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 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.
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%.
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.
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.
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.
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.
Conflicts of interest
There are no conflicts of interest.
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Keywords:© 2013 Egyptian Public Health Association
chemotherapeutic intervention; praziquantel; prevalence; risk factors; urinary schistosomiasis