Summary
Intestinal helminths, schistosomiasis and malaria have been recognized for decades to be major public health problems in Zanzibar, United Republic of Tanzania. During the evaluation of the impact of the Zanzibar Helminth Control Programme, baseline parasitological data on 3,605 schoolchildren were collected in Pemba Island. Prevalence of intestinal helminth infections was 72%, 94% and 96% for Ascaris lumbricoides, Trichuris tichiura and hookworm, respectively. Thirty one percent of children tested positive for haematuria, a reliable indicator of urinary schistosomiasis in the study area. Malaria parasites were found in 61% of children. Hookworm infections and haematuria were more prevalent in boys. Sixty seven percent of the children were infected with all three helminths, and 28% of children harbored double infections. No association was found between intestinal helminths and schistosomiasis or malaria. Children living in rural areas were more heavily infected with hookworms, schistosomiasis and malaria compared to children in towns. Results from this study provided relevant information for designing a Plan of Action for the integrated control of Filariasis, Intestinal Helminths, Malaria and Schistosomiasis in Zanzibar.
Introduction
It is widely recognized that schoolchildren carry the heaviest burden of morbidity due to intestinal helminths and schistosomiasis infection (1). Apart from the morbidity associated with acute infections, the burden of chronic parasitic infections may affect physical fitness (2), cognitive performance (3), nutritional status and growth (4) and school attendance (5) of school age children. Acute and chronic malaria infections are considered an important factor affecting the performances of school age children in endemic areas (6).
Parasitic infections have been recognized for decades to be major public health problems in Zanzibar, United Republic of Tanzania (7–9). Malaria is the major public health problem accounting for more than 30% of child mortality (10). The present strategy of malaria control is based on early diagnosis and prompt case treatment. Major constraints are the lack of an efficient referral system, increasing resistance of Plasmodium falciparum to chloroquine and shortage of second line antimalarial drugs. Schistosomiasis control was initiated in 1986 through a school-based approach and was integrated in 1994 within a National Plan of Action for the control of Schistosomiasis and Intestinal Helminth Infection. The strategy adopted was based on regular chemotherapy of schoolchildren with praziquantel and mebendazole administered as single doses in association with health education sessions. Children were selected for treatment with praziquantel on the basis of the presence of haematuria (7), while mebendazole was given as targeted mass treatment due to the high prevalence and intensity of helminthic infection (8). An inexpensive and effective drug and health education delivery system was set up through the teachers with supervision from health staff of the Helminth Control Programme.
In 1994 the Ministry of Health of Zanzibar, in collaboration with the World Health Organization and The Johns Hopkins University, recognized the need to evaluate the impact of the Helminth Control Programme. A large scale longitudinal survey was planned to collect nutritional and parasitological data on growth, iron deficiency, vitamin A status, malaria, haematuria and prevalence and intensity of soil transmitted nematodes infection in school children. The baseline nutritional status data have been published elsewhere (11). The epidemiology and the geographical distribution of parasitic infections, their association and the implication for integrated control are presented here.
Materials and methods
The Survey was conducted on the island of Pemba, Tanzania by the staff of the Pemba Helminth Control Programme. Important features of the island have been described in detail elsewhere (7)
The survey was carried out in April-May 1994 12 schools, 3 from each district, where randomly selecting from the 72 schools on Pemba Island. From these schools 3,944 children enrolled in 76 morning classes of standards 1-4 were invited to participate in the study. 3,605 children participated in the survey.
In every school, demographic information, weight, height and stool, urine and blood samples were collected from each child. The sample collection rates were 100%, 99% and 97% for blood, urine and stool samples, respectively. Urine was tested with a reagent strip for semiquantitative values of haematuria (Hemastix, Ames-Miles Laboratories, Helkhart, IN). In this population, microhaematuria is diagnostic for urinary schistosomiasis (69% sensitivity and 88% specificity) (12). Children testing positive for visual haematuria were treated with praziquantel 40 mg/kg body weight. Haemoglobin, erythrocyte protoporphyrin and serum ferritin were assessed as part of the nutritional evaluation (11). Those with severe anaemia (Hb below 7 gram/dl) received mebendazole 500 mg as a single dose and ferrous sulphate 25 mg tablets twice a day for one month. A malaria thin and thick smear was also made for each child. Children with fever were treated with a standard dose of pyrimetamine-sulfadoxine according to weight.. All children were treated with mebendazole 500 mg as a single dose at the end of the trial.
In the laboratory, stool samples were processed by the Kato-Katz technique according to WHO recommendations (13) and examined for helminth eggs; samples containing more than 10,000 eggs were reexamined using a modified Stoll dilution technique (14). Thick and thin blood smears were stained with 3% Giemsa solution and malaria parasites were counted against leucocytes to calculate parasitemia per microliter of blood (13), and identified by species. Quality control for malaria and intestinal helminths, was performed by two supervisors by reexamining 10% of the slides chosen at random. Agreement between readers was excellent for the presence of malaria parasitemia (k=0.93) and parasite density were also highly reliable with an interclass correlation of 0.85. Interclass correlation between staff and quality control readings were 0.88 for Ascaris lumbricoides egg per gram (epg), 0.79 for Trichuris trichiura epg, and 0.89 for hookworm epg. Data were entered into a microcomputer using the Epi-info package.
Statistical analysis
Intensity of intestinal helminth infections were measured by the eggs per gram of faeces (epg). The geometric mean was used to normalize the over dispersed distribution of worm intensity. Infections were classified as light, moderate and heavy according to WHO criteria given in table 2 (15), for hookworm infection categories where 2,000 and 5,000 epg were used to define the lower boundaries of moderate and heavy infections, respectively. Differences between prevalence were tested by Chi square statistic and means were compared using Student's t statistic. Associations between parasites infections were investigated by 2x2 contingency tables for each combination of parasites. The association between parasite infections was measured using the ratio of prevalence and tested using the Chi square statistic.
Table 2.
Prevalence and intensity categories of intestinal helminths, malaria and haematuria in Zanzibari schoolchildren.
| A.lumbricoides | T.trichiura | Hookworms | Malaria | Haematuria | |||
|---|---|---|---|---|---|---|---|
| Prevalence | 72.0% | 96.0% | 93.7% | 60.6% | 30.5% | ||
| Intensity (epg) | (Parasite/μl of blood) | ||||||
| Negative | 28.0% | 4.0% | 6.3% | 0 | 39.4% | Negative | 69.5% |
| Light | 51.7% | 54.9% | 74.7% | 1-999 | 47.0% | Microhaematuria + | 16.0% |
| Moderate | 20.2% | 40.1% | 15.5% | 1000-4999 | 12.6% | Microhaematuria ++ | 11.0% |
| Heavy | 0.1% | 1.0% | 3.5% | 5000+ | 1.0% | Visual haematuria | 3.5% |
| A.lumbricoides | T.trichiura | Hookworms |
|---|---|---|
| Light=1-4999 epg | Light=1-999 epg | Light=1-1999 epg |
| Mod=5000-49999 epg. | Mod=1000-9999 epg. | Mod=2000-4999 epg. |
| Heavy= 50000+ epg | Heavy= 10000+ epg | Heavy= 5000+ epg |
Results
The demographic characteristics of the study population are shown in Table 1.
Table 1.
Characteristics of study sample
| Age (y) | % frequency |
|---|---|
| < 7 | 1.3 |
| 7.0 - 8.9 | 20.4 |
| 9.0 - 10.9 | 44.1 |
| 11.0 - 12.9 | 26.0 |
| > 13 | 8.2 |
| Sex (% boys) | 51.8 |
| Sex ratio by age (% girls) | |
| < 7 | 50.0 |
| 7 - 8 | 51.1 |
| 9 - 10 | 51.2 |
| 11 - 12 | 44.9 |
| 13 - 14 | 36.8 |
| > 14 | 13.9 |
| Children in rural schools | 80.6 % |
Late school enrolment and Progressive drop-out of girls characterize this school population.
The children were hazily infected by parasites (Table 2). The prevalence of intestinal helminth infections was 72%, 94% and 96% for A. lumbricoides, T. trichiura and hookworm, respectively. 30% of the children tested positive for haematuria. Malaria parasites were found in 61% of the children but parasitemia was of low density, 47 % of children had less than 1,000 parasites per microliter of blood and only 1% had more than 5,000 parasites per microliter of blood. All infections were P. falciparum; in less than 5% of slides P. malariae was also identified.
Hookworm infection was more prevalent in boys who were also more heavily infected (table 3).Visual haematuria was 4.8% in boys and 2.2% in girls (relative prevalence 2.21 for boys, 95% CI 1,51-3,22). Microhaematuria was also more prevalent in boys but this difference was less dramatic.
Table 3.
Prevalence of parasitic infections by sex, age and rural or urban location
| Boys n=1851 |
Girls n=1720 |
Age < 10 n=1565 |
Age >= 10 n=1872 |
Rural n=2905 |
Urban n=700 |
All n=3578 |
|
|---|---|---|---|---|---|---|---|
|
A. lumbricoides any infection moderate +heavy infection* |
73.4 21.9 |
70.4 18.6 |
74.4 23.1 |
70.0 ** 18.0 *** |
72.0 20.3 |
||
|
T. trichiura any infection moderate + heavy infection* |
95.9 42.5 |
96.1 39.6 |
96.4 43.2 |
95.7 39.3† |
96.0 41.1 |
||
| Hookworm any infection moderate + heavy infection* |
94.7 21.1 |
92.7* 16.8** |
93.4 18.4 |
94.1 19.4 |
94.2 21.8 |
91.8* 7.4*** |
93.7 19.0 |
| Malaria any parasitemia >1,000 parasites/μl |
60.6 13.8 |
60.7 13.4 |
45.7 15.8 |
54.3 11.7 *** |
62.4 13.8 |
91.8* 7.4* |
60.6 13.6 |
| 29.0 | |||||||
| Total hematuria Visual haematuria Microhaematuria # |
32.6 4.8 28.4 |
28.1** 2.2*** 26.3 |
3.5 26.8 |
31.6 3.5 28.5 |
3.8 31.3 |
2.2* 16.0*** |
30.5 3.5 27.0 |
Prevalence and intensity of A.lumbricoides infection and intensity of T.trichiura was slightly lower in older children (table 3). Malaria parasitemia (>1,000 parasites/ microliter) was also lightly in younger children (p<0.001). Prevalence and intensity of Hookworm and S. haematobium infections did not differ by age.
The prevalence of malaria parasitemia hookworm infection and haematuria was smaller in urban than rural schoolchildren (Table 3) This difference was small for malaria but was large for hookworm infection and haematuria.
Multiple infections with helminths were common. Only one child was negative for all the parasites. 67.2% of children were infected with all 3 helminths and 28.0% of them harbored double infections. The association between each pair of geohelminths, both for prevalence and intensity, was higher than expected by chance (Table 4). Children free from infection due to any one of the geohelminths were more likely to be free from infection of any of the other two helminths. The pairwise relative prevalence of not being infected varies between 2.0 (CI= 1.44 - 2.78) for A. lumbricoides and T. trichiura and 2.97 (CI= 1.95-4.31) for T. trichiura and the hookworms. In contrast there was a negative association between hookworm infection and haematuria (Table 5).
Table 4.
Associations between geohelminth infections categories.
| n | Trichuris | ||
| <1,000 epg | ≥1,000 epg | ||
| Hookworm | |||
| <2,000 epg | 2783 | 65.9% | 34.1% |
| ≥2,000 epg | 653 | 28.9% | 71.1% |
| n | Ascaris | ||
| <5,000 epg | ≥5,000 epg | ||
| Trichuris | |||
| <1,000 epg | 2024 | 91.0% | 9.0% |
| ≥1,000 epg | 1412 | 63.5% | 36.5% |
| n | Hookworm | ||
| <2,000 epg | ≥2,000 epg | ||
| Ascaris | |||
| <5,000 epg | 2739 | 85.8% | 14.2% |
| ≥5,000 epg | 697 | 62.0% | 38.0% |
p< 0.0001
Table 5.
Hookworm infection by haematuria
| n | Haematuria | ||
|---|---|---|---|
| Neg | Pos | ||
| Hookworm | |||
| Neg | 215 | 56.8% | 43.2% |
| 70.2% | 29.8% | ||
| Pos | 3214 | ||
p<0.001
Discussion
We have documented a very heavy burden of parasitic infections in Zanzibari schoolchildren. A number of other recent studies in East Africa have found high rates of geohelminth infections, especially in coastal areas (16–18). Although the prevalence of infection with any helminth varies among these studies, they have all found, as we did, that most schoolchildren are infected with at least one helminth. However, the intensity of geohelminth infections from our survey, particularly of hookworms, is striking. The rates are higher than in other studies of African schoolchildren and from other parts of the world such as Jamaica (5), India (19) and China (20).
We also found that 31% of schoolchildren in our study had haematuria a reliable indicator of schistosomiasis infection in this population (12). This is the average prevalence of haematuria maintained by the ongoing schistosomiasis control programme, based on yearly selective treatment of children in schools where hematuria is more than 20%. This survey was performed about ten months after the previous treatment with Praziquantel. The 54% prevalence estimated in 1986, before the intervention, is similar to the prevalence found in other studies in sub-Saharan Africa, such as the 76.4% and 55% prevalence found respectively in Niger (21) and in Ethiopia (18). The chronic loss of blood in urine was recognized by Prual et al. (21) to be an important cause of iron-deficiency anaemia.
We found no difference in either prevalence or intensity of A.lumbricoides and T. trichiura infection by sex: boys had slightly heavier hookworm infection. These results are in agreement with other studies from Madagascar (16) and Nigeria (22).
We also found that visual haematuria in boys was more than twice as prevalent in girls. This is in agreement with several other studies which have found higher rates of schistosomiasis among boys, possibly reflecting higher exposure to infection due to closer contact with water bodies (18, 23, 24).
We found that A.lumbricoides and T. trichiura infections decreased after age 10, but, there was no change of hookworm infection with age. Others have found that infection with A.lumbricoides and T. trichiura, in school children remained constant with age, whereas the intensity of hookworm infection increased steadily with age (25).
Finally, we looked at the interaction between different parasites. We found a strong positive association among the three helminths, as demonstrated also by Booth et al. (26) with data from the same environment. Although we expected A.lumbricoides and T. trichiura to be most strongly associated, our findings suggest that frequent contacts with soil contaminated with human faeces, equally expose the children to all three geohelminth infections regardless of oral or percutaneous transmission. Although Necator americanus is the predominant hookworm species on Pemba, 27% of children are infected with Ancylostoma duodenale (27), and its possible faecal-oral transmission may account in part for the association with the other geohelminths A.lumbricoides and T. trichiura. The negative association between hookworm infection and schistosomiasis is surprising. Children infected with hookworms are less likely to have haematuria. The expected positive association might have been reversed in Pemba as a consequence of the periodic treatment with Praziquantel that children have been receiving since 1986.
We also looked at the difference between children attending schools in urban and rural areas. Generally, we found similar prevalence but increased intensity of the geohelminths, in rural areas. These findings contrast with those of previous results (28) in the same population, in a smaller sample size. It is interesting to note that in rural areas where transmission is more intense and prevalence is very high, higher exposure is reflected only by higher intensity of infection. As expected we also found a large difference in schistosomiasis, with the prevalence of hematuria almost doubled in rural children. The strong association between schistosomiasis and water bodies and the availability of piped water in urban areas are likely to account for this difference. Malaria parasitemia was also higher in rural schoolchildren. Malaria inoculation rate might be lower in urban areas because of lower mosquito density and the more common use of bednets (29). Urban children was also have better access to medication than children living in rural areas.
In conclusion, the parasite burden is distributed broadly, and, although there is a difference between urban and rural areas, parasitic infections are still high in both. The burden of disease associated with parasitic infections has been shown to have a negative impact on iron status of schoolchildren in this population (11). The iron status of our population was very poor: 62% of children were anaemic and 78% of anaemia was associated with iron deficiency. Iron-deficiency anaemia is an important public health problem in Zanzibar schoolchildren (11). Although schistosomiasis and malaria can contribute to its etiology, the most important cause in schoolchildren are the intestinal blood loss due to hookworm infections and poor diet (11,30).
Our findings have a number of implications for public health intervention in Zanzibar. First, the high prevalence of intestinal helminthiasis and schistosomiasis among schoolchildren justifies the implementation of school-based interventions, such as periodic anthelminthic treatment. Because of the enormously high prevalence and the availability of safe and inexpensive single-dose drugs, screening individuals for selective treatment is not cost-effective. Indicators for morbidity such as intensity of infection and visual haematuria on a sample of the population should be sufficient for monitoring and guiding control programme. Similarly, the relatively even distribution by age and by sex does not justify a priori selection of schoolchildren for treatment. However, the large decrease of school attendance in girls with increasing age will cause a large proportion of older girls to be missed through school-based interventions in Zanzibar. This is an important and unresolved challenge because uncontrolled parasitic infections will cause women to be their reproductive lives at high risk of anaemia.
These results advocate the need for integrated control, also taking into account other endemic diseases, like filariasis, that can be controlled using a similar strategy. The presented results have led to the preparation of a Plan of Action for the Integrated control of Intestinal Helminths, Filariasis, Malaria and Schistosomiasis by the Ministry of Health of Zanzibar with the technical support from the Division for Control of Tropical Diseases of the World Health Organization (31). Malaria control is an especially complex issue, but it can be implemented in an Integrated Disease Control Programme where resources are shared and intervention is carried out at the central and at the community level with the supervision and coordination from the District Health Management Team (31).
Acknowledgments
The authors thank the Pemba Public Health Team for their excellent work in collecting these data. The study was funded by a cooperative agreement between the Office of Health and Nutrition, United States Agency for International Development and the Johns Hopkins University. Additional support was provided by the WHO Programme of Control of Intestinal Parasitic Infections.
Contributor Information
M. Albonico, Division of Communicable Diseases, World Health Organization.
H.M. Chwaya, Ministry of Health, Zanzibar, United Republic of Tanzania.
A. Montresor, Division of Control of Tropical Diseases, World Health Organization.
K.S. Alawi, Ministry of Health, Zanzibar, United Republic of Tanzania.
L. Savioli, Schistosomiasis and Intestinal Parasites Unit, Division of Control of Tropical Diseases, World Health Organization.
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