Spatio-temporal variability in transmission risk of human schistosomes and animal trematodes in a seasonally desiccating East African landscape.

Different populations of hosts and parasites experience distinct seasonality in environmental factors, depending on local-scale biotic and abiotic factors. This can lead to highly heterogeneous disease outcomes across host ranges. Variable seasonality characterizes urogenital schistosomiasis, a neglected tropical disease caused by parasitic trematodes (Schistosoma haematobium). Their intermediate hosts are aquatic Bulinus snails that are highly adapted to extreme rainfall seasonality, undergoing prolonged dormancy yearly. While Bulinus snails have a remarkable capacity for rebounding following dormancy, we investigated the extent to which parasite survival within snails is diminished. We conducted an investigation of seasonal snail schistosome dynamics in 109 ponds of variable ephemerality in Tanzania from August 2021 to July 2022. First, we found that ponds have two synchronized peaks of schistosome infection prevalence and observed cercariae, though of lower magnitude in the fully desiccating than non-desiccating ponds. Second, we evaluated total yearly schistosome prevalence across an ephemerality gradient, finding ponds with intermediate ephemerality to have the highest infection rates. We also investigated dynamics of non-schistosome trematodes, which lacked synonymity with schistosome patterns. We found peak schistosome transmission risk at intermediate pond ephemerality, thus the impacts of anticipated increases in landscape desiccation could result in increases or decreases in transmission risk with global change.

Spatiotemporal variability in transmission risk of human schistosomes and animal trematodes in a seasonally desiccating East African landscape.

Different populations of hosts and parasites experience distinct seasonality in environmental factors, depending on local-scale biotic and abiotic factors. This can lead to highly heterogenous disease outcomes across host ranges. Variable seasonality characterizes urogenital schistosomiasis, a neglected tropical disease caused by parasitic trematodes (Schistosoma haematobium). Their intermediate hosts are aquatic Bulinus snails that are highly adapted to extreme rainfall seasonality, undergoing dormancy for up to seven months yearly. While Bulinus snails have a remarkable capacity for rebounding following dormancy, parasite survival within snails is greatly diminished. We conducted a year-round investigation of seasonal snail-schistosome dynamics in 109 ponds of variable ephemerality in Tanzania. First, we found that ponds have two synchronized peaks of schistosome infection prevalence and cercariae release, though of lower magnitude in the fully desiccating ponds than non-desiccating ponds. Second, we evaluated total yearly prevalence across a gradient of an ephemerality, finding ponds with intermediate ephemerality to have the highest infection rates. We also investigated dynamics of non-schistosome trematodes, which lacked synonymity with schistosome patterns. We found peak schistosome transmission risk at intermediate pond ephemerality, thus the impacts of anticipated increases in landscape desiccation could result in increases or decreases in transmission risk with global change.

Test-Treat-Track-Test-Treat Strategy for Control of Schistosomiasis in Two Low-Prevalence Villages in Northwestern Tanzania.

Mass drug administration of praziquantel becomes a less attractive strategy for elimination of schistosomiasis in low-prevalence areas due to cost implications and low treatment compliance. We aimed to determine the feasibility of a Test-Treat-Track-Test-Treat (5T) strategy in two low-prevalence villages; the 5T strategy has been successfully implemented in diseases such as malaria. A total of 200 school children aged 6-12 years were randomly selected from two schools and tested for Schistosoma mansoni infection using the point-of-care circulating cathodic antigen test. Schistosoma mansoni-positive children, referred to as first-generation cases (FGCs), were tracked and treated including up to five members of their families. Second-generation cases, identified by the FGCs as their close, non-relative contacts, were also tracked, tested, and treated, including up to five members of their families. The prevalence of schistosomiasis among screened FGCs was 16.5% (33/200) in both villages. Twenty-four FGCs were included in the study. Prevalence among 94 contacts of FGCs was 46.8% (44/94). The proportion was higher in Muda than Bulunga village (61.2% versus 31.1%, χ2 = 10.6611, P = 0.005). Prevalence among SGCs and their contacts was 37.5% (9/24) and 47.1% (49/104), respectively. Overall, the 5T strategy identified 102 additional cases out of 222 tracked from FGCs, 95% of whom were treated, at a total time of 52 hours. Our data demonstrate the potential of the 5T strategy in identifying and treating additional cases in the community and hence its practicality in schistosomiasis control in low-prevalence settings at relatively low time and resources investment.

A novel theatre-based behaviour change approach for influencing community uptake of schistosomiasis control measures.

BACKGROUND: Appropriate behaviour change with regard to safe water contact practices will facilitate the elimination of schistosomiasis as a public health concern. Various approaches to effecting this change have been trialled in the field but with limited sustainable outcomes. Our case study assessed the effectiveness of a novel theatre-based behaviour change technique (BCT), in combination with cohort awareness raising and capacity training intervention workshops. METHODOLOGY: Our study was carried out in four rural communities in the Mwanza region of Tanzania and in the semi-urban town of Kemise, Ethiopia. We adapted the Risk, Attitude, Norms, Ability and Self-regulation (RANAS) framework and four phases using a mixed methods approach. Participatory project phase engagement and qualitative formative data were used to guide the design of an acceptable, holistic intervention. Initial baseline (BL) data were collected using quantitative questionnaire surveys with 804 participants in Tanzania and 617 in Ethiopia, followed by the theatre-based BCT and capacity training intervention workshops. A post-intervention (PI) survey was carried out after 6 months, with a participant return rate of 65% in Tanzania and 60% in Ethiopia. RESULTS: The intervention achieved a significant improvement in the knowledge of schistosomiasis transmission being associated with poorly managed sanitation and risky water contact. Participants in Tanzania increased their uptake of preventive chemotherapy (males: BL, 56%; PI, 73%, females: BL, 43%; PI, 50%). There was a significant increase in the selection of sanitation (Tanzania: BL, 13%; PI, 21%, Ethiopia: BL, 63%; PI, 90%), safe water and avoiding/minimising contact with infested waters as prevention methods in Tanzania and Ethiopia. Some of the participants in Tanzania followed on from the study by building their own latrines. CONCLUSIONS: This study showed that substantial positive behaviour changes in schistosomiasis control can be achieved using theatre-based BCT intervention and disease awareness training. With the appropriate sensitisation, education and stakeholder engagement approaches, community members were more open to minimising risk-associated contact with contaminated water sources and were mobilised to implement preventive measures.

Transmission potential of human schistosomes can be driven by resource competition among snail intermediate hosts.

Predicting and disrupting transmission of human parasites from wildlife hosts or vectors remains challenging because ecological interactions can influence their epidemiological traits. Human schistosomes, parasitic flatworms that cycle between freshwater snails and humans, typify this challenge. Human exposure risk, given water contact, is driven by the production of free-living cercariae by snail populations. Conventional epidemiological models and management focus on the density of infected snails under the assumption that all snails are equally infectious. However, individual-level experiments contradict this assumption, showing increased production of schistosome cercariae with greater access to food resources. We built bioenergetics theory to predict how resource competition among snails drives the temporal dynamics of transmission potential to humans and tested these predictions with experimental epidemics and demonstrated consistency with field observations. This resource-explicit approach predicted an intense pulse of transmission potential when snail populations grow from low densities, i.e., when per capita access to resources is greatest, due to the resource-dependence of cercarial production. The experiment confirmed this prediction, identifying a strong effect of infected host size and the biomass of competitors on per capita cercarial production. A field survey of 109 waterbodies also found that per capita cercarial production decreased as competitor biomass increased. Further quantification of snail densities, sizes, cercarial production, and resources in diverse transmission sites is needed to assess the epidemiological importance of resource competition and support snail-based disruption of schistosome transmission. More broadly, this work illustrates how resource competition can sever the correspondence between infectious host density and transmission potential.

Village Response to Mass Drug Administration for Schistosomiasis in Mwanza Region, Northwestern Tanzania: Are We Missing Socioeconomic, Cultural, and Political Dimensions?

Praziquantel (PZQ)-based mass drug administration (MDA) is the main approach for controlling schistosomiasis in endemic areas. Interventions such as provision and use of clean and safe water, minimizing contacts with infested water, disposal of human waste in latrines, and snail control provide additional key interventions to break the transmission cycle and could complement and perhaps sustain the benefits of MDA. However, all interventions deployed need to be accepted by the targeted communities. A qualitative study was conducted to examine factors that might differentiate villages which did not show a substantial decrease in Schistosoma mansoni prevalence despite repeated, high treatment coverage referred to as "persistent hotspot (PHS) villages" from villages which showed a substantial decrease in prevalence referred to as "responding (RES) villages." A convenient sample of adults was drawn from eight villages. Thirty-nine key informants were interviewed and 16 focus groups were held with a total of 123 participants. Data were analyzed manually using a thematic content approach. In both PHS and RES villages, schistosomiasis was not considered to be a priority health problem because of its chronic nature, lack of knowledge and awareness, and poverty among study communities. Persistent hotspot villages exhibited poor leadership style, lack of or insufficient social engagement, little or lack of genuine community participation, little motivation, and commitment to schistosomiasis control compared with RES villages where there were commitment and motivation to fight schistosomiasis. We support the view of scholars who advocate for the adoption of a biosocial approach for effective and sustainable PZQ-based MDA for schistosomiasis control.

Community knowledge, perceptions and water contact practices associated with transmission of urinary schistosomiasis in an endemic region: a qualitative cross-sectional study.

BACKGROUND: In an effort to complement the current chemotherapy based schistosomiasis control interventions in Shinyanga district, community knowledge, perceptions and water contact practices were qualitatively assessed using focus group discussions and semi structured interviews involving 271 participants in one S. haematobium prevalent community of Ikingwamanoti village, Shinyanga district, Northwestern, Tanzania. METHODS: In October, 2016 we conducted 29 parent semi structured interviews and 16 focus group discussions with a total of 168 parent informants. Adult participants were conveniently selected from three sub-villages of Butini, Miyu, and Bomani of Ikingwamanoti village, Shinyanga district. In March, 2017, a total of 103 children informants participated in 10 focus group discussions and 20 semi structured interviews, administered to children from standard four, five, six and seven attending Ikingwamanoti Primary School. Note taking and digital recorders were used to collect narrative data for thematic analysis of emergent themes. RESULTS: Among participants, 75% parents and 50% children considered urinary schistosomiasis as a low priority health problem. Of the informants, 70% children and 48.3% parents had misconceptions about the cause, modes of transmission and control of schistosomiasis demonstrating gaps in their biomedical knowledge of the disease. Assessment of treatment seeking behavior for urinary schistosomiasis revealed a combination of traditional and modern health care sectors. However, modern medicines were considered effective in the treatment of urinary schistosomiasis. Lack of alternative sources of water for domestic and recreational activities and unhygienic water use habits exposed community members to high risk of acquiring urinary schistosomiasis. CONCLUSION: Use of Schistosoma haematobium contaminated water sources for daily domestic and recreational use facilitated contraction of urinary schistosomiasis among community members in Shinyanga district. People's perceptions of urinary schistosomiasis as a less priority health problem promoted persistence of the disease. Future efforts to control urinary schistosomiasis should take into account integrated approaches combining water, sanitation and hygiene, health education, alternative sources of clean and safe water to facilitate behavior change.

Geographical and behavioral risks associated with Schistosoma haematobium infection in an area of complex transmission.

BACKGROUND: Schistosoma haematobium infection in endemic areas varies depending on the nature and complexity of the transmission networks present. Studies of micro-geographical transmission of S. haematobium infection indicate that discrepancy in prevalence between households is associated with diverse water contact behaviors and transmission that is restricted to particular sites harboring snail intermediate hosts. Detection of variations in the transmission sources with complex transmission networks of water bodies is required for optimization of malacological control. Longitudinal parasitological and malacological surveys were conducted to investigate geographical variations in transmission of urogenital schistosomiasis in Ikingwamanoti village, Shinyanga District, Tanzania. METHODS: Urine samples were collected at baseline and follow-up time points from 282 school-aged children and examined microscopically for the presence of S. haematobium eggs. Malacological surveys involved collection of Bulinus nasutus every month from 30 sites. Snails were examined for patent infections. Global positioning system was used to map household distances from S. haematobium transmission sites, while water contact behavior was assessed using a questionnaire. RESULTS: Schistosoma haematobium infection was observed to be prevalent among older children (12-14 years) compared to younger groups prior to treatment, but no significant difference in infection prevalence was observed at one-year. Boys were highly infected than girls at both time points. No spatial influence was observed between children's infection and the distance from child's residence to the nearby snail habitats nor was any significant association observed between children's reported water contact behavior with S. haematobium infection. However, malacological surveys with cercarial shedding combined with GPS data detected significant variation among different water sources in the transmission of S. haematobium with children living in households near to ponds with high B. nasutus populations having the highest prevalence of infection. CONCLUSIONS: Interaction between malacological surveys with cercarial shedding combined with GPS mapping in endemic settings can help detection of transmission sources even in areas with complex transmission networks. Subsequent studies are needed to determine whether the combination of GPS mapping and parasitology screens can aid the detection of transmission hotspots across varied transmission settings to enhance schistosomiasis control programmes.

The Efficacy of Single-Dose versus Double-Dose Praziquantel Treatments on Schistosoma mansoni Infections: Its Implication on Undernutrition and Anaemia among Primary Schoolchildren in Two On-Shore Communities, Northwestern Tanzania.

Administering more than one treatment may increase Praziquantel cure and egg reduction rates, thereby hastening achievement of schistosomiasis transmission control. A total of 431 S. mansoni-infected schoolchildren were randomized to receive either a single or repeated 40 mg/kg Praziquantel dose. Heights, weights, and haemoglobin levels were determined using a stadiometer, weighing scale, and HemoCue, respectively. At 8 weeks, cure rate was higher on repeated dose (93.10%) compared to single dose (68.68%) (p < 0.001). The egg reduction rate was higher on repeated dose (97.54%) compared to single dose (87.27%) (p = 0.0062). Geometric mean egg intensity was lower among those on repeated dose (1.30 epg) compared to single dose (3.18 epg) (p = 0.036) but not at 5 (p > 0.05) and 8 (p > 0.05) months with no difference in reinfection rate. No difference in the prevalence of stunting was observed between the two treatment regimens (p > 0.05) at 8 months, but there was an increase in the prevalence of wasting among those on repeated dose (p < 0.001). There was an increase in the mean haemoglobin levels at 8 months with no difference between the two arms (p > 0.05). To achieve reduction of transmission intensity and disease control in highly endemic areas, repeated treatments alone may not be sufficient. This trial was registered with PACTR201601001416338.

Coinfection of intestinal schistosomiasis and malaria and association with haemoglobin levels and nutritional status in school children in Mara region, Northwestern Tanzania: a cross-sectional exploratory study.

BACKGROUND: Schistosomiasis represents a major public health problem in Tanzania despite ongoing national control efforts. This study examined whether intestinal schistosomiasis is associated with malaria and assessed the contribution of intestinal schistosomiasis and malaria on anaemia and undernutrition in school children in Mara region, North-western Tanzania. METHODS: Stool samples were collected from each of 928 school children randomly selected from 5 schools and examined for intestinal schistosomiasis using the Kato Katz method. Finger prick blood samples were collected and examined for malaria parasites and haemoglobin concentrations using the Giemsa stain and Haemocue methods, respectively. Nutritional status was assessed by taking anthropometric measurements. RESULTS: The overall prevalence and infection intensity of S. mansoni was 85.6% (794/928) and 192 (100-278), respectively. The prevalence of malaria was 27.4% (254/928) with significant differences among villages (χ 2  = 96.11, p < 0.001). The prevalence of anaemia was 42.3% (392/928) with significant differences among villages (χ 2  = 39.61, p < 0.001). The prevalence of stunting, thinness and underweight was 21, 6.8 and 1.3%, respectively. Stunting varied significantly by sex (χ 2  = 267.8, p < 0.001), age group (χ 2  = 96.4, p < 0.001) and by village (χ 2  = 20.5, p < 0.001). Out of the 825 infected children, 217 (26.4%) had multiple parasite infections (two to three parasites). The prevalence of co-infections occurred more frequently in boys than in girls (χ 2  = 21.65, p = 0.010). Mean haemoglobin concentrations for co-infected children was significantly lower than that of children not co-infected (115.2 vs 119.6; t = 0.01, p = 0.002). Co-infected children were more likely to be stunted than children who were not co-infected (χ 2  = 11.6, p = 0.003). On multivariate analysis, age group, village of residence and severe anaemia were significant predictors of stunting after adjusting for sex and infection status. CONCLUSIONS: Intestinal schistosomiasis and malaria are prevalent in Mara region. Coinfections of these parasites as well as chronic undernutrition were also common. We recommend Mara region to be included in national schistosomiasis control programmes.

Knowledge, attitude, and practices on intestinal schistosomiasis among primary schoolchildren in the Lake Victoria basin, Rorya District, north-western Tanzania.

BACKGROUND: Globally school-age children, adolescents and young adults bear the highest burden of schistosomiasis. When developing a specific intervention to improve community's knowledge, attitudes, and practices (KAPs), existing KAPs must be taken into account. Therefore, this study was designed to determine schoolchildren's KAPs on schistosomiasis in the study area. METHODS: A cross-sectional study was conducted in Busanga and Kibuyi villages involving 513 schoolchildren. A pre-tested questionnaire was used to collect socio-demographic data and to assess KAP on schistosomiasis among primary schoolchildren in the study area. RESULTS: Of the 488 interviewed children, 391 (80.12%) reported to have heard of schistosomiasis, with the majority 289 (73.91%) citing school as the source of this knowledge. Swimming in the lake, worms, witchcraft, and mosquitoes were mentioned to be the cause for intestinal schistosomiasis. Fishing in the lake, drinking unboiled lake water, walking bare footed, and shaking hands were reported to be practices that may lead to contracting schistosomiasis. Only 156 (39.90%) of the study respondents reported to know the signs of intestinal schistosomiasis. Avoiding swimming in the lake, drinking unboiled water and eating unwashed fruits were mentioned as preventive measures. Nearly 85% (412) reported understanding that there was a disease known as schistosomiasis; additionally, 419 (85.86%) considered schistosomiasis as a dangerous disease and 418 (85.66%) believed that schistosomiasis was treatable. Fishermen and schoolchildren were reported to be groups most at risk of schistosomiasis infection. Visiting the lake (for swimming and other gatherings) was a common practice among study participants 471 (96.52%).Nearly 93% (451) of participants mentioned using lake water for domestic chores, and, although 407 (84.61%) reported to own a toilet at home, only 229 (55.31%) reported to always use a toilet for sanitation purposes. CONCLUSION AND RECOMMENDATION: Despite a high rate of awareness among schoolchildren regarding schistosomiasis, there was a persistent gap amongst the children regarding the causes, modes of transmission, symptoms, and preventive measures for the disease. Therefore, an appropriate health education intervention is needed in order to inculcate better knowledge, attitudes, and practices amongst schoolchildren regarding its transmission, control, and prevention as part of a successful schistosomiasis campaign.

Longitudinal survey on the distribution of Biomphalaria sudanica and B. choanomophala in Mwanza region, on the shores of Lake Victoria, Tanzania: implications for schistosomiasis transmission and control.

BACKGROUND: Schistosomiasis is hyper-endemic in the Lake Victoria basin; with intestinal schistosomiasis plaguing communities adjacent to the lake, where the intermediate host snails live. The two intermediate host species of Schistosoma mansoni in the Mwanza region are Biomphalaria sudanica, found on the banks of the lakes, and B. choanomphala, found in the lake itself. There are few longitudinal surveys documenting changing abundance and differential transmission patterns of these Biomphalaria snails across seasons and years. We undertook 15 field surveys at 26 sites over four years to determine the parameters that influence Biomphalaria abundance, presence of S. mansoni-shedding snails and impact of schistosomiasis treatment interventions on transmission potential in the Mwanza region. RESULTS: Statistical analysis revealed seasonal difference in the abundance of B. sudanica with the highest number of snails found in the dry season (Kruskal-Wallis χ 2 = 37.231, df = 3, P < 0.0001). Water measurements were not associated with B. sudanica abundance; however, high levels of rainfall did have a negative effect on B. sudanica [coefficient effect -0.1405, 95% CI (-0.2666, -0.0144)] and B. choanomphala abundance [coefficient effect -0.4388, 95% CI (-0.8546, -0.0231)] potentially due to inundation of sites "diluting" the snails and influencing collection outcome. Biomphalaria sudanica snails were found at all sites whereas B. choanomphala were far more focal and only found in certain sites. Shedding Biomphalaria did not show any variation between dry and rainy seasons; however, a decrease in shedding snails was observed in year 4 of the study. CONCLUSIONS: Biomphalaria sudanica is uniformly present in the Mwanza region whereas B. choanomphala is far more focal. Seasonality plays a role for B. sudanica abundance, likely due to its habitat preference on the banks of the lake, but not for B. choanomphala. The decrease in shedding Biomphalaria abundance in Year 4 could be linked to ongoing schistosomiasis treatment efforts in the neighbouring human populations. The highest number of shedding Biomphalaria was observed at sites with high levels of human movement. Prioritising snail control at such sites could greatly reduce transmission in these high-risk areas.