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. 2024 May 9;24:478. doi: 10.1186/s12879-024-09386-x

Human adenoviruses in children with gastroenteritis: a systematic review and meta-analysis

Pegah Khales 1, Mohammad Hossein Razizadeh 2,3, Saied Ghorbani 1, Afagh Moattari 1, Jamal Sarvari 1, Hassan Saadati 4, Shirin Sayyahfar 5, Zahra Salavatiha 2, Morteza Haghighi Hasanabad 3, Vahdat Poortahmasebi 6,7, Ahmad Tavakoli 5,✉
PMCID: PMC11084101  PMID: 38724898

Abstract

Purpose

Human adenoviruses (HAdVs) have always been suggested as one of the main causes of gastroenteritis in children. However, no comprehensive report on the global epidemiology of these viruses in pediatric gastroenteritis is available.

Methods

A systematic search was conducted to obtain published papers from 2003 to 2023 in three main databases PubMed, Scopus, and Web of Science.

Results

The estimated global pooled prevalence of HAdV infection in children with gastroenteritis was 10% (95% CI: 9-11%), with a growing trend after 2010. The highest prevalence was observed in Africa (20%, 95% CI: 14–26%). The prevalence was higher in inpatients (11%; 95% CI: 8-13%) and patients aged 5 years old and younger (9%; 95% CI: 7-10%). However, no significant difference was observed between male and female patients (P = 0.63). The most prevalent species was found to be the species F (57%; 95% CI: 41-72%). The most common HAdVs observed in children with gastroenteritis were types 40/41, 38, and 2. Analysis of case-control studies showed an association between HAdV and gastroenteritis in children (OR: 2.28, 95% CI; 1.51–3.44).

Conclusion

This study provided valuable insights into the importance of HAdVs in children with gastroenteritis, especially in hospitalized and younger children. The results can be used in future preventive measurements and the development of effective vaccines.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12879-024-09386-x.

Keywords: Gastroenteritis, Human adenoviruses, Pediatrics, Epidemiology, Children

Introduction

Acute gastroenteritis is a serious threat to health that affects individuals of any age. It is especially serious for the very young, such as newborns and young children [1, 2]. Because of their underdeveloped immunity, children are more susceptible to diarrheal illnesses. Different enteric pathogens, including bacteria, viruses, protozoa, helminths, and fungi, can cause diarrhea. These pathogens are typically transmitted by ingesting contaminated food, water, or things infected with feces [3]. Previous studies have shown that the virus is the most common cause of acute gastroenteritis in individuals younger than 18 years of age [4, 5]. The most common causes of acute gastroenteritis in children are rotavirus, norovirus (NoV), human adenovirus (HAdV), and human astrovirus (HAstV) [6, 7].

HAdV is a member of the Adenoviridae family and the Mastadenovirus genus. HAdV is a non-enveloped, medium-sized virus (70–100 nm) with an icosahedral nucleocapsid that contains a 34–45 kbp double-stranded linear DNA genome [8, 9]. HAdVs have been divided into seven species A to G based on pathogenicity and genetic features, with 115 distinct HAdVs genotypes being identified [10]. Based on the percentage of guanine plus cytosine in their DNA and other biochemical and biophysical criteria which are classified into 7 species (A-G). The word serotype is used to point to types up to 51 while newer types, which were differentiated by novel sequences or recombinant phylogeny in genes coding for major capsid proteins are known as genotype. Species G is composed of one type (type 52) and is extremely rare while other species are found in patients with various diseases including gastroenteritis, conjunctivitis, respiratory infections, and to a lesser extent in intussusception in infants, hemorrhagic cystitis, meningoencephalitis, myocarditis, and hepatitis [11]. HAdV infection, a highly infectious disease, can infect a range of organs, including upper and lower respiratory tracts, gastrointestinal tract, urinary tract, eye, and other systems [11]. . Tissue tropisms vary by species. It has been determined that the primary cause of acute gastroenteritis among the seven species is the HAdV F species, also known as enteric HAdV, which contains the HAdV-F40 and HAdV-F41 genotypes [12–15]. Enteric species F (genotypes F40/41) strains were predicted using a mathematical model to be the third most common agent responsible for mortality in diarrheal children under the age of five, after rotavirus and Shigella [16]. Furthermore, stool samples from patients with acute gastroenteritis have regularly revealed the presence of several other non-enteric HAdV species (HAdV A-E and G species), including HAdV A, B, C, and D [12, 13, 15, 17–20].

While there are many reports from different parts of the world, there is a gap of knowledge in understanding the epidemiology and association of HAdVs and pediatric gastroenteritis. This study aims to fulfill this gap by comprehensively analysis various factors including age group, gender, geographical teacher, clinical setting, diagnostics methods, species, and genotypes in pediatrics gastroenteritis for the first time to provide valuable insights into the current status of HAdVs in children with gastroenteritis.

Methods

The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guideline served as the foundation for this systematic review and meta-analysis approach [21].

Search strategy

To discover relevant papers, a systematic literature search was undertaken utilizing three electronic databases including PubMed, Scopus, and Web of Science. The literature search was restricted to the period between inception to June 24, 2023. Table S1 provides information about the search terms for each database. We manually searched the reference lists of pertinent articles to find further research that met the eligibility criteria. For data management, the systematic literature search was loaded into EndNote software version X8 (Thomson Reuters, California, USA).

Selection criteria

Studies were considered qualified if they reported: (1) case-control and cross-sectional studies providing data related to the prevalence of enteric and non-enteric HAdVs among children less than 18 years with gastroenteritis published in the English language in peer-reviewed journals; (2) the prevalence of HAdV genome in stool samples and rectal swabs; (3) studies detecting HAdV genome by polymerase chain reaction (PCR)-based methods; (4) studies detecting the prevalence of HAdV among inpatients and outpatients; (5) original articles and short communications with sufficient data. Studies that met any of the following criteria were excluded: (1) the prevalence of HAdV infection among adults patients with gastroenteritis; (2) the prevalence of HAdV infection among children presenting gastroenteritis with underlying conditions such as transplant recipients, HIV, immunocompromised status, and cancers; (3) the incidence of HAdV infection among children with gastroenteritis; (4) samples other than stool such as oral swabs, serum, cerebrospinal fluid, and conjunctival swabs; (5) detection of HAdV by assays othe than PCR-based methods such as antigen detection assays, immunochromatography, Loop-mediated isothermal amplification, next-generation sequencing-based viral metagenomics, microarray, latex agglutination, electronmicroscopy, DNA restriction enzyme analysis, enzyme immunoassay, culture techniques, immunoelectron microscopy, and nucleic acid hybridization; (6) seroprevalence of HAdV antibodies; (7) studies included patients with non-gastroenteritis symptoms such as respiratory symptoms, acute severe hepatitis, and asymptomatic; (8) letters, case series, notes, review articles, case reports, posters, and conference abstracts; (9) articles published in languages other than English.

Data extraction and quality assessment

Two reviewers separately examined the titles and abstracts of all identified papers, and studies that were unrelated to the study topic were eliminated. The reviewers got full texts of the selected papers and further analyzed them, and those that did not meet the inclusion criteria were excluded. Finally, any differences among reviewers were settled by consulting with a third reviewer. Utilizing a modified checklist based on strengthening the reporting of observational studies in epidemiology (STROBE), a quality assessment of the retrieved studies was carried out [22, 23]. The checklist consisted of 12 questions that addressed various methodological approaches. Studies that received a validity score of at least 8 out of a maximum of 12 were considered eligible for the main meta-analysis. One reviewer extracted the data listed below from each eligible article: first author’s last name, year of publication, year of sampling, study location, study design, sample size, age ranges of patients, age groups of patients, the gender of patients, number of HAdV-positive cases, HAdV detection methods, types of patient care, species, and genotype of HAdV. The retrieved data were entered into a pre-designed Excel spreadsheet (Microsoft Corporation, Redmond, Washington, USA).

Statistical analysis

We pooled the HAdV infection in children suffering from gastroenteritis using the metaprop package [24]. We applied the random-effects meta-analysis framework and subgroup analysis was conducted based on region, gender, age, detection method, sampling time, types of patient care, and genotype of HAdV. We also conducted meta-analyses of risk estimates for gastroenteritis and exposure to HAdV, and we reported pooled estimates of odds ratio (OR) and 95% CIs. DerSimonian and Laird method was used to compute the pooled estimate of OR with confidence interval (95% CI) using random models. Statistical heterogeneity between studies was evaluated with Cochran’s Q test and quantified by I2 statistic [25]. We investigated the presence and the effect of publication bias using a combination of the visual inspection of funnel plots that were constructed, plotting the logarithmically transformed ORs against the standard error of the associated log (OR) and Begg’s test and Egger’s test. All statistical tests were two-tailed and the significance level was considered less than 0.05 for all, except heterogeneity test that were set at less than 0.1, and statistical analyses were performed using Stata 14.1 (Stata Corp, College Station, TX, USA).

Results

Literature search

During the initial search, 3733 papers were identified, and 40 further papers were discovered by manually examining the reference lists of pertinent research. A total of 1592 duplicate papers were initially removed, and 1766 additional papers were removed after a manual check of titles and abstracts. After a thorough evaluation of the full text of the remaining 415 papers to determine their eligibility for the meta-analysis, 251 of them were removed. According to the modified STROBE checklist, 155 publications were deemed to be of good quality (scoring of 8 or higher), with 9 papers were failed to get a score of 8. Finally, this systematic review and meta-analysis contained 155 papers. An overview of the selection of relevant studies is depicted in Fig. 1.

Fig. 1.

Fig. 1

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Flowchart presenting the steps of literature search and selection

Study characteristics

Out of the 155 studies considered, 134 were cross-sectional and 21 were case-control in design. The articles’ publication dates varied from 2003 to 2023. The largest research involved 85,001 gastroenteritis cases [26], while the smallest contained 24 cases [27]. Out of the 155 papers included in this meta-analysis, 19 research examined the gender distribution of HAdV infection, and 80 studies looked into the genotype distribution of HAdVs. Specific primers for the detection of HAdVs group F (types 40 and 41) and universal primers identifying all types of HAdVs have been used in 37 and 118 studies, respectively. The majority of study populations (n = 103,815) were children under 5 years of age and 12,982 were children between the ages of 6 and 18 years old. The majority of studies (n = 29) were conducted in China, followed by Brazil (n = 12), India (n = 11), and Japan (n = 10). Regarding the continent, 84 were conducted in Asia, 26 in South America, 18 in Europe, 16 in North America, 9 in Africa, and 2 in Oceania. The characteristics of included studies in this systematic review and meta-analysis are summarized in Table 1.

Table 1.

Characteristics of studies included in the systematic review and meta-analysis

Author (Ref) Publication Year Location Study design Age Range Number of cases No. Positive in cases Number of controls No. Positive in controls
Oh [28] 2003 Germany Cross-Sectional 29 days to 15.5 years 217 31
Phan [29] 2004 Japan Cross-Sectional 2 months to 14 years 236 9
Yan [30] 2004 China Cross-Sectional Under 7 years 207 12
Akihara [31] 2005 Japan Case-Control 1 month to 2 years 88 11 833 96
Logan [32] 2006 Ireland Cross-Sectional Under 18 years 220 11
Phan [33] 2006 Japan Cross-Sectional 5 months to 8 years 125 1
Reither [34] 2007 Ghana Case-Control Under 12 years 243 67 124 39
Chen [35] 2007 Taiwan Cross-Sectional 3 months to 18 years 257 51
Fabiana [36] 2007 Italy Cross-Sectional 2 months to 12 years 313 29
Nguyen [37] 2007 Vietnam Cross-Sectional 37 days to 9 years 1010 32
Shimizu [38] 2007 Japan Cross-Sectional 3 months to 14 years 337 27
Gomara [39] 2008 UK Cross-Sectional Under 6 years 685 66
Jin [40] 2008 China Cross-Sectional Under 5 years 1110 85
Silva [41] 2008 Ghana Cross-Sectional Under 11 years 367 73
Verma [42] 2008 India Cross-Sectional Under 5 years 439 34
Dey [43] 2009 Japan Cross-Sectional Under 10 years 628 28
Dey [44] 2009 Bangladesh Cross-Sectional 2 months to 3.2 years 917 17
Jin [45] 2009 China Cross-Sectional Under 5 years 544 18
Kittigul [46] 2009 Thailand Cross-Sectional Under 15 years 131 4
Li [47] 2009 Hong Kong Cross-Sectional Under 18 years 209 7
Nakanishi [48] 2009 Japan Cross-Sectional Under 14 years 877 33
Podkolzin [49] 2009 Russia Cross-Sectional Under 14 years 3208 119
Sdiri-Loulizi [50] 2009 Tunisia Cross-Sectional Under 12 years 788 18
Cunliffe [51] 2010 UK Cross-Sectional Under 16 years 576 83
Rasanen [52] 2010 Finland Cross-Sectional Under 15 years 50 5
Zhang [53] 2011 China Case-Control Under 5 years 201 10 53 5
Khamrin [54] 2011 Japan Cross-Sectional Under 5 years 235 8
Rimoldi [55] 2011 Italy Cross-Sectional Under 18 years 273 4
Braun [27] 2012 USA Case-Control Under 2 years 24 11 78 43
Chaimongkol [56] 2012 Thailand Cross-Sectional Under 5 years 160 3
Grant [57] 2012 USA Cross-Sectional Under 9 months 247 3
Lee [58] 2012 South Korea Cross-Sectional Under 18 years 2064 113
Ouyang [59] 2012 China Cross-Sectional Under 5 years 766 135
Rezaei [60] 2012 Iran Cross-Sectional Under 5 years 100 8
Seo [61] 2012 South Korea Cross-Sectional Under 10 years 310 48
Chhabra [62] 2013 USA Case-Control Under 5 years 782 93 499 9
Al-Thani [63] 2013 Qatar Cross-Sectional Under 10 years 121 11
Chen [64] 2013 China Cross-Sectional Under 5 years 811 22
Chen [65] 2013 Taiwan Cross-Sectional Under 18 years 755 69
Dey [66] 2013 Japan Cross-Sectional Under 15 years 7185 565
Ren [67] 2013 China Cross-Sectional Under 5 years 477 30
So [68] 2013 South Korea Cross-Sectional 1 month to 11 years 186 0
Zhu [69] 2013 China Cross-Sectional Under 3 years 749 6
Kabayiza [70] 2014 Rwanda Case-Control Under 5 years 544 216 162 68
Chhabra [71] 2014 Soviet Union Cross-Sectional Under 5 years 495 20
Kabayiza [72] 2014 Rwanda Cross-Sectional Under 5 years 880 216
Liu [73] 2014 China Cross-Sectional Under 6 years 2233 219
Mitui [74] 2014 Turkey and Bangladesh Cross-Sectional Under 5 years 288 168
Raboni [75] 2014 Brazil Cross-Sectional Under 5 years 225 45
Soli [76] 2014 New Guinea Cross-Sectional Under 5 years 199 23
Amaral [77] 2015 Brazil Cross-Sectional Under 5 years 591 12
Chen [78] 2015 Taiwan Cross-Sectional Under 5 years 2810 105
Khoshdel [79] 2015 Iran Cross-Sectional Under 5 years 100 22
La Rosa [19] 2015 Albania Cross-Sectional 2 months to 7 years 142 33
Lekana-Douki [80] 2015 Gabon Cross-Sectional Under 5 years 317 62
Liu [81] 2015 China Cross-Sectional Under 5 years 2171 150
Lu [82] 2015 China Cross-Sectional Under 5 years 436 31
Mladenova [83] 2015 Bulgaria Cross-Sectional Under 3 years 115 11
Osborne [84] 2015 USA Cross-Sectional Under 18 years 941 95
Patil [85] 2015 India Cross-Sectional Under 9 years 950 12
Thongprachum [86] 2015 Japan Cross-Sectional Under 15 years 2381 134
Yu [87] 2015 China Cross-Sectional Under 5 years 18,266 879
Zhang [88] 2015 China Cross-Sectional Under 14 years 1128 76
Li [89] 2016 China Case-Control Under 5 years 461 50 461 12
Ouédraogo [90] 2016 Burkina Faso Case-Control Under 5 years 263 82 50 25
Steyer [91] 2016 Slovenia Case-Control Under 6 years 297 22 88 0
Brown [92] 2016 UK Cross-Sectional Under 18 years 1393 146
Dashti [93] 2016 Iran Cross-Sectional Under 5 years 2682 132
Jin [94] 2016 South Korea Cross-Sectional 1 month to 16 years 345 26
Liu [95] 2016 China Cross-Sectional Under 5 years 3147 324
Nakamura [96] 2016 Japan Cross-Sectional Under 15 years 1796 88
Reis [97] 2016 Brazil Cross-Sectional Under 12 years 377 47
Shen [98] 2016 China Cross-Sectional Under 18 years 137 3
Colak [99] 2017 Turkey Cross-Sectional Under 5 years 180 25
Cornejo-Tapia [100] 2017 Peru Cross-Sectional Under 5 years 117 17
Costa [101] 2017 Brazil Cross-Sectional Under 2 years 172 74
Hawash [102] 2017 Saudi Arabia Cross-Sectional Under 18 years 76 5
Kim [103] 2017 South Korea Cross-Sectional Under 16 years 415 56
Lu [104] 2017 China Cross-Sectional Under 5 years 674 32
Stockmann [105] 2017 USA Cross-Sectional Under 18 years 1089 71
Zaki [106] 2017 Egypt Cross-Sectional Under 5 years 100 20
Qiu [107] 2018 China Case-Control Under 18 years 273 79 361 26
Adam [108] 2018 Sudan Cross-Sectional Under 5 years 437 7
Alcala [109] 2018 Venezuela Cross-Sectional Under 5 years 227 26
Biscaro [110] 2018 Italy Cross-Sectional 2 months to 15 years 510 35
Primo [111] 2018 Brazil Cross-Sectional Under 10 years 2009 107
Yu [112] 2018 Taiwan Cross-Sectional Under 5 years 837 13
Hassan [113] 2019 USA Case-Control Under 2 years 330 75 272 44
Iturriza-Gomara [114] 2019 Malawi Case-Control Under 5 years 684 199 527 14
Lima [115] 2019 Brazil Case-Control 2 months to 3 years 588 19 573 5
Shen [116] 2019 China Case-Control Under 18 years 273 24 361 16
Tilmanne [117] 2019 Belgium Case-Control Under 16 years 178 12 165 5
Arashkia [118] 2019 Iran Cross-Sectional Under 5 years 376 16
Arowolo [119] 2019 Nigeria Cross-Sectional Under 5 years 175 9
Elmahdy [120] 2019 Egypt Cross-Sectional Under 5 years 60 17
Gaensbauer [121] 2019 Guatemala Cross-Sectional 6 to 35 months 316 41
Gelaw [13] 2019 Ethiopia Cross-Sectional Under 5 years 450 144
Goldar [122] 2019 India Cross-Sectional 6 months to 5 years 80 27
Harb [123] 2019 Iraq Cross-Sectional Under 5 years 155 53
Kumthip [12] 2019 Thailand Cross-Sectional Under 5 years 2312 165
Portal [124] 2019 Brazil Cross-Sectional Under 9 years 219 110
Pratte-Santos [125] 2019 Brazil Cross-Sectional Under 12 years 134 81
Tatte [126] 2019 India Cross-Sectional Under 5 years 185 5
Theamboonlers [127] 2019 Thailand Cross-Sectional Under 15 years 442 87
Farfan-Garcia [128] 2020 Colombia Case-Control Under 5 years 431 14 430 1
Pabbaraju [129] 2020 Canada Case-Control Under 18 years 3347 629 1355 97
Dey [130] 2020 Bangladesh Cross-Sectional Under 15 years 574 24
Kim [131] 2020 South Korea Cross-Sectional Under 5 years 740 7
Lambisia [132] 2020 Kenya Cross-Sectional Under 5 years 984 120
Mohammadi [133] 2020 Iran Cross-Sectional Under 5 years 103 3
Mousavi Nasab [134] 2020 Iran Cross-Sectional Under 5 years 120 6
Romo-Saenz [135] 2020 Mexico Cross-Sectional Under 5 years 57 8
Sharif [136] 2020 Bangladesh Cross-Sectional Under 15 years 387 22
Zhu [137] 2020 China Cross-Sectional Under 5 years 1220 37
Alsuwaidi [138] 2021 UAE Case-Control Under 5 years 203 35 73 2
Harrison [139] 2021 USA Case-Control Under 11 years 660 51 624 9
Huang [140] 2021 China Case-Control Under 5 years 383 21 327 13
Mero [141] 2021 Guinea-Bissau Case-Control Under 5 years 228 40 201 32
Abdel-Rahman [142] 2021 Qatar Cross-Sectional 3 months and 14 years 901 59
Barsoum [143] 2021 Ireland Cross-Sectional Under 3 years 150 19
Chandra [144] 2021 India Cross-Sectional Under 5 years 3882 351
Chang [145] 2021 China Cross-Sectional Under 18 years 2692 193
De Francesco [146] 2021 Italy Cross-Sectional Under 18 years 476 34
Gopalkrishna [147] 2021 India Cross-Sectional Under 5 years 308 25
Huang [14] 2021 China Cross-Sectional Under 5 years 656 49
Lu [148] 2021 China Cross-Sectional Under 5 years 804 28
Ndjangangoye [149] 2021 Gabon Cross Sectional Under 15 years 66 54
Olivares [150] 2021 Brazil Cross-Sectional Under 5 years 458 139
Rossouw [151] 2021 South Africa Cross-Sectional Under 5 years 221 15
Souza [152] 2021 Brazil Cross-Sectional Under 18 years 1992 166
Souza [153] 2021 Brazil Cross-Sectional Under 14 years 3419 171
Wang [26] 2021 China Cross-Sectional Under 18 years 85,001 2284
Abbasi [154] 2022 Iran Cross-Sectional Under 7 years 173 4
Allayeh [155] 2022 Egypt Cross-Sectional Under 5 years 447 35
Al-Nasrawy [156] 2022 Iraq Cross-Sectional Under 3 years 450 150
Colito [157] 2022 Cape Verde Cross-Sectional Under 12 years 105 7
do Nascimento [158] 2022 Brazil Cross-Sectional Under 18 years 1012 227
Dong [159] 2022 China Cross-Sectional Under 5 years 897 106
Gelaw [160] 2022 Ethiopia Cross-Sectional Under 5 years 38 7
Jo [161] 2022 South Korea Cross-Sectional Under 9 years 184 1
Li [162] 2022 China Cross-Sectional Under 14 years 160 15
Mihala [163] 2022 Australia Cross-Sectional Under 2 years 11,111 2171
Mitra [164] 2022 India Cross-Sectional Under 5 years 3157 276
Othma [165] 2022 Egypt Cross-Sectional Under 5 years 50 3
Shams [166] 2022 Iran Cross-Sectional Under 15 years 130 23
Tang [20] 2022 China Cross-Sectional Under 14 years 1352 60
Yılmaz [167] 2022 Turkey Cross-Sectional Under 18 years 94 13
Bhat [168] 2023 India Cross-Sectional 1 month to 18 years 109 0
Borkakoty [169] 2023 India Cross-Sectional Under 5 years 407 187
Eifan [170] 2023 Saudi Arabia Cross-Sectional Under 18 years 97 6
Hugho [3] 2023 Tanzania Cross-Sectional Under 5 years 146 29
Joshi [16] 2023 India Cross-Sectional Under 5 years 1167 61
Lu [171] 2023 China Cross-Sectional Under 15 years 1048 97
Ndjangangoye [172] 2023 Gabon Cross Sectional Under 15 years 284 75
Potgieter [173] 2023 South Africa Cross-Sectional Under 5 years 275 52
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Prevalence of HAdV infection among children with gastroenteritis

The estimated global pooled prevalence of HAdV infection among 222,267 gastroenteritis-affected children from 51 countries was 10% (95% CI: 9-11%; I²=98.6%; P < 0.001). By age, children aged 13 to 24 months had a slightly greater prevalence of HAdV (14%; 95% CI: 9-20%) than children of other ages (P = 0.56). The frequency of HAdV infection was similar between males and females (8%; 95% CI: 6-11% vs. 8%; 95% CI: 6-10%, respectively; P = 0.63) (Table 2).

Table 2.

Subgroup analysis of the prevalence of HAdV infection among pediatric patients with gastroenteritis

Group Number of studies Pooled prevalence (%) (95%CI) Heterogeneity test
I2%, p-value		 Differences between subgroups; χ2 test
(p-value)
Overall prevalence - 155 0.10 (0.09–0.11) 98.63, < 0.001
Study design Cross-sectional 134 0.10 (0.08–0.11) 98.58, < 0.001 P = 0.01
Case-control 21 0.15 (0.11–0.20) 97.32, < 0.001
Method Nested PCR 8 0.23 (0.12–0.37) 98.17, < 0.001 P < 0.001
Multiplex PCR 44 0.05 (0.04–0.06) 94.27, < 0.001
Real-time PCR 29 0.15 (0.12–0.19) 98.27, < 0.001
Conventional PCR 61 0.09 (0.08–0.11) 98.09, < 0.001
Multiplex Real-time PCR 13 0.17 (0.10–0.26) 97.74, < 0.001
Primer Universal 118 0.10 (0.09–0.12) 98.84, < 0.001 P = 0.60
Group F 37 0.10 (0.08–0.12) 95.87, < 0.001
Sampling time 1996–2000 2 0.32 (0.26–0.37) NA P < 0.001
2001–2005 16 0.08 (0.04–0.12) 97.74, < 0.001
2006–2010 36 0.08 (0.06–0.09) 95.15, < 0.001
2011–2015 42 0.12 (0.10–0.15) 98.88, < 0.001
2016–2020 51 0.11 (0.08–0.13) 97.21, < 0.001
2021–2022 8 0.13 (0.06–0.21) 99.14, < 0.001
Continent South America 26 0.16 (0.10–0.22) 98.61, < 0.001 P < 0.001
Asia 84 0.07 (0.06–0.08) 97.70, < 0.001
Europe 18 0.09 (0.07–0.12) 92.45, < 0.001
Africa 9 0.20 (0.14–0.26) 97.93, < 0.001
North America 16 0.12 (0.08–0.18) 96.96, < 0.001
Oceania 2 0.19 (0.19–0.20) NA
Gender Male 19 0.08 (0.06–0.11) 90.64, < 0.001 P = 0.63
Female 19 0.08 (0.06–0.10) 87.95, < 0.001
Age (month) 0–6 18 0.08 (0.05–0.12) 93.26, < 0.001 P = 0.56
7–12 17 0.09 (0.06–0.13) 95.36, < 0.001
13–24 19 0.14 (0.09–0.20) 95.31, < 0.001
25–36 12 0.11 (0.04–0.19) 90.97, < 0.001
37–48 8 0.10 (0.02–0.22) 86.23, < 0.001
49–60 8 0.06 (0.00-0.16) 80.80, < 0.001
Age (year) 0–5 38 0.11 (0.08–0.13) 98.49, < 0.001 P < 0.001
6–18 23 0.04 (0.02–0.05) 83.87, < 0.001
Patient type Outpatients 27 0.07 (0.05–0.08) 95.88, < 0.001 P = 0.09
Inpatients 62 0.09 (0.07–0.10) 96.95, < 0.001
Species A 7 0.05 (0.01–0.11) 71.62, < 0.001 P < 0.001
B 6 0.05 (0.01–0.11) 80.03, < 0.001
C 8 0.29 (0.16–0.44) 88.67, < 0.001
D 5 0.09 (0.02–0.19) 88.08, < 0.001
E 2 0.05 (0.01–0.12) NA
F 7 0.57 (0.41–0.72) 89.01, < 0.001
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According to our subgroup analysis, the highest prevalence of HAdV infection was seen in pediatric gastroenteritis patients from Gabon (42%, 95% CI: 16-70%), followed by Iraq (34%, 95% CI: 30-37%), Ethiopia (31%, 95% CI: 27-35%), and Rwanda (30%, 95%CI: 28-33%). Figure 2 depicts the global distribution of HAdV infection among children with gastroenteritis.

Fig. 2.

Fig. 2

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The global map presents the geographical variations in the prevalence of HAdV infection among pediatric patients with gastroenteritis in a period of 11 years (2003–2023)

With respect to HAdV detection methods, Nested PCR, Multiplex PCR, Real-time PCR, Conventional PCR, and Multiplex Real-time PCR methods were used. The prevalence of HAdV was 23% (95% CI: 12–37%), 5% (95% CI: 4–6%), 15% (95% CI: 12–19%), 9% (95% CI: 8–11%), and 17% (95% CI: 10–26%), when Nested PCR, Multiplex PCR, Real-time PCR, Conventional PCR, and Multiplex Real-time PCR methods were used, respectively (P < 0.001). Regarding patient setting, the higher prevalence of HAdV was found in inpatients than in outpatients (9%; 95% CI: 7-10% vs. 7%; 95% CI: 5-8%, respectively); however, the difference was not statistically significant (P = 0.09) (Table 2).

A time trend analysis was conducted to assess variations in the prevalence of HAdV infection over time throughout the world. According to this analysis, the prevalence of HAdV was the highest (32%; 95% CI: 26-37%) between the years of 1996 and 2000. Since 2001 until 2010, the number of HAdV-positive cases among pediatric patients with gastroenteritis was dramatically decreased, so that the prevalence was 8% (95% CI: 4-12%) between the years of 2001 and 2005, and 8% (95% CI: 6-9%) between the years of 2006 and 2010. However, the prevalence of HAdV infection was remarkably increased after the year 2010, reaching a peak of 13% (95% CI: 6-21%) during the years of 2021 and 2022 (P < 0.001) (Table 2).

Regarding the continent, Africa showed a higher prevalence of HAdV in pediatric patients with gastroenteritis (20%, 95% CI: 14–26%) compared to Oceania (19%, 95% CI: 19–20%), the South America (16%, 95% CI: 10–22%), the North America (12%, 95% CI: 8–18%), Europe (9%, 95% CI: 7–12%), and the Asia (7%, 95% CI: 6–8%) (P < 0.001) (Table 2).

Distribution of species and types of HAdVs

Our results showed that the majority of HAdVs circulating in pediatric patients with gastroenteritis belonged to species F (57%; 95% CI: 41-72%) and species C (29%; 95% CI: 16-44%) (P < 0.001). Overall, twenty-eight types of HAdVs were detected among pediatric patients with gastroenteritis across studies. The most prevalent HAdVs observed in children with gastroenteritis were types 40/41 (59%, 95% CI: 49–68%), 38 (25%, 95% CI: 0–79%), and 2 (12%, 95% CI: 7–17%). Figure 3 shows more details on the frequency of HAdV types in children with gastroenteritis. Types 6 (20%; 95% CI: 12-28%) and 37 (5%; 95% CI: 1-14%) in Africa, types 1 (15%; 95% CI: 0-42%), 2 (29%; 95% CI: 17-43%) and 5 (12%; 95% CI: 3-28%) in Europe, types 3 (13%; 95% CI: 3-18%), 4 (1%; 95% CI: 0-2%), and 18 (4%; 95% CI: 0-10%) in Asia, and types 7 (8%; 95% CI: 2-20%), 12 (17%; 95% CI: 8-30%), 40/41 (66%; 95% CI: 17-100%) in South America were the most prevalent types in each one of the mentioned geographical areas. Africa and South America had equally the highest percentage of type 31 (Africa:12%; 95% CI: 0-33%; South America: 12%; 95% CI: 6-19% ) Analysis of other types in different continents was not possible due to lack or low number of reports.

Fig. 3.

Fig. 3

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Distribution of HAdV types in children with gastroenteritis

Prevalence of HAdV infection before and after coronavirus disease 2019 (COVID-19)

Our analysis indicated that the prevalence of HAdV among children with gastroenteritis in studies with the sampling time in 2019 and earlier was (10%, 95% CI: 9–11%) while the prevalence in studies with sampling time from 2020 and later was (13%, 95% CI: 6–21%), showing a statistically significant difference (P < 0.001).

Association of HAdV infection with gastroenteritis among children

The second analysis used data from case-control studies to look into the relationship between HAdV infection and the risk of gastroenteritis in children. There were 10,482 gastroenteritis patients and 7618 controls in 21 case-control studies. The results showed that the overall pooled odds ratio (OR) of the association of HAdV infection (detected by universal + species F primers) and gastroenteritis was 2.29 (95% CI: 1.52–3.44; I2 = 89.6%) (Fig. 4). The association was much stronger between HAdV species F (detected by species F primers) and gastroenteritis (4.0; 95% CI: 1.68–9.53; I2 = 91.1%) than between all types of HAdV (detected by universal primers) and gastroenteritis (1.75; 95% CI: 1.10–2.79; I2 = 88.4%).

Fig. 4.

Fig. 4

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Forest plot of the association between HAdV infection and gastroenteritis risk in pediatric patients according to the random effect model in case case-control studies using universal and F primers for the detection of HAdV

Based on the funnel plot (Fig. 5) there was no evidence of publication bias in the meta-analysis, which was statistically supported by Begg’s test (p = 0.55) and Egger’s test (p = 0.82).

Fig. 5.

Fig. 5

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Funnel plot for assessment of publication bias

Sensitivity analysis

In a sensitivity analysis by successively removing a particular study at a time to assess the influence of every single study on pooled results, a significant positive association [range of summary ORs 2.14–2.43] between HAdV infection and gastroenteritis among children was observed consistently and did not alter the pooled results, which indicated that the meta-analysis model is robust.

Discussion

Acute gastroenteritis is still a prominent global health threat for children, especially in developing countries. In recent years, the improvements in sanitation have led to a decrease in the prevalence of bacterial and parasitical agents in the development of acute gastroenteritis, making viruses the main causative agent of the disease. While individuals of all ages can be infected by HAdVs, children are the main targets of these viruses. To the best of our knowledge, no systematic review and meta-analysis has been performed on the prevalence of HAdVs and pediatric patients with gastroenteritis. Our results showed a high (10%) prevalence of HAdVs in children with gastroenteritis, which highlights the role of HAdVs as a main cause of gastroenteritis among children worldwide. While rotavirus was known as the main cause of pediatric gastroenteritis, the introduction of rotavirus vaccine is changing the pattern [174, 175]. We exhibited a higher prevalence of HAdVs infection in studies published after 2010, which show the increasing trend of HAdVs in the pathogenesis of pediatric gastroenteritis. Furthermore, the analysis of case-control studies indicated an association (OR: 2.28, 95% CI; 1.51–3.44) between HAdV infection and gastroenteritis in children. Therefore, in addition to respiratory infections [176], HAdVs are important pathogens in gastroenteritis among children.

Among the different regions, the highest prevalence was observed in Africa. Low micronutrition (such as vitamins and trace elements) intake as a result of malnutrition is a key factor that abates the ability of both innate and adaptive immune systems to fight pathogens [177]. Also, poor sanitation and hygiene can be a key contributor that facilitates the infection of the gastrointestinal tract by enteric viruses [178]. Other continents with high prevalence were South America and Oceania. Therefore, our results delineate an epidemiologic pattern with higher prevalence in the southern hemisphere. This can be due to malnutrition and lack of proper hygiene, which make children prone to infectious gastroenteritis by negatively affecting the immune system and exposing children to viral agents [174]. Interestingly, there was a significantly higher prevalence of HAdV in pediatric gastroenteritis cases after the initiation of the COVID-19 pandemic. It might be due to the fact that despite the effects of social distancing and mask mandate on respiratory infections, their effects on preventing viral gastroenteritis were limited and in some regions, schools were less focused on preventing gastroenteritis and therefore, school authorities could not efficiently report gastroenteritis cases, which enables the viruses to be transmitted to other children [179]. Moreover, the rise of malnutrition due to financial restrictions and lack of access to school meals for children [180] is another factor, which makes children more vulnerable to viral infection by weakening the immune system [181].

Our results did not indicate a significant difference (P value = 0.06) between male and female patients. This suggests that the occurrence of HAdVs-related gastroenteritis does not exhibit a gender-based pattern among children. After puberty, different compartments of the immune system are affected by sex hormones. For example, androgens including dihydrotestosterone (DHT) and testosterone can suppress immune cell activities in post-pubertal individuals [182]. However, the impacts of sex hormones are not significant in this study due to the age of the included patients. Studies on various viral infections in children resulted in different results and therefore, a specific sex is not prone to viral infections [183].

Exploring the age-specific prevalence of HAdVs in pediatric gastroenteritis showed intriguing patterns in the distribution of infections across different age groups. Notably, the prevalence of HAdVs was significantly higher (P < 0.001) in children younger than 5 years old, which shows the higher susceptibility of this age group. This difference aligns with the well-established notion that young children are more susceptible to viral infections. This vulnerability is primarily due to the immaturity of their immune systems, which does not provide robust protection against viral pathogens [184]. Additionally, younger children often have limited pre-existing immunity and may lack previous exposure to HAdVs, which makes them more prone to infection [185]. The increased possibility of close contact in daycare settings, preschools, and households may further contribute to a higher risk of transmission in this age group. As children advance to later childhood, their immune systems become more mature [184] and exposure in early life fosters a natural immunity to pathogens [174, 184]. Behavioral changes such as improved hygiene practices may also help the reduction of the risk of diarrhea [186]. These findings highlight the importance of monitoring HAdV transmission and infection in childcare and healthcare settings to avoid future outbreaks.

More than half of typed HAdVs in our study belonged to species F, which consisted of types 40/41 that are known for their role in gastroenteritis [11]. In addition, no significant difference (P = 0.06) was observed between universal primers and those that were designed to only detect species F, which shows the remarkable prevalence of this species in HAdVs-related gastroenteritis cases. Interestingly, we observed that species C, which is known to cause respiratory symptoms [11], is the second most prevalent species in pediatric gastroenteritis cases. This underscores the clinical importance of species C as a causative agent of respiratory and gastrointestinal infections among children. These data are good indicators of the most prevalent species and can be used to design effective vaccines.

In the context of clinical settings, the pooled prevalence for inpatients was found to be slightly higher than the prevalence among outpatients. While this difference did not reach statistical significance (P = 0.09), the trend suggests a potential association between HAdV infections and increased disease severity necessitating hospitalization. Noteworthy, the lack of statistical significance may stem from various factors, including heterogeneity in study populations, variations in healthcare practices, and potential underreporting in outpatient settings. Further research into the specific factors contributing to the observed prevalence differences between inpatients and outpatients can provide valuable insights into the clinical implications of HAdVs-associated gastroenteritis.

This systematic review and meta-analysis faced some limitations. There were no studies from some countries in various geographic regions such as Africa and Europe. We recommend researchers to conduct epidemiologic studies in those countries with no previous reports to gain a comprehensive insight into the HAdV epidemiology in pediatric gastroenteritis. Some reports did not mention the characteristics of isolated viruses including species and genotypes. Finally, in the context of systematic review and meta-analysis studies, publication bias and study heterogeneity are inevitable limitations.

Conclusion

This systematic review and meta-analysis highlights HAdVs as significant and increasing causes of pediatric gastroenteritis globally, particularly affecting children under 5 years old. The prevalence is considerably high in Africa, with also remarkable rates in South America and Oceania, which shows a southern hemisphere predominance possibly linked to factors such as malnutrition and poor sanitation. Furthermore, the absence of a gender-based pattern suggests equal susceptibility among male and female pediatric patients. Variations in diagnostic approaches indicate the importance of choosing sensitive tests such as Nested PCR. The dominance of species F adenoviruses, genotypes 40/41, shows potential targets for vaccine development. A higher prevalence among inpatients can be indicative of the potential of HAdVs to cause severe gastrointestinal symptoms. These results suggest future epidemiologic investigations, particularly in underrepresented regions to address existing gaps in HAdVs epidemiology in pediatric gastroenteritis.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Material 1 (13.7KB, docx)

Acknowledgements

Not applicable.

Author contributions

A.T designed and administrated the study. H.S performed all statistical analyses. P.K, M.H.R, and S.G wrote the initial draft. M.H.R and H.S constructed all maps and graphs. A.M, J.S, V.P, and S.S performed intellectual interpretation. P.K, A.T, Z.S, M.H.H, and M.H.R performed search strategy and data extraction. All authors read and approved the final draft.

Funding

This study was not financially supported by any individual, agency, or institution.

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Declarations

Competing interests

The authors declare no competing interests.

Footnotes

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Supplementary Materials

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Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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