Dentate gyrus−cornu ammonis (CA) 4 volume is decreased and associated with depressive episodes and lipid peroxidation in bipolar II disorder: Longitudinal and cross-sectional analyses

Bipolar Disorders

Volumn 18, Issue 8, 2016, Pages 657-668

  Elvsåshagen, Torbjørn ^a,b   Zuzarte, Pedro ^c,d   Westlye, Lars T ^a,b   Bøen, Erlend ^e   Josefsen, Dag ^a   Boye, Birgitte ^a,b   Hol, Per K ^a   Malt, Ulrik F ^a,b   Young, L Trevor ^d,f   Andreazza, Ana C ^d,f  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c UNIVERSITY OF LISBON   (Portugal)

^d UNIVERSITY OF TORONTO   (Canada)

^e DIAKONHJEMMET HOSPITAL   (Norway)

^f CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

Author keywords

atrophy; bipolar disorder; dentate gyrus; depression; depressive episode; hippocampus; lipid peroxidation; oxidative stress

Indexed keywords

4 HYDROXYNONENAL; AMFEBUTAMONE; BIOLOGICAL MARKER; CARBAMAZEPINE; CITALOPRAM; ESCITALOPRAM; FLUOXETINE; LAMOTRIGINE; LIPID HYDROPEROXIDE; LITHIUM; METHYLPHENIDATE; MIANSERIN; MIRTAZAPINE; NITRAZEPAM; OXAZEPAM; QUETIAPINE; SERTRALINE; TOPIRAMATE; VALPROIC ACID; VENLAFAXINE; ZOPICLONE; 4-HYDROXY-2-NONENAL; ALDEHYDE;

ADULT; ARTICLE; BIPOLAR II DISORDER; BRAIN SIZE; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DENTATE GYRUS; DEPRESSION; FEMALE; HIPPOCAMPUS; HUMAN; IMAGE SEGMENTATION; LIPID PEROXIDATION; LONGITUDINAL STUDY; MALE; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; OXIDATIVE STRESS; PRIORITY JOURNAL; BIPOLAR DISORDER; DIAGNOSTIC IMAGING; METABOLISM; ORGAN SIZE; PATHOLOGY; PHYSIOLOGY; PROCEDURES; PSYCHOLOGY; STATISTICS;

ADULT; ALDEHYDES; BIOMARKERS; BIPOLAR DISORDER; CROSS-SECTIONAL STUDIES; DENTATE GYRUS; DEPRESSION; FEMALE; HUMANS; LIPID PEROXIDATION; MAGNETIC RESONANCE IMAGING; MALE; ORGAN SIZE; OXIDATIVE STRESS; STATISTICS AS TOPIC;

EID: 85007275579     PISSN: 13985647     EISSN: 13995618     Source Type: Journal    
DOI: 10.1111/bdi.12457     Document Type: Article

References (87)

1. Angst J. The emerging epidemiology of hypomania and bipolar II disorder. J Affect Disord. 1998;50:143–151.
2. Phillips ML, Kupfer DJ. Bipolar disorder diagnosis: challenges and future directions. Lancet. 2013;381:1663–1671.
3. Angst J, Cui L, Swendsen J, et al. Major depressive disorder with subthreshold bipolarity in the National Comorbidity Survey Replication. Am J Psychiatry. 2010;167:1194–1201.
4. Angst J, Gamma A, Benazzi F, Ajdacic V, Eich D, Rossler W. Toward a re-definition of subthreshold bipolarity: epidemiology and proposed criteria for bipolar-II, minor bipolar disorders and hypomania. J Affect Disord. 2003;73:133–146.
5. Rihmer Z, Pestality P. Bipolar II disorder and suicidal behavior. Psychiatr Clin North Am. 1999;22:667–673.
6. Novick DM, Swartz HA, Frank E. Suicide attempts in bipolar I and bipolar II disorder: a review and meta-analysis of the evidence. Bipolar Disord. 2010;12:1–9.
7. Elvsåshagen T, Westlye LT, Bøen E, et al. Evidence for reduced dentate gyrus and fimbria volume in bipolar II disorder. Bipolar Disord. 2013;15:167–176.
8. Andreazza AC, Kauer-Sant'anna M, Frey BN, et al. Oxidative stress markers in bipolar disorder: a meta-analysis. J Affect Disord. 2008;111:135–144.
9. Kapczinski F, Vieta E, Andreazza AC, et al. Allostatic load in bipolar disorder: implications for pathophysiology and treatment. Neurosci Biobehav Rev. 2008;32:675–692.
10. Berk M, Kapczinski F, Andreazza AC, et al. Pathways underlying neuroprogression in bipolar disorder: focus on inflammation, oxidative stress and neurotrophic factors. Neurosci Biobehav Rev. 2011;35:804–817.
11. Spalding KL, Bergmann O, Alkass K, et al. Dynamics of hippocampal neurogenesis in adult humans. Cell. 2013;153:1219–1227.
12. Eriksson PS, Perfilieva E, Bjork-Eriksson T, et al. Neurogenesis in the adult human hippocampus. Nat Med. 1998;4:1313–1317.
13. Santarelli L, Saxe M, Gross C, et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science. 2003;301:805–809.
14. Sahay A, Hen R. Adult hippocampal neurogenesis in depression. Nat Neurosci. 2007;10:1110–1115.
15. Snyder JS, Soumier A, Brewer M, Pickel J, Cameron HA. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature. 2011;476:458–461.
16. Van Leemput K, Bakkour A, Benner T, et al. Automated segmentation of hippocampal subfields from ultra-high resolution in vivo MRI. Hippocampus. 2009;19:549–557.
17. Huang Y, Coupland NJ, Lebel RM, et al. Structural changes in hippocampal subfields in major depressive disorder: a high-field magnetic resonance imaging study. Biol Psychiatry. 2013;74:62–68.
18. Gold SM, Kern KC, O'Connor MF, et al. Smaller cornu ammonis 2-3/dentate gyrus volumes and elevated cortisol in multiple sclerosis patients with depressive symptoms. Biol Psychiatry. 2010;68:553–559.
19. Ho NF, Hooker JM, Sahay A, Holt DJ, Roffman JL. In vivo imaging of adult human hippocampal neurogenesis: progress, pitfalls and promise. Mol Psychiatry. 2013;18:404–416.
20. Haukvik UK, Westlye LT, Morch-Johnsen L, et al. In vivo hippocampal subfield volumes in schizophrenia and bipolar disorder. Biol Psychiatry. 2015;77:581–588.
21. Mathew I, Gardin TM, Tandon N, et al. Medial temporal lobe structures and hippocampal subfields in psychotic disorders: findings from the Bipolar-Schizophrenia Network on Intermediate Phenotypes (B-SNIP) study. JAMA Psychiatry. 2014;71:769–777.
22. Post RM, Fleming J, Kapczinski F. Neurobiological correlates of illness progression in the recurrent affective disorders. J Psychiatr Res. 2012;46:561–573.
23. Kulak A, Steullet P, Cabungcal JH, et al. Redox dysregulation in the pathophysiology of schizophrenia and bipolar disorder: insights from animal models. Antioxid Redox Signal. 2013;18:1428–1443.
24. Magalhaes PV, Jansen K, Pinheiro RT, et al. Peripheral oxidative damage in early-stage mood disorders: a nested population-based case-control study. Int J Neuropsychopharmacol. 2012;15:1043–1050.
25. Machado-Vieira R, Andreazza AC, Viale CI, et al. Oxidative stress parameters in unmedicated and treated bipolar subjects during initial manic episode: a possible role for lithium antioxidant effects. Neurosci Lett 2007;421:33–36.
26. Benes FM, Matzilevich D, Burke RE, Walsh J. The expression of proapoptosis genes is increased in bipolar disorder, but not in schizophrenia. Mol Psychiatry. 2006;11:241–251.
27. Andreazza AC, Shao L, Wang JF, Young LT. Mitochondrial complex I activity and oxidative damage to mitochondrial proteins in the prefrontal cortex of patients with bipolar disorder. Arch Gen Psychiatry. 2010;67:360–368.
28. Scola G, McNamara RK, Croarkin PE, et al. Lipid peroxidation biomarkers in adolescents with or at high-risk for bipolar disorder. J Affect Disord. 2016;192:176–183.
29. Andreazza AC, Gildengers A, Rajji TK, Zuzarte PM, Mulsant BH, Young LT. Oxidative stress in older patients with bipolar disorder. Am J Geriatric Psychiatry. 2015;23:314–319.
30. Tuncel OK, Sarisoy G, Bilgici B, et al. Oxidative stress in bipolar and schizophrenia patients. Psychiatry Res. 2015;228:688–694.
31. Miller AH, Maletic V, Raison CL. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol Psychiatry. 2009;65:732–741.
32. Che Y, Wang JF, Shao L, Young T. Oxidative damage to RNA but not DNA in the hippocampus of patients with major mental illness. J Psychiatry Neurosci. 2010;35:296–302.
33. Versace A, Andreazza AC, Young LT, et al. Elevated serum measures of lipid peroxidation and abnormal prefrontal white matter in euthymic bipolar adults: toward peripheral biomarkers of bipolar disorder. Mol Psychiatry. 2014;19:200–208.
34. Sheehan DV, Lecrubier Y, Sheehan KH, et al. The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry. 1998;59(Suppl. 20):22–33.
35. Suppes T, Leverich GS, Keck PE, et al. The Stanley foundation bipolar treatment outcome network. II. Demographics and illness characteristics of the first 261 patients. J Affect Disord. 2001;67:45–59.
36. Drake R, Mueser K, McHugo G. Clinical rating scales: Alcohol Use Scale (AUS), Drug Use Scale (DUS), and Substance Abuse Treatment Scale (SAYS). In: Sederer L, Dickey B, eds. Outcomes Assessment in Clinical Practice. Williams & Wilkins: Baltimore; 1996: 113–116.
37. Montgomery SA, Åsberg M. A new depression scale designed to be sensitive to change. Br J Psychiatry. 1979;134:382–389.
38. Young RC, Biggs JT, Ziegler VE, Meyer DA. A rating scale for mania: reliability, validity and sensitivity. Br J Psychiatry. 1978;133:429–435.
39. Fischl B, Salat DH, Busa E, et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron. 2002;33:341–355.
40. Fischl B, Salat DH, van der Kouwe AJ, et al. Sequence-independent segmentation of magnetic resonance images. NeuroImage. 2004;23(Suppl. 1):S69–84.
41. Teicher MH, Anderson CM, Polcari A. Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum. Proc Natl Acad Sci USA. 2012;109:E563–572.
42. Hooser SB, McCarthy JM, Wilson CR, Harms JL, Stevenson G, Everson RJ. Effects of storage conditions and hemolysis on vitamin E concentrations in porcine serum and liver. J Vet Diagn Invest. 2000;12:365–368.
43. Kapczinski F, Dal-Pizzol F, Teixeira AL, et al. A systemic toxicity index developed to assess peripheral changes in mood episodes. Mol Psychiatry. 2010;15:784–786.
44. Sheline YI, Gado MH, Kraemer HC. Untreated depression and hippocampal volume loss. Am J Psychiatry. 2003;160:1516–1518.
45. Kapczinski F, Dal-Pizzol F, Teixeira AL, et al. Peripheral biomarkers and illness activity in bipolar disorder. J Psychiatr Res. 2011;45:156–161.
46. Sheline YI, Sanghavi M, Mintun MA, Gado MH. Depression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. J Neurosci. 1999;19:5034–5043.
47. Gerritsen L, Comijs HC, van der Graaf Y, Knoops AJ, Penninx BW, Geerlings MI. Depression, hypothalamic pituitary adrenal axis, and hippocampal and entorhinal cortex volumes–the SMART Medea study. Biol Psychiatry. 2011;70:373–380.
48. Javadapour A, Malhi GS, Ivanovski B, Chen X, Wen W, Sachdev P. Hippocampal volumes in adults with bipolar disorder. J Neuropsychiatry Clin Neurosci. 2010;22:55–62.
49. Moorhead TW, McKirdy J, Sussmann JE, et al. Progressive gray matter loss in patients with bipolar disorder. Biol Psychiatry. 2007;62:894–900.
50. Zou Y, Corniola R, Leu D, et al. Extracellular superoxide dismutase is important for hippocampal neurogenesis and preservation of cognitive functions after irradiation. Proc Natl Acad Sci USA. 2012;109:21522–21527.
51. Manji H, Kato T, Di Prospero NA, et al. Impaired mitochondrial function in psychiatric disorders. Nat Rev Neurosci. 2012;13:293–307.
52. Huang TT, Zou Y, Corniola R. Oxidative stress and adult neurogenesis–effects of radiation and superoxide dismutase deficiency. Semin Cell Dev Biol. 2012;23:738–744.
53. Wang JF, Shao L, Sun X, Young LT. Increased oxidative stress in the anterior cingulate cortex of subjects with bipolar disorder and schizophrenia. Bipolar Disord. 2009;11:523–529.
54. Andreazza AC, Wang JF, Salmasi F, Shao L, Young LT. Specific subcellular changes in oxidative stress in prefrontal cortex from patients with bipolar disorder. J Neurochem. 2013;127:552–561.
55. Ozcan ME, Gulec M, Ozerol E, Polat R, Akyol O. Antioxidant enzyme activities and oxidative stress in affective disorders. Int Clin Psychopharmacol. 2004;19:89–95.
56. Banerjee U, Dasgupta A, Rout JK, Singh OP. Effects of lithium therapy on Na+-K+-ATPase activity and lipid peroxidation in bipolar disorder. Prog Neuropsychopharmacol Biol Psychiatry. 2012;37:56–61.
57. Hatch J, Andreazza A, Olowoyeye O, Rezin GT, Moody A, Goldstein BI. Cardiovascular and psychiatric characteristics associated with oxidative stress markers among adolescents with bipolar disorder. J Psychosom Res. 2015;79:222–227.
58. Brown NC, Andreazza AC, Young LT. An updated meta-analysis of oxidative stress markers in bipolar disorder. Psychiatry Res. 2014;218:61–68.
59. Lindqvist D, Mueller S, Mellon SH, et al. Peripheral antioxidant markers are associated with total hippocampal and CA3/dentate gyrus volume in MDD and healthy controls-preliminary findings. Psychiatry Res. 2014;224:168–174.
60. Onodera K, Omoi NO, Fukui K, et al. Oxidative damage of rat cerebral cortex and hippocampus, and changes in antioxidative defense systems caused by hyperoxia. Free Radical Res. 2003;37:367–372.
61. Sato H, Takahashi T, Sumitani K, Takatsu H, Urano S. Glucocorticoid generates ROS to induce oxidative injury in the hippocampus, leading to impairment of cognitive function of rats. J Clin Biochem Nutr. 2010;47:224–232.
62. Fukui K, Omoi NO, Hayasaka T, et al. Cognitive impairment of rats caused by oxidative stress and aging, and its prevention by vitamin E. Ann N Y Acad Sci. 2002;959:275–284.
63. Che Y, Cui YH, Tan H, Andreazza AC, Young LT, Wang JF. Abstinence from repeated amphetamine treatment induces depressive-like behaviors and oxidative damage in rat brain. Psychopharmacology. 2013;227:605–614.
64. Andreazza AC, Kauer-Sant'Anna M, Frey BN, et al. Effects of mood stabilizers on DNA damage in an animal model of mania. J Psychiatry Neurosci. 2008;33:516–524.
65. Arnone D, McKie S, Elliott R, et al. State-dependent changes in hippocampal grey matter in depression. Mol Psychiatry. 2013;18:1265–1272.
66. Malykhin NV, Carter R, Seres P, Coupland NJ. Structural changes in the hippocampus in major depressive disorder: contributions of disease and treatment. J Psychiatry Neurosci. 2010;35:337–343.
67. Vermetten E, Vythilingam M, Southwick SM, Charney DS, Bremner JD. Long-term treatment with paroxetine increases verbal declarative memory and hippocampal volume in posttraumatic stress disorder. Biol Psychiatry. 2003;54:693–702.
68. Yucel K, McKinnon MC, Taylor VH, et al. Bilateral hippocampal volume increases after long-term lithium treatment in patients with bipolar disorder: a longitudinal MRI study. Psychopharmacology. 2007;195:357–367.
69. Yucel K, Taylor VH, McKinnon MC, et al. Bilateral hippocampal volume increase in patients with bipolar disorder and short-term lithium treatment. Neuropsychopharmacology. 2008;33:361–367.
70. Wang Z, Neylan TC, Mueller SG, et al. Magnetic resonance imaging of hippocampal subfields in posttraumatic stress disorder. Arch Gen Psychiatry. 2010;67:296–303.
71. Mueller SG, Ng P, Neylan T, et al. Evidence for disrupted gray matter structural connectivity in posttraumatic stress disorder. Psychiatry Res. 2015;234:194–201.
72. Rossi R, Lanfredi M, Pievani M, et al. Volumetric and topographic differences in hippocampal subdivisions in borderline personality and bipolar disorders. Psychiatry Res. 2012;203:132–138.
73. Boen E, Westlye LT, Elvsashagen T, et al. Smaller stress-sensitive hippocampal subfields in women with borderline personality disorder without posttraumatic stress disorder. J Psychiatry Neurosci. 2014;39:127–134.
74. Vermetten E, Vythilingam M, Schmahl C, et al. Alterations in stress reactivity after long-term treatment with paroxetine in women with posttraumatic stress disorder. Ann N Y Acad Sci. 2006;1071:184–202.
75. Belvederi Murri M, Prestia D, Mondelli V, et al. The HPA axis in bipolar disorder: Systematic review and meta-analysis. Psychoneuroendocrinology 2016;63:327–342.
76. O'Donnell ML, Creamer M, Pattison P. Posttraumatic stress disorder and depression following trauma: understanding comorbidity. Am J Psychiatry. 2004;161:1390–1396.
77. Zimmerman DJ, Choi-Kain LW. The hypothalamic-pituitary-adrenal axis in borderline personality disorder: a review. Harv Rev Psychiatry. 2009;17:167–183.
78. Zanarini MC, Frankenburg FR, Dubo ED, et al. Axis I comorbidity of borderline personality disorder. Am J Psychiatry. 1998;155:1733–1739.
79. Ayala A, Munoz MF, Arguelles S. Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell Longev. 2014;2014:360438.
80. Riahi Y, Cohen G, Shamni O, Sasson S. Signaling and cytotoxic functions of 4-hydroxyalkenals. Am J Physiol Endocrinol Metab. 2010;299:E879–886.
81. Joshi YB, Pratico D. Lipid peroxidation in psychiatric illness: overview of clinical evidence. Oxid Med Cell Longev. 2014;2014:828702.
82. Halliwell B. Lipid peroxidation, antioxidants and cardiovascular disease: how should we move forward? Cardiovasc Res. 2000;47:410–418.
83. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007;39:44–84.
84. Frank E, Nimgaonkar VL, Phillips ML, Kupfer DJ. All the world's a (clinical) stage: rethinking bipolar disorder from a longitudinal perspective. Mol Psychiatry. 2015;20:23–31.
85. Kapczinski F, Magalhaes PV, Balanza-Martinez V, et al. Staging systems in bipolar disorder: an International Society for Bipolar Disorders Task Force Report. Acta Psychiatr Scand. 2014;130:354–363.
86. Pfaffenseller B, Fries GR, Wollenhaupt-Aguiar B, et al. Neurotrophins, inflammation and oxidative stress as illness activity biomarkers in bipolar disorder. Expert Rev Neurother. 2013;13:827–842.
87. Marizzoni M, Antelmi L, Bosch B, et al. Longitudinal reproducibility of automatically segmented hippocampal subfields: A multisite European 3T study on healthy elderly. Hum Brain Mapp. 2015;36:3516–3527.