Intestinal schistosomiasis in chimpanzees on Ngamba Island, Uganda: observations on liver fibrosis, schistosome genetic diversity and praziquantel treatment.

Despite treatment with praziquantel (PZQ) at 40 mg/kg in food, several chimpanzees on Ngamba Island Chimpanzee Sanctuary (NICS) continue to excrete eggs of Schistosoma mansoni. To monitor disease, 8 animals were closely examined under anaesthesia in March 2011 with portable ultrasonography and by rectal snip biopsy. Schistosome genetic diversity had been previously assayed within 4 of these chimpanzees, finding extensive diversity with 27 DNA barcodes encountered, although none was common to all animals. Calcified schistosome eggs were found in the rectal snips from 5 chimpanzees and liver fibrosis was clearly documented, indicative of progressive disease in 6 animals, the latter being surprisingly advanced in a younger chimpanzee. All 8 animals were treated under anaesthesia by oral gavage with PZQ at 60 mg/kg dosing that was well tolerated. These animals were again re-examined in June 2012 using stool and urine sampling. Only 1 chimpanzee appeared to be free from infection and active egg excretion was confirmed in 6 animals. If intestinal schistosomiasis is to be controlled within this setting, a long-term disease management plan is required which should combine active case-detection with an insistent treatment regime with praziquantel for these chimpanzees, exploring perhaps the performance of even higher dosing.

Field survey for strongyloidiasis in eastern Uganda with observations on efficacy of preventive chemotherapy and co-occurrence of soil-transmitted helminthiasis/intestinal schistosomiasis.

Following our previous field surveys for strongyloidiasis in western Uganda, 120 mothers and 232 children from four villages in eastern Uganda were examined, with two subsequent investigative follow-ups. As before, a variety of diagnostic methods were used: Baermann concentration, Koga agar plate and strongyloidid enzyme-linked immunosorbent assay (ELISA), as well as Kato-Katz faecal smears for detection of eggs of other helminths. At baseline, the general prevalence of Strongyloides stercoralis was moderate: 5.4% as estimated by Baermann and Koga agar methods combined. A much higher estimate was found by ELISA (42.3%) which, in this eastern setting, appeared to be confounded by putative cross-reaction(s) with other nematode infections. Preventive chemotherapy using praziquantel and albendazole was offered to all participants at baseline. After 21 days the first follow-up was conducted and 'cure rates' were calculated for all parasites encountered. Eleven months later, the second follow-up assessed longer-term trends. Initial treatments had little, if any, effect on S. stercoralis, and did not alter local prevalence, unlike hookworm infections and intestinal schistosomiasis. We propose that geographical patterns of strongyloidiasis are likely not perturbed by ongoing praziquantel/albendazole campaigns. Antibody titres increased after the first follow-up then regressed towards baseline levels upon second inspection. To better define endemic areas for S. stercoralis, careful interpretation of the ELISA is warranted, especially where diagnosis is likely being confounded by polyparasitism and/or other treatment regimens; new molecular screening tools are clearly needed.

Molecular epidemiology and phylogeography of Schistosoma mansoni around Lake Victoria.

Intestinal schistosomiasis continues to be a major public health problem in sub-Saharan Africa, and is endemic in communities around Lake Victoria. Interest is growing in the molecular evolution and population genetic structure of Schistosoma mansoni and we describe a detailed analysis of the molecular epidemiology and phylogeography of S. mansoni from Lake Victoria. In total, 388 cytochrome oxidase 1 (COI) sequences were obtained from 25 sites along the Ugandan, Tanzanian and Kenyan shorelines of Lake Victoria, and 122 unique barcodes were identified; 9 corresponded to previously discovered barcodes from Lakes Victoria and Albert. A subset of the data, composed of COI sequences from miracidia from 10 individual children, was used for population genetics analyses; these results were corroborated by microsatellite analysis of 4 isolates of lab-passaged adult worms. Overall, 12 barcodes were found to be shared across all 3 countries, whereas the majority occurred singly and were locally restricted. The population genetics analyses were in agreement in revealing high diversity at the level of the human host and negligible population structuring by location. The lack of correlation between genetic distance and geographical distance in these data may be attributed to the confounding influence of high intra-individual diversity as well as human migration between communities.

Rapid mapping of schistosomiasis and other neglected tropical diseases in the context of integrated control programmes in Africa.

There is growing interest and commitment to the control of schistosomiasis and other so-called neglected tropical diseases (NTDs). Resources for control are inevitably limited, necessitating assessment methods that can rapidly and accurately identify and map high-risk communities so that interventions can be targeted in a spatially-explicit and cost-effective manner. Here, we review progress made with (1) mapping schistosomiasis across Africa using available epidemiological data and, more recently, climate-based risk prediction; (2) the development and use of morbidity questionnaires for rapid identification of high-risk communities of urinary schistosomiasis; and (3) innovative sampling-based approaches for intestinal schistosomiasis, using the lot quality assurance sampling technique. Experiences are also presented for the rapid mapping of other NTDs, including onchocerciasis, loiasis and lymphatic filariasis. Future directions for an integrated rapid mapping approach targeting multiple NTDs simultaneously are outlined, including potential challenges in developing an integrated survey tool. The lessons from the mapping of human helminth infections may also be relevant for the rapid mapping of malaria as its control efforts are intensified.

Process evaluation of schistosomiasis control in Uganda, 2003 to 2006: perceptions, attitudes and constraints of a national programme.

Schistosomiasis is widespread in Uganda along large lakes and rivers with approximately 4 million people infected. Hookworm infections also prevalent throughout the country, while infections with Ascaris lumbricoides and Trichuris trichiura are mainly found in south-western Uganda. A national programme aimed at controlling morbidity due to these infections was launched in 2003. This article describes the perceptions, attitudes, constraints and experiences of those implementing the programme and those receiving the treatment. The study used qualitative data collected largely in two districts but also from 18 other districts implementing the programme. Results showed that mass treatment was perceived to be beneficial because the drugs make people feel better. However, side-effects of praziquantel (PZQ), the smell and size of the tablets and the use of height, not weight, to determine dose were raised as major factors discouraging people from taking the drug. Generally, most of the end-users were appreciative of the programme and were beginning to demand regular treatment. Nevertheless, intensive and sustained health education is still vital for improvement of treatment coverage, especially among the non-compliers. It was repeatedly highlighted that there is a need to stock PZQ in all health facilities in endemic areas. Provision of incentives to drug distributors and to involve as many stakeholders as possible in the planning phase were also raised by respondents. Lessons learned for the development and success of a helminth control programme at a national scale are discussed.

Molecular epidemiology of Schistosoma mansoni in Uganda: DNA barcoding reveals substantial genetic diversity within Lake Albert and Lake Victoria populations.

Representative samples of Ugandan Schistosoma mansoni from Lake Albert and Lake Victoria were examined using DNA barcoding, sequence analysis of two partially overlapping regions - ASMIT (396 bp) & MORGAN (617 bp) - of the mitochondrial cytochrome oxidase subunit I (cox1). The Victorian sample exhibited greater nucleotide diversity, 1.4% vs. 1.0%, and a significant population partition appeared as barcodes did not cross-over between lakes. With one exception, Lake Albert populations were more mixed by sampled location, while those from Lake Victoria appeared more secluded. Using statistical parsimony, barcode ASMIT 1 was putatively ancestral to all others and analysis of MORGAN cox1 confirmed population diversity. All samples fell into two of five well-resolved lineages; sub-lineages therein broadly partitioning by lake. It seems that barcode ASMIT 1 (and close variants) was likely widely dispersed throughout the Nilotic environment but later diversified in situ, and in parallel, within Lake Albert and Lake Victoria. The genetic uniformity of Ugandan S. mansoni can no longer be assumed, which might better explain known epidemiological heterogeneities. While it appears plausible that locally evolved heritable traits could spread through most of the Lake Albert populations, it seems unlikely they could quickly homogenise into Lake Victoria or amongst populations therein.

The Schistosomiasis Control Initiative (SCI): rationale, development and implementation from 2002-2008.

Schistosomiasis remains one of the most prevalent parasitic diseases in developing countries. After malaria, schistosomiasis is the most important tropical disease in terms of human morbidity with significant economic and public health consequences. Although schistosomiasis has recently attracted increased focus and funding for control, it has been estimated that less than 20% of the funding needed to control the disease in Africa is currently available. In this article the following issues are discussed: the rationale, development and objectives of the Schistosomiasis Control Initiative (SCI)-supported programmes; the management approaches followed to achieve implementation by each country; mapping, monitoring and evaluation activities with quantifiable impact of control programmes; monitoring for any potential drug resistance; and finally exit strategies within each country. The results have demonstrated that morbidity due to schistosomiasis has been reduced by the control programmes. While challenges remain, the case for the control of schistosomiasis has been strengthened by research by SCI teams and the principle that a national programme using 'preventive chemotherapy' can be successfully implemented in sub-Saharan Africa, whenever the resources are available. SCI and partners are now actively striving to raise further funds to expand the coverage of integrated control of neglected tropical diseases (NTDs) in sub-Saharan Africa.

Effect of seasonal rainfall and other environmental changes, on snail density and infection rates with Schistosoma mansoni fifteen years after the last snails' study in Kigungu, Entebbe, Uganda.

BACKGROUND: The last study on snail population density in relation to rainfall pattern in Kigungu canoe landing and recreational sites on Lake Victoria shore was earlier carried out about fifteen years ago. This study also reviewed the influence of other environmental factors on the snails' infection rate. OBJECTIVE: To reassess the density dynamic of Biomphalaria (B) choanomphala and Biomphalaria (B) pfeifferi, which act as the intermediate host for S. mansoni and Bulinus (B) globosus, and Bulinus (B) tropicus, which act as intermediate host for S. haematobium. DESIGN: Retrospective study. SETTING: Busy canoe landing sites along Lake Victoria in Kigungu fishing village were selected for the snail sampling. RESULTS: Nine thousand one hundred and ninety four B. choanomphala were collected over the study period. The numbers of B. choanomphala collected in each yearwas 4742 (51.6%) and 4452 (48.4%) in 2004 and 2005 respectively. Of the 4742 B. Choanomphala collected in 2004, 82 (1.7%) shed human cercariae and 329 (6.7%) shed non-human cercariae. Whereas in 2005, out of 4452 B. choanomphala collected 302 (6.85%) shed non-human cercariae and 82 (1.8%) shed human cercariae. Similarly, 4173 B. pfeifferi were also collected in the same period. Out of which 2224 (53.3%) were collected in 2004 and 1949 (46.7%) in 2005. For B. pfeifferi, 42 (1.9%) out of 2224 snails collected in 2004 shed human cercariae and 246 (11.1%) shed non-human cercariae. While in 2005, 33 out of 1949 snails (1.7%) shed human cercariae and 159 (8.2%) shed non-human cercariae. Other snails of medical importance collected included 292 B. globosus and 3094 B. tropicus. None of the Bulinus spp. collected shed any human cercariae but 37 (2.1%) and 30 (2.3%) B. tropicus shed non-human cercariae in 2004 and 2005 respectively. In 2004 and 2005, the area received, 1729mm and 1959mm of rainfall respectively, The mean rainfall during the year was 144.05 mm and 163.3 mm in 2004 and 2005 respectively. There was a negative correlation between rainfalls and snail density dynamic. CONCLUSION: We have found in this study that in spite of the bush clearing of the papyrus swamps which originally was the major habitats for B. choanomphala, B. pfeifferi and the Bulinus spp the intermediate host for schistosome at all canoe landing sites at Kigungu, these snails are still present. Moreover, that their population density dynamic and infection rate are inversely proportional to the rainfall pattern.

The epidemiology of schistosomiasis in Lango region Uganda 60 years after Schwetz 1951: Can schistosomiasis be eliminated through mass drug administration without other supportive control measures?

INTRODUCTION: Lango region is the only known endemic region for urinary and intestinal schistosomiasis in Uganda. Although there has been no significant improvement in sanitation and safe water supply in the region over years, the endemicity and prevalence of Schistosoma haematobium, in particular, have declined, perhaps due to yearly mass treatment campaigns implemented since 2003. METHODS: We report the epidemiology of Urinary and Intestinal schistosomiasis in Lango since 1951-2011 determined through Microscopic examinations for S. mansoni and S. haematobium respectively. A retrospective data review from 195 to 2011 was done to establish the prevalence over the years in the region. We performed Poisson regression analysis to observe trends in epidemiology before and after control was initiated in 2002. In addition, malacological surveys were undertaken in 2007 to assess local transmission potential. FINDINGS: Contrary to earlier records, S. haematobium was low and confined to a few putative foci, with declined in infections from 28.2% in 1951 to 2.48% by 2011. Although this decline can be attributed to control, this was already much lower in 1967 than 1951, long before control interventions began suggesting that environmental changes may have made the habitat less suitable for the transmission of S. haematobium. Compared to the historical records S. mansoni prevalence first increased up immediately before control interventions in 2003, significantly declined (p=<0.001) until 2007. However, in 2007 and 2011 declined insignificant, (p = 0.656). No snail has ever been isolated shedding S. haematobium cercariae but many Bulinus snail spp. were found shedding S. bovis cercariae. CONCLUSION: This suggests that a combination of environmental and mass treatment has had a significant impact on transmission in Lango region.

Data on the pre-MDA and post MDA interventions for Schistosoma mansoni and Schistosoma haematobium in a co-endemic focus in Uganda: 1951-2011.

The dataset for this article contains Urinary and Intestinal Schistosomiasis from Lango region, northern Uganda which is the only known co-endemic region for S.mansoni and S.haematobium. Reported in the data, is the retrospective data review for historical information before interventions were implemented before 2003 and after interventions were implemented in 2003 by the national control program. In 2007 and 2011, parasitological surveys were conducted in the region to validate Schistosomiasis trends following World Health Organization (WHO) guidelines for surveys. In addition, malacological surveys were undertaken in 2007 to assess local transmission potential. The dataset can provide an insight into the health implications of Schistosomiasis control in co-endemic focus in Uganda, "The epidemiology of schistosomiasis in Lango region Uganda 60 years after Schwetz 1951: Can schistosomiasis be eliminated through mass drug administration without other supportive control measures?" (Adriko et al., 2018) [10].

The WHO dose pole for the administration of praziquantel is also accurate in non-African populations.

In 2001, WHO developed a pole for the administration of praziquantel without the use of weighing scales, with encouraging results in African populations. In the present study, the pole was tested on height/weight data from 9354 individuals from 11 non-African countries. In more than 98% of the individuals (95% CI 97.8-98.4) the pole estimated an acceptable dosage (30-60 mg/kg), a performance statistically similar to that observed in African populations. Reproducing the present pole in the form of a strip of paper and including it in each container of praziquantel would greatly facilitate the administration of the drug in large-scale interventions.

Modeling the distribution of Schistosoma mansoni and host snails in Uganda using satellite sensor data and Geographical Information Systems.

The potential value of MODIS satellite sensor data on Normalized Difference Vegetation Index (NDVI) and land surface temperatures (LST) for describing the distribution of the Schistosoma mansoni-"Biomphalaria pfeifferi"/Biomphalaria sudanica parasite-snail system in inland Uganda, were tested by developing annual and seasonal composite models, and iteratively analysing for their relationship with parasite and snail distribution. The dry season composite model predicted an endemic area that produced the best fit with the distribution of schools with > or =5% prevalence. NDVI values of 151-174, day temperatures of 26-36 degrees C, and night temperatures of 15-20 degrees C were used as criteria for the prediction model. Using the same approach with host snail data indicated that most of Uganda is suitable "B. pfeifferi"/B. sudanica habitat, except for possibly the north-eastern region of the country. The parasite, however, appears to be restricted in its distribution in both the north-eastern and the south-western regions of Uganda. The absence of disease in the south-west can not be attributed to the absence of snail hosts. Results suggest a combination of satellite sensor data on temperature and standard climate data on precipitation, as the best ecological determinants of the S. mansoni-"B. pfeifferi"/B. sudanica system. Satellite composite models and logistic regression analysis, suggest low night time temperature as one of the significant factors inhibiting S. mansoni transmission in the south-western highland areas of Uganda. The developed models are, however, unique, representing species-specific ecologic preferences of the S. mansoni-"B. Pfeifferi"/B. sudanica system in inland Uganda. Further validation studies are needed to test the value of the model in other countries in East Africa.

Efficacy and side effects of praziquantel treatment in a highly endemic Schistosoma mansoni focus at Lake Albert, Uganda.

The aim of the study was to assess the efficacy and side effects following single and repeated (6 weeks apart) praziquantel treatment (40 mg/kg) in a Schistosoma mansoni-endemic focus with long-standing transmission at Lake Albert in Uganda between December 1996 and January 1997. The results were based on 482 individuals, randomly representing all age and both gender groups. The cure rate following the first and second treatments was 41.9% and 69.1%, respectively. The cure rate was higher in adults than in children, irrespective of intensity of infection. In addition, the cure rate declined markedly with increasing intensity of infection. The reduction in intensity of infection was marked, being 97.7% and 99.6% after the first and second treatments, respectively. A pre- and post-treatment symptom questionnaire revealed a broad range of side effects, including abdominal pain and diarrhoea. However, no serious or long-lasting complications affecting compliance were observed. The marked reductions in faecal egg excretion and the acceptable level of side effects point to a single praziquantel treatment (40mg/kg) as the strategy of choice in such a highly endemic S. mansoni focus.

Epidemiology and morbidity of Schistosoma mansoni infection in a fishing community along Lake Albert in Uganda.

Schistosoma mansoni infection, associated morbidity and symptoms were studied in Piida fishing community at Butiaba, along Lake Albert, Uganda, from November 1996 to January 1997. The study revealed that S. mansoni is highly endemic with an overall prevalence of 72%, a mean intensity of 419.4 eggs per gram (epg) faeces (geometric mean for positives only), with 37.8% of males and 33.0% of females excreting over 1000 epg. Prevalence and intensity peaked in the 10-14 year old age group and decreased with increasing age. Females were less heavily infected than males. Differences were also shown between tribes. Diarrhoea and abdominal pain were commonly reported in Piida. However, no clear-cut correlation between intensity of S. mansoni infection and these conditions could be demonstrated, indicating that retrospective questionnaires concerning S. mansoni related-symptomatology are of limited value. Organomegaly, as assessed by ultrasonography, was frequent and hepatomegaly was associated with heavy S. mansoni infection. No correlation was demonstrated between splenomegaly and infection. This study emphasizes that schistosomiasis mansoni is a major public health problem in Piida fishing community and presumably also in many similar fishing communities. These observations call for immediate intervention and can help in planning long-term strategies for sustainable morbidity control.

Hepatosplenic morbidity in two neighbouring communities in Uganda with high levels of Schistosoma mansoni infection but very different durations of residence.

Peri-portal fibrosis can be a serious sequelae of Schistosoma mansoni infection. Age or duration of exposure have been identified as important risk factors, but their relative importance cannot be easily separated. Here, we have compared two cohorts, aged 6-50 years and resident for ten years or since birth, from two neighbouring villages (Booma and Bugoigo) on the eastern shore of Lake Albert, Uganda. Parasitological measurements were similar, whereas the prevalence of peri-portal fibrosis was 5-fold higher in Booma. Data from the cohorts were pooled to assess the relative contribution of age and duration of residency on the risk of disease. Amongst adults, duration of residency was the critical risk factor--individuals aged 17-31 years resident for more 22 years had an almost 12-fold increased risk of fibrosis than those resident for less than 15 years. Height-standardised Splenic Vein Diameter (SVD), Portal Vein Diameter (PVD), Para-sternal Liver Length (PLL) and Spleen Length (SL) values were all higher in Booma, and each organometric parameter except PLL increased with the severity of fibrosis. Our results clearly demonstrate that duration of exposure is a critical risk factor for the development of peri-portal fibrosis and its sequelae in adults. This parameter should therefore be a routine measurement during epidemiological surveys of S. mansoni.

Spatial and intensity-dependent variations in associations between multiple species helminth infections.

Estimated associations between infections with different helminth species can be used to predict the proportion of a population infected with multiple species infections. This is an important measure of disease burden, as those with multiple infections are often at an increased risk of morbidity. In this paper, we investigate variation amongst the estimated associations between Ascaris lumbricoides, Trichuris trichiura and hookworm, over a number of different spatial levels among schoolchildren in Cameroon. Associations between species were largely homogeneous within districts, provinces and ecological zones, although variation between these regions was identified, implying that a single measure of association may not be appropriate in different epidemiological settings. Further data collected amongst school children in Kenya and Uganda were analysed, to assess the dependence of the associations on the intensity of infection. It was found that the strength of the association between A. lumbricoides and T. trichiura increased with intensity, such that those with more intense infections with one species are increasingly likely to harbour concurrent intense infections with the other species. The implications of these results are discussed in relation to the estimation of the disease burden due to multiple helminth species.

Epidemiology of schistosomiasis in Kampala, Uganda.

A survey for intestinal schistosomiasis was carried out in grade six pupils (5,313 pupils, 10-15 years) in over 80% of all primary schools in Kampala. The aim of the survey was to assess the prevalence and intensity of schistosomiasis in Kampala school children and to ascertain if transmission was occurring within the city. The prevalence of the disease was only 4.1% (216/5,313) and egg load generally low (< 500 eggs per gram of stool). Most infected pupils came from areas outside Kampala known to be endemic for intestinal schistosomiasis. It cannot be precluded however, that some infections were contracted in Lake Victoria and the Kabaka's Lake within Kampala city. It was suggested that it would be more cost effective if schistosomiasis control measures were applied at this stage.

Schistosoma mansoni along Lake Albert, Kibale District, Western Uganda.

Four hundred and fifty one human strata living in the three fishing villages of Ndiaga, Kabukanga and Rwabikongoro along Lake Albert shore in Kibale District were examined for S. mansoni infection using Kato/Katz method. Of the 451 people, 409 (90.7%) were found infected with S. mansoni with geometric mean egg count of 561.3 eggs per gram (epg) faeces. Males had significantly higher mean egg counts than females, 608.3 epg and 415.6 epg respectively. All S. mansoni infected individuals were treated with praziquantel at 40 mg/kg body weight. Other common parasites observed were Asaris lumbricoides, Trichuris trichiura and hookworms. These were treated with mebendazole. Snail infection rate among the 115 Biomphalaria sudanica and the 56 B. stanleyi were 5.2% and 3.6% respectively. All the 66 Bulinus (B) tropicus found, were negative for cercariae shedding. The main pulmonate snails were 250 Lymnae natalensis, 500 Pila ovata and 375 Bellamya spp were the commonest prosobranchs followed by Bivalves (101).

Human intestinal parasites in primary school children in Kampala, Uganda.

A cross sectional survey on intestinal parasite infections was carried out in 5,313 pupils between the ages of ten and fifteen years in 98 primary schools in Kampala. The aim was to identify the types and distribution of intestinal parasites and to estimate the prevalence in school children. Trichuris trichiura (28%), Ascaris lumbricoides (17%) and hookworms (12.9%) were common infections among the children. Other less commonly found parasites were S.mansoni, Strongyloides stercolaris, Taenia sp, Enterobius vermicularis, Giardia lamblia, Entamoeba coli and E. histolytica. Refuse dumps are probably a significant source of transmission of intestinal helminthic infections in Kampala.

Epidemiology of intestinal helminth infestations among schoolchildren in southern Uganda.

OBJECTIVE: To determine the prevalence and intensity of intestinal helminth species among school children in southern Uganda. DESIGN: A cross-sectional survey using a randomly selected sample. SETTING: Eighteen districts of southern Uganda. SUBJECT: Two thousand and four school children aged two to twenty years (93.3%, aged 5-10 years) selected from classes 1 and 2 in 26 randomly selected primary schools. RESULTS: Overall, 55.9% of children were infected with either hookworm, Ascanis lumbricoides or Trichuris trichiura. The prevalence of A. lumbricoides was 17.5% ( range 0-66.7% by school), T. trichiura was 7.3% (0-45.0%) and hookworm 44.5% (15.6-86.0%). The prevalence of A. lumbricoides and T. trichiura was greatest in western districts while hookworm infection was more evenly distributed across the country. CONCLUSION: Mass antihelminthic treatment of school children was warranted in 13 of the 18 districts as more than 50% of the children were infected with an intestinal nematode. It is likely that pre-school children are similarly infected.