Prenatal Maternal Stress Causes Preterm Birth and Affects Neonatal Adaptive Immunity in Mice

Garcia‐Flores, Valeria; Romero, Roberto; Furcron, Amy-Eunice; Levenson, Dustyn; Galaz, José; Zou, Chengrui; Hassan, Sonia S.; Hsu, Chaur‐Dong; Olson, David M.; Metz, Gerlinde A. S.; Gomez‐Lopez, Nardhy

doi:10.3389/fimmu.2020.00254

Cited by 30 publications

(33 citation statements)

References 96 publications

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“…This rise may be due to a compensatory mechanism in response to the adverse/extended intrauterine environment [84,85], which is reflected by the appropriate weight gain in infants at 3 weeks of age. A similar compensatory mechanism has also been observed in infants born to mothers who experienced chronic prenatal stress [170]. Nevertheless, the immunocompetence of pups born to dams of advanced age remains to be elucidated.…”

Section: Discussionmentioning

confidence: 57%

The effects of advanced maternal age on T-cell subsets at the maternal–fetal interface prior to term labor and in the offspring: a mouse study

Levenson

Romero

Garcia‐Flores

et al. 2020

Clinical and Experimental Immunology

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Summary Women who conceive at 35 years of age or older, commonly known as advanced maternal age, have a higher risk of facing parturition complications and their children have an increased risk of developing diseases later in life. However, the immunological mechanisms underlying these pathological processes have yet to be established. To fill this gap in knowledge, using a murine model and immunophenotyping, we determined the effect of advanced maternal age on the main cellular branch of adaptive immunity, T cells, at the maternal–fetal interface and in the offspring. We report that advanced maternal age impaired the process of labor at term, inducing dystocia and delaying the timing of delivery. Advanced maternal age diminished the number of specific proinflammatory T‐cell subsets [T helper type 1 (Th1): CD4+IFN‐γ+, CD8+IFN‐γ+ and Th9: CD4+IL‐9+], as well as CD4+ regulatory T cells (CD4+CD25+FoxP3+ T cells), at the maternal–fetal interface prior to term labor. Advanced maternal age also altered fetal growth and survival of the offspring in early life. In addition, infants born to advanced‐age mothers had alterations in the T‐cell repertoire but not in CD71+ erythroid cells (CD3−CD71+TER119+ cells). This study provides insight into the immune alterations observed at the maternal–fetal interface of advanced‐age mothers and their offspring.

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Section: Discussionmentioning

confidence: 57%

The effects of advanced maternal age on T-cell subsets at the maternal–fetal interface prior to term labor and in the offspring: a mouse study

Levenson

Romero

Garcia‐Flores

et al. 2020

Clinical and Experimental Immunology

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“…These changes, in turn, may have modulated the immune system response that plays an active role in preterm labor initiation. [40][41][42] With additional consideration to unemployment, the financial stress associated with loss of income for those unemployed during the pandemic was partially offset by the unprecedented income support and eviction moratoria by the federal government as part of the pandemic response. As a result, pandemic-associated unemployment was, for some, a less financially stressful experience than unemployment might have been under standard circumstances.…”

Section: Discussionmentioning

confidence: 99%

Neighborhood deprivation and preterm delivery during the coronavirus 2019 pandemic

Fisher¹,

Sakowicz²,

Barnard³

et al. 2022

American Journal of Obstetrics & Gynecology MFM

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Background Prior studies have reported decreases in preterm delivery (PTD) incidence during the coronavirus 2019 (COVID-19) pandemic, however findings are inconsistent. Given wide disparities in the pandemic's impact across communities, neighborhood deprivation may explain observed variation in the relationship between the COVID-19 pandemic and preterm delivery. Objective To characterize changes in the incidence of PTD during the COVID-19 pandemic with attention to effect modification introduced by neighborhood hardship. Study Design This retrospective cohort study included all pregnant patients who delivered at an urban tertiary care hospital during the pandemic (April-November 2020) or pre-pandemic (April-November 2019). We compared the incidence of PTD, spontaneous PTD, and medically indicated PTD prior to 37 weeks’ gestation across epochs. Planned analyses stratified the cohorts by neighborhood deprivation metrics defined by residential zip code, including median neighborhood household income and hardship index (a composite index including dependency, educational attainment, unemployment, poverty, per capita income, and crowded housing). The Breslow-Day test for homogeneity assessed the association of delivery epoch and neighborhood deprivation with PTD outcome. Results Of 16,544 eligible deliveries, 8.7% occurred preterm. Incidences of PTD (8.4% vs. 9.0%, p=0.17), spontaneous PTD (5.0 vs 5.4%, p=0.27), and medically indicated PTD (3.2% v 3.5%, p=0.47) were similar between the pandemic and pre-pandemic epochs. However, PTD (OR 0.78, 95% CI 0.64-0.96) and spontaneous PTD (OR 0.76, 95% CI 0.59-0.99) decreased from the pre-pandemic to pandemic epoch in those living in neighborhoods <50 th percentile for median income (Breslow-Day p-values 0.047 and 0.036, respectively). Similarly, PTD (OR 0.78, 95% CI 0.64-0.97) and spontaneous PTD (OR 0.74, 95% CI 0.57-0.98) decreased for those inhabiting neighborhoods in the highest-hardship quartile (Breslow-Day p-values 0.045 and 0.029, respectively). Conclusion Populations residing in socioeconomically disadvantaged neighborhoods experienced reductions in preterm delivery during the COVID-19 pandemic. Neighborhood-level social determinants of health offer insight into the complex etiologies that contribute to preterm delivery, and provide opportunities for public health, equity-focused prevention strategies.

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“…Prenatal maternal stress can also impact the neonatal adaptive immunity along generations. Garcia-Flores et al (2020) used a murine model of prenatal maternal stress across three generations. The authors applied four stress procedures including swimming, restraint, shaking, and white noise for one week in 10 days post-coitum in three generation of dams and evaluated the adaptive immune response of neonates.…”

Section: Maternal Stress and Fetal Programming Of Immune Responsementioning

confidence: 99%

Programming of Vascular Dysfunction by Maternal Stress: Immune System Implications

et al. 2022

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A growing body of evidence highlights that several insults during pregnancy impact the vascular function and immune response of the male and female offspring. Overactivation of the immune system negatively influences cardiovascular function and contributes to cardiovascular disease. In this review, we propose that modulation of the immune system is a potential link between prenatal stress and offspring vascular dysfunction. Glucocorticoids are key mediators of stress and modulate the inflammatory response. The potential mechanisms whereby prenatal stress negatively impacts vascular function in the offspring, including poor hypothalamic–pituitary–adrenal axis regulation of inflammatory response, activation of Th17 cells, renin–angiotensin–aldosterone system hyperactivation, reactive oxygen species imbalance, generation of neoantigens and TLR4 activation, are discussed. Alterations in the immune system by maternal stress during pregnancy have broad relevance for vascular dysfunction and immune-mediated diseases, such as cardiovascular disease.

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Prenatal Maternal Stress Causes Preterm Birth and Affects Neonatal Adaptive Immunity in Mice

Cited by 30 publications

References 96 publications

The effects of advanced maternal age on T-cell subsets at the maternal–fetal interface prior to term labor and in the offspring: a mouse study

The effects of advanced maternal age on T-cell subsets at the maternal–fetal interface prior to term labor and in the offspring: a mouse study

Neighborhood deprivation and preterm delivery during the coronavirus 2019 pandemic

Programming of Vascular Dysfunction by Maternal Stress: Immune System Implications

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