Abnormal white matter integrity as a structural endophenotype for bipolar disorder

Psychological Medicine

Volumn 46, Issue 7, 2016, Pages 1547-1558

  Sarlcicek A ^a,b   Zorlu, N ^a   Yalln, N ^b   Hldlroglu C ^b   Cavusoglu B ^b   Ceylan, D ^b,c   Ada, E ^b   Tunca, Z ^b   Ozerdem A ^b  

^a IZMIR KATIP CELEBI UNIVERSITY   (Turkey)

^b DOKUZ EYLUL UNIVERSITY   (Turkey)

^c Psychiatry Clinic Gümü hane State Hospital   (Turkey)

Author keywords

Bipolar disorder; diffusion tensor imaging; endophenotypes; fractional anisotropy; siblings; white matter

Indexed keywords

BIOLOGICAL MARKER;

ADULT; BIPOLAR DISORDER; DIFFUSION TENSOR IMAGING; ENDOPHENOTYPE; FEMALE; HUMAN; MALE; MIDDLE AGED; NERVE TRACT; PATHOLOGY; SIBLING; WHITE MATTER;

ADULT; BIOMARKERS; BIPOLAR DISORDER; DIFFUSION TENSOR IMAGING; ENDOPHENOTYPES; FEMALE; HUMANS; MALE; MIDDLE AGED; NEURAL PATHWAYS; SIBLINGS; WHITE MATTER;

EID: 84960109212     PISSN: 00332917     EISSN: 14698978     Source Type: Journal    
DOI: 10.1017/S0033291716000180     Document Type: Article

References (81)

1. Adler CM, DelBello MP, Strakowski SM (2006). Brain network dysfunction in bipolar disorder. CNS Spectrums 11, 312-320.
2. Ahn MS, Breeze JL, Makris N, Kennedy DN, Hodge SM, Herbert MR, Seidman LJ, Biederman J, Caviness VS, Frazier JA (2007). Anatomic brain magnetic resonance imaging of the basal ganglia in pediatric bipolar disorder. Journal of Affective Disorders 104, 147-154.
3. Arat HE, Chouinard VA, Cohen BM, Lewandowski KE, Ongür D (2015). Diffusion tensor imaging in first degree relatives of schizophrenia and bipolar disorder patients. Schizophrenia Research 161, 329-339.
4. Ashtari M (2012). Anatomy and functional role of the inferior longitudinal fasciculus: a search that has just begun. Developmental Medicine and Child Neurology 54, 6-7.
5. Barnea-Goraly N, Chang KD, Karchemskiy A, Howe ME, Reiss AL (2009). Limbic and corpus callosum aberrations in adolescents with bipolar disorder: a tract-based spatial statistics analysis. Biological Psychiatry 66, 238-244.
6. Barysheva M, Jahanshad N, Foland-Ross L, Altshuler LL, Thompson PM (2013). White matter microstructural abnormalities in bipolar disorder: a whole brain diffusion tensor imaging study. NeuroImage Clinical 2, 558-568.
7. Bellani M, Perlini C, Ferro A, Cerruti S, Rambaldelli G, Isola M, Cerini R, Dusi N, Andreone N, Balestrieri M, Pozzi Mucelli R, Tansella M, Brambilla P (2012). White matter microstructure alterations in bipolar disorder. Functional Neurology 27, 29-34.
8. Benedetti F, Absinta M, Rocca MA, Radaelli D, Poletti S, Bernasconi A, Dallaspezia S, Pagani E, Falini A, Copetti M, Colombo C, Comi G, Smeraldi E, Filippi M (2011). Tract-specific white matter structural disruption in patients with bipolar disorder. Bipolar Disorders 13, 414-424.
9. Botteron KN, Vannier MW, Geller B, Todd RD, Lee BC (1995). Preliminary study of magnetic resonance imaging characteristics in 8-to 16-year-olds with mania. Journal of the American Academy of Child and Adolescent Psychiatry 34, 742-749.
10. Bruno S, Cercignani M, Ron MA (2008). White matter abnormalities in bipolar disorder: a voxel-based diffusion tensor imaging study. Bipolar Disorders 10, 460-468.
11. Caetano SC, Silveira CM, Kaur S, Nicoletti M, Hatch JP, Brambilla P, Sassi R, Axelson D, Keshavan MS, Ryan ND, Birmaher B, Soares JC (2008). Abnormal corpus callosum myelination in pediatric bipolar patients. Journal of Affective Disorders 108, 297-301.
12. Cannon DM, Walshe M, Dempster E, Collier DA, Marshall N, Bramon E, Murray RM, McDonald C (2012). The association of white matter volume in psychotic disorders with genotypic variation in NRG1, MOG and CNP: a voxel-based analysis in affected individuals and their unaffected relatives. Translational Psychiatry 2, e167.
13. Chaddock CA, Barker GJ, Marshall N, Schulze K, Hall MH, Fern A, Walshe M, Bramon E, Chitnis XA, Murray R, McDonald C (2009). White matter microstructural impairments and genetic liability to familial bipolar I disorder. British Journal of Psychiatry 194, 527-534.
14. Chaddock-Heyman L, Erickson KI, Voss MW, Powers JP, Knecht AM, Pontifex MB, Drollette ES, Moore RD, Raine LB, Scudder MR, Hillman CH, Kramer AF (2013). White matter microstructure is associated with cognitive control in children. Biological Psychology 94, 109-115.
15. Chan WY, Yang GL, Chia MY, Woon PS, Lee J, Keefe R, Sitoh YY, Nowinski WL, Sim K (2010). Cortical and subcortical white matter abnormalities in adults with remitted first-episode mania revealed by tract-based spatial statistics. Bipolar Disorders 12, 383-389.
16. Clark L, Kempton MJ, Scarná A, Grasby PM, Goodwin GM (2005). Sustained attention-deficit confirmed in euthymic bipolar disorder but not in first-degree relatives of bipolar patients or euthymic unipolar depression. Biological Psychiatry 57, 183-187.
17. Emsell L, Chaddock C, Forde NJ, Van Hecke W, Barker GJ, Leemans A, Sunaert S, Walshe M, Bramon E, Cannon DM, Murray R, McDonald C (2014). White matter microstructural abnormalities in families multiply affected with bipolar I disorder: a diffusion tensor tractography study. Psychological Medicine 44, 2139-2150.
18. Emsell L, Leemans A, Langan C, Van Hecke W, Barker GJ, McCarthy P, Jeurissen B, Sijbers J, Sunaert S, Cannon DM, McDonald C (2013b). Limbic and callosal white matter changes in euthymic bipolar I disorder: an advanced diffusion magnetic resonance imaging tractography study. Biological Psychiatry 73, 194-201.
19. First MB, Spitzer RL, Gibbon M, Williams JBW (1996). Structured Clinical Interview for DSM-IV Axis I Disorders. American Psychiatric Press: Washington, DC.
20. Frazier JA, Breeze JL, Papadimitriou G, Kennedy DN, Hodge SM, Moore CM, Howard JD, Rohan MP, Caviness VS, Makris N (2007). White matter abnormalities in children with and at risk for bipolar disorder. Bipolar Disorders 9, 799-809.
21. Frey BN, Andreazza AC, Nery FG, Martins MR, Quevedo J, Soares JC, Kapczinski F (2007). The role of hippocampus in the pathophysiology of bipolar disorder. Behavioural Pharmacology 18, 419-430.
22. Garibotto V, Scifo P, Gorini A, Alonso CR, Brambati S, Bellodi L, Perani D (2010). Disorganization of anatomical connectivity in obsessive compulsive disorder: a multiparameter diffusion tensor imaging study in a subpopulation of patients. Neurobiology of Disease 37, 468-476.
23. Georgieva L, Dimitrova A, Ivanov D, Nikolov I, Williams NM, Grozeva D, Zaharieva I, Toncheva D, Owen MJ, Kirov G, O'Donovan MC (2008). Support for neuregulin 1 as a susceptibility gene for bipolar disorder and schizophrenia. Biological Psychiatry 64, 419-427.
24. Ghaemi SN, Sachs GS, Chiou AM, Pandurangi AK, Goodwin K (1999). Is bipolar disorder still underdiagnosed? Are antidepressants overutilized? Journal of Affective Disorders 52, 135-144.
25. Ha TH, Her JY, Kim JH, Chang JS, Cho HS, Ha K (2011). Similarities and differences of white matter connectivity and water diffusivity in bipolar I and II disorder. Neuroscience Letters 505, 150-154.
26. Haller S, Xekardaki A, Delaloye C, Canuto A, Lövblad KO, Gold G, Giannakopoulos P (2011). Combined analysis of grey matter voxel-based morphometry and white matter tract-based spatial statistics in late-life bipolar disorder. Journal of Psychiatry and Neuroscience 36, 391-401.
27. Harsan LA, Poulet P, Guignard B, Steibel J, Parizel N, de Sousa PL, Boehm N, Grucker D, Ghandour MS (2006). Brain dysmyelination and recovery assessment by noninvasive in vivo diffusion tensor magnetic resonance imaging. Journal of Neuroscience Research 83, 392-402.
28. Haznedar MM, Roversi F, Pallanti S, Baldini-Rossi N, Schnur DB, Licalzi EM, Tang C, Hof PR, Hollander E, Buchsbaum MS (2005). Fronto-thalamo-striatal gray and white matter volumes and anisotropy of their connections in bipolar spectrum illnesses. Biological Psychiatry 57, 733-742.
29. Hirschfeld RM, Calabrese JR, Weissman MM, Reed M, Davies MA, Frye MA, Keck PE Jr., Lewis L, McElroy SL, McNulty JP, Wagner KD (2003). Screening for bipolar disorder in the community. Journal of Clinical Psychiatry 64, 53-59.
30. Houenou J, Wessa M, Douaud G, Leboyer M, Chanraud S, Perrin M, Poupon C, Martinot JL, Paillere-Martinot ML (2007). Increased white matter connectivity in euthymic bipolar patients: diffusion tensor tractography between the subgenual cingulate and the amygdalo-hippocampal complex. Molecular Psychiatry 12, 1001-1010.
31. Kafantaris V, Kingsley P, Ardekani B, Saito E, Lencz T, Lim K, Szeszko P (2009). Lower orbital frontal white matter integrity in adolescents with bipolar I disorder. Journal of the American Academy of Child and Adolescent Psychiatry 48, 79-86.
32. Kubicki M, Westin CF, Maier SE, Mamata H, Frumin M, Ersner-Hershfield H, Kikinis R, Jolesz FA, McCarley R, Shenton ME (2002). Diffusion tensor imaging and its application to neuropsychiatric disorders. Harvard Review of Psychiatry 10, 324-336.
33. Lazar M, Weinstein DM, Tsuruda JS, Hasan KM, Arfanakis K, Meyerand ME, Badie B, Rowley HA, Haughton V, Field A, Alexander AL (2003). White matter tractography using diffusion tensor deflection. Human Brain Mapping 18, 306-321.
34. Lichtenstein P, Yip BH, Björk C, Pawitan Y, Cannon TD, Sullivan PF, Hultman CM (2009). Common genetic determinants of schizophrenia and bipolar disorder in Swedish families: a population-based study. Lancet 373, 234-239.
35. Liebermann D, Ostendorf F, Kopp UA, Kraft A, Bohner G, Nabavi DG, Kathmann N, Ploner CJ (2013). Subjective cognitive-Affective status following thalamic stroke. Journal of Neurology 260, 386-396.
36. Linke J, King AV, Poupon C, Hennerici MG, Gass A, Wessa M (2013). Impaired anatomical connectivity and related executive functions: differentiating vulnerability and disease marker in bipolar disorder. Biological Psychiatry 74, 908-916.
37. Lu LH, Zhou XJ, Fitzgerald J, Keedy SK, Reilly JL, Passarotti AM, Sweeney JA, Pavuluri M (2012). Microstructural abnormalities of white matter differentiate pediatric and adult-onset bipolar disorder. Bipolar Disorders 14, 597-606.
38. Lu LH, Zhou XJ, Keedy SK, Reilly JL, Sweeney JA (2011). White matter microstructure in untreated first episode bipolar disorder with psychosis: comparison with schizophrenia. Bipolar Disorders 13, 604-613.
39. MacQueen GM, Grof P, Alda M, Marriott M, Young LT, Duffy A (2004). A pilot study of visual backward masking performance among affected versus unaffected offspring of parents with bipolar disorder. Bipolar Disorders 6, 374-378.
40. Macritchie KA, Lloyd AJ, Bastin ME, Vasudev K, Gallagher P, Eyre R, Marshall I, Wardlaw JM, Ferrier IN, Moore PB, Young AH (2010). White matter microstructural abnormalities in euthymic bipolar disorder. British Journal of Psychiatry 196, 52-58.
41. Mahon K, Burdick KE, Ikuta T, Braga RJ, Gruner P, Malhotra AK, Szeszko PR (2013). Abnormal temporal lobe white matter as a biomarker for genetic risk of bipolar disorder. Biological Psychiatry 73, 177-182.
42. Martino J, Brogna C, Robles SG, Vergani F, Duffau H (2010). Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data. Cortex 46, 691-699.
43. McGuffin P, Rijsdijk F, Andrew M, Sham P, Katz R, Cardno A (2003). The heritability of bipolar affective disorder and the genetic relationship to unipolar depression. Archives of General Psychiatry 60, 497-502.
44. McIntosh AM, Moorhead TW, Job D, Lymer GK, Muñoz Maniega S, McKirdy J, Sussmann JE, Baig BJ, Bastin ME, Porteous D, Evans KL, Johnstone EC, Lawrie SM, Hall J (2008). The effects of a neuregulin 1 variant on white matter density and integrity. Molecular Psychiatry 13, 1054-1059.
45. Merikangas KR, Akiskal HS, Angst J, Greenberg PE, Hirschfeld RMA, Petukhova M, Kessler RC (2007). Lifetime and 12-month prevalence of bipolar spectrum disorder in the National Comorbidity Survey replication. Archives of General Psychiatry 64, 543-552.
46. Mori S, Oishi K, Jiang H, Jiang L, Li X, Akhter K, Hua K, Faria AV, Mahmood A, Woods R, Toga AW, Pike GB, Neto PR, Evans A, Zhang J, Huang H, Miller MI, van Zijl P, Mazziotta J (2008). Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. NeuroImage 40, 570-582.
47. Nichols TE, Holmes AP (2002). Nonparametric permutation tests for functional neuroimaging: a primer with examples. Human Brain Mapping 15, 1-25.
48. Nortje G, Stein DJ, Radua J, Mataix-Cols D, Horn N (2013). Systematic review and voxel-based meta-Analysis of diffusion tensor imaging studies in bipolar disorder. Journal of Affective Disorders 150, 192-200.
49. Oertel-Knöchel V, Reinke B, Alves G, Jurcoane A, Wenzler S, Prvulovic D, Linden D, Knöchel C (2014). Frontal white matter alterations are associated with executive cognitive function in euthymic bipolar patients. Journal of Affective Disorders 155, 223-233.
50. Ongür D, Drevets WC, Price JL (1998). Glial reduction in the subgenual prefrontal cortex in mood disorders. Proceedings of the National Academy of Sciences of the United States of America 95, 13290-13295.
51. Ozerdem A, Güntekin B, Saatçi E, Tunca Z, Baar E (2010). Disturbance in long distance gamma coherence in bipolar disorder. Progress in Neuro-Psychopharmacology and Biological Psychiatry 34, 861-865.
52. Ozerdem A, Güntekin B, Tunca Z, Baar E (2008). Brain oscillatory responses in patients with bipolar disorder manic episode before and after valproate treatment. Brain Research 1235, 98-108.
53. Pavuluri MN, Birmaher B, Naylor MW (2005). Pediatric bipolar disorder: a review of the past 10 years. Journal of the American Academy of Child and Adolescent Psychiatry 44, 846-871.
54. Quintin P, Benkelfat C, Launay JM, Arnulf I, Pointereau-Bellenger A, Barbault S, Alvarez JC, Varoquaux O, Perez-Diaz F, Jouvent R, Leboyer M (2001). Clinical and neurochemical effect of acute tryptophan depletion in unaffected relatives of patients with bipolar affective disorder. Biological Psychiatry 50, 184-190.
55. Robinson LJ, Ferrier IN (2006). Evolution of cognitive impairment in bipolar disorder: a systematic review of cross-sectional evidence. Bipolar Disorders 8, 103-116.
56. Skudlarski P, Schretlen DJ, Thaker GK, Stevens MC, Keshavan MS, Sweeney JA, Tamminga CA, Clementz BA, O'Neil K, Pearlson GD (2013). Diffusion tensor imaging white matter endophenotypes in patients with schizophrenia or psychotic bipolar disorder and their relatives. American Journal of Psychiatry 170, 886-898.
57. Smith SM (2002). Fast robust automated brain extraction. Human Brain Mapping 17, 143-155.
58. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TE (2006). Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage 31, 1487-1505.
59. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23, 208-219.
60. Smith SM, Nichols TE (2009). Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage 44, 83-98.
61. Smoller JW, Finn CT (2003). Family, twin, and adoption studies of bipolar disorder. American Journal of Medical Genetics Part C: Seminars in Medical Genetics 123, 48-58.
62. Song J, Bergen SE, Kuja-Halkola R, Larsson H, Landén M, Lichtenstein P (2015). Bipolar disorder and its relation to major psychiatric disorders: a family-based study in the Swedish population. Bipolar Disorders 17, 184-193.
63. Sprooten E, Brumbaugh MS, Knowles EE, McKay DR, Lewis J, Barrett J, Landau S, Cyr L, Kochunov P, Winkler AM, Pearlson GD, Glahn DC (2013). Reduced white matter integrity in sibling pairs discordant for bipolar disorder. American Journal of Psychiatry 170, 1317-1325.
64. Sprooten E, Sussmann JE, Clugston A, Peel A, McKirdy J, Moorhead TW, Anderson S, Shand AJ, Giles S, Bastin ME, Hall J, Johnstone EC, Lawrie SM, McIntosh AM (2011). White matter integrity in individuals at high genetic risk of bipolar disorder. Biological Psychiatry 70, 350-356.
65. Strakowski SM, Delbello MP, Adler CM (2005). The functional neuroanatomy of bipolar disorder: a review of neuroimaging findings. Molecular Psychiatry 10, 105-116.
66. Sussmann JE, Lymer GK, McKirdy J, Moorhead TW, Muñoz Maniega S, Job D, Hall J, Bastin ME, Johnstone EC, Lawrie SM, McIntosh AM (2009). White matter abnormalities in bipolar disorder and schizophrenia detected using diffusion tensor magnetic resonance imaging. Bipolar Disorders 11, 11-18.
67. Swann AC, Lijffijt M, Lane SD, Steinberg JL, Moeller FG (2009a). Severity of bipolar disorder is associated with impairment of response inhibition. Journal of Affective Disorders 116, 30-36.
68. Swann AC, Lijffijt M, Lane SD, Steinberg JL, Moeller FG (2009b). Increased trait-like impulsivity and course of illness in bipolar disorder. Bipolar Disorders 11, 280-288.
69. Thomson PA, Christoforou A, Morris SW, Adie E, Pickard BS, Porteous DJ, Muir WJ, Blackwood DH, Evans KL (2007). Association of neuregulin 1 with schizophrenia and bipolar disorder in a second cohort from the Scottish population. Molecular Psychiatry 12, 94-104.
70. Tkachev D, Mimmack ML, Ryan MM, Wayland M, Freeman T, Jones PB, Starkey M, Webster MJ, Yolken RH, Bahn S (2003). Oligodendrocyte dysfunction in schizophrenia and bipolar disorder. Lancet 362, 798-805.
71. Torgerson CM, Irimia A, Leow AD, Bartzokis G, Moody TD, Jennings RG, Alger JR, Van Horn JD, Altshuler LL (2013). DTI tractography and white matter fiber tract characteristics in euthymic bipolar I patients and healthy control subjects. Brain Imaging and Behavior 7, 129-139.
72. Uranova NA, Vostrikov VM, Orlovskaya DD, Rachmanova VI (2004). Oligodendroglial density in the prefrontal cortex in schizophrenia and mood disorders: a study from the Stanley Neuropathology Consortium. Schizophrenia Research 67, 269-275.
73. Vederine FE, Wessa M, Leboyer M, Houenou J (2011). A meta-Analysis of whole-brain diffusion tensor imaging studies in bipolar disorder. Progress in Neuro-Psychopharmacology and Biological Psychiatry 35, 1820-1826.
74. Versace A, Ladouceur CD, Romero S, Birmaher B, Axelson DA, Kupfer DJ, Phillips ML (2010). Altered development of white matter in youth at high familial risk for bipolar disorder: a diffusion tensor imaging study. Journal of the American Academy of Child and Adolescent Psychiatry 49, 1249-1259.
75. Vostrikov VM, Uranova NA, Orlovskaya DD (2007). Deficit of perineuronal oligodendrocytes in the prefrontal cortex in schizophrenia and mood disorders. Schizophrenia Research 94, 273-280.
76. Wessa M, Houenou J, Leboyer M, Chanraud S, Poupon C, Martinot JL, Paillére-Martinot ML (2009). Microstructural white matter changes in euthymic bipolar patients: a wholebrain diffusion tensor imaging study. Bipolar Disorders 11, 504-514.
77. Wheeler-Kingshott CAM, Cercignani M (2009). About "axial" and "radial" diffusivities. Magnetic Resonance in Medicine 61, 1255-1260.
78. Xu J, Kober H, Carroll KM, Rounsaville BJ, Pearlson GD, Potenza MN (2012). White matter integrity and behavioral activation in healthy subjects. Human Brain Mapping 33, 994-1002.
79. Xu J, Rasmussen I-A, Berntsen EM, Moss K, Shnier R, Lagopoulos J, Malhi GS (2007). A growth in bipolar disorder? Acta Psychiatrica Scandinavica 115, 246-250.
80. Zanetti MV, Jackowski MP, Versace A, Almeida JR, Hassel S, Duran FL, Busatto GF, Kupfer DJ, Phillips ML (2009). State-dependent microstructural white matter changes in bipolar I depression. European Archives of Psychiatry and Clinical Neuroscience 259, 316-328.
81. Zorlu N, Gelal F, Kuserli A, Cenik E, Durmaz E, Saricicek A, Gulseren S (2013). Abnormal white matter integrity and decision-making deficits in alcohol dependence. Psychiatry Research 214, 382-388.