Microstructural white matter alterations in psychotic disorder: A family-based diffusion tensor imaging study

Schizophrenia Research

Volumn 146, Issue 1-3, 2013, Pages 291-300

  Domen, Patrick A E ^a   Michielse, Stijn ^a   Gronenschild, Ed ^a   Habets, Petra ^a   Roebroeck, Alard ^c   Schruers, Koen ^a   Van Os, Jim ^a,b   Marcelis, Machteld ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Diffusion tensor imaging; Fractional anisotropy; Healthy siblings; Intermediate phenotype; Schizophrenia; White matter

Indexed keywords

CANNABIS; NEUROLEPTIC AGENT;

ARTICLE; BRAIN REGION; CORONA RADIATA (BRAIN); CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; EXTERNAL CAPSULE; FORCEPS MAJOR; FORCEPS MINOR; FRACTIONAL ANISOTROPY; GENETIC RISK; HUMAN; MAJOR CLINICAL STUDY; MOOD DISORDER; NEUROIMAGING; POSTERIOR THALAMIC RADIATION; PRIORITY JOURNAL; PSYCHOSIS; SEX DIFFERENCE; SIBLING; SUBSTANCE ABUSE; WHITE MATTER;

ADOLESCENT; ADULT; ANISOTROPY; BRAIN MAPPING; CORPUS CALLOSUM; DIAGNOSTIC AND STATISTICAL MANUAL OF MENTAL DISORDERS; DIFFUSION TENSOR IMAGING; FAMILY HEALTH; FEMALE; HUMANS; LEUKOENCEPHALOPATHIES; LONGITUDINAL STUDIES; MALE; MIDDLE AGED; PSYCHIATRIC STATUS RATING SCALES; PSYCHOTIC DISORDERS; SEX CHARACTERISTICS; YOUNG ADULT;

EID: 84875930047     PISSN: 09209964     EISSN: 15732509     Source Type: Journal    
DOI: 10.1016/j.schres.2013.03.002     Document Type: Article

References (83)

1. Andersen S.L., Tomada A., Vincow E.S., Valente E., Polcari A., Teicher M.H. Preliminary evidence for sensitive periods in the effect of childhood sexual abuse on regional brain development. J. Neuropsychiatry Clin. Neurosci. 2008, 20(3):292-301.
2. Andreasen N.C., Flaum M., Arndt S. The Comprehensive Assessment of Symptoms and History (CASH). An instrument for assessing diagnosis and psychopathology. Arch. Gen. Psychiatry 1992, 49(8):615-623.
3. Andreasen N.C., Paradiso S., O'Leary D.S. "Cognitive dysmetria" as an integrative theory of schizophrenia; a dysfunction in cortical-subcortical-cerebellar circuitry. Schizophr. Bull. 1998, 24(2):203-218.
4. Andreasen N.C., Pressler M., Nopoulos P., Miller D., Ho B.C. Antipsychotic dose equivalents and dose-years: a standardized method for comparing exposure to different drugs. Biol. Psychiatry 2010, 67(3):255-262.
5. Annett M. A classification of hand preference by association analysis. Br. J. Psychol. 1970, 61(3):303-321.
6. APA Diagnostic and Statistical Manual of Mental Disorders 2000, American Psychiatric Association, Washington, DC. 4th ed.
7. Ardekani B.A., Nierenberg J., Hoptman M.J., Javitt D.C., Lim K.O. MRI study of white matter diffusion anisotropy in schizophrenia. Neuroreport 2003, 14(16):2025-2029.
8. Bell R.P., Foxe J.J., Nierenberg J., Hoptman M.J., Garavan H. Assessing white matter integrity as a function of abstinence duration in former cocaine-dependent individuals. Drug Alcohol Depend. 2011, 114(2-3):159-168.
9. Boos H.B., Mandl R.C., van Haren N.E., Cahn W., van Baal G.C., Kahn R.S., Hulshoff Pol H.E. Tract-based diffusion tensor imaging in patients with schizophrenia and their non-psychotic siblings. Eur. Neuropsychopharmacol. 2012, 10.1016/j.euroneuro.2012.05.015.
10. Bora E., Yucel M., Fornito A., Pantelis C., Harrison B.J., Cocchi L., Pell G., Lubman D.I. White matter microstructure in opiate addiction. Addict. Biol. 2012, 17(1):141-148.
11. Burns J., Job D., Bastin M.E., Whalley H., Macgillivray T., Johnstone E.C., Lawrie S.M. Structural disconnectivity in schizophrenia: a diffusion tensor magnetic resonance imaging study. Br. J. Psychiatry 2003, 182:439-443.
12. Cahn W., Hulshoff Pol H.E., Caspers E., van Haren N.E., Schnack H.G., Kahn R.S. Cannabis and brain morphology in recent-onset schizophrenia. Schizophr. Res. 2004, 67(2-3):305-307.
13. Camchong J., Lim K.O., Sponheim S.R., Macdonald A.W. Frontal white matter integrity as an endophenotype for schizophrenia: diffusion tensor imaging in monozygotic twins and patients' nonpsychotic relatives. Front. Hum. Neurosci. 2009, 3:35.
14. Chaim T.M., Schaufelberger M.S., Ferreira L.K., Duran F.L., Ayres A.M., Scazufca M., Menezes P.R., Amaro E., Leite C.C., Murray R.M., McGuire P.K., Rushe T.M., Busatto G.F. Volume reduction of the corpus callosum and its relationship with deficits in interhemispheric transfer of information in recent-onset psychosis. Psychiatry Res. 2010, 184(1):1-9.
15. Cheung V., Cheung C., McAlonan G.M., Deng Y., Wong J.G., Yip L., Tai K.S., Khong P.L., Sham P., Chua S.E. A diffusion tensor imaging study of structural dysconnectivity in never-medicated, first-episode schizophrenia. Psychol. Med. 2008, 38(6):877-885.
16. Clark K.A., Nuechterlein K.H., Asarnow R.F., Hamilton L.S., Phillips O.R., Hageman N.S., Woods R.P., Alger J.R., Toga A.W., Narr K.L. Mean diffusivity and fractional anisotropy as indicators of disease and genetic liability to schizophrenia. J. Psychiatr. Res. 2011, 45(7):980-988.
17. DeLisi L.E. The effect of cannabis on the brain: can it cause brain anomalies that lead to increased risk for schizophrenia?. Curr. Opin. Psychiatry 2008, 21(2):140-150.
18. Ellison-Wright I., Bullmore E. Meta-analysis of diffusion tensor imaging studies in schizophrenia. Schizophr. Res. 2009, 108(1-3):3-10.
19. Friston K.J. The disconnection hypothesis. Schizophr. Res. 1998, 30:115-125.
20. Friston K.J., Frith C.D. Schizophrenia: a disconnection syndrome?. Clin. Neurosci. 1995, 3(2):89-97.
21. Gasparotti R., Valsecchi P., Carletti F., Galluzzo A., Liserre R., Cesana B., Sacchetti E. Reduced fractional anisotropy of corpus callosum in first-contact, antipsychotic drug-naive patients with schizophrenia. Schizophr. Res. 2009, 108(1-3):41-48.
22. Goghari V.M., Rehm K., Carter C.S., MacDonald A.W. Regionally specific cortical thinning and gray matter abnormalities in the healthy relatives of schizophrenia patients. Cereb. Cortex 2007, 17(2):415-424.
23. Habets P., Marcelis M., Gronenschild E., Drukker M., van Os J. Reduced cortical thickness as an outcome of differential sensitivity to environmental risks in schizophrenia. Biol. Psychiatry 2010, 69(5):487-494.
24. Hao Y., Yan Q., Liu H., Xu L., Xue Z., Song X., Kaneko Y., Jiang T., Liu Z., Shan B. Schizophrenia patients and their healthy siblings share disruption of white matter integrity in the left prefrontal cortex and the hippocampus but not the anterior cingulate cortex. Schizophr. Res. 2009, 114(1-3):128-135.
25. Ho B.C., Andreasen N.C., Ziebell S., Pierson R., Magnotta V. Long-term antipsychotic treatment and brain volumes: a longitudinal study of first-episode schizophrenia. Arch. Gen. Psychiatry 2011, 68(2):128-137.
26. Hua K., Zhang J., Wakana S., Jiang H., Li X., Reich D.S., Calabresi P.A., Pekar J.J., van Zijl P.C., Mori S. Tract probability maps in stereotaxic spaces: analyses of white matter anatomy and tract-specific quantification. NeuroImage 2008, 39(1):336-347.
27. Hubl D., Koenig T., Strik W., Federspiel A., Kreis R., Boesch C., Maier S.E., Schroth G., Lovblad K., Dierks T. Pathways that make voices: white matter changes in auditory hallucinations. Arch. Gen. Psychiatry 2004, 61(7):658-668.
28. Hulshoff Pol H.E., Schnack H.G., Mandl R.C., Brans R.G., van Haren N.E., Baare W.F., van Oel C.J., Collins D.L., Evans A.C., Kahn R.S. Gray and white matter density changes in monozygotic and same-sex dizygotic twins discordant for schizophrenia using voxel-based morphometry. NeuroImage 2006, 31(2):482-488.
29. Jones D.K., Cercignani M. Twenty-five pitfalls in the analysis of diffusion MRI data. NMR Biomed. 2010, 23(7):803-820.
30. Kanaan R.A., Kim J.S., Kaufmann W.E., Pearlson G.D., Barker G.J., McGuire P.K. Diffusion tensor imaging in schizophrenia. Biol. Psychiatry 2005, 58(12):921-929.
31. Kanaan R.A., Allin M., Picchioni M., Barker G.J., Daly E., Shergill S.S., Woolley J., McGuire P.K. Gender differences in white matter microstructure. PLoS One 2012, 7(6):e38272.
32. Kay S.R., Fiszbein A., Opler L.A. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull. 1987, 13(2):261-276.
33. Knochel C., Oertel-Knochel V., Schonmeyer R., Rotarska-Jagiela A., van de Ven V., Prvulovic D., Haenschel C., Uhlhaas P., Pantel J., Hampel H., Linden D.E. Interhemispheric hypoconnectivity in schizophrenia: fiber integrity and volume differences of the corpus callosum in patients and unaffected relatives. NeuroImage 2012, 59(2):926-934.
34. Konrad A., Winterer G. Disturbed structural connectivity in schizophrenia primary factor in pathology or epiphenomenon?. Schizophr. Bull. 2008, 34(1):72-92.
35. Konrad A., Vucurevic G., Musso F., Stoeter P., Dahmen N., Winterer G. ErbB4 genotype predicts left frontotemporal structural connectivity in human brain. Neuropsychopharmacology 2009, 34(3):641-650.
36. Kubicki M., McCarley R., Westin C.F., Park H.J., Maier S., Kikinis R., Jolesz F.A., Shenton M.E. A review of diffusion tensor imaging studies in schizophrenia. J. Psychiatr. Res. 2007, 41(1-2):15-30.
37. Kubicki M., Styner M., Bouix S., Gerig G., Markant D., Smith K., Kikinis R., McCarley R.W., Shenton M.E. Reduced interhemispheric connectivity in schizophrenia-tractography based segmentation of the corpus callosum. Schizophr. Res. 2008, 106(2-3):125-131.
38. Kyriakopoulos M., Bargiotas T., Barker G.J., Frangou S. Diffusion tensor imaging in schizophrenia. Eur. Psychiatry 2008, 23(4):255-273.
39. Lane S.D., Steinberg J.L., Ma L., Hasan K.M., Kramer L.A., Zuniga E.A., Narayana P.A., Moeller F.G. Diffusion tensor imaging and decision making in cocaine dependence. PLoS One 2010, 5(7):e11591.
40. Lederbogen F., Kirsch P., Haddad L., Streit F., Tost H., Schuch P., Wust S., Pruessner J.C., Rietschel M., Deuschle M., Meyer-Lindenberg A. City living and urban upbringing affect neural social stress processing in humans. Nature 2011, 474(7352):498-501.
41. Liao Y., Huang X., Wu Q., Yang C., Kuang W., Du M., Lui S., Yue Q., Chan R.C., Kemp G.J., Gong Q. Is depression a disconnection syndrome? Meta-analysis of diffusion tensor imaging studies in patients with MDD. J. Psychiatry Neurosci. 2012, 37(4):110180.
42. Makris N., Seidman L.J., Ahern T., Kennedy D.N., Caviness V.S., Tsuang M.T., Goldstein J.M. White matter volume abnormalities and associations with symptomatology in schizophrenia. Psychiatry Res. 2010, 183(1):21-29.
43. Marenco S., Radulescu E. Imaging genetics of structural brain connectivity and neural integrity markers. NeuroImage 2010, 53(3):848-856.
44. Maxwell M. Family Interview for Genetic Studies (FIGS): Manual for FIGS 1992, Clinical Neurogenetics Branch, Intramural Research Program, National Institute of Mental Health, Bethesda, MD.
45. McDonald C., Bullmore E.T., Sham P.C., Chitnis X., Wickham H., Bramon E., Murray R.M. Association of genetic risks for schizophrenia and bipolar disorder with specific and generic brain structural endophenotypes. Arch. Gen. Psychiatry 2004, 61(10):974-984.
46. McIntosh A.M., Moorhead T.W., Job D., Lymer G.K., Munoz Maniega S., McKirdy J., Sussmann J.E., Baig B.J., Bastin M.E., Porteous D., Evans K.L., Johnstone E.C., Lawrie S.M., Hall J. The effects of a neuregulin 1 variant on white matter density and integrity. Mol. Psychiatry 2008, 13(11):1054-1059.
47. Menzler K., Belke M., Wehrmann E., Krakow K., Lengler U., Jansen A., Hamer H.M., Oertel W.H., Rosenow F., Knake S. Men and women are different: diffusion tensor imaging reveals sexual dimorphism in the microstructure of the thalamus, corpus callosum and cingulum. NeuroImage 2011, 54(4):2557-2562.
48. Mitelman S.A., Torosjan Y., Newmark R.E., Schneiderman J.S., Chu K.W., Brickman A.M., Haznedar M.M., Hazlett E.A., Tang C.Y., Shihabuddin L., Buchsbaum M.S. Internal capsule, corpus callosum and long associative fibers in good and poor outcome schizophrenia: a diffusion tensor imaging survey. Schizophr. Res. 2007, 92(1-3):211-224.
49. Miyata J., Yamada M., Namiki C., Hirao K., Saze T., Fujiwara H., Shimizu M., Kawada R., Fukuyama H., Sawamoto N., Hayashi T., Murai T. Reduced white matter integrity as a neural correlate of social cognition deficits in schizophrenia. Schizophr. Res. 2010, 119(1-3):232-239.
50. Mori S., Oishi K., Jiang H., Jiang L., Li X., Akhter K., Hua K., Faria A.V., Mahmood A., Woods R., Toga A.W., Pike G.B., Neto P.R., Evans A., Zhang J., Huang H., Miller M.I., van Zijl P., Mazziotta J. Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. NeuroImage 2008, 40(2):570-582.
51. Munoz Maniega S., Lymer G.K., Bastin M.E., Marjoram D., Job D.E., Moorhead T.W., Owens D.G., Johnstone E.C., McIntosh A.M., Lawrie S.M. A diffusion tensor MRI study of white matter integrity in subjects at high genetic risk of schizophrenia. Schizophr. Res. 2008, 106(2-3):132-139.
52. Narr K.L., Hageman N., Woods R.P., Hamilton L.S., Clark K., Phillips O., Shattuck D.W., Asarnow R.F., Toga A.W., Nuechterlein K.H. Mean diffusivity: a biomarker for CSF-related disease and genetic liability effects in schizophrenia. Psychiatry Res 2009, 171(1):20-32.
53. Navari S., Dazzan P. Do antipsychotic drugs affect brain structure? A systematic and critical review of MRI findings. Psychol. Med. 2009, 39(11):1763-1777.
54. Olabi B., Ellison-Wright I., McIntosh A.M., Wood S.J., Bullmore E., Lawrie S.M. Are there progressive brain changes in schizophrenia? A meta-analysis of structural magnetic resonance imaging studies. Biol. Psychiatry 2011, 70(1):88-96.
55. Patel S., Mahon K., Wellington R., Zhang J., Chaplin W., Szeszko P.R. A meta-analysis of diffusion tensor imaging studies of the corpus callosum in schizophrenia. Schizophr. Res. 2011, 129(2-3):149-155.
56. Peters B.D., de Haan L., Dekker N., Blaas J., Becker H.E., Dingemans P.M., Akkerman E.M., Majoie C.B., van Amelsvoort T., den Heeten G.J., Linszen D.H. White matter fibertracking in first-episode schizophrenia, schizoaffective patients and subjects at ultra-high risk of psychosis. Neuropsychobiology 2008, 58(1):19-28.
57. Peters B.D., Blaas J., de Haan L. Diffusion tensor imaging in the early phase of schizophrenia: what have we learned?. J. Psychiatr. Res. 2010, 44(15):993-1004.
58. Price G., Bagary M.S., Cercignani M., Altmann D.R., Ron M.A. The corpus callosum in first episode schizophrenia: a diffusion tensor imaging study. J. Neurol. Neurosurg. Psychiatry 2005, 76(4):585-587.
59. Price G., Cercignani M., Parker G.J., Altmann D.R., Barnes T.R., Barker G.J., Joyce E.M., Ron M.A. Abnormal brain connectivity in first-episode psychosis: a diffusion MRI tractography study of the corpus callosum. NeuroImage 2007, 35(2):458-466.
60. Rametti G., Junque C., Falcon C., Bargallo N., Catalan R., Penades R., Garzon B., Bernardo M. A voxel-based diffusion tensor imaging study of temporal white matter in patients with schizophrenia. Psychiatry Res. 2009, 171(3):166-176.
61. Rotarska-Jagiela A., Schonmeyer R., Oertel V., Haenschel C., Vogeley K., Linden D.E. The corpus callosum in schizophrenia-volume and connectivity changes affect specific regions. NeuroImage 2008, 39(4):1522-1532.
62. Seok J.H., Park H.J., Chun J.W., Lee S.K., Cho H.S., Kwon J.S., Kim J.J. White matter abnormalities associated with auditory hallucinations in schizophrenia: a combined study of voxel-based analyses of diffusion tensor imaging and structural magnetic resonance imaging. Psychiatry Res. 2007, 156(2):93-104.
63. Skelly L.R., Calhoun V., Meda S.A., Kim J., Mathalon D.H., Pearlson G.D. Diffusion tensor imaging in schizophrenia: relationship to symptoms. Schizophr. Res. 2008, 98(1-3):157-162.
64. Smieskova R., Fusar-Poli P., Allen P., Bendfeldt K., Stieglitz R.D., Drewe J., Radue E.W., McGuire P.K., Riecher-Rossler A., Borgwardt S.J. The effects of antipsychotics on the brain: what have we learnt from structural imaging of schizophrenia?-a systematic review. Curr. Pharm. Des. 2009, 15(22):2535-2549.
65. Smith S.M. Fast robust automated brain extraction. Hum. Brain Mapp. 2002, 17(3):143-155.
66. Smith S.M., Nichols T.E. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage 2009, 44(1):83-98.
67. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E., Johansen-Berg H., Bannister P.R., De Luca M., Drobnjak I., Flitney D.E., Niazy R.K., Saunders J., Vickers J., Zhang Y., De Stefano N., Brady J.M., Matthews P.M. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 2004, 23(Suppl. 1):S208-S219.
68. Smith S.M., Jenkinson M., Johansen-Berg H., Rueckert D., Nichols T.E., Mackay C.E., Watkins K.E., Ciccarelli O., Cader M.Z., Matthews P.M., Behrens T.E. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage 2006, 31(4):1487-1505.
69. Solowij N., Yucel M., Respondek C., Whittle S., Lindsay E., Pantelis C., Lubman D.I. Cerebellar white-matter changes in cannabis users with and without schizophrenia. Psychol. Med. 2011, 41(11):2349-2359.
70. StataCorp Stata Statistical Software: Release 12 2009, StataCorp LP, College Station, TX.
71. Steel R.M., Bastin M.E., McConnell S., Marshall I., Cunningham-Owens D.G., Lawrie S.M., Johnstone E.C., Best J.J. Diffusion tensor imaging (DTI) and proton magnetic resonance spectroscopy (1H MRS) in schizophrenic subjects and normal controls. Psychiatry Res. 2001, 106(3):161-170.
72. Sullivan E.V., Adalsteinsson E., Hedehus M., Ju C., Moseley M., Lim K.O., Pfefferbaum A. Equivalent disruption of regional white matter microstructure in ageing healthy men and women. Neuroreport 2001, 12(1):99-104.
73. Szeszko P.R., Robinson D.G., Ashtari M., Vogel J., Betensky J., Sevy S., Ardekani B.A., Lencz T., Malhotra A.K., McCormack J., Miller R., Lim K.O., Gunduz-Bruce H., Kane J.M., Bilder R.M. Clinical and neuropsychological correlates of white matter abnormalities in recent onset schizophrenia. Neuropsychopharmacology 2008, 33(5):976-984.
74. van der Gaag M., Hoffman T., Remijsen M., Hijman R., de Haan L., van Meijel B., van Harten P.N., Valmaggia L., de Hert M., Cuijpers A., Wiersma D. The five-factor model of the positive and negative syndrome scale II: a ten-fold cross-validation of a revised model. Schizophr. Res. 2006, 85(1-3):280-287.
75. van Os J., Linscott R.J. Introduction: the extended psychosis phenotype-relationship with schizophrenia and with ultrahigh risk status for psychosis. Schizophr. Bull. 2012, 38(2):227-230.
76. van Os J., Kenis G., Rutten B.P. The environment and schizophrenia. Nature 2010, 468(7321):203-212.
77. Walterfang M., Wood S.J., Velakoulis D., Pantelis C. Neuropathological, neurogenetic and neuroimaging evidence for white matter pathology in schizophrenia. Neurosci. Biobehav. Rev. 2006, 30(7):918-948.
78. Wang F., Jiang T., Sun Z., Teng S.L., Luo X., Zhu Z., Zang Y., Zhang H., Yue W., Qu M., Lu T., Hong N., Huang H., Blumberg H.P., Zhang D. Neuregulin 1 genetic variation and anterior cingulum integrity in patients with schizophrenia and healthy controls. J. Psychiatry Neurosci. 2009, 34(3):181-186.
79. WHO Composite International Diagnostic Interview (CIDI) 1990, World Health Organization, Geneva.
80. Woodruff P.W., Phillips M.L., Rushe T., Wright I.C., Murray R.M., David A.S. Corpus callosum size and inter-hemispheric function in schizophrenia. Schizophr. Res. 1997, 23(3):189-196.
81. Zalesky A., Fornito A., Seal M.L., Cocchi L., Westin C.F., Bullmore E.T., Egan G.F., Pantelis C. Disrupted axonal fiber connectivity in schizophrenia. Biol. Psychiatry 2011, 69(1):80-89.
82. Zou L.Q., Xie J.X., Yuan H.S., Pei X.L., Dong W.T., Liu P.C. Diffusion tensor imaging study of the anterior limb of internal capsules in neuroleptic-naive schizophrenia. Acad. Radiol. 2008, 15(3):285-289.
83. Zuliani R., Moorhead T.W., Bastin M.E., Johnstone E.C., Lawrie S.M., Brambilla P., O'Donovan M.C., Owen M.J., Hall J., McIntosh A.M. Genetic variants in the ErbB4 gene are associated with white matter integrity. Psychiatry Res. 2011, 191(2):133-137.