Prenatal Two-Hit Stress Affects Maternal and Offspring Pregnancy Outcomes and Uterine Gene Expression in Rats: Match or Mismatch?
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Maternal stress and inflammation excesses can lead to adverse pregnancy outcomes and offspring development. We evaluated whether distinct prenatal stressors affect pregnancy, maternal and offspring outcomes, and uterine gene expression differently when combined than either alone. Long-Evans dams were exposed to psychological or/and (two-hit) immune stress (interleukin-1 beta [IL-1β]), on gestational days 12-18 and 17-delivery, respectively. Gestational length, maternal weight gain, glycaemia and corticosterone levels, offspring weight, and gender effects were recorded. Maternal and offspring uteri were collected at weaning and on postnatal day 160 correspondingly. Uterine expression of genes involved in local progesterone metabolism, neuroendocrine and immune systems were analyzed using quantitative real-time polymerase chain reaction. Maternal two-hit stress increased gestational length variation and the occurrence of adverse pregnancy outcomes while reducing gestational weight gain. Pup weight was negatively affected by prenatal stressors in a gender-specific way. In dams, IL-1β upregulated gene expression of neuroendocrine (Crh, Crhr1) and cytokine genes (Il1b, Il1rn, Il6, and Il10). Conversely, transcriptional patterns in offspring uteri were more variable with gene-specific up- or downregulation by each stressor separately, while exposure to both extensively reduced the expression of neuroendocrine (Hsd11b1), cytokine (Il1a, Il1rn, Il6), and IL-1 receptor genes. In conclusion, maternal stress affects physiological and molecular processes in dams and their offspring; two hits have different effects than single stressors. Outcomes appear generation-, gender-, and stressor-specific. Dampening of offspring uterine gene expression after exposure to multiple stressors could fit within the match/mismatch hypothesis of perinatal programming, with offspring preparing for a stressful life.
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Maternal stress increased gestational length variation, adverse pregnancy outcomes, and reduced gestational weight gain.
“For instance, maternal stress increased gestational length variation, adverse pregnancy outcomes, and reduced gestational weight gain.”
From Comprehensive review of chronic stress pathways and the efficacy of behavioral stress reduction programs (BSRPs) in managing diseases. (2024) · cites this paper as [30]
Prenatal stressors negatively affected pup weight, with differential impacts based on gender.
“Prenatal stressors negatively affected pup weight, with differential impacts based on gender.”
From Comprehensive review of chronic stress pathways and the efficacy of behavioral stress reduction programs (BSRPs) in managing diseases. (2024) · cites this paper as [30]
Maternal stress can influence pregnancy outcomes and offspring health in a gender-specific manner.
“Maternal stress can also influence pregnancy outcomes and offspring health in a gender-specific manner.”
From Comprehensive review of chronic stress pathways and the efficacy of behavioral stress reduction programs (BSRPs) in managing diseases. (2024) · cites this paper as [30]
Stress upregulated neuroendocrine and cytokine gene expression in dams, while offspring exhibited varied transcriptional responses depending on the specific stressors experienced.
“Moreover, stress upregulated neuroendocrine and cytokine gene expression in dams, while offspring exhibited varied transcriptional responses depending on the specific stressors experienced [30].”
From Comprehensive review of chronic stress pathways and the efficacy of behavioral stress reduction programs (BSRPs) in managing diseases. (2024) · cites this paper as [30]
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Intergenerational pathways linking maternal early life adversity to offspring birthweight
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Shchaslyvyi, A. Y., Antonenko, S. V., & Telegeev, G. D. (2024) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph21081077 · Cited by 73 · see citing works
Climate change is a major stressor causing poor pregnancy outcomes and child development
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Maternal immune activation generates anxiety in offspring: A translational meta-analysis
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Prenatal Maternal Stress Causes Preterm Birth and Affects Neonatal Adaptive Immunity in Mice
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Racial disparities in pregnancy outcomes: genetics, epigenetics, and allostatic load
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Aging, Social Distancing, and COVID-19 Risk: Who is more Vulnerable and Why?
Faraji, J., & Metz, G. A. S. (2021) · Aging and Disease · doi:10.14336/ad.2021.0319 · Cited by 40 · see citing works
Mabry, S., Wilson, E. N., Bradshaw, J. L., Gardner, J. J., Fadeyibi, O., Vera, E., Osikoya, O., Cushen, S. C., Karamichos, D., Goulopoulou, S., et al. (2023) · Biology of Sex Differences · doi:10.1186/s13293-023-00557-0 · Cited by 26 · see citing works
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Environmental epigenetics: new horizons in redefining biological and health outcomes
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Social Isolation Stress Modulates Pregnancy Outcomes and the Inflammatory Profile of Rat Uterus
Lopes, N. A., Falkenberg, E. A., Wiley, C., Patel, V., Serrano-Lomelin, J. A., Fang, X., Weiler, A. M., McCreary, J. K., Metz, G. A. S., & Olson, D. M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23116169 · Cited by 16 · see citing works
Shuffrey, L. C., Morales, S., Jacobson, M. H., Enlow, M. B., Ghassabian, A., Margolis, A. E., Lucchini, M., Carroll, K. N., Crum, R. M., Dabelea, D., et al. (2023) · Child Development · doi:10.1111/cdev.13938 · Cited by 15 · see citing works
Evaluating different models of maternal stress on stress-responsive systems in prepubertal mice
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Lopes, N. A., Ambeskovic, M., King, S. E., Faraji, J., Soltanpour, N., Falkenberg, E. A., Scheidl, T. B., Patel, M. M., Fang, X., Metz, G. A. S., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24043734 · Cited by 12 · see citing works
Multiple prenatal stresses increase sexual dimorphism in adult offspring behavior
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Ageing, Social Distancing, and COVID-19 Risk: Who is more Vulnerable?Preprint
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- Authors
- Verstraeten, B. S. E., McCreary, J. K., Weyers, S., Metz, G. A. S., & Olson, D. M.
- Affiliations
- University of Alberta (CA)
- University of Lethbridge (CA)
- Ghent University (BE)
- Corresponding author
- Metz, Gerlinde A S
- Olson, David M
- Venue
- Biology of Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 2018-07-30
- Volume
- 100
- Issue
- 1
- Pages
- 195-207
- ISSN
- 0006-3363 (ISSN-L)
- 1529-7268
- PMC
- PMC6335212
- OpenAlex
- W2886406582
- Cited by
- 28
- References
- 103
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 4 · 2023: 7 · 2022: 1 · 2021: 4 · 2020: 6 · 2019: 3
- FWCI
- 3.59
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Biology of Reproduction (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Ghent University Academic Bibliography (Ghent University) (submittedVersion)
- Funders
- Research Foundation—Flanders
- Canadian Institutes of Health Research (363195, 119513)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Keywords
- prenatal stress, maternal stress, immune stress, IL-1β, adverse pregnancy outcomes, uterine gene expression, perinatal programming, match-mismatch hypothesis, cytokine genes, corticosterone, gestation length, pup weight, sex differences, offspring development
- MeSH terms
- Animals, Behavior, Animal, Corticosterone, Female, Male, Pregnancy, Pregnancy Outcome, Prenatal Exposure Delayed Effects, Stress, Psychological, Uterus, Gene Expression, Rats, Long-Evans, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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