https://orcid.org/0000-0001-7344-310X
ABSTRACT
Rotavirus gastroenteritis imposes a heavy burden on low- and middle-income countries. The World Health Organization defines the Eastern Mediterranean region (WHO-EMRO) as a diverse area in terms of socioeconomic status and health indicators. Rotavirus vaccination has been introduced, at least partially, in 19 out of the 22 EM countries; however, vaccine coverage remains low, and data on rotavirus disease burden is scarce.
Available data on rotavirus prevalence, seasonality, vaccination status, and genotype evolution was systematically compiled following a literature review that identified 165 relevant WHO-EMRO epidemiology studies published between 1990 and 2017.
Although the infectious agents responsible for acute gastroenteritis vary over time, rotavirus remained the leading cause of acute gastroenteritis in children, as seen in 76.3% of reviewed publications. Younger children (<2 years old) were at higher risk and thus increased vaccination coverage and surveillance systems are required to reduce the rotavirus gastroenteritis burden in WHO-EMRO countries.
Introduction
Rotavirus (RV) is the leading cause of diarrheal morbidity and mortality in young children worldwide and causes severe acute gastroenteritis (AGE) requiring hospitalization, and if dehydration is not treated in time leads to mortality especially in the developing world.Citation1 By the age of five years, nearly every child will have had an episode of RV gastroenteritis (RVGE), one in five of them will visit a clinic, one in 65 will be hospitalized, and approximately 1 out of 293 will eventually have a fatal outcome.Citation2,Citation3 According to a report, more than 90% of RVGE deaths in 2013 occurred in 72 low-income and low-middle-income countries.Citation4 Implementation of an RV vaccination in national immunization programs (NIPs) reduces the RV disease burden substantially.Citation5 Countries need to have adequate knowledge and information on local burden, trends, and age distribution of disease to help decision-makers consider the introduction of an RV vaccine as part of their immunization programs.Citation6
The Eastern Mediterranean region, as defined by the World Health Organization (WHO-EMRO region, ), is a geographically and socioeconomic diverse area with varying health indicators. At present, the region has a population of over 656 million (81.4 million (12.4% of the total population) – is under 5 years of age).Citation7 RV-associated mortality and morbidity also vary considerably in the region: the annual morbidity rates among children under five years of age ranged from 0 to 112/100,000 with an average mortality rate of 39/10,000 per year.Citation5,Citation8 Low-income countries (e.g. Afghanistan, Pakistan, Sudan, Yemen, and Somalia) had a higher mortality rate due to RVGE compared with countries where the per capita income was high (e.g. Saudi Arabia and Kuwait). However, the overall hospital and health center visits due to RVGE among children under five years of age was similar in both high- and low-income WHO-EMRO countries.Citation5,Citation8,Citation9
Figure 1. WHO-EMRO region countries (i.e. Afghanistan, Bahrain, Djibouti, Egypt, Iran (Islamic Republic of), Iraq, Jordan, Kuwait, Lebanon, Libya, Morocco, Occupied Palestine Territory, Oman, Pakistan, Qatar, Somalia, Sudan, Syrian Arab Republic, Tunisia, United Arab Emirates (UAE), and Yemen) included in the study.
UAE: United Arab Emirates.
An RV vaccine has been introduced as part of the NIPs in 15 out of the 22 countries (albeit partially in Pakistan and Palestine) in the WHO-EMRO region. Vaccine coverage is predominantly suboptimal, with the exception of Saudi Arabia, with 97% vaccine coverage, and burden of disease data are still scarce.1,Citation6,Citation10 Furthermore, a lack of surveillance systems prevents decision makers from understanding the magnitude of the problem and the need for RVGE prevention through vaccination.Citation11
The purpose of this literature review is to assess the burden of RVGE in the pediatric population and to summarise the current status of recommendations for RV vaccination across the WHO-EMRO region. Moreover, this review will also be useful as a baseline for post-vaccination surveillance for both AGE and RVGE.
Results
Four hundred and twenty-six articles were identified through the search process as of 5th December 2017. Two hundred and thirteen publications were excluded and 213 were included for full-text review. One hundred and sixty-five publications were included in the qualitative assessment (). The countries and number of associated references from which published data were obtained are: Afghanistan (1),Citation12 Bahrain (3), Citation13–Citation15 Egypt (17),Citation16–Citation32 Iran (37),Citation33–Citation68 Iraq (3),Citation41,Citation69,Citation70 Jordan (9),Citation71–Citation79 Kuwait (2),Citation80,Citation81 Lebanon (3),Citation82–Citation84 Libya (5),Citation85–Citation89 Morocco (9),Citation90–Citation98 Oman (4),Citation99–Citation102 Palestine (2),Citation103,Citation104 Pakistan (15),Citation105–Citation119 Qatar (1),Citation120 Saudi Arabia (21),Citation121–Citation141 Somalia (2),Citation142,Citation143 Sudan (4),Citation144–Citation147 Tunisia (20),Citation148–Citation167 United Arab Emirates (UAE) (3),Citation168–Citation170 and Yemen (4).Citation171–Citation174 No study related to Djibouti could be retrieved.
Figure 2. Literature search strategy (limited to articles published between 1990 and 2017 with abstracts in English or French) using the keywords “rotavirus” and “[country name]”.
![Figure 2. Literature search strategy (limited to articles published between 1990 and 2017 with abstracts in English or French) using the keywords “rotavirus” and “[country name]”.](/cms/asset/68971396-e1d5-461f-9347-c19ec5119a90/khvi_a_1603984_f0002_b.gif)
Details on study subjects, dates, settings and calculated RV prevalence from the studies across the region is shown in Tables S1-S3. Table S1 presents data from the North African countries (Egypt, Morocco, Tunisia, Somalia, Sudan, and Libya), Table S2 includes the Middle Eastern countries (Saudi Arabia, Lebanon, Bahrain, Oman, Palestine, Qatar, UAE, Yemen, Jordan, Iraq, and Kuwait) and Table S3 shows data from the Asian countries (Iran, Pakistan, and Afghanistan). A total of 113,959 cases of confirmed RVGE are reported in this review, with the highest number from Pakistan (n = 13,546) and the lowest from Somalia (n = 213).
Prevalence of RVGE
The prevalence of RV infection from different studies across the three regions (Nord Africa, Middle East, and Asia) is shown in .
Table 1. Prevalence of RVGE among AGE cases in studies from 1990 to 2017, per country.
Among the 165 articles included in this review, 152 (92.1%) reported RV prevalence data. The mean RV prevalence among AGE cases in the EMRO countries with more than two studies was between 21.4% (Sudan) and 46.6% (Oman) and the median was between 19.0% and 48.9%. The prevalence of RV in AGE cases was over 20% in 121 (79.6%) of them, with the highest reported rates observed in Egypt (76.9%), Afghanistan (76.2%) and Iran (70.2%). (, )Citation66 There were differences in RV isolation rates among multiple studies conducted within the same country, e.g. Pakistan (8.2% to 65.9%), Saudi Arabia (3.9% to 65.5%) and Egypt (range: 11% to 76.9%). However, in other countries, prevalence appeared to vary less, as seen by a narrower distribution in for certain countries including Morocco (17.2% to 44%), Tunisia (6.1% to 33.9%), or Jordan (26.6% to 49.5%)
Figure 3. Prevalence of RVGE among cases of AGE in individual studies per country.
The overall incidence was reported for studies detailing prevalence over several years, except when the study was comparing pre- and post-vaccination periods. In this case, the latest value was retained, as more actual.
There were also important differences in inpatient and outpatient RV prevalence. For example, in Egypt, in the 2011–2012 period, and using the same technique, the RV prevalence was 29.9% for outpatients and 43.9% for inpatientsCitation;29 in Tunisia, this prevalence was 18.5% and 24.9%,Citation166 and in Bahrain 6% and 27.4%, respectively.Citation13
Changes in the detection of RVGE over time
In Jordan, the RVGE detection rates among AGE cases were fairly constant over a ten-year period (25% in 1995, 35.2% in 2002, 24.7% in 2003, and 25.8% in 2004).Citation76 On the other hand, the proportion of RVGE cases appears to have increased over time in Pakistan; as the RVGE rates were ranging from 8.2% to 29% in the earlier years (1985–1996),Citation105,Citation107,Citation116 while in the more recent years (2007–2014) the reported rates were ranging from 23.8 to 65.9.Citation110–Citation115,Citation118,Citation119 This can be due to the difference of sensibility of EIA used during these two different periods, or to the choice and characteristics of patients investigated.
A reduction in RVGE occurrence is clearly evident after the introduction of RV vaccination in some countries. For instance, there was a 41.5% reduction in RV detection rate in the post-vaccination period compared to the pre-vaccination period in Morocco.Citation96 In Yemen there was a steady decline in RV detection following vaccine introduction; the detection rates during the pre-vaccination period was 43.8% and 37.4% in 2009 and 2010, respectively, but declined during the post-vaccination period to 17.9% in 2013 and to 10.5% in 2014.Citation174 In the same study, a 75.9% reduction in hospitalization due to RV diarrhea was reported over five years (2009: 43.8%; 2014: 10.5%). Banajeh et al.Citation173 also showed that in Yemen, after vaccination had started, the prevalence of RVGE decreased by 48% and the hospitalization rate due to RV diarrhea declined from 42.9% during the pre-vaccination period (2007/2011) to 18.5% in the post-vaccination period (2013/2014). A similar pattern was observed in Saudi Arabia, where the RVGE prevalence was reduced from 12% to 46% to 9.2% over a three-year period following the introduction of the RV vaccine in 2013.Citation141
Concomitant enteropathogens
About one fourth (38 of 165) of the reviewed publications concomitantly reported isolation of pathogens other than RV. However, RV was most frequently responsible for AGE cases in 29/38 (76.3%), second most frequent in 5/38 (13.2%) and third most frequent in 3/38 (7.9%) of the studies. Norovirus, Astrovirus, and Adenovirus were other common viral pathogens detected in AGE cases ().
Table 2. Distribution of enteropathogens isolated in AGE cases in the WHO-EMRO region.
RVGE seasonality patterns
A seasonality pattern of RVGE was reported in 95 of the 165 (57.6%) reviewed studies. Most studies (66/95, 69.5%) reported a peak of RVGE in the cold season from November to April. However, some studies also showed exceptional RVGE peaks occurring in late summer.Citation22,Citation111,Citation154,Citation172 Studies from Iran, Bahrain, and Saudi Arabia did not observe any seasonal variation of RVGE.Citation13,Citation39,Citation132
Detection techniques used
A total of 126 out of 147 studies that described RVGE prevalence also reported the isolation technique used for RV detection: 97 studies (77%) used enzyme immunoassay (EIA), 12 (9.5%) used latex agglutination (LA), 25 (19.8%) used polymerase chain reaction (PCR), 4 (3.2%) used polyacrylamide gel electrophoresis (PAGE) techniques, and a comparison with electron microscopy (EM) was made in 2 studies. Some of the studies also compared detection rates based on which techniques had been used. In Egypt, the positivity of RV detection varied between 34% and 39.5% according to LA and EIA techniques, respectively.Citation16 In Jordan, the sensitivity of EM and EIA RV detection techniques were 18.9% vs. 39.6%, respectively.Citation72 In Egypt, the sensitivity was higher when PCR (76.9%) was used as compared to EIA (67.7%).Citation30
Nosocomial RV infection
Nosocomial infection due to RV is also common. A study in Iraq showed that 32.4% of hospitalized children had nosocomial infections and 18.5% of them were due to RV.Citation41 The nosocomial infection rate was 33.3% in Morocco,Citation92 and in three different studies from Iran, the reported rates were 26.3%, 18.5% and 30%.Citation38,Citation41,Citation54
Disease severity and mortality rates
In Morocco, 1 child per 32 RV-infected children was hospitalized and 1 child per 389 RV-infected children died due to RVGE in a group of children under 5 years of age.Citation91 Another Moroccan study reported that 30% of hospitalizations for diarrhea were due to RVGE, with a mortality rate of 40–50%.Citation90 In Pakistan, 1 child per 40 infected children under 5 years of age had an episode of severe RVGE per year.Citation117 A meta-analysis spanning from 1989 to 2004 estimated 19,933 deaths due to RVGE in Pakistan, constituting 3.8% of the global RVGE mortality.Citation109 In Iran, 2,700 deaths due to RVGE occurred per year; it was estimated that 13–40% of all cases of diarrhea were due to RV and that 30% of them required hospitalization.Citation37,Citation40,Citation47
RV genotype and evolution of genotypes post-vaccine introduction
The genotype distribution of RV isolates in different studies was also reviewed. We evaluated the genotype combinations, where both G and P capsid protein combinations are reported. Studies conducted in 13 WHO-EMRO region countries (Bahrain, Egypt, Iran, Iraq, Jordan, Libya, Lebanon, Morocco, Oman, Pakistan, Saudi Arabia, Tunisia, and Yemen) reported RV genotype distribution (). Studies from Afghanistan, Palestine, Qatar, Somalia, and Sudan did not report on genotype distribution; Kuwait and UAE reported only G- or P-type, and were therefore not included in this evaluation. Overall, the genotype distribution was diverse across the region.
Table 3. RV genotype distribution (%) in WHO-EMRO countries.
G1P[8] was the most prevalent genotype combination in 7 of the 13 countries (i.e. Iran, Saudi Arabia, Jordan, Bahrain, Morocco, Iraq) for which data from the past 15 years are available ().Citation15,Citation34,Citation37,Citation45,Citation48,Citation57,Citation69,Citation78,Citation79,Citation90,Citation93–Citation96,Citation98,Citation100–Citation102,Citation130–Citation132,Citation138,Citation139,Citation141
G1P[8] and G2P[4] were the most common genotypes in Yemen and Egypt.Citation19,Citation23,Citation24,Citation27,Citation29,Citation32,Citation83,Citation84,Citation171,Citation172 In Lebanon, the genotype distribution varied over time and geographical location: the G4P[8] type disappeared from the northern part of the country in two out of the three studied seasons, while the G2P[4] genotype did not.Citation83 In Oman, the distribution pattern of the G2P[4] and G1P[8] RV genotypes also varied with time.Citation100–Citation102
In Tunisia, both G1P[8] and G3P[8] were common, followed by G4P[8].Citation148,Citation158,Citation159,Citation162–Citation164,Citation166 RV genotype G9 was first detected in 2004 in Tunisia and from 2010, there was an increase in the prevalence of related genotypes (10.3–37.5%).Citation165,Citation166
In Pakistan, the distribution of genotype combinations was heterogeneousCitation110–Citation112,Citation117,Citation118 and G12P[6] was found to be one of the most prevalent RV genotype in 2014.Citation115
The introduction of RV vaccines had a substantial effect on G1P[8] detection. In Saudi Arabia, a decrease was noted in G1P[8] detection from 51% to 37.1% after the vaccine was introduced, but G2P[4] increased from 21.6% to 33.3%.Citation141
In Morocco, a periodic decrease in the detection of G1P[8] genotype was reported: 57% one-year post-vaccination and 54.7% two years post-vaccination.Citation96 However, G2P4 was detected in 15% of samples in the pre-vaccination period and in 54% and 33% of samples, respectively, in the second and third years following the vaccine introduction. An increase was also seen for G9P[8] (7.8% in the pre-vaccination period, 16.6% and 67% in the second and third year of the post-vaccination period, respectively).
In Yemen, the G1P[8] detection rate increased from 45.5% to 87.5% and the G2P[4] detection rate decreased from 76.5% to 0.2% after vaccine implementation.Citation173 In another study in Yemen, the G1P[8] detection rate increased from 15% in the pre-vaccination period to 31% in the post-vaccination period and became the predominant genotype, followed by G9P[8] (27.5%).Citation174
In Iran, there was also an emergence of new RV genotypes over time, with G12P[8] being detected for the first time in 2016.Citation57 In Egypt, genotype G6P[14] was first reported in 2011.Citation26
Like in other parts of the world, mixed or non-typeable RV strains have also been detected in the WHO-EMRO region. In Iran, mixed genotype combinations, including G1P[4] and G1P[8], were detected in two studies, and the rate of mixed genotypes varied from 2.7% to 33.3%.Citation47,Citation49 Non-typed (Nt) strain detection in Iran ranged from 5% to 40.9%.Citation34,Citation68 In Pakistan, Egypt and Tunisia, the detection rates for mixed RV genotypes were 6.7%, 7% and 5.9%, respectively.Citation19,Citation113,Citation148
Vaccination status
The demographic characteristics and the type of RV vaccine used in the WHO-EMRO countries are shown in . An RV vaccine was available in 19 (86.4%) of the 22 WHO-EMRO countries; either publicly (10/22), both publicly and privately (5/22), or only privately (4/22). No RV vaccine was available in three (13.6%) WHO-EMRO countries (Iran, Somalia, and Syria). Fifteen (72.7%) WHO-EMRO countries had introduced an RV vaccine in their NIP (Afghanistan, Bahrain, Djibouti, Iraq, Jordan, Kuwait, Libya, Morocco, Pakistan, Palestine, Qatar, Saudi Arabia, Sudan, UAE, and Yemen). Six (27.3%) of the 22 EMRO countries were eligible for GAVI support. ().
Table 4. Demographics and RV vaccination status of the 22 WHO-EMRO countries.
Discussion
This review evaluated the RV infection status in the WHO-EMRO region, identified reductions in RV prevalence and mortality following implementation of RV vaccination and described existing RV surveillance systems in the region.
In the WHO-EMRO region, the observed RVGE burden varied between countries. In general, a low RVGE prevalence (<30%) was observed in Egypt, Saudi Arabia, and Tunisia, and a high prevalence (>30%) was reported in Iran, Lebanon, Morocco, Jordan, and Oman.Citation8 The annual proportion of RVGE among reported episodes of AGE in the under-five-years-of-age population in this region was 42%, and recent studies have estimated that about 65,000 children die each year from RV infections in the 22 WHO-EMRO countries.Citation9 This is likely to be an underestimation of the true prevalence, due to inadequate surveillance systems and lack of routine RV testing. Although a majority (81.8%) of EMRO countries have implemented RV vaccination, seven countries (Egypt, Iran, Lebanon, Oman, Somalia, Syria, and Tunisia) have not yet implemented RV vaccination in their NIPs. Furthermore, no RV vaccine is available in three (13.6%) EMRO countries (Iran, Somalia, and Syria).
RV was the most common AGE agent in the WHO-EMRO region in 76.3% of the reviewed studies. Our review also revealed that there is a wide variation (>20% difference between studies) in RV isolation rates in different studies conducted within the same countries; for example, in Iran,Citation40 Pakistan,Citation105,Citation114 Saudi ArabiaCitation132,Citation135 and Morocco,Citation89,Citation95 the difference of reported isolation rates was wide. However, in countries such as TunisiaCitation156,Citation163 and Jordan,Citation74,Citation78 the rate differences were smaller. Differences in study design, patient selection, and case definition could contribute to explain differences in observed incidences across studies.
This review also confirmed that as in Western Europe,Citation179 G1P[8] and G2P[4] are the predominant genotypes circulating in the WHO-EMRO region and that available RV vaccines can provide protection against them. It is apparent that the circulating RV strain distribution regularly changes, as well as the dominant genotype, even in the absence of vaccines. Interestingly, G12P[8], a recently emerging serotype previously detected in Europe, Asia, and the Americas, has also been reported in some studies in Saudi Arabia.Citation8,Citation139,Citation141 Unusual genotypes such as G1P[6], G2P[6], G3P[9], G4P[6], G9P[6] and G9P[8] have been detected in different countries,Citation118,Citation132,Citation148,Citation157 including the recent emergence of genotype G12P[6] in PakistanCitation115 and of genotype G12P[8] in Iran.Citation60 Data of genotyping diversity from the WHO-EMRO region confirm that these findings are not specific to a particular geographic location but a natural phenomenon worldwide.
Mixed genotype combinations were detected in Iran,Citation49,Citation60 Tunisia,Citation149,Citation150 and Pakistan.Citation112 These results are similar to recent findings in India, Indonesia, and Vietnam and are likely due to reassortments.Citation10 The proportion of non-typeable and partially typeable genotype combinations also varied widely across countries.Citation6,Citation48,Citation49,Citation100 Differences in laboratory techniques, as well as different geographic settings, can explain these findings. With the use of more appropriate genotyping primers and advanced molecular techniques, the proportion of non-typeable strains has decreased in recent studies.
A shift in genotype predominance and circulation before and after vaccine introduction is not unusual and cannot be attributed to available vaccines. Countries such as Australia and Brazil that have used different vaccines have also faced the re-emergence of G2 strains after vaccine introduction.Citation180,Citation181 These data simply reflect the normal fluctuation in RV genotype frequency. In order to substantiate any vaccine pressure on genotype shift, continued surveillance over time, detailed phylogenic analysis, and full RV genome sequencing are required. Although these measures are currently not in place in the WHO-EMRO region, policy measures aimed at implementing these measures would greatly enhance our understanding of changes in RV strain circulation in the region.
In general, RV infections peak in the cooler winter months, and this pattern is similar for all WHO-EMRO countries except Gulf region countries. Studies from Saudi Arabia and neighboring countries showed no distinct peak, as RV disease was observed throughout the year with occasional peaks irrespective of season.Citation132
Several countries that have implemented routine childhood vaccination against RV have documented a dramatic impact on severe diarrhea and RVGE requiring hospitalization.Citation182–185 In the WHO-EMRO region, a small number of studies also show the effectiveness of vaccination on RVGE hospitalization, as well as RV detection in AGE cases. The results of these studies reflect that vaccination can markedly reduce RVGE disease burden, especially hospitalization due to diarrhea.Citation99,Citation141,Citation173,Citation174
The WHO recommends sentinel surveillance before and after the introduction of vaccines to monitor vaccine impact. As financial resources may be limited in this region, regional governments should consider sharing their data with local laboratories or existing surveillance networks to help achieve this goal. Documentation of the burden of disease and of circulating strains is essential for decision-making on vaccine introduction and vaccine effectiveness assessments. The burden of RVGE and the circulation of different RV strains should be monitored in a surveillance system and through standardized methods, which would enable comparisons between countries.
We observed that no single standard technique was used to isolate and genotype RV from stool samples. This is likely to have led to a variation of estimates, not only in different countries but also across studies conducted within a country. Thus, we decided to present descriptive results instead of direct comparisons.
The various studies reported here included patients from different age strata in both in- and outpatient settings, which may potentially lead to misclassifications. It is easily conceivable that patients admitted as inpatients were suffering from more severe disease and were therefore more likely to yield a pathogen from their stool sample than outpatient stool samples originating from patients with less severe infections. This was evident from studies in Saudi Arabia,Citation127 where the RV detection rate was 5.9% in outpatient settings compared with 34.6% in inpatient settings; in IranCitation66 the rates were 20.9% and 79.1% in outpatient and inpatient settings, respectively.
Variations in the estimates between and within countries could also be due to different study populations, study time periods, RV isolation and detection techniques, and the definition of RVGE used as study inclusion criteria. In some countries such as Afghanistan, Bahrain, Iraq, Kuwait, Lebanon, Palestine, Qatar, Somalia, and Sudan, the number of studies and subjects enrolled was not adequate for accurately estimating the burden and strain distribution of RVGE.
Although our review is one of the first to explore the prevalence of RV in the WHO-EMRO region, it has several limitations. Firstly, there is also a possible bias in identifying a denominator for the estimates. In some studies, RV rates were detected over total stool samples collected, while in others, the RV proportion was reported among the cases where at least one pathogen was detected. Secondly, our search was limited to published studies with abstracts in English and French, which may have resulted in the exclusion of studies published only in local languages. Thirdly, gaps in reporting from several WHO-EMRO countries may be due to political instability and not a lack of RV infections, and political instability may also prevent the successful implementation of vaccination programs and longitudinal RV vaccine studies.
In conclusion, this review of 165 studies from WHO-EMRO countries revealed that RV was strongly associated with young age in children and remained the dominant etiology of diarrhea requiring hospitalization, even in countries that had recently introduced RV vaccination. The collated data in this study will serve as useful baseline RV epidemiological data for the planning and implementation of vaccination programs in the region. Although the burden of RVGE is likely to decrease following the successful introduction of RV vaccination programs, as exemplified by Yemen,Citation171 ongoing surveillance is needed to determine the residual burden of RV, the genotype distribution of RV, and to monitor the evolving etiology of diarrhea in these countries. Data compiled in this report highlights that nearly all serious infections due to diarrhea occurred in children under 2 years of age, which stresses the need for protection early in life, and advocates for RV vaccine schedule completion by 12 months of age.
Methods
The inclusion criteria for the search was any publication in English or French in a country of the WHO-EMRO region on RV diarrhea in children less than five years of age during the period of January 1990 to December 5, 2017. We used the keywords “rotavirus” and “[country name]” (for each individual country out of the 22 included in the WHO-EMRO) to search in The National Library of Medicine’s PubMed and grey literature (). We also included publications in local medical journals and in local languages for which abstracts in English or in French were available. We further reviewed the cross-referenced articles from the retrieved ones.
A total of 426 published articles were identified, 387 from PubMed and 39 from local journals. Articles studying animals or environment (97), reporting the clinical aspects of infection studies (116), studying vaccine implementation or cost-effectiveness (32), or using non-standard detection techniques (16) were excluded, and 165 articles were included for complete full-text review and qualitative assessment ().
Authors, year of publication, type of article, patient type and numbers were reported for each publication. The prevalence of RV infection mentioned in the articles was the main focus of this study, and we also retained articles mentioning RVGE mortality, or RV genotyping. In addition, and where available, data on nosocomial infections, seasonality, techniques used for the detection, RV genotype distribution, variation over time in the proportion of RVGE, and evolution of genotype distribution, presence of other enteric co-pathogens and the vaccination status of the country was also abstracted. Each datum was abstracted by one author, and crossed-check by another author. Next, we calculated the RVGE prevalence as the number of reported RVGE cases over the total number of samples included in each study, to use a standard measure of the RVGE prevalence. When possible (i.e. when three studies or more were retrieved for one country), the mean and median prevalence was given for each country. Data were stratified by country.
Trademark statement
Rotarix is a trademark of the GSK group of companies. Rotateq is a trademark of Merck and Co Inc.
Disclosure of potential conflicts of interest
All authors are employed by the GSK group of companies. SB, SO, PP, MAG, MK, YL, KH, and DS hold shares in the GSK group of companies.
Authors’ contribution
Selim Badur, Mohammad AbdelGhany, Mansour Khalaf, Youness Lagoubi, Onur Ozudogru, and Kashif Hanif performed the literature search. All authors contributed to acquisition of data, analysis and interpretation of data, and revised the article critically for important intellectual content. All authors provided final approval of the submitted version.
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The authors thank the Business & Decision Life Sciences platform for editorial assistance and manuscript coordination, on behalf of GSK. Amandine Radziejwoski coordinated the manuscript development and editorial support. Stefan Amisten provided editorial support.
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