Global Research Trends on Major Pathogenic Enteric Viruses (1990–2024): A Bibliometric Analysis of Epidemiology, Transmission, and Public Health Impact
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Design (PICOS Criteria)
- Population (P): The scientific literature on the major pathogenic enteric viruses defined in this study was published between 1 January 1990, and 31 December 2024. We included publications addressing enteric viruses of significant public health importance, including rotavirus (family Sedoreoviridae), norovirus, sapovirus, and astrovirus (Caliciviridae, Astroviridae), as well as adenovirus (Adenoviridae). Within the Picornaviridae family, we considered enteroviruses (non-polio enteroviruses such as coxsackievirus and echovirus), as well as human parechoviruses (genus Parechovirus) and Aichi virus (genus Kobuvirus), both of which are increasingly recognized as enteric pathogens. For clarity, parechoviruses and Aichi virus were treated as distinct categories, not as subgroups of enteroviruses.
- Intervention (I): Bibliometric studies (i.e., analyses of publication trends, authorship, citations, keyword co-occurrence).
- Comparator (C): Not applicable.
- Outcomes (O): Research trends, including publication volume, geographic distribution, collaboration networks, thematic evolution, and methodological shifts in diagnostics and prevention.
- Study designs (S): Original research articles and review papers.
2.2. Information Sources and Search Strategy
Search Details
- Keywords and MeSH:
- o
- General: “enteric viruses”, “gastroenteritis”, “diarrhea”, “vomiting”, “dehydration”, “fecal-oral transmission”, “public health”, “epidemiology”, “transmission”, “diagnosis”, “prevention”, “vaccination”, “sanitation”, “hygiene”.
- o
- Specific: “rotavirus”, “norovirus”, “enteric adenovirus”, “astrovirus”, “sapovirus”, “viral gastroenteritis”, “waterborne diseases”, “foodborne diseases”, “outbreaks”, “clinical manifestations”, “molecular diagnostics”, “antigen-based tests”, “electron microscopy”, “oral rehydration therapy”, “vaccine efficacy”, “global burden”, “low-income countries”, “high-income countries”.
- o
- MeSH Terms: “Enterovirus Infections”[Mesh], “Gastroenteritis”[Mesh], “Diarrhea”[Mesh], “Vomiting”[Mesh], “Dehydration”[Mesh], “Fecal-Oral Route”[Mesh], “Public Health”[Mesh], “Epidemiology”[Mesh], “Disease Transmission, Infectious”[Mesh], “Diagnosis”[Mesh], “Prevention & Control”[Mesh], “Vaccination”[Mesh], “Sanitation”[Mesh], “Hygiene”[Mesh], “Rotavirus”[Mesh], “Norovirus”[Mesh], “Adenoviruses, Human”[Mesh], “Astroviridae”[Mesh], “Sapovirus”[Mesh].
- Boolean Example: (“enteric virus*” OR “gastroenter*” OR diarrh*) AND (“fecal-oral transmiss*” OR “public health” OR epidemiolog*).
- Wildcards Examples: “enteric virus*”, “enterovir*”, “gastroenter*”, “diarrh*”, “vomit*”, “dehydrat*”, “fecal-oral transmiss*”, “public health*”, “epidemiol*”, “transmiss*”, “diagnos*”, “prevent*”, “vaccinat*”, “sanitat*”, “hygien*”.
- Timeframe: 1990–2024 (search performed 1 February 2025).
- Search Queries:
- o
- Scopus Query:
TITLE-ABS-KEY( ( rotavirus OR norovirus OR “enteric adenovirus” OR “adenovirus F40” OR “adenovirus F41” OR astrovirus OR sapovirus OR enterovir* OR coxsackievirus* OR echovirus* OR “Aichi virus” OR kobuvirus OR parechovirus* OR picornaviridae ) AND ( “viral gastroenter*” OR gastroenteritis OR diarrh* OR vomit* OR dehydrat* OR “fecal-oral” OR waterborne OR foodborne ) AND ( epidemiol* OR transmiss* OR diagnos* OR “molecular surveillance” OR “genomic sequenc*” OR prevent* OR vaccinat* OR “antiviral therap*” OR WASH OR sanitati* OR “climate change” ) ) AND ( LIMIT-TO(DOCTYPE, “ar”) OR LIMIT-TO(DOCTYPE, “re”) ) AND ( EXCLUDE(SUBJAREA, “VETE”) OR EXCLUDE(SUBJAREA, “AGRI”) ) AND (PUBYEAR > 1989 AND PUBYEAR < 2025) AND ( LIMIT-TO(LANGUAGE, “English”) OR LIMIT-TO(LANGUAGE, “French”) ) - o
- PubMed Query:
( ( rotavirus[Title/Abstract] OR rotavirus[MeSH Terms] OR norovirus[Title/Abstract] OR norovirus[MeSH Terms] OR “enteric adenovirus”[Title/Abstract] OR “adenovirus F40”[Title/Abstract] OR “adenovirus F41”[Title/Abstract] OR “Adenoviridae”[MeSH Terms] OR astrovirus[Title/Abstract] OR “Astroviridae”[MeSH Terms] OR sapovirus[Title/Abstract] OR enterovirus[Title/Abstract] OR “Enterovirus Infections”[MeSH Terms] OR coxsackievirus[Title/Abstract] OR echovirus[Title/Abstract] OR “Aichi virus”[Title/Abstract] OR kobuvirus[Title/Abstract] OR parechovirus[Title/Abstract] OR “Parechovirus”[MeSH Terms] OR “human parechovirus”[Title/Abstract] OR picornaviridae[Title/Abstract] ) AND ( “gastroenteritis”[Title/Abstract] OR “Gastroenteritis”[MeSH Terms] OR diarrh*[Title/Abstract] OR “Diarrhea”[MeSH Terms] OR vomit*[Title/Abstract] OR “Dehydration”[MeSH Terms] OR “fecal-oral route”[MeSH Terms] OR “waterborne diseases”[MeSH Terms] OR “foodborne diseases”[MeSH Terms] ) AND ( epidemiology[MeSH Terms] OR “disease transmission”[MeSH Terms] OR diagnosis[MeSH Terms] OR “molecular surveillance”[Title/Abstract] OR “genomic sequencing”[Title/Abstract] OR prevention[MeSH Terms] OR vaccination[MeSH Terms] OR “antiviral agents”[MeSH Terms] OR sanitation[MeSH Terms] OR “climate change”[MeSH Terms] ) ) AND (english[Language] OR french[Language]) AND (“1990/01/01”[Date - Publication]: “2024/12/31”[Date - Publication]) AND (Humans[Mesh]).
2.3. Eligibility Criteria
- Inclusion Criteria: Research articles and reviews in English and French on the epidemiology, transmission, diagnosis, prevention, and public health of enteric viruses. We acknowledge that this language restriction may underrepresent research published in languages other than English, such as Spanish, Portuguese, Chinese, or in non-indexed regional journals, which is a potential source of selection bias.
- Exclusion Criteria: Studies should directly relate to epidemiology or public health and focus on human enteric viruses. Exclude animal-only research, non-English/French papers, and non-peer-reviewed sources such as conference proceedings, non-peer-reviewed book chapters, and editorials.
- Focus Specification: To maintain a focus on gastroenteritis, the analysis of enterovirus-related publications was restricted to those reporting on gastrointestinal manifestations or fecal viral excretion.
- Age: No age restrictions were applied; pediatric and adult studies were included.
- Co-infections: Studies reporting coinfections (viral, bacterial, and/or parasitic agents) were included only if virus-specific data could be unequivocally extracted (e.g., if results were stratified by pathogen or if viral outcomes were reported separately). If viral data could not be separated from non-viral outcomes, the article was excluded from virus-specific thematic analyses but documented in the selection journal.
2.4. Study Selection Process
2.5. Data Extraction and Management
2.5.1. Export and Import
- PubMed: Retrieved PMID, title, abstract, author names, affiliations, publication date, keywords, MeSH terms, and citation metadata (where available).
- Scopus: Retrieved EID/DOI, title, abstract, author names, affiliations, publication date, keywords, citation counts, journal name, and other bibliometric fields.
- All exports were saved as CSV and imported into RStudio (v4.3.3) using bibliometrix, readr, or data.table.
2.5.2. Deduplication and Cleaning
- Priority matching by DOI, when available; otherwise, exact title, first author, and year. Via distinct() and dplyr (v1.1.0) to remove precise duplicates.
- Standardized author names (“LastName Initials”), harmonized institution and country names (ISO standards).
- Institutions: Cleaned common variants/spelling differences (e.g., “Univ. of X” vs. “University of X”).
- Flagged records missing key metadata fields (e.g., no publication year, no affiliation data). A total of 108 records were excluded at this stage due to missing affiliation data, as noted in Section 2.4.
- All preprocessing steps, counts at each stage, and any manual corrections were logged in R scripts for reproducibility.
- During the pre-processing steps, 709 records that could not be retrieved during Biblioshiny export (as noted in Section 2.5) were logged and excluded. Then, 108 records (1.2% of the evaluated records) were excluded due to missing key metadata (specifically, affiliation data), and zero records were flagged for manual correction of import errors.
2.6. Subset and Thematic Filtering
2.6.1. Regional Subsets
- West Africa (Ghana, Nigeria, Senegal, Côte d’Ivoire, Mali, Burkina Faso, Benin, and Togo). Any record with at least one author affiliation in these countries was included; multi-affiliation papers were counted in each relevant subset but tracked to avoid double-counting when aggregating global metrics (204 records).
- Southern Africa (Botswana, Namibia, South Africa, Zimbabwe, Zambia, Malawi) with the same inclusion logic as above (309 records).
2.6.2. Risk-Factor Keywords
- Terms: “sanitation,” “water,” “population density,” “zoonotic” (and variants via wildcard truncation if relevant, e.g., ‘sanitat*’, ‘zoonot*’). Automated search in title/abstract/keywords flagged 7422 articles; each was manually validated.
2.7. Automated Epidemiological Extraction
- Targets: Incidence, mortality, and morbidity estimates mentioned in titles/abstracts.
- Method: Regex patterns capturing numeric-per-population expressions; ~10% randomly checked and refined iteratively. Results are reported descriptively.
2.8. Bibliometric Analyses
- Productivity trends: Yearly counts; CAGR (compound annual growth rate) with 95% CIs calculated per standard formulas.
- Key contributors:
- o
- Author-, institution-, and country-level metrics: total publications and average citations per document.
- Impact Metrics: H-index, total/average citations by author/institution/country based on the collected dataset snapshot (full counting).
- Journal ranking: By publications count and impact factor (sourced from Journal Citation Reports for the relevant year; details in script).
- Software:
2.9. Contextualization and Sensitivity Analyses
- Sensitivity analysis for rotavirus dominance: To assess whether the observed trends were strongly influenced by rotavirus research, we (i) excluded all publications explicitly mentioning rotavirus and (ii) applied a fractional counting method (where each article mentioning “k” viruses contributes “1/k” to each virus’s count).
- Contextualization of publication growth: to determine if the observed increase in publications in 2021 was specific to our field or part of a broader trend in biomedical publishing, we compared the annual growth of our corpus to the total number of publications indexed in PubMed each year. PubMed was chosen as the global reference because it offers free and exhaustive access to biomedical publications. The data on global PubMed production was obtained via the Entrez API.
3. Results
3.1. Study Selection
3.2. Descriptive Analysis
3.2.1. General Overview
3.2.2. Geographic and Institutional Distribution
3.3. A Research Landscape Dominated by Rotavirus
Comparison with General Biomedical Publication Trends
3.4. Trends in Epidemiology and Methods
3.5. Transmission Dynamics and Risk Factors
3.6. Public Health Impact
4. Discussion
4.1. Rotavirus Predominance: Causes and Implications
4.2. COVID-19 and the 2021 Publication Surge
4.3. Geographic Disparities
4.4. Methodological Trends
4.5. Transmission Dynamics and Risk Factors
4.6. Thematic Focus at the Expense of Antivirals
4.7. Policy Implications
- Expand equitable rotavirus immunization coverage, particularly in low- and middle-income countries (LMICs), through Gavi-supported platforms and reinforcement of cold-chain logistics;
- Scale genomic surveillance infrastructures in underserved regions by funding local laboratories, training scientists, and ensuring access to sequencing tools and data analysis platforms;
- Adopt integrated One Health surveillance in zoonotic hotspots by combining human, animal, and environmental monitoring to improve early detection and outbreak response;
- Invest in sustainable WASH (Water, Sanitation, and Hygiene) systems, recognizing that diagnostics and vaccines are insufficient without foundational public health infrastructure;
- Ensure inclusive knowledge sharing and data equity by strengthening open-access repositories, FAIR data standards, and inclusive platforms for LMIC researchers (e.g., preprints, community peer review);
- Incorporate climate and socio-demographic data into future surveillance models to anticipate outbreak risks in vulnerable populations and improve public health preparedness.
- Address gender and equity barriers in access to prevention, diagnosis, and care, with a focus on context-specific health education and resource allocation;
- Together, these measures provide a roadmap for stakeholders to strengthen surveillance, prevention, and research equity, thereby reducing the global burden of enteric viruses.
5. Conclusions and Limitations
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Family | Virus | Key Epidemiological Features | Transmission Routes | Public Health Impact | Prevention/Treatment | Research Challenges | References |
---|---|---|---|---|---|---|---|
Sedoreoviridae | Rotavirus | Leading cause of severe pediatric diarrhea globally; peak incidence in children <5 years | Fecal–oral, contaminated water/food | High morbidity and mortality in LMICs; seasonal epidemics | Vaccination, WASH interventions, supportive care | Strain diversity, vaccine escape variants, limited surveillance in LMICs | [3] |
Caliciviridae | Norovirus, Sapovirus | Major cause of gastroenteritis across all ages; frequent outbreaks in closed settings | Fecal–oral, contaminated food/water, fomites | High burden in both HICs and LMICs; outbreaks in hospitals, cruise ships, schools | Hygiene, outbreak control measures, vaccine development ongoing | High genetic diversity, short-lived immunity, limited vaccines | [16,17] |
Adenoviridae | Enteric adenovirus (F40/F41) | Causes diarrhea primarily in infants and young children | Fecal–oral | Moderate global burden; associated with sporadic outbreaks | Supportive care, hygiene measures | Limited epidemiological data, few diagnostics in LMICs | [18,19] |
Astroviridae | Astrovirus | Often mild diarrhea in children; some severe cases in immunocompromised | Fecal–oral | Underrecognized; global incidence unclear | Hygiene, supportive care | Limited surveillance, low research attention | [14,20] |
Picornaviridae 1 | Enteroviruses (genus Enterovirus; e.g., coxsackievirus, echovirus). Other enteric picornaviruses include human parechoviruses (HPeV; genus Parechovirus) and Aichi virus (AiV; genus Kobuvirus) | Clinical spectrum ranges from gastroenteritis to occasional systemic/CNS disease; some types associated with severe neonatal disease (e.g., certain HPeV types) | Fecal–oral, waterborne | Significant pediatric morbidity in outbreaks; variable detection across settings | Supportive care; some experimental antivirals | Diagnostic heterogeneity, limited surveillance, taxonomic and nomenclature confusion in older literature | [21,22,23,24] |
Hepeviridae | Hepatitis E virus (HEV) | Enterically transmitted hepatitis; high risk in pregnant women | Fecal–oral, contaminated water | Severe outbreaks in LMICs; high mortality in pregnancy | Vaccination (restricted availability), WASH | Poor surveillance, limited vaccine coverage outside China | [25] |
Hepatoviridae | Hepatitis A virus (HAV) | Self-limiting acute hepatitis; widespread global exposure | Fecal–oral | Moderate burden; epidemics in regions with poor sanitation | Vaccination, WASH | Limited genomic surveillance, outbreak prediction challenges | [26] |
Country | Total Publications | Corresponding Authorships | Leadership Share (%) * |
---|---|---|---|
USA | 2205 | 349 | 15.8 |
China | 932 | 80 | 8.6 |
Japan | 641 | 129 | 20.1 |
India | 438 | 64 | 14.6 |
Brazil | 363 | 45 | 12.4 |
Italy | 335 | 48 | 14.3 |
France | 325 | 70 | 21.5 |
South Korea | 309 | 38 | 12.3 |
Australia | 282 | 69 | 24.5 |
Germany | 223 | 24 | 10.8 |
Country | Articles | Institution | Articles | Journal | Articles |
---|---|---|---|---|---|
USA | 3180 | Centers for Disease Control and Prevention | 902 | Journal of Medical Virology | 432 |
China | 1912 | National Center for Immunization and Respiratory Diseases | 521 | Vaccine | 378 |
Japan | 1034 | University of Liverpool | 362 | Journal of Clinical Microbiology | 246 |
India | 874 | Christian Medical College | 341 | Pediatric Infectious Disease Journal | 214 |
Brazil | 689 | Baylor College of Medicine | 318 | PLOS One | 195 |
Italy | 602 | International Centre for Diarrhoeal Disease Research | 287 | Viruses | 168 |
UK | 511 | Emory University | 263 | Epidemiology and Infection | 151 |
Spain | 498 | University of Virginia | 244 | Archives of Virology | 147 |
France | 472 | Chiang Mai University | 229 | Journal of Infectious Diseases | 139 |
South Korea | 438 | Nihon University School of Medicine | 196 | BMC Infectious Diseases | 133 |
Keyword | 1990–1999 % | 2000–2009 % | 2010–2019 % | 2020–2024 % |
---|---|---|---|---|
Children | 54.0 | 48.5 | 51.7 | 50.8 |
Gastroenteritis | 42.3 | 52.5 | 55.1 | 46.0 |
Diarrhea | 56.9 | 44.7 | 42.0 | 41.1 |
Norovirus | 0.0 | 26.6 | 35.9 | 32.7 |
Genome sequencing | 10.6 | 16.5 | 19.4 | 26.2 |
Gastroenteritis | 42.3 | 52.5 | 55.1 | 46.0 |
Rotavirus vaccines | 18.6 | 17.0 | 19.2 | 16.7 |
Outbreak | 10.8 | 24.3 | 18.0 | 15.6 |
RT-PCR | 4.7 | 15.0 | 13.8 | 10.4 |
Adenovirus | 9.5 | 7.4 | 7.1 | 9.8 |
Astrovirus | 11.1 | 9.5 | 6.7 | 7.8 |
Sapovirus | 0.0 | 3.5 | 4.7 | 6.0 |
Molecular epidemiology | 2.7 | 6.1 | 5.8 | 4.9 |
Wastewater | 0.9 | 1.8 | 1.9 | 2.5 |
Serotyping | 26.6 | 9.9 | 3.6 | 1.8 |
RT-PCR | 4.7 | 15.0 | 13.8 | 10.4 |
Study Type | Number of Studies | Percentage |
---|---|---|
Vaccine | 3311 | 39.8% |
Morbidity | 2045 | 24.6% |
Molecular/Genetic | 1890 | 22.7% |
Incidence/Prevalence | 1042 | 12.5% |
Mortality | 31 | 0.4% |
Other | 1 | 0.0% |
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Alotaibi, M.; Al-Khalaifah, H.; Bouhoudan, A. Global Research Trends on Major Pathogenic Enteric Viruses (1990–2024): A Bibliometric Analysis of Epidemiology, Transmission, and Public Health Impact. Pathogens 2025, 14, 938. https://doi.org/10.3390/pathogens14090938
Alotaibi M, Al-Khalaifah H, Bouhoudan A. Global Research Trends on Major Pathogenic Enteric Viruses (1990–2024): A Bibliometric Analysis of Epidemiology, Transmission, and Public Health Impact. Pathogens. 2025; 14(9):938. https://doi.org/10.3390/pathogens14090938
Chicago/Turabian StyleAlotaibi, Mohammad, Hanan Al-Khalaifah, and Assia Bouhoudan. 2025. "Global Research Trends on Major Pathogenic Enteric Viruses (1990–2024): A Bibliometric Analysis of Epidemiology, Transmission, and Public Health Impact" Pathogens 14, no. 9: 938. https://doi.org/10.3390/pathogens14090938
APA StyleAlotaibi, M., Al-Khalaifah, H., & Bouhoudan, A. (2025). Global Research Trends on Major Pathogenic Enteric Viruses (1990–2024): A Bibliometric Analysis of Epidemiology, Transmission, and Public Health Impact. Pathogens, 14(9), 938. https://doi.org/10.3390/pathogens14090938