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Urinary schistosomiasis among schoolchildren in Yemen: prevalence, risk factors, and the effect of a chemotherapeutic intervention

Al-Waleedi, Ali A.a; El-Nimr, Nessrin A.c; Hasab, Ali A.c; Bassiouny, Hassan K.d; Al-Shibani, Latifa A.b

The Journal Of The Egyptian Public Health Association: December 2013 - Volume 88 - Issue 3 - p 130–136
doi: 10.1097/01.EPX.0000441277.96615.96
Original articles
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Background Schistosomiasis is one of the most important public health problems in Yemen. The prevalence of urinary schistosomiasis varies considerably across different parts of Yemen and was estimated to be 10% among schoolchildren in Sana’a. Praziquantel (PZQ) is highly effective against all five major human species of schistosomes.

Objectives The aim of the present work was to estimate the prevalence of urinary schistosomiasis, describe the risk factors associated with its endemicity, and implement and assess a chemotherapeutic intervention using PZQ in a village in Yemen.

Patients and methods The sample included 696 schoolchildren from a village in Abyan Governorate. During the baseline school survey, personal, sociodemographic, and environmental data, and data on practices in relation to water contact were collected from each study participant using a predesigned structured questionnaire. Urine samples from each participant were examined for macrohematuria and the presence of Schistosoma haematobium eggs. The chemotherapeutic intervention was assessed 3 and 6 months after the treatment and certain indicators were calculated.

Results The prevalence of S. haematobium was 18.1%. The main significant risk factors were male sex; proximity of houses to water ponds; and using pond water for swimming, agricultural activities, and for bathing in houses. PZQ treatment reduced the prevalence of infection and decreased the prevalence of high-intensity infection. Survival analysis showed that the probability of residual infection also dropped after the treatment intervention.

Conclusion and recommendations Male sex and using pond water for various activities were the main significant risk factors associated with urinary schistosomiasis. PZQ is still a cornerstone drug in reducing or eliminating morbidity associated with schistosomiasis infection. Health education programs tailored for the community are required for the control and prevention of urinary schistosomiasis. To address schoolchildren, school curricula should include lessons about urinary schistosomiasis.

aDepartment of Community Medicine, Public Health and Family Medicine, Faculty of Medicine, Aden University, Aden

bDepartment of Medical Parasitology, Faculty of Medicine and Health Sciences, Sana’a University, Sana’a, Yemen

Departments of cEpidemiology

dTropical Health, High Institute of Public Health, Alexandria University, Alexandria, Egypt

Correspondence to Nessrin A. El-Nimr, Department of Epidemiology, High Institute of Public Health, 165 El-Horrya Ave., El-Hadara, 21311 Alexandria, Egypt Tel: + 01005051138;e-mail: dr.elnimr@gmail.com; nessrine_ahmed@hotmail.com

Received June 23, 2013

Accepted August 31, 2013

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Introduction

Human schistosomiasis continues to be a global public health problem in the developing world 1,2. Because it is a chronic insidious disease, it is poorly recognized at early ages and becomes a threat to development as it disables men and women during their most productive years 2.

Schistosomiasis is the second major public health problem in Yemen after malaria 3,4. Yemen has the second highest prevalence of schistosomiasis in the Eastern Mediterranean WHO region, after Sudan 3. The prevalence rates vary considerably across different parts of Yemen. The prevalence of urinary schistosomiasis varies from 10% among schoolchildren in Sana’a, to 49 and 52% in Sada’a and Hajjah, respectively 5. In certain areas such as Taiz, infection rates as high as 100% have been reported among schoolchildren, with an overall prevalence rate of 64%. In the Hajjah province, the 11–15-year age group was reported as being most affected by Schistosoma haematobium infection (67.6%) 6. Environmental factors and expansion of agricultural facilities, with associated improvement in irrigation systems and construction of dams, have led to the generation of an optimal environment for fresh-water snails, resulting in an increase in the prevalence of schistosomiasis 7,8.

Despite safe and effective treatment for schistosomiasis being available in Yemen, and safe water supply being provided for household use in the country (51% covered), the infection rate is not expected to decrease substantially in the near future. This assumption is based on the expansion of cultivated areas associated with the Dam Construction Policy and inadequate coverage of household water supply (49% still lack household water supply). A large proportions of houses (37%) still lack latrines, and there is inadequacy in public health services and a high level of illiteracy (50%) 9. Population growth, low access to health services, and the increased number of water development projects are, among others, the main contributing factors to this problem 3.

Praziquantel (PZQ) is highly effective against all five major species of schistosomes infecting humans. In the case of S. haematobium, the cure rate in the field has been estimated to be between 80 and 95% 10. It has a good tolerability and is easily administered as a single oral dose 1,10. In addition, the drug has become less expensive. Thus PZQ remains a powerful tool for disease prevention and control 10.

The aim of the present work was to estimate the prevalence of urinary schistosomiasis, describe the epidemiologic factors associated with its endemicity, and implement a chemotherapeutic intervention using PZQ in a village in Abyan Governorate, Republic of Yemen, and then to assess its effect after 3 and 6 months.

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Patients and methods

The study was conducted in a village about 25 km away from the Capital of Abyan Governorate during the period from January 2011 to the end of August 2011. The most endemic area with urinary schistosomiasis in Abyan Governorate is the Khanfar district. The selected village is considered to be the largest village in this district and represents the most concentrated foci of high urinary schistosomiasis prevalence among school children (37.5%) 3.

The minimum required sample size was calculated to be 640 students. The calculation was based on an expected urinary schistosomiasis prevalence of 37.5% among schoolchildren 3 and the least acceptable value of 33.75%. All schoolchildren aged between 10 and 16 years in the only school in the village were included, as they amounted to 696 students (305 boys and 391 girls). Schoolchildren were the favored target group because the peak prevalence of schistosomiasis has been found in this age group 11. This children in this age group also suffer from nutritional deficiencies as they undergo a period of intense physical and mental development. Besides, there is generally good compliance from children and parents.

Estimation of the baseline prevalence of urinary schistosomiasis and identification of the main factors associated with its endemicity was carried out during the first phase of the study. A baseline school survey was conducted using both a predesigned structured questionnaire and urine analysis. Personal, sociodemographic, and environmental data, and data on practices in relation to contact with water were collected from each study participant. Each participant was to provide a urine sample. Each urine sample was analyzed for detection of visible hematuria (macrohematuria), detection of S. haematobium eggs in urine by microscopic examination using the carbolfuchsin centrifugation sedimentation technique 12, and estimation of the intensity of infection (i.e. number of eggs/10 ml urine). Accordingly, the community category diagnosis was determined on the basis of the prevalence of schistosomiasis infection (by microscopic examination) and the prevalence of macrohematuria 10.

During the second phase, an intervention approach (one group pretest post-test design) was used. The chemotherapeutic intervention program adopted depended on the community category diagnosis. The results of the first phase showed that the community category diagnosis of the studied village was moderate prevalence, defined by the WHO as less than 30% macrohematuria or greater than 10% macrohematuria, but less than 50% prevalence of infection (by microscopic examination) 10. Accordingly, PZQ (40 mg/kg body weight) was administered as a single oral dose to all infected schoolchildren.

The intervention program was assessed 3 and 6 months after treatment. All treated individuals were asked to supply urine samples to be examined for the presence of both macrohematuria and S. haematobium eggs.

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Ethical considerations

The study was approved by the ethics committee at the High Institute of Public Health. In addition, approval was obtained from the Ministry of Health and the Local Health Authority in Abyan Governorate. Before a child was included in the study, informed oral consent was obtained from the parents and the child, and it was assured that consent was obtained under confidentiality.

All the participants identified as positive for urinary schistosomiasis were treated with a single oral dose of PZQ (40 mg/kg body weight). The drug was administered under the supervision of the physician of the Health Unit and the health visitors of the school.

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Statistical analysis

Data were edited, cleaned, and analyzed using SPSS for Windows version 16.0 (SPSS Inc., Chicago, Illinois, USA). Quantitative data were described in terms of mean and SD, whereas percentage was used to describe categorical data. Pearson’s χ2-test was used for analysis of categorical data. Multiple logistic regression analysis was used to estimate the strength of association between the exposure and a binary outcome. Survival analysis was used to estimate the probability of urinary schistosomiasis infection 3 and 6 months after treatment. All statistical analyses were carried out using two-tailed tests, and a P-value of less than 0.05 was considered to be statistically significant.

The following indicators were used for the assessment in the chemotherapeutic program 13:

  • Egg-negative rate: the proportion of infected schoolchildren who were treated and had no Schistosoma spp. eggs in urine 3 months after treatment.
  • Egg-positive rate: the proportion of schoolchildren who remained positive for Schistosoma spp. eggs 3 months after treatment.
  • Reinfection rate: the proportion of schoolchildren who had no Schistosoma spp. eggs at the first examination (3 months after treatment) and who were found to be infected at subsequent examination (6 months after treatment).
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Results

Figure 1 shows that the prevalence of S. haematobium among schoolchildren was 18.1%. Table 1 shows the distribution of schoolchildren infected with and those uninfected with S. haematobium according to sociodemographic and environmental factors. Older schoolchildren had significantly higher prevalence of urinary schistosomiasis compared with younger ones. Boys showed higher rates of S. haematobium infection compared with girls. This difference was not statistically significant.

Figure 1

Figure 1

Table 1

Table 1

The higher the level of education of the schoolchildren’s parents, the lower the prevalence of schistosomiasis. This association was found to be statistically significant. Infected children were 1.63 times more likely to have uneducated mothers compared with uninfected children [odds ratio (OR)=1.63, 95% confidence interval (CI)=1.10–2.40]. Children whose fathers were farmers and mothers were housewives showed higher rates of S. haematobium infection. However, the association between the fathers’ occupation and the prevalence of schistosomiasis was not significant, whereas that between the mothers’ occupation and the prevalence of schistosomiasis was statistically significant. Infected children were 1.69 times more likely to have mothers who did not work compared with uninfected children (OR=1.69, 95% CI=1.05–2.71). The higher the crowding index, the higher the prevalence of urinary schistosomiasis. This association was statistically significant.

With regard to environmental factors, Table 1 shows that schoolchildren who did not have tap water in their houses, who lived in areas where open trenches were used for disposing sewage, and who lived near ponds had a higher prevalence of urinary schistosomiasis. The association between the presence of tap water and the prevalence of schistosomiasis was not significant, whereas the association of the type of sewage disposal system and the proximity of the houses to ponds with the prevalence of schistosomiasis was statistically significant. Infected children were 4.3 times more likely to have been living near water ponds compared with uninfected children (OR=4.26, 95% CI=2.85–6.38).

Table 2 describes the relationship between the knowledge and practices of schoolchildren with regard to water contact and their S. haematobium prevalence rates. Schoolchildren who knew that contact with pond water was a mode of transmission of schistosomiasis had a statistically significantly lower rate of schistosomiasis infection compared with those who did not know (OR=0.67, 95% CI=0.46–0.99). It is also clear from the table that children who reported contact with ponds for various activities had higher rates of urinary schistosomiasis compared with those who did not report such activities. The association between each of the activities and the prevalence of S. haematobium was statistically significant, except for using ponds for bathing cattle. The OR ranged from 2.08 to 11.9.

Table 2

Table 2

Table 3 shows logistic regression analysis with the factors affecting the prevalence of S. haematobium infection among schoolchildren as the dependent variables. All factors associated with the presence of Schistosoma spp. eggs were used to build the logistic regression model. Only five independent factors were found to significantly affect the prevalence of S. haematobium infection among schoolchildren. These factors were male sex (OR=2.47, 95% CI=1.35–4.54), living near ponds (OR=2.53, 95% CI=1.42–4.49), swimming in ponds (OR=4.44, 95% CI=2.29–8.61), using pond water for agricultural activities (OR=2.48, 95% CI=1.23–5.02), and using pond water for bathing in houses (OR=3.21, 95% CI=1.49–6.91). The model correctly classified 71.8% of cases.

Table 3

Table 3

Of 126 infected schoolchildren, 122 received PZQ treatment; thus, the calculated participation rate was 96.8%. Three months after the intervention, 114 schoolchildren of 122 were reassessed with a participation rate of 93.4%. Six months after the intervention, 104 of 114 children were reassessed with a participation rate of 93.9%.

The rate of egg positivity, intensity of S. haematobium infection, and macrohematuria 3 and 6 months after intervention are shown in Table 4. The rate of egg positivity was reduced by 51.4%, from 18.1% at the baseline survey to 8.8% 3 months after the intervention. It was further reduced by 84.5%, from 18.1% at the baseline survey to 2.8% 6 months after the intervention. The rate of egg negativity was 91.2%, whereas the reinfection rate was 0%.

Table 4

Table 4

The majority of infections (85.7%) at the baseline survey were light (<50 eggs/10 ml urine), and only 14.3% of the children had a high intensity of infection. Three months after the intervention, high-intensity infection was reduced by 100% (from 14.3 to 0%), which remained at the zero level 6 months after the intervention. In contrast, the prevalence of macrohematuria at the baseline survey was 5.6%, which increased to 10.5% 3 months after the intervention and was reduced to 2.8% 6 months after the intervention.

Applying survival analysis to determine the probability of residual infection after treatment with PZQ, the infection rate was found to drop to 0.0877 at the third month and to 0.0263 at the sixth month after the treatment intervention.

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Discussion

The results of the current study show that the prevalence rate of urinary schistosomiasis among schoolchildren in the studied village was 18.1%. This figure is lower than that reported in 2005 from the north of Sana’a (58.9%) 5 and in 2009 from Abyan and Taiz Governorates (21.4%) 3. This decrease could be attributed to the activities of the national schistosomiasis control program in Yemen.

As regards the epidemiologic factors associated with endemicity of urinary schistosomiasis in Abyan Governorate, the present study showed that the highest prevalence rate was among children of the age group 14–16 years. These findings are in accordance with those of other studies on the pattern of infection in children from Yemen 8,14. Similar findings were also reported from Côte d’Ivoire 15 and Kenya 16. With regard to sex, boys showed a higher prevalence than girls. This is probably because boys are more in contact with infested water bodies as a result of engaging in swimming and/or agriculture activities. Several studies reported a higher infection rate among male individuals compared female individuals 17–19. In contrast, a study conducted in Nigeria reported that female individuals had a higher prevalence of S. haematobium infection compared with male individuals 20.

The present results showed that a lower level of education of the children’s parents was a risk factor for urinary schistosomiasis. This could be because of the lack of proper knowledge about the disease and its prevention, which leads to the inability of the parents to properly educate their children. Similar findings were reported from Nigeria 19,21, whereas other studies found no significant relationship between the parents’ education and schistosomiasis infection among students in Yemen 9,14,22. With regard to the fathers’ occupation, the present study showed that children whose fathers were farmers had higher rates of schistosomiasis infection, probably because they joined their fathers at the farm. A similar finding was reported by Houmsou et al.19.

It was also noticed that the prevalence of S. haematobium was higher among children from families with a high crowding index. Similar findings were reported from Nigeria 21, whereas conflicting results have been reported from Brazil 23.

As regards environmental factors, the prevalence of S. haematobium infection was found to be higher among schoolchildren who did not have access to tap water, those who used open trenches or water streams for sewage drainage, and those who lived near ponds. Comparable findings were reported in Yemen by Al-Shibani 24. The present results reported a significant association between the prevalence of schistosomiasis infection and the children’s knowledge and their reported water contact frequency. These findings coincided with those reported in Yemen in 2000 9 and in 2012 22 and in Malawi 17.

The factors that were significantly associated with urinary schistosomiasis infection as shown in the logistic regression model were male sex, living near ponds, swimming in ponds, using pond water for agricultural activities, and using pond water for bathing in houses. The logistic regression analysis in the study conducted by Deribe et al.25 in Darfur showed that only age and address were independently associated with the presence of Schistosoma spp. eggs, whereas the study conducted by Houmsou et al.19 in Nigeria reported that various water-contact-related activities by children were significantly associated with schistosomiasis infection.

The main objective of schistosomiasis control is to reduce or eliminate morbidity or at least serious disease 13. PZQ is the main tool for morbidity control 26. It is a safe drug that can be delivered at the most peripheral levels of drug delivery by nonmedical personnel 27. PZQ has an overall cure rate of 60–90% in individuals living in endemic areas 13.

The current results show that the rate of egg positivity of S. haematobium was reduced from the baseline by 51.4% (from 18.1 to 8.8%) 3 months after the intervention, and there was further reduction by 68.2% (from 8.8 to 2.8%) 6 months after the intervention, with a total reduction of 84.5% from baseline prevalence to 6 months after the intervention. These findings were in accordance with those reported by many authors in Yemen 5, Burkina Faso 28, and Cameroon 29.

In schistosomiasis infection, the intensity of infection is a better indicator of morbidity than the prevalence, as it reflects the number of worms infecting the individuals, and it is also a more reliable marker of treatment success, defined as the removal of egg-laying worms 30. The marked reduction in the prevalence of high-intensity infection observed in the current study after PZQ chemotherapy suggests that even a single round of mass chemotherapy could have a sustainable impact on S. haematobium infection and associated morbidity in children. The same observation was made in several studies 31–34.

The present work provides information on some implications for chemotherapeutic intervention and probability of infection after treatment. PZQ had an impact on the prevalence. The rate of egg positivity was 8.8% and the rate of egg negativity was 92.2%. The relative contribution of high-intensity infection among egg-positive individuals was also reduced. The probability of residual infection also reduced after the treatment intervention. None of the children were reinfected after the treatment intervention.

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Conclusion and recommendations

The findings of this study indicate that S. haematobium infection is still endemic among children in Abyan Governorate, Yemen, with a high prevalence of infection among older schoolchildren and among boys. Water-contact-related activities were also among the risk factors for endemicity of urinary schistosomiasis in this area. Not only schoolchildren, but also adults are considered at risk in endemic areas. These include people with occupations involving contact with infested water, such as farmers or women whose domestic tasks bring them in contact with infested water, as in the case of parents of the studied schoolchildren. PZQ is still a cornerstone drug for reducing or eliminating morbidity associated with schistosomiasis infection. Mass chemotherapy should be considered for high and moderate prevalence areas.

Health education programs tailored for the community are required for the control and prevention of urinary schistosomiasis in the study areas. To address schoolchildren, school curricula should include lessons about urinary schistosomiasis in the community. In addition, mass and local media messages emphasizing on the risk factors and modes of transmission of schistosomiasis, as well as the hazards of using pond water for recreational, domestic, or agricultural activities should be broadcasted. Finally, educational campaigns about schistosomiasis prevention targeting parents should be conducted in endemic areas.

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Acknowledgements

The authors thank the staff of the National Schistosomiasis Control Project (NSCP) in Sana’a, the capital of Yemen, the staff of the NSCP in Abyan Governorate, the Director of the Schistosomiasis Control Program, the Director of the Health Unit, the School Director, his assistant, the school teachers, as well as the community leaders in the study village for their efforts, cooperation, and patience.

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Conflicts of interest

There are no conflicts of interest.

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Keywords:

chemotherapeutic intervention; praziquantel; prevalence; risk factors; urinary schistosomiasis

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