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      Epidemiology, Seasonality and Factors Associated with Rotavirus Infection among Children with Moderate-to-Severe Diarrhea in Rural Western Kenya, 2008–2012: The Global Enteric Multicenter Study (GEMS)

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          Abstract

          Objective

          To evaluate factors associated with rotavirus diarrhea and to describe severity of illness among children <5 years old with non-dysenteric, moderate-to-severe diarrhea (MSD) in rural western Kenya.

          Methods

          We analyzed data from children <5 years old with non-dysenteric MSD enrolled as cases in the Global Enteric Multicenter Study (GEMS) in Kenya. A non-dysenteric MSD case was defined as a child with ≥3 loose stools in 24 hrs. and one or more of the following: sunken eyes, skin tenting, intravenous rehydration, or hospitalization, who sought care at a sentinel health center within 7 days of illness onset. Rotavirus antigens in stool samples were detected by ELISA. Demographic and clinical information was collected at enrollment and during a single follow-up home visit at approximately 60 days. We analyzed diarrhea severity using a GEMS 17 point numerical scoring system adapted from the Vesikari score. We used logistic regression to evaluate factors associated with rotavirus infection.

          Results

          From January 31, 2008 to September 30, 2012, among 1,637 (92%) non-dysenteric MSD cases, rotavirus was detected in stools of 245 (15.0%). Rotavirus-positive compared with negative cases were: younger (median age, 8 vs. 13 months; p<0.0001), had more severe illness (median severity score, 9 vs 8; p<0.0001) and had to be hospitalized more frequently (37/245 [15.1%] vs. 134/1,392 [9.6%]), p <0.013). Independent factors associated with rotavirus infection included age 0–11 months old (aOR = 5.29, 95% CI 3.14–8.89) and presenting with vomiting ≥3 times/24hrs (aOR = 2.58, 95% CI [1.91–3.48]). Rotavirus was detected more commonly in warm and dry months than in the cool and rainy months (142/691 [20%] vs 70/673 [10%]) p<0.0001).

          Conclusions

          Diarrhea caused by rotavirus is associated with severe symptoms leading to hospitalization. Consistent with other settings, infants had the greatest burden of disease.

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          Most cited references34

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          Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis.

          Guillermo Ruiz-Palacios, Irene Pérez-Schael, F Velázquez … (2006)
          The safety and efficacy of an attenuated G1P[8] human rotavirus (HRV) vaccine were tested in a randomized, double-blind, phase 3 trial. We studied 63,225 healthy infants from 11 Latin American countries and Finland who received two oral doses of either the HRV vaccine (31,673 infants) or placebo (31,552 infants) at approximately two months and four months of age. Severe gastroenteritis episodes were identified by active surveillance. The severity of disease was graded with the use of the 20-point Vesikari scale. Vaccine efficacy was evaluated in a subgroup of 20,169 infants (10,159 vaccinees and 10,010 placebo recipients). The efficacy of the vaccine against severe rotavirus gastroenteritis and against rotavirus-associated hospitalization was 85 percent (P<0.001 for the comparison with placebo) and reached 100 percent against more severe rotavirus gastroenteritis. Hospitalization for diarrhea of any cause was reduced by 42 percent (95 percent confidence interval, 29 to 53 percent; P<0.001). During the 31-day window after each dose, six vaccine recipients and seven placebo recipients had definite intussusception (difference in risk, -0.32 per 10,000 infants; 95 percent confidence interval, -2.91 to 2.18; P=0.78). Two oral doses of the live attenuated G1P[8] HRV vaccine were highly efficacious in protecting infants against severe rotavirus gastroenteritis, significantly reduced the rate of severe gastroenteritis from any cause, and were not associated with an increased risk of intussusception. (ClinicalTrials.gov numbers, NCT00139347 and NCT00263666.) Copyright 2006 Massachusetts Medical Society.
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            Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine.

            Timo Vesikari, David Matson, Penelope H Dennehy … (2006)
            Rotavirus is a leading cause of childhood gastroenteritis and death worldwide. We studied healthy infants approximately 6 to 12 weeks old who were randomly assigned to receive three oral doses of live pentavalent human-bovine (WC3 strain) reassortant rotavirus vaccine containing human serotypes G1, G2, G3, G4, and P[8] or placebo at 4-to-10-week intervals in a blinded fashion. Active surveillance was used to identify subjects with serious adverse and other events. The 34,035 infants in the vaccine group and 34,003 in the placebo group were monitored for serious adverse events. Intussusception occurred in 12 vaccine recipients and 15 placebo recipients within one year after the first dose including six vaccine recipients and five placebo recipients within 42 days after any dose (relative risk, 1.6; 95 percent confidence interval, 0.4 to 6.4). The vaccine reduced hospitalizations and emergency department visits related to G1-G4 rotavirus gastroenteritis occurring 14 or more days after the third dose by 94.5 percent (95 percent confidence interval, 91.2 to 96.6 percent). In a nested substudy, efficacy against any G1-G4 rotavirus gastroenteritis through the first full rotavirus season after vaccination was 74.0 percent (95 percent confidence interval, 66.8 to 79.9 percent); efficacy against severe gastroenteritis was 98.0 percent (95 percent confidence interval, 88.3 to 100 percent). The vaccine reduced clinic visits for G1-G4 rotavirus gastroenteritis by 86.0 percent (95 percent confidence interval, 73.9 to 92.5 percent). This vaccine was efficacious in preventing rotavirus gastroenteritis, decreasing severe disease and health care contacts. The risk of intussusception was similar in vaccine and placebo recipients. (ClinicalTrials.gov number, NCT00090233.) Copyright 2006 Massachusetts Medical Society.
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              2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis.

              Jacqueline E. Tate, Anthony Burton, Cynthia Boschi-Pinto … (2012)
              WHO recommends routine use of rotavirus vaccines in all countries, particularly in those with high mortality attributable to diarrhoeal diseases. To establish the burden of life-threatening rotavirus disease before the introduction of a rotavirus vaccine, we aimed to update the estimated number of deaths worldwide in children younger than 5 years due to diarrhoea attributable to rotavirus infection. We used PubMed to identify studies of at least 100 children younger than 5 years who had been admitted to hospital with diarrhoea. Additionally, we required the studies to have a data collection midpoint of the year 2000 or later, to be done in full-year increments, and to assesses diarrhoea attributable to rotavirus with EIAs or polyacrylamide gel electrophoresis. We also included data from countries that participated in the WHO-coordinated Global Rotavirus Surveillance Network (consisting of participating member states during 2009) and that met study criteria. For countries that have introduced a rotavirus vaccine into their national immunisation programmes, we excluded data subsequent to the introduction. We classified studies into one of five groups on the basis of region and the level of child mortality in the country in which the study was done. For each group, to obtain estimates of rotavirus-associated mortality, we multiplied the random-effect mean rotavirus detection rate by the 2008 diarrhoea-related mortality figures for countries in that group. We derived the worldwide mortality estimate by summing our regional estimates. Worldwide in 2008, diarrhoea attributable to rotavirus infection resulted in 453,000 deaths (95% CI 420,000-494,000) in children younger than 5 years-37% of deaths attributable to diarrhoea and 5% of all deaths in children younger than 5 years. Five countries accounted for more than half of all deaths attributable to rotavirus infection: Democratic Republic of the Congo, Ethiopia, India, Nigeria, and Pakistan; India alone accounted for 22% of deaths (98,621 deaths). Introduction of effective and available rotavirus vaccines could substantially affect worldwide deaths attributable to diarrhoea. Our new estimates can be used to advocate for rotavirus vaccine introduction and to monitor the effect of vaccination on mortality once introduced. Copyright © 2012 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                Donald R. Olson: 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): 5 August 2016
                Publication date Collection: 2016
                Volume: 11
                Issue: 8
                Electronic Location Identifier: e0160060
                Affiliations
                [1 ]Centre for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya
                [2 ]Division of Viral Diseases, US Centers for Disease Control and Prevention, Atlanta, GA, United States of America
                [3 ]Division of Foodborne, Waterborne and Environmental Diseases, US Centers for Disease Control and Prevention, Atlanta, GA, United States of America
                [4 ]US Centers for Disease Control and Prevention, Kisumu, Kenya
                [5 ]Global Disease Detection Division, Kenya Office of the US Centers for Disease Control and Prevention, Nairobi, Kenya
                [6 ]University of Maryland, School of Medicine, Center for Vaccine Development, Baltimore, MD, United States of America
                [7 ]Department of Pediatrics, University of Virginia School of Medicine, Charlottesville, VA, United States of America
                [8 ]CDC India, Delhi, India
                [9 ]University of Tampere School of Health Sciences, Tampere, Finland
                [10 ]Emory Global Health Institute, Emory University, Atlanta Georgia, United States of America
                New York City Department of Health and Mental Hygiene, UNITED STATES
                Author notes

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

                • Conceived and designed the experiments: RO JET CEO JW TA MML EDM KLK THF DN JP. Nataro KFL RFB.

                • Performed the experiments: RO JET CEO JW TA JO JBO CCB MBP FM JP. Nataro KAS AOA PJ.

                • Analyzed the data: RO JET CEO TA JW JP. Nuorti EDM RFB.

                • Contributed reagents/materials/analysis tools: RO JET CEO TA JW FM KAS AOA PJ JBO JO UDP MBP CCB DN THF KLK JP. Nataro SP MML KFL JP. Nuorti EDM RFB.

                • Wrote the paper: RO JET CEO TA JW JP. Nuorti UDP KFL KLK EDM RFB.

                Article
                Publisher ID: PONE-D-16-11431
                DOI: 10.1371/journal.pone.0160060
                PMC ID: 4975461
                PubMed ID: 27494517
                SO-VID: 6b3947f1-f67f-4b7d-9712-df1809669fd7
                License:

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                Date received : 19 March 2016
                Date accepted : 13 July 2016
                Page count
                Figures: 4, Tables: 4, Pages: 17
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000865, Bill and Melinda Gates Foundation;
                Award ID: Grants # 38874 (GEMS) and #OPP10333572 (GEMS1A)
                Award Recipient :
                This study was funded by the Bill and Melinda Gates Foundation, Grants # 38874 (GEMS) and #OPP10333572 (GEMS1A), Myron M. Levine (PI) through the University of Maryland, School of Medicine, Center for Vaccine Development, Baltimore, MD USA. The funder had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
                Subject: Biology and life sciences
                Subject: Organisms
                Subject: Viruses
                Subject: RNA viruses
                Subject: Reoviruses
                Subject: Rotavirus
                Subject: Biology and Life Sciences
                Subject: Microbiology
                Subject: Medical Microbiology
                Subject: Microbial Pathogens
                Subject: Viral Pathogens
                Subject: Reoviruses
                Subject: Rotavirus
                Subject: Medicine and Health Sciences
                Subject: Pathology and Laboratory Medicine
                Subject: Pathogens
                Subject: Microbial Pathogens
                Subject: Viral Pathogens
                Subject: Reoviruses
                Subject: Rotavirus
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Viruses
                Subject: Viral Pathogens
                Subject: Reoviruses
                Subject: Rotavirus
                Subject: Medicine and Health Sciences
                Subject: Infectious Diseases
                Subject: Viral Diseases
                Subject: Rotavirus Infection
                Subject: Medicine and Health Sciences
                Subject: Gastroenterology and Hepatology
                Subject: Diarrhea
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Signs and Symptoms
                Subject: Diarrhea
                Subject: Medicine and Health Sciences
                Subject: Pathology and Laboratory Medicine
                Subject: Signs and Symptoms
                Subject: Diarrhea
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Signs and Symptoms
                Subject: Dehydration (Medicine)
                Subject: Medicine and Health Sciences
                Subject: Pathology and Laboratory Medicine
                Subject: Signs and Symptoms
                Subject: Dehydration (Medicine)
                Subject: People and Places
                Subject: Geographical Locations
                Subject: Africa
                Subject: Kenya
                Subject: Medicine and Health Sciences
                Subject: Women's Health
                Subject: Maternal Health
                Subject: Breast Feeding
                Subject: Medicine and Health Sciences
                Subject: Pediatrics
                Subject: Neonatology
                Subject: Breast Feeding
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Head
                Subject: Eyes
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Head
                Subject: Eyes
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Ocular System
                Subject: Eyes
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Ocular System
                Subject: Eyes
                Subject: Biology and Life Sciences
                Subject: Physiology
                Subject: Physiological Processes
                Subject: Vomiting
                Subject: Medicine and Health Sciences
                Subject: Physiology
                Subject: Physiological Processes
                Subject: Vomiting
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Signs and Symptoms
                Subject: Vomiting
                Subject: Medicine and Health Sciences
                Subject: Pathology and Laboratory Medicine
                Subject: Signs and Symptoms
                Subject: Vomiting
                Custom metadata
                Data Availability This data was collected confidentially from patients after providing informed voluntary consent that their information would be protected and would not be shared by the study Investigators and the Institutional Review Board (IRB). Please send requests to: Gates Enterics Project, Center for Vaccine Development, University of Maryland, Baltimore, 685 W. Baltimore St., Room 480, Baltimore, MD, 21201, USA; Phone: (410) 706-5328, Fax: (410) 706-6205.

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