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Patterns of concurrent hookworm infection and schistosomiasis in schoolchildren in Tanzania
TRANSACTIONSOFTHEROYALSOCIETYOFTROPICALMEDICINEANDHYGIENE(I999)93,497-502
Patterns of concurrent in Tanzania
hookworm
infection
and schistosomiasis
in schoolchildren
‘National Institute for Medical N. J. S. Lwambo’,‘, J. E. Siza’, S. Brooke3, D. A. P. BundgY3 and H. Guyatt’ Research, Mwanza Research Centre, I? 0. Box 1462, Mwanza, Tanzania; ’ Wellcome Trust Centre for the Epidemiology of Infectious Disease, University of Oxford, South Parks Road, Oxford OX1 3FY, UK; ‘Scientt~c Coordinating Centre of the Partnership for Child Development, University of Oxford, South Parks Road, Oxford OX1 3FY, UK Abstract A cross-sectional study of 6897 schoolchildren in 59 out ofthe 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 Necawr americanus) and S. mansoni were the most common helminth species infecting schoolchildren in the district. The prevalences of Ascaris lumbrikoides 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. hookworm infection, schistosomiasis, polyparasitism, spatial distribution, geographical information system (GIS), schoolchildren, prevalence, Tanzania
Keywords:
Introduction In Tanzania, schistosomiasis occurs in all 25 regions of the United Republic (DOUMENGE et al., 1987). Except for the eastern coastal zone of the country, Schistosoma haematobium and S. mansoni infections often occur together, typically in combination with geohelminth infections (hookworm, Ascarii lumbricoides, Tnihuris triihiura) (KIwIA, 198 1). Hookworm infection is primarily due to Necator americanus. It has been suggested that where both schistosome infection and geohelminth infection are prevalent in the same locality it may be beneficial to combine their control (BUNDY et al., 199 1). The public health importance of schistosomiasis and intestinal helminths for children in Tanzania and elsewhere has been demonstrated by a number of studies (LWAMBO et al., 1992; PARTNERSHIP FOR CHILD DEVELOPMENT, 1997; STOLTZFLJS et al., 1997a). As a result, there are now initiatives to control these infections using schools to deliver broad-spectrum benzimidazoles and praziquantel (HALL et al., 1997; PARTNERSHIP FOR CHILD DEVELOPMENT, 1997; SAVIOLI et al., 1997). Whether this approach can be generalized to other areas of Africa, or indeed extended within Tanzania, will depend on a clearer understanding of the patterns of multiple infection in schoolchildren, and the spatial distribution of infections. The aim of the present study is to describe the patterns of concurrent helminth infecrion in schoolchildren. and among schools, throughout an entire district in Tanzania, in order to assess the geographical distribution of helminth infection andmultiple-species infection. The study was conducted in Mwanza Region on the shores of Lake Victoria. Proximity to the lake allowed a specific investigation of the effect of distance from a large water-body, a potentially major source of infection for schistosomiasis. Materials and Methods Study area The study was conducted in 1997 in Magu District, Mwanza Region of Tanzania. Magu is one of the 7 Author for correspondence: Helen Guyan, Wellcome Trust Centre for the Epidemiology of Infectious Disease, University of Oxford, South Parks Road, Oxford OX1 3FY, UK; e-mail helen.guyatt@,ceid.ox.ac.uk
districts of Mwanza Region and is bordered by Lake Victoria on the north. It lies between latitude 02” 07’S to 02” 38’S and longitude 33” 07’E and 34” 09’E at an altitude of 1000-l 500 m above sea level. Seasonal streams run in valleys towards Lake Victoria. Sandy loam with moderate-to-good drainage occurs in most of the district. Rainfall is seasonal and unreliable, and mean monthly temperatures range from 18°C to 28°C. In 1988 the population of Magu District was 310 918, which is serviced by 155 primary schools, 2 hospitals, 4 health centres and 34 dispensaries. Sampling schools A topographical map of Magu District was divided into 20 squares equal in size and 3 schools were chosen from each square to give a total of 60 schools. If some schools were clustered then only 1 school was selected from the cluster, and others were selected from elsewhere in the square. This was done to ensure spatial heterogeneity. In each school, 120 children in standards 2,3,4, and 5 were selected randomly for parasitological and anthropometric examination. Many of these rural schools were small, and this fact, compounded by average attendance rates of 75%, meant that in many schools all children were selected to achieve the target sample size, and in some cases slightly fewer than 120 children were present. Investigations Each child was asked to provide urine and stool specimens. The urine specimen was inspected for visual haematuria, and a reagent strip was used to detect microhaematuria. The specimen was preserved by adding a few drops of formalin and transported to the laboratory for microscope examination after sedimentation/centrifugation. Results were recorded as positive or negative for S. haematobium. Stool was collected and preserved by adding 1.0 mL of formalin in the field before being transported to the laboratory. In the laboratory stool was processed by the formol-ether concentration method and qualitatively examined for S. mansoni and geohelminth ova. Finger-prick blood samples were collected from a 50% subsample, and haemoglobin concentration was determined by a portable digital Haemoglobinometer (He-
498
N. J. S.
mocue Ltd, Sheffield, UK). Height was measured to the nearest 0.1 cm using a fixed-base stadiometer (CMS Weighting Equipment, UK). Geographical information system (GIS) analyses
A Magellan (Magellan Systems Corp.; San Dimas, CA, USA) global positioning system (GPS) was used to calculate the latitude and longitude of each of the 59 schools included in the study. The use of the GPS incurs an error of 100 m horizontally, but this was considered sufficiently accurate for the purposes of the present study. A 1:50 000 map of the study area was handdigitized. In addition to the school locations, GPS measurements were also taken of certain key features in the area, termed as ground control points, which included road junctions, bridges, and features of the lakeshore. These were then used to geo-register the digitized map to the school locations. The location of each school was linked to the parasitological data using unique school identifiers. The prevalence of infection at each school was displayed using ArcView GIS (Version 3.00, Environmental Systems Research Institute Inc.; CA, USA). ArcView GIS functions were used to measure the distance between each school and Lake Victoria. The programme computes all possible distances from each school to the lake, and selects the smallest distance using a minimization procedure. Data analysis
Spearman’s rank correlation was used to test association between the prevalence of infection and distance from the lake. Prevalences of each helminth species by age and sex were analysed using logistic regression, with an interaction term between age and sex included if found to be significant. Anaemia was defined as haemoglobin concentration < 120 g/L. Z-scores of height-forage were calculated by comparison with medians of the United States National Center for Health Statistics (NCHS) reference values. Children were classified as stunted if their z-score was in excess of 2 standard deviations (SD) below the NCHS median. Results
Data are presented here for 59 schools instead of 60 since 1 school could not be surveyed because of heavy rain preventing accessby road over a period of months. Twenty-five children were also excluded because of incomplete records. A total number of 6897 children from 59 schools were included in the present analyses, aged between 7 and 20 years, with approximately equal Table
1. Prevalence
of infection
and under-nutrition
numbers of boys and girls. The sample size in each school ranged between 94 and 125 with a-mean of 117. Table 1 shows the overall orevalence of infection with the intestinal nematodes and schistosomiasis in Magu District. Most ofthe childreninthe district (76.2%) were infected with at least 1 species of helminth. The predominant species were S. haematobium (56.5%), S. mansoni (10.9%) and hookworm (37.0%). Anaemia (62.9%) and stunting (42.4%) were very common in the schoolchildren and widespread throughout the district. The age- and sex-specific prevalences of S. haematobium, S. mansoni and hookworm are deoicted in Fiaure 1. The prevalence of S. haematobium andhookworminfection increases with age, but the rise in hookworm is less marked. Logistic regression analysis indicated that there was a significant relationship between prevalence and age for both S. haematobium (P < 0.0001) and hookworm (P < 0.0001). The prevalence of S. mansoni infection remained relatively constant for all agesat around lo%, and was not shown to differ significantly by age in the logistic regression analysis (P = 0.217). There was a significant relationship between host sex and the prevalence of S. haematobium (P
Overall (range in schools) % Prevalence of infection S. haematobium S. mansoni
Any schistosome infection Hookworm A. lumbricoides T. trikhiura
Any helminth infection Prevalence of under-nutrition Anaemia (Hb <120 g/L)b Stunting (HAZ -=-2 z-scores)’
LWAMBOETAL.
in Magu District,
Boys (n =P31) 0
Tanzania
by sex
Girls 0 (n =G4@)
p”
56.5 (13.6-86.7) 10.9 (0.0-64.4) 63.4 (21.7-87.6) 37.0 (7.4-62.0) 0.1 (0.0-1.0) 0.2 (0.0-2.5) 76.2 (45.7-92.7)
61.7 12.0 68.9 39.4 0.1 0.1 86.3
51.4 9.9 58.0 34.7 ;:;
0.008 o*ooo 1 0.004 0.02 0.546 0.658
72.2
0.001
62.9 (40.0- 100) 42.4 (18.2-63.6)
62.8 49.5
62.5 35.5
0.098 0.000 1
“Tested using logistic regression. bReduced sample size (boys, n = 1628; girls, n = 1657). ‘Height-for-age z-scores.
HOOKWORM AND SCHISTOSOMIASISIN TANZANIA
499
80
---C S. haemacobiz4m (males) - .A - S. mansoni (females)
- - * - . S. haematobium(females) - 4 - S. mansoni (males) . - * - - Hookworm (females) -O-Hookworm (males)
60
7+s (57186)
9 (1311178)
IO (276/357)
11 (3021398)
12 (5191616)
13 (5971595)
14 (563/529)
15 (4751440)
16 (2591173)
17 (171179)
18+ (81115)
Age in years(samplesizefor boys/girls) Fig. 1. Prevalence of helminth infection by age and sex of schoolchildren in Magu District.
Table 2. Prevalence
of single and multiple
infections
in schoolchildren
Overall (range in schools) % Single infection S. haematobium only S. mansoni only Hookworm only Double infection S. haematobium1.S. mansoni S. haematobium/Hookworm S. mansoni/Hookworm Triple infection S. haematobiumls. mansonilHookworm “Tested using logistic regression.
in Magu District, Boys (n =i431)
Tanzania
by sex
Girls 0 (n =G466)
p”
31.7 (5.0-63.6) 4.7 (0.0-41.5) 12.7 (0.8-44.3)
33.0 11.3 4.8
30.4 14.1 4.2
0.02 0.00 1 0.834
4.0 (0.0-2 1.O) 22.1 (3.4-44.2) 3.5 (0.0-20.8)
4.7 25.6 4.1
3.3 18.6 2~9
0.004 0*0001 0.008
1.6
1-o
1.3 (0.0-8.3)
prevalence class (60-69.9%). The distribution of hookworm prevalence was symmetrical, with most schools having a prevalence between 30% and 39.9% (Fig. 2~). Figure 3 shows the geographical distribution of infection prevalence in relation to Lake Victoria. Schools with a high prevalence of S. mansoni infection were less than 5 km from the shore (Fig. 4). For S. haematobium the pattern was rather different: schools with high and moderate prevalences of the infection were found at all distances from the lakeshore, and those at the lakeshore tended to have the lowest prevalence (Fig. 4). Overall, these patterns illustrate a significant inverse relationship between the prevalence of the 2 schistosome species at the school level (r = -0.5 19, P < 0.0001). The distribution of hookworm infection was found to be relatively homogeneous in Magu District and showed no systematic relationship with distance from the lake.
0.02
Discussion The present study shows that S. haematobium, S. mansoni and hookworm are common infections among schoolchildren in Magu District, Tanzania. In accordance with other studies in Tanzania and elsewhere (STOLTZ~S et al., 1997a, 1997b; PARTNERSHIP FOR CHILD DEVELOPMENT, 1998), the study also demonstrates that stunting and anaemia are highly prevalent among schoolchildren. It is likely that these schoolchildren are subject to significant developmental constraints as a consequence of their poor health. Many of the children harboured both schistosomes and hookworm. Such multiple-species infections are now regarded as the norm in many parts of Africa (BUCK et al., 1978; CHUNGE et al., 1991, 1995; BOOTH et a&, 1998a, 1998b). The prevalence of schistosomiasis and hookworm infection was higher in boys, which is con-
500
N. J. S.
80
(4
1
0
O.l-
lo-
20- 30- 40-
50- 60- 70-
Prevalence of S. mansoni infection
80-
90-
(%)
80
@I
1 70 60 i? 508 c 2 401
“0 s
3020 10 0,
I 0
I O.l-
1 lo-
n
20-
, 30-
40-
I 50-
I 60-
, 70-
Prevalence of S. haemazobium infection
I 80-
I 90-
(%)
80
(4
70 1 60
8 Ewl 40 % s 30 20 10 2
500 i 0
O.l-
lo-
20-
1 30-
40-
50-
Prevalence of hookworm
60infection
70-
SO- 90-
(%)
Fig. 2. Frequency distribution of the main species of helminths by school. (a) S. mamom, (b) S. haematobium, and (c) hookworm. &tent with other studies (BUNDY & BLUMENTHAL, 1990). Interestingly, boys were more likely to be infected with multiple helminth species than girls. It is unclear whether these differences can be attributed to differences in host exposure or host susceptibility. An inverse spatial relationship between the prevalences of S. haematobium and S.~mansoni was obsenred in the district. Studies in the Senegal River Basin have suggested that S. malzsoni is preval&t close to the river only, and that S. haematobium is more widespread, although dam construction appears to have resulted in
LWAMBO ETAL.
both species occurring throughout the watershed (PICQUET et al., 1996). In Egypt the 2 species occupy separate niches, although these may not be systematically related to proximity to the Nile perse (MICHELSON et al., 1993). In the present study the highest prevalence of S. haematobium infection occurred in the hinterland ftuthest from the lakeshore, and lowest along the lakeshore. In contrast, the few schools with high prevalence of S. mansoni infection were located within a few kilometres of the Lake. The observed spatial distribution of schistosomes in Magu District may be explained by the occurrence of their snail intermediate hosts and their ecological relationship between different types of waterbodies. Biomphalaria choanomphala in Lake Victoria, and Biom. sudanica, which is found adjacent to the lake, are the main intermediate snail hosts of S. mansoni in the area. Biom. pfeifferi, which occurs in permanent ponds, has a sporadic distribution and is responsible for only seasonal transmission of S. mansoni. This distribution of Biomphalaria spp. hosts might, at least in part, explain the high prevalence of S. mansoniat the lakeshore and the low prevalence but wide distribution of S. mansoni in schools away from the lakeshore. Children away from the lake would have acquired their infection locally from Biom. pfeifferi but are exposed to a lower level of transmission than children living on the lakeshore who are exposed to a higher perennial level of transmission. In contrast, S. haematobium has 3 snail intermediate hosts in the area: Bulinus nasutus. Bu. aficanus and Bu. elobosus. The most abundant and widesiread is Bu. nasut”,, which is found in temporary habitats throughout the district because of its ability to survive the long dry season by aestivation. Bu. africanus occurs in temporary streams, while Bu. globosus colonizes permanent ponds. Thus the snail intermediate hosts of S. haematobium occupy a mosaic of habitats throughout the district, such that transmission of the parasite is widespread but seasonal, peaking in transmission after the rainv season (WEBBE. 1962). This snail pattern may accouni for the observed widespread distribution of S. haematobium infection in schoolchildren throughout Magu District. These patterns of S. mansoni and S. haematobium in relation to large water-bodies confirm previous work conducted in East Africa. In Uganda, NELSON (1958, 1959) reported that the prevalence of S. mansoni was highest along the shores of Lake Albert, decreasing in prevalence away from the lake. On the shores of Lake Victoria in Mwanza Region, Tanzania, it has been observed previously that S. haematobium does not occur owing to the absence of Bulinus spp. but does occur inland in small, static water-bodies which harbour the species (MCCULLOUGH, 1972). In Mwanza District previous studies have shown that Biom. pfea$‘en’ is not found in such water-bodies and tended to be associated with permanent water-bodies and moderately abundant aquatic vegetation OJCTEBBE, 1962). The homogeneous distribution ofhookworm throughout the area is not amenable to a similarly straightforward biological association, but presumably reflects general poverty and low standards-of hygiene throughout the area, It is unclear whv A. lumbricoides and T. trichiura are relatively rare, but this has been observed previously in areas where hookworm infection and schistosomiasis are common (BOOTH & BIJNDY, 1992), and presumably reflects the different environmental requirements of these species. From a public health perspective it is apparent that the distributions of the 2 schistosome species in this district should be considered together since the drug of choice, praziquantel, is effective against both species. Considering these species together, the combined prevalence of S. mansoni or S. haematobium at any school within the district ranged from 22% to 88%. The mean prevalence is 63.4%. which is meater than 50.0% prevalence recommended by the-world Health Organization as
HOOKWORM
AND
SCHISTOSOMIASIS
501
IN TANZANIA
Prevalence of infection(%I * . 0 .
I
Shaamatoblum
S.mansonl
Al
Hookworm
Any schistosome infection
Fig. 3. Spatial distribution
0 0.1-24.9 25-49.9 50+
30 MU
Olo
of the main helminths infecting schoolchildren
in Magu District.
.
A A A
AA* AA% ,,
5
AAA AA.,,,AJ+/$A$tAA
10
AAk
,,
15
20
25
‘%A
30
35
40
45
Distance to lake (km) Fig. 4. Prevalence of the two schisrosomes in relation fo distance from the shore of Lake Victoria
the threshold for mass treatment (WHO, 1993). Indeed, 83% of schools had a combined prevalence in excess of 50%. Furthermore, hookworm occurs more often than not as a multiple infection with schistosomiasis, which suggests that both hookworm infection and schistosomiasis could be usefully treated using a common delivery system (BUNDY et al., 1991; PARTNERSHIP FOR CHILD DEVELOPMENT, 1997). These conclusions support the concept of a generally applicable school-based strategy but that control needs to be assessed according to local ptevalences (BROOKER et al., 1999), which will depend crucially on the factors that determine the local spatial distributions. In addition
(A S. PZUYZSOX~, 6 S. haemacobium).
the appropriateness of any school-based strategy needs to be examined in relation to the proportion of children attending school and any differential risks of infection for those children in or out of school. Acknowledgement
The authors thank the Magu District Education Officer, and all the teachers and schoolchildren in the district for participating in the study. Gratitude is also extended to Mr H. Nagai, Mr J. Stevenson, and Mr H. Moyo for assistance in fieldwork and Miss Violet Kiwelu for entering the data in the computer. We thank Professor Charles Kihamia and the staff of Ushirikiano wa Kumwendeleza Mtoto Tanzania (UKUMTA) for their assistance with logistic support for the project. The fieldwork was
502
N. J. S. LWAMBO ETAL.
funded by the Wellcome Trust. N. J. S. L. is in receipt of a Wellcome Trust Research Development Award in Tropical Medicine. S. B. is in receipt of a Wellcome Trust Prize Studentshiu. D. A. P. B. and H. G. aratefullv acknowledge the SUDDORof the’ Wellcome Trust.
References Booth, M. & Bundy, D. A. P. (1992). Comparative prevalences of Ascark lumbrikoides, Trichurik trichiura, and hookworm infections and the prospects for control. Parasitology, 105, 151-157. Booth, M., Bundy, D. A. I’., Albonico, M., Chwaya, H. M., Alawi, K. S. & Savioli, L. (1998a). Associations among multiple geohelminth species infections in schoolchildren from Pemba Island. Parasitology, 116, 85-93. Booth, M., Mayombana, C. & Kilima, P. (1998b). The population biology and epidemiology of schistosome and geohelminth infections among schoolchildren in Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene, 92,491-495. Brooker, S.. Booth, M. & Guvatt, H. L. (1999). Comoarisons of schist&me andgeohelmhth infection pre;alenceg in schoolaged children from selected areas of Africa: implications for rapid assessment and combined control. Transactions of the Royal Society of Tropical Medicine and Hygiene, 93 125- 126. Buck, A. +, Anderson, R. I., MacRae, A. A. &Fain, A. (1978). Epidemiology of poly parasitism. I. Occurrence, frequency and distribution of multiple infections in rural communities in Chad, Peru, Afghanistan, and Zaire. Tropenmedizin und Parasitologic, 29, 6 l-70. Bundy, D. A. P. & Blumenthal, U. (1990). Human behaviour and epidemiology of helminth infection: the role of behaviour in exposure to infections. In: Parasitism and Host Behaviour, C. J. Barnard &J. M. Behnke (editors). London: Taylor and Francis, pp. 264-289. Bundy, D. A. P., Chandiwana, S. K., Homeida, M. M. A., Yoon. S. & Mott. K. E. (1991). The enidemiolodcalimplications bf a multipl&infec&on approach-to the co&o1 of himan helminth infections. Transactions of the Royal Society of Tropical Medicine and Hygiene, 85, 274-276. Chunge, R. N., Karumba, I’. N., Nagelkerke, N., Kaleli, N., Wamwea, M., M&so, N., Andala, E. 0. & Kinoti, S. N. (1991). Intestinal parasites in a rural community in Kenya: cross-sectional surveys with emphasis on prevalence, incidence, duration of infection, and polyparasitism. East African MedicalJournal, 68, 112-123. Chunge, R. N., Karumba, N., Ouma, J. H., Thiongo, F. W., Sturrock, R. F. & Butterworth, A. E. (1995). Polyparasitism in two rural communities with endemic Schistosoma mansoni infection in Machakos District, Kenya. Journal of Tropical Medicine and Hygiene, 98,440-444. Doumenge, J. P., Mott, K. E. & Cheung, C. (1987). Atlas of the Global Distribution of Schistosomiasis. Bordeaux: Presses Universitaires de Bordeaux. Hall, A., Orinda, V., Bundy, D. A. P. & Broun, D. (1997). Promoting child health through helminth control-a way forward? Parasitology Today, 13,4 1 l-4 13.
Kihamia, C. M. (1981). Intestinal helminths in Tanzania. Dares-Salaam Medical Journal, 8, 127 - 129. Lwambo,N. J. S.,Bundy,D.A. P. &Medley, G. F. H. (1992).A new approach to morbidity risk assessment in hookworm endemic communities. Epidemiology and Infection, 108, 469-481. McCullough, F. S. (1972). The distribution of Schistosoma mansoni and S. haemawbium in East Africa. Tropical and Geographical Medicine, 24, 199-207. Michelson, M. K., Azziz, F. A., Gamil, F. M., Wahid, A. A., Richards, F. O., Juranek, D. D., Habib, A. M. & Spencer, H. C. (1993). Recent trends in the prevalence and distribution of schistosomiasis in the Nile delta region. American 3ournal of Tropical Medicine and Hygiene, 49,76-87. Nelson, G. S. E. (1958). Schtiwsoma mansoni infection in the West-Nile district of Uganda. Part II. The distribution of S. mansoni with a note on the probable vectors. East African MedicalJournal, 35,335-344. Nelson, G. S. E. (1959). Schiswsoma mansoni infection in the West-Nile district of Uganda. Part V. Host-parasite relationships. EastAfrican MedicdJoumal, 36,29-34. Parmership for Child Development (1997). Better health, nutrition and education for the school-aged child. Transactions of the Royal Society of Tropikal Medicine and Hygiene, 91, l-2. Partnership for Child Development (1998). The health and
nutritional status of schoolchildren in tica:
evidence from
school-based health programmes in Ghana and Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene, 92,254-261. Picquet, M., Emould, J. C., Vercruysse, J., Southgate, V. R., Mbaye, A., Sambou, B., Niang, M. & Rollinson, D. (1996). The epidemiology of human schistosomiasis in the Senegal river basin. Transactions of the Royal Society of Tropical Medicine and Hygiene, 90, 340-346. Savioli, L., Renganathan, E., Montresor, A., Davis, A. & Behbehani, K. (1997). Control of schistosomiasis-a global picture. Parasitology Today, 13,444-448. Stoltzfus,, R. J., Chwaya, H. M., Tielsch, J. M., Schulze, K. J., Albomco, M. & Savioli, L. (1997a). Epidemiology of iron deficiency anemia in Zanzibari schoolchildren: the importance of hookworms. American Journal of Clinical Nutrition, 65, 153-159. Stoltzfus, R. J., Albonico, M., Tielsch, J. M., Chwaya, H. M. & Savioli, L. (1997b). Linear growth retardation in Zanzibari school children. Journal of Nutritikn, 127, 1099- 1105. Webbe, G. (1962). The transmission of Schistosoma haematobium in an area of Lake Province, Tanganyika. Bulletin of the World Health Organization, 27, 59-85. WHO (1993). The Control of Schistosomiasis. Geneva: World Health Organization, Technical Report Series, no. 830.
Received 12 March 1999; revised 6 May publication 2 June 1999
1999; accepted for
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Patterns of concurrent in Tanzania
hookworm
infection
and schistosomiasis
in schoolchildren
‘National Institute for Medical N. J. S. Lwambo’,‘, J. E. Siza’, S. Brooke3, D. A. P. BundgY3 and H. Guyatt’ Research, Mwanza Research Centre, I? 0. Box 1462, Mwanza, Tanzania; ’ Wellcome Trust Centre for the Epidemiology of Infectious Disease, University of Oxford, South Parks Road, Oxford OX1 3FY, UK; ‘Scientt~c Coordinating Centre of the Partnership for Child Development, University of Oxford, South Parks Road, Oxford OX1 3FY, UK Abstract A cross-sectional study of 6897 schoolchildren in 59 out ofthe 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 Necawr americanus) and S. mansoni were the most common helminth species infecting schoolchildren in the district. The prevalences of Ascaris lumbrikoides 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. hookworm infection, schistosomiasis, polyparasitism, spatial distribution, geographical information system (GIS), schoolchildren, prevalence, Tanzania
Keywords:
Introduction In Tanzania, schistosomiasis occurs in all 25 regions of the United Republic (DOUMENGE et al., 1987). Except for the eastern coastal zone of the country, Schistosoma haematobium and S. mansoni infections often occur together, typically in combination with geohelminth infections (hookworm, Ascarii lumbricoides, Tnihuris triihiura) (KIwIA, 198 1). Hookworm infection is primarily due to Necator americanus. It has been suggested that where both schistosome infection and geohelminth infection are prevalent in the same locality it may be beneficial to combine their control (BUNDY et al., 199 1). The public health importance of schistosomiasis and intestinal helminths for children in Tanzania and elsewhere has been demonstrated by a number of studies (LWAMBO et al., 1992; PARTNERSHIP FOR CHILD DEVELOPMENT, 1997; STOLTZFLJS et al., 1997a). As a result, there are now initiatives to control these infections using schools to deliver broad-spectrum benzimidazoles and praziquantel (HALL et al., 1997; PARTNERSHIP FOR CHILD DEVELOPMENT, 1997; SAVIOLI et al., 1997). Whether this approach can be generalized to other areas of Africa, or indeed extended within Tanzania, will depend on a clearer understanding of the patterns of multiple infection in schoolchildren, and the spatial distribution of infections. The aim of the present study is to describe the patterns of concurrent helminth infecrion in schoolchildren. and among schools, throughout an entire district in Tanzania, in order to assess the geographical distribution of helminth infection andmultiple-species infection. The study was conducted in Mwanza Region on the shores of Lake Victoria. Proximity to the lake allowed a specific investigation of the effect of distance from a large water-body, a potentially major source of infection for schistosomiasis. Materials and Methods Study area The study was conducted in 1997 in Magu District, Mwanza Region of Tanzania. Magu is one of the 7 Author for correspondence: Helen Guyan, Wellcome Trust Centre for the Epidemiology of Infectious Disease, University of Oxford, South Parks Road, Oxford OX1 3FY, UK; e-mail helen.guyatt@,ceid.ox.ac.uk
districts of Mwanza Region and is bordered by Lake Victoria on the north. It lies between latitude 02” 07’S to 02” 38’S and longitude 33” 07’E and 34” 09’E at an altitude of 1000-l 500 m above sea level. Seasonal streams run in valleys towards Lake Victoria. Sandy loam with moderate-to-good drainage occurs in most of the district. Rainfall is seasonal and unreliable, and mean monthly temperatures range from 18°C to 28°C. In 1988 the population of Magu District was 310 918, which is serviced by 155 primary schools, 2 hospitals, 4 health centres and 34 dispensaries. Sampling schools A topographical map of Magu District was divided into 20 squares equal in size and 3 schools were chosen from each square to give a total of 60 schools. If some schools were clustered then only 1 school was selected from the cluster, and others were selected from elsewhere in the square. This was done to ensure spatial heterogeneity. In each school, 120 children in standards 2,3,4, and 5 were selected randomly for parasitological and anthropometric examination. Many of these rural schools were small, and this fact, compounded by average attendance rates of 75%, meant that in many schools all children were selected to achieve the target sample size, and in some cases slightly fewer than 120 children were present. Investigations Each child was asked to provide urine and stool specimens. The urine specimen was inspected for visual haematuria, and a reagent strip was used to detect microhaematuria. The specimen was preserved by adding a few drops of formalin and transported to the laboratory for microscope examination after sedimentation/centrifugation. Results were recorded as positive or negative for S. haematobium. Stool was collected and preserved by adding 1.0 mL of formalin in the field before being transported to the laboratory. In the laboratory stool was processed by the formol-ether concentration method and qualitatively examined for S. mansoni and geohelminth ova. Finger-prick blood samples were collected from a 50% subsample, and haemoglobin concentration was determined by a portable digital Haemoglobinometer (He-
498
N. J. S.
mocue Ltd, Sheffield, UK). Height was measured to the nearest 0.1 cm using a fixed-base stadiometer (CMS Weighting Equipment, UK). Geographical information system (GIS) analyses
A Magellan (Magellan Systems Corp.; San Dimas, CA, USA) global positioning system (GPS) was used to calculate the latitude and longitude of each of the 59 schools included in the study. The use of the GPS incurs an error of 100 m horizontally, but this was considered sufficiently accurate for the purposes of the present study. A 1:50 000 map of the study area was handdigitized. In addition to the school locations, GPS measurements were also taken of certain key features in the area, termed as ground control points, which included road junctions, bridges, and features of the lakeshore. These were then used to geo-register the digitized map to the school locations. The location of each school was linked to the parasitological data using unique school identifiers. The prevalence of infection at each school was displayed using ArcView GIS (Version 3.00, Environmental Systems Research Institute Inc.; CA, USA). ArcView GIS functions were used to measure the distance between each school and Lake Victoria. The programme computes all possible distances from each school to the lake, and selects the smallest distance using a minimization procedure. Data analysis
Spearman’s rank correlation was used to test association between the prevalence of infection and distance from the lake. Prevalences of each helminth species by age and sex were analysed using logistic regression, with an interaction term between age and sex included if found to be significant. Anaemia was defined as haemoglobin concentration < 120 g/L. Z-scores of height-forage were calculated by comparison with medians of the United States National Center for Health Statistics (NCHS) reference values. Children were classified as stunted if their z-score was in excess of 2 standard deviations (SD) below the NCHS median. Results
Data are presented here for 59 schools instead of 60 since 1 school could not be surveyed because of heavy rain preventing accessby road over a period of months. Twenty-five children were also excluded because of incomplete records. A total number of 6897 children from 59 schools were included in the present analyses, aged between 7 and 20 years, with approximately equal Table
1. Prevalence
of infection
and under-nutrition
numbers of boys and girls. The sample size in each school ranged between 94 and 125 with a-mean of 117. Table 1 shows the overall orevalence of infection with the intestinal nematodes and schistosomiasis in Magu District. Most ofthe childreninthe district (76.2%) were infected with at least 1 species of helminth. The predominant species were S. haematobium (56.5%), S. mansoni (10.9%) and hookworm (37.0%). Anaemia (62.9%) and stunting (42.4%) were very common in the schoolchildren and widespread throughout the district. The age- and sex-specific prevalences of S. haematobium, S. mansoni and hookworm are deoicted in Fiaure 1. The prevalence of S. haematobium andhookworminfection increases with age, but the rise in hookworm is less marked. Logistic regression analysis indicated that there was a significant relationship between prevalence and age for both S. haematobium (P < 0.0001) and hookworm (P < 0.0001). The prevalence of S. mansoni infection remained relatively constant for all agesat around lo%, and was not shown to differ significantly by age in the logistic regression analysis (P = 0.217). There was a significant relationship between host sex and the prevalence of S. haematobium (P
Overall (range in schools) % Prevalence of infection S. haematobium S. mansoni
Any schistosome infection Hookworm A. lumbricoides T. trikhiura
Any helminth infection Prevalence of under-nutrition Anaemia (Hb <120 g/L)b Stunting (HAZ -=-2 z-scores)’
LWAMBOETAL.
in Magu District,
Boys (n =P31) 0
Tanzania
by sex
Girls 0 (n =G4@)
p”
56.5 (13.6-86.7) 10.9 (0.0-64.4) 63.4 (21.7-87.6) 37.0 (7.4-62.0) 0.1 (0.0-1.0) 0.2 (0.0-2.5) 76.2 (45.7-92.7)
61.7 12.0 68.9 39.4 0.1 0.1 86.3
51.4 9.9 58.0 34.7 ;:;
0.008 o*ooo 1 0.004 0.02 0.546 0.658
72.2
0.001
62.9 (40.0- 100) 42.4 (18.2-63.6)
62.8 49.5
62.5 35.5
0.098 0.000 1
“Tested using logistic regression. bReduced sample size (boys, n = 1628; girls, n = 1657). ‘Height-for-age z-scores.
HOOKWORM AND SCHISTOSOMIASISIN TANZANIA
499
80
---C S. haemacobiz4m (males) - .A - S. mansoni (females)
- - * - . S. haematobium(females) - 4 - S. mansoni (males) . - * - - Hookworm (females) -O-Hookworm (males)
60
7+s (57186)
9 (1311178)
IO (276/357)
11 (3021398)
12 (5191616)
13 (5971595)
14 (563/529)
15 (4751440)
16 (2591173)
17 (171179)
18+ (81115)
Age in years(samplesizefor boys/girls) Fig. 1. Prevalence of helminth infection by age and sex of schoolchildren in Magu District.
Table 2. Prevalence
of single and multiple
infections
in schoolchildren
Overall (range in schools) % Single infection S. haematobium only S. mansoni only Hookworm only Double infection S. haematobium1.S. mansoni S. haematobium/Hookworm S. mansoni/Hookworm Triple infection S. haematobiumls. mansonilHookworm “Tested using logistic regression.
in Magu District, Boys (n =i431)
Tanzania
by sex
Girls 0 (n =G466)
p”
31.7 (5.0-63.6) 4.7 (0.0-41.5) 12.7 (0.8-44.3)
33.0 11.3 4.8
30.4 14.1 4.2
0.02 0.00 1 0.834
4.0 (0.0-2 1.O) 22.1 (3.4-44.2) 3.5 (0.0-20.8)
4.7 25.6 4.1
3.3 18.6 2~9
0.004 0*0001 0.008
1.6
1-o
1.3 (0.0-8.3)
prevalence class (60-69.9%). The distribution of hookworm prevalence was symmetrical, with most schools having a prevalence between 30% and 39.9% (Fig. 2~). Figure 3 shows the geographical distribution of infection prevalence in relation to Lake Victoria. Schools with a high prevalence of S. mansoni infection were less than 5 km from the shore (Fig. 4). For S. haematobium the pattern was rather different: schools with high and moderate prevalences of the infection were found at all distances from the lakeshore, and those at the lakeshore tended to have the lowest prevalence (Fig. 4). Overall, these patterns illustrate a significant inverse relationship between the prevalence of the 2 schistosome species at the school level (r = -0.5 19, P < 0.0001). The distribution of hookworm infection was found to be relatively homogeneous in Magu District and showed no systematic relationship with distance from the lake.
0.02
Discussion The present study shows that S. haematobium, S. mansoni and hookworm are common infections among schoolchildren in Magu District, Tanzania. In accordance with other studies in Tanzania and elsewhere (STOLTZ~S et al., 1997a, 1997b; PARTNERSHIP FOR CHILD DEVELOPMENT, 1998), the study also demonstrates that stunting and anaemia are highly prevalent among schoolchildren. It is likely that these schoolchildren are subject to significant developmental constraints as a consequence of their poor health. Many of the children harboured both schistosomes and hookworm. Such multiple-species infections are now regarded as the norm in many parts of Africa (BUCK et al., 1978; CHUNGE et al., 1991, 1995; BOOTH et a&, 1998a, 1998b). The prevalence of schistosomiasis and hookworm infection was higher in boys, which is con-
500
N. J. S.
80
(4
1
0
O.l-
lo-
20- 30- 40-
50- 60- 70-
Prevalence of S. mansoni infection
80-
90-
(%)
80
@I
1 70 60 i? 508 c 2 401
“0 s
3020 10 0,
I 0
I O.l-
1 lo-
n
20-
, 30-
40-
I 50-
I 60-
, 70-
Prevalence of S. haemazobium infection
I 80-
I 90-
(%)
80
(4
70 1 60
8 Ewl 40 % s 30 20 10 2
500 i 0
O.l-
lo-
20-
1 30-
40-
50-
Prevalence of hookworm
60infection
70-
SO- 90-
(%)
Fig. 2. Frequency distribution of the main species of helminths by school. (a) S. mamom, (b) S. haematobium, and (c) hookworm. &tent with other studies (BUNDY & BLUMENTHAL, 1990). Interestingly, boys were more likely to be infected with multiple helminth species than girls. It is unclear whether these differences can be attributed to differences in host exposure or host susceptibility. An inverse spatial relationship between the prevalences of S. haematobium and S.~mansoni was obsenred in the district. Studies in the Senegal River Basin have suggested that S. malzsoni is preval&t close to the river only, and that S. haematobium is more widespread, although dam construction appears to have resulted in
LWAMBO ETAL.
both species occurring throughout the watershed (PICQUET et al., 1996). In Egypt the 2 species occupy separate niches, although these may not be systematically related to proximity to the Nile perse (MICHELSON et al., 1993). In the present study the highest prevalence of S. haematobium infection occurred in the hinterland ftuthest from the lakeshore, and lowest along the lakeshore. In contrast, the few schools with high prevalence of S. mansoni infection were located within a few kilometres of the Lake. The observed spatial distribution of schistosomes in Magu District may be explained by the occurrence of their snail intermediate hosts and their ecological relationship between different types of waterbodies. Biomphalaria choanomphala in Lake Victoria, and Biom. sudanica, which is found adjacent to the lake, are the main intermediate snail hosts of S. mansoni in the area. Biom. pfeifferi, which occurs in permanent ponds, has a sporadic distribution and is responsible for only seasonal transmission of S. mansoni. This distribution of Biomphalaria spp. hosts might, at least in part, explain the high prevalence of S. mansoniat the lakeshore and the low prevalence but wide distribution of S. mansoni in schools away from the lakeshore. Children away from the lake would have acquired their infection locally from Biom. pfeifferi but are exposed to a lower level of transmission than children living on the lakeshore who are exposed to a higher perennial level of transmission. In contrast, S. haematobium has 3 snail intermediate hosts in the area: Bulinus nasutus. Bu. aficanus and Bu. elobosus. The most abundant and widesiread is Bu. nasut”,, which is found in temporary habitats throughout the district because of its ability to survive the long dry season by aestivation. Bu. africanus occurs in temporary streams, while Bu. globosus colonizes permanent ponds. Thus the snail intermediate hosts of S. haematobium occupy a mosaic of habitats throughout the district, such that transmission of the parasite is widespread but seasonal, peaking in transmission after the rainv season (WEBBE. 1962). This snail pattern may accouni for the observed widespread distribution of S. haematobium infection in schoolchildren throughout Magu District. These patterns of S. mansoni and S. haematobium in relation to large water-bodies confirm previous work conducted in East Africa. In Uganda, NELSON (1958, 1959) reported that the prevalence of S. mansoni was highest along the shores of Lake Albert, decreasing in prevalence away from the lake. On the shores of Lake Victoria in Mwanza Region, Tanzania, it has been observed previously that S. haematobium does not occur owing to the absence of Bulinus spp. but does occur inland in small, static water-bodies which harbour the species (MCCULLOUGH, 1972). In Mwanza District previous studies have shown that Biom. pfea$‘en’ is not found in such water-bodies and tended to be associated with permanent water-bodies and moderately abundant aquatic vegetation OJCTEBBE, 1962). The homogeneous distribution ofhookworm throughout the area is not amenable to a similarly straightforward biological association, but presumably reflects general poverty and low standards-of hygiene throughout the area, It is unclear whv A. lumbricoides and T. trichiura are relatively rare, but this has been observed previously in areas where hookworm infection and schistosomiasis are common (BOOTH & BIJNDY, 1992), and presumably reflects the different environmental requirements of these species. From a public health perspective it is apparent that the distributions of the 2 schistosome species in this district should be considered together since the drug of choice, praziquantel, is effective against both species. Considering these species together, the combined prevalence of S. mansoni or S. haematobium at any school within the district ranged from 22% to 88%. The mean prevalence is 63.4%. which is meater than 50.0% prevalence recommended by the-world Health Organization as
HOOKWORM
AND
SCHISTOSOMIASIS
501
IN TANZANIA
Prevalence of infection(%I * . 0 .
I
Shaamatoblum
S.mansonl
Al
Hookworm
Any schistosome infection
Fig. 3. Spatial distribution
0 0.1-24.9 25-49.9 50+
30 MU
Olo
of the main helminths infecting schoolchildren
in Magu District.
.
A A A
AA* AA% ,,
5
AAA AA.,,,AJ+/$A$tAA
10
AAk
,,
15
20
25
‘%A
30
35
40
45
Distance to lake (km) Fig. 4. Prevalence of the two schisrosomes in relation fo distance from the shore of Lake Victoria
the threshold for mass treatment (WHO, 1993). Indeed, 83% of schools had a combined prevalence in excess of 50%. Furthermore, hookworm occurs more often than not as a multiple infection with schistosomiasis, which suggests that both hookworm infection and schistosomiasis could be usefully treated using a common delivery system (BUNDY et al., 1991; PARTNERSHIP FOR CHILD DEVELOPMENT, 1997). These conclusions support the concept of a generally applicable school-based strategy but that control needs to be assessed according to local ptevalences (BROOKER et al., 1999), which will depend crucially on the factors that determine the local spatial distributions. In addition
(A S. PZUYZSOX~, 6 S. haemacobium).
the appropriateness of any school-based strategy needs to be examined in relation to the proportion of children attending school and any differential risks of infection for those children in or out of school. Acknowledgement
The authors thank the Magu District Education Officer, and all the teachers and schoolchildren in the district for participating in the study. Gratitude is also extended to Mr H. Nagai, Mr J. Stevenson, and Mr H. Moyo for assistance in fieldwork and Miss Violet Kiwelu for entering the data in the computer. We thank Professor Charles Kihamia and the staff of Ushirikiano wa Kumwendeleza Mtoto Tanzania (UKUMTA) for their assistance with logistic support for the project. The fieldwork was
502
N. J. S. LWAMBO ETAL.
funded by the Wellcome Trust. N. J. S. L. is in receipt of a Wellcome Trust Research Development Award in Tropical Medicine. S. B. is in receipt of a Wellcome Trust Prize Studentshiu. D. A. P. B. and H. G. aratefullv acknowledge the SUDDORof the’ Wellcome Trust.
References Booth, M. & Bundy, D. A. P. (1992). Comparative prevalences of Ascark lumbrikoides, Trichurik trichiura, and hookworm infections and the prospects for control. Parasitology, 105, 151-157. Booth, M., Bundy, D. A. I’., Albonico, M., Chwaya, H. M., Alawi, K. S. & Savioli, L. (1998a). Associations among multiple geohelminth species infections in schoolchildren from Pemba Island. Parasitology, 116, 85-93. Booth, M., Mayombana, C. & Kilima, P. (1998b). The population biology and epidemiology of schistosome and geohelminth infections among schoolchildren in Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene, 92,491-495. Brooker, S.. Booth, M. & Guvatt, H. L. (1999). Comoarisons of schist&me andgeohelmhth infection pre;alenceg in schoolaged children from selected areas of Africa: implications for rapid assessment and combined control. Transactions of the Royal Society of Tropical Medicine and Hygiene, 93 125- 126. Buck, A. +, Anderson, R. I., MacRae, A. A. &Fain, A. (1978). Epidemiology of poly parasitism. I. Occurrence, frequency and distribution of multiple infections in rural communities in Chad, Peru, Afghanistan, and Zaire. Tropenmedizin und Parasitologic, 29, 6 l-70. Bundy, D. A. P. & Blumenthal, U. (1990). Human behaviour and epidemiology of helminth infection: the role of behaviour in exposure to infections. In: Parasitism and Host Behaviour, C. J. Barnard &J. M. Behnke (editors). London: Taylor and Francis, pp. 264-289. Bundy, D. A. P., Chandiwana, S. K., Homeida, M. M. A., Yoon. S. & Mott. K. E. (1991). The enidemiolodcalimplications bf a multipl&infec&on approach-to the co&o1 of himan helminth infections. Transactions of the Royal Society of Tropical Medicine and Hygiene, 85, 274-276. Chunge, R. N., Karumba, I’. N., Nagelkerke, N., Kaleli, N., Wamwea, M., M&so, N., Andala, E. 0. & Kinoti, S. N. (1991). Intestinal parasites in a rural community in Kenya: cross-sectional surveys with emphasis on prevalence, incidence, duration of infection, and polyparasitism. East African MedicalJournal, 68, 112-123. Chunge, R. N., Karumba, N., Ouma, J. H., Thiongo, F. W., Sturrock, R. F. & Butterworth, A. E. (1995). Polyparasitism in two rural communities with endemic Schistosoma mansoni infection in Machakos District, Kenya. Journal of Tropical Medicine and Hygiene, 98,440-444. Doumenge, J. P., Mott, K. E. & Cheung, C. (1987). Atlas of the Global Distribution of Schistosomiasis. Bordeaux: Presses Universitaires de Bordeaux. Hall, A., Orinda, V., Bundy, D. A. P. & Broun, D. (1997). Promoting child health through helminth control-a way forward? Parasitology Today, 13,4 1 l-4 13.
Kihamia, C. M. (1981). Intestinal helminths in Tanzania. Dares-Salaam Medical Journal, 8, 127 - 129. Lwambo,N. J. S.,Bundy,D.A. P. &Medley, G. F. H. (1992).A new approach to morbidity risk assessment in hookworm endemic communities. Epidemiology and Infection, 108, 469-481. McCullough, F. S. (1972). The distribution of Schistosoma mansoni and S. haemawbium in East Africa. Tropical and Geographical Medicine, 24, 199-207. Michelson, M. K., Azziz, F. A., Gamil, F. M., Wahid, A. A., Richards, F. O., Juranek, D. D., Habib, A. M. & Spencer, H. C. (1993). Recent trends in the prevalence and distribution of schistosomiasis in the Nile delta region. American 3ournal of Tropical Medicine and Hygiene, 49,76-87. Nelson, G. S. E. (1958). Schtiwsoma mansoni infection in the West-Nile district of Uganda. Part II. The distribution of S. mansoni with a note on the probable vectors. East African MedicalJournal, 35,335-344. Nelson, G. S. E. (1959). Schiswsoma mansoni infection in the West-Nile district of Uganda. Part V. Host-parasite relationships. EastAfrican MedicdJoumal, 36,29-34. Parmership for Child Development (1997). Better health, nutrition and education for the school-aged child. Transactions of the Royal Society of Tropikal Medicine and Hygiene, 91, l-2. Partnership for Child Development (1998). The health and
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school-based health programmes in Ghana and Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene, 92,254-261. Picquet, M., Emould, J. C., Vercruysse, J., Southgate, V. R., Mbaye, A., Sambou, B., Niang, M. & Rollinson, D. (1996). The epidemiology of human schistosomiasis in the Senegal river basin. Transactions of the Royal Society of Tropical Medicine and Hygiene, 90, 340-346. Savioli, L., Renganathan, E., Montresor, A., Davis, A. & Behbehani, K. (1997). Control of schistosomiasis-a global picture. Parasitology Today, 13,444-448. Stoltzfus,, R. J., Chwaya, H. M., Tielsch, J. M., Schulze, K. J., Albomco, M. & Savioli, L. (1997a). Epidemiology of iron deficiency anemia in Zanzibari schoolchildren: the importance of hookworms. American Journal of Clinical Nutrition, 65, 153-159. Stoltzfus, R. J., Albonico, M., Tielsch, J. M., Chwaya, H. M. & Savioli, L. (1997b). Linear growth retardation in Zanzibari school children. Journal of Nutritikn, 127, 1099- 1105. Webbe, G. (1962). The transmission of Schistosoma haematobium in an area of Lake Province, Tanganyika. Bulletin of the World Health Organization, 27, 59-85. WHO (1993). The Control of Schistosomiasis. Geneva: World Health Organization, Technical Report Series, no. 830.
Received 12 March 1999; revised 6 May publication 2 June 1999
1999; accepted for
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