Skip to main content
Download PDF

Impact of chemical snail control on intermediate host snail populations for urogenital schistosomiasis elimination in Pemba, Tanzania: findings of a 3-year intervention study

Parasites & Vectors volume 17, Article number: 489 (2024) Cite this article

Abstract

Background

The World Health Organization (WHO) has set the goal of eliminating schistosomiasis as a public health problem globally by 2030 and to interrupt transmission in selected areas. Chemical snail control is one important measure to reduce transmission and achieve local elimination. We aimed to assess the impact of several rounds of chemical snail control on the presence and number of the Schistosoma haematobium intermediate snail host (Bulinus spp.) in water bodies (WBs) on Pemba Island, Tanzania, a setting targeted for elimination of urogenital schistosomiasis.

Methods

During the three annual intervention periods of the SchistoBreak study implemented in the north of Pemba from 2020 to 2024, malacological surveys were conducted up to four times per period in WBs of hotspot implementation units (IUs). Present freshwater snail species, vegetation, and WB characteristics were recorded. If Bulinus were found, the snails were inspected for Schistosoma infection and snail control with niclosamide was conducted.

Results

Across the three intervention periods, a total of 112 WBs were identified in 8 hotspots IUs. The spatial distribution of WBs with Bulinus per IU was heterogeneous, ranging from 0.0% (0/15) of WBs infested in one IU in 2022 to 80.0% (8/10) of WBs infested in one IU in 2021. Bulinus presence was significantly associated with lower pH values in WBs (odds ratio: 0.2, 95% confidence interval 0.1–0.4). A total of 0.2% (6/2360) of collected Bulinus were shedding Schistosoma cercariae. Following snail control, the number of Bulinus decreased or remained absent in 56.7% (38/67) of visits at WBs when compared with the previous visit in 2021, 54.9% (28/51) in 2022, and 33.3% (32/96) in 2023. In a total of 43.1% (22/55) of initially infested WBs, no Bulinus were found in the survey round conducted a few weeks after the first application of niclosamide. However, 25.4% (14/55) of WBs showed a pattern of recurring Bulinus presence.

Conclusions

The distribution of WBs containing Bulinus was very heterogeneous. The percentage of Bulinus with patent Schistosoma infection in our study area was extremely low. Repeated niclosamide application reduced the number of Bulinus in WBs, but snails often recurred after one or multiple treatments. While chemical mollusciciding can reduce snail numbers, to fully break the S. haematobium transmission cycle, timely diagnosis and treatment of infected humans, access to clean water, sanitation, and health communication remain of prime importance.

Trial registration: ISRCTN, ISRCTN91431493. Registered 11 February. 2020, https://www.isrctn.com/ISRCTN91431493

Graphical Abstract

Background

Schistosomiasis is a neglected tropical disease that is prevalent in 78 countries worldwide, with a particularly high prevalence in sub-Saharan African countries [1]. The infective agent is a parasitic blood fluke of the genus Schistosoma spp., which is transmitted in a human–snail–human life cycle [2]. The intermediate hosts of the African Schistosoma species are freshwater snails of different parasite-specific genera, which thrive in natural freshwater bodies, have a reproduction optimum at 25 °C, and can survive dry periods by estivating around the margins of water bodies [3, 4].

The World Health Organization (WHO) has set the goal of eliminating schistosomiasis as a public health problem globally and to interrupt Schistosoma transmission in selected areas by 2030 [1, 2]. To achieve this goal, the WHO recommends the implementation of interventions that address the human–snail–human life cycle at different stages simultaneously [5]. These interventions encompass a number of different strategies, including mass drug administration (MDA) with praziquantel of populations at risk of Schistosoma infection, behavior change communication measures, improvements in access to water, sanitation, and hygiene, and chemical snail control with the molluscicide niclosamide [5, 6].

Chemical snail control is recommended as a measure to reduce the intermediate host snail populations [6]. Since niclosamide is not only harmful to snails but may also cause damage to the environment and harms other invertebrates, amphibians, and fish, it should only be applied focally or in specific seasons [6]. Its application is particularly recommended for persistent hotspots of Schistosoma transmission, where several rounds of MDA have not resulted in a significant decrease of infection prevalence [5, 6]. Moreover, in combination with other interventions, snail control is expected to accelerate schistosomiasis elimination [5].

Schistosomiasis research, including many malacological and parasitological studies, has a century-long history on the Zanzibar Islands of the United Republic of Tanzania [7]. Studies showed that the only autochthonously transmitted Schistosoma species in Zanzibar infecting humans is S. haematobium and that the main, and likely only, freshwater snail species responsible for its transmission is Bulinus globosus [8,9,10]. Equally long is the history of interventions to mitigate urogenital schistosomiasis on the islands, including different approaches for snail control [11]. In 2010, the overall S. haematobium prevalence on the islands was < 10%, and efforts to eliminate schistosomiasis as a public health problem and to interrupt transmission started with the Zanzibar Elimination of Schistosomiasis Transmission (ZEST) project in 2012 [12]. For the first time in Zanzibar, in randomized areas, large-scale snail control with niclosamide was conducted in addition to biannual MDA, but no added impact was identified owing to very low numbers of infected individuals at the end of the trial in 2017 [12, 13]. In the subsequent SchistoBreak study (2020–2024), snail control was applied in remaining hotspot areas in the north of Pemba Island, together with regular MDA and behavior change communication measures to advance elimination [14].

The research presented here covers results from malacological surveys and mollusciciding interventions conducted in the hotspot areas of the SchistoBreak study. Our aim was to assess the impact of several rounds of chemical snail control on the presence and number of Bulinus in targeted water bodies.

Methods

Study setting

The SchistoBreak study was conducted in the north of Pemba, one of the two main islands of the Zanzibar Archipelago. The island is located around 30 km off the Tanzanian mainland and is divided into four districts, which are subdivided into 129 small administrative areas, called shehias [15]. The SchistoBreak study was implemented in the districts Micheweni and Wete in 20 shehias, referred to hereinafter as implementation units (IUs) [14]. Implementation units with S. haematobium prevalence ≥ 3.0% in an annual school-based parasitological survey or ≥ 2.0% in an annual household-based parasitological survey were considered to be hotspot areas [14, 16]. In these hotspot areas, a combined intervention package consisting of annual school-based and community-based MDA, behavior change communication measures, and snail control were implemented to accelerate urogenital schistosomiasis elimination [14].

Malacological surveys and snail control

The locations of freshwater bodies in the SchistoBreak study area were mainly identified through an initial survey of IU characteristics, conducted at the onset of the study in 2020 [16]. Additional water bodies and their locations were pointed out by children who were part of surveillance-response interventions in low-prevalence IUs [17]. To decide whether a waterbody in a hotspot IU should be treated with niclosamide, malacological surveys were conducted to investigate whether Bulinus were present [14]. To conduct the malacological surveys, two experienced field workers entered the water with protective gear and searched the shoreline for freshwater snails in a 20-m distance for 10 min. The snails were identified morphologically at genus level and the numbers were recorded with a predesigned questionnaire, using the software Open Data Kit (ODK, www.opendatakit.org), installed on Samsung Galaxy Tab A tablets. All collected snails were placed back into the water, with the exception of Bulinus, which were transported in plastic containers containing water from the water body to the Public Health Laboratory–Ivo de Carneri (PHL-IdC) in Chake Chake. Here, the snails were kept overnight at room temperature and examined for cercariae shedding the following day. For this purpose, each snail was placed in a single well of a multiple-well plate and covered with drinking water. The plate was placed in direct sunlight as shedding is stimulated by light [18]. After 30 min, each well was inspected for Schistosoma cercariae using a dissection microscope. Subsequently, the snails were placed back in the sunlight and wells were inspected again for cercariae after 15 min.

In addition, at the waterbodies, the type of water body (stream/river, pond/lake), temperature, pH value, and conductivity of the water were measured using a water meter (HI98129 Kombi-Tester; Hanna Instruments Deutschland GmbH, Vöhringen, Germany), and information about size, depth, sediment, steepness of shorelines, rice cultivation, vegetation growth, and whether the water body was permanent was recorded in ODK.

Snail control using the molluscicide niclosamide (WP83,1; Bayer AG Crop Science Division, Monheim, Germany) was conducted at human water contact sites at all freshwater bodies in a hotspot IU where Bulinus were found, in the current malacological survey, and subsequently at any previous visit during the SchistoBreak study, and additionally, if data from the ZEST study had indicated an infestation with Bulinus in the past. The nature and size of the freshwater body dictated the machine with which niclosamide was applied. At small water bodies, plastic backpack sprayers (Farmate, Taizhou Sunny Agricultural Machinery Co., LTd, Taizhou, China) were used; at larger water bodies, a gasoline-powered sprayer (Zhejiang O O Power Machinery Co., Ltd, Zhejiang, China) was applied. The initial concentration of niclosamide in water was 8–10 g of wettable powder dissolved in 1 L of water taken from the water body. One backpack sprayer can hold an initial volume of 10 L of water, in which 80 g of niclosamide was dissolved. The barrel attached to the gasoline-powered sprayer can hold an initial volume of 100 L of water, in which 1000 g of niclosamide was dissolved. The amount of niclosamide and the machines used for each application were recorded in ODK, as well as the area in square meters that was sprayed.

Every water body in a hotspot IU was visited, surveyed, and potentially sprayed with niclosamide up to four times per intervention period of the SchistoBreak study, which covered the months of May–November in each of 2021, 2022, and 2023.

Data management and statistical analyses

The data collected in ODK were sent to a secured specific ODK server at the Swiss Tropical and Public Health Institute in Allschwil, Switzerland. Subsequently, the data were cleaned with STATA/IC 16.1 (StataCorp LLC, College Station, TX, USA) and analyzed using R version 4.3.2 (www.rproject.org).

To assess the association between environmental factors or the presence of other snail genera with the presence of Bulinus, univariable and multivariable logistic regressions were conducted and odds ratios (ORs) with 95% confidence intervals (CIs) were determined. All naïve water bodies in 2021–2023, where snail control had not been previously conducted during the SchistoBreak study, were included in the models. Stepwise selection was used to develop the model of the multivariable regression. Variables with a generalized variance inflation factor > 10 were excluded from the multivariable regression owing to multicollinearity.

The geolocation of water bodies where malacological surveys were conducted was mapped. The number of Bulinus found during each visit was stratified into the following categories: zero, 1–9, 10–24, and 25–127. Furthermore, it was indicated whether water bodies were dry when visited. Water bodies overlapping on the map were jittered manually.

To assess the overall change in Bulinus numbers per intervention period, the number of Bulinus per water body, visit, and intervention period, respectively, was determined for all water bodies where niclosamide was applied at every visit during the intervention period. Hence, the analysis followed a longitudinal design, examining the same water bodies during each intervention period. Water bodies that were already subjected to snail control in intervention period 1 were excluded from the analysis in intervention period 2. Moreover, it was assessed after how many rounds of niclosamide application zero Bulinus were found, and whether Bulinus reoccurred, i.e., when a water body showed a positive–negative–positive pattern on visit 1–3 or in visit 2–4 despite repeated snail control.

To show the change of Bulinus numbers from one visit to the next visit at the same water body after the application of niclosamide, scatterplots were created for all water bodies, where snail control was conducted after the malacological survey of the previous visit and that were not dry on any of the compared visits. To visualize the change, a diagonal with a slope of 1 was inserted. Here, the analysis did not follow a longitudinal approach but water bodies were analyzed from one visit to the next visit. Water bodies that were already subjected to snail control in intervention period 1 were excluded from intervention period 2. Success was defined as either a reduction in snail numbers from one visit to the next or as maintaining zero snails.

Results

Water bodies with freshwater snails per year

In the SchistoBreak study, five IUs were considered hotspot IUs in 2021, four in 2022, and three in 2023 (Table 1). In total, there were eight different hotspot IUs identified across the project time. In the three intervention periods, 50 water bodies were visited up to four times in hotspot IUs in 2021, 59 in 2022 and 57 in 2023. In total, 112 different water bodies were visited up to four times across the three periods. Among the 112 water bodies, 97 (86.6%) were streams, 7 (6.3%) were ponds, and 2 (1.8%) were of other types.

Table 1 Water bodies with freshwater snails
Full size table

In the study area, across the three intervention periods, water bodies were found to be infested with freshwater snails of the genera Bulinus, Lanistes, and Lymnaea. The genus Thiara was only found in 2021. No water body was found to be infested with Cleopatra or Pila. Prior to the implementation of snail control, during the initial visit of each intervention period, 54.2% (26/48) of the water bodies in 2021 were found to be infested with Bulinus, 25.9% (15/58) in 2022, and 31.6% (18/57) in 2023. Across all intervention periods, a total of 2360 Bulinus were collected at water bodies and subjected to examination for the presence of cercariae. Only 0.2% (6/2360) of the Bulinus were shedding cercariae.

Environmental factors associated with Bulinus presence in untreated water bodies

At the initial visit of water bodies, before any of them had been treated with niclosamide, the odds of finding Bulinus were significantly higher in water bodies with muddy sediment (multivariable OR: 46.6, 95% CI 4.5–729.5, P < 0.01) than in water bodies with sandy sediment only (Fig. 1; Supplementary file 1). Furthermore, the odds of finding Bulinus were lower in water bodies that were a rice field (multivariable OR: 0.08, 95% CI 0.01–0.8) compared with water bodies where no irrigation farming was conducted. Bulinus presence was significantly associated with lower pH values in both the univariable and the multivariable model (multivariable OR: 0.2, 95% CI 0.07–0.4, P < 0.001). In the multivariable model, the presence of Bulinus was significantly associated with the presence of snails of the genus Lanistes (multivariable OR: 6.5, 95% CI 2.0–25.4, P < 0.01).

Fig. 1
figure 1

Environmental predictor variables for Bulinus presence. Environmental predictor variables for Bulinus presence at water bodies (WBs) that were not (yet) sprayed with niclosamide in the north of Pemba, Tanzania

Full size image

Water bodies with Bulinus per implementation unit and year

In 2021, at the initial visit, the proportion of water bodies with Bulinus per IU ranged from 29.4% (5/17) in one IU to 80.0% (8/10) in another IU (Fig. 2B). A total of 50 water bodies were visited up to four times throughout the intervention period, and 56.0% (28/50) of these were found to be infested with Bulinus at least once during the visits.

Fig. 2
figure 2

Water bodies with Bulinus in the study area. Schistosomiasis hotspot areas in the north of Pemba (A) and the presence and number of Bulinus in water bodies in 2021 (B), 2022 (C), and 2023 (D). Visits 1–4 from outside to inside circle. To optimize visualization, the locations of overlapping water bodies have been manually jittered. Number of Bulinus: green: 0; yellow: 1–9; orange: 10–24; red: 25–127; black: dry; grey: not assessed

Full size image

In 2022, the proportion of water bodies with Bulinus per IU ranged from 0.0% (0/15) to 66.7% (4/6) at the initial visit Fig. 2C. During the intervention period, a total of 59 water bodies were visited up to four times, and in 35.6% (21/59), Bulinus were found on at least one visit Fig. 2D.

In 2023, during the first visit, the proportion of water bodies with Bulinus per IU ranged from 18.8% (3/16) to 56.2% (9/16). A total of 57 water bodies were visited up to four times throughout the intervention period, and 43.9% (25/57) harbored Bulinus on at least one visit (Fig. 2D).

Throughout all three intervention periods, 48.2% (54/112) of the water bodies were dry during at least one visit and hence temporary, while 51.8% (58/112) were never dry and hence permanent. Overall, in 33.3% (18/54) of the temporary water bodies, Bulinus were found at least once. In 22.2% (12/54) of the temporary water bodies, ten or more Bulinus were found at least once. Conversely, in 60.3% (35/58) of the permanent water bodies, Bulinus were found at least once, and in 46.6% (27/58) ten or more Bulinus were found at least once.

Change in number of Bulinus after mollusciciding, per intervention period

The following paragraphs describe the change in the total number of Bulinus and different categories of Bulinus numbers, respectively, in water bodies that were infested at the initial visit of the intervention period and hence treated with niclosamide at the initial and all subsequent visits of the respective intervention period unless a water body was dry (Fig. 3 A-C).

Intervention period 1 (2021)

During the first visit in the first intervention period, a total of 1006 Bulinus were found in 26 water bodies, which were subsequently treated with niclosamide. Across the intervention period, 49,380 g of niclosamide was used to spray 16,875 m of shoreline. By the last visit, the number of Bulinus was reduced by 92.8% to 72 Bulinus found in 16 water bodies. A total of 29.2% (7/24) of the water bodies exhibited a consistent decline in the number of Bulinus from higher to lower categories or remained at zero from one visit to the next (Fig. 3A). Another 70.8% (17/24) of the water bodies showed oscillating patterns between the categories, and no water body exhibited a consistent increase in the categories. Finally, in 20.8% (5/24) of the water bodies, Bulinus reoccurred in visit 3 or 4, while no Bulinus had been found during visit 2 or 3, respectively.

In the same 24 water bodies, 296 snails of the genus Lanistes were found during the first visit. By the last visit, the number of Lanistes was reduced by 87.8% to 36 Lanistes found in 16 water bodies.

Intervention period 2 (2022)

During the first visit in the second intervention period, a total of 133 Bulinus were found in 11 water bodies that were not dry and had not already been visited in the first intervention period. The 11 water bodies were subsequently subjected to snail control. Across the intervention period, 39,860 g of niclosamide was used to spray 10,092 m of shoreline. By the last visit, the number of Bulinus had decreased by 95.5% to a total of six Bulinus in five water bodies. A total of 27.3% (3/11) of the water bodies exhibited a consistent decline in the number of Bulinus from higher to lower categories or remained at zero from one visit to the next (Fig. 3B). Another 72.7% (8/11) of the water bodies showed oscillating patterns within the categories. No water body exhibited a consistent increase in the categories. In a total of 9.1% (1/11) of the water bodies, Bulinus reoccurred in visit 3 or 4, while no Bulinus had been found during visit 2 or 3, respectively.

In the same 11 water bodies, 108 snails of the genus Lanistes were found during the first visit. By the last visit, the number of snails was reduced by 77.8% to 24 Lanistes found in 5 water bodies.

Intervention period 3 (2023)

During the first visit in the last intervention period, a total of 274 Bulinus were found in 18 water bodies, which were subsequently sprayed with niclosamide. Across the intervention period, 50,840 g of niclosamide was used to spray 17,639 m of shoreline. By the last visit, the number of Bulinus had decreased by 36.1% to a total of 175 Bulinus in these water bodies. A total of 66.7% (12/18) of the water bodies exhibited a consistent decline in the number of Bulinus from higher to lower categories or remained at zero from one visit to the next (Fig. 3C). Another 33.3% (6/18) of the water bodies showed oscillating patterns within the categories, and no water body exhibited a consistent increase in the categories. In a total of 38.9% (7/18) of the water bodies, Bulinus reoccurred in visit 3 or 4 after zero Bulinus had been found during visit 2 or 3, respectively.

In the same 18 water bodies, 199 Lanistes were found during the first visit. By the last visit, the number of Lanistes was reduced by 68.8% to 62 snails.

Fig. 3
figure 3

Number of Bulinus after snail control. Number of Bulinus in water bodies (WBs) that contained Bulinus at the initial visit and received snail control at least once during the intervention periods in 2021 (A), 2022 (B), or 2023 (C)

Full size image

Change in number of Bulinus after mollusciciding, per visit and intervention period

The following paragraphs describe the change in the number of Bulinus in infested water bodies per visit after niclosamide was applied in the previous visit (Fig. 4A–I).

Fig. 4
figure 4

Number of Bulinus in water bodies before and after mollusciciding. Number of Bulinus in water bodies in hotspot areas per visit (1–4) and per intervention period (2021–2023). Between the compared visits, niclosamide was applied to the water bodies. To optimize visualization, the axes of the first figure (A) range from 0 to 150 while the axes of the other figures (B–I) range from 0 to 60. Jittering was used to allow all points to be shown

Full size image

Intervention period 1 (2021)

In 2021, a total of 24 water bodies were treated with niclosamide at visit 1. Comparing the number of Bulinus found at visit 1 and visit 2, in 83.3% (20/24) of the water bodies, the number of Bulinus decreased or remained zero. From visit 2 to visit 3, Bulinus numbers were reduced or remained zero in 54.5% (12/22) of previously treated water bodies. From visit 3 to 4, Bulinus numbers had decreased or remained zero in 28.6% (6/21) of previously treated water bodies. Overall, in the intervention period of 2021, the number of Bulinus decreased or remained zero in 56.7% (38/67) of the comparisons of Bulinus numbers from current to previous visit.

Intervention period 2 (2022)

In 2022, a total of 19 water bodies were treated with niclosamide at the first visit. From the first to the second visit, in 68.4% (13/19) of the water bodies, the number of Bulinus decreased or remained zero. From visit 2 to visit 3 and from visit 3 to 4, Bulinus numbers in 42.1% (8/19) and 53.8% (7/13) of the water bodies decreased or remained zero, respectively. Overall, in the intervention period of 2022, the number of Bulinus decreased or remained zero in 54.9% (28/51) of the comparisons of Bulinus numbers from the current to the previous visit.

Intervention period 3 (2023)

In 2023, a total of 42.4% of the water bodies were treated with niclosamide at the first visit. The comparison of the first with the second visit showed that, in 42.4% (14/33) of the water bodies, the number of Bulinus was reduced or remained zero. From visit 2 to visit 3, Bulinus numbers decreased or remained zero in 16.1% (5/31) of previously treated water bodies. From visit 3 to 4, Bulinus numbers decreased or remained zero in 40.6% (13/32) of previously treated water bodies. Overall, in the intervention period of 2023, the number of Bulinus decreased in 33.3% (32/96) of the comparisons of Bulinus numbers from the current to the previous visit.

Water bodies with a reduction of Bulinus to zero across visits and intervention periods

The following paragraph describes the change of the number of water bodies infested with Bulinus from the first to the fourth visit, when water bodies were treated with niclosamide on all visits.

Throughout all three intervention periods, there were 55 water bodies that contained Bulinus at the first visit and where snail control was subsequently conducted on all following visits (Table 2). Among them, 51 were not dry during the second visit, and 43.1% (22/51) of these water bodies had zero Bulinus at this second visit. At the third visit, 45.7% (21/46) of the water bodies that were not dry had zero Bulinus. At the fourth visit, 47.4% (18/38) of the water bodies that were not dry had zero Bulinus. A total of 10.9% (6/55) of the water bodies never reached zero Bulinus, despite the consecutive application of niclosamide.

Table 2 Water bodies with a reduction of Bulinus to zero
Full size table

Discussion

The elimination of schistosomiasis as a public health problem globally and the interruption of Schistosoma transmission in selected areas are goals defined by the WHO for 2030 [1, 2]. Chemical snail control is recommended as a measure to diminish the intermediate host snail populations and, in combination with other interventions, is expected to reduce transmission significantly and thus to hasten elimination [5, 6]. We aimed to assess the impact of several rounds of chemical snail control on the presence and number of Bulinus in water bodies of hotspot IUs of the SchistoBreak study on Pemba Island, Tanzania, a setting targeted for elimination of urogenital schistosomiasis.

We found that many water bodies were located in the hotspot IUs of our study area. However, the distribution of water bodies containing Bulinus was highly heterogeneous, and the only clear predictor for the occurrence of Bulinus was a low pH value of the water. Moreover, Bulinus were found more often in water bodies with muddy riverbanks, which aligns with results from a study conducted in Ethiopia [19]. Additional, but no unique explanatory factors for Bulinus occurrence were reported in other studies from Zanzibar and elsewhere [10, 20,21,22,23], making it hard to clearly predict intermediate host snail presence or absence. Overall, only a tiny percentage (0.2%) of snails shed Schistosoma cercariae in our study. The very low rate of patent Schistosoma infections in intermediate host snails in Pemba is in line with previous studies from the Zanzibar Islands [22, 24, 25]. All these findings point to the very focal transmission of Schistosoma and underline the importance of conducting malacological surveys and mapping of snails to decide whether and where niclosamide should be applied [19, 26]. Since niclosamide not only kills snails but also has detrimental effects on other invertebrates, amphibians, and fish, it should be used very carefully and only at foci where intermediate host snails thrive and people are at risk of Schistosoma infection [5, 27]. In our study, we found that the use of niclosamide not only has an impact on Bulinus but also reduced the number of snails of the genus Lanistes. Moreover, while the niclosamide in our study was donated, it needs to be flagged that buying the molluscicide is expensive [28]. Hence, to keep environmental and financial costs at the lowest possible level, snail control with niclosamide should only be conducted at confirmed intermediate host snail habitats, in areas where schistosomiasis is endemic.

Our results clearly show that repeated rounds of snail control effectively reduced the number of Bulinus over time, and numerous water bodies became snail-free after the initial application of niclosamide. A decline in the number of intermediate host snails is expected to reduce the risk of Schistosoma transmission to humans [6] and hence to support the WHO elimination goals. Indeed, a review of 63 studies on focal snail control indicated that, the longer the duration of snail control, the lower the odds of human Schistosoma infection [29]. These findings underscore the impact of snail control on human infection and highlight the need for a prolonged intervention duration for successful schistosomiasis elimination.

The quick recurrence of Bulinus in some of the water bodies that were treated with several rounds of niclosamide indicates that the mollusciciding has no enduring impact on Bulinus presence and that the snail populations in our study were not fully eliminated. While this suggests that the impact on the ecosystem with a focus on Bulinus is not dramatic, it also illustrates that rapidly rebounding snail populations pose a risk of recrudescence of Schistosoma transmission and jeopardize the elimination goals.

As recommended by the WHO, for a more sustainable impact on human infections, snail control should be implemented together with other interventions, including treatment with praziquantel, water sanitation and hygiene measures, and behavior change interventions [5]. A combination of interventions not only can result in prevalence reduction but also supports the cost-efficiency of interventions, as shown by simulations from Kenya where adding snail control to school-based MDA was found to be more cost-effective than MDA alone in 95% of the simulations [28]. Ideally, praziquantel treatment interventions are timed to seasonal Schistosoma transmission and snail control. Studies showed that snail control is conducted best during the peak transmission season to maximize the impact of molluscicides, while minimizing the frequency of intervention rounds and thereby reducing negative adverse effects on the environment [30,31,32]. These studies also indicated that MDA is conducted best during the low-transmission season when snail density is at its minimum. However, very likely, neither snail control nor treatment interventions, nor a combination thereof, will result in the complete interruption of Schistosoma transmission. To achieve and maintain elimination, people living in endemic areas need to have access to improved water and hygiene facilities to avoid contact with potentially Schistosoma cercariae-contaminated freshwater from lakes or streams. Without the requisite infrastructure, a change in human behavior cannot occur. Furthermore, this change in behavior will require that people living in endemic areas understand how Schistosoma infections are transmitted, what health consequences an infection can have, and how the infection can be prevented.

Of note, our study has several limitations. First, Bulinus are hermaphrodites and a single surviving snail can multiply into a new population. Hence, results on the reduction of snail number categories are to be interpreted with care. Second, the water flow, inflow, and outflow of water bodies may have influenced the effectiveness of mollusciciding owing to rapid dilution of the niclosamide concentration after spraying. Third, snails and cercariae were only identified morphologically at genus level and no molecular analyses were conducted to determine the species. Hence, the very low numbers of Schistosoma cercariae found may have been due to infection of Bulinus with either S. haematobium or S. bovis. Determination of the Schistosoma species in future studies will be important to shed light on the potential for hybrid species to emerge as a future concern for elimination.

Conclusions

The distribution of water bodies containing Bulinus was very heterogeneous, and the main predictor for Bulinus occurrence was low pH of the water. Chemical snail control reduced the number of Bulinus in water bodies, particularly when niclosamide was applied in multiple rounds. However, in many water bodies, snails reoccurred after one or multiple treatments. Our results show that chemical snail control can help to reduce snail numbers. However, to fully break the S. haematobium life cycle, timely diagnosis and treatment of infected humans, improved access to clean water and sanitation, and increased health literacy of people living in endemic areas remain of prime importance.

Availability of data and materials

Data are provided within the manuscript or supplementary information files.

Abbreviations

CI:

Confidence interval

IU:

Implementation unit

MDA:

Mass drug administration

OR:

Odds ratio

PHL-IdC:

Public Health Laboratory–Ivo de Carneri

WHO:

World Health Organization

References

  1. World Health Organization. Ending the neglect to attain the sustainable development goals: a road map for neglected tropical diseases 2021–2030. World Health Organization. License: CC BY-NC-SA 3.0 IGO. 2020. https://apps.who.int/iris/handle/10665/338565. Accessed 18 Nov 2024.

  2. World Health Organization. Weekly epidemiological record. Schistosomiasis and soil-transmitted helminthiases: progress report, 2021. vol. 48. Geneva; 2022. pp. 621–32. https://www.who.int/publications/i/item/who-wer9748-621-632. Accessed 18 Nov 2024.

  3. Rollinson D, Stothard JR, Southgate VR. Interactions between intermediate snail hosts of the genus Bulinus and schistosomes of the Schistosoma haematobium group. Parasitology. 2001;123:S245–60. https://doiorg.publicaciones.saludcastillayleon.es/10.1017/s0031182001008046.

    Article  PubMed  Google Scholar 

  4. Webbe G. The transmission of Schistosoma haematobium in an area of Lake Province, Tanganyika. Bull World Health Organ. 1962;27:59–85.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. World Health Organization. WHO guideline on control and elimination of human schistosomiasis. License: CC BY-NC-SA 3.0 IGO. 2022. https://apps.who.int/iris/handle/10665/351856. Accessed 18 Nov 2024.

  6. World Health Organization. Field use of molluscicides in schistosomiasis control programmes—an operational manual for programme managers. 2017. p. 50. https://www.who.int/publications/i/item/9789241511995. Accessed 18 Nov 2024.

  7. Trippler L, Knopp S, Welsche S, Webster BL, Stothard JR, Blair L, et al. The long road to schistosomiasis elimination in Zanzibar: a systematic review covering 100 years of research, interventions and control milestones. Adv Parasitol. 2023. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/bs.apar.2023.06.001.

    Article  PubMed  Google Scholar 

  8. Stothard JR, Rollinson D. Molecular characterization of Bulinus globosus and B. nasutus on Zanzibar, and an investigation of their roles in the epidemiology of Schistosoma haematobium. Trans R Soc Trop Med Hyg. 1997;91:353–7. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/s0035-9203(97)90105-x.

    Article  CAS  PubMed  Google Scholar 

  9. Stothard JR, Loxton N, Rollinson D, Mgeni AF, Khamis S, Ameri H, et al. The transmission status of Bulinus on Zanzibar Island (Unguja), with implications for control of urinary schistosomiasis. Ann Trop Med Parasitol. 2000;94:87–94. https://doiorg.publicaciones.saludcastillayleon.es/10.1080/00034983.2000.11813517.

    Article  CAS  PubMed  Google Scholar 

  10. Allan F, Dunn AM, Emery AM, Stothard JR, Johnston DA, Kane RA, et al. Use of sentinel snails for the detection of Schistosoma haematobium transmission on Zanzibar and observations on transmission patterns. Acta Trop. 2013;128:234–40. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.actatropica.2013.01.003.

    Article  PubMed  Google Scholar 

  11. Mozley A. XXVI—the fresh-water mollusca of the Tanganyika territory and Zanzibar Protectorate, and their relation to human schistosomiasis. Trans R Soc Edinb. 1939;59:687–744. https://doiorg.publicaciones.saludcastillayleon.es/10.1017/S0080456800017403.

    Article  Google Scholar 

  12. Knopp S, Mohammed KA, Ali SM, Khamis IS, Ame SM, Albonico M, et al. Study and implementation of urogenital schistosomiasis elimination in Zanzibar (Unguja and Pemba islands) using an integrated multidisciplinary approach. BMC Public Health. 2012;12:930. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/1471-2458-12-930.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Knopp S, Person B, Ame SM, Ali SM, Hattendorf J, Juma S, et al. Evaluation of integrated interventions layered on mass drug administration for urogenital schistosomiasis elimination: a cluster-randomised trial. Lancet Glob Health. 2019;7:e1118–29. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/S2214-109X(19)30189-5.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Trippler L, Hattendorf J, Ali SM, Ame SM, Juma S, Kabole F, et al. Novel tools and strategies for breaking schistosomiasis transmission: Study protocol for an intervention study. BMC Infect Dis. 2021;21:1024. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12879-021-06620-8.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Ministry of Finance and Planning-National Bureau of Statistics Tanzania, President's Office-Finance and Planning-Office of the Chief Government Statistician Zanzibar. Administrative units population distribution report. 2022. https://www.nbs.go.tz/nbs/takwimu/Census2022/Administrative_units_Population_Distribution_Report_Tanzania_volume1a.pdf. Accessed 18 Nov 2024.

  16. Trippler L, Ali SM, Ame SM, Hattendorf J, Suleiman KR, Ali MN, et al. Fine-scale-mapping of Schistosoma haematobium infections at the school and community levels and intermediate host snail abundance in the north of Pemba Island: baseline cross-sectional survey findings before the onset of a 3-year intervention study. Parasit Vectors. 2022;15:292. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13071-022-05404-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Trippler L, Taylor L, Ali MN, Najim SO, Khamis KS, Hattendorf J, et al. Test-treat-track-test-treat (5T) approach for Schistosoma haematobium elimination on Pemba Island, Tanzania. BMC Infect Dis. 2024;24:661. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12879-024-09549-w.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Gryseels B. Schistosomiasis. Infect Dis Clin N Am. 2012;26:383–97. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.idc.2012.03.004.

    Article  Google Scholar 

  19. Meleko A, Li S, Turgeman DB, Bruck M, Kesete NZ, Zaadnoordijk W, et al. Schistosomiasis control in Ethiopia: the role of snail mapping in endemic communities. Trop Med Infect Dis. 2022. https://doiorg.publicaciones.saludcastillayleon.es/10.3390/tropicalmed7100272.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Moser W, Greter H, Schindler C, Allan F, Ngandolo BN, Moto DD, et al. The spatial and seasonal distribution of Bulinus truncatus, Bulinus forskalii and Biomphalaria pfeifferi, the intermediate host snails of schistosomiasis, in N’Djamena, Chad. Geospat Health. 2014;9:109–18. https://doiorg.publicaciones.saludcastillayleon.es/10.4081/gh.2014.9.

    Article  PubMed  Google Scholar 

  21. Manyangadze T, Chimbari MJ, Rubaba O, Soko W, Mukaratirwa S. Spatial and seasonal distribution of Bulinus globosus and Biomphalaria pfeifferi in Ingwavuma, uMkhanyakude district, KwaZulu-Natal, South Africa: implications for schistosomiasis transmission at micro-geographical scale. Parasit Vectors. 2021;14:222. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13071-021-04720-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Pennance T, Person B, Muhsin MA, Khamis AN, Muhsin J, Khamis IS, et al. Urogenital schistosomiasis transmission on Unguja Island, Zanzibar: characterisation of persistent hot-spots. Parasit Vectors. 2016;9:646. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13071-016-1847-0.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Knopp S, Person B, Ame SM, Mohammed KA, Ali SM, Khamis IS, et al. Elimination of schistosomiasis transmission in Zanzibar: baseline findings before the onset of a randomized intervention trial. PLoS Negl Trop Dis. 2013. https://doiorg.publicaciones.saludcastillayleon.es/10.1371/journal.pntd.0002474.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Allan F, Ame SM, Tian-Bi YNT, Hofkin BV, Webster BL, Diakité NR, et al. Snail-related contributions from the schistosomiasis consortium for operational research and evaluation program including xenomonitoring, focal mollusciciding, biological control, and modeling. Am J Trop Med Hyg. 2020;103:66–79. https://doiorg.publicaciones.saludcastillayleon.es/10.4269/ajtmh.19-0831.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Knopp S, Ame SM, Person B, Hattendorf J, Rabone M, Juma S, et al. A 5-year intervention study on elimination of urogenital schistosomiasis in Zanzibar: parasitological results of annual cross-sectional surveys. PLoS Negl Trop Dis. 2019. https://doiorg.publicaciones.saludcastillayleon.es/10.1371/journal.pntd.0007268.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Sokolow SH, Wood CL, Jones IJ, Lafferty KD, Kuris AM, Hsieh MH, et al. To reduce the global burden of human schistosomiasis, use ‘old fashioned’ snail control. Trends Parasitol. 2018;34:23–40. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.pt.2017.10.002.

    Article  PubMed  Google Scholar 

  27. Yang Q, Liu M, Huang D, Xiong W, Yu Q, Guo T, et al. A survey and ecological risk assessment of niclosamide and its degradation intermediate in Wucheng waters within Poyang Lake Basin, China. Pol J Environ Stud. 2021;30:433–51. https://doiorg.publicaciones.saludcastillayleon.es/10.15244/pjoes/117695.

    Article  CAS  Google Scholar 

  28. Lo NC, Gurarie D, Yoon N, Coulibaly JT, Bendavid E, Andrews JR, et al. Impact and cost-effectiveness of snail control to achieve disease control targets for schistosomiasis. Proc Natl Acad Sci USA. 2018;115:E584–91. https://doiorg.publicaciones.saludcastillayleon.es/10.1073/pnas.1708729114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. King CH, Sutherland LJ, Bertsch D. Systematic review and meta-analysis of the impact of chemical-based mollusciciding for control of Schistosoma mansoni and S. haematobium transmission. PLoS Negl Trop Dis. 2015;9:e0004290. https://doiorg.publicaciones.saludcastillayleon.es/10.1371/journal.pntd.0004290.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Augusto G, Magnussen P, Kristensen TK, Appleton CC, Vennervald BJ. The influence of transmission season on parasitological cure rates and intensity of infection after praziquantel treatment of Schistosoma haematobium-infected schoolchildren in Mozambique. Parasitology. 2009;136:1771–9. https://doiorg.publicaciones.saludcastillayleon.es/10.1017/S0031182009006210.

    Article  CAS  PubMed  Google Scholar 

  31. Huang Q, Gurarie D, Ndeffo-Mbah M, Li E, King CH. Schistosoma transmission in a dynamic seasonal environment and its impact on the effectiveness of disease control. J Infect Dis. 2020;225:1050–61. https://doiorg.publicaciones.saludcastillayleon.es/10.1093/infdis/jiaa746.

    Article  PubMed Central  Google Scholar 

  32. Sturrock R, Barnish G, Upatham ES. Snail findings from an experimental mollusciciding programme to control Schistosoma mansoni transmission on St. Lucia. Int J Parasitol. 1974;4:231–40. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/0020-7519(74)90079-4.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to the shehas for their collaboration and support of the SchistoBreak study, for indicating the water bodies in the communities, for helpful discussions, and for advice on local conditions. We express our gratitude to the community members who welcomed us and provided valuable and important information about the water bodies in their area. We are indebted to all SchistoBreak study team members from the PHL-IdC and the Neglected Tropical Diseases Programme for their great support in implementing the project activities. We profoundly thank the Bayer AG Crop Science Division in Monheim, Germany, for donating niclosamide and regularly monitoring its activity, which has been fundamental for the implementation of snail control interventions in our study.

Funding

Funding for the study has been obtained from the Swiss National Science Foundation (SNSF; Bern, Switzerland) via a PRIMA Grant (PR00P3_179753) of Stefanie Knopp. This funding source had no role in the design and execution of this study, analyses and interpretation of the data, or decision to submit the manuscript for publication.

Author information

Authors and Affiliations

  1. Swiss Tropical and Public Health Institute, Allschwil, Switzerland

    Lydia Trippler, Jan Hattendorf & Stefanie Knopp

  2. University of Basel, Basel, Switzerland

    Lydia Trippler, Jan Hattendorf & Stefanie Knopp

  3. Public Health Laboratory-Ivo de Carneri, Chake-Chake, Pemba, United Republic of Tanzania

    Said Mohammed Ali, Amour Khamis Amour & Khamis Rashid Suleiman

  4. Department of Preventive Services and Health Education, Zanzibar Ministry of Health, Chake-Chake, Pemba, United Republic of Tanzania

    Msanif Othman Masoud

  5. Neglected Diseases Program, Zanzibar Ministry of Health, Chake-Chake, Pemba, United Republic of Tanzania

    Zahor Hamad Mohammed

  6. Neglected Diseases Program, Zanzibar Ministry of Health, Zanzibar Town, Unguja, United Republic of Tanzania

    Shaali Makame Ame & Fatma Kabole

Authors
  1. Lydia Trippler
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Said Mohammed Ali
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Msanif Othman Masoud
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Zahor Hamad Mohammed
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Amour Khamis Amour
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Khamis Rashid Suleiman
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. Shaali Makame Ame
    View author publications

    You can also search for this author inPubMed Google Scholar

  8. Fatma Kabole
    View author publications

    You can also search for this author inPubMed Google Scholar

  9. Jan Hattendorf
    View author publications

    You can also search for this author inPubMed Google Scholar

  10. Stefanie Knopp
    View author publications

    You can also search for this author inPubMed Google Scholar

Contributions

S.K. acquired the funding for the SchistoBreak study. L.T., Sa.M.A., J.H., and S.K. conceptualized the SchistoBreak study. Sa.M.A. and S.K. initiated the SchistoBreak study. L.T. and S.K. performed the data curation. L.T. conducted the formal analysis and data visualization for the research article. M.O.M., Z.H.M., A.H.A., and K.R.S. contributed significantly to the data collection at water bodies and snail control. K.R.S. examined snails for cercariae shedding. L.T., J.H., and S.K. conceptualized the statistical methods of the study. L.T., Sa.M.A., Sh.M.A., F.K., and S.K. were responsible for the management of the research activity planning. L.T., Sa.M.A., Sh.M.A., and S.K. mentored the core team, and M.O.M., Z.H.M., A.H.A., K.R.S., Sa.M.A., Sh.M.A., and F.K. advised regarding local conditions. L.T. and S.K. drafted the first version of the research article. All authors made substantial contributions to the study, and reviewed and approved the submitted version of the manuscript.

Corresponding author

Correspondence to Stefanie Knopp.

Ethics declarations

Ethics approval and consent to participate

The SchistoBreak study protocol was waived by the ethics committee in Switzerland (Ethikkommission Nordwest- und Zentralschweiz; EKNZ) on 23 October 2019 (Req-2019-00951). It subsequently received annual ethical approval by the Zanzibar Health Research Institute (ZAHRI). The first approval was given on 13 December 2019 (ZAHREC/03/PR/December/2019/12), and the latest approval was given on 31 March 2023 (ZAHREC/04/AMEND/MARCH/2023/03). The study was registered prospectively at ISRCTN (ISCRCTN91431493). At the beginning of each annual intervention period, the leaders of the IUs (shehas) were invited to meetings at the PHL-IdC. In the meetings, updates on the SchistoBreak study results were presented. Moreover, challenges of surveys and interventions were discussed and concerns addressed, and the shehas were invited to support the project by announcing the forthcoming activities in their communities.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

13071_2024_6565_MOESM1_ESM.pdf

Supplementary Material 1: Table 1: Environmental factors associated with Bulinus presence in water bodies in the north of Pemba, Tanzania (PDF).

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Trippler, L., Ali, S.M., Masoud, M.O. et al. Impact of chemical snail control on intermediate host snail populations for urogenital schistosomiasis elimination in Pemba, Tanzania: findings of a 3-year intervention study. Parasites Vectors 17, 489 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13071-024-06565-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13071-024-06565-2

Keywords

Parasites & Vectors

ISSN: 1756-3305

Contact us