Introduction

Schistosomiasis, caused by trematode worms of the genus Schistosoma, is one of the neglected tropical diseases (NTDs); a group of infections that disproportionately affect low-income populations. It remains a major public health problem in tropical and subtropical regions with an estimated 220 million people infected [1,2]. Transmission occurs through contact with water that has been contaminated with faeces or urine containing parasite eggs, and in which intermediate snail hosts breed. The urogenital or gastrointestinal tracts are impacted depending on the infecting species. Infection is associated with non-specific morbidities such as anaemia, growth retardation, and impairment of cognitive development, thus can lead to reduced work capacity; whilst long-term exposure to infection is associated with specific severe morbidities that can be fatal [3]. In sub-Saharan Africa, schistosomiasis is common, particularly in low—income areas without access to safe drinking water and adequate sanitation. At least 90% of those in need of schistosomiasis treatment are living in Africa [4].

Interventions to control schistosomiasis have varied over time and space. Early national control programmes, such as the Sudanese Blue Nile Health Project (started in 1979) and the Egyptian national programme (started in 1988), used a combination of chemotherapy, snail control, provision of clean water and sanitation, and infrastructural development [5,6]. Such multi-approach control programmes are now the exception rather than the rule [7], though the latest edition of the WHO roadmap for control of NTDs emphasises the need to return to multi-approach programmes [8]. Instead, due to the combined low cost, good safety record and high efficacy of the anti-schistosomal drug praziquantel (PZQ), preventative chemotherapy (PC) through mass drug administration (MDA) on a population scale became the mainstay of internationally funded national schistosomiasis control programmes. The WHO originally set a 2025 target for these PC programmes of schistosomiasis morbidity control (defined as <5% of school-aged children (SAC) having a heavy infection), followed by eradication as a public health burden where possible [8]. This has since been revised in the latest Roadmap for NTD control to elimination of schistosomiasis as a public health problem (defined as <1% of SAC having a heavy infection), in all endemic countries by 2030 [1]. However, schistosomiasis elimination efforts have rarely succeeded and only in relatively isolated situations [7]. Elimination requires extensive (and by extension expensive) integrated approaches, and when not feasible, the tools available have to be optimal to gain the greatest outcomes [9]. The elements that result in optimal tools are often not appreciated, hence the need for medical anthropological studies to improve understanding of programme limitations.

PC interventions involve a variety of elements relating to the target population, the drug to be used and the organisations implementing the intervention. These include population sensitisation, drug procurement and distribution, reporting accuracy and varying involvement of international partners, national government Ministries of Health and Education, and local government and community structures. The interactions of these elements cut across different spheres of influence (from international to local), resulting in non-linear effects on outcomes and a wide range of circumstances may have an impact on the results. In addition, several operational strategies for drug delivery can be adopted depending on the endemicity and national policies. These include variation in platform (school- or community-based), target groups (SAC or SAC alongside adults) and frequency (year or biennially). Given the complexity in PC programme design and implementation, identifying the barriers and facilitators that affect programmes’ ability to meet recommended targets is difficult.

Despite, the complexity, since its internationally supported inception in 2003, MDA using PZQ has led to substantial country-level success in attainment towards the original 2025 goals [10–12]. However, regardless of several years of well-implemented MDA coverage, variation in transmission, at times as focal as an individual village, can result in failure to substantially decrease prevalence and mean intensity of schistosomiasis infections at the micro-geographical level [13,14]. Precision mapping or research studies are required to detect these village-to-village differences and precise characterisation of a “hotspot” needs to be applied to understand why some villages fail to decline in their infection status. Only with this understanding can determination of whether enhanced MDA efforts alone will suffice or whether additional control measures will be required in individual areas [14].

In Uganda, MDA began in 2003 through the support of the Schistosomiasis Control Initiative (SCI; now Unlimit Health), and 400,000 PZQ treatments were distributed that year [15–17]. Subsequently, treatment coverage increased each following year with 1.8 million individuals treated by 2007 [18], resulting in significant reductions in S. mansoni prevalence, intensity, and associated morbidity [12,19]. Other countries employing MDA have reported similar successes [20]. As a result of these findings, WHO’s strategy for disease control in some African nations, including Uganda, has been updated to include the interruption of transmission by 2030 [21]. In common with other countries Uganda has areas of continued high schistosomiasis transmission or hotspots; and contributing to this continued high transmission could be coverage rates of the programme in these areas. Social factors are likely amongst those that play an important role in MDA uptake. An individual’s positioning in the community’s social network, trust in the community drug distributors (CDDs) for health advice [22], and engagement by the community leaders [23] have all been noted amongst facilitating factors. On the other hand, poor leadership, insufficient social engagement, lack of genuine community participation, low motivation by the CDDs and their commitment to schistosomiasis control [23], and the side effects associated with PZQ [24,25] are reported inhibitors of treatment uptake. To be able to avert the barriers while promoting facilitating factors in these persistent schistosomiasis hotspots, an understanding of what the local barriers and facilitators are and what causes them is required. The aim of the current paper is to investigate these barriers and facilitators of MDA, specifically in persistent hotspots along Lake Albert, Uganda.

Materials and methods

Results

Facilitators of mass drug adminstation

Barriers to mass drug administration

Discussion

The three high S. mansoni endemicity sub-counties of Buseruka, Kabaale and Kigorobya, are situated in Hoima District, Western Uganda which has a long Lake Albert shoreline. This geography, combined with the socio-ecological interactions between the lake shore communities and the lake itself, results in this area being one of the most significant hotspots of schistosomiasis transmission globally. To determine the influence of social factors in participation in the control programme, this study examined the barriers and facilitators of MDA within these communities.

As for the facilitating factors, study participants commonly reported that they had been sensitised on the dangers of the disease (schistosomiasis) and PZQ as a drug that is effective in treating schistosomiasis and they were aware of the MDA programme and its purpose. This compelled them to participate in MDA because they wanted to get cured and live in good health. We additionally found that those who suspected having been infected, or those with symptoms of schistosomiasis participated in treatment to a higher degree. Additionally, participants knew that receiving no treatment can lead to death, and therefore such fears compelled them to participate. Participants reported that they wanted to continue with the drug because they were aware of the risks when still exposed to lake waters and by extension to the disease; thus, the preventative rather than curative benefits of participation were also understood. Several studies from elsewhere in Uganda also reveal that the lived experience of the health benefits of treatment and of knowing others who have had improved health after taking PZQ, leads to MDA uptake [18,24,36]. At the same time, quantitative analysis has shown that knowledge of the disease is a positive predictor of treatment [37] and systematic review of the factors affecting the uptake of preventive chemotherapy treatment for schistosomiasis in sub-Saharan Africa also revealed that people participate in PC programmes as a result of their knowledge and awareness of the signs, effects, and transmission cycle of schistosomiasis [3]. Together these findings highlight that health communication regarding the disease is vital for strong uptake of PC.

People also participated in MDA programmes because they were encouraged and registered by the CDDs/VHTs who visit homes to carry out sensitisation and encourage participation. The significant role played by CDDs in sensitising the communities is in line with the findings of Corley et al. [38] and Krentel et al. [39], who highlight CDDs as a “valuable human resource” in the motivation and education of communities, promoting the sustainable uptake of NTD activities. Krentel et al. went on to recommend the recognition of CDD contribution by programme managers, whilst acknowledging that non-performance in volunteer roles can also inhibit programmatic achievements [39]. Fleming et al. [40] also cite positive and negative influence of these volunteers on programmatic outcomes in the Ugandan districts of Kamuli, Pallisa, Mukono, and Yumbe. For instance, positive influence was seen through their participation in sensitisation and mobilisation campaigns, treatment and writing of coverage reports based on their treatment register. On the other hand, lack of availability, capacity, acceptance, and, indeed, ownership of the programme by the CDDs led to negative outcomes. Similar findings have been reported from the other East African countries of Rwanda [41] and Tanzania [42]. Our participants further reported that it was not only that the CDDs/VHTs provided information, but that they knew the people who distributed the medicine and placed importance on this. In Kagadi and Ntoroko Districts on the southern shores of Lake Albert CDDs/VHTs are the primary health seeking point of contact for schistosomiasis, inferring trust is held in them [43], whilst in Mayuge District, Uganda a direct tie (close friendship) between CDDs and community members was associated with enhanced treatment uptake [22]. These findings resonate with those of our study; emphasising the need for CDDs to be picked from those well-connected within the community. The delivery of the drug at home by the CDDs, free of charge, as a facilitator was also a key finding.

When it comes to the inhibiting factors, we found out that participants commonly reported that people feared the nasty side effects of PZQ; a well reported barrier to the uptake of treatment [37,44,45]. In the Ugandan context, this barrier has been found both qualitatively [46] and quantitatively [37]. Unlike our study, which involved youth and adults, both these studies involved children and adults as their target respondents and so age-related influences cannot be ruled out as a reason for differences in the influence of side-effects on uptake. In particular, in our study, the benefits of treatment were found to outweigh the fear of these side effects for many participants, and in fact, many linked these side effects to the strength and effectiveness of the drug.

Although women are more likely to take part, worries during pregnancy can be an inhibitory factor. Pregnant women were reportedly not participating because they were worried that the drug caused abortion or affected them in some other way. They also reported that they were informed not to participate. WHO has indicated that pregnancy is often cited as a reason for non-compliance [47], potentially resulting from the ineligibility of pregnant and lactating women in the early years of the programme; a recommendation which has since been reversed for those beyond the first trimester of pregnancy [48]. Reproductive and sexual fears amongst men through beliefs of the drug making them either infertile or impotent were also reported. The same unfounded fear was noted in Mayuge District, Uganda [44] and Morogoro, Tanzania [49]. If such misconceptions are not addressed it can drastically limit the uptake of PC.

Some people were reported to be ignorant about the programme, especially the Congolese migrants. For a group such as these, there is a need for effective communication and community engagement to ensure compliance with MDA and other treatment measures [50]. We found that because of the protracted insecurity in the DRC, most of the Congolese migrants in this study were new or recent arrivals. Parker et al [24] previously reported a great deal of distrust and antipathy between some locals and migrants in Nebbi District, north-western Uganda, which presents additional communication and community engagement challenges. As a result, some community members miss out on health education and mobilisation, leading to a lack of or inadequate knowledge about MDA. Such lack of or inadequate knowledge among the migrant population has been reported in other studies, as highlighted by the systematic review of knowledge, attitudes, and practices related to schistosomiasis in sub-Saharan Africa [51]. Cross-border movement and its negative impact on programmes occurs across health spheres that use an MDA approach [52], so its negative influence is likely be seen in other public health programmes being implemented in these communities.

Another reason for poor mobilisation was information concerning MDA implementation not reaching some people in the community due to their economic behaviours, in particular a fishing method called ‘salacio’ as practiced by some of the fishermen. The same finding was reported for fishing communities in Kagadi and Ntoroko Districts [43]. In a situation of this nature, Adriko et al. [37] in their study in Mayuge District, Uganda, suggest that improved educational campaigns and effective mobilization could increase health-seeking behaviour and improve community-wide MDA, even to such community members. A study by Coulibaly et al. [53] in Côte d’Ivoire supports these conclusions with findings that anytime was suitable for treatments if people were informed sufficiently in advance. Whilst in their systematic review, Torres Vitolas et al argue that there is a need to involve trusted local leaders with a reach to the sectors of communities missed during VHT and CDD mobilisation activities [54]. In response to their findings in Kagadi and Ntoroko Districts, Ayonlitho et al recommend strengthening the CDD/VHT structure to allow sustainable availability of PZQ for those who seek treatment outside of the control programme distribution window [43].

Some people did not participate because they knew they were not infected or they thought they were safe and not at risk of getting infected with schistosomiasis. Whilst the very old did not participate because they didn’t see the need as they have always lived in the area (and by extension with the disease). This overlaps with research from Zanzibar where people reported missing PZQ because they felt healthy [55] and is an example of interacting bio-social factors contributing to low drug coverages [37].

Concerning study limitations, the study did not coincide with the months for MDA, so corroboration through structured observation of how the benefits of treatment outweighed the fear of side effects was not possible. Secondly, we acknowledge that the duration spent on data collection (the six weeks of November to December) could have limited data collection from study participants who are subject to a migratory process. Equally important and related to migration, the study tools were only translated into two main local languages, Alur and Lunyoro, and interviews were conducted in English, Alur and Lunyoro. Thus, those who speak other minority languages present amongst these lakeshore communities may be missing amongst our participants due to a language barrier.

Conclusion and recommendations

Our research findings indicate a range of inhibiting and facilitating factors in the adherence to MDA. The inhibiting factors include, among others, social factors that have a contextual consequence on uptake, such as religious and political influence and positioning within the community that can lead to ignorance of the programme; but also factors directly related to the intervention, notably the side effects, size, taste and smell of the drug. However, facilitating factors such as knowledge of the severity of the disease, and the fact that people take their health seriously have greatly facilitated praziquantel uptake. Equally important, the localised, no cost availability of the drug, and the sensitisation and drug delivery by known individuals, combined with lived experience, either their own or of others, were perceived to outweigh the negative factors related to the drug and its side effects. Additionally, there is strong evidence that the participants had a very good understanding about why the side effects occur and their transitory nature and for the majority side-effects were not inhibitory to uptake of treatment.

Arising from the study findings we propose that more needs to be done to counter the unfounded rumours about the drug, and to reach those not receiving messaging regarding MDA from the CDDs. The findings highlight a need for continuous education and sensitisation on schistosomiasis causes, prevention and treatment to the community members; particularly given that most of them are mobile workers with occupations conducted at the lake. A good community engagement plan or strategy is important and should include the use of expert patients/champions/survivors, alongside local leaders and health workers to advocate for the drug and to encourage uptake in the community. Involvement of all stakeholders: district, village, traditional and religious leaders alongside the CDDs and VHTs in mobilising people for participation will be crucial. Sensitisation, recruitment, training and motivation of drug distributors from within the communities is also key. Finally, treatment supporters such as patient’s relatives, community volunteers working with the programme, medical workers, and pharmacists within the community among others could help to assuage fears of side effects and counter unfounded rumours to ensure greater uptake.

Supporting information

Acknowledgments

At the time of drafting this manuscript, the first author Mr. Paskari Odoi was a postgraduate student in Medical Anthropology at the Department of Sociology and Anthropology, School of Social Sciences, Makerere University. We are grateful for the support from the Department, as well as the implementation research team under the FibroScHot project. The authors would also like to acknowledge the contribution from the Hoima District Health Office and the community members of Kabaale, Buseruka and Kigorobya sub-counties, who were very supportive and ensured that this study was conducted without any significant challenges.