Patterns of concurrent hookworm infection and schistosomiasis in schoolchildren in Tanzania

A cross-sectional study of 6897 schoolchildren in 59 out of the 155 primary schools in Magu District on the shores of Lake Victoria, Tanzania, was undertaken in 1997 to determine the prevalence of single- and multiple-species helminth infection. Schistosoma haematobium, hookworm (primarily Necator americanus) and S. mansoni were the most common helminth species infecting schoolchildren in the district. The prevalences of Ascaris lumbricoides and Trichuris trichiura were negligible (< 1%). Anaemia and stunting were highly prevalent and widespread. Hookworm and S. mansoni occurred more frequently in multiple infections with other helminths than as single-species infections, but triple-species infection was rare. Analysis of the frequency distribution of infection amongst schools showed that prevalences of S. haematobium and hookworm tended to be normally distributed, with medians 75% and 45%, respectively, while the distribution of S. mansoni was markedly skewed such that only 17% schools had a prevalence greater than 20%. An inverse association between S. mansoni and S. haematobium was observed. Geographical information system (GIS) analysis indicated that S. mansoni infection was highly prevalent only along the shore of Lake Victoria, whilst S. haematobium was homogeneously prevalent everywhere except the lakeshore. This pattern appears to reflect the distribution of schistosome species-specific snail intermediate hosts. The results imply that joint treatment for hookworm infection and schistosomiasis would be beneficial throughout the district.     

The burden of polyparasitism among primary schoolchildren in rural and farming areas in Zimbabwe

A cross-sectional study was conducted in Zimbabwe among 1303 primary schoolchildren from a rural (53.3%) and a commercial farming area (46.7%) to determine the prevalence of co-infection by helminths and Plasmodium falciparum. Urine was examined on three successive days using the filtration method. Two stool specimens were processed using the Kato-Katz method and a third specimen was processed using the sedimentation method. Plasmodium falciparum was diagnosed from thick blood films. The prevalence of Schistosoma haematobium in the rural and farming areas was 66.8% and 52.3%, respectively, and for S. mansoni the prevalence was 12.4% and 22.7%, respectively. Plasmodium falciparum, hookworms, Ascaris lumbricoides and Trichuris trichiura occurred only in the farming area, with a prevalence of 27.9%, 23.7%, 2.1%, 2.3%, respectively. Co-infection and triple infection with schistosomes, P. falciparum and soil-transmitted helminths occurred in the commercial farming area only. Hookworm and S. mansoni infections were associated with P. falciparum malaria (P<0.001, OR=2.48, 95% CI 1.56-3.93 and P=0.005, OR=1.85, 95% CI 1.20-2.87, respectively). Overlap of helminths with malaria is a concern among primary schoolchildren and incorporating helminth control in programmes aiming to control malaria will improve funding and increase the efficiency of control for neglected tropical diseases in identified co-endemic settings.     

Fibre-optic sigmoidoscopy compared with the Kato technique in diagnosis and evaluation of the intensity of Schistosoma mansoni infection.

450 patients in Riyadh, Saudi Arabia, complaining of chronic abdominal pain and, coming from different countries endemic for schistosomiasis, were examined endoscopically using fibre-optic colono- or sigmoidoscopes, and rectal biopsies were examined for Schistosoma mansoni ova. After a preliminary study showed that more than 6 biopsies did not increase the positivity rate, 6 biopsies were taken from the rectum and examined by transparency technique. 280 were positive for S. mansoni, 9 of them having in addition S. haematobium. 4 patients had polyps in the sigmoid colon and rectum. When these positive cases were examined using duplicate 50 mg Kato smears, only 160 (57.1%) were positive. There was a highly positive correlation between the intensity of infection as graded by the 2 techniques. We recommend examination of 6 rectal biopsies using fibre-optic sigmoidoscopy when available in small communities with a patchy distribution of schistosomiasis like Saudi Arabia. The method could also be used to exclude schistosomiasis in persons who have moved from rural to urban or non-endemic areas and are unlikely to be re-exposed to infection.     

Schistosomiasis in Ethiopia

The literature on schistosomiasis in Ethiopia is reviewed with the objective of bringing together in one paper diverse sources which may not be available to those interested in schistosomiasis. Particular attention is given to the influence of altitude and climate, snail ecology and government economic programs on the distribution of schistosomiasis. Out of 365 communities studied between 1961 and 1986 for Schistosomiasis mansoni, cases were reported from 225 (62%), and in 85 (23%) the prevalence ranged from 10 to 92%. Most transmission sites and S. mansoni infections are in agricultural communities along streams between 1300 and 2000 m altitude infested with Biomphalaria pfeifferi, the major snail intermediate host. S. mansoni transmission above 2200 m and below 800 m is precluded in many parts of Ethiopia by low and high water temperatures, respectively. Schistosomiasis haematobium cases have been reported from 30 of the 54 communities studied, 17 of them with infection rates between 14 and 75%. Endemic S. haematobium appears to be confined in its distribution to lowlands below 800 m altitude. The highly focal distribution of S. haematobium transmission is largely due to the nonsusceptibility of most bulinine snails to the Ethiopian strain of the parasite and low water temperatures in the highlands. Water resources development, resettlement programs, refugee migration and other population movements may result in the spread of endemic S. mansoni. Lack of information on snail host/parasite relationships and the ecology of proven and suspected snail hosts does not permit predictions on the spread of endemic S. haematobium. Past and present schistosomiasis control programs in Ethiopia are reviewed and recommendations made for the national control program.     

Questionnaires for rapid screening of schistosomiasis in sub-Saharan Africa

New initiatives are aiming to reduce the global burden of schistosomiasis, mainly through the large-scale application of chemotherapy. To target chemotherapy effectively, rapid assessment procedures are needed for identifying high-risk communities that are foci for the disease. In this review, we examine the development and validation of simple school questionnaires for screening communities for Schistosoma haematobium and S. mansoni rapidly and inexpensively. The focus is on sub-Saharan Africa, where 85% of the current schistosomiasis burden is concentrated. For more than a decade, the questionnaire approach has been validated in 10 countries, with 133 880 children interviewed in 1282 schools, and with 54 996 children examined for S. haematobium. The questionnaires were well accepted, highly reliable, and of low cost. The success of the questionnaires is explained by the fact that S. haematobium infections were easily perceived through the presence of blood in urine. Evidence from 48 258 children interviewed in 545 schools indicated that reported blood in stools and bloody diarrhoea are valuable indicators for community diagnosis of S. mansoni. However, the diagnostic performance of the questionnaires for S. mansoni was weaker than for S. haematobium, and although these results are encouraging, the questionnaires need additional validation. Recently, questionnaires were extended from community to individual diagnosis and showed considerable promise. Questionnaires are now available for promptly defining the magnitude of schistosomiasis in a large area, which will allow limited resources for morbidity control to be allocated optimally.     

Patterns of helminth infection and relationship to BCG vaccination in Karonga District, northern Malawi

Surveys of enteric and urinary helminth infections were carried out in 1999 among 501 schoolchildren and among 320 adolescents and young adults participating in a study of immune responses to BCG vaccine in Karonga District, northern Malawi. Hookworm, Schistosoma mansoni and S. haematobium infections were detected in 64%, 27% and 20% of schoolchildren and in 55%, 40% and 25% of the immunology study subjects, respectively. Other helminths were appreciably less common. The prevalence of 'at least one' helminth infection was 76% among schoolchildren, ranging from 60% to 92% in the 4 schools, and was 79% in the immunology study participants. There was no evidence for an association between the presence of a BCG scar and presence or intensity of infection with worms in the schoolchildren, nor evidence that BCG vaccination of adolescents and young adults had any effect on the prevalence of helminth infections 1 year later.     

Estimating prevalence of community morbidity due to intestinal helminths: prevalence of infection as an indicator of the prevalence of disease.

The rational design of helminth control programmes for endemic areas requires that the limited resources be focused on the communities in greatest need. The process of locality-targetting would be facilitated by a simple, inexpensive method of assessing morbidity at the community level. This paper describes how a simple model of the distribution of infection in human populations can use infection prevalence data to predict the proportion of heavy, and potentially clinically significant, infections in a community. Analysis of observed data for Ascaris lumbricoides indicates that the risk of clinical ascariasis increases non-linearly with the prevalence of infection. The predicted prevalence of morbidity is low up to approximately 60% prevalence of infection, but increases very rapidly thereafter. Analyses of data for Trichuris trichiura, Schistosoma mansoni, S. haematobium and the hookworms suggests qualitatively similar patterns. The application of the model in predicting resource requirements for control is illustrated using infection prevalence data for A. lumbricoides in Brazil.     

Serodiagnosis of human Schistosoma mansoni infections: enhanced sensitivity and specificity in ELISA using a fraction containing S. mansoni egg antigens omega 1 and alpha 1

Six fractions of Schistosoma mansoni egg homogenate obtained by cation exchange chromatography were tested in an enzyme-linked immunosorbent assay (ELISA) for their efficacy in serodiagnosis of human S. mansoni infections. One cationic fraction (CEF6) containing egg antigens omega 1 and alpha 1, was found to be highly reactive with a S. mansoni positive reference serum pool. 94 of 95 sera from individuals infected with S. mansoni gave a positive reaction with CEF6, and no cross reactivity was obtained with this antigenic fraction and sera from donors infected with heterologous non-schistosome parasites and cases of avian cercarial dermatitis. Only 10 of 165 sera from patients with S. haematobium and three of 10 sera from patients with S. japonicum were positive with S. mansoni egg CEF6. In one group of patients from West Africa, examined both serologically and parasitologically at a six-monthly interval, the measurement of antibody to CEF6 provided a more sensitive diagnostic aid than stool examination.     

Time delays between patient and laboratory selectively affect accuracy of helminth diagnosis

Studies of intestinal helminth infections are influenced by the constraints of sample collection, as identification of helminth ova in stools is affected by the time since evacuation from the host. Different methods may be required to optimise diagnostic sensitivity under different study conditions. In the context of studies in rural Malawi, we collected stool samples with different time delays from production by subjects to sample collection by field staff, to examination in the laboratory. Stools were processed by Kato-Katz (KK) or formol-ether concentration (FEC) methods. Hookworm and Schistosoma mansoni were the most common helminths identified. The prevalence of hookworm was higher with KK (270/988, 27%) than with FEC (191/988, 19%). Comparison was made between the results from the two methods according to the timing of the processing steps. Delays in processing did not affect retrieval of S. mansoni. A decrease in sensitivity of almost 50% for detection of hookworm was observed with either method when preservation/refrigeration was delayed by more than 3h. A delay of 1 day from refrigeration or preservation to laboratory processing also reduced the sensitivity for hookworm by 50% for both methods. Care must be taken in studies of multiple helminth infections owing to the selective reduction of hookworm ova during transport. This is particularly critical when samples are not preserved, even over short periods of time, and even with formalin preservation.     

Are there interactions between schistosomes and intestinal nematodes?

A survey for intestinal parasites was carried out in a homogenous rice cultivation area, in which people had equal opportunities of acquiring the local endemic helminthiases, including schistosomiasis mansoni. The numbers of Schistosoma mansoni eggs excreted in faeces were counted. Infections with S. mansoni, Ascaris lumbricoides, ancylostomes and Trichuris trichiura were not randomly distributed, but were correlated, depending on the species of worms present. The S. mansoni egg counts were positively correlated with ancylostome infection but inversely correlated with A. lumbricoides and T. trichiura. Patients with schistosomiasis associated with 2 other helminth infections excreted more S. mansoni eggs than the patients with S. mansoni plus only one other helminth infection.     

The impact of iron supplementation on reinfection with intestinal helminths and Schistosoma mansoni in western Kenya

A randomized, placebo-controlled, double-blind trial was carried out in 1994-96 among 231 children and 181 adults in order to determine the effects of iron on reinfection rates and intensities of hookworm, Ascaris lumbricoides, Trichuris trichiura and Schistosoma mansoni. Adults given 60 mg elemental iron twice-weekly for 12 months had significantly lower reinfection rates of A. lumbricoides (16.7% vs 31.9%, P = 0.046), T. trichiura (6.9% vs 20.6%, P = 0.03) and S. mansoni (38.3% vs 61.8%, P = 0.008) compared to adults given placebo. In contrast, adults allocated to iron had a significantly higher reinfection rate of hookworm at the 4-month examination (11.1% vs 0%, P = 0.009), but the difference was not significant at 8- and 12-month follow-up examinations. Iron supplementation had no effect on reinfection intensities in adults. Surprisingly, iron supplementation had no effect on either reinfection rates or intensities in children. Multiple logistic regression analyses controlling for baseline infection status confirmed the effect in adults of iron on A. lumbricoides, T. trichiura and S. mansoni reinfection rates. The effect is suggested to be due to reduced risk behaviour, to improved immune function or to unfavourable host gut conditions caused by an increased oxidative stress. In each case, the lack of effect in children remains to be explained. In contrast, iron supplementation apparently was short-lived in favour of hookworm infection, an effect that needs further clarification. The findings suggest that iron supplementation has a role to play in helminth control programmes and that intraluminal factors may contribute to the regulation of some helminth infections.     

Non-human vertebrate hosts of Schistosoma haematobium and Schistosoma mansoni

The author reviews the results of experimental infections of various species of mammals, other than man, with S. haematobium and S. mansoni, and discusses investigations in Africa and Brazil into the possibility of the natural infection of non-human vertebrates with these two parasites. Only a few species, besides monkeys, could be easily infected with S. haematobium in the laboratory, while-outside man-natural infection with this parasite appears to be practically non-existent. On the other hand, many animals are good experimental hosts for S. mansoni, and at least 21 species of mammals have been found infected with this parasite in Africa and America. It is thus possible to state, provisionally, that man is the only reservoir of S. haematobium, but the question still remains open where S. mansoni is concerned. Further research is suggested in order to assess the importance of non-human reservoirs in the epidemiology of bilharziasis.     

Epidemic Schistosoma mansoni in a known S. haematobium area

An epidemic of bloody diarrhoea was observed in 1997 and 1998 in Bessoum, north Cameroon. Of 1176 inhabitants, 16.7% went for medical consultation to a public health centre located 10 km away. This epidemic was probably due to the recent introduction of Schistosoma mansoni in an ancient focus of S. haematobium, following the development of irrigated farming. The prevalences amongst primary school children were 76.6% for S. haematobium in urine, and 60.9% for S. mansoni in stool. S. mansoni was found in urine in 28.1%. This epidemic emergence may be secondary to interspecific competition between the 2 schistosomes.     

Multiplex real-time PCR for the detection and quantification of Schistosoma mansoni and S. haematobium infection in stool samples collected in northern Senegal

A multiplex real-time PCR assay for the detection and quantification of Schistosoma mansoni and S. haematobium DNA in faecal samples was developed and evaluated as an alternative diagnostic method to study the epidemiology of schistosomiasis. Primers and probes targeting the cytochrome c oxidase gene were designed for species-specific amplification and were combined with an internal control. Using positive control DNA extracted from adult Schistosoma worms and negative control samples (n=150) with DNA from a wide range of intestinal microorganisms, the method proved to be sensitive and 100% specific. For further evaluation, duplicate stool specimens with varying S. mansoni egg loads were collected in northern Senegal from pre-selected individuals (n=88). The PCR cycle threshold values, reflecting parasite-specific DNA loads in faeces, showed significant correlation with microscopic egg counts both for S. mansoni in stool and S. haematobium in urine. The Schistosoma detection rate of PCR (84.1%) was similar to that of microscopy performed on duplicate stool samples (79.5%). The simple faecal sample collection procedure and the high throughput potential of the multiplex real-time PCR provide a powerful diagnostic tool for epidemiological studies on schistosomiasis in remote areas, with possibilities for extension to other helminths or protozoa using additional molecular targets.     

Changes in human schistosomiasis levels after the construction of two large hydroelectric dams in central C?te d'Ivoire.

The construction of large dams has been shown to increase the prevalence and intensity of human schistosomiasis. However, until now no study had been carried out to assess the impact of such a project in Côte d''Ivoire. For Kossou and Taabo, two large dams which became operational in the 1970s, baseline data are available on schistosomiasis prevalence in the surrounding area before dam construction, so that the changes in schistosomiasis levels can be assessed. We re-evaluated the prevalence of Schistosoma haematobium and S. mansoni in November 1992, by analysing 548 urine and 255 stool samples, respectively, from schoolchildren from five villages around each lake. A marked increase in the overall prevalence of S. haematobium was observed, from 14% to 53% around Lake Kossou and from 0 to 73% around Lake Taabo. Baseline data for S. mansoni are only available for Lake Taabo, where a prevalence of 3% was found in 1979 and where the prevalence in 1992 was still low at 2%. The construction of these two large dams therefore led to little change in S. mansoni prevalence but to a significant increase in that of S. haematobium.     

Epidemiology of Schistosoma mansoni infection and its relationship to snail distribution in a village at the Nile bank south to Cairo

The relationship between epidemiology of S. mansoni infection and snail distribution at a village, related to Guiza Governorate and lies south to Cairo, was investigated. A systematic random sample of houses was selected. All inhabitants of the houses were invited to share in the study. The Number examined was 704. Urine and stools were examined using Nucleopore filtration and standard Kato-Katz techniques, respectively. Snail collection was done from 35 sites along the water bodies related to the village. Snails collected were examined by cercariae shedding under light. Snail differentiation was done. The results showed that the prevalence of Schistosoma mansoni human infection was 25.1 % and GMEC was 2.4 +/- 5.5. Schistosoma haematobium infection was zero percent. Biomphlaria alexandrina snail infection rate was 3.7% with density equal 0.5 +/- 1.3. Bulinus truncatus snail infection rate was zero percent. The pattern of S. mansoni human infection was closely related to snail distribution and infection. Presence of a hybrid species of B. alexandrina and B. glabrata may explain the epidemiological pattern found in the studied village.     

Diagnosis of schistosomiasis

Schistosomiasis affects around 200 million persons in the world despite improved knowledge of its epidemiology and physiopathology and significant therapeutic advances. Reliable diagnosis at present is based on observation of the parasite eggs. Schistosoma mansoni causes hepatointestinal schistosomiasis, and S. haematobium causes genitourinary disease. Other species are less frequently observed. The parasites develop in the intrahepatic blood vessels. The females migrate to different parts of the body to lay their eggs, still in the blood vessels. The eggs of different species are of variable size, but all contain a larva called miracidium and all possess a spur. Precise diagnosis is based on the morphologic characteristics of the eggs. As the eggs block different organs, especially the liver, they cause inflammatory granulomas to form. The different species of schistosomas have different geographic distributions that depend partly on the distribution of their mollusk intermediate hosts. S. mansoni and S. haematobium are present in Africa and S. mansoni is also found in the Americas. The eggs of S. haematobium are present most frequently in the urine, while in other species they are found in the stool. The procedure for collecting and preparing the specimens is described. Rectal biopsies obtained during consultations can be examined immediately if facilities are available, and biopsies may also be taken during surgical procedures. The size, color, shape, shell, and spur of eggs of each species are described, and characteristics peculiar to each are noted.     

The effect of the community-directed treatment approach versus the school-based treatment approach on the prevalence and intensity of schistosomiasis and soil-transmitted helminthiasis among schoolchildren in Tanzania

This study compared the effect of the community-directed treatment (ComDT) approach and the school-based treatment approach on the prevalence and intensity of schistosomiasis and soil-transmitted helminthiasis (STH) among schoolchildren. Following a parasitological survey in a randomly selected sample of 1140 schoolchildren, school-age children in 10 study villages received one dose of praziquantel (40 mg/kg body weight) against schistosomiasis and one dose of albendazole (400mg) against STH. Five of these villages implemented the ComDT approach and received treatment by community drug distributors, while school teachers administered treatment in five other villages using the school-based approach. At 12 months follow-up, the prevalence of Schistosoma mansoni and Trichuris trichiura infections were similar between the ComDT and the school-based approaches when examined in randomly selected schoolchildren (10.1 vs. 9.4%, P=0.66 and 0.8 vs. 1.4%, P=0.37). However, the prevalence of S. haematobium and hookworm infections were significantly lower in the ComDT approach villages compared to the school-based approach villages (10.6 vs. 16.3%, P=0.005 and 2.9 vs. 5.8%, P=0.01, respectively). The results showed that the ComDT approach is at least as effective as the school-based approach in reducing prevalence and intensity of schistosomiasis and STH among schoolchildren.     

Study of gastro-intestinal helminths of scavenging chickens in four rural districts of Amhara region, Ethiopia.

A total of 267 rural scavenging chickens were examined from October 1998 to August 1999 in four woredas (districts) of the Amhara Region, Ethiopia. Of these chickens, 243 (91.01%) were found to harbour one to nine different helminth parasites and 24 (8.99%) were free of helminth parasites. A significant difference (P < 0.01) was found between the prevalence rates of helminth parasites in the different agro-ecological zones; the highest prevalence was observed in the lowland areas. This suggests that agro-ecology has a major influence on the distribution of helminth parasites. Nematodes recovered included Heterakis gallinarum (17.28%), Subulura brumpti (17.60%), Ascaridia galli (35.58%), Cheilospirura hamulosa (0.75%) and Dyspharynx spiralis (2.62%). The principal cestode species encountered were Raillietina echinobothrida (25.84%), Raillietina tetragona (45.69%), Raillietina cesticillus (5.62%), Amoebotaenia sphenoides (40.45%), Davainea proglottina (1.12%) and Choanotaenia infundibulum (4.49%).     

Preliminary evaluation of morbidity due to S. haematobium and S. mansoni in the area of the future Adjarala Dam in Benin

The aim of this study was to provide a preliminary assessment of morbidity due to schistosomiasis in the area of the future Adjarala Dam in Benin. We included 412 schoolchildren from five villages in the study. The mean age of the children was 9.4 +/- 2.3 years and the sex ratio (F/M) was 0.94. These children underwent parasitological examination. The children provided urine samples, which were examined by eye, filtered and tested for blood and protein. Stool samples were examined using Kato's technique and an ultrasound scan of the urinary tract was performed. We carried out a survey of snails at the possible transmission sites of all the villages, with a view to identifying the intermediate hosts. We detected S. mansoni and S. haematobium in the area. Urinary schistosomiasis was mesoendemic (prevalence of 19.7%) whereas schistosomiasis due to S. mansoni was hypoendemic (prevalence of 3. 9%). Ultrasound scans showed that 28% of the children had bladder lesions and that 2.5% were carriers of hydronephrosis. We compared the diagnostic performances of the various indirect indicators of morbidity. We found that a history of hematuria was the most sensitive indicator (88%) but that the sensitivity of this indicator differed significantly according to the sex of the child. Hematuria >= 1+ was the most effective indicator. Snail surveys showed that Biomphalaria pfeifferi and Bulinus globosus were present in the area.