Understanding the relationship between environment, agriculture and health: An interdisciplinary challenge

In an editorial last year, Prof. Kathryn Monk explained the importance to environmental research of an interdisciplinary approach. She has asked me to share with readers some further, personal thoughts on this topic. I am an ecologist by training, but I spent much of my career managing agricultural research programmes in tropical regions. For the last ten years, I have held a position in a school of public health. This varied disciplinary experience has given me the opportunity to explore and understand interactions between environment, agriculture and human health. It is helpful to think of environment, agriculture, and health as points in a triangle, each having specific interactions with an adjacent sector, but also being influenced by more complex, three-way interactions. For environmental scientists, the interactions with agriculture are probably the most familiar. Extensive planting of crops like rice and oil palm has dramatic effects on biological diversity, water systems and their function, and soils. The importance of healthy environments to agriculture is repeatedly demonstrated. Thirty years ago, I had the opportunity to review the Indonesian national programme on integrated pest management in rice. Use of pesticides on rice was, paradoxically, causing severe outbreaks of pests like brown planthopper. The environmental processes behind this were actually quite complex. Soon after flooding, aquatic arthropods colonizing rice paddies provided a food source for generalist predators that moved in and built levels capable of suppressing subsequent pest invasion. Pesticides killed off this general predator community, while the pests, which lay their eggs inside plants, were less affected and their populations exploded in this predator-free environment (Settle et al. 1996).  Integrated Pest Management (IPM) on rice, pioneered in countries like Indonesia, was for many years a leading example of the value of integrating environmental and agricultural research.Environmental scientists will be less familiar, perhaps, with the interactions between agriculture and health, so here is a short introduction. Agricultural systems have two impacts on health, which for historical reasons have been treated as separate disciplines in the health sector. They produce food that contributes to nutrition, which is usually, but not always, a health benefit, and they produce distinct health risks, including diseases associated with food and food production, and toxins associated with agriculture, such as the pesticide just mentioned

Investigating the impacts of humans and dogs on the spatial and temporal activity of wildlife in urban woodlands

Humans can derive enormous benefit from the natural environment and the wildlife they see there, but increasing human use of natural environments may negatively impact wildlife, particularly in urban green spaces. Few studies have focused on the trade-offs between intensive human use and wildlife use of shared green spaces in urban areas. In this paper, we investigate the impacts of humans and their dogs on wildlife within an urban green space using camera trap data from Hampstead Heath, London. Spatial and temporal activity of common woodland bird and mammal species were compared between sites with low and high frequency of visits by humans and dogs. There was no significant difference in the spatial or temporal activity of wildlife species between sites with lower and higher visitation rates of humans and dogs, except with European hedgehogs (Erinaceus europaeus) which showed extended activity in the mornings and early evenings in sites with lower visitation rates. This may have implications for the survival and reproductive success of European hedgehogs. Our results suggest that adaptation to human and dog activity deserves greater study in urban green spaces, as would a broader approach to measuring possible anthropogenic effects

Quantifying the Relationship between Antibiotic Use in Food-Producing Animals and Antibiotic Resistance in Humans.

It is commonly asserted that agricultural production systems must use fewer antibiotics in food-producing animals in order to mitigate the global spread of antimicrobial resistance (AMR). In order to assess the cost-effectiveness of such interventions, especially given the potential trade-off with rural livelihoods, we must quantify more precisely the relationship between food-producing animal antimicrobial use and AMR in humans. Here, we outline and compare methods that can be used to estimate this relationship, calling on key literature in this area. Mechanistic mathematical models have the advantage of being rooted in epidemiological theory, but may struggle to capture relevant non-epidemiological covariates which have an uncertain relationship with human AMR. We advocate greater use of panel regression models which can incorporate these factors in a flexible way, capturing both shape and scale variation. We provide recommendations for future panel regression studies to follow in order to inform cost-effectiveness analyses of AMR containment interventions across the One Health spectrum, which will be key in the age of increasing AMR

A Meta-Analysis to Estimate Prevalence of Resistance to Tetracyclines and Third Generation Cephalosporins in Enterobacteriaceae Isolated from Food Crops.

Application of human and animal waste to fields and water sources and on-farm antimicrobial usage are documented contributors to the occurrence of antimicrobial resistance (AMR) in agricultural domains. This meta-analysis aimed to determine the prevalence of resistance to tetracycline (TET) and third generation cephalosporins (3GC) in Enterobacteriaceae isolated from food crops. TET was selected in view of its wide use in agriculture, whereas 3GC were selected because of the public health concerns of reported resistance to these critically important antibiotics in the environment. Forty-two studies from all six world regions published between 2010 and 2022 met the eligibility criteria. A random effects model estimated that 4.63% (95% CI: 2.57%, 7.18%; p-value: <0.0001) and 3.75% (95%CI: 2.13%, 5.74%; p-value: <0.0001) of surveyed food crops harboured Enterobacteriaceae resistant to TET and 3GC, respectively. No significant differences were observed between pre- and post-harvest stages of the value chain. 3GC resistance prevalence estimates in food crops were highest for the African region (6.59%; 95% CI: 2.41%, 12.40%; p-value: <0.0001) and lowest for Europe (1.84%; 95% CI: 0.00%, 6.02%; p-value: <0.0001). Considering the rare use of 3GC in agriculture, these results support its inclusion for AMR surveillance in food crops. Integrating food crops into One Health AMR surveillance using harmonized sampling methods could confirm trends highlighted here

Quantitatively evaluating the cross-sectoral and One Health impact of interventions: A scoping review and case study of antimicrobial resistance.

BACKGROUND: Current frameworks evaluating One Health (OH) interventions focus on intervention-design and -implementation. Cross-sectoral impact evaluations are needed to more effectively tackle OH-issues, such as antimicrobial resistance (AMR). We aimed to describe quantitative evaluation methods for interventions related to OH and cross-sectoral issues, to propose an explicit approach for evaluating such interventions, and to apply this approach to AMR. METHODS: A scoping review was performed using WebofScience, EconLit, PubMed and gray literature. Quantitative evaluations of interventions that had an impact across two or more of the human, animal and environment sectors were included. Information on the interventions, methods and outcome measures found was narratively summarised. The information from this review informed the construction of a new approach to OH-related intervention evaluation, which then was applied to the field of AMR. RESULTS: The review included 90 studies: 73 individual evaluations (from 72 papers) and 18 reviews, with a range of statistical modelling (n = 13 studies), mathematical modelling (n = 53) and index-creation/preference-ranking (n = 14) methods discussed. The literature highlighted the need to (I) establish stakeholder objectives, (II) establish quantifiable outcomes that feed into those objectives, (III) establish agents and compartments that affect these outcomes and (IV) select appropriate methods (described in this review) accordingly. Based on this, an evaluation model for AMR was conceptualised; a decision-tree of intervention options, a compartmental-microeconomic model across sectors and a general-equilibrium (macroeconomic) model are linked. The outcomes of this multi-level model (including cost-utility and Gross Domestic Product impact) can then feed into multi-criteria-decision analyses that weigh respective impact estimates alongside other chosen outcome estimates (for example equity or uncertainty). CONCLUSION: In conclusion, stakeholder objectives are key in establishing which evaluation methods (and associated outcome measures) should be used for OH-related interventions. The stated multi-level approach also allows for sub-systems to be modelled in succession, where resources are constrained

Governing the UN Sustainable Development Goals: Interactions, Infrastructures, and Institutions

Three of the eight Millennium Development Goals (MDGs) concerned health. There is only one health goal in 17 proposed Sustainable Development Goals (SDGs). Critiques of the MDGs included missed opportunities to realise positive interactions between goals. Here we report on an interdisciplinary analytical review of the SDG process, in which experts in different SDG areas identified potential interactions through a series of interdisciplinary workshops. This process generated a framework that reveals potential conflicts and synergies between goals, and how their interactions might be governed

Characteristics and Global Occurrence of Human Pathogens Harboring Antimicrobial Resistance in Food Crops: A Scoping Review

BackgroundThe role of the crop environment as a conduit for antimicrobial resistance (AMR) through soil, water, and plants has received less attention than other sectors. Food crops may provide a link between the agro-environmental reservoir of AMR and acquisition by humans, adding to existing food safety hazards associated with microbial contamination of food crops.ObjectivesThe objectives of this review were: (1) to use a systematic methodology to characterize AMR in food crop value chains globally, and (2) to identify knowledge gaps in understanding exposure risks to humans.MethodsFour bibliographic databases were searched using synonyms of AMR in food crop value chains. Following two-stage screening, phenotypic results were extracted and categorized into primary and secondary combinations of acquired resistance in microbes of concern based on established prioritization. Occurrence of these pathogen-AMR phenotype combinations were summarized by sample group, value chain stage, and world region. Sub-analyses on antimicrobial resistance genes (ARG) focused on extended-spectrum beta-lactamase and tetracycline resistance genes.ResultsScreening of 4,455 citations yielded 196 studies originating from 49 countries, predominantly in Asia (89 studies) and Africa (38). Observations of pathogen-phenotype combinations of interest were reported in a subset of 133 studies (68%). Primary combinations, which include resistance to antimicrobials of critical importance to human medicine varied from 3% (carbapenem resistance) to 13% (fluoroquinolones), whereas secondary combinations, which include resistance to antimicrobials also used in agriculture ranged from 14% (aminoglycoside resistance) to 20% (aminopenicillins). Salad crops, vegetables, and culinary herbs were the most sampled crops with almost twice as many studies testing post-harvest samples. Sub-analysis of ARG found similar patterns corresponding to phenotypic results.DiscussionThese results suggest that acquired AMR in opportunistic and obligate human pathogens is disseminated throughout food crop value chains in multiple world regions. However, few longitudinal studies exist and substantial heterogeneity in sampling methods currently limit quantification of exposure risks to consumers. This review highlights the need to include agriculturally-derived AMR in monitoring food safety risks from plant-based foods, and the challenges facing its surveillance.</jats:sec

Integrating agriculture and health research for development: LCIRAH as an interdisciplinary programme to address a global challenge.

The multiple burdens of persistent undernutrition and micronutrient deficiencies, along with the rapidly growing rates of overweight, obesity, and associated chronic diseases, are major challenges globally. The role of agriculture and the food system in meeting these challenges is very poorly understood. Achieving food security and addressing malnutrition in all its forms, a Sustainable Development Goal, requires an understanding of how changing food systems affect health outcomes and the development of new tools to design and evaluate interventions. An interinstitutional programme to address this interdisciplinary research challenge is described. Over the past seven years, the Leverhulme Centre for Integrative Research on Agriculture and Health has built a portfolio of successful and innovative research, trained a new cadre of interdisciplinary researchers in “Agri‐Health,” and built an international research community with a particular focus on strengthening research capacity in low‐ and middle‐income countries. The evolution of this programme is described, and key factors contributing to its success are discussed that may be of general value in designing interdisciplinary research programmes directed at supporting global development goals

Lessons from agriculture for the sustainable management of malaria vectors.

Willem Takken and colleagues argue for the expansion of insecticide monotherapy in malaria control by taking lessons from agriculture and including more sustainable integrated vector management strategies