Enteric and non-enteric adenoviruses associated with acute gastroenteritis in pediatric patients in Thailand, 2011 to 2017

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Abstract

Human adenovirus (HAdV) is known to be a common cause of diarrhea in children worldwide. Infection with adenovirus is responsible for 2–10% of diarrheic cases. To increase a better understanding of the prevalence and epidemiology of HAdV infection, a large scale and long-term study was needed. We implemented a multi-year molecular detection and characterization study of HAdV in association with acute gastroenteritis in Chiang Mai, Thailand from 2011 to 2017. Out of 2,312 patients, HAdV was detected in 165 cases (7.2%). The positive rate for HAdV infection was highest in children of 1 and 2 years of age compared to other age groups. HAdV subgroup C (40.6%) was the most prevalent, followed by subgroups F (28.5%), B (20.6%), A and D (4.8% each), and E (0.6%). Of these, HAdV-F41 (22.4%), HAdV-C2 (18.2%), HAdV-B3 (15.2%), and HAdV-C1 (13.3%) were the most common genotypes detected. HAdV infection occurred throughout the year with a higher detection rate between May and July. In conclusion, our study demonstrated the infection rate, seasonal distribution and genotype diversity of HAdV infection in children with diarrhea in Chiang Mai, Thailand over a period of 7 year. Not only enteric adenovirus (F40 and F41) but also non-enteric adenovirus (B3, C1, C2) may play an important role in gastroenteritis in this area. The information will be beneficial for the prevention and control of HAdV outbreaks in the future.

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Adenoviruses in the immunocompromised host.

J Hierholzer (1992)

Adenoviruses are among the many pathogens and opportunistic agents that cause serious infection in the congenitally immunocompromised, in patients undergoing immunosuppressive treatment for organ and tissue transplants and for cancers, and in human immunodeficiency virus-infected patients. Adenovirus infections in these patients tend to become disseminated and severe, and the serotypes involved are clustered according to the age of the patient and the nature of the immunosuppression. Over 300 adenovirus infections in immunocompromised patients, with an overall case fatality rate of 48%, are reviewed in this paper. Children with severe combined immunodeficiency syndrome and other primary immunodeficiencies are exposed to the serotypes of subgroups B and C that commonly infect young children, and thus their infections are due to types 1 to 7 and 31 of subgenus A. Children with bone marrow and liver transplants often have lung and liver adenovirus infections that are due to an expanded set of subgenus A, B, C, and E serotypes. Adults with kidney transplants have viruses of subgenus B, mostly types 11, 34, and 35, which cause cystitis. This review indicates that 11% of transplant recipients become infected with adenoviruses, with case fatality rates from 60% for bone marrow transplant patients to 18% for renal transplant patients. Patients with AIDS become infected with a diversity of serotypes of all subgenera because their adult age and life-style expose them to many adenoviruses, possibly resulting in antigenically intermediate strains that are not found elsewhere. Interestingly, isolates from the urine of AIDS patients are generally of subgenus B and comprise types 11, 21, 34, 35, and intermediate strains of these types, whereas isolates from stool are of subgenus D and comprise many rare, new, and intermediate strains that are untypeable for practical purposes. It has been estimated that adenoviruses cause active infection in 12% of AIDS patients and that 45% of these infections terminate in death within 2 months. In all immunocompromised patients, generalized illness involving the central nervous system, respiratory system, hepatitis, and gastroenteritis usually have a fulminant course and result in death. Treatments for adenovirus infections are of little proven value, although certain purine and pyrimidine analogs have shown beneficial effects in vitro and may be promising drugs.

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Human Adenovirus Associated with Severe Respiratory Infection, Oregon, USA, 2013–2014

Magdalena Scott, Christina Chommanard, Xiaoyan Lu … (2016)

HAdV-B7 might be reemerging in the United States.

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Importance of enteric adenoviruses 40 and 41 in acute gastroenteritis in infants and young children.

I Uhnoo, G Wadell, L. Svensson … (1984)

In a prospective 1-year study of acute infantile gastroenteritis, adenoviruses were detected in the stools or by seroconversions, or both, in 56 of 416 (13.5%) ill children. By use of DNA restriction enzyme analysis, enzyme immunoassay, and culture techniques, 33 of 56 (59%) adenovirus specimens were identified as enteric adenoviruses 40 and 41 (Ad40 and Ad41). They were found as the sole recognizable cause of diarrhea in 30 of 416 (7.2%) ill children and in 0 of 200 controls. Three additional ill children had enteric adenoviruses as a part of a dual infection. Evidence for established adenoviruses (Ad1 through Ad39) in gastroenteritis was found in 15 of 416 (3.6%) ill children but also in 3 of 200 (1.5%) controls. Eight adenovirus specimens remained untyped. Seroconversions were demonstrated in 17 of 18 (94%) paired serum samples from patients shedding enteric adenoviruses. The predominant symptom of infections with enteric adenoviruses was diarrhea, with a mean duration of 8.6 days (Ad40) and 12.2 days (Ad41). One-third of the children with Ad41 infections had prolonged symptoms (greater than or equal to 14 days). The frequency of respiratory symptoms was low (21%). The established adenoviruses presented a different clinical picture, characterized by diarrhea of shorter duration, higher fever, and significantly increased occurrence of respiratory symptoms (79%). In conclusion, enteric adenoviruses appear to be an important cause of acute infantile gastroenteritis, second only to rotaviruses in this study.

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Author and article information

Contributors

Kattareeya Kumthip: Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: Writing – original draft

Pattara Khamrin: Role: ConceptualizationRole: Data curationRole: Investigation

Hiroshi Ushijima: Role: Methodology

Niwat Maneekarn:

ORCID: http://orcid.org/0000-0001-5665-3332

Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing – review & editing

Wenyu Lin: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, CA USA )

ISSN (Electronic): 1932-6203

Publication date (Electronic): 1 August 2019

Publication date Collection: 2019

Volume: 14

Issue: 8

Electronic Location Identifier: e0220263

Affiliations

[1 ] Department of Microbiology, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand

[2 ] Center of Excellence in Emerging and Re-emerging Diarrheal Viruses, Chiang Mai University, Chiang Mai, Thailand

[3 ] Department of Developmental Medical Sciences, School of International Health, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan

[4 ] Division of Microbiology, Department of Pathology and Microbiology, Nihon University School of Medicine, Tokyo, Japan

Harvard Medical School, UNITED STATES

Author notes

Competing Interests: The authors have declared that no competing interests exist.

* E-mail: niwat.m@ 123456cmu.ac.th

Author information

Niwat Maneekarn http://orcid.org/0000-0001-5665-3332

Article

Publisher ID: PONE-D-19-10354

DOI: 10.1371/journal.pone.0220263

PMC ID: 6675392

PubMed ID: 31369615

SO-VID: 470c8eba-2d0f-4ef1-a5b7-c57afe7d9828

License:

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 11 April 2019

Date accepted : 11 July 2019

Page count

Figures: 5, Tables: 2, Pages: 12

Funding

Funded by: funder-id http://dx.doi.org/10.13039/501100004396, Thailand Research Fund;

Award ID: KKMRG6180145

Award Recipient : Kattareeya Kumthip

This work was supported by the grant from the Thailand Research Fund (KKMRG6180145). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Data Availability The nucleotide sequences of human adenovirus described in this study are available in the GenBank database under the accession numbers MK674616 to MK674780.

Enteric and non-enteric adenoviruses associated with acute gastroenteritis in pediatric patients in Thailand, 2011 to 2017

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Most cited references 20

Adenoviruses in the immunocompromised host.

Human Adenovirus Associated with Severe Respiratory Infection, Oregon, USA, 2013–2014

Importance of enteric adenoviruses 40 and 41 in acute gastroenteritis in infants and young children.

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