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Intestinal parasitic infections and associated factors among pregnant women in Ethiopia: a systematic review and meta-analysis

Abstract

Background

Intestinal parasitic infections (IPIs) are public health problems widely distributed in the world and cause significant morbidity and mortality; many of which occur among women of reproductive age. IPIs caused by helminthes and protozoan parasites are common among pregnant women. Data on the national pooled prevalence of intestinal parasites and associated factors during pregnancy is not documented well in Ethiopia. This review aims at summarizing evidences on the burden of IPIs and associated factors among pregnant women in Ethiopia.

Methods

Published and unpublished studies were thoroughly searched at MEDLINE/PubMed, EMBASE, Google Scholar, CINAHL, Cochrane library and Science Direct. In addition, repositories of Addis Ababa, Gondar and Jimma Universities were searched. Eligible studies were selected following the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guideline. The pooled prevalence of intestinal parasites and summary odds ratios (ORs) were determined with 95 % confidence intervals (CI). Sub-groups analyses were done based on study region, types of parasites, methods of stool examination and study setting. The statistical analyses were performed using STATA version 14.0 software.

Results

Among 168 retrieved studies, 31 studies with a total population of 12,118 pregnant women were included. The estimated pooled prevalence of IPIs among pregnant women in Ethiopia was 27.32 % (95 % CI: 20.61, 33.87 %). In the subgroup analysis, Oromia and Amhara regions had the highest prevalence with a 29.78 % (95 % CI: 15.97, 43.60) and 29.63 % (95 % CI: 15.37, 43.89); respectively. In addition, studies conducted in the community showed higher prevalence than institution based studies (49.93 % Vs 24.84 %; respectively). The most prevalent type of intestinal parasite identified were Hookworm followed by Ascaris lumbricoides with a pooled prevalence of 11.2 and 10.34 %, respectively. In our analysis; residence, being bare footed, lack of hand washing habit and eating uncooked/raw vegetables were significantly associated with IPIs among pregnant women in Ethiopia.

Conclusions

Prevalence of IPIs during pregnancy is relatively high in Ethiopia. Poor hygienic practices were identified as risk factors. Based on our finding, targeted preventive measures shall be considered so as to prevent morbidity and mortality due to IPIs.

Peer Review reports

Background

IPIs are public health problems widely distributed throughout the world causing significant morbidity, many of which occur among women of reproductive age. Pregnant women are one of high-risk population for these infections [1]. IPIs caused by helminths and protozoan parasites are common among pregnant women and experience more severe infections [2]. However, the severity depends on different factors, including parasitic load, species, inter-pregnancy intervals, nutritional status, poor hygiene and lack of safe drinking water, climate, poverty, immunity status, and the presence of co-existing infections [2,3,4,5,6,7,8].

Physiological changes during pregnancy modify the maternal immunity that brings tolerance to the growing fetus and susceptibility to different infections. IPIs are common during pregnancy that aggravates the effect leading to “a double burden to carry” and causes serious problems to the mother as well as to the embryo/fetus [1, 9]. Moreover, IPIs might cause anemia; induce deficiencies of iron, total energy, protein, folate and zinc all of which results in low pregnancy weight gain and intrauterine growth retardation (IUGR), greater risks of infection, low birth weight (LBW) and higher perinatal mortality rates [1, 10,11,12,13].

IPIs are reportedly identified as the leading causes of maternal mortality in developing countries especially in the tropics and subtropics [9, 14, 15]. A recent systematic review and Meta-analysis on global prevalence and associated risk factors of IPIs revealed that IPIs in pregnant women is high especially in low and middle income countries [16]. Many other studies were conducted to assess the burden of soil-transmitted helminths (STH) and their effect during pregnancy. Preventive chemotherapy (PC) was introduced as a control program in order to reduce the burden of the infection, but it has been neglected for at-risk women of reproductive ages. The overall coverage of PC was reported as less than 75 % in Ethiopia [17] howing the possibility of the high burden of intestinal parasites. Although it is expected to be high, data on the national pooled prevalence of intestinal parasites and associated factors during pregnancy is not yet documented well in Ethiopia. Therefore; this systematic review and Meta-analysis aims at providing summarized evidence on the burden of IPIs and associated factors among pregnant women in Ethiopia.

Methods

Data Bases and Search strategy

Both Published and unpublished studies regarding the magnitude of IPIs and associated factors among pregnant women in Ethiopia were thoroughly searched by two authors (ZA and AM) at databases of MEDLINE/PubMed, EMBASE, Google Scholar, CINAHL, Cochrane Library and Science Direct. Additionally, repositories of Addis Ababa University, University of Gondar and Jimma University were searched manually to get unpublished student research works related to the topic. Reference lists of eligible studies were checked to maximize the inclusion of relevant studies. The search was not bounded by year of publication. As a result, all articles published and/or reported up to 25th May, 2020 were included. The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) checklist was strictly followed to select potential studies (Fig. 1).

Fig. 1
figure1

PRISMA chart flow showing article selection process

“Prevalence” “Magnitude”, “Epidemiology”, “Intestinal Parasite”, “Intestinal parasitosis”, “Helmenthiasis”, “Hookworm” “ Ascaris lumbricoides OR A. lumbericoids”, “Schistosomia Mansoni OR S. mansoni”, “ Giardia lamblia OR G. lamblia”, “ Strongyloides stercolaris OR S. stercolaris”, “Entamoeba histolytica OR E. hisolytica”, “ Trichuris trichiura OR T. trichiura”, “ Hymenolepis nana OR H. nana”, “Taenia species”, “Enterobius vermicularis OR E. vermicularis”, “Associated Factors”, “Determinants” “Pregnant Women”, “Pregnant Mother” and “Ethiopia” were the key searching terms employed independently and/ or in combination by Boolean operators: “OR” or/and “AND” to bring key concepts together to identify relevant papers. Particularly, studies from MEDLINE/PubMed database were searched by using the following Medical Science Heading (MeSH) terms: (((“parasitic infection“[All Fields] OR “intestinal parasite“[All Fields]) OR (“intestinal diseases, parasitic/epidemiology” [MeSH Terms] OR “intestinal diseases, parasitic“[MeSH Terms])) AND ((((“pregnant women” [All Fields] OR “pregnant mothers“[All Fields]) OR “pregnant mothers attending anc“[All Fields]) AND “pregnant women attending anc“[All Fields]) OR ((“pregnant women“[MeSH Terms] OR “pregnant women/epidemiology“[MeSH Terms]) OR “mothers“[MeSH Terms]))) AND “Ethiopia“[All Fields]. EndNote X7 was also used to manage duplication of articles.

Inclusion criteria

  • Language of publication/written: English.

  • Year of publication/report: Up to May 25th of 2020.

  • Study design: observational studies (cross-sectional, case-control and cohort).

  • Outcome: magnitude of IPIs and/ or associated factors.

  • Study population: Pregnant women.

  • Study setting: At (institution or community based).

  • Study country: Ethiopia.

  • Diagnostic modality: Stool examination (either wet mount or concentration or both).

  • Type of parasite: Either protozoa or helminthes or both

  • Types of articles: Both published and unpublished.

  • Types of publication: Peer reviewed, full text articles.

Exclusion criteria

  • Articles which failed to report the number of study participants and number of cases.

  • Inaccessible full text articles due to non-responsiveness of the corresponding authors upon frequent inquiry through email by two authors (ZA and AM).

  • Systematic reviews and meta-analysis.

  • Articles that did not provide calculable prevalence or ORs for associated factors.

Data extraction

Data pertaining authors' to name with publication year, study period, study design, study setting, study area/region, technique of stool examination, sample size, numbers of pregnant women infected with intestinal parasites and or prevalence of IPIs and species of parasites isolated were extracted from the eligible articles using Microsoft Excel 2013 sheet especially designed for this study. Similarly, a separate data extraction tool was developed for each identified associated factors which contain authors name and publication year. Two by wo tables were also employed to obtain the odds ratio from each study. All associated factors reported by at least two studies were included for pooled analysis.

Quality assessment

Three authors, (ZA, AM and HD), rated the quality of included studies utilizing Newcastle – Ottawa Scale which enables to assess the quality of each article by their methodological merit, comparability caliber and outcome excellence [18]. In due process, arguments between the authors were settled through in-depth discussion and articles were included upon consensus.

Statistical analysis

The extracted data were transferred to STATA software version 14.0 to analyze the pooled prevalence of IPIs and odds ratios of the associated factors. Heterogeneity among included studies was assessed using percentage of variance (I2) and P-values. Random effect model was employed to estimate the pooled prevalence of intestinal parasites and summary odds ratios of factors associated with infections.

Begg’s rank test and Egger’s regression intercept tests were also carried out to indicate the correlation between the effect sizes and sampling variance in order to determine publication bias.

Subgroup analysis was done based on study region, types of parasites (helminthic, protozoa or both species), technique of stool examination (formalin-ether concentration, direct wet mount, or both and others) and study setting (institution or community based).

Protocols and registration

This systematic review and Meta-analysis is registered on PROSPERO under a registration number of CRD42020189115 and can be accessed at https://www.crd.york.ac.uk/PROSPERO.

Results

Characteristics of the included articles

A total of 31 studies were included in this systematic review and meta-analysis. The number of pregnant women participated in the studies ranged from 85 to 783 [19, 20] constituting a total population of 12,118. The reported prevalence of IPIs was ranging from 7.3 % [21, 22] to 76.0 % [20]. Twenty nine studies [4, 5, 10, 12, 19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43] were cross-sectional while the rest two were case-controls [11, 44]. The studies were published from 2013 up to 2020. Regarding geographical distribution, 10 studies were reported from Amhara region [4, 10, 20, 25, 33, 34, 36,37,38, 40], 8 from SNNPR [23, 26,27,28,29, 42,43,44], 8 from Oromia [5, 11, 12, 24, 32, 35, 39, 41], 4 from Tigray [19, 22, 30, 31] and One from Addis Ababa [21] (Table 1).

Table 1 General characteristic of the included articles for systematic review and meta-analysis pertaining magnitude and associated factors of IPIs among pregnant women in Ethiopia

Pooled prevalence of intestinal parasitic infection among pregnant women in Ethiopia

The estimated pooled prevalence of IPIs among pregnant women in Ethiopia is 27.32 % (95 % CI: 20.61, 33.87; I2 = 98.9 % p = < 0.001) (Fig. 2). Statistically significant heterogeneity was observed in the estimation of this pooled prevalence. Begg’s rank and Egger’s regression tests were carried out to statistically determine publication bias [45]. Based on the results, absence of significant publication bias was declared objectively with P = 0.068 and P = 0.063, consecutively.

Fig. 2
figure2

Forest plot of the pooled prevalence of IPIs among pregnant mothers in Ethiopia

IPIs and anemia

Among the included articles 16 of them [5, 10,11,12,13, 21, 22, 25, 26, 28, 33, 35, 37, 38, 41, 44] reported that IPIs are significantly associated with anemia during pregnancy while 4 studies [27, 29, 34, 43] revealed that there is no association between occurrence of anemia among pregnant mothers who contracted IPIs. A single study disclosed that IPIs during pregnancy are significantly associated with maternal under-nutrition [36].

Types of intestinal parasite

In this study, the most prevalent type of intestinal parasite identified was Hookworm followed by Ascaris lumbricoides with a prevalence of 11.12 % (95 %CI: 8.21, 14.02) and 10.34 (95 %CI: 7.09, 13.59); respectively. The least reported parasites are Enterobius vermicularis and Taenia species (Table 2).

Table 2 Pattern of Intestinal parasites among pregnant women

Subgroup analysis

A subgroup analysis based on study regions revealed that Oromia had the highest prevalence estimate accounting 29.78 % (95 % CI: 15.97, 43.60) closely followed by Amhara region 29.63 % (95 % CI: 15.37, 43.89), Tigray region 27.74 % (95 % CI: 6.56, 48.93) and SNNPR 24.23 % (95 % CI: 17.61, 30.85) (Fig. 3). Another subgroup analysis by study setting showed higher prevalence in studies done in the community than studies done institutions with a pooled prevalence of 49.93 % (95 %CI: 20.49, 79.37) and 24.84 % (95 %CI: 19.51, 30.17); respectively (Fig. 4). A similar analysis depending on the technique of stool examination indicates a combination of formalin-ether concentration and direct wet mount reported a higher prevalence of IPIs (35.99 %; 95 % CI: 26.22 ,45.78) than studies that used a single stool examination to diagnose intestinal parasites (Fig. 5).

Fig. 3
figure3

Forest plot of subgroup analysis based on regions

Fig. 4
figure4

Forest plot of subgroup analysis based on study setting

Fig. 5
figure5

Forest plot of subgroup analysis based on techniques of stool examination

Factors associated with intestinal parasitic infection among pregnant women in Ethiopia

Our analysis identified that residence area, being bare footed, hand washing habit and eating uncooked/raw vegetables have significant association with the occurrence of IPIs among pregnant women. Pregnant women from rural areas were 6.3 more likely to develop IPIs when compared to urban dweller pregnant mothers (OR = 6.31; 95 % CI: 20, 32.99; P = 0.002) (Fig. 6 A). Likewise, a barefooted women were 2.79 times more likely to be infected with IPIs than those who wore shoes (OR = 2.79; 95 % CI: 1.82, 9.48; P = 0.01) (Fig. 6B). Similarly; pregnant women who had no hand washing habit and who consumed uncooked/raw vegetables were more likely to be infected with intestinal parasites compared to their counterparts (OR = 3.02 ; 95 % CI: 1.64, 14.33; P < 0.001) (Fig. 6 C) and (OR = 1.24; 95 % CI: 1.65, 2.37; P < 0.001) (Fig. 6 C); respectively.

Fig. 6
figure6

Forest plot indicating odds ratio of factors associated with intestinal parasitic infection among pregnant women in Ethiopia. (A) Residence, (B) Bare foot, (C) Hand washing habit and (D) consume raw vegetables.

Discussion

Women living in low-income countries are at a higher risk of acquiring IPIs that leads to severe anemia. This scenario will put both the mother and the baby at higher risk of morbidity and mortality. This study was conducted to summarize the current evidence of IPIs and associated factors among pregnant women in Ethiopia.

31 eligible studies that have quantified the magnitude of IPIs were included. Accordingly, the pooled prevalence of IPIs among pregnant women in Ethiopia was estimated to be 27.32 %. However, this pooled prevalence is less than studies from Brazil, where 57.1 % pregnant women were harbored at least one parasite [46],Cameroon (31.91 %) [47],India (42.67 %) [48] and Colombia (41 %) [49].

But, our finding is higher than reports from Kenya (24 and 13.8 %) [50, 51], Ghana (23.0 %) [52], Nigeria (20.8 %) [53], Sudan (13.0 %) [54] and other multicounty studies (20 %) [55]. These differences might be attributed to socioeconomic status, poor hygiene and sanitary facilities, weather, climate and environmental factors in the countries. It is also estimated that more than one-third of Sub-Sahara population are infected with at least one species of helminths [56]. Though pregnant women are vulnerable to IPIs, being pregnant was not yet regarded as a significant risk factor for acquiring enteric parasitic infections in Benin [57].

Hookworm and Ascariasis infection were the most prevalent in this review. Similarly, a global systematic review and meta-analysis identified Hookworm and Ascaris lumbricoides as the leading helminths affecting pregnant women while Giardia lamblia and Entamoeba histolytica lead protozal infection [16]. The most prevalent types of intestinal parasite identified among pregnant women were Ascaris lumbricoides followed and Hookworm in Kenya and Benin [51, 57]. Another study in Kenya identified Hookworm as one of the most common infestation at the first ANC visit [50]. Giardia lamblia and Ascaris lumbricoides in Colombia [49], Schistosoma mansoni and Trichuris Trichiura in Ghana [58] were the most prevalent parasitic infections. Trichuris trichiura was reported as a predominant parasite followed by A. lumbricoides in other study [59] and A. lumbricoides was dominantly identified parasites followed by T. trichiura Venezuela [60].

In addition, our subgroup analysis indicated that the rates of IPIs among pregnant women varied across different regions of the country, study settings and technique of stool examination. As a result, the prevalence is higher in Oromia and Amhara regional state.

Studies conducted in the community showed a higher prevalence than studies done in institutions with a pooled prevalence of 49.93 % (95 %CI: 20.49, 79.37) and 24.84 % (95 %CI: 19.51, 30.17); respectively. This might be related with inadequate water supply and poor sanitation [61]. On the other hand, studies that used a combination of formalin-ether concentration and direct wet mount stool examination techniques reported a higher prevalence of IPIs (35.99 %; 95 %CI: 26.22, 45.78) than studies that used a single stool examination to diagnose intestinal parasites. This evidenced that the detection rate of intestinal parasites improved by concentrating stool samples [39].

Different factors for IPIs were analyzed and the pooled odds ratio was summarized. As a result, rural residents, being bare footed, poor hand washing habits and eating uncooked/raw vegetables have significant association with the occurrence of IPIs among pregnant women in Ethiopia. Similarly, the high occurrence of parasitic infection has been related to the poor hygiene condition [46] and residence area [16, 47] in other studies. It is also evidenced that factors influencing the continuous transmission of IPIs in sub-Saharan countries include poor sanitation and hygiene and non-availability of potable water for domestic use [53]. In line with our analysis, pregnant women who practiced hand washing regularly had lesser infection in India, Kenya and Benin [48, 51, 57].

Contradicting to this view, the prevalence of intestinal parasites was almost same in both rural and urban pregnant women in India [48]. The finding of this review was consistent with studies in Benin where pregnant women who consume uncooked/raw vegetables from food vendors were more likely to be infected with intestinal parasites. However, in contrary to our review result; being barefooted was not significantly affect the prevalence of IPIs [57]. Consuming unwashed vegetable and being barefooted were associated with IPIs among pregnant women [59].

In line with a review conducted in Sub-Saharan countries [53, 56], we also found that the odds of IPIs were found to be higher in pregnant mothers living in rural areas. Because, place of residence, usually determines people’s lifestyles, income, social and cultural activities, and most notably their health conditions.

Strengths and limitations

Our meta-analysis tried to elucidate a national figure on prevalence of IPIs during pregnancy. It included studies done both at institution and community settings. Both cros-sectional and case control stud designs were included which enabled us to identify temporal relationship among predictors and outcome variables. As per our search, this is the first analysis done in Ethiopia. However, this meta-analysis is done only on 5 regions of Ethiopia and as a result; the whole image of the problem might be under represented.

Conclusions

Our systematic review and meta-analysis has estimated a high prevalence of IPIs during pregnancy in Ethiopia. The result indicates the need for priority interventions targeted to improve maternal health during pregnancy. Investing in maternal health is also a key strategy to reduce low birth weight and preterm birth. Apart from socio- economic factors, IPIs during pregnancy are related with poor hygienic practices, being barefooted and eating habits of raw vegetables. Therefore, an optimal personal hygiene and developing shoes wearing habit by the mothers is essential to meet both maternal and child requirements and reduce adverse health consequences in addition to spaced pregnancy. To prevent anemia, pregnant women are advised to take iron, folate supplements, eat iron-rich foods, and prevent intestinal worms.

Availability of data and materials

The datasets used during the current study are available at the corresponding author upon reasonable request.

Abbreviations

OR:

odds ratio

CI:

confidence interval

IPIs:

Intestinal parasitic infections

IUGR:

Intrautrine growth retardation

STH:

soil-transmitted helminths

PC:

preventive chemotherapy

PRISMA:

preferred reporting items for systematic review and meta analysis

SNNPR:

southern national, nationalities and peoples region

ANC:

antenatal care

References

  1. 1.

    Alfonso J. Rodr´ıguez-Morales RABea. Intestinal Parasitic Infections among pregnant women in Venzuela. Infectious Diseases in Obstetrics Gynecology. 2006;2006:1–5.

    Google Scholar 

  2. 2.

    Nipurte Roopal PS, Koticha Avani N, Gita, Mehta Preeti. Correlation of sociodemographic factors and intestinal parasites in pregnant women. Int J Res Med Sci. 2020;8(1):244–51.

    Article  Google Scholar 

  3. 3.

    H. MPAIRWE RTAE. Pregnancy and helminth infections. Parasite Immunol. 2014;36:328–37.

    Article  Google Scholar 

  4. 4.

    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(1):530.

    Article  Google Scholar 

  5. 5.

    Ejeta E, Alemnew B, Fikadu A, Fikadu M, Tesfaye L, Birhanu T, et al. Prevalence of anaemia in pregnant womens and associated risk factors in Western Ethiopia. Food Sci Qual Manag. 2014;31(6):82–91.

  6. 6.

    Susana Vaz Nery AJP, Ebba, Abate, et al The role of water, sanitation and hygiene interventions in reducing soil-transmitted helminths: interpreting the evidence and identifying next steps. Parasites Vectors. 2019;12(273):1–8.

  7. 7.

    Akinbo FOOT, Okaka CE, Oriakhi MO. Co-infection of malaria and intestinal parasites among pregnant women in Edo State, Nigeria. J Med Trop. 2017;19:43–8.

    Article  Google Scholar 

  8. 8.

    Nigatu Tuasha1 EH, Berhanu Erko and Beyene Petros. Comorbidity of intestinal helminthiases among malaria outpatients of Wondo Genet health centers, southern Ethiopia. BMC Infectious Diseases. 2019;19(659):1–8.

  9. 9.

    Ntombela JMT-GaNP. A Double Load to Carry: Parasites and Pregnancy. South Afr J Infect Dis. 2014;29(2):52–5.

    Google Scholar 

  10. 10.

    Asrie F. Prevalence of anemia and its associated factors among pregnant women receiving antenatal care at Aymiba Health Center, northwest Ethiopia. Journal of blood medicine. 2017;8:35.

    Article  Google Scholar 

  11. 11.

    Tulu BD, Atomssa EM, Mengist HM. Determinants of anemia among pregnant women attending antenatal care in Horo Guduru Wollega Zone, West Ethiopia: Unmatched case-control study. PloS one. 2019;14(10):e0224514.

    CAS  Article  Google Scholar 

  12. 12.

    Kefiyalew F, Zemene E, Asres Y, Gedefaw L. Anemia among pregnant women in Southeast Ethiopia: prevalence, severity and associated risk factors. BMC Res Notes. 2014;7(1):771.

    Article  Google Scholar 

  13. 13.

    Mengist HM, Zewdie O, Belew A. Intestinal helminthic infection and anemia among pregnant women attending ante-natal care (ANC) in East Wollega, Oromia, Ethiopia. BMC Res Notes. 2017;10(1):440.

    Article  Google Scholar 

  14. 14.

    Samuel Crowther Kofi Tay EANaWW. Parasitic infections and maternal anaemia among expectant mothers in the Dangme East District of Ghana. BMC Res Notes. 2017;10(3):1–9.

  15. 15.

    Hopkins CH. Pregnant with Parasites: Assessing Parasitic Infections in Pregnant Women of the Kwale District. Independent Study Project (ISP) Collection, 1491. 2013.

  16. 16.

    Taghipour A, Ghodsian S, Jabbari M, Olfatifar M, Abdoli A, Ghaffarifar F. Global prevalence of intestinal parasitic infections and associated risk factors in pregnant women: a systematic review and meta-analysis. Transactions of the Royal Society of Tropical Medicine and Hygiene. 2020.

  17. 17.

    WHO. 2030 targets for soil-transmitted helminthiases control programmes. Geneva: World Health Organization. CC BY-NC-SA 3.0 IGO. Neglected tropical diseases. 2019.

  18. 18.

    Luchini C, Stubbs B, Solmi M, Veronese N. Assessing the quality of studies in meta-analysis: advantages and limitations of the Newcastle Ottawa Scale. World J Meta-Anal. 2017;5:1–48.

    Google Scholar 

  19. 19.

    Gebreegziabiher D, Desta K, Desalegn G, Howe R, Abebe M. The effect of maternal helminth infection on maternal and neonatal immune function and immunity to tuberculosis. PloS one. 2014;9(4):1–7.

  20. 20.

    Feleke BE, Jember TH. Prevalence of helminthic infections and determinant factors among pregnant women in Mecha district, Northwest Ethiopia: a cross sectional study. BMC Infect Dis. 2018;18(1):373.

    Article  Google Scholar 

  21. 21.

    Fassil R. Prevalence of Anemia Among Pregnant Women Attending Antenatal Care at Selam Health Center. Addis Ababa: Addis Ababa University; 2016.

    Google Scholar 

  22. 22.

    Kebede A, Gerensea H, Amare F, Tesfay Y, Teklay G. The magnitude of anemia and associated factors among pregnant women attending public institutions of Shire Town, Shire, Tigray, Ethiopia N. 2018. BMC research notes. 2018;11(1):1–6.

  23. 23.

    Bolka A, Gebremedhin S. Prevalence of intestinal parasitic infection and its association with anemia among pregnant women in Wondo Genet district, Southern Ethiopia: a cross-sectional study. BMC Infect Dis. 2019;19(1):483.

    Article  Google Scholar 

  24. 24.

    Yesuf DA, Abdissa LT, Gerbi EA, Tola EK. Prevalence of intestinal parasitic infection and associated factors among pregnant women attending antenatal care at public health facilities in Lalo Kile district, Oromia, Western Ethiopia. BMC Res Notes. 2019;12(1):735.

    Article  Google Scholar 

  25. 25.

    Alem M, Enawgaw B, Gelaw A, Kena T, Seid M, Olkeba Y. Prevalence of anemia and associated risk factors among pregnant women attending antenatal care in Azezo Health Center Gondar town, Northwest Ethiopia. 2013.

  26. 26.

    Lebso M, Anato A. Loha3 E. Prevalence of anemia and associated factors among pregnant women in Southern Ethiopia: A community based cross-sectional study. PloS one. 2017;12(12):1–11.

  27. 27.

    Bekele A, Tilahun M, Mekuria A. Prevalence of anemia and its associated factors among pregnant women attending antenatal care in health institutions of Arba Minch Town, Gamo Gofa Zone, Ethiopia: a cross-sectional study. Anemia. 2016;2016.

  28. 28.

    Gedefaw L, Ayele A, Asres Y, Mossie A. Anaemia and associated factors among pregnant women attending antenatal care clinic in Walayita Sodo town, Southern Ethiopia. Ethiopian journal of health sciences. 2015;25(2):155–64.

    Article  Google Scholar 

  29. 29.

    Getahun W, Belachew T, Wolide AD. Burden and associated factors of anemia among pregnant women attending antenatal care in southern Ethiopia: cross sectional study. BMC Res Notes. 2017;10(1):276.

    Article  Google Scholar 

  30. 30.

    Berhe B, Mardu F, Legese H, Gebrewahd A, Gebremariam G, Tesfay K, et al. Prevalence of anemia and associated factors among pregnant women in Adigrat General Hospital, Tigrai, northern Ethiopia, 2018. BMC Res Notes. 2019;12(1):310.

    Article  Google Scholar 

  31. 31.

    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(1):644.

    Article  Google Scholar 

  32. 32.

    Getachew M, Tafess K, Zeynudin A, Yewhalaw D. Prevalence Soil Transmitted Helminthiasis and malaria co-infection among pregnant women and risk factors in Gilgel Gibe dam Area, Southwest Ethiopia. BMC Res Notes. 2013;6(1):263.

    Article  Google Scholar 

  33. 33.

    Hailu T, Kassa S, Abera B, Mulu W, Genanew A. Determinant factors of anaemia among pregnant women attending antenatal care clinic in Northwest Ethiopia. Tropical diseases, travel medicine and vaccines. 2019;5(1):13.

  34. 34.

    Helion Belay AM, Tariku A, Woreta SA, Demissie GD, Asrade G. Anemia and Associated Factors among Pregnant Women Attending Prenatal Care in Rural Dembia District, North West Ethiopia: A cross-Sectional Study. Ecol Food Nutr. 2020;59(2):154–74.

    Article  Google Scholar 

  35. 35.

    Kenea A, Negash E, Bacha L, Wakgari N. Magnitude of Anemia and Associated Factors among Pregnant Women Attending Antenatal Care in Public Hospitals of Ilu Abba Bora Zone, South West Ethiopia: A Cross-Sectional Study. Anemia. 2018;2018.

  36. 36.

    Kumera G, Gedle D, Alebel A, Feyera F, Eshetie S. Undernutrition and its association with socio-demographic, anemia and intestinal parasitic infection among pregnant women attending antenatal care at the University of Gondar Hospital, Northwest Ethiopia. Maternal health neonatology perinatology. 2018;4(1):18.

    Article  Google Scholar 

  37. 37.

    Kumera G, Haile K, Abebe N, Marie T, Eshete T. Anemia and its association with coffee consumption and hookworm infection among pregnant women attending antenatal care at Debre Markos Referral Hospital, Northwest Ethiopia. PloS one. 2018;13(11):1–14.

  38. 38.

    Melku M, Addis Z, Alem M, Enawgaw B. Prevalence and predictors of maternal anemia during pregnancy in Gondar, Northwest Ethiopia: an institutional based cross-sectional study. Anemia. 2014;2014:1–9.

  39. 39.

    Mengist HM, Demeke G, Zewdie O, Belew A. Diagnostic performance of direct wet mount microscopy in detecting intestinal helminths among pregnant women attending ante-natal care (ANC) in East Wollega, Oromia, Ethiopia. BMC Res Notes. 2018;11(1):276.

    Article  Google Scholar 

  40. 40.

    Shiferaw MB, Zegeye AM, Mengistu AD. Helminth infections and practice of prevention and control measures among pregnant women attending antenatal care at Anbesame health center, Northwest Ethiopia. BMC Res Notes. 2017;10(1):274.

    Article  Google Scholar 

  41. 41.

    Tefera G. Determinants of anemia in pregnant women with emphasis on intestinal helminthic infection at Sher-Ethiopia Hospital, Ziway, Southern Ethiopia. Immunol Infect Dis. 2014;2(4):33–9.

    Google Scholar 

  42. 42.

    Tesfaye DJ. Prevalence of intestinal helminthiases and associated factors among pregnant women attending antenatal clinic of Nigist Eleni Mohammed memorial hospital, Hossana, Southern Ethiopia. Open Access Library Journal. 2015;2(07):1.

    Google Scholar 

  43. 43.

    Zekarias B, Meleko A, Hayder A, Nigatu A, Yetagessu T. Prevalence of anemia and its associated factors among pregnant women attending antenatal care (ANC) in Mizan Tepi University Teaching Hospital, South West Ethiopia. Health Science Journal. 2017;11(5):1–8.

    Article  Google Scholar 

  44. 44.

    Weldekidan F, Kote M, Girma M, Boti N, Gultie T. Determinants of anemia among pregnant women attending antenatal clinic in public health facilities at Durame Town: unmatched case control study. Anemia. 2018;2018.

  45. 45.

    Lin L, Chu H. Quantifying publication bias in meta-analysis. Biometrics. 2018;74(3):785–94.

    Article  Google Scholar 

  46. 46.

    Maria Celia Dos Santos JMC-C, Carvalho-Neto,Marcus C. M.R.LIMA And Marisa Cristina. Enteric Parasites and Commensal in Pregnant Women Seen at the University Hospital Federal University of Uberlandia, State of Minas Gerais, Brazil. 1998;40(3):193–5.

  47. 47.

    Calvin Tonga CNB. Flore Chanceline Tchanga, Jacqueline Félicité Yengue, Godlove Bunda Wepnje, Hervé Nyabeyeu Nyabeyeu, Lafortune Kangam, Larissa Nono Kouodjip, Patrick Ntonga Akono, Léopold Gustave Lehman. Schistosomiasis among pregnant women in Njombe-Penja health district, Cameroon. J Infect Dev Ctries. 2019;13(12):1150–8.

  48. 48.

    Nipurte Roopal PS, Koticha, Avani. Nataraj Gita and Mehta Preeti. Correlation of sociodemographic factors and intestinal parasites in pregnant women. International Journal of Research in Medical Sciences. 2019;8(1):244–51.

  49. 49.

    Angela FE, Aranzales KR, Guenter Froeschl. Ángela María Pinzón Rondón and Maria Delius. Prevalence and risk factors for intestinal parasitic infections in pregnant women residing in three districts of Bogotá, Colombia. BMC Public Health. 2018;2018:1–15.

  50. 50.

    Elizabeth M. McClure SRM, Mungai P, Malhotra I, King CL, Goldenberg RL, Hudgens MG. Anna Maria Siega-Riz1, Arlene E. Dent. The Association of Parasitic Infections in Pregnancy and Maternal and Fetal Anemia: A Cohort Study in Coastal Kenya. PLOS Neglected Tropical Diseases. 2014;8(2):1–8.

  51. 51.

    Wekesa AW, Muleke CSM,CI. and R. Odhiambo4. Intestinal Helminth Infections in Pregnant Women Attending Antenatal Clinic at Kitale District Hospital, Kenya. Journal of Parasitology Research. 2014;2014:1–5.

  52. 52.

    Godwin Fuseini DE. Bugre Gumah Kalifa and Dave Knight. Plasmodium and intestinal helminths distribution among pregnant women in the Kassena-Nankana District of Northern Ghana. Entomology and Nematology. 2010;1(2):19–24.

  53. 53.

    Abiola Fatimah Adenowoa BEO. Bolajoko Idiat Ogunyinkaa and Abidemi Paul Kappoa. Impact of human schistosomiasis in sub-Saharan Africa. b r a z j i n f e c t d i s 2015;19(2):196–205.

  54. 54.

    Abelrahman Khalid MAA, Abellatif Ashmaig AM, Ibrahim, Abdel-Aziz M, Ahmed I Adam. Schistosoma mansoni infection among prenatal attendees at a secondary-care hospital in central Sudan. International Journal of Gynecology and Obstetrics. 2012;116(2012).

  55. 55.

    WHO. Guideline: preventive chemotherapy to control soil-transmitted helminth infections in at-risk population groups. Geneva. Licence: CC BY-NC-SA 30 IGO. 2017.

  56. 56.

    Dadi HDDaAF. Burden and determinants of malnutrition among pregnant women in Africa: A systematic review and meta-analysis. PLOS ONE. 2019;14(9):1–19.

  57. 57.

    Frederick Olusegun Akinbo EO. Adedapo Babatunde Anibaba Ande. Intestinal Nematodes Infection among Pregnant Women in Benin City. Nigerian Journal of Experimental and Clinical Biosciences. 2020;3(2):65–70.

  58. 58.

    NANI EA. IMPACT OF SCHISTOSOMIASIS AND SOIL TRANSMITTED HELMINTH INFECTION AMONG PREGNANT. WOMEN IN THE DANGME EAST DISTRICT, GREATER ACCRA REGION. 2014.

  59. 59.

    Albert Njeru FMaSM. Status of Soil-transmitted helminthiasis among pregnant women attending antenatal clinic in Kilifi county hospital, Kenya. 2019.

  60. 60.

    Rodríguez-Morales AJ, Barbella RA, Case C, Arria M, Ravelo M, Perez H, et al. Intestinal parasitic infections among pregnant women in Venezuela. Infectious diseases in obstetrics and gynecology. 2006;2006.

  61. 61.

    Jeff rey Bethony SB, Marco Albonico, Stefan M Geiger, Alex Loukas, David Diemert, Peter J Hotez. <Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm.pdf>. lancet. 2006;367:1521–32.

    Article  Google Scholar 

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Acknowledgements

We would like to acknowledge all academic staffs of Addis Ababa University, Debre Tabor University and Bahir Dar University who helped us in this particular study.

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No funding was obtained for this study’.

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ZA responsible for design, article selection, data extraction, statistical analysis and manuscript drafting. AM, HD, GS were involved in selection of articles, statistical analysis and manuscript editing. AA reviewed the protocols, tools, analysis and manuscript editing. All the authors read and approved the final draft of the manuscript.

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Correspondence to Zelalem Animaw.

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Animaw, Z., Melese, A., Demelash, H. et al. Intestinal parasitic infections and associated factors among pregnant women in Ethiopia: a systematic review and meta-analysis. BMC Pregnancy Childbirth 21, 474 (2021). https://doi.org/10.1186/s12884-021-03908-0

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Keywords

  • Intestinal parasites
  • pregnant women
  • systematic review
  • meta-analysis
  • pregnancy
  • Ethiopia