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Are we overestimating risk of enteric pathogen spillover from wild birds to humans?
Biological Reviews ( IF 11.0 ) Pub Date : 2020-01-31 , DOI: 10.1111/brv.12581
Olivia M Smith 1 , William E Snyder 2 , Jeb P Owen 2
Affiliation  

Enteric illnesses remain the second largest source of communicable diseases worldwide, and wild birds are suspected sources for human infection. This has led to efforts to reduce pathogen spillover through deterrence of wildlife and removal of wildlife habitat, particularly within farming systems, which can compromise conservation efforts and the ecosystem services wild birds provide. Further, Salmonella spp. are a significant cause of avian mortality, leading to additional conservation concerns. Despite numerous studies of enteric bacteria in wild birds and policies to discourage birds from food systems, we lack a comprehensive understanding of wild bird involvement in transmission of enteric bacteria to humans. Here, we propose a framework for understanding spillover of enteric pathogens from wild birds to humans, which includes pathogen acquisition, reservoir competence and bacterial shedding, contact with people and food, and pathogen survival in the environment. We place the literature into this framework to identify important knowledge gaps. Second, we conduct a meta‐analysis of prevalence data for three human enteric pathogens, Campylobacter spp., E. coli, and Salmonella spp., in 431 North American breeding bird species. Our literature review revealed that only 3% of studies addressed the complete system of pathogen transmission. In our meta‐analysis, we found a Campylobacter spp. prevalence of 27% across wild birds, while prevalence estimates of pathogenic E. coli (20%) and Salmonella spp. (6.4%) were lower. There was significant bias in which bird species have been tested, with most studies focusing on a small number of taxa that are common near people (e.g. European starlings Sturnus vulgaris and rock pigeons Columba livia) or commonly in contact with human waste (e.g. gulls). No pathogen prevalence data were available for 65% of North American breeding bird species, including many commonly in contact with humans (e.g. black‐billed magpie Pica hudsonia and great blue heron Ardea herodias), and our metadata suggest that some under‐studied species, taxonomic groups, and guilds may represent equivalent or greater risk to human infection than heavily studied species. We conclude that current data do not provide sufficient information to determine the likelihood of enteric pathogen spillover from wild birds to humans and thus preclude management solutions. The primary focus in the literature on pathogen prevalence likely overestimates the probability of enteric pathogen spillover from wild birds to humans because a pathogen must survive long enough at an infectious dose and be a strain that is able to colonize humans to cause infection. We propose that future research should focus on the large number of under‐studied species commonly in contact with people and food production and demonstrate shedding of bacterial strains pathogenic to humans into the environment where people may contact them. Finally, studies assessing the duration and intensity of bacterial shedding and survival of bacteria in the environment in bird faeces will help provide crucial missing information necessary to calculate spillover probability. Addressing these essential knowledge gaps will support policy to reduce enteric pathogen spillover to humans and enhance bird conservation efforts that are currently undermined by unsupported fears of pathogen spillover from wild birds.

中文翻译:

我们是否高估了野生鸟类向人类传播肠道病原体的风险?

肠道疾病仍然是世界范围内第二大传染病源,野生鸟类被怀疑是人类感染的来源。这导致人们努力通过威慑野生动物和清除野生动物栖息地来减少病原体外溢,特别是在农业系统内,这可能会损害保护工作和野生鸟类提供的生态系统服务。此外,沙门氏菌属。是鸟类死亡的一个重要原因,导致更多的保护问题。尽管对野生鸟类中的肠道细菌进行了大量研究,并制定了阻止鸟类进入食物系统的政策,但我们仍缺乏对野生鸟类参与将肠道细菌传播给人类的全面了解。在这里,我们提出了一个框架来理解肠道病原体从野鸟到人类的溢出,包括病原体获取、宿主能力和细菌脱落、与人和食物的接触以及病原体在环境中的存活。我们将文献放入这个框架中,以确定重要的知识差距。其次,我们对 431 种北美繁殖鸟类中三种人类肠道病原体弯曲杆菌属、大肠杆菌和沙门氏菌属的流行数据进行了荟萃分析。我们的文献综述显示,只有 3% 的研究涉及病原体传播的完整系统。在我们的荟萃分析中,我们发现了一种弯曲杆菌属。野生鸟类的流行率为 27%,而致病性大肠杆菌 (20%) 和沙门氏菌的流行率估计。(6.4%) 较低。测试的鸟类物种存在显着偏差,大多数研究都集中在人类附近常见的少数类群(例如欧洲八哥 Sturnus vulgaris 和岩鸽 Columba livia)或通常与人类排泄物接触的分类群(例如海鸥)。没有 65% 的北美繁殖鸟类的病原体流行数据,包括许多经常与人类接触的物种(例如黑嘴喜鹊 Pica hudsonia 和大蓝鹭 Ardea herodias),我们的元数据表明,一些研究不足的物种,与大量研究的物种相比,分类群和行会可能代表同等或更大的人类感染风险。我们得出的结论是,目前的数据没有提供足够的信息来确定肠道病原体从野生鸟类溢出到人类的可能性,因此排除了管理解决方案。文献中对病原体流行的主要关注可能高估了肠道病原体从野生鸟类溢出到人类的可能性,因为病原体必须在感染剂量下存活足够长的时间,并且是一种能够定植人类以引起感染的菌株。我们建议未来的研究应该集中在大量与人类和食品生产接触的未充分研究的物种上,并证明对人类致病的细菌菌株会排放到人们可能接触它们的环境中。最后,评估鸟类粪便中细菌脱落的持续时间和强度以及环境中细菌存活的研究将有助于提供计算溢出概率所需的关键缺失信息。
更新日期:2020-01-31
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