White matter differences in euthymic bipolar I disorder: a combined magnetic resonance imaging and diffusion tensor imaging voxel-based study
Corresponding Author
Louise Emsell
Clinical Neuroimaging Laboratory, National University of Ireland Galway, Galway, Ireland
Translational MRI, Department of Imaging and Pathology, KU Leuven and Radiology, University Hospitals Leuven, Leuven, Belgium
Corresponding author:
Dr. Louise Emsell
Department of Radiology (MIRC)
University Hospital Gasthuisberg
UZ Herestraat 49 - Box 7003
Leuven 3000
Belgium
Fax: +32 16 34 37 65
E-mail: [email protected]
Search for more papers by this authorCamilla Langan
Clinical Neuroimaging Laboratory, National University of Ireland Galway, Galway, Ireland
Search for more papers by this authorWim Van Hecke
Department of Radiology, University Hospital Antwerp, Edegem, Antwerp, Belgium
icoMetrix nv, Leuven, Belgium
Search for more papers by this authorGareth J Barker
Department of Neuroimaging, Institute of Psychiatry, King's College London, Centre for Neuroimaging Sciences, London, UK
Search for more papers by this authorAlexander Leemans
Image Sciences Institute, University Medical Center Utrecht, Utrecht, The Netherlands
Search for more papers by this authorStefan Sunaert
Translational MRI, Department of Imaging and Pathology, KU Leuven and Radiology, University Hospitals Leuven, Leuven, Belgium
Search for more papers by this authorPeter McCarthy
Clinical Neuroimaging Laboratory, National University of Ireland Galway, Galway, Ireland
Search for more papers by this authorRachel Nolan
Clinical Neuroimaging Laboratory, National University of Ireland Galway, Galway, Ireland
Search for more papers by this authorDara M Cannon
Clinical Neuroimaging Laboratory, National University of Ireland Galway, Galway, Ireland
Search for more papers by this authorColm McDonald
Clinical Neuroimaging Laboratory, National University of Ireland Galway, Galway, Ireland
Search for more papers by this authorCorresponding Author
Louise Emsell
Clinical Neuroimaging Laboratory, National University of Ireland Galway, Galway, Ireland
Translational MRI, Department of Imaging and Pathology, KU Leuven and Radiology, University Hospitals Leuven, Leuven, Belgium
Corresponding author:
Dr. Louise Emsell
Department of Radiology (MIRC)
University Hospital Gasthuisberg
UZ Herestraat 49 - Box 7003
Leuven 3000
Belgium
Fax: +32 16 34 37 65
E-mail: [email protected]
Search for more papers by this authorCamilla Langan
Clinical Neuroimaging Laboratory, National University of Ireland Galway, Galway, Ireland
Search for more papers by this authorWim Van Hecke
Department of Radiology, University Hospital Antwerp, Edegem, Antwerp, Belgium
icoMetrix nv, Leuven, Belgium
Search for more papers by this authorGareth J Barker
Department of Neuroimaging, Institute of Psychiatry, King's College London, Centre for Neuroimaging Sciences, London, UK
Search for more papers by this authorAlexander Leemans
Image Sciences Institute, University Medical Center Utrecht, Utrecht, The Netherlands
Search for more papers by this authorStefan Sunaert
Translational MRI, Department of Imaging and Pathology, KU Leuven and Radiology, University Hospitals Leuven, Leuven, Belgium
Search for more papers by this authorPeter McCarthy
Clinical Neuroimaging Laboratory, National University of Ireland Galway, Galway, Ireland
Search for more papers by this authorRachel Nolan
Clinical Neuroimaging Laboratory, National University of Ireland Galway, Galway, Ireland
Search for more papers by this authorDara M Cannon
Clinical Neuroimaging Laboratory, National University of Ireland Galway, Galway, Ireland
Search for more papers by this authorColm McDonald
Clinical Neuroimaging Laboratory, National University of Ireland Galway, Galway, Ireland
Search for more papers by this authorAbstract
Objectives
A broad range of subtle and markedly heterogenous neuroanatomical abnormalities of grey matter and white matter have been reported in bipolar disorder. Euthymic bipolar disorder patients represent a clinically homogenous group in which to identify trait-based biomarkers of bipolar disorder. In this study, we sought to clarify the nature and extent of neuroanatomical differences in a large, clinically homogeneous group of euthymic bipolar disorder patients.
Methods
Structural magnetic resonance imaging (sMRI) was obtained for 60 patients with prospectively confirmed euthymic bipolar I disorder and 60 individually age- and gender-matched healthy volunteers. High angular resolution diffusion tensor imaging (DTI) scans were obtained for a subset of this sample comprising 35 patients and 43 controls. Voxel-based analysis of both sMRI and DTI data sets was performed.
Results
Bipolar disorder patients displayed global reductions in white matter volume and fractional anisotropy reductions in the corpus callosum, posterior cingulum, and prefrontal white matter compared with controls. There were corresponding increases in radial diffusivity in the callosal splenium in patients compared with controls. No significant group differences were detected in grey matter. In patients, lithium was associated with a bilateral increase in grey matter volume in the temporal lobes, but not with any DTI parameter.
Conclusions
Euthymic bipolar I disorder is characterized by both diffuse global white matter deficits and potential regional disorganization in interhemispheric and longitudinal tracts, while grey matter appears to be preserved.
References
- 1Robinson LJ, Thompson JM, Gallagher P et al. A meta-analysis of cognitive deficits in euthymic patients with bipolar disorder. J Affect Disord 2006; 93: 105–115.
- 2Langan C, McDonald C. Neurobiological trait abnormalities in bipolar disorder. Mol Psychiatry 2009; 14: 833–846.
- 3Kempton MJ, Geddes JR, Ettinger U, Williams SC, Grasby PM. Meta-analysis, database, and meta-regression of 98 structural imaging studies in bipolar disorder. Arch Gen Psychiatry 2008; 65: 1017–1032.
- 4Hallahan B, Newell J, Soares JC et al. Structural magnetic resonance imaging in bipolar disorder: an international collaborative mega-analysis of individual adult patient data. Biol Psychiatry 2011; 69: 326–335.
- 5Vederine FE, Wessa M, Leboyer M, Houenou J. A meta-analysis of whole-brain diffusion tensor imaging studies in bipolar disorder. Prog Neuropsychopharmacol Biol Psychiatry 2011; 35: 1820–1826.
- 6Emsell L, McDonald C. The structural neuroimaging of bipolar disorder. Int Rev Psychiatry 2009; 21: 297–313.
- 7Usher J, Menzel P, Schneider-Axmann T et al. Increased right amygdala volume in lithium-treated patients with bipolar I disorder. Acta Psychiatr Scand 2010; 121: 119–124.
- 8Moore GJ, Cortese BM, Glitz DA et al. A longitudinal study of the effects of lithium treatment on prefrontal and subgenual prefrontal gray matter volume in treatment-responsive bipolar disorder patients. J Clin Psychiatry 2009; 70: 699–705.
- 9Lyoo IK, Dager SR, Kim JE et al. Lithium-induced gray matter volume increase as a neural correlate of treatment response in bipolar disorder: a longitudinal brain imaging study. Neuropsychopharmacology 2010; 35: 1743–1750.
- 10Foland-Ross LC, Thompson PM, Sugar CA et al. Investigation of cortical thickness abnormalities in lithium-free adults with bipolar I disorder using cortical pattern matching. Am J Psychiatry 2011; 168: 530–539.
- 11Davis KA, Kwon A, Cardenas VA, Deicken RF. Decreased cortical gray and cerebral white matter in male patients with familial bipolar I disorder. J Affect Disord 2004; 82: 475–485.
- 12El-Badri SM, Cousins DA, Parker S et al. Magnetic resonance imaging abnormalities in young euthymic patients with bipolar affective disorder. Br J Psychiatry 2006; 189: 81–82.
- 13Baldaçara L, Nery-Fernandes F, Rocha M et al. Is cerebellar volume related to bipolar disorder? J Affect Disord 2011; 135: 305–309.
- 14Sussmann JE, Lymer GK, McKirdy J et al. White matter abnormalities in bipolar disorder and schizophrenia detected using diffusion tensor magnetic resonance imaging. Bipolar Disord 2009; 11: 11–18.
- 15Macritchie KA, Lloyd AJ, Bastin ME et al. White matter microstructural abnormalities in euthymic bipolar disorder. Br J Psychiatry 2010; 196: 52–58.
- 16Houenou J, Wessa M, Douaud G et al. Increased white matter connectivity in euthymic bipolar patients: diffusion tensor tractography between the subgenual cingulate and the amygdalo-hippocampal complex. Mol Psychiatry 2007; 12: 1001–1010.
- 17Wessa M, Houenou J, Leboyer M et al. Microstructural white matter changes in euthymic bipolar patients: a whole-brain diffusion tensor imaging study. Bipolar Disord 2009; 11: 504–514.
- 18Zanetti MV, Jackowski MP, Versace A et al. State-dependent microstructural white matter changes in bipolar I depression. Eur Arch Psychiatry Clin Neurosci 2009; 259: 316–328.
- 19Basser PJ, Mattiello J, LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 1994; 103: 247–254.
- 20Tournier JD, Mori S, Leemans A. Diffusion tensor imaging and beyond. Magn Reson Med 2011; 65: 1532–1556.
- 21 American Psychiatric Association. DSM-IV-TR Diagnostic and Statistical Manual of Mental Disorders, 4th edn. Arlington, TX: American Psychiatric Press Inc., 1994.
- 22Thompson JM, Gallagher P, Hughes JH et al. Neurocognitive impairment in euthymic patients with bipolar affective disorder. Br J Psychiatry 2005; 186: 32–40.
- 23Hamilton M. A rating scale for depression. J Neurol Psychiatry 1960; 23: 56–62.
- 24Young RC, Ziegler VE, Meyer DA. A rating scale for mania: reliability, validity and sensitivity. Br J Psychiatry 1978; 133: 429–435.
- 25Jones DK, Williams SC, Gasston D, Horsfield MA, Simmons A, Howard R. Isotropic resolution diffusion tensor imaging with whole brain acquisition in a clinically acceptable time. Hum Brain Mapp 2002; 15: 216–230.
- 26Sled JG, Zijdenbos AP, Evans AC. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 1998; 17: 87–97.
- 27Smith SM. Fast robust automated brain extraction. Hum Brain Mapp 2002; 17: 143–155.
- 28 Wellcome Department of Imaging Neuroscience. SPM Software – Statistical Parametric Mapping, 2005. Available from: http://www.fil.ion.ucl.ac.uk/spm/software/spm5/ [accessed October 2009].
- 29Wright IC, McGuire PK, Poline JB et al. A voxel-based method for the statistical analysis of gray and white matter density applied to schizophrenia. Neuroimage 1995; 2: 244–252.
- 30Worsley KJ, Taylor JE, Tomaiuolo F, Lerch J. Unified univariate and multivariate random field theory. Neuroimage 2004; 23 (Suppl. 1): S189–S195.
- 31Leemans A, Jeurissen B, Sijbers J, Jones D. ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data. 17th Annual Meeting of Intl Soc Mag Reson Med. Hawaii, USA, 2009.
- 32Jones DK, Leemans A. Diffusion tensor imaging. Methods Mol Biol 2011; 711: 127–144.
- 33Jones D. The signal intensty must be modulated by the determinant of the Jacobian when correcting for eddy currents in diffusion MRI. International Society for Magnetic Resonance in Medicine – 18th Scientific Meeting. Stockholm, Sweden, 2010.
- 34Leemans A, Jones DK. The B-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med 2009; 61: 1336–1349.
- 35Van Hecke W, Leemans A, Sage CA et al. The effect of template selection on diffusion tensor voxel-based analysis results. Neuroimage 2011; 55: 566–573.
- 36Van Hecke W, Sijbers J, D'Agostino E et al. On the construction of an inter-subject diffusion tensor magnetic resonance atlas of the healthy human brain. Neuroimage 2008; 43: 69–80.
- 37Van Hecke W, Leemans A, D'Agostino E et al. Nonrigid coregistration of diffusion tensor images using a viscous fluid model and mutual information. IEEE Trans Med Imaging 2007; 26: 1598–1612.
- 38Van Hecke W, Leemans A, De Backer S, Jeurissen B, Parizel PM, Sijbers J. Comparing isotropic and anisotropic smoothing for voxel-based DTI analyses: a simulation study. Hum Brain Mapp 2010; 31: 98–114.
- 39Konarski JZ, McIntyre RS, Kennedy SH, Rafi-Tari S, Soczynska JK, Ketter TA. Volumetric neuroimaging investigations in mood disorders: bipolar disorder versus major depressive disorder. Bipolar Disord 2008; 10: 1–37.
- 40Yucel 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.
- 41Sassi RB, Nicoletti M, Brambilla P et al. Increased gray matter volume in lithium-treated bipolar disorder patients. Neurosci Lett 2002; 329: 243–245.
- 42Bora E, Fornito A, Yucel M, Pantelis C. Voxelwise meta-analysis of gray matter abnormalities in bipolar disorder. Biol Psychiatry 2010; 67: 1097–1105.
- 43McDonald C, Bullmore E, Sham P et al. Regional volume deviations of brain structure in schizophrenia and psychotic bipolar disorder: computational morphometry study. Br J Psychiatry 2005; 186: 369–377.
- 44Bruno SD, Barker GJ, Cercignani M, Symms M, Ron MA. A study of bipolar disorder using magnetization transfer imaging and voxel-based morphometry. Brain 2004; 127: 2433–2440.
- 45Scherk H, Kemmer C, Usher J, Reith W, Falkai P, Gruber O. No change to grey and white matter volumes in bipolar I disorder patients. Eur Arch Psychiatry Clin Neurosci 2008; 258: 345–349.
- 46McIntosh AM, Job DE, Moorhead TW et al. Voxel-based morphometry of patients with schizophrenia or bipolar disorder and their unaffected relatives. Biol Psychiatry 2004; 56: 544–552.
- 47Kempton MJ, Salvador Z, Munafo MR et al. Structural neuroimaging studies in major depressive disorder: meta-analysis and comparison with bipolar disorder. Arch Gen Psychiatry 2011; 68: 675–690.
- 48Benedetti F, Yeh PH, Bellani M et al. Disruption of white matter integrity in bipolar depression as a possible structural marker of illness. Biol Psychiatry 2011; 69: 309–317.
- 49Wang F, Kalmar JH, Edmiston E et al. Abnormal corpus callosum integrity in bipolar disorder: a diffusion tensor imaging study. Biol Psychiatry 2008; 64: 730–733.
- 50Bellani M, Yeh PH, Tansella M, Balestrieri M, Soares JC, Brambilla P. DTI studies of corpus callosum in bipolar disorder. Biochem Soc Trans 2009; 37: 1096–1098.
- 51Walterfang M, Malhi GS, Wood AG et al. Corpus callosum size and shape in established bipolar affective disorder. Aust N Z J Psychiatry 2009; 43: 838–845.
- 52Mahon K, Burdick KE, Szeszko PR. A role for white matter abnormalities in the pathophysiology of bipolar disorder. Neurosci Biobehav Rev 2010; 34: 533–554.
- 53Tkachev D, Mimmack ML, Ryan MM et al. Oligodendrocyte dysfunction in schizophrenia and bipolar disorder. Lancet 2003; 362: 798–805.
- 54Konradi C, Sillivan SE, Clay HB. Mitochondria, oligodendrocytes and inflammation in bipolar disorder: evidence from transcriptome studies points to intriguing parallels with multiple sclerosis. Neurobiol Dis 2012; 45: 37–47.
- 55McIntosh AM, Hall J, Lymer GK, Sussmann JE, Lawrie SM. Genetic risk for white matter abnormalities in bipolar disorder. Int Rev Psychiatry 2009; 21: 387–393.
- 56McDonald C, Zanelli J, Rabe-Hesketh S et al. Meta-analysis of magnetic resonance imaging brain morphometry studies in bipolar disorder. Biol Psychiatry 2004; 56: 411–417.
- 57Coyle TR, Kochunov P, Patel RD et al. Cortical sulci and bipolar disorder. NeuroReport 2006; 17: 1739–1742.
- 58Kim YK, Jung HG, Myint AM, Kim H, Park SH. Imbalance between pro-inflammatory and anti-inflammatory cytokines in bipolar disorder. J Affect Disord 2007; 104: 91–95.
- 59Goldstein BI, Kemp DE, Soczynska JK, McIntyre RS. Inflammation and the phenomenology, pathophysiology, comorbidity, and treatment of bipolar disorder: a systematic review of the literature. J Clin Psychiatry 2009; 70: 1078–1090.
- 60Alexander AL, Hasan KM, Lazar M, Tsuruda JS, Parker DL. Analysis of partial volume effects in diffusion-tensor MRI. Magn Reson Med 2001; 45: 770–780.
- 61Vos SB, Jones DK, Viergever MA, Leemans A. Partial volume effect as a hidden covariate in DTI analyses. Neuroimage 2011; 55: 1566–1576.
- 62Alexander DC. Multiple-fiber reconstruction algorithms for diffusion MRI. Ann N Y Acad Sci 2005; 1064: 113–133.
- 63Wheeler-Kingshott CA, Cercignani M. About “axial” and “radial” diffusivities. Magn Reson Med 2009; 61: 1255–1260.
- 64Brietzke E, Kapczinski F. TNF-alpha as a molecular target in bipolar disorder. Prog Neuropsychopharmacol Biol Psychiatry 2008; 32: 1355–1361.
- 65Henley SM, Ridgway GR, Scahill RI et al. Pitfalls in the use of voxel-based morphometry as a biomarker: examples from huntington disease. AJNR Am J Neuroradiol 2010; 31: 711–719.
- 66Bookstein FL. “Voxel-based morphometry” should not be used with imperfectly registered images. Neuroimage 2001; 14: 1454–1462.
- 67Jones DK, Symms MR, Cercignani M, Howard RJ. The effect of filter size on VBM analyses of DT-MRI data. Neuroimage 2005; 26: 546–554.
- 68Regier DA, Farmer ME, Rae DS et al. Comorbidity of mental disorders with alcohol and other drug abuse. Results from the Epidemiologic Catchment Area (ECA) Study. JAMA 1990; 264: 2511–2518.
- 69Pfefferbaum A, Rosenbloom M, Rohlfing T, Sullivan EV. Degradation of association and projection white matter systems in alcoholism detected with quantitative fiber tracking. Biol Psychiatry 2009; 65: 680–690.
- 70Emsell L, Leemans A, Langan C et al. Limbic and callosal white matter changes in euthymic bipolar I disorder: an advanced diffusion magnetic resonance imaging tractography study. Biol Psychiatry 2013; 73: 194–201.
- 71Smith SM, Jenkinson M, Woolrich MW et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004; 23 (Suppl. 1): S208–S219.
