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Interhemispheric white matter integrity in young people with bipolar disorder and at high genetic risk

Published online by Cambridge University Press:  13 June 2016

G. Roberts
Affiliation:
School of Psychiatry, University of New South Wales, Sydney, NSW, Australia Black Dog Institute, Prince of Wales Hospital, Randwick, NSW,Australia
W. Wen
Affiliation:
School of Psychiatry, University of New South Wales, Sydney, NSW, Australia Prince of Wales Hospital, Sydney, NSW, Australia
A. Frankland
Affiliation:
School of Psychiatry, University of New South Wales, Sydney, NSW, Australia Black Dog Institute, Prince of Wales Hospital, Randwick, NSW,Australia
T. Perich
Affiliation:
School of Psychiatry, University of New South Wales, Sydney, NSW, Australia Black Dog Institute, Prince of Wales Hospital, Randwick, NSW,Australia
E. Holmes-Preston
Affiliation:
School of Psychiatry, University of New South Wales, Sydney, NSW, Australia Black Dog Institute, Prince of Wales Hospital, Randwick, NSW,Australia
F. Levy
Affiliation:
School of Psychiatry, University of New South Wales, Sydney, NSW, Australia Prince of Wales Hospital, Sydney, NSW, Australia
R. K. Lenroot
Affiliation:
School of Psychiatry, University of New South Wales, Sydney, NSW, Australia Neuroscience Research Australia, Sydney, NSW, Australia
D. Hadzi-Pavlovic
Affiliation:
School of Psychiatry, University of New South Wales, Sydney, NSW, Australia Black Dog Institute, Prince of Wales Hospital, Randwick, NSW,Australia
J. I. Nurnberger
Affiliation:
Department of Psychiatry, Indiana University School of Medicine, Indianapolis, IN, USA
M. Breakspear
Affiliation:
Division of Mental Health Research, Queensland Institute of Medical Research, Brisbane, QLD, Australia Royal Brisbane and Women's Hospital, Brisbane, QLD, Australia
P. B. Mitchell*
Affiliation:
School of Psychiatry, University of New South Wales, Sydney, NSW, Australia Black Dog Institute, Prince of Wales Hospital, Randwick, NSW,Australia Prince of Wales Hospital, Sydney, NSW, Australia
*
*Address for correspondence: P. B. Mitchell, Scientia Professor Philip Mitchell, School of Psychiatry, University of New South Wales, Prince of Wales Hospital, Randwick, NSW 2031, Australia. (Email: phil.mitchell@unsw.edu.au)

Abstract

Background

White matter (WM) impairments have been reported in patients with bipolar disorder (BD) and those at high familial risk of developing BD. However, the distribution of these impairments has not been well characterized. Few studies have examined WM integrity in young people early in the course of illness and in individuals at familial risk who have not yet passed the peak age of onset.

Method

WM integrity was examined in 63 BD subjects, 150 high-risk (HR) individuals and 111 participants with no family history of mental illness (CON). All subjects were aged 12 to 30 years.

Results

This young BD group had significantly lower fractional anisotropy within the genu of the corpus callosum (CC) compared with the CON and HR groups. Moreover, the abnormality in the genu of the CC was also present in HR participants with recurrent major depressive disorder (MDD) (n = 16) compared with CON participants.

Conclusions

Our findings provide important validation of interhemispheric abnormalities in BD patients. The novel finding in HR subjects with recurrent MDD – a group at particular risk of future hypo/manic episodes – suggests that this may potentially represent a trait marker for BD, though this will need to be confirmed in longitudinal follow-up studies.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2016 

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References

Aboitiz, F, Scheibel, AB, Fisher, RS, Zaidel, E (1992). Fiber composition of the human corpus callosum. Brain Research 598, 143153.CrossRefGoogle ScholarPubMed
Ajilore, O, Vizueta, N, Walshaw, P, Zhan, L, Leow, A, Altshuler, LL (2015). Connectome signatures of neurocognitive abnormalities in euthymic bipolar I disorder. Journal of Psychiatric Research 68, 3744.Google Scholar
Arnone, D, McIntosh, A, Chandra, P, Ebmeier, K (2008). Meta-analysis of magnetic resonance imaging studies of the corpus callosum in bipolar disorder. Acta Psychiatrica Scandinavia 118, 357362.Google Scholar
Assaf, Y, Pasternak, O (2008). Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. Journal of Molecular Neuroscience 34, 5161.Google Scholar
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, 238244.Google Scholar
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, 558568.Google Scholar
Bauer, IE, Ouyang, A, Mwangi, B, Sanches, M, Zunta-Soares, GB, Keefe, RS, Huang, H, Soares, JC (2015). Reduced white matter integrity and verbal fluency impairment in young adults with bipolar disorder: a diffusion tensor imaging study. Journal of Psychiatric Research 62, 115122.Google Scholar
Bearden, CE, Van Erp, TG, Dutton, RA, Boyle, C, Madsen, S, Luders, E, Kieseppa, T, Tuulio-Henriksson, A, Huttunen, M, Partonen, T, Kaprio, J, Lonnqvist, J, Thompson, PM, Cannon, TD (2011). Mapping corpus callosum morphology in twin pairs discordant for bipolar disorder. Cerebral Cortex 21, 24152424.CrossRefGoogle ScholarPubMed
Bellani, M, Brambilla, P (2011). Diffusion imaging studies of white matter integrity in bipolar disorder. Epidemiology and Psychiatric Sciences 20, 137140.Google Scholar
Bellani, M, Yeh, P-H, Tansella, M, Balestrieri, M, Soares, J, Brambilla, P (2009). DTI studies of corpus callosum in bipolar disorder. Biochemical Society Transactions 37, 10961098.Google Scholar
Benjamini, Y, Hochberg, Y (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological) 57, 289300.CrossRefGoogle Scholar
Bessette, KL, Nave, AM, Caprihan, A, Stevens, MC (2014). White matter abnormalities in adolescents with major depressive disorder. Brain Imaging and Behavior 8, 531541.Google Scholar
Birmaher, B, Axelson, D, Monk, K, Kalas, C, Goldstein, B, Hickey, MB, Obreja, M, Ehmann, M, Iyengar, S, Shamseddeen, W, Kupfer, D, Brent, D (2009). Lifetime psychiatric disorders in school-aged offspring of parents with bipolar disorder: the Pittsburgh Bipolar Offspring study. Archives of General Psychiatry 66, 287296.Google Scholar
Breakspear, M, Roberts, G, Green, MJ, Nguyen, VT, Frankland, A, Levy, F, Lenroot, R, Mitchell, PB (2015). Network dysfunction of emotional and cognitive processes in those at genetic risk of bipolar disorder. Brain 138, 34273439.Google Scholar
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, 527534.Google Scholar
Chao, T-C, Chou, M-C, Yang, P, Chung, H-W, Wu, M-T (2009). Effects of interpolation methods in spatial normalization of diffusion tensor imaging data on group comparison of fractional anisotropy. Magnetic Resonance Imaging 27, 681690.Google Scholar
Chiang, M-C, Barysheva, M, McMahon, KL, De Zubicaray, GI, Johnson, K, Montgomery, GW, Martin, NG, Toga, AW, Wright, MJ, Shapshak, P, Thompson, PM (2012). Gene network effects on brain microstructure and intellectual performance identified in 472 twins. Journal of Neuroscience 32, 87328745.Google Scholar
Davidson, RJ, Irwin, W (1999). The functional neuroanatomy of emotion and affective style. Trends in Cognitive Science 3, 1121.CrossRefGoogle ScholarPubMed
De Lacoste, MC, Kirkpatrick, JB, Ross, ED (1985). Topography of the human corpus callosum. Journal of Neuropathology and Experimental Neurology 44, 578591.Google Scholar
Duffy, A (2010). From predisposition to illness: genetically sensitive intermediate pathways to mood disorders. British Journal of Psychiatry 197, 341342.Google Scholar
Emsell, L, Chaddock, C, Forde, N, Van Hecke, W, Barker, GJ, Leemans, A, Sunaert, S, Walshe, M, Bramon, E, Cannon, D, 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, 21392150.Google Scholar
Endicott, J, Spitzer, RL, Fleiss, JL, Cohen, J (1976). The Global Assessment Scale: a procedure for measuring overall severity of psychiatric disturbance. Archives of General Psychiatry 33, 766771.Google Scholar
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, 799809.Google Scholar
Galinowski, A, Miranda, R, Lemaitre, H, Paillère Martinot, ML, Artiges, E, Vulser, H, Goodman, R, Penttilä, J, Struve, M, Barbot, A, Fadai, T, Poustka, L, Conrod, P, Banaschewski, T, Barker, GJ, Bokde, A, Bromberg, U, Büchel, C, Flor, H, Gallinat, J, Garavan, H, Heinz, A, Ittermann, B, Kappel, V, Lawrence, C, Loth, E, Mann, K, Nees, F, Paus, T, Pausova, Z, Poline, JB, Rietschel, M, Robbins, TW, Smolka, M, Schumann, G, Martinot, JL; IMAGEN Consortium (2015). Resilience and corpus callosum microstructure in adolescence. Psychological Medicine 45, 22852294.Google Scholar
Geller, B, Zimerman, B, Williams, M, Bolhofner, K, Craney, JL, DelBello, M, Soutullo, C (2001). Reliability of the Washington University in St. Louis Kiddie Schedule for Affective Disorders and Schizophrenia (WASH-U-KSADS) mania and rapid cycling sections. Journal of the American Academy of Child and Adolescent Psychiatry 40, 450455.CrossRefGoogle Scholar
Hajek, T, Carrey, N, Alda, M (2005). Neuroanatomical abnormalities as risk factors for bipolar disorder. Bipolar Disorders 7, 393403.Google Scholar
Heng, S, Song, AW, Sim, K (2010). White matter abnormalities in bipolar disorder: insights from diffusion tensor imaging studies. Journal of Neural Transmission 117, 639654.Google Scholar
Hillegers, MH, Reichart, CG, Wals, M, Verhulst, FC, Ormel, J, Nolen, WA (2005). Five-year prospective outcome of psychopathology in the adolescent offspring of bipolar parents. Bipolar Disorders 7, 344350.Google Scholar
Imperati, D, Colcombe, S, Kelly, C, Di Martino, A, Zhou, J, Castellanos, FX, Milham, MP (2011). Differential development of human brain white matter tracts. PLoS ONE 6, e23437.Google Scholar
Jones, DK, Griffin, LD, Alexander, DC, Catani, M, Horsfield, MA, Howard, R, Williams, SC (2002). Spatial normalization and averaging of diffusion tensor MRI data sets. NeuroImage 17, 592617.CrossRefGoogle ScholarPubMed
Kaufman, J, Birmaher, B, Brent, D, Rao, U, Flynn, C, Moreci, P, Ryan, N (1997). Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. Journal of the American Academy of Child and Adolescent Psychiatry 36, 980988.Google Scholar
Lagopoulos, J, Hermens, DF, Hatton, SN, Tobias-Webb, J, Griffiths, K, Naismith, SL, Scott, EM, Hickie, IB (2013). Microstructural white matter changes in the corpus callosum of young people with bipolar disorder: a diffusion tensor imaging study. PLOS ONE 8, e59108.Google Scholar
Lebel, C, Gee, M, Camicioli, R, Wieler, M, Martin, W, Beaulieu, C (2012). Diffusion tensor imaging of white matter tract evolution over the lifespan. NeuroImage 60, 340352.CrossRefGoogle ScholarPubMed
Leckman, J, Sholomskas, D, Thompson, W, Belanger, A, Weissman, M (1982). Best estimate of lifetime psychiatric diagnosis: a methodological study. Archives of General Psychiatry 39, 879883.Google Scholar
Leow, A, Ajilore, O, Zhan, L, Arienzo, D, Gadelkarim, J, Zhang, A, Moody, T, Van Horn, J, Feusner, J, Kumar, A, Thompson, P, Altshuler, L (2013). Impaired inter-hemispheric integration in bipolar disorder revealed with brain network analyses. Biological Psychiatry 73, 183193.Google Scholar
Li, J, Kale, Edmiston E, Chen, K, Tang, Y, Ouyang, X, Jiang, Y, Fan, G, Ren, L, Liu, J, Zhou, Y, Jiang, W, Liu, Z, Xu, K, Wang, F (2014). A comparative diffusion tensor imaging study of corpus callosum subregion integrity in bipolar disorder and schizophrenia. Psychiatry Research 221, 5862.Google Scholar
Liao, Y, Huang, X, Wu, Q, Yang, C, Kuang, W, Du, M, Lui, S, Yue, Q, Chan, RC, Kemp, GJ, Gong, Q (2013). Is depression a disconnection syndrome? Meta-analysis of diffusion tensor imaging studies in patients with MDD. Journal of Psychiatry and Neuroscience 38, 4956.Google Scholar
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, 908916.CrossRefGoogle ScholarPubMed
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, 177182.Google Scholar
Matsuo, K, Kopecek, M, Nicoletti, M, Hatch, J, Watanabe, Y, Nery, F, Zunta-Soares, G, Soares, J (2011). New structural brain imaging endophenotype in bipolar disorder. Molecular Psychiatry 17, 412420.Google Scholar
McCormack, C, Green, MJ, Rowland, JE, Roberts, G, Frankland, A, Hadzi-Pavlovic, D, Joslyn, C, Lau, P, Wright, A, Levy, F, Lenroot, RK, Mitchell, PB (2016). Neuropsychological and social cognitive function in young people at genetic risk of bipolar disorder. Psychological Medicine 46, 745758.Google Scholar
McDonald, C, Bullmore, ET, Sham, PC, Chitnis, X, Wickham, H, Bramon, E, Murray, RM (2004). Association of genetic risks for schizophrenia and bipolar disorder with specific and generic brain structural endophenotypes. Archives of General Psychiatry 61, 974984.Google Scholar
McKenna, BS, Theilmann, RJ, Sutherland, AN, Eyler, LT (2015). Fusing functional MRI and diffusion tensor imaging measures of brain function and structure to predict working memory and processing speed performance among inter-episode bipolar patients. Journal of the International Neuropsychological Society 21, 330341.Google Scholar
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, 192200.Google Scholar
Nurnberger, JI Jr, McInnis, M, Reich, W, Kastelic, E, Wilcox, HC, Glowinski, A, Mitchell, P, Fisher, C, Erpe, M, Gershon, ES, Berrettini, W, Laite, G, Schweitzer, R, Rhoadarmer, K, Coleman, VV, Cai, X, Azzouz, F, Liu, H, Kamali, M, Brucksch, C, Monahan, PO (2011). A high-risk study of bipolar disorder: childhood clinical phenotypes as precursors of major mood disorders. Archives of General Psychiatry 68, 10121020.Google Scholar
Perich, T, Lau, P, Hadzi-Pavlovic, D, Roberts, G, Frankland, A, Wright, A, Green, M, Breakspear, M, Corry, J, Radlinska, B, McCormack, C, Joslyn, C, Levy, F, Lenroot, R, Nurnberger, JIJ, Mitchell, PB (2015). What clinical features precede the onset of bipolar disorder? Journal of Psychiatric Research 62, 7177.CrossRefGoogle ScholarPubMed
Phillips, ML, Swartz, HA (2014). A critical appraisal of neuroimaging studies of bipolar disorder: toward a new conceptualization of underlying neural circuitry and a road map for future research. American Journal of Psychiatry 171, 829843.Google Scholar
Poletti, S, Bollettini, I, Mazza, E, Locatelli, C, Radaelli, D, Vai, B, Smeraldi, E, Colombo, C, Benedetti, F (2015). Cognitive performances associate with measures of white matter integrity in bipolar disorder. Journal of Affective Disorders 174, 342352.Google Scholar
Roberts, G, Green, MJ, Breakspear, M, McCormack, C, Frankland, A, Wright, A, Levy, F, Lenroot, R, Chan, HN, Mitchell, PB (2013). Reduced inferior frontal gyrus activation during response inhibition to emotional stimuli in youth at high risk of bipolar disorder. Biological Psychiatry 74, 5561.Google Scholar
Roybal, DJ, Barnea-Goraly, N, Kelley, R, Bararpour, L, Howe, ME, Reiss, AL, Chang, KD (2015). Widespread white matter tract aberrations in youth with familial risk for bipolar disorder. Psychiatry Research 232, 184192.Google Scholar
Sarrazin, S, d'Albis, MA, McDonald, C, Linke, J, Wessa, M, Phillips, M, Delavest, M, Emsell, L, Versace, A, Almeida, J, Mangin, JF, Poupon, C, Le Dudal, K, Daban, C, Hamdani, N, Leboyer, M, Houenou, J (2015). Corpus callosum area in patients with bipolar disorder with and without psychotic features: an international multicentre study. Journal of Psychiatry and Neuroscience 40, 352359.Google Scholar
Sarrazin, S, Poupon, C, Linke, J, Wessa, M, Phillips, M, Delavest, M, Versace, A, Almeida, J, Guevara, P, Duclap, D, Duchesnay, E, Mangin, JF, Le Dudal, K, Daban, C, Hamdani, N, D'Albis, MA, Leboyer, M, Houenou, J (2014). A multicenter tractography study of deep white matter tracts in bipolar I disorder: psychotic features and interhemispheric disconnectivity. JAMA Psychiatry 71, 388396.Google Scholar
Saxena, K, Tamm, L, Walley, A, Simmons, A, Rollins, N, Chia, J, Soares, JC, Emslie, GJ, Fan, X, Huang, H (2012). A preliminary investigation of corpus callosum and anterior commissure aberrations in aggressive youth with bipolar disorders. Journal of Child and Adolescent Psychopharmacology 22, 112119.CrossRefGoogle ScholarPubMed
Shaffer, D, Gould, MS, Brasic, J, Ambrosini, P, Fisher, P, Bird, H, Aluwahlia, S (1983). A Children's Global Assessment Scale (CGAS). Archives of General Psychiatry 40, 12281231.Google Scholar
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, 886898.Google Scholar
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, 14871505.Google Scholar
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, 13171325.Google Scholar
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, 350356.Google Scholar
Thomason, ME, Thompson, PM (2011). Diffusion imaging, white matter, and psychopathology. Clinical Psychology 7, 6385.Google Scholar
Vederine, F-E, Wessa, M, Leboyer, M, Houenou, J (2011). A meta-analysis of whole-brain diffusion tensor imaging studies in bipolar disorder. Progress in Neuropsychopharmacology and Biological Psychiatry 35, 18201826.Google Scholar
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, 12491259.Google Scholar
Walterfang, M, Wood, AG, Barton, S, Velakoulis, D, Chen, J, Reutens, DC, Kempton, MJ, Haldane, M, Pantelis, C, Frangou, S (2009). Corpus callosum size and shape alterations in individuals with bipolar disorder and their first-degree relatives. Progress in Neuro-Psychopharmacology and Biological Psychiatry 33, 10501057.CrossRefGoogle ScholarPubMed
Wechsler, D (1999). Wechsler Abbreviated Scale of Intelligence. The Psychological Corporation: Harcourt Brace & Company: New York.Google Scholar
Xu, K, Jiang, W, Ren, L, Ouyang, X, Kong, L, Womer, F, Liu, Z, Blumberg, HP, Tang, Y, Wang, F (2013). Impaired interhemispheric connectivity in medication-naive patients with major depressive disorder. Journal of Psychiatry and Neuroscience 38, 4348.Google Scholar
Young, R, Biggs, J, Ziegler, V, Meyer, D (1978). A rating scale for mania: reliability, validity and sensitivity. British Journal of Psychiatry 133, 429435.Google Scholar
Yurgelun-Todd, DA, Silveri, MM, Gruber, SA, Rohan, ML, Pimentel, PJ (2007). White matter abnormalities observed in bipolar disorder: a diffusion tensor imaging study. Bipolar Disorders 9, 504512.Google Scholar
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