Molluscicidal and antioxidant activities of silver nanoparticles on the multi-species of snail intermediate hosts of schistosomiasis

Abstract

Background Schistosomiasis, also known as bilharzia, is the second important parasitic disease after malaria. The present study aimed to evaluate the molluscicidal effects of silver nanoparticles on Biomphalaria alexandrina, B. glabrata, Oncomelania hupensis, snail intermediate hosts of intestinal schistosomes (i.e. Schistosoma mansoni and S. japonicum), along with the changes their antioxidant enzymes. Methods Silver (Ag) nano powder (Ag-NPs) was selected to test the molluscicidal effects on three species of freshwater snails. Exposure to Ag-NPs induced snail mortality and the LC50 and LC90 values of Ag-NPs for each snail species were calculated by probit analysis. Control snails were maintained under the same experimental conditions in dechlorinated water. Snail hemolymph was collected to measure the levels of antioxidant enzymes, such as total antioxidants capacity (TCA), glutathione (GSH), catalase (CAT) and nitric oxide (NO). In addition, the non-target organism, Daphnia magna, was exposed to a series of Ag-NPs concentration, similar to the group of experimental snails, in order to evaluate the LC50 and LC90 and compare these values to those obtained for the targeted snails. Results The results indicated that Ag-NPs had a molluscicidal effect on tested snails with the variation in lethal concentration. The LC50 values of Ag-NPs for B. alexandrina snails exposed for 24, 48, 72 hrs and 7 days were 7.91, 5.69, 3.83 and 1.91 parts per million (ppm), respectively. The LC50 values for B. glabrata snails exposed for 24, 48, 72 hrs and 7 days were 16.55, 10.44, 6.91 and 4.13 ppm, respectively, while the LC50 values for O. hupensis snails exposed for 24, 48, 72 hrs and 7 days were 46.5, 29.85, 24.49 and 9.62 ppm, respectively. Moreover, there is no mortality detected on D. magna when exposed to more than double and half concentration (50 ppm) of Ag-NPs during a continuous period of 3 hrs, whereas the LC90 value for B. alexandrina snails was 18 ppm. The molluscicidal effect of the synthesized Ag-NPs seems to be linked to a potential reduction of the antioxidant activity in the snail’s hemolymph. Conclusions Synthesized Ag-NPs have a clear molluscicidal effect against various snail intermediate hosts of intestinal schistosome parasites and could potentially serve as next generation molluscicides. Author summary Schistosomiasis is one of the major parasitic diseases with socio-economic and health importance in the developing world. Control of snail intermediate hosts of human schistosomes is an essential part of the program on fighting schistosomiasis. This study evaluated the effect of silver nanoparticles (Ag-NPs) on the snail intermediate hosts of Schistosoma mansoni, i.e. Biomphalaria alexandrina, B. glabrata, and the intermediate host of S. japonicum, i.e. Oncomelania hupensis. The results revealed that LC50 values of Ag-NPs against B. alexandrina, B. glabrata and O. hupensis were 7.91, 16.55 and 46.5 ppm, respectively, after 24 hrs of exposure. The results also revealed that O. hupensis snails tolerate better the toxic effect of Ag-NPs than B. alexandrina and B. glabrata snails. We also demonstrated that the freshwater crustacean Daphnia magna tolerate even higher concentration of Ag-NPs compared to the three species of snail intermediate hosts of schistosomes. Experiments on exposure of B. alexandrina to the sub-lethal concentration (LC25) of Ag-NPs obviously altered the antioxidant enzymes in the snail’s hemolymph. From the aforementioned results, Ag-NPs exhibited a promising molluscicidal activity against the snail intermediate hosts of human schistosomes, could eventually be used in the national schistosomiasis control program.