Highly efficient maternal-fetal Zika virus transmission in pregnant rhesus macaques

Sydney M. Nguyen, Kathleen M. Antony, Dawn M. Dudley, Sarah Kohn, Heather A. Simmons, Bryce Wolfe, M. Shahriar Salamat, Leandro B.C. Teixeira, Gregory J. Wiepz, Troy H. Thoong, Matthew T. Aliota, Andrea M. Weiler, Gabrielle L. Barry, Kim L. Weisgrau, Logan J. Vosler, Mariel S. Mohns, Meghan E. Breitbach, Laurel M. Stewart, Mustafa N. Rasheed, Christina M. NewmanMichael E. Graham, Oliver E. Wieben, Patrick A. Turski, Kevin M. Johnson, Jennifer Post, Jennifer M. Hayes, Nancy Schultz-Darken, Michele L. Schotzko, Josh A. Eudailey, Sallie R. Permar, Eva G. Rakasz, Emma L. Mohr, Saverio Capuano, Alice F Tarantal, Jorge E. Osorio, Shelby L. O’Connor, Thomas C. Friedrich, David H. O’Connor, Thaddeus G. Golos

Research output: Contribution to journalArticle

79 Citations (Scopus)

Abstract

Infection with Zika virus (ZIKV) is associated with human congenital fetal anomalies. To model fetal outcomes in nonhuman primates, we administered Asian-lineage ZIKV subcutaneously to four pregnant rhesus macaques. While non-pregnant animals in a previous study contemporary with the current report clear viremia within 10–12 days, maternal viremia was prolonged in 3 of 4 pregnancies. Fetal head growth velocity in the last month of gestation determined by ultrasound assessment of head circumference was decreased in comparison with biparietal diameter and femur length within each fetus, both within normal range. ZIKV RNA was detected in tissues from all four fetuses at term cesarean section. In all pregnancies, neutrophilic infiltration was present at the maternal-fetal interface (decidua, placenta, fetal membranes), in various fetal tissues, and in fetal retina, choroid, and optic nerve (first trimester infection only). Consistent vertical transmission in this primate model may provide a platform to assess risk factors and test therapeutic interventions for interruption of fetal infection. The results may also suggest that maternal-fetal ZIKV transmission in human pregnancy may be more frequent than currently appreciated.

Original languageEnglish (US)
Article numbere1006378
JournalPLoS Pathogens
Volume13
Issue number5
DOIs
StatePublished - May 1 2017

Fingerprint

Macaca mulatta
Mothers
Pregnancy
Fetus
Viremia
Primates
Head
Extraembryonic Membranes
Decidua
Choroid
First Pregnancy Trimester
Optic Nerve
Fetal Development
Infection
Cesarean Section
Femur
Placenta
Retina
Reference Values
RNA

ASJC Scopus subject areas

  • Parasitology
  • Microbiology
  • Immunology
  • Molecular Biology
  • Genetics
  • Virology

Cite this

Nguyen, S. M., Antony, K. M., Dudley, D. M., Kohn, S., Simmons, H. A., Wolfe, B., ... Golos, T. G. (2017). Highly efficient maternal-fetal Zika virus transmission in pregnant rhesus macaques. PLoS Pathogens, 13(5), [e1006378]. https://doi.org/10.1371/journal.ppat.1006378

Highly efficient maternal-fetal Zika virus transmission in pregnant rhesus macaques. / Nguyen, Sydney M.; Antony, Kathleen M.; Dudley, Dawn M.; Kohn, Sarah; Simmons, Heather A.; Wolfe, Bryce; Salamat, M. Shahriar; Teixeira, Leandro B.C.; Wiepz, Gregory J.; Thoong, Troy H.; Aliota, Matthew T.; Weiler, Andrea M.; Barry, Gabrielle L.; Weisgrau, Kim L.; Vosler, Logan J.; Mohns, Mariel S.; Breitbach, Meghan E.; Stewart, Laurel M.; Rasheed, Mustafa N.; Newman, Christina M.; Graham, Michael E.; Wieben, Oliver E.; Turski, Patrick A.; Johnson, Kevin M.; Post, Jennifer; Hayes, Jennifer M.; Schultz-Darken, Nancy; Schotzko, Michele L.; Eudailey, Josh A.; Permar, Sallie R.; Rakasz, Eva G.; Mohr, Emma L.; Capuano, Saverio; Tarantal, Alice F; Osorio, Jorge E.; O’Connor, Shelby L.; Friedrich, Thomas C.; O’Connor, David H.; Golos, Thaddeus G.

In: PLoS Pathogens, Vol. 13, No. 5, e1006378, 01.05.2017.

Research output: Contribution to journalArticle

Nguyen, SM, Antony, KM, Dudley, DM, Kohn, S, Simmons, HA, Wolfe, B, Salamat, MS, Teixeira, LBC, Wiepz, GJ, Thoong, TH, Aliota, MT, Weiler, AM, Barry, GL, Weisgrau, KL, Vosler, LJ, Mohns, MS, Breitbach, ME, Stewart, LM, Rasheed, MN, Newman, CM, Graham, ME, Wieben, OE, Turski, PA, Johnson, KM, Post, J, Hayes, JM, Schultz-Darken, N, Schotzko, ML, Eudailey, JA, Permar, SR, Rakasz, EG, Mohr, EL, Capuano, S, Tarantal, AF, Osorio, JE, O’Connor, SL, Friedrich, TC, O’Connor, DH & Golos, TG 2017, 'Highly efficient maternal-fetal Zika virus transmission in pregnant rhesus macaques', PLoS Pathogens, vol. 13, no. 5, e1006378. https://doi.org/10.1371/journal.ppat.1006378
Nguyen SM, Antony KM, Dudley DM, Kohn S, Simmons HA, Wolfe B et al. Highly efficient maternal-fetal Zika virus transmission in pregnant rhesus macaques. PLoS Pathogens. 2017 May 1;13(5). e1006378. https://doi.org/10.1371/journal.ppat.1006378
Nguyen, Sydney M. ; Antony, Kathleen M. ; Dudley, Dawn M. ; Kohn, Sarah ; Simmons, Heather A. ; Wolfe, Bryce ; Salamat, M. Shahriar ; Teixeira, Leandro B.C. ; Wiepz, Gregory J. ; Thoong, Troy H. ; Aliota, Matthew T. ; Weiler, Andrea M. ; Barry, Gabrielle L. ; Weisgrau, Kim L. ; Vosler, Logan J. ; Mohns, Mariel S. ; Breitbach, Meghan E. ; Stewart, Laurel M. ; Rasheed, Mustafa N. ; Newman, Christina M. ; Graham, Michael E. ; Wieben, Oliver E. ; Turski, Patrick A. ; Johnson, Kevin M. ; Post, Jennifer ; Hayes, Jennifer M. ; Schultz-Darken, Nancy ; Schotzko, Michele L. ; Eudailey, Josh A. ; Permar, Sallie R. ; Rakasz, Eva G. ; Mohr, Emma L. ; Capuano, Saverio ; Tarantal, Alice F ; Osorio, Jorge E. ; O’Connor, Shelby L. ; Friedrich, Thomas C. ; O’Connor, David H. ; Golos, Thaddeus G. / Highly efficient maternal-fetal Zika virus transmission in pregnant rhesus macaques. In: PLoS Pathogens. 2017 ; Vol. 13, No. 5.
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AU - Antony, Kathleen M.

AU - Dudley, Dawn M.

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AU - Simmons, Heather A.

AU - Wolfe, Bryce

AU - Salamat, M. Shahriar

AU - Teixeira, Leandro B.C.

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AU - Thoong, Troy H.

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AU - Mohns, Mariel S.

AU - Breitbach, Meghan E.

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AU - Rasheed, Mustafa N.

AU - Newman, Christina M.

AU - Graham, Michael E.

AU - Wieben, Oliver E.

AU - Turski, Patrick A.

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AU - Hayes, Jennifer M.

AU - Schultz-Darken, Nancy

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AU - Rakasz, Eva G.

AU - Mohr, Emma L.

AU - Capuano, Saverio

AU - Tarantal, Alice F

AU - Osorio, Jorge E.

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