Prevalence and Determinants of Geohelminthiasis among School-Age Children in Jimma City, Ethiopia

School-age children (SAC) are at a higher risk of geohelminth or soil-transmitted helminth (STH) infections due to their practice of walking and playing barefoot, lack of adequate sanitary facilities, and poor personal hygiene. In Ethiopia, periodic deworming has been implemented since 2013 with the aim of interrupting the transmission of STH in children by 2025. To evaluate the likely success of such a control program, it is crucial to monitor the transmission of STH, especially in peri-urban settings where environmental sanitation is modest. The aim of this study was to determine the prevalence and determinants of STH infections among SAC in peri-urban areas of Jimma City, Southwestern Ethiopia. A community-based cross-sectional study was conducted in five peri-urban Kebeles of Jimma City from July to September, 2021. Systematic random sampling was used to select 522 households with at least one child, and 478 children (5–15 years old) were recruited randomly from the households. Data on sociodemographic and potential risk factors were collected using a structured questionnaire. Stool samples from each study participant were collected and examined microscopically using the Kato–Katz technique. Multivariate logistic regression model was used to identify risk factors associated with STH infections. The prevalence of any STH among SAC was 23.4%, with Ascaris lumbricoides being the predominant STH species (15.7%), followed by Trichuris trichiura (9%) and hookworm (2.1%). Most (86.6%) of the STH-positive SAC had a single infection and a light infection intensity (88.2%), with a mean intensity of 367.4 eggs per gram. Location of Kebele (AOR = 2.73; 95% CI: 1.21–6.16, p=0.016), lack of hand washing after defecation (AOR = 6.39; 95% CI: 3.16–12.95, p < 0.001), untrimmed fingernails (AOR = 2.65; 95% CI: 1.56–4.51, p < 0.001), and lack of previous deworming (AOR = 2.90; 95% CI: 1.47–5.74, p=0.002) were significant predictors for STH infections among SAC. In conclusion, the study revealed that STH infections are significant health problem in the peri-urban areas of Jimma City. Strengthening periodic deworming and improving children's hygiene through health education are required to reduce the transmission.


Background
Soil-transmitted helminths (STHs) or geohelminths are the most widespread human parasitic infections in tropical and subtropical regions of the world where hygienic practices are poor and sanitary facilities are scarce [1][2][3].Globally, more than 4.5 billion people are at risk of STH infection, with about 25% of the world population estimated to have been infected with at least one STH species leading to over 1.94 million disability-adjusted life years lost due to STH-related morbidity every year [4,5].Sub-Saharan Africa (SSA), Latin America, India, China, and East Asia are the most afected regions, sharing the highest burden of STH infections [6].Ascaris lumbricoides, Trichuris trichiura, and hookworms (Necator americanus and Ancylostoma duodenale) are the main parasitic species causing geohelminthiasis in the world [5].
Soil-transmitted helminths are mainly transmitted by eggs that are passed in the feces of infected people.Te adult worms live in the intestine, where they produce thousands of eggs each day, which may contaminate the environment, vegetables, and other food items that lack adequate sanitation [7][8][9].Te infections are mostly abundant among communities, particularly children, living in areas where there is no access to basic infrastructural amenities such as potable water supply, hygiene, and sanitary facilities [10][11][12].Children are the most vulnerable group for STH infections due to their practice of walking and playing barefoot, frequent contact with contaminated soil, and poor personal hygiene [13].
High-intensity STH infections and polyparasitism may cause severe clinical manifestations in children, including abdominal pain, diarrhea, blood and protein loss, anemia, and rectal prolapse [5].Chronic and subclinical infections could lead to stunting, reduced body mass index, and impaired physical and cognitive development in children [14].Apart from the direct morbidity, STH infections could lead to low school enrollment, reduced school performance, and absenteeism [15], ultimately slowing educational advancement and economic development of endemic countries.
In SSA, helminth infections account for up to 85% of the neglected tropical diseases' burden, with up to one-third of the SSA population infected by one or more STH species [16].Children, especially SAC, are the most afected in the region, with over 41 million children estimated to have been parasitized with at least one STH species [17].In the past decades, there have been reports of a substantial reduction in the intensity of STH infections as a result of preventive chemotherapy and improved water, sanitation, and hygiene programs across Africa [17,18].Nevertheless, it remains a public health concern in many African countries and continues to cause major socioeconomic problems in the region [19].
Ethiopia is one of the SSA countries carrying the highest burden of STH infections, with an estimated 9 million preschool-aged children and 25 million SAC living in STH endemic areas [20,21].Since 2013, periodic mass drug administration (MDA) using single-dose albendazole (400 mg) or mebendazole (500 mg) has been widely implemented against STH in children in endemic areas of the country with the aim of eliminating STH-related morbidity by reducing moderate-and heavy-intensity infections to less than 1% by 2020 and interrupting the transmission by 2025 [20,21].Despite the national strategies implemented to lessen the burden of STH infections through preventive chemotherapy, the disease still remains a major public health concern in many parts of Ethiopia [22].To evaluate the likely success of this control program, it is crucial to monitor the transmission of STH and identify the contributing factors, especially in peri-urban settings where environmental sanitation is modest.Tis study was conducted to determine the prevalence and determinants of STH infections among SAC in peri-urban areas of Jimma City, Southwestern Ethiopia.

Study Design and Setting.
A community-based crosssectional study was carried out in fve peri-urban Kebeles (the smallest administration unit in Ethiopia) of Jimma City from July to September, 2021.Jimma City is located at 356 km southwest of Addis Ababa, the capital city of Ethiopia.Te city is characterized by a semiarid type of climate with an average annual rainfall of 800-2,500 mm and a temperature range of 20-30 °C [23].Te total population of Jimma City was estimated to be 205,384 in 2018 [24].Te city is administratively divided into 17 Kebeles (12 urban and 5 peri-urban Kebeles) [25].Te study area has been under biannual MDA since 2013.

Sample Size and Sampling
Procedure.Te sample size was determined using a single population proportion formula assuming STH prevalence of 21.7% obtained from the national mapping of STH and Schistosome infections in Ethiopia [22].By using 95% confdence interval, a marginal error of 5%, and a design efect of 2, the total sample size was calculated to be 522.All of the fve peri-urban Kebeles of Jimma City were included in the study.Systematic random sampling was used to select 522 households, and one schoolaged child (5-15 years old) was selected for participation in the study from each household.A lottery method was used to select SAC from the households that had more than one child.Te sample size was allocated proportionally to each study site based on the number of households in each Kebele.

Qualitative Data Collection and
Processing.Data on sociodemographic characteristics of the SAC, personal hygiene practices, and other potential risk factors for STH infections were collected using a pretested structured questionnaire.Te questionnaire was frst prepared in English and then translated into the local language of the study area (Afaan Oromoo).After obtaining written informed consent from the household head of the SAC, trained community health workers conversant in the local language conducted the house-to-house survey to collect the qualitative data.

Stool Sample Collection and Examination.
A single stool sample (about 5 g) was collected from each study participant using a clean and leak-proof screw cap container and labelled with a unique identifcation number.All collected stool samples were stored in a plastic bag and transported to the Medical Parasitology Laboratory of Jimma University within 2 hours.Te samples were then processed using Kato-Katz smear and examined microscopically to detect ova of the STH and quantify the intensity of infections based on fecal egg count (eggs per gram) according to the World Health Organization (WHO) guidelines [26].

Sociodemographic Characteristics of the Study
Participants.Out of 522 enrolled SAC, complete data (samples) were obtained from 478 (91.6%) children.Of the 478 SAC, 259 (54.2%) were males and 219 (45.8%) were females.Te mean age of the study participants was 8.89 ± 2.83 years.Te majority (88.1%) of the SAC were enrolled at school.Overall, 62% and 64.8% of the children's fathers and mothers had completed primary education, respectively.One-third of the fathers were engaged in agricultural activity, while 44.3% of mothers were housewives (Table 1).

Prevalence of STH among School-Age Children.
Overall, 140 (29.3%) and 112 (23.4%) of the SAC were positive for at least one species of intestinal helminths and STH, respectively.Ascaris lumbricoides was the most predominant STH species, detected in 15.7% of study participants, followed by T. trichiura (9.0%) and hookworm (2.1%).
In addition to the STH, fve cases of Schistosoma mansoni, thirty-one cases of Hymenolepis nana, six cases of Enterobius vermicularis, and one case of Taenia species were identifed in the stool specimens.Te majority (86.6%) of the SAC were infected by single species of STH, while double and triple infections were found in 12.5% and 0.9% of the SAC, respectively.Double infections were mainly due to A. lumbricoides and T. trichiura (Figure 1).Most of the SAC infected with A. lumbricoides (82.7%) and T. trichiura (95.3%) and all infected with hookworm had a light infection intensity, and no heavy infection intensity was detected in any cases.Te overall geometric mean fecal egg count for A. lumbricoides, T. trichiura, and hookworm was 688.8, 146.7, and 170.7 eggs per gram (EPG), respectively (Table 2)

Water Supply, Sanitation, and Hygiene-(WASH-) Related
Conditions of SAC's Households.Overall, 97.1% of the SAC's households had access to an improved source of water for drinking.Protected well/spring was the most commonly used source of water by the households both for drinking and domestic use.Most (93.7%) of the households had private toilet facilities, while 4.8% of them reported that they shared toilet facilities with neighbors and 1.5% practiced open defecation.Te majority (57.5%) of the households used improved toilet facilities (traditional pit latrines with slab, ventilated improved latrines, and fush latrines), but only 12.9% of them had hand washing facilities around the latrines.Most of the households practiced improper solid and liquid waste disposal systems (Table 3).

Factors Associated with STH Infections among SAC.
Multivariable logistic regression analysis showed that location of Kebele, hand washing after defecation, status of the fngernails, and history of deworming had a signifcant association with STH infections in SAC (Table 4).Children living in Kofe Kebele were 2.7 (AOR � 2.73, 95% CI: 1.21-6.16)times more likely to be infected with STH compared to those residing in Ifabula Kebele.Te prevalence of STH infections was 6.4 (AOR � 6.39, 95% CI: 3.16-12.95)times higher among children who often wash their hands after defecation as compared to those who always wash their hands after defecation.Te odds of having STH were 2.6 (AOR � 2.65, 95% CI: 1.56-4.51)times higher among children who had untrimmed fngernails as compared to children who had trimmed their fngernails.Children who were not reportedly dewormed during the last MDA in 2020 were 2.9 (AOR � 2.90, 95% CI: 1.47-5.74)times more at risk of being infected with STH as compared to those who were treated (Table 4).

Discussion
In Ethiopia, intensive STH control through periodic MDA among children has been widely implemented with the aim of interrupting the transmission of STH in endemic areas by 2025.In this study, the overall prevalence of at least one species of STH among SAC in peri-urban areas of Jimma City was 23.4%, indicating that the transmission is still ongoing in the community at a level of public health concern.Recent studies conducted in Sekela, Western Ethiopia, and Blue Nile Basin, Northwest Ethiopia, have also reported a similar magnitude of STH infection prevalence among SAC [27,28].
According to the WHO, STH endemic areas are classifed into three transmission categories in line with the application of MDA in SAC [26].Tese are high-risk areas where STH infection prevalence exceeds 50%, moderate-risk areas with parasite prevalence between 20% and 50%, and low-risk areas with STH prevalence below 20%.Based on this category, the current study areas would be classifed into the moderate risk level, suggesting that control measures should be intensifed to further reduce STH prevalence and transmission among the SAC.

Journal of Tropical Medicine
On the other hand, the overall prevalence of STH documented in this study is higher than that of studies conducted in Ambo town (12.6%),Goro (15.8%), and Babile town (0.47%) in Ethiopia [42][43][44], Zambia (14.4%) [45], and Kenya (17%) [46].Such variations could be attributed to diferences in personal hygiene, environmental sanitation, availability of adequate and safe water supply, and the socioeconomic status of the community [47].Diferences in diagnostic methods used for the detection of STH could also contribute to the variations in STH prevalence documented in diferent studies.Te Kato-Katz technique was used in the present study, while McMaster and formolether concentration techniques were used in studies conducted in Ambo, Goro, and Babile [42][43][44].In this study, the prevalence of STH varied even between the peri-urban Kebeles, indicating that STH prevalence could also vary between villages within a defned geographical area.Other studies have also documented a considerable and distinct   Journal of Tropical Medicine spatial heterogeneity of STH infection prevalence and intensity [23,48,49].In this study, A. lumbricoides was the most prevalent STH (15.7%) among the SAC, followed by T. trichiura (9%) and hookworm (2.1%).Te predominance of A. lumbricoides is consistent with the fndings of other studies conducted among SAC in diferent parts of Ethiopia [27,29,32,34,36,42,50] and abroad [37,39,45].Te higher prevalence of A. lumbricoides could be due to the fact that Ascaris eggs can withstand harsh environmental conditions more than the other species of STH and can easily sustain its transmission [51,52].In contrast to the present study, several other studies have reported the predominance of hookworm over the other STH species [33,35,43,53,54].Tis diference might be due to diferences in prevention measures used, climate variability, and other environmental factors.For instance, in settings where children often walk barefoot, hookworm is more prevalent as the infection occurs through skin penetration by larvae of the parasite [53].In the current study, most of the SAC (94%) reported that they often wear shoes, and this might have contributed to the lower hookworm infection prevalence in this study.It has been documented that climate variability may also favor the occurrence of hookworm species due to its unique ability to undergo developmental arrest as dauer larvae in human tissues as a means of surviving extreme weather conditions [55][56][57].Reports of the national STH prevalence survey also showed that A. lumbricoides is the predominant species in the highland and coldest regions of Ethiopia, such as Oromia and the southern region, while hookworm is more prevalent in the warmest regions, such as Benishangul-Gumuz and Gambella [22].

Journal of Tropical Medicine
Te reduction in moderate-to-heavy intensity infections is one of the indicators of the STH control program's success.STH is considered a public health problem by the WHO if at least 1% of SAC have moderate-to-heavy intensity infections [58].In this study, about 88.3% of the STH-positive SAC had light-intensity infections, while the remaining 11.7% had moderate infections, indicating that STHs are still a public health problem in the study area.Although the overall prevalence of STH infections among SAC in this study is signifcantly reduced compared to the previous studies conducted in the study area before the commencement of MDA [29,31], the prevalence of moderate-to-heavy STH infections in the current study is higher than the national report (2%) [22], suggesting that periodic deworming and other prevention measures should be strengthened in the area to further reduce the burden of STH.
In the present study, hand washing habit, status of the fngernail, deworming status, and location of the Kebeles were the key predictors of STH infections among SAC.Children who do not wash their hands after latrine use were six times more likely to be infected with STH compared to those who always wash their hands.Tis fnding is consistent with studies conducted in diferent settings in Ethiopia [27,28,34,59] and abroad [38,41].Moreover, children who had untrimmed fngernails were 2.6 times more likely to be infected with STH as compared to those who had trimmed their fngernails.Other studies have also reported a contribution of untrimmed fngernails to increased STH transmission among SAC [27,35,42].Tis highlights the need to strengthen health education and awareness creation for SAC to improve their personal hygiene in order to interrupt the transmission of STH.
Children who had not taken anthelminthic drugs within one year of the study were three times more likely to be infected with STH as compared to their counterparts.A similar study was reported from India, where children who never took antihelminthics were more afected by STH than their counterparts [60].
Te limitation of this study is that the prevalence and infection intensity of STH were determined by examination of a single stool specimen from each study participant.Tis may underestimate the actual STH infection prevalence among the SAC.

Conclusion
Te fndings of this study showed moderate level of STH infection prevalence among SAC living in the peri-urban areas of Jimma City.Te higher prevalence of moderateintensity STH infection (11.7%) above the target level (<1%) set by the national STH control program indicates that STHs are still a major health problem of the community of the peri-urban Kebeles.Lack of hand washing habit after latrine use, untrimmed fngernails, and lack of access to deworming were the key predictors of the STH infections among the SAC.Strengthening periodic deworming and provision of personal and environmental hygiene education and adequate sanitation facilities are required in order to eliminate STH as a public health problem and break transmission in children by 2025.
25th bivariate and multivariable logistic regression analyses were used to identify the candidate variables and determinants of STH infections, respectively.Bivariate logistic regression analysis was used to identify variables with p values ≤0.25.Multivariable logistic regression analysis was performed to identify the predictors of STH infections among SAC.Adjusted odds ratio (AOR) with 95% confdence intervals was computed, and a p value less than 0.05 was considered statistically signifcant during the analysis.

Table 1 :
Sociodemographic characteristics of school-age children in peri-urban Kebeles of Jimma City, Ethiopia, July to September 2021.

Table 2 :
Intensity of STH infections among SAC in the peri-urban Kebeles of Jimma City, Ethiopia, July to September 2021 (n � 748).

Table 3 :
Water supply, sanitation, and hygiene conditions of SAC's households and distribution of STH among the SAC in the peri-urban Kebeles of Jimma City, Ethiopia.
Improved toilet facilities include traditional pit latrines with slab, ventilated pit latrines, and fush latrines.Unimproved toilet facilities include pit latrines without slab.Protected water source includes tap water, tube hole/borehole, and protected well/spring.Unprotected water source includes unprotected hole/ spring and surface water.

Table 4 :
Factors associated with soil-transmitted helminth infection among the SAC of peri-urban Kebeles of Jimma City, Ethiopia.