Using environmental DNA for the detection of Schistosoma mansoni: toward improved environmental surveillance of schistosomiasis

Abstract

Schistosomiasis is a waterborne, infectious disease with high morbidity and significant economic burdens affecting more than 250 million people globally. Disease control has, with notable success, for decades focused on drug treatment of infected human populations, but a recent paradigm shift now entails moving from control to elimination. To achieve this ambitious goal more sensitive diagnostic tools are needed to monitor progress towards transmission interruption in the environment, especially in low-intensity infection areas. We report on the development of an environmental DNA (eDNA) based tool to efficiently detect DNA traces of the parasite Schistosoma mansoni directly in the aquatic environment, where the non-human part of the parasite life cycle occurs. To our knowledge, this is the first report of the successful detection of S. mansoni in freshwater samples using aquatic eDNA. True eDNA was detected in as few as 10 cercariae/L water in laboratory experiments. The field applicability of the method was tested at known transmission sites in Kenya, where comparison of schistosome detection by conventional snail surveys (snail collection and cercariae shedding) with eDNA (water samples) showed 71% agreement between the methods. The eDNA method furthermore detected schistosome presence at two additional sites where snail shedding failed, demonstrating a higher sensitivity of eDNA sampling. We conclude that eDNA provides a promising new tool to significantly improve the environmental surveillance of S. mansoni. Given the proper method and guideline development, eDNA could become an essential future component of the schistosomiasis control tool box needed to achieve the goal of elimination.SignificanceAccurate detection and delineation of schistosomiasis transmission sites will be vital in on-going efforts to control and ultimately eliminate one of the most neglected tropical parasitic diseases affecting more than 250 million people worldwide. Conventional methods to detect parasites in the environment are cumbersome and have low sensitivity. We therefore developed an environmental DNA (eDNA) based method for schistosome detection in aquatic environments. Aquatic eDNA showed higher sensitivity than conventional snail surveys. We conclude that eDNA is a promising non-invasive and sensitive tool for environmental surveillance of schistosomiasis transmission. As the efforts and aims to control the disease are transitioning towards complete transmission interruption, this could be the robust and cost-effective surveillance tool needed in the “end game” of schistosomiasis.

Validation of an eDNA-based method for the detection of wildlife pathogens in water

“…from these organisms. Previous studies with invertebrates and parasites in mesocosms have reported more variable detection success, in accordance with our findings (but see Sengupta et al 2019 for 100 % detection efficiency of Schistosoma mansoni). Mauvisseau et al (2019) sampled water from mesocosms containing Freshwater Pearl Mussels (Margaritifera margaritifera) and were able to detect their DNA in all mesocosms with only one of two assays used, with evidence for inconsistent detection in biological and technical replicates.…”

“…Knowledge of pathogens in the environment is also important for human health and for the mitigation and prevention of zoonoses (Cunningham et al 2017). Furthermore, it eases planning of disease control, and even informs eradication measures, for example of Schistosoma mansoni in Kenya (Sengupta et al 2019). Therefore, comprehensive and regularly updated monitoring campaigns and surveillance for the creation of maps of parasite prevalence (Diarra et al 2019) are important to implement management measures effectively.…”

Comparative analysis of time-based and quadrat sampling in seasonal population dynamics of intermediate hosts of human schistosomes

“…Beyond the problem of compensatory feedbacks, the observation of density feedbacks warrants the evaluation of the effect of reductions in snail populations in terms of transmission potential to humans as subject to non-linearities in cercarial productivity with resource availability [35,36]. Novel approaches leveraging DNA-based tools such as PCR for the identification of snail and schistosome species [3], as well as environmental-DNA (eDNA) quantification techniques recently developed for schistosomes can play in important role in investigating these issues [64].…”

Applications of environmental DNA (eDNA) in ecology and conservation: opportunities, challenges and prospects

“…Biological invasions, pests, and diseases constitute one of the most serious threats for global biodiversity and cause adverse environmental, economic and public health impacts (Sengupta et al 2019;Tingley et al 2019;Walsh et al 2019). There is thus an urgent need to develop effective monitoring and management strategies to contain the spread and establishment of these harmful biological agents (Marshall & Stepien 2019;Orzechowski et al 2019).…”