Health Science Journal

Keywords

Pooled prevalence; Intestinal parasite; Pregnant women; Ethiopia

Background

Intestinal parasites (IP) are responsible for morbidity of about 450 million people worldwide; women of reproductive age and children in developing countries are disproportionately affected by IP. There is high burden of IP in list income countries because of poverty, lack of safe drinking water, poor hygiene, and malnutrition [1]. In developing countries, almost half the population does not have access to sanitary facilities and only most people of the world practice open defecation, which is the main risk factor for dissemination of IP in the community. In parts of Africa, only about 24% of the population residing in the rural parts of sub-Saharan Africa use improved sanitation system [2].

According to the World Health Organization (WHO) reports, more than one billion of the world’s populations are chronically infected with soil transmitted helminthes (STHs) [3]. About 40% of disease burden of all tropical infections is due to geo-helminths [4]. WHO established a prevalence of 20% as a minimum limit at which infections may be regarded as a generalized public health problem [5].

Pregnant women are at high risk of IP infection because of their close relationship with children. Also, most of these parasites are transmitted through contaminated soil and most of soil eating habit is commonly observed among pregnant women [6]. IP infections during pregnancy can affect the health of mother, fetus and child. Pregnant women often experience more severe infections than their non-pregnant counterparts because of immune-modulation and physiological changes that occur during pregnancy [7]. More than 44 million pregnancies are complicated by maternal Hookworm infection and 10 million pregnant women in Africa are infected with Schistosomiasis [8]. Several studies have been conducted to assess the prevalence and effects of intestinal helminthes among pregnant women and their children [8,9].

Untreated IP infection among pregnant women can influence the fetal immune system. In utero stimulation with helminth-derived antigens is believed to divert fetal immunity towards anergy, tolerance, or T helper 2 responses [10]. In utero exposure to helminth derived antigens has been considered as one of the risk factors in offspring for enhanced susceptibility to infections such as Tuberculosis [10]. Intestinal infection among pregnant women affects the health of mother and fetus; moreover, it shifts the immunity towards which is not protective for intracellular microbes. Therefore, we envisaged to determine the pooled prevalence of intestinal parasites among pregnant women in Ethiopia so that concerned bodies will take appropriate measure to reduce or prevent its transmission.

Methods

Search strategy

The search was conducted using six databases: PubMed, Google Scholar, HINARI and Cochrane Library by a special index search terms (medical subject headings (MeSH) "Intestinal diseases, parasitic" OR "intestinal" AND "diseases" AND "parasitic" OR "parasitic intestinal diseases" OR "intestinal" AND "parasite" OR "intestinal parasite" AND "epidemiology" OR "epidemiology" OR "prevalence" OR "prevalence" AND "gravidity" OR "gravidity" OR "pregnant" AND "ethiopia" OR "Ethiopia". The limit of language was English and search was restricted to humans only. We also screened reference lists of selected studies for any potentially relevant studies that had not been identified through the searches. The Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guideline was used to report the result of this systematic review and meta-analyses.

Inclusion criteria and exclusion criteria

Data extraction:

The data extraction was done by five researchers (SH, MM, MMA, BTT, TLA) using a standardized and pretested format. The data abstraction format included first author, study design, country, publication year, sample size, study population, the number who tested positive for intestinal parasite. Any disagreement that occurs during data extraction between researchers was handled through.

Quality assessment:

Nine point Joanna Briggs Institute (JBI) critical appraisal tool for systematic review was used to determine the quality of articles collected. The tool uses the following criteria [11]. Individual studies were assigned a score that was computed using different parameters in line with the review objectives. The responses were scored 1 for “Yes” and 0 for “Not reported”. Total scores ranged between 0 and 9. Studies with medium (fulfilling 50% of quality assessment parameter) and high qualities were included for analysis [11]. Accordingly, the overall score was 251.

Statistical analysis:

Data entry and analysis was done using STATA (version 14). The summary of the pooled prevalence of IP with 95% CI was obtained using the random effects model, due to the possibility of heterogeneity among the studies.

Results

Identified studies

Through electronic database search, we have found a total of 622 studies. Of which, 563 were excluded based on the titles and abstracts. Also 33 articles were excluded after full text review since they don’t reported prevalence of IP among pregnant women finally, 30 studies were found to be eligible and included in the meta–analysis (Figures 1 and 2). Included articles exhibited high heterogeneity according to Cochrane Q test (5820.71 test, p <0.0001) and I2 test (I2=99.5%), and Tau-squared (706.840) (P<0.0001) which is indicative to use random effects model. Eggers regression intercept test indicated evidence of publication bias (Figure 3).

Figure 1 Flow diagram of the studies included in the Metaanalysis.

Figure 2 Forest plot for the prevalence of IP among pregnant women in Ethiopia.

Figure 3 Funnel plot for the prevalence of IP among pregnant women in Ethiopia.

Study characteristics

Selected articles were published from 2009 to 2020. Also, all included publications were obtained from 5 regions and 1 Multicenter regional study, but no data was obtained from other regions (Afar, Benishangul-Gumuz and Somali). The total study populations involved in this systematic review and meta-analysis were 12,212. A total of thirty studies were considered eligible for quantitative syntheses (Table 1). A total of thirty studies were considered eligible for quantitative syntheses (Table 1). The prevalence of IP across study regions is as follows: Amhara region, 1285 (31.72%); Oromia region, 1062 (29.04%); Southern region, 868 (29.48%); Tigray, 427 (29.29%); population from Tigray; and Gambella, 95 (26.39%). The study population varied from 180 to 970,and was conducted between the years 2009-2019. The prevalence of IP in the community, and health institution was 27.37% and 53.43% respectively (Table 1).

Table 1. Prevalence of intestinal parasitic infection among pregnant women in Ethiopia.

Meta-analysis of prevalence of IP

The estimated pooled prevalence of IP among pregnant women in the current review and meta-analysis was 31.75% (95% CI: 22.20-41.30) (Figure 2). Pooled prevalence of IP among regions were as follows: Amhara, 31.72% (95% CI: 16.35-47.10); Oromia, 29.04% (95% CI; 14.09-43.99); South Ethiopia, 29.48% (95% CI: 18.27-40.70); Tigray, 29.29% (7.96-50.61); Gambella, 26.39% (21.84-30.94. The pooled prevalence within a year 2009-2016 was 34.80% (95% CI: 16.72-52.88) and within 2017-2020 29.97% (95% CI: 20.31-39.62) (Table 2). A pooled prevalence of 27.37% (20.48-34.26) from health facility and 53.43% (30.19-76.68) from community were found (Figure 4). Moreover, meta-regression model was conducted among the above study parameters to identify the possible source of heterogeneity though none of them was statistically significant.

Figure 4 Forest plot for the prevalence of IP across study sites among pregnant women in Ethiopia.

Table 2. Subgroup meta-analysis of IP prevalence in Ethiopia from 2009-2020.

Subgroup analysis of IP among pregnant women

The pooled prevalence of Hook worm was 11.46% (95%CI; 8.62- 14.30) and A. lumbricoides was 10.44% (95%CI; 8.27,12.60) (Table 3).

Table 3. The pooled Prevalence of different intestinal parasites among pregnant women in Ethiopia from 2009 to 2020.

Discussion

Parasitic infection among pregnant women can be asymptomatic or can cause anemia, deficiency of nutrients, and can affect the immune response of child [12-41]. IP infections can severely affect affect both the pregnant women and fetus. As a result, WHO recommended treatment of pregnant women for helminthic infections [41]. There are several studies addressing IP among children and pregnant women in Ethiopia; however, there is no summarized report among pregnant women so as to inform policymakers and health care providers. In this review and meta-analysis we aimed to estimate pooled prevalence of IP among pregnant women in Ethiopia.

The overall pooled prevalence of IP among pregnant women in Ethiopia is 31.75% which is higher than the lower limit prevalence (20%) set by WHO to consider IP as a public health concern [5]. The finding of this review and meta-analysis is lower than proportion of intestinal parasite among pregnant women reported from worldwide study [42]. In contrast to this review and meta-analysis, higher prevalence of intestinal parasites (73.9%) was reported from Venezuelan pregnant women [43]. It is also relatively low compared to prevalence of intestinal parasite infection (37.3%) reported from the Northwestern parts of Ethiopia [22]. Our finding is in line with finding reported Ghana (30.5%) [44].

The most prevalent parasite identified in this review and meta-analysis was Hookworm (11.46%) followed by A. lumbricoides (10.44%). The prevalence of the rest parasite such as E. histolytica, G. lamblia, T. trichiura, S. mansoni was less than 2%. Unlike the current review and meta-analysis, a higher prevalence of A. lumbricoides (57%) and low prevalence of Hookworm (8.1%) was reported from Venezuelan pregnant women [43]. High prevalence of Hookworm and A. lumbricoides could be due to the suitability of the environment along with the high fertility of A. lumbricoides and the stability of eggs in the soil.

In contrast to this review, a high prevalence of Hookworm (49.8%) was reported from pregnant women living in Gojam, Ethiopia. Moreover, the prevalence of E. histolytica/dispar (40.8%) and G. lamblia (19.1%) reported from pregnant women residing in West Gojjam is higher than our finding [22]. Study from other places also reported a high prevalence of Hookworm (19%), A. lumbricoides (17%) and T. trichiura (11%), and E. histolytica/dispar (9%) and G.lamblia (8%) [45]. These variations in prevalence of IP and proportion of parasite among pregnant women due to socio-economic differences, environmental sanitation, habits of shoe wearing, and Laboratory methods.

In this review, the pooled prevalence of IP varies slightly across different regions of Ethiopia with the highest prevalence from Amhara (31.72%) followed by Southern Ethiopia (29.48%), Tigray (29.29), Oromia (29.04%) and Gambella (26.39%). We observed relative reduction of pooled prevalence of IPs from 34.8% in 2009-2016 to 29.97% in 2017-2020 indicating some work has be done to reduce burden of IP among pregnant women in various parts of Ethiopia.

A higher prevalence of IP (53.43%) was observed among studies conducted in the community as compared to those which was conducted in health facilities (27.37%). This indicates high number of intestinal parasites are being circulated in the community and missed by health care workers. This emphasizes the importance of mass screening of pregnant women in the community to come up with true burden of IP among pregnant women plan for suitable prevention and control.

Moreover, considering that as there is no ‘gold standard’ test for detection of intestinal helminths, a variety of parasitological methods have been utilized in different parts of Ethiopia such as formalin–ether concentration technique, Kato-Katz methods which may be responsible for variation of prevalence observed in this analysis.

Conclusion

This review and meta-analysis found a high prevalence of IP among pregnant women which is greater than the minimum limit set by WHO to be considered as public health concern. The pooled prevalence we found in this review varied across different regions and study sites with highest from Amhara and community respectively. There was slight reduction of IP parasites among pregnant women from 2009-2016 to 2017-2020.

Conflicts of Interest

The authors declare there is no competing interest.

Funding Statement

We did not receive any funding for this work.

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