Field-derived Schistosoma mansoni and Biomphalaria pfeifferi in Kenya: a compatible association characterized by lack of strong local adaptation, and presence of some snails able to persistently produce cercariae for over a year

Abstract

BackgroundSchistosoma 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.MethodsWe 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.ResultsAlthough 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.ConclusionsThere 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-014-0533-3) contains supplementary material, which is available to authorized users.

Transcriptional responses ofBiomphalaria pfeifferiandSchistosoma mansonifollowing exposure to niclosamide, with evidence for a synergistic effect on snails following exposure to both stressors

“…The snail mounts a considerable transcriptomic response to the presence of cercariae-producing sporocysts [23] and it is not hard to imagine that the energy demand placed on infected snails by continual production of cercariae takes an additional toll. The mortality rate of B. pfeifferi infected with S. mansoni is significantly higher than that noted for unexposed control snails [25]. The molluscicideexposed infected snails selected for sequencing were alive when sampled, but the transcriptional profiles suggested they were not thriving.…”

“…Biomphalaria pfeifferi used in Illumina sequencing were collected from Kasabong stream in Asembo Village, Nyanza Province, western Kenya (34.42037°E, 0.15869°S) and transferred to our field lab at The Centre for Global Health Research (CGHR) at Kisian, western Kenya. Snails sized 6-9mm in shell diameter were placed under natural light to check for shedding of digenetic trematode cercariae [25]. Snails shedding only S. mansoni cercariae and non-shedding controls were used in this study.…”

The Effect of Climate Change and the Snail-Schistosome Cycle in Transmission and Bio-Control of Schistosomiasis in Sub-Saharan Africa

“…There are many Biomphalaria species in places like Lake Victoria in Uganda where high transmission takes place [14]. In sub-Saharan Africa, studies have shown that the wide geographical distribution of S. mansoni is related to the presence of Biomphalaria snail species in the region [55,56].…”

“…This type of climatic factor may have future effects on the transmission of schistosomiasis in SSA because certain snail intermediate hosts such as Oncomelania which is not found in Africa, actually have the ability to withstand and survive dry environments for extended periods of time due to their operculum, which is capable of closing shell during periods of drought for as long as 2-4 months [13,77,78]. However, prolonged drought in some countries like Nigeria, Ethiopia and Zimbabwe, has resulted in a remarkable reduction in the prevalence of schistosomiasis due to a decrease in the reproductive and survival rate of snails responsible for transmission of the parasite in those areas, as well as the decrease in the transmission sites [56,[79][80][81].…”

“…Studies have shown that during aestivation, uninfected Bulinus snail species have the ability to withstand longer periods of drought than infected snails [56,57,82]. This implies that during drought, infected snails die off and this alters the transmission of schistosomiasis in drought-stricken areas [15,56,57,82]. Mutuku and co-workers [56] analyzed temporal changes on the spatial transmission pattern of S. haematobium worms on different age groups and their relationship to ponds infested with Bulinus snails in coastal Kenya.…”