ArticleNature medicine2018
Congenital Zika virus infection as a silent pathology with loss of neurogenic output in the fetal brain.
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Article in Nature medicine, 2018. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 107 papers, 1 of them a synthesis that pooled it.
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107citing papers in PubMed, 1 pooled it
20.0field-weighted citation impact, top 1% of its field
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Who cites it
107 citing papers in PubMed, 1 synthesis or guideline pooled it, 164 citations in OpenAlex.
- Differential impact of COVID-19 in pregnant women from high-income countries and low- to middle-income countries: A systematic review and meta-analysis.International journal of gynaecology and obstetrics: the official organ of the International Federation of Gynaecology and Obstetrics · 2021Pooled it
- Influenza A virus infection induces immune dysregulation in the placenta and fetus without vertical transmission in nonhuman primates.Science advances · 2026Article
- A single-cell transcriptomic atlas of the pigtail macaque placenta in late gestation.BMC genomics · 2026Article
- NOD2 activation reprograms infiltrating inflammatory monocytes in the Zika virus infected CNS to maintain neural correlates of learning and memory.bioRxiv : the preprint server for biology · 2026Article
- Neural cells are susceptible to historic and recently emerged Oropouche virus strains.PLoS pathogens · 2026Article
- A single-cell transcriptomic atlas of the periventricular proliferative zone in the late gestation fetal brain in the pigtail macaque.Frontiers in neuroscience · 2026Article
- Zika virus and the fetal-maternal interface: deciphering the mechanisms of placental infection and implications for pregnancy outcomes.Emerging microbes & infections · 2025Review
- Evaluating potential associations between prior maternal yellow fever vaccination and protection against infant adverse outcomes following Zika virus antenatal exposure.International journal of epidemiology · 2025Article
- Modeling Virus-Associated Central Nervous System Disease in Non-Human Primates.International journal of molecular sciences · 2025Review
- The human neural cell atlas of Zika virus infection in developing brain tissue.Cell reports. Medicine · 2025Article
- Role of non-human primate models in accelerating research and developing countermeasures against Zika virus infection.The Lancet. Microbe · 2025Review
- Article
- Article
- Granular cytoplasmic inclusions in astrocytes and microglial activation in the fetal brain of pigtail macaques in response to maternal viral infection.Acta neuropathologica communications · 2025Article
- Early and Long-Term Adverse Outcomes of In Utero Zika Exposure.Pediatrics · 2025Article
- Zika virus encephalitis causes transient reduction of functional cortical connectivity.Neurophotonics · 2025Article
- Animal Models, Therapeutics, and Vaccine Approaches to Emerging and Re-Emerging Flaviviruses.Viruses · 2024Review
- Emerging and reemerging infectious diseases: global trends and new strategies for their prevention and control.Signal transduction and targeted therapy · 2024Review
- Ad26.M.Env ZIKV vaccine protects pregnant rhesus macaques and fetuses against Zika virus infection.NPJ vaccines · 2024Article
- Transcriptomic Signatures of Zika Virus Infection in Patients and a Cell Culture Model.Microorganisms · 2024Article
47 more citing papers are in PubMed but not listed here.
Corrections and comments
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Authors and funding
42 authors at 6 institutions in 2 countries.
Kristina M Adams WaldorfDepartment of Obstetrics & Gynecology, University of Washington, Seattle, Washington, USA.ORCID 0000-0002-6939-7224
Branden R NelsonCenter for Integrative Brain Research, Seattle Children's Research Institute, Seattle, Washington, USA.
Jennifer E Stencel-BaerenwaldCenter for Innate Immunity and Immune Disease, University of Washington, Seattle, Washington, USA.
Colin StudholmeDepartment of Pediatrics, University of Washington, Seattle, Washington, USA.
Raj P KapurDepartment of Pathology, University of Washington, Seattle, Washington, USA.
Blair ArmisteadDepartment of Global Health, University of Washington, Seattle, Washington, USA.
Christie L WalkerDepartment of Obstetrics & Gynecology, University of Washington, Seattle, Washington, USA.
Sean MerillatCenter for Global Infectious Disease Research, Seattle Children's Research Institute, Seattle, Washington, USA.
Jay VornhagenDepartment of Global Health, University of Washington, Seattle, Washington, USA.ORCID 0000-0002-1685-302X
Jennifer Tisoncik-GoCenter for Innate Immunity and Immune Disease, University of Washington, Seattle, Washington, USA.
Audrey BaldessariWashington National Primate Research Center, Seattle, Washington, USA.
Michelle ColemanDepartment of Pediatrics, University of Washington, Seattle, Washington, USA.
Manjiri K DigheDepartment of Radiology, University of Washington, Seattle, Washington, USA.
Dennis W W ShawDepartment of Radiology, University of Washington, Seattle, Washington, USA.
Justin A RobyCenter for Innate Immunity and Immune Disease, University of Washington, Seattle, Washington, USA.
Veronica Santana-UfretCenter for Global Infectious Disease Research, Seattle Children's Research Institute, Seattle, Washington, USA.
Erica BoldenowDepartment of Pediatrics, University of Washington, Seattle, Washington, USA.
Junwei LiDepartment of Bioengineering, University of Washington, Seattle, Washington, USA.
Xiaohu GaoDepartment of Bioengineering, University of Washington, Seattle, Washington, USA.
Michael A DavisCenter for Innate Immunity and Immune Disease, University of Washington, Seattle, Washington, USA.
Jesica A SwanstromDepartment of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA.
Kara JensenDepartment of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA.
Douglas G WidmanDepartment of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA.
Ralph S BaricDepartment of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA.
Joseph T MedwidDepartment of Biology, New Mexico State University, Las Cruces, New Mexico, USA.
Kathryn A HanleyDepartment of Biology, New Mexico State University, Las Cruces, New Mexico, USA.
Jason OgleWashington National Primate Research Center, Seattle, Washington, USA.
G Michael GoughWashington National Primate Research Center, Seattle, Washington, USA.
Wonsok LeeWashington National Primate Research Center, Seattle, Washington, USA.
Chris EnglishWashington National Primate Research Center, Seattle, Washington, USA.
W McIntyre DurningWashington National Primate Research Center, Seattle, Washington, USA.
Jeff ThielDepartment of Radiology, University of Washington, Seattle, Washington, USA.ORCID 0000-0002-4228-7121
Chris GatenbyDepartment of Radiology, University of Washington, Seattle, Washington, USA.
Elyse C DeweyCenter for Innate Immunity and Immune Disease, University of Washington, Seattle, Washington, USA.
Marian R FairgrieveCenter for Innate Immunity and Immune Disease, University of Washington, Seattle, Washington, USA.
Rebecca D HodgeAllen Institute for Brain Science, Seattle, Washington, USA.
Richard F GrantWashington National Primate Research Center, Seattle, Washington, USA.
LaRene KullerWashington National Primate Research Center, Seattle, Washington, USA.
William B DobynsCenter for Integrative Brain Research, Seattle Children's Research Institute, Seattle, Washington, USA.
Robert F HevnerCenter for Integrative Brain Research, Seattle Children's Research Institute, Seattle, Washington, USA.
Michael GaleCenter for Innate Immunity and Immune Disease, University of Washington, Seattle, Washington, USA.
Lakshmi RajagopalCenter for Innate Immunity and Immune Disease, University of Washington, Seattle, Washington, USA.
University of Washington · USInfectious Disease Research Institute · USUniversity of North Carolina at Chapel Hill · USNew Mexico State University · USSeattle Children's Hospital · USAllen Institute for Brain Science · US
Funding
Washington National Primate Research CenterP51OD010425 · OD · UNIVERSITY OF WASHINGTON · PI Mari Ostendorf · 2012 to 2026
$201.8MUnlocking Zika Virus Immune Control and Pathogenesis with the Collaborative CrossU19AI100625 · NIAID · UNIV OF NORTH CAROLINA CHAPEL HILL · PI HEISE, MARK T · 2012 to 2021
$36.6MWaNPRC Macaca nemestrina SPF Breeding ColonyU42OD011123 · OD · UNIVERSITY OF WASHINGTON · PI Melissa R Berg, Cindy Buckmaster · 2012 to 2026
$34.4MWest Nile Virus and host control of innate defensesU19AI083019 · NIAID · UNIVERSITY OF WASHINGTON · PI CLARK, EDWARD A · 2009 to 2018
$22.5MIntellectual and Developmental Disabilities Research CenterU54HD083091 · NICHD · UNIVERSITY OF WASHINGTON · PI DOHERTY, DANIEL · 2014 to 2019
$7.9MACADEMIC PEDIATRIC INFECTIOUS DISEASET32HD007233 · NICHD · SEATTLE CHILDREN'S HOSPITAL · PI KEVIN B URDAHL · 1985 to 2026
$6.7MDiseases of Public Health Importance Training GrantT32AI007509 · NIAID · UNIVERSITY OF WASHINGTON · PI LUND, JENNIFER M · 1997 to 2024
$6.3MMolecular Basis of Flavivirus Cross-Neutralization by Human AntibodiesR01AI107731 · NIAID · UNIV OF NORTH CAROLINA CHAPEL HILL · PI DESILVA, ARAVINDA M. · 2013 to 2022
$5.3MMotion Robust Mapping of Human Brain Microstructure and Macrostructure In-UteroR01NS055064 · NINDS · UNIVERSITY OF WASHINGTON · PI STUDHOLME, COLIN · 2006 to 2017
$4.1MGBS mediated in utero fetal injuryR01AI100989 · NIAID · SEATTLE CHILDREN'S HOSPITAL · PI ADAMS WALDORF, KRISTINA M., RAJAGOPAL, LAKSHMI · 2012 to 2016
$3.9MInnate Immune Control of West Nile VirusR01AI104002 · NIAID · UNIVERSITY OF WASHINGTON · PI DIAMOND, MICHAEL S, GALE, MICHAEL · 2013 to 2017
$3.7MMotion Robust Mapping of Human Brain Functional Connectivity Changes in UteroR01EB017133 · NIBIB · UNIVERSITY OF WASHINGTON · PI STUDHOLME, COLIN · 2013 to 2016
$2.5MNEI NIH HHS F32 EY015631NEI NIH HHS L40 EY016882NIAID NIH HHS R01 AI100989NIAID NIH HHS R01 AI104002NIAID NIH HHS R01 AI107731NIAID NIH HHS T32 AI007509NIAID NIH HHS U19 AI083019NIAID NIH HHS U19 AI100625NIBIB NIH HHS R01 EB017133NICHD NIH HHS T32 HD007233NICHD NIH HHS U54 HD083091NIH HHS P51 OD010425NIH HHS R21 OD023838NIH HHS U42 OD011123NINDS NIH HHS R01 NS055064NINDS NIH HHS R01 NS085081NINDS NIH HHS R01 NS092339
Abstract
Zika virus (ZIKV) is a flavivirus with teratogenic effects on fetal brain, but the spectrum of ZIKV-induced brain injury is unknown, particularly when ultrasound imaging is normal. In a pregnant pigtail macaque (Macaca nemestrina) model of ZIKV infection, we demonstrate that ZIKV-induced injury to fetal brain is substantial, even in the absence of microcephaly, and may be challenging to detect in a clinical setting. A common and subtle injury pattern was identified, including (i) periventricular T2-hyperintense foci and loss of fetal noncortical brain volume, (ii) injury to the ependymal epithelium with underlying gliosis and (iii) loss of late fetal neuronal progenitor cells in the subventricular zone (temporal cortex) and subgranular zone (dentate gyrus, hippocampus) with dysmorphic granule neuron patterning. Attenuation of fetal neurogenic output demonstrates potentially considerable teratogenic effects of congenital ZIKV infection even without microcephaly. Our findings suggest that all children exposed to ZIKV in utero should receive long-term monitoring for neurocognitive deficits, regardless of head size at birth.
Indexed as
AnimalsDisease Models, AnimalFemaleFetusHumansMacaca nemestrinaMicrocephalyNeurogenesisPregnancyPregnancy Complications, InfectiousZika VirusZika Virus Infection
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