Posttraumatic stress disorder symptom severity is associated with left hippocampal volume reduction: A meta-analytic study

CNS Spectrums

Volumn 22, Issue 4, 2017, Pages 363-372

  Nelson, Michael D ^a   Tumpap, Alecia M ^a  

^a GONZAGA UNIVERSITY   (United States)

Author keywords

hippocampus; magnetic resonance imaging; meta analysis; Posttraumatic stress disorder; symptom severity

Indexed keywords

ARTICLE; BRAIN SIZE; CLINICIAN ADMINISTERED PTSD SCALE; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; DISEASE SEVERITY; HIPPOCAMPUS; HUMAN; LEFT HIPPOCAMPUS; NEUROTOXICITY; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; RATING SCALE; RIGHT HIPPOCAMPUS; DIAGNOSTIC IMAGING; META ANALYSIS; NUCLEAR MAGNETIC RESONANCE IMAGING; ORGAN SIZE; PATHOLOGY; PSYCHOLOGY; SEVERITY OF ILLNESS INDEX;

HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; ORGAN SIZE; SEVERITY OF ILLNESS INDEX; STRESS DISORDERS, POST-TRAUMATIC;

EID: 85006320749     PISSN: 10928529     EISSN: None     Source Type: Journal    
DOI: 10.1017/S1092852916000833     Document Type: Article

References (80)

1. American Psychiatric Association (APA). Diagnostic and Statistical Manual of Mental Disorders, 5th ed. Washington, DC: American Psychiatric Association; 2013.
2. Villarreal G, Hamilton DA, Petropoulus H, et al. Reduced hippocampal volume and total white matter volume in posttraumatic stress disorder. Biol Psychiatry. 2002; 52(2): 119-125.
3. Kessler RC, Berglund P, Delmer O, Jin R, Merikangas KR, Walters EE. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry. 2005; 62(6): 593-602. http://jamanetwork.com/journals/jamapsychiatry/fullarticle/208678.
4. Kessler RC, Chiu WT, Demler O, Merikangas KR, Walters EE. Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry. 2005; 62(6): 617-627. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2847357/pdf/nihms176704.pdf.
5. Squire LR, Zola-Morgan S. The medial temporal lobe memory system. Science. 1991; 253(5026): 1380-1386.
6. Treves A, Rolls ET. Computational analysis of the role of the hippocampus in memory. Hippocampus. 1994; 4(3): 374-391.
7. van Strien NM, Cappaert NLM, Witter MP. The anatomy of memory: An interactive overview of the parahippocampal-hippocampal network. Nat Rev Neurosci. 2009; 10(4): 273-282.
8. Vermetten E, Bremner JD. Circuits and systems in stress: Applications to neurobiology and treatment in posttraumatic stress disorder. Depress Anxiety. 2002; 16(1): 14-38.
9. Brewin CR, Kleiner JS, Vasterling JJ, Field AP. Memory for emotionally neutral information in posttraumatic stress disorder: A meta-analytic investigation. J Abnorm Psychol. 2007; 116(3): 448-463.
10. Johnsen GE, Asbjørnsen AE. Consistent impaired verbal memory in PTSD: Ameta-analysis. J Affect Disord. 2008; 111(1): 74-82. Epub ahead of print Apr 2.
11. Burgess N, Maguire EA, O'Keefe J. The human hippocampus and spatial and episodic memory. Neuron. 2002; 35(4): 625-641. http://www.cell.com/neuron/fulltext/S0896-6273(02)00830-9.
12. Giap BT, Jong CN, Ricker JH, Cullen NK, Zafonte RD. The hippocampus: Anatomy, pathophysiology, and regenerative capacity. J Head Trauma Rehabil. 2000; 15(3): 875-894.
13. Squire LR. Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychol Rev. 1992; 99(2): 195-231.
14. Erratum in Psychol Rev. 1992; 99(3): 582.
15. Weiss SJ.Neurobiological alterations associated with traumatic stress. Perspect Psychiatr Care. 2007; 43(3): 114-122.
16. Bremner JD, Randall P, Scott TM, et al. MRI-based measurement of hippocampal volume in patients with combat-related posttraumatic stress disorder. Am J Psychiatry. 1995; 152(7): 973-981. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3233767/pdf/nihms-340189.pdf.
17. Bremner JD. Neuroimaging of posttraumatic stress disorder. Psychiatr Ann. 1998; 28(8): 445-450.
18. Tischler L, Brand SR, Stavitsky K, et al. The relationship between hippocampal volume and declarative memory in a population of combat veterans with and without PTSD. Ann N Y Acad Sci. 2006; 1071(1): 405-409.
19. Levy-Gigi E, Szabo C, Richter-Levin G, Kéri S. Reduced hippocampal volume is associated with overgeneralization of negative context in individuals with PTSD. Neuropsychology. 2015; 29(1): 151-161. Epub ahead of print Jul 28, 2014.
20. Milad MR, Wright CI, Orr SP, Pitman RK, Quirk GJ, Rauch SL. Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol Psychiatry. 2007; 62(5): 446-454. Epub ahead of print Jan 9.
21. Milad MR, Orr SP, Lasko NP, Chang Y, Rauch SL, Pitman RK. Presence and acquired origin of reduced recall for fear extinction in PTSD: Results of a twin study. J Psychiatr Res. 2008; 42(7): 515-520; Epub ahead of print Feb 29. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2377011/pdf/nihms46966.pdf.
22. Höschl C, Hajek T. Hippocampal damage mediated by corticosteroids: A neuropsychiatric research challenge. Eur Arch Psychiatry Clin Neurosci. 2001; 251(Suppl 2): II81-II88.
23. Vermetten E, Bremner JD. Circuits and systems in stress, I: Preclinical studies. Depress Anxiety. 2002; 15(3): 126-147.
24. Teicher M, Tomoda A, Andersen S. Neurobiological consequences of early stress and childhoodmaltreatment: Are results from human and animal studies comparableAnn N Y Acad Sci. 2006; 1071(1): 313-323.
25. Duman RS, Malberg J, Nakagawa S. Regulation of adult neurogenesis by psychotropic drugs and stress. J Pharmacol Exp Ther. 2001; 299(2): 401-407. http://jpet.aspetjournals.org/content/299/2/401.long.
26. Li L, Chen S, Liu J, Zhang J, He Z, Lin X. Magnetic resonance imaging and magnetic resonance spectroscopy study of deficits in hippocampal structure in fire victims with recent-onset posttraumatic stress disorder. Can J Psychiatry. 2006; 51(7): 431-437.
27. Schuff N, Marmar CR, Weiss DS, et al. Reduced hippocampal volume and N-acetyl aspartate in posttraumatic stress disorder. Ann N Y Acad Sci. 1997; 821(1): 516-520.
28. Schuff N, Neylan TC, Lenoci MA, et al. Decreased hippocampal N-acetylaspartate in the absence of atrophy in posttraumatic stress disorder. Biol Psychiatry. 2001; 50(12): 952-959. https://www. ncbi.nlm.nih.gov/pmc/articles/PMC2733624/pdf/nihms125448. pdf.
29. Shu XJ, Xue L, Liu W, et al. More vulnerability of left than right hippocampal damage in right-handed patients with post-traumatic stress disorder. Psychiatry Res. 2013; 212(3): 237-244. Epub ahead of print Nov 11, 2012.
30. Bossini L, Tavanti M, Calossi S, et al. Magnetic resonance imaging volumes of the hippocampus in drug-naïve patients with posttraumatic stress disorder without comorbidity conditions. J Psychiatr Res. 2008; 42(9) 752-762. Epub ahead of print Sep 24, 2007.
31. Bremner JD, Randall P, Vermetten E, et al. Magnetic resonance imaging-based measurement of hippocampal volume in posttraumatic stress disorder related to childhood physical and sexual abuse: A preliminary report. Biol Psychiatry. 1997; 41(1): 23-32. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3229101/pdf/nihms-340184.pdf.
32. Bremner JD, Vythilingam M, Vermetten E, et al. MRI and PET study of deficits in hippocampal structure and function in women with childhood sexual abuse and posttraumatic stress disorder. Am J Psychiatry. 2003; 160(5): 924-932. http://ajp.psychiatryonline. org/doi/full/10.1176/appi.ajp.160.5.924.
33. Chalavi S, Vissia EM, Giesen ME, et al. Abnormal hippocampal morphology in dissociative identity disorder and post-traumatic stress disorder correlates with childhood trauma and dissociative symptoms. Hum Brain Mapp. 2015; 36(5): 1692-1704. Epub ahead of print Dec 29, 2014. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4400262/pdf/nihms-673286.pdf.
34. Emdad R, Bonekamp D, Sondergaard HP, et al. Morphometric and psychometric comparisons between non-substance-abusing patients with posttraumatic stress disorder and normal controls. Psychother Psychosom. 2006; 75(2): 122-132.
35. Gurvits TV, Shenton ME, Hokama H, et al. Magnetic resonance imaging study of hippocampal volume in chronic, combat-related posttraumatic stress disorder. Biol Psychiatry. 1996; 40(11): 1091-1099. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2910907/pdf/nihms170395.pdf.
36. Hedges DW, Allen S, Tate DF, et al. Reduced hippocampal volume in alcohol and substance naïve Vietnam combat veterans with posttraumatic stress disorder. Cogn Behav Neurobiol. 2003; 16(4): 219-224.
37. Lindauer RJL, Vlieger EJ, Jalink M, et al. Smaller hippocampal volume in Dutch police officers with posttraumatic stress disorder. Biol Psychiatry. 2004; 56(5): 356-363.
38. Morey RA, Gold AL, Labar KS, et al. Amygdala volume changes in posttraumatic stress disorder in a large case-controlled veterans group. Arch Gen Psychiat. 2012; 69(11): 1169-1178. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3647246/pdf/nihms 452834.pdf.
39. Pavi L, Gregurek R, Rados M, et al. Smaller right hippocampus in war veterans with posttraumatic stress disorder. Psychiatry Res. 2007; 154(2): 191-198; Epub ahead of print Jan 26.
40. Schmahl C, Berne K, Krause A, et al. Hippocampus and amygdala volumes in patients with borderline personality disorder with or without posttraumatic stress disorder. J Psychiatry Neurosci. 2009; 34(4): 289-295. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2702446/pdf/0340289.pdf.
41. Shin LM, Shin PS, Heckers S, et al. Hippocampal function in posttraumatic stress disorder. Hippocampus. 2004; 14(3): 292-300.
42. Starevi A, Dimitrijevi I, Aksi M, et al. Brain changes in patients with posttraumatic stress disorder and associated alcoholism: MRI-based study. Psychiatr Danub. 2015; 27(1): 78-83. http://www.hdbp.org/psychiatria-danubina/pdf/dnb-vol27-no1/dnb-vol27-no1-78.pdf.
43. Vythilingam M, Luckenbaugh DA, Lam T, et al. Smaller head of the hippocampus in Gulf War-related posttraumatic stress disorder. Psychiatry Res. 2005; 139(2): 89-99.
44. Weniger G, Lange C, Sachsse U, Irle E. Amygdala and hippocampal volumes and cognition in adult survivors of childhood abuse with dissociative disorders. Acta Psychiatr Scand. 2008; 118(4): 281-290.
45. Wignall EL, Dickson JM, Vaughan P, et al. Smaller hippocampal volume in patients with recent-onset posttraumatic stress disorder. Biol Psychiatry. 2004; 56(11): 832-836.
46. Winter H, Irle E. Hippocampal volume in adult burn patients with and without posttraumatic stress disorder. Am J Psychiatry. 2004; 161(12): 2194-2200.
47. Bonne O, Brandes D, Giboa A, et al. Longitudinal MRI study of hippocampal volume in trauma survivors with PTSD. Am J Psychiatry. 2001; 158(8): 1248-1251. https://www.ncbi.nlm.nih. gov/pmc/articles/PMC2819102/pdf/nihms170397.pdf.
48. Eckart C, Kaufmann J, Kanowski M, et al. Magnetic resonance volumetry and spectroscopy of hippocampus and insula in relation to severe exposure of traumatic stress. Psychophysiology. 2012; 49(2): 261-270. Epub ahead of print Oct 21, 2011.
49. Fennema-Notestine C, Stein MB, Kennedy CM, Archibald SL, Jernigan TL. Brain morphometry in female victims of intimate partner violence with and without posttraumatic stress disorder. Biol Psychiatry. 2002; 52(11): 1089-1101.
50. Freeman T, Kimbrell T, Booe L, et al. Evidence of resilience: Neuroimaging in former prisoners of war. Psychiatry Res. 2006; 146(1): 59-64; Epub ahead of print Dec 19, 2005.
51. Gilbertson MW, Shenton ME, Ciszewski A, et al. Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nat Neurosci. 2002; 5(11): 1242-1247. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2819093/pdf/nihms170404.pdf.
52. Golier JA, Yehuda R, De Santi S, Segal S, Dolan S, de Leon MJ. Absence of hippocampal volume differences in survivors of the Nazi Holocaust with and without posttraumatic stress disorder. Psychiatry Res. 2005; 139(1): 53-64.
53. Hara E, Matsuoka Y, Hakamata Y, et al. Hippocampal and amygdalar volumes in breast cancer survivors with posttraumatic stress disorder. J Neuropsychiatry Clin Neurosci. 2008; 20(3): 302-308. http://neuro.psychiatryonline.org/doi/full/10.1176/jnp.2008.20.3.302.
54. Jatzko A, Rothenhofer S, Schmitt A, et al. Hippocampal volume in chronic posttraumatic stress disorder (PTSD): MRI study using two different evaluation methods. J Affect Disord. 2006; 94(1-3): 121-126. Epub ahead of print May 15.
55. Landré L, Destrieux C, Baudry M, et al. Preserved subcortical volumes and cortical thickness in women with sexual abuserelated PTSD. Psychiatry Res. 2010; 183(3): 181-186; Epub ahead of print Aug 4.
56. Pederson CL, Maurer SH, Kaminski PL, et al. Hippocampal volume and memory performance in a community-based sample of women with posttraumatic stress disorder secondary to child abuse. J Trauma Stress. 2004; 17(1): 37-40.
57. Starevi A, Srdjan P, Radojicic Z, et al. Volumetric analysis of amygdala, hippocampus, and prefrontal cortex in therapy-naïve PTSD participants. BioMed Res Int. 2014; 2014: 1-6. Article ID 968495.
58. Wang Z, Neylan TC, Mueller SG, et al. Magnetic resonance imaging of hippocampal subfields in posttraumatic stress disorder. Arch Gen Psychiatry. 2010; 67(3): 296-303. https://www.ncbi.nlm. nih.gov/pmc/articles/PMC2848481/pdf/nihms184801.pdf.
59. Yehuda R, Golier JA, Tischler L, et al. Hippocampal volume in aging combat veterans with and without post-traumatic stress disorder: Relation to risk and resilience factors. J Psychiatr Res. 2007; 41(5): 435-445; Epub ahead of print Jan 30, 2006.
60. Yehuda R, Golier JA, Bierer LM, et al.Hydrocortisone responsiveness in Gulf War veterans with PTSD: Effects on ACTH, declarative memory hippocampal [18F]FDG uptake on PET. Psychiatry Res. 2010; 184(2). 117-127. Epub ahead of print Oct 8.
61. Kitayama N, Vaccarino V, KutnerM, Weiss P, Bremner JD.Magnetic resonance imaging (MRI) measurement of hippocampal volume in posttraumatic stress disorder: A meta-analysis. J Affect Disord. 2005; 88(1): 79-86.
62. Smith ME. Bilateral hippocampal volume reduction in adults with post-traumatic stress disorder: A meta-analysis of structural MRI studies. Hippocampus. 2005; 15(6): 798-807.
63. Karl A, Schaefer M, Malta LS, Dorfel D, Rohleder N, Werner A. A meta-analysis of structural brain abnormalities in PTSD. Neurosci Biobehav Rev. 2006; 30(7): 1004-1031. Epub ahead of print May 26.
64. Woon 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(7): 1181-1188. Epub ahead of print Jun 21.
65. Woon FL, Hedges DW. Hippocampal and amygdala volumes in children and adults with childhood maltreatment-related posttraumatic stress disorder: A meta-analysis. Hippocampus. 2008. 18(8): 729-736.
66. Woon F, Hedges DW. Gender does not moderate hippocampal volume deficits in adults with posttraumatic stress disorder: A metaanalysis. Hippocampus. 2011; 21(3): 243-252. Epub ahead of print Sep 29, 2010.
67. O'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): 1-33. Epub ahead of print Jan 30.
68. Blake DD, Weathers FW, Nagy LM, et al. The development of a clinician-administered PTSD scale. J Trauma Stress. 1995; 8(1): 75-90.
69. Lindauer RJ, Olff M, van Meijel EP, Carlier IV, Gersons BP. Cortisol, learning, memory, and attention in relation to smaller hippocampal volume in police officers with posttraumatic stress disorder. Biol Psychiatry. 2006; 59(2): 171-177.
70. Admon R, Milad M R, Hendler T. A causal model of post-traumatic stress disorder: Disentangling predisposed from acquired neural abnormalities. Trends Cogn Sci. 2013; 17(7): 337-347. Epub ahead of print Jun 12.
71. Apfel BA, Ross J, Hlavin J, et al. Hippocampal volume differences in Gulf War veterans with current versus lifetime posttraumatic stress disorder symptoms. Biol Psychiatry. 2011; 69: 541-548. Epub ahead of print Nov 20, 2010. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3259803/pdf/nihms291995.pdf.
72. Cohen J. Statistical Power Analysis for the Behavioral Sciences, 2nd ed. Hillsdale, NJ: Lawrence Erlbaum; 1988.
73. Weathers FW, Ruscio AM, Keane TM. Psychometric properties of nine scoring rules for the Clinician-Administered Posttraumatic Stress Disorder Scale. Psychol Assess. 1999; 11(2): 124-133.
74. Borenstein M, Hedges LV, Higgins JPT, Rothstein HR. Introduction to Meta-Analysis.West Sussex, UK:Wiley; 2009. https://www.metaanalysis-workshops.com/download/bookChapterSample.pdf.
75. Hedges LV, Olkin I. Statistical Methods for Meta-Analysis. New York: Academic Press; 1985.
76. Cooper H, Hedges LV, Valentine JC, eds. The Handbook of Research Synthesis and Meta-Analysis, 2nd ed. New York: The Russell Sage Foundation; 2009.
77. Admon R, Leykin D, Lubin G, et al. Stress-induced reduction in hippocampal volume and connectivity with the ventromedial prefrontal cortex are related to maladaptive responses to stressful military service. Hum Brain Mapp. 2013; 34(11): 2808-2816. Epub ahead of print Jul 17, 2012.
78. Koenigs M, Huey ED, Raymont V, et al. Focal brain damage protects against post-traumatic stress disorder in combat veterans. Nat Neurosci. 2008; 11(2): 232-237. Epub ahead of print Dec 23, 2007. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2693133/pdf/nihms-108233.pdf.
79. van 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(13): 2737-2746. Epub ahead of print May 4.
80. Zhang J, Tan Q, Yin H, et al. Decreased gray matter volume in the left hippocampus and bilateral calcarine cortex in coal mine flood disaster survivors with recent-onset PTSD. Psychiatry Res. 2011; 192(2): 84-90.