Publications by authors named "Umesh D Parashar"

432 Publications

Diversity of rotavirus strains circulating in Haiti before and after introduction of monovalent vaccine.

IJID Reg 2022 Sep 14;4:146-151. Epub 2022 Jul 14.

Division of Viral Diseases, National Center for Immunization and Respiratory Diseases (NCIRD), CDC, Atlanta, Georgia, USA.

Background: Haiti introduced a monovalent human group A rotavirus (RVA) vaccine (Rotarix) into its routine infant immunization program in April 2014. The goal of the surveillance program was to characterize RVA strains circulating in Haiti before and after RVA vaccine introduction.

Methods: Stool samples were collected from children <5 years old presenting with acute gastroenteritis at 16 hospitals in Haiti. RVA antigen enzyme immunoassay (EIA) testing was performed, and G and P genotypes were determined for positive specimens. In this study, genotype data for samples collected from May 2012 through April 2014 (the pre-vaccine introduction era) and May 2014 through July 2019 (post-vaccine introduction era) were analyzed.

Results: A total of 809 specimens were tested by the Centers for Disease Control and Prevention. During the pre-vaccine introduction era (May 2012 through April 2014), G12P[8] was the predominant genotype, detected in 88-94% of specimens. There was a high prevalence of the equine-like G3P[8] genotype among Haitian children with RVA after vaccine introduction.

Conclusions: The predominance of equine-like G3P[8] in three of five RVA seasons post-vaccine introduction suggests possible vaccine-specific selection pressure in Haiti. These temporal variations in RVA genotype predominance will require continued monitoring in Haiti as the vaccination program continues.
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http://dx.doi.org/10.1016/j.ijregi.2022.07.007DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9340491PMC
September 2022

Interim Analysis of Acute Hepatitis of Unknown Etiology in Children Aged <10 Years - United States, October 2021-June 2022.

MMWR Morb Mortal Wkly Rep 2022 Jul 1;71(26):852-858. Epub 2022 Jul 1.

On April 21, 2022, CDC issued a health advisory encouraging U.S. clinicians to report all patients aged <10 years with hepatitis of unknown etiology to public health authorities, after identification of similar cases in both the United States (1) and Europe. A high proportion of initially reported patients had adenovirus detected in whole blood specimens, thus the health advisory encouraged clinicians to consider requesting adenovirus testing, preferentially on whole blood specimens. For patients meeting the criteria in the health advisory (patients under investigation [PUIs]), jurisdictional public health authorities abstracted medical charts and interviewed patient caregivers. As of June 15, 2022, a total of 296 PUIs with hepatitis onset on or after October 1, 2021, were reported from 42 U.S. jurisdictions. The median age of PUIs was 2 years, 2 months. Most PUIs were hospitalized (89.9%); 18 (6.1%) required a liver transplant, and 11 (3.7%) died. Adenovirus was detected in a respiratory, blood, or stool specimen of 100 (44.6%) of 224 patients. Current or past infection with SARS-CoV-2 (the virus that causes COVID-19) was reported in 10 of 98 (10.2%) and 32 of 123 (26.0%) patients, respectively. No common exposures (e.g., travel, food, or toxicants) were identified. This nationwide investigation is ongoing. Further clinical data are needed to understand the cause of hepatitis in these patients and to assess the potential association with adenovirus.
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http://dx.doi.org/10.15585/mmwr.mm7126e1DOI Listing
July 2022

Trends in Acute Hepatitis of Unspecified Etiology and Adenovirus Stool Testing Results in Children - United States, 2017-2022.

MMWR Morb Mortal Wkly Rep 2022 Jun 17;71(24):797-802. Epub 2022 Jun 17.

In November 2021, CDC was notified of a cluster of previously healthy children with hepatitis of unknown etiology evaluated at a single U.S. hospital (1). On April 21, 2022, following an investigation of this cluster and reports of similar cases in Europe (2,3), a health advisory* was issued requesting U.S. providers to report pediatric cases of hepatitis of unknown etiology to public health authorities. In the United States and Europe, many of these patients have also received positive adenovirus test results (1,3). Typed specimens have indicated adenovirus type 41, which typically causes gastroenteritis (1,3). Although adenovirus hepatitis has been reported in immunocompromised persons, adenovirus is not a recognized cause of hepatitis in healthy children (4). Because neither acute hepatitis of unknown etiology nor adenovirus type 41 is reportable in the United States, it is unclear whether either has recently increased above historical levels. Data from four sources were analyzed to assess trends in hepatitis-associated emergency department (ED) visits and hospitalizations, liver transplants, and adenovirus stool testing results among children in the United States. Because of potential changes in health care-seeking behavior during 2020-2021, data from October 2021-March 2022 were compared with a pre-COVID-19 pandemic baseline. These data do not suggest an increase in pediatric hepatitis or adenovirus types 40/41 above baseline levels. Pediatric hepatitis is rare, and the relatively low weekly and monthly counts of associated outcomes limit the ability to interpret small changes in incidence. Ongoing assessment of trends, in addition to enhanced epidemiologic investigations, will help contextualize reported cases of acute hepatitis of unknown etiology in U.S. children.
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http://dx.doi.org/10.15585/mmwr.mm7124e1DOI Listing
June 2022

Major Changes in Spatiotemporal Trends of US Rotavirus Laboratory Detections After Rotavirus Vaccine Introduction-2009-2021.

Pediatr Infect Dis J 2022 Sep 1;41(9):759-763. Epub 2022 Jun 1.

From the Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, GA.

For the 15 years before rotavirus vaccine introduction in 2006, annual rotavirus activity in the United States showed a distinct spatiotemporal pattern, peaking first in the Southwest and last in the Northeast. We modeled spatiotemporal trends in rotavirus laboratory detections from 2009 to 2021. Laboratories reporting to the National Respiratory and Enteric Virus Surveillance System were eligible for inclusion in a given surveillance year (July to June) if ≥1 polymerase chain reaction or enzyme immunoassay rotavirus test per week was reported during ≥26 weeks and totaling ≥100 annual tests. For each laboratory, the season peak was the week with the highest 7-week moving average of the number of rotavirus positive tests during the national season, defined as the period with a 3-week moving average of >10% rotavirus positivity lasting ≥2 consecutive weeks. We input peak week as a continuous variable and the geospatial coordinates of each laboratory into a spherical variogram model for Kriging spatial interpolation. We also created a state-level bivariate choropleth map using tertiles of the 2010-2019 average birth rates and rotavirus vaccine coverage. Following the established biennial trend, the 2010-2011, 2012-2013, 2014-2015, 2016-2017, and 2018-2019 surveillance years had >10% rotavirus positivity for ≥2 weeks and were included in the geospatial analysis. During all 5 seasons included in the geospatial analysis, the earliest peak week occurred in Oklahoma, Arkansas, and the western Gulf coast, a pattern markedly different from prevaccine seasons. These states also had the average lowest rotavirus vaccine coverage and highest birth rate, suggesting that more rapid accumulation of susceptible children drives annual rotavirus season activity. Increasing vaccine coverage remains a key tool in reducing rotavirus burden.
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http://dx.doi.org/10.1097/INF.0000000000003598DOI Listing
September 2022

Understanding Variation in Rotavirus Vaccine Effectiveness Estimates in the United States: The Role of Rotavirus Activity and Diagnostic Misclassification.

Epidemiology 2022 Sep 18;33(5):660-668. Epub 2022 May 18.

Division of Viral Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, GA.

Background: Estimates of rotavirus vaccine effectiveness (VE) in the United States appear higher in years with more rotavirus activity. We hypothesized rotavirus VE is constant over time but appears to vary as a function of temporal variation in local rotavirus cases and/or misclassified diagnoses.

Methods: We analyzed 6 years of data from eight US surveillance sites on 8- to 59-month olds with acute gastroenteritis symptoms. Children's stool samples were tested via enzyme immunoassay (EIA); rotavirus-positive results were confirmed with molecular testing at the US Centers for Disease Control and Prevention. We defined rotavirus gastroenteritis cases by either positive on-site EIA results alone or positive EIA with Centers for Disease Control and Prevention confirmation. For each case definition, we estimated VE against any rotavirus gastroenteritis, moderate-to-severe disease, and hospitalization using two mixed-effect regression models: the first including year plus a year-vaccination interaction, and the second including the annual percent of rotavirus-positive tests plus a percent positive-vaccination interaction. We used multiple overimputation to bias-adjust for misclassification of cases defined by positive EIA alone.

Results: Estimates of annual rotavirus VE against all outcomes fluctuated temporally, particularly when we defined cases by on-site EIA alone and used a year-vaccination interaction. Use of confirmatory testing to define cases reduced, but did not eliminate, fluctuations. Temporal fluctuations in VE estimates further attenuated when we used a percent positive-vaccination interaction. Fluctuations persisted until bias-adjustment for diagnostic misclassification.

Conclusions: Both controlling for time-varying rotavirus activity and bias-adjusting for diagnostic misclassification are critical for estimating the most valid annual rotavirus VE.
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http://dx.doi.org/10.1097/EDE.0000000000001501DOI Listing
September 2022

Acute Hepatitis and Adenovirus Infection Among Children - Alabama, October 2021-February 2022.

MMWR Morb Mortal Wkly Rep 2022 May 6;71(18):638-640. Epub 2022 May 6.

During October-November 2021, clinicians at a children's hospital in Alabama identified five pediatric patients with severe hepatitis and adenovirus viremia upon admission. In November 2021, hospital clinicians, the Alabama Department of Public Health, the Jefferson County Department of Health, and CDC began an investigation. This activity was reviewed by CDC and conducted consistent with applicable federal law and CDC policy.
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http://dx.doi.org/10.15585/mmwr.mm7118e1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9098244PMC
May 2022

Effectiveness of Monovalent Rotavirus Vaccine in Mozambique, a Country with a High Burden of Chronic Malnutrition.

Vaccines (Basel) 2022 Mar 15;10(3). Epub 2022 Mar 15.

Instituto Nacional de Saúde (INS), EN1, Bairro da Vila-Parcela nº 3943, Distrito de Marracuene, Maputo 264, Mozambique.

Mozambique introduced monovalent rotavirus vaccine (Rotarix) in September 2015. We evaluated the effectiveness of Rotarix under conditions of routine use in Mozambican children hospitalized with acute gastroenteritis (AGE). A test negative case-control analysis was performed on data collected during 2017-2019 from children <5 years old, admitted with AGE in seven sentinel hospital sites in Mozambique. Adjusted VE was calculated for ≥1 dose of vaccine vs. zero doses using unconditional logistic regression, where VE = (1 - aOR) × 100%. VE estimates were stratified by age group, AGE severity, malnutrition, and genotype. Among 689 children eligible for analysis, 23.7% were rotavirus positive (cases) and 76.3% were negative (controls). The adjusted VE of ≥1 dose in children aged 6-11 months was 52.0% (95% CI, -11, 79), and -24.0% (95% CI, -459, 62) among children aged 12-23 months. Estimated VE was lower in stunted than non-stunted children (14% (95% CI, -138, 66) vs. 59% (95% CI, -125, 91)). Rotavirus vaccination appeared moderately effective against rotavirus gastroenteritis hospitalization in young Mozambican children. VE point estimates were lower in older and stunted children, although confidence intervals were wide and overlapped across strata. These findings provide additional evidence for other high-mortality countries considering rotavirus vaccine introduction.
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http://dx.doi.org/10.3390/vaccines10030449DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8953339PMC
March 2022

Trends in rotavirus laboratory detections and internet search volume before and after rotavirus vaccine introduction and in the context of the COVID-19 pandemic-- United States 2000-2021.

J Infect Dis 2022 Feb 20. Epub 2022 Feb 20.

Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, GA, USA.

Background: Since rotavirus vaccines became available in the United States in 2006, there have been reductions in rotavirus hospitalizations, changes in seasonality, and the emergence of a biennial trend of rotavirus activity. Reductions in other pathogens have been associated with COVID-19 mitigation measures. We assessed ongoing rotavirus disease trends during the COVID-19 pandemic.

Methods: We report a 3-week moving average of the number of rotavirus tests, positive tests, and the percent positivity from laboratories reporting to the National Respiratory and Enteric Virus Surveillance System (NREVSS) from July 2000-June 2021. To complement NREVSS data, we analyzed Google internet search interest in "rotavirus" from July 2004 to June 2021.

Results: Declines in rotavirus activity following vaccine introduction and the biennial trend are evident through the 2018-2019 surveillance year. In 2019-2021, rotavirus test positivity was below the historic ranges during the months of typically high rotavirus activity and precipitous declines were noted in March 2020.

Conclusions: In the 15 years since rotavirus vaccine was introduced, the number of laboratory-detected rotavirus infections has been consistently lower than during the pre-vaccine era. During the COVID-19 pandemic, rotavirus activity was suppressed. There may be many rotavirus susceptible children during the 2021-2022 rotavirus season.
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http://dx.doi.org/10.1093/infdis/jiac062DOI Listing
February 2022

Impact of rotavirus vaccination on rotavirus hospitalizations in Taiwanese children.

Vaccine 2021 12 14;39(49):7135-7139. Epub 2021 Nov 14.

Division of Pediatric Infectious Diseases, Chang Gung Memorial Hospital, Taoyuan City, Taiwan; Chang Gung University College of Medicine, Taoyuan City, Taiwan. Electronic address:

In 2006, two rotavirus vaccines were licensed in Taiwan but were not added to the national immunization schedule. National Health Insurance data from 2003 through 2017 were used to compare rotavirus-associated pediatric hospitalizations before and after vaccine introduction. Rotavirus hospitalization rates among children < 5 years of age significantly declined by 24% (95% confidence interval [CI] 23 - 25%) in post-vaccine compared to pre-vaccine rotavirus seasons. Rotavirus hospitalization rates declined by 42% (95% CI 39 - 44%) among infants < 12 months of age, and by 38% (95% CI 36 - 40%) among children 12 - 23 months of age. These findings suggest that, despite not being included in the national immunization schedule, rotavirus vaccines had a measurable impact on reducing rotavirus hospitalization burden among Taiwanese children.
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http://dx.doi.org/10.1016/j.vaccine.2021.10.064DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9014808PMC
December 2021

Rotavirus infection among children under five years of age hospitalized with acute gastroenteritis in Myanmar during 2018-2020 - Multicentre surveillance before rotavirus vaccine introduction.

Vaccine 2021 11 24;39(47):6907-6912. Epub 2021 Oct 24.

Department of Medical Research, Ministry of Health and Sports, Myanmar.

Background: Rotavirus gastroenteritis (RVGE) is a leading cause of severe diarrhea in children under-five worldwide, with the majority of mortality in lower -income countries. This study aimed to provide baseline information on epidemiology of rotavirus and circulating strains before rotavirus vaccine introduction in Myanmar.

Methods: Hospital-based, prospective surveillance was conducted from May 2018 to January 2020 at four sentinel sites; two hospitals in Lower Myanmar, one hospital each in Middle Myanmar and East Myanmar. Children under five years of age hospitalized for acute gastroenteritis were enrolled; demographic and clinical data were collected. Stool samples were screened by ELISA (ProSpecT™ Rotavirus, OXOID-UK) for rotavirus antigen and a subset of ELISA positive samples were genotyped by reverse transcription polymerase chain reaction.

Results: Rotavirus was detected in 45.7% (799/1750) of cases enrolled at three sites in May 2018-April 2019 and 42.5% (521/1227) at four sites in May 2019-January 2020. RVGE cases were predominantly male (58.7%; 775/1320) and 92.6% (1223/1320) of RVGE cases occurred in <2 years old. Rotavirus detection was higher in the cold and dry season (November-April). RVGE compared to non-RVGE cases had more frequent vomiting (78.3% Vs 68.1%, p < 0.01), fever (65.8% Vs 61.3%, p = 0.01), severe dehydration (3.6% Vs 2.1%, p < 0.01) and requirement of treatment by IV fluid (58.3% Vs 53.1%, p < 0.01). The most prevalent genotypes identified were G1P[6] (113/359, 31.5%), G1P[8] (94/359, 26.2%) and G2P[4] (33/359, 9.2%).

Conclusions: This study confirms the persistent high prevalence of RVGE among children under-five admitted to hospitals in different parts of Myanmar and the diversity of rotavirus strains over time prior to vaccine introduction. The rotavirus vaccine was introduced nationwide in February 2020 in Myanmar and these data will be important baseline data for post-vaccination monitoring of vaccine impact and circulating strains.
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http://dx.doi.org/10.1016/j.vaccine.2021.10.014DOI Listing
November 2021

Comparing statistical methods for detecting and estimating waning efficacy of rotavirus vaccines in developing countries.

Hum Vaccin Immunother 2021 11 6;17(11):4632-4635. Epub 2021 Oct 6.

Centers for Disease Control and Prevention, Atlanta, GA, USA.

Introduction: Vaccination has significantly reduced morbidity and mortality resulting from rotavirus infection worldwide. However, rotavirus vaccine efficacy (VE) appears to wane over the first 2 years since vaccination, particularly in developing countries. Statistical methods for detecting VE waning and estimating its rate have been used in a few studies, but comparisons of methods for evaluating VE waning have not yet been performed. In this work we present and compare three methods - Durham's method, Tian's method, and time-dependent covariate (TDC) method - based on generalizations of the Cox proportional hazard model.

Methods: We developed a new stochastic agent-based simulation model to generate data from a hypothetical rotavirus vaccine trial where the protective efficacy of the vaccine may vary over time. Input parameters to the simulation model were obtained from studies on rotavirus infections in four developing countries. We applied each of the methods to four simulated datasets and compared the type-1 error probabilities and the powers of the resulting statistical tests. We also compared estimated and true values of VE over time.

Results: Durham's method had the highest power of detecting true VE waning of the three methods. This method also provided quite accurate estimates of VE in each period and of the per-period drop in VE.

Conclusions: Durham's method is somewhat more powerful than the other two Cox proportional hazards model-based methods for detecting VE waning and provides more information about the temporal behavior of VE.
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http://dx.doi.org/10.1080/21645515.2021.1968738DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8828126PMC
November 2021

Epidemiology of intussusception in infants less than one year of age in Ghana, 2012-2016.

Pan Afr Med J 2021 29;39(Suppl 1). Epub 2021 Jul 29.

Noguchi Medical Institute for Medical Research, University of Ghana, Accra, Ghana.

Introduction: we examined the epidemiology, clinical and demographic characteristics of intussusception in Ghanaian infants.

Methods: active sentinel surveillance for pediatric intussusception was conducted at Komfo Anokye Teaching Hospital in Kumasi and Korle Bu Teaching Hospital in Accra. From March 2012 to December 2016, infants < 1 year of age who met the Brighton Collaboration level 1 diagnostic criteria for intussusception were enrolled. Data were collected through parental interviews and medical records abstraction.

Results: a total of 378 children < 1 year of age were enrolled. Median age at onset of intussusception was 27 weeks; only 12 cases (1%) occurred in infants < 12 weeks while most occurred in infants aged 22-34 weeks. Median time from symptom onset until referral to a tertiary hospital was 2 days (IQR: 1-4 days). Overall, 35% of infants were treated by enema, 33% had surgical reduction and 32% required surgical reduction and bowel resection. Median length of hospital stay was 5 days (IQR: 3-8 days) with most patients (95%) discharged home. Eleven (3%) infants died. Infants undergoing enema reduction were more likely than those treated surgically to present for treatment sooner after symptom onset (median 1 vs 3 days; p < 0.0001) and have shorter hospital stays (median 3 vs 7 days; p < 0.001).

Conclusion: Ghanaian infants had a relatively low case fatality rate due to intussusception, with a substantial proportion of cases treated non-surgically. Early presentation for treatment, possibly enhanced by community-based health education programs and health information from various media platforms during the study period might contribute to both the low fatality rate and high number of successful non-surgical treatments in this population.
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http://dx.doi.org/10.11604/pamj.supp.2021.39.1.25445DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8437423PMC
October 2021

Acute intestinal intussusception among children under five years of age admitted in an Ouagadougou hospital, Burkina Faso, 2008-2013: epidemiological, clinical and therapeutic aspects.

Pan Afr Med J 2021 28;39(Suppl 1). Epub 2021 Jul 28.

Centers for Disease Control and Prevention, Atlanta, United States.

Introduction: acute intestinal intussusception is a life-threatening surgical condition. In some settings, rotavirus vaccines have been associated with a low-level increased risk of intussusception. We describe the epidemiology, clinical manifestations and management of intussusception in a tertiary referral hospital in Burkina Faso prior to the introduction of rotavirus vaccine in October 2013.

Methods: we retrospectively reviewed medical records of all children under 5 years of age treated at the Charles de Gaulle Pediatric Hospital for intussusception meeting the Brighton level 1 diagnostic criteria, from October 31st, 2008 to October 30th, 2013. We report the incidence of intussusception as well as descriptive characteristics of these cases.

Results: a total of 107 Brighton level 1 intussusception cases were identified, representing a hospital incidence of 21.4 cases / year. There were 69 males and 38 females (sex ratio of 1.8), with a median age of 8 months (range 2 months to 4 years). Sixty-two percent of intussusception cases occurred among infants (n = 67 cases). The average time from symptom onset to seeking medical consultation was 3.8 days +/- 2.7 (range 0 to 14 days). Treatment was mainly surgical (105 patients, 98.1%) with 35 patients (32.7%) undergoing intestinal resection. Thirty-seven patients (35.5%) experienced post-operative complications. The mortality rate was 9.3%. Intestinal resection was a risk factor for death from intussusception.

Conclusion: in this review of intussusception hospitalizations prior to rotavirus vaccine introduction in Burkina Faso, delays in seeking care were common and were associated with mortality.
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http://dx.doi.org/10.11604/pamj.supp.2021.39.1.25270DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8437429PMC
October 2021

Epidemiology of intussusception among infants in Ethiopia, 2013-2016.

Pan Afr Med J 2021 27;39(Suppl 1). Epub 2021 Jul 27.

Centers for Disease Control and Prevention, Atlanta, GA, USA.

Introduction: intussusception is a condition in which one segment of the bowel prolapses into another causing obstruction. Information on the epidemiology of intussusception in sub-Saharan Africa is limited. We describe the sociodemographic and clinical characteristics of children with intussusception in Ethiopia.

Methods: active surveillance for children < 12 months of age with intussusception was conducted at six sentinel hospitals in Ethiopia. Limited socio-economic and clinical data were collected from enrolled children. Characteristics among children who died and children who survived were compared using the Wilcoxon rank sum test for continuous variables and Chi-square tests for categorical variables.

Results: total of 164 children < 12 months of age with intussusception were enrolled; 62% were male. The median age at symptom onset was 6 months with only 12 (7%) of cases occurring in the first 3 months of life. Intussusception was reduced by surgery in 90% of cases and 10% were reduced by enema; 13% of cases died. Compared to survivors, children who died had a significantly longer time to presentation to the first health care facility and to the treating health care facility (median 3 days versus 2 days, p = 0.02, respectively).

Conclusion: the high mortality rate, late presentation of intussusception cases, and lack of modalities for non-surgical management at some facilities highlight the need for better management of intussusception cases in Ethiopia.
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http://dx.doi.org/10.11604/pamj.supp.2021.39.1.21299DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8437422PMC
October 2021

Epidemiology of intussusception in sub-Saharan Africa.

Pan Afr Med J 2021 27;39(Suppl 1). Epub 2021 Jul 27.

Centers for Disease Control and Prevention, Atlanta, Georgia, USA.

This supplement contains the findings from intussusception surveillance conducted in 9 countries. These articles provide information on the age distribution of intussusception in the first year of life with cases peaking at 4-6 months of age, highlight the high proportion of cases in most, but not all, countries that undergo surgery and often require bowel resection for the treatment of intussusception, and show the variability of treatment outcomes in different countries. These data will be important for improving diagnosis and treatment of intussusception in young children in sub-Saharan Africa.
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http://dx.doi.org/10.11604/pamj.supp.2021.39.1.30287DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8437424PMC
October 2021

Comparative genomic analysis of genogroup 1 and genogroup 2 rotaviruses circulating in seven US cities, 2014-2016.

Virus Evol 2021 Jan 12;7(1):veab023. Epub 2021 Mar 12.

Division of Viral Diseases, Centers for Disease Control and Prevention, Viral Gastroenteritis Branch, Atlanta, GA, USA.

For over a decade, the New Vaccine Surveillance Network (NVSN) has conducted active rotavirus (RVA) strain surveillance in the USA. The evolution of RVA in the post-vaccine introduction era and the possible effects of vaccine pressure on contemporary circulating strains in the USA are still under investigation. Here, we report the whole-gene characterization (eleven ORFs) for 157 RVA strains collected at seven NVSN sites during the 2014 through 2016 seasons. The sequenced strains included 52 G1P[8], 47 G12P[8], 18 G9P[8], 24 G2P[4], 5 G3P[6], as well as 7 vaccine strains, a single mixed strain (G9G12P[8]), and 3 less common strains. The majority of the single and mixed strains possessed a Wa-like backbone with consensus genotype constellation of G1/G3/G9/G12-P[8]-I1-R1-C1-M1-A1-N1-T1-E1-H1, while the G2P[4], G3P[6], and G2P[8] strains displayed a DS-1-like genetic backbone with consensus constellation of G2/G3-P[4]/P[6]/P[8]-I2-R2-C2-M2-A2-N2-T2-E2-H2. Two intergenogroup reassortant G1P[8] strains were detected that appear to be progenies of reassortment events between Wa-like G1P[8] and DS-1-like G2P[4] strains. Two Rotarix vaccine (RV1) and two RV5 derived (vd) reassortant strains were detected. Phylogenetic and similarity matrices analysis revealed 2-11 sub-genotypic allelic clusters among the genes of Wa- and DS-1-like strains. Most study strains clustered into previously defined alleles. Amino acid (AA) substitutions occurring in the neutralization epitopes of the VP7 and VP4 proteins characterized in this study were mostly neutral in nature, suggesting that these RVA proteins were possibly under strong negative or purifying selection in order to maintain competent and actual functionality, but fourteen radical (AA changes that occur between groups) AA substitutions were noted that may allow RVA strains to gain a selective advantage through immune escape. The tracking of RVA strains at the sub-genotypic allele constellation level will enhance our understanding of RVA evolution under vaccine pressure, help identify possible mechanisms of immune escape, and provide valuable information for formulation of future RVA vaccines.
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http://dx.doi.org/10.1093/ve/veab023DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8432945PMC
January 2021

Impact of Monovalent Rotavirus Vaccine on Rotavirus Hospitalizations among Children Younger Than 5 Years of Age in the Ouest and Artibonite Departments, Haiti, 2013 to 2019.

Am J Trop Med Hyg 2021 08 16;105(5):1309-1316. Epub 2021 Aug 16.

CDC Country Office, Port-au-Prince, Haiti.

Rotavirus is responsible for 26% of diarrheal deaths in Latin America and the Caribbean. Haiti introduced the monovalent rotavirus vaccine in April 2014. The objective of this analysis is to describe the impact of the rotavirus vaccine on hospitalizations among Haitian children younger than 5 years old during the first 5 years after introduction. This analysis includes all children with diarrhea who were enrolled as part of a sentinel surveillance system at two hospitals from May 2013 to April 2019. We compare the proportion of rotavirus-positive specimens in each post-vaccine introduction year to the pre-vaccine period. To account for the potential dilution of the proportion of rotavirus-positive specimens from a waning cholera outbreak, we also analyzed annual trends in the absolute number of positive stools, fit a two-component finite-mixture model to the negative specimens, and fit a negative binomial time series model to the pre-vaccine rotavirus-positive specimens to predict the number of rotavirus diarrhea hospital admissions in the absence of rotavirus vaccination. The overall percentage of rotavirus-positive specimens declined by 22% the first year after introduction, increased by 17% the second year, and declined by 33% to 50% the subsequent 3 years. All sensitivity analyses confirmed an overall decline. We observed a clear annual rotavirus seasonality before and after vaccine introduction, with the greatest activity in December through April, and a biennial pattern, with high sharp peaks and flatter longer periods of increased rotavirus activity in alternating years, consistent with suboptimal vaccination coverage. Overall, our study shows evidence that the introduction of the rotavirus vaccine reduced the burden of severe rotavirus diarrhea.
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http://dx.doi.org/10.4269/ajtmh.21-0414DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8592188PMC
August 2021

Global Experience With Rotavirus Vaccines.

J Infect Dis 2021 12;224(12 Suppl 2):S792-S800

Viral Gastroenteritis Branch, US Centers for Disease Control and Prevention, Atlanta, Georgia, USA.

Rotavirus is a major cause of severe pediatric diarrhea worldwide. In 2006, 2 live, oral rotavirus vaccines, Rotarix and RotaTeq, were licensed for use in infants and were rapidly adopted in many high- and middle-income settings where efficacy had been demonstrated in clinical trials. Following completion of successful trials in low-income settings, the World Health Organization (WHO) recommended rotavirus vaccination for all infants globally in 2009. In 2018, 2 new rotavirus vaccines, Rotasiil and Rotavac, were prequalified by WHO, expanding global availability. As of March 2021, rotavirus vaccines have been introduced nationally in 106 countries. Since, Rotavirus vaccines have demonstrated effectiveness against severe disease and mortality, even among age groups in eligible for vaccination. Cross-genotypic protection has been demonstrated, and the favorable benefit-risk profile of these vaccines continues to be confirmed. Ongoing research seeks to better understand reasons for the geographic disparities in effectiveness observed, in order to optimize vaccine strategies worldwide.
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http://dx.doi.org/10.1093/infdis/jiab399DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8687052PMC
December 2021

Cytokine profiles in children with acute intussusception in South Africa.

Cytokine 2021 10 17;146:155639. Epub 2021 Jul 17.

South African Medical Research Council/Wits Vaccines and Infectious Diseases Analytics Research Unit, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.

Serum specimens of children hospitalized with acute intussusception (IS; n = 407) were analyzed for various pro- and anti-inflammatory cytokines to identify host markers specifically for IS compared to other surgical conditions (n = 235) or acute gastroenteritis (AGE; n = 68) in a cross-sectional study design. We showed that children with IS had elevated levels of pro-inflammatory cytokines IFN-γ, TNF-α, MIP-1β, IL-1β, IL-2, IL-6, IL-7, IL-8, and IL-17 as well as anti-inflammatory cytokines IL-1RA, IL-4, IL-5, and IL-13 compared to those admitted with surgical conditions or AGE symptoms, indicating these cytokines as markers for IS. In addition, we showed an increase in C-reactive protein (CRP) levels in children with IS. This study is the first to show a broad cytokine profile and identify cytokine markers in children with IS.
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http://dx.doi.org/10.1016/j.cyto.2021.155639DOI Listing
October 2021

Clinical presentation and management of childhood intussusception in South Africa.

Pediatr Surg Int 2021 Oct 2;37(10):1361-1370. Epub 2021 Jul 2.

South African Medical Research Council: Vaccines and Infectious Diseases Analytics Research Unit, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.

Purpose: We assessed management and outcomes for intussusception at nine academic hospitals in South Africa.

Methods: Patients ≤ 3 years presenting with intussusception between September 2013 and December 2017 were prospectively enrolled at all sites. Additionally, patients presenting between July 2012 and August 2013 were retrospectively enrolled at one site. Demographics, clinical information, diagnostic modality, reduction methods, surgical intervention and outcomes were reviewed.

Results: Four hundred seventy-six patients were enrolled, [54% males, median age 6.5 months (IQR 2.6-32.6)]. Vomiting (92%), bloody stool (91%), abdominal mass (57%), fever (32%) and a rectal mass (29%) represented advanced disease: median symptom duration was 3 days (IQR 1-4). Initial reduction attempts included pneumatic reduction (66%) and upfront surgery (32%). The overall non-surgical reduction rate was 28% and enema perforation rate was 4%. Surgery occurred in 334 (70%), 68 (20%) patients had perforated bowel, bowel resection was required in 61%. Complications included recurrence (2%) and nosocomial sepsis (4%). Length of stay (LOS) was significantly longer in patients who developed complications. Six patients died-a mortality rate of 1%. There was a significant difference in reduction rates, upfront surgery, bowel resection, LOS and mortality between centres with shorter symptom duration compared longer symptom duration.

Conclusion: Delayed presentation was common and associated with low success for enema reduction, higher operative rates, higher rates of bowel resection and increased LOS. Improved primary health-care worker education and streamlining referral pathways might facilitate timely management.
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http://dx.doi.org/10.1007/s00383-021-04946-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8408053PMC
October 2021

Effectiveness of monovalent rotavirus vaccine against hospitalizations due to all rotavirus and equine-like G3P[8] genotypes in Haiti 2014-2019.

Vaccine 2021 07 27;39(32):4458-4462. Epub 2021 Jun 27.

Division of Viral Diseases, NCIRD, CDC, USA.

Background: Rotavirus vaccines are effective in preventing severe rotavirus. Haiti introduced 2-dose monovalent (G1P[8]) rotavirus vaccine recommended for infants at 6 and 10 weeks of age in 2014. We calculated the effectiveness of rotavirus vaccine against hospitalization for acute gastroenteritis in Haiti.

Methods: We enrolled children 6-59 months old admitted May 2014-September 2019 for acute watery diarrhea at any sentinel surveillance hospital. Stool was tested for rotavirus using enzyme immunoassay (EIA) and genotyped with multiplex one-step RT-PCR assay and Sanger sequencing for stratification by genotype. We used a case-negative design where cases were children positive for rotavirus and controls were negative for rotavirus. Only children eligible for vaccination were included and a child was considered vaccinated if vaccine was given ≥ 14 days before enrollment. We used unconditional logistic regression to calculate odds ratios and calculated 2-dose and 1-dose vaccine effectiveness (VE) as (1 - odds ratio) * 100.

Results: We included 129 (19%) positive cases and 543 (81%) negative controls. Among cases, 77 (60%) were positive for equine-like G3P[8]. Two doses of rotavirus vaccine were 66% (95% CI: 44, 80) effective against hospitalizations due to any strain of rotavirus and 64% (95% CI: 33, 81) effective against hospitalizations due to the equine-like G3P[8] genotype.

Conclusions: These findings are comparable to other countries in the Americas region. To the best of our knowledge, this is the first VE estimate both against the equine-like G3P[8] genotype and from a Caribbean country. Overall, these results support rotavirus vaccine use and demonstrate the importance of complete vaccination.
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http://dx.doi.org/10.1016/j.vaccine.2021.06.055DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8474148PMC
July 2021

Rotavirus Infection, Illness, and Vaccine Performance in Malnourished Children: A Review of the Literature.

Pediatr Infect Dis J 2021 10;40(10):930-936

Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia.

Live, oral rotavirus vaccines are more effective at preventing rotavirus disease in countries with low child mortality compared with high child mortality. Among several hypotheses, poorer protection in malnourished children, who are more prevalent in countries with high child mortality, may partially explain this difference. We conducted a literature search to identify articles with a laboratory-confirmed rotavirus endpoint that evaluated differences by malnutrition status in rotavirus vaccine effectiveness and vaccine efficacy (VE) or the prevalence of rotavirus infection or illness among children <5 years old. We identified 7 analyses from 11 countries published from 2007 to 2019 that stratified rotavirus VE by malnutrition status. Among well-nourished children, VE point estimates ranged from 71% to 84% in observational studies and 26% to 61% in clinical trials. Among malnourished children, they ranged from -28% to 45% in observational studies and -3% to 61% in clinical trials. The relative difference between VE in well-nourished and malnourished children by length-for-age ranged from 37% to 64%, by weight-for-age ranged from 0% to 107%, and by weight-for-height ranged from -65% to 137%. We identified 3 cohort and 6 cross-sectional studies of natural rotavirus infection and illness and none reported that malnourished children were more susceptible to rotavirus infection or illness than well-nourished children. Overall, rotavirus vaccines may offer less protection to children with malnutrition than well-nourished children. As malnourished children often have worse outcomes from diarrhea, high rotavirus vaccine coverage and a better understanding of the performance of oral rotavirus vaccines in this population is important, though our finding that malnourished children may be less susceptible to rotavirus provides important context and information for vaccine evaluation design.
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http://dx.doi.org/10.1097/INF.0000000000003206DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8489158PMC
October 2021

Novel vaccine safety issues and areas that would benefit from further research.

BMJ Glob Health 2021 05;6(Suppl 2)

Essential Medicines and Health Products, Organisation Mondiale de la Sante, Geneve, Switzerland.

Vaccine licensure requires a very high safety standard and vaccines routinely used are very safe. Vaccine safety monitoring prelicensure and postlicensure enables continual assessment to ensure the benefits outweigh the risks and, when safety problems arise, they are quickly identified, characterised and further problems prevented when possible. We review five vaccine safety case studies: (1) dengue vaccine and enhanced dengue disease, (2) pandemic influenza vaccine and narcolepsy, (3) rotavirus vaccine and intussusception, (4) human papillomavirus vaccine and postural orthostatic tachycardia syndrome and complex regional pain syndrome, and (5) RTS,S/adjuvant system 01 malaria vaccine and meningitis, cerebral malaria, female mortality and rebound severe malaria. These case studies were selected because they are recent and varied in the vaccine safety challenges they elucidate. Bringing these case studies together, we develop lessons learned that can be useful for addressing some of the potential safety issues that will inevitably arise with new vaccines.
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http://dx.doi.org/10.1136/bmjgh-2020-003814DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8137224PMC
May 2021

Rotavirus Strain Distribution before and after Introducing Rotavirus Vaccine in India.

Pathogens 2021 Apr 1;10(4). Epub 2021 Apr 1.

The Wellcome Trust Research Laboratory, Division of Gastrointestinal Sciences, Christian Medical College, Vellore 632004, India.

In April 2016, an indigenous monovalent rotavirus vaccine (Rotavac) was introduced to the National Immunization Program in India. Hospital-based surveillance for acute gastroenteritis was conducted in five sentinel sites from 2012 to 2020 to monitor the vaccine impact on various genotypes and the reduction in rotavirus positivity at each site. Stool samples collected from children under 5 years of age hospitalized with diarrhea were tested for group A rotavirus using a commercial enzyme immunoassay, and rotavirus strains were characterized by RT-PCR. The proportion of diarrhea hospitalizations attributable to rotavirus at the five sites declined from a range of 56-29.4% in pre-vaccine years to 34-12% in post-vaccine years. G1P[8] was the predominant strain in the pre-vaccination period, and G3P[8] was the most common in the post-vaccination period. Circulating patterns varied throughout the study period, and increased proportions of mixed genotypes were detected in the post-vaccination phase. Continuous long-term surveillance is essential to understand the diversity and immuno-epidemiological effects of rotavirus vaccination.
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http://dx.doi.org/10.3390/pathogens10040416DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8066972PMC
April 2021

Rotavirus Genotype Trends and Gastrointestinal Pathogen Detection in the United States, 2014-2016: Results From the New Vaccine Surveillance Network.

J Infect Dis 2021 11;224(9):1539-1549

Centers for Disease Control and Prevention, Atlanta, Georgia, USA.

Background: Following the implementation of rotavirus vaccination in 2006, severe acute gastroenteritis (AGE) due to group A rotavirus (RVA) has substantially declined in US children. We report the RVA genotype prevalence as well as coinfection data from 7 US New Vaccine Surveillance Network sites during 3 consecutive RVA seasons, 2014-2016.

Methods: A total of 1041 stool samples that tested positive for RVA by Rotaclone enzyme immunoassay were submitted to the Centers for Disease Control and Prevention (CDC) for RVA genotyping and multipathogen testing.

Results: A total of 795 (76%) samples contained detectable RVA when tested at the CDC. Rotavirus disease was highest in children < 3 years of age. Four G types (G1, G2, G9, and G12) accounted for 94.6% of strains while 2 P types (P[4] and P[8]) accounted for 94.7% of the strains. Overall, G12P[8] was the most common genotype detected in all 3 seasons. Stepwise conditional logistic analysis found year and study site were significant predictors of genotype. Twenty-four percent of RVA-positive specimens contained other AGE pathogens.

Conclusions: G12P[8] predominated over 3 seasons, but strain predominance varied by year and study site. Ongoing surveillance provides continuous tracking and monitoring of US genotypes during the postvaccine era.
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http://dx.doi.org/10.1093/infdis/jiab177DOI Listing
November 2021

Pediatric Respiratory and Enteric Virus Acquisition and Immunogenesis in US Mothers and Children Aged 0-2: PREVAIL Cohort Study.

JMIR Res Protoc 2021 Feb 12;10(2):e22222. Epub 2021 Feb 12.

Division of Foodborne, Waterborne, and Environmental Diseases, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, United States.

Background: Acute gastroenteritis (AGE) and acute respiratory infections (ARIs) cause significant pediatric morbidity and mortality. Developing childhood vaccines against major enteric and respiratory pathogens should be guided by the natural history of infection and acquired immunity. The United States currently lacks contemporary birth cohort data to guide vaccine development.

Objective: The PREVAIL (Pediatric Respiratory and Enteric Virus Acquisition and Immunogenesis Longitudinal) Cohort study was undertaken to define the natural history of infection and immune response to major pathogens causing AGE and ARI in US children.

Methods: Mothers in Cincinnati, Ohio, were enrolled in their third trimester of pregnancy, with intensive child follow-up to 2 years. Blood samples were obtained from children at birth (cord), 6 weeks, and 6, 12, 18, and 24 months. Whole stool specimens and midturbinate nasal swabs were collected weekly and tested by multipathogen molecular assays. Saliva, meconium, maternal blood, and milk samples were also collected. AGE (≥3 loose or watery stools or ≥1 vomiting episode within 24 hours) and ARI (cough or fever) cases were documented by weekly cell phone surveys to mothers via automated SMS text messaging and review of medical records. Immunization records were obtained from registries and providers. follow-up ended in October 2020. Pathogen-specific infections are defined by a PCR-positive sample or rise in serum antibody.

Results: Of the 245 enrolled mother-child pairs, 51.8% (n=127) were White, 43.3% (n=106) Black, 55.9% (n=137) publicly insured, and 86.5% (n=212) initiated breastfeeding. Blood collection was 100.0% for mothers (n=245) and 85.7% for umbilical cord (n=210). A total of 194/245 (79.2%) mother-child pairs were compliant based on participation in at least 70% (≥71/102 study weeks) of child-weeks and providing 70% or more of weekly samples during that time, or blood samples at 18 or 24 months. Compliant participants (n=194) had 71.0% median nasal swab collection (IQR 30.0%-90.5%), with 98.5% (191/194) providing either an 18- or 24-month blood sample; median response to weekly SMS text message surveys was 95.1% (IQR 76.5%-100%). Compliant mothers reported 2.0 AGE and 4.5 ARI cases per child-year, of which 25.5% (160/627) and 38.06% (486/1277) of cases, respectively, were medically attended; 0.5% of AGE (3/627) and 0.55% of ARI (7/1277) cases were hospitalized.

Conclusions: The PREVAIL Cohort demonstrates intensive follow-up to document the natural history of enteric and respiratory infections and immunity in children 0-2 years of age in the United States and will contribute unique data to guide vaccine recommendations. Testing for pathogens and antibodies is ongoing.

International Registered Report Identifier (irrid): RR1-10.2196/22222.
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http://dx.doi.org/10.2196/22222DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7910118PMC
February 2021

Hospital-based Surveillance for Pediatric Norovirus Gastroenteritis in Bangladesh, 2012-2016.

Pediatr Infect Dis J 2021 03;40(3):215-219

Centers for Disease Control and Prevention, Atlanta, GA.

Background: Globally, noroviruses are recognized as an important cause of acute gastroenteritis (AGE), but data from low and middle-income countries are limited.

Aims: To examine the epidemiology and strain diversity of norovirus infections among children hospitalized for AGE in Bangladesh.

Methods: We implemented active surveillance of children <5 years of age hospitalized with AGE at 8 geographically dispersed tertiary care hospitals in Bangladesh from July 2012 to June 2016. We tested random samples of AGE cases stratified by site and age group for norovirus by real-time RT-PCR. Noro-positive specimens were genotyped. Coinfection with rotavirus was assessed based on prior EIA testing.

Results: We enrolled 5622 total AGE cases, of which 1008 were tested for norovirus. Total of 137 (14%) AGE cases tested positive for norovirus (range, 11%-17% by site). Most (94%) norovirus-associated hospitalizations were among children less than 2 years of age. Norovirus was detected year-round, with higher detection from March to June (20%-38%) and November to January (9%-18%). Genogroup II (GII) noroviruses were detected in 96% of cases, and the most frequent genotypes were GII.4 Sydney [P4 New Orleans] (33%), GII.3 [P16] (20%), and GII.4 Sydney [P16] (11%). The proportion of norovirus-positive specimens was significantly greater among rotavirus-negative AGE patients compared with rotavirus-positive AGE patients (27% vs. 5%, P < 0.001). As measured by the Vesikari severity score, a similar proportion of norovirus and rotavirus positive AGE patients were considered severe (68% vs. 70%, P = 0.86).

Conclusions: Norovirus is an important cause of AGE hospitalization in Bangladeshi children with most infections caused by GII viruses.
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http://dx.doi.org/10.1097/INF.0000000000002989DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9006183PMC
March 2021

Multiple Introductions and Predominance of Rotavirus Group A Genotype G3P[8] in Kilifi, Coastal Kenya, 4 Years after Nationwide Vaccine Introduction.

Pathogens 2020 Nov 24;9(12). Epub 2020 Nov 24.

Kenya Medical Research Institute (KEMRI)-Wellcome Trust Research Programme, off Hospital Road, Kilifi 80108, Kenya.

Globally, rotavirus group A (RVA) remains a major cause of severe childhood diarrhea, despite the use of vaccines in more than 100 countries. RVA sequencing for local outbreaks facilitates investigation into strain composition, origins, spread, and vaccine failure. In 2018, we collected 248 stool samples from children aged less than 13 years admitted with diarrheal illness to Kilifi County Hospital, coastal Kenya. Antigen screening detected RVA in 55 samples (22.2%). Of these, VP7 (G) and VP4 (P) segments were successfully sequenced in 48 (87.3%) and phylogenetic analysis based on the VP7 sequences identified seven genetic clusters with six different GP combinations: G3P[8], G1P[8], G2P[4], G2P[8], G9P[8] and G12P[8]. The G3P[8] strains predominated the season ( = 37, 67.2%) and comprised three distinct G3 genetic clusters that fell within Lineage I and IX (the latter also known as equine-like G3 Lineage). Both the two G3 lineages have been recently detected in several countries. Our study is the first to document African children infected with G3 Lineage IX. These data highlight the global nature of RVA transmission and the importance of increasing global rotavirus vaccine coverage.
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http://dx.doi.org/10.3390/pathogens9120981DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7761311PMC
November 2020

Persistence of Maternal Anti-Rotavirus Immunoglobulin G in the Post-Rotavirus Vaccine Era.

J Infect Dis 2021 07;224(1):133-136

Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA.

To assess whether titers of anti-rotavirus immunoglobulin G persist during the post-rotavirus vaccine era, the Pediatric Respiratory and Enteric Virus Acquisition and Immunogenesis Longitudinal (PREVAIL) Cohort analyzed serum samples collected from Cincinnati-area mothers and young infants in 2017-2018. Rotavirus-specific antibodies continue to be transferred from US mothers to their offspring in the post-rotavirus vaccine era, despite dramatic decreases in childhood rotavirus gastroenteritis.
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http://dx.doi.org/10.1093/infdis/jiaa715DOI Listing
July 2021
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