Prevalence and Associated Risk Factors of Human Intestinal Helminths Parasitic Infections in Ethiopia: A Systematic Review and Meta-Analysis

Background Intestinal helminth infections are still public health problems in tropical and subtropical countries including Ethiopia. This review and meta-analysis aimed to produce the pooled prevalence and associated risk factors of human intestinal helminth parasitic infections (HIHPIs) in Ethiopia. Methods Articles written in English were searched from online databases. Sixty-seven studies were included. Meta-analysis was computed using STATA version 14. Result The pooled prevalence of HIHPIs was (33.35%, 95% CI: 28.85%, 37.86%). Ascaris lumbricoides (10.84%, 95% CI: 9.34, 12.34), hookworm spp. (8.89%, 95% CI: 7.75, 10.04), Schistosoma mansoni (4.22%, 95% CI: 3.64, 4.81), Trichuris trichiura (2.51%, 95% CI: 2.17, 2.86), Hymenolepis nana (2.29%, 95% CI: 1.96, 2.63), Taenia species (1.01%, 95% CI: 0.80, 1.22), Strongyloides stercoralis (1.17%, 95% CI: 0.92, 1.41), and Enterobius vermicularis(0.71%, 95% CI: 0.52, 0.90) were recorded. Handwashing before food (OR: 5.22,95% CI: 3.49, 6.94), handwashing after toilet (OR: 3.03, 95%; CI: 1.01, 5.05), age (OR: 1.66, 95% CL. 1.09, 2.23), open defecation (OR: 2.42, 95% CI: 1.60, 3.24), eating raw and unwashed vegetables/fruits (OR: 1.98, 95%; CI: 1.30, 2.66), maternal education (OR: 1.81, 95% CI: 0.91, 2.72), family income (OR: 2.00, 95% CI: 0.87, 3.31), source of drinking water (OR: 3.12, 95% CI: 1.96, 4.27), swimming/contact with river water (OR: 1.90, 95% CI: 1.11, 2.69), barefoot (OR: 3.28, 95% CI: 1.67, 4.88), playing with soil (OR: 2.64, 95% CI: 1.40, 3.88), and family size (OR: 3.75, 95% CI: 2.03, 5.46) were factors associated with HIHPIs in Ethiopia. High heterogeneity of the prevalence of HIHPIs was observed among the studies within and among regions (I2 > 99.6% and P ≤ 0.001). Conclusion HIHPIs in Ethiopia were significantly high. Therefore, special attention should be given by all stakeholders to minimize HIHPIs in Ethiopia.


Background
Parasitic infections caused by intestinal helminths are among the most prevalent global infections, especially in developing countries [1,2]. e global annual burden of parasitic infections reaches 3.5 billion. Intestinal parasitic infections (IPIs) account for over 450 million annual morbidities and 200,000 mortalities [3]. Intestinal helminths (IHs) are among such infections that need special emphasis in developing countries [4]. ey result in two billion global infections; Ascariasis (250 million), Schistosomiasis (200 million), hookworm (151 million), and Strongyloidiasis (100 million) [5]. Trichuriasis, another helminth disease, also infects around 800 million people worldwide [6]. e most frequent intestinal helminths in Ethiopia are A. lumbricoides, hookworm spp., S. mansoni, H. nana, T. trichiura, E. vermicularis, S. stercoralis, and Taenia species [7]. Infections with these parasites usually lead to nutritional depletion, poor immunity in infants, mucosal loss and lymphatic leakage, and local hemorrhages [8]. eir associated factors are difficulties in adopting optimal personal hygienic practices, shoe-wearing habit, lack of clean and safe water, high population density, poor waste disposal, noncompliance with health standards, poor postdefecation handwashing, incorrect fingernail trimming, and eating raw meat/vegetables [1,[8][9][10]. Many studies have been conducted to determine the prevalence and associated risk factors of HIHPIs among people in different parts of Ethiopia. However, the prevalence reflected in these small and fragmented studies varied widely and remained inconclusive. Additionally, there is no nationwide study about the prevalence and factors associated with HIHPIs among the people in Ethiopia. erefore, this review and metaanalysis aimed to determine the pooled prevalence and associated risk factors of HIHPIs among the people of Ethiopia.

Study Design and
Setting. Ethiopia is located in the horn of Africa bounded by North and South Sudan on the west, Somalia and Djibouti on the East, Eritrea on the North and northwest, and Kenya on the South [11]. Ethiopian population is estimated to be 113,869,098. is population is equivalent to 1.47% of the global population. About 21.3% (24,463,423) of the Ethiopian population lives in urban areas. e country's population has a median age of 19.5 years. e population density of Ethiopia is 115 people km −2 (298 people mi −2 ). e total land area is 1,100,000 Km 2 [12].

Search Strategies.
We searched articles written in English on international databases such as Pub Med/MED-LINE, Science Direct, Web of Science, and Google Scholar [13]. Literature was collected within the time interval of December 2019-January 2020. e core search terms and phrases used were "prevalence," "intestinal helminths parasites," "associated risk factors," and "Ethiopia". e search terms were used separately and in combination with the Boolean operators "OR" or "AND". Finally, the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) checklist was used to present and report the results of the study [13].

Inclusion and Exclusion
Criteria. Studies published from 2010 to January 2020 were included. All observational study designs (cross-sectional, case-control, and cohort) reporting the prevalence of intestinal parasitic infections and their associated risk factors among people in Ethiopia were included. Articles that were not accessible, articles written in languages other than English, and articles published before 2010 were excluded.

Outcomes of the Study.
e measurement outcome of this study had two main outcome variables: the prevalence of HIHPIs and factors associated with HIHPIs. HIHPIs are defined as infections caused by one or more human helminth parasites [10].

Data Extraction.
e data extraction protocol was prepared and evaluated by all authors We extracted information on the name of the author and year of publication, population studied, region and sites of study or focus, total sample size and the number of positives, estimated prevalence, species of intestinal parasites, and potential risk factors associated with individual species of HIHPs.

Quality Assessment of Individual Studies Included in the Meta-Analysis.
e Grading of Recommendation Assessment Development and Evaluation (GRADE) approach was used to assess the overall quality of evidence [14]. Methodological quality, comparability of the outcome, and statistical analysis of the study were the three major assessment tools that were utilized to declare the quality of the study. Publications with total scores of five to six points were considered as high quality, three to four as moderate quality, and two and below as low quality.

Risk of Publication Bias across Studies Included in is
e risks of publication bias across the studies were assessed using funnel plot symmetry and Egger's test.
e Egger's test p-value < 0.05 was used to determine the presence of publication bias across the studies. e cause of publication bias was assessed using a sensitivity test and regression test.

Data Analysis.
e prevalence of HIHPIs was computed by dividing the total number of HIHPI cases by the total number of participants in the studies multiplied by 100. Besides, we used a random-effect model to estimate the pooled effect size (prevalence of HIHPIs). Cochrane Q-test and I 2 statistics were used to assess heterogeneity among the studies [15]. To sort out the causes of heterogeneity, we conducted a subgroup analysis based on the region of the study, the nature of study participants, study year, and sample size in individual studies. 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 the prevalence of HIHPIs among respondents. e meta-analysis was conducted using STATA Corp College Station, TX software version 14. P-values < 0.05 were considered statistically significant.

Result
Out of the 321 articles retrieved, 62 articles were excluded due to duplicates, 80 articles due to their titles, and 79 due to their abstracts. e remaining 100 full-text articles were assessed for their eligibility. Twenty-three articles were excluded because of not fulfilling specific inclusion criteria and data extraction protocol. Consequently, 67 studies met the eligibility criteria and were included in the final metaanalysis ( Figure 1).

Characteristics of Original Studies.
Among the 67 studies selected, a total of 102, 265 study participants were involved to determine the pooled prevalence of HIHPIs and their associated risk factors among the people of Ethiopia. Among the studies, 85.07% and 14.9% were cross-sectional and retrospective studies, respectively. e sample size of the selected studies ranged from 118 to 21611 (Table 1).

Risk of Publication Bias across the Studies Included in the Meta-Analysis.
e funnel plot symmetry proves the presence of publication bias among the studies included in the present meta-analysis ( Figure 4). Similarly, Egger's test results (P < 0.05) indicate the presence of a publication bias among the studies.

Factors Associated with HIHPIs among People in Ethiopia.
Handwashing habits before food, handwashing after toilet, age, open field defecation, the habit of eating raw and unwashed vegetables/fruits, maternal education, levels of income, source of drinking water, swimming, walking on barefoot, playing with soil, and family size were significantly associated with HIHPIs.
is difference might be due to the variation in the environment and living conditions of the study participants [26]. Ethiopian people are known for eating raw meat [110]. e prevalence of S. stercoralis (1.17%) in this metaanalysis was higher than in the study conducted in Ghana (0.3%) [101]. However, it was lower than the study outcome of Angola (12.8%) [111] and Alabama (7.3%) [112]. Such variations in the prevalence of helminth infections attribute to variations in water supplies, sanitation, and hygiene [33]. Weakening immunity due to HIV/AIDS among HIV-positive people might also be the other reason for the variation. e prevalence of E. vermicularis (0.71%) in this metaanalysis was in line with the study conducted in Tepi Town, South West Ethiopia (0.26%) [1,9]. However, it was lower than the worldwide prevalence (2.3%) and the study conducted in Cambodia (1.1%) [86]. is variation might be due to the differences in the distribution of helminth species in different geographical areas, variations in water supplies, sanitation, hygiene, and methodology used during helminth identification [33,54]. e habit of suckling fingers/learning materials and playing with soil may be the reasons for enterobiasis infections [113].
e subgroup analysis of this study indicated that the highest prevalence of HIHPIs was observed in Oromia region ( 30, 16.10). e possible justification for this difference might be due to the peculiarities in sociodemographic, environmental, geographical, and behavioral characteristics. HIH-PIs prevalence in five of the regions, namely, Oromia (38.45%), SNNPR (35.58%), Addis Ababa (34.45%), Amhara (33.84%), and Harare (26.80%) was higher than the global prevalence (24%) [81]. Prevalence of only the two regions: Tigray (20.38%) and Benishangul-Gumuz (12.70%) had a better prevalence compared to the globe. e prevalence of HIHPIs in the first five years (2010-2014), 44.64% (95% CI: 34.39, 54.89), was higher than in the second round 2015-2019 (29.08%; 95% CI: 24.12, 34.04). e result showed that the trend of HIHPIs in Ethiopia was reduced. e outcome was similar to a systematic review, and meta-analysis was conducted in Ethiopia in which the pooled prevalence in the years 1997-2002, 2003-2008, 2009-2014, and >2014 was 71%, 42%, 48%, and 42%, respectively [115]. e potential reason for this decreasing rate might be due to the development of awareness about the transmission and prevention mechanisms of HIHPIs and mass deworming programs [116]. e prevalence of HIHPIs was the highest among urban dwellers (53.45%, 95% CI: −2. 28, 109.19). It was higher than the report in the study conducted in the Gamo area, Ethiopia (39.9%) [66]. e lowest prevalence of HIHPIs was among patients (17.96%, 95% CI: 14.07, 21.85). It was similar to the study conducted in Shawura, Ethiopia (20.1%) [8]. ese differences might come from the differences in diagnostic methods, population density, and geographical and behavioral characteristics. e odds of having intestinal helminthic parasite infections in children up to the age of 14 years were 1.66 times higher than in adults. It agrees with the study conducted in tropical semiurban communities [117], Ghana [118], and Yemen [119]. Children are vulnerable to infections with HIHPIs because of a lack of well-developed immune systems and playing habits in fecal-contaminated soil [71].
People from large family sizes (greater than six) were 3.75 times more likely to have HIHPIs than those from family sizes less than six. It was similar to that of human intestinal protozoan parasitic infections (HIPPIs) (OR: 3.7, 95% CI: 1.45-5.85) [80]. It agrees with the studies performed in Ethiopia [40] and Ghana [101]. It might be because a large family size increases the chance of contact with each other and may also increase HIHPI transmission. On the other hand, large families could not get adequate medication and treatment.
Uneducated people were 1.81-fold more likely to have HIHPIs than the educated. is finding agreed with the study conducted in Kenya [120], Ghana [101], Bolivian [121], and South Africa [102]. It might be because uneducated people may lack the necessary knowledge and practice towards the transmission/prevention of intestinal helminth parasites.
People with a low-income level were twice likely to have HIHPIs compared to their counterparts. is finding agreed with the studies conducted in Dembiya district, North e Scientific World Journal Ethiopia [19], and Haramaya University cafeterias [36]. It might be because low-income people fail to fulfill their sanitary requirements. e odds of intestinal helminth parasite infections among people drinking untreated water were 3.12 times than those who used to drink treated water. It is in line with the studies from Indonesia [96], Uganda [122], and South Africa [102]. It might be because drinking and using untreated water may be a route for human helminth infections [123]. e odds of HIHPI occurrence among people who did not wash their hands before feeding were 5.22 times higher than those who did.
is finding agrees with the studies conducted in Indonesia [96], the Eastern Region of Nepal [124], and Indonesia [125]. It might be because unwashed hands contain dust particles and microorganisms that facilitate the transmission of microorganisms fecal-orally.
Likewise, people who did not have handwashing habits after defecation were 3.03 times more likely to be infected with intestinal helminths than those who had handwashing habits. is result was higher than HIPPIs (OR: 2.82, 95% CI: 2.01-3.63) [80]. is finding agreed with the studies conducted in Indonesia [96], Uganda [122], Cameroon [125], and South Africa [102]. It might be because unwashed hands after defecation may contain stool materials and facilitate the transmission of microorganisms fecal-orally. e odds of HIHPI occurrence were 2.42 times higher among different groups of people with open field defecation habits than their counterparts. It was close to that of human HIPPIs (OR: 2.91, 95% CI: 1.60-4.21) [80].
is finding agrees with a study conducted in Indonesia [96]. It might be because open field defecation would be a source of contamination to food and water sources.
People who had eaten leftover food and raw and unwashed vegetables/fruits were 1.98 times more likely to be infected with intestinal helminth parasites than those who had not. is finding is in line with the study conducted in Sri Lanka [95]. It might be because leftover food and raw and unwashed vegetables/fruits may contain HIHPs [123]. e odds of having intestinal helminth parasitic infections among people who had the habit of walking barefoot were 3.28 times higher than their counterparts. is finding agrees with studies conducted in Bolivia [121] and South Africa [102]. e reason might be helminths may have easy access into the body through skin penetration.
People who used to play with soil were 2.64 times more likely to be infected with intestinal helminth parasitic infections than those who did not. is finding agrees with the studies conducted in Turkey [126], Bolivia [121], and South Africa [102]. It might be because people who used to play with soil may have contact with soil-transmitted helminths' eggs, larvae, or adults [127].
Lastly, participants who used to swim in rivers were 1.90 times more likely to acquire HIHPIs than their counterparts.
is finding is in line with the studies conducted in Ethiopia in Adi Remets town [21], Bahir Dar town [7], and Jimma town [61]. It might be because river waters may get contaminated with the ova, larvae, or adult helminth parasites.

Limitations of the Study
Lack of studies from Dire Dewa, Gambela, Somali, Afar, Harare, and Benishangul-Gumuz regions may underestimate both the pooled and subgroup prevalence of HIHPIs in Ethiopia. Lack of molecular techniques in the studies failed to identify hookworm species.

Conclusion
HIHPI prevalence among people in Ethiopia was high and still a major public health concern. e prevalent helminths identified were Ascaris lumbricoides, hookworm, Schistosoma mansoni, Trichuris trichiura, Hymenolepis nana, Taenia species, Strongyloides stercoralis, and Enterobius in descending order. Handwashing before food and after toilet, age, the habit of eating raw and unwashed vegetables/fruits, level of education, levels of income, source of drinking water, playing with soil, walking on barefoot, and family size were significantly associated with HIHPIs.

Recommendation
Particular emphasis shall be given to mass treatment and health education. Moreover, studies are needed in Gambella, Afar, Somali, Dire Dewa, Benishangul-Gumuz, and Harare regions.

AAU:
Addis Ababa University AIDS: Acquired immuno deficiency syndrome CD4: Cluster of differentiation HAART: Highly active antiretroviral therapy HIHPIs: Human intestinal helminth parasitic infection HIHPs: Human intestinal helminth parasites HIPPIs: Human intestinal protozoan parasitic infections HIV: Human immuno deficiency virus IPIs: Intestinal parasitic infections OR: Odds ratio PRISMA: Preferred reporting items for systematic reviews and meta-analysis checklist SNNP: Southern nations, nationalities, and people STH: Soil-transmitted helminths WHO: World Health Organization.

Data Availability
All related data have been presented within the article and supplementary data. e data set supporting the conclusions of this article is available from the corresponding author upon request.

Ethical Approval
Our study is an investigation of the literature and does not need ethical approval for retrieving the already available public content.

Conflicts of Interest
e authors declare that they have no conflicts of interest.

Authors' Contributions
ML developed the draft proposal under the supervision of DD. Statistical analysis was guided by DT. All authors (ML, DD, and DT) critically reviewed, provided substantive feedback, and contributed to the intellectual content of this paper and made substantial contributions to the conception, conceptualization, and manuscript preparation of this systematic review. All authors read and approved the final manuscript. Figure S1. Odds ratio between age and HIHPIs in Ethiopia. Figure S2. Odds ratio between family size and HIHPIs in Ethiopia. Figure S3. Odds ratio between family education level and HIHPIs in Ethiopia. Figure S4. Odds ratio between income level and HIHPIs in Ethiopia. Figure S5. Odds ratio between source of drinking water and HIHPIs in Ethiopia. Figure S6. Odds ratio between no habit of handwashing before feeding and HIHPIs in Ethiopia. Figure S7. Odds ratio between no handwashing after defecation and HIHPIs in Ethiopia. Figure S8.

Supplementary Materials
Odds ratio between open-field defecation and HIHPIs in Ethiopia. Figure S9. Odds ratio between eating raw food and HIHPIs in Ethiopia. Figure S10.
Odds ratio between walking on barefoot and HIHPIs in Ethiopia. (Supplementary Materials)