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Pooled prevalence and genetic diversity of norovirus in Africa: a systematic review and meta-analysis

Virology Journal volume 19, Article number: 115 (2022) Cite this article

Abstract

Background

Noroviruses are the leading cause of acute gastroenteritis in all age groups globally. The problem is magnified in developing countries including Africa. These viruses are highly prevalent with high genetic diversity and fast evolution rates. With this dynamicity, there are no recent review in the past five years in Africa. Therefore, this review and meta-analysis aimed to assess the prevalence and genetic diversity of noroviruses in Africa and tried to address the change in the prevalence and genetic diverisity the virus has been observed in Africa and in the world.

Methods

Twenty-one studies for the pooled prevalence, and 11 out of the 21 studies for genetic characterization of norovirus were included. Studies conducted since 2006, among symptomatic cases of all age groups in Africa, conducted with any study design, used molecular diagnostic methods and reported since 2015, were included and considered for the main meta-analysis. PubMed, Cochrane Library, and Google Scholar were searched to obtain the studies. The quality the studies was assessed using the JBI assessment tool. Data from studies reporting both asymptomatic and symptomatic cases, that did not meet the inclusion criteria were reviewed and included as discussion points. Data was entered to excel and imported to STATA 2011 to compute the prevalence and genetic diversity. Heterogeneity was checked using I2 test statistics followed by subgroup and sensitivity analysis. Publication bias was assessed using a funnel plot and eggers test that was followed by trim and fill analysis.

Result

The pooled prevalence of norovirus was 20.2% (95% CI: 15.91, 24.4). The highest (36.3%) prevalence was reported in Ghana. Genogroup II noroviruses were dominant and reported as 89.5% (95% CI: 87.8, 96). The highest and lowest prevalence of this genogroup were reported in Ethiopia (98.3%), and in Burkina Faso (72.4%), respectively. Diversified genotypes had been identified with an overall prevalence of GII. 4 NoV (50.8%) which was followed by GII.6, GII.17, GI.3 and GII.2 with a pooled prevalence of 7.7, 5.1, 4.6, and 4.2%, respectively.

Conclusion

The overall pooled prevalence of norovirus was high in Africa with the dominance of genogroup II and GII.4 genotype. This prevalence is comparable with some reviews done in the same time frame around the world. However, in Africa, an in increasing trained of pooled prevalence had been reported through time. Likewise, a variable distribution of non-GII.4 norovirus genotypes were reported as compared to those studies done in the world of the same time frame, and those previous reviews done in Africa. Therefore, continuous surveillance is required in Africa to support future interventions and vaccine programs.

Introduction

Acute gastroenteritis (AGE) is the second greatest burden of all infectious diseases worldwide, in which the burden is high in low-income countries [1]. Rotavirus and norovirus (NoV) are the leading causes of AGE globally [2]. In Africa, NoV outbreaks and associated gastroenteritis were first reported in South Africa in 1993 with the two strains Norwalk (GI.1) and Hawaii (GII.1) [3].

Noroviruses are a group of non-enveloped viruses having a single-stranded positive-sense RNA genome. They are assigned to the Caliciviridae family [4]. Based on the variation on the major capsid protein (VP1) coding region, NoVs are classified into 10 genogroups (GI-GX) and 49 genotypes. From these genogroups, GI, GII, and GIV are known to infect humans [5]. Genogroup II is by far the most frequently reported genogroup comprising about 27 genotypes. According to some previous studies, GII.4 is the predominant genotype responsible for about 55–97% of the disease burden [6, 7] with an increased evolution rate due to accumulated mutations in the capsid region [8]. As a result of this, different GII.4 variant strains including the GII.4 US95/96 strain in 1995, GII.4 Farmington Hills in 2002, GII.4 Hunter in 2004, GII.4 Den Haag in 2006, GII.4 New Orleans in 2009, and GII.4 Sydney in 2012 [9] were reported. A new variant, GII.4 Hong Kong, was also reported recently in China that are associated with increased outbreaks [10]. Non-GII.4 NoVs commonly GII.17, GII.3, GII.6, GII.10, and GII.2 were also reported in developing countries including Africa [11,12,13]

Nowadays NoVs are considered as the leading cause of diarrheal death over 5 years of age, and the second in under 5 children with similar patterns across the globe [2]. It had been also reported as the leading cause of food-borne associated gastroenteritis [14]. As a result of this, it is responsible for about 10–20% of hospitalizations, severe diarrhea, dehydration, and death in the elderly and under 5 children [15].

In developing countries, NoV-associated mortality had been previously estimated to be as high as 212,000 deaths per year in under 5 children [16]. According to one review in developing countries, the prevalence of NoV was 17% [17]. Another epidemiological review of NoV in African children with gastroenteritis reported an overall prevalence of 13.5% [13]. Similarly, a systematic review of studies performed between 1993 and June 2015 among children in Sub-Saharan Africa also revealed a prevalence of 12.6% [18].

Increased awareness of this diversified pathogen has placed considerable interest in developing diagnostics, antivirals, and vaccines, as well as finding more effective ways to interrupt its transmission. Although primary studies had been performed in various countries in Africa, and one systematic review was reported in 2016, organized and up-to-date systematic review and meta-analysis has not been investigated recently in Africa. Some primary studies showed an increased prevalence of NoV with high genetic diversity in Africa [11, 19,20,21], and in other areas too [10, 22]. In this vaccine development era with an increased emergence of new genetic variants, updated and organized data is a priority which provides a space for the present study. Therefore, the purpose of this systematic review and meta-analysis is to assess the pooled prevalence and genetic diversity of NoVs in Africa.

Review questions

The research questions were developed based on the condition, context, and population (CoCoPop) approach. This systematic review and meta-analysis involve two review questions:

  1. (1)

    Has the pooled prevalence of NoVs among individuals with gastroenteritis in Africa changed in the past 5 years, and is it consistent with global prevalence?

  2. (2)

    Are the genogroup and genotype distribution of NoVs in Africa highly variable and differ from previous studies?

Methods and materials

Study area and period

A total of 21 studies reporting their finding between 2015 and 2021 all from the five regions of Africa (six studies each in Central and East Africa; four in South Africa, two studies from each North and West African country) were considered. The review process was conducted from March 01, 2021, to May 30, 2021. From the 21 studies, 9,238 individual participants were considered for the evaluation of the pooled prevalence of NoV. On the other hand, 11 of the 21 studies which reported genogroup and genotypic information were used for the assessment of the genetic diversity of NoV in Africa.

Review protocol development

Cochrane Library, Google Scholar, PubMed, and other databases were checked for the presence of similar studies to avoid duplication. To answer the review questions, a review protocol was developed and registered on PROSPERO with the registration number CRD42021251475.

Search strategy

Cochrane Library, PubMed, and Google Scholar were searched to identify potential articles on the prevalence and genetic diversity of NoVs in Africa. The following terms with Medical Subject Headings (MeSH) and all fields were used to search. Boolean operators (AND, OR, NOT) were also used to narrow and widen the scope of our search. Publications were identified using the search terms “epidemiology”, “molecular epidemiology” “prevalence”, “burden”, “norovirus”, “human norovirus infection”, “human caliciviruses” “acute gastroenteritis”, “acute diarrhea”, “Africa” and related terms.

The studies were assessed repeatedly in three consecutive steps to determine their eligibility. In step 1, the studies were evaluated considering only the information presented in the title and abstract. When the abstract was available, the study was further assessed for full texts. The full texts of the articles selected for step 2 were read to evaluate their eligibility and adequacy for data extraction; in step 3 the studies were re-evaluated to determine their eligibility for meta-analysis and systematic reviews of the outcome variables. Search results were combined into the EndNote X9 file and duplicates were removed.

Eligibility criteria

Inclusion criteria In this meta-analysis, studies that reported the prevalence and genetic diversity of NoVs in all ages of human subjects in African countries. Studies carried out in hospitalized patients, outpatient departments and community settings were included. In addition, studies that employed cross-sectional, case control and national surveillances, molecular technique and those published in English language were included. Studies that recruited with at least 50 study participants were considered eligible. Furthermore, studies were also considered for this analysis irrespective of the duration of the study.

Exclusion criteria Review articles, meta-analysis and those studies that did not satisfy the required information indicated in the inclusion criteria were excluded. As most studies did not consider seasonality, it could not be established for norovirus infections in this review too.

Data extraction

Two independent reviewers made an abstract and full-text review. When there was a disagreement, a discussion was made to reach a consensus with the involvement of a 3rd reviewer. From the eligible articles, data were extracted and sorted by the following variables: the leading author, reporting year and study period, country, study design, African region, age group, diagnostic methods used, number of positives, genotyped samples, and genotypes.

Quality appraisal

This systematic review and meta-analysis was performed following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guideline [23]. The Joanna Briggs Institute (JBI) quality appraisal checklist was used to assess the quality of individual papers [24].

Data analysis

The retrieved data was entered to excel and then imported to STATA version 11. Primarily the fixed effect model was done. However, a random-effect model was employed at the end due to the existence of heterogeneity between studies. The estimated proportion of each genogroup (GI and GII NoVs) was assessed by dividing the number of each genogroup by the total genotyped samples. The overall pooled prevalence and genotype distribution was calculated and displayed on graphs and tables. Heterogenicity was assessed by using the forest plot and Galbraith plot. Publication bias was checked by inspecting the funnel plot symmetry (subjectively) and by Egger's tests (objectively), with a significant publication bias at (p > 0.05) [25]. Trim and Fill analysis was used to see the effect of publication bias.

Result

Characteristics of included studies

A total of 7072 research articles had been retrieved from all the databases. After removing duplications 3000 articles were left for further analysis. In the second step, 2900 articles were excluded after reading their titles and abstracts and the remaining 100 studies were assessed for full-text review. Seventy-nine studies were excluded for additional reasons. Finally, twenty-one of the articles were considered for the assessment of the overall prevalence of NoV. Eleven out of the 21 studies articles were considered for the genetic diversity study (Fig. 1).

Fig. 1
figure 1

PRISMA study selection flow diagram of included studies for analysis

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In this review, NoV prevalence was defined as a proportion of NoV positive cases to the total number of gastroenteritis cases screened. The proportions of studies based on data from outpatients, communities and hospitalized patients were 8/21 (38%) each, 8/21 (38%), and 5/21 (23.8%), respectively. More generally, 13/21 (61.9%) studies were conducted in the health facility as compared to 8/21 (38.1%) studies conducted in the community setting. Similarly, most of the studies 16/21 (76.2%) were conducted among under 5 children while the remaining 5/21 studies were conducted in older ages. Most of the included articles were from Central and East African regions. Similarly, most of the studies (57.14%) were cross-sectional studies. All the included studies employed molecular diagnostic methods and were reported between 2015 to 2021. Furthermore, almost all of the included studies were conducted since 2010, except one study conducted in Kenya between 2006 to 2009.

The pooled prevalence of norovirus in Africa

A total of 9,238 stool samples, from 21 studies, had been analyzed for the assessment of the pooled prevalence of NoV (Table 1). According to the subjective assessment of the Galbraith plot (Additional file 1: Figure S1), we had observed heterogenicity among individual studies. Therefore, we applied a random-effect model for estimating the overall prevalence. Accordingly, the overall pooled prevalence of NoV was 20. 2% (95% CI: 15.9, 24.4). The highest (36.3%), and lowest prevalence (8.4%), were reported in Ghana and Cameroon, respectively. As shown in the forest plot (Fig. 2), statistically significant heterogeneity was identified (I2 = 96.8%; p-value < 0.001). As there was significant heterogeneity among the studies subgroup and sensitivity analysis was done.

Table 1 Descriptive summary of 21 studies included in the meta-analysis for the pooled prevalence of human noroviruses in Africa among studies reported from 2015 to 2021
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Fig. 2
figure 2

Forest plot of pooled prevalence of NoV among individuals with gastroenteritis in Africa: The pooled prevalence represented by the X-axis, and the list of included papers represented by Y-axis, The red line represents the minimum possible prevalence value (0). The dashed line represents the mean pooled NoV prevalence estimate. The gray box represents the weight of each study contributing to the pooled prevalence estimate. The black dot at the center of the gray box represents the point prevalence estimate of each study and the horizontal line indicates the 95% confidence interval for estimates of each study. The blue diamond represents the 95% confidence interval of the pooled NoV prevalence estimate

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In our review, three out of 21 studies reported the prevalence of NoV among asymptomatic individuals. The average prevalence of NoV in these studies was 7.1% (95% CI: 5.2, 9.4). More specifically, a study conducted in Burkina Faso reported the prevalence of NoV as 6% in asymptomatic individuals where as to 20.9% among symptomatic cases. Similarly, a study in Malawi reported a prevalence of 8.54%, and 12.15% for asymptomatic and symptomatic cases, respectively. However, a zero prevalence of NoV was reported among asymptomatic controls, and 11.1% among symptomatic cases in a study conducted in Nigeria.

Subgroup analysis

The studies were stratified by study area (African region), study design, sample size, age group, and molecular diagnostic methods used to identify the possible source of heterogeneity. Based on this analysis, the pooled prevalence of norovirus among under 5 children was 19.25 (95%CI: 14.4, 23.5), whereas the prevalence of NoV among studies participants older than 5 years of age was 23.77% (95% CI: 15.9, 33.5). The pooled prevalence of NoV in community-based, hospitalized and outpatient studies were 25.24, 20.30, and 18.68%, respectively (Table 2).

Table 2 Subgroup analysis for the pooled estimate of NoVs from 21 studies reported from 2015 to 2021
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Sensitivity analysis

Sensitivity analysis revealed no significant difference except for some outlier studies that deviate from the overall estimate. As all the studies lie within the 95% confidence interval the pooled prevalence is not affected by the individual study (Additional file 1: Figure S2).

Genetic diversity of noroviruses

Eleven out of the 21 studies that were conducted between 2010 and 2019 were used to assess the genetic diversity of NoV. Almost all of the studies had reported both GI and GII NoVs except one study conducted in Malawi that reported only GII NoV. The prevalence of GII was by far higher in all of the studies. The pooled prevalence of GII NoV was 89.5% (95% CI: 84.6, 94.5%) with a substantial heterogeneity (I2 = 69.1%; p-value = 0.001). The highest pooled prevalence of GII NoV had been reported as 98.3, and 97.4% in Ethiopia, and Cammeroon, respectively while the lowest was reported in in Burkina Faso (72.4%) (Fig. 3).

Fig. 3
figure 3

GII NoVs among all eleven molecularly characterized samples: The pooled prevalence GII NoVs had been represented by the X-axis, and the list of included papers represented by Y-axis, The bold vertical line represents the minimum possible prevalence value (0). The dashed line represents the mean pooled GII NoV prevalence estimate. The gray box represents the weight of each study contributing to the pooled prevalence estimate. The black dot at the center of the gray box represents the point prevalence estimate of each study and the horizontal line indicates the 95% confidence interval for estimates of each study. The blue diamond represents the 95% confidence interval of the pooled GII NoV prevalence estimate

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In this review, the dominance GII.4 NoV genotypes was also observed. This was followed by GII.6, GII.17, and GII.2, respectively. Similarly, GI.3 was the dominant genotype among all GI NoVs. The highest prevalence of non-GII.4 NoVs (GII.6) was reported in Ethiopia followed by a study conducted in Angola. The dominance of GII.17, among all non-GII.4 norovirus was also reported in the two studies conducted in Ethiopia. Similarly, the dominance of GII.7 and GII.10, from all non-GII.4 NoVs identified, was also seen in the studies done from Angola and Ethiopia, respectively. The highest prevalence of GI NoVs was reported in a study conducted in Angola. Most the included articles used open reading frame-2 (ORF-2) for genotyping and or sequencing, but some studies [12, 19, 20, 26, 27] used dual systems of genotyping using both ORF-1 and ORF-2.

The GII.4 was the leading genotype of all the GII NoVs (53.5%) (Additional file 1: Figure S3), and among all the reported genotypes (50.81%). However, the prevalence of non-GII.4 NoV genotypes was high with a prevalence of 7.7, 5.1, 4.6, and 4.2%, for GII. 6, GII.17, GI.3, and GII.2, respectively. Previously rare genotypes including GII.20, GII.9, GI.1, GI.2, and GI.8. were also reported in our review (Fig. 4). Recombinant types like GII.Pe/GII.4, GII. P4/GII.4 (in Botswana), GII.g/GII.12 (in Ethiopia), and GII.Pg/GII.1 (in South Africa) were also reported. The most common reported GII.4 variants in this review were Sydney 2012 and New Orleans 2009.

Fig. 4
figure 4

The distribution of NoV genotypes in Africa: The GII.4 is the leading among all the eleven molecularly characterized samples in our review which is followed by GII.6, GII.17. GI.3, GII.2, and others

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Assessment of publication bias

The result of the funnel plot showed some publication bias as indicated by the slight asymmetrical distribution of articles (Fig. 5 left). Eggers tests were conducted and also confirmed the presence of publication bias (Fig. 5 right). Therefore, trim and fill analysis was done to show the effect and magnitude of the publication bias (Additional file 1: Figure S4). Similar to the pooled prevalence, an asymmetrical distribution for GII NoVs among genotyped samples were observed (Additional file 1: Figure S5 left). This asymmetry was also confirmed by Egger's tests. The results of Egger's tests showed that there was a slight statistically significant publication bias in estimating the pooled proportion of GII NoV among those genotyped samples (y-intercept = 2.45; p-value < 0.05) (Additional file 1: Figure S5 right).

Fig. 5
figure 5

Funnel plot symmetry to check the presence or absence of publication bias: left The pooled prevalence of NoVs in Africa from studies reporting between 2015 to 2021; right Egger’s publication bias plot. Each dot represents individual studies. The x-axis represents precision (reciprocal of the standard error of the estimate). The y-axis represents log transformed standardized effect (estimate divided by its standard error)

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Discussion

Norovirus is the leading cause of non-bacterial epidemic AGE in all age groups globally [14]. The burden is high in developing countries with poor socio-economic status [1]. Several studies reported that NoVs have been frequently identified around the globe [28,29,30,31,32]. With a vaccine in a pipeline [33], an updated systematic review is a priority to provide comprehensive data. Therefore, this study aimed to assess the overall pooled prevalence and genetic diversity of NoV in Africa, and assure weather there is a changing prevalence and or genetic diversity of this pathogen is occured.

In this study, the pooled prevalence and genetic diversity of NoVs were reviewed and analyzed from studies conducted on patients with gastroenteritis and published between January 2015 and April 2021. According to this systematic review and meta-analysis, the pooled prevalence of NoV, among the included 21 studies, was 20.2% (95% CI: 15.9, 24.4). This study indicated the burden of NoV infection in Africa was high that might have an impact on the routine management of AGE cases. The present pooled prevalence was in agreement with one recent global review which was conducted almost in same time frame (2015 to 2020) from 45 countries across the world that was 17.7% (95% CI: 16.3%-19.2%) [34]. Our finding was also somewhat in agreement with a review done from 52 studies in China which was 16.68% (95% CI 16.63–16.72) [35].

In contrast, our finding was higher than a previous review conducted in Africa 13.5% (95% CI 12.7–14.3) [13], another review conducted from 1990 to 2013 in Africa 11% (95% CI 8–14%) [36], and a review done in Sub-Saharan Africa 14.2% published before 2015 [18]. The source of this variation could be the difference in the study participants, the study period, and the study setting. These reviews considered those studies published before 2015. This might be associated with an increased prevalence and dynamic change or evolution of the virus from time to time, and the domination of this virus over the others [5, 22]. The other source of variation might also be the exclusion criteria sated as they excluded outbreak cases, and included only sporadic cases in their analysis [36].

More specifically, the pooled prevalence of NoV among under 5 children was lower among under 5 children 19.25 (95%CI: 14.4, 23.5) as compared to the prevalence of NoV among studies participants older than 5 years of age 23.77% (95% CI: 15.9, 33.5). This was in agreement with the recent global report among under 5 children 19.0 (95% CI: 17.3–20.8) and older than 5 years 17.6% (95% CI: 13.0% –23.5%) [34]. A similar agreement of prevalence had been reported in one study done in China with children ≤ 5 years 17.39% (95% CI: 17.32–17.47), and among adult patients 19.28% (95% CI: 19.23–19.33) [35]. The pooled prevalence was also higher in community-based studies that is 25.24% (95% CI: 20.2, 28.9) as compared to 20.30, and 18.68% for studies conducted among hospitalized, and OPD, respectively. A comparable gradient of decreasing prevalence was also reported from one previous global systematic review conducted from 1997 to 2021 that is 20, 18, and 15% for studies conducted in community, outpatients, and hospital settings, respectively [37]. A comparable result was also reported in another previous global systematic review with 24, 20, and 17% for community and outpatient settings, and inpatient settings, respectively [14].

In our review, three studies reported the prevalence of NoV among asymptomatic individuals with an average prevalence of 7.1% (95% CI 6.3–9.1). This was in agreement with the prevalence of NoV in asymptomatic patients reported from 28 studies across the globe done in the same time frame with our study that was 6.7% (95% CI: 5.1%-8.8%) [34]. Our finding was, however, slightly lower than a previous report in Africa that reported an overall prevalence of 9.7% (95% CI 8.4–11.1) among asymptomatic groups [13], and a review in Sub-Saharan Africa children was (9.2%) [6]. The difference might be due to the time frame when the review was conducted. That is, we included studies published 2015 and 2021 while other previous African studies were considered those studies published before 2015. The other discrepancy might be the number of included studies reporting asymptomatic participants. For example, for the one reporting 9.2% from a review in done Sub-Saharan Africa, the number of included studies were 8 as compared to our review that only included 3 studies.

Genogroup GII is the leading NoV genogroup in the world [34, 38]. In this study, from all the included eleven studies for genetic analysis, the commonest NoV genogroup detected was NoV GII which was 89.5% (95% CI 84.5,94.5) with a small proportion of NoV GI (8.4%). Our finding was in agreement with the recent global review done almost in a similar time frame that reported as 92.9% (95% CI: 90.6%–94.6%) for GII, and 6.7% (95% CI: 5.2%–8.5%) for GI [34]. The same is true for the previous review conducted in Africa where GII strains represented 88.5% of all detected NoVs, and GI strains 3.4% [13]. In contrast to our finding, a lower prevalence of GII (76.4%), with an increased prevalence of GI NoVs (21.7%) was reported in the previous review done in Sub-Saharan countries [6]. The same is true for the previous review done in Africa from studies published between 1990 and 2013 that is 81% (95% CI 73–87%) for GII and, 18% (95% CI 12–24%) for GI. This might be the inclusion of studies published before 2015 and after 2015 as seen in our case that could be associated to the genetic variations because of mutation or evolution of the virus, and or recombination events through time [8, 39]. The source of discrepancy might also be due the inclusion criteria in this study. They only included age groups ≤ 17 years as compared to our review considered all age groups [40]. The other source of variation might be the setting as they only include Sub-Saharan Africa as compared to our study considered all African studies.

The GII.4 NoV genotype have been dominating in the past two decades, and hence it is responsible for a great disease burden causing outbreaks and sporadic cases of gastroenteritis [41, 42]. This genotype has high mutation rate where the new variants emerged every 2 to 3 years [22, 40]. However, the emergence of different strains of GII.4 and non-GII.4 genotypes have become a common occurrence in the past five years across different countries in the world [5, 11, 12, 22, 43]. This might be due to genetic variations because of mutation and recombination events occurred in this specific virus [8, 39].

In this review, a great diversity of NoV genotypes were reported ranging from GII.1 to GII.21, except GII.5, GII.8, GII.11, GII.15, GII.18, and GII.19, with the predominance of GII.4, 50.8% (95% CI 40.60, 66.48) from all identified genotypes (Fig. 4). This was also true for GI NoV that comprise of GI.1 to GI.9, with the dominance of GI.3 (4.6%) of all the reported NoV genotypes. The great diversity and distribution of different genotypes in our finding was in agreement with the previous review in Sub-Saharan Africa except for some differences in the number of genotype distributions [18]. Our finding was in agreement with the previous studies done in Africa that also reported the dominance of GII.4 NoVs which was 54.1% [13], 65.2% for a review in Sub-Saharan Africa [6]. A similar finding was observed in the recent global studies with 59.3% (95% CI: 53.4%–64.9%) [34], and 52% [38]. These findings assured the dominance of GII.4 NoVs in the world generally and in Africa specifically.

Next to GII.4, GII.6, GII.17, GI.3and GII.2 with a prevalence of 7.7%, 5.1%, 4.6%, 4.2%, respectively were also highly reported in our review. This report is in agreement with a previous study where an increased prevalence of non-GII.4 NoV had been reported in different parts of China and Japan as a single variant or as a recombinant type [44,45,46]. These might be associated with an increased prevalence of other genotypes through time other than the GII.4 NoV which include GII.17, GII.6, GII.2, and GII.3 in different countries since 2014 with the most prevalent genotype change occurred during the 2015–2017 period which can increase cross transmission from one setting to another through time [11, 12, 45, 47,48,49]. In contrast to this the previous review conducted in Africa by 2016 reported a dominance of other genotypes including GII.3 (12.2%), GI.3 (3.6%), and GII.6 (3%), with a lower prevalence rate of GII.17, and GII.2 was reported. A similar dominance of GII.3 (14%), that was followed by GII.2 (11%), and GII.6 (5%) genotypes was also reported in one global review [38]. The same is true for another global review done from 2015 to 2020 reported a high prevalence of (14.9%, 95% CI: 10.6%–20.5%) for GII.3 [34]. An increased prevalence of GII.2 (50%), and GII.17 (15.38%) between 2014 to 2019 were also reported in China [35]. This showed the highest evolutionary dynamics of NoV strains from time to time that demonstrates a changing prevalence and diversity of NoV genotypes over time in Africa and globally [14, 50, 51]

Among all genotyped NoVs, GI.3 with 4.6% was the dominant genotype with in GI NoVs that was followed by GI.5 (1.9%). This was in agreement with other reviews, where a dominance of GI.3 NoV was reported in the previous review done in Africa 3.5% [13], and in a recent review done in the world 4% [38].

Our finding reported a substantial to considerably high heterogenicity as measured in the subjective and objective assessment methods. Therefore, we stratified studies into the study region, diagnostic method, study design, severity of the disease, setting, and age groups. Regional estimates of NoV infection in the subgroup analysis showed a lower prevalence of 17.5% in Eastern Africa compared to a higher prevalence of 30% in the North Africa region. This regional difference can be attributable to that in Eastern Africa, 75% of study participants were all age groups compared to the studies conducted in North Africa that considered children. Most studies in the Eastern African region also used the most sensitive diagnostic method Rt-qPCR. The prevalence of NoV infection differs based on laboratory diagnostic methods used. Higher prevalence was detected by Rt-qPCR (21%) as compared to conventional RT-PCR (18%) (Table 2). In this review, the sensitivity analysis revealed no significant difference except for some outlier studies that deviate from the overall estimate. As all the studies lie within the 95% confidence interval the pooled prevalence is not affected (Additional file 1: Figure S2). On the other hand, a significant publication bias had been reported. The reason might be due inclusion of only published papers and or studies published in the English language.

Limitations of this review

The first limitation of this study was that our finding reported a substantial to considerably high heterogenicity as measured in the subjective and objective assessment methods which might have an effect on the pooled prevalence. The source of this observed heterogeneity could be due to differences in the spatio-temporal and epidemiological patterns of the included studies. We tried to minimize this by doing subgroup analysis and sensitivity analysis. Another issue was that only English articles or reports, and published studies had been considered for analysis which might be associated with some of the observed publication bias in our report. Although the seasonality of NoV infections was important for effective health care planning, in our review we could not establish the seasonality as it was inconsistent in the individual studies. In addition to this, the review was made in 21 studies conducted from 15 out of the 54 African countries which might be difficult to generalize or conclude for Africa. Despite this limitation, our study provided updated information regarding NoV associated gastroenteritis and its genetic diversity, which is relevant for vaccine development and to implement intervention mechanisms.

Conclusion and recommendation

The overall pooled prevalence of NoV in Africa was still high, with more than one-fifth of the individuals with AGE are affected. This finding might be used to point out and estimate the burden of NoV-associated AGE in Africa in the past 5 years, where there is a lack of surveillance systems. It is also important to developed diagnostic and management approaches. The pooled prevalence of NoV in our review is high and comparable with some reviews and studies done in the same time frame around the world including China. However, in Africa, as compared to those previous studies conducted in the different time frame, the pooled prevalence is in the increasing trained through time. Except for a few data, the genotype distribution of NoV in Africa was high and somewhat different from the previous global and African trends. The GII and GII.4 were the dominant genogroup and genotype, respectively. However, a relative increase in the distribution of unusual genotypes including, but not limited to GII.6, GII.17, GII.2, and others was observed in the region as compared to the dominance of other non-GII.4 genotypes that include GII.3 from those previous reviews done in Africa with a different time frame as well as GII.2, GII.3, and GII.17 in the world reported in the same time frame. In line with this, although GII genogroup and GII.4 genotypes are still dominating in the world and in Africa generally, non-GII.4 Therefore, continuous networked surveillance is a priority to provide updated data that target future interventions and inform vaccine development strategies in the continent.

Availability of data and materials

The dataset(s) supporting the conclusions of this article is (are) included within the article and the data that support the findings of this study are available from the corresponding author [DT], upon reasonable request.

Abbreviations

AGE:

Acute gastroenteritis

GI:

Genogroup I

GII:

Genogroup II

JBI:

Joanna Briggs Institute

MeSH:

Medical subject heading

NoV:

Norovirus

OPD:

Outpatient department

ORF:

Open reading frame

PRISMA:

Preferred reporting items for systematic reviews and meta-analyses

RNA:

Ribonucleic acid

RT-PCR:

Reverse transcriptase polymerase chain reaction

Rt-qPCR:

Real time quantitative polymerase chain reaction

STATA:

Statistics and data

WHO:

World Health Organization

References

  1. Troeger C, Forouzanfar M, Rao PC, Khalil I, Brown A, Reiner RC Jr, et al. Estimates of global, regional, and national morbidity, mortality, and aetiologies of diarrhoeal diseases: a systematic analysis for the global burden of disease study 2015. Lancet Infect Dis. 2017;17(9):909–48.

    Google Scholar 

  2. Bányai K, Estes MK, Martella V, Parashar UD. Viral gastroenteritis. Lancet. 2018;392:175–86.

    PubMed  PubMed Central  Google Scholar 

  3. Taylor MB, Schildhauer CI, Parker S, Grabow WO, Jiang X, Estes MK, et al. Two successive outbreaks of SRSV-associated gastroenteritis in South Africa. J Med Virol. 1993;41(1):18–23.

    CAS  PubMed  Google Scholar 

  4. Green K, Knipe D, Howley P, Cohen J, Griffin D, Lamb R, et al. Caliciviridae: the noroviruses. Fields virology.In: Knipe DM, Howley PM. Fields virology Lippincott Williams & Wilkins, Wolters Kluwer Business, Philadelphia2007949–980. 2013.

  5. Chhabra P, de Graaf M, Parra GI, Chan MC-W, Green K, Martella V, et al. Updated classification of norovirus genogroups and genotypes. J Gen Virol. 2019;100(10):1393.

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Munjita SM. Current status of norovirus infections in children in Sub-Saharan Africa. 2015.

  7. Desai R, Hembree CD, Handel A, Matthews JE, Dickey BW, McDonald S, et al. Severe outcomes are associated with genogroup 2 genotype 4 norovirus outbreaks: a systematic literature review. Clin Infect Dis. 2012;55(2):189–93.

    PubMed  PubMed Central  Google Scholar 

  8. Parra GI, Squires RB, Karangwa CK, Johnson JA, Lepore C, Sosnovtsev SV, et al. Static and evolving norovirus genotypes: implications for epidemiology and immunity. PLoS Pathog. 2017;13(1): e1006136.

    PubMed  PubMed Central  Google Scholar 

  9. Leshem E, Wikswo M, Barclay L, Brandt E, Storm W, Salehi E, et al. Effects and clinical significance of GII. 4 Sydney norovirus, United States, 2012–2013. Emerg Infect Dis. 2013;19(8):1231.

    PubMed  PubMed Central  Google Scholar 

  10. Chan MC-W, Roy S, Bonifacio J, Zhang L-Y, Chhabra P, Chan JC, et al. Detection of norovirus variant GII. 4 Hong Kong in Asia and Europe, 2017–2019. Emerg Infect Dis. 2021;27(1):289.

    PubMed  PubMed Central  Google Scholar 

  11. Gelaw A, Pietsch C, Mann P, Liebert U. Molecular detection and characterisation of sapoviruses and noroviruses in outpatient children with diarrhoea in Northwest Ethiopia. Epidemiology & Infection. 2019;147.

  12. Sisay Z, Djikeng A, Berhe N, Belay G, Gebreyes W, Abegaz WE, et al. Prevalence and molecular characterization of human noroviruses and sapoviruses in Ethiopia. Adv Virol. 2016;161(8):2169–82.

    CAS  Google Scholar 

  13. Mans J, Armah GE, Steele AD, Taylor MB. Norovirus epidemiology in Africa: a review. PLoS ONE. 2016;11(4): e0146280.

    PubMed  PubMed Central  Google Scholar 

  14. Ahmed SM, Hall AJ, Robinson AE, Verhoef L, Premkumar P, Parashar UD, et al. Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis. 2014;14(8):725–30.

    PubMed  PubMed Central  Google Scholar 

  15. Lopman BA, Steele D, Kirkwood CD, Parashar UD. The vast and varied global burden of norovirus: prospects for prevention and control. PLoS Med. 2016;13(4): e1001999.

    PubMed  PubMed Central  Google Scholar 

  16. Pires SM, Fischer-Walker CL, Lanata CF, Devleesschauwer B, Hall AJ, Kirk MD, et al. Aetiology-specific estimates of the global and regional incidence and mortality of diarrhoeal diseases commonly transmitted through food. PLoS ONE. 2015;10(12): e0142927.

    PubMed  PubMed Central  Google Scholar 

  17. Nguyen G, Phan K, Teng I, Pu J, Watanabe T. A systematic review and meta-analysis of the prevalence of norovirus in cases of gastroenteritis in developing countries. Wolters Kluwer Health; 2017.

  18. Munjita SM. Current status of norovirus infections in children in sub-Saharan Africa. J Trop Med. 2015. https://doi.org/10.1155/2015/309648.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Ouédraogo N, Kaplon J, Bonkoungou IJO, Traoré AS, Pothier P, Barro N, et al. Prevalence and genetic diversity of enteric viruses in children with diarrhea in Ouagadougou, Burkina Faso. PLoS one. 2016;11(4): e0153652.

    PubMed  PubMed Central  Google Scholar 

  20. Makhaola K, Moyo S, Lechiile K, Goldfarb DM, Kebaabetswe LP. Genetic and epidemiological analysis of norovirus from children with gastroenteritis in Botswana, 2013–2015. BMC Infect Dis. 2018;18(1):246.

    PubMed  PubMed Central  Google Scholar 

  21. Osazuwa F, Okojie R, Akinbo FO, Johnson W, Grobler H. Genetic diversity of norovirus among children under 5 years in the South-South region of Nigeria. New Zealand J Med Lab Sci. 2020;74(1):39.

    Google Scholar 

  22. Parra GI. Emergence of Norovirus Strains: A Tale of Two Genes. Virus Evolution. 2019;5(2):vez048.

  23. Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097.

    PubMed  PubMed Central  Google Scholar 

  24. Peters M, Godfrey C, McInerney P, Soares C, Khalil H, Parker D. The Joanna Briggs Institute reviewers’ manual 2015: methodology for JBI scoping reviews. 2015.

  25. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994. https://doi.org/10.2307/2533446.

    Article  PubMed  Google Scholar 

  26. Rossouw E, Brauer M, Meyer P, Plessis NMd, Avenant T, Mans J. Virus Etiology, Diversity and Clinical Characteristics in South African Children Hospitalised with Gastroenteritis. Viruses. 2021;13(2):215.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Mulondo G, Khumela R, Kabue J, Traore A, Potgieter N. Molecular characterization of norovirus strains isolated from older children and adults in impoverished communities of Vhembe District, South Africa. Advances in Virology. 2020. https://doi.org/10.1155/2020/8436951.

    Article  PubMed  PubMed Central  Google Scholar 

  28. McAtee C, Webman R, Gilman R, Mejia C, Bern C, Apaza S, et al. Burden of norovirus and rotavirus in children after rotavirus vaccine introduction, Cochabamba, Bolivia. Am J Trop Med Hyg. 2015;94(1):212–7.

    PubMed  Google Scholar 

  29. Doll MK, Gagneur A, Tapiéro B, Charest H, Gonzales M, Buckeridge DL, et al. Temporal changes in pediatric gastroenteritis after rotavirus vaccination in Quebec. Pediatr Infect Dis J. 2016;35(5):555–60.

    PubMed  Google Scholar 

  30. Farfán-García AE, Imdad A, Zhang C, Arias-Guerrero MY, Sánchez-Álvarez NT, Iqbal J, et al. Etiology of acute gastroenteritis among children less than 5 years of age in Bucaramanga, Colombia: A case-control study. PLoS Negl Trop Dis. 2020;14(6): e0008375.

    PubMed  PubMed Central  Google Scholar 

  31. Bozkurt D, Selimoğlu MA, Otlu B, Sandıkkaya A. Eight different viral agents in childhood acute gastroenteritis. Turkish J Pediatr. 2015;57(1).

  32. Nakamura N, Kobayashi S, Minagawa H, Matsushita T, Sugiura W, Iwatani Y. Molecular epidemiology of enteric viruses in patients with acute gastroenteritis in Aichi Prefecture, Japan, 2008/09− 2013/14. J Med Virol. 2016;88(7):1180–6.

    PubMed  Google Scholar 

  33. Ramani S, Neill FH, Ferreira J, Treanor JJ, Frey SE, Topham DJ, et al. B-cell responses to intramuscular administration of a bivalent virus-like particle human norovirus vaccine. Clin Vaccine Immunol. 2017;24(5):e00571-e616.

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Farahmand M, Moghoofei M, Dorost A, Shoja Z, Ghorbani S, Kiani SJ, et al. Global prevalence and genotype distribution of norovirus infection in children with gastroenteritis: a meta-analysis on 6 years of research from 2015 to 2020. Rev Med Virol. 2022;32(1): e2237.

    PubMed  Google Scholar 

  35. Wei N, Ge J, Tan C, Song Y, Wang S, Bao M, et al. Epidemiology and evolution of norovirus in China. Hum Vaccin Immunother. 2021;17(11):4553–66.

    CAS  PubMed  Google Scholar 

  36. Kabue JP, Meader E, Hunter PR, Potgieter N. Human Norovirus prevalence in Africa: a review of studies from 1990 to 2013. Tropical Med Int Health. 2016;21(1):2–17.

    Google Scholar 

  37. Liao Y, Hong X, Wu A, Jiang Y, Liang Y, Gao J, et al. Global prevalence of norovirus in cases of acute gastroenteritis from 1997 to 2021: an updated systematic review and meta-analysis. Microb Pathog. 2021;161: 105259.

    CAS  PubMed  Google Scholar 

  38. Cannon JL, Bonifacio J, Bucardo F, Buesa J, Bruggink L, Chan MC-W, et al. Global trends in norovirus genotype distribution among children with acute gastroenteritis. Emerging Infect Dis. 2021;27(5):1438.

    CAS  Google Scholar 

  39. Malm M, Tamminen K, Lappalainen S, Uusi-Kerttula H, Vesikari T, Blazevic V. Genotype considerations for virus-like particle-based bivalent norovirus vaccine composition. Clin Vaccine Immunol. 2015;22(6):656–63.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Ramani S, Atmar RL, Estes MK. Epidemiology of human noroviruses and updates on vaccine development. Curr Opin Gastroenterol. 2014;30(1):25.

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Li H-y, Zhang Y-g, Lei X, Song J, Duan Z-J. Prevalence of noroviruses in children hospitalized for acute gastroenteritis in Hohhot China 2012–2017. BMC Infect Dis. 2019;19(1):595.

    PubMed  PubMed Central  Google Scholar 

  42. Mugyia AE, Ndze VN, Akoachere JFT, Browne H, Boula A, Ndombo PK, et al. Molecular epidemiology of noroviruses in children under 5 years of age with acute gastroenteritis in Yaoundé. Cameroon J Med Virol. 2019;91(5):738–43.

    PubMed  Google Scholar 

  43. Lu L, Zhong H, Su L, Cao L, Xu M, Dong N, et al. Detection and molecular characterization of human adenovirus infections among hospitalized children with acute diarrhea in Shanghai, China, 2006–2011. Canadian J Infect Dis Med Microbiol. 2017. https://doi.org/10.1155/2017/9304830.

    Article  Google Scholar 

  44. Nagasawa K, Matsushima Y, Motoya T, Mizukoshi F, Ueki Y, Sakon N, et al. Phylogeny and immunoreactivity of norovirus GII. P16-GII. 2, Japan, winter 2016–17. Emerg Infect Dis. 2018;24(1):144.

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Lu J, Sun L, Fang L, Yang F, Mo Y, Lao J, et al. Gastroenteritis outbreaks caused by norovirus GII. 17, Guangdong Province, China 2014–2015. Emerg Infect Dis. 2015;21(7):1240.

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Lu J, Fang L, Sun L, Zeng H, Li Y, Zheng H, et al. Association of GII. P16-GII. 2 recombinant norovirus strain with increased norovirus outbreaks, Guangdong, China 2016. Emerg Infect Dis. 2017;23(7):1188.

    PubMed  PubMed Central  Google Scholar 

  47. Chen L, Xu D, Wu X, Liu G, Ji L. An increasing prevalence of non-GII. 4 norovirus genotypes in acute gastroenteritis outbreaks in Huzhou, China, 2014–2018. Arch Virol. 2020;165(5):1121–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Fu J, Ai J, Jin M, Jiang C, Zhang J, Shi C, et al. Emergence of a new GII. 17 norovirus variant in patients with acute gastroenteritis in Jiangsu, China, September 2014 to March 2015. Eurosurveillance. 2015;20(24):21157.

    PubMed  Google Scholar 

  49. Gao Z, Liu B, Huo D, Yan H, Jia L, Du Y, et al. Increased norovirus activity was associated with a novel norovirus GII. 17 variant in Beijing, China during winter 2014–2015. BMC Infect Dis. 2015;15(1):1–7.

    Google Scholar 

  50. White P. Evolution of norovirus. Clin Microbiol Infect. 2014;20(8):741–5.

    CAS  PubMed  Google Scholar 

  51. Fu J, Bao C, Huo X, Hu J, Shi C, Lin Q, et al. Increasing recombinant strains emerged in norovirus outbreaks in Jiangsu, China: 2015–2018. Sci Rep. 2019;9(1):1–9.

    Google Scholar 

  52. Esteves A, Nordgren J, Tavares C, Fortes F, Dimbu R, Saraiva N, et al. Genetic diversity of norovirus in children under 5 years of age with acute gastroenteritis from Angola. Epidemiol Infect. 2018;146(5):551–7.

    CAS  PubMed  Google Scholar 

  53. Louya VM, Vouvoungui C, Koukouikila-Koussounda F, Veas F, Kobawila SC, Ntoumi F. Molecular characterization of norovirus infection responsible for acute diarrhea in Congolese hospitalized children under five years old in Brazzaville, Republic of Congo. Int J Infect Dis. 2019;88:41–8.

    Google Scholar 

  54. Rönnelid Y, Bonkoungou I, Ouedraogo N, Barro N, Svensson L, Nordgren J. Norovirus and rotavirus in children hospitalised with diarrhoea after rotavirus vaccine introduction in Burkina Faso. Epidemiol Infect. 2020. https://doi.org/10.1017/S0950268820002320.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Lekana-Douki SE, Kombila-Koumavor C, Nkoghe D, Drosten C, Drexler JF, Leroy EM. Molecular epidemiology of enteric viruses and genotyping of rotavirus A, adenovirus and astrovirus among children under 5 years old in Gabon. Int J Infect Dis. 2015;34:90–5.

    PubMed  Google Scholar 

  56. Shioda K, Cosmas L, Audi A, Gregoricus N, Vinjé J, Parashar UD, et al. Population-based incidence rates of diarrheal disease associated with norovirus, sapovirus, and astrovirus in Kenya. PLoS one. 2016;11(4): e0145943.

    PubMed  PubMed Central  Google Scholar 

  57. Wainaina E, Otieno CA, Kamau J, Nyachieo A, Lowther SA. Norovirus infections and knowledge, attitudes and practices in food safety among food handlers in an informal urban settlement, Kenya 2017. BMC Public Health. 2020;20:1–8.

    Google Scholar 

  58. Hungerford D, Jere KC, Bar-Zeev N, Harris JP, Cunliffe NA, Iturriza-Gómara M. Epidemiology and genotype diversity of norovirus infections among children aged< 5 years following rotavirus vaccine introduction in Blantyre. Malawi J Clin Virol. 2020;123: 104248.

    CAS  PubMed  Google Scholar 

  59. Howard LM, Mwape I, Siwingwa M, Simuyandi M, Guffey MB, Stringer JS, et al. Norovirus infections in young children in Lusaka Province, Zambia: clinical characteristics and molecular epidemiology. BMC Infect Dis. 2017;17(1):1–9.

    Google Scholar 

  60. Makhaola K, Moyo S, Lechiile K, Goldfarb DM, Kebaabetswe LP. Genetic and epidemiological analysis of norovirus from children with gastroenteritis in Botswana, 2013–2015. BMC Infect Dis. 2018;18(1):1–8.

    Google Scholar 

  61. Kabue Ngandu J-P. Molecular characterization of norovirus stains circulating in rural communities of Limpopo Province of South Africa 2018.

  62. Nxele NV. Norovirus in children 5 years and below presenting with diarrhoea in KwaZulu-Natal 2017.

  63. Tatay EM, El Hussein ARM, Mustafa MO, Elkhidir IM, Enan KA. Molecular Detection of Norovirus 1, 2 in Children Less than 5 Years with Gastroenteritisin Al Jazeera State, Sudan. 2018.

  64. El Sayed-Zaki M, Eid AR, El Ashry AY, M Al-Kasaby N. Molecular study of norovirus in pediatric patients with gastroenteritis. Open Microbiol J. 2019. https://doi.org/10.2174/1874285801913010324.

    Article  Google Scholar 

  65. Lartey BL, Quaye O, Damanka SA, Agbemabiese CA, Armachie J, Dennis FE, et al. Understanding pediatric norovirus epidemiology: a decade of study among Ghanaian Children. Viruses. 2020;12(11):1321.

    CAS  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Medical Laboratory Sciences, College of Health Sciences, Debre Tabor University, P.O. Box 272, Debre Tabor, Ethiopia

    Dessie Tegegne Afework

  2. Department of Medical Microbiology, College of Medicine and Health Sciences, University of Gondar, P.O. Box 196, Gondar, Ethiopia

    Dessie Tegegne Afework, Getachew Ferede Endalew, Aschalew Gelaw Adugna & Baye Gelaw Tarekegn

  3. Department of Nursing, College of Health Sciences, Debre Tabor University, P.O. Box 272, Debre Tabor, Ethiopia

    Mulu Kebede Shumie

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Contributions

DT: developed the study protocol, searched and selected primary studies, extracted the data, analyzed the data and draft the manuscript. MK: was involved in searching and selection of primary studies. BG, AG, and GF were involved in data analysis and revised the manuscript. All authors have read and agreed to publish this manuscript.

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Afework, D.T., Shumie, M.K., Endalew, G.F. et al. Pooled prevalence and genetic diversity of norovirus in Africa: a systematic review and meta-analysis. Virol J 19, 115 (2022). https://doi.org/10.1186/s12985-022-01835-w

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