https://orcid.org/0000-0001-7561-4873
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Figures
Abstract
Background
Granular mapping conducted in Kakamega and Bungoma counties of western Kenya provided strong evidence of intestinal schistosomiasis among school-age children in this area. However, it was unclear whether the observed infections were due to active transmission. To address this gap, a follow-up malacology survey was conducted to determine the presence of snail vectors and ascertain active transmission.
Methods
Nineteen Wards with ≥10% prevalence of Schistosoma mansoni were selected from Kakamega and Bungoma counties. From these Wards, 42 primary schools with the highest prevalence of S. mansoni were used to identify nearby water bodies with human-water contact activities for sampling snail vectors. Live snails were sampled by experienced collectors using a handheld dip-net scoop in standardized sampling frames for ~30 minutes at each water body. Snails were counted and identified to species-level based on shell morphology. Site locations sampled for snails were mapped using a geographical information system, and the type of water body recorded. All Biomphalaria and Bulinus snails were transported to the laboratory where they were screened for cercariae. Cercariae were identified to basic taxonomic groups using standard identification keys. The relative and mean abundance and prevalence of Schistosoma sp. infection in snails was determined.
Results
Out of 4,245 snails collected, 3,341 (78.7%, 95% CI: 77.5-79.9) were putatively identified as Biomphalaria pfeifferi, 88 (2.1%, 95% CI: 1.7-2.5) as Bulinus globosus, 664 (15.6%, 95% CI: 14.6-16.7) as Lymnaea natalensis and 152 (3.6%) as other species. B. pfeifferi were found in 36 out of the 42 primary school regions (85.7%), with the highest number (605 snails) recorded at Indangalasia in Lusheya-Lubinu Ward. A total of 87 (2.6%, 95% CI: 2.07-3.14) B. pfeifferi shed Schistosoma sp. cercariae. The mean abundance of B. pfeifferi was similar between streams (16 ± 35) and swamps/marshes (20 ± 31) (P = 0.356), but was higher compared to rivers (4 ± 10) (P = 0.005).
Conclusions
The high abundance of B. pfeifferi coupled with the observation of field-caught snails shedding cercariae confirms autochthonous schistosomiasis transmission corroborating the reported human infections in Kakamega and Bungoma counties. Incorporation of focal snail control to complement chemotherapy will accelerate interruption of transmission in these areas.
Author summary
Recent mapping in Kakamega and Bungoma Counties of western Kenya showed many cases of intestinal schistosomiasis (bilharzia). However, it was unclear whether the transmission of the disease was taking place on site. To investigate this, a snail survey was conducted, because certain freshwater snails carry and release the parasite that infects people. The survey sampled water bodies near 42 primary school regions in 19 Wards where infection levels were high. Snails were collected, identified by species, and tested in the laboratory to see if they were releasing infectious parasite larvae. Out of 4,245 snails collected, most (about 79%) were Biomphalaria pfeifferi, the main carrier of Schistosoma mansoni. These snails were found at 36 out of 42 primary school regions sampled for snails, especially in streams and swamps. Importantly, 2.6% of them were actively shedding parasite larvae, meaning they were capable of infecting people. These findings confirm that schistosomiasis transmission is ongoing in these counties, not just a result of past exposure or imported cases. This study suggests that, in addition to treating people with medication, targeted snail control in high-risk areas could help stop transmission faster.
Citation: Odiere MR, Kepha S, Kihara J, Juma C, Kioko D, Wakesho F, et al. (2026) Biomphalaria pfeifferi infected with Schistosoma spp. in Kakamega and Bungoma counties, western Kenya confirms autochthonous transmission of intestinal schistosomiasis. PLoS Negl Trop Dis 20(5): e0014276. https://doi.org/10.1371/journal.pntd.0014276
Editor: Jennifer A. Downs, Weill Cornell Medical College, UNITED STATES OF AMERICA
Received: September 28, 2025; Accepted: April 16, 2026; Published: May 4, 2026
Copyright: © 2026 Odiere et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All data supporting the findings of this study are uploaded as supplementary file.
Funding: This work was supported by The END Fund through the Deworming Innovation Fund (DIF), Award Number: KEN-004-AMRK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Schistosomiasis (SCH) is a snail-borne, inflammatory disease that infects an estimated 240 million people globally [1], with over 90% of the global burden borne by sub-Saharan Africa [2]. In Kenya, approximately 9 million people are estimated to be infected [3] and approximately 17.4 million are at risk of schistosomiasis [4]. Both Schistosoma mansoni which is responsible for intestinal schistosomiasis and S. haematobium, which causes urogenital schistosomiasis are present in Kenya [3]. Considerable progress has been made in bringing schistosomiasis under control and with the aim of proceeding to elimination [5,6], with chemotherapy as the cornerstone of the intervention strategies. Although chemotherapy has considerably reduced prevalence and intensity of infection [7], it is acknowledged that mass drug administration (MDA) alone is insufficient to reduce transmission. The existence of persistent hotspots of schistosomiasis transmission [8,9] underscore the challenge of spatial heterogeneity in MDA success which is likely multifactorial, with snail distribution, abundance and genetics predicted to play a large role [10–12].
Snail control remains critical for breaking the cycle of SCH transmission. The risk of reinfection remains if infected snails continue releasing parasites into water sources, even with regular MDA campaigns. Indeed, WHO recommends the implementation of targeted snail control where feasible [9], with resolution WHA70.16 on the Global Vector Control Response (GVCR) 2017–2030 [13] calling on Member States to develop or adapt national vector control strategies and operational plans to align with the GVCR strategy. Implementation of effective snail control requires among other things an understanding of the occurrence of the responsible snails and ecological factors sustaining their distribution. However, the delineation of when and where transmission actually occurs is made difficult due to the longevity of schistosome infections in the human host coupled with the high vagility of humans [14], focal nature of infections and diverse species of reservoir hosts. Delimiting the species of snail present is important in informing not only the transmission dynamics (where human-infective cercariae are actually being produced and thus likely sites of active transmission), but also in the design of effective snail control interventions. For instance, surface molluscicides may not be effective against Biomphalaria choanomphala, a deep-water snail [15]. In addition, it helps in the timely identification/increased vigilance of invasive snail species that have the potential to influence transmission dynamics and/or exert negative economic and environmental impacts – as is the case of Orientogalba viridis in Malawi [16] and Pomacea canaliculata in Kenya [17].
Three main endemic regions for schistosomiasis are recognized in Kenya; the Coastal region (where the main spp. is S. haematobium), parts of Central and Lower Eastern region (both S. haematobium and S. mansoni) and the Lake Victoria basin area (where the main spp. is S. mansoni) (3). The distribution of the disease is determined, to a large extent, by the presence or absence of Biomphalaria and Bulinus snails, which act as the obligatory intermediate hosts for S. mansoni and S. haematobium, respectively. Several species of the shallow-water Biomphalaria snails are involved in transmission across sub-Saharan Africa [15]. Three species of Biomphalaria are involved in transmission in Kenya: 1) Biomphalaria pfeifferi, whose distribution includes tributaries feeding Lake Victoria, and in small impoundments and both seasonal and perennial streams throughout the country, except in the tropical lowland belt along the coast; 2) Biomphalaria sudanica, mainly found along the shores of Lake Victoria and Lake Jipe and their surrounding swamps; and 3) Biomphalaria choanomphala, a deeper water inhabitant of Lake Victoria [15,18]. In western Kenya, most malacological surveys have been confined around Lake Victoria [14, 19- 24] with a dearth of surveys in counties of western Kenya that do not border the lake, including Kakamega and Bungoma.
The prevalence of intestinal schistosomiasis in Kenya is highest (>50%) in the Mwea Irrigation Scheme in central Kenya and in the Lake Victoria basin in western Kenya [3]. The four counties of western Kenya (Kakamega, Bungoma, Vihiga and Trans Nzoia) have historically been considered non-endemic for schistosomiasis or with limited transmission [25,26], due to among other factors inadequate data on infections in humans. However, results of the recent (September 2021) granular mapping survey confirmed the presence of schistosomiasis and revealed that a total of 19 Wards in Kakamega and Bungoma counties had prevalence of schistosomiasis ≥10% [27]. Whereas the survey provided evidence that schistosomiasis was endemic in the 4 counties, it also revealed several foci with low number of infections raising the question as to whether transmission was occurring autochthonously or whether they were imported cases. To address the aforementioned gap and as part of additional surveillance activities, the presence, species and prevalence of Schistosoma spp. in snail vectors for schistosomiasis was assessed in 19 Wards with highest S. mansoni prevalence (>10%) in Kakamega and Bungoma counties of western Kenya. We hypothesized that (i) snail vectors of Schistosoma spp. are present in in the study areas and, (ii) that the prevalence of Schistosoma infection among host snails is greater than zero, providing evidence of autochthonous transmission of schistosomiasis in the study areas. The survey was part of interventions being piloted towards the interruption of transmission for schistosomiasis through END Fund’s DIF M&E framework that envisages sustainable and context-appropriate snail control measures.
Materials and methods
Ethics statement
The study received approval from the Institutional Scientific Ethics Review Committee (ISERC) of the University of Eastern Africa Baraton (UEAB), approval # UEAB/ISERC/06/06/2023.
The authors confirm that the ethical policies of the journal, as noted on the journal’s author guidelines page, have been adhered to.
Study area and population
This study was conducted in Kakamega and Bungoma counties of western Kenya in February 2025 (Fig 1). Kakamega county is located at 00°20′N 34°46′E in the Western part of Kenya and covers an area of 3,051.3 Km2. The county is served by two main rivers, Yala and Isiukhu, with several streams and springs. Bungoma county lies between latitude 000 28’ and latitude 10 30’ North of the Equator, and longitude 340 20’ East and 350 15’ East of the Greenwich Meridian and covers an area of 3,032.4 Km2. The major physical features in Bungoma include Mt. Elgon, several hills (Chetambe, Sang’alo and Kabuchai), rivers (Nzoia, Kuywa, Sosio, Kibisi and Sio-Malaba/Malakisi), waterfalls such as Nabuyole and Teremi, and several dams. The temperatures in the 2 counties range from 180C to 290C. The region experiences two rainy seasons, the long rains in March to July and short rains in August to October. The average annual rainfall is between 1,280–2,214 mm for Kakamega and 400–1,800mm for Bungoma.
The 2 counties have a combined population of approximately 3,538,149 based on the 2019 census [28]. The main ethnic communities are Luhya, Teso and Sabot. Communities in the region practice a mixture of both subsistence and cash crop farming, with sugar cane being the preferred large-scale cash crop. Other economic activities include cottage Industries, tea farming, horticulture, livestock farming, wholesale and retail trade, quarrying and mining. Based on results of the granular mapping [27], S. mansoni was the main schistosome species in the two counties. The very few cases of S. haematobium were confined to few pockets.
Study sites sampled
The cross-sectional study involved 284 snail sampling sites selected from 42 primary school regions purposively selected in 19 Wards with the highest prevalence of S. mansoni in school-age children (SAC) in Kakamega and Bungoma counties (Fig 1) based on granular mapping data of 2021 [27]. Ten Wards with 22 primary school regions were included in Kakamega and 9 Wards with 20 primary school regions for Bungoma. Briefly, 2 primary school regions with the highest S. mansoni prevalence were selected in each Ward, 2 primary school regions that tied in S. mansoni prevalence were included and lastly 2 primary school regions that had the highest S. haematobium prevalence in SAC were also included. In each primary school region, water bodies including canals, rivers, streams, ponds, swamps/marshes and dams (Fig 2) where there was evidence of human-water contact activities were selected for snail sampling with the help of local community health promoters (CHPs). A river was considered as generally larger, deeper, with more continuous flow than a stream, while a stream was a smaller tributary that fed into a river. Each of the 284 sites sampled for snails in the primary school regions was visited once during the dry season (February 2025).
Snail sampling
Four teams each comprising of 5 personnel conducted the sampling, 2 teams in Kakamega (11 sites per team) and 2 teams in Bungoma (10 sites per team). Working closely with the local CHP in charge of a village, an effort was made to identify the main water bodies at each selected primary school region, where several ideal sampling points (range: 1–15) were explored at each water body. Snails were sampled by four experienced collectors using a scoop that is a dip-net, with a mesh size of about 2 mm, supported by a metal frame and mounted on a wooden handle 2 metres long.
A timed direct search method was employed, where at each sampling point, a total of 20 random scoops were made on every sampling occasion. The area/size per sampling point was approximately 5 m2 whereas lengths of 10 metres along streams, rivers and canals were used. Sampling time was fixed at 30 minutes at each water body and was carried out between 0900 hours and 1400 hours. The same collectors scooped for snails throughout so as to achieve some level of standardized sampling effort. The maximum time spent at each sampled site was not more than 2 hours, and each team covered 2 sites per day.
At each site, snails were separated, counted and identified to species-level based on shell morphological characteristics using standard taxonomic identification keys [29,30]. Briefly, morphological characters, included the general shape of the shell, shape of the whorls, number of coils and shape of the aperture. In order to determine the geographic distribution of snails the global positioning system (GPS) coordinates of all sampled habitats was geotagged using Kobo Collect Application (Cambridge, MA, USA). Data was collected in the field electronically using designed forms in Kobo Collect Application on android phones. All Biomphalaria and Bulinus snails from each sampled site were kept in separate well-labelled wide mouthed plastic containers with some aquatic vegetation from each of the sampled water bodies in order to maintain good aeration. All other snails were released back into the water body after examination. All Biomphalaria and Bulinus snails were transported to the Ministry of Health’s Vector-borne and Neglected Tropical Diseases Laboratory in Kakamega and MoH’s county Referral Hospital laboratory in Bungoma where they were screened for cercariae.
Snail screening for cercariae
To screen for patent infections, each snail was placed in an individual well of a 24-well plastic tissue culture plate containing 2 mL of bottled mineral water. The plate was exposed to indirect sunlight for 2 hours (1400–1600 hours) to induce cercarial shedding, a logistically driven timeframe that falls outside the optimal 0800–1300 hours emergence period for S. mansoni cercariae in Biomphalaria snails in this region [14]. This timeframe also overlaps with that for S. rodhaini, known to occur in this setting [14]. Based on the morphological criteria for identification of cercariae used in this study, the cercariae species could not be distinguished morphologically between S. mansoni and S. rodhaini or for any other Schistosoma sp.
Individual wells were then examined with the aid of a dissecting microscope for the presence or absence of cercariae. Upon staining with 1–2 drops of iodine, shed cercariae were identified to basic taxonomic groups using standard identification keys [31]. A sub-set (~10 snails per site) of snails that shed mammalian cercariae and non-shedders were preserved in individual vials in absolute ethanol for molecular analysis later.
Other variables
The presence or absence of human activity such as bathing, washing clothes, fishing and agricultural practices were recorded. The type of water body at each of the sampled sites was also recorded.
Statistical analysis
Data was exported from the Kobo Collect server in xls format and statistical analysis performed using STATA v.18 (StataCorp.; College Station, TX, USA). P values < 0.05 were considered statistically significant. Most of our analysis focused on B. pfeifferi as opposed to B. globosus since the evidence (human infections) [27] strongly supported the role of S. mansoni in transmission in this setting, but we also include some analysis for B. globosus where relevant. Unless otherwise indicated, values are presented as means ± S.D. GPS coordinates for each primary school region were used to generate a map of the snail abundance and cercarial shedding sites using R statistical software (v4.4.0; R Core Team 2021). Data were checked for normality and homogeneity of variance. The mean B. pfeifferi snail abundance was computed as the total number of snails collected per primary school region divided by the number of snail sampling locations in the school region. A two-sample Mann-Whitney U-test (equivalent to Wilcoxon rank-sum test) was used to compare the difference in mean snail abundance and also prevalence of infection for B. pfeifferi between the sites in Kakamega and Bungoma counties. Prevalence of schistosome infection in snails (as determined through cercarial emergence) was computed as the proportion of snails shedding cercariae. To determine whether mean abundance of B. pfeifferi differed between primary school regions with human S. mansoni prevalence <10% and those with ≥10% (from granular mapping data), we performed generalized linear model (GLM) in STATA v18, with the random effect of school and using the family negative binomial and link as logit. To determine the likelihood of finding an infected snail and the total number of snails, we correlated the number of B. pfeifferi positive for Schistosoma sp. cercariae with the total number of B. pfeifferi snails at primary school region using spearman correlation (rs). To determine if the abundance of B. pfeifferi snails at a particular primary school regions was associated with schistosome infection rates in school-age children (granular mapping data of September 2021), we correlated the mean number of snails collected at a school region with the initial prevalence in SAC at the corresponding region using spearman correlation (rs). The Kruskal-Wallis test with post-hoc Dunn’s test was used to compare the difference in mean B. pfeifferi snail abundance among the different types of water sources.
Results
Snail abundance
A total of 4,245 snails were collected across the 284 sites in the 42 primary school regions, with all but one school region yielding snails. A rich snail species diversity was observed in the sites sampled, with a total of 7 freshwater snail species putatively identified. Overall, B. pfeifferi was the dominant species (78.7%) collected followed by Lymnaea natalensis (15.6%). Other snail species identified included Bulinus globosus, Melanoides tuberculata, Physa acuta, Pila ovata and Ceratophallus spp. (Table 1 and S1 Data). No Biomphalaria sudanica snails were found at any of the sampled locations.
The mean abundance of B. pfeifferi was 1.8-fold higher in sampled sites in Kakamega (102 ± 131) compared to sites in Bungoma county (56 ± 103) (Z = -2.169, P = 0.0301). The converse was true for the mean abundance of B. globosus which was 1.5-fold higher in sites in Bungoma (3 ± 6) relative to sites in Kakamega county (2 ± 6) (Z = 2.334, P = 0.0196).
The mean B. pfeifferi abundance was lower in primary school regions with ≥10% S. mansoni prevalence compared to regions with <10% S. mansoni prevalence (Y = -1.54x + 3.91, P = 0.011), but was highly variable among regions. For instance, at Okanya primary school region in Bungoma, one of the regions with <10% S. mansoni prevalence it was high (mean abundance = 115 snails), while the mean abundance was low (1 snail) in Mahola primary school region in Kakamega, one of the regions with ≥10% S. mansoni prevalence.
A summary of the total number of snails, number of B. pfeifferi and B. globosus and the number of snails that shed any type of cercariae in Kakamega and Bungoma Counties by Ward is presented in Table 2.
A total of 1,106 and 2,235 B. pfefferi snails were collected in Bungoma and Kakamega counties, respectively (Table 2). Maraka Ward in Bungoma County had the highest number of snails that shed mammalian schistosome cercariae (Table 2). In Kakamega county, the highest number of snails that shed mammalian schistosome cercariae was 18 and 16 for Bunyala West Ward and Lusheya-Lubinu Wards, respectively (Table 2).
Spatial distribution of snails and Schistosoma cercarial shedding
B. pfeifferi were found in 36 out of the 42 primary school regions (85.7%) distributed across all the 19 Wards that were selected for the survey while B. globosus were recovered in only 8 primary school regions (19%) located in 6 Wards (Table 3). High B. pfeifferi abundance was noted in school regions closer to river Nzoia and associated tributaries (Fig 3). B. pfeifferi was collected at all the 8 school regions where B. globosus was present, except for 1 school region (Mikokwe in Bumula Ward). The highest number of B. pfeifferi (605 snails) was recorded at Indangalasia school region (Table 3) in Lusheya-Lubinu Ward, which interestingly also had both a high number of positive snails (16 snails) and high S. mansoni prevalence (35%) in SAC from granular mapping. The highest number of B. globosus (29 snails) was recorded at Lutasio school region in Khalaba Ward (Table 3), Kakamega county.
Overall, of the 3,341 B. pfeifferi snails collected, 87 (2.6%, 95% CI: 2.07-3.14) shed Schistosoma sp. cercariae. Cercarial shedding was recorded in 13 out of 42 school regions (31%; 95% CI: 17–45%) and shedding was highly variable among sites (Table 3). Out of these 13 school regions where shedding occurred, 7 were in Bungoma and 6 in Kakamega county (Fig 3). With respect to having high overall number of B. pfeifferi snails that shed cercariae, two school regions stood out from the rest, Kisembe in Kakamega county where 18 snails shed and Maraka PEFA in Bungoma county where 19 snails shed (Table 3). There was no difference in prevalence of Schistosoma sp. infection in B. pfeifferi between the school regions in Kakamega and Bungoma counties (Z = 1.037, P = 0.2999). 56 out of 2,235 (2.5%) and 31 out of 1,106 (2.8%) B. pfeifferi snails collected from Kakamega and Bungoma counties, respectively, shed S. mansoni cercariae. There was no correlation between the number of B. pfeifferi positive for Schistosoma sp. cercariae and the total number of B. pfeifferi snails (rs = 0.0864, P = 0.5853). Similarly, neither the total number nor the mean number of B. pfeifferi collected at the school regions was significantly correlated with S. mansoni prevalence in SAC, (rs = 0.1601, P = 0.3099) and (rs = 0.1490; P = 0.3447), respectively (Fig 4).
Prevalence of Schistosoma sp. cercariae in B. pfeifferi varied spatially and ranged from 1.2-72.0% among school regions where infected snails were found (Table 3). Prevalence of Schistosoma sp. cercariae in B. pfeifferi was highest at the Kisembe primary school region (72%) in Bunyala West Ward, Kakamega county, which also recorded a high prevalence of S. mansoni (40.7%) among SAC in the granular mapping survey [27]. Other school regions that had high cercarial shedding included Maraka PEFA primary (61.3%) in Maraka Ward and Kambini primary (38.5%) in Kimilili Ward, both in Bungoma county (Table 3). The prevalence of S. mansoni among SAC in the granular mapping survey was 50% and 28.3% for Maraka PEFA and Kambini schools, respectively. Nevertheless, the heterogeneity between school regions with high S. mansoni prevalence in SAC in relation to cercarial shedding in B. pfeifferi snails is worth noting as the pattern is difficult to succinctly characterize. For instance, while Kamuli primary school region recorded S. mansoni prevalence of 61.7% among SAC with a total of 135 B. pfeifferi collected, none of the snails shed cercariae. On the other hand, Kikwechi primary school region which recorded S. mansoni prevalence of 44.6% among SAC with a total of 83 B. pfeifferi collected, only 1 snail shed cercariae (Table 3). No B. pfeifferi snails were collected around Ebwaliro primary school region which interestingly recorded S. mansoni prevalence of 45% among SAC in the granular mapping survey.
Of the 88 B. globosus collected, none shed Schistosoma sp. cercariae cercariae.
Infection of Biomphalaria pfeifferi and Bulinus globosus with other digenetic trematodes
A total of 24 B. pfeifferi snails shed non-Schistosoma cercariae, which included Xiphidio cercariae, Echinostome cercariae and Amphistome cercariae.
Four out of the 88 B. globosus snails collected at Matili F.Y.M school region in Kimilili Ward, Bungoma county shed echinostome cercariae. None of the snails that shed cercariae were found to have double infections (e.g., to be simultaneously shedding two different kinds of cercariae).
A summary of the different types of cercariae shed by B. pfeifferi and B. globosus is presented in Table 4.
Distribution of snails of Biomphalaria pfeifferi snails among water bodies sampled in Kakamega and Bungoma counties
The total and relative B. pfeifferi abundance was highest in streams relative to the other types of water bodies sampled (Fig 5).
The mean B. pfeifferi snail abundance was significantly different across the different types of water bodies sampled (H = 25.5, P = 0.0001). While the mean abundance of B. pfeifferi was similar between streams and swamps/marshes, the proportion by type of water body was highest in streams (80.3%) (Table 5). The mean B. pfeifferi abundance at the streams was higher compared to rivers (P = 0.005) and ponds (P = 0.005) (Table 5). Dams/water pans did not yield any B. pfeifferi snails.
Discussion
A prerequisite to implementation of effective vector control strategies requires among other things an understanding of the vectors and ecological factors sustaining their distribution. The present study confirmed the presence, species and infectionj of Biomphalaria and Bulinus snails with Schistosoma sp. answering the lingering and intriguing question of autochthonous transmission of intestinal schistosomiasis in Kakamega and Bungoma counties. Few malacology studies have been conducted in this setting. Whereas one study documented high snail species composition and diversity in the bordering county of Trans Nzoia and suggested their potential as vectors for trematodes [32], this study looked at land and not freshwater snails. Both B. pfeifferi and B. sudanica have been reported in the neighboring county of Busia [33], while Biomphalaria and Bulinus snails were found in Uganda’s Mt. Elgon area [34]. Several Biomphalaria spp. including B. sudanica, B. choanomphala, B. smithi, B. stanleyi, B. angulosa and B. pfeifferi transmit S. mansoni in East Africa [35], but B. pfeifferi is arguably the most important due to its widespread distribution and its relatively high susceptibility to schistosome infections [36]. B. pfeifferi is known to prefer shallow/swampy water, with plant detritus as a substratum [37]. We found B. pfeifferi at 36 out of the 42 primary school regions (85.7%), with a preponderance for occurrence in streams and rivers. River Nzoia and its tributaries are the main sources of infection. There was no obvious indication that the closely related species B. sudanica plays a role in S. mansoni transmission in any of the sites sampled as no snails of this species were found. The distribution of snails across sampled locations was heterogeneous, and this may be explained by a combination of environmental and ecological factors (water physicochemical conditions, water speed, pollution, habitat type) [38], seasonal factors (dry season, heavy rains) [39], biological interactions (predators and competition) [40,41] and human-related factors (environmental modifications, pollution etc) [42,43] known to affect snail distribution.
Four types of digenetic trematode cercariae (Schistosoma sp., xiphidio, echinostome and amphistome) were shed by B. pfeifferi snails in our study, reflecting a fairly narrow biodiversity. Although antagonistic trematode interactions in snail hosts can affect schistosomiasis transmission [44], this likely doesn’t influence transmission dynamics in this setting given the low trematode biodiversity and absence of co-infections in B. pfeifferi. A low proportion of B. pfeifferi (2.6%) in our study shed Schistosoma sp. cercariae, likely to be those of S. mansoni, although we cannot rule out cercariae of S. rodhaini, known to occur in this setting [14]. S. mansoni cercariae emerge diurnally, peaking at dawn and midday [14] when their putative hosts enter the water and are available for infection. S. mansoni and S. rodhaini simultaneously infect Biomphalaria snails [14,45], with S. rodhaini’s entire shedding period extending from 1430–1030 hours [45], which overlaps with the shedding period in our study. However, based on the associated epidemiology (confirmed S. mansoni infections among SAC [27]) and, to some extent, the shedding pattern it is most likely that these were S. mansoni rather than S. rodhaini. The low proportion of cercarial shedding in our study is consistent with other studies that reported shedding ranging from below 1% to about 3% [14,19–21,46–48], although higher prevalence of 13.1% [49] and 24.4% [50] have also been reported. Absence of shedding even in areas of high transmission is also documented [51,52]. Nevertheless, it should be noted that even minimal exposure to cercariae-infested water can result in infection [53], even with only a few snails shedding [54]. Few infected snails shedding cercariae daily can potentially translate into a large number of human infections.
Several explanations may be advanced for the low numbers of snails shedding Schistosoma cercariae in our study. First, our study sampled snails in the afternoon (1400–1600 hrs), which may have missed the peak shedding time. Relative to other studied populations such as S. mansoni from Cameroon that typically undergo peak emergence around noon or later [55], peak cercarial emergence of S. mansoni in Biomphalaria snails from Lake Victoria in western Kenya occurs earlier between 0800–1300 hours [14]. Other explanations proposed for low shedding and which were discussed in detail in our previous work [19] include: (i) low infection rates or brief time points (pulses) for release of cercariae [56,57]; (ii) sampling challenges - schistosomiasis is highly localized, and the wide distribution of snails complicates identifying hotspots of infection; (iii) environmental and biological factors - infection may be suppressed by environmental contaminants or organisms like rotifers [58]; (iv) pre-patent infections [59,60] that may be underestimated using the cercarial emergence technique [61]; and (v) seasonal influence - snail infection and cercarial output vary by season [46,51], with highest cercarial output expected in the drier and hotter periods [62,63] when human-water contact is longer and more frequent and with snail concentration in the fewer water sources relative to other seasons [64]. Given that the present study was conducted in February, which is drier and hotter, the 2.6% cercarial output which is higher relative to the prevalence reported in several other studies may be reflective of this higher cercarial transmission potential in drier periods. Our findings corroborate the pattern observed for Bulinus spp. in Iringa, Tanzania, where Schistosoma spp. cercarial emergence was higher during the dry season [63], but contrasts with other studies from Tanzania [39,65] and South Africa [47] that reported higher cercarial emergence during the rainy season (presumably when temperatures are lower). Elsewhere, Gouvras and others [66] observed that shedding by Biomphalaria did not show any variation between dry and rainy seasons. Seasonal variations in cercarial shedding have implications for the design of control interventions. For instance, a mollusciciding programme should ideally be planned in a way that maximizes decrease in transmission at a minimum cost [67]. Therefore, proper timing of mollusciciding is important as it would not be advisable to apply molluscicides when there is very little or no transmission occurring. The WHO recommends that MDA should be conducted when the risk of reinfection is low [68], because higher reinfection rates cause the prevalence of infection to return to pre-treatment levels. To complement this, it is advised to reduce snail populations by applying molluscicides at least 5–7 weeks before MDA - a strategy that ensures reduced snail population and subsequently, a lower risk of reinfection [68].
In terms of transmission potential, a larger snail population means the probability of a parasite encountering and infecting a snail also increases, leading to a greater likelihood of finding infected snails [20]. Interestingly and rather counter-intuitive, we did not find an association between the number of B. pfeifferi positive for S. mansoni and the total number of B. pfeifferi snails. Other studies on S. haematobium in Bulinus truncatus along the Nile delta [62,69] reported similar findings. However, Gouvras and others [66] found that the number of shedding snails was positively associated with abundance of B. sudanica. Our finding suggests that while snail abundance is important for understanding disease transmission, infection prevalence depends not just on snail abundance but also on parasite density in water, snail susceptibility to different Schistosoma spp. and environmental conditions [24]. Furthermore, our study did not find an association between the prevalence of S. mansoni infection in B. pfeifferi and prevalence in humans (SAC), consistent with the study by Mutuku and others [20], but in contrast to Wang et al. [70]. The disparity in infection levels between snails and humans is supported by modeling studies that show that only a small percentage of snails need to be infected and shedding for high levels of human infection to occur [71]. We cannot rule out the fact that the disparity in infection levels between snails and humans in our study could simply be due to temporal variation, given that prevalence data in SAC was collected back in September 2021.
It is noteworthy mentioning that implementation of snail control activities requires competencies in malacology. This is especially important considering the limited capacity in snail control that exists in endemic countries, contributed in part by the priority given to preventive chemotherapy and the abandonment of snail control. Leveraging new tools and technologies such as artificial intelligence (AI) will go a long way in building capacity for the surveillance and evaluation of snail control activities, especially where interruption of transmission is envisaged. In this regard, the WHO App. for the identification of intermediate host snails [72] currently under development will be an invaluable resource in predicting snail species especially where there is uncertainty and has great potential to enhance snail control interventions in poor resource settings. In addition, to facilitate implementation of snail control, WHO published on specific standardized procedures and criteria for efficacy testing and evaluation, and a manual on the use of molluscicides in the field [68], and plans to strengthen capacities of health staff in medical malacology to reinforce snail control activities in countries [73].
The current study was not without limitations. First, we did not keep and maintain non-shedding snails for screening at a later time point for detection of snails that may have harbored pre-patent infections at the time of initial collection. It is plausible that some of the non-shedders may have harbored pre-patent infections and therefore the reported prevalence of infection in snails may have been underestimated. Pre-patent infections can substantially exceed patent infections [60] and are known to last for several weeks with only a proportion of snails reaching the stage of cercarial shedding [59]. However, methods such as crushing snails or the maintenance of non-shedding snails in search of larvae to clarify such pre-patent infections are unsuitable for large-scale monitoring and were beyond the scope of the current survey. Third, identification of cercariae was based on morphological characteristics which allow for identification of cercariae to the Schistosoma genus level, and species was not confirmed by molecular techniques. The suggestion for S. mansoni cercariae though not confirmed, is corroborated by the observed infections among SAC in the study areas [27]. Fourth, data on the abundance and infection of Schistosoma sp. mansoni in snails and that of S. mansoni infection in SAC was not contemporaneous, which may have weakened chances of detecting any useful associations. Fifth, we did not employ dredging to look for deep-dwelling snails, especially in dams.
Our findings of snail vectors and their shedding of S. mansoni cercariae provide solid evidence for autochthonous transmission in Kakamega and Bungoma counties of western Kenya. This argues for incorporation of focal snail control where feasible to complement chemotherapy alongside other interventions to accelerate interruption of transmission in these areas. The multiple water contact sites add to the complexity of vector control required in this setting. Whereas the impact of chemical-based molluscicides on schistosomiasis transmission has been documented, this approach is fraught with challenges among them cost, toxicity and the need for regular application [74]. Novel solutions that offer a lower cost, more sustainable option, for instance, simple measures such as fencing or bridging to keep people, particularly children, away from the water can be implemented in the confirmed transmission sites. These can be complemented by the provision of alternative facilities for water contact activities, such as swimming and laundry, where possible. Other cost-effective measures for safe water supply, including collection of rainwater can also be employed to minimize contact with transmission sites. Leveraging initiatives such as citizen science projects [75] could support consistent monitoring of snail species abundance and distribution as well as increasing awareness and participation among the communities in this setting.
Supporting information
S1 Data. Supplementary file field lab and malacology data.
https://doi.org/10.1371/journal.pntd.0014276.s001
(XLSX)
Acknowledgments
We thank the community health promoters who supported this study, Ministry of Health and Division of Vector Borne and Neglected Tropical Diseases (DVBNTD) both at the National and county Governments. We are very grateful to George Ogara, Kennedy Andiego, Meredith Odhiambo, Polycarp Odongo, Churchil Orao, John Oguso, Peter Olila, Austin Okinyo, Enock Sichangi, James Emisiko, Austin Wamalwa and Gabriel Wamalwa for supporting collection and identification of snails and who worked tirelessly to ensure the survey was a success. We also acknowledge the support from the Ministry of Interior and National Administration, and the National and County governments of Kakamega and Bungoma.
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