Abstract
Background:
A Soil-transmitted helminthic infection (STHIs) remains a notable health problem in resource-limited countries.
Objective:
This systematic review and meta-analysis aimed to determine the overall prevalence of STH infections in Ethiopia.
Methods:
Articles written in English were searched from online public databases. Searching terms taken separately and jointly were “prevalence,” “soil-transmitted helminths” “nematode,” “Geo-helminths,” “roundworm,” “Necator,” “Ancylostoma,” “Ascaris,” “Trichuris,” “hookworm,” “whipworm,” “S. strecoralies,” “associated factors,” and “Ethiopia.” We used STATA version 14 for meta-analysis and Cochran’s Q test statistics and the I2 test for heterogeneity.
Result:
From 297 reviewed articles 41 fulfilled the inclusion criteria. The pooled prevalence of STH infections in Ethiopia was 36.78% Ascaris lumbricoides had the highest pooled prevalence 17.63%, followed by hook worm12.35%. Trichuris trichiura 7.24% when the prevalence of S. strecoralies was 2.16% (95% CI: 0.97-3.35). Age, sex, residence, family education level, lack of shoe wearing habits and open defecation were identified as risk factors for STH infection. Eating unwashed and uncooked fruit and vegetables increased the risk of STH infection by 1.88 times while untrimmed finger nail and lack of hand washing habits increase the risk of STH infection by 1.28 and 3.16 times respectively with 95% CI.
Limitation:
Lack of published studies from Afar, Gambela, Somali, and Benshangul gumuz regions may affect the true picture. The other limitation is that the search strategy will be restricted articles published only in the English language but there might be articles that published using another language.
Conclusion:
Ascaris lumbricoides, hookworms and Trichuris trichiura, are the most prevalent soil-transmitted helminthes infections in Ethiopia. Age, sex, residence, family education level, lack of shoe wearing habits Open defecation untrimmed finger nail and lack of hand washing habits significantly associated with STH infection. When eating unwashed, uncooked fruit and vegetables were not significantly associated with STH infection. Strategic use of anti-helminthic, health education, and adequate sanitation, taking into account this epidemiologic information is helpful in the control of STH infections in Ethiopia.
Keywords: Ethiopia, meta-analysis, prevalence, risk factors, soil-transmitted helminthic infections, systematic review
Introduction
Soil-transmitted helminthes (STH) are among the leading causes of global health problems especially among the poorest and deprived communities where implementation of control measures is difficult. 1 Globally more than 2 billion people are infected by at least one of the commonest species namely: Ascaris lumbricoides (the roundworm), Trichuris trichiura (the whipworm) Strongyloides stercoralis (threadworm), and the hookworms; Ancylostoma duodenale and Necator americanus. 2 Recent estimates suggested that 819 million people worldwide are infected among A. lumbricoides, 465 million with T. trichiura, and 439 million with hookworm infection, 2 and 4 billion are at risk of infection. 3 More than 613 million school-age children in the world are at risk of STH infection. 3
Preschool-age children (PSAC), school-age children (SAC), 3 and women of reproductive age are WHO-identified risk groups. 4 School-age children between the ages of 5 to 15 in most developing countries are at the highest risk of chronic helminth infection and helminth-associated morbidities. 5 More than 568 million SAC live in areas where these parasites are intensively transmitted and require treatments. Although the global target is to eliminate morbidity due to STH infections in children by 2020, 3 these infections are still huge health problems in developing countries including Ethiopia affecting millions of SAC. Child under nutrition (mainly involving stunting, wasting, and underweight) has also been a serious global public health problem in the developing world including Ethiopia. 6
The prevalence of STH infection was 25.4% in Rwanda. 7 In a study done in South Asia Ascaris was the commonest STH identified with an overall prevalence of 18% followed by Trichuris 14% and hookworm 12%. 8 Hookworm prevalence was highest in Laos, Vietnam, and Cambodia. There was geographical overlap in countries with high prevalence rates for Trichuris and Ascaris (Malaysia, Philippines, Myanmar, Vietnam, and Bangladesh). When available data from school-aged children (SAC) were analyzed, the prevalence of Ascaris 25% and Trichuris 22%, were higher than among the general population while that of hookworm was 10%. 8 The pooled prevalence estimate of STH was 54.8% with A. lumbricoides had the highest prevalence of 44.6% while, T. trichiura, hookworms, and S. stercoralis recorded pooled prevalence estimate of 31.9%, 23.0%, and 3.4%, respectively in Nigeria. 9
Ethiopia is among sub-Saharan African countries with the highest-burden and where the disease remains an important public health problem particularly among school and pre-school age children. 10 The national prevalence of hookworms, A. lumbricoides, and T. trichiura in Ethiopia were 16%, 37%, and 30%, respectively. 11 In Ejaji (Shoa, Oromia) STHs were detected in 38.2% of the children, 17.9%, 16.5%, and 10.0% of the children were infected with the hookworms, A. lumbricoides and T. trichiura, respectively. 12 In a study done in Gena Bossa, the prevalence of STH was 38.3%. In Debre Tabor, the prevalence of STH was 11.8%, 7% of A. lumbricoides, 3.2% of hookworm, and 1.2% of T. trichiura. 13
Transmission results from ingestion of eggs and contact with fecally contaminated soil. A. lumbricoides and T. trichiura are primarily spread through fecal transmission (usually ingestion of parasite eggs in feces), whereas hookworm and S. stercoralis are through skin penetration of infective larvae. Poverty, poor environmental sanitation, unsafe human waste disposal systems, and lack of safe water supply, low socio-economic status of the country, poor personal hygiene, frequent outdoor exposures, and the presence of environmental conditions considered as risk factors for soil-transmitted helminthic infections. 14
In Ethiopia, singly there are a lot of research papers are available regarding the national magnitude of soil transmitted helminthic infections and associated risk factors in different parts of the country. In addition there are also few systematic review and meta-analysis evidences about prevalence and associated risk factors of STH in Ethiopia. However, the evidences were not recent and conducted in a single study setting (either school age children or pregnant women). Hence, due to absence of recent and comprehensive systemic review about prevalence of STH infections in Ethiopia, this meta-analysis was conducted in order to produce the pooled prevalence of soil transmitted helminthic infections and associated risk factors from available studies in Ethiopia.
Methods
Country profile
Ethiopia is located in the Horn of Africa and covers 1 104 300 km2. The total land area is 1 000 000 km2 (386 102 square miles). Five countries border to Ethiopia: Eritrea to the North, Djibouti, and Somalia to the East, Sudan and South Sudan to the West, and Kenya to the South. 15 The current population of Ethiopia is 113 881 451 in, 2020, based on Worldometer 16 elaboration of the latest United Nations data, which is equivalent to 1.47% https://www.worldometers.info/world-population/. About 21.3% of the population is urban (24 463 423) people in 2020. Economically, although Ethiopia has been labeled an “emerging third world nation,” it still is struggling. The economy depends greatly on agriculture, which is responsible for 43.2% of the Gross Domestic Product and 80% of the country’s exports. 15
Search strategy
The systematic review and meta-analysis were performed according to the Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) guidelines. We conducted an extensive search in PubMed, Google Scholar, Science direct, World Cat, and Cochrane Library. 17 The search terms were used separately and in combination using Boolean operators like “OR” or “AND.” By using core search terms and phrases, such as “soil-transmitted helminths” OR “nematode” OR “Necator” OR “Ancylostoma” OR “Ascaris” OR “Trichuris” “hookworm” OR “roundworm,” OR “Geo-helminths” OR “whipworm,” “Associated factor” AND Ethiopia Since it was one of the objectives of the study to determine the prevalence and distribution of STH infections across Ethiopia, study selection was restricted to studies with clearly stated sample sizes, the number of positive samples, and study locations as well as associated risk factors (conducted between December 1, 2019 and Junary13, 2020).
Criteria for inclusion and exclusion of studies
In this systematic review, different age groups like school-age children, pre-school-age children, pregnant women as well other groups from the community were involved. The articles collected through the searches were evaluated for inclusion in the meta-analysis based on the following criteria: (i) only studies containing primary data on STH, (ii) only studies conducted in the English language, (iii) cross-sectional studies, (iv) studies that reported prevalence and risk factors (v), and journals studied from 2009 to 2019 were included in the study; however, duplicate publications or extension of analysis from an original study were excluded and studies, where the full publication was obtained or completely lacked or incompletely presented needed raw data, were excluded from the study.
Data extraction
The data extraction protocol consists of the name of the country, study area, year of the study, type of study, sample size, age of participants, number of positive cases, species of STH parasites, and potential risk factors associated with individual species of STH, and diagnostic methods employed. If the year of the study did not state which year the study took place, the year of publication was used instead. Also, if the study was conducted over a range of years then the latest year of the stated range was used.
Quality assessment
The Grading of Recommendations Assessment, Development and Evaluation (GRADE) approach was used to assess the overall quality of evidence. 18 The quality of each study was declared using the 3 major assessment tools (methodological quality, comparability, and outcome and statistical analysis of the study). Two points were given to each criterion. Publications with a total score of 5 to 6 points were considered to be high, 4 points to be moderate, and 0 to 3 points to be low-quality publications. 18 The association between soil-transmitted helminth parasitic infections and associated risk factors was calculated in the form of the log odds ratio. The odds ratio was calculated for the common associated risk factors of the reported studies by using STATA version14 software.
Risk of publication bias
The risks of publication bias across studies were assessed using funnel plot symmetry and Egger’s test. Egger’s test (P-value < .05) was used to determine the presence of publication bias across studies.
Data analysis
The pooled prevalence of STH was calculated by dividing the total positive cases by the total study subjects included in this meta-analysis. Cochran’s Q test and I2 statistics were used to assess heterogeneity among the studies. 19 There was a clear heterogeneity in the prevalence of STH parasitic infections across studies included in this meta-analysis; we used a random-effects model to estimate the pooled effect size. To sort out the causes of heterogeneity, we conduct a subgroup analysis based on the region of the study, the nature of study participants, study year, and sample size included in individual studies. The presence of publication bias was assessed using Egger’s test and the symmetry of the funnel plot. The cause of publication bias was assessed using a sensitivity test and regression test. Forest plot format was used to present the pooled point prevalence with 95% CI. A log odds ratio was used to decide the association between associated risk factors and STH parasitic infections among respondents included in the studies. The meta-analysis was conducted using Stata software (version 14, Stata Corp, College Station, TX), where P < .05 was considered statistically significant.
Results
Literature search and selection
A total of 297 articles on the prevalence and associated risk factors of soil transmitted helminthic infections in Ethiopia were retrieved. Eighty-four of these articles were excluded due to duplicates. From the remaining 213 articles, 61 were excluded after review of their titles (titles were not related to soil transmitted helminthic infections) and 48 were excluded after review of abstracts (lack of full information about soil transmitted helminthic infections). The remaining 104 full-text articles were accessed and assessed for eligibility based on the inclusion criteria and information indicated in the data extraction protocol. As a result, 58 articles were further excluded in the data extraction protocol. From the remaining 46 articles 5 of them were removed due to lack OR, 95% CI, and the number of positive cases (meaning the report was only based on estimated prevalence percent). Thus, only 41 (13.8%) of the studies met the eligibility criteria and were included in the final systematic review and meta-analysis study (Figure 1).
Figure 1.
PRISMA flow diagram of articles considered for the review on STH infections among the Ethiopian population.
Characteristics of the eligible studies
Table 1 presents the characteristics of the studies meta-analyzed. Forty-one (41) studies were eligible and thus were included in the meta-analysis. Studies were conducted between 2009 and 2019 and all of them were cross-sectional studies. Fifteen, sixteen, and ten of the studies were carried out between 2009 and 2012, 2013 and 2015 as well as 2017 and 2019, respectively. This review is based on the criteria of 5 regions, such as Amhara (15 articles), Oromia (8 articles), Southern part of Ethiopia (13 articles) Tigray (4 articles), and from Harari one article were involved. Five studies were carried out within the hospital, another 5 were within the community, and 31 were in school settings. The prevalence of STH infections among eligible studies ranged between 0.47% and 74.3% (Table 1).
Table 1.
List and characteristics of 41 eligible studies.
| Author | Study year | Region | Study setting | Sample size | Case | Prevalence (95% CI) | Quality assessment |
|---|---|---|---|---|---|---|---|
| Alemu et al | 2009 | Amhara | School based | 319 | 138 | 43.3 (37.8-48.9) | 6 |
| Mekonnen et al | 2009 | Oromia | Community-based | 1021 | 600 | 58.8 (55.7-61.8) | 6 |
| Alelign et al | 2010 | Amhara | School-based | 384 | 211 | 54.9 (49.8-59.9) | 6 |
| Tekeste et al | 2010 | Amhara | School-based | 316 | 87 | 27.5 (22.7-32.8) | 4 |
| Adissu and Asmamaw | 2011 | Amhara | School-based | 365 | 76 | 20.8 (16.8-25.4) | 4 |
| Getachew et al | 2011 | Oromia | Hospital-based | 388 | 159 | 41.1 (36.0-46.0) | 6 |
| Teklemariam et al | 2011 | Tigray | School-based | 480 | 32 | 6.7 (4.6-9.3) | 5 |
| Abera and Nibert | 2012 | Amhara | School-based | 385 | 169 | 43.9 (38.9-49.0) | 6 |
| Abossie and Seid | 2012 | SNNPR | School-based | 400 | 290 | 72.5 (67.8-76.8) | 5 |
| Alemu et al | 2012 | SNNPR | School-based | 405 | 67 | 16.5 (13.1-20.5) | 5 |
| Debalke et al | 2012 | Oromia | School-based | 366 | 233 | 63.7 (58.5-68.6) | 5 |
| Gelaw et al | 2012 | Amhara | School-based | 304 | 36 | 11.8 (8.4-16.0) | 6 |
| Mathewos et al | 2012 | Amhara | School-based | 261 | 144 | 55.2 (48.9-61.3) | 4 |
| Terefe et al | 2012 | Harari | School-based | 644 | 3 | 0.47(0.001-0.01) | 5 |
| Ephrem et al | 2012 | Oromia | Community-based | 234 | 111 | 47.4 (40.9-54.0) | 4 |
| Seid et al | 2013 | Tigray | School-based | 442 | 29 | 6.6 (4.4-9.3) | 5 |
| Abdi et al | 2014 | Amhara | School-based | 408 | 273 | 66.9 (62.1-71.5) | 6 |
| Derso et al | 2014 | Amhara | Hospital-based | 384 | 53 | 13.8 (10.5-17.7) | 5 |
| Afework et al | 2014 | Amhara | School based | 384 | 252 | 65.6 (60.6-70.4) | 5 |
| Alemayehu and Tomass | 2014 | SNNPR | School-based | 374 | 278 | 74.3 (69.6-78.7) | 5 |
| Andualem | 2014 | Amhara | School based | 358 | 125 | 34.9 (29.9-40.1) | 5 |
| Shumbej et al | 2014 | SNNPR | Community-based | 377 | 88 | 23.3 (19.2-27.9) | 4 |
| Alemu et al | 2015 | Amhara | Community-based | 401 | 98 | 24.4 (20.3-28.9) | 5 |
| Emana et al | 2015 | Oromia | School based | 302 | 117 | 38.7 (33.2-44.5) | 6 |
| Samuel et al | 2015 | Oromia | School-based | 321 | 41 | 12.8 (9.3-16.9) | 6 |
| Tadege and Shimeli | 2015 | SNNPR | School-based | 374 | 197 | 52.4 (47.5-57.8) | 6 |
| Zerdo et al | 2015 | SNNPR | School-based | 410 | 165 | 40.4 (35.5-45.1) | 6 |
| Feleke and Jember | 2016 | Amhara | Hospital based | 783 | 459 | 58.6 (55.1-62.1) | 6 |
| Ibrahim et al | 2016 | Oromia | School based | 340 | 151 | 44.4 (39.0-49.9) | 5 |
| Mengist et al | 2016 | Oromia | Hospital-based | 372 | 92 | 24.7 (20.4-29.4) | 5 |
| Tekalign et al | 2016 | SNNPR | Community-based | 377 | 265 | 70.3 (65.4-74.9) | 6 |
| Alemu et al | 2017 | SNNPR | School-based | 391 | 121 | 30.9 (26.4-35.8) | 6 |
| Eyamo et al | 2017 | SNNPR | School-based | 384 | 200 | 52.0 (46.9-57.2) | 4 |
| Teshale et al | 2017 | Tigray | School-based | 410 | 26 | 6.3 (4.2-9.2) | 6 |
| Sitotaw et al | 2017 | Amhara | School-based | 406 | 63 | 15.5 (12.1-19.4) | 6 |
| Weldesenbet et al | 2017 | SNNPR | School-based | 600 | 57 | 9.5 (6.5-11.2) | 5 |
| Alemu et al | 2018 | SNNPR | School-based | 351 | 70 | 19.9 (15.9-24.5) | 6 |
| YarinbabErgat and Darcha | 2018 | SNNPR | School based | 303 | 116 | 38.3 (32.8-44.0) | 4 |
| Gebrehiwet et al | 2018 | Tigray | Hospital-based | 448 | 241 | 53.4 (49.0-58.5) | 5 |
| Molla and Mamo | 2018 | SNNPR | School-based | 443 | 239 | 54 (49.2-58.7) | 6 |
| Workineh et al | 2019 | Amhara | School based | 340 | 45 | 13.2 (9.8-17.3) | 6 |
Quality of studies included in the meta-analysis
The quality score of each original study ranged between 4 and the highest 6 (Table 1). The overall quality of the articles included in this meta-analysis is very good.
Risk of publication bias across studies included in the meta-analysis
The funnel plot symmetry demonstrates the presence of publication bias among studies included in this meta-analysis (Figure 2). Similarly, the Egger’s test results (P < .05) indicate publication bias among studies.
Figure 2.
Funnel plot indicate publication bias across studies in this meta-analysis.
Pooled prevalence of soil-transmitted helminthic infections
A random-effects model was employed to estimate the pooled prevalence of STH infections in Ethiopia. The overall national prevalence of STH infections was 36.78% (95% CI: 28.79-44.77) (Figure 3).
Figure 3.
Forest plot for the overall prevalence of STH infections in Ethiopia.
Subgroup analysis
High pooled prevalence of STH infection was reported from SNNPR 42.61% (95% CI: 29.20-56.01), followed by Oromia 41.43% (95% CI: 28.02-54.85) and Amhara 36.64% (95% CI: 26.12-47.16), whereas the low prevalence of STH infections was observed in Harar 0.47% (95% CI: 0.10-1.36) followed by Tigray region 18.08% (95% CI: 3.30-32.87) (Figures 3 and 4).
Figure 4.
Regional distribution of STH in Ethiopia.
In the study setting highest pooled prevalence estimate was 44.84% (95% CI: 26.14-63.53) in the community-based studies followed by hospital-based studies 38.31% (95% CI: 20.03, 56.59) and the least was 35.22% (95% CI: 26.89-43.56) in school-based studies (Figure 5).
Figure 5.
The overall prevalence of STH s in Ethiopia by study nature (participants).
In the study period the highest pooled prevalence estimate was recorded between 2013 and 2016; 40.73% (95% CI: 28.79-52.66) followed by the study period between 2009 and 2012 with pooled prevalence estimate was 37.59% (95% CI: 23.47, 51.72) and the least was recorded in between 2017 and 2019; 29.21% (95% CI: 17.94, 40.48) (Figures 6–8).
Figure 6.
Pooled prevalence of STH infections from 2009 to 2012.
Figure 7.
Pooled prevalence of STH infections from 2013 to 2016.
Figure 8.
Pooled prevalence of STH infections from 2017 to 2019.
Common STH infections in Ethiopia
A. lumbricoides had the highest pooled prevalence estimate of 17.63% (95% CI: 14.30-20.96) followed by hookworms 12.35% (95% CI: 9.91-14.79), T. trichiura 7.24% (95% CI: 5.84-8.63) and S. stercoralis 2.16% (95% CI: 0.97-3.35), respectively (Figures 6–9).
Figure 9.
Prevalence of A. lumberecoides.
Figure 10.
Prevalence of hookworm.
Figure 11.
Prevalence of Trichuris trichura.
Factors associated with STH infections in Ethiopia
In this Meta-analysis, we have reviewed several potential risk factors associated with STH infections in Ethiopia. Age, sex, residence, open field defecation, lack of hand washing habit, the habit of eating raw and unwashed fruit and vegetables, shoe wearing habits, family education level, and fingernail trimming and cleanness habits were associated with STH infections.
The association between age and STH infection in people of Ethiopia was computed from 14 studies (1, 3, 8, 12, 14, 22, 27-29, 33, 35, 37, 38, 41). Age (children up to 14 years) was significantly associated with the prevalence of STH parasitic infections. The odds of having STH in children (up to 14 years) were 2.23 times higher than those in adults (95% CI: 1.68-2.77) (Figure 13).
Figure 13.
Pooled prevalence OR of age.
Figure 14.
Pooled prevalence in sex.
The association between residence and STH infections was analyzed from 5 studies (11, 20, 21, 28, and 41). People who live in a rural setting were 1.22 times (95% CI: 0.00-2.44) more likely to be infected with STH parasitic infections than people who live in urban areas (Figure 12). The pooled results of 18 studies (3, 7, 8, 9, 12, 18, 21-24, 26, 28, 33-35, 37, 39, 41) showed that lack of handwashing habits were strongly associated with infection with STH infections in Ethiopia. The odds of having STH parasitic infections was 3.16 times (95% CI: 2.05-4.27) higher among people who did not wash their hands after defecation than people who wash their hands (Figure 15).
Figure 12.
Prevalence of S. stercoralis.
Figure 15.
Pool prevalence of residence.
Figure 16.
Lack of handwashing habits.
The association between the habits of eating raw, unwashed fruits and vegetables with STH parasitic infections was evaluated from 6 studies (26, 28, 30-32, 35). But in this study people who had habits of eating raw, unwashed fruits and vegetables are not significantly associated with STH (Figure 17). The association between fingernail trimming and cleanness habits and STH parasitic infection in the people of Ethiopia was computed from 7 studies (7, 8, 15, 22, 29, 33, 41). The pooled results showed that individuals with poor fingernail trimming and cleanness habits were 1.28 times (95% CI: 0.65-1.91) more likely to be infected with STH parasitic infection than their counterparts (Figure 18).
Figure 17.
Habits of eating raw, unwashed fruits, and vegetables.
Figure 18.
Pooled of untrimmed fingernail.
The association between family education level and STH parasitic infection in the people of Ethiopia was computed from 4 studies (21, 28, 30, 34). The pooled results showed that uneducated families were 1.76 times (95% CI: 0.17-3.35) more likely to have STH parasitic infections than those who were educated (Figure 19). The pooled results of 9 studies (3, 8, 17, 21, 23, 28, 35, 38, 39) showed that lack of shoe-wearing habits was strongly associated with STH parasitic infection among people in Ethiopia. In the analysis lack of shoe-wearing habits in the people were 2.52 times (95% CI: 1.22-3.82) more likely to be infected with STH parasitic infections than who had the habit of wearing shoe (Figure 20).
Figure 19.
Family education level.
Figure 20.
Lack of shoe-wearing habit.
The association between open field defecation and intestinal protozoan parasitic infection among people in Ethiopia was conducted in 14 studies (7, 9, 16, 21, 24, 26, 28-31, 34, 35, 38, 41). People who practiced open field defecation were 2.25 times (95% CI: 1.44-3.06) more likely to have STH parasitic infections than those who did not practice open field defecation (Figure 21).
Figure 21.
Open field defecation.
Discussion
The present study was designed to complement global efforts toward the control of neglected tropical diseases by providing useful epidemiological data that will aid their control. The study provides information on endemic species of STHs, their national and regional prevalence, their distribution with regions, species, periods, and settings. The findings will (i) help in assessing successes of sporadic STHs control programs in Ethiopia which usually target children and pregnant women (ii) provide information that will serve as a guide for targeted and cost-effective control which is a subject of debate globally. 20
The overall pooled prevalence of STH parasitic infection in the present study was 36.78%. The study was following the result in Chencha town 36.8% 21 and Gena Bossa 38.3%. 22 The result was higher than the report in Rwanda 25.4%. 7 However, the prevalence was less than 54.8% 9 reported in Nigeria and Indonesia at 57.4%. 23 This variation could be due to the topographic and study period difference in which the communities would improve their living standard, personal and environmental hygiene through time.
From regions the highest pooled prevalence estimate of STH was 42.61% in Southern Ethiopia. The finding in Nigeria with the prevalence of STH was 54.8%. 9 The result in Rwanda STH infections was 65.8%. 24 On the other hand, the result was greater than the report in Cameroon 24.1%, 25 and the result in Nigeria 8.3%. 26 This variation may be due to environmental factors such as temperature, humidity, soil moisture, and rainfall. Other factors may be differences in levels of hygiene and sanitation, environmental contamination 27 as well as the specificity and sensitivity of the diagnostic methods employed by the individual studies. This suggests that this region may be the most endemic for STHs in Ethiopia. Since cost-effective control requires knowledge of the community for the correct choice of anthelmintic strategy, this information may be useful for stakeholders in STHs control. The lower prevalence was 0.47% reported in the Hareri region. The finding was almost similar to the result in central Kenya 0.2%. 28 The low prevalence may be attributable to the extremely high temperature in these regions which may not support the environmental survival of eggs and larvae of these parasites.
Studies carried out in communities and in hospitals other than school-based were recorded the highest pooled prevalence estimates probably due to the sporadic STHs control programs in Ethiopia, which usually target school and hospitalized children. However, the burden of these parasites is not restricted to children. 9
In the study period 2009 to 2012 (37.59%) pooled prevalence estimate was recorded; however, the average coverage increases from 2003 to 2013 as a trend in the region of Southeast Asia. 29 This may be due to limited access of mass drug administration to different areas and lack of awareness creation to the society. The pooled prevalence was increased between 2013 and 2016 (40.73%); this can be mass drug administration was not given properly and the stakeholders gave less attention to the infection. However, in the period from 2017 to 2019, the pooled prevalence estimate was (29.21%) which is less than the other study periods. This might be due to awareness creation of the societies, access to education to school children, and proper mass drug deworming programs for school-age children.
The species of STH infection reported in Ethiopia during the period under review are similar to those reported in other sub-Saharan African countries like Kenya. 30 This finding shows that these parasites are still endemic in the region suggesting that extra efforts are required to achieve the WHO’s goal of eradication in sub-Saharan Africa by 2020.
A. lumbricoides was the most prevalent species 17.8% of STHs reported during the period under review which is in agreement with the study in South Asia 18%, 8 in South Africa 18.3% 31 and the study in Ejaji Ethiopia 16.5%. 12 But, it is greater than the study in Debre Tabor the prevalence of 7% of A. lumbricoides. 13 The high prevalence of A. lumbricoides observed by the present study may be attributable to high environmental contamination resulting from a large number of infected people, the durability of Ascaris eggs under varying environmental conditions 32 the high fecundity 33 as well as the sticky nature of the shell of Ascaris egg 34 which aids its attachment on human hands, fruits, and vegetables.
In the current study pooled prevalence estimate of hookworm was 12.4%. This result was comparable with the study done in Arba Minch Zuria district, the prevalence was 14.5%. 35 However, the result was greater than the report in Debre Tabor 3.2% 13 and the report from Babile 6.7%. 36 On the contrary to the present finding, higher rates of hookworm were reported near Lake Awassa 62.5%, 37 Langano 64.7%, 38 and Southwest Ethiopia 40.8%. 39 This variation might be due to altitude, environmental, socio-economic, and behavioral differences of the residences.
The pooled prevalence estimate of T. trichiura was 7.24% in this study and this is in line with the result in Ejaji 10.0% 12 and the study in Yirgacheffe 7.2%. 40 Nevertheless, the result was greater than the result conducted in rural areas of southern Thailand at 2.1%, 41 in rural western Uganda 0.2%, 42 and Maytsbri 2.2%. 43 On the contrary, the result was lower than the study conducted in South Asia (14%) 8 and Nigeria 31.9%. 9 This difference could be due to the environmental and study period difference. People living in tropical and subtropical areas of the world are at the highest risk of infection by T. trichiura. In addition to this populations without reliable access to safe water and sanitation elsewhere are also at increased risk of this infection.
In this study the prevalence of S. strecoralies was 2.16%. And the result is in agreement with the study in Nigeria 3.4%. 9 The study done in Gena Bossa Ethiopia 3.3% 22 and the result reported from Bahir Dar town is 2.6% 44 However, it was lower than the result in Mecha town 7.5%. 45 The low prevalence of S. stercoralis may be due to its’ peculiar characteristics that require different diagnostic methods than other STH, and for this reason, is frequently not identified.
Associated risk factors of soil-transmitted helminths
The AOR of age that is associated with soil-transmitted helminth parasitic infection in the Meta-analysis was 2.23 (95% CI: 1.68-2.77) (1, 3, 8, 12, 14, 22, 27-29, 33, 35, 37, 38, 41). This finding was in agreement with the findings in Umolante district (Southern Ethiopia) 46 infections are more prevalent in the age groups 10 to 14 years in the study area. This is an indication that younger children are more exposed since they usually play in the open fields 47 and they frequently involve themselves fully in activities that bring them in contact with the source of infection. 48 Another study conducted elsewhere also showed the highest infection rates among the age groups 5 to 14 years. 49 However, a report from Mizan Aman town has shown that younger children were more infected with intestinal parasites. 50 This is perhaps, children in these age groups are more engaged in outdoor activities like farming as a result they have more exposure to those STH parasitic infections.
The AOR of sex in the current systematic review was 0.88 (95% CI: 0.39-1.37) (7, 11, 14, 21, 31, 41). This finding was in line with the finding in the Umolante district (Southern Ethiopia) 46 and Jimma town. 51 This might be due to environmental factors, such as frequent exposure of an individual to the soil, the probability to contact with fecal materials, lack of safe water supply, and poverty.
Besides, people who live in a rural setting were having an AOR of 1.22 (95% CI: 0.00, 2.44) (11, 20, 21, 28, 41). The result was similar to the result in Sekela Primary School, Western Ethiopia 52 and with the report in Brazil. 53 This could be due to the reason that rural people have less access to water, lack of environmental sanitation, and poor personal hygiene.
Among associated risk factors, hand washing habit before the meal was 3.16 (95% CI: 2.05-4.27) folds higher among people that didn’t have regular hand washing habit (3, 7, 8, 9, 12, 18, 21-24, 26, 28, 33-35, 37, 39, 41). This finding was in line with the previous study conducted in Nigeria, 54 in Indonesia, 23 in Sekela Primary School, Western Ethiopia, 52 and in Bazou (West Cameroon) lack of hand washing habit before the meal was also reported as a risk factor for STH infection. 55 This might be due to the reason that proper hand washing practices break the chain of transmission for soil-transmitted helminthic parasitic infection.
Concerning the odd ratio of eating raw and unwashed fruits and vegetables is 1.88 times (95% CI: 1.45-2.31) greater from people eating cooked and washed fruit and vegetables (26, 28, 30-32, 35). But not significantly associated with STH. The result is following the result in Sekela Primary School, Western Ethiopia, 52 and the results in Birbir town. 56 This could be due to washing fruits and vegetables before consumption reduces the risk of acquiring parasitic infection.
The association between fingernail trimming and cleanness habits and STH parasitic infection in the people of Ethiopia was computed from 7 studies (7, 8, 15, 22, 29, 33, 41). The pooled results showed that individuals with poor fingernail trimming and cleanness habits were 1.28 times (95% CI: 0.65-1.91) more likely to be infected with STH parasitic infection than their counterparts. This finding is in agreement with the result in Sekela Primary School, Western Ethiopia, 52 and the finding in Tilili town. 57 This is probably due to lack of awareness, poor hygiene practice, and socio-demographic factors of the people.
The association between family education level and STH parasitic infection in the people of Ethiopia was computed from 4 studies (21, 28, 30, 34). The pooled results showed that uneducated families were 1.76 times (95% CI: 0.17-3.35) more likely to have soil-transmitted helminth parasitic infections than those who were educated. The finding is almost similar to the result in Sekela Primary School, Western Ethiopia, 52 the finding in Kenya, 58 and the result in East Wollega. 59 This might be due to educated family aware their children to practice personal hygiene, not to play with soil, hand washing practice before a meal and after defecation.
The pooled results of 9 studies (3, 8, 17, 21, 23, 28, 35, 38, 39) showed that lack of shoe-wearing habits was strongly associated with STH parasitic infection among people in Ethiopia. In the analysis lack of shoe-wearing habits in the people were 2.52 times (95% CI: 1.22-3.82) more likely to be infected with STH parasitic infections than those who had the habit of wearing a shoe. This finding was similar to the study finding from Sekela Primary School, Western Ethiopia, 52 and the result in Motta town. 60 This could be primarily due to poverty, frequent outdoor exposures, and the presence of environmental conditions in the country. 14
Moreover, people who did not have private latrine were 2.25 times (95% CI: 1.44-3.06) more likely to be infected by STH infections when compared to those who possess private latrines (1, 2, 4, 6, 9, 10, 18, 19, 20, 26, 27, 28, 30, 31). This finding was in agreement with findings in Indonesia 23 ) and the study conducted in South Western Cameroon 61 also showed that open defecation is a risk factor for STH infections. This might be due to the absence of latrines that exposed people to parasites because of the existing improper defecation system.
Limitation of the Study
There are potential limitations to this study. The data were obtained from 5 regions of Ethiopia (Amhara, Harari, Oromia, SNNPR, and Tigray regions) and even small numbers of studies were taken from each region. However, there is a lack of published studies from Afar, Gambela, Benshangul gumuz, and Somali regions which in turn may not fully represent the prevalence of soil-transmitted helminths and associated risk factors in Ethiopia. The other limitation of this study was an inability to directly compare studies due to the differences in diagnostic techniques.
Conclusions and Recommendations
STH infections are greatly prevalent and well distributed across Ethiopia and within the community; hospital and school settings with the highest prevalence reported in community-based studies. A. lumbricoides was the most prevalent of the STH species. The Pooled prevalence estimates of STH in Ethiopia were the most prevalent in the study area SNNPR and from 2013 to 2016. Among associated risk factors, hand washing habit before the meal was 3.16 folds higher among people that didn’t have regular hand washing habit. Moreover, People who did not wear shoes always were 2.52 times more likely to be infected with STH than their counterparts. We recommended to the Ethiopian government Community-based strategic drug administration than school-based and its effective implementation is vital to the control of soil-transmitted helminthic infections. Although the infection is common to all age groups, pregnant women and children need special attention. We also recommended that improved personal and environmental sanitation, health education, and good handling of affected individuals are very important for the control of soil-transmitted helminthic infections.
Footnotes
Declaration of conflicting interests: The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding: The author(s) received no financial support for the research, authorship, and/or publication of this article.
Availability of Data and Materials: The data set in this study is available from the corresponding author on reasonable request.
ORCID iD: Gedam Tola
https://orcid.org/0000-0002-9179-6408
References
- 1. Mascarini-Serra L. Prevention of soil-transmitted helminth infection. J Glob Infect Dis. 2011;3:175-182. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2. Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors. 2014;7:37. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3. World Health Organization. Soil-Transmitted Helminthiases: Eliminating as Public Health Problem Soil-Transmitted Helminthiases in Children: Progress Report 2001-2010 and Strategic Plan 2011-2020. WHO; 2012. [Google Scholar]
- 4. World Health Organization. Guideline: Preventive Chemotherapy to Control Soil-Transmitted Helminthic Infections in at-Risk Population Groups. WHO; 2017. [PubMed] [Google Scholar]
- 5. Gyorkos TW, Gilbert NL. Blood drain soil-transmitted helminths and anemia in pregnant women. PLoS Negl Trop Dis. 2014;8:e2912. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6. Tariku A, Woldie H, Fekadu A, Adane AA, Ferede AT, Yitayew S. Nearly half of preschool children are stunted in Dembia district, northwest Ethiopia: a community based cross-sectional study. Arch Public Health. 2016;74:13. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7. Staudacher O, Heimer J, Steiner F, et al. Soil-transmitted helminths in southern highland Rwanda: associated factors and effectiveness of school-based preventive chemotherapy. Trop Med Int Health. 2014;19:812-824. [DOI] [PubMed] [Google Scholar]
- 8. Silver ZA, Kaliappan SP, Samuel P, et al. Geographical distribution of soil transmitted helminths and the effects of community type in South Asia and South East Asia – aa systematic review. PLoS Negl Trop Dis. 2018;12:e0006153. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9. Karshima SN. Prevalence and distribution of soil-transmitted helminth infections in Nigerian children: a systematic review and meta-analysis. Infect Dis Poverty. 2018;7:69. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10. Gashaw F, Aemero M, Legesse M, et al. Prevalence of intestinal helminth infection among school children in Maksegnit and Enfranz towns, northwestern Ethiopia, with emphasis on Schistosoma mansoni infection. Parasit Vectors. 2015;8:567. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11. Tadesse Z, Hailemariam A, Kolaczinski JH. Potential for integrated control of neglected tropical diseases in Ethiopia. Trans R Soc Trop Med Hyg. 2008;102:213-214. [DOI] [PubMed] [Google Scholar]
- 12. 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. J Infect Dev Ctries. 2018;12:1134-1141. [DOI] [PubMed] [Google Scholar]
- 13. 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. J Parasitol Res. 2020;2020:2521750. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14. Adefioye O, Efunshile A, Ojurongbe O, et al. Intestinal helminthiasis among school children in Ilie, Osun state, southwest, Nigeria. Sierra Leone J Biomed Res. 2011;3:43-48. [Google Scholar]
- 15. Dean C. Implementation of Culturally Sensitive and Informed Health Education as a Part of the ‘Wash Approach’ to Controlling Soil-Transmitted Helminth Infections in the Rural Village of Bati Kelo, East Shewa Zone. Adama Wereda; 2017. [Google Scholar]
- 16. Worldometers. https://www.worldometers.info/world-population/ethiopia-population/2020.
- 17. Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6:e1000097. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18. Atkins D, Eccles M, Flottorp S, et al. Systems for grading the quality of evidence and the strength of recommendations I: critical appraisal of existing approaches the GRADE working group. BMC Health Serv Res. 2004;4:38. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19. Rücker G, Schwarzer G, Carpenter JR, Schumacher M. Undue reliance on I2 in assessing heterogeneity may mislead. BMC Med Res Methodol. 2008;8:79. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20. Turner HC, Truscott JE, Hollingsworth TD, Bettis AA, Brooker SJ, Anderson RM. Cost and cost-effectiveness of soil-transmitted helminth treatment programmes: systematic review and research needs. Parasit Vectors. 2015;8:355. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21. Zerdo Z, Yohanes T, Tariku B. Soil-transmitted helminth reinfection and associated risk factors among school-age children in Chencha district, southern Ethiopia: a cross-sectional study. J Parasitol Res. 2016;2016:4737891. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22. 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. J Trop Dis. 2019;5:2. [Google Scholar]
- 23. Pasaribu AP, Alam A, Sembiring K, Pasaribu S, Setiabudi D. Prevalence and risk factors of soil-transmitted helminthiasis among school children living in an agricultural area of north Sumatera, Indonesia. BMC Public Health. 2019;19:1066. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24. Rujeni N, Morona D, Ruberanziza E, Mazigo HD. Schistosomiasis and soil-transmitted helminthiasis in Rwanda: an update on their epidemiology and control. Infect Dis Poverty. 2017;6:8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25. Tchuem Tchuenté LA, Kamwa Ngassam RI, Sumo L, et al. Mapping of schistosomiasis and soil-transmitted helminthiasis in the regions of Centre, east and west Cameroon. PLoS Negl Trop Dis. 2012;6:e1553. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26. Adewale B, Rahaman O, Aina O, Sulyman MA. Schistosoma mansoni and soil transmitted helminth (STH) infections among pregnant women attending primary health care facilities in Lagos mainland, Nigeria. J Biosci Med. 2018;06:64-70. [Google Scholar]
- 27. Cundill B, Alexander N, Bethony JM, Diemert D, Pullan RL, Brooker S. Rates and intensity of re-infection with human helminths after treatment and the influence of individual, household, and environmental factors in a Brazilian community. Parasitology. 2011;138:10.1017/S0031182011001132-10.1017/S0031182011001416. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28. Masaku J, Mutungi F, Gichuki PM, Okoyo C, Njomo DW, Njenga SM. High prevalence of helminths infection and associated risk factors among adults living in a rural setting, central Kenya: a cross-sectional study. Trop Med Health. 2017;45:15. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29. Dunn JC, Turner HC, Tun A, Anderson RM. Epidemiological surveys of, and research on, soil-transmitted helminths in Southeast Asia: a systematic review. Parasit Vectors. 2016;9:31. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30. Kepha S, Nuwaha F, Nikolay B, et al. Epidemiology of coinfection with soil transmitted helminths and Plasmodium falciparum among school children in Bumula district in western Kenya. Parasit Vectors. 2015;8:314. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31. Sacolo-Gwebu H, Chimbari M, Kalinda C. Prevalence and risk factors of schistosomiasis and soil-transmitted helminthiases among preschool aged children (1–5 years) in rural KwaZulu-Natal, South Africa: a cross-sectional study. Infect Dis Poverty. 2019;8:47. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32. O’Lorcain P, Holland CV. The public health importance of Ascaris lumbricoides. Parasitology. 2000;121 Suppl:S51-S71. [DOI] [PubMed] [Google Scholar]
- 33. Hall A, Holland C. Geographical variation in Ascaris lumbricoides fecundity and its implications for helminth control. Parasitol Today. 2000;16:540-544. [DOI] [PubMed] [Google Scholar]
- 34. Quilès F, Balandier JY, Capizzi-Banas S. In situ characterisation of a microorganism surface by Raman microspectroscopy: the shell of Ascaris eggs. Anal Bioanal Chem. 2006;386:249-255. [DOI] [PubMed] [Google Scholar]
- 35. Alemu G, Aschalew Z, Zerihun E. Burden of intestinal helminths and associated factors three years after initiation of mass drug administration in Arbaminch Zuria district, southern Ethiopia. BMC Infect Dis. 2018;18:435. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36. Yami A, Mamo Y, Kebede S. Prevalence and predictors of intestinal helminthiasis among school children in Jimma zone; a cross-sectional study. Ethiop J Health Sci. 2011;21:167-174. [PMC free article] [PubMed] [Google Scholar]
- 37. Merid Y, Hegazy M, Mekete G, Teklemariam S. Intestinal helminthic infection among children at Lake Awassa area, south Ethiopia. Ethiop J Health Dev. 2001;15:1. [Google Scholar]
- 38. Legesse M, Erko B. Prevalence of intestinal parasites among school children in a rural area close to the southeast of Lake Langano, Ethiopia. Ethiop J Health Dev. 2005;18:116-120. [Google Scholar]
- 39. Demissie F, Petros B, Kebede A. Hookworm species distribution among school children in Asendabo town, Jimma Zone, South West Ethiopia. Ethiop J Health Sci. 2008;18. [Google Scholar]
- 40. Molla E, Mamo H. Soil-transmitted helminth infections, anemia and undernutrition among schoolchildren in Yirgacheffee, South Ethiopia. BMC Res Notes. 2018;11:585. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41. Kache R, Phasuk N, Viriyavejakul P, Punsawad C. Prevalence of soil-transmitted helminth infections and associated risk factors among elderly individuals living in rural areas of southern Thailand. BMC Public Health. 2020;20:1882. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42. Ojja S, Kisaka S, Ediau M, et al. Prevalence, intensity and factors associated with soil-transmitted helminths infections among preschool-age children in Hoima district, rural western Uganda. BMC Infect Dis. 2018;18:408. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43. Gebrehiwet MG, Medhaniye AA, Alema HB. Prevalence and associated factors of soil transmitted helminthes among pregnant women attending antenatal care in Maytsebri primary hospital, north Ethiopia. BMC Res Notes. 2019;12:644. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44. Derso A, Nibret E, Munshea A. Prevalence of intestinal parasitic infections and associated risk factors among pregnant women attending antenatal care center at Felege Hiwot Referral Hospital, northwest Ethiopia. BMC Infect Dis. 2016;16:530. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45. Elfu Feleke B. Epidemiology of hookworm infection in the school-age children: a comparative cross-sectional study. Iran J Parasitol. 2018;13:560-566. [PMC free article] [PubMed] [Google Scholar]
- 46. Alemu M. Prevalence of intestinal schistosomiasis and soil transmitted helminthiasis among primary school children in Umolante district, South Ethiopia. Clin Med Res. 2014;3:174-180. [Google Scholar]
- 47. Dejene T, Asmelash T. Impact of irrigation on the prevalence of intestinal parasite infections with emphasis on schistosomiasis in Hintallo-Wejerat north Ethiopia. Ethiop J Health Sci. 2008;18:33-38. [Google Scholar]
- 48. Okpala H, Agwu I, Chimezie O, Nwobu G, Ohihoin A. Survey of the prevalence of schistosomiasis among pupils in Apata and Laranto areas in Jos, Plateau state. Online J Health Allied Sci. 2004;1:1. [Google Scholar]
- 49. Kurup R. Control of intestinal parasites among children in two communities of south Saint Lucia. J Rural Trop Public Health. 2010;9:95-100. [Google Scholar]
- 50. Jejaw A, Zemene E, Alemu Y, Mengistie Z. High prevalence of Schistosoma Mansoni and other intestinal parasites among elementary school children in southwest Ethiopia: a cross-sectional study. BMC Public Health. 2015;15:600. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 51. Debalke S, Worku A, Jahur N, Mekonnen Z. Soil transmitted helminths and associated factors among schoolchildren in government and private primary school in Jimma town, southwest Ethiopia. Ethiop J Health Sci. 2013;23:237-244. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52. Tolera A, Dufera M. The prevalence of soil-transmitted helminths and associated risk factors among school children at Sekela primary school, western Ethiopia. J Parasitol Res. 2020;2020:8885734. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 53. Carneiro FF, Cifuentes E, Tellez-Rojo MM, Romieu I. The risk of Ascaris lumbricoides infection in children as an environmental health indicator to guide preventive activities in Caparaó and Alto Caparaó, Brazil. Bull World Health Organ. 2002;80:40-46. [PMC free article] [PubMed] [Google Scholar]
- 54. Amuta EU, Houmsou RS, Mker SD. Knowledge and risk factors of intestinal parasitic infections among women in Makurdi, Benue state. Asian Pac J Trop Dis med. 2010;3:993-996. [Google Scholar]
- 55. Tchakounté BN, Nkouayep VR, Poné JW. Soil contamination rate, prevalence, intensity of infection of geohelminths and associated risk factors among residents in Bazou (west Cameroon). Ethiop J Health Sci. 2018;28:63-72. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 56. 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 Infect Dis. 2019;19:270. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57. Abera A, Nibret E. Prevalence of gastrointestinal helminthic infections and associated risk factors among schoolchildren in Tilili town, northwest Ethiopia. Asian Pac J Trop Dis Med. 2014;7:525-530. [DOI] [PubMed] [Google Scholar]
- 58. McClure EM, Meshnick SR, Mungai P, et al. The association of parasitic infections in pregnancy and maternal and fetal anemia: a cohort study in coastal Kenya. PLoS Negl Trop Dis. 2014;8:e2724. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59. Mengist HM, Zewdie O, Belew A. Intestinal helminthic infection and anemia among pregnant women attending antenatal care (ANC) in East Wollega, Oromia, Ethiopia. BMC Res Notes. 2017;10:440. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 60. Andualem Asemahagn M. Parasitic infection and associated factors among the primary school children in Motta town, western Amhara, Ethiopia. Am J Public Health Res. 2014;2:248-254. [Google Scholar]
- 61. Tabi ESB, Eyong EM, Akum EA, Löve J, Cumber SN. Soil-transmitted helminth infection in the Tiko health district, South West region of Cameroon: a post-intervention survey on prevalence and intensity of infection among primary school children. Pan Afr Med J. 2018;30:74. [DOI] [PMC free article] [PubMed] [Google Scholar]





















