Maternal influenza infection during pregnancy impacts postnatal brain development in the rhesus monkey
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Background Maternal infection with influenza and other pathogens during pregnancy has been associated with increased risk for schizophrenia and neurodevelopmental disorders. In rodent studies, maternal inflammatory responses to influenza affect fetal brain development. However, to verify the relevance of these findings to humans, research is needed in a primate species with more advanced prenatal corticogenesis.Methods Twelve pregnant rhesus monkeys were infected with influenza, A/Sydney/5/97 (H3N2), 1 month before term (early third trimester) and compared with 7 control pregnancies. Nasal swabs and blood samples confirmed viral shedding and immune activation. Structural magnetic resonance imaging was conducted at 1 year; behavioral development and cortisol reactivity were also assessed.Results Maternal infections were mild and self-limiting. At birth, maternally derived influenza-specific immunoglobulin G was present in the neonate, but there was no evidence of direct viral exposure. Birth weight and gestation length were not affected, nor were infant neuromotor, behavioral, and endocrine responses. However, magnetic resonance imaging analyses revealed significant reductions in cortical gray matter in flu-exposed animals. Regional analyses indicated the largest gray matter reductions occurred bilaterally in cingulate and parietal areas; white matter was also reduced significantly in the parietal lobe.Conclusions Influenza infection during pregnancy affects neural development in the monkey, reducing gray matter throughout most of the cortex and decreasing white matter in parietal cortex. These brain alterations are likely to be permanent, given that they were still present at the monkey-equivalent of older childhood and thus might increase the likelihood of later behavioral pathology.
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Rhesus monkeys whose mothers were infected with influenza during pregnancy had reduced cortical gray matter.
“a reduction in cortical gray matter was noted in rhesus monkeys whose mothers were infected with influenza during pregnancy (Short et al., 2010).”
From Neuroinflammation as a risk factor for attention deficit hyperactivity disorder (2019) · cites this paper as Short et al., 2010
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Self-citationMaternal immune activation in nonhuman primates alters social attention in juvenile offspring
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Maternal prenatal infection and anxiety predict neurodevelopmental outcomes in middle childhood
O'Connor, T. G., Ciesla, A. A., Sefair, A. V., Thornburg, L. L., Brown, A. S., Glover, V., & O'Donnell, K. J. (2022) · Journal of Psychopathology and Clinical Science · doi:10.1037/abn0000746 · Cited by 31 · see citing works
- Authors
- Short, S. J., Lubach, G. R., Karasin, A. I., Olsen, C. W., Styner, M., Knickmeyer, R. C., Gilmore, J. H., & Coe, C. L.
- Affiliations
- University of Wisconsin–Madison (US)
- University of North Carolina at Chapel Hill (US)
- Corresponding author
- Short, Sarah J.
- ORCID
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2010-05
- Volume
- 67
- Issue
- 10
- Pages
- 965-973
- ISSN
- 0006-3223 (ISSN-L)
- PMC
- PMC3235476
- OpenAlex
- W2037555832
- Cited by
- 202
- References
- 86
- Citations by year
- 2026: 11 · 2025: 4 · 2024: 19 · 2023: 10 · 2022: 14 · 2021: 17 · 2020: 18 · 2019: 9 · 2018: 18 · 2017: 6 · 2016: 12 · 2015: 8 · 2014: 8 · 2013: 11 · 2012: 14
- FWCI
- 5.28
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- UNC Libraries
- Funders
- National Institute of Allergy and Infectious Diseases (AI067518)
- National Institute of Mental Health (F31 MH076606)
- National Institute of Child Health and Human Development (HD383386)
- University of North Carolina Conte Center for Schizophrenia Research (MH 064065)
- University of North Carolina Neurodevelopmental Disorders Research Center (HD 03110)
- Topics
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
- Keywords
- maternal influenza infection, pregnancy, postnatal brain development, rhesus monkeys, white matter reduction, parietal cortex, cingulate cortex, maternal-fetal immune transfer, influenza H3N2, schizophrenia risk, neurodevelopmental disorders, cortisol response, birth weight
- MeSH terms
- Animals, Animals, Newborn, Brain, Female, Hydrocortisone, Macaca mulatta, Male, Orthomyxoviridae Infections, Pregnancy, Pregnancy Complications, Infectious, Pregnancy, Animal, Prenatal Exposure Delayed Effects, Influenza A Virus, H3N2 Subtype
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