Cited by 158Birth, Development, and HealthChild Abuse and TraumaStress Responses and Cortisol

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Translating basic research knowledge on the biological embedding of early-life stress into novel approaches for the developmental programming of lifelong health

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Heim, Christine M., Entringer, Sonja, Buss, Claudia·2019·Psychoneuroendocrinology

DOI 10.1016/j.psyneuen.2018.12.011PMC PMC6561839

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Abstract

This review integrates scientific knowledge obtained over the past few decades on the biological mechanisms that contribute to the profound association between exposure to early adversity, including childhood trauma and prenatal stress, and the lifelong elevated risk to develop a broad range of diseases. We further discuss insights into gene-environment interactions moderating the association between early adversity and disease manifestation and we discuss the role of epigenetic and other molecular processes in the biological embedding of early adversity. Based on these findings, we propose potential mechanisms that may contribute to the intergenerational transmission of risk related to early adversity from the mother to the fetus. Finally, we argue that basic research knowledge on the biological embedding of early adversity must now be translated into novel intervention strategies that are mechanism-driven and sensitive to developmental timing. Indeed, to date, there are no diagnostic biomarkers of risk or mechanism-informed interventions that we can offer to victims of early adversity in order to efficiently prevent or reverse adverse health outcomes. Such translational efforts can be expected to have significant impact on both clinical practice and the public health system, and will promote precision medicine in pediatrics and across the lifespan.

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“…including cardiovascular disease, diabetes, obesity, psychiatric diseases like depression, dementia, and schizophrenia (Armanios and Blackburn, 2012; Haycock et al., 2014; Ma et al., 2011; Zhao et al., 2013) and earlier mortality (Cawthon et al., 2003; Kimura et al., 2008; Rode et al., 2015).”
Background
Maternal IL-6 during pregnancy can be estimated from newborn brain connectivity and predicts future working memory in offspring
Rudolph, M. D., Graham, A. M., Feczko, E., Miranda-Dominguez, O., Rasmussen, J. M., Nardos, R., Entringer, S., Wadhwa, P. D., Buss, C., & Fair, D. A. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0128-y · Cited by 374
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Reduced Medial Prefrontal Cortex Volume in Adults Reporting Childhood Emotional Maltreatment
van Harmelen, A.-L., van Tol, M.-J., van der Wee, N. J. A., Veltman, D. J., Aleman, A., Spinhoven, P., van Buchem, M. A., Zitman, F. G., Penninx, B. W. J. H., & Elzinga, B. M. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.06.011 · Cited by 362
Embryonic exposure to corticosterone modifies the juvenile stress response, oxidative stress and telomere length
Haussmann, M. F., Longenecker, A. S., Marchetto, N. M., Juliano, S. A., & Bowden, R. M. (2011) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2011.1913 · Cited by 357
The dexamethasone/corticotropin-releasing factor test in men with major depression: role of childhood trauma
Heim, C., Mletzko, T., Purselle, D., Musselman, D. L., & Nemeroff, C. B. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.07.002 · Cited by 353
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The effect of genotype and in utero environment on interindividual variation in neonate DNA methylomes
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Telomeres: Cancer to Human Aging
Stewart, S. A., & Weinberg, R. A. (2006) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.22.010305.104518 · Cited by 349
Rearing effects on cerebrospinal fluid oxytocin concentration and social buffering in rhesus monkeys
Winslow, J. T., Noble, P. L., Lyons, C. K., Sterk, S. M., & Insel, T. R. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300128 · Cited by 345
Childhood maltreatment and telomere shortening: preliminary support for an effect of early stress on cellular aging
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Alterations in the Vaginal Microbiome by Maternal Stress Are Associated With Metabolic Reprogramming of the Offspring Gut and Brain
Jašarević, E., Howerton, C. L., Howard, C. D., & Bale, T. L. (2015) · Endocrinology · doi:10.1210/en.2015-1177 · Cited by 329
Human transgenerational responses to early-life experience: potential impact on development, health and biomedical research
Pembrey, M., Saffery, R., Bygren, L. O., & Network in Epigenetic Epidemiology (2014) · Journal of Medical Genetics · doi:10.1136/jmedgenet-2014-102577 · Cited by 325
Prenatal stress, development, health and disease risk: A psychobiological perspective—2015 Curt Richter Award Paper
Entringer, S., Buss, C., & Wadhwa, P. D. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.08.019 · Cited by 324
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Interaction of childhood stress with hippocampus and prefrontal cortex volume reduction in major depression
Frodl, T., Reinhold, E., Koutsouleris, N., Reiser, M., & Meisenzahl, E. M. (2010) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2010.01.006 · Cited by 323
Reduced prefrontal cortical gray matter volume in young adults exposed to harsh corporal punishment
Tomoda, A., Suzuki, H., Rabi, K., Sheu, Y.-S., Polcari, A. M., & Teicher, M. H. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.03.005 · Cited by 318
Decreased Cortical Representation of Genital Somatosensory Field After Childhood Sexual Abuse
Heim, C. M., Mayberg, H. S., Mletzko, T., Nemeroff, C. B., & Pruessner, J. C. (2013) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2013.12070950 · Cited by 318
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Telomere length and early severe social deprivation: linking early adversity and cellular aging
Drury, S. S., Theall, K., Gleason, M. M., Smyke, A. T., De Vivo, I., Wong, J. Y. Y., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (2012) · Molecular Psychiatry · doi:10.1038/mp.2011.53 · Cited by 316
Obesity Risk for Female Victims of Childhood Sexual Abuse: A Prospective Study
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Abuse-Related Posttraumatic Stress Disorder and Alterations of the Hypothalamic-Pituitary-Adrenal Axis in Women With Chronic Pelvic Pain
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Effect of childhood physical abuse on cortisol stress response
Carpenter, L. L., Shattuck, T. T., Tyrka, A. R., Geracioti, T. D., & Price, L. H. (2011) · Psychopharmacology · doi:10.1007/s00213-010-2007-4 · Cited by 307
Maternal and Environmental Influences on the Adrenocortical Response to Stress in Weanling Rats
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Distress during pregnancy: Epigenetic regulation of placenta glucocorticoid-related genes and fetal neurobehavior
Monk, C., Feng, T., Lee, S., Krupska, I., Champagne, F. A., & Tycko, B. (2016) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2015.15091171 · Cited by 304
Maternal prenatal depressive symptoms predict infant NR3C1 1F and BDNF IV DNA methylation
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Peripheral Blood Leukocyte Telomere Length and Mortality Among 64 637 Individuals From the General Population
Rode, L., Nordestgaard, B. G., & Bojesen, S. E. (2015) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djv074 · Cited by 297
Prenatal Stress or High-Fat Diet Increases Susceptibility to Diet-Induced Obesity in Rat Offspring
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Maternal pregnancy-specific anxiety is associated with child executive function at 6–9 years age
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Maternal Systemic Interleukin-6 During Pregnancy Is Associated With Newborn Amygdala Phenotypes and Subsequent Behavior at 2 Years of Age
Graham, A. M., Rasmussen, J. M., Rudolph, M. D., Heim, C. M., Gilmore, J. H., Styner, M., Potkin, S. G., Entringer, S., Wadhwa, P. D., Fair, D. A., et al. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.05.027 · Cited by 282
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Review and management of clozapine side effects.
Miller, D. D. (2000) · PubMed · Cited by 281
Maltreatment in Childhood and Adolescence
Häuser, W., Schmutzer, G., Brähler, E., & Glaesmer, H. (2011) · Deutsches Ärzteblatt international · doi:10.3238/arztebl.2011.0287 · Cited by 278
Telomere Length and Mortality: A Study of Leukocytes in Elderly Danish Twins
Kimura, M., Hjelmborg, J., Gardner, J. P., Bathum, L., Brimacombe, M. B., Lu, X., Christiansen, L., Vaupel, J. W., Aviv, A., & Christensen, K. (2008) · American Journal of Epidemiology · doi:10.1093/aje/kwm380 · Cited by 277
Early life adversity and telomere length: a meta-analysis
Ridout, K. K., Levandowski, M., Ridout, S. J., Gantz, L., Goonan, K., Palermo, D., Price, L. H., & Tyrka, A. R. (2018) · Molecular Psychiatry · doi:10.1038/mp.2017.26 · Cited by 273
Childhood adversities are associated with shorter telomere length at adult age both in individuals with an anxiety disorder and controls
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Childhood trauma associated with short leukocyte telomere length in posttraumatic stress disorder
O'Donovan, A., Epel, E., Lin, J., Wolkowitz, O., Cohen, B., Maguen, S., Metzler, T., Lenoci, M., Blackburn, E., & Neylan, T. C. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.01.035 · Cited by 262
Maternal psychosocial stress during pregnancy is associated with newborn leukocyte telomere length
Entringer, S., Epel, E. S., Lin, J., Buß, C., Shahbaba, B., Blackburn, E. H., Simhan, H. N., & Wadhwa, P. D. (2012) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2012.11.033 · Cited by 257
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The effects of early life stress on the epigenome: From the womb to adulthood and even before
Provençal, N., & Binder, E. B. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2014.09.001 · Cited by 255
Cortisol in mother's milk across lactation reflects maternal life history and predicts infant temperament
Hinde, K., Skibiel, A. L., Foster, A. B., Rosso, L. A. D., Mendoza, S. P., & Capitanio, J. P. (2014) · Behavioral Ecology · doi:10.1093/beheco/aru186 · Cited by 254
Intergenerational Transmission of Maternal Childhood Maltreatment Exposure: Implications for Fetal Brain Development
Buss, C., Entringer, S., Moog, N. K., Toepfer, P., Fair, D. A., Simhan, H. N., Heim, C. M., & Wadhwa, P. D. (2017) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2017.03.001 · Cited by 250
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Selective inhibitors of the FK506-binding protein 51 by induced fit
Gaali, S., Kirschner, A., Cuboni, S., Hartmann, J., Kozany, C., Balsevich, G., Namendorf, C., Fernandez-Vizarra, P., Sippel, C., Zannas, A. S., et al. (2015) · Nature Chemical Biology · doi:10.1038/nchembio.1699 · Cited by 245 · cited 1×
“Targeted “bottom up” approaches, such as the use of FKBP51 blockers (currently in animal models), represent an attempt of a direct counteraction of the biological embedding effects of ELS (Gaali et al., 2015).”
Background
Effect of childhood trauma on adult depression and neuroendocrine function: sex-specific moderation by CRH receptor 1 gene
Heim, C. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.041.2009 · Cited by 245
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Stress In Utero: Prenatal Programming of Brain Plasticity and Cognition
Bock, J., Wainstock, T., Braun, K., & Segal, M. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.02.036 · Cited by 244
Maternal psychosocial stress during pregnancy alters the epigenetic signature of the glucocorticoid receptor gene promoter in their offspring: A meta-analysis
Palma-Gudiel, H., Córdova-Palomera, A., Eixarch, E., Deuschle, M., & Fañanás, L. (2015) · Epigenetics · doi:10.1080/15592294.2015.1088630 · Cited by 240
Maternal Adverse Childhood Experiences and Infant Development
Racine, N. M., Plamondon, A., Madigan, S. L., McDonald, S., & Tough, S. (2018) · PEDIATRICS · doi:10.1542/peds.2017-2495 · Cited by 240
Early life adversity and the epigenetic programming of hypothalamic-pituitary-adrenal function
Anacker, C., O'Donnell, K. J., & Meaney, M. J. (2014) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2014.16.3/canacker · Cited by 237
Prepartum and Postpartum Maternal Depressive Symptoms Are Related to Children’s Brain Structure in Preschool
Lebel, C., Walton, M., Letourneau, N., Giesbrecht, G. F., Kaplan, B. J., & Dewey, D. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.12.004 · Cited by 237
Prenatal stress and developmental programming of human health and disease risk: concepts and integration of empirical findings
Entringer, S., Buß, C., & Wadhwa, P. D. (2010) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e3283405921 · Cited by 236
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The molecular genetic architecture of attention deficit hyperactivity disorder
Hawi, Z., Cummins, T. D. R., Tong, J., Johnson, B. P., Lau, R., Samarrai, W., & Bellgrove, M. A. (2015) · Molecular Psychiatry · doi:10.1038/mp.2014.183 · Cited by 226
Gene × Environment Interactions: From Molecular Mechanisms to Behavior
Halldorsdottir, T., & Binder, E. B. (2016) · Annual Review of Psychology · doi:10.1146/annurev-psych-010416-044053 · Cited by 222
Effects of Early and Recent Adverse Experiences on Adrenal Response to Psychosocial Stress in Depressed Adolescents
Rao, U., Hammen, C. L., Ortiz, L. R., Chen, L.-A., & Poland, R. E. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.05.012 · Cited by 221
Association between Telomere Length and Type 2 Diabetes Mellitus: A Meta-Analysis
Zhao, J., Miao, K., Wang, H., Ding, H., & Wang, D. W. (2013) · PLoS ONE · doi:10.1371/journal.pone.0079993 · Cited by 220
Fetal Exposure to Maternal Depressive Symptoms Is Associated With Cortical Thickness in Late Childhood
Sandman, C. A., Buss, C., Head, K., & Davis, E. P. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.06.025 · Cited by 219
Maternal Interleukin-6 concentration during pregnancy is associated with variation in frontolimbic white matter and cognitive development in early life
Rasmussen, J. M., Graham, A. M., Entringer, S., Gilmore, J. H., Styner, M. A., Fair, D. A., Wadhwa, P. D., & Buß, C. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.04.020 · Cited by 215
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Association between childhood maltreatment and adult emotional dysregulation in a low-income, urban, African American sample: Moderation by oxytocin receptor gene
Bradley, B., Westen, D., Mercer, K. B., Binder, E. B., Jovanovic, T., Crain, D., Wingo, A., & Heim, C. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000162 · Cited by 213
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Fetal Glucocorticoid Exposure Is Associated with Preadolescent Brain Development
Davis, E. P., Sandman, C. A., Buß, C., Wing, D. A., & Head, K. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.03.009 · Cited by 209
Intergenerational transmission of maltreatment and psychopathology: the role of antenatal depression
Plant, D. T., Barker, E. D., Waters, C. S., Pawlby, S., & Pariante, C. M. (2013) · Psychological Medicine · doi:10.1017/s0033291712001298 · Cited by 201
Differential susceptibility to the environment: Toward an understanding of sensitivity to developmental experiences and context
Ellis, B. J., & Boyce, W. T. (2011) · Development and Psychopathology · doi:10.1017/s095457941000060x · Cited by 199
Reduced orbitofrontal and temporal grey matter in a community sample of maltreated children
De Brito, S. A., Viding, E., Sebastian, C. L., Kelly, P. A., Mechelli, A., Maris, H., & McCrory, E. J. (2013) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2012.02597.x · Cited by 194
The fetal programming of telomere biology hypothesis: an update
Entringer, S., de Punder, K., Buß, C., & Wadhwa, P. D. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2017.0151 · Cited by 194
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Intergenerational Effect of Maternal Exposure to Childhood Maltreatment on Newborn Brain Anatomy
Moog, N. K., Entringer, S., Rasmussen, J. M., Styner, M., Gilmore, J. H., Kathmann, N., Heim, C. M., Wadhwa, P. D., & Buss, C. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.07.009 · Cited by 189
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Maternal care modulates the relationship between prenatal risk and hippocampal volume in women but not in men
Buss, C., Lord, C., Wadiwalla, M., Hellhammer, D. H., Lupien, S. J., Meaney, M. J., & Pruessner, J. C. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3252-06.2007 · Cited by 187
Alterations in amygdala–prefrontal circuits in infants exposed to prenatal maternal depression
Posner, J., Cha, J., Roy, A. K., Peterson, B. S., Bansal, R., Gustafsson, H. C., Raffanello, E., Gingrich, J., & Monk, C. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.146 · Cited by 184 · cited 1×
“Several other independent research groups have in recent years provided evidence for maternal stress during pregnancy predicting newborn (Posner et al., 2016; Qiu et al., 2017; Rifkin-Graboi et al., 2015; Scheinost et al., 2016), child (El Marroun et al.”
Background
Fetal Programming of Body Composition, Obesity, and Metabolic Function: The Role of Intrauterine Stress and Stress Biology
Entringer, S., Buß, C., Swanson, J. M., Cooper, D. M., Wing, D. A., Waffarn, F., & Wadhwa, P. D. (2012) · Journal of Nutrition and Metabolism · doi:10.1155/2012/632548 · Cited by 176
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Early childhood adversity and pregnancy outcomes
Smith, M. V., Gotman, N., & Yonkers, K. A. (2016) · Maternal and Child Health Journal · doi:10.1007/s10995-015-1909-5 · Cited by 175
Imaging Genetics and Genomics in Psychiatry: A Critical Review of Progress and Potential
Bogdan, R., Salmeron, B. J., Carey, C. E., Arpana Agrawal, A., Calhoun, V. D., Garavan, H., Hariri, A. R., Heinz, A., Hill, M. N., Holmes, A., et al. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.12.030 · Cited by 174
Meta-analysis of associations between childhood adversity and hippocampus and amygdala volume in non-clinical and general population samples
Calem, M., Bromis, K., McGuire, P., Morgan, C., & Kempton, M. J. (2017) · NeuroImage Clinical · doi:10.1016/j.nicl.2017.02.016 · Cited by 171
Childhood trauma history differentiates amygdala response to sad faces within MDD
Grant, M. M., Cannistraci, C., Hollon, S. D., Gore, J., & Shelton, R. (2011) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2010.12.004 · Cited by 166
An update on the interaction between the serotonin transporter promoter variant (5-HTTLPR), stress and depression, plus an exploration of non-confirming findings
Sharpley, C. F., Palanisamy, S. K. A., Glyde, N. S., Dillingham, P. W., & Agnew, L. L. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.07.030 · Cited by 164
Impact of prenatal stress on long term body weight is dependent on timing and maternal sensitivity
MUELLER, B., & Bale, T. L. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.05.019 · Cited by 162
Stress exposure in early post-natal life reduces telomere length: an experimental demonstration in a long-lived seabird
Herborn, K. A., Heidinger, B. J., Boner, W., Noguera, J. C., Adam, A., Daunt, F., & Monaghan, P. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.3151 · Cited by 161
Association of Maternal Exposure to Childhood Abuse With Elevated Risk for Autism in Offspring
Roberts, A. L., Lyall, K., Rich-Edwards, J. W., Ascherio, A., & Weisskopf, M. G. (2013) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.447 · Cited by 160
Prenatal Stress Exposure Related to Maternal Bereavement and Risk of Childhood Overweight
Li, J., Olsen, J., Vestergaard, M., Obel, C., Baker, J. L., & Sørensen, T. I. A. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011896 · Cited by 150
Early adverse events, HPA activity and rostral anterior cingulate volume in MDD
Treadway, M. T., Grant, M. M., Ding, Z., Hollon, S. D., Gore, J. C., & Shelton, R. C. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004887 · Cited by 142
Maternal childhood abuse and offspring adjustment over time
Collishaw, S., Dunn, J., O’Connor, T. G., Golding, J., & THE AVON LONGITUDINAL STUDY OF PARENTS AND CHILDREN STUDY TEAM (2007) · Development and Psychopathology · doi:10.1017/s0954579407070186 · Cited by 141
The Association of Telomere Length With Family Violence and Disruption
Drury, S. S., Mabile, E., Brett, Z. H., Esteves, K. C., Jones, E., Shirtcliff, E. A., & Theall, K. P. (2014) · PEDIATRICS · doi:10.1542/peds.2013-3415 · Cited by 141
Antenatal Maternal Anxiety Predicts Variations in Neural Structures Implicated in Anxiety Disorders in Newborns
Rifkin-Graboi, A. E., Meaney, M. J., Chen, H., Bai, J., Hameed, W. B., Tint, M. T., Broekman, B. F. P., Chong, Y. S., Gluckman, P. D., Fortier, M. V., et al. (2015) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2015.01.013 · Cited by 140
Fetal Programming of Brain Development: Intrauterine Stress and Susceptibility to PsychopathologyA Presentation from the European Society for Paediatric Endocrinology (ESPE) New Inroads to Child Health (NICHe) Conference on Stress Response and Child Health in Heraklion, Crete, Greece, 18 to 20 May 2012.
Buß, C., Entringer, S., & Wadhwa, P. D. (2012) · Science Signaling · doi:10.1126/scisignal.2003406 · Cited by 138
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Glucocorticoid receptor gene polymorphisms and childhood adversity are associated with depression: New evidence for a gene–environment interaction
Bet, P. M., Penninx, B. W. J. H., Bochdanovits, Z., Uitterlinden, A. G., Beekman, A. T. F., van Schoor, N. M., Deeg, D. J. H., & Hoogendijk, W. J. G. (2009) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30886 · Cited by 138
The Impact of Maternal Childhood Abuse on Parenting and Infant Temperament
Lang, A. J., Gartstein, M. A., Rodgers, C. S., & Lebeck, M. M. (2010) · Journal of Child and Adolescent Psychiatric Nursing · doi:10.1111/j.1744-6171.2010.00229.x · Cited by 137
Prenatal stress alters amygdala functional connectivity in preterm neonates
Scheinost, D., Kwon, S. H., Lacadie, C., Sze, G., Sinha, R., Constable, R. T., & Ment, L. R. (2016) · NeuroImage: Clinical · doi:10.1016/j.nicl.2016.08.010 · Cited by 130
Maternal Exposure to Childhood Trauma Is Associated During Pregnancy With Placental-Fetal Stress Physiology
Moog, N. K., Buss, C., Entringer, S., Shahbaba, B., Gillen, D. L., Hobel, C. J., & Wadhwa, P. D. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.08.032 · Cited by 129
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Nonsteroidal Anti-Inflammatory Treatment Prevents Delayed Effects of Early Life Stress in Rats
Brenhouse, H. C., & Andersen, S. L. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.05.006 · Cited by 127
Impaired Executive Function Mediates the Association between Maternal Pre-Pregnancy Body Mass Index and Child ADHD Symptoms
Buß, C., Entringer, S., Davis, E. P., Hobel, C. J., Swanson, J. M., Wadhwa, P. D., & Sandman, C. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037758 · Cited by 126
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The Generation R Study: A Review of Design, Findings to Date, and a Study of the 5-HTTLPR by Environmental Interaction From Fetal Life Onward
Tiemeier, H. W., Velders, F. P., Székely, E., Roza, S. J., Dieleman, G. C., Jaddoe, V. W. V., Uitterlinden, A. G., White, T. J. H., Bakermans‐Kranenburg, M. J., Albert Hofman, D., et al. (2012) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2012.08.021 · Cited by 124
Effects of Antenatal Maternal Depressive Symptoms and Socio-Economic Status on Neonatal Brain Development are Modulated by Genetic Risk
Qiu, A., Shen, M., Buß, C., Chong, Y. S., Kwek, K. Y. C., Saw, S., Gluckman, P. D., Wadhwa, P. D., Entringer, S., Styner, M. A., et al. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx065 · Cited by 123
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Implications of newborn amygdala connectivity for fear and cognitive development at 6-months-of-age
Graham, A. M., Buss, C., Rasmussen, J. M., Rudolph, M. D., Demeter, D. V., Gilmore, J. H., Styner, M., Entringer, S., Wadhwa, P. D., & Fair, D. A. (2016) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.09.006 · Cited by 122
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Prenatal Stress, Telomere Biology, and Fetal Programming of Health and Disease RiskA Presentation from the European Society for Paediatric Endocrinology (ESPE) New Inroads to Child Health (NICHe) Conference on Stress Response and Child Health in Heraklion, Crete, Greece, 18 to 20 May 2012.
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Authors: Heim, C. M., Entringer, S., & Buss, C.
Affiliations: University of California, Irvine (US)
Corresponding author: Entringer, Sonja
Buss, Claudia
ORCID: Entringer, Sonja
Buss, Claudia
Venue: Psychoneuroendocrinology
Publisher: Elsevier BV
Published: 2019-07
Volume: 105
Pages: 123-137
ISSN: 0306-4530 (ISSN-L)
DOI: 10.1016/j.psyneuen.2018.12.011
PMC: PMC6561839
OpenAlex: W2905562542
Cited by: 158
References: 227
Citations by year: 2026: 13 · 2025: 21 · 2024: 18 · 2023: 25 · 2022: 35 · 2021: 21 · 2020: 18 · 2019: 7
FWCI: 2.20
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Psychoneuroendocrinology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: Bundesministerium für Bildung und Forschung (01KR1301, 01GL1743)
Deutsche Forschungsgemeinschaft (EXC257, EN 851/2-1)
European Research Council (ERC 639766, ERC 678073)
U.S. Public Health Service
National Institutes of Health (P50 HD-551411, 5UG3OD023349, R01 HD-065825, R01 AG-050455, R01 MH-105538, R01 HD-060628, MH 58922)
Topics: Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords: early life stress, biological embedding, developmental programming, childhood trauma, prenatal stress, gene-environment interaction, epigenetics, intergenerational transmission, mother-to-child transmission, precision medicine, developmental timing, disease risk
MeSH terms: Psychological Trauma, Adverse Childhood Experiences, Animals, Brain, Female, Humans, Pregnancy, Prenatal Exposure Delayed Effects, Stress, Psychological, Epigenesis, Genetic, Telomere Shortening, Gene-Environment Interaction

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Translating basic research knowledge on the biological embedding of early-life stress into novel approaches for the developmental programming of lifelong health

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