Schistosoma haematobium effects on Plasmodium falciparum infection modified by soil-transmitted helminths in school-age children living in rural areas of Gabon

BackgroundMalaria burden remains high in the sub-Saharan region where helminths are prevalent and where children are often infected with both types of parasites. Although the effect of helminths on malaria infection is evident, the impact of these co-infections is not clearly elucidated yet and the scarce findings are conflicting. In this study, we investigated the effect of schistosomiasis, considering soil-transmitted helminths (STH), on prevalence and incidence of Plasmodium falciparum infection.MethodologyThis longitudinal survey was conducted in school-age children living in two rural communities in the vicinity of Lambaréné, Gabon. Thick blood smear light microscopy, urine filtration and the Kato-Katz technique were performed to detect malaria parasites, S. haematobium eggs and, STH eggs, respectively. P. falciparum carriage was assessed at inclusion, and incidence of malaria and time to the first malaria event were recorded in correlation with Schistosoma carriage status. Stratified multivariate analysis using generalized linear model was used to assess the risk of plasmodium infection considering interaction with STH, and survival analysis to assess time to malaria.Main findingsThe overall prevalence on subject enrolment was 30%, 23% and 9% for S. haematobium, P. falciparum infections and co-infection with both parasites, respectively. Our results showed that schistosomiasis in children tends to increase the risk of plasmodium infection but a combined effect with Trichuris trichiura or hookworm infection clearly increase the risk (aOR = 3.9 [95%CI: 1.7–9.2]). The incidence of malaria over time was 0.51[95%CI: 0.45–0.57] per person-year and was higher in the Schistosoma-infected group compared to the non-infected group (0.61 vs 0.43, p = 0.02), with a significant delay of time-to first-malaria event only in children aged from 6 to 10-years-old infected with Schistosoma haematobium.ConclusionsOur results suggest that STH enhance the risk for P. falciparum infection in schistosomiasis-positive children, and when infected, that schistosomiasis enhances susceptibility to developing malaria in young children but not in older children.

研究背景
疟疾负担在蠕虫流行的撒哈拉以南非洲地区依然居高不下，该区域儿童往往同时感染这两类寄生虫。尽管蠕虫对疟疾感染的影响已较为明确，但此类共感染的具体致病机制尚未被完全阐明，且现有有限研究结果存在分歧。本研究针对土源性蠕虫（soil-transmitted helminths, STH）合并血吸虫病的情况，探究其对恶性疟原虫（Plasmodium falciparum）感染的患病率与发病率的影响。

研究方法
本纵向队列研究在加蓬兰巴雷内周边两个乡村社区的学龄儿童中开展。研究分别采用厚血膜光镜检查、尿液过滤法及加藤-卡特（Kato-Katz）技术检测疟疾寄生虫、埃及血吸虫（Schistosoma haematobium）虫卵与土源性蠕虫虫卵。入组时即对恶性疟原虫携带情况进行评估，并记录疟疾发病率及首次疟疾发病时间，同时结合血吸虫携带状态进行关联分析。采用广义线性模型开展分层多因素分析，以评估土源性蠕虫与血吸虫共感染时恶性疟原虫感染的风险；并通过生存分析探究疟疾发病时间。

主要研究结果
研究对象入组时的总体感染率分别为：埃及血吸虫感染30%、恶性疟原虫感染23%，两类寄生虫共感染9%。本研究结果显示，儿童血吸虫感染可升高恶性疟原虫感染风险；而当合并鞭虫（Trichuris trichiura）或钩虫感染时，感染风险进一步显著升高（调整后比值比（adjusted odds ratio, aOR）=3.9，95%置信区间：1.7~9.2）。随访期间疟疾发病率为0.51例/人年（95%置信区间：0.45~0.57），血吸虫感染组发病率（0.61例/人年）高于未感染组（0.43例/人年，p=0.02）；仅在6~10岁感染埃及血吸虫的儿童中，首次疟疾发病时间存在显著延迟。

研究结论
本研究结果表明，在血吸虫感染阳性儿童中，土源性蠕虫会进一步升高恶性疟原虫感染风险；且对于年幼儿童而言，血吸虫感染会增加其疟疾易感性，但该效应在年长儿童中并不显著。