Zika virus infection in pregnant rhesus macaques causes placental dysfunction and immunopathology

Alec J. Hirsch (), Victoria H. J. Roberts, Peta L. Grigsby, Nicole Haese, Matthias C. Schabel, Xiaojie Wang, Jamie O. Lo, Zheng Liu, Christopher D. Kroenke, Jessica L. Smith, Meredith Kelleher, Rebecca Broeckel, Craig N. Kreklywich, Christopher J. Parkins, Michael Denton, Patricia Smith, Victor DeFilippis, William Messer, Jay A. Nelson, Jon D. Hennebold, Marjorie Grafe, Lois Colgin, Anne Lewis, Rebecca Ducore, Tonya Swanson, Alfred W. Legasse, Michael K. Axthelm, Rhonda MacAllister, Ashlee V. Moses, Terry K. Morgan, Antonio E. Frias () and Daniel N. Streblow ()
Additional contact information
Alec J. Hirsch: Oregon Health and Science University (OHSU)
Victoria H. J. Roberts: ONPRC
Peta L. Grigsby: ONPRC
Nicole Haese: Oregon Health and Science University (OHSU)
Matthias C. Schabel: OHSU
Xiaojie Wang: OHSU
Jamie O. Lo: OHSU
Zheng Liu: OHSU
Christopher D. Kroenke: OHSU
Jessica L. Smith: Oregon Health and Science University (OHSU)
Meredith Kelleher: ONPRC
Rebecca Broeckel: Oregon Health and Science University (OHSU)
Craig N. Kreklywich: Oregon Health and Science University (OHSU)
Christopher J. Parkins: Oregon Health and Science University (OHSU)
Michael Denton: Oregon Health and Science University (OHSU)
Patricia Smith: Oregon Health and Science University (OHSU)
Victor DeFilippis: Oregon Health and Science University (OHSU)
William Messer: OHSU
Jay A. Nelson: Oregon Health and Science University (OHSU)
Jon D. Hennebold: ONPRC
Marjorie Grafe: OHSU
Lois Colgin: ONPRC
Anne Lewis: ONPRC
Rebecca Ducore: ONPRC
Tonya Swanson: Oregon National Primate Research Center (ONPRC)
Alfred W. Legasse: Oregon National Primate Research Center (ONPRC)
Michael K. Axthelm: Oregon National Primate Research Center (ONPRC)
Rhonda MacAllister: ONPRC
Ashlee V. Moses: Oregon Health and Science University (OHSU)
Terry K. Morgan: OHSU
Antonio E. Frias: ONPRC
Daniel N. Streblow: Oregon Health and Science University (OHSU)

Nature Communications, 2018, vol. 9, issue 1, 1-15

Abstract: Abstract Zika virus (ZIKV) infection during pregnancy leads to an increased risk of fetal growth restriction and fetal central nervous system malformations, which are outcomes broadly referred to as the Congenital Zika Syndrome (CZS). Here we infect pregnant rhesus macaques and investigate the impact of persistent ZIKV infection on uteroplacental pathology, blood flow, and fetal growth and development. Despite seemingly normal fetal growth and persistent fetal-placenta-maternal infection, advanced non-invasive in vivo imaging studies reveal dramatic effects on placental oxygen reserve accompanied by significantly decreased oxygen permeability of the placental villi. The observation of abnormal oxygen transport within the placenta appears to be a consequence of uterine vasculitis and placental villous damage in ZIKV cases. In addition, we demonstrate a robust maternal-placental-fetal inflammatory response following ZIKV infection. This animal model reveals a potential relationship between ZIKV infection and uteroplacental pathology that appears to affect oxygen delivery to the fetus during development.

Date: 2018
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DOI: 10.1038/s41467-017-02499-9

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