-animal production industry is a source of antibiotic-resistant bacteria that can infect people.
- Genomic data are elucidating, in unprecedented detail, the pathways by which antibiotic-resistant bacteria move between food animals and humans.
- The phenomenon of animal-to-human transmission was exemplified on a large scale in 2005–2006, when the Canadian government asked Québec broiler chicken hatcheries to stop injecting chicken eggs with ceftiofur.
- The problem of antibiotic resistance stems from excessive use of existing drugs, exacerbated by inadequate development of new drugs.
- Antibiotic use and bacterial transmission among patients, medical staff, and visitors drive the emergence of resistant pathogens in medical settings.
- Antibiotic use in outpatient populations may also contribute to resistance in the community, and in many countries, antibiotics can be purchased over the counter, leading to inappropriate use and resistance.
- An abundance of evidence details the spread of antibiotic resistance between food animals and people.
- Genomic technologies can also track the movements of specific resistance genes and reconstruct bacterial transmission events among networks of individual hosts, for example, to trace outbreaks of multidrug-resistant bacteria in clinical settings.
- The reconstructed transmission pathways of a deadly outbreak of multidrug-resistant K. pneumoniae implicated environmental reservoirs within the hospital and “silent” carriers in perpetuating the outbreak.
- The recent discovery of a novel mobile colistin-resistance gene is a clear example of local-scale antibiotic use rapidly leading to global-scale patterns of resistance.
Limitations Noted in the Document
- The document does not provide specific data and models to estimate the public health burden of antibiotic-resistant human infections attributable to antibiotic use in food-animal production.
- The review article primarily focuses on the application of ecological principles and genomic data without detailing the specific methodologies used in the genomic analyses.
- The scope is limited to the role of ecology, and it does not explore other factors influencing antibiotic resistance, such as socio-economic and policy aspects.
- The study acknowledges that despite the public health threat of accelerated antibiotic resistance, scientists are unable to quantify how antibiotic use in food-animal production shapes the expansion of resistant microbial strains in food and medical systems.
- The data and models to estimate the public health burden of antibiotic-resistant human infections attributable to antibiotic use in food-animal production are lacking.
- The study focuses on high-resolution phylogenomic data, but the specific genomic techniques and the depth of analysis are not detailed.
Conclusion
The study underscores the critical need to understand and manage the spread of antibiotic resistance, emphasizing the role of ecological principles and genomic technologies. The food-animal production sector is a major driver of resistance, and the study advocates for a multidisciplinary approach to tackle this issue. The review highlights that integrating ecological approaches with genomic data can strengthen drug resistance management and improve ecological theory. Applying ecological principles, such as resource subsidies, metapopulations, and species invasions, to high-resolution phylogenomics data can provide valuable insights into the spread of antibiotic resistance. Ecological models can improve understanding of resistance epidemiology, as genomic techniques generate powerful data describing the linkages between animal-borne bacteria and humans. Moreover, the use of genomics can trace bacterial transmission with high precision. The authors suggest that managing the spread of antibiotic resistance requires understanding the ecological interactions of resistant bacteria throughout the microbiosphere. The widespread use of antibiotics in food-animal production accelerates the evolution of resistant strains, an important source of new antibiotic-resistant bacterial pathogens in people. Genomic technologies are illuminating the evolutionary histories of some emergent resistant pathogens and their patterns of occurrence and transmission between food animals and humans, together revealing a dynamic and integrated ecosystem of antibiotic resistance.