Prenatal earthquake stress exposure in different gestational trimesters is associated with methylation changes in the glucocorticoid receptor gene (NR3C1) and long-term working memory in adulthood
Open accessAbstract
Prenatal stress exposure is thought to affect the long-term development of the foetal brain via the HPA axis and to change health outcomes in adulthood, including working memory (WM). The potential mechanism is that there is a critical period of brain development of the foetus, which is a result of selective adaptation to the external environment. The human glucocorticoid gene (NR3C1) is associated with memory and cognition. This study investigates the association between earthquake stress during pregnancy and CpG methylation of the NR3C1 exon 1 F promoter and its influence on working memory in adulthood. DNA methylation analysis using bisulfite sequencing PCR was quantified in 176 subjects who were exposed or not exposed to intrauterine earthquake and were divided into three groups based on the pregnancy trimester. The Hopkins Verbal Learning Test-Revised (HVLT-R) and Brief Visuospatial Memory Test-Revised (BVMT-R) were used to assess working memory performance. The methylated NR3C1 exon 1 F promoter of the prenatal earthquake exposure (PEE) group was significantly higher than that of the control group (CN). Analysis of subgroups indicated that the subjects in the second trimester of PEE group showed significantly higher methylation than those in the third trimester. Significantly low BVMT-R scores were detected in those who experienced prenatal earthquake in the second trimester of PEE group. Methylated CpG site 1 may play a critical role in contributing to lower BVMT-R scores in the second trimester in the PEE group, and may offer a potential epigenetic mechanism that links prenatal stress and long-term effects on working memory.
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Exposures occurring in utero or during early childhood, periods characterized by heightened biological plasticity, have been associated with more pronounced neurocognitive and psychological effects.
“Developmental timing appears to play an important role in shaping outcomes, as exposures occurring in utero or during early childhood, periods characterized by heightened biological plasticity, have been associated with more pronounced neurocognitive and psychological effects (7, 10, 11).”
From Epigenetic changes associated with multi-generational trauma: characterization, mechanisms, and therapeutics (2026) · cites this paper as [10]
The Introduction describes the foetal period as vulnerable to lasting cognitive effects and links early-life stress to emotional and cognitive outcomes. The Results report poorer adult memory after prenatal earthquake exposure, with differences by gestational trimester. The paper does not establish that early-childhood exposure has more pronounced neurocognitive or psychological effects than exposure at other ages. Page numbers were not available in our copy. (LLM, conf=0.84)
Experimental — accuracy not yet measuredIn earthquake cohorts, early gestational exposure was associated with poorer working memory in adulthood.
“Similar developmental sensitivity has been reported in earthquake cohorts, where early gestational exposure was associated with poorer working memory in adulthood (10).”
From Epigenetic changes associated with multi-generational trauma: characterization, mechanisms, and therapeutics (2026) · cites this paper as [10]
The Results (Comparison of working memory in the PEE and CN groups; page unavailable) report lower memory-test scores among adults exposed prenatally to the earthquake than among controls. But the trimester comparison does not support poorer performance specifically after early (first-trimester) exposure: first-trimester participants scored significantly higher on the visuospatial test than those exposed in the second or third trimester. The Discussion identifies the second trimester as the group with the worst visuospatial-memory performance. (LLM, conf=0.88)
Experimental — accuracy not yet measuredEven when examining the same gene, findings may differ depending on the nature of the traumatic exposure.
“Even when examining the same gene, findings may differ depending on the nature of the traumatic exposure.”
From Epigenetic changes associated with multi-generational trauma: characterization, mechanisms, and therapeutics (2026) · cites this paper as [10]
The Results (page unavailable) report different NR3C1 methylation findings depending on which trimester prenatal earthquake exposure occurred. That supports the broader point that findings for the same gene can vary with exposure circumstances, but the paper does not compare different kinds of traumatic exposure or establish that findings vary with the nature of the trauma. (LLM, conf=0.78)
Experimental — accuracy not yet measuredGestational exposure to the Tangshan earthquake was associated with increased methylation of NR3C1, a key regulator of glucocorticoid signaling.
“Gestational exposure to the Tangshan earthquake was associated with increased methylation of NR3C1, a key regulator of glucocorticoid signaling (10).”
From Epigenetic changes associated with multi-generational trauma: characterization, mechanisms, and therapeutics (2026) · cites this paper as [10]
Increased methylation of NR3C1 has been reported in both earthquake survivors and survivors of the Tutsi genocide, yet associations with cognitive and psychiatric outcomes differ across contexts.
“For example, increased methylation of NR3C1 has been reported in both earthquake survivors and survivors of the Tutsi genocide, yet associations with cognitive and psychiatric outcomes differ across contexts (10, 88).”
From Epigenetic changes associated with multi-generational trauma: characterization, mechanisms, and therapeutics (2026) · cites this paper as [10]
Across multiple trauma contexts, altered methylation of NR3C1 has been reported, including genocide exposure, childhood maltreatment, and natural disasters.
“Across multiple trauma contexts, altered methylation of NR3C1 has been reported, including genocide exposure, childhood maltreatment, and natural disasters (10, 82, 88, 89).”
From Epigenetic changes associated with multi-generational trauma: characterization, mechanisms, and therapeutics (2026) · cites this paper as [10]
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- Authors
- Wang, R., Wang, J., Xu, S., Wang, L., Song, M., An, C., & Wang, X.
- Affiliations
- Hebei Medical University (CN)
- Corresponding author
- Wang, Xueyi
- Venue
- Translational Psychiatry
- Published
- 2022-04-29
- Volume
- 12
- Issue
- 1
- Pages
- 176-176
- ISSN
- 2158-3188 (ISSN-L)
- PMC
- PMC9054818
- OpenAlex
- W4225150335
- Cited by
- 17
- References
- 51
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 5 · 2023: 3
- FWCI
- 2.87
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Translational Psychiatry (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- National Natural Science Foundation of China (81271489)
- Department of Health of Hebei Province
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- prenatal stress, glucocorticoid receptor gene, NR3C1, DNA methylation, CpG methylation, working memory, visuospatial memory, hypothalamic-pituitary-adrenal axis, pregnancy trimesters, epigenetics, brain development
- MeSH terms
- Adult, Female, Glucocorticoids, Humans, Hypothalamo-Hypophyseal System, Memory, Short-Term, Pituitary-Adrenal System, Pregnancy, Pregnancy Trimesters, Prenatal Exposure Delayed Effects, Receptors, Glucocorticoid, DNA Methylation, Earthquakes
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