Neuropsychiatric outcomes in offspring after fetal exposure to maternal influenza infection during pregnancy: A systematic review

Fung, Stephen; Fakhraei, Romina; Condran, Georgia; Regan, Annette K.; Dimanlig-Cruz, Sheryll; Ricci, Christina; Foo, Damien; Sarna, Mohinder; Török, TorokEszter; Fell, Deshayne B.

doi:10.1016/j.reprotox.2022.09.002

Cited by 16 publications

(14 citation statements)

References 92 publications

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“…The association of virus infections during pregnancy and anomalies in the offspring's fetal neurodevelopment are widely studied, not only as a result of earlier impacts observed at birth, such as the microcephaly determined by Zika virus (ZIKV) infection (Guardado et al, 2022) but also because of the increased risk in neuropsychiatric outcomes in later stages of life (Fung et al, 2022). Despite the epidemiological and experimental studies showing the association between these apparently non‐related events (Ganguli & Chavali, 2021; Simões e Silva et al, 2016), the cellular and molecular mechanisms underlying these effects are still unclear.…”

Section: Discussionmentioning

confidence: 99%

Assessing the role of Ndel1 oligopeptidase activity in congenital Zika syndrome: Potential predictor of congenital syndrome endophenotype and treatment response

Christoff,

Nani,

Lessa

et al. 2023

Journal of Neurochemistry

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Maternal infections are among the main risk factors for cognitive impairments in the offspring. Zika virus (ZIKV) can be transmitted vertically, causing a set of heterogeneous birth defects, such as microcephaly, ventriculomegaly and corpus callosum dysgenesis. Nuclear distribution element like‐1 (Ndel1) oligopeptidase controls crucial aspects of cerebral cortex development underlying cortical malformations. Here, we examine Ndel1 activity in an animal model for ZIKV infection, which was associated with deregulated corticogenesis. We observed here a reduction in Ndel1 activity in the forebrain associated with the congenital syndrome induced by ZIKV isolates, in an in utero and postnatal injections of different inoculum doses in mice models. In addition, we observed a strong correlation between Ndel1 activity and brain size of animals infected by ZIKV, suggesting the potential of this measure as a biomarker for microcephaly. More importantly, the increase of interferon (IFN)‐beta signaling, which was used to rescue the ZIKV infection outcomes, also recovered Ndel1 activity to levels similar to those of uninfected healthy control mice, but with no influence on Ndel1 activity in uninfected healthy control animals. Taken together, we demonstrate for the first time here an association of corticogenesis impairments determined by ZIKV infection and the modulation of Ndel1 activity. Although further studies are still necessary to clarify the possible role(s) of Ndel1 activity in the molecular mechanism(s) underlying the congenital syndrome induced by ZIKV, we suggest here the potential of monitoring the Ndel1 activity to predict this pathological condition at early stages of embryos or offspring development, during while the currently employed methods are unable to detect impaired corticogenesis leading to microcephaly. Ndel1 activity may also be possibly used to follow up the positive response to the treatment, such as that employing the IFN‐beta that is able to rescue the ZIKV‐induced brain injury.image

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Section: Discussionmentioning

confidence: 99%

Assessing the role of Ndel1 oligopeptidase activity in congenital Zika syndrome: Potential predictor of congenital syndrome endophenotype and treatment response

Christoff,

Nani,

Lessa

et al. 2023

Journal of Neurochemistry

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“…These data were confirmed by a recent systematic review conducted by Fung and colleagues, which confirmed an increased risk for schizophrenia and other primary psychotic disorders in children exposed to maternal Influenza infection during pregnancy, especially during the first and second trimesters. Moreover, the authors reported an increased risk of developing ASD in offspring exposed to maternal Influenza infection throughout the whole gestation ( Fung et al, 2022 ).…”

Section: The Impact Of Prenatal Influenza Infection On Neuropsychiatr...mentioning

confidence: 99%

Impact of respiratory viral infections during pregnancy on the neurological outcomes of the newborn: current knowledge

Manti,

Spoto,

Nicotera

et al. 2024

Front. Neurosci.

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Brain development is a complex process that begins during pregnancy, and the events occurring during this sensitive period can affect the offspring’s neurodevelopmental outcomes. Respiratory viral infections are frequently reported in pregnant women, and, in the last few decades, they have been related to numerous neuropsychiatric sequelae. Respiratory viruses can disrupt brain development by directly invading the fetal circulation through vertical transmission or inducing neuroinflammation through the maternal immune activation and production of inflammatory cytokines. Influenza virus gestational infection has been consistently associated with psychotic disorders, such as schizophrenia and autism spectrum disorder, while the recent pandemic raised some concerns regarding the effects of severe acute respiratory syndrome coronavirus 2 on neurodevelopmental outcomes of children born to affected mothers. In addition, emerging evidence supports the possible role of respiratory syncytial virus infection as a risk factor for adverse neuropsychiatric consequences. Understanding the mechanisms underlying developmental dysfunction allows for improving preventive strategies, early diagnosis, and prompt interventions.

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“…We hypothesized that the placental gene expression response was contingent on one or more circulating cytokines/chemokines secreted by the maternal lungs in response to LPS 41 . Therefore, we measured concentrations of 11 cyto-and chemokines (Ccl2, 4,7,11,17,20,24,Cxcl1,13,16 and Il6) in maternal plasma at all time points using the Luminex platform. We compared maternal plasma protein abundance changes (LPS vs.…”

Section: Circulating Il6 Is a Candidate For Inducing Placental Immune...mentioning

confidence: 99%

“…Less is known about short-term placental and fetal manifestations of MIA when the immunogen is targeted to the lungs, as in respiratory infections and maternal airway inflammation [14][15][16][17][18][19][20] , which are common during pregnancy: 49.6% of control mothers in the National Birth Defects Prevention Study reported respiratory infections during pregnancy 21,22 .…”

Section: Introductionmentioning

confidence: 99%

Pulmonary maternal immune activation does not extend through the placenta but leads to fetal metabolic adaptation

Hansen

Krautz

Rago

et al. 2023

Preprint

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Maternal immune system activation (MIA) during pregnancy can disrupt the fetal environment, causing postnatal susceptibility to disorders. How the placenta and the fetus respond to acute MIA over time is unknown. Here, we characterized the response to acute maternal pulmonary inflammation across time in maternal and fetal organs using multi-omics. Unlike maternal organs which mounted strong innate immune responses, the placenta upregulated tissue-integrity genes, likely to prevent fetal exposure to infections, and downregulated growth-associated genes. Subsequently, the placenta upregulated biosynthesis and endoplasmic reticulum stress genes in order to return to homeostasis. These responses likely protected the fetus, since we observed no immune response in fetal liver. Instead, likely due to nutrient depletion, the fetal liver displayed metabolic adaptations, including increases in lipids containing docosahexaenoic acid, crucial for fetal brain development. Our study shows, for the first time, the integrated temporal response to pulmonary MIA across maternal and fetal organs.

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Neuropsychiatric outcomes in offspring after fetal exposure to maternal influenza infection during pregnancy: A systematic review

Cited by 16 publications

References 92 publications

Assessing the role of Ndel1 oligopeptidase activity in congenital Zika syndrome: Potential predictor of congenital syndrome endophenotype and treatment response

Assessing the role of Ndel1 oligopeptidase activity in congenital Zika syndrome: Potential predictor of congenital syndrome endophenotype and treatment response

Impact of respiratory viral infections during pregnancy on the neurological outcomes of the newborn: current knowledge

Pulmonary maternal immune activation does not extend through the placenta but leads to fetal metabolic adaptation

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