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Article

Neonatal Development in Prenatally Zika Virus-Exposed Infant Macaques with Dengue Immunity

by
Karla Ausderau
1,2,
Sabrina Kabakov
1,
Elaina Razo
3,
Ann M. Mitzey
4,
Kathryn M. Bach
1,
Chelsea M. Crooks
5,
Natalie Dulaney
1,
Logan Keding
4,
Cristhian Salas-Quinchucua
5,
Lex G. Medina-Magües
5,
Andrea M. Weiler
6,
Mason Bliss
6,
Jens Eickhoff
7,
Heather A. Simmons
6,
Andres Mejia
6,
Kathleen M. Antony
8,
Terry Morgan
9,
Saverio Capuano III
6,
Mary L. Schneider
1,
Matthew T. Aliota
10,
Thomas C. Friedrich
5,6,
David H. O’Connor
6,11,
Thaddeus G. Golos
4,6,8 and
Emma L. Mohr
3,*add Show full author list remove Hide full author list
1
Department of Kinesiology, Occupational Therapy Program, University of Wisconsin–Madison, Madison, WI 53706, USA
2
Waisman Center, University of Wisconsin–Madison, Madison, WI 53706, USA
3
Department of Pediatrics, School of Medicine and Public Health, University of Wisconsin–Madison, Madison, WI 53792, USA
4
Department of Comparative Biosciences, University of Wisconsin–Madison, Madison, WI 53706, USA
5
Department of Pathobiological Sciences, University of Wisconsin–Madison, Madison, WI 53706, USA
6
Wisconsin National Primate Research Center, University of Wisconsin–Madison, Madison, WI 53715, USA
7
Department of Biostatistics and Medical Informatics, University of Wisconsin–Madison, Madison, WI 53792, USA
8
Department of Obstetrics and Gynecology, University of Wisconsin–Madison, Madison, WI 53705, USA
9
Center for Developmental Health, Department of Obstetrics and Gynecology, Knight Cardiovascular Institute, Oregon Health & Science University, Portland, OR 97239, USA
10
Department of Veterinary and Biomedical Sciences, University of Minnesota, Minneapolis, MN 55108, USA
11
Department of Pathology and Laboratory Medicine, University of Wisconsin–Madison, Madison, WI 53705, USA
 
add Show full affiliation list
 
remove Hide full affiliation list
*
Author to whom correspondence should be addressed.
Viruses 2021, 13(9), 1878; https://doi.org/10.3390/v13091878
Submission received: 23 June 2021 / Revised: 14 September 2021 / Accepted: 15 September 2021 / Published: 20 September 2021
(This article belongs to the Special Issue Pediatric Viral Infection Long-Term Consequences)
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Abstract

Infants exposed to Zika virus (ZIKV) prenatally may develop birth defects, developmental deficits, or remain asymptomatic. It is unclear why some infants are more affected than others, although enhancement of maternal ZIKV infection via immunity to an antigenically similar virus, dengue virus (DENV), may play a role. We hypothesized that DENV immunity may worsen prenatal ZIKV infection and developmental deficits in offspring. We utilized a translational macaque model to examine how maternal DENV immunity influences ZIKV-exposed infant macaque neurodevelopment in the first month of life. We inoculated eight macaques with prior DENV infection with ZIKV, five macaques with ZIKV, and four macaques with saline. DENV/ZIKV-exposed infants had significantly worse visual orientation skills than ZIKV-exposed infants whose mothers were DENV-naive, with no differences in motor, sensory or state control development. ZIKV infection characteristics and pregnancy outcomes did not individually differ between dams with and without DENV immunity, but when multiple factors were combined in a multivariate model, maternal DENV immunity combined with ZIKV infection characteristics and pregnancy parameters predicted select developmental outcomes. We demonstrate that maternal DENV immunity exacerbates visual orientation and tracking deficits in ZIKV-exposed infant macaques, suggesting that human studies should evaluate how maternal DENV immunity impacts long-term neurodevelopment.
Keywords: macaque model; prenatal ZIKV exposure; neurodevelopment; maternal DENV infection macaque model; prenatal ZIKV exposure; neurodevelopment; maternal DENV infection

Share and Cite

MDPI and ACS Style

Ausderau, K.; Kabakov, S.; Razo, E.; Mitzey, A.M.; Bach, K.M.; Crooks, C.M.; Dulaney, N.; Keding, L.; Salas-Quinchucua, C.; Medina-Magües, L.G.; et al. Neonatal Development in Prenatally Zika Virus-Exposed Infant Macaques with Dengue Immunity. Viruses 2021, 13, 1878. https://doi.org/10.3390/v13091878

AMA Style

Ausderau K, Kabakov S, Razo E, Mitzey AM, Bach KM, Crooks CM, Dulaney N, Keding L, Salas-Quinchucua C, Medina-Magües LG, et al. Neonatal Development in Prenatally Zika Virus-Exposed Infant Macaques with Dengue Immunity. Viruses. 2021; 13(9):1878. https://doi.org/10.3390/v13091878

Chicago/Turabian Style

Ausderau, Karla, Sabrina Kabakov, Elaina Razo, Ann M. Mitzey, Kathryn M. Bach, Chelsea M. Crooks, Natalie Dulaney, Logan Keding, Cristhian Salas-Quinchucua, Lex G. Medina-Magües, and et al. 2021. "Neonatal Development in Prenatally Zika Virus-Exposed Infant Macaques with Dengue Immunity" Viruses 13, no. 9: 1878. https://doi.org/10.3390/v13091878

APA Style

Ausderau, K., Kabakov, S., Razo, E., Mitzey, A. M., Bach, K. M., Crooks, C. M., Dulaney, N., Keding, L., Salas-Quinchucua, C., Medina-Magües, L. G., Weiler, A. M., Bliss, M., Eickhoff, J., Simmons, H. A., Mejia, A., Antony, K. M., Morgan, T., Capuano, S., III, Schneider, M. L., ... Mohr, E. L. (2021). Neonatal Development in Prenatally Zika Virus-Exposed Infant Macaques with Dengue Immunity. Viruses, 13(9), 1878. https://doi.org/10.3390/v13091878

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