Biosecurity and water, sanitation, and hygiene (WASH) interventions in animal agricultural settings for reducing infection burden, antibiotic use, and antibiotic resistance: a One Health systematic review

Publikation: Bidrag til tidsskriftReviewForskningfagfællebedømt

  • Chris E.Pinto Jimenez
  • Sarai Keestra
  • Pranav Tandon
  • Oliver Cumming
  • Amy J. Pickering
  • Moodley, Arshnee
  • Clare I.R. Chandler

Prevention and control of infections across the One Health spectrum is essential for improving antibiotic use and addressing the emergence and spread of antibiotic resistance. Evidence for how best to manage these risks in agricultural communities—45% of households globally—has not been systematically assembled. This systematic review identifies and summarises evidence from on-farm biosecurity and water, sanitation, and hygiene (WASH) interventions with the potential to directly or indirectly reduce infections and antibiotic resistance in animal agricultural settings. We searched 17 scientific databases (including Web of Science, PubMed, and regional databases) and grey literature from database inception to Dec 31, 2019 for articles that assessed biosecurity or WASH interventions measuring our outcomes of interest; namely, infection burden, microbial loads, antibiotic use, and antibiotic resistance in animals, humans, or the environment. Risk of bias was assessed with the Systematic Review Centre for Laboratory Animal Experimentation tool, Risk of Bias in Non-Randomized Studies of Interventions, and the Appraisal tool for Cross-Sectional Studies, although no studies were excluded as a result. Due to the heterogeneity of interventions found, we conducted a narrative synthesis. The protocol was pre-registered with PROSPERO (CRD42020162345). Of the 20 672 publications screened, 104 were included in this systematic review. 64 studies were conducted in high-income countries, 24 studies in upper-middle-income countries, 13 studies in lower-middle-income countries, two in low-income countries, and one included both upper-middle-income countries and lower-middle-income countries. 48 interventions focused on livestock (mainly pigs), 43 poultry (mainly chickens), one on livestock and poultry, and 12 on aquaculture farms. 68 of 104 interventions took place on intensive farms, 22 in experimental settings, and ten in smallholder or subsistence farms. Positive outcomes were reported for ten of 23 water studies, 17 of 35 hygiene studies, 15 of 24 sanitation studies, all three air-quality studies, and 11 of 17 other biosecurity-related interventions. In total, 18 of 26 studies reported reduced infection or diseases, 37 of 71 studies reported reduced microbial loads, four of five studies reported reduced antibiotic use, and seven of 20 studies reported reduced antibiotic resistance. Overall, risk of bias was high in 28 of 57 studies with positive interventions and 17 of 30 studies with negative or neutral interventions. Farm-management interventions successfully reduced antibiotic use by up to 57%. Manure-oriented interventions reduced antibiotic resistance genes or antibiotic-resistant bacteria in animal waste by up to 99%. This systematic review highlights the challenges of preventing and controlling infections and antimicrobial resistance, even in well resourced agricultural settings. Most of the evidence emerges from studies that focus on the farm itself, rather than targeting agricultural communities or the broader social, economic, and policy environment that could affect their outcomes. WASH and biosecurity interventions could complement each other when addressing antimicrobial resistance in the human, animal, and environmental interface.

OriginalsprogEngelsk
TidsskriftThe Lancet Planetary Health
Vol/bind7
Udgave nummer5
Sider (fra-til)e418-e434
ISSN2542-5196
DOI
StatusUdgivet - 2023
Eksternt udgivetJa

Bibliografisk note

Funding Information:
This project was commissioned and funded through the Improving Human Health project at the London School of Hygiene & Tropical Medicine (LSHTM), a collaboration with the International Livestock Research Institute, as part of the Agriculture for Nutritional and Health Research Programme of the Consultative Group on International Agricultural Research, a global consortium of donors and research centres for agricultural development (grant number CPR21–0B3–2017). The authors thank Jeff Waage, Jo Lines, and the professionals from the International Livestock Research Institute from Kenya and Viet Nam for their feedback during the development of the research protocol. We are grateful to Maria Bernardez for her logistic support through the conduction of this research, to Molly Pugh-Jones for her assistance in data extraction, to the librarian of the LSHTM who peer reviewed our search terms and strategy, and to the AnthroAMR group at LSHTM for their feedback and support during the development of this systematic review. We especially acknowledge the collaboration of Franck Berthe (World Bank), Claire Chase (World Bank), and Kate Medlicott (WHO; information provided in this publication reflects the views of the individual staff and not of WHO as an organisation). The study's funder had no role in study design, data collection, data analysis, data interpretation, or report writing. Collected data from articles will be available on request to the corresponding author. Full access to the protocol is available at PROSPERO CRD42020162345.

Funding Information:
This project was commissioned and funded through the Improving Human Health project at the London School of Hygiene & Tropical Medicine (LSHTM), a collaboration with the International Livestock Research Institute, as part of the Agriculture for Nutritional and Health Research Programme of the Consultative Group on International Agricultural Research, a global consortium of donors and research centres for agricultural development (grant number CPR21–0B3–2017). The authors thank Jeff Waage, Jo Lines, and the professionals from the International Livestock Research Institute from Kenya and Viet Nam for their feedback during the development of the research protocol. We are grateful to Maria Bernardez for her logistic support through the conduction of this research, to Molly Pugh-Jones for her assistance in data extraction, to the librarian of the LSHTM who peer reviewed our search terms and strategy, and to the AnthroAMR group at LSHTM for their feedback and support during the development of this systematic review. We especially acknowledge the collaboration of Franck Berthe (World Bank), Claire Chase (World Bank), and Kate Medlicott (WHO; information provided in this publication reflects the views of the individual staff and not of WHO as an organisation). The study's funder had no role in study design, data collection, data analysis, data interpretation, or report writing. Collected data from articles will be available on request to the corresponding author. Full access to the protocol is available at PROSPERO CRD42020162345.

Publisher Copyright:
© 2023 The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY-NC-ND 4.0 license.

ID: 367541553