Department of Global Health and Development, Faculty of Public Health and Policy, London School of Hygiene & Tropical Medicine, London, UK; Antimicrobial Resistance Centre, London School of Hygiene & Tropical Medicine, London, UK; Agriculture and Infectious Disease Group, London School of Hygiene & Tropical Medicine, London, UK.
Department of Global Health and Development, Faculty of Public Health and Policy, London School of Hygiene & Tropical Medicine, London, UK; Agriculture and Infectious Disease Group, London School of Hygiene & Tropical Medicine, London, UK.
Lancet Planet Health. 2023 May;7(5):e418-e434. doi: 10.1016/S2542-5196(23)00049-9.
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.
预防和控制整个大健康领域的感染对于改善抗生素的使用和应对抗生素耐药性的出现和传播至关重要。关于如何在农业社区(占全球家庭的 45%)中最好地管理这些风险的证据尚未得到系统收集。本系统评价确定并总结了农场生物安全和水、环境卫生(WASH)干预措施的证据,这些措施有可能直接或间接地减少动物农业环境中的感染和抗生素耐药性。我们从数据库成立到 2019 年 12 月 31 日,在 17 个科学数据库(包括 Web of Science、PubMed 和区域数据库)和灰色文献中搜索了评估生物安全或 WASH 干预措施的文章,这些措施测量了我们感兴趣的结果;即感染负担、微生物负荷、动物、人类或环境中的抗生素使用和抗生素耐药性。使用系统评价中心实验室动物实验工具、非随机干预措施的偏倚风险评估和横断面研究评估工具评估了偏倚风险,但没有因偏倚风险而排除任何研究。由于发现的干预措施存在异质性,我们进行了叙述性综合。该方案已在 PROSPERO(CRD42020162345)上预先注册。在筛选出的 20672 篇论文中,有 104 篇被纳入本系统评价。64 项研究在高收入国家进行,24 项在中上收入国家进行,13 项在中下收入国家进行,2 项在低收入国家进行,1 项同时包括中上收入国家和中下收入国家。48 项干预措施集中在畜牧业(主要是猪),43 项集中在家禽(主要是鸡),1 项集中在畜牧业和家禽,12 项集中在水产养殖农场。104 项干预措施中的 68 项发生在密集型农场,22 项发生在实验环境中,10 项发生在小农或自给型农场。23 项水研究中有 10 项、35 项卫生研究中有 17 项、24 项环境卫生研究中有 15 项、所有三项空气质量研究中有三项以及 17 项其他与生物安全相关的干预措施中有 11 项报告了积极结果。总共,26 项研究中有 18 项报告了感染或疾病减少,71 项研究中有 37 项报告了微生物负荷减少,5 项研究中有 4 项报告了抗生素使用减少,20 项研究中有 7 项报告了抗生素耐药性减少。总体而言,57 项阳性干预措施中有 28 项和 30 项阴性或中性干预措施中有 17 项存在高偏倚风险。农场管理干预措施成功地减少了高达 57%的抗生素使用。以粪便为导向的干预措施减少了动物粪便中抗生素抗性基因或抗生素抗性细菌的数量,最高可达 99%。本系统评价强调了预防和控制感染和抗生素耐药性的挑战,即使在资源丰富的农业环境中也是如此。大多数证据来自于侧重于农场本身的研究,而不是针对农业社区或更广泛的社会、经济和政策环境,这些环境可能会影响他们的结果。在人类、动物和环境界面中应对抗生素耐药性时,WASH 和生物安全干预措施可以相辅相成。