https://orcid.org/0000-0002-0543-5463
Figures
Abstract
Background
Routine epidemiological data are essential for monitoring the effectiveness of preventive chemotherapy (PC), optimizing resource allocation, and addressing the evolving needs in the elimination of soil-transmitted helminthiasis (STH). This study assesses the prevalence, intensity, and associated risk factors of STH following five rounds of albendazole-based PC in three implementation units (IUs) in Ondo State, Nigeria.
Methodology
Fresh stool samples were collected from 2,093 children aged 5–14 years across 45 systematically selected schools in three IUs: Ese-Odo, Irele, and Ile-Oluji. The samples were analyzed using the Kato-Katz technique. Additionally, standardized questionnaires were administered to gather data on demographics and access to water, sanitation, and hygiene (WASH) resources. Data analysis was conducted using R software version 4.3.2, with a 95% confidence interval.
Principal findings/conclusions
The parasitological data indicated a significant decline in the aggregated prevalence of STH across the three IUs. In Ese-Odo, the prevalence decreased to 25.8% (95% CI: 23.0–29.0) from 39% at baseline (d = −34%, p = 0.00). In Irele, prevalence dropped to 9.7% (95% CI: 7.6–12.0) from 51.3% at baseline (d = −81%, p = 0.00), and in Ile-Oluji, prevalence was reduced to 6.4% (95% CI: 4.6–8.7) from 23% at baseline (d = −72.2%, p = 0.00). The most prevalent STH species was Ascaris lumbricoides, with infection rates of 25.5%, 9.4%, and 6.4% in Ese-Odo, Irele, and Ile-Oluji, respectively, followed by Trichuris trichiura in Ese-Odo (2.7%) and Irele (0.4%), while hookworm infections were detected only in Irele (0.7%). The majority of infections were of low intensity in Ese-Odo (91.0%), Irele (96.8%), and Ile-Oluji (100%). Access to improved sanitation (17.7%, 54.9%, and 58.2%), improved water sources (24.5%, 66.1%, and 69.8%), and handwashing facilities (9.0%, 39.6%, and 25.4%) was suboptimal and significantly varied across Ese-Odo, Irele, and Ile-Oluji, respectively (p < 0.05). Open defecation rates were high in Ese-Odo (54.2%), Irele (36.3%), and Ile-Oluji (34.3%). In Ese-Odo, significant risk factors for STH infection included the use of hand-pump boreholes (AOR: 2.44, 95% CI: 1.23–4.88, p = 0.01), unprotected dug wells (AOR: 3.25, 95% CI: 0.96–11.36, p = 0.06), ventilated improved pit latrines (AOR: 3.95, 95% CI: 1.13–16.1, p = 0.04), pit latrines without a slab (AOR: 2.19, 95% CI: 1.27–3.8, p = 0.01), and failure to use soap after defecation, both when soap was available (AOR: 12.09, 95% CI: 1.86–112.97, p = 0.01) and when soap was unavailable (AOR: 8.19, 95% CI: 1.73–76.65, p = 0.04). In Irele, access to protected dug wells was marginally significant (AOR: 1.79, 95% CI: 0.96–3.21, p = 0.06), while in Ile-Oluji, access to river water emerged as a significant risk factor (AOR: 7.97, 95% CI: 1.81–58.58, p = 0.02). The use of rainwater was found to be protective across all three IUs. These findings demonstrate significant progress in reducing STH prevalence across the three IUs following PC interventions. However, the data underscores the need for enhanced efforts to improve access to and use of WASH facilities to achieve STH elimination.
Author summary
The World Health Organization (WHO) recommends reducing soil-transmitted helminthiasis (STH) prevalence to below 20% and moderate-to-heavy infections to less than 2% in treated areas to achieve elimination targets. Endemic countries, including Nigeria, have implemented mass albendazole administration to children aged 5–14 years to meet these goals. After a decade of such interventions in Nigeria, reassessing the infection status is essential for determining whether to adjust or discontinue the program. This study analyzed stool samples from 2,093 children across three implementation units (IUs) in Ondo State. The results indicated significant reductions in STH prevalence to below 20% in two of the three IUs, with no heavy infections reported in any IU. While these findings demonstrate the effectiveness of the PC interventions, the study also identified poor access to water, sanitation, and hygiene (WASH) resources, highlighting the need for improvements in these areas to sustain progress and prevent infection resurgence.
Citation: Mogaji HO, Olamiju FO, Oyinlola F, Achu I, Adekunle ON, Udofia LE, et al. (2025) Prevalence, intensity and risk factors of soil-transmitted helminthiasis after five effective rounds of preventive chemotherapy across three implementation units in Ondo State, Nigeria. PLoS Negl Trop Dis 19(1): e0012533. https://doi.org/10.1371/journal.pntd.0012533
Editor: María Victoria Periago, Consejo Nacional de Investigaciones Cientificas y Tecnicas, Fundación Mundo Sano, ARGENTINA
Received: September 12, 2024; Accepted: December 16, 2024; Published: January 6, 2025
Copyright: © 2025 Mogaji et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: The datasets used and analyzed during the current study have been attached as Supporting information [See here at https://zenodo.org/records/14269956.].
Funding: This study was supported by The END Neglected Diseases Fund (ENDFund) as part of 2023 financial support to FOO of Mission To Safe The Helpless (MITOSATH) for the control and elimination of PC-NTDs in Ondo State, Nigeria. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Authors LM and MO received a salary from The END Neglected Diseases Fund (ENDFund).
Competing interests: The authors have declared that no competing interests exist.
Introduction
Soil-transmitted helminthiasis (STH) is a widespread yet preventable neglected tropical disease, affecting over 1.5 billion people globally, with a significant burden in sub-Saharan Africa [1–3]. STH is caused by four parasitic nematodes: Ascaris lumbricoides (roundworm), Trichuris trichiura (whipworm), Necator americanus (hookworm), and Ancylostoma duodenale (hookworm), which require soil for the development of their eggs [3,4]. Infection occurs primarily through the fecal-oral route, with individuals ingesting infective eggs of roundworm and whipworm or through skin penetration by hookworm larvae [3–6]. Transmission is often facilitated by inadequate infrastructure, particularly poor sanitation and hygiene practices, leading to contamination of water, soil, and food [7,8]. Rural and marginalized urban populations are particularly vulnerable, where sanitation and hygiene facilities are often absent or underutilized [9,10]. Young children, due to their developing immunity and increased exposure, face a higher risk of infection, resulting in adverse health outcomes such as malnutrition, anemia, impaired cognitive development, and educational disruptions [3,11–13]. These detrimental effects underscore the importance of preventive chemotherapy (PC), which involves mass administration of albendazole or mebendazole to at-risk populations [14].
The World Health Organization (WHO) has adopted PC as a primary strategy to control and eliminate STH [3,15]. Over the past decade, the WHO, in collaboration with two pharmaceutical companies GlaxoSmithKline and Johnson & Johnson, has coordinated the distribution of over 600 million donated medicines [16]. PC programs are implemented based on the prevalence of STH, determined through baseline epidemiological surveys in which biannual PC is recommended when prevalence exceeds 50%, annual PC is advised when prevalence is between 20% and 49.9%, and clinical case management is suggested when prevalence is below 20% [2,3,15,16]. It is anticipated that treating approximately 75% of school-aged children over a period of 5–6 years will lead to a substantial reduction in STH endemicity [15,16]. Therefore, epidemiological surveys after five of effective (≥75%) rounds of PC are essential to evaluate program impact, optimize resource allocation, adjust or discontinue PC frequency, and mitigate the risk of developing drug resistance [2,3,15,16].
Nigeria, with its large population, is the most endemic country for STH compared to other sub-Saharan African countries [1,17–19]. Over the past 8 years, the country has benefited from PC programs supported by donated medicines, and some areas are now presumed to have significantly reduced STH prevalence [20]. Given these developments, it is critical to conduct impact assessments to determine the status of STH to guide decisions on future PC interventions. In this study, we evaluated the prevalence and intensity of STH following five effective rounds of albendazole PC interventions in three implementation units (IUs), corresponding to Local Government Areas (LGAs), in Ondo State, Nigeria.
Materials and Methods
Ethics
This study received ethical approval from the Ondo State Health Research Ethics Committee (approval number: NHREC/18/08/2016) and the Neglected Tropical Diseases Unit of the Federal Ministry of Health (reference number: NSCP/6/7/IV/23). Prior to data collection, we engaged key stakeholders from the Ministries of Health and Education at both the State and LGA levels in the study areas. This included organizing community meetings with representatives from the participating communities and schools. During these meetings, we provided detailed information to community leaders, teachers, parents, and children about the study’s objectives, procedures, and target population. Participation in the study was entirely voluntary and required written informed assent from the minors (aged 5–14 years) and written consent from their legal guardians. Children who agreed to participate provided written assent in the form of signatures or, where applicable, thumbprints on pre-printed informed consent forms (ICFs) on the day of sample collection. Only assenting children whose parents had previously provided written consent, and who also received consent from a teacher on the day of sample collection, were included in the study.
Study area and settings
This study was conducted in the Ese-Odo, Irele, and Ile-Oluji Local Government Areas (LGAs) of Ondo State, located in Southwestern Nigeria. Ondo State comprises 18 LGAs with a population exceeding three million people. Baseline epidemiological mapping for soil-transmitted helminthiasis (STH) was conducted in 2013, revealing that 4 LGAs had endemicity levels below 20%, 12 had endemicity between 20% and 50%, and 2 LGAs had endemicity above 50% [20] (Fig 1). Since 2013, the Federal and State Ministries of Health, in collaboration with partners such as EndFUND and Mission to Save the Helpless (MITOSATH), have implemented more than nine rounds of preventive chemotherapy (PC) with albendazole [20]. To date, an average of five effective PC rounds with therapeutic coverage exceeding 75% has been achieved. The three LGAs included in this assessment have met the minimum requirement of 5–6 effective PC rounds, making them eligible for an impact assessment survey.
This map was created using primary data collected by the authors and developed in ArcGIS v10.3 software. Shapefiles for Nigeria, including boundary polygons and water bodies across all administrative levels, were sourced from publicly accessible databases available at Humanitarian Data Exchange, and are licensed under CC BY 4.0 (https://data.humdata.org/). No changes were made to the original shapefiles. The authors grant permission for the reuse of this map without restriction, provided appropriate credit is given to the source.
Study design and selection of sampling sites
This assessment utilized a cross-sectional sampling design conducted between March and April 2024. Data were collected through standardized questionnaires, and stool samples were obtained from school-aged children (SAC) across 45 systematically selected sampling sites (15 per LGA) in three Local Government Areas (LGAs). The sampling sites comprised government-owned primary schools, and participants (children aged 5–14 years) were selected following World Health Organization (WHO) guidelines [21]. Schools within each LGA were stratified by sub-districts (wards), and one school per ward was randomly selected using a paper ballot system from every five schools. This method ensured unbiased selection and adequate geographic representation across the LGAs and Wards [21].
Sample size determination and selection of study participants
The World Health Organization (WHO) recommends recruiting 50 SAC aged 5–14 years to assess worm burden and the impact of preventive chemotherapy (PC) [15]. However, recent guidelines suggest prioritizing 30 older SAC aged 10–14 years [21]. To comply with both sets of recommendations, we recruited a minimum of 50 SAC per school, including 30 late SAC (10–14 years) and 20 early SAC (5–9 years). A total sample size of 750 children was targeted for recruitment in each Local Government Area (LGA).
Selection of study participants and exclusion criteria
Participants were recruited on school premises with the assistance of teachers. Children aged 5–9 years were selected from the first three primary school classes, with 6–7 boys and girls recruited per class. Children aged 10–14 years were selected from the fourth, fifth, and sixth primary school classes, with a target of at least 10 children (five boys and five girls) per class. A systematic selection process was employed: children were lined up by class and sex, assigned a number, and a sampling interval was calculated by dividing the total number of children by the required sample size per class. The first child was chosen through a paper ballot, and subsequent children were selected by adding the sampling interval to the previous child’s position. If the target sample size for a class was not met, additional children were recruited from the same class, school, or community. Exclusion criteria included children outside the target age range (5–14 years), those who were unwell, and those whose parents’ declined participation.
Questionnaire administration
We utilized a closed-ended electronic questionnaire to collect epidemiological data from participants. Two types of questionnaires were administered via Android or iOS devices: (i) a school form and (ii) an individual questionnaire, both of which have been previously validated and employed in similar epidemiological surveys by our research team [10,22,23]. The school form captured information on school names, geographic coordinates, enrolment figures, and the availability of water, sanitation, and hygiene (WASH) facilities. The individual questionnaire collected demographic data, including age, sex, parental occupation, household WASH facilities, and parasitological results from the stool samples. Copies of the questionnaires are accessible at https://zenodo.org/records/11080490. All data were collected electronically and securely transferred to a remote backup server following each interview. Interviews were conducted in Yoruba and held confidentially, with a legal guardian or parent present when necessary.
Collection of stool samples
Before administering the questionnaires, participants were required to complete informed consent forms and were assigned unique identification tags. These tags were affixed to their consent forms, sterile specimen containers, microscopic slides, and result sheets to maintain rigorous quality control throughout the data collection process. Participants were provided with applicator sticks, a plain sheet of paper, tissue paper, and soap to assist with stool collection. The voiding and collection process was supervised by a teacher and a member of the field team to ensure proper sample collection within the first hour of distribution and to prevent sample contamination or sharing. Bar soaps were distributed as incentives to promote good hygiene practices, with care taken to ensure that participants’ decisions to participate were voluntary and free from coercion.
Parasitological assessment of stool samples
Stool samples were processed on-site within two hours of collection at a mobile laboratory set up by the field team. The Kato-Katz technique was used to process the specimens, and a single thick smear was prepared from each sample. After a clearing period of 30 min, the smears were examined microscopically for parasite eggs [24]. For quality assurance, each slide was re-examined by a second microscopist, and egg counts were verified [24]. A participant was classified as positive if at least one egg from any of the target parasites was detected per slide.
Data Collection and Management
Data collection was remotely monitored using the KoboCollect platform, with field supervisors recording daily summaries through a closed-tracking tool developed in Microsoft Excel. This approach facilitated the triangulation of electronic uploads and enabled timely resolution of any discrepancies. Two distinct tracking tools were utilized during the study: one for school field forms and another for parasitology components. All collected data were imported into R Studio (version 4.3.2) for subsequent analysis using the tidyverse, gtsummary, stats and broom packages. The data were encoded using a predefined codebook, with prevalence data recorded as numeric values—‘0’ indicating no infection and ‘1’ indicating infection for each observed soil-transmitted helminth (STH) species with an egg count greater than one. Overall infection status (i.e., any STH infection) was determined by summing values across rows using the ‘rowSums’ function. Infection intensity, expressed as eggs per gram (EPG) of stool, was calculated by multiplying the number of eggs observed per smear by 24. The intensity of Ascaris lumbricoides was classified as low (1–4,999 EPG), moderate (5,000–49,999 EPG), or high (≥50,000 EPG) [15]. For hookworms, intensities were classified as low (1–1,999 EPG), moderate (2,000–3,999 EPG), or high (≥4,000 EPG) [15]. Trichuris trichiura infections were categorized as low (1–999 EPG), moderate (1,000–9,999 EPG), or high (≥10,000 EPG) [15].
Data analysis and interpretation
The analysis and interpretation of data for preventive chemotherapy (PC) adjustments followed the most recent World Health Organization (WHO) guidelines for STH prevalence impact assessment surveys [21]. Local Government Areas (LGAs) were categorized into four prevalence groups: (1) <2%, (2) 2% to <10%, (3) 10% to <20%, and (4) ≥20%. For LGAs in the first group, PC is recommended only during specific events, alongside the establishment and maintenance of surveillance systems. For LGAs in the second group, biennial PC over 5 years is recommended, with continuous surveillance. LGAs in the third group are advised to implement annual PC for 5 years with ongoing surveillance, while those in the fourth group are required to administer annual PC for 5 years. The aggregated proportion of moderate and heavy infections (MHI) was also calculated for each LGA, using a threshold of ≤2%, where the upper bound of the 95% confidence interval (CI) was below this limit.
The percentage change in prevalence between baseline and impact assessment surveys was also computed. To evaluate associations between variables, chi-squared tests were employed, and Clopper-Pearson confidence intervals were calculated for prevalence estimates, where applicable. Univariate and multivariate logistic regression models were conducted to assess relationships between predictor variables (e.g., demographic characteristics and WASH conditions) and outcome variables (e.g., presence of any STH infection). Only variables with p ≤ 0.05 in univariate analysis were included in multivariate models. Confounders and multicollinearity were examined using the Variance Inflation Factor (VIF), and variables with a VIF exceeding five were excluded. Crude and adjusted odds ratios (ORs) with 95% CIs were calculated, with a significance level set at 0.05. Spatial distribution maps of STH across LGAs were generated using ArcGIS version 10.8. Further details on the dataset can be accessed at https://zenodo.org/records/14269956.
Results
Profile of study locations and participants
Table 1 presents a comprehensive profile of the study locations across the three Local Government Areas (LGAs) of Ese-Odo, Irele, and Ile-Oluji. Each LGA consists of ten sub-units, or wards, all of which were surveyed, achieving 100% geographic coverage. Sampling encompassed 22.1% of the 68 schools in Ese-Odo, 24.6% of the 61 schools in Irele, and 17.6% of the 85 schools in Ile-Oluji. Of the 750 school-aged children (SAC) targeted for recruitment in each LGA, 722 children (96.3%) were recruited in Ese-Odo, 750 children (100%) in Irele, and 621 children (82.8%) in Ile-Oluji. Stool samples were collected from 691 children in Ese-Odo (95.7%), 668 children in Irele (89.1%), and 613 children in Ile-Oluji (98.7%). The proportion of male participants exceeded that of females across all LGAs, comprising 54.0% in Ese-Odo, 50.4% in Irele, and 51.4% in Ile-Oluji. Additionally, a higher percentage of participants were in the 10–14-year age group: 54.8% in Ese-Odo, 59.6% in Irele, and 52.2% in Ile-Oluji (Table 1).
Prevalence and soil-transmitted helminthiasis across the LGAs
Table 2 provides a summary of the prevalence of soil-transmitted helminthiasis (STH) across the three surveyed Local Government Areas (LGAs): Ese-Odo, Irele, and Ile-Oluji. In Ese-Odo, 176 out of 691 individuals (25.5%) were infected with Ascaris lumbricoides (95% confidence interval [CI]: 22.0%–29.0%), with no cases of hookworm detected (0%). Nineteen individuals (2.7%) were found to have Trichuris trichiura infections (95% CI: 1.7%–4.3%). The overall prevalence of any STH in Ese-Odo was 25.8% (95% CI: 23.0%–29.0%). This represents a 37% reduction from the baseline prevalence of 40.7%, with a risk ratio of 0.63. However, species’ specific prevalence increased for Ascaris lumbricoides (14.35%) and Trichuris trichiura infection (3.85%).
In Irele, of the 668 individuals assessed, 63 (9.4%) were infected with Ascaris lumbricoides (95% CI: 7.4%–12.0%), 5 (0.7%) were found to have hookworm infections (95% CI: 0.28%–1.8%), and 3 (0.4%) were infected with Trichuris trichiura (95% CI: 0.12%–1.4%). The overall prevalence of any STH in Irele was 9.7% (95% CI: 7.6%–12.0%), indicating an 81% reduction from the baseline prevalence of 50.9%, with a risk ratio of 0.19. There was also a reduction in species’ specific prevalence for Ascaris lumbricoides (−66.7%), hookworms (−96.7%) and Trichuris trichiura infection (−82.6%).
In Ile-Oluji, out of 613 individuals surveyed, 39 (6.4%) were infected with Ascaris lumbricoides (95% CI: 4.6%–8.7%), with no cases of hookworm or Trichuris trichiura (0%, 95% CI: 0–0.78%). The overall STH prevalence in Ile-Oluji was 6.4% (95% CI: 4.6%–8.7%). This reflects a 72% decrease from the baseline prevalence of 23%, with a risk ratio of 0.28.
Site-specific prevalence and spatial distribution of soil-transmitted helminthiasis across the three LGAs
Figs 2–4 display the endemicity maps for the three Local Government Areas (LGAs) included in the study. In 2011, Ese-Odo LGA was classified as endemic, with an overall prevalence of 39%, placing it in the 20–50% prevalence category. As a result, preventive chemotherapy (PC) was administered annually for 5 years. Although the current impact assessment showed a reduction in overall prevalence, the LGA remains within the same endemicity threshold (20–50%), with more than 50% of surveyed sites reporting a prevalence above 20% (Fig 2).
This map was created using primary data collected by the authors and developed in ArcGIS v10.3 software. Shapefiles for Nigeria, including boundary polygons and water bodies across all administrative levels, were sourced from publicly accessible databases available at Humanitarian Data Exchange, and are licensed under CC BY 4.0 (https://data.humdata.org/). No changes were made to the original shapefiles. The authors grant permission for the reuse of this map without restriction, provided appropriate credit is given to the source.
This map was created using primary data collected by the authors and developed in ArcGIS v10.3 software. Shapefiles for Nigeria, including boundary polygons and water bodies across all administrative levels, were sourced from publicly accessible databases available at Humanitarian Data Exchange, and are licensed under CC BY 4.0 (https://data.humdata.org/). No changes were made to the original shapefiles. The authors grant permission for the reuse of this map without restriction, provided appropriate credit is given to the source.
This map was created using primary data collected by the authors and developed in ArcGIS v10.3 software. Shapefiles for Nigeria, including boundary polygons and water bodies across all administrative levels, were sourced from publicly accessible databases available at Humanitarian Data Exchange, and are licensed under CC BY 4.0 (https://data.humdata.org/). No changes were made to the original shapefiles. The authors grant permission for the reuse of this map without restriction, provided appropriate credit is given to the source.
In Irele LGA, the baseline prevalence was 51.3%, placing it in the category requiring PC twice annually for 5 years. The current impact assessment revealed a significant reduction in overall prevalence to 9.7%, moving the LGA into the 2–10% prevalence category. Only 2 of the 15 surveyed sites in Irele reported a prevalence above 20% (Fig 3).
In Ile-Oluji LGA, the baseline prevalence was 23%, placing it in the 20–50% endemicity category, which required annual PC for 5 years. The current impact assessment indicated a decrease in overall prevalence to 6.4%, positioning the LGA within the 2–10% threshold. Similar to Irele, only 2 of the 15 surveyed sites in Ile-Oluji had a prevalence above 20% (Fig 4). Detailed site-specific sex, age and prevalence data are provided in the Supporting information (Tables A and B in S1 File).
Intensity soil-transmitted helminthiasis infections across the three LGAs
Table 3 presents the distribution of potential morbidities associated with soil-transmitted helminth (STH) infections among the study participants. In Ese-Odo, 160 individuals (23.2%) infected with Ascaris lumbricoides had light infections, 15 (2.2%) had moderate infections, and one participant (0.1%) had a heavy infection. The 95% confidence intervals (CIs) for these infection levels ranged from 20% to 27% for light infections, 1.3% to 3.6% for moderate infections, and 0.01% to 0.93% for heavy infections (p = 0.001). For Trichuris trichiura, 19 participants (2.7%) exhibited light infections, with no moderate or heavy infections observed (p = 0.001).
In Irele, 61 individuals (9.1%) infected with Ascaris lumbricoides had light infections, and two participants (0.3%) had moderate infections (p = 0.001). The 95% CIs for light infections were 7.1–12%, and for moderate infections, 0.05–1.2%. Trichuris trichiura prevalence was very low, with only three participants (0.4%) exhibiting light infections, and no cases of moderate or heavy infections were detected (p = 0.064). Additionally, among the five participants (0.7%) infected with hookworms, all had light infections, with no moderate or heavy infections reported (p = 0.001).
In Ile-Oluji, 39 participants (6.4%) infected with Ascaris lumbricoides had light infections, with 95% CIs ranging from 4.6% to 8.7% (p = 0.001). No cases of moderate or heavy infections were observed for any of the helminths.
Status of water, sanitation and hygiene resources across the three LGAs
Table 4 details the status of water, sanitation, and hygiene (WASH) resources in the three local government areas (LGAs) studied. In Ese-Odo, the majority of the population, 579 individuals (80.2%), relied primarily on rivers as their main water source. Only a small fraction of participants had access to improved water sources, including protected dug wells (13.2%) and handpump boreholes (10.5%), while public taps were scarcely available (0.8%). Open defecation was a common practice, with 391 participants (54.2%) reporting this behavior. Pit latrines were widely used, with 119 participants (16.5%) utilizing pits without slabs and 66 participants (9.1%) using pits with slabs. A minority had access to flush toilets (5.8%) or ventilated improved pit latrines (2.8%). Regarding hygiene practices, only 65 participants (9.0%) reported having handwashing facilities in their toilets, and even fewer, 50 participants (6.9%), had access to soap within these facilities.
Similarly, in Irele, rivers were the most common water source, used by 442 participants (58.9%). Rainwater collection was another prevalent practice, reported by 329 participants (43.9%). Unprotected dug wells were used by 184 participants (24.5%), while public taps and handpump boreholes were available to 163 (21.7%) and 212 (28.3%) participants, respectively. Open defecation remained widespread and practiced by 272 participants (36.3%). Flush toilets were more commonly used in this LGA, with 220 participants (29.3%) reporting their use, followed by pit toilets with slabs (22.7%) and without slabs (19.5%). Handwashing facilities were available to 297 participants (39.6%), while 251 participants (33.5%) had soap in their toilets. A high proportion, 211 participants (84.1%), reported using soap after defecation.
In Ile-Oluji, rainwater was the primary water source for 366 participants (58.9%), followed by rivers, which were used by 339 participants (54.6%). Protected dug wells were another important water source for 275 participants (44.3%), though public taps (18.7%) and hand pumps (6.8%) were less frequently used. Open defecation was reported by 213 participants (34.3%). Among sanitation facilities, pit latrines with slabs were used by 154 participants (24.8%), flush toilets by 147 participants (23.7%), pit toilets without slabs by 68 participants (11.0%), and ventilated improved pit latrines by 60 participants (9.7%). Handwashing facilities were present in the toilets of 158 participants (25.4%), and 150 participants (94.9%) reported using soap after defecation, indicating a high level of hygiene compliance in this LGA.
Association between demography, WASH and STH infections
Tables 5–7 present the results of logistic regression analyses evaluating the associations between sex, age, and water, sanitation, and hygiene (WASH) variables with the risk of soil-transmitted helminth (STH) infection. In Ese-Odo (Table 5), the adjusted model identified several significant risk factors, including the use of handpump boreholes (adjusted odds ratio [AOR]: 2.44; 95% confidence interval [CI]: 1.23–4.88; p = 0.01), reliance on unprotected dug wells (AOR: 3.25; 95% CI: 0.96–11.36; p = 0.06), the use of ventilated improved pit latrines (AOR: 3.95; 95% CI: 1.13–16.1; p = 0.04), and pit latrines without slabs (AOR: 2.19; 95% CI: 1.27–3.8; p = 0.01). Not using soap after defecation, despite having access to it, was also a strong risk factor (AOR: 12.09; 95% CI: 1.86–112.97; p = 0.01), as was the absence or non-use of soap after defecation (AOR: 8.19; 95% CI: 1.73–76.65; p = 0.04). The use of rainwater was identified as a protective factor against infection (AOR: 0.39; 95% CI: 0.24–0.64; p < 0.001).
In Irele (Table 6), the adjusted model revealed that access to protected dug wells was a marginally significant risk factor (AOR: 1.79; 95% CI: 0.96–3.21; p = 0.06), while the use of pit latrines without slabs was associated with a lower risk of infection (AOR: 0.38; 95% CI: 0.13–0.87; p = 0.04).
In Ile-Oluji (Table 7), access to rivers was a significant risk factor for STH infection (AOR: 7.97; 95% CI: 1.81–58.58; p = 0.02), while access to rainwater was found to be protective (AOR: 0.47; 95% CI: 0.22–0.97; p = 0.05).
Discussion
This study represents the first official impact assessment of soil-transmitted helminthiasis (STH) in Ondo State, following a decade of preventive chemotherapy (PC) interventions using albendazole. The importance of this assessment is underscored by several factors: first, to evaluate the efficacy of PC in reducing worm burden; second, to avoid the misallocation of resources to areas where they are no longer necessary, thereby maximizing returns on investment in underserved regions; and finally, to generate evidence necessary for measuring progress and optimizing PC programs for maximal effectiveness [15].
Recent guidelines from the World Health Organization (WHO) emphasize that for an area to meet elimination targets, all implementation units must achieve four critical conditions: reducing overall prevalence to below 20%, reducing the prevalence of moderate and heavy infections to less than 2% (including upper confidence intervals), reaching women of reproductive age (WRA), and improving access to water, sanitation, and hygiene (WASH), with a particular focus on eliminating open defecation [21]. While most country programs, including that of Ondo State, have concentrated on meeting the first two conditions, less attention has been given to the equitable allocation of resources for WRA and investment in WASH. The findings of this assessment underscore the need to expand PC interventions by integrating comprehensive WASH strategies.
The assessment found significant reductions in STH infections across the three local government areas (LGAs) evaluated. In Irele and Ile-Oluji LGAs, prevalence decreased to below 10%, with Irele experiencing an 81% reduction and Ile-Oluji a 72% reduction. Consequently, participants in Irele are now at only 0.19 times the risk of STH compared to baseline, while participants in Ile-Oluji are at 0.28 times the baseline risk. These results align with WHO recommendations of conducting PC every 2 years over 5 years, followed by continuous surveillance [15]. However, in Ese-Odo, the reduction in prevalence was modest, decreasing from 39% at baseline to 25.8% at the time of assessment, with prevalence still exceeding 20%. Species’ specific prevalence also showed increased risk for Ascaris (1.14), and Trichuris (1.04). The risk of STH in Ese-Odo (0.63) remained considerably higher than in the other LGAs, indicating a need for annual PC over the next 5 years [15]. Ese-Odo had the poorest WASH conditions among the three LGAs, with a very considerable proportion of those sampled practicing open defecation, lacking access to handwashing facilities and relying heavily on rivers as their primary water source. Similar observations of limited progress despite PC interventions have been documented in countries such as Angola [25] and Kenya [26,27], where failures in implementation or lack of access to WASH have constrained program effectiveness [25,28].
While prevalence is commonly used to assess endemicity, infection intensity—measured by the number of parasitic eggs per gram of feces—is a more critical indicator of infection burden. Intensity levels provide a clearer indication of morbidity, as reductions in infection intensity correspond to diminished health risks from STH infections [29]. In line with WHO recommendations, the goal is to reduce the proportion of individuals with moderate or heavy infections to below 2% [15]. Among the three LGAs, only Ese-Odo had 2.3% of participants with moderate and heavy infections, predominantly due to Ascaris lumbricoides. Despite conducting six effective PC rounds (coverage >75%) out of nine since 2013, the high transmission rate in Ese-Odo raises concerns about demographic factors, WASH access, and the quality of implementation over the past decade [25].
Spatial analysis revealed that in Ese-Odo, more than 60% of sampled sites had prevalence rates ranging from 26% to 81%, with these high-prevalence areas widely dispersed. Baseline epidemiological surveys, conducted over a decade ago, used limited sampling strategies (typically five sites) within smaller frames to represent entire districts. Such methodologies reduce the ability to detect hotspots, particularly in areas with sparse or heterogeneously distributed infections [29,30]. Thus, the minimal reduction in prevalence observed in Ese-Odo may result from an underestimation of endemicity at baseline, a factor that influenced the decision to implement annual PC. Similar findings have been reported elsewhere, where outbreaks occurred in areas previously considered low endemic based on inadequate baseline data [28]. Consequently, robust assessment methodologies should be prioritized during PC program formulation or adjustments to ensure that sampling strategies are comprehensive and effective.
A disaggregated risk analysis was conducted to examine the relationship between infection data and WASH variables. Social-ecological systems, particularly those related to WASH, are critical to the transmission of STH [10]. The study hypothesized that the limited reduction in prevalence and higher proportion of moderate to heavy infections may be linked to inadequate WASH access. The data supported this hypothesis, revealing poor access to improved sanitation, water sources, and handwashing facilities across the LGAs. Ese-Odo stood out, with only 17.7% of households using improved sanitation facilities, 25% using improved water sources, and just 9% having access to handwashing facilities. Open defecation rates were alarmingly high at 54.2%, much worse than in the other LGAs. Regression models indicated that inadequate hygiene practices, such as failure to use soap after defecation, presented the highest risk for STH infection, followed by the use of unimproved latrines and water sources. These findings align with recent reports [31,32] and highlight the need for targeted interventions to improve WASH access and hygiene practices within these communities.
From a policy perspective, these findings underscore the need for timely impact assessments after five effective PC rounds, as recommended by WHO, to prevent resource wastage. Routine continuation of PC without evaluating its effectiveness leads to unnecessary expenditures in drug procurement and program operations, diverting funds from other health priorities. While past arguments pointed to the lack of standardized methods for impact assessment as a challenge, the recent WHO Monitoring and Evaluation (M&E) framework for schistosomiasis and STH provides clear guidelines for evaluation [21]. Donors and partners should thus prioritize impact assessments to enhance programmatic decision-making, prevent resource misallocation, and optimize the value of their investments. Further research into the comparative costs of conducting impact assessments versus continuing routine PC without evaluation is needed to provide stronger evidence of cost-efficiency. The present data offer clear evidence of the financial savings that can be achieved through timely evaluations, reinforcing the importance of sustainable and impactful disease control programs.
Although this study demonstrates a significant reduction in worm burden across the study LGAs, we acknowledge potential bias due to the exclusion of non-government schools and non-enrolled children. Our sampling targeted government-owned primary schools, which serve most school-aged children in these areas, where non-government schools are usually few, sparsely populated, and generally have better WASH facilities. As a result, worm burden among children in government-owned schools likely provides a more representative estimate of STH status. Additionally, while the absence of non-enrolled children and those unavailable during sampling may introduce some bias, our methodology adheres to WHO recommendations, supporting the validity of our findings despite these limitations. Finally, the absence of baseline data for WASH across the study locations makes it difficult to distinguish the individual contributions of WASH improvements and MDA.
Conclusion
The implementation of the preventive chemotherapy (PC) program for soil-transmitted helminthiasis (STH) has proven highly effective in Irele and Ile-Oluji, with prevalence rates reduced to less than 10%. However, in Ese-Odo, the reduction in prevalence has been limited to 66%, with current rates still around 25% and moderate-to-heavy infections persisting at 2.3%. The continued transmission of STH in Ese-Odo a riverine LGA is largely attributed to inadequate access to and use of water, sanitation, and hygiene (WASH) facilities. Given these findings, a shift to biennial PC in Irele and Ile-Oluji is recommended, while annual PC should be maintained in Ese-Odo for the next 5 years. Additionally, targeted investments in WASH infrastructure, with a priority focus on Ese-Odo, are crucial to complement PC efforts and facilitate progress toward STH elimination as a public health issue. Finally, this study emphasizes the importance of conducting impact assessments after five effective rounds of PC, as recommended by WHO, to optimize resource allocation and ensure the sustainability of control programs.
Supporting information
S1 File. Table A. Sex and Age characteristics of study participants across the three LGAs. Table B. Soil-transmitted helminthiasis prevalence across the three LGAs.
https://doi.org/10.1371/journal.pntd.0012533.s001
(DOCX)
Acknowledgments
We extend our heartfelt gratitude to the community leaders, health workers, education secretaries, and staff of the NTDs Control Department, Ondo State Ministry of Health, for their unwavering support and cooperation throughout this study. We sincerely acknowledge the contributions of individuals who served as field supervisors, technicians, interviewers, and members of the technical support team. We also appreciate the broader health community for their support and collaboration in this endeavor. The efforts of the following field workers are duly acknowledged: Jacob Babasola Ajayi, Oluwaseun Bunmi Awosolu, Oyinkansola Suliat Fadiji, Azeez God’sgift Ibrahim, Adedotun Ayodeji Bayegun, Cynthia Uchechukwu Umunnakwe, Olajumoke Olubukola Taiwo, Olubukola Deborah Adelakun, Effiong Okon Odiongenyi, Victor Kayode Gboyega, Stephen Ayodeji Oluwole, Ifeoluwa Adeniyi George, Promise Funmilayo Akinwale, Uzodimma Ikechukwu Vincent, Ridwan Olamilekan Mogaji, Oladotun Joseph Bankole, Damilola Rachael Adeleye, Boluwatife Ifeoluwa Adebayo, Abdulrahman Afolamade Aladejana, Orosunnegan Dunsin Elizabeth and Uwem Aniefiok Essien. Their dedication and hard work were instrumental to the success of this impact assessment.
References
- 1. Hotez PJ, Kamath A. Neglected tropical diseases in sub-saharan Africa: review of their prevalence, distribution, and disease burden. PLoS Negl Trop Dis. 2009;3(8):e412. pmid:19707588
- 2.
World Health Organization (WHO). Ending the neglect to attain the sustainable development goals: a road map for neglected tropical diseases 2021–2030. Geneva: World Health Organization; 2020.
- 3. World Health Organization (WHO). Fact sheet: soil transmitted helminthiasis [Online]; 2024 [cited 2024 Aug 8. ]. Available from: https://www.who.int/news-room/fact-sheets/detail/soil-transmitted-helminth-infections
- 4.
Sharma S, Anand N. Parasitic diseases: an overview, Chapter 1. In: Approaches to design and synthesis of antiparasitic drugs. Lucknow, India; 1997;25:1–45 ISBN: 978-0-444-89476-2.
- 5. Else KJ, Keiser J, Holland CV, Grencis RK, Sattelle DB, et al. Whipworm and roundworm infections. Nat Rev Dis Primers. 2020:28;6(1):44. pmid:32467581.
- 6.
Ghodeif AO, Hookworm JH. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2024 [cited 2024 Aug 8. ]. Available from: https://www.ncbi.nlm.nih.gov/books/NBK546648/
- 7. Ziegelbauer K, Speich B, Mäusezahl D, Bos R, Keiser J, Utzinger J. Effect of sanitation on soil-transmitted helminth infection: systematic review and meta-analysis. PLoS Med. 2012;9(1):e1001162. pmid:22291577
- 8. Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman MC. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med. 2014;11(3):e1001620. pmid:24667810
- 9. Mascarini-Serra L. Prevention of soil-transmitted Helminth infection. J Glob Infect Dis. 2011;3(2):175–82. pmid:21731306.
- 10. Ekpo UF, Mogaji HO. Feasibility of helminth worm burden as a marker for assessing the impact and success of water, sanitation, and hygiene interventions (WASH) for the control of neglected tropical diseases. Niger J Parasitol Res. 2023;1. Available from: https://njpar.com.ng/index.php/home/article/view/382
- 11. Crompton DWT, Whitehead RR. Hookworm infections and human iron metabolism. Parasitology. 1993;107(S1):S137–45.
- 12. Pabalan N, Singian E, Tabangay L, Jarjanazi H, Boivin MJ, Ezeamama AE. Soil-transmitted helminth infection, loss of education and cognitive impairment in school-aged children: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2018;12(1):e0005523. pmid:29329288
- 13. Ezeamama AE, Bustinduy AL, Nkwata AK, Martinez L, Pabalan N, Boivin MJ, et al. Cognitive deficits and educational loss in children with schistosome infection: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2018;12(1):e0005524. pmid:29329293
- 14. World Health Organization (WHO). Control of neglected tropical diseases. Preventive chemotherapy; 2024 [cited 2024 Aug 8. ]. Available from: https://www.who.int/teams/control-of-neglected-tropical-diseases/interventions/strategies/preventive-chemotherapy
- 15. World Health Organization (WHO). Helminth control in school-age children: a guide for managers of control programmes; 2011 [cited 2024 Aug 8. ]. Available from: https://www.who.int/neglected_diseases/resources/9789241548267/en/
- 16. Montresor A, Mupfasoni D, Mikhailov A, Mwinzi P, Lucianez A, Jamsheed M, et al. The global progress of soil-transmitted helminthiases control in 2020 and World Health Organization targets for 2030. PLoS Negl Trop Dis. 2020;14(8):e0008505. pmid:32776942
- 17. Oyeyemi OT, Okunlola OA. Soil-transmitted helminthiasis (STH) endemicity and performance of preventive chemotherapy intervention programme in Nigeria (in year 2021). Sci Rep. 2023;13(1):10155. pmid:37349411
- 18. Hotez PJ, Asojo OA, Adesina AM. Nigeria: “Ground Zero” for the high prevalence neglected tropical diseases. PLoS Negl Trop Dis. 2012;6(7):e1600. pmid:22860138
- 19. Mogaji HO, Johnson OO, Adigun AB, Adekunle ON, Bankole S, Dedeke GA, et al. Estimating the population at risk with soil transmitted helminthiasis and annual drug requirements for preventive chemotherapy in Ogun State, Nigeria. Sci Rep. 2022;12(1):2027. pmid:35132144
- 20. Expanded Special Project for Elimination of Neglected Tropical Diseases (ESPEN). [cited 2024 August 8. ]. Available from: https://espen.afro.who.int/countries/nigeria
- 21.
World Health Organization (WHO). Assessing schistosomiasis and soil-transmitted helminthiases control programmes: monitoring and evaluation framework. Geneva: World Health Organization; 2024 [cited 2024 Nov 11. ]. Licence: CC BY-NC-SA 3.0 IGO. Available from: https://iris.who.int/bitstream/handle/10665/379352/9789240099364-eng.pdf
- 22. Mogaji HO, Dedeke GA, Bada BS, Bankole S, Adeniji A, Fagbenro MT, et al. Distribution of ascariasis, trichuriasis and hookworm infections in Ogun State, Southwestern Nigeria. PLoS One. 2020;15(6):e0233423. pmid:32511237
- 23. Mogaji HO, Dedeke GA, Jaiyeola OA, Adeniran AA, Olabinke DB, Oluwole AS, et al. A preliminary survey of school-based water, sanitation, hygiene (WASH) resources and soil-transmitted helminthiasis in eight public schools in Odeda LGA, Ogun State, Nigeria. Parasitol Open. 2017;3:e16.
- 24.
World Health Organization. Bench aids for the diagnosis of intestinal parasites. 2nd ed; 2019 [cited 2024 April 27. ]. Available from: https://www.who.int/publications-detail-redirect/9789241515344
- 25. Bartlett AW, Mendes EP, Dahmash L, Palmeirim MS, de Almeida MC, Peliganga LB, et al. School-based preventive chemotherapy program for schistosomiasis and soil-transmitted helminth control in Angola: 6-year impact assessment. PLoS Negl Trop Dis. 2023;17(5):e0010849. pmid:37196040
- 26. Okoyo C, Campbell SJ, Williams K, Simiyu E, Owaga C, Mwandawiro C. Prevalence, intensity and associated risk factors of soil-transmitted helminth and schistosome infections in Kenya: Impact assessment after five rounds of mass drug administration in Kenya. PLoS Negl Trop Dis. 2020;14(10):e0008604. pmid:33027264
- 27. Mwandawiro C, Okoyo C, Kihara J, Simiyu E, Kepha S, Campbell SJ, et al. Results of a national school-based deworming programme on soil-transmitted helminths infections and schistosomiasis in Kenya: 2012-2017. Parasit Vectors. 2019;12(1):76. pmid:30732642
- 28. Olamiju F, Nebe OJ, Mogaji H, Marcus A, Amodu-Agbi P, Urude RO, et al. Schistosomiasis outbreak during COVID-19 pandemic in Takum, Northeast Nigeria: Analysis of infection status and associated risk factors. PLoS One. 2022;17(1):e0262524. pmid:35061823
- 29. Montresor A, Crompton DWT, Bundy DAP, Hall A, Savioli L. Guidelines for the evaluation of soil transmitted helminthiasis and schistosomiasis at community level; 1988 [cited 2024August 8. ]. Available from: https://iris.who.int/handle/10665/63821
- 30. Knowles SCL, Sturrock HJW, Turner H, Whitton JM, Gower CM, Jemu S, et al. Optimising cluster survey design for planning schistosomiasis preventive chemotherapy. PLoS Negl Trop Dis. 2017;11(5):e0005599. pmid:28552961
- 31. Atangana E, Oberholster PJ. Assessment of water, sanitation, and hygiene target and theoretical modeling to determine sanitation success in sub-Saharan Africa. Environ Dev Sustain. 2022;25:13353–77. pmid:36090188
- 32. Phillips AE, Ower AK, Mekete K, Liyew EF, Maddren R, Belay H, et al. Association between water, sanitation, and hygiene access and the prevalence of soil-transmitted helminth and schistosome infections in Wolayita, Ethiopia. Parasit Vectors. 2022;15(1):410. pmid:36333779