Agrochemicals increase risk of human schistosomiasis by supporting higher densities of intermediate hosts

Abstract

Schistosomiasis is a snail-borne parasitic disease that ranks among the most important water-based diseases of humans in developing countries. Increased prevalence and spread of human schistosomiasis to non-endemic areas has been consistently linked with water resource management related to agricultural expansion. However, the role of agrochemical pollution in human schistosome transmission remains unexplored, despite strong evidence of agrochemicals increasing snail-borne diseases of wildlife and a projected 2- to 5-fold increase in global agrochemical use by 2050. Using a field mesocosm experiment, we show that environmentally relevant concentrations of fertilizer, a herbicide, and an insecticide, individually and as mixtures, increase densities of schistosome-infected snails by increasing the algae snails eat and decreasing densities of snail predators. Epidemiological models indicate that these agrochemical effects can increase transmission of schistosomes. Identifying agricultural practices or agrochemicals that minimize disease risk will be critical to meeting growing food demands while improving human wellbeing.

Emerging human infectious diseases and the links to global food production

“…Although this sort of integrative thinking has been historically rare because agriculture and public health have been perceived as disparate disciplines, it is beginning to slowly penetrate these distinct fields of study. For example, several agrochemicals seem to increase the risk of human schistosomiasis and agriculturally derived zoonotic pathogens, and thus researchers are actively attempting to identify agrochemicals that might 'kill two birds with one stone' , reducing crop pests and thus increasing food production while not increasing or even decreasing human pathogens [137][138][139] . Similarly, researchers are beginning to consider the introduction of prawns as biological control agents of schistosomiasis, which could simultaneously decrease disease and increase nutrition -because restored prawns can be fished, harvested and consumed without compromising their diseasecontrolling benefits 61,140 .…”

Effect of agrochemical exposure on Schistosoma mansoni cercariae survival and activity

“…Schistosoma miracidia and cercariae might be sensitive to environmental contaminants given their occurrence in freshwater environments during transition between intermediate and definitive hosts (34). Surprisingly, previous studies have not reported significant lethal effects of pesticide exposure on either life stage of Schistosoma (32). In contrast, similar trematode species found in North American snails are known to be sensitive as cercariae to the commonly applied herbicides atrazine (35, 36) and glyphosate (37), as well as organophosphate, pyrethroid, and neonicotinoid insecticides (38).…”

“…Given that the concentrations of insecticides reported in samples from developing regions all fall below concentrations used in the current study (46, 47, 52–54), it is unlikely that Schistosoma cercariae suffer direct mortality from pesticide exposure. Previous research has also reported no influence of chlorpyrifos (organophosphate) or atrazine (triazine) exposure at environmentally relevant concentrations on S. mansoni survival over 12 hr (32). While the indirect effects of agrochemicals have been shown to potentially propagate schistosomiasis (32), the results of this study suggest that, due to substantial cercarial tolerance, direct toxicity of pesticides is not an apparent counteractive or mitigating factor for disease risk.…”

“…Cercariae and miracidia are short-lived organisms, generally only having enough reserves to live for approximately 24 hours (31). In an outdoor mesocosm experiment, populations of intermediate snail hosts were shown to increase following bottom-up and top-down indirect effects caused by herbicide and insecticide exposure, respectively (32). Thus, human infection risk was predicted to increase following pesticide contamination of aquatic systems.…”

“…Interestingly, the method of assigning cercarial survival differed among these studies. Survival can be assessed with 1) general swimming or climbing movement (36), 2) movement following stimuli (35, 38–40), or 3) Trypan blue staining (32). Complicating the use of either activity or dyes to examine effects of pesticide exposure is that many insecticides cause paralysis; thus, paralyzed cercariae cannot respond to stimuli but can excrete Trypan blue, which is absorbed by dead cells and excreted by living cells (41, 42).…”