Association of infrastructure and operations with antibiotic resistance potential in the dairy environment in India

Abstract

The dairy industry in developing countries is often associated with inappropriate use of antibiotics and the subsequent contamination of the environment with co-selectors of antibiotic resistance. However, the specific factors in dairy farm environments that influence antibiotic resistance levels and the subsequent exposure risks to farm workers are unknown. We examined the link between the infrastructure and operations of the dairy farm and the antibiotic resistance potential in India, which is the highest producer and consumer of dairy products globally. We sampled sixteen dairy farms in the Dehradun district, India, that varied in their herd size, infrastructure, and operational features during winter, summer, and monsoon. We collected samples of dung, manure, wastewater, manure-amended, and control soil from these farms. We quantified six antibiotic resistance genes (ARGs) (sul1, sul2, parC, mcr5, ermF, and tetW), an integron integrase gene cassette (intI1), and 16S rRNA gene copies as an indicator for total bacterial count. We observed that the infrastructure and the operations of the dairy farms were significantly associated with antibiotic resistance potential in the dairy environment. For example, with increased ventilation and exposure to external weather, the levels of sul2 (x͂=10^−1.63) and parC (x͂=10^−4.24) in manure increased. When farmers administered antibiotics without veterinary consultation, the relative levels of intI1 (x͂=10^−2.36), sul2 (x͂=10^−1.58), and tetW (x͂=10^−3.04) in manure were lower than the cases where professional advice was sought. Small-scale farms had lower relative ARG levels than medium- and large-scale farms, except for mcr5 (x͂=10^−3.98) in wastewater. In different sample types, the relative ARG levels trended as manure-amended soil (x͂=10^−2.34) > wastewater (x͂=10^−2.90)> manure (x͂=10^−3.39)> dung (x͂=10^−2.54). ARGs correlated with the marker for horizontal gene transfer, intI1, which exacerbates overall antibiotic resistance levels. Exposure assessment showed that the agriculture farm workers working in manure-amended agriculture farms are exposed to higher antibiotic resistance potential than dairy farm workers, who manually handle dung. Our study showed that the link between the dairy infrastructure (ventilation and floor type) and operations (scale of operation and veterinary consultation) and the antibiotic resistance potential in the dairy farm environment was statistically significant. This knowledge paves the way for designing interventions that can minimize the antibiotic resistance potential on dairy farms and in affected environments and thus reduce the public health burden of antibiotic-resistant infections in the dairy industry and dairy workers in India.