Abstract
Background
Soil-transmitted helminth (STH) infection is a widespread problem globally, particularly in rural areas. In Ethiopia, the prevalence of STH infection is high. The prevalence of Ascaris lumbricoides and hookworm infections has not diminished in spite of the nation's strict STH prevention and control measures for decants. Additionally, variables linked to the high prevalence of A. lumbricoides and hookworm infections are not adequately addressed.
Objective
This study aimed to determine the prevalence and risk factors of STHs among students in the Fogera district, northwest Ethiopia.
Method
A cross-sectional study design was employed in two primary schools in the Fogera district in February–March 2023. The stool samples were collected from the students and examined using saline wet mount and double Kato–Katz technique. Data were entered and analyzed using SPSS Version 25. Descriptive statistics was used to compute the prevalence of STHs. Factors associated with hookworm and A. lumbricoides infections were analyzed by logistic regression. Variables with p < 0.05 in the multivariate logistic regression were considered significant.
Results
Among 463 schoolchildren, totally, the prevalence of STHs was 25.3%. The prevalence of A. lumbricoides and hookworm infections was 55 (11.9%) and 62 (13.4%), respectively. Mothers' lack of education (AOR = 24.99; 95% CI = 7.05–88.67; p < 0.001), fathers' lack of education (AOR = 3.03; 95% CI = 1.18–7.7; p = 0.021), school latrine nonusage at school (AOR = 4.53; 95% CI = 1.89–10.95; p < 0.001), untrimmed fingernails (AOR = 7.31; 95% CI = 2.57–20.81; p < 0.001), no handwashing after toilet use (AOR = 14.87; 95% CI = 3.97–55.75; p < 0.001), no handwashing before eating (AOR = 30.05; 95% CI = 11.05–81.74; p < 0.001), the absence of handwashing facility at home (AOR = 5.86; 95% CI = 2.19–15- 64; p < 0.001), and irregular wearing of shoes (AOR = 18.59; 95% CI = 6.89–50.13; p < 0.001) were significantly associated with STH infection.
Conclusion
The prevalence of A. lumbricoides was significant. Poor implementation of water, sanitation, and hygiene was a risk factor for A. lumbricoides and hookworm infection. Hence, health education on the transmission of STHs should be advocated to parents and schoolchildren.
Keywords: A. lumbricoides, fogera, hookworm, prevalence, schoolchildren
1. Introduction
Soil-transmitted helminths (STHs) refer to the intestinal worms infecting humans that are transmitted through contaminated soil (“helminth” means parasitic worm): Ascaris lumbricoides (sometimes called just “Ascaris“), whipworm (Trichuris trichiura), and hookworm (Ancylostoma duodenale and Necator americanus) [1]. STH infections are among the most common infections worldwide and affect the poorest and most deprived communities. They are transmitted by eggs present in human feces, which in turn contaminate soil in areas where sanitation is poor [2]. Intestinal worms produce a wide range of symptoms including intestinal manifestations (diarrhea and abdominal pain), general malaise, and weakness. Hookworms cause chronic intestinal blood loss that results in anemia. STHs are transmitted by eggs that are passed in the feces of infected people. Adult worms live in the intestine where they produce thousands of eggs each day [3].
STH infections are grouped by the World Health Organization (WHO) as neglected tropical diseases [2]. Over 1.5 billion people are infected with STH infections worldwide or 24% of the world's population. Infections are widely distributed in tropical and subtropical areas, with the greatest numbers occurring in sub-Saharan Africa, the United States, China, and East Asia [3]. From STH, A. lumbricoides and T. trichiura are the most common nematode parasites of humans in Ethiopia. However, in hookworm, N. americanus is more prevalent in Ethiopia than An. duodenale, species of hookworm [4].
The poorest and most marginalized groups are primarily affected by STH infections, which are among the most prevalent infections globally [3]. Over 1.5 billion individuals globally, or 24% of the global population, suffer from STH diseases [3]. Their infections are prevalent in warm, moist climates with poor sanitation and hygiene [1]. They are the most common worldwide, affecting impoverished communities [1, 5]. The transmission occurs through eggs present in human feces, contaminating soil in areas with inadequate sanitation. Intestinal worms cause various symptoms, including diarrhea, abdominal pain, general malaise, and weakness [3]. Tropical and subtropical regions are rife with infections; sub-Saharan Africa, the United States, China, and East Asia have the highest rates of infection. More than 568 million school-age children and over 267 million preschool-age children who reside in locations where these parasites are heavily spread due to unwashed hands after defecation, unwashed hands after playing with soil, being barefoot, unavailable latrines, not dewormed regularly, and limited awareness have a high prevalence of infections [3].
Ethiopia ranks 13th among more than 40 African countries in terms of the prevalence of each group of illnesses [6]. STH is still highly prevalent in many areas of Ethiopia particularly among schoolchildren [7]. Children from rural communities have a higher prevalence of STHs compared to those from urban communities. The prevalence of STH in Ethiopia is 33%, with A. lumbricoides being the most common among children [8]. Parasitic helminth infections rank as the second most common cause of outpatient morbidity in Ethiopia due to factors such as poor toilet coverage and low-quality drinking water [9]. The pooled prevalence estimates for A. lumbricoides and hookworm in Ethiopia are 17.63% and 12.35%, respectively [10].
The intensity of A. lumbricoides and hookworm varies by location in Ethiopia. For example, the study conducted in Tachgayint indicated a light intensity [11], and the study conducted in Jimma indicated that the intensity of these infections is moderate. The number of worms in an individual's body determines the intensity of A. lumbricoides and hookworm infections. This is usually determined by counting the number of eggs in a stool sample. A larger egg count implies a more severe illness [1].
The identification of risk factors associated with STHs may vary across different locations, making it essential for policymakers to have this information to develop targeted preventive strategies [12]. Factors such as warm climates, adequate moisture, poor personal and environmental hygiene, lack of sanitation and education, walking barefoot, and poor health or nutrition status can increase the risk of infection [13]. In Ethiopia, poor living standards, inadequate sanitation, and limited knowledge about basic health promotion contribute to the widespread distribution of intestinal helminths [14]. Helminthiasis ranks as the second most common cause of outpatient morbidity in the country, following malaria [15]. Extensive research conducted in Ethiopia indicates a significant prevalence of intestinal parasite infections. Children, who both spread and suffer from these diseases, are most affected by parasite infections such as A. lumbricoides and hookworm [16].
Despite control efforts, the infections remain prevalent and show no significant decline [17]. The Fogera district, as reported in its annual health report, experiences a higher prevalence compared to other districts in the South Gondar Zone administration, especially schoolchildren [18, 19]. The prevalence of infections among schoolchildren in the research region is currently unknown. Factors such as open defecation, limited toilet coverage, lack of access to clean drinking water and sanitation facilities, and unhygienic practices such as walking barefoot and consuming unwashed raw fruits and vegetables from the market have been observed. Therefore, this study aims to fill this knowledge gap by determining the prevalence and associated risk factors of soil-transmitted infections among primary school students in the Fogera district, northwest Ethiopia.
2. Materials and Methods
2.1. Description of the Study Area
The study was conducted in two primary schools at the Fogera district, Amhara regional state, northwest Ethiopia (Figure 1). The schools are situated 4 km away from Woreta town, the capital city of the district, 44 km from Debre Tabor (the capital of South Gondar Zone), 57 km from Bahir Dar (the capital of Amhara regional state), and 612 km from Addis Abeba (the capital city of Ethiopia). The schools have a total of 1025 pupils, with 801 in Nora Mender and 224 in Alemmia. The majority of the population are farmers engaged in settled mixed agriculture, focusing on crops such as rice, onions, and maize, using both irrigation practices and the summer season. Geographically, the area is located at latitude 180 42′ 34″N and longitude 310 16′ 84″E, with an altitude of 1847 m above sea level. The mean annual rainfall in the study area is approximately 1280 mm, and the mean annual minimum and maximum temperatures are 11.9°C and 28.84°C, respectively, with a mean temperature of 20.37°C (Woreta Administrative Office, 2020).
Figure 1.

Map of the study area.
2.2. Study Design
A cross-sectional study design was employed to determine the prevalence and associated risk factors of A. lumbricoides and hookworm infection among students in Fogera.
2.3. Study Population
Schoolchildren were selected as the study population because school-age children typically have the highest intensity of worm infection. Hence, the study population consisted of 463 (216 males and 247 females) schoolchildren (6–14 years) enrolled in February–March 2023 in Fogera.
2.4. Sampling Techniques and Sample Size Determination
The participants were selected by systematic random sampling techniques to ensure the inclusion of STH infections. So, the Kth interval was determined by dividing the total sample size of 463 by the total study population of 1025 (from 224, 115 were selected in Alemmia school, and out of 801, 348 were selected from Nora Mender school), resulting in a Kth interval value of ∼2. Next, the first study participants were chosen using a simple random sampling technique, and the second study participants were selected through a lottery system. Subsequently, every Kth (second) interval participant was selected until the total sample size of 463 was achieved.
The required sample was calculated using the following formula [17]:t
| (1) |
There is no study conducted in the study area about prevalence and associated risk factors of A. lumbricoides and hookworm infections among schoolchildren. Hence, based on the above formula, the sample size (n) would be 384 due to the p value of 50%, which is the lack of the study on the prevalence in the study area. To account for a 21% nonresponse rate, an additional 21% of the calculated sample size was added. Therefore, the total sample size was 384 + 384 ∗ 0.21 = 463. Thus, a total of 463 students (247 females and 216 males) were selected from the primary schools of the Fogera district.
The intensity of infections was determined by using the threshold level reported by WHO [20] (Table 1).
Table 1.
Threshold of intensity of infections.
| Threshold of intensity of infection (EPG) | |||
|---|---|---|---|
| STH species | Light | Moderate | Heavy |
| Ascaris lumbricoides | 1–4999 | 5000–49,999 | ≥ 50,000 |
| Trichuris trichiura | 1–999 | 1000–9999 | ≥ 10,000 |
| Hookworms | 1–1999 | 2000–3999 | ≥ 4000 |
2.5. Eligibility Criteria
2.5.1. Inclusion Criteria
This study included students who tested positive for STH infections from primary schools that were highly vulnerable to STH due to the presence of lowland and suitable soil types at the Fogera district. The age range of the students was between 6 and 14 years. Inclusion criteria required that the parents/guardians of the children agreed to their participation in the study, students tested positive for STHs, and students aged 6–14 without recent deworming.
2.5.2. Exclusion Criteria
Students who tested negative for parasitic infections, were in the age group above/below the required, were with diarrheic stool, with anti-helminthic drugs, or had previously consumed antihelminthic drugs, or whose parents/guardians did not agree to their participation in the study were excluded from the present study.
2.6. Data Collection Method
2.6.1. Questionnaire Survey
The questionnaire was initially written in English. After that, it was translated into Amharic, the working language, so that study participants could provide sociodemographic information and information about risk factors for STH infection. Throughout the data collection process, each study participant received comprehensive explanations regarding the purpose of the study, and sociodemographic data and risk factors of the study participants who are unable to read and write were collected by the data collector. Furthermore, to ensure the anonymity and confidentiality of the collected data, all 463 participants were assigned a unique identification number.
2.6.2. Stool Collection Process and Parasitological Examination
The authors went to the study site, which is the two primary schools of Fogera, for the collection of the stool sample for parasitological examination. The students were provided with instructions on how to collect stool samples. Labeled stool collection cups with applicator sticks were distributed to each child, and they were instructed to provide close to 2 g of fresh stool specimens. The students went to the toilet of the school to bring the stool sample for the lab examination. The collected stool samples from the students were transported to Woreta Health Centre in an icebox with an ice pack for laboratory processing to prevent the parasite from being damaged by environmental factors like temperature. To examine the stool samples for the presence or absence of STHs, direct wet mount microscopy and two slides of the Kato–Katz technique were utilized. The examination was performed by two medical laboratory technologists using a compound light microscope.
Data quality was meticulously maintained through a series of precise measures. To begin with, laboratory personnel underwent comprehensive training on various aspects, including stool sample collection, processing, diagnosis, and reporting. Similarly, data collectors were trained on using questionnaires, and these questionnaires were pretested before actual data collection.
Additionally, thorough checks were conducted to ensure the integrity of the collected data. The filled questionnaires were meticulously examined to ensure completeness, and the stool cups were appropriately labeled with unique serial numbers. Moreover, the samples were promptly transported to the nearby health institution without delay.
Stringent adherence to standard operating procedures was maintained throughout the entire process, emphasizing the accuracy of the test results. Regular supervision by the principal investigator ensured consistent quality control and oversight. To mitigate any potential observer bias, stool slides were examined independently by experienced laboratory personnel. Their observations were recorded on separate sheets for later comparison. In cases where discrepancies emerged, the principal investigator personally reviewed and verified the results. Overall, the quality assurance procedures were implemented across the pre-analytical, analytical, and postanalytical stages. This comprehensive approach ensured that the data collected and analyzed maintained a high standard of accuracy and reliability.
2.7. Variables of the Study
2.7.1. Independent Variables
The independent variables in this study encompassed a range of sociodemographic characteristics (age, sex, parental education, name of school), environmental characteristics (drinking water source), behavioral and personal characteristics (frequent sucking of fingernails, lack of handwashing before eating and after toilet use, and eating raw vegetables or fruits), and socioeconomic characteristics (not wearing shoes and washing facility at home).
2.7.2. Dependent Variables
The prevalence of STH infection was the dependent variable of this study.
2.8. Method of Data Analysis
The data were entered into Excel 2016 and analyzed using Statistical Package for the Social Sciences (SPSS) Version 25 software for the prevalence and risk factors. The prevalence of STHs was calculated as the percentage of children who tested positive for these species out of the total number of children with complete data. The association and strength of association between risk factors and infections were determined using logistic regressions.
3. Results
3.1. Sociodemographic Characteristics of the Respondents in the Study Area
The participants had the following sociodemographic characteristics: majority were females (53.3%), aged 6–9 (54.4%), with uneducated mothers (65.0%) and fathers (62.9%), and educated at Nora Mender school (75.2%) (Table 2).
Table 2.
Sociodemographic characteristics of study participants among students in the Fogera district, northwest Ethiopia, in 2023 (n = 463).
| Variables | Categories | Frequency | Percentage |
|---|---|---|---|
| Sex | Male | 216 | 46.7 |
| Female | 247 | 53.3 | |
| Total | 463 | 100.0 | |
|
| |||
| Age | 6–9 | 252 | 54.4 |
| 10–14 | 211 | 45.6 | |
| Total | 463 | 100.0 | |
|
| |||
| Name of school | Nora Mender | 348 | 75.2 |
| Alemmia | 115 | 24.8 | |
| Total | 463 | 100.0 | |
|
| |||
| Mothers' education | Educated | 162 | 35 |
| Uneducated | 301 | 65 | |
| Total | 463 | 100.0 | |
|
| |||
| Fathers' education | Educated | 172 | 37.1 |
| Uneducated | 291 | 62.9 | |
| Total | 463 | 100.0 | |
3.2. The Prevalence of STH Infections Among Participants Based on Sociodemographic Characteristics
The prevalence and distribution of participants based on age, sex, school names, mothers' education, and fathers' education showed that most students were infected in the age group of 10–14 (33.6%), males (28.2%), with uneducated mothers and with uneducated fathers (35.5%), and educated at Alemmia school (27.8%) for these infections. However, A. lumbricoides infection was higher in Alemmia school (15.7%), while hookworm infection was higher in Nora Mender school (13.8%). The overall prevalence of A. lumbricoides and hookworm was higher in Alemmia school (27.8%) than in Nora Mender school (24.4%) (Table 3). The combined prevalence of the two parasites was 25.3%.
Table 3.
The prevalence of STH infection among participants based on sociodemographic characteristics.
| Variables | Categories | N (%) | Parasitic species | |||
|---|---|---|---|---|---|---|
| A. lumbricoides | Hookworm | |||||
| Positive | Negative | Positive | Negative | |||
| Age | 6–9 | 252 (54.4) | 24 (9.6) | 228 (90.4) | 22 (8.7) | 230 (91.7) |
| 10–14 | 211 (45.6) | 31 (14.7) | 180 (85.3) | 40 (18.9) | 171 (81.1) | |
|
| ||||||
| Sex | Male | 216 (46.7) | 28 (13.0) | 188 (87.0) | 33 (15.3) | 183 (84.7) |
| Female | 247 (53.3) | 27 (10.9) | 220 (89.1) | 29 (11.7) | 218 (88.3) | |
|
| ||||||
| Name of school | Nora Mender | 348 (75.2) | 37 (10.6) | 311 (89.4) | 48 (13.8) | 300 (86.2) |
| Alemmia | 115 (24.8) | 18 (15.7) | 97 (84.3) | 14 (12.2) | 101 (87.8) | |
|
| ||||||
| Mothers' education | Educated | 162 (35) | 3 (1.9) | 157 (98.1) | 7 (4.4) | 153 (95.6) |
| Uneducated | 301 (65) | 52 (17.2) | 251 (82.8) | 55 (18.2) | 248 (81.8) | |
|
| ||||||
| Fathers' education | Educated | 172 (37.1) | 10 (5.8) | 162 (94.2) | 20 (11.6) | 152 (88.4) |
| Uneducated | 291 (62.9) | 45 (15.5) | 246 (84.5) | 42 (14.4) | 249 (85.6) | |
|
| ||||||
| Total | 463 (100) | 55 (11.9) | 408 (88.1) | 62 (13.4) | 401 (86.6) | |
3.3. Prevalence of Parasitic Infection Among Respondents
Out of 463 stool specimens collected and examined, 129 (27.9%) were found positive for one helminth infection. Four species: A. lumbricoides, hookworm, Hymenolepis nana, and Schistosoma mansoni of parasitic infections were identified in the study. Hookworm was the first predominate parasite detected in 62 (13.4%) followed by A. lumbricoides 55 (11.9%). Additionally, H. nana and S. mansoni were also detected in eight (1.7%) and four (0.8%), respectively. Males (68; 14.7%) were mostly affected than females (61; 13.2%) (Table 4).
Table 4.
The prevalence of parasitic infection among students in the Fogera district, northwest Ethiopia, in 2023 (n = 463).
| Study subject (n = 463) |
A. lumbricoides
n (%) |
Hookworm n (%) |
S. mansoni
n (%) |
H. nana
n (%) |
Total n (%) |
|---|---|---|---|---|---|
| Male | 28 (13.0) | 33 (15.3) | 3 (1.4) | 4 (1.8) | 68 (14.7) |
| Female | 27 (10.9) | 29 (11.7) | 1 (0.4) | 4 (1.6) | 61 (13.2) |
| Total | 55 (11.9) | 62 (13.4) | 4 (0.8) | 8 (1.7) | 129 (27.9) |
3.4. Intensity of Infections in the Study Area
In the study area, the intensity of A. lumbricoides and hookworm infections was classified as light (Table 5).
Table 5.
Intensity of infections in the study area.
| Types of parasites | Arithmetic mean | Intensity of infections |
|---|---|---|
| Ascaris lumbricoides | 459.5 | Light |
| Hookworm | 475.8 | Light |
3.5. Strength of Association Between Risk Factors and A. lumbricoides and Hookworm Infections
3.5.1. Multivariate Logistic Regression
Based on the multivariate logistic regression analysis, uneducated mothers, uneducated fathers, not using latrine/toilet at home, not using latrine/toilet at school, irregular wearing of shoes, untrimmed fingernail status, the absence of handwashing facility at home, not washing hands after using the toilet, and not washing hands before meal were predictor factors for STH infection in the study area (p < 0.05) (Table 5).
Students having uneducated mothers were 24.99 times (AOR = 24.99; 95% CI = 7.05–88.67; p < 0.001) more likely to contract STH infections than those having educated mothers. Students having uneducated fathers were 3.03 times (AOR = 3.03; 95% CI = 1.18–7.77; p = 0.021) more likely to contract STH infections than those having educated fathers. Students not using latrine/toilet at school were 4.53 times (AOR = 4.53; 95% CI = 1.89–10.85; p < 0.001) more likely to contract STH infections than those using latrine/toilet at school.
Students that are irregular in wearing shoes were 18.59 times (AOR = 18.59; 95% CI = 6.89–50.13; p < 0.001) more likely to contract STH infections than those who always wear shoes. Students having untrimmed fingernail status were 7.31 times (AOR = 7.31; 95% CI = 2.57–20.81; p < 0.001) more likely to contract STH infections than those having trimmed fingernails. Students having no handwashing facility at home were 5.86 times (AOR = 5.86; 95% CI = 2.19–15.64; p < 0.001) more likely to contract STH infections than those having a handwashing facility at home. Students that are not washing hands after using the toilet were 14.87 times (AOR = 14.87; 95% CI = 3.97–55.75; p < 0.001) more likely to contract STH infections than those who wash hands after using the toilet. Students that were not washing hands before a meal were 30.05 times (AOR = 30.05; 95% CI = 11.05–81.74; p < 0.001) more likely to contract STH infections than those washing hands before a meal (Table 6).
Table 6.
Logistic regression analysis of important risk factors for soil-transmitted helminth infections.
| Variables | Categories | Parasite infection status | COR | AOR | |||
|---|---|---|---|---|---|---|---|
| Positive (n, %) | Negative (n, %) | 95% CI | p value | 95% CI | p value | ||
| Sex | Male | 60 (12.96) | 156 (33.7) | 1.28 (0.84, 1.95) | 0.246 | ||
| Female | 57 (12.3) | 190 (41.04) | 1 | ||||
|
| |||||||
| Grade | 5–7 | 62 (13.4) | 168 (36.3) | 0.68 (0.14, 3.28) | 0.63 | ||
| 1–4 | 53 (11.45) | 170 (36.72) | 0.85 (0.55, 1.29) | 0.44 | |||
| Kindergarten | 2 (0.4) | 8 (1.73) | 1 | ||||
|
| |||||||
| Name of school | Nora Mender | 87 (25.0) | 261 (56.4) | 1.06 (0.65, 1.72) | 0.82 | ||
| Alemmia | 30 (26.08) | 85 (18.4) | 1 | ||||
|
| |||||||
| Age | 10–14 | 71 (15.3) | 140 (30.2) | 2.27 (1.48, 3.49) | < 0.001∗ | 1.8 (0.72, 4.5) | 0.21 |
| 6–9 | 46 (10.0) | 206 (44.5) | 1 | 1 | |||
|
| |||||||
| Mothers' education | Uneducated | 108 (23.33) | 189 (40.8) | 6.69 (3.55, 12.6) | < 0.001∗ | 24.9 (7.05, 88.67) | < 0.001∗∗ |
| Educated | 9 (1.94) | 157 (33.9) | 1 | 1 | |||
|
| |||||||
| Fathers' education | Uneducated | 88 (19.0) | 203 (43.8) | 2.14 (1.34, 3.43) | 0.002∗ | 3.03 (1.18, 7.77) | 0.021∗∗ |
| Educated | 29 (6.3) | 143 (30.9) | 1 | ||||
|
| |||||||
| Latrine/toilet usage at home | No | 95 (20.5) | 230 (49.7) | 2.18 (1.30, 3.64) | 0.003∗ | 0.96 (0.33, 2.80) | 0.94 |
| Yes | 22 (47.5) | 116 (25.1) | 1 | 1 | |||
|
| |||||||
| Latrine/toilet usage at school | No | 82 (17.7) | 62 (13.4) | 11.45 (6.69, 18.86) | < 0.001∗ | 4.53 (1.89, 10.85) | 0.001∗∗ |
| Yes | 35 (7.6) | 284 (61.4) | 1 | 1 | |||
|
| |||||||
| Shoe-wearing habit | Sometimes | 109 (45.1) | 72 (15.6) | 17.39 (10.15, 29.82) | < 0.001∗ | 18.59 (6.89, 50.13) | < 0.001∗∗ |
| Always | 8 (1.7) | 274 (59.2) | 1 | ||||
|
| |||||||
| Drinking water source | Well water | 69 (14.9) | 101 (21.8) | 4.88 (2.84, 8.38) | < 0.001∗ | 2.79 (0.95, 8.22) | 0.063 |
| Stream | 26 (5.6) | 88 (19.0) | 2.11 (1.13, 3.94) | 0.019∗ | 1.09 (0.34, 3.54) | 0.88 | |
| Tap water | 22 (4.8) | 157 (33.9) | 1 | ||||
|
| |||||||
| Status of fingernails | Untrimmed | 99 (21.4) | 171 (36.9) | 5.6 (3.27, 9.71) | < 0.001∗ | 7.31 (2.57, 20.81) | < 0.001∗∗ |
| Trimmed | 18 (3.9) | 175 (37.8) | 1 | 1 | |||
|
| |||||||
| Handwashing facility at home | No | 93 (20.1) | 169 (36.5) | 4.06 (2.47, 6.66) | < 0.001∗ | 5.86 (2.19, 15.64) | < 0.001∗∗ |
| Yes | 24 (5.2) | 177 (38.2) | 1 | 1 | |||
|
| |||||||
| Handwash after using toilet | No | 108 (23.3) | 214 (46.2) | 7.4 (3.63, 15.11) | < 0.001∗ | 14.87 (3.97, 55.75) | < 0.001∗∗ |
| Yes | 9 (1.9) | 132 (28.5) | 1 | 1 | |||
|
| |||||||
| Handwash before feeding | No | 92 (19.9) | 42 (9.1) | 26.6 (15.4, 46.04) | < 0.001∗ | 30.05 (11.05, 81.74) | < 0.001∗∗ |
| Yes | 25 (5.4) | 304 (65.7) | 1 | 1 | |||
|
| |||||||
| Eating of raw vegetables or fruits | Yes | 93 (20.1) | 187 (40.4) | 3.29 (2.01, 5.41) | < 0.001∗ | 1.65 (0.58, 4.64) | 0.35 |
| No | 24 (5.2) | 159 (34.3) | 1 | ||||
Note: Edu = Education.
Abbreviations: AOR = adjusted odds ratio, COR = crude odds ratio.
∗Indicates COR-associated value and we should do the AOR association.
∗∗Indicates AOR-associated factors, meaning the factors are highly related with the prevalence.
4. Discussion
In the current study, the overall prevalence of A. lumbricoides and hookworm infections among students attending two primary schools was found to be 25.3% (95% CI: 21.5%–29.4%). According to the WHO classification, areas of infection risk are categorized into three groups: high-risk areas with a prevalence greater than 50%, moderate-risk areas with a prevalence between 20% and 50%, and low-risk areas with a prevalence lower than 20% [21]. Consequently, the study area in question falls within the moderate-risk category, indicating that no intervention is required at present but rather a case-by-case treatment approach.
The prevalence in the present study is higher than in the previous studies from Handuras (18.9%) [22], Northeast India (16.8%) [23], Adamawa state in Nigeria (19.4%) [24], Ngorongoro Conservation Area in Tanzania (17%) [25], Ethiopia (21.6%) [17], Sekela, Western Ethiopia (16.1%) [26], Gedeo zone (22.2%) [27], and Birbir town (14.2%) [28]. However, it is lower than in previous studies from Kandahar in Afghanistan (26.2%) [29], Laguna de Perlas (Nicaragua) (39.8%) [30], Ethiopia (27.5%) [31], southern Ethiopia (41.1%) [32], Amhara region (37.4%) [33], Tachgayint woreda (31.7%) [34], Yeki district (27.5%) [35], Kola Diba (42.7%) [9], Mettu town (67.1%) [36], and in wetland and nonwetland area of Blue Nile Basin (30.3%) [19]. The differences in study periods, the location of the study area, personal hygiene, and factors relating to environmental hygiene, ecological factors, as well as economic and cultural issues affecting students and the community may all be contributing causes to these variations in prevalence [32, 37]. The sociocultural determinants, behavioral traits, climatic conditions, application of preventive and control measures, and frequency and application of mass drug administration on intestinal parasites among different countries and regions may all play a role in the inconsistent prevalence of the infection.
Ascariasis is a common public health problem of preschool and primary schoolchildren in developing countries [38]. A. lumbricoides was 11.9% prevalent in the study area. It was categorized as a low-risk area by the WHO guidelines for classifying infection-risky places. This result was higher than those of studies done in Brazil (2.4%) [39], Bolifamba, Buea in Cameroon (3.9%) [40], Ngorongoro Conservation Area in Tanzania (4%) [25], and Ethiopia (11.2%) [41]. However, it is lower than the results of several earlier investigations reported a higher prevalence of A. lumbricoides in Kandahar in Afghanistan (18.7%) [29], Kakamega County in Kenya (43.5%) [42], Ethiopia (13.98%) [43], shore of Lake Hawassa (44.4%) [44], Dessie city (18.5%) [45], Blue Nile Basin in northwest Ethiopia (20.4%) [19], and Gedeo zone (18.6%) [27]. This might be caused by subpar sanitation, a lack of restrooms, the area's elevation, the kind of soil, or the fact that autumnal cases were highest in September [38]. A. lumbricoides was found in one type of individual in the other study, which is comparable to the current study. This shows that these parallels may be due to similarities in the physical setting of the study area, ecological factors, as well as sociocultural influences on students and the general public.
The prevalence of hookworm in the study area was 13.4%. According to WHO guidelines to classify the risky areas of infections, it was grouped under low-risk area. This result was lower than that of the study done in the Amhara region (20.6%) [33], Kerewo town (37.4%) [46], Dera district (21.7%) [47], and Durbete (46.9%) [48]. However, the result of the present study was higher than that of the study done in Northeast India (7.4%) [23], Benin (3.2%) [49], Honduras (1.9%) [22], Adamawa state in Nigeria (5.0%) [24], Kandahar in Afghanistan (7.5%) [29], Ngorongoro Conservation Area in Tanzania (13%) [25], Laguna de Perlas (Nicaragua) (12.7%) [30], Bolifamba, Buea in Cameroon (2%) [40], Ethiopia (8.89%) [50], Ethiopia (10.4%) [17], and Ethiopia (12.51%) [43]. This difference among the above findings with the present one might be due to several environmental, social, and geographical factors [51], and might be due to the difference in socioeconomic status, health information, waste disposal system, sample collection season, soil type, as well as climatic and topographic factors of the study areas.
When we look at the prevalence of infections in each school, the highest prevalence (26.1%) was found in the students of Alemmia primary school, while the lowest prevalence (25.1%) was found in the students of Nora Mender primary school. Health education seeks to modify people's attitudes toward their health and cleanliness as well as their behavior in general. Knowledge is frequently increased by disseminating information on the disease and the potential adoption of preventive actions. This may be due to the fact that Nora Mender primary school and the health facility are relatively close by (side by side), making it easier for health professionals to convey information to the schoolchildren about the healthcare system than at Alemmia primary school, which is located far away from the health center. Based on parasite infection, Alemmia primary school was highly prevalent in A. lumbricoides compared to Nora Mender, and in hookworm, Nora Mender primary school was highly prevalent compared to Alemmia primary school. This might be the position of the environment and their soil type, which means Alemmia primary school is slightly elevated and has loam soil in nature than Nora Mender primary school, so this type of environmental nature is suitable for A. lumbricoides [52]. In Nora Mender primary school, the environment has clay soil type and has a lower elevation point than Alemmia primary school, so this type of soil and the elevation point lower than 2000 m above sea level are suitable for hookworm [53].
In this study, the age group from 10 to 14 years old was more affected than 6–9 years. This difference might be due to the fact that these children have a better chance of attending school. In addition, the main reported reasons for not taking treatment were not attending school and treatment not given. These findings can be justified by the high coverage observed in our study among school-attending children [54]. Similarly, the studies done in eastern Côte d'Ivoire [55], Ethiopia [54], Rama town [56], Birbir town [28], and Medebay Zana woreda in Tigray [57] found consistent results. However, the results of the studies done in Northeast India [23], Gog Gob [27] primary schools in northwest Ethiopian [58], and Ogun state in Nigeria [59] were contradictory.
According to WHO guidelines [20], the infection of STHs in this study was classified as light-intensity infections. The intensity of STHs is categorized as light, moderate, or heavy based on the arithmetic mean of positive participants [60]. Almost all positive cases of A. lumbricoides and hookworm infection exhibited light intensity, which is consistent with previous reports in the Gurage zone of south-central Ethiopia [34]. However, other previous studies have reported occurrences of moderate- and heavy-intensity infections rather than light-intensity infections [61]. This variation could have a positive impact on validating the elimination of A. lumbricoides and hookworm infections and the appearance of infections in different countries, including our own, and the study area may be subject to a routine deworming treatment.
In this study, not washing hands before eating showed a significant association with the prevalence of STH infection. Similar findings were reported in various locations in Ethiopia, including Durbete town, Dessie city, southern Ethiopia, Ambo town, Goro southwest Shewa, and the shore of Lake Hawassa [10, 11, 45, 48, 50, 62]. The WHO states that areas with poor sanitation tend to have the highest prevalence of such infection [63]. Another risk factor that exhibited a statistically significant association with STH infection was the mother's education level. In this study, it was found that the mother's education level was associated with the prevalence of A. lumbricoides infection among students. Similar findings have been reported in previous studies conducted in various regions of Ethiopia, such as in southern Ethiopia [43, 50], in Mettu town [36], and in Ambo town [62].
The absence of latrine/toilet usage at school was found to be significantly associated with the development of STH infection in this research. Similar results were reported in studies conducted in Sekela, western Ethiopia [26], and Endemata primary school at Debre Markos town [13]. These consistent findings highlight the importance of proper sanitation facilities, specifically latrine/toilet usage, in reducing the risk of infections.
Untrimmed fingernails were found to be significantly associated with the development of STH infection. Consistent findings have been reported in several studies conducted in Ethiopia such as in southern Ethiopia, in Blue basin in northwest Ethiopia [19], in Hiruy Abaregawi rural Debre Tabor [64], in Mettu town [36], in Goro, southwest Shewa [65], in Ejaji [66], in Gob Gob primary school in northwest Ethiopia [58], and in Sekela, western Ethiopia [26]. These consistent findings highlight the importance of maintaining trimmed fingernails as a preventive measure against A. lumbricoides infection. Proper hand hygiene, including regular nail trimming, can significantly reduce the risk of transmitting pathogens and subsequent infection.
Additionally, it was found that students with uneducated fathers had a significant association with STH infection. This finding is consistent with other reports from Ambesamie [67], Dessie city [45], Ambo town [62], and Chencha town [68]. And the absence of handwashing facilities at home was also significantly associated with parasite infection in this study. Consistent results supporting this association were reported in Chencha town [68]. These findings highlight the importance of education and access to proper hygiene facilities in preventing and controlling parasite infections. The educational level of the father can influence household practices and awareness regarding hygiene, which in turn can impact the transmission of these parasitic infections. Similarly, the availability of handwashing facilities at home plays a crucial role in promoting hand hygiene and reducing the risk of infection transmission. Therefore, efforts to improve education and hygiene infrastructure can contribute to the prevention and control of STH infection among students.
Not washing hands after using the toilet has shown a significant association with STH infections. Consistent findings supporting this association have been reported in various studies such as in Kandahar in Afghanistan [29], in Northeast India [23], in southern Ethiopia [10, 50], in Blue basin in northwest Ethiopia [19], in Medebay Zana woreda in Tigray [57], and in Birbir town [28]. These consistent results highlight the importance of washing hands after using the toilet as a protective measure against infections, particularly infections caused by STH. Proper hand hygiene, including thorough handwashing with soap and water, is crucial in preventing the transmission of pathogens and reducing the risk of infections.
Irregular wearing of shoes has been found to be significantly associated with the development of STH infection. Consistent results supporting this association have been reported in various studies such as in Kandahar in Afghanistan [29], in Bolifamba Buea in Cameroon [40], in southern Ethiopia [43], in northwest Ethiopia [69], in Gena bossa woreda [46], in Sekela in western Ethiopia [26], and in Tachgayint [34]. These consistent findings highlight the importance of regular and proper use of footwear in preventing hookworm infection. Wearing shoes provides a physical barrier between the feet and the environment, reducing the risk of exposure to hookworm infection present in the soil or contaminated surfaces. Therefore, maintaining regular and appropriate use of shoes can contribute to protecting against hookworm infection and promoting overall foot hygiene. The predominant mode of hookworm transmission through skin penetration highlights the significance of proper sanitation and hygiene practices, especially in environments with contaminated soil. Most of the time, hookworm transmission occurs through skin penetration, although there are instances where hookworm parasites can be transmitted to humans through the ingestion of filariform larvae of An. duodenale in contaminated food [70]. In the present study, mothers' education was found to be less likely to be associated with hookworm infection. This finding aligns with the results reported in Indonesia [71]. However, it is reassuring to note that in this study, mothers' education did not appear to be a major risk factor for hookworm infection.
These varying findings could be attributed to factors such as the hygienic conditions of latrines, the quality of household stored water, and indicators of malnutrition such as height and weight for age [72]. It is important to consider that the relationship between these variables and the prevalence of infections can be influenced by various contextual factors, including differences in geographical locations, sanitation practices, and individual behaviors.
5. Conclusion
In conclusion, the overall prevalence of A. lumbricoides and hookworm infections among students attending two primary schools was found to be 25.3%. The study area falls within the moderate-risk category according to the WHO classification. The prevalence of infections differed between the two primary schools, with higher prevalence observed in Alemmia primary school for A. lumbricoides (15.7%) and Nora Mender primary school for hookworm (13.8%). Due to their outdoor playing habits, males had a slightly higher prevalence of infections compared to females. More infections affected the age group of 10–14 years old than 6–9 years old.
The result of infection risk factors indicated that uneducated parents, not using latrine or toilet at school, not having a washing facility at home, not washing hands after toilet and before eating, and not trimming fingernails were identified as cardinal risk factors for A. lumbricoides infection, and irregular wearing of shoes, age between 10 and 14 years, and not washing hands after toilet use were major risk factors for hookworm infection among the study subjects and contributed to the high prevalence of A. lumbricoides and hookworm infections.
5.1. Recommendations
It is essential to plan and carry out preventive and control programs, raise health awareness in study areas, and decrease the burden of diseases. Further integrated control measures must be developed, including a safe water supply, washing program, access to toilets, home education initiatives, shoe wearing, and the creation of an environment free from open defecation. Community awareness must also be increased, and student health must be promoted through health education and good personal hygiene. In order to lessen the impact of the diseases, it is crucial to regularly consecutively deworm students, devise and implement prevention and control programs, and promote health awareness in study locations. Additionally, it is advised to administer a double or treble dose rather than a single dose when treating sick persons.
5.2. Limitations of the Study
This study is limited to primary schools, which restricts the generalizability of the findings. Including schools from other districts would have provided a more comprehensive assessment of the prevalence of these infections. The lack of availability of data on open defecation and deworming was considered a limitation for this study. Additionally, the absence of polymerase chain reaction (PCR)–based methods prevented the identification of specific hookworm species. In addition, we recognize several limitations in this study. Firstly, due to limited resources and laboratory facilities, we could not perform molecular diagnostic techniques like polymerase chain reaction (PCR) to distinguish between hookworm species. This means that our findings do not identify the exact species involved, which could have offered clearer insights into the epidemiology and informed species-specific control strategies. Secondly, we did not collect data on open defecation practices, an important risk factor for hookworm transmission. Not including this variable may restrict our analysis of related risk factors and could underestimate the impact of sanitation on the observed prevalence. Despite these limitations, the study offers valuable baseline information for public health planning and emphasizes the need for more research that includes better diagnostics and thorough behavioral data.
Funding Statement
No funding was received for this research.
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Ethics Statement
The researcher sought ethical approval from the ethical review board of Bar Dar University's Science College prior to initiating the investigation. Permission letters were obtained from the health and education offices at the zonal and district levels. Written informed consent was obtained from the parents/guardians of the children after providing them with an explanation of the study's purpose and objectives. Additionally, the children were asked for their assent before participating in the study. If any study participants tested positive for intestinal parasites other than A. lumbricoides and hookworm, they were referred to nearby health institutions.
Consent
Please see the Ethics Statement.
Disclosure
The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.
Conflicts of Interest
The authors declare no conflicts of interest.
Author Contributions
Miseganaw Sisay developed the conception of the articles, designed the methodology, participated in data collection, manuscript drafting, and data analysis, and approved the final manuscript. Destaw Damtie participated in designing and editing and finally approved the manuscript. Tadesse Hailu participated in data collection, analysis, and editing and finally approved the final draft. Woyneshet Gelaye, Alemtsehay Kolech, and Solomon Alebele participated in editing and finally approved the final draft.
Supporting Information
Additional supporting information can be found online in the Supporting Information section.
Supporting information related to this paper, including extended data tables, additional figures, and detailed method descriptions, is included to support the findings and is available upon request or in the online supporting file.
References
- 1.CDC. Soil Transmitted Helminthiasis. Centers of Disease Control and Prevention. https://www.cdc.gov/parasites/sth/index.html .
- 2.Tee M. Z., Lee S. C., Er Y. X., et al. Efficacy of Triple Dose Albendazole Treatment for Soil-Transmitted Helminth Infections. Plos One . 2022;17(8):p. e0272821. doi: 10.1371/journal.pone.0272821. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.WHO. Soil Transmitted Helimnth Infections. https://www.who.int/news-room/fact-sheets/detail/soil-transmitted-helminth-infections .
- 4.Tefera E., Belay T., Mekonnen S. K., Zeynudin A., Belachew T. Therapeutic Efficacy of Different Brands of Albendazole Against Soil Transmitted Helminths Among Students of Mendera Elementary School, Jimma, Southwest Ethiopia. The Pan African Medical Journal . 2015;22:p. 252. doi: 10.11604/pamj.2015.22.252.6501. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Barry M. A., Simon G. G., Mistry N., Hotez P. J. Global Trends in Neglected Tropical Disease Control and Elimination: Impact on Child Health. Archives of Disease in Childhood . 2013;98(8):635–641. doi: 10.1136/archdischild-2012-302338. [DOI] [PubMed] [Google Scholar]
- 6.ECVS. Measuring Treatment Coverage for Schistosomiasis and Soil Transmitted Helminths With Preventive Chemotherapy
- 7.Maddren R., Phillips A., Ower A., et al. Soil-Transmitted Helminths and Schistosome Infections in Ethiopia: A Systematic Review of Progress in Their Control Over the Past 20 Years. Parasites & Vectors . 2021;14(1):97–15. doi: 10.1186/s13071-021-04600-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Chelkeba L., Mekonnen Z., Emana D., Jimma W., Melaku T. Prevalence of Soil-Transmitted Helminths Infections Among Preschool and School-Age Children in Ethiopia: A Systematic Review and Meta-Analysis. Glob Health Res Policy . 2022;7(1):p. 9. doi: 10.1186/s41256-022-00239-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Hussein A., Alemu M., Ayehu A. Soil Contamination and Infection of School Children by Soil-Transmitted Helminths and Associated Factors at Kola Diba Primary School, Northwest Ethiopia: An Institution-Based Cross-Sectional Study. Journal of Tropical Medicine . 2022;2022:1–8. doi: 10.1155/2022/4561561. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Aemiro A., Menkir S., Tegen D., Tola G. Prevalence of Soil-Transmitted Helminthes and Associated Risk Factors Among People of Ethiopia: A Systematic Review and Meta-Analysis. Information Display . 2022;15:p. 11786337211055437. doi: 10.1177/11786337211055437. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Eyamo T., Girma M., Alemayehu T., Bedewi Z. Soil-Transmitted Helminths and Other Intestinal Parasites Among Schoolchildren in Southern Ethiopia. Research and Reports in Tropical Medicine . 2019;10:137–143. doi: 10.2147/rrtm.s210200. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Alelign T., Degarege A., Erko B. Soil-Transmitted Helminth Infections and Associated Risk Factors Among Schoolchildren in Durbete Town, Northwestern Ethiopia. Journal of Parasitology Research . 2015;2015:1–5. doi: 10.1155/2015/641602. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Fenta A., Mesganaw B., Belachew F., et al. Prevalence and Risks of Soil Transmitted Helminths Among Ethiopian School Children: A Cross-Sectional Study. Asian Pacific Journal of Tropical Medicine . 2022;15(3):121–127. doi: 10.4103/1995-7645.338438. [DOI] [Google Scholar]
- 14.Hailu T., Abera B., Mulu W., Kassa S., Genanew A., Amor A. Prevalence and Factors Associated With Intestinal Parasitic Infections Among Pregnant Women in West Gojjam Zone, Northwest Ethiopia. Journal of Parasitology Research . 2020;2020:1–6. doi: 10.1155/2020/8855362. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Samuel F. Status of Soil-Transmitted Helminths Infection in Ethiopia. American Journal of Health Research . 2015;3(3):170–176. doi: 10.11648/j.ajhr.20150303.21. [DOI] [Google Scholar]
- 16.Mengistu W., Melaku W., Tesfu F. The Prevalence of Intestinal Helminthic Infections and Associated Risk Factors Among School Children in Lumame Town, Northwest, Ethiopia. Journal of Parasitology and Vector Biology . 2014;6(10):156–165. doi: 10.5897/jpvb2014.0159. [DOI] [Google Scholar]
- 17.Alemu G., Mekonnen F., Nega M., Muluneh C. Trend of Soil-Transmitted Helminths in Ethiopian Children: A Systematic Review and Meta-Analysis (2000-2018) Journal of Parasitology Research . 2021;2021:2021–13. doi: 10.1155/2021/5638836. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Sgzhd. The Prevalence of Soil Transmitted Helimnths in South Gondar Zone. 2022.
- 19.Genet A., Motbainor A., Samuel T., Azage M. Prevalence and Associated Factors of Soil Transmitted Helminthiasis Among School-Age Children in Wetland and Non-Wetland Areas of Blue Nile Basins, Northwest Ethiopia: A Community-Based Comparative Study. Sage Open Medicine . 2021;9:p. 20503121211063354. doi: 10.1177/20503121211063354. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.WHO. Prevention and Control of Schistosomiasis and Soil-Transmitted Helminthiasis: Report of a WHO Expert Committee . World Health Organization; 2002. [PubMed] [Google Scholar]
- 21.Organization W. H. Soil-Transmitted Helminthiases: Eliminating as Public Health Problem Soil-Transmitted Helminthiases in Children: Progress Report 2001-2010 and Strategic Plan 2011-2020 . World Health Organization; 2012. [Google Scholar]
- 22.Matamoros G., Rueda M. M., Rodríguez C., et al. High Endemicity of Soil-Transmitted Helminths in a Population Frequently Exposed to Albendazole but No Evidence of Antiparasitic Resistance. Tropical Medicine and Infectious Disease . 2019;4(2):p. 73. doi: 10.3390/tropicalmed4020073. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Deka S., Barua D., Bahurupi Y., Kalita D. Assessment of the Prevalence of Soil-Transmitted Helminth Infections and Associated Risk Factors Among School-Aged Children in a Flood Affected Area of Northeast India. The American Journal of Tropical Medicine and Hygiene . 2021;105(2):480–489. doi: 10.4269/ajtmh.20-1238. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Pukuma M. S., Thadawus D., Augustine L. M. Soil Transmitted Helminths Among School Aged Children in Hong Local Government Area of Adamawa State, Nigeria. Animal Research International . 2022;19(1) [Google Scholar]
- 25.Eltantawy M., Orsel K., Schroeder A., et al. Soil Transmitted Helminth Infection in Primary School Children Varies With Ecozone in the Ngorongoro Conservation Area, Tanzania. Tropical Medicine and Health . 2021;49(1):22–12. doi: 10.1186/s41182-021-00310-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Tolera A., Dufera M. The Prevalence of Soil-Transmitted Helminths and Associated Risk Factors Among School Children at Sekela Primary School, Western Ethiopia. Journal of Parasitology Research . 2020;2020:1–7. doi: 10.1155/2020/8885734. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Wudneh F., Gebeyehu Y. Prevalence of Intestinal Helminths and Its Associated Risk Factors Among Primary School Children in Gedeo Zone, Southern Ethiopia. Ethiopian Medical Journal . 2022;60(2) [Google Scholar]
- 28.Alemu G., Abossie A., Yohannes Z. Current Status of Intestinal Parasitic Infections and Associated Factors Among Primary School Children in Birbir Town, Southern Ethiopia. BMC Infectious Diseases . 2019;19(1):p. 270. doi: 10.1186/s12879-019-3879-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Rahimi B. A., Mahboobi B. A., Wafa M. H., Sahrai M. S., Stanikzai M. H., Taylor W. R. Prevalence and Associated Risk Factors of Soil-Transmitted Helminth Infections in Kandahar, Afghanistan. BMC Infectious Diseases . 2022;22(1):361–369. doi: 10.1186/s12879-022-07336-Z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Muñoz-Antoli C., Pavón A., Pérez P., Toledo R., Esteban J. Soil-Transmitted Helminth Infections in Schoolchildren of Laguna De Perlas (Nicaragua) Journal of Tropical Pediatrics . 2017;63(2):124–134. doi: 10.1093/tropej/fmw061. [DOI] [PubMed] [Google Scholar]
- 31.Hailegebriel T., Nibret E., Munshea A. Prevalence of Soil-Transmitted Helminth Infection Among School-Aged Children of Ethiopia: A Systematic Review and Meta-Analysis. Infectious Diseases: Research and Treatment . 2020;13:p. 1178633720962812. doi: 10.1177/1178633720962812. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Eyamo T., Girma M., Alemayehu T., Bedewi Z. Soil-Transmitted Helminths and Other Intestinal Parasites Among Schoolchildren in Southern Ethiopia. Research and Reports in Tropical Medicine . 2019;10:137–143. doi: 10.2147/rrtm.s210200. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Nute A. W., Endeshaw T., Stewart A. E. P., et al. Prevalence of Soil-Transmitted Helminths and Schistosoma Mansoni Among a Population-Based Sample of School-Age Children in Amhara Region, Ethiopia. Parasites & Vectors . 2018;11(1):p. 431. doi: 10.1186/s13071-018-3008-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Eyayu T., Yimer G., Workineh L., et al. Prevalence, Intensity of Infection and Associated Risk Factors of Soil-Transmitted Helminth Infections Among School Children at Tachgayint Woreda, Northcentral Ethiopia. Plos One . 2022;17(4):p. e0266333. doi: 10.1371/journal.pone.0266333. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Gebrezgabiher G., Yewhalaw D., Ayana M., Hailu A., Mekonnen Z. Impact of Ivermectin Mass Drug Administration on Burden of Soil-Transmitted Helminths in Onchocerciasis Control and Elimination Programs, Yeki District, Southwest Ethiopia. Plos One . 2022;17(2):p. e0263625. doi: 10.1371/journal.pone.0263625. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Yeshanew S., Bekana T., Truneh Z., Tadege M., Abich E., Dessie H. Soil-Transmitted Helminthiasis and Undernutrition Among Schoolchildren in Mettu Town, Southwest Ethiopia. Scientific Reports . 2022;12(1):p. 3614. doi: 10.1038/s41598-022-07669-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Ojha S. C., Jaide C., Jinawath N., Rotjanapan P., Baral P. Geohelminths: Public Health Significance. The Journal of Infection in Developing Countries . 2014;8(01):005–016. doi: 10.3855/jidc.3183. [DOI] [PubMed] [Google Scholar]
- 38.Ali S. A., Niaz S., Aguilar-Marcelino L., et al. Prevalence of Ascaris lumbricoides in Contaminated Faecal Samples of Children Residing in Urban Areas of Lahore, Pakistan. Scientific Reports . 2020;10(1):21815–21818. doi: 10.1038/s41598-020-78743-Y. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Oishi C. Y., Klisiowicz D. d R., Seguí R., et al. Reduced Prevalence of Soil-Transmitted Helminths and High Frequency of Protozoan Infections in the Surrounding Urban Area of Curitiba, Paraná, Brazil. Parasite Epidemiology and Control . 2019;7:p. e00115. doi: 10.1016/j.parepi.2019.e00115. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Ako S. E., Edith A., Vicky T. N., Abiabia A. N., Kimbi H. K. Persistent Soil-Transmitted Helminth Infections and Associated Risk Factors Among Children Aged Between 4 and 12 in Mile 16 Bolifamba, Buea, Cameroon: 6 Months Post-Deworming Campaign. International Journal of TropICAL DiseASE & Health . 2018;32(4):1–9. doi: 10.9734/ijtdh/2018/44165. [DOI] [Google Scholar]
- 41.Alemu G., Mekonnen F., Nega M., Muluneh C. Trend of Soil-Transmitted Helminths in Ethiopian Children: A Systematic Review and Meta-Analysis (2000-2018) Journal of Parasitology Research . 2021;2021:1–13. doi: 10.1155/2021/5638836. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Ngonjo T. W. Effectiveness of Albendazole on Soil Transmitted Nematodes Among School Going Children in Kakamega County, Kenya . Kenyatta University; 2020. [Google Scholar]
- 43.Assemie M. A., Shitu Getahun D., Hune Y., et al. Prevalence of Intestinal Parasitic Infection and Its Associated Factors Among Primary School Students in Ethiopia: A Systematic Review and Meta-Analysis. PLOS Neglected Tropical Diseases . 2021;15(4):p. e0009379. doi: 10.1371/journal.pntd.0009379. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Tadege B., Shimelis T. Infections With Schistosoma Mansoni and Geohelminths Among School Children Dwelling Along the Shore of the Lake Hawassa, Southern Ethiopia. Plos One . 2017;12(7):p. e0181547. doi: 10.1371/journal.pone.0181547. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.Aschale A., Adane M., Getachew M., et al. Water, Sanitation, and Hygiene Conditions and Prevalence of Intestinal Parasitosis Among Primary School Children in Dessie City, Ethiopia. Plos One . 2021;16(2):p. e0245463. doi: 10.1371/journal.pone.0245463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46.Teklemariam Ergat Y., Abebe Demissie D. Prevalence and Determinants of Soil Transmitted Helminthes Infections Among Primary School Children in Kerewo Town, Gena Bossa Woreda, Ethiopia: Cross Sectional Study. Journal of Infectious Diseases and Epidemiology . 2019;5:p. 90. doi: 10.23937/2474-3658/1510090. [DOI] [Google Scholar]
- 47.Tegen D., Damtie D. Prevalence and Risk Factors Associated With Intestinal Parasitic Infection Among Primary School Children in Dera District, Northwest Ethiopia. The Canadian Journal of Infectious Diseases & Medical Microbiology . 2021;2021:1–15. doi: 10.1155/2021/5517564. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 48.Alelign T., Degarege A., Erko B. Soil-Transmitted Helminth Infections and Associated Risk Factors Among Schoolchildren in Durbete Town, Northwestern Ethiopia. Journal of Parasitology Research . 2015;2015:1–5. doi: 10.1155/2015/641602. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 49.Avokpaho E. F., Houngbégnon P., Accrombessi M., et al. Factors Associated With Soil-Transmitted Helminths Infection in Benin: Findings From the Deworm3 Study. Plos Neglected Tropical Diseases . 2021;15(8):p. e0009646. doi: 10.1371/journal.pntd.0009646. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50.Liyih M., Damtie D., Tegen D. Prevalence and Associated Risk Factors of Human Intestinal Helminths Parasitic Infections in Ethiopia: A Systematic Review and Meta-Analysis. The Scientific World Journal . 2022;2022:1–15. doi: 10.1155/2022/3905963. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 51.Hailu T., Mulu W., Abera B. Prevalence and Determinant Factors of Hookworm Infection Among School Age Children in Jawe District, Northwest Ethiopia. African Health Sciences . 2019;19(3):2439–2445. doi: 10.4314/ahs.v19i3.18. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52.Wardell R., Clements A. C., Lal A., et al. An Environmental Assessment and Risk Map of Ascaris lumbricoides and Necator americanus Distributions in Manufahi District, Timor-Leste. Plos Neglected Tropical Diseases . 2017;11(5):p. e0005565. doi: 10.1371/journal.pntd.0005565. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 53.Mabaso M., Appleton C., Hughes J., Gouws E. The Effect of Soil Type and Climate on Hookworm (Necator americanus) Distribution in Kwazulu‐Natal, South Africa. Tropical Medicine and International Health . 2003;8(8):722–727. doi: 10.1046/j.1365-3156.2003.01086.x. [DOI] [PubMed] [Google Scholar]
- 54.Asfaw M., Zerdo Z., Churko C., et al. Preventive Chemotherapy Coverage Against Soil-Transmitted Helminthiases Among School Age Children in Vertical Versus Integrated Treatment Approaches: Implications From Coverage Validation Survey in Ethiopia. Medrxiv . 2020 doi: 10.1371/journal.pone.0235281. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55.Loukouri A., Méité A., Kouadio O. K., et al. Prevalence, Intensity of Soil-Transmitted Helminths, and Factors Associated With Infection: Importance in Control Program With Ivermectin and Albendazole in Eastern Côte d’ivoire. Journal of Tropical Medicine . 2019;2019:1–10. doi: 10.1155/2019/7658594. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 56.Yeshitila Y. G., Zewde H., Mekene T., Manilal A., Lakew S., Teshome A. Prevalence and Associated Risk Factors of Intestinal Parasites Among Schoolchildren From Two Primary Schools in Rama Town, Northern Ethiopia. The Canadian Journal of Infectious Diseases & Medical Microbiology . 2020;2020:5750891–5750898. doi: 10.1155/2020/5750891. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57.Teshale T., Belay S., Tadesse D., Awala A., Teklay G. Prevalence of Intestinal Helminths and Associated Factors Among School Children of Medebay Zana Wereda; North Western Tigray, Ethiopia 2017. BMC Research Notes . 2018;11(1):p. 444. doi: 10.1186/s13104-018-3556-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 58.Alemu M., Anley A., Tedla K. Magnitude of Intestinal Parasitosis and Associated Factors in Rural School Children, Northwest Ethiopia. Ethiopian Journal of Health Sciences . 2019;29(1):923–928. doi: 10.4314/ejhs.v29i1.14. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59.Akinsanya B., Taiwo A., Adedamola M., Okonofua C. An Investigation on the Epidemiology and Risk Factors Associated With Soil-Transmitted Helminth Infections in Ijebu East Local Government Area, Ogun State, Nigeria. Scientific African . 2021;12:p. e00757. doi: 10.1016/j.sciaf.2021.e00757. [DOI] [Google Scholar]
- 60.WHO. Assessing the Efficacy of Anthelminthic Drugs Against Schistosomiasis and Soil-Transmitted Helminthiases. 2013.
- 61.Gebreyesus T. D., Tadele T., Mekete K., et al. Prevalence, Intensity, and Correlates of Schistosomiasis and Soil-Transmitted Helminth Infections After Five Rounds of Preventive Chemotherapy Among School Children in Southern Ethiopia. Pathogens . 2020;9(11):p. 920. doi: 10.3390/pathogens9110920. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 62.Samuel F., Demsew A., Alem Y., Hailesilassie Y. Soil Transmitted Helminthiasis and Associated Risk Factors Among Elementary School Children in Ambo Town, Western Ethiopia. BMC Public Health . 2017;17(1):p. 791. doi: 10.1186/s12889-017-4809-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 63.WHO. Bench Aids for the Diagnosis of Intestinal Parasites . World Health Organization; 2019. [Google Scholar]
- 64.Workineh L., Kiros T., Damtie S., Andualem T., Dessie B. Prevalence of Soil-Transmitted Helminth and Schistosoma Mansoni Infection and Their Associated Factors Among Hiruy Abaregawi Primary School Children, Rural Debre Tabor, North West Ethiopia: A Cross-Sectional Study. Journal of Parasitology Research . 2020;2020:1–7. doi: 10.1155/2020/2521750. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 65.Tiruneh T., Geshere G., Ketema T. Prevalence and Determinants of Soil-Transmitted Helminthic Infections Among School Children at Goro Primary School, South West Shewa, Ethiopia. International Journal of Pediatrics . 2020;2020:1–7. doi: 10.1155/2020/8612054. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 66.Ibrahim T., Zemene E., Asres Y., et al. Epidemiology of Soil-Transmitted Helminths and Schistosoma Mansoni: A Base-Line Survey Among School Children, Ejaji, Ethiopia. The Journal of Infection in Developing Countries . 2018;12(12):1134–1141. doi: 10.3855/jidc.9665. [DOI] [PubMed] [Google Scholar]
- 67.Feleke D. G., Ali A., Bisetegn H., Debash H., Birara W., Andualem A. Soil-Transmitted Helminthes and Schistosoma Mansoni Infections Among Primary School Children at Ambasame Primary School, North-West Ethiopia: A Cross-Sectional Study. BMC Pediatrics . 2022;22(1):p. 477. doi: 10.1186/s12887-022-03534-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 68.Abossie A., Seid M. Assessment of the Prevalence of Intestinal Parasitosis and Associated Risk Factors Among Primary School Children in Chencha Town, Southern Ethiopia. BMC Public Health . 2014;14(1):p. 166. doi: 10.1186/1471-2458-14-166. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 69.Muluneh C., Hailu T., Alemu G. Prevalence and Associated Factors of Soil-Transmitted Helminth Infections Among Children Living With and Without Open Defecation Practices in Northwest Ethiopia: A Comparative Cross-Sectional Study. The American Journal of Tropical Medicine and Hygiene . 2020;103(1):266–272. doi: 10.4269/ajtmh.19-0704. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 70.Kucik C. J., Martin G. L., Sortor B. V. Common Intestinal Parasites. American Family Physician . 2004;69(5):1161–1168. [PubMed] [Google Scholar]
- 71.Sakti H., Nokes C., Subagio Hertanto W., et al. Evidence for an Association Between Hookworm Infection and Cognitive Function in Indonesian School Children. Tropical Medicine and International Health . 1999;4(5):322–334. doi: 10.1046/j.1365-3156.1999.00410.x. [DOI] [PubMed] [Google Scholar]
- 72.Harris M., Alzua M. L., Osbert N., Pickering A. Community-Level Sanitation Coverage More Strongly Associated With Child Growth and Household Drinking Water Quality Than Access to a Private Toilet in Rural Mali. Environmental Science & Technology . 2017;51(12):7219–7227. doi: 10.1021/acs.est.7b00178. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Additional supporting information can be found online in the Supporting Information section.
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
