Abstract
Background
Soil-transmitted helminthiases (STH) and schistosomiasis are parasitic neglected tropical diseases (NTDs) of significant public health importance globally, including Nigeria. Urogenital schistosomiasis is highly endemic in Apojola, a rural community in Ogun State, southwest Nigeria, but data on STH and intestinal schistosomiasis in the neglected community are lacking.
Objectives
To determine the prevalence and intensity of STH and intestinal schistosomiasis and the risk factors associated with the infections in Apojola.
Methods
The study was community-based and cross-sectional. A structured questionnaire was used to obtain information on socio-demographic, personal, and household WASH characteristics of the study population. Stool samples were collected and processed for parasitological examination using the triplicate Kato-Katz (K-K) smears.
Results
A total of 283 individuals (males, 50.2%; females, 49.8%) aged 3 to 65 years (mean age ± S.D.: 19.6 ± 14.8 years) participated in the study. No case of intestinal schistosomiasis was recorded in the study, while the overall prevalence of any STH was 38.2%: A. lumbricoides (24.0%) and hookworms (25.8%). Prevalence of infection was not significantly different between males and females for any STH (40.1% vs. 36.2%, χ2 = 0.473, p = 0.492); A. lumbricoides (23.2% vs. 22.7%, χ2 = 0.012, p = 0.913); or hookworms (28.2% vs. 23.4%; p = 0.360; χ2 = 0.839), but significantly varied with age for any STH (χ2 = 22.225, p = 0.002); A. lumbricoides (χ2 = 16.354, p = 0.022); or hookworms (χ2 = 20.001, p = 0.006). The intensity of infection was neither associated with gender nor age and was mostly light. Walking barefoot, toilet type (absent/bush), and irregular washing of fruits and/or vegetables before consumption were significantly associated with STH.
Conclusion
Our data indicate that intestinal schistosomiasis is not prevalent in Apojola and that the community is a moderate-risk area for STH. Hence, the current annual preventive chemotherapy for STH (PC STH) with albendazole or mebendazole in school-aged children (SAC) through the school-based delivery programme should be extended to non-enrolled SAC and pre-SAC using other delivery platforms. This should be complemented with regular and effective health education campaigns as well as water, sanitation, and hygiene (WASH)-related interventions.
Supplementary Information
The online version contains supplementary material available at 10.1186/s12879-024-10175-9.
Keywords: Soil-transmitted helminthiases, Intestinal schistosomiasis, Community-based, Prevalence, Apojola, Nigeria
Introduction
Soil-transmitted helminthiases (STH) and schistosomiasis are the two most prevalent parasitic neglected tropical diseases (NTDs) globally. They overly affect the tropics and subtropics, particularly, resource-poor, vulnerable, and underprivileged rural communities with limited access to safe water sources, sanitation, hygiene, and adequate health facilities [1, 2]. The major STH are ascariasis (caused by Ascaris lumbricoides) and trichuriasis (by Trichuris trichiura), both transmitted through ingestion of food or water contaminated with the infective eggs, and hookworm infection (due to Ancylostoma duodenale and Necator americanus), acquired mostly via percutaneous entry by infective larvae. Schistosomiasis is caused by trematode species of the genus Schistosoma; the intestinal form is due to Schistosoma mansoni, Schistosoma japonicum, Schistosoma mekongi, Schistosoma intercalatum, and Schistosoma guineensis, while Schistosoma haematobium is responsible for urogenital disease. Humans get infected through percutaneous entry by schistosome cercariae (larvae released by the snail intermediate hosts) during contact with contaminated freshwater.
Globally, STH and schistosomiasis constitute considerable socio-economic and public health challenges and disease burdens, accounting for about 1.38 million and 1.75 million disability-adjusted life years (DALYs), respectively [3]. Recently, over a billion people, 897.9 million of whom were children, were estimated to require preventive chemotherapy (PC) for STH in 87 endemic countries, while some 264.3 million people (134.9 million school-aged children [SAC] and 129.4 million adults) in 50 endemic countries required the same for schistosomiasis [4–6]. Although both diseases do not usually result in significant mortality rates, they often lead to severe and subtle morbidity proportionate to worm burden [7, 8].
Individually and collectively, moderate-to-heavy intensity STH and schistosomiasis can cause considerable morbidity, including anaemia and micronutrient deficiencies [4]. For the STH, others are intestinal obstruction, impaired physical and cognitive development leading to poor educational performances and absenteeism, especially in SAC, lower work output, and adverse pregnancy outcomes in adults [7, 9, 10]. Intestinal schistosomiasis is characterised by abdominal pain, diarrhoea, and blood in stools, while hepatosplenomegaly, periportal fibrosis (PPF), portal hypertension, oesophageal varices, haematemesis, and ascites are common in chronic or advanced cases [2, 8, 11].
There has been a concerted effort to scale up STH and schistosomiasis control. The WHO’s new road map to guide action against NTDs [2] targets each of the two diseases for elimination as a public health problem (EPHP) in all endemic countries by 2030. To this end, the WHO recommends an integrated approach to their control and elimination: preventive chemotherapy (the periodic administration of anthelmintic medicines; albendazole or mebendazole for STH and praziquantel for schistosomiasis, to the entire population or at-risk population groups), improvement of water, sanitation, and hygiene (WASH) and behaviour change, and snail control and environmental management (for schistosomiasis) [4, 8].
Both STH and schistosomiasis are not only endemic in Nigeria but continue to be major public health problems [12–14]. The country ranks highest both in the number of people requiring PC and in disease burdens for STH and schistosomiasis in sub-Saharan Africa and globally, respectively [3, 5, 6].
In Nigeria, prevention and control of both diseases is mainly by annual or biannual PC, commonly in SAC. This is achieved through the school-based deworming programmes of the federal and state governments, in collaboration with the WHO, pharmaceutical companies, and non-governmental development organisations (NGDOs) [12, 15]. However, because the out-of-school children and adult populations are seldom covered in such programmes, infections persist in those that are infected and who may continue to contaminate the environment leading to reinfection soon after PC in treated individuals. Since the need for and frequency of PC are guided by local prevalence of infection as determined through parasitological surveys [16], it is imperative to periodically conduct such surveys in order to assess the efficacy of PC and/or guide the review of implementation strategies. Moreover, identification of the risk factors associated with infection in any setting is pivotal to the success of control intervention.
Previous epidemiological studies on STH and/or intestinal schistosomiasis in Nigeria, particularly Ogun State, were most commonly school-based or conducted among select population groups, especially SAC and pre-SAC [15, 17–19]. Data from community-based studies are scanty. STH and schistosomiasis are both moderately-to-highly endemic in Ogun State [13, 14]. A study by Oluwole et al. [15] on the spatial co-distribution of both diseases in the state showed that while STH was prevalent in all the 20 Local Government Areas (LGAs), schistosomiasis was prevalent in 10; S. mansoni, the main cause of intestinal schistosomiasis in Nigeria [13], was less widely distributed (in 3 LGAs) than S. haematobium (in 10 LGAs).
Urogenital schistosomiasis is highly endemic in Apojola [20–22], a neglected rural community in Odeda LGA of Ogun state, southwest Nigeria. However, there is a lack of information on the status of STH and intestinal schistosomiasis in the community. The present study aimed to determine the community-based prevalence and intensity of STH and intestinal schistosomiasis among the human population in Apojola, as well as identify the risk factors associated with these infections. These will serve to guide appropriate targeted and cost-effective disease control in the community.
Materials and methods
Study design and area
The study design was cross-sectional. The community-based study was carried out in Apojola, Odeda Local Government Area (LGA) of Ogun state, southwest Nigeria (Fig. 1). Odeda is one of the 20 LGAs in Ogun State and is headquartered in Odeda, a town located about 10 km on the outskirts of Abeokuta, the state capital. Apojola is a small rural community in Obete, one of the ten wards in Odeda LGA. The community is located on the shore of the Oyan River dam (7°15′30″ N, 3°15′20″ Ε) [21]: a large multipurpose reservoir situated about 20 km north-west of Abeokuta. Since the establishment of the dam in the early 1990s, urogenital schistosomiasis has consistently been endemic in the community [20–22].
Fig. 1.
Map of Odeda Local Government Area (LGA) showing the study community
Odeda LGA is ecologically homogeneous. The vegetation is both tropical rainforest and guinea savanna [23]. The climate is humid tropical, characterised by two distinct weather seasons: the wet season marked by bimodal rainfall starts in March, peaks in July and September, with a dry snap in August, while the dry season, usually accompanied by the harmattan cold, runs from November to March [24]. Annual precipitation ranges from 1400 to 1500 mm, while the mean annual air temperature is about 30 ℃. Humidity is lowest (37–54%) at the peak of the dry season in February and highest (78–85%) at the peak of the wet season between June and September [24].
Apojola lacks infrastructure like electricity, health care facilities, adequate road transport, and waste disposal systems. The only public borehole facility in the community is non-functional; hence, the community is highly dependent on water from the Oyan River for economic, domestic, recreational, laundry, and other purposes. The community is multi-ethnic and comprises mainly the Hausa, Fulani, and Idoma, with a few individuals of the Yoruba (that predominate in the state) and Igbo tribes. The predominant occupations in the community are farming and fishing, primarily for subsistence but sometimes commercial. The annual school-based PC STH (with mebendazole or albendazole) and PC schistosomiasis (with praziquantel) programmes are delivered to SAC through the only public primary school in the community. However, many of the SAC are out-of-school.
Study population and size
The study was carried out between October 2020 and January 2021. All households and/or residents of the community were considered potentially eligible and invited to participate in the study. Participant recruitment was carried out between October and November 2020.
Inclusion criteria
(i) Being at least 3 years of age and (ii) having resided in the community for at least 3 months prior to the sampling.
Exclusion criteria
(i) a refusal to provide written informed consent; and (ii) the use of antischistosomal therapy with praziquantel and/or anthelmintic treatment with albendazole or mebendazole less than 3 months prior to the sampling.
Sample size was determined using the formula n = z2pq/e2, where n = minimum sample size; z = 1.96 (i.e., critical value of the normal distribution at 95% level of confidence); p = prevalence; q = 1—p; and e = effect size (i.e., design effect; a correction factor for adjustment of required sample size when cluster sampling is used).
A 44.1% prevalence of urogenital schistosomiasis in the study area [22] was used [i.e., 0.441], while a design effect of 6% (i.e., 0.06) was considered. The minimum sample size was calculated to be 263. However, to compensate for non-responsiveness by eligible individuals, we added 10% (i.e., 26.3) to the minimum sample size to give a final sample size of 289.
Study locations were selected in the community using purposive sampling, a non-probability method. Due to the unavailability of a sampling frame, we considered the use of a two-stage method as the most appropriate and exigent technique for the recruitment of participants. This involved the use of a cluster sampling method for the delineation of the study locations, followed by the use of a simple random sampling (SRS) method.
Participant interviews/questionnaires
A structured questionnaire was administered to all participants to gather information on socio-demographic, individual, and household WASH characteristics, among other variables. The questionnaire for the study was part of one that was developed for a larger study on schistosomiasis, soil-transmitted helminthiases, and malaria in the study area (Supplementary File 1). This questionnaire contains no previously published parts. The questionnaire was administered in English. For participants who did not understand English, informed interpreters verbally translated the questionnaire into pidgin English and/or local languages.
Sample collection
Stool samples were collected weekly (for six weeks) in the morning (8.00—9.00 h.) between November and December, 2020. Each participant received a clean polythene sheet and a sterile leakproof universal bottle with a code number the day before sampling. Participants were instructed to defecate directly on the polythene sheet (to avoid contamination) the next morning, and immediately thereafter, transfer a sample of the stool into the bottle using the plastic scoop supplied with the bottle. Stool samples were submitted to the research team at two sites within the community: the public primary school and the market square (both centrally located).
The stool samples were transported to the laboratory in a cooler box with ice packs on the same day for processing (within 4 h after collection) and parasitological analysis.
Processing and microscopy of stool samples
Each stool sample was homogenised by stirring and then processed for parasitological examination using the standard Kato-Katz (K-K) thick smear technique [25]. Briefly, a stool sample was passed through a nylon screen of the K-K kit. The sieved stool was then used to fill the hole of a 41.7 mg K-K template (Vestergaard Frandsen Group, Denmark) on a glass slide. The template was removed, and the cylinder of stool that was left behind was covered with a pre-soaked (≥ 24 h in aqueous glycerol-3% aqueous malachite green solution) cellophane strip. The smears were prepared in triplicate to ensure the reliability of the diagnosis. Smears were examined microscopically and read twice: first, within 30 min of preparation to prevent overclarification of hookworm eggs, and again after 2 h for the eggs of other soil-transmitted helminths (STHs) and Schistosoma species [25].
The eggs were identified using standard morphological keys [25], counted using a hand tally counter, and the numbers recorded according to the helminth species. The intensity of infection, expressed as eggs per gram (epg) of faeces of each helminth, was calculated by multiplying the average egg count of the triplicate smears by a factor of 24. The intensity of infection was classified as light, moderate, or heavy according to the WHO criteria [1].
Each slide was read by two independent investigators (KFS, KTU). A third investigator (AAA) re-read 10% of the slides (positive and negative; selected randomly) to ensure quality control (QC). If there was a discrepancy between normal and QC readings, the entire series of discordant slides was re-examined/re-read.
Statistical analysis
Data were entered into a Microsoft Excel spreadsheet, checked for errors, and then imported into Stata 12.0 statistical software (StataCorp, TX, USA) for analysis. The overall prevalences of any STH, A. lumbricoides and hookworms in the population were calculated and stratified by age and gender among other variables. The independent t-test was used to compare mean egg counts of A. lumbricoides and hookworms between genders while the analysis of variance (ANOVA/F-test) was used to compare mean egg counts among the different age groups. In order to identify the independent contribution of each risk factor (variable) to infection, those with significant association (i.e., p < 0.05) in bivariate analysis were included in a multivariable logistic regression analysis. The dependent variable was a presence-or-absence outcome of infection. The odds ratios (ORs) were used to assess the risks of infection.
In all cases, statistical significance was set at p < 0.05.
Ethical considerations
Ethical approvals were granted by the Health Research Ethics Committees of the College of Medicine, University of Lagos (Ref: CMUL/HREC/01/20/713), and the Ogun State Ministry of Health, Abeokuta (Ref: HPRS/381/337).
Advocacy visits were made to the study area, during which meetings were held with the community leaders, family heads, the head teacher and staff of the only public primary school to secure their support and cooperation for the study. They were also informed about the objectives, procedures, benefits, and potential risks (if any) of the study.
Written informed consent was obtained from each subject (parent or legal guardian in the case of a minor) before participation in the study. They were also informed of their rights to refuse participation in the study and to withdraw at any time during the study without their rights of access to any intervention being affected. Participant confidentiality was ensured through a coding process.
At the end of the study, only consenting individuals received a free single dose 500 mg mebendazole (Vermox®) tablets. Infected individuals were notified of their status and referred to the primary health care centre in Obete for adequate medical treatment.
Study reporting
We used the STROBE (Strengthening the reporting of observational studies in epidemiology) guidelines [26] (Supplementary File 2) in guiding the reporting of the present study.
Results
Study population
A total of 317 individuals were confirmed eligible for participation in the study. However, the study included 289 individuals, 6 of whom either refused to provide stool samples or returned empty bottles. We analyzed data from only 283 participants who completed the questionnaire and provided appropriate stool samples. The participants ranged in age from 3 to 65 years (mean age ± S.D. of 19.6 ± 14.8 years). Table 1 shows the socio-demographic characteristics of the study population. There were 142 (50.2%) males and 141 (49.8%) females. A little over a quarter (27.6%) of the participants were aged 10–14 years, while those aged ≤ 4 years constituted the lowest percentage (6.0%). About a third of the participants were either married (33.9%), engaged in farming (31.1%), or unemployed (30.0%). About half (47.7%) of the participants had primary education, while none had tertiary education or access to water closet facilities. The majority of the respondents lived in houses made of clay or mud (82.3%), with thatched roofing (83.0%), or without toilet facilities (i.e., defecating in the bush [63.2%]). The majority of the participants belonged to households with a size of 4–6 (58.7%) and had an average monthly family income of less than ₦18,000 (66.1%).
Table 1.
Socio-demographic characteristics of the study population in Apojola
| Variables | Categories | Number (%) |
|---|---|---|
| Gender | Male | 142 (50.2) |
| Female | 141 (49.8) | |
| Age (years) | ≤ 4 | 17 (6.0) |
| 5–9 | 59 (20.8) | |
| 10–14 | 78 (27.6) | |
| 15–19 | 30 (10.6) | |
| 20–29 | 27 (9.5) | |
| 30–39 | 35 (12.4) | |
| 40–49 | 19 (6.7) | |
| ≥ 50 | 18 (6.4) | |
| Marital status | Married | 96 (33.9) |
| Single/divorced/ Widowed | 187 (66.1) | |
| Household size | 1–3 | 19 (6.7) |
| 4–6 | 166 (58.7) | |
| > 6 | 98 (34.6) | |
| Level of education | None | 64 (22.6) |
| Non-formal | 50 (17.7) | |
| Primary | 135 (47.7) | |
| Secondary | 34 (12.0) | |
| Tertiary | 0 (0.0) | |
| Occupationa | Unemployed | 85 (30.0) |
| Fishing | 63 (22.3) | |
| Farming | 88 (31.1) | |
| Trading | 36 (12.7) | |
| Artisanship | 5 (1.8) | |
| Schooling | 84 (29.7) | |
| Herding | 7 (2.5) | |
| Housing type | Cement | 37 (13.1) |
| Clay/Mud | 233 (82.3) | |
| Plank | 13 (4.6) | |
| Roofing type | Aluminium | 48 (17.0) |
| Thatched | 235 (83.0) | |
| Floor type | Cement | 121 (42.8) |
| Earth/soil | 162 (57.2) | |
| Toilet type | Pit Latrine | 104 (36.7) |
| Absent/Bush | 179 (63.3) | |
| Water closet | 0 (0.0) | |
| Average monthly | < 18,000 | 96 (33.9) |
| Family income (₦) | ≥ 18,000 | 187 (66.1) |
Total number of respondents = 283
aMultiple responses recorded
Prevalence of STH and intestinal schistosomiasis
All the stool samples did not contain any eggs belonging to an intestinal schistosome species. Table 2 shows the prevalence of STH based on socio-demographic factors among the study participants in Apojola. One hundred and eight (108) participants (overall prevalence of 38.2%) had at least one soil-transmitted helminth (STH) egg in their stool samples. A. lumbricoides (24.0%) and hookworms (25.8%) were the only soil-transmitted helminths (STHs) identified. There was no statistically significant difference in the prevalence of infection between genders: any STH (males, 40.1% vs. females, 36.2%, χ2 = 0.473, p = 0.492), A. lumbricoides (males, 23.2% vs. females, 22.7%, χ2 = 0.012, p = 0.913), or hookworms (males, 28.2% vs. females, 23.4%, χ2 = 0.839, p = 0.360). However, the differences in prevalence between the age groups were statistically significant: any STH (χ2 = 22.225, p = 0.002), A. lumbricoides (χ2 = 16.354, p = 0.022), and hookworms (χ2 = 20.001, p = 0.006) (Table 2). Children aged 5–9 and 10–14 years recorded the highest prevalences of A. lumbricoides (40.7%) and hookworms (38.5%), respectively (Table 2).
Table 2.
Prevalence of STH by socio-demographic factors among study population in Apojola
| Variables (N) | A. lumbricoides | Hookworms | Any STHa,b | ||||||
|---|---|---|---|---|---|---|---|---|---|
| n (%) | χ2 | p-value | n (%) | χ2 | p-value | n (%) | χ2 | p-value | |
| Overall (283) | 65 (24.0) | - | - | 73 (25.8) | - | - | 108 (38.2) | - | - |
| Gender | 0.012 | 0.913 | 0.839 | 0.360 | 0.473 | 0.492 | |||
| Male (142) | 33 (23.2) | 40 (28.2) | 57 (40.1) | ||||||
| Female (141) | 32 (22.7) | 33 (23.4) | 51 (36.2) | ||||||
| Age (years) | 16.354 | 0.022* | 20.001 | 0.006* | 22.225 | 0.002* | |||
| ≤ 4 (17) | 3 (17.7) | 5 (29.4) | 8 (47.1) | ||||||
| 5–9 (59) | 24 (40.7) | 19 (32.2) | 32 (54.2) | ||||||
| 10–14 (78) | 18 (23.1) | 30 (38.5) | 35 (44.9) | ||||||
| 15–19 (30) | 7 (23.3) | 7 (23.3) | 12 (40.0) | ||||||
| 20–29 (27) | 3 (11.1) | 6 (22.2) | 8 (29.6) | ||||||
| 30–39 (35) | 5 (14.3) | 4 (11.4) | 7 (20.0) | ||||||
| 40–49 (19) | 3 (15.8) | 1 (5.3) | 4 (21.1) | ||||||
| ≥ 50 (18) | 2 (11.1) | 1 (5.6) | 2 (11.1) | ||||||
| Level of Education | 1.650 | 0.647 | 5.078 | 0.166 | 6.254 | 0.100 | |||
| None (64) | 16 (25.0) | 16 (25.0) | 27 (42.2) | ||||||
| Non-Formal (50) | 11 (22.0) | 12 (24.0) | 15 (30.0) | ||||||
| Primary (135) | 33 (24.4) | 41 (30.4) | 58 (43.0) | ||||||
| Secondary (34) | 5 (14.7) | 4 (11.8) | 8 (23.5) | ||||||
| Household size | 0.551 | 0.759 | 0.496 | 0.780 | 0.375 | 0.829 | |||
| 1–3 (19) | 4 (21.1) | 4 (21.1) | 6 (31.6) | ||||||
| 4–6 (166) | 36 (21.7) | 45 (27.1) | 64 (38.6) | ||||||
| > 6 (98) | 25 (25.5) | 24 (24.5) | 38 (38.8) | ||||||
| Marital status | 7.297 | 0.007* | 13.119 | < 0.001* | 16.332 | < 0.001* | |||
| Single (187) | 52 (27.8) | 61 (32.6) | 87 (46.5) | ||||||
| Married (96) | 13 (13.5) | 12 (12.5) | 21 (21.9) | ||||||
| Occupationc | 6.726 | 0.347 | 6.726 | 0.346 | 12.580 | 0.043* | |||
| Unemployed (85) | 19 (22.4) | 21 (24.7) | 34 (40.0) | ||||||
| Fishing (63) | 11 (17.5) | 9 (14.3) | 16 (25.4) | ||||||
| Farming (88) | 20 (22.7) | 18 (20.5) | 30 (34.1) | ||||||
| Trading (36) | 6 (16.7) | 5 (13.9) | 8 (22.2) | ||||||
| Artisanship (5) | 0 (0.0) | 3 (60.0) | 3 (60.0) | ||||||
| Schooling (84) | 26 (31.0) | 29 (34.5) | 42 (50.0) | ||||||
| Herding (7) | 0 (0.0) | 1 (14.3) | 1 (14.3) | ||||||
| Average monthly family income (₦) | 12.725 | < 0.001* | 8.479 | 0.004* | 11.930 | 0.001* | |||
| < 18,000 (96) | 34 (35.4) | 35 (36.5) | 50 (52.1) | ||||||
| ≥ 18,000 (187) | 31 (16.6) | 38 (20.4) | 58 (31.0) | ||||||
| Housing type | 1.670 | 0.434 | 2.353 | 0.308 | 3.842 | 0.146 | |||
| Cement (37) | 6 (16.2) | 10 (27.0) | 12 (32.4) | ||||||
| Clay/Mud (233) | 57 (24.5) | 62 (26.7) | 94 (40.3) | ||||||
| Plank (13) | 2 (15.4) | 1 (7.7) | 2 (15.4) | ||||||
| Floor type | 0.262 | 0.609 | 3.016 | 0.082 | 3.151 | 0.076 | |||
| Cement (121) | 26 (21.5) | 25 (20.7) | 39 (32.2) | ||||||
| Earth/sand (162) | 39 (24.1) | 48 (29.8) | 69 (42.6) | ||||||
| Roofing type | 1.297 | 0.255 | 0.324 | 0.569 | 0.571 | 0.450 | |||
| Aluminium (48) | 8 (16.7) | 14 (29.2) | 16 (33.3) | ||||||
| Thatched (235) | 57 (24.3) | 59 (25.1) | 92 (39.2) | ||||||
| Toilet type | 5.345 | 0.021* | 5.983 | 0.014* | 8.802 | 0.003* | |||
| Pit Latrine (104) | 16 (15.4) | 18 (17.5) | 28 (26.9) | ||||||
| Absent/Bush (179) | 49 (27.4) | 55 (30.7) | 80 (44.7) |
N Number of subjects examined
n (%) = number infected (prevalence)
aNo case of T. trichiura infection recorded
bMixed STH (A. lumbricoides and hookworms) infections recorded in subjects
cMultiple responses recorded
*Significant (p<0.05)
Participants’ level of education, household size, housing type, and floor type were not significantly associated with A. lumbricoides (p = 0.647, p = 0.759, p = 0.434, and p = 0.609, respectively), hookworms (p = 0.166, p = 0.780, p = 0.308, and p = 0.082, respectively), or any STH (p = 0.100, p = 0.829, p = 0.146, and p = 0.076, respectively).
However, participants’ age, marital status, occupation, average monthly family income, and toilet type were significantly associated with A. lumbricoides (p = 0.022, p = 0.007, p < 0.001, and p = 0.021, respectively), hookworms (p = 0.006, p < 0.001, p = 0.004, and p = 0.014, respectively), or any STH (p = 0.002, p = < 0.001, p = 0.001, and p = 0.003, respectively). Occupation was significantly associated (p = 0.043) only with any STH (Table 2).
The prevalence of A. lumbricoides and hookworm coinfection was 10.6%, most (80%) were recorded in children aged 5–9 and 10–14 years (i.e., SAC).
Table 3 shows the prevalence of STH in Apojola based on individual and household WASH factors, knowledge of STH, and deworming history.
Table 3.
Prevalence of STH in Apojola by individual and household WASH factors, knowledge of STH and deworming history
| Variables (N) | A. lumbricoides | Hookworms | Any STHa,b | ||||||
|---|---|---|---|---|---|---|---|---|---|
| n (%) | χ2 | p-value | n (%) | χ2 | p-value | n (%) | χ2 | p-value | |
| Overall (283) | 65 (24.0) | - | - | 73 (25.8) | - | - | 108 (38.2) | - | - |
| Walking barefoot | 8.126 | 0.017* | 31.352 | < 0.001* | 26.920 | < 0.001* | |||
| Always (35) | 7 (20.0) | 15 (42.9) | 17 (48.6) | ||||||
| Sometimes (183) | 51 (27.9) | 58 (31.9) | 84 (45.9) | ||||||
| No (65) | 7 (10.77) | 0 (0.0) | 7 (10.8) | ||||||
| Wash fruits and/or vegetables before eating | 14.647 | < 0.001* | 3.160 | 0.075 | 14.811 | < 0.001* | |||
| Always (146) | 20 (13.7) | 31 (21.4) | 40 (27.4) | ||||||
| Sometimes (137) | 45 (32.9) | 42 (30.7) | 68 (49.6) | ||||||
| Handwashing before eating | 11.914 | 0.001* | 4.328 | 0.037* | 10.473 | 0.001* | |||
| Always (229) | 43 (18.8) | 53 (23.3) | 77 (33.6) | ||||||
| Sometimes (54) | 22 (40.7) | 20 (37.0) | 31 (57.4) | ||||||
| Handwashing After toilet use | 0.239 | 0.625 | 0.068 | 0.794 | 0.867 | 0.352 | |||
| Always (228) | 51 (22.4) | 58 (25.5) | 84 (36.8) | ||||||
| Sometimes (55) | 14 (25.5) | 15 (27.3) | 24 (43.6) | ||||||
| Wipe used after defecation | 14.093 | 0.001* | 9.744 | 0.008* | 15.830 | < 0.001* | |||
| Water (238) | 45 (18.9) | 53 (22.4) | 79 (33.2) | ||||||
| Plant leaf (10) | 4 (40.0) | 4 (40.0) | 7 (70.0) | ||||||
| Water/Plant leaf (35) | 16 (45.7) | 16 (45.7) | 22 (62.9) | ||||||
| Fingernail biting/ Finger sucking | 18.399 | < 0.001* | 0.038 | 0.981 | 7.970 | 0.019* | |||
| Always (8) | 3 (37.5) | 2 (25.0) | 4 (50.0) | ||||||
| Sometimes (94) | 35 (37.2) | 25 (26.6) | 46 (48.9) | ||||||
| No (181) | 27 (14.9) | 46 (25.6) | 58 (32.0) | ||||||
| Eating food that has fallen on ground | 9.142 | 0.010* | 3.869 | 0.144 | 11.450 | 0.003* | |||
| Sometimes (56) | 21 (37.5) | 18 (32.1) | 32 (57.1) | ||||||
| No (227) | 44 (19.4) | 55 (24.3) | 76 (33.5) | ||||||
| Drinking untreated water | 3.500 | 0.174 | 0.745 | 0.689 | 0.969 | 0.616 | |||
| Always (1) | 0 (0.0) | 1 (100.0) | 1 (100.0) | ||||||
| Sometimes (45) | 15 (33.3) | 10 (22.2) | 19 (42.2) | ||||||
| No (237) | 50 (21.1) | 62 (26.2) | 88 (37.1) | ||||||
| Knowledge of STH | 6.891 | 0.009* | 1.468 | 0.226 | 7.459 | 0.006* | |||
| Yes (202) | 38 (18.8) | 48 (23.9) | 67 (33.2) | ||||||
| No (81) | 27 (33.3) | 25 (30.9) | 41 (50.6) | ||||||
| Deworming history | 3.981 | 0.137 | 0.892 | 0.640 | 5.272 | 0.072 | |||
| Yes (207) | 42 (20.3) | 51 (24.8) | 71 (34.3) | ||||||
| No (51) | 17 (33.3) | 14 (27.5) | 25 (49.0) | ||||||
| Don’t know (24) | 6 (25.0) | 8 (33.3) | 12 (50.0) | ||||||
N Number of subjects examined
n (%) = number infected (prevalence)
aNo case of T. trichiura infection recorded
bMixed STH (A. lumbricoides and hookworms) infections recorded in subjects
*Significant (p < 0.05)
Handwashing after toilet use, drinking untreated water, and deworming history were not significantly associated with A. lumbricoides (p = 0.625, p = 0.174, and p = 0.137, respectively), hookworms (p = 0.794, p = 0.689, and p = 0.640, respectively), or any STH (p = 0.352, p = 0.616, and p = 0.072, respectively). However, walking barefoot, handwashing before eating, and wipes used after defecation were significantly associated with A. lumbricoides (p = 0.017, 0.001, and 0.001, respectively), hookworms (p < 0.001, p = 0.037, and p = 0.008, respectively), or any STH (p = < 0.001, p = 0.001, and p < 0.001, respectively).
Washing fruits and/or vegetables before eating, fingernail biting/finger sucking, eating food that has fallen on ground, and knowledge of STH were significantly associated only with A. lumbricoides (p < 0.001, p < 0.001, p = 0.010, and p = 0.009, respectively) or any STH (p < 0.001, p = 0.019, p = 0.003, and p = 0.006, respectively).
Intensity of STH
Mean egg counts of A. lumbricoides and hookworms in infected individuals ranged from 8 to 50,784 epg and 8 to 5,128 epg, respectively. Table 4 shows the mean egg counts (MECs) of the two STHs, stratified by age and gender, among the study population. There was no statistically significant difference between the higher MEC of A. lumbricoides in females and the lower MEC in males (1769.8 vs. 1703.8, t[281] = -0.091, p = 0.927). Similarly, there was no statistically significant difference in the MECs of hookworms between males and females (285.2 vs. 190.2, t[281] = 1.061, p = 0.290). The differences in MECs between the age groups were also not statistically significant for A. lumbricoides (F[7,275] = 2.023, p = 0.052) and hookworms (F[7,275] = 1.114, p = 0.352). Children aged 5–9 and ≤ 4 years recorded the highest MECs of A. lumbricoides (3783.2 epg) and hookworms (499.8 epg), respectively.
Table 4.
Mean egg counts (MECs) of STHs among the study population in Apojola
| A. lumbricoidesa | test statistic | p-value | Hookworma | test statistic | p-value | |
|---|---|---|---|---|---|---|
| Gender | -0.091b | 0.927 | 1.061b | 0.290 | ||
| Male | 1703.8 ± 449.2 | 285.2 ± 72.1 | ||||
| Female | 1769.8 ± 568.6 | 190.2 ± 53.1 | ||||
| Age | 2.023c | 0.052 | 1.114c | 0.352 | ||
| ≤ 4 | 879.1 ± 479.0 | 499.8 ± 208.8 | ||||
| 5–9 | 3783.2 ± 1127.7 | 283.1 ± 118.8 | ||||
| 10–14 | 2458.4 ± 897.6 | 332.8 ± 95.7 | ||||
| 15–19 | 622.1 ± 471.6 | 156.5 ± 83.5 | ||||
| 20–29 | 729.5 ± 689.9 | 178.4 ± 106.8 | ||||
| 30–39 | 474.9 ± 309.3 | 186.9 ± 149.6 | ||||
| 40–49 | 180.6 ± 148.6 | 0.4 ± 0.4 | ||||
| ≥ 50 | 176.0 ± 175.5 | 5.3 ± 5.3 | ||||
| Total | 1736.71 ± 361.4 | 237.9 ± 44.8 |
aValues are means ± S.E
bt(281)
cF(7,275)
Table 5 shows the distribution of light, moderate, and heavy-intensity STH cases by gender and age among the infected participants. The majority of infections with A. lumbricoides (63.1%) and hookworms (86.3%) were of light intensity. All but one of the heavy intensity cases were recorded in SAC (5–9 and 10–14 years) (Table 4). Four (4) of the heavy intensity cases were due to hookworms. The two cases of STH (one hookworm and one co-infection of A. lumbricoides and hookworms) recorded in adults aged ≥ 50 years were both of light intensity.
Table 5.
The distribution of light, moderate and heavy intensity cases among infected participants in Apojola
| Number (%) of infected participants | ||||||
|---|---|---|---|---|---|---|
| A. lumbricoidesa | Hookwormb | |||||
| Light | Moderate | Heavy | Light | Moderate | Heavy | |
| Gender | ||||||
| Male | 20 (60.6) | 13 (39.4) | 0 (0.0) | 34 (85.0) | 3 (7.5) | 3 (7.5) |
| Female | 21 (65.6) | 10 (31.3) | 1 (3.1) | 29 (87.9) | 3 (9.1) | 1 (3.0) |
| Age | ||||||
| ≤ 4 | 2 (66.7) | 1 (33.3) | 0 (0.0) | 4 (80.0) | 1 (20.0) | 0 (0.0) |
| 5–9 | 13 (54.2) | 11 (45.8) | 0 (0.0) | 17 (89.5) | 0 (0.0) | 2(10.5) |
| 10–14 | 9 (50.0) | 8 (44.4) | 1 (5.6) | 25 (83.3) | 4 (13.3) | 1 (3.3) |
| 15–19 | 6 (85.7) | 1 (14.3) | 0 (0.0) | 7 (100.0) | 0 (0.0) | 0 (0.0) |
| 20–29 | 2 (66.7) | 1 (33.3) | 0 (0.0) | 5 (83.3) | 1 (16.7) | 0 (0.0) |
| 30–39 | 4 (80.0) | 1 (20.0) | 0 (0.0) | 3 (75.0) | 0 (0.0) | 1(25.0) |
| 40–49 | 3 (100.0) | 0 (0.0) | 0 (0.0) | 1 (100.0) | 0 (0.0) | 0 (0.0) |
| 2 (100.0) | 0 (0.0) | 0 (0.0) | 1 (100.0) | 0 (0.0) | 0 (0.0) | |
| Total (%) | 41 (63.1) | 23 (35.4) | 1 (1.5) | 63 (86.3) | 6 (8.2) | 4 (5.5) |
aLight = 1—4,999 epg; Moderate = 5,000—49,999 epg; Heavy = ≥ 50,000 epg
bLight = 1—1,999 epg; Moderate = 2,000—3,999 epg; Heavy = ≥ 4,000 epg
Risk factors associated with STH
Table 6 shows the result of a multivariable logistic regression analysis of risk factors associated with infection (i.e., with p-values ≤ 0.05 on bivariate analysis). Toilet type was the only risk factor/variable that was significantly associated with A. lumbricoides (p = 0.044), hookworms (p = 0.041), and any STH (p = 0.040). Trading was only significantly associated with A. lumbricoides (p = 0.043), while walking barefoot was only significantly associated with hookworms (p < 0.001). Washing fruits and/or vegetables before eating was significantly associated with A. lumbricoides (p = 0.012) but marginally with any STH (p = 0.047).
Table 6.
Multivariable logistic regression analysis of associations between socio-demographic, individual and household WASH factors and STH in Apojola
| Factors (N) | A. lumbricoides | Hookworms | Any STHa,b | ||||||
|---|---|---|---|---|---|---|---|---|---|
| n (%) | OR (95% CI) | p-value | n (%) | OR (95% CI) | p-value | n (%) | OR (95% CI) | p-value | |
| Age (years) | |||||||||
| ≤ 4* (17) | |||||||||
| 5–9 (59) | 24 (40.7) | 1.179 (0.372; 3.737) | 0.780 | 19 (32.2) | 1.172 (0.369; 3.725) | 0.788 | 32 (54.2) | 1.187 (0.373; 3.771) | 0.771 |
| 10–14 (78) | 18 (23.1) | 0.839 (0.267; 2.636) | 0.763 | 30 (38.5) | 0.835 (0.265; 2.631) | 0.758 | 35 (44.9) | 0.847 (0.269; 2.669) | 0.776 |
| 15–19 (30) | 7 (23.3) | 0.666 (0.192; 2.309) | 0.522 | 7 (23.3) | 0.645 (0.179; 2.312) | 0.500 | 12 (40.0) | 0.707 (0.197; 2.536) | 0.595 |
| 20–29 (27) | 3 (11.1) | 0.426 (0.081; 2.306) | 0.312 | 6 (22.2) | 0.420 (0.073; 2.435) | 0.334 | 8 (29.6) | 0.464 (0.079; 2.728) | 0.395 |
| 30–39 (35) | 5 (14.3) | 0.259 (0.040; 1.678) | 0.157 | 4 (11.4) | 0.274 (0.039; 1.917) | 0.192 | 7 (20.0) | 0.299 (0.041; 2.191) | 0.235 |
| 40–49 (19) | 3 (15.8) | 0.235 (0.033; 1.684) | 0.150 | 1 (5.3) | 0.247 (0.032; 1.906) | 0.180 | 4 (21.1) | 0.257 (0.032; 2.049) | 0.200 |
| ≥ 50 (18) | 2 (11.1) | 0.113 (0.012; 1.044) | 0.055 | 1 (5.6) | 0.116 (0.012; 1.114) | 0.062 | 2 (11.1) | 0.117 (0.012; 1.139) | 0.065 |
| Marital status | |||||||||
| Single (187) | 52 (27.8) | 0.806 (0.206; 3.159) | 0.758 | 61 (32.6) | 0.935 (0.207; 4.214) | 0.930 | 87 (46.5) | 0.785 (0.197; 3.125) | 0.731 |
| Married* (96) | 13 (13.5) | 12 (12.5) | 21 (21.9) | ||||||
| Occupationc | |||||||||
| Unemployed* (85) | 19 (22.4) | 21 (24.7) | 34 (40.0) | ||||||
| Fishing (63) | 11 (17.5) | 0.565 (0.917, 1.738) | 0.197 | 9 (14.3) | 0.577 (0.209, 1.594) | 0.289 | 16 (25.4) | 0.450 (0.180, 1.125) | 0.088 |
| Farming (88) | 20 (22.7) | 0.983 (0.467, 2.073) | 0.965 | 18 (20.5) | 0.645 (0.308, 1.351) | 0.245 | 30 (34.1) | 0.744 (0.389, 1.427) | 0.374 |
| Trading (36) | 6 (16.7) | 0.364 (0.043, 3.072) | 0.043** | 5 (13.9) | 0.278 (0.035, 2.324) | 0.237 | 8 (22.2) | 0.156 (0.019, 1.295) | 0.085 |
| Artisanship (5) | 0 (0.0) | NS | 3 (60.0) | 1.250 (0.108, 14.498) | 0.858 | 3 (60.0) | 0.703 (0.061, 0.090) | 0.777 | |
| Schooling (84) | 26 (31.0) | 1.422 (0.693, 2.922) | 0.693 | 29 (34.5) | 1.300 (0.655, 2.579) | 0.453 | 42 (50.0) | 1.406 (0.743, 2.663) | 0.295 |
| Herding (7) | 0 (0.0) | NS | 1 (14.3) | 0.500 (0.035, 4.527) | 0.537 | 1 (14.3) | 0.281 (0.031, 2.524) | 0.275 | |
| Average monthly family income (₦) | |||||||||
| < 18,000 (96) | 34 (35.4) | 1.571 (0.515; 4.794) | 0.427 | 35 (36.5) | 1.573 (0.515; 4.804) | 0.427 | 50 (52.1) | 1.594 (0.522; 4.868) | 0.413 |
| ≥ 18,000* (187) | 31 (16.6) | 38 (20.4) | 58 (31.0) | ||||||
| Toilet type | |||||||||
| Pit Latrine* (104) | 16 (15.4) | 18 (17.5) | 28 (26.9) | ||||||
| Absent/Bush (179) | 49 (27.4) | 1.778 (1.016; 3.112) | 0.044** | 55 (30.7) | 1.799 (1.025; 3.162) | 0.041** | 80 (44.7) | 1.806 (1.028; 3.174) | 0.040** |
| Walking barefoot | |||||||||
| Always (35) | 7 (20.0) | 0.813 (0.373; 1.769) | 0.601 | 15 (42.9) | 1.512 (0.603; 3.789) | 0.378 | 17 (48.6) | 1.512 (0.603; 3.789) | 0.378 |
| Sometimes* (183) | 51 (27.9) | 58 (31.9) | 84 (45.9) | ||||||
| No (65) | 7 (10.8) | 0.319 (0.093; 1.094) | 0.069 | 0 (0.0) | 0.139 (0.047; 0.411) | < 0.001** | 7 (10.8) | 0.319 (0.093; 1.094) | 0.069 |
| Wash fruits and/or vegetables before eating | |||||||||
| Always (146) | 20 (13.7) | 0.411 (0.206; 0.822) | 0.012** | 31 (21.4) | NS | 40 (27.4) | 0.553 (0.309; 0.993) | 0.047** | |
| Sometimes* (137) | 45 (32.9) | 42 (30.7) | 68 (49.6) | ||||||
| Handwashing before eating | |||||||||
| Always (229) | 43 (18.8) | 53 (23.3) | 77 (33.6) | ||||||
| Sometimes* (54) | 22 (40.7) | 1.735 (0.702; 4.287) | 0.233 | 20 (37.0) | 1.045 (0.537; 2.037) | 0.896 | 31 (57.4) | 1.311 (0.609; 2.816) | 0.488 |
| Wipe used after defecation | |||||||||
| Water (238) | 45 (18.9) | 0.597 (0.131; 2.731) | 0.506 | 53 (22.4) | 0.294 (0.073; 1.181) | 0.084 | 79 (33.2) | 0.269 (0.064; 1.145) | 0.076 |
| Paper* (10) | 4 (40.0) | 4 (40.0) | 7 (70.0) | ||||||
| Plant leaf (35) | 16 (45.7) | 1.782 (0.346; 9.186) | 0.490 | 16 (45.7) | 0.742 (0.162; 3.406) | 0.702 | 22 (62.9) | 0.655 (0.135; 3.174) | 0.599 |
| Fingernail biting/ Finger sucking | |||||||||
| Always (8) | 3 (37.5) | 1.192 (0.216; 6.572) | 0.840 | 2 (25.0) | NS | 4 (50.0) | 1.491 (0.320; 6.945) | 0.611 | |
| Sometimes* (94) | 35 (37.2) | 25 (26.6) | 46 (48.9) | ||||||
| No (181) | 27 (14.9) | 0.354 (0.062; 2.031) | 0.244 | 46 (25.6) | NS | 58 (32.0) | 0.999 (0.208; 4.804) | 0.999 | |
| Eating food that has fallen on ground | |||||||||
| Sometimes*(56) | 21 (37.5) | 18 (32.1) | 32 (57.1) | ||||||
| No (227) | 44 (19.4) | 0.461 (0.184; 1.159) | 0.100 | 55 (24.3) | NS | 76 (33.5) | 0.519 (0.221; 1.218) | 0.132 | |
| Knowledge of STH | |||||||||
| Yes* (202) | 38 (18.8) | 48 (23.9) | 67 (33.2) | ||||||
| No (81) | 27 (33.3) | 0.933 (0.398; 2.188) | 0.873 | 25 (30.9) | NS | 41 (50.6) | 1.662 (0.763; 3.619) | 0.201 | |
N: number of respondents
n: number infected
NS did not meet threshold (p < 0.05) on bivariate analysis to be included in multivariate analysis
*Reference category
**Significant p-value
aNo case of T. trichiura infection recorded
bMixed species STH (A. lumbricoides and hookworms) infections recorded in subjects
cMultiple responses recorded
Although age was not significantly associated with infection, the table shows that participants aged 15–19 years were about 30–33% less likely to have A. lumbricoides (OR = 0.666 [95% CI, 0.192; 2.309], p = 0.522) or any STH (OR = 0.707 [95% CI, 0.197; 2.536]; p = 0.595) compared to children aged ≤ 4 years. Adults aged 40–49 years were about four times less likely to have hookworms (OR = 0.247 [95% CI: 0.032, 1.906]; p = 0.180) compared to children aged ≤ 4 years.
Respondents who sometimes wash their hands before eating were about 70% more likely to have A. lumbricoides (OR = 1.735 [95% CI, 0.702; 4.287]; p = 0.233) compared to those who always wash their hands before eating.
Participants who use water for cleansing after defecation were about 30% less likely to have hookworms than those who use paper (OR = 0.294 [95% CI: 0.073; 1.181], p = 0.084]). Participants who always engage in fingernail biting/finger sucking were about 50% more likely to have any STH (OR = 1.491 [95% CI: 0.320, 6.945]; p = 0.611) compared to those who sometimes engage in such acts. Subjects who do not eat food that has fallen on the ground were about two times less likely to have A. lumbricoides (OR = 0.461 [95% CI, 0.184; 1.159]; p = 0.100) or any STH (OR = 0.519 [95% CI: 0.221, 1.218]; p = 0.132) compared to those who sometimes engage in the act.
Discussion
The present community-based study, which found no single case of intestinal schistosome infection, indicates that intestinal schistosomiasis is not prevalent in Apojola. However, the overall prevalence of STH was 38.2%, and the only identified STHs were A. lumbricoides and hookworms, with respective overall prevalences of 24.0% and 25.8%. Prevalence and intensity of infection were not significantly associated with gender. However, while prevalence varied significantly with age, intensity of infection was not associated with age. Children aged 5–9 and 10–14 years (i.e., SAC) accounted for 80% of the only five heavy intensity cases, while most infections were light in intensity. Toilet type (absent/bush), walking barefoot, and inadequate washing of fruits and/or vegetables before eating were significantly associated with any STH, A. lumbricoides, or hookworm infections in the present study.
There are no published reports of S. mansoni infection in Apojola. However, the absence of the helminth in the community aligns with the findings in Odeda LGA, of a study that examined the spatial distribution of schistosomiasis in Ogun State [15]. We did not conduct snail sampling, but our findings may be partially because of the absence of the snail intermediate host, Biomphalaria pfeifferi, in the Oyan River, the primary water source for the community and the site of schistosomiasis transmission. Suffice it to say that concurrent STH and S. mansoni infections have been reported in other parts of the state and the country [15, 27].
The overall prevalence of STH (38.2%) in the present study is comparable to those reported in other studies: 38% in Odeda LGA, Ogun State, Nigeria [28], 38.8% in the rural areas of KwaZulu-Natal, South Africa [29], and 38% in rural Rwanda [30]. It is, however, lower than the prevalences reported in similar studies in Nigeria (> 50%) [31, 32], Kenya (44.05%) [33], and Cameroon (51.5%) [34]. Our prevalence is higher compared to those reported in other parts of the state and the country (6.5–34.64%) [15, 28, 35–40], Uganda (26.5%) [41], Cameroon (24.10%) [42], urban Rwanda (13%) [30], southern Ethiopia [43], and Angola [44]. The disparities in the prevalence of STH between our study and others could be due to variability in the environmental factors (temperature, humidity, precipitation, soil moisture) that influence transmission and risk of infection, the setting (urban vs. rural) and sampling design (community vs. school-based), the socio-economic, cultural, demographic, WASH characteristics, and size of the study population, as well as in the diagnostic methods employed [30, 41, 42, 45, 46].
There is little or no previous information on STH in Apojola. However, the non-existence of T. trichiura in our study is in agreement with the reported absence of the helminth in Odeda LGA [15, 38], and other parts of the country [27, 36, 47, 48]. However, other studies have documented the presence of this helminth in Odeda LGA, albeit at low prevalence rates of 1.6% [37] and 5.1% [28].
The prevalence of hookworms was marginally higher compared to that of A. lumbricoides in the present study. Although A. lumbricoides is often reported as the most prevalent STH in Nigeria [15, 18, 28, 32, 38, 40] and elsewhere [30, 33, 44, 46, 49], higher prevalences of hookworms have been reported within Odeda LGA [15, 37, 38] and in Uganda [41]. Our finding could be due to the rural and agrarian nature of the study area, which may be more favourable for hookworm transmission.
The 24.0% prevalence of A. lumbricoides in the present study is comparable to the 23.8% predicted for Odeda LGA [28] but lower than the 40.3% [32] and 43.5% [33] reported in southeast Nigeria and Kenya, respectively. It is however, higher than the 12.36% predicted for the state [28], the 5.7% and 5.56% reported elsewhere in the state [39] and in the country [40], respectively, as well as the prevalences reported in Cameroon [34, 42], and Uganda [41]. The 25.8% prevalence of hookworms in the present study is higher than the 14.5% and 6.16% predicted for Odeda LGA and Ogun state, respectively [28], as well as the figures reported in other parts of Nigeria [32, 40], in Uganda [41], northern Iran [50], Kenya [33], and Cameroon [42].
It appears logical to state that the variability in the occurrence and distribution of STHs between endemic settings is possibly due to the heterogeneity of environmental factors and transmission dynamics, which may contribute to the preponderance of some species in certain areas. This may help to explicate the disparities in the occurrence and prevalence of the STHs between the present study and others. For instance, T. trichiura, which was nonexistent in the present study community, was reported in some other localities within Odeda LGA of the state [37] and was also the most prevalent species elsewhere [34, 42, 51].
The highest prevalences of any STH (54.2%), A. lumbricoides (40.7%), and hookworms (38.5%) in the present study were recorded amongst children aged 5–9 years, 5–9 years, and 10–14 years, respectively (all SAC). This finding was not surprising, as SAC have been frequently reported to have higher prevalences of STHs than other age groups in the human population due to their involvement in activities that put them at higher risks of infection (e.g., playing with soil and other poor personal hygiene practices) and their underdeveloped immunity [45, 52, 53]. The prevalence of STH in SAC in the present study (48.9% from combined prevalences of 54.2% [5–9 years] and 44.9% [10–14 years]) falls within the moderate prevalence range (20–49.9%) reported by Oyeyemi and Okunlola [14] for SAC in Odeda LGA. Although the prevalence of infection in SAC is used as an indicator of the prevalence in the general population, in the present study, the prevalence in the former was much higher than in the latter (38.2%). Either way, the prevalence was ≥ 20% and < 50% and indicates, according to the WHO risk categorisation [54], that Apojola is a moderate-risk area for STH.
The moderate prevalence (47.1%) of STH in pre-SAC in the present study may have important implications for the effectiveness of PC STH interventions. The WHO guidelines for PC STH [16, 55] recommend treatment of pre-SAC in addition to SAC. Unfortunately, due to non-enrolment in schools and the lack of an efficient delivery platform, pre-SAC is traditionally seldom covered in such programmes which are targeted almost exclusively at SAC through the school-based delivery campaigns [12, 14, 15]. Our finding therefore underscores the potential epidemiological risk(s) of infections in pre-SAC if excluded from PC STH, as they could serve as reservoirs of infection. Our finding reinforces the advocacy for an overhaul of the implementation strategies to effectively integrate pre-SAC into PC STH interventions [14, 41, 56–58].
The prevalence of infection in the present study was not associated with gender. This is in contrast to the study by Odinaka et al. [36], who reported a statistically significant difference in prevalence of STH between genders. It is noteworthy that while some studies reported no gender-related prevalence of STH [15, 38, 40, 50], a few of these also found significantly higher prevalence(s) of one or more STHs in either gender [15, 38].
Several risk factors, including playing/walking barefoot, consumption of uncooked or unwashed fruits and vegetables, open drinking water source, open/indiscriminate defecation, ownership of domestic animals, not washing hands after defecation, soil eating (geophagy), and not deworming, have been shown to be significantly associated with STH in different endemic settings [30, 40, 41]. Reports indicate that these factors vary significantly across different settings [30]. In the present study, although bivariate analysis indicated many significant risk factors, logistic regression analysis showed that only toilet type (absent/bush), walking barefoot, and irregular washing of fruits and/or vegetables before eating were significantly (p < 0.05) associated with any STH, A. lumbricoides, or hookworms. The significant associations between consumption of inadequately washed fruits and/or vegetables and A. lumbricoides, and between walking barefoot and hookworms were not surprising, given the modes of transmission of these helminths. Infection with A. lumbricoides is transmitted only through consumption of food or water contaminated with the infective eggs; hence, the consumption of inadequately washed fruits and/or vegetables comes with a high risk of exposure to infection. For hookworms, acquired mainly through percutaneous larval entry, walking barefoot, especially on contaminated soil, increases the risk of infection [59].
A strength of the present study is its community-based design, which allowed for data generation across all strata of the population (including pre-SAC, SAC, and adults), thus ensuring representativeness and generalizability of our findings, which may typify the situation in other communities. However, the present study is not without limitations. Firstly, the examination of a single stool sample per participant. Given the daily variation in helminth egg output and the low sensitivity of the K-K technique, especially in light intensity infections [60–62], the examination of multiple stool samples collected over several consecutive days per participant would have been more desirable and reliable. However, this was impractical due to poor participants’ compliance, logistics challenges, and financial constraints. Although we tried to compensate for this limitation by stirring each sample before processing and also by preparing triplicate smears from each stool sample, there is a likelihood of an underestimation of the true prevalence of STH in our study population. Secondly, a number of the socio-demographic variables and WASH characteristics disclosed by the participants (parents/legal guardians in the cases of minors) were not directly observable by us. The possibility of bias in disclosure exists, especially for respondents who either forgot some questions or gave answers they thought would please the interviewers.
Conclusion
The study did not detect any cases of intestinal schistosomiasis. The overall prevalence of STH (38.2%) shows that Apojola is a moderate-risk area for STH. Gender did not significantly influence the prevalence and intensity of infection. The study found significant associations between STH and walking barefoot, toilet type (absent/bush), and irregular washing of fruits and/or vegetables before consumption. The moderate prevalence (47.1%) of STH in pre-SAC in the study may have important implications for the effectiveness of PC STH interventions in the community. The current annual PC STH with albendazole or mebendazole in SAC in the community should be sustained. Furthermore, we suggest reviewing and expanding the school-based delivery strategy for PC STH to include non-enrolled SAC and pre-SAC, in line with the WHO's recommendation. Finally, an integrated control strategy that combines regular and effective health education campaigns and WASH-related interventions to complement PC STH should be institutionalised in the community.
Supplementary Information
Acknowledgements
We are grateful to the community leaders, family heads, Head Teacher and teachers of the only primary school in the community, Mrs. Ajayi and Mrs. Williams, both of the primary health care office in Obete, for their support in mobilising community members for participation in the study. We thank all the inhabitants of Apojola and in particular, the participants, for their understanding and cooperation in the conduct of the study. We express our gratitude to the Primary Health Care Office, Obete, for donation of the mebendazole tablets.
Authors’ contributions
Conceptualization: A.A.A. Data curation: A.A.A, K.T.U. and K.F.S. Formal analysis: O.J.A. and N.I.B. Funding: A.A.A., K.T.U, K.F.S., R.B.A., V.A.N., F.E.E. and A.O.K. Investigation: A.A.A., K.T.U, K.F.S., R.B.A., V.A.N., F.E.E. and A.O.K. Methodology: A.A.A., K.T.U. and K.F.S. Project administration: A.A.A. and A.O.K. Resources: A.A.A., K.T.U. and K.F.S. Software: A.A.A. and O.J.A. Supervision: A.A.A. Validation: A.A.A., K.T.U. and K.F.S. Visualization: A.A.A. Writing—original draft: K.T.U. and K.F.S. All authors reviewed the manuscript and agreed with the submission.
Funding
The authors declare that no funding or financial support for the study, authorship, and/or publication of this article was received from funding agencies in the public, commercial, or not-for-profit sectors.
Data availability
Data is provided within the manuscript or supplementary information files.
Declarations
Ethics approval and consent to participate
Ethical approvals for the study were granted by the Health Research Ethics Committees of the College of Medicine, University of Lagos (Ref: CMUL/HREC/01/20/713) and the Ogun State Ministry of Health, Abeokuta (Ref: HPRS/381/337).
Following full disclosure of the objectives, procedures and benefits of the study, written informed consent was obtained from each subject (parent or legal guardian in the case of a minor) before participation in the study. They were also informed of their rights to refuse participation in the study and to withdraw at any time during the study without affecting their rights of access to any intervention. Participants’ confidentiality was ensured through a coding process.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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