Host immunity, nutrition and coinfection alter longitudinal infection patterns of schistosomes in a free ranging African buffalo population.

Host immunity, nutrition and coinfection alter longitudinal infection patterns of schistosomes in a free ranging African buffalo population.
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DOI:
10.1371/journal.pntd.0006122
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发表时间:
2017-12
影响因子:
3.8
通讯作者:
Steinauer ML
Steinauer ML
中科院分区:
医学2区
文献类型:
--
作者:
Beechler BR;Jolles AE;Budischak SA;Corstjens PLAM;Ezenwa VO;Smith M;Spaan RS;van Dam GJ;Steinauer ML

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血吸虫是具有全球重要性的吸虫寄生虫,导致数百万人、牲畜和野生动物感染。大多数关于血吸虫病的研究都涉及人类受试者;因此,在没有干预的情况下调查寄生虫动态的纵向研究很少。因此,尽管对血吸虫病进行了数十年的研究,但我们对血吸虫病在自然宿主群体中生态学的理解主要集中在环境暴露和获得性免疫如何影响寄生虫的获得,而对宿主生理学、合并感染和在没有药物治疗的情况下清除的影响知之甚少。我们对自由放养的非洲水牛进行了为期 4 年的研究,以调查自然血吸虫动力学。我们询问(i)血吸虫感染的空间和时间模式是什么; (ii) 个体宿主体内的寄生虫负担如何随时间变化; (iii) 哪些宿主因素(免疫、生理、合并感染)和环境因素(季节、地点)解释了水牛血吸虫的获取和损失模式?血吸虫感染在水牛中很常见。微观地理结构解释了宿主之间寄生虫负担的一些变化,表明了传播热点。总体而言,寄生虫负担随着时间的推移而逐渐增加。然而,旱季血吸虫丰度的增加被雨季的损失部分抵消,一些宿主表现出感染完全清除。水牛血吸虫损失的变化与免疫和营养因素以及胃肠道蠕虫库珀虫的共同感染有关。我们的结果表明,血吸虫感染在自由生活的哺乳动物宿主群体中具有惊人的动态性,并指出宿主因素在驱动寄生虫清除变化中的作用,但不是由季节变化和空间栖息地利用驱动的寄生虫获取。我们的研究说明了纵向研究对于发现个体动物和种群寄生虫动态机制的力量。血吸虫是一种具有全球重要性的寄生虫,影响着全世界 2 亿多人,同时也感染牲畜和野生动物。尽管对人类血吸虫病进行了数十年的研究,但对于未经治疗的自然人群中感染模式的驱动因素却知之甚少。我们利用对非洲水牛的研究来了解地理、营养、免疫和合并感染如何驱动血吸虫的获得和损失。我们的研究最引人注目的结果是,个体体内的血吸虫负担随季节变化,一些宿主能够完全清除感染,而另一些宿主则无法做到这一点。水牛清除感​​染的能力受到免疫反应和与其他胃肠道寄生虫合并感染的影响,而宿主免疫和合并感染对于确定水牛是否被感染并不重要。在设计人类血吸虫病控制规划时应考虑这些结果。
Schistosomes are trematode parasites of global importance, causing infections in millions of people, livestock, and wildlife. Most studies on schistosomiasis, involve human subjects; as such, there is a paucity of longitudinal studies investigating parasite dynamics in the absence of intervention. As a consequence, despite decades of research on schistosomiasis, our understanding of its ecology in natural host populations is centered around how environmental exposure and acquired immunity influence acquisition of parasites, while very little is known about the influence of host physiology, coinfection and clearance in the absence of drug treatment. We used a 4-year study in free-ranging African buffalo to investigate natural schistosome dynamics. We asked (i) what are the spatial and temporal patterns of schistosome infections; (ii) how do parasite burdens vary over time within individual hosts; and (iii) what host factors (immunological, physiological, co-infection) and environmental factors (season, location) explain patterns of schistosome acquisition and loss in buffalo? Schistosome infections were common among buffalo. Microgeographic structure explained some variation in parasite burdens among hosts, indicating transmission hotspots. Overall, parasite burdens ratcheted up over time; however, gains in schistosome abundance in the dry season were partially offset by losses in the wet season, with some hosts demonstrating complete clearance of infection. Variation among buffalo in schistosome loss was associated with immunologic and nutritional factors, as well as co-infection by the gastrointestinal helminth Cooperia fuelleborni. Our results demonstrate that schistosome infections are surprisingly dynamic in a free-living mammalian host population, and point to a role for host factors in driving variation in parasite clearance, but not parasite acquisition which is driven by seasonal changes and spatial habitat utilization. Our study illustrates the power of longitudinal studies for discovering mechanisms underlying parasite dynamics in individual animals and populations. Schistosomes are a parasite of global importance, affecting over 200 million people worldwide, while also infecting livestock and wildlife. Despite decades of research on schistosomiasis in humans, little is known about what drives patterns of infection in untreated naturally occurring populations. We took advantage of a study in African buffalo to understand how geography, nutrition, immunity and coinfection drive schistosome acquisition and loss. The most striking outcome of our study was that schistosome burden varied seasonally within an individual, with some hosts able to completely clear infection, and others unable to do so. The ability of a buffalo to clear infection was affected by immune response and co-infection with other gastrointestinal parasites while host immunity and coinfection were not important in determining whether a buffalo became infected. These outcomes should be taken into consideration when designing control programs for human schistosomiasis.
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