Smaller hippocampal volume following sexual assault in women is associated with post-traumatic stress disorder
Corresponding Author
Y. Quidé
School of Psychiatry, University of New South Wales (UNSW), Randwick, NSW, Randwick, NSW, Australia
Neuroscience Research Australia, Randwick, NSW, Australia
Yann Quidé, School of Psychiatry, University of New South Wales, Sydney, NSW 2052, Australia.
E-mails: [email protected]; [email protected]
Search for more papers by this authorF. Andersson
UMR 1253, iBrain, Université de Tours, Inserm, Tours, France
Search for more papers by this authorD. Dufour-Rainfray
UMR 1253, iBrain, Université de Tours, Inserm, Tours, France
CHRU de Tours, Tours, France
Search for more papers by this authorC. Descriaud
Centre for Victims of Sexual Assault, CHRO, Orléans, France
Search for more papers by this authorB. Brizard
UMR 1253, iBrain, Université de Tours, Inserm, Tours, France
Search for more papers by this authorV. Gissot
CIC 1415, Inserm, Clinical Investigation Centre, CHRU de Tours, Tours, France
Search for more papers by this authorH. Cléry
UMR 1253, iBrain, Université de Tours, Inserm, Tours, France
Search for more papers by this authorM-P. Carrey Le Bas
Departmental Association for Assistance to Victims of Criminal Offenses, ADAVIP 37, France Victims 37, Tours, France
Search for more papers by this authorS. Osterreicher
Centre for Victims of Sexual Assault, CH de Blois, Blois, France
Search for more papers by this authorP. Saint-Martin
Legal Medicine Service, CHRU de Tours, Tours, France
Search for more papers by this authorW. El-Hage
UMR 1253, iBrain, Université de Tours, Inserm, Tours, France
CHRU de Tours, Tours, France
CIC 1415, Inserm, Clinical Investigation Centre, CHRU de Tours, Tours, France
Search for more papers by this authorCorresponding Author
Y. Quidé
School of Psychiatry, University of New South Wales (UNSW), Randwick, NSW, Randwick, NSW, Australia
Neuroscience Research Australia, Randwick, NSW, Australia
Yann Quidé, School of Psychiatry, University of New South Wales, Sydney, NSW 2052, Australia.
E-mails: [email protected]; [email protected]
Search for more papers by this authorF. Andersson
UMR 1253, iBrain, Université de Tours, Inserm, Tours, France
Search for more papers by this authorD. Dufour-Rainfray
UMR 1253, iBrain, Université de Tours, Inserm, Tours, France
CHRU de Tours, Tours, France
Search for more papers by this authorC. Descriaud
Centre for Victims of Sexual Assault, CHRO, Orléans, France
Search for more papers by this authorB. Brizard
UMR 1253, iBrain, Université de Tours, Inserm, Tours, France
Search for more papers by this authorV. Gissot
CIC 1415, Inserm, Clinical Investigation Centre, CHRU de Tours, Tours, France
Search for more papers by this authorH. Cléry
UMR 1253, iBrain, Université de Tours, Inserm, Tours, France
Search for more papers by this authorM-P. Carrey Le Bas
Departmental Association for Assistance to Victims of Criminal Offenses, ADAVIP 37, France Victims 37, Tours, France
Search for more papers by this authorS. Osterreicher
Centre for Victims of Sexual Assault, CH de Blois, Blois, France
Search for more papers by this authorP. Saint-Martin
Legal Medicine Service, CHRU de Tours, Tours, France
Search for more papers by this authorW. El-Hage
UMR 1253, iBrain, Université de Tours, Inserm, Tours, France
CHRU de Tours, Tours, France
CIC 1415, Inserm, Clinical Investigation Centre, CHRU de Tours, Tours, France
Search for more papers by this authorAbstract
Objective
Exposure to sexual assault is a significant risk factor to develop post-traumatic stress disorder (PTSD) in females. The early neurobiological changes leading to the development of PTSD remain understudied and unclear in this population.
Methods
Participants were 27 adult females recruited within a month following exposure to sexual assault (T1) and 20 age-matched non-exposed controls. Among the victims, 10 participants met (PTSD+) and 15 did not meet (PTSD−) DSM-IV criteria for PTSD 6 months post-trauma (T2). At both visits, hippocampal and amygdala volumes were extracted from magnetic resonance imaging scans, and indices of total diurnal cortisol changes were derived from individual areas under the curve relative to the ground (AUCg). Measures at T1 were compared between groups at T1, measures at T2 between groups at T2, and measures at T1 between groups at T2.
Results
At T1, victims had significantly smaller bilateral hippocampal volumes, but not AUCg, than controls. At T2, neither hippocampal volume nor AUCg significantly differed among the groups. However, the PTSD+ group had significantly smaller hippocampal volumes at T1 than the control group, but not compared to the PTSD− group.
Conclusions
This study indicates that having smaller hippocampal volumes is a risk factor to develop PTSD in females exposed to sexual assault.
Supporting Information
Filename | Description |
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acps12920-sup-0001-TableS1.docxWord document, 90.9 KB | Table S1. Correlations between hippocampal volumes and levels of education, depressive, dissociative and anxiety symptoms in females three weeks following sexual assault (T1) who developed (PTSD+) or not (PTSD−) posttraumatic stress disorder at a six months follow-up. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1Bicanic I, de ROOS C, van WESEL F, SINNEMA G, van de PUTTE E. Rape-related symptoms in adolescents: short- and long-term outcome after cognitive behavior group therapy. Eur J Psychotraumatol 2014; 5: 22969. https://doi.org/10.3402/ejpt.v5.22969
- 2Carmassi C, Dell'Osso L, Manni C et al. Frequency of trauma exposure and Post-Traumatic Stress Disorder in Italy: analysis from the World Mental Health Survey Initiative. J Psychiatr Res 2014; 59: 77–84.
- 3Barth SK, Kimerling RE, Pavao J et al. Military sexual trauma among recent veterans: correlates of sexual assault and sexual harassment. Am J Prev Med 2016; 50: 77–86.
- 4Liu H, Petukhova MV, Sampson NA et al. Association of DSM-IV posttraumatic stress disorder with traumatic experience type and history in the World Health Organization world mental health surveys. JAMA Psychiatry 2017; 74: 270–281.
- 5Chivers-Wilson KA. Sexual assault and posttraumatic stress disorder: a review of the biological, psychological and sociological factors and treatments. Mcgill J Med 2006; 9: 111–118.
- 6 WHO. Understanding and addressing violence against women; 2012 Contract No.: Document Number|.
- 7Nickerson A, Steenkamp M, Aerka IM et al. Prospective investigation of mental health following sexual assault. Depress Anxiety 2013; 30: 444–450.
- 8Peter-Hagene LC, Ullman SE. Social reactions to sexual assault disclosure and problem drinking: mediating effects of perceived control and PTSD. J Interpers Violence 2014; 29: 1418–1437.
- 9Carper TL, Mills MA, Steenkamp MM, Nickerson A, Salters-Pedneault K, Litz BT. Early PTSD symptom sub-clusters predicting chronic posttraumatic stress following sexual assault. Psychol Trauma 2015; 7: 442–447.
- 10Pegram SE, Abbey A. Associations between sexual assault severity and psychological and physical health outcomes: similarities and differences among African American and Caucasian survivors. J Interpers Violence 2016; https://doi.org/10.1177/0886260516673626
- 11Burnam MA, Stein JA, Golding JM et al. Sexual assault and mental disorders in a community population. J Consult Clin Psychol 1988; 56: 843–850.
- 12Kilpatrick DG, Ruggiero KJ, Acierno R, Saunders BE, Resnick HS, Best CL. Violence and risk of PTSD, major depression, substance abuse/dependence, and comorbidity: results from the National Survey of Adolescents. J Consult Clin Psychol 2003; 71: 692–700.
- 13Smith ME. Bilateral hippocampal volume reduction in adults with post-traumatic stress disorder: a meta-analysis of structural MRI studies. Hippocampus 2005; 15: 798–807.
- 14Woon FL, Sood S, Hedges DW. Hippocampal volume deficits associated with exposure to psychological trauma and posttraumatic stress disorder in adults: a meta-analysis. Prog Neuropsychopharmacol Biol Psychiatry 2010; 34: 1181–1188.
- 15Morey RA, Gold AL, Labar KS et al. Amygdala volume changes in posttraumatic stress disorder in a large case-controlled veterans group. Arch Gen Psychiatry 2012; 69: 1169–1178.
- 16O'Doherty DC, Chitty KM, Saddiqui S, Bennett MR, Lagopoulos J. A systematic review and meta-analysis of magnetic resonance imaging measurement of structural volumes in posttraumatic stress disorder. Psychiatry Res 2015; 232: 1–33.
- 17Logue MW, van Rooij SJH, Dennis EL et al. Smaller hippocampal volume in posttraumatic stress disorder: a multi-site ENIGMA-PGC study. Biol Psychiat 2018; 83: 244–253.
- 18Meewisse ML, Reitsma JB, de Vries GJ, Gersons BP, Olff M. Cortisol and post-traumatic stress disorder in adults: systematic review and meta-analysis. Br J Psychiatry 2007; 191: 387–392.
- 19Miller GE, Chen E, Zhou ES. If it goes up, must it come down? Chronic stress and the hypothalamic-pituitary-adrenocortical axis in humans. Psychol Bull 2007; 133: 25–45.
- 20Morris MC, Hellman N, Abelson JL, Rao U. Cortisol, heart rate, and blood pressure as early markers of PTSD risk: a systematic review and meta-analysis. Clin Psychol Rev 2016; 49: 79–91.
- 21de Kloet CS, Vermetten E, Geuze E, Kavelaars A, Heijnen CJ, Westenberg HG. Assessment of HPA-axis function in posttraumatic stress disorder: pharmacological and non-pharmacological challenge tests, a review. J Psychiatr Res 2006; 40: 550–567.
- 22Sherin JE, Nemeroff CB. Post-traumatic stress disorder: the neurobiological impact of psychological trauma. Dialogues Clin Neurosci 2011; 13: 263–278.
- 23Aardal-Eriksson E, Eriksson TE, Thorell LH. Salivary cortisol, posttraumatic stress symptoms, and general health in the acute phase and during 9-month follow-up. Biol Psychiatry 2001; 50: 986–993.
- 24Quidé Y, Cléry H, Andersson F et al. Neurocognitive, emotional and neuroendocrine correlates of exposure to sexual assault in women. J Psychiatry Neurosci 2018; 43: 170116.
- 25Landré L, Destrieux C, Baudry M et al. Preserved subcortical volumes and cortical thickness in women with sexual abuse-related PTSD. Psychiatry Res 2010; 183: 181–186.
- 26Bonne O, Brandes D, Gilboa A et al. Longitudinal MRI study of hippocampal volume in trauma survivors with PTSD. Am J Psychiatry 2001; 158: 1248–1251.
- 27van Rooij SJH, Stevens JS, Ely TD et al. The role of the hippocampus in predicting future PTSD symptoms in recently traumatized civilians. Biol Psychiat 2017; [Epub ahead of print]. https://doi.org/10.1016/j.biopsych.2017.09.005
- 28Gilbertson MW, Shenton ME, Ciszewski A et al. Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nat Neurosci 2002; 5: 1242–1247.
- 29van Rooij SJ, Kennis M, Sjouwerman R, van den Heuvel MP, Kahn RS, Geuze E. Smaller hippocampal volume as a vulnerability factor for the persistence of post-traumatic stress disorder. Psychol Med 2015; 45: 2737–2746.
- 30Xie H, Claycomb Erwin M, Elhai JD et al. Relationship of hippocampal volumes and posttraumatic stress disorder symptoms over early post-trauma periods. Biol Psychiatry 2018.
- 31Conrad CD. Chronic stress-induced hippocampal vulnerability: the glucocorticoid vulnerability hypothesis. Rev Neurosci 2008; 19: 395–411.
- 32Kim EJ, Pellman B, Kim JJ. Stress effects on the hippocampus: a critical review. Learn Mem 2015; 22: 411–416.
- 33Babson KA, Woodward SH, Schaer M, Sephton SE, Kaloupek DG. Salivary cortisol and regional brain volumes among veterans with and without posttraumatic stress disorder. Biol Psychiatry Cogn Neurosci Neuroimaging 2017; 2: 372–379.
- 34Blake DD, Weathers FW, Nagy LM et al. The development of a clinician-administered PTSD scale. J Trauma Stress 1995; 8: 75–90.
- 35Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J. An inventory for measuring depression. Arch Gen Psychiatry 1961; 4: 561–571.
- 36Collet L, Cottraux J. The shortened Beck depression inventory (13 items). Study of the concurrent validity with the Hamilton scale and Widlocher's retardation scale. Encephale 1986; 12: 77–79.
- 37Spielberger CD, Gorsuch RL, Lushene R, Vagg PR, Jacobs GA. Manual for the state-trait anxiety inventory. Palo Alto, CA: Consulting Psychologists Press; 1983.
- 38Bruchon-Schweitzer M, Paulhan I. Inventaire d'anxiété état-trait (forme Y) [Manual for the State-Trait Anxiety Inventory (STAI)]. Paris: Consulting Psychologist Press, Edition Française: Editions de Centre de Psychologie Appliquée; 1993.
- 39Marmar CR, Weiss DS, Metzler TJ. The peritraumatic dissociative experiences questionnaire. In: JP Wilson, TM Keane, eds. Assessing psychological trauma and posttraumatic stress disorder. Washington, DC: The Guildford Press; 1997: 412–428.
- 40Birmes P, Brunet A, Benoit M et al. Validation of the Peritraumatic Dissociative Experiences Questionnaire self-report version in two samples of French-speaking individuals exposed to trauma. Eur Psychiatry 2005; 20: 145–151.
- 41Bernstein EM, Putnam FW. Development, reliability, and validity of a dissociation scale. J Nerv Ment Dis 1986; 174: 727–735.
- 42Darves-Bornoz JM, Degiovanni A, Gaillard P. Validation of a French version of the Dissociative experiences scale in a rape-victim population. Can J Psychiatry 1999; 44: 271–275.
- 43Sheehan DV, Lecrubier Y, Sheehan KH et al. The mini-international neuropsychiatric interview (MINI): the development and validation of a structured diagnostic interview for DSM-IV and ICD-10. J Clin Psychiatry 1998; 59: 22–33.
- 44Pruessner JC, Kirschbaum C, Meinlschmid G, Hellhammer DH. Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology 2003; 28: 916–931.
- 45Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis: I. Segmentation and surface reconstruction. NeuroImage 1999; 9: 179–194.
- 46Fischl B, Sereno MI, Dale AM. Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. NeuroImage 1999; 9: 195–207.
- 47Fischl B, Salat DH, Busa E et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 2002; 33: 341–355.
- 48Siegel S. Nonparametric statistics. Am Stat 1957; 11: 13–19.
- 49Altman DG, Gore SM, Gardner MJ, Pocock SJ. Statistical guidelines for contributors to medical journals. Br Med J (Clin Res Ed) 1983; 286: 1489–1493.
- 50Lindgren L, Bergdahl J, Nyberg L. Longitudinal evidence for smaller hippocampus volume as a vulnerability factor for perceived stress. Cereb Cortex 2016; 26: 3527–3533.
- 51Maren S, Phan KL, Liberzon I. The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat Rev Neurosci 2013; 14: 417–428.
- 52Garfinkel SN, Abelson JL, King AP et al. Impaired contextual modulation of memories in PTSD: an fMRI and psychophysiological study of extinction retention and fear renewal. J Neurosci 2014; 34: 13435–13443.
- 53Jovanovic T, Norrholm SD, Fennell JE et al. Posttraumatic stress disorder may be associated with impaired fear inhibition: relation to symptom severity. Psychiatry Res 2009; 167: 151–160.
- 54Milad MR, Pitman RK, Ellis CB et al. Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biol Psychiatry 2009; 66: 1075–1082.
- 55Risser HJ, Hetzel-Riggin MD, Thomsen CJ, McCanne TR. PTSD as a mediator of sexual revictimization: the role of reexperiencing, avoidance, and arousal symptoms. J Trauma Stress 2006; 19: 687–698.
- 56Ullman SE. Sexual revictimization, PTSD, and problem drinking in sexual assault survivors. Addict Behav 2016; 53: 7–10.
- 57Calem M, Bromis K, McGuire P, Morgan C, Kempton MJ. Meta-analysis of associations between childhood adversity and hippocampus and amygdala volume in non-clinical and general population samples. Neuroimage Clin 2017; 14: 471–479.
- 58Li Y, Seng JS. Child maltreatment trauma, posttraumatic stress disorder, and cortisol levels in women: a literature review. J Am Psychiatr Nurses Assoc 2018; 24: 35–44.
- 59Quidé Y, Witteveen AB, El-Hage W, Veltman DJ, Olff M. Differences between effects of psychological versus pharmacological treatments on functional and morphological brain alterations in anxiety disorders and major depressive disorder: a systematic review. Neurosci Biobehav Rev 2012; 36: 626–644.
- 60Sekiguchi A, Kotozaki Y, Sugiura M et al. Resilience after 3/11: structural brain changes 1 year after the Japanese earthquake. Mol Psychiatry 2015; 20: 553–554.
- 61 WHO. Guidelines for the management of conditions specifically related to stress. Geneva: World Health Organization; 2013.
- 62Lee DJ, Schnitzlein CW, Wolf JP, Vythilingam M, Rasmusson AM, Hoge CW. Psychotherapy versus pharmacotherapy for posttraumatic stress disorder: systemic review and meta-analyses to determine first-line treatments. Depress Anxiety 2016; 33: 792–806.
- 63Kirschbaum C, Kudielka BM, Gaab J, Schommer NC, Hellhammer DH. Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosom Med 1999; 61: 154–162.
- 64Ferree NK, Kamat R, Cahill L. Influences of menstrual cycle position and sex hormone levels on spontaneous intrusive recollections following emotional stimuli. Conscious Cogn 2011; 20: 1154–1162.
- 65Bryant RA, Felmingham KL, Silove D, Creamer M, O'Donnell M, McFarlane AC. The association between menstrual cycle and traumatic memories. J Affect Disord 2011; 131: 398–401.