Treatment availability and capacity building
Uganda's National Control Programme for combating intestinal schistosomiasis and STHs has been active since 2003, and although regular monitoring has occurred at intervals since then, this is the first comprehensive overview of the status of treatment infrastructure and health capacity on the districts adjacent to Lake Victoria. The results here paint a mixed picture; on the one hand, some villages appear to function well in terms of drug availability, regular training of CMDs and administration of mass treatment. However, there were also locations, such as much of Wakiso district islands, where people were sceptical about the efficacy or need to take PZQ, while in Masaka district there was a noticeable absence of volunteers willing to take on the role of CMD. The reasons given for refusal included the distance between sites and the lack of adequate funding for travel. Even within a district with generally good treatment coverage, there were islands that did not conform to what was being observed elsewhere in the district. For example, on one island in Kalangala district, all inhabitants refused to take PZQ, citing experience of severe side-effects after swallowing the drugs during an earlier treatment campaign. High perceived risk of treatment has been associated with non-compliance with treatment in other studies , and so may limit the effectiveness of future treatment campaigns where side-effects have been noted. These heterogeneities in responses to treatment, added to the epidemiological variations seen across the region in terms of parasite prevalence, indicate the challenges to maintaining effective and efficient disease control. One limitation of this study was the lack of funding for follow-up visits to all of the communities surveyed in order to check up on the actions of the newly-trained CMDs and to see whether MDA was now being carried out more regularly.
High disease prevalence and observation of co-infection
The eastern part of Lake Victoria is known to be a highly endemic zone for intestinal schistosomiasis [5, 21]. In 2007, Masaka and Mpigi districts were added to the roster of districts receiving MDA, based on data showing increased disease levels as compared to the original 2003 baseline data . This current survey revealed that despite regular chemotherapy and educational interventions, levels of intestinal schistosomiasis are still very high. The only exception is Rakai district, which continues to have low, almost negligible, levels of S. mansoni. The data here also support earlier evidence of a geographical west to east cline along Uganda's Lake Victoria shoreline of increasing schistosomiasis prevalence, although the observation of significant local heterogeneities should be taken into consideration. The reasons for this purported cline are not fully understood, but may relate to climatic variation along the lakeshore, or indeed differences in population density or sanitation infrastructure. Large-scale variation in prevalence may be more a residue of sampling effort or treatment history, and indeed if given too much weight, may confound smaller-scale patterns of variation which are crucial for local disease management recommendations [23, 24].
The patterns of distributions of STH and malaria infections are less geographically skewed and more evenly distributed by district, but again, there are exceptions. Masaka district has significantly higher prevalence of T. trichiura infection than the overall average, for example. This is somewhat surprising, since all three STHs are successfully treated with albendazole, and prevalence of hookworm and A. lumbricoides are not noticeably elevated. One possibility is the observation of particularly poor sanitary and hygiene infrastructure in many locations along Masaka's Lake Victoria shoreline, encouraging STH transmission; if soil conditions here are more suitable for persistence of T. trichiura eggs than in other areas, this could go some way to explaining why the infection rate of this species of helminth is higher in Masaka than elsewhere. Indeed, a soil map of Uganda shows mineral hydropmorphic soils in Masaka district, and extending to Rakai, in contrast to ferrallitic soils along the rest of the Lake Victoria shoreline in Uganda .
In terms of malaria prevalence, Wakiso and Kalangala districts have significantly lower levels of Plasmodium spp. than the overall average. For the former, this may be due to the generally more urban environment of the district, as well as its proximity to cities such as Entebbe and Kampala, where health infrastructure is better. Kalangala is a rural and remote district with many islands and limited connectivity to health centres; therefore the lower malaria prevalence is likely due to environmental factors, such as unsuitable habitat for the mosquito vectors. Indeed, some environmental modeling work has shown that like intestinal schistosomiasis, malaria risk is predicted to be slightly lower in the western portions of Lake Victoria as opposed to the eastern [26, 27]. However, future surveys should also focus on training and education for behavioural control mechanisms such as bed net possession and insecticide use, neither of which was directly measured in this survey, to see whether these factors are contributing to the lower malarial prevalence observed in Kalangala.
The relatively high incidence of malaria and schistosomiasis co-infections, particularly in districts such as Bugiri and Jinja, was a very significant finding. Bugiri District also had high levels of co-infection of STH with both schistosomiasis and malaria, marking it out as a key region for future surveys of co-infection incidence and also the health effects of infection with multiple parasites. There is a large body of research on the immune activity of patients co-infected with different parasites, with some evidence suggesting malaria leads to increased susceptibility to S. mansoni infection [28, 29], but also reports of modulation of malaria via up-regulation of the immune system as a result of helminth infection . In these cases, treating for the helminth can result in a significant increase in the burden of malaria, further complicating decisions regarding appropriate control measures. On the other hand, certain areas within individual districts had notably high levels of one infection as compared to another, such as high malaria but low schistosomiasis prevalence in some of the islands in Mayuge district, as compared to low malaria and high schistosomiasis prevalence on the Koome islands in Mukono district. Managing these complex interactions is one of the many challenges facing existing and future control measures for NTDs in the Lake Victoria region.
Challenges for control of NTDs in the context of remote island communities
Several points can be made relating to the current status of disease distribution and control interventions based on the results of these surveys. Firstly, it is clear that prevalence of intestinal schistosomiasis, STH and malaria continue to be high in many of the islands and the districts bordering on Lake Victoria. Consequently, the National Control Programme, which has been successful in reducing intensity and disease-related morbidity , needs to improve treatment coverage and efficacy of existing control measures in the areas studied.
In the context of the islands of Lake Victoria, logistical challenges were identified as a huge obstacle for regular training of CMDs, and timely and frequent delivery of drugs. Community health workers are often compelled to travel, by wooden canoes for several hours, to reach the outer islands in the lake; fuel for canoe engines is expensive, and often unavailable. Another challenge is the high level of population itinerancy and migration throughout the region; this has been observed in other studies , and migration was cited as a key reason for treatment coverage during the survey only being estimated at approximately 70%, although residency length was not included in the questionnaire presented here. This highlights the need to include measures of itinerancy in future surveys, for accurate identification of the scale of population movement in the region. A solution would be to provide adequate funding to local health officers for local travel; however, even if such funds were available, supervision and accountability of the system must simultaneously improve in order to ensure the investment reaches the people who need it the most.
The question of funding, and in particular, sustainability of control initiatives, is intrinsic to creating an effective yet efficient programme for reducing disease burden. Although chemotherapy has been the mainstay of control tactics in the last decade, it is clear that MDA alone will not sufficiently eliminate transmission of schistosomiasis, especially in hyper-endemic areas such as the Lake Victoria islands. What is required is a combination of political will, education and improvements in access to sanitation and clean water, alongside a committed and consistent chemotherapy regime . Indeed, such an integrated approach has proved successful for the on-going and sustainable control of helminthes and intestinal parasites in other island settings, such as the Seychelles , where improved socio-economic status has also contributed to reduction in disease. Given the correlation of such factors with increased disease risk in this study, overall economic development may also prove to be highly beneficial in this setting. However, in Lake Victoria, the scale of the problem is larger; moreover, given the levels of co-infection with malaria observed here and in other studies , any control strategy in East Africa will also have to take into account the possibility, and indeed relatively high probability, of co-infection with malaria.
As with intestinal helminthes, controlling malaria may also be achievable through a combination of access to treatment, distribution of bednets and indoor residual spraying. We mobilized communities to select CMDs who were immediately trained and started distributing medicines and disseminating health education messages. These CMDs could also be trained to deliver malaria control interventions such as distributing insecticide-treated mosquito nets and ACTs among these hard-to-reach communities, therefore providing additional health benefits without the need to identify and/or train additional health workers. Bednets may also have additional protective benefits against other infections, such as lymphatic filariasis, also transmitted via mosquito vectors . Thus integrated monitoring of schistosomiasis, STH and malaria is indeed as appealing as the widely advocated integrated delivery of preventive chemotherapy (PCT) packages against NTDs [2, 35]. With the ever-limited resources, especially in sub-Saharan countries, it is clear that integrating surveys and control of intestinal helminthes along with malaria is likely to provide the most efficient method of scaling up the control of the targeted multiple parasitic infections across a regional scale.