Perinatal stress and methylation of the NR3C1 gene in newborns: systematic review
Open accessAbstract
Adverse experiences in the perinatal period have been associated with the methylation of the human glucocorticoid receptor gene (NR3C1) and long-term diseases. We conducted a systematic review on the association between adversities in the perinatal period and DNA methylation in the 1 F region of the NR3C1 gene in newborns. We explored the MEDLINE, Web of Science, Scopus, Scielo, and Lilacs databases without time or language limitations. Two independent reviewers performed the selection of articles and data extraction. A third participated in the methodological quality assessment and consensus meetings at all stages. Finally, ten studies were selected. Methodological quality was considered moderate in six and low in four. Methylation changes were reported in 41 of the 47 CpG sites of exon 1 F. Six studies addressed maternal conditions during pregnancy: two reported methylation changes at the same sites (CpG 10, 13, 20, 21 and 47), and four at one or more sites from CpG 35 to 39. Four studies addressed neonatal parameters and morbidities: methylation changes at the same sites 4, 8, 10, 16, 25, and 35 were reported in two. Hypermethylation associated with stressful conditions prevailed. Hypomethylation was more often associated with protective conditions (maternal-foetal attachment during pregnancy, breast milk intake, higher birth weight or Apgar). In conclusion, methylation changes in several sites of the 1 F region of the NR3C1 gene in newborns and very young infants were associated with perinatal stress, but more robust and comparable results are needed to corroborate site-specific associations.
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In mice exposed to predator odors during pregnancy, there was elevated transcript abundance of CRHR1 in the amygdala and decreased BDNF transcript abundance in the hippocampus, correlated with site-specific DNA methylation changes.
“Specifically, there was an elevated transcript abundance of the CRHR1 in the amygdala and decreased the BDNF transcript abundance in the hippocampus, correlated with site-specific DNA methylation changes [39,112].”
From Comprehensive review of chronic stress pathways and the efficacy of behavioral stress reduction programs (BSRPs) in managing diseases. (2024) · cites this paper as [39]
Prenatal stress significantly reduced the percentage of the peripheral lymphocyte T CD8+ subset in male offspring.
“Additionally, prenatal stress decreased the total peripheral leukocyte count, altered differential counts by decreasing lymphocytes and increasing neutrophils and eosinophils, and significantly reduced the percentage of the peripheral lymphocyte T CD8+ subset in male offspring.”
From Comprehensive review of chronic stress pathways and the efficacy of behavioral stress reduction programs (BSRPs) in managing diseases. (2024) · cites this paper as [39]
The corticosterone response to immobilization stress disappeared in control animals after 10 days but persisted in prenatally stressed animals.
“For example, the corticosterone response to immobilization stress disappeared in control animals after 10 days but persisted in prenatally stressed animals.”
From Comprehensive review of chronic stress pathways and the efficacy of behavioral stress reduction programs (BSRPs) in managing diseases. (2024) · cites this paper as [39]
Prenatal stress altered differential counts by decreasing lymphocytes and increasing neutrophils and eosinophils.
“Additionally, prenatal stress decreased the total peripheral leukocyte count, altered differential counts by decreasing lymphocytes and increasing neutrophils and eosinophils, and significantly reduced the percentage of the peripheral lymphocyte T CD8+ subset in male offspring.”
From Comprehensive review of chronic stress pathways and the efficacy of behavioral stress reduction programs (BSRPs) in managing diseases. (2024) · cites this paper as [39]
In mice, exposure to predator odors during pregnancy increased corticosterone response and altered gene expression related to stress in the offspring.
“Also, in mice, exposure to predator odors during pregnancy increased corticosterone response and altered gene expression related to stress in the offspring.”
From Comprehensive review of chronic stress pathways and the efficacy of behavioral stress reduction programs (BSRPs) in managing diseases. (2024) · cites this paper as [39]
In a study involving pregnant Sprague Dawley rats, daily stress during the last week of gestation led to significant alterations in the offspring's HPA axis and immune competence.
“In a study involving pregnant Sprague Dawley rats, daily stress during the last week of gestation led to significant alterations in the offspring’s HPA axis and immune competence.”
From Comprehensive review of chronic stress pathways and the efficacy of behavioral stress reduction programs (BSRPs) in managing diseases. (2024) · cites this paper as [39]
Prenatal stress decreased the total peripheral leukocyte count in offspring.
“Additionally, prenatal stress decreased the total peripheral leukocyte count, altered differential counts by decreasing lymphocytes and increasing neutrophils and eosinophils, and significantly reduced the percentage of the peripheral lymphocyte T CD8+ subset in male offspring.”
From Comprehensive review of chronic stress pathways and the efficacy of behavioral stress reduction programs (BSRPs) in managing diseases. (2024) · cites this paper as [39]
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Cites
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & for the PRISMA Group (2009) · BMJ · doi:10.1136/bmj.b2535 · Cited by 83,823 · see citing works
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & The PRISMA Group (2009) · PLoS Medicine · doi:10.1371/journal.pmed.1000097 · Cited by 64,042 · see citing works
Wang, G., Ma, R., Qiao, G., Wada, K., Aizawa, Y., & Satoh, T. (2015) · Integrative Medicine International · doi:10.1159/000368408 · Cited by 18,759 · see citing works
Epigenetic programming by maternal behavior
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., & Meaney, M. J. (2004) · Nature Neuroscience · doi:10.1038/nn1276 · Cited by 6,177 · see citing works
DNA methylation and its basic function
Moore, L. D., Le, T., & Fan, G. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2012.112 · Cited by 4,906 · see citing works
Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse
McGowan, P. O., Sasaki, A., D'Alessio, A. C., Dymov, S., Labonté, B., Szyf, M., Turecki, G., & Meaney, M. J. (2009) · Nature Neuroscience · doi:10.1038/nn.2270 · Cited by 3,531 · see citing works
Born Too Soon: The global epidemiology of 15 million preterm births
Blencowe, H. K., Cousens, S. N., Chou, D., Oestergaard, M. Z., Say, L., Moller, A., Kinney, M. V., Lawn, J. E., & the Born Too Soon Preterm Birth Action Group (see acknowledgement for full list) (2013) · Reproductive Health · doi:10.1186/1742-4755-10-s1-s2 · Cited by 2,214 · see citing works
Steroid Receptor Interactions with Heat Shock Protein and Immunophilin Chaperones*
Pratt, W. B., & Toft, D. O. (1997) · Endocrine Reviews · doi:10.1210/edrv.18.3.0303 · Cited by 1,791 · see citing works
Allele-specific FKBP5 DNA demethylation mediates gene–childhood trauma interactions
Klengel, T., Mehta, D., Anacker, C., Rex-Haffner, M., Pruessner, J. C., Pariante, C. M., Pace, T. W. W., Mercer, K. B., Mayberg, H. S., Bradley, B., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3275 · Cited by 1,447 · see citing works
Oberlander, T. F., Weinberg, J., Papsdorf, M., Grunau, R., Misri, S., & Devlin, A. M. (2008) · Epigenetics · doi:10.4161/epi.3.2.6034 · Cited by 1,432 · see citing works
Charting a dynamic DNA methylation landscape of the human genome
Ziller, M. J., Gu, H., Müller, F., Donaghey, J., Tsai, L. T.-Y., Kohlbacher, O., De Jager, P. L., Rosen, E. D., Bennett, D. A., Bernstein, B. E., et al. (2013) · Nature · doi:10.1038/nature12433 · Cited by 1,357 · see citing works
Stetler, C., & Miller, G. E. (2011) · Psychosomatic Medicine · doi:10.1097/psy.0b013e31820ad12b · Cited by 1,123 · see citing works
Sex-Specific Programming of Offspring Emotionality after Stress Early in Pregnancy
Mueller, B. R., & Bale, T. L. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1424-08.2008 · Cited by 988 · see citing works
Turecki, G., & Meaney, M. J. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.11.022 · Cited by 796 · see citing works
Joubert, B. R., Håberg, S. E., Nilsen, R. M., Wang, X., Vollset, S. E., Murphy, S. K., Huang, Z., Hoyo, C., Midttun, Ø., Cupul-Uicab, L. A., et al. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1205412 · Cited by 716 · see citing works
Epigenetics: A Historical Overview
Holliday, R. (2006) · Epigenetics · doi:10.4161/epi.1.2.2762 · Cited by 712 · see citing works
Maternal care as a model for experience-dependent chromatin plasticity?
Meaney, M. J., & Szyf, M. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.07.006 · Cited by 658 · see citing works
Davies, M. N., Volta, M., Pidsley, R., Lunnon, K., Dixit, A., Lovestone, S., Coarfa, C., Harris, R. A., Milosavljevic, A., Troakes, C., et al. (2012) · Genome Biology · doi:10.1186/gb-2012-13-6-r43 · Cited by 630 · see citing works
Behavioral problems after early life stress: contributions of the hippocampus and amygdala
Hanson, J. L., Nacewicz, B. M., Sutterer, M. J., Cayo, A. A., Schaefer, S. M., Rudolph, K. D., Shirtcliff, E. A., Pollak, S. D., & Davidson, R. J. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.04.020 · Cited by 627 · see citing works
Modulation of the Hypothalamic-Pituitary-Adrenal Axis by Early Life Stress Exposure
van Bodegom, M., Homberg, J. R., & Henckens, M. J. A. G. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00087 · Cited by 562 · see citing works
Epigenetic and immune function profiles associated with posttraumatic stress disorder
Uddin, M., Aiello, A. E., Wildman, D. E., Koenen, K. C., Pawelec, G., de los Santos, R., Goldmann, E., & Galea, S. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910794107 · Cited by 518 · see citing works
Braun, P. R., Han, S., Hing, B., Nagahama, Y., Gaul, L. N., Heinzman, J. T., Grossbach, A. J., Close, L., Dlouhy, B. J., Howard, M. A., et al. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0376-y · Cited by 467 · see citing works
The glucocorticoid responses are shaped by molecular chaperones
Grad, I., & Picard, D. (2007) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2007.05.018 · Cited by 423 · see citing works
Mechanisms of glucocorticoid receptor signaling during inflammation
Smoak, K. A., & Cidlowski, J. A. (2004) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2004.06.010 · Cited by 420 · see citing works
Kirschke, E., Goswami, D., Southworth, D., Griffin, P. R., & Agard, D. A. (2014) · Cell · doi:10.1016/j.cell.2014.04.038 · Cited by 399 · see citing works
Smith, A. K., Kilaru, V., Klengel, T., Mercer, K. B., Bradley, B., Conneely, K. N., Ressler, K. J., & Binder, E. B. (2015) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32278 · Cited by 355 · see citing works
Palma-Gudiel, H., Córdova-Palomera, A., Leza, J. C., & Fañanás, L. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.05.016 · Cited by 347 · see citing works
The Consequences of Early‐Life Adversity: Neurobiological, Behavioural and Epigenetic Adaptations
Maccari, S., Krugers, H. J., Morley‐Fletcher, S., Moshe Szyf, A., & Brunton, P. J. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12175 · Cited by 347 · see citing works
Labonte, B., Yerko, V., Gross, J., Mechawar, N., Meaney, M. J., Szyf, M., & Turecki, G. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.01.034 · Cited by 345 · see citing works
Mulligan, C., D'Errico, N., Stees, J., & Hughes, D. (2012) · Epigenetics · doi:10.4161/epi.21180 · Cited by 342 · see citing works
Cortisol and DHEA in development and psychopathology
Kamin, H. S., & Kertes, D. A. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.11.018 · Cited by 311 · see citing works
Maternal prenatal depressive symptoms predict infant<i>NR3C1</i>1F and<i>BDNF</i>IV DNA methylation
Braithwaite, E., Kundakovic, M., Ramchandani, P., Murphy, S., & Champagne, F. (2015) · Epigenetics · doi:10.1080/15592294.2015.1039221 · Cited by 299 · see citing works
Associations Between Early Life Stress and Gene Methylation in Children
Romens, S. E., McDonald, J., Svaren, J., & Pollak, S. D. (2015) · Child Development · doi:10.1111/cdev.12270 · Cited by 299 · see citing works
Neonatal Therapeutic Intervention Scoring System: A Therapy-Based Severity-of-Illness Index
Gray, J. E., Richardson, D. K., McCormick, M. C., Workman‐Daniels, K., & Goldmann, D. A. (1992) · PEDIATRICS · doi:10.1542/peds.90.4.561 · Cited by 296 · see citing works
Ranger, M., Chau, C. M. Y., Garg, A., Woodward, T. S., Beg, M. F., Björnson, B., Poskitt, K. J., Fitzpatrick, K., Synnes, A. R., Miller, S. P., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0076702 · Cited by 288 · see citing works
Walton, E., Hass, J., Liu, J., Roffman, J. L., Bernardoni, F., Roessner, V., Kirsch, M., Schackert, G., Calhoun, V., & Ehrlich, S. (2016) · Schizophrenia Bulletin · doi:10.1093/schbul/sbv074 · Cited by 286 · see citing works
Seth, S., Lewis, A. J., & Galbally, M. (2016) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-016-0915-y · Cited by 274 · see citing works
Hompes, T., Izzi, B., Gellens, E., Morreels, M., Fieuws, S., Pexsters, A., Schops, G., Dom, M., Van Bree, R., Freson, K., et al. (2013) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2013.03.009 · Cited by 262 · see citing works
Byun, H., Siegmund, K. D., Pan, F., Weisenberger, D. J., Kanel, G. C., Laird, P. W., & Yang, A. S. (2009) · Human Molecular Genetics · doi:10.1093/hmg/ddp445 · Cited by 255 · see citing works
On the outside, looking in: A review and evaluation of the comparability of blood and brain “‐omes”
Tylee, D. S., Kawaguchi, D. M., & Glatt, S. J. (2013) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32150 · Cited by 243 · see citing works
Sex differences in prenatal epigenetic programing of stress pathways
Bale, T. L. (2011) · Stress · doi:10.3109/10253890.2011.586447 · Cited by 237 · see citing works
Commentary: The seven plagues of epigenetic epidemiology
Heijmans, B. T., & Mill, J. (2012) · International Journal of Epidemiology · doi:10.1093/ije/dyr225 · Cited by 208 · see citing works
Epigenetics of Early Child Development
Murgatroyd, C., & Spengler, D. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00016 · Cited by 195 · see citing works
Argentieri, M. A., Nagarajan, S., Seddighzadeh, B., Baccarelli, A., & Shields, A. E. (2017) · EBioMedicine · doi:10.1016/j.ebiom.2017.03.044 · Cited by 189 · see citing works
Depression in pregnancy, infant birth weight and DNA methylation of imprint regulatory elements
Liu, Y., Murphy, S. K., Murtha, A. P., Fuemmeler, B. F., Schildkraut, J. M., Huang, Z., Overcash, F. M., Kurtzberg, J., Jirtle, R. L., Iversen, E. S., et al. (2012) · Epigenetics · doi:10.4161/epi.20734 · Cited by 188 · see citing works
11β-hydroxysteroid dehydrogenases: changing glucocorticoid action
Seckl, J. R. (2004) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2004.09.001 · Cited by 185 · see citing works
Examining the Intersection of Sex and Stress in Modelling Neuropsychiatric Disorders
Goel, N., & Bale, T. L. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01843.x · Cited by 182 · see citing works
Non, A. L., Binder, A. M., Kubzansky, L. D., & Michels, K. B. (2014) · Epigenetics · doi:10.4161/epi.28853 · Cited by 172 · see citing works
van der Knaap, L. J., Riese, H., Hudziak, J. J., Verbiest, M. M. P. J., Verhulst, F. C., Oldehinkel, A. J., & van Oort, F. V. A. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.22 · Cited by 165 · see citing works
Lowe, R., Gemma, C., Beyan, H., Hawa, M. I., Bazeos, A., Leslie, R. D., Montpetit, A., Rakyan, V. K., & Ramagopalan, S. V. (2013) · Epigenetics · doi:10.4161/epi.24362 · Cited by 160 · see citing works
Epigenetic programming by stress and glucocorticoids along the human lifespan
Zannas, A. S., & Chrousos, G. P. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.35 · Cited by 158 · see citing works
Early life adversity, genomic plasticity, and psychopathology
Turecki, G., Ota, V., Belangero, S. I., Jackowski, A. P., & Kaufman, J. (2014) · The Lancet Psychiatry · doi:10.1016/s2215-0366(14)00022-4 · Cited by 149 · see citing works
Transcriptional control of the glucocorticoid receptor: CpG islands, epigenetics and more
Turner, J. D., Alt, S. R., Cao, L., Vernocchi, S., Trifonova, S. T., Battello, N., & Muller, C. P. (2010) · Biochemical Pharmacology · doi:10.1016/j.bcp.2010.06.037 · Cited by 145 · see citing works
Stress and the epigenetic landscape: a link to the pathobiology of human diseases?
Johnstone, S. E., & Baylin, S. B. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2881 · Cited by 125 · see citing works
Maternal Stress, Preterm Birth, and DNA Methylation at Imprint Regulatory Sequences in Humans
Vidal, A. C., Neelon, S. E. B., Liu, Y., Tuli, A. M., Fuemmeler, B. F., Hoyo, C., Murtha, A. P., Huang, Z., Schildkraut, J. M., Overcash, F. M., et al. (2014) · Genetics & Epigenetics · doi:10.4137/geg.s18067 · Cited by 113 · see citing works
Maternal prenatal stress and infant DNA methylation: A systematic review
Sosnowski, D. W., Booth, C., York, T. P., Amstadter, A. B., & Kliewer, W. (2018) · Developmental Psychobiology · doi:10.1002/dev.21604 · Cited by 111 · see citing works
Nemoda, Z., Massart, R., Suderman, M. J., Hallett, M. T., Li, T., Coote, M. L., Cody, N. A. L., Sun, Z. S., Soares, C. N., Turecki, G., et al. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.32 · Cited by 110 · see citing works
Towards elimination of maternal deaths: maternal deaths surveillance and response
Hounton, S., de Bernis, L., Hussein, J., Graham, W. J., DANEL, I. A., Byass, P., & Mason, E. M. (2013) · Reproductive Health · doi:10.1186/1742-4755-10-1 · Cited by 101 · see citing works
Burris, H. H., Braun, J. M., Byun, H., Tarantini, L., Mercado, A., Wright, R. J., Schnaas, L., Baccarelli, A., Wright, R. O., & Téllez‐Rojo, M. M. (2013) · Epigenomics · doi:10.2217/epi.13.24 · Cited by 96 · see citing works
Neurobehavior Related to Epigenetic Differences in Preterm Infants
Lester, B. M., Marsit, C. J., Giarraputo, J., Hawes, K., LaGasse, L. L., & Padbury, J. F. (2015) · Epigenomics · doi:10.2217/epi.15.63 · Cited by 89 · see citing works
Provenzi, L., Fumagalli, M., Sirgiovanni, I., Giorda, R., Pozzoli, U., Morandi, F., Beri, S., Menozzi, G., Mosca, F., Borgatti, R., et al. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00099 · Cited by 88 · see citing works
Sparrow, S. A., Manning, J. R., Cartier, J., Anblagan, D., Bastin, M. E., Piyasena, C., Pataky, R., Moore, E. J., Semple, S. I., Wilkinson, A. G., et al. (2016) · Translational Psychiatry · doi:10.1038/tp.2015.210 · Cited by 85 · see citing works
Progress in Epigenetics of Depression
Peña, C. J., & Nestler, E. J. (2018) · Progress in Molecular Biology and Translational Science · doi:10.1016/bs.pmbts.2017.12.011 · Cited by 84 · see citing works
Montirosso, R., Provenzi, L., Fumagalli, M., Sirgiovanni, I., Giorda, R., Pozzoli, U., Beri, S., Menozzi, G., Tronick, E., Morandi, F., et al. (2016) · Child Development · doi:10.1111/cdev.12492 · Cited by 83 · see citing works
Montirosso, R., & Provenzi, L. (2015) · Journal of Obstetric, Gynecologic & Neonatal Nursing · doi:10.1111/1552-6909.12559 · Cited by 81 · see citing works
Fumagalli, M., Provenzi, L., Carli, P. D., Dessimone, F., Sirgiovanni, I., Giorda, R., Cinnante, C. M., Squarcina, L., Pozzoli, U., Triulzi, F. M., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0190602 · Cited by 77 · see citing works
Cárdenas, A., Faleschini, S., Hidalgo, A. P. C., Rifas‐Shiman, S. L., Baccarelli, A., DeMeo, D. L., Litonjua, A. A., Neumann, A., Felix, J. F., Jaddoe, V. W. V., et al. (2019) · Clinical Epigenetics · doi:10.1186/s13148-019-0653-x · Cited by 73 · see citing works
Early-Life Stress: From Neuroendocrine Mechanisms to Stress-Related Disorders
Pervanidou, P., & Chrousos, G. P. (2018) · Hormone Research in Paediatrics · doi:10.1159/000488468 · Cited by 69 · see citing works
NR3C1 hypermethylation in depressed and bullied adolescents
Efstathopoulos, P., Andersson, F., Melas, P. A., Yang, L. L., Villaescusa, J. C., Rüegg, J., Ekström, T. J., Forsell, Y., Galanti, M. R., & Lavebratt, C. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0169-8 · Cited by 66 · see citing works
Wang, X.-M., Tian, F., Fan, L., Xie, C., Niu, Z., & Chen, W. (2019) · BMC Medical Genomics · doi:10.1186/s12920-018-0466-3 · Cited by 66 · see citing works
Kantake, M., Yoshitake, H., Ishikawa, H., Araki, Y., & Shimizu, T. (2014) · BMJ Open · doi:10.1136/bmjopen-2014-005318 · Cited by 54 · see citing works
Epigenetic Biomarkers of Preterm Birth and Its Risk Factors
Knight, A. K., & Smith, A. K. (2016) · Genes · doi:10.3390/genes7040015 · Cited by 45 · see citing works
Mansell, T., Vuillermin, P., Ponsonby, A., Collier, F., Saffery, R., Barwon Infant Study Investigator Team, & Ryan, J. L. (2016) · Development and Psychopathology · doi:10.1017/s0954579416000183 · Cited by 45 · see citing works
Prenatal substance exposure and offspring development: Does DNA methylation play a role?
Knopik, V. S., Marceau, K., Bidwell, L. C., & Rolan, E. (2018) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2018.01.009 · Cited by 45 · see citing works
Casavant, S. G., Cong, X. S., Moore, J., & Starkweather, A. R. (2019) · Early Human Development · doi:10.1016/j.earlhumdev.2019.03.003 · Cited by 41 · see citing works
Effect of Stress on the Hypothalamic-Pituitary-Adrenal Axis in the Fetus and Newborn
Ng, P. C. (2011) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2010.11.012 · Cited by 38 · see citing works
Medical morbidities and DNA methylation of NR3C1 in preterm infants
Giarraputo, J., DeLoach, J., Padbury, J. F., Uzun, A., Marsit, C. J., Hawes, K., & Lester, B. M. (2016) · Pediatric Research · doi:10.1038/pr.2016.185 · Cited by 29 · see citing works
Allostatic Load and Biomarkers of Stress in the Preterm Infant: An Integrative Review
Casavant, S. G., Cong, X. S., FITCH, R. H., Moore, J., Rosenkrantz, T. S., & Starkweather, A. R. (2019) · Biological Research For Nursing · doi:10.1177/1099800418824415 · Cited by 29 · see citing works
Carli, M. M. D., Baccarelli, A., Trevisi, L., Pantic, I., Brennan, K. J. M., Hacker, M. R., Loudon, H., Brunst, K. J., Wright, R. O., Wright, R. J., et al. (2017) · Epigenomics · doi:10.2217/epi-2016-0109 · Cited by 27 · see citing works
Stressful Newborn Memories: Pre-Conceptual, In Utero, and Postnatal Events
Papadopoulou, Z. L., Vlaikou, A., Theodoridou, D., Markopoulos, G. S., Tsoni, K., Agakidou, E., Drosou‐Agakidou, V., Turck, C. W., Filiou, M. D., & Syrrou, M. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00220 · Cited by 18 · see citing works
Methylation changes and pathways affected in preterm birth: a role for SLC6A3 in neurodevelopment
Arpón, A., Milagro, F. I., Laja, A., Segura, V., de Pipaón, M. S., Riezu‐Boj, J. I., & Martínez, J. A. (2017) · Epigenomics · doi:10.2217/epi-2017-0082 · Cited by 17 · see citing works
Conradt, E. D., Adkins, D. E., Crowell, S. E., Monk, C. E., & Kobor, M. S. (2018) · Development and Psychopathology · doi:10.1017/s0954579418000688 · Cited by 16 · see citing works
Locus-specific DNA methylation prediction in cord blood and placenta
Ma, B., Allard, C., Bouchard, L., Perron, P., Mittleman, M. A., Hivert, M., & Liang, L. (2019) · Epigenetics · doi:10.1080/15592294.2019.1588685 · Cited by 16 · see citing works
“Epigenethics” in the Neonatal Intensive Care Unit
Provenzi, L., & Montirosso, R. (2015) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2015.43 · Cited by 15 · see citing works
Epigenetic Modifications Following Noxious Stimuli in Infants
Hatfield, L. A., Hoffman, R. K., Polomano, R. C., & Conley, Y. P. (2018) · Biological Research For Nursing · doi:10.1177/1099800417754141 · Cited by 15 · see citing works
Kantake, M., Ohkawa, N., Iwasaki, T., Ikeda, N., Awaji, A., Saito, N., Shoji, H., & Shimizu, T. (2018) · Clinical Epigenetics · doi:10.1186/s13148-018-0497-9 · Cited by 14 · see citing works
(1918) · Journal of the American Ceramic Society · doi:10.1111/j.1151-2916.1918.tb17232.x · Cited by 5 · see citing works
Maternal prenatal depressive symptoms predict infant NR3C1 1F and BDNF IV methylation
Braithwaite, E., Kundaković, M., Ramchandani, P. G., Murphy, S. E., & Champagne, F. A. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.07.398 · Cited by 4 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- Labonte B, Yerko V, Gross J, et al. Differential gluco- corticoid receptor exon 1 B, 1 C, and 1 H expression and methylation in suicide completers with a history of childhood abuse. Biol Psychiatry. 2012;72(1):41-48.
- Casavant SG, Cong X, Fitch RH, et al. Biomarkers of Stress in the Preterm Infant: an Integrative Review. Biol Res Nurs. 2019;21(2):210-223.
- McGowan PO, Sasaki A, D'Alessio AC, et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci. 2009;12(3):342-348.
Cited by
Sorted by citations
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Hypothalamic NR3C1 DNA methylation in rats exposed to prenatal stress
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Enacting biosocial complexity: Stress, epigenetic biomarkers and the tools of postgenomics
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de Mello, P. F. T. C., Ryan, S., & Fichorova, R. N. (2023) · Microorganisms · doi:10.3390/microorganisms11030551 · Cited by 8 · see citing works
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Self-citationLiu, C., Liu, H., Li, H., Yang, D., Li, Y., Wang, R., Zhu, J., Ma, S., & Guan, S. (2025) · PLoS ONE · doi:10.1371/journal.pone.0313705 · Cited by 7 · see citing works
Obrycka, P., Soczyńska, J., Butyńska, K., Frątczak, A., Hałaburdo, J., Gawełczyk, W., & Woźniak, S. (2026) · Cells · doi:10.3390/cells15030222 · Cited by 5 · see citing works
Gultig, K. D., de Rooij, S. R., Hilberdink, C. E., Olff, M., Roseboom, T. J., & van Zuiden, M. (2023) · European Journal of Psychotraumatology · doi:10.1080/20008066.2023.2219075 · Cited by 4 · see citing works
Stress and DNA Methylation of Blood Leukocytes among Pregnant Latina Women
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Born early, age fast: Consequences of premature birth on chronic disease and accelerated ageing
Gauda, E. B., Ivanovska, J., Mascarenhas, D., Antwi, J., Mohammadi, A., & Jasani, B. (2026) · The Journal of Physiology · doi:10.1113/jp289277 · Cited by 1 · see citing works
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Breivik, T. J., Gjermo, P. E., Opstad, P. K., Murison, R. C. C., von Hörsten, S., & Fristad, I. (2025) · Life · doi:10.3390/life15101572 · Cited by 1 · see citing works
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Epigenetics and pharmacoepigenetics of neuropsychiatric disorders
Cacabelos, R., Cacabelos, N., Iglesias, O.-M., Tellado, I., & Naidoo, V. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-18722-3.00020-7
Campanha, P. D. P. A., de Magalhães‐Barbosa, M. C., Brasil, A. D. A., Paravidino, V. B., Soares‐Lima, S. C., Lopes, M. D. S. A., dos Santos, P. V. B. E., Milone, L. T. V., Salú, M. D. S., Saide, S. C. A. D. O., et al. (2025) · Epigenetics Reports · doi:10.1080/28361512.2025.2545608
Self-citationSoerensen, A. E., Vos, S., Braeken, M. A. K. A., van den Heuvel, M. I., den Bergh, B. R. H. V., & Nawrot, T. S. (2025) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2025.107728
Epigenetic Inheritance: Maintaining and Fine-Tuning Origin-Specific Features Across Generations
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The coding of evolutionary processes, learning, and intelligence
Saba, L. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-44728-0.00008-1
Landolt, M. A., Strebel, N. L., Moehrlen, U., Ochsenbein, N., Strübing, N., Burkhardt, T., D'Addario, C., Pucci, M., Bodenmann, A., & Grünblatt, E. (2026) · Epigenetics · doi:10.1080/15592294.2026.2632976
Herrera-Huerta, C. A., Saldivar-Tapia, C. A., Avilez, L. D. C. M., Gastélum, C. D. G., Robles, E. C., Gea, P. M., & Durand, A. I. B. (2026) · Ciencia Latina Revista Científica Multidisciplinar · doi:10.37811/cl_rcm.v10i1.23367
- Authors
- Chalfun, G., Reis, M. M., de Oliveira, M. B. G., de Araújo Brasil, A., dos Santos Salú, M., da Cunha, A. J. L. A., Prata-Barbosa, A., & de Magalhães-Barbosa, M. C.
- Affiliations
- Department of Pediatrics, D’Or Institute for Research and Education (Idor), Rio de Janeiro, RJ, Brazil
- D’Or Institute for Research and Education (BR)
- ORCID
- Venue
- Epigenetics
- Publisher
- Informa UK Limited
- Published
- 2021-10-01
- Volume
- 17
- Issue
- 9
- Pages
- 1003-1019
- ISSN
- 1559-2294 (ISSN-L)
- 1559-2308
- PMC
- PMC9487734
- OpenAlex
- W3200668831
- Cited by
- 22
- References
- 87
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 3 · 2023: 4 · 2022: 3
- FWCI
- 0.61
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Epigenetics (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- no funding associated
- Topics
- 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
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Keywords
- perinatal stress, DNA methylation, NR3C1, glucocorticoid receptor gene, neonates, CpG sites, breast milk intake, birth weight, Apgar score, maternal-fetal attachment, hypermethylation, hypomethylation
- MeSH terms
- Exons, Female, Humans, Infant, Infant, Newborn, Pregnancy, Protein Processing, Post-Translational, Receptors, Glucocorticoid, DNA Methylation
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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