Prevalence and factors associated with persistent transmission of Schistosoma haematobium among primary school children after five rounds of mass drug administration using praziquantel: A cross sectional study in Mkuranga district,Tanzania

Introduction

Globally, over 200 million people are infected with urinary schistosomiasis, and 85% of these cases are found in Sub-Saharan Africa where children aged 5-19 years are at a higher risk of infection. In Tanzania, all administrative regions have some level of schistosomiasis infection, ranging from 12.7% to 87.6%, with higher prevalence along the coast of the Indian Ocean and shores of Lake Victoria. ¹

The Global schistosomiasis control programme encourages the endemic communities to adopt mass drug administration (MDA) using praziquantel (PZQ) as a control strategy for urinary schistosomiasis based on existing levels of prevalence. Through the Ministry of Health in Tanzania the campaign for mass drug administration (MDA) using praziquantel was adopted and launched in July 2005 in various phases. Phase I of MDA implementation was conducted in 2005 and 2007 in eleven regions, while Phase II was conducted in 2008 in six regions which are highly endemic for S. haematobium. Communities were selected for MDA on the basis of existing prevalence levels of Schistosomiasis. In schools or in areas with prevalence of <10% praziquantel is made available in local health facilities, in areas with prevalence of 10–50% praziquantel MDA is given to all school age children plus other high-risk groups in the community. ¹

The Pwani region in coastal Tanzania was involved in the praziquantel MDA campaigns during Phase II implementation in 2011, which covered six districts including Mkuranga district. ²

Before MDA in Mkuranga district, the prevalence of frank haematuria among school children was 9.7%, equivalent to an average of 10% egg positivity prevalence by microscopic sample analysis for S. haematobium, However, according to the World Health Organization, if a MDA had been conducted for five consecutive years in an area, the Schistosoma prevalence was expected to decline.

Methods

Our study was conducted in Mkuranga district located near water bodies. Mkuranga lies between latitude 6° 35’ and 7° 30’ S and between longitudes 38° 45’ and 39° 30’ E, and has several rivers, ponds, marshy swamps and irrigated rice fields which provide a suitable environment for Bulinus snail as an intermediate host for S. haematobium. Lack of hygienic urine disposal and certain play habits predispose schoolchildren to infections.^3,4

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Figure 1.

A map of Tanzania showing the study area (Mkuranga district in Pwani region).

A quantitative cross-sectional study was conducted. Primary school pupils of standard II-VII who attended school on the day of data collection were included in the study. Pupils from standard I were excluded because they did not participate in earlier rounds of MDA, since they had not yet joined primary school. School children with a history of being clinically ill and who had used anti-schistosome drugs within a period of three months before the study, were also excluded.

A multi-stage sampling technique was used to obtain pupils from their respective schools and classes. In the first stage, four out of twelve primary schools located near water bodies were randomly selected. In the second stage of sampling, based on probability proportional to size (PPS), 116, 98, 95 and 87 pupils were randomly selected from Kilimahewa, Kitumbo, Tengelea, and Kipara primary schools respectively to complete the sample size of 396 pupils.

Data collection was carried out by investigators and four trained research assistants. Parasitological examination of urine specimens and quantitative questionnaire interviews were used for data collection. Each pupil was interviewed regarding, socio-demographic characteristics, drug uptake status and water contact activities. After the interviews, pupils were instructed and guided on how to collect a urine sample and were provided with a sterile wide-mouthed plastic container, 50mls volume with a screw cap, labeled with their identification numbers) and asked to bring a clean terminal catch of urine. The collected urine samples were immediately mixed with one drop of 37% formalin to preserve the samples and fix the eggs to prevent hatching and bacterial growth. ⁵ After urine collection, all preserved samples were placed in a box and transported to the Muhimbili National Hospital (NMH) laboratory for examination by the principal investigator, assisted by two laboratory technicians.

10mls of each urine sample was syringed and filtered using a 25 mm diameter filter holder and a nuclear pore filter with twelve micrometer pores. The filtrate from the filter was placed on a glass slide and microscopically examined for Schistosoma haematobium ova (magnification: 10 × 40). ⁶ Samples found to have at least one ovum were recorded as infected and the number of ova present in each specimen was counted and recorded on the laboratory data collection form. Furthermore, several pupils in the study area were observed to determine their actual water contact activities that might expose them to Schistosoma haematobium infection.

Questionnaires were checked for correct use of codes and completeness. Data were coded,validated and analyzed using SPSS version 22.0. Descriptive statistical analysis was performed to summarize socio-demographic data, infection status, drug uptake and types of water contact activities. Pearson's chi-square statistical tests were used to compare proportions between groups. Logistic regression analyses were performed to determine association between infection status as an outcome and other independent variables. Crude odds ratios (COR) were estimated by bivariate logistic regression analysis to determine factors to be included in the final model. Thereafter, adjusted odds ratios (AOR) were computed using multivariable logistic regression analysis by taking all variables with significant association in a bivariate analysis. The statistical significance level of P < 0.05 and 95% confidence interval (CI) were used in all analysis.

Results

A total of 396 primary school children from standard II-VII with a mean age of 11 years, range between 6 to 16 years participated in the study. More than half 55.1% (218) of pupils were aged ≤11 years, females were 51.3% (203) and more than a quarter 29.3% (116) studied at Kilimahewa primary school (Table 1). The overall prevalence of S. haematobium infection in Mkuranga district was 5.8% and there was no variation of the prevalence across socio-demographic groups (Table 1).

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Table 1.

Prevalence of S. haematobium infection according to socio-demographic characteristics (n = 396).

Variable	Category	Examined (N)	Positive (%)
Age group	≤11	218	15(6.9)
	12–13	120	8(6.7)
	≥14	58	0(0.0)
Gender	Female	203	11(5.4)
	Male	193	12(6.2)
Class level	Standard II-III	131	10(7.6)
	Standard IV-V	137	7(5.1)
	Standard VI-VI	128	6(4.7)

Out of 396 pupils, more than half 60.1% (238) admitted swimming in the water bodies compared to other water contact activities (Table 2). Some 11.6% (46/396) pupils were observed to contact water bodies during their usual social activities, the majority being observed swimming, bathing, washing clothes and washing legs in a pond (Figure 1 & 2).

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Figure 2.

Water contact activities observed at Kipara and Kilimahewa pond.

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Table 2.

Type of water contact activities among primary school children (N = 396).

Water contact activity	N (%)
Fetching water in a pond	142(35.9)
Washing clothes in a pond	135(34.1)
Swimming in a pond	238(60.1)
Bathing in a pond	137(34.6)
Vegetable gardening	146(36.9)
Fishing	134(33.8)
Crossing a river/stream on wayto school	107(27.0)
Cross a pond on way to school	105(26.5)
Cross swamp area on way to school	93(23.5)
Cross temporary water pools	133(33.6)
Cross paddy field on way to school	114(28.8)
Watering animals	78(19.7)
Washing legs on way to school	146(36.9)

Almost three quarters, 72.5% (287) of the children had participated in MDA campaigns at some point, with 40.7% in only one round, 36.6% in two rounds, 17.8% in three rounds and 4.9% in more than four rounds. (Figure 3)

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Figure 3.

Proportion of pupils who participated in MDA campaigns.

In both bivariate and multivariate analysis, water contact activities were significantly associated with S. haematobium infection (P < 0.2; P < 0.05 respectively). (Table 3).

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Table 3.

Factors associated with S. haematobium infection: Logistic Regression Analysis.

Bivariate			Multivariate
Variable	COR(95%CI)	P-Value	AOR(95%CI)	P-value
Age group
≤11	Ref
12–13	0.97(0.40–2.35)	0.940	0.53(0.23–1.22)	0.134
≥14	0.00(0.00–0.00)	0.997
Gender
Female	0.86(0.37–2.01)	0.734	0.95(0.33–2.75)	0.931
Male	Ref
MDA uptake
Yes	Ref
No	0.72(0. 26–1.99)	0.524	0.50(0.14–1.75)	0.276
Fetching water
Yes	3.27(1.35–7.91)	0.009	0.39(0.11–0.99)	0.048
No	Ref
Washing clothes
Yes	3.94(1.63–9.58)	0.002	0.80(0.27–2.34)	0.679
No	Ref
Swimming
Yes	4.74(1.38–16.23)	0.013	0.12(0.03–0.57)	0.007
No	Ref
Bathing
Yes	4.76(1.91–11.88)	0.001	0.17(0.05–0.53)	0.002
No	Ref
Fishing
Yes	4.00 (1.65–9.70)	0.002	0.23(0.074–0.73)	0.012
No	Ref
Gardening
Yes	2.84(1.20–6.74)	0.018	0.75(0.255–2.18)	0.593
No	Ref
Cross river/stream
Yes	2.98(1.27–6.97)	0.012	0.38(0.13–1.10)	0.075
No	Ref
Cross a pond
Yes	3.59(1.53–8.41)	0.003	0.20(0.07–0.59)	0.003
No	Ref
Cross paddy field
Yes	4.20(1.76–5.76)	0.001	0.09(0.03–0.31)	0.000
No	Ref

Key: χ² = Pearson Chi-square test; COR: Crude odds ratio AOR: Adjusted odds ratio P < 0.05.

Discussion

Our study indicates that urinary schistosomiasis is still a public health problem among school pupils with a significant prevalence of 5.8%. Transmission has been demonstrated to be influenced by high-risk water contact activities. Such lifestyle and activities be unavoidable. Reduction of contact with potentially infected water may be achieved through piped water systems, and water treatment by killing the cercaria or extermination of the snail species vectors using molluscides which are more selective to Bulinus species and less harmful to the aquatic ecosystem. ⁷ We also note that pupil participation in MDA campaigns was below the WHO goal. ⁸

We recommend that MDA campaigns need to be accompanied by minimizing contact with infected water.