Beating the brain about abuse: Empirical and meta-analytic studies of the association between maltreatment and hippocampal volume across childhood and adolescence

Abstract We present new empirical data and meta-analytic evidence for the association of childhood maltreatment with reduced hippocampal volume. In Study 1, we examined the effects of maltreatment experiences reported during the Adult Attachment Interview on hippocampal volume in female twin pairs. We found that reduced hippocampal volume was related to childhood maltreatment. In addition, individuals who reported having experienced maltreatment at older ages had larger reductions in hippocampal volume compared to individuals who reported maltreatment in early childhood. In Study 2, we present the results of a meta-analysis of 49 studies (including 2,720 participants) examining hippocampal volume in relation to experiences of child maltreatment, and test the moderating role of the timing of the maltreatment, the severity of maltreatment, and the time after exposure to maltreatment. The results of the meta-analysis confirmed that experiences of childhood maltreatment are associated with a reduction in hippocampal volume and that the effects of maltreatment are more pronounced when the maltreatment occurs in middle childhood compared to early childhood or adolescence.

[1]  I. Myin-Germeys,et al.  Brain-Derived Neurotrophic Factor/FK506-Binding Protein 5 Genotype by Childhood Trauma Interactions Do Not Impact on Hippocampal Volume and Cognitive Performance , 2014, PloS one.

[2]  D. Veltman,et al.  Can pharmacological and psychological treatment change brain structure and function in PTSD? A systematic review. , 2014, Journal of psychiatric research.

[3]  H. Steele,et al.  Adverse Childhood Experiences (ACEs) questionnaire and Adult Attachment Interview (AAI): implications for parent child relationships. , 2014, Child abuse & neglect.

[4]  F. Woermann,et al.  Mesiotemporal Volume Loss Associated with Disorder Severity: A VBM Study in Borderline Personality Disorder , 2013, PloS one.

[5]  Martin H. Teicher,et al.  Childhood maltreatment and psychopathology: A case for ecophenotypic variants as clinically and neurobiologically distinct subtypes. , 2013, The American journal of psychiatry.

[6]  L. Williams,et al.  Early Exposure to Traumatic Stressors Impairs Emotional Brain Circuitry , 2013, PloS one.

[7]  M. Yücel,et al.  Childhood maltreatment and psychopathology affect brain development during adolescence. , 2013, Journal of the American Academy of Child and Adolescent Psychiatry.

[8]  P. DeRosse,et al.  Sex differences in resilience to childhood maltreatment: effects of trauma history on hippocampal volume, general cognition and subclinical psychosis in healthy adults. , 2013, Journal of psychiatric research.

[9]  Laurie M. Baker,et al.  Impact of early vs. late childhood early life stress on brain morphometrics , 2013, Brain Imaging and Behavior.

[10]  Julia M. Sheffield,et al.  Reduced gray matter volume in psychotic disorder patients with a history of childhood sexual abuse , 2013, Schizophrenia Research.

[11]  J. Meaney,et al.  Early life adversity is associated with brain changes in subjects at family risk for depression , 2012, The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry.

[12]  S. Cooper,et al.  Childhood trauma and hippocampal and amygdalar volumes in first-episode psychosis. , 2012, Schizophrenia bulletin.

[13]  Theo Vos,et al.  The Long-Term Health Consequences of Child Physical Abuse, Emotional Abuse, and Neglect: A Systematic Review and Meta-Analysis , 2012, PLoS medicine.

[14]  C. Zeanah,et al.  Diagnosing PTSD in early childhood: an empirical assessment of four approaches. , 2012, Journal of traumatic stress.

[15]  Maarten A. S. Boksem,et al.  No Laughing Matter: Intranasal Oxytocin Administration Changes Functional Brain Connectivity during Exposure to Infant Laughter , 2012, Neuropsychopharmacology.

[16]  Walter Heindel,et al.  Limbic Scars: Long-Term Consequences of Childhood Maltreatment Revealed by Functional and Structural Magnetic Resonance Imaging , 2012, Biological Psychiatry.

[17]  Martin H. Teicher,et al.  Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum , 2012, Proceedings of the National Academy of Sciences.

[18]  Rajita Sinha,et al.  Corticostriatal-limbic gray matter morphology in adolescents with self-reported exposure to childhood maltreatment. , 2011, Archives of pediatrics & adolescent medicine.

[19]  A. Danese,et al.  Childhood maltreatment predicts unfavorable course of illness and treatment outcome in depression: a meta-analysis. , 2011, The American journal of psychiatry.

[20]  Maarten A. S. Boksem,et al.  Oxytocin Modulates Amygdala, Insula, and Inferior Frontal Gyrus Responses to Infant Crying: A Randomized Controlled Trial , 2011, Biological Psychiatry.

[21]  Essi Viding,et al.  The Impact of Childhood Maltreatment: A Review of Neurobiological and Genetic Factors , 2011, Front. Psychiatry.

[22]  C. Peterson,et al.  Infantile amnesia across the years: a 2-year follow-up of children's earliest memories. , 2011, Child development.

[23]  G. Rambaldelli,et al.  Dorsolateral prefrontal cortex and hippocampus sustain impulsivity and aggressiveness in borderline personality disorder. , 2011, Journal of affective disorders.

[24]  L. Price,et al.  Effect of childhood physical abuse on cortisol stress response , 2011, Psychopharmacology.

[25]  M. Bakermans-Kranenburg,et al.  Physiological reactivity to infant crying: a behavioral genetic study , 2010, Genes, brain, and behavior.

[26]  N. Koutsouleris,et al.  Interaction of childhood stress with hippocampus and prefrontal cortex volume reduction in major depression. , 2010, Journal of psychiatric research.

[27]  Essi Viding,et al.  Research review: the neurobiology and genetics of maltreatment and adversity. , 2010, Journal of child psychology and psychiatry, and allied disciplines.

[28]  J. Martineau,et al.  Preserved subcortical volumes and cortical thickness in women with sexual abuse-related PTSD , 2010, Psychiatry Research: Neuroimaging.

[29]  D. Veltman,et al.  Reduced anterior cingulate and orbitofrontal volumes in child abuse-related complex PTSD. , 2010, The Journal of clinical psychiatry.

[30]  P. Ellis,et al.  Prospectively ascertained child maltreatment and its association with DSM-IV mental disorders in young adults. , 2010, Archives of general psychiatry.

[31]  Brian B. Avants,et al.  Early parental care is important for hippocampal maturation: Evidence from brain morphology in humans , 2010, NeuroImage.

[32]  G. Weniger,et al.  Reduced amygdala and hippocampus size in trauma-exposed women with borderline personality disorder and without posttraumatic stress disorder. , 2009, Journal of psychiatry & neuroscience : JPN.

[33]  M. Rutter,et al.  Amygdala, hippocampal and corpus callosum size following severe early institutional deprivation: the English and Romanian Adoptees study pilot. , 2009, Journal of child psychology and psychiatry, and allied disciplines.

[34]  Larry V. Hedges,et al.  Fixed‐Effect Versus Random‐Effects Models , 2009, Introduction to Meta‐Analysis.

[35]  Gustavo Turecki,et al.  Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse , 2009, Nature Neuroscience.

[36]  Vaibhav Diwadkar,et al.  Structural brain abnormalities in borderline personality disorder: A voxel-based morphometry study , 2008, Psychiatry Research: Neuroimaging.

[37]  D. Hedges,et al.  Hippocampal and amygdala volumes in children and adults with childhood maltreatment‐related posttraumatic stress disorder: A meta‐analysis , 2008, Hippocampus.

[38]  Suzanne Wood,et al.  Reduced posterior hippocampal volume in posttraumatic stress disorder. , 2008, The Journal of clinical psychiatry.

[39]  Martin H. Teicher,et al.  Preliminary evidence for sensitive periods in the effect of childhood sexual abuse on regional brain development. , 2008, The Journal of neuropsychiatry and clinical neurosciences.

[40]  B. Egeland,et al.  Identification of child maltreatment using prospective and self-report methodologies: a comparison of maltreatment incidence and relation to later psychopathology. , 2008, Child abuse & neglect.

[41]  Martin H. Teicher,et al.  Stress, sensitive periods and maturational events in adolescent depression , 2008, Trends in Neurosciences.

[42]  K. Roelofs,et al.  Diminished cortisol responses to psychosocial stress associated with lifetime adverse events A study among healthy young subjects , 2008, Psychoneuroendocrinology.

[43]  C. Xiong,et al.  Childhood adversity predicts earlier onset of major depression but not reduced hippocampal volume , 2008, Psychiatry Research: Neuroimaging.

[44]  Sarah E. Scholin,et al.  Using Cue Words to Investigate the Distribution of Autobiographical Memories in Childhood , 2007, Psychological science.

[45]  H. Möller,et al.  Hippocampal volume reduction and history of aggressive behaviour in patients with borderline personality disorder , 2007, Psychiatry Research: Neuroimaging.

[46]  M. Gunnar,et al.  Bringing basic research on early experience and stress neurobiology to bear on preventive interventions for neglected and maltreated children. , 2006, Development and psychopathology.

[47]  Martin H. Teicher,et al.  Neurobiological Consequences of Early Stress and Childhood Maltreatment: Are Results from Human and Animal Studies Comparable? , 2006, Annals of the New York Academy of Sciences.

[48]  E. Gordon,et al.  Early Life Stress and Morphometry of the Adult Anterior Cingulate Cortex and Caudate Nuclei , 2006, Biological Psychiatry.

[49]  J. Read,et al.  Childhood trauma, psychosis and schizophrenia: a literature review with theoretical and clinical implications , 2005, Acta psychiatrica Scandinavica.

[50]  G. D. den Heeten,et al.  Effects of psychotherapy on hippocampal volume in out-patients with post-traumatic stress disorder: a MRI investigation , 2005, Psychological Medicine.

[51]  Desmond K. Runyan,et al.  The dimensions of maltreatment: introduction. , 2005, Child abuse & neglect.

[52]  C. Nemeroff,et al.  Effects of phenytoin on memory, cognition and brain structure in post-traumatic stress disorder: a pilot study , 2005, Journal of psychopharmacology.

[53]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[54]  Martin H. Teicher,et al.  Delayed Effects of Early Stress on Hippocampal Development , 2004, Neuropsychopharmacology.

[55]  Michael J Meaney,et al.  Epigenetic programming by maternal behavior , 2004, Nature Neuroscience.

[56]  R. Sullivan,et al.  Hemispheric Asymmetry in Stress Processing in Rat Prefrontal Cortex and the Role of Mesocortical Dopamine , 2004, Stress.

[57]  Cathy L Pederson,et al.  Hippocampal Volume and Memory Performance in a Community-Based Sample of Women with Posttraumatic Stress Disorder Secondary to Child Abuse , 2004, Journal of traumatic stress.

[58]  Steven M. Southwick,et al.  Long-term treatment with paroxetine increases verbal declarative memory and hippocampal volume in posttraumatic stress disorder , 2003, Biological Psychiatry.

[59]  S. Southwick,et al.  MRI and PET study of deficits in hippocampal structure and function in women with childhood sexual abuse and posttraumatic stress disorder. , 2003, The American journal of psychiatry.

[60]  M. Newcomb,et al.  Development and validation of a brief screening version of the Childhood Trauma Questionnaire. , 2003, Child abuse & neglect.

[61]  Eric Vermetten,et al.  Childhood trauma associated with smaller hippocampal volume in women with major depression. , 2002, The American journal of psychiatry.

[62]  Matcheri S. Keshavan,et al.  Brain structures in pediatric maltreatment-related posttraumatic stress disorder: a sociodemographically matched study , 2002, Biological Psychiatry.

[63]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[64]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[65]  Stephen M. Smith,et al.  Accurate, Robust, and Automated Longitudinal and Cross-Sectional Brain Change Analysis , 2002, NeuroImage.

[66]  D. Chapman,et al.  Adverse childhood experiences, alcoholic parents, and later risk of alcoholism and depression. , 2002, Psychiatric services.

[67]  E. Waters,et al.  Stability of attachment representations: the transition to marriage. , 2002, Developmental psychology.

[68]  K. Lynch,et al.  Childhood abuse as a risk factor for suicidal behavior in borderline personality disorder. , 2002, Journal of personality disorders.

[69]  O. Hart,et al.  The psychometric characteristics of the traumatic experiences checklist (TEC): first findings among psychiatric outpatients , 2002 .

[70]  Stephan Eliez,et al.  Attenuation of frontal asymmetry in pediatric posttraumatic stress disorder , 2001, Biological Psychiatry.

[71]  D. Cicchetti,et al.  The impact of child maltreatment and psychopathology on neuroendocrine functioning , 2001, Development and Psychopathology.

[72]  D. Cicchetti,et al.  Diverse patterns of neuroendocrine activity in maltreated children , 2001, Development and Psychopathology.

[73]  M. Gunnar,et al.  Low cortisol and a flattening of expected daytime rhythm: Potential indices of risk in human development , 2001, Development and Psychopathology.

[74]  K. Frustaci,et al.  A pilot longitudinal study of hippocampal volumes in pediatric maltreatment-related posttraumatic stress disorder , 2001, Biological Psychiatry.

[75]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[76]  P. Matthews,et al.  Normalized Accurate Measurement of Longitudinal Brain Change , 2001, Journal of computer assisted tomography.

[77]  M. Zwaan,et al.  Magnetic resonance imaging volumes of the hippocampus and the amygdala in women with borderline personality disorder and early traumatization. , 2000, Archives of general psychiatry.

[78]  F. Song,et al.  The causes, consequences and detection of publication bias in psychiatry , 2000, Acta psychiatrica Scandinavica.

[79]  D C Rubin,et al.  The distribution of early childhood memories , 2000, Memory.

[80]  David R. Jones,et al.  Empirical assessment of effect of publication bias on meta-analyses , 2000, BMJ : British Medical Journal.

[81]  S Duval,et al.  Trim and Fill: A Simple Funnel‐Plot–Based Method of Testing and Adjusting for Publication Bias in Meta‐Analysis , 2000, Biometrics.

[82]  D. Fergusson,et al.  The stability of child abuse reports: a longitudinal study of the reporting behaviour of young adults , 2000, Psychological Medicine.

[83]  E. Waters,et al.  Attachment security in infancy and early adulthood: a twenty-year longitudinal study. , 2000, Child development.

[84]  L. Sroufe,et al.  Attachment from infancy to early adulthood in a high-risk sample: continuity, discontinuity, and their correlates. , 2000, Child development.

[85]  B. J. Casey,et al.  Developmental traumatology part II: brain development∗ ∗ See accompanying Editorial, in this issue. , 1999, Biological Psychiatry.

[86]  M. Gunnar,et al.  Dampening of the cortisol response to handling at 3 months in human infants and its relation to sleep, circadian cortisol activity, and behavioral distress. , 1998, Developmental psychobiology.

[87]  M. Stein,et al.  Hippocampal volume in women victimized by childhood sexual abuse , 1997, Psychological Medicine.

[88]  R. Bronen,et al.  Magnetic resonance imaging-based measurement of hippocampal volume in posttraumatic stress disorder related to childhood physical and sexual abuse—a preliminary report , 1997, Biological Psychiatry.

[89]  E. Waters,et al.  Discriminant validity of the adult attachment interview. , 1996, Child development.

[90]  A. Bifulco,et al.  Childhood Experience of Care and Abuse (CECA): a retrospective interview measure. , 1994, Journal of child psychology and psychiatry, and allied disciplines.

[91]  D. Benoit,et al.  Stability and transmission of attachment across three generations. , 1994, Child development.

[92]  Marinus H. van IJzendoorn,et al.  Stability and Discriminant Validity of the Adult Attachment Interview: A Psychometric Study in Young Israeli Adults , 1994 .

[93]  R. Sapolsky,et al.  Hippocampal damage associated with prolonged glucocorticoid exposure in primates , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[94]  R. Sapolsky,et al.  Maturation of the adrenocortical stress response: Neuroendocrine control mechanisms and the stress hyporesponsive period , 1986, Brain Research Reviews.

[95]  B. McEwen,et al.  Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[96]  P. Magnus,et al.  Predicting zygosity in Norwegian twin pairs born 1915–1960 , 1983, Clinical genetics.

[97]  A. Mechelli,et al.  The University of Birmingham ( Live System ) Reduced orbitofrontal and temporal grey matter in a community sample of maltreated children , 2016 .

[98]  D. Cicchetti,et al.  Longitudinal associations among child maltreatment, social functioning, and cortisol regulation. , 2012, Developmental psychology.

[99]  A Stuchlík,et al.  Delayed effects of elevated corticosterone level on volume of hippocampal formation in laboratory rat. , 2010, Physiological research.

[100]  B. Quinn,et al.  Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. , 2010, Developmental science.

[101]  E. Hesse The Adult Attachment Interview: Protocol, method of analysis, and empirical studies. , 2008 .

[102]  M. Main,et al.  Studying differences in language usage in recounting attachment history: An introduction to the AAI. , 2008 .

[103]  C. Nemeroff,et al.  The role of early adverse experience and adulthood stress in the prediction of neuroendocrine stress reactivity in women: A multiple regression analysis , 2002, Depression and anxiety.

[104]  V. Felitti [The relationship of adverse childhood experiences to adult health: Turning gold into lead]. , 2002, Zeitschrift fur Psychosomatische Medizin und Psychotherapie.

[105]  Paul van Geert,et al.  A longitudinal study of basal cortisol in infants: Intra-individual variability, circadian rhythm and developmental trends , 2002 .

[106]  Vincent J. Felitti Belastungen in der Kindheit und Gesundheit im Erwachsenenalter: die Verwandlung von Gold in Blei. , 2002 .

[107]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

[108]  E. Waters,et al.  The stability of attachment security from infancy to adolescence and early adulthood: general introduction. , 2000, Child development.

[109]  F. Frankenburg,et al.  Biparental failure in the childhood experiences of borderline patients. , 2000, Journal of personality disorders.

[110]  M. Bakermans-Kranenburg,et al.  A Psychometric Study of the Adult Attachment Interview : Reliability and Discriminant Validity , 1993 .

[111]  D. Cicchetti Defining child maltreatment: The interface between policy and research , 1993 .

[112]  Brian Mullen,et al.  Advanced BASIC meta-analysis , 1989 .

[113]  J. V. Van eekelen,et al.  Stress, glucocorticoids and development. , 1988, Progress in brain research.