Introduction Schistosomiasis or bilharzia, one of the most prevalent neglected tropical diseases (NTDs), is still a public health problem in many developing countries in the tropics and subtropics with approximately 240 million infected people and about 700 million people worldwide are at risk of this infection [1]. Over 90% of the disease is currently found in sub-Saharan Africa, where more than 200,000 deaths are annually attributed to schistosomiasis, and Middle East and North Africa regions [2]–[4]. Despite intensive efforts to control the disease, schistosomiasis together with soil-transmitted helminthiasis continue to represent more than 40% of the disease burden caused by all tropical diseases, excluding malaria [5]. Schistosomiasis is mainly caused by three different species of blood-dwelling fluke worms of the genus Schistosoma namely Schistosoma haematobium (causes urinary schistosomiasis), S. mansoni and S. japonicum (both cause intestinal schistosomiasis). Clinical manifestations of schistosomiasis are associated with the species-specific oviposition sites and the burden of infection [6]. Urinary schistosomiasis is characterized by haematuria as a classical sign. It is associated with bladder and uretral fibrosis, sandy patches in the bladder mucosa and hydronephrosis that are commonly seen in chronic cases while bladder cancer is possible as late stage complication [7]. On the other hand, intestinal clinical manifestations include abdominal pain, diarrhea, and blood in the stool. In advanced cases, hepatosplenomegaly is common and is repeatedly associated with ascites and other signs of portal hypertension [8], [9]. Among the Middle East countries, Yemen has the highest percentage of people living in poverty where more than 50% of the population of nearly 25 million people lives below the poverty line [10]. The country has been unstable for several years, suffering from civil wars, a deteriorating economy and severe depletion in water resources. With regards to NTDs, Yemen is endemic for at least 8 NTDs namely soil-transmitted helminthiasis, schistosomiasis, onchocerciasis, lymphatic filariasis, leishmaniasis, fascioliasis, trachoma and leprosy. Moreover, the country ranks first in trachoma; second in schistosomiasis, ascariasis, fascioliasis and leprosy; and fourth in trichuriasis and cutaneous leishmaniasis [4]. In 2008, Yemen launched its first campaign to eliminate schistosomiasis as a national public health problem with the aim of eliminating schistosomiasis-related morbidity through annual treatment to school-age children with a financial support from the World Bank and World Health Organization (WHO) [11]. Despite of these support and efforts to control the disease in Yemen, the prevalence of schistosomiasis remains largely unchanged (since 1970s) with prominent morbidity [12]–[17]. Moreover, new foci of schistosomiasis transmission have been identified. Hence, the aims of the present study were to determine the prevalence and distribution of schistosomiasis and to identify the associated key factors of this disease among Yemeni children in rural areas which are undergoing active control and prevention surveillances. It is hoped that findings of this study will assist public health authorities to identify and implement integrated and effective control measures to reduce the prevalence and burden of schistosomiasis significantly in rural Yemen. Materials and Methods Ethical statement The study protocol was approved by the Medical Ethics Committee of the University of Malaya Medical Centre (Ref. no: 968.4). It was also approved by the Hodeidah University, Yemen and permission to start data collection was also given by the Yemen Schistosomiasis National Control Project. The head of households and children were informed about the study objectives and methods and the priority of the consent for inclusion of children. Moreover, they were informed that they could withdraw their children from the study without any consequences. Thus, written and signed or thumb-printed informed consents were obtained from all adult participants before starting the survey. Similarly, written and signed or thumb-printed informed consents were taken from parents or guardians, on behalf of their children. All the infected children were treated with a single dose of 40 mg/kg body weight praziquantel tablets. Each child swallows the tablets with some water, while being observed by the researcher and medical officer (Direct Observed Therapy) [18]. Study design A cross-sectional community-based study was carried out among children aged ≤15 years in rural areas in Yemen. Data were collected in a period of seven months from January to July 2012. In each province, two rural districts were selected randomly from the available district list and then two villages within the selected districts were considered in collaboration with the Schistosomiasis Control Project office in each province. The number of inhabitants per household was recorded and all of them were invited to participate in this study. Unique reference codes were assigned to each households and study participants. Study area This study was carried out in five provinces in Yemen namely Taiz, Ibb, Dhamar, Sana'a and Hodiedah. These provinces are endemic for schistosomiasis and undergoing active surveillances by the schistosomiasis national control project. The highest prevalence of schistosomiasis was reported in Hajjah and Taiz provinces [15], [17]. However, we could not collect samples from Hajjah during the sampling period due to civil war which occurred in 3 provinces including Hajjah. Sana'a and Dhamar represent the mountainous areas at an altitude of >2000 m above sea level with a total population of 4 million. Taiz, Hodiedah and Ibb represent the country's coastal plains and foothills at an altitude of 10 178 (44.5) Gender Males 238 (59.5) Females 162 (40.5) Residency Sana'a 77 (19.3) Taiz 76 (19.0) Ibb 69 (17.3) Hodiedah 85 (21.3) Dhamar 93 (23.3) Socioeconomic status Fathers' education level Not educated 191 (47.8) Primary school 104 (26.0) Secondary school 78 (19.5) University 27 (6.8) Fathers' occupational status Government employees/professionals 171 (42.7) Farmers 195 (48.8) Not working 34 (8.5) Working mothers 21 (5.3) Low household income ( 10 years compared to those aged ≤10 years (37.6% vs 27.0%; χ2 = 5.135; P = 0.023). Similarly, male children had higher prevalence of schistosomiasis than females (33.6% vs 29.0%). However, the difference was not statistically significant (χ2 = 0.942; P = 0.332). With regards to the intensity of infections, 22.1% and 8.1% of S. haematobium and S. mansoni infections respectively were of heavy intensities (Table 2). 10.1371/journal.pntd.0002377.t002 Table 2 Prevalence and intensity of schistosomiasis among Yemeni children who participated in this study (n = 400). Intensity of infection* Type of infection S. haematobium S. mansoni N % Mean (ep10ml) N % Mean (epg) Light 74 77.9 17 19 51.4 50 Moderate - - - 15 40.5 212 Heavy 21 22.1 340 3 8.1 637 Overall 95 23.8 89 37 9.3 163 * According to WHO [18]. ep10ml, Number of eggs per 10 ml of urine. epg, Number of eggs per gram of faeces. Clinical manifestations of schistosomiasis Children who participated in this study underwent physical examination and haemoglobin level was measured. Hepatosplenomegaly and anaemia were reported in 9.5% (38/400) and 39.5% (158/400) of the children, respectively. Moreover, 15.8% (63/400) had fever whilst 24.1% (96/400) had diarrhea. Of these studied children, 26.0% (104/400) and/or 15.0% (60/400) claimed to have haematuria and bloody stool, respectively. The association between schistosomiasis and the presence of hepatosplenomegaly and anaemia was examined. Children with S. mansoni infection had a significantly higher rate of hepatosplenomegaly (18.9%; 95% CI = 9.5, 34.2) when compared with those without S. mansoni infection (8.3%; 95% CI = 5.8, 11.4) whereas no significant difference in the case of S. haematobium infection. A significant association between the intensity of S. mansoni infection and hepatosplenomegaly was also reported (P = 0.033). Moreover, the presence of hepatosplenomegaly was significantly higher among children with mixed infection (both Schistosoma species) compared to those with single infection (P>0.05). On the other hand, the association between schistosomiasis and anaemia among these children was not significant (P>0.05). Factors associated with schistosomiasis Results of univariate and multivariate analyses for the association of schistosomiasis with demographic, socioeconomic, environmental and behavioural factors are shown in Tables 3 and 4. 10.1371/journal.pntd.0002377.t003 Table 3 Univariate analysis of factors associated with schistosomiasis among Yemeni children who participated in this study (n = 400). Variables Schistosomiasis No. examined Infected n (%) OR(95% CI) P Age >10 years 178 37.6 1.6 (1.1, 2.5) 0.023* ≤10 years 222 27.0 1 Gender Male 238 33.6 1.2 (0.8, 1.9) 0.332 Female 162 29.0 1 Fathers' educational levels Non educated 191 38.2 1.8 (1.2, 2.7) 0.008* Educated (at least primary education) 209 25.8 1 Fathers' occupational status Farmers 195 33.8 1.3 (0.8, 2.0) 0.236 Not working 34 38.2 1.6 (0.7, 3.4) 0.233 Government employees & professionals 171 28.1 1 Mothers' occupational status Farmer and/or daily labourer 21 47.6 2.0 (0.8, 4.9) 0.109 Not working 279 30.9 1 Household monthly income 10 years (37.6%; 95% CI = 30.8, 44.5) had significantly higher prevalence of schistosomiasis when compared with those aged ≤10 years (27.0%; 95% CI = 21.6, 33.2). Similarly, the prevalence of schistosomiasis was significantly higher among children of non educated fathers (38.2%; 95% CI = 31.6, 45.3) and those from families with low household monthly income (38.7%; 95% CI = 32.9, 44.9) when compared with the children of fathers with at least 6 years of formal education (25.8%; 95% CI = 20.4, 32.2) and those from families with household monthly income of ≥YER20,000 (19.7%; 95% CI = 14.1, 26.9). Moreover, it was found that the presence of other family members infected with schistosomiasis showed significant association with higher prevalence of schistosomiasis (P 10 years were more prone to be infected than younger children. This is in agreement with previous reports from Yemen and other countries [6], [14], [39]–[41]. This could be explained by the excessive mobility of children at this age and they may become more exposed to infected water while swimming/playing or fetching water for domestic purposes or helping in agriculture activities. With regards to gender, the present study found no significant difference in the prevalence of schistosomiasis between male and female participants. However, we found that boys had significantly higher intensity of both Schistosoma species than girls. These are consistent with many other reports in other countries [42], [43]. Males usually have higher prevalence rates of schistosomiasis than females and this was attributed to religious and cultural reasons or to water contact behavior [14], [15], [39], [41], [44]. However, significantly higher infection rates among females compared to their males counterparts have been also reported elsewhere [45], [46]. In Yemen and many other Islamic countries, females are prohibited from bathing in open water sources whereas the males frequently play and swim during their leisure time. On the other hand, females are responsible of fetching water and washing clothes and utensils at these water sources, and therefore, have similar exposure to infective stages. Female education remains a key challenge and gender gap in education in Yemen is among the highest in the world [47]. Hence, community-based drug distribution should also be considered together with the school-based control in order to reach this group and reduce the transmission in the entire communities. The present study is the first to provide information about the key factors associated with schistosomiasis in Yemen. We found significant associations between the high prevalence of schistosomiasis and the age of children, presence of other family member infected with schistosomiasis, fathers' educational level, household monthly income, lacking toilets and piped water supplies in the households, living nearby streams, pools, water pumps, and living in areas where foreigners seen play/swim in open water. The findings of the present study showed that children who live in houses with the presence of other family members infected with Schistosoma species were at a 4 folds higher risk of getting schistosomiasis. Thus, screening and treating other family members should be considered in the control measures. To the best of our knowledge, no previous study has reported on the association of the presence of other family members infected with Schistosoma as a risk factor for schistosomiasis. Although the disease is not transmitted directly from human-to-human but members of a same family may share their activities at water sources such as playing, swimming and washing and therefore, they have similar exposure to the source of infection. Moreover, an infected family member may contract the disease and then contribute to its transmission at the open water sources nearby where other family members may also use. The association between schistosomiasis and water contact is well documented. The fetching of water and living close to a stream and/or a water pool were identified as significant risk factors for schistosomiasis in the present study. Similar findings have been reported in previous studies among rural children and adolescents in different countries [40], [41], [48], [49]. Water storage, streams, dams and pools may all provide favourable breeding sites for snails and therefore, potentially, support the continued transmission of schistosomiasis in these areas. Schistosomiasis is a poverty-related disease and our findings showed that children belong to families with a low household monthly income were 2.3 times more likely to be infected compared to those belonging to families with a household monthly income of ≥YER20,000. We have also identified fathers' educational level as a significant predictor of schistosomiasis among the children studied; however, this association was not retained by the logistic regression model. Previous studies among rural communities in Yemen found no association between the prevalence of schistosomiasis and the fathers' or participants' educational status [14], [16]. In Cote d'Ivoire and Nigeria, the higher education level of the head of family was identified as a protective factor against S. haematobium infection [39], [40]. In the present study, the absence of a functioning toilet in the house was significantly associated with the prevalence of schistosomiasis and this was in accordance with previous studies [18], [50], [51]. A similar significant association of schistosomiasis with using unsafe water for drinking and for other household purposes was reported in the present study. This association is related to the higher exposure to the infected water during the fetching process. Surprisingly, there were strong negative associations between schistosomiasis and the presence of a water pump nearby, and living in areas where foreigners were seen playing/swimming in open water sources. The water pump is usually used to provide drinking water or water for agriculture and therefore, people living close to and fetching water for their needs from a water pump are at lower exposure to the infected water in streams and/or pools. Areas where foreigners might be seen frequently are tourist areas and therefore, expected to undergo a better level of cleanliness and services including mollusciciding. However, these significant associations were not retained by the multivariate analysis. Population migration such as rural-urban migration, forced displacement and the rise of ecotourism may extend the disease to new areas or may cause a shift in snail population especially when the migration is accompanied with some water development projects. Moreover, most of the foreign visitors to these areas, mostly in Ibb province, were from Saudi Arabia and many Yemeni immigrants to USA or UK. Although Saudi Arabia has achieved the elimination of schistosomiasis in 2002, new cases are still reported in southern region, border areas with Yemen [52]. Therefore, cross-border collaboration and regional control programmes are essential, with regular long-term surveillance to detect and treat any new or residual infections [52], [53]. A previous study among a group of 129 Israelis of Yemeni origin found that S. mansoni eggs and specific anti- S. mansoni IGE were reported positive in 12% and 37% individuals, respectively [54]. In earlier report among 218 Yemeni workers in the San Joaquin Valley of California, eggs of S. mansoni were detected in 56% of them with 16% and 27% had heavy and moderate infections, respectively [55]. The authors showed that those who returned to Yemen for short visits had significantly higher egg count compared to those who were away from Yemen for more than 5 years. Rural communities in Yemen share similar socioeconomic and health profiles with a different climate. Coastal plains and foothills (Taiz, Ibb and Hodeidah) have more streams whereas mountainous areas (Sana'a and Dhamar) have more water pools/troughs and dams. Our study provides a community-based knowledge of schistosomiasis status among children with a poor socioeconomic, environmental and personal hygiene background. Thus, we may speculate that the findings of the present study can be generalised to rural areas in other provinces in Yemen. However, further investigations are required to confirm these conjectures. Conclusion This study reveals an alarmingly high prevalence of schistosomiasis among rural children in Yemen and this supports an urgent need to re-evaluate the current control measures and implement an integrated, targeted and effective schistosomiasis control measures. Regional control programmes are essential to prevent the dissemination of the infection to new areas at neighbouring countries. Screening of other family members and treating the infected individuals should be adopted by the public health authorities in combating this infection in these communities. Besides periodic drug distribution, health education regarding good personal hygiene and good sanitary practices, provision of clean and safe drinking water, introduction of proper sanitation are imperative among these communities in order to curtail the transmission and morbidity caused by schistosomiasis. Supporting Information Checklist S1 STROBE Checklist. (DOC) Click here for additional data file.
