Abstract

Schistosoma mansoni is widely distributed in sub-Saharan Africa with Biomphalaria pfeifferi being its most widespread and important snail intermediate host. Few studies have examined the compatibility of field-derived B. pfeifferi snails with S. mansoni miracidia derived from human hosts. We investigated compatibility (as defined by shedding of cercariae following exposure to miracidia) of two isolates of S. mansoni from school children from Asao (western Kenya) and Mwea (central Kenya) with B. pfeifferi collected directly from Asao stream or the Mwea rice fields. We exposed snails from both regions to four different doses of miracidia (1, 5, 10 and 25) from sympatric or allopatric S. mansoni, and maintained them in a shaded, screened out-of-doors rearing facility in Kisian, in western Kenya. Both snail survival and the number of snails that became infected were monitored weekly. This was done for 25 weeks post-exposure (PE). Those infected snails which survived beyond this period were monitored until they all died. Although overall survival of Mwea snails maintained in western Kenya was generally low, both sympatric and allopatric combinations of parasites and snails exhibited high compatibility (approximately 50% at a dose of one miracidium per snail), with an increase in infection rates as the miracidial dose was increased (P < 0.002). Schistosomes were no more compatible with sympatric than allopatric snails, nor were snails less compatible with sympatric than allopatric schistosomes. Snail mortality increased significantly with dose of miracidia (P < 0.05). Approximately 3% of Asao snails exposed to a low dose of sympatric miracidia (1 or 5) continued to shed cercariae for as long as 58 weeks post exposure. There were no significant local adaptation effects for either schistosomes or snails. Also, the existence of “super-survivor” snails is noteworthy for its implications for current control initiatives that mostly rely on mass drug administration (MDA). Long-term shedders could provide an ongoing source of cercariae to initiate human infections for many months, suggesting care is required in considering how human MDA treatments are timed. Future control programs should incorporate means to eliminate infected snails to complement chemotherapy interventions in controlling schistosomiasis.

Highlights

  • Schistosoma mansoni is widely distributed in sub-Saharan Africa with Biomphalaria pfeifferi being its most widespread and important snail intermediate host

  • Infection rates 4 and 5 weeks post exposure Because we used field snails with unknown history, we checked for the presence of pre-existing infections and any snail that shed cercariae before the pre-patent period was over was excluded from the study

  • Relative to the one miracidium dose infection rate (49.5%), the proportion of snails infected at higher doses was significantly higher: 5 miracidia (71.1%, Odds Ratio (OR) = 2.51 [95% Confidence Interval (CI) = 1.42 – 4.44]; p = 0.002); 10 miracidia (87.0%, OR = 6.84 [95% CI = 3.15 – 14.88]; p < 0.001) and 25 miracidia (96.7%, OR = 29.96 [95% CI = 8.85 – 101.37]; p < 0.001)

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Summary

Introduction

Schistosoma mansoni is widely distributed in sub-Saharan Africa with Biomphalaria pfeifferi being its most widespread and important snail intermediate host. In Kenya, B. pfeifferi is widely distributed, including in the tributaries feeding Lake Victoria, canals in major irrigation schemes in the Kano plains (Western Kenya) or in the Mwea irrigation scheme in central Kenya; it is found in small impoundments and both seasonal and perennial streams throughout the country, except in the tropical lowland belt along the coast of Kenya [9] Populations of this species and of the schistosome it transmits can be widely separated by regions of aridity in Kenya. B. pfeifferi is a strong self-fertilizer [17] and its movement is relatively limited owing to its restriction to aquatic habitats Based on these considerations, S. mansoni might be expected to exhibit strong local adaptation to B. pfeifferi, as manifested by shorter pre-patent periods, higher compatibility, or higher levels of cercariae production when exposed to sympatric as opposed to allopatric snails. These topics have not been addressed in Africa with a reciprocal cross design approach using field-derived snails and parasites not subjected to the biases resulting from prior laboratory propagation; this approach better represents the conditions in natural transmission sites

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