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. 2020 Mar 20;16(10):2472–2478. doi: 10.1080/21645515.2020.1729027

Sero-prevalence of rubella among pregnant women in Sub-Saharan Africa: a meta-analysis

Zemenu Yohannes Kassa 1,✉, Siraj Hussen 1, Solomon Asnake 1
PMCID: PMC7644194  PMID: 32195620

ABSTRACT

Background: Rubella continues to be a leading cause of vaccine-preventable congenital birth defects and permanent organ damage, especially in developing countries. For women who are infected with the rubella virus (RV) before conception or during the first trimester of pregnancy, the unborn child has up to a 90% probability of developing congenital rubella syndrome. There are limited data on the seroprevalence of the rubella virus among pregnant women in Sub-Saharan Africa. Therefore, the aim of this study was done to determine the pooled seroprevalence of rubella among pregnant women in Sub-Saharan Africa.

Methods: The PRISMA guidelines protocol was followed to write the systematic review and meta-analysis. Published studies were searched in Medline, PubMed, Google scholar, advance google and Cochrane Library. The search terms on the databases are: “rubella”OR “rubeo*”, “rubella”AND“seroepidemiology”, “seroprevalen *” OR “prevalen*”, “seroprevalen *” OR “seroimmun*”, “rubella antibod*”AND “pregnan*”, “seroprevalen *” AND “sub-Saharan Africa”.The heterogeneity of studies was weighed using Cochran’s Q test and I2 test statistics. Publication bias was assessed by using Egger’s and Begg’s test.

Results: Twenty-eight studies were included in this meta-analysis. The pooled seroprevalence of anti-RV IgG among pregnant women in Sub-Saharan African was 89.0% (95%CI: 84.6–92.3), and the pooled prevalence of anti-RV IgM among pregnant women in Sub-Saharan Africa was 5.1% (95%CI: 2.6–9.9).

Conclusion: This meta-analysis showed that seronegativity and acute infection with RV among pregnant women in sub-Saharan Africa is high compared to other studies and the WHO threshold among women of child-bearing age. This finding calls for primary health care providers to make the community aware of this rubella-susceptible group and its healthcare burden, with the desired outcome that sub-Saharan Africa countries would introduce an implementation strategy for rubella vaccination of pregnant women and women of child-bearing age.

KEYWORDS: Meta-analysis, rubella virus, pregnant women, Sub-Saharan Africa

Background

Health care has improved the introduction of different types of vaccines worldwide. Unfortunately, infectious diseases remain a major cause of maternal and child morbidity and mortality in resource-limited countries, including Sub-Saharan Africa.1 Of these, the rubella virus (RV) continues to be the main risk factor of women’s health and their fetuses during pregnancy.2 Rubella, sometimes called German measles or three days measles, is a contagious disease caused by the rubella virus.3

RV infection is a major cause of congenital birth defects and mental retardation for the unborn child. In 2015, the worldwide incidence of rubella infection was 3.3 million, including more than 100,000 cases of congenital rubella syndrome (CRS).4,5 RV infection occurring before conception, early pregnancy or at less than 11 weeks of gestational age is associated with CRS, whose symptoms include miscarriage, cataracts, heart defects, sensor neural deafness, and permanent abnormalities such as heart defects, pulmonary artery stenosis, hypoplasia, eye defects, intellectual and psychomotor disabilities, and speech defects.6-9 The highest risk of CRS occurs in countries where women of reproductive age lack immunity to the disease, neither having been vaccinated or having had rubella infection.10 For women infected with RV before conception or during the first trimester of pregnancy, the unborn child has up to a 90% probability of developing CRS.11,12

Rubella vaccine, which is cost-effective, safe and effective, is commonly available and given routinely in middle and high-income countries as part of vaccination programs, where it has eradicated the RV and CRS.13 However, it is not available in most parts of developing countries, including sub-Saharan Africa.14 A single dose of RV-containing vaccine (RCV) has been introduced in 27 countries in Africa, where RCV coverage was only 32%. In 2018, 11,787 cases of rubella and 18 cases of CRS were reported in Africa.15

There are limited data on the seroprevalence of RV among pregnant women in sub-Saharan Africa. This study is needed to describe the status of pregnant women for seroprevalence of RV among pregnant women, and it should help decision-makers, ministers of health, stakeholders, public health experts and clinicians toward the possible prevention and control of rubella infection and CRS.

Methods

Search strategy

This study used a systematic review and meta-analysis of published studies. The PRISMA guidelines protocol was followed to write this systematic review.16 Published studies were searched in Medline, PubMed, Google scholar, advance google and Cochrane Library. The search terms on the databases are: “rubella”OR “rubeo*”, “rubella”AND“seroepidemiology”, “seroprevalen *” OR “prevalen*”, “seroprevalen *” OR “seroimmun*”, “rubella antibod*”AND “pregnan*”, “seroprevalen *” AND “sub-Saharan Africa”. The limit of language was English, and the limit of the study group was human. Searching of articles was carried out from January to June 2017.

Study selection, data extraction, and quality assessment

All included studies were cross-sectional and published during 2003–2017. Study selection was done by three authors who independently reviewed the studies, and disagreements were resolved through discussion and consensus. The critical appraisal was done before the extraction of data. Data extraction was based on the Joanna Briggs Institute (JBI) critical appraisal tools,17 by which the following criteria are established: the sample frame appropriate to address the target population, appropriate sample size, adequate sample size, clearly description of study subject and setting, data analysis conducted with sufficient coverage, valid methods used for the identification of the condition, the condition measured in a standard reliable way for all participants, use of appropriate statistical analysis method, and adequate response rate which is inadequate. The low response rate was managed appropriately.17 A mean quality score was used to assess the quality of studies included in the meta-analysis. Studies that scored above the mean of the quality score were grouped into the high-quality score, and those below the mean were grouped as the low-quality score (additional file table S1).

Statistical analysis

Data entry and analysis were done using a comprehensive meta-analysis (version 3.1). The summary of the pooled prevalence of rubella virus infection with 95%CI was obtained using the random effect model, due to the possibility of heterogeneity among the studies.

Sub-group analysis

Sub-group analysis was performed based on the type of Geographical zone; (East Africa, Central Africa, Southern Africa, and West Africa), and Year of study; (2003–2007, 2008–2012, and 2013–2017).

Heterogeneity and publication bias

The heterogeneity of studies was weighed using Cochran’s Q test and I2 test statistics. A p-value <0.10 indicated heterogeneity between the studies.18 Publication bias was assessed by Egger’s and Begg’s test, and a p-value <0.05 shows publication bias.19

Results

A total of 88 articles were identified through electronic database searching. Articles were screened using their titles, abstracts and full article review. A total of 60 articles were excluded using their title, abstracts and full article review by exclusion criteria. Consequently, 28 studies were included in this meta-analysis (Figure 1).

Figure 1.

Figure 1.

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Flow diagram of the studies included in the Meta-analysis

Study characteristics of seroprevalence of rubella IgG among pregnant women

The total study population screened for anti-RV IgG was 10,616 in three regions of Sub-Saharan Africa: East Africa, West Africa, and Southern Africa (Table 2). The sample size of the study population varied from 51 to 2044. (Table 1)

Table 2.

Subgroup analysis of rubella infection among pregnant women in Sub-Saharan Africa

  Study parameters Subgroup Studies included Prevalence %(95% CI) I2% P-value
IgG Study year 2003–2007 2 95.9(94.6–97.0) 48.66 0.163
2008–2012 10 83.7(74.4.0–90.1) 97.00 <0.001
2013–2017 14 90.6(84.4–94.5) 96.98 <0.001
Geographical zone West Africa 16 88.6(81.7–93.1) 97.08 <0.001
East Africa 6 86.8(75.1–93.5) 96.70 <0.001
Southern Africa 4 93.3(84.2–97.3) 97.68 <0.001
IgM Study year 2008–2012 5 3.5(1.6–7.5) 82.97 <0.001
2013–2017 9 6.7(2.7–15.5) 96.94 <0.001
Geographical zone West Africa 11 6.9(3.3–13.9) 96.26 <0.001
East Africa 3 1.9(0.8–4.6) 65.11 0.057
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Table 1.

Sero-prevalence of rubella among pregnant women in sub-Saharan Africa: a systematic review and meta-analysis

          Rubella pre. (%)
    
Authors, publication year [Reference] Country Study design Study population Sample size IgG+ IgM+ Specimen Diagnostic methods
Makemgue (2016)20 Cameroon cross-sectional Pregnant women 400 91.75   Blood ELISA
Fokunang et al. (2010)21 Cameroon cross-sectional Pregnant women 211 88.6   Blood ELISA
Kwofie et al. (2015)22 Ghana cross-sectional Pregnant women 89 92.3 6.6 Blood ELISA
Völker et al. (2017)23 Ghana cross-sectional Pregnant women 180 79.6 4.7 Blood ELISA
Adam et al. (2013)24 Sudan cross-sectional Pregnant women 500 95.1   Blood ELISA
Hamdan et al. (2011)25 Sudan Cross-sectional Pregnant women 231 65.3 3.4 Blood ELISA
Hamdan et al. (2011)26 Sudan Cross-sectional Pregnant women 80 68.8   Blood ELISA
Ghoma et al. (2012)27 Burkina Faso Cross-sectional Pregnant women 100 77.0 1.0 Blood ELISA
Marc et al. (2013)28 Burkina Faso Cross-sectional Pregnant women 341 95.0   Blood ELISA
Tamirat et al. (2017)29 Ethiopia Cross-sectional Pregnant women 422 86.3 2.1 Blood ELISA
Kombich (2012)30 Kenya Cross-sectional Pregnant women 470 92.9   Blood ELISA
Mamvura et al. (2015)31 Zimbabwe Cross-sectional Pregnant women 51 92   Blood ELISA
Berno Mwambe et al. (2014)32 Tanzania Cross-sectional Pregnant women 350 92.6 0.3 Blood ELISA
Anna et al. (2010)33 Namibia Cross-sectional Pregnant women 2044 85   Blood EIA
Barreto et al. (2006)34 Mozambique Cross-sectional Pregnant women 974 95.3   Blood ELISA
Gubio et al. (2015)35 Nigeria Cross-sectional Pregnant women 900 63.3 4.3 Blood ELISA
Onwere et al. (2014)36 Nigeria Cross-sectional Pregnant women 345 95.4   Blood ELISA
Kolawole et al. (2014)37 Nigeria Cross-sectional Pregnant women 200 87.5   Blood ELISA
Koki (2014)38 Nigeria Cross-sectional Pregnant women 288   17.4 Blood ELISA
Oyinloye et al. (2014)39 Nigeria Cross-sectional Pregnant women 90 83.3 37.8 Blood ELISA
Amina et al. (2010)40 Nigeria Cross-sectional Pregnant women 430 97.9   Blood ELISA
Grace (2009)41 Nigeria Cross-sectional Pregnant women 534   3.9 Blood EIA
Agbede et al. (2011)42 Nigeria Cross-sectional Pregnant women 92 84.8   Blood ELISA
Adewumi et al. (2014)43 Nigeria Cross-sectional Pregnant women 272 91.54 1.84 Blood ELISA
Olajide et al. (2015)44 Nigeria Cross-sectional Pregnant women 160 93.1 38.8 Blood ELISA
Onakewhor & Chiwuzie (2011)45 Nigeria Cross-sectional Pregnant women 300 53.0 9.7 Blood ELISA
Corcoran et al. (2005)46 S. Africa Cross-sectional Pregnant women 1158 96.5   Blood ELISA
De Paschale et al. (2014)47 Benin Cross-sectional Pregnant women 283 94.0 0.0 Blood ELISA
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EIA: Enzymeimmuno Assay, ELISA: Enzyme linked immune sorbent assay

Twenty-six (93%) of the 28 studies were reported with a seroprevalence of anti-RV IgG among pregnant women, which used in this meta-analysis. The Cochran’s Q and I2 statistic for this antibody was 947.509 and 97.4% (p < .001), respectively. The pooled seroprevalence of anti-RV IgG among pregnant women was 89.0% (95%CI: 84.6–92.3) (Figure 2). Egger’s regression intercept p = .009 and Begg 0.494

Figure 2.

Figure 2.

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The forest plot sero prevalence of rubella IgG among pregnant women

Study characteristics of anti-Rv IgM among pregnant women

In this meta-analysis, a total study population screened for anti-RV IgM was 4006 in two regions of Sub-Saharan Africa: East Africa, West Africa (Table 2). The sample size of the study population was varied from 89 to 900. Fourteen (50%) of the 28 studies reported anti-RV IgM among pregnant women, which was used in the meta-analysis. The Cochran’s Q and I2 statistic for thus IgM for pregnant women was 324.508 and 96.0% (p < .001). The pooled prevalence of this IgM among pregnant women was 5.1% (95%CI: 2.6–9.9) (Figure 3). Egger’s regression intercept 0.049 and Begg p = .411

Figure 3.

Figure 3.

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The forest plot prevalence of rubella IgM among pregnant women

Subgroup analysis

The pooled seroprevalence of anti-RV IgG among pregnant women in Sub-Saharan African was 89.0% (95%CI: 84.6–92.3) (Figure 2). Subgroup analysis was carried out by different study characteristics, e.g. years of study since 2003–2007 was 95.9% (95%CI: 94.6–97.0), since 2008–2012 was 83.7% (74.4–90.1), and since 2013–2017 was 90.6% (95%CI: 84.4–94.5). Subgroup analysis by geographical region revealed that 88.6% (95% CI; 81.7–93.1) in West Africa, 86.8% (95% CI; 75.1–93.5) in East Africa, and 93.3% (95% CI; 84.2–97.3) in Southern Africa.

The pooled prevalence of anti-RV IgM among pregnant women in Sub-Saharan African was 5.1% (95%CI: 2.6–9.9) (Figure 3). Subgroup analysis was carried out by different study characteristics, e.g. years of study since 2008–2012 was 3.5% (95%CI: 1.6–7.5), and was 6.7% (2.7–15.5) since 2013–2017. Subgroup analysis by geographical region revealed 6.9% (95% CI; 3.3–13.9) in West Africa and 1.9%(95% CI; 0.8–4.6) in East Africa.

Discussion

CRS is a significant public health threat in resource-constrained countries. Most of sub-Saharan Africa countries have not introduced rubella vaccine due to lack of evidence of the burden of rubella virus .48 However, the cost of rubella infection complications and CRS is high, especially when compared to the very low cost of vaccination. Most middle- and high-income countries have introduced the rubella vaccine, and these countries have dramatically reduced incidence while developing countries not eradication of RV and CRS.

This meta-analysis was carried out to identify the pooled seroprevalence of anti-RV IgG and IgM among pregnant women in sub-Saharan African. Studies showed that RV is common in different sub-Saharan Africa countries, indicating a substantial number of susceptible reproductive-age women with a possible risk of giving birth to a child with CRS .14

This review found higher seronegativity compared to the WHO threshold of <5% seronegativity of a childbearing-age woman .49 This rate seronegativity is far below what Africa had planned by 2030 .50 This finding coincides with a systematic review done in sub-Saharan Africa which showed that the seronegativity of rubella among pregnant women was only 10% .14 This finding is higher than that found in a meta-analysis showing that the pooled RV seronegativity among pregnant women worldwide was 9.4% .51 Seronegativity is different from one country to another due to the cutoff point of seronegativity difference, the diagnosis method to isolate IgG, and false seropositivity. This difference in seronegativity rates maybe because almost all high- and middle-income countries have introduced a rubella vaccination strategy, but most sub-Saharan Africa countries have not yet introduced the rubella vaccination as a strategy to reduce the rate of CRS.

This finding is inconsistent with that in a meta-analysis of RV seronegativity for both childbearing-aged women and pregnant women in different regions: 6.9% in the Middle East region, 7.6% in the European region, 9.7% in the America region, 10.7% in the Africa region, and 19.4% in the East Asian region .51 The possible explanations of these differences might be the study population, different cutoff points of seronegativity, diagnosis methods, and vaccination implementation strategy.

This finding is in agreement with a single study done in Canada showing that RV seronegativity among pregnant women in Canada was 12%.52 Other studies showed rates of 5.9% in Spain and 7.6% in Spain immigrants, 53 2.8% in Brazil, 54 3.5% in England, 55 and 4.2% in Sweden .56

This finding is different from that in a study done among childbearing-aged women in Turkey showing 3.8%,57 4.3% average seronegativity in 17 countries,49 8.7% in Taiwan, 58 9.1% in Jordan,59 9.7% in Egypt, 60 15.8% in Singapore,61 22.9% in eleven Asian countries,62 and 31.1% in Bangladesh .63

The pooled prevalence of anti-RV IgM among pregnant women in sub-Saharan African was 5.1%. This finding showed that pregnant women commonly had acute RV infection in sub-Saharan Africa. This finding is higher than 0.3% found in a systematic review of sub-Saharan Africa .14

This meta-analysis of pooled RV seroprevalence among pregnant women in Sub-Saharan Africa has several implications for decision-makers and policy planners to achieve sustainable development goal three to ensure healthy lives and promote wellbeing for all ages. This study also is crucial to show RV susceptibility among pregnant women. Thus, sub-Saharan Africa countries and their policymakers can use this information for an evidence-based strategy to introduce rubella vaccination and a national surveillance system of rubella infection during pregnancy. This meta-analysis is an input for developing countries, stakeholders and policymakers to develop diagnostic and introduce RV vaccination programs. RV remains is a public-health threat in developing countries to develop CRS, for prevalence is high. Potential limitations of this study include variable assays, false-positive values, different cutoff points of seroprevalence, and unreported or under-reported or different diagnostic methods. Other important limitations are the use of pregnant women as a search term, the heterogeneity of subjects, and that the studies analyzed data from only 13 African countries.

Conclusion

This meta-analysis shows that seronegativity and acute infection with RV among pregnant women in sub-Saharan Africa is high compared to data reported in other studies and to the WHO threshold among women of child-bearing age. These findings call for primary healthcare providers to make the community aware of this rubella-susceptible group and its healthcare burden, with the desired outcome that sub-Saharan Africa countries would introduce an implementation strategy for rubella vaccination of pregnant women and women of child-bearing age.

Funding Statement

There was no funding or sponsoring organization for this paper

Abbreviations

CRS

congenital rubella syndrome

WHO

World Health Organization

Disclosure of potential conflicts of interest

No potential conflicts of interest were disclosed.

Authors’ contributions

ZY and SH contributed to the design of the study, collected, entered, analyzed, interpreted the data, and prepared the manuscript. SA contributed to data analysis, interpretation and drafted the manuscript. All authors read and approved the final manuscript.

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