ABSTRACT
Schistosomiasis and anemia, are one of the leading global public health problem among children between age 5 and 14 years in marginalized settings. In this study, we provide prevalence and intensity data for both conditions in three southwestern states of Nigeria, where such are lacking. Epidemiological assessment involving parasitological analysis of urine and blood samples was conducted among 1783 consenting school-aged children in Ondo, Osun, Ekiti States of Nigeria. Participants’ age and sex data were obtained using field forms, and statistical analysis was performed in R software with a significance level of 95%. An overall prevalence of 26.8% and 29.5% was recorded for urinary schistosomiasis and anemia, respectively. Prevalence varied by location with (40.3% and 29.8%) in Ondo (34.4% and 37.5%) in Osun and (13.4% and 20.9%) in Ekiti for urinary schistosomiasis and anemia, respectively (p=0.00). Schistosoma infections were found among males (28.7%, p=0.05) and children between the age 9–11 years (30.0%, p=0.01). About 36% of children with anemia was also infected with schistosomiasis. Children who were positive for schistosomiasis (OR:1.51; 95% CI: 1.19, 1.93; p=0.001) and between the age category 15–16 years, (OR:1.86; 95% CI: 1.12, 3.09; p<0.05) were twice likely to become anemic. Our findings have shown that children infected with schistosomiasis are twice likely to become anemic than those without infection. It is important to complement ongoing MDA programmes targeted at schistosomiasis with nutrition intervention programs for example micronutrient supplementation for better impact and cost-effectiveness.
KEYWORDS: Urinary schistosomiasis, School-aged children, Anemia, Microhaematuria, Nigeria
Introduction
Schistosomiasis is one of the most common neglected tropical diseases (NTDs) requiring public health attention in the world and is caused by water-borne trematode parasites of the genus Schistosoma [1]. It is widely distributed in Africa, the Middle East, the Caribbean, Brazil, Venezuela and Suriname [1,2]. More than 206 million people in 78 countries are currently affected [2], with 90% of them living in Africa [2,3]. Schistosoma haematobium, one of the six known species of Schistosoma, is the predominant cause of schistosomiasis in the African region [2]. This parasitic worm primarily inhabits the vesicular and pelvic venous plexus of the bladder, leading to urinary schistosomiasis [4]. The severity of infection, including the duration of infestation and the number of parasites, as well as the migration of the worms through various organs and tissues, contribute to the pathological effects of the disease [4–6]. Additionally, inflammatory responses to the eggs laid by the adult worms further contribute to the pathology [4–6]. The disease can lead to complications such as bladder and ureter fibrosis, kidney damage, and in advanced cases, bladder cancer [4–6].
The majority of S. haematobium infections predominantly occur in childhood due to domestic and recreational activities in water bodies infested with the parasite [7,8]. The most common symptom of infection is hematuria, which is characterized by the presence of blood in the urine. Hematuria is a result of the entrapment of terminally spined S. haematobium eggs in the bladder, ureters, and genital tract. The inflammatory response to the eggs results in the destruction of parenchymal tissue, inflammation, and fibrosis, ultimately leading to significant blood loss in over 50% of cases [9]. This condition has been associated with anemia, which is another significant global public health problem that particularly affects young children and pregnant women [10].
Anemia is characterized by a lower-than-expected number of red blood cells or a decreased concentration of hemoglobin in the blood [10]. This condition diminished the blood’s capacity to transport oxygen to bodily tissues for metabolic activities. Individuals with anemia may experience symptoms such as fatigue, weakness, dizziness, shortness of breath, pale or yellowish skin, arrhythmia, hypersomnia, back pain, and headaches [11]. Both anemia and schistosomiasis often manifest during childhood, and their continued neglect may contribute to increased susceptibility to other infectious diseases, fatigue, reduced physical capacity, lower cognitive function, and diminished economic productivity as affected individuals grow into adulthood [12,13].
In the past decade, the World Health Organization (WHO) has implemented a large-scale administration of praziquantel (PZQ) medicines to children aged 5 to 14 as a strategy to control schistosomiasis [14]. Since 2010, over 250 million doses of PZQ have been distributed globally, with approximately 75.3 million people treated in 2021 alone [1,15]. The aim of schistosomiasis control programs is to reduce the prevalence of moderate- and heavy-intensity infections and overall infection rates to eliminate the associated morbidity [15]. Nigeria is among the countries in Africa where schistosomiasis is endemic [1]. The country has 36 states and 774 local government areas (LGAs), with 708 LGAs mapped by the Federal Ministry of Health (FMoH), and 608 of them identified as endemic areas [16]. Since 2009, treatment with praziquantel has been implemented in 27 states with the support of WHO, UNICEF, and partner organizations including Mission to save the helpless (MITOSATH), Sightsavers, AMEN Foundation, among others [16]. Anemia has been reported to be endemic in areas with a high schistosomiasis burden, thus presenting opportunities for integrating schistosomiasis control programs with micronutrient supplementation [17]. In Nigeria, emerging evidence shows that children infected with urinary schistosomiasis have poor anemic status [18–20]. This study, therefore aims to contribute to existing body of evidence in areas where schistosomiasis control programs are been implemented, but the relationship between anemia and urinary schistosomiasis are not yet known. The findings of this study could contribute to the ongoing discussion regarding the potential integration of nutrition intervention programs and mass drug administration (MDA) programs for schistosomiasis control, with a focus on the cost-effectiveness of such integrated approaches.anemiaurinaryanemiaurinary
Methodology
Study area
The study was conducted in three randomly selected states in the southwestern region of Nigeria, namely Osun, Ondo, and Ekiti (Figure 1). These states were purposively selected from the six states in the region, owing to the absence of literatures on schistosomiasis and anemia after a surface web-search. Ekiti has a population estimate of approximately 3.7 million inhabitants, while Ondo and Osun have around 4.7 million each [21]. The selected states share similar characteristics in terms of climate, topography, and rurality index, which ranges from 3.6 in Ekiti to 3.9 in Osun and Ondo [22]. The presence of fertile soil, tropical rainforests, lakes, and rivers in these areas supports agricultural and fishing activities, as well as the transmission of schistosomiasis [23–25].
Figure 1.
Map of southwest Nigeria, showing the study locations as highlight with Nigeria as inset.
Study design, sample size estimations and selection of study participants
This study utilized a cross-sectional sampling design, involving the administration of questionnaires and collection of urine and blood samples from school-aged children. The study design and sample size estimations followed the guidelines provided by the World Health Organization (WHO) for helminthiasis surveys [26,27]. In total, seven local government areas (LGAs) were randomly selected across the three states: three LGAs in Ekiti, two LGAs each in Osun and Ondo. Within each LGA, a list of government-owned primary schools was obtained, and a stratified random cluster sampling method was used to select five schools, resulting in a total of 15 schools in Ekiti, 10 schools in Ondo, and 10 schools in Osun [27]. The sample size estimation followed WHO guidelines, which recommend recruiting a minimum of 50 pupils per school for helminthiasis surveys [26]. A total of 750 children from Ekiti, 500 children from Ondo, and 500 children from Osun, all between the ages of 5 and 14 years were targeted for enrollment. Within each school, children were selected based on their class grade (ranging from 1 to 6) using a systematic approach based on the enrollment figures provided by the school authorities [26]. In total, 1,783 children were enrolled in the study, with 789 children from Ekiti, 494 children from Ondo, and 500 children from Osun states, respectively.
Collection of blood and urine samples
A simplified field form was utilized to collect basic demographic details such as age and gender (refer to S1 for further details). Each participant was provided with a sterile urine specimen bottle that was pre-labeled with their unique identification number. They were instructed to provide 10 ml of urine within a one-hour timeframe, specifically between 10:00 am and 2:00 pm. Upon arrival, blood samples were collected from the participants using the capillary method. A sterile lancet was used to prick the participant’s thumb, and the capillary blood was collected into a capillary tube, which was then sealed with wax. Both the urine and blood samples were stored in ice-boxes to maintain their integrity and transported to the laboratory for further processing.
Parasitological assessment of blood and urine samples
All the collected blood and urine samples were promptly sorted and transported to the parasitology laboratory within a maximum of 2 hours after collection to ensure sample integrity. To identify Schistosoma haematobium (S. haematobium) eggs, the urine filtration method was employed. In this process, 10 ml of the urine sample was vigorously shaken and passed through a Whatman membrane filter. The filter, containing any captured eggs, was then carefully placed on a clean microscopic slide. The slide was examined under a microscope using both the x10 and x40 objective lenses to search for eggs with characteristic terminal spines. Quality control measures were implemented by having another microscopist reexamine the slides and re-count the eggs to ensure accuracy. A participant was considered infected if egg counts were recorded on both sheets of the two microscopists who examined the slides. The intensity of S. haematobium infection, indicated by the number of eggs per 10 ml of urine, was also determined and used to classify infections as light (1–49 eggs/10 ml of urine) or heavy (>50 eggs/10 ml of urine).
For the blood samples, capillary tubes containing the samples were spun in a microhematocrit centrifuge at a relative centrifugation force of 12,000–15,000 for 5 minutes. The resulting pack cell volume count (PCV) was then read. Two readings were taken for each sample, and an average was calculated. Participants were categorized based on their PCV levels to determine their anemia status. Those with a PCV of ≥46% were classified as non-anemic, PCV between 45% and 36% as mildly anemic, PCV between 36% and 34% as moderately anemic, and PCV < 34% as severely anemic.
Data management and analysis
The data obtained from the study were entered into Microsoft Excel, and imported into R software version 4.3.2 for analysis. Descriptive statistics, such as frequencies and percentages, were used to summarize and describe the variables of interest. To assess the associations between prevalence data, age, and gender, Chi-square statistics and logistic regression were employed. The odds ratio (OR) was calculated to estimate the magnitude of association between schistosomiasis, age, gender, and anemia. A significance level of 95% was used to determine statistical significance.
Results
Demographic characteristics of study participants
Table 1 shows the gender and age distribution of the study participants. A total of 1783 school aged children from 3 states; Ekiti (789, 44.2%), Ondo (494, 27.7%) and Osun (500, 28.0%), were enrolled into this study. The majority of the participants were males (944, 52.9%), compared to females (839, 47.1%). The gender distribution did not significantly differ across the states (p = 0.301). In terms of age category, the majority of participants fell between the ages of 9 and 11 (897, 50.3%). This was followed by children aged 5–8 years (540, 30.3%), 12–14 years (258, 14.5%), and 15–16 years (88, 4.9%). There were significant differences in the age distribution of participants across the states (p = 0.000).
Table 1.
Demographic characteristics of study participants.
| States |
|||||
|---|---|---|---|---|---|
| Variables | Ekiti (%) | Ondo (%) | Osun (%) | Total (%) | p-value |
| Gender | |||||
| Female | 382 (48.4) | 218 (44.1) | 239 (47.8) | 839 (47.1) | 0.301 |
| Male | 407 (51.6) | 276 (55.9) | 261 (52.2) | 944 (52.9) | |
| Total | 789 (100) | 494 (100) | 500 (100) | 1783 (100) | |
| Age in years | |||||
| 5–8 | 235 (29.8) | 173 (35.0) | 132 (26.4) | 540 (30.3) | 0.000 |
| 9–11 | 294 (37.2) | 290 (58.8) | 313 (62.6) | 897 (50.3) | |
| 12–14 | 197 (25.0) | 17 (3.4) | 44 (8.8) | 258 (14.5) | |
| 15–16 | 63 (8.0) | 14 (2.8) | 11 (2.2) | 88 (4.9) | |
| Total | 789 (100) | 494 (100) | 500 (100) | 1783 (100) | |
Prevalence and intensity of urinary schistosomiasis among the study participants
Table 2 shows the prevalence of urinary schistosomiasis among the study participants. Out of the 1783 participants examined, a total of 477 (26.8%) were infected with S. haematobium parasites. The prevalence varied across the states, with the highest prevalence observed in Ondo (40.3%), followed by Osun (34.4%) and Ekiti (13.4%) (p = 0.00). There were significant differences in the prevalence of infection across the states. Furthermore, the prevalence of schistosomiasis was significantly higher among males (28.7%) compared to females (25.6%) (p = 0.05). Among the different age categories, children between the ages of 9 and 11 years had the highest prevalence of infection (30.0%) (p = 0.01). In terms of infection intensity, the majority of the infected participants had light infections, with egg counts below 50 per 10 ml of urine examined. There were no significant differences in the proportion of participants with different infection intensities across gender (p = 0.71) and age categories (p = 0.86).
Table 2.
Prevalence and intensity of urinary schistosomiasis among the study participants.
|
S. haematobium infection |
||||||||
|---|---|---|---|---|---|---|---|---|
| Prevalence |
Intensity |
|||||||
| NR | NE | Positives (%) | Negatives (%) | p-value | Light | Heavy | p-value | |
| Location | ||||||||
| Ekiti | 789 | 789 | 106 (13.4) | 683 (86.6) | 0.00* | 106 (100) | 0 (0) | 0.02* |
| Ondo | 494 | 494 | 199 (40.3) | 295 (59.7) | 192 (96.5) | 7 (3.5) | ||
| Osun | 500 | 500 | 172 (34.4) | 328 (65.6) | 161 (93.6) | 11(6.4) | ||
| Total | 1783 | 1783 | 477 (26.8) | 1306 (73.2) | 459 (96.2) | 18 (3.8) | ||
| Gender | ||||||||
| Female | 839 | 839 | 206 (24.6) | 633 (75.4) | 0.05* | 199 (96.6) | 7 (3.4) | 0.71 |
| Male | 944 | 944 | 271 (28.7) | 673 (71.3) | 260 (95.9) | 11 (4.1) | ||
| Total | 1783 | 1783 | 477 (26.8) | 1306 (73.2) | 459 (96.2) | 18 (3.8) | ||
| Age groups (in years) | ||||||||
| 5–8 | 540 | 540 | 118 (21.9) | 422 (78.1) | 0.01* | 115(87.5) | 3 (2.5) | 0.86 |
| 9–11 | 897 | 897 | 269 (30.0) | 628 (70.0) | 258 (95.9) | 11 (4.1) | ||
| 12–14 | 258 | 258 | 71 (27.5) | 187 (72.5) | 68 (95.8) | 3 (4.2) | ||
| 15–16 | 88 | 88 | 19 (21.6) | 69 (78.4) | 18 (94.7) | 1 (5.3) | ||
| Total | 1783 | 1783 | 477 (26.8) | 1306 (73.2) | 459 (96.2) | 18 (3.8) | ||
NR: Number of children recruited; NE: Number of children examined; * significant difference at 95%.
Prevalence and intensity of anemia among the study participants
Table 3 shows the prevalence and intensity of anemia among the study participants. Of the 1783 participants, a total of 417 (29.5%) had anemia. The prevalence of anemia varied across the states, with the highest prevalence observed in Osun (37.5%), followed by Ondo (29.8%) and Ekiti (20.9%) (p = 0.00). There were significant differences in the prevalence of anemia across the states. Furthermore, the prevalence of anemia was higher among males (30.6%) compared to females (28.5%). Among the different age categories, children between the ages of 15 and 16 years had the highest prevalence of anemia (45.8%). In terms of anemia intensity, the majority of the participants in Osun (76.3%) and Ondo (79.4%) had moderate anemia, while in Ekiti, the majority had mild anemia (47%). Similarly, among males and females, the majority had moderate anemia. However, among children between the age group 15–16, the majority had mild anemia (81.8%), compared to other age groups where the majority had moderate anemia (48.4%–80.5%). There were significant differences in the proportion of participants by anemia intensity across the age categories (p = 0.00).
Table 3.
Prevalence and intensity of anemia among the study participants.
| Anemia |
|||||||||
|---|---|---|---|---|---|---|---|---|---|
| Prevalence |
Intensity |
||||||||
| NR | NE | Positives | Negatives | p-value | Mild | Moderate | Severe | value | |
| Location | |||||||||
| Ekiti | 789 | 478 | 100 (20.9) | 378 (79.1) | 0.00* | 52 (52.0) | 47 (47.0) | 1 (1.0) | 0.00* |
| Ondo | 494 | 439 | 131 (29.8) | 308 (70.2) | 27 (20.6) | 104 (79.4) | 0 (0) | ||
| Osun | 500 | 496 | 186 (37.5) | 310 (62.5) | 36 (19.4) | 142 (76.3) | 8 (4.3) | ||
| Total | 1783 | 1413 | 417 (29.5) | 996(70.5) | 115 (27.6) | 293 (70.3) | 9 (2.2) | ||
| Gender | |||||||||
| Female | 839 | 674 | 191 (28.3) | 483(71.7) | 0.36 | 47 (24.6) | 140 (73.3) | 4 (2.1) | 0.45 |
| Male | 944 | 739 | 226 (30.6) | 513(69.4) | 68 (30.1) | 153 (67.7) | 5 (2.2) | ||
| Total | 1783 | 1413 | 417 (29.5) | 996(70.5) | 115 (27.6) | 293 (70.3) | 9 (2.2) | ||
| Age groups | |||||||||
| 5–8 | 540 | 409 | 128 (31.3) | 281 (68.7) | 0.002* | 23 (18.0) | 103 (80.5) | 2 (1.6) | 0.00* |
| 9–11 | 897 | 737 | 194 (26.3) | 543 (73.7) | 36 (18.6) | 154 (79.4) | 4 (2.1) | ||
| 12–14 | 258 | 195 | 62 (31.8) | 133 (68.2) | 29 (46.8) | 30 (48.4) | 3 (4.8) | ||
| 15–16 | 88 | 72 | 33 (45.8) | 39 (54.2) | 27 (81.8) | 6 (18.2) | 0 (0) | ||
| Total | 1783 | 1413 | 417 (29.5) | 996 (70.5) | 115 (27.6) | 293 (70.3) | 9 (2.2) | ||
NR: Number of children recruited; NE: Number of children examined; * significant difference at 95%.
Association between anemia, schistosomiasis, location, gender and age categories
Table 4 shows the association between anemia, schistosomiasis, location, gender and age categories. Among those infected with schistosomiasis, approximately 36% were also anemic. Schistosomiasis showed a significant association with anemia. Children who tested positive for schistosomiasis had increased odds of being anemic, with an odds ratio (OR) of 1.51 (95% CI: 1.19, 1.93), indicating that they were twice as likely to become anemic compared to those who tested negative (p = 0.001). Location was also associated with anemia. Children from Osun had higher odds of being anemic, with an odds ratio of 2.27 (95% CI: 1.70, 3.02), followed by children from Ondo with an odds ratio of 1.61 (95% CI: 1.19, 2.17) compared to children from Ekiti (p = 0.002 and p = 0.000, respectively).
Table 4.
Association between anemia, schistosomiasis, location, gender and age categories.
| Prevalence of Anemia |
|||||
|---|---|---|---|---|---|
| N= 1413 | Positives | Negatives | OR (95% CI) | p-value | |
| Prevalence of Schistosomiasis | |||||
| Negative | 981 | 263 (26.8) | 718 (73.2) | 1 | - |
| Positive | 432 | 154 (35.6) | 278 (64.4) | 1.51(1.19,1.93) | 0.001 |
| Total | 1413 | 417 (29.5) | 996 (70.5) | ||
| State | |||||
| Ekiti | 478 | 100 (20.9) | 378 (79.1) | 1 | |
| Ondo | 439 | 131 (29.8) | 308 (70.2) | 1.61(1.19,2.17) | 0.002 |
| Osun | 496 | 186 (37.5) | 310 (62.5) | 2.27(1.70,3.02) | 0.000 |
| Total | 1413 | 417 (29.5) | 996 (70.5) | ||
| Gender | |||||
| Female | 674 | 191 (28.3) | 483(71.7) | 1 | |
| Male | 739 | 226 (30.6) | 513(69.4) | 1.11(0.89, 1.40) | 0.36 |
| Total | 1413 | 417 (29.5) | 996 (70.5) | ||
| Age groups | |||||
| 5–8 | 409 | 128 (31.3) | 281 (68.7) | 1 | |
| 9–11 | 737 | 194 (26.3) | 543 (73.7) | 0.78(0.60,1.02) | 0.07 |
| 12–14 | 195 | 62 (31.8) | 133 (68.2) | 1.02(0.71, 1.48) | 0.12 |
| 15–16 | 72 | 33 (45.8) | 39 (54.2) | 1.86(1.12,3.09) | 0.02 |
| Total | 1413 | 417 (29.5) | 996 (70.5) | ||
X2: Chi-square value; df: degree of freedom; OR: Odd ratio; CI: Confidence interval; * significant difference at 95%.
Discussion
There is paucity of published data on the anemic status of children infected with schistosomiasis in Nigeria. This study therefore provides additional information to support the emerging need of prevalence data on schistosomiasis and anemia among school-aged children. An overall prevalence of 26.8% was observed for urinary schistosomiasis among the 1783 examined children in three southwestern states of Nigeria i.e. Osun, Ondo and Ekiti. Before now, WHO recommended annual MDA (once in a year) among school-aged children when schistosomiasis prevalence is between 10% and 49.9% [14]. However, recent WHO guidelines stipulate biennial MDA (once in 2 years) to 50% of the school-aged children when prevalence is between 10% and 49.9% [28]. Our findings therefore re-validate the endemicity of schistosomiasis and the need for ongoing MDA campaigns across the study states.
Although, the prevalence estimates reported for schistosomiasis remains within the WHO recommended thresholds for biennial MDA [14], they are significantly higher in Osun and Ondo, compared to Ekiti. These estimates also varied when compared with other studies within each state [23–25,29,30], with the disparities better explained by the socio-ecological and environmental conditions of each study location [31]. Furthermore, we observed a significantly high prevalence for light infection (i.e. egg outputs below 50 per 10 ml of urine), which probably suggests that that morbidity associated with schistosomiasis might be under control because of ongoing MDA programs [32,33]. These findings are not entirely surprising, as the three study states are long-time beneficiaries of MDA implemented by Federal Ministry of Health (FMOH) with the support of Mission to Save the Helpless (MITOSATH) in Ekiti and Ondo State, and AMEN foundation in Osun State [34]. However, it is of importance to note that infection was higher among male gender and younger children, which corroborates with previous reports from Nigeria [31,35–37]. Risky behaviors such as swimming and playing in infested waterbodies have been highlighted as one of the significant pathways to acquiring infection among young male children [37–39]. It is therefore imperative to complement ongoing MDA campaigns with efforts targeted at improving children’s’ awareness about the disease and transmission patterns [37].
On the other hand, our findings revealed a prevalence of 29.5% for anemia across the study states, with specific prevalence approaching 38% in Osun, 30% in Ondo and 21% in Ekiti. The paucity of published evidence on anemia among school-aged children in the three states hindered our efforts to compare states’ specific prevalence data. Nevertheless, our overall prevalence is lower than the 73% reported by Bamidele in Osun [40], and the 69% reported by Gayawan [41] for all the six southwestern states. Also, the prevalence appears lower than the WHO threshold of 40% that portrays anemia as a severe public health problem within an area [42]. Nevertheless, our estimates remain worrisome, and confirms that anemia has been a long-held public health challenge among African school-aged children [12].
Our univariate regression model revealed that schistosomiasis, location, and age are important predictors of anemia. Children between ages 15 and 16 are twice more likely to become anemic compared to younger children, and children recruited from Osun and Ondo, are also twice exposed to becoming anemic compared to children in Ekiti. In addition, children infected with schistosomiasis are twice more likely to become anemic compared to those who are uninfected. Previous studies from Nigeria and Ethiopia have also shown that children infected with intestinal parasites [43], and malaria [44,45] are more likely to be anemic than those who are not-infected. However, the causes of anemia are multifactorial, with implication on parasitic infection [43–46], low dietary iron intake [47], sickle cell anemia [48] and malnutrition [45,49]. As such, the relationship between schistosomiasis and anemia remains unclear [50], and potential mechanisms including extra-corporeal loss of iron, splenomegaly leading to red blood cell sequestration, autoimmune hemolysis and anemia of inflammation have recently been discussed here [9].
Conclusion
Our findings have shown that children infected with schistosomiasis are twice likely to become anemic than those without infection, with a high proportion of our study participant been positive for schistosomiasis and anemia. Although, majority of the participants exhibited moderate intensity for both health condition, however, the case of neglect of this population may contribute to worsening of both conditions, with Schistosoma infection, transiting from light to heavy infection, and the anemia transiting from mild/moderate to severe condition. It is therefore important to address these public health issues by complementing existing nutrition intervention programs with micronutrient supplementation, or possibly integrate them with ongoing MDA programmes targeted at schistosomiasis for cost-effectiveness anemia
Limitation of the study
A significant limitation of this research is the absence of an assessment of other intestinal parasites like hookworms and Trichuris spp., as well as blood parasites such as Plasmodium spp., which might have an impact on anemia. Second, the data collected from the study participants were limited to age and sex, which restricted the scope of covariates considered in the anemia model.anemia
Statement of authors’ contribution
BA, MAM designed and conceptualized the study. BA, MAM, JBB prepared the protocol, while BA, MAM, JBB, HOM improved the protocol, BA, MAM, MAS, DOA participated in field surveys and data collection. MBA, DOA, EOB handled laboratory analysis of urine and blood specimens. HOM performed all statistical analysis and prepared the first draft of the manuscript. All authors contributed to the development of the final manuscript and approved its submission.
Acknowledgements
We are grateful to the community leaders, school authorities and parents across the study areas
Funding Statement
This work received partial support from the Nigerian Institute of Medical Research Grant for studies on Neglected Tropical Diseases [Grant number 0000134].
Disclosure statement
No potential conflict of interest was reported by the author(s).
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Supporting files
S1 : Field Form
Ethics statement and considerations
The study protocol was approved by the ethical review board of the Nigerian Institute of Medical Research (NIMR/MR/15.S). Requisite approvals and field permits were also obtained from the three study states prior to commencement of data collection. Permissions were also obtained from school authorities and parents of the study participants. Only children who were above 6 years of age, and whose parents consented to their participation through a written informed consent, were invited to participate in the study. Children’s assent was obtained verbally and also documented through an assent form in the presence of the class teacher. Unique identifiers and a password protected database were also used to ensure anonymity and confidentiality through the study procedures. The study procedures were implemented in accordance with the ethical standards of the Helsinki Declaration (1964, amended most recently in 2008) of the World Medical Association.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.