Intestinal schistosomiasis among schoolchildren in Sana’a Governorate, Yemen: Prevalence, associated factors and its effect on nutritional status and anemia

Abstract

Intestinal schistosomiasis is a neglected tropical disease, causing morbidity and mortality in tropical and subtropical countries. Despite the frequent implementation of mass drug administration with praziquantel, the reinfection with Schistosoma mansoni is still common in Yemen. In addition, there is a scarcity of information on the impact of S. mansoni on nutritional status and anemia among schoolchildren. The present study aimed to determine prevalence and risk factors of intestinal schistosomiasis and investigate its impact on nutritional status and anemia among schoolchildren in Sana’a Governorate, Yemen. It was conducted in 2018 on 445 schoolchildren aged 5–15 years. Biodata, socio-economic, demographic, behavioral and environmental data were collected using a standard questionnaire. S. mansoni was identified and quantified by microscopic examination of Kato-Katz fecal smear. Hemoglobin concentration and anthropometric measurements were estimated using standard methods. The prevalence of S. mansoni was higher in Al-Haimah Al-Dakheliah (33.9%) than Bani Mater (1.4%). Household without tap water (Adjusted Odds Ratio (AOR) = 2.9, 95% Confidence interval (CI): 1.12, 7.55, P = 0.028) was the independent risk factor of the infection. The prevalence of wasting and stunting was 25.0% (95%CI: 21.2%, 29.2%) and 45.8% (95%CI: 41.2%, 50.5%), respectively. The prevalence of underweight among schoolchildren aged 5–10 years was 27.3% (95%CI: 21.9%, 33.4%). The prevalence of anemia was 31.7% (95%CI: 27.5%, 36.2%) with 0.5%, 21.1% and 10.1% being severe, moderate and mild anemia, respectively. S. mansoni (AOR = 4.1, 95%CI: 2.16, 7.84, P < 0.001) and early adolescence (AOR = 6.8, 95%CI: 4.26, 10.82, P < 0.001) were independent predictors of stunting among schoolchildren. The early adolescent schoolchildren (AOR = 3.1, 95%CI: 1.86, 4.97, P < 0.001) and children from families with low (AOR = 2.1, 95%CI: 1.01, 4.15, P = 0.046) or moderate wealth (AOR = 2.3, 95%CI: 1.11, 4.77, P = 0.026) were significantly more wasted.

Early adolescence (AOR = 1.8, 95%CI:1.14, 2.78, P = 0.011), female (AOR = 1.6, 95%CI: 1.03, 2.43, P = 0.038) and Al-Haimah Al-Dakheliah District (AOR = 3.4, 95%CI: 1.20, 9.55, P = 0.021) were independent risk factors for anemia. The study findings indicate highly focal prevalence of schistosomiasis in Sana’a Governorate with a public health significance that varies from low to high risk. Approximately half of schoolchildren were stunted, which was associated with S. mansoni infection and early adolescence. One quarter of schoolchildren were wasted with early adolescent schoolchildren and children from poor families being at high risk of wasting. Anemia was a moderate public health threat affecting the female and the early adolescent schoolchildren. The study suggests the implementation of control measures to combat schistosomiasis and integrated diseases control programmes to improve the health status of schoolchildren in Sana’a Governorate.

Introduction

Human schistosomiasis is a neglected tropical disease caused by Schistosoma species and occurs mainly in tropical and sub-tropical countries [1]. It causes severe morbidity and mortality with an estimated global burden of 1.4 million disability-adjusted life-years (DALYs)[2]. Schistosoma species with high global prevalence include S. haematobium (urogenital schistosomiasis), S. mansoni and S. japonicum (intestinal schistosomiasis)[1]. Intestinal schistosomiasis in schoolchildren compromises growth, physical fitness, cognitive function and educational achievement and causes anemia [3–5].

In Yemen, schistosomiasis has been a public health problem since 1922[6] with a patchy distribution and different infection rates, ranging from 15% to 100% [7–14]. A combined Yemen-WHO project for controlling schistosomiasis was set up in 1973, which estimated that 25% of the population were infected with S. mansoni and/or S. haematobium [15,16]. After implementing several campaigns of school-based mass drug administration (MDA) with praziquantel, the prevalence of S. mansoni at country level dropped to 2.5% with a district-based prevalence ranging from 0.0 to 35.7% [17]. In the nationwide survey conducted in 2017, three years after the previous survey, the prevalence of S. mansoni increased to 7.4% [18]. Malnutrition and anemia are other threats affecting schoolchildren in Yemen where 59%, 47% and 18% of school-aged children were found stunted, underweight and anemic, respectively [19]. However, there is a paucity of information about the impact of S. mansoni on the nutritional status and anemia among schoolchildren in Yemen [20]. Thus, the present study aimed to determine prevalence of S. mansoni, identify factors associated with the infection and its impact on nutritional status and anemia among schoolchildren in rural communities of Sana’a Governorate, Yemen.

Methods

Study area, design and subjects

This is a cross-sectional study conducted in the rural areas of Sana’a Governorate, Yemen. Schoolchildren aged 6–15 years were the study population. Children who had taken iron, nutritional supplements or anti-parasitic drugs in the last six months prior to the study were excluded.

Sample size and sampling strategy

The minimum sample size required for the study was 358 schoolchildren which was calculated by Epi Info | CDC (https://www.cdc.gov/epiinfo/index.html)) using the following parameters: 95% confidence interval, ± 5% precision and the highest recently reported prevalence of S. mansoni (37%) [17]. However, 445 schoolchildren were enrolled in the study to replace participant for not providing fecal sample. A multistage sampling approach was used for selecting schoolchildren where two districts from rural areas of Sana’a Governorate were randomly selected, followed by random selection of one school from each district. Children from each school were selected by systematic random sampling from the students record until the required sample size was obtained. If a selected child refused to participate or was not eligible, he/she was replaced by the next student in the record. The number of students selected from each school was proportional to the size of the school.

The study questionnaire

Biodata, socio-economic, demographic, behavioral and environmental data were collected using a pre-designed, structured questionnaire through a face-to-face interview. The questionnaire included questions about durable items, animals and agricultural land owned by households; household’s source of drinking water; sanitation coverage; father and mother education; and the number of household’s members.

Parasitological investigations

A single fresh fecal sample was collected from each participant in a dry, clean plastic container, labeled with the child’s name and identification number. At the field, a Kato-Katz thick fecal smear was prepared from each fecal sample and the rest of feces were preserved in 10% formalin. The Kato-Katz thick fecal smears were then transported to the Parasitology Laboratory in the Faculty of Medicine and Health Sciences, Sana’a University and examined for S. mansoni [21]. The intensity of S. mansoni was classified into light (1–99 EPG), moderate (100–399 EPG) and high intensity (≥ 400 EPG) [22]. The public health significance of the prevalence of S. mansoni was classified into high risk (≥30%), moderate risk (≥10 and <30%) and low risk (<10%) as suggested by the national control strategy [17].

Hemoglobin estimation

A single measurement of hemoglobin concentration from each child was conducted using a portable hemoglobin analyzing system HB 301+ (HemoCue1 AB, Angelhome, Sweden) on blood collected by finger-prick following the manufacturer instruction. Children were classified into anemic or non-anemic (Hb ≥ 115 g/l for children aged 5–10 years and Hb ≥ 120 g/l for children aged 11–15 years), and subsequently as mild (Hb = 110–114 g/l for children aged 5–10 years and Hb = 114–119 g/l for children aged 11–15 years), moderate (Hb = 80–109 g/l) and severe anemia (Hb < 80 g/l) after adjusting the hemoglobin measurement for altitude according to WHO reference[23]. The public health significance of anemia prevalence was classified as normal (≤ 4.9%), mild (5.0–19.9%), moderate (20.0–39.9%) and severe (≥ 40%)[23].

Anthropometric measurements

For anthropometric measurements, standing height of each child was measured to the nearest 0.1 cm using a portable stadiometer (Seca, model 208) and his/her weight was measured to the nearest 0.1 kg using a digital weight scale. The age of each participant was retrieved from the birth certificate or school records. The collected measures were used for calculating height-for-age z-score (HAZ), weight-for-age z-score (WAZ) and BMI-for-age z-score (BAZ) using the WHO AnthroPlus software for the global application of the WHO reference 2007 for 5–19 years[24]. The WHO reference data for WAZ used by the WHO AnthroPlus software were for age ≤ 10 years; therefore, underweight was estimated for children aged 5–10 years old. The nutritional indicators for school-age children were defined as follows:

[Figure omitted. See PDF.]

https://doi.org/10.1371/journal.pntd.0009757.t001

Statistical analysis

Data were analyzed using IBM SPSS Statistics for Windows, version 23.0 (IBM Corp., Armonk, NY, USA). The wealth indices were determined using the principal component analysis (PCA) of durable items, animals and agricultural land owned by households. The constructed PCA-based scores of households were divided into five quintiles and three wealth categories, where households’ residents with the lowest 40%, the middle 40% and the highest 20% of household wealth quintiles were classified as low, middle and high, respectively[25]. Categorical variables were presented in frequencies. The association between independent and dependent variables was tested using Pearson’s chi-square with reporting odds ratio (OR) and its corresponding 95% confidence interval (CI). Multivariable analysis using entry binary logistic regression model was conducted including all predicting variables and the adjusted OR with its corresponding 95%CI were reported. P-value of <0.05 was considered significant.

Ethics statement

The study protocol was approved by Research and Ethics Committee (REC) of the Faculty of Medicine and Health Sciences, Sana’a University. Approval of school headmasters/ headmistresses was also taken after explaining the significance of the study. Each child was voluntary involved after receiving information in a way that the child can understand and give his/her assent. No informed consent was obtained from child’s parents/guardians, although they were informed about the study and had the right to refuse the participation of their child. Anonymity, dignity and privacy of the child and his/her family were protected.

Results

Characteristic of study population

Table 1 summarizes the characteristics of participants. A total of 445 schoolchildren were enrolled in this study. Their age ranged between 5 and 15 years with a mean of 10 ± 2.54. The majority of children (70.6%) were in the age group of 5–11 years. About 82% of the children belonged to families with more than 5 members. More than half of the children were living in houses without proper sanitation coverage (no toilet or flush/pour flush to open area) and about one-third had unimproved source of drinking water. Although no much difference in the characteristics of the study participants between the two districts, the majority of schoolchildren in Al-Haimah Al-Dakheliah District are living in houses without access to improved sanitation.

[Figure omitted. See PDF.]

Table 1. Distribution of the study population by socio-demographic information, Sana’a Governorate, Yemen.

https://doi.org/10.1371/journal.pntd.0009757.t002

Prevalence and factors associated with Schistosoma mansoni

The prevalence of S. mansoni was higher in Al-Haimah Al-Dakheliah (33.9%) than in Bani Mater (1.4%). The intensity of S. mansoni was classified as heavy (4.1%), moderate (3.6%) and light intensity infection (10.3%) (Table 2).

[Figure omitted. See PDF.]

Table 2. Distribution of Schistosoma mansoni infection among schoolchildren in the rural areas of Sana’a Governorate, Yemen (N = 445).

https://doi.org/10.1371/journal.pntd.0009757.t003

Univariable analysis was restricted to Al-Haimah Al-Dakheliah District where the prevalence of schistosomiasis was high, which identified a significant association between S. mansoni infection and uneducated mother (OR = 3.0, 95% CI: 1.11, 8.21, P = 0.024) and households without tap water (OR = 3.5, 95% CI: 1.49, 8.29, P = 0.003). Multivariate analysis identified households without tap water (adjusted OR = 2.9, 95% CI: 1.12, 7.55, P = 0.028) as an independent risk factor of S. mansoni (Table 3).

[Figure omitted. See PDF.]

Table 3. Factors associated with Schistosoma mansoni among schoolchildren in Sana’a Governorate, Yemen (N = 227)&.

https://doi.org/10.1371/journal.pntd.0009757.t004

Prevalence and factors associated with stunting, wasting and underweight

The prevalence of stunting among schoolchildren was 45.8% with 26.3% of the children being severely stunted while the prevalence of wasting was 25% with 9.7% of the children being severely wasted. Children aged 11–15 years had significantly higher rates of stunting and wasting than children aged 5–10 years. Among schoolchildren aged 5–10 years, 27.3% of them were diagnosed as underweight and 10.8% were classified as severe underweight (Table 4).

[Figure omitted. See PDF.]

Table 4. Prevalence of underweight, stunting and wasting among schoolchildren in Sana’a Governorate, Yemen*.

https://doi.org/10.1371/journal.pntd.0009757.t005

Univariable analysis showed that schoolchildren resident in Al-Haimah Al -Dakheliah District (OR = 2.2, 95%CI:1.20, 4.06, P = 0.011) and living in houses with unimproved sanitation (OR = 1.9, 95%CI:1.02, 3.41, P = 0.043) or infected with S. mansoni (OR = 2.0, 95%CI: 1.01, 4.05, P = 0.045) were at high risk of developing underweight. However, underweight had negative association with educated fathers (OR = 0.5, 95%CI: 0.27, 0.98, P = 0.041). Multivariable analysis did not identify an independent risk factor of underweight (Table 5).

[Figure omitted. See PDF.]

Table 5. Factors associated with underweight among schoolchildren, Sana’a Governorate, Yemen (N = 231).

https://doi.org/10.1371/journal.pntd.0009757.t006

Stunting was significantly associated with children aged 11–15 years (OR = 5.6, 95%CI: 3.73, 8.44, P <0.001), females (OR = 1.5, 95%CI: 1.01, 2.13, P = 0.047) and S. mansoni infection (OR = 4.0, 95%CI: 2.00, 8.01, P = 0.002). Multivariable analysis identified the infection with S. mansoni and early adolescence as independent risk factors of stunting (Table 6).

[Figure omitted. See PDF.]

Table 6. Factors associated with stunting among schoolchildren, Sana’a Governorate, Yemen (N = 445).

https://doi.org/10.1371/journal.pntd.0009757.t007

Wasting was associated with children aged 11–15 years (OR = 2.9, 95%CI: 1.86, 4.60, P < 0.001), households without tap water (OR = 1.9, 95%CI: 10, 3.28, P = 0.021) and children from families placed in the middle category of wealth indices (OR = 2.2, 95%CI: 1.12, 4.15, P = 0.022). Multivariable analysis identified children aged 11–15 years, and the middle and poor categories of wealth indices as independent risk factors of wasting (Table 7).

[Figure omitted. See PDF.]

Table 7. Factors associated with wasting among schoolchildren, Sana’a Governorate, Yemen (N = 445).

https://doi.org/10.1371/journal.pntd.0009757.t008

Prevalence and factors associated with anemia

The prevalence of anemia among schoolchildren was 31.7% (95%CI: 27.5%, 36.2%) with 0.5%, 21.1% and 10.1% being severe, moderate and mild anemia, respectively. Univariable analysis showed that schoolchildren from Al-Haimah Al–Dakheliah District (OR = 3.9, 95%CI: 2.12, 6.97, P <0.001), whose mothers were uneducated (OR = 2.5, 95%CI: 1.11, 5.69, P = 0.023), and those living in houses with unimproved sanitation (OR = 3.2, 95%CI: 1.11, 5.69, P <0.001) and without tap water (OR = 2.2, 95%CI: 1.10, 4.52, P = 0.024) were at higher risk of anemia. Multivariable analysis using binary logistic regression model identified female (AOR = 1.6, 95%CI:1.03, 2.43, P = 0.038), Al-Haimah Al–Dakheliah District (AOR = 3.4, 95%CI:1.20, 9.55, P = 0.021) and early adolescence (11–15 years) (AOR = 1.8, 95%CI:1.14, 2.78, P = 0.011) as independent risk factors of anemia among schoolchildren (Table 8).

[Figure omitted. See PDF.]

Table 8. Factors associated with anemia schoolchildren in Sana’a Governorate, Yemen (N = 445).

https://doi.org/10.1371/journal.pntd.0009757.t009

Discussion

The present study indicated focal prevalence of S. mansoni among schoolchildren in Sana’a Governorate. At district level, the study placed Al-Haimah Al–Dakheliah and Bani Mater districts at high and low risk of schistosomiasis (33.9% and 1.4%, respectively). The presence of foci with high infection rates, although the pressure of MDA campaigns, can be explained by the high reinfection rate of S. mansoni. A recent study conducted in Ethiopia reported high reinfection rate of S. mansoni after 6 months of treatment with praziquantel[26]. The reinfection with S. mansoni was found to be affected by socioeconomic status, level of education of the household head and the baseline heavy infection[27], which may justify the variation in the prevalence of S. mansoni between the two districts. These findings, in turn, suggest that MDA campaigns should be integrated with additional measures to control schistosomiasis.

Multivariable analysis identified having no tap water at home as an independent risk factor of S. mansoni in Al-Haimah Al–Dakheliah District. This observation could be explained by the possibility of children’s responsibility of bringing household’s water, a common practice in Yemen, which increased their contact with unsafe water and made them prone to S. mansoni infection [28,29]. The result suggests an integration of MDA of praziquantel and the delivery of a community-based WASH programme as an effective approach for combating schistosomiasis in these communities. The positive impact of WASH intervention on deworming programmes has been well evidenced [30,31].

The nutritional status of schoolchildren in Yemen has been neglected despite its significant impact on cognitive and educational achievement[5]. In the present study, the prevalence of stunting, underweight and wasting among schoolchildren aged 5–15 years was 45.8%, 27.3% and 25%, respectively. The study reported lower prevalence of stunting and underweight and five-times higher prevalence of wasting compared to stunting, underweight and wasting reported in previous studies conducted among schoolchildren in Al Mahweet and Sada’ah governorates, Yemen[19,20]. The prevalence of stunting and wasting were higher among schoolchildren aged 11–15 years than those aged 5–10 years. These findings are consistent with previous studies conducted in Pakistan [32], Tanzania[33] and Madagascar[34]. The increased prevalence of stunting and wasting with age could be explained in part by the accumulated exposure of the older children to childhood diseases and inadequate diets [35].

Schistosoma mansoni is an independent risk factor of stunting among schoolchildren in Sana’a Governorate. The association between S. mansoni and stunting was reported in different studies [4,36,37].

Underweight takes into account both acute malnutrition (wasting) and chronic malnutrition (stunting). In the present study, a significant association between S. mansoni and underweight was found using univariable analysis although the multivariable analysis model did not confirm this association. Schoolchildren belonging to families with poor and middle wealth indices were at high risk of being acute malnourished. This finding is consistent with previous reports from Ethiopia [38] and India [39], which could reflect the inadequate feeding among children from families with low wealth indices.

The prevalence of anemia represents a moderate and severe public health problem among schoolchildren in Bani Matar and Al-Haimah Al -Dakheliah districts, respectively. Although the causes of anemia in the present study have not been identified, iron deficiency is one of the primary causes of anemia in the Yemeni communities [40]. The reason behind the high prevalence of anemia in Al-Haimah Al -Dakheliah District is not clear, although it may be attributed to socioeconomic status: 90% of the children belonged to families with moderate and poor wealth indices. Schoolchildren aged 11–15 years were at two times higher risk of being anemic compared to younger age group. This finding is consistent with previous studies conducted among children in different countries [41–46], which could be explained by the hyperactivity during this age together with high demand of micronutrient and limited consumption of a variety of food sources due to the household food insecurity [47], which can be reduced by school feeding [48,49]. The gender female was also an independent risk factor of anemia, which is in line with previous studies [50,51]. It is noteworthy that anemia among schoolchildren may lead to impaired cognitive function [52]. No significant association was found between S. mansoni and anemia, which is consistent with previous studies conducted elsewhere [28,33].

The present study is limited by the low number of districts and schools enrolled in the study, which prevents the conclusion about the overall prevalence of schistosomiasis at governorate level because the disease is highly focal, although study findings are consistent with the results of the latest nationwide survey. However, the study sample size and design are appropriate to assess the association between schistosomiasis and nutritional status of schoolchildren in Sana’a Governorate.

In conclusion, the study findings showed highly focal prevalence of schistosomiasis in Sana’a Governorate with a public health significance that varies from low to high risk. Schoolchildren living in houses without tap water are at high risk of the infection. Schoolchildren harboring the parasite and early adolescent children had high prevalence of stunting. Besides, early adolescent schoolchildren and children belonged to families with middle or poor wealth were wasted. Anemia is a moderate public health threat with early adolescent and female schoolchildren, being at higher risk. The study findings suggest adopting integrated control measures for the control of schistosomiasis such as MDA and WASH, and integrated diseases control progarmmes for improving the health status of schoolchildren.

Acknowledgments

Authors thank children participated in the study and the management of schools for cooperation. We thank Dr. Rashad Abdul-Ghani, Department of Parasitology, Faculty of Medicine, Sana’a university, Yemen, for his valuable comments during the study design. The authors acknowledge Ahmed Alhabibi, Mohammed Attif, Farhan Y Al-Jaberi and Moa’ath A. Mansour for their help in the fieldwork.

Citation: Al-Haidari SA, Mahdy MAK, Al-Mekhlafi AM, Al Murisi WMS, Thabit AAQ, Al-Amad MA, et al. (2021) Intestinal schistosomiasis among schoolchildren in Sana’a Governorate, Yemen: Prevalence, associated factors and its effect on nutritional status and anemia. PLoS Negl Trop Dis 15(9): e0009757. https://doi.org/10.1371/journal.pntd.0009757

References

1. World Health Organization. 2018. Schistosomiasis: status of schistosomiasis endemic countries World Health Organization; [Available from: https://apps.who.int/neglected_diseases/ntddata/sch/sch.html.

2. GBD DALYs and Hale Collaborators. 2018. Global, regional, and national disability-adjusted life-years (DALYs) for 359 diseases and injuries and healthy life expectancy (HALE) for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet. 392(10159):1859–922. pmid:30415748

3. Koukounari A, Fenwick A, Whawell S, Kabatereine NB, Kazibwe F, Tukahebwa EM, et al. 2006. Morbidity indicators of Schistosoma mansoni: relationship between infection and anemia in Ugandan schoolchildren before and after praziquantel and albendazole chemotherapy. The American journal of tropical medicine and hygiene. 75(2):278–86. pmid:16896133

4. Kabongo MM, Linsuke S, Baloji S, Mukunda F, Raquel IDL, Stauber C, et al. 2018. Schistosoma mansoni infection and its association with nutrition and health outcomes: a household survey in school-aged children living in Kasansa, Democratic Republic of the Congo. The Pan African medical journal. 31:197. pmid:31086641

5. Ezeamama AE, Bustinduy AL, Nkwata AK, Martinez L, Pabalan N, Boivin MJ, et al. 2018. Cognitive deficits and educational loss in children with schistosome infection-A systematic review and meta-analysis. PLoS neglected tropical diseases. 12(1):e0005524. pmid:29329293

6. Grevai S. 1922. Schistosomiasis (Bilharziasis) in Arabia. Ind J Med Research 10:943–7.

7. Kuntz RE. 1952. Schistosoma mansoni and Shaematobium in the Yemen, Southwest Arabia; with a report of an unusual factor in the epidemiology of Schistosomiasis mansoni. J Parasitol. 38(1):24–8. pmid:14928148

8. Kuntz RE, Malakatis GM, Lawless DK, Strome CP. 1953. Medical mission to the Yemen, Southwest Arabia, 1951. II. A cursory survey of the intestinal protozoa and helminth parasites in the people of the Yemen. The American journal of tropical medicine and hygiene. 2(1):13–9. pmid:13007917

9. Kuz’mtsn IL. 1966. [Distribution and clinical features of urinary schistosomiasis in Yemen]. Med Parazitol (Mosk). 35(5):564–6. pmid:6003345

10. Parrinello A. 1966. [Electrocardiographic modifications from antimony in a group of Yemenite patients affected by schistosomiasis]. Rass Clin Ter. 65(2):121–5. pmid:5943145

11. Mancioli M, Parrinello A. 1967. [Nitrothiamidazole in the treatment of schistosomiasis in Yemen. Preliminary clinical study in relation to the possibility of a mass therapy]. Clin Ter. 42(1):15–55. pmid:5597000

12. Prokhorov AF. 1969. [On the problem of schistosomiasis in the Yemen Arab Republic]. Med Parazitol (Mosk). 38(1):91–4. pmid:5371118

13. Zaiachkovskii SM. 1971. [Epidemiology and clinical picture of intestinal schistosomiasis in Yemen]. Med Parazitol (Mosk). 40(4):409–11. pmid:5134371

14. Arfaa F. 1972. Studies on schistosomiasis in the Yemen Arab Republic. The American journal of tropical medicine and hygiene. 21(4):421–4. pmid:5065694

15. Daffalla A. 1988. Schistosomiasis control project in Y.A.R. Assignment Report. WHO office, Sana’a, Yemen.

16. Arfaa F. 1980. Schistosomiasis control: Southern Uplands Rural Development Project. Y.A.R. Assignment Report WHO office, Sana’a, Yemen.

17. Johari NA. 2014. Mapping of Schistosomiasis and Soil-transmitted helminths in Yemen, and the push for elimination (master thesis). London: Imperial College.

18. World Bank. 2018. Final Report of Schistosomiasis Control Project in Yemen (P113102). World Bank.

19. Raja’a YA, Sulaiman SM, Elkarib SA, Mubarak JS. 2001. Nutritional status of Yemeni schoolchildren in Al-Mahweet Governorate. Eastern Mediterranean health journal 7(1–2):204–10. pmid:12596971

20. Raja’a YA, Mubarak JS. 2006. Intestinal parasitosis and nutritional status in schoolchildren of Sahar district, Yemen. Eastern Mediterranean Health Journal. 12. pmid:17361690

21. Katz N, Chaves A, Pellegrino J. 1972. A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo. 14(6):397–400. pmid:4675644

22. Montresor A, Crompton, David WT, Hall A, Bundy DAP, Savioli L, et al. 1998. Guidelines for the evaluation of soil-transmitted helminthiasis and schistosomiasis at community level: a guide for managers of control programmes World Health Organization.

23. World Health Oganization. 2017. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Available from: http://www.who.int/vmnis/indicators/haemoglobin. pdf.

24. World Health Oganization. 2009. WHO AnthroPlus for personal computers Manual: Software for assessing growth of the world’s children and adolescents. Geneva: World Health Organization.

25. Vyas S, Kumaranayake L. 2006. Constructing socio-economic status indices: how to use principal components analysis. Health policy and planning. 21(6):459–68. pmid:17030551

26. Woldegerima E, Bayih AG, Tegegne Y, Aemero M, Jejaw Zeleke A. 2019. Prevalence and Reinfection Rates of Schistosoma mansoni and Praziquantel Efficacy against the Parasite among Primary School Children in Sanja Town, Northwest Ethiopia. Journal of parasitology research. 2019:3697216. pmid:31179124

27. Gazzinelli A, Oliveira-Prado R, Matoso LF, Veloso BM, Andrade G, Kloos H, et al. 2017. Schistosoma mansoni reinfection: Analysis of risk factors by classification and regression tree (CART) modeling. PloS one. 12(8):e0182197. pmid:28813451

28. Tukahebwa EM, Magnussen P, Madsen H, Kabatereine NB, Nuwaha F, Wilson S, et al. 2013. A very high infection intensity of Schistosoma mansoni in a Ugandan Lake Victoria Fishing Community is required for association with highly prevalent organ related morbidity. PLoS neglected tropical diseases. 7(7):e2268. pmid:23936559

29. Matthys B, Tschannen AB, Tian-Bi NT, Comoe H, Diabate S, Traore M, et al. 2007. Risk factors for Schistosoma mansoni and hookworm in urban farming communities in western Cote d’Ivoire. Tropical medicine & international health: TM & IH. 12(6):709–23. pmid:17550468

30. Vaz Nery S, Pickering AJ, Abate E, Asmare A, Barrett L, Benjamin-Chung J, et al. 2019. The role of water, sanitation and hygiene interventions in reducing soil-transmitted helminths: interpreting the evidence and identifying next steps. Parasites & vectors. 12(1):273. pmid:31138266

31. Vaz Nery S, Traub RJ, McCarthy JS, Clarke NE, Amaral S, Llewellyn S, et al. 2019. WASH for WORMS: A Cluster-Randomized Controlled Trial of the Impact of a Community Integrated Water, Sanitation, and Hygiene and Deworming Intervention on Soil-Transmitted Helminth Infections. The American journal of tropical medicine and hygiene. 100(3):750–61. pmid:30628573

32. Khuwaja S, Selwyn BJ, Shah SM. 2005. Prevalence and correlates of stunting among primary school children in rural areas of southern Pakistan. Journal of tropical pediatrics. 51(2):72–7. pmid:15677373

33. Munisi DZ, Buza J, Mpolya EA, Kinung’hi SM. 2016. Schistosoma mansoni Infections, Undernutrition and Anaemia among Primary Schoolchildren in Two Onshore Villages in Rorya District, North-Western Tanzania. PloS one. 11(12):e0167122. pmid:27936031

34. Aiga H, Abe K, Andrianome VN, Randriamampionona E, Razafinombana AR, Murai T, et al. 2019. Risk factors for malnutrition among school-aged children: a cross-sectional study in rural Madagascar. BMC public health. 19(1):773. pmid:31208397

35. Dureab F, Al-Falahi E, Ismail O, Al-Marhali L, Al Jawaldeh A, Nuri NN, et al. 2019. An Overview on Acute Malnutrition and Food Insecurity among Children during the Conflict in Yemen. Children (Basel). 6(6). pmid:31195654

36. Sircar AD, Mwinzi PNM, Onkanga IO, Wiegand RE, Montgomery SP, Secor WE. 2018. Schistosoma mansoni Mass Drug Administration Regimens and Their Effect on Morbidity among Schoolchildren over a 5-Year Period-Kenya, 2010–2015. The American journal of tropical medicine and hygiene. 99(2):362–9. pmid:29893197

37. Assis AM, Prado MS, Barreto ML, Reis MG, Conceicao Pinheiro SM, Parraga IM, et al. 2004. Childhood stunting in Northeast Brazil: the role of Schistosoma mansoni infection and inadequate dietary intake. Eur J Clin Nutr. 58(7):1022–9. pmid:15220944

38. Getaneh Z, Melku M, Geta M, Melak T, Hunegnaw MT. 2019. Prevalence and determinants of stunting and wasting among public primary school children in Gondar town, northwest, Ethiopia. BMC pediatrics. 19(1):207. pmid:31238889

39. Tigga PL, Sen J, Mondal N. 2015. Association of some socio-economic and socio-demographic variables with wasting among pre-school children of North Bengal, India. Ethiop J Health Sci. 25(1):63–72. pmid:25733786

40. Ministry of Public Health and Population. 2013. Yemen National Health and Demographic Survey. Ministry of Health and Population, Yemen.

41. Chandrakumari AS, Sinha P, Singaravelu S, Jaikumar S. 2019. Prevalence of Anemia Among Adolescent Girls in a Rural Area of Tamil Nadu, India. Journal of family medicine and primary care. 8(4):1414–7. pmid:31143731

42. Elayappen A, Muthukumar A. 2014. Anemia in an Adolescent Male: Is It a Red Flag? Glob Pediatr Health. 1:2333794X14550524.

43. Engidaw MT, Wassie MM, Teferra AS. 2018. Anemia and associated factors among adolescent girls living in Aw-Barre refugee camp, Somali regional state, Southeast Ethiopia. PloS one. 13(10):e0205381. pmid:30308060

44. Rati SA, Jawadagi S. 2014. Prevalence of Anemia among adolescent girls studying in selected schools. Int J Sci Res. 3(8):1237–42.

45. Regasa RT, Haidar JA. 2019. Anemia and its determinant of in-school adolescent girls from rural Ethiopia: a school based cross-sectional study. BMC Womens Health. 19(1):98. pmid:31315626

46. Gonete KA, Tariku A, Wami SD, Derso T. 2018. Prevalence and associated factors of anemia among adolescent girls attending high schools in Dembia District, Northwest Ethiopia, 2017. Arch Public Health. 76:79. pmid:30598822

47. Adelman S, Gilligan DO, Konde-Lule J, Alderman H. 2019. School Feeding Reduces Anemia Prevalence in Adolescent Girls and Other Vulnerable Household Members in a Cluster Randomized Controlled Trial in Uganda. J Nutr. 149(4):659–66. pmid:30926996

48. Neervoort F, von Rosenstiel I, Bongers K, Demetriades M, Shacola M, Wolffers I. et.al 2013. Effect of a school feeding programme on nutritional status and anaemia in an urban slum: a preliminary evaluation in Kenya. J Trop Pediatr. 59(3):165–74. pmid:23243080

49. Rakesh PS, George LS, Joy TM, George S, Renjini BA, Beena KV. et.al 2019. Anemia Among School Children in Ernakulam District, Kerala, India. Indian J Hematol Blood Transfus. 35(1):114–8. pmid:30828157

50. Abou-Zeid AH, Abdel-Fattah MM, Al-Shehri AS, Hifnawy TM, Al-Hassan SA. 2006. Anemia and nutritional status of schoolchildren living at Saudi high altitude area. Saudi Med J. 27(6):862–9. pmid:16758052

51. Egbi G, Steiner-Asiedu M, Kwesi FS, Ayi I, Ofosu W, Setorglo J, et al. Anaemia among school children older than five years in the Volta Region of Ghana. The Pan African medical journal. 2014;17 Suppl 1:10. pmid:24644526

52. Bahrami A, Khorasanchi Z, Tayefi M, Avan A, Seifi N, Tavakoly Sany SB, et al. 2019. Anemia is associated with cognitive impairment in adolescent girls: A cross-sectional survey. Appl Neuropsychol Child. 1–7. pmid:30661397