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. 2020 Jan 28;20:117. doi: 10.1186/s12889-020-8222-y

Epidemiology of intestinal parasitic infections in preschool and school-aged Ethiopian children: a systematic review and meta-analysis

Legese Chelkeba 1,2,✉, Zeleke Mekonnen 3, Yonas Alemu 3, Daniel Emana 3
PMCID: PMC6988312  PMID: 31992252

Abstract

Background

Numerous studies have been carried out on assessing the prevalence of intestinal parasites infections (IPIs) amongpreschool and school-age children in Ethiopia, but there is lack of study systematically gathered and analyzedinformation for policymakers. Therefore, the aim of this systematic review and meta-analysis was to provide a summary on prevalence, geographical distribution and trends of IPIs among preschool and school-age childrenin Ethiopia.

Methods

The search were carried out in Medline via PubMed, Scopus, Science Direct, Web of Science, and Google Scholar from 1996to July2019 for studies describing prevalence of IPIs among preschooland school-age children. We conducted meta-regression to understand the trends and the source of heterogeneity and pooled the prevalence using ‘metaprop’ command using STATA software version 14.

Results

Eighty-three(83) studies examining 56,786 fecal specimens were included. The prevalence of IPIs was 48%(95%CI: 42 to 53%) and showedsignificantly decreasing trends 17% (95% CI: 2.5 to 32%) for each consecutive 6 years) and was similar in males and females. The pooled prevalence in years 1997–2002, 2003–2008, 2009–2014 and > 2014 was 71% (95% CI: 57 to 86%), 42% (95% CI: 27 to 56%), 48% (95% CI: 40 to 56%) and 42% (95% CI: 34 to 49%), respectively. Poly-parasitism was observed in 16% (95% CI: 13 to 19%,) of the cases.

Conclusion

Intestinal parasite infections are highly prevalent among preschool and school-age children and well distributed across the regional states of Ethiopia. Southern and Amhara regional states carry the highest burden. We observed significant decreasing trends in prevalence of IPIs among preschool and school-ageEthiopian children over the last two decades. Therefore, this study is important to locate the geographical distribution and identified high risk areas that should be prioritized further interventions, which complement global efforts towards elimination of IPIs infections by 2020.

Keywords: Preschool-age children, School-age children, Intestinal parasites, Ethiopia, Meta-analysis

Background

Parasitic infections caused by intestinal helminths and protozoan are among the most prevalent infections in developing countries carrying high burden of morbidity and mortality in these areas [1]. Specifically, economically disadvantaged children living in tropical and sub-tropical regionswith a limited or no access to safe drinking water, inadequate sanitation, and substandard housing are the most affected ones [2]. Epidemiological evidence suggests that an estimated over one billion people in the world, majorly children were infected with intestinal parasites caused by helminths and protozoa [3]. Majority of the infections were due to Ascaris lumbricoides, hookworm, and Trichuris trichiura [4, 5]. More than 267 million preschool-age children and 568 million school-age children live in areas where these parasites are intensively transmitted [6]. Cryptosporidium species, Entamoeba histolytica and Giardia duodenalis were the most common protozoan infections in children under 5 years in sub-Saharan Africa [7].

The regional distribution and prevalence differences of IPIs among children are mainly due to differences in degree of fecal contamination of water and food, climatic, environmental and socio-culture [8–10]. The prevalence among under-five, preschool and school children were reported as 17.7% in Riyadh, Saudi Arabia [11], 52.8% in an urban slum of Karachi, Pakistan [12], 19.6% in Zambia [13] and 30% in Khartoum, Sudan [13]. In Ethiopia, prevalence varies across the regions in the country. For instance, the prevalence was 85.1% in Wondo Genet (Southern region) [14], 48.1% in Aynalem village (Tigray region) [15], 17.4% in Debre Birhan (Amhara region) [16], 26.6% in Hawassa (Southern region) [17], 24.3% in Wonji Shoa Sugar Estate (Oromia region) [18], 18.7% in Woreta (Amhara region) [19], 25.6% in Dembiya (Amhara region) [20] and 41.1% in Jimma town (Oromia region) [21].

School-agechildren are the most affected ones due to their habits of playing or handling of infested soils, eating with soiled hands, unhygienic toilet practices, drinking and eating of contaminated water and food [22]. Intestinal parasite infections lead to malnutrition, mal-absorption, anemia, intestinal obstruction, mental and physical growth retardation, diarrhea, impaired work capacity, and reduced growth rate constituting important health and social problems [10, 18, 23, 24].

Numerous epidemiological studies have been performed on assessing the prevalence of IPIs among children in Ethiopia, but there is lack of systematically gathered and analyzed information for policymakers. Therefore, the aim of this systematic and meta-analysis was to provide a summary on prevalence, geographical distribution and trends of IPIs among preschool and school-age children in Ethiopia.

Methods

Search strategy and data extraction

The search were carried out in Medline via PubMed, Scopus, Science Direct, Web of Science and Google Scholar using searching terms intestinal parasite infection” OR “helminths” OR “protozoa” AND “Ethiopia”. Searching was carried out on articles published from 1997 to March,2019 and limited human studieswith language restriction to English. A manual search for additional relevant studies using references from retrieved articles and related systematic reviews was also performed to identify original articles we might have missed. Conference abstracts and unpublished studies were excluded. We did our analyses according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement [25].

Participants, inclusion and exclusion criteria

Two authors independently (LCH&DE) assessed the inclusion criteria and disagreement was solved by discussion with the third author (ZM). We included the studies if they met the following criteria: the study design was an observational study (prospective cohort, case-control, retrospective cohort, or cross-sectional) or controlled clinical trial which documented the baseline prevalence or incidence of IPIs. We included all studies reported the rateor proportion of IPIs in preschool and/or school-age children or both. We excluded studies reporting case reports, case series, studies that compared the sensitivity and specificity of different methods used for diagnosis of intestinal parasites and studies not reported either prevalence or incidence of IPIs as outcome of interest. The terms preschool and school-age children were defined according to the original studies. Accordingly, preschool-age children were defined aschildren of age below 5 years while,school-agechildren were children of age 5 and above. Poly-parasitism was defined as concurrent infection with different species of intestinal parasites either helminths or protozoa.

Data extraction and quality assessment

The two authors (LCH and DE) defined protocol for data extraction and assessed them independently for eligibility and disagreements were resolved by discussion with the third author (ZM). We extracted information on name of the first author and year of publication, study design, population studied (preschool age children, school age children or both), gender, region & sites of study, Method (s) for identification of the parasites, total sample size and the number of the positives (percentage). The Grading of Recommendation Assessment, development and Evaluation (GRADE) approach was used to assess the overall quality of evidence [26]. Accordingly, studies were given one point each if theyhad probability sampling, larger sample sizes of more than 200, and repeated detection and up to four points could be assignedto each study. Publications with a total score of 3–4 points were considered as high quality, whereas 2 points represented moderate quality and scores of 0–1 represented low quality.

Statistical analysis

We used forest plots to estimate pooled effect size and effect of each study with their confidence interval (CI) to provide a visual summary of the data. A random-effects model was used in this meta-analysis because of anticipated heterogeneity. All reported P values were 2-sided and were statistical significant if P < 0.05. Statistical heterogeneity among studies was expressed as the P value (Cochran’s Q statistic), where a P < 0.05 and I2 ≤ of 25–50% were considered as low heterogeneity and I2 > 50% indicated substantial heterogeneity. We also used Begg’s Funnel plot and Egger’s regression test for evaluating the possibility of publication bias. A potential source of heterogeneity was investigated by subgroup andmeta-regression analysis. The factors included were geographical regions and cities of Ethiopia, age of children (preschool vs. school-age children), and years of publication (1997–2002, 2003–2008, 2009–2014 and > 2014). We conducted meta-analysis using ‘metaprop’ commandusing STATA software, version 14, STATA Corp,College Station, TX.

Results

Literature searches and selection

We identified systematically 1198 publications, of which 83 were eligible for inclusion in the final analyses. The details of our search strategy were depicted in Fig. 1. Our initial search of electronic databases such as Medline via PubMed, Scopus, Science direct, Web of Sciences and Google scholar yielded 1195 articles and 3 articles manually from which 186 records remained after removing 1012 duplications. Up on screening the articles, 99 articles were further excluded; 90 were irrelevant because they were not specifically about preschool or school-age children, 6 studies were about sensitivity and specify of diagnosis of IPIs, 3 articles were review articles. Up on further access to the full texts of 87 articles, 4 were excluded for the following reasons; 2 were meta-analyses and 2 articles lacked outcome of interest. Finally, 83 published between 1997 and 2019 fulfilling the inclusion criteria were included in the analyses.

Fig. 1.

Fig. 1

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Flow diagram showing the selection process

The sample size of the included studies ranged from 100 [27] to 15,455 [28] with a total number of 56,786 participants [14, 16, 17, 21, 24, 27–103]. Most of the studies were reported from Amhara regional 33(40%) followed by Oromia region 21(25%). The rests were reported from South region 18(22%), Tigray region 9(11%), Benishangul-Gumuz region 1(1%) and Addis Ababa city 1(1%). With regard to the study design, majority of the studies were cross sectional in design (79 studies), 2 were controlled clinical trials, 2 were prospective follow up cohort studies and 1 was case-control. Sixty six studies were about IPIs in school-age children, 13 were in preschool-age children (under-five) and 4 were studies involved both preschool and school-age children. According to our quality assessment criteria, 34 publications were of high quality with a score of 3, 12 had a score of 2 indicating moderate quality and the remaining 37 were of low quality with a score of zero or one [Table 1]. Prevalence estimate and heterogeneity analysis.

Table 1.

Characteristics of the 83 eligible studies of intestinal parasite infections in Ethiopia

Author Study design Population Male Female Study site (s)Region Methods No. sample No. positive (%) Quality assessment
Degarege 2013 [40] Cross-sectional School children 187 216 Tikur Wuha, Gojam,Amhara region Kato-Katz 403 235 (58.3%) 2
Abdi 2017 [75] cross-sectional School children 207 201 Zegie Peninsula, Gojam, Amhara region Formalin-ether 408 282 (69.1%) 3
Abera 2014 [76] Cross-sectional School children 193 192 Bahir Dar, Amhara region Formal-ether 385 170 (44.2%) 3
Wegayehu 2013 [51] Cross-sectional School children 191 193 GirarJarso and Dera, North Shewa Zone, Oromia Region Direct and formalin- ether and modified Ziehl-Neelsen 384 81(21.1%) 2
Amare 2013 [35] Cross-sectional School children 218 187 Gondar town, Amhara region Direct, formal-ether and Kato-Katz 405 92(22.7%) 3
Gelaw 2013 [45] cross-sectional School children 170 134 University of Gondar Community School, Amhara region Direct and formol-ether 304 104 (34.2%) 3
Abossie 2014 [78] Cross-sectional School children 191 209 GamoGofa Zone, South region Direct and formol-ether 400 324(81.0%) 3
Mathewos 2014 [57] Cross-sectional School children 139 122 Gorgora and Chuahit towns, Gondar, Amhara region Direct, formol-ether and modified Ziehl-Neelsen 261 174 (66.7%) 2
Gizaw 2018 [20] Cross-sectional Preschool children 106 119 Dembiya, Gondar Zone, Amhara region Kato-Katz 225 58(25.8%) 3
Wegayehuet 2016 [77] Cross-sectional Both 154 132 Holetta, Sendafa and Chancho, Oromia region PCR 312 48(16.8%) 2
Yimam 2016 [74] Cross-sectional School children 187 216 Tikur Wuha Elementary School, Amhara region Formol-ether and Kato-Katz 403 235(58.3%) 3
Hailegebriel 2017 [79] Cross-sectional School children 177 182 Dona Berber, Bahir Dar, Amhara region Formol-ether 359 235 (65.5%) 3
Alemu 2018 [80] Cross-sectional School children 196 195 ArbaminchZuria, South region Formol-ether 391 182(46.5%) 2
Alemu 2019 [82] Cross-sectional School children 180 171 Birbir town GamoGofa, South region Direct and formol-ether 351 95 (27.1%) 3
Mekonnen 2019 [19] Cross-sectional Preschool children 152 158 Woreta health center, Gondar, Amhara region Direct and Kato-Katz 310 58 (18.70%) 3
Jejaw 2015 [41] Cross-sectional School children 228 232 Mizan-Aman town Bench Maji, South region Direct and formol-ether and Kato-Katz 460 353 (76.7%) 3
Alemu 2016 [81] Cross- sectional Preschool children 183 218 Dembiya District, Gondar, Amhara region Kato-Katz 401 141 (35.2%) 3
Alemayehu 2017 [58] Cross-sectional School children 287 216 Wolaita Zone, South region Kato-Katz and formalin-ether 503 363(72.2%) 3
Gashaw 2015 [61] Cross-sectional School children 255 295 Maksegnit and Enfranz Towns, Gondar, Amhara region Kato-Katz 550 365(66.4%) 3
Bajiro 2016 [83] Cross-sectional School children 238 262 Jimma town, Oromia region Kato-Katz 500 120(24%) 3
Amor 2016 [84] Cross-sectional School children 225 171 Rural area of Bahir Dar, Amhara region Formol ether 396 327(82.6%) 3
Nute 2018 [28] Cross-sectional School children 418 8037 Ten zones of the Amhara region Formol ether 15,455 5626(36.4%) 3
Zemene 2018 [16] Cross-sectional Preschool children 118 118 DebreBirhan hospital, North Shewa, Amhara region Direct and the formol-ether 247 43 (17.4% 1
Gebretsadik 2018 [85] Cross sectional Preschool children 133 99 Dessie referral Hospital, Amhara region Direct, formol-ether and modifiedZiehl-Neelsen 232 36 (15.5%) 1
Mulatu 2015 [17] Cross-sectional Preschool children 81 77 Adare Hospital and Millennium Health Centre, Hawassa, South region Direct, formol-ether and modifiedZiehl-Neelsen 158 42 (26.6%) 3
Bekana 2019 [86] Cross-sectional School children 172 145 Guma and YachiYisa in Gomma, Jimma, Oromia region Kato-Katz and formol-ether - 317 224 (70.4%) 3
Diro 2015 [87] prospective cohort Both 85 37 University of Gondar and Kahsay Abera Humera hospitals, Amhara region Direct, formol-ether and Kato-Katz 122 58(47.5%) 1
Birhanu 2018 [88] cross sectional School children 194 228 Pawe Town, Benishangul-Gumuz Region Direct 422 130 (30.8%) 1
Fentie 2013 [32] Cross-sectional School children 361 159 Lake Tana Basin, Amhara region Kato–Katz and formol-ether 520 371(71.3%) 3
Aiemjoy 2017 [66] Cross-sectional Preschool children NA NA GonchaSisoEnese, Gojam, Amhara region Formol-ether 212 138 (65.1%) 2
Desalegn 2014 [31] Cross-sectional School children 271 315 Jimma Town, Jimma, Oromia Direct and formol-ether 586 134 (33.9%) 3
Gebrehiwot 2014 [104] Cross sectional Preschool children 195 179 WonjiShoa Sugar, Oromia region Kato-Katz 374 91(24.3%) 2
Leta 2018 [89] Cross sectional School children NA NA 53 schools of Amhara region Kato-Katz 2650 354 (13.4%) 3
King 2013 [42] cross sectional Both 1130 1228 South Gondar, Amhara region Formol-ether 2338 1471(63%) 3
Mekonnen 2013 [90] Clinical trial School children NA NA 14 schools of Jimma town, Oromia region Kato-Katz 840 437(52%) 3
Mahmud 2015 [47] Clinical trial School children 152 217 Mekele University, Tigray region Direct, formal-ether and Kato-Katz 369 267(73%) 3
Mahmud 2013 [48] cross-sectional School children 288 312 Mekele, Tigray Direct, formol-ether and Kato-Katz 600 421 (72%) 3
Tefera 2017 [72] Cross sectional School children 282 433 Mendera, Jimma, Oromia region McMaster 715 346(48.4%) 2
Tefera 2015 [91] Cross sectional School children 364 280 Babble town, Harrerge, Oromia region McMaster 644 89 (13.8%) 2
Nguyen 2012 [24] Cross sectional School children 341 323 AngolelaWoreda, Amhara region Formal- ether 664 202(30.4%) 3
Hailu 2018 [92] Cross sectional School children 186 223 Bahir Dar, Amhara region Formol-ether 409 237 (58%) 2
Beyene 2014 [21] Cross sectional School children 114 146 Jimma Health Center, Jimma, Oromia region Direct and formol-ether 260 129 (49.6%) 3
Alemu 2011 [34] Cross sectional School children 157 162 Zarima town, Gondar, Amhara region Direct and Kato-Katz 319 263 (82.4%) 3
Alemayehu 2015 [93] Cross sectional School children 201 183 DembaGirara, Woliata, South region Direct and Kato-Katz 384 328 (85.4%) 1
Ali 1999 [94] Cross sectional School children 161 121 Asendabo Town, Jimma, Oromia region Direct and Kato-thick 282 243(86.2%) 0
Tulu 2016 [68] Cross sectional School children 251 241 Birbir, Bale Zone, Oromia region Direct and formol-ether 492 131(26.6%) 0
Unasho 2013 [73] Cross sectional School children 189 217 Gedeo, Woliata and Kambata and Amaro, South region Direct 406 170 (41.9%) 0
Belyhun 2010 [53] Follow up cohort Preschool children NA NA Butajira town, South region Formol-ether 905 44 (4.9%) 3
Tulu 2014 [43] Cross sectional School children 172 168 Delo-Mena, Bale Zone, Oromia region Direct and formol-ether 340 89(26.2%) 1
Erosie 2002 [44] Cross sectional School children NA NA BolosoSorie, South region Formol-ether 421 292(69.4%) 1
Tadesse 2005 [39] Cross sectional School children 271 144 Babile town, Harrerge, Oromia region Formal ether 415 113(27.2%) 0
Adamu 2005 [52] Cross sectional Preschool children 149 147 Police hospital, Armed Forces General hospital, and Tikur Anbessa Hospital, Addis Ababa Direct, formol-ether and Modified Ziehl-Neelsen 296 69(23.3%) 0
Jemaneh 1999 [95] Cross sectional School children 439 439 Gondar town, Gondar, Amhara region Kato-Katz 878 437(49.7%) 0
Dejenie 2009 [60] Cross sectional School children 1012 998 Central Tigray, Tigray region Direct 2000 571(28.6%) 0
Dejenie 2010 [69] Cross sectional School children 319 303 Tigray, Tigray region Kato-Katz 622 165(26.5%) 0
Nyantekyi 2010 [14] Cross sectional Preschool children 140 148 Wondo Genet, South region Kato-Katz and formal-ether 288 245 (85.1%) 1
Legesse 2010 [56] Cross sectional School children 167 214 Adama town, Oromia region Kato-Katz and formol-ether 381 263 (69%) 0
Terefe 2011 [64] Cross sectional School children 218 201 Bushulo, Hawassa, South region Kato-Katz 419 282(67.3%) 1
Assefa 2013 [59] Cross sectional School children 267 190 Suburbs of Mekelle city, Tigray region Kato-Katz 457 109 (23.9%) 0
Debalke 2013 [96] Cross sectional School children 161 205 Jimma town, Oromia region McMaster 366 166(45.4%) 1
Dejene 2008 [97] Cross sectional School children 481 319 Hintallo-Wejerat, Tigray region Formal- ether 800 285(35.6%) 0
Fekadu 2008 [27] Cross sectional School children 63 37 Asendabo town, Jimma, Oromia region Harada-Mori (Test tube culture) 100 66(66%) 0
Haileamlak 2005 [33] Cross sectional Preschool children 487 437 Jimma Zone, Jimma, Oromia region Direct and formal-ether 924 530(57.4%) 1
Jemaneh 2001 [46] Cross sectional School children 282 405 Chilga, Gondar Zone, Amhara region Kato-Katz 687 470(68.4%) 1
Firdu 2014 [71] Case-control Both 135 95 Yirgalem Hospital, South region Direct formol-ether and modified Ziehl-Neelsen 230 74(32.2%) 1
Wale 2014 [65] Cross sectional School children 206 196 Lumame town, Amhara region Direct and formal ether 402 219(54.5%) 1
Teklemariam 2014 [70] Cross sectional School children 252 228 Enderta, Tigray region Formalin-ether 480 199(41.5%) 0
Ayalew 2011 [36] Cross sectional School children 358 346 Delgi, Gondar, Amhara region Direct and formol-ether 704 562 (79.8%) 2
Merid 2001 [38] Cross sectional School children NA NA Lake Hawassa, South region Direct and formol- Ether 150 139(92.7%) 0
Assefa 1998 [30] Cross sectional School children 479 219 Wollo, Amhara region Formal-ether 698 304 (43.3%) 0
Roma 1997 [50] Cross sectional School children 352 168 Wondo-Genet, South region Formol-ether 520 465 (89.4%) 1
Abera 2013 [98] cross sectional School children 397 381 Bahir Dar special zones, Amhara region Kato-Katz and formal-ether 772 401(51.5%) 3
Kidane 2014 [55] Cross sectional School children 177 207 Wukrowereda, Tigray region Direct 384 233(60.7%) 0
Alamir 2013 [29] Cross sectional School children 192 207 Dagi, Amhara region Direct and formal-ether 399 311(77.9%) 0
Kabeta 2017 [99] Cross sectional Preschool children NA NA HawassaZuria, South region Direct smear and formal-ether 587 301(51.3%) 1
Shumbej 2015 [100] Cross sectional Preschool children 165 212 Butajira, South region McMaster 377 104 (27.6%) 3
Tadege 2017 [101] Cross sectional School children 235 139 Finchawa and Tullo, South region Formol-ether 374 254(67.9%) 3
Andualem 2014 [102] Cross sectional School children 168 190 Motta, Gojam, Amhara region Direct and formal-ether 358 245(68.4%) 0
Reji 2011[51) Cross sectional School children NA NA Adama town, Oromia region Kato-Katz 358 127 (35.5%) 1
Alemu 2014 [67] Cross sectional School children 211 194 Umolante, GamoGofa, South region Kato-Katz 405 109(26.9%) 0
Samuel 2015 [105] Cross sectional School children NA NA Ambo town, Oromia region Formol-ether 375 47(12.6%) 3
Teshale 2018 [103] Cross section School children 240 170 MedebayZana, Tiray region Kato-katz 410 52(12.7%) 1
Tekeste 2013 [63] Cross sectional School children 170 156 Gorgora, Amhara region Kato-katz 326 110(36.8%) 2
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Abbreviations: NA not available; PCR Polymerase chain reaction

A total of 27,354 of the 56,786 children examined during the period under review were infected with one or more species of intestinal parasites yielding an overall prevalence of (n = 27,354) 48%(95%CI: 42 to 53%) with substantial heterogeneity (I2 = 99.50%, regression coefficient: -0.23, 95% CI: − 0.38 to − 0.09, p = 0.002, Fig. 2). A range of parasites were detected in the studies including Ascaris lumbricoides, Hookworm, Trichuris trichuria, Strongyloides stercoralis, Enterobius vermicularis, Schistosoma mansoni, Hymenolepsis nana, Taenia species, Giardia lamblia/intestinalis/duodenalis, Entamoeba histolytica/dispar and Cryptosporidium species. Subgroup analysis showed that the prevalence of IPIs was 56% (95%CI: 39 to 73%) in Southern region, 51%(95%CI: 43 to 58%) in Amhara region, 40% (95%CI: 31 to 50%) in Oromia region, and 41%(95%CI: 28 to 54%) in Tigray region as shown in Figs. 3 and 4. The age related prevalence was 52% (95%CI: 46 to 58%,) in school-age children and 30% (95%CI: 18 to 34%) preschool-age children (p = 0.002) as shown in Fig. 5.

Fig. 2.

Fig. 2

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Begg’s funnel plot and Egger test for heterogeneityof intestinal parasite infections among Ethiopian children

Fig. 3.

Fig. 3

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Regional distribution of intestinal parasite infections in Ethiopian children from 1997 to 2019

Fig. 4.

Fig. 4

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Forest plot showing the geographic distribution of intestinal parasite infections in Ethiopia Children

Fig. 5.

Fig. 5

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Forest plot showing age related distribution of intestinal parasite infections in Ethiopia children

The pooled prevalence of IPIs in year 1997–2002, 2003–2008, 2009–2014 and > 2014 was 71% (95% CI: 57 to 86%), 42% (95% CI: 27 to 56%), 48% (95% CI: 40 to 56%) and 42% (95% CI: 34 to 49%), respectively [Fig. 6]. We did meta-regression analyses to search for the sources of heterogeneity. We detected no significance difference in geographical distribution (regression coefficient: 0.025, 95% CI: − 0.11 to 0. 06, p = 0.56) as shown Fig. 7a.The results of the analyses showed that age (regression coefficient: 0.38, 95% CI: 0.15 to 0.60, p = 0.002, Fig. 7b) and year of publication (regression coefficient: -0.17, 95% CI: − 0.32 to − 0.025, p = 0.023, Fig. 7c) might be sources of heterogeneity,

Fig. 6.

Fig. 6

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Forest plot showing trend of intestinal parasite infections in Ethiopia children

Fig. 7.

Fig. 7

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Meta regression result of (a). the geographic distribution (b). the distribution by age C. distribution by year of publication of Intestinal parasite infections among Ethiopian children

Prevalence of IPIs by area of residence, gender and poly-parasitism status

Thirteen studies (N = 12,356) reported the proportion of IPIs based on residence area. The pooled prevalence of overall IPI was not significantly differ between rural and urban areas; rural 22 95% CI: 10 to 30%, Additional file 1) and urban 23% (95% CI: 14 to 32%, Additional file 2). Forty two studies (N = 36,218) had separate data on the prevalence of IPIs for males and females. The pooled prevalence formales was 24% (95%: CI 20 to 28%, Additional file 3) while, it was 22% (95% CI: 18 to 25%, Additional file 4) for females. Poly-parasitism was observed in 16% (95% CI: 13 to 19%, Additional file 5) of children and 36% (95% CI: 30 to 41%, Additional file 6) of children were infected with a single species of parasite.

Discussion

The pooled prevalence of IPIs in preschool and school-age Ethiopian children was 48%(95%CI: 42 to 53%). The prevalence is higher in Southern (56%) and Amhara regions (51%).We observed a significant decrease in the prevalence of IPIs among children in Ethiopia over the last two decades (22 years). The burden of infection was higher among school-age children compared to preschool-age children (52% vs.30%, p = 0.002), however, it was similar in males and females as well as in urban and rural inhabitants. Poly-parasitism was observed in 16% of preschool and school-age children while, single infection was documented in 36% of the children participated in the study.

The overall pooled prevalence estimate (48%) observed in the present systematic review and meta-analysis is similar to the study from Nigeria (54.8%) [106], Rwanda (50.5%) [107], Afghanistan(47.6%) [108],Syria (42.5%) [109] and in Palestine (40.5%) [110]. However, the finding of this systematic review and meta-analysis is higher than that of Cameron(24.1%) [111], Rwanda (25.4%) [112], Iran (38%) [113], Turkey(31.7–37.2%) [114] and Egypt (26.5%) [115]. The difference might be attributed to socio-economic status, poor hygiene and sanitary facilities, weather, climate and environmental factors. For example, a study in Ethiopia showed that Ascaris lumbricoidesinfections were more common in children living in households with lower incomes (prevalence ratio = 6.68, 95% CI = 1.01–44.34) and that Giardia lamblia infections were more common in children living in households that used an unprotected water source (prevalence ratio = 1.95, 95% CI = 0.96–3.99) [32]. In addition, most Ethiopian communities have the habit of consuming uncooked meat, which mightincrease the risk of exposure to human helminths. Many of Ethiopian population where the studies conducted involved in irrigation activities for the cultivation of vegetables during the dry season. This irrigation canals create media for the reproduction of vector snails, which might be the cause of the appearance of endemicity of Trematodes infections in the area. It might also be attributed to the specificity and sensitivity of the diagnostic methods employed by the individual studies.

The meta-regression of prevalence of IPIs over time showedsignificant decreasing trends in each 6-years block by 17% (95% CI: 2.5 to 32%) and this declined prevalence was probably due to socioeconomic development, improvement in sanitation and large-scale deworming programs. Many studies from around the world have reported a significant decreasing trend in the prevalence of overall IPIs in recent years,such as the global burden of disease study [5], study from Burkina Faso [116], Nepal [117], Brazil [118] and other from 43 Sub-Saharan [119]. Despite many initiatives and efforts to introduce mass deworming program and improvement in water quality and sanitation, IPIs are still prevalentand the decrease in trend is less than that of other countries (Ethiopia 42% in 2016–2019 vs. Nepal 20. 4% in 211–2015 and Brazil 23.8% in 2010–2011). This might be possibly due to insufficient financial supports in implementation of the strategies that have been known to reduce the infection such as access to safe water supply, personal hygiene and sanitation, deworming and public health awareness.. In addition, lack of political commitment, social and environmental factors might also contribute for the higher prevalence of IPIs in the country. Inadequate community involvement and ownership of control activities are also another possible reason.

The prevalence of IPIs in school-age children was (52%), which was significantly higher than in preschool-age children (30%). This is similar to the study by Jayarani 2014 [120] and Workneh 2014 [121], but opposite to the study by Daryani 2017 [113]. School children carry the heaviest burden of the intestinal parasite associated morbidity due to their habits of playing or handling of contaminated soils, eating with soiled hands, unhygienic toilet practices, drinking and eating of contaminated water and food [22] compared to preschool-age children who usually cared by families. The current control efforts in Ethiopia usually target school-age children, but a significant proportion of preschool-agechildren (30% in this study) were also infected and can be source for the re-infection of treated school-age children. Therefore, it worthy revising the national control program based on regional and national prevalence which included preschool children and other population at risk.

In the present study, the prevalence of IPIs in females (22%) was similar to males (24%), which is similar to the study by Gelaw 2013 [45], but in contrast to study by Daryani 2017 [113] in Iran. In Iran, report indicated that more females have (30.9%) have IPIs than males (16.5%). The difference might be due to cultural and behavioral difference between the two countries.

The distribution of IPIs in this study was relatively similar in both urban and rural areas. This might be due to absence of proper human waste disposal systems, the shortage of safe water supply, the social and poor environmental or personal hygiene in many unplanned urban areas in Ethiopia in addition to similarity of eating habit and life style of both urban and rural areas of the country. So far, reports from Africa and South Asia countries are conflicting. Some were reported higher infection rates of IPIs in rural areas compared to urban areas [122–126] and others reported higher rate of infections in urban children [127]. In fact, comparable data on IPIs in urban and rural settings are very limited. For instance, only 13 studies out of 83 studies included in this meta-analysis were reported prevalence of IPIs in both urban and rural areas and therefore, indicating more work to be done in the future to resolve this issue.

We estimated the geographical distribution and identified high risk areas that should be prioritized control interventions, which complement global efforts towards elimination of IPIs infections by 2020. In addition, this work also highlighted the need for survey in areas where data are not available such as Somalia region, Afar region, Harari, Dire Dawa city and Gambella region or scarce (Addis Ababa city and Benishangul-Gumuz region). The essence of current systematic review and meta- analysis of IPIs data analysis among preschool and school-age children in Ethiopian were to support the efforts undertaken to control and eliminate neglected tropical diseasesby nurturing or supplementing useful national epidemiological data. We hope that the findings of current study provide valuable information to the policymakers, National Health Bureau and other concerned bodies about national and regional distribution and their prevalence in Ethiopia preschool and school-children.

There are a few limitations of the present meta-analysis, which may affect the results. First of all, the review protocol is not registered which could be source of bias.. It is prudent to interpret the results of this study as 37(44.6%) of the included studies were low quality based on our quality assessment criteria. In all of studies included in this review, single stool sample examination were used despite multiple stool samples recommendation for standard diagnosis and therefore, possible underestimation of the prevalence. There is also substantial heterogeneity observed between the studies that affect the interpretation of the results. However, we did meta-regression analyses on various sources including geographical distribution, age category and year of publication. These might comefrom age category (P = 0.002) and year of publication (P = 0.023) but not from geographic distribution (p = 0.56).

Conclusion

Intestinal parasite infections are highly prevalent and well distributed across the regional states of Ethiopia. Southern and Amhara regional states carry the highest burden. Although school-age children have higher prevalence of IPIs compared to preschool-age children, the prevalence is still unacceptably higher among preschool-age children. We observed a gradual, but significant decrease in prevalence of IPIsamong preschool and school-agein Ethiopian in the last two decades with no significant difference between males and females. The prevalence in the most recent 6 years was around 42% compared to 71% in the late 1990s.Place of residence has no effect on the burden of IPIs among preschool and school-age in Ethiopian. Sixteen percent (16%) of preschool and school-age children had concurrent poly-parasitism infections.

Supplementary information

12889_2020_8222_MOESM1_ESM.docx (185KB, docx)

Additional file 1. Forest plot showing prevalence of intestinal parasite infections among rural preschool and school-age children in Ethiopia.

12889_2020_8222_MOESM2_ESM.docx (180KB, docx)

Additional file 2. Forest plot showing prevalence of intestinal parasite infections among Urban Ethiopia children.

12889_2020_8222_MOESM3_ESM.docx (386KB, docx)

Additional file 3. Forest plot showing prevalence of intestinal parasite infections among male Ethiopian children.

12889_2020_8222_MOESM4_ESM.docx (376KB, docx)

Additional file 4. Forest plot showing prevalence of intestinal parasite infections among female Ethiopian children.

12889_2020_8222_MOESM5_ESM.docx (375.6KB, docx)

Additional file 5. Forest plot showing prevalence poly-parasitism infections among Ethiopian children.

12889_2020_8222_MOESM6_ESM.docx (362.9KB, docx)

Additional file 6. Forest plot showing prevalence intestinal parasite infections with single species of parasite among Ethiopian children.

Acknowledgements

We thank Dr. Kefiyalew Getahun for his contribution in constructing geographical map of Ethiopia.

Abbreviations

CI

Confidence interval

GRADE

Grading of Recommendations Assessment, Development and Evaluation

IPIs

Intestinal parasite infections

MDA

Mass drug administration

NGOs

Non-governmental organizations

PRISMA

Preferred Reporting Items for Systematic Reviews and Meta-Analyses

STHs

Soil-transmitted helminths

Authors’ contributions

LCH and ZM conceived the study. LCH and YA extracted the data, and independently decided for inclusion or exclusion, and in events of disagreement, ZM helped to resolve. LCH and DE performed all the statistical analyses. LCH and YA prepared manuscript with the help from DE. All authors read and approved the final manuscript.

Funding

We did not receive any funding support for this work.

Availability of data and materials

The datasets used and/or analyzed during the current study available from the corresponding author on reasonable request.

Ethics approval and consent to participate

None applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Footnotes

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Legese Chelkeba, Email: Legese.chelkeba@gmail.com.

Zeleke Mekonnen, Email: Zeleke.Mekonnen@ju.edu.et.

Yonas Alemu, Email: alemuyonas@yahoo.com.

Daniel Emana, Email: Daniel.emana@ju.edu.et.

Supplementary information

Supplementary information accompanies this paper at 10.1186/s12889-020-8222-y.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

12889_2020_8222_MOESM1_ESM.docx (185KB, docx)

Additional file 1. Forest plot showing prevalence of intestinal parasite infections among rural preschool and school-age children in Ethiopia.

12889_2020_8222_MOESM2_ESM.docx (180KB, docx)

Additional file 2. Forest plot showing prevalence of intestinal parasite infections among Urban Ethiopia children.

12889_2020_8222_MOESM3_ESM.docx (386KB, docx)

Additional file 3. Forest plot showing prevalence of intestinal parasite infections among male Ethiopian children.

12889_2020_8222_MOESM4_ESM.docx (376KB, docx)

Additional file 4. Forest plot showing prevalence of intestinal parasite infections among female Ethiopian children.

12889_2020_8222_MOESM5_ESM.docx (375.6KB, docx)

Additional file 5. Forest plot showing prevalence poly-parasitism infections among Ethiopian children.

12889_2020_8222_MOESM6_ESM.docx (362.9KB, docx)

Additional file 6. Forest plot showing prevalence intestinal parasite infections with single species of parasite among Ethiopian children.

Data Availability Statement

The datasets used and/or analyzed during the current study available from the corresponding author on reasonable request.

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