Influence of early life stress on later hypothalamic–pituitary–adrenal axis functioning and its covariation with mental health symptoms: A study of the allostatic process from childhood into adolescence
Open accessAbstract
The hypothalamic–pituitary–adrenal (HPA) axis is a primary mechanism in the allostatic process through which early life stress (ELS) contributes to disease. Studies of the influence of ELS on children's HPA axis functioning have yielded inconsistent findings. To address this issue, the present study considers multiple types of ELS (maternal depression, paternal depression, and family expressed anger), mental health symptoms, and two components of HPA functioning (traitlike and epoch-specific activity) in a long-term prospective community study of 357 children. ELS was assessed during the infancy and preschool periods; mental health symptoms and cortisol were assessed at child ages 9, 11, 13, and 15 years. A three-level hierarchical linear model addressed questions regarding the influences of ELS on HPA functioning and its covariation with mental health symptoms. ELS influenced traitlike cortisol level and slope, with both hyper- and hypoarousal evident depending on type of ELS. Further, type(s) of ELS influenced covariation of epoch-specific HPA functioning and mental health symptoms, with a tighter coupling of HPA alterations with symptom severity among children exposed previously to ELS. Results highlight the importance of examining multiple types of ELS and dynamic HPA functioning in order to capture the allostatic process unfolding across the transition into adolescence.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The functioning of such brain regions is affected long before children start school and impacts key learning systems, including self-regulation, executive functions, attention, memory, stress reactivity, and language.
“The functioning of such brain regions is affected long before children start school and impacts key learning systems, including self-regulation, executive functions, attention, memory, stress reactivity, and language (e.g., Essex et al., 2011).”
From Malleability, plasticity, and individuality: How children learn and develop in context<sup>1</sup> (2019) · cites this paper as Essex et al., 2011
The Methods (Measures; page unavailable) document stress exposure during infancy and preschool, and the Discussion (page unavailable) links early-life stress to later changes in HPA functioning. The paper thus supports an effect on stress-response functioning, but it does not establish effects on the full list of learning systems, including executive functions, memory, and language. (LLM, conf=0.88)
Experimental — accuracy not yet measuredChronic stress is associated with impairments in key brain centers, including the limbic system, through processes that are mediated and modulated by the HPA axis.
“Chronic stress is associated with impairments in key brain centers, including the limbic system, through processes that are mediated and modulated by the HPA axis.”
From Malleability, plasticity, and individuality: How children learn and develop in context<sup>1</sup> (2019) · cites this paper as Essex et al., 2011
The paper’s Abstract says HPA-axis cortisol can directly affect the brain and that childhood exposure may alter brain receptor sensitivity; it also links stress neurobiology to cortico-limbic pathways. The Discussion describes stress-related down-regulation of HPA functioning. Neither passage establishes impairment of key brain centers, including the limbic system, mediated by the HPA axis. Page numbers are unavailable in our copy. (LLM, conf=0.84)
Experimental — accuracy not yet measuredHigher early-life cortisol is linked to poorer emotion regulation, lower social competence, and later anxiety and depression symptoms.
“Increased cortisol levels early in life are associated with poor emotion regulation, less social competence, and later symptoms of anxiety and depression2,3.”
From Developmental pathways to amygdala–prefrontal function and internalizing symptoms in adolescence (2012) · cites this paper as [3]
ELS may sensitize HPA-axis feedback circuitry, producing atypical basal cortisol and structural/functional changes in amygdala and vmPFC.
“Other work suggests that aspects of ELS may sensitize the neural circuitry that regulates HPA-axis feedback resulting in atypical basal cortisol levels (e.g., heightened or blunted cortisol function2,3), as well as structural and functional changes in brain regions involved in affective reactivity and regulation, such as the amygdala5 and ventromedial prefrontal cortex (vmPFC)6,7.”
From Developmental pathways to amygdala–prefrontal function and internalizing symptoms in adolescence (2012) · cites this paper as [3]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The CES-D Scale: A Self-Report Depression Scale for Research in the General Population
Radloff, L. S. (1977) · Applied Psychological Measurement · doi:10.1177/014662167700100306 · Cited by 53,267 · see citing works
Missing data: our view of the state of the art
Schafer, J. L., & Graham, J. W. (2002) · Psychological Methods · doi:10.1037/1082-989x.7.2.147 · Cited by 11,638 · see citing works
Protective and Damaging Effects of Stress Mediators
McEwen, B. S. (1998) · New England Journal of Medicine · doi:10.1056/nejm199801153380307 · Cited by 6,733 · cited 12× · see citing works
“As part of the allostatic process (McEwen, 1998),”
BackgroundInfluentialEpigenetic 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
Handbook of Emotion Regulation
Lambert, K. G. (2007) · JAMA · doi:10.1001/jama.298.15.1808 · Cited by 4,900 · see citing works
The concept of allostasis in biology and biomedicine
McEwen, B. S., & Wingfield, J. C. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(02)00024-7 · Cited by 3,302 · cited 1× · see citing works
“The maintenance of flexibility, variability, and rhythmicity in HPA functioning are important healthy allostatic components (McEwen & Wingfield, 2003).”
BackgroundHandbook of emotion regulation
Gross, J. (2014) · Choice Reviews Online · doi:10.5860/choice.52-1127 · Cited by 3,280 · see citing works
Drug Addiction, Dysregulation of Reward, and Allostasis
Koob, G. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(00)00195-0 · Cited by 2,953 · see citing works
Risky families: Family social environments and the mental and physical health of offspring
Repetti, R. L., Taylor, S. E., & Seeman, T. E. (2002) · Psychological Bulletin · doi:10.1037/0033-2909.128.2.330 · Cited by 2,884 · see citing works
Allostatic load biomarkers of chronic stress and impact on health and cognition
Juster, R.-P., McEwen, B. S., & Lupien, S. J. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.10.002 · Cited by 2,565 · see citing works
Goodman, S. H., & Gotlib, I. H. (1999) · Psychological Review · doi:10.1037/0033-295x.106.3.458 · Cited by 2,493 · see citing works
Miller, G. E., Chen, E., & Zhou, E. S. (2007) · Psychological Bulletin · doi:10.1037/0033-2909.133.1.25 · Cited by 2,467 · see citing works
BOYCE, W. T., & ELLIS, B. J. (2005) · Development and Psychopathology · doi:10.1017/s0954579405050145 · Cited by 2,078 · see citing works
The neurobiology of stress and development.
Gunnar, M., & Quevedo, K. (2007) · Annual Review of Psychology · doi:10.1146/annurev.psych.58.110405.085605 · Cited by 2,011 · cited 10× · see citing works
“…the allostatic process is the growing body of research focused on the neurobiology of stress during childhood, including the primary allostatic mediators of the HPA axis and sympathetic–adrenomedullary (SAM) system and associated corticolimbic pathways (reviewed in Gunnar & Quevedo, 2007).”
BackgroundResultInfluentialThe link between childhood trauma and depression: insights from HPA axis studies in humans
Heim, C., Newport, D. J., Mletzko, T., Miller, A. H., & Nemeroff, C. B. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.03.008 · Cited by 1,704 · see citing works
Addiction and the brain antireward system
Koob, G. F., & Le Moal, M. (2008) · Annual Review of Psychology · doi:10.1146/annurev.psych.59.103006.093548 · Cited by 1,457 · see citing works
The Adaptive Calibration Model of stress responsivity
Del Giudice, M., Ellis, B. J., & Shirtcliff, E. A. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.11.007 · Cited by 1,373 · see citing works
Self-citationMurray, L., Fiori-Cowley, A., Hooper, R., & Cooper, P. (1996) · Child Development · doi:10.2307/1131637 · Cited by 1,311 · see citing works
Risk and Protective Factors in the Development of Psychopathology
(1990) · Cambridge University Press eBooks · doi:10.1017/cbo9780511752872 · Cited by 1,305 · see citing works
Murray, L., Fiori-Cowley, A., Hooper, R., & Cooper, P. (1996) · Child Development · doi:10.1111/j.1467-8624.1996.tb01871.x · Cited by 1,302 · see citing works
Connell, A. M., & Goodman, S. H. (2002) · Psychological Bulletin · doi:10.1037/0033-2909.128.5.746 · Cited by 956 · see citing works
Cummings, E. M., & Davies, P. T. (2002) · Journal of Child Psychology and Psychiatry · doi:10.1111/1469-7610.00003 · Cited by 891 · see citing works
Paternal depression in the postnatal period and child development: a prospective population study
Ramchandani, P., Stein, A., Evans, J., & O'Connor, T. G. (2005) · The Lancet · doi:10.1016/s0140-6736(05)66778-5 · Cited by 819 · see citing works
KRAEMER, H. C., Measelle, J. R., Ablow, J. C., Essex, M. J., Boyce, W. T., & Kupfer, D. J. (2003) · American Journal of Psychiatry · doi:10.1176/appi.ajp.160.9.1566 · Cited by 765 · see citing works
Self-citationChild maltreatment and the developing HPA axis
Tarullo, A. R., & Gunnar, M. R. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.010 · Cited by 737 · see citing works
Neurobiological mechanisms for opponent motivational processes in addiction
Koob, G. F., & Moal, M. L. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2008.0094 · Cited by 702 · see citing works
Essex, M. J., Klein, M. H., Cho, E., & Kalin, N. H. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01553-6 · Cited by 698 · see citing works
Self-citationMaternal 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
A multimethodological analysis of cumulative risk and allostatic load among rural children
Evans, G. W. (2003) · Developmental Psychology · doi:10.1037/0012-1649.39.5.924 · Cited by 624 · see citing works
Cicchetti, D., & Toth, S. L. (2008) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2008.01979.x · Cited by 617 · see citing works
Neurobiological and psychiatric consequences of child abuse and neglect
Heim, C., Shugart, M., Craighead, W. E., & Nemeroff, C. B. (2010) · Developmental Psychobiology · doi:10.1002/dev.20494 · Cited by 613 · see citing works
The Developmental Psychopathology of Anxiety
Vasey, M. W., Bosmans, G., & Ollendick, T. H. (2014) · Springer eBooks · doi:10.1007/978-1-4614-9608-3_27 · Cited by 605 · see citing works
Effects of paternal depression on fathers' parenting behaviors: a meta-analytic review
Wilson, S., & Durbin, C. E. (2010) · Clinical Psychology Review · doi:10.1016/j.cpr.2009.10.007 · Cited by 603 · see citing works
Research Review: The neurobiology and genetics of maltreatment and adversity
McCrory, E., De Brito, S. A., & Viding, E. (2010) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2010.02271.x · Cited by 598 · see citing works
LUPIEN, S. J., King, S., Meaney, M. J., & McEwen, B. S. (2001) · Development and Psychopathology · doi:10.1017/s0954579401003133 · Cited by 594 · see citing works
Child's stress hormone levels correlate with mother's socioeconomic status and depressive state
Lupien, S. J., King, S., Meaney, M. J., & McEwen, B. S. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)00965-3 · Cited by 532 · see citing works
Salivary cortisol levels in children adopted from Romanian orphanages
GUNNAR, M. R., MORISON, S. J., CHISHOLM, K., & SCHUDER, M. (2001) · Development and Psychopathology · doi:10.1017/s095457940100311x · Cited by 517 · see citing works
The Development of Self-Control of Emotion: Intrinsic and Extrinsic Influences
Fox, N. A., & Calkins, S. D. (2003) · Motivation and Emotion · doi:10.1023/a:1023622324898 · Cited by 488 · see citing works
Cicchetti, D., & Valentino, K. (2015) · Wiley eBooks · doi:10.1002/9780470939406.ch4 · Cited by 469 · see citing works
Diverse patterns of neuroendocrine activity in maltreated children
Cicchetti, D., & Rogosch, F. (2001) · Development and Psychopathology · doi:10.1017/s0954579401003145 · Cited by 437 · see citing works
Marceau, K., Ram, N., Houts, R. M., Grimm, K. J., & Susman, E. J. (2011) · Developmental Psychology · doi:10.1037/a0023838 · Cited by 389 · see citing works
ELLIS, B. J., ESSEX, M. J., & BOYCE, W. T. (2005) · Development and Psychopathology · doi:10.1017/s0954579405050157 · Cited by 383 · see citing works
Self-citationFamily socialization of emotional expression and nonverbal communication styles and skills.
Halberstadt, A. G. (1986) · Journal of Personality and Social Psychology · doi:10.1037//0022-3514.51.4.827 · Cited by 369 · see citing works
Grych, J. H., Fincham, F. D., Jouriles, E. N., & McDonald, R. (2000) · Child Development · doi:10.1111/1467-8624.00255 · Cited by 351 · see citing works
Risk and resilience: genetic and environmental influences on development of the stress response
Gillespie, C. F., Phifer, J., Bradley, B., & Ressler, K. J. (2009) · Depression and Anxiety · doi:10.1002/da.20605 · Cited by 351 · see citing works
The Experience, Expression, and Control of Anger
Spielberger, C. D., Krasner, S. S., & Solomon, E. P. (1988) · Contributions to psychology and medicine · doi:10.1007/978-1-4612-3824-9_5 · Cited by 348 · see citing works
Depressive Disorders in Maltreated Children
Kaufman, J. (1991) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-199103000-00014 · Cited by 346 · see citing works
Calkins, S. D., & Hill, A. (2007) · Cited by 340 · see citing works
Cicchetti, D., Rogosch, F. A., Gunnar, M. R., & Toth, S. L. (2010) · Child Development · doi:10.1111/j.1467-8624.2009.01393.x · Cited by 337 · see citing works
Parental investment theory and gender differences in the evolution of inhibition mechanisms.
Bjorklund, D. F., & Kipp, K. (1996) · Psychological Bulletin · doi:10.1037/0033-2909.120.2.163 · Cited by 328 · see citing works
Stress hormone levels of children of depressed mothers
ASHMAN, S. B., DAWSON, G., PANAGIOTIDES, H., YAMADA, E., & WILKINSON, C. W. (2002) · Development and Psychopathology · doi:10.1017/s0954579402002080 · Cited by 310 · see citing works
Estimating between- and within-individual variation in cortisol levels using multilevel models
Hruschka, D. J., Kohrt, B. A., & Worthman, C. M. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.03.002 · Cited by 303 · see citing works
Development of perceptual expertise in emotion recognition
Pollak, S. D., Messner, M., Kistler, D. J., & Cohn, J. F. (2008) · Cognition · doi:10.1016/j.cognition.2008.10.010 · Cited by 302 · see citing works
'Big build': hidden depression in men
Brownhill, S., Wilhelm, K. A., Barclay, L. M., & Schmied, V. A. (2005) · Australian & New Zealand Journal of Psychiatry · doi:10.1080/j.1440-1614.2005.01665.x · Cited by 300 · see citing works
Stress Neurobiology and Developmental Psychopathology
Gunnar, M. R., & Vázquez, D. M. (2015) · Wiley eBooks · doi:10.1002/9780470939390.ch13 · Cited by 291 · see citing works
Kochanska, G., Philibert, R. A., & Barry, R. A. (2009) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2008.02050.x · Cited by 272 · see citing works
Low salivary cortisol levels and externalizing behavior problems in youth
SHIRTCLIFF, E. A., GRANGER, D. A., BOOTH, A., & JOHNSON, D. (2005) · Development and Psychopathology · doi:10.1017/s0954579405050091 · Cited by 264 · see citing works
Self-citationESSEX, M. J., BOYCE, W. T., GOLDSTEIN, L. H., ARMSTRONG, J. M., KRAEMER, H. C., & KUPFER, D. J. (2002) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-200205000-00017 · Cited by 253 · see citing works
Self-citationMaternity Leave And Women's Mental Health
Hyde, J. S., Klein, M. H., Essex, M. J., & Clark, R. (1995) · Psychology of Women Quarterly · doi:10.1111/j.1471-6402.1995.tb00291.x · Cited by 253 · see citing works
Self-citationThe impact of early adverse care on HPA axis development: Nonhuman primate models
Sánchez, M. M. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.012 · Cited by 247 · see citing works
Neurobiology of empathy and callousness: Implications for the development of antisocial behavior
Shirtcliff, E. A., Vitacco, M. J., Graf, A., Gostisha, A. J., Merz, J., & Zahn‐Waxler, C. (2009) · Behavioral Sciences & the Law · doi:10.1002/bsl.862 · Cited by 244 · see citing works
Self-citationThe psychobiology of emotion: the role of the oxytocinergic system
Uvnäs-Moberg, K., Arn, I., & Magnusson, D. (2005) · International Journal of Behavioral Medicine · doi:10.1207/s15327558ijbm1202_3 · Cited by 238 · see citing works
Exploring Risk Factors for the Emergence of Children's Mental Health Problems
Essex, M. J., Kraemer, H. C., Armstrong, J. M., Boyce, W. T., Goldsmith, H. H., Klein, M. H., Woodward, H., & Kupfer, D. J. (2006) · Archives of General Psychiatry · doi:10.1001/archpsyc.63.11.1246 · Cited by 233 · see citing works
Self-citationMaternal depression and infant cortisol: influences of timing, comorbidity and treatment
Brennan, P. A., Pargas, R. C. M., Walker, E. F., Green, P., Newport, D. J., & Stowe, Z. N. (2008) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2008.01914.x · Cited by 233 · see citing works
Shirtcliff, E. A., & Essex, M. J. (2008) · Developmental Psychobiology · doi:10.1002/dev.20336 · Cited by 231 · see citing works
Self-citationShirtcliff, E. A., Allison, A. L., Armstrong, J. M., Slattery, M. J., Kalin, N. H., & Essex, M. J. (2011) · Developmental Psychobiology · doi:10.1002/dev.20607 · Cited by 230 · see citing works
Self-citationHalligan, S. L., Herbert, J., Goodyer, I., & Murray, L. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.09.011 · Cited by 217 · see citing works
A historical perspective on the discipline of developmental psychopathology
Cicchetti, D. (1990) · Cambridge University Press eBooks · doi:10.1017/cbo9780511752872.003 · Cited by 216 · see citing works
Ellis, B. J., Shirtcliff, E. A., Boyce, W. T., Deardorff, J., & Essex, M. J. (2011) · Development and Psychopathology · doi:10.1017/s0954579410000660 · Cited by 210 · see citing works
Self-citationKnutsson, U., Dahlgren, J., Marcus, C., Rosberg, S., Brönnegård, M., Stierna, P., & Albertsson-Wikland, K. G. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.2.3769 · Cited by 209 · see citing works
Childhood Stress and Family Environment
Flinn, M. V., & England, B. G. (1995) · Current Anthropology · doi:10.1086/204444 · Cited by 208 · see citing works
Child Maltreatment and Adolescent Development
Trickett, P. K., Negriff, S. L., Ji, J., & Peckins, M. K. (2011) · Journal of Research on Adolescence · doi:10.1111/j.1532-7795.2010.00711.x · Cited by 203 · see citing works
Harkness, K. L., Stewart, J. G., & Wynne‐Edwards, K. E. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.07.006 · Cited by 200 · see citing works
Neuroendocrine dysregulation following early social deprivation in children
Fries, A. B. W., Shirtcliff, E. A., & Pollak, S. D. (2008) · Developmental Psychobiology · doi:10.1002/dev.20319 · Cited by 192 · see citing works
Self-citationRuttle, P. L., Shirtcliff, E. A., Serbin, L. A., Fisher, D. B., Stack, D. M., & Schwartzman, A. E. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.10.015 · Cited by 188 · see citing works
Self-citationAltered neuroendocrine activity in maltreated children related to symptoms of depression
Hart, J., Gunnar, M., & Cicchetti, D. (1996) · Development and Psychopathology · doi:10.1017/s0954579400007045 · Cited by 188 · see citing works
Intervention effects on foster parent stress: Associations with child cortisol levels
Fisher, P. A., & Stoolmiller, M. (2008) · Development and Psychopathology · doi:10.1017/s0954579408000473 · Cited by 186 · see citing works
Screening for childhood mental health problems: outcomes and early identification
Essex, M. J., KRAEMER, H. C., Slattery, M. J., Burk, L. R., Boyce, W. T., Woodward, H. R., & Kupfer, D. J. (2009) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2008.02015.x · Cited by 181 · see citing works
Self-citationPendry, P., & Adam, E. K. (2007) · International Journal of Behavioral Development · doi:10.1177/0165025407074634 · Cited by 181 · see citing works
Anger Attacks in Depression – Evidence for a Male Depressive Syndrome
Winkler, D., Pjrek, E., & Kasper, S. F. (2005) · Psychotherapy and Psychosomatics · doi:10.1159/000086321 · Cited by 180 · see citing works
Essex, M. J., Klein, M. H., Cho, E., & KRAEMER, H. C. (2003) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/01.chi.0000046849.56865.1d · Cited by 177 · see citing works
Self-citationDavies, P. T., Sturge-Apple, M. L., Cicchetti, D., & Cummings, E. M. (2007) · Developmental Psychology · doi:10.1037/0012-1649.43.4.918 · Cited by 171 · see citing works
Cicchetti, D., & Rogosch, F. A. (2007) · Development and Psychopathology · doi:10.1017/s0954579407000399 · Cited by 168 · cited 2× · see citing works
“…including social and academic functioning, cognitive styles and biases, emotional/behavioral dysregulation, and alterations in stress neurobiology (Cicchetti & Rogosch, 2007; Cicchetti & Valentino, 2006; Essex et al., 2006; Gunnar & Quevedo, 2007; Heim, Shugart, Craighead, & Nemeroff, 2010).”
BackgroundBernard, K., & Dozier, M. (2010) · Developmental Psychology · doi:10.1037/a0020660 · Cited by 167 · see citing works
Multilevel perspectives on pathways to resilient functioning
Cicchetti, D., & Curtis, W. J. (2007) · Development and Psychopathology · doi:10.1017/s0954579407000314 · Cited by 156 · see citing works
(2009) · doi:10.5005/jp/books/11350_6 · Cited by 156 · see citing works
BOYCE, W. T., ESSEX, M. J., ALKON, A., GOLDSMITH, H. H., KRAEMER, H. C., & KUPFER, D. J. (2006) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/01.chi.0000237706.50884.8b · Cited by 150 · see citing works
Self-citationBeyond the Stress Concept: Allostatic Load—A Developmental Biological and Cognitive Perspective
Lupien, S., Ouellet-Morin, I., Hupbach, A., Tu, M., Buss, C., Walker, D., Pruessner, J., & McEwen, B. (2015) · Wiley eBooks · doi:10.1002/9780470939390.ch14 · Cited by 149 · see citing works
Toth, S. L., Rogosch, F. A., Sturge‐Apple, M. L., & Cicchetti, D. (2009) · Child Development · doi:10.1111/j.1467-8624.2008.01254.x · Cited by 141 · see citing works
Knutsson, U. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.82.2.536 · Cited by 140 · see citing works
Cicchetti, D., & Curtis, W. J. (2015) · Wiley eBooks · doi:10.1002/9780470939390.ch1 · Cited by 136 · see citing works
Bureau, J.-F., Easterbrooks, M. A., & Lyons-Ruth, K. (2009) · Development and Psychopathology · doi:10.1017/s0954579409000285 · Cited by 132 · see citing works
The past as prologue to the future: The times, they've been a-changin'
Cicchetti, D., & Sroufe, L. A. (2000) · Development and Psychopathology · doi:10.1017/s0954579400003011 · Cited by 131 · see citing works
Kim, J., Cicchetti, D., Rogosch, F. A., & Manly, J. T. (2009) · Development and Psychopathology · doi:10.1017/s0954579409000480 · Cited by 129 · see citing works
Gross, H. E., Shaw, D. S., Moilanen, K. L., Dishion, T. J., & Wilson, M. N. (2008) · Journal of Family Psychology · doi:10.1037/a0013514 · Cited by 122 · see citing works
Feng, X., Shaw, D. S., Skuban, E. M., & Lane, T. J. (2007) · Journal of Family Psychology · doi:10.1037/0893-3200.21.4.714 · Cited by 114 · see citing works
Boyce, W. T., Essex, M. J., Woodward, H. R., Measelle, J. R., Ablow, J. C., & Kupfer, D. J. (2002) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-200205000-00016 · Cited by 112 · see citing works
Self-citationSchreiber, J. E., Shirtcliff, E., Hulle, C. V., Lemery-Chalfant, K., Klein, M. H., Kalin, N. H., Essex, M. J., & Goldsmith, H. H. (2006) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2006.07.005 · Cited by 112 · see citing works
Self-citationAllostasis model facilitates understanding race differences in the diurnal cortisol rhythm
Skinner, M. L., Shirtcliff, E. A., Haggerty, K. P., Coe, C. L., & Catalano, R. F. (2011) · Development and Psychopathology · doi:10.1017/s095457941100054x · Cited by 104 · see citing works
Self-citationTrapolini, T., Ungerer, J. A., & McMahon, C. A. (2008) · Attachment & Human Development · doi:10.1080/14616730801900712 · Cited by 104 · see citing works
Murray, L., Halligan, S. L., Goodyer, I. M., & Herbert, J. (2009) · Journal of Affective Disorders · doi:10.1016/j.jad.2009.06.034 · Cited by 94 · see citing works
Cicchetti, D., & Blender, J. A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408033101 · Cited by 92 · see citing works
Weems, C. F., & Carrión, V. G. (2007) · Journal of Traumatic Stress · doi:10.1002/jts.20251 · Cited by 92 · see citing works
Fathering in family context and child adjustment: A longitudinal analysis.
Schacht, P. M., Cummings, E. M., & Davies, P. T. (2009) · Journal of Family Psychology · doi:10.1037/a0016741 · Cited by 88 · see citing works
Coe, C. L., Lubach, G. R., & Shirtcliff, E. A. (2007) · Pediatric Research · doi:10.1203/pdr.0b013e318045be53 · Cited by 81 · see citing works
Self-citationHastings, P. D., Shirtcliff, E. A., Klimes‐Dougan, B., Allison, A. L., DeRose, L. M., Kendziora, K. T., Usher, B. A., & Zahn‐Waxler, C. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000538 · Cited by 80 · see citing works
Self-citationFather contributions to cortisol responses in infancy and toddlerhood.
Mills-Koonce, R., Family Life Project, Garrett-Peters, P., Barnett, M. A., Granger, D. A., Blair, C., & Cox, M. J. (2010) · Developmental Psychology · doi:10.1037/a0021066 · Cited by 80 · see citing works
Hastings, P. D., Ruttle, P. L., Serbin, L. A., Mills, R. S. L., Stack, D. M., & Schwartzman, A. E. (2011) · Developmental Psychobiology · doi:10.1002/dev.20545 · Cited by 76 · see citing works
Self-citationDavies, P. T., Sturge‐Apple, M. L., Cicchetti, D., Manning, L. G., & Zale, E. (2009) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2009.02154.x · Cited by 70 · see citing works
Koss, K. J., George, M. R. W., Bergman, K. N., Cummings, E. M., Davies, P. T., & Cicchetti, D. (2011) · Journal of Experimental Child Psychology · doi:10.1016/j.jecp.2011.02.007 · Cited by 63 · see citing works
The Role of Glucocorticoids in Anxiety Disorders: A Critical Analysis
Gunnar, M. R. (2001) · Oxford University Press eBooks · doi:10.1093/med:psych/9780195123630.003.0007 · Cited by 59 · see citing works
Depressive symptoms in mothers and children: Preschool attachment as a moderator of risk.
Milan, S., Snow, S. T., & Belay, S. (2009) · Developmental Psychology · doi:10.1037/a0016164 · Cited by 51 · see citing works
Attachment patterns and emotion regulation strategies in the second year
Crugnola, C. R., Tambelli, R., Spinelli, M., Gazzotti, S., Caprin, C., & Albizzati, A. (2010) · Infant Behavior and Development · doi:10.1016/j.infbeh.2010.11.002 · Cited by 48 · see citing works
Marital conflict typology and children's appraisals: The moderating role of family cohesion.
Lindahl, K. M., & Malik, N. (2011) · Journal of Family Psychology · doi:10.1037/a0022888 · Cited by 46 · see citing works
Maternal Sensitivity and Communication Styles
Hwa-Froelich, D. A., Cook, C. A. L., & Flick, L. H. (2008) · Journal of Early Intervention · doi:10.1177/1053815108324754 · Cited by 44 · see citing works
Masharani, U. B., Shiboski, S. C., Eisner, M. D., Katz, P., Janson, S. L., Granger, D. A., & Blanc, P. D. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.03.003 · Cited by 43 · see citing works
Weems, C. F., & Carrión, V. G. (2008) · Journal of Pediatric Psychology · doi:10.1093/jpepsy/jsn087 · Cited by 33 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
Self-citationThe neurobiology of depression and antidepressant action
Willner, P., Scheel-Krüger, J., & Belzung, C. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.12.007 · Cited by 519 · see citing works
Barlow, D. H., Ellard, K. K., Sauer-Zavala, S., Bullis, J. R., & Carl, J. R. (2014) · Perspectives on Psychological Science · doi:10.1177/1745691614544528 · Cited by 491 · see citing works
Developmental pathways to amygdala–prefrontal function and internalizing symptoms in adolescence
Burghy, C. A., Stodola, D. E., Ruttle, P. L., Molloy, E. K., Armstrong, J. M., Oler, J. A., Fox, M. E., Hayes, A. S., Kalin, N. H., Essex, M. J., et al. (2012) · Nature Neuroscience · doi:10.1038/nn.3257 · Cited by 397 · see citing works
Self-citationAdverse Childhood Experiences and Child Health in Early Adolescence
Flaherty, E. G., Thompson, R., Dubowitz, H., Harvey, E. M., English, D. J., Proctor, L. J., & Runyan, D. K. (2013) · JAMA Pediatrics · doi:10.1001/jamapediatrics.2013.22 · Cited by 353 · see citing works
Malleability, plasticity, and individuality: How children learn and develop in context<sup>1</sup>
Cantor, P., Osher, D., Berg, J., Steyer, L., & Rose, T. (2019) · Applied Developmental Science · doi:10.1080/10888691.2017.1398649 · Cited by 328 · see citing works
“The functioning of such brain regions is affected long before children start school and impacts key learning systems, including self-regulation, executive functions, attention, memory, stress reactivity, and language (e.g., Essex et al., 2011).”
BackgroundPruessner, M., Cullen, A. E., Aas, M., & Walker, E. F. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.12.013 · Cited by 315 · see citing works
Beyond allostatic load: Rethinking the role of stress in regulating human development
Ellis, B. J., & Del Giudice, M. (2014) · Development and Psychopathology · doi:10.1017/s0954579413000849 · Cited by 290 · see citing works
Theall, K. P., Brett, Z. H., Shirtcliff, E. A., Dunn, E. C., & Drury, S. S. (2013) · Social Science & Medicine · doi:10.1016/j.socscimed.2013.02.030 · Cited by 175 · see citing works
Self-citationMaternal PTSD associates with greater glucocorticoid sensitivity in offspring of Holocaust survivors
Lehrner, A., Bierer, L. M., Passarelli, V., Pratchett, L. C., Flory, J. D., Bader, H. N., Harris, I. R., Bedi, A., Daskalakis, N. P., Makotkine, I., et al. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.11.019 · Cited by 160 · see citing works
Hostinar, C. E., & Gunnar, M. R. (2013) · Journal of Clinical Child & Adolescent Psychology · doi:10.1080/15374416.2013.804387 · Cited by 153 · see citing works
Bick, J., Naumova, O., Hunter, S., Barbot, B., Lee, M., Luthar, S. S., Raefski, A., & Grigorenko, E. L. (2012) · Development and Psychopathology · doi:10.1017/s0954579412000806 · Cited by 140 · see citing works
Latent trait cortisol (LTC) levels: Reliability, validity, and stability
Doane, L. D., Chen, F. R., Sladek, M. R., Van Lenten, S. A., & Granger, D. A. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.01.017 · Cited by 79 · see citing works
Cordero, M. I., Moser, D. A., Manini, A., Suardi, F., Sancho-Rossignol, A., Torrisi, R., Rossier, M. F., Ansermet, F., Dayer, A. G., Rusconi-Serpa, S., et al. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.02.007 · Cited by 72 · see citing works
Age of trauma onset and HPA axis dysregulation among trauma-exposed youth
Kuhlman, K. R., Vargas, I., Geiss, E. G., & Lopez‐Duran, N. L. (2015) · Journal of Traumatic Stress · doi:10.1002/jts.22054 · Cited by 75 · see citing works
Oler, J. A., Birn, R. M., Patriat, R., Fox, A. S., Shelton, S. E., Burghy, C. A., Stodola, D. E., Essex, M. J., Davidson, R. J., & Kalin, N. H. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.03.045 · Cited by 67 · see citing works
Self-citationValentino, K., Hibel, L. C., Cummings, E. M., Nuttall, A. K., Comas, M., & McDonnell, C. G. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000917 · Cited by 48 · see citing works
Boschen, K. E., Keller, S. M., Roth, T. L., & Klintsova, A. Y. (2018) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2017.12.009 · Cited by 24 · see citing works
Nephew, B., Murgatroyd, C., Pittet, F., & Febo, M. (2015) · Journal of Reward Deficiency Syndrome · doi:10.17756/jrds.2015-017 · Cited by 20 · see citing works
- Authors
- Essex, M. J., Shirtcliff, E. A., Burk, L. R., Ruttle, P. L., Klein, M. H., Slattery, M. J., Kalin, N. H., & Armstrong, J. M.
- Affiliations
- University of Wisconsin–Madison (US)
- LSU New Orleans (US)
- Corresponding author
- Essex, Marilyn J.
- Venue
- Development and Psychopathology
- Publisher
- Cambridge University Press (CUP)
- Published
- 2011-10-21
- Volume
- 23
- Issue
- 4
- Pages
- 1039-1058
- ISSN
- 0954-5794 (ISSN-L)
- 1469-2198
- PMC
- PMC3266106
- OpenAlex
- W2120681311
- Cited by
- 212
- References
- 117
- Citations by year
- 2026: 11 · 2025: 8 · 2024: 5 · 2023: 9 · 2022: 8 · 2021: 10 · 2020: 15 · 2019: 12 · 2018: 16 · 2017: 17 · 2016: 21 · 2015: 21 · 2014: 28 · 2013: 20 · 2012: 9
- FWCI
- 7.38
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Development and Psychopathology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (P50MH052354, K01MH077687, P50MH069315, R01MH044340, P50MH084051)
- National Center for Research Resources (UL1RR025011)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P30HD003352)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Social Sciences › Psychology › Clinical Psychology › Child and Adolescent Psychosocial and Emotional Development
- Keywords
- early life stress, hypothalamic-pituitary-adrenal axis, cortisol, maternal depression, paternal depression, psychiatric symptoms, hyperarousal, hypoarousal, children, adolescence, HPA axis reactivity
- MeSH terms
- Adolescent, Adult, Anger, Mental Disorders, Child, Child, Preschool, Circadian Rhythm, Depressive Disorder, Family, Female, Humans, Hydrocortisone, Hypothalamo-Hypophyseal System, Infant, Longitudinal Studies, Male, Pituitary-Adrenal System, Saliva, Stress, Psychological, Child of Impaired Parents
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review