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Published in: Neuroradiology 8/2016

01-08-2016 | Functional Neuroradiology

Evaluation of white matter integrity in systemic lupus erythematosus by diffusion tensor magnetic resonance imaging: a study using tract-based spatial statistics

Authors: Diogo Goulart Corrêa, Nicolle Zimmermann, Denis Batista Pereira, Thomas M. Doring, Tania Maria Netto, Nina Ventura, Rochele Paz Fonseca, Emerson Leandro Gasparetto

Published in: Neuroradiology | Issue 8/2016

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Abstract

Introduction

The aim of this study was to evaluate the white matter integrity in brains of patients with systemic lupus erythematosus (SLE) using a voxel-based analyses of diffusion tensor imaging (DTI) data.

Methods

Fifty-seven patients with SLE were compared to 36 control patients who were matched by gender, age, education, and Mini Mental State Examination score. DTI was performed along 30 noncollinear directions in a 1.5 Tesla scanner. For tract-based spatial statistics (TBSS), a white matter skeleton was created, and a permutation-based inference with 5000 permutations and a threshold of p < 0.05 was used to identify abnormalities in fractional anisotropy (FA). The mean (MD), radial (RD), and axial diffusivities (AD) were also projected onto the mean FA skeleton.

Results

We found a significant decrease of global FA in SLE patients compared to controls. The areas of reduced FA included the right superior corona radiata, the right superior longitudinal fasciculus, the body of the corpus callosum, the right inferior fronto-occipital fasciculus, the right thalamic radiation, and the right uncinate fasciculus. Patients with SLE also had increased AD and RD in several areas. Substantial overlap of areas with increased AD and RD occurred and were spatially much more extensive than the areas of reduced FA.

Conclusion

Significant increases of AD values were concordant to those of RD and MD and more extensive than FA changes. Analyzing all diffusivity parameters, using TBSS, can detect more white matter microstructural changes in patients with SLE than analyzing FA alone.
Literature
1.
go back to reference Unterman A, Nolte JE, Boaz M et al (2010) Neuropsychiatric syndromes in systemic lupus erythematosus: a meta-analysis. Semin Arthritis Rheum 30:985–992 Unterman A, Nolte JE, Boaz M et al (2010) Neuropsychiatric syndromes in systemic lupus erythematosus: a meta-analysis. Semin Arthritis Rheum 30:985–992
3.
go back to reference ACR Ad hoc Committee on Neuropsychiatric Lupus Nomenclature (1999) The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 42:599–608CrossRef ACR Ad hoc Committee on Neuropsychiatric Lupus Nomenclature (1999) The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 42:599–608CrossRef
5.
go back to reference Luyendijk J, Steens SCA, Ouwendijk WJN et al (2011) Neuropsychiatric systemic lupus erythematosus lessons learned from magnetic resonance imaging. Arthritis Rheum 63:722–732CrossRefPubMed Luyendijk J, Steens SCA, Ouwendijk WJN et al (2011) Neuropsychiatric systemic lupus erythematosus lessons learned from magnetic resonance imaging. Arthritis Rheum 63:722–732CrossRefPubMed
6.
go back to reference Jennings JE, Sundgren PC, Attwood J, McCune J, Maly P (2004) Value of MRI of the brain in patients with systemic lupus erythematosus and neurologic disturbance. Neuroradiology 46:15–21CrossRefPubMed Jennings JE, Sundgren PC, Attwood J, McCune J, Maly P (2004) Value of MRI of the brain in patients with systemic lupus erythematosus and neurologic disturbance. Neuroradiology 46:15–21CrossRefPubMed
7.
go back to reference Appezenler S, Vasconcelos Faria A, Li LM et al (2008) Quantitative magnetic resonance imaging analyses and clinical significance of hyperintense white matter lesions in systemic lupus erythematosus patients. Ann Neurol 64:635–643CrossRef Appezenler S, Vasconcelos Faria A, Li LM et al (2008) Quantitative magnetic resonance imaging analyses and clinical significance of hyperintense white matter lesions in systemic lupus erythematosus patients. Ann Neurol 64:635–643CrossRef
8.
go back to reference Lee KL, Mok CC (2004) Role of neuroimaging in the management of neuropsychiatric lupus. Hong Kong Bull Rheum Dis 4:26–30 Lee KL, Mok CC (2004) Role of neuroimaging in the management of neuropsychiatric lupus. Hong Kong Bull Rheum Dis 4:26–30
9.
go back to reference Sibbitt WL Jr, Brooks WM, Kornfeld M et al (2009) Magnetic resonance imaging and brain histopathology in neuropsychiatric systemic lupus erythematosus. Semin Arthritis Rheum 40:32–52CrossRefPubMedPubMedCentral Sibbitt WL Jr, Brooks WM, Kornfeld M et al (2009) Magnetic resonance imaging and brain histopathology in neuropsychiatric systemic lupus erythematosus. Semin Arthritis Rheum 40:32–52CrossRefPubMedPubMedCentral
10.
go back to reference Brooks WM, Sibbitt WL Jr, Kornfeld M et al (2010) The histopathologic associates of neurometabolite abnormalities in fatal neuropsychiatric systemic lupus erythematosus. Arthritis Rheum 62:2055–2063PubMedPubMedCentral Brooks WM, Sibbitt WL Jr, Kornfeld M et al (2010) The histopathologic associates of neurometabolite abnormalities in fatal neuropsychiatric systemic lupus erythematosus. Arthritis Rheum 62:2055–2063PubMedPubMedCentral
11.
go back to reference Appenzeller S, Li LM, Costallat LT et al (2005) Evidence of reversible axonal dysfunction in systemic lupus erythematosus: a proton MRS study. Brain 128:2933–2940CrossRefPubMed Appenzeller S, Li LM, Costallat LT et al (2005) Evidence of reversible axonal dysfunction in systemic lupus erythematosus: a proton MRS study. Brain 128:2933–2940CrossRefPubMed
12.
go back to reference Kozora E, Arciniegas DB, Filley CM et al (2005) Cognition, MRS neurometabolites, and MRI volumetrics in non-neuropsychiatric systemic lupus erythematosus: preliminary data. Cogn Behav Neurol 18:159–162CrossRefPubMed Kozora E, Arciniegas DB, Filley CM et al (2005) Cognition, MRS neurometabolites, and MRI volumetrics in non-neuropsychiatric systemic lupus erythematosus: preliminary data. Cogn Behav Neurol 18:159–162CrossRefPubMed
13.
go back to reference Emmer BJ, Steens SC, Steup-Beekman GM et al (2006) Detection of change in CNS involvement in neuropsychiatric SLE: a magnetization transfer study. J Magn Reson Imaging 24:812–816CrossRefPubMed Emmer BJ, Steens SC, Steup-Beekman GM et al (2006) Detection of change in CNS involvement in neuropsychiatric SLE: a magnetization transfer study. J Magn Reson Imaging 24:812–816CrossRefPubMed
14.
go back to reference Zhang L, Harrison M, Heier LA et al (2007) Diffusion changes in patients with systemic lupus erythematosus. Magn Reson Imaging 25:399–405CrossRefPubMed Zhang L, Harrison M, Heier LA et al (2007) Diffusion changes in patients with systemic lupus erythematosus. Magn Reson Imaging 25:399–405CrossRefPubMed
15.
go back to reference Welsh RC, Rahbar H, Foerster B et al (2007) Brain diffusivity in patients with neuropsychiatric systemic lupus erythematosus with new acute neurological symptoms. J Magn Reson Imaging 26:541–551CrossRefPubMed Welsh RC, Rahbar H, Foerster B et al (2007) Brain diffusivity in patients with neuropsychiatric systemic lupus erythematosus with new acute neurological symptoms. J Magn Reson Imaging 26:541–551CrossRefPubMed
16.
go back to reference Hughes M, Sundgren PC, Fan X et al (2007) Diffusion tensor imaging in patients with acute onset of neuropsychiatric systemic lupus erythematosus: a prospective study of apparent diffusion coefficient, fractional anisotropy values, and eigenvalues in different regions of the brain. Acta Radiol 48:213–222CrossRefPubMed Hughes M, Sundgren PC, Fan X et al (2007) Diffusion tensor imaging in patients with acute onset of neuropsychiatric systemic lupus erythematosus: a prospective study of apparent diffusion coefficient, fractional anisotropy values, and eigenvalues in different regions of the brain. Acta Radiol 48:213–222CrossRefPubMed
17.
go back to reference Emmer BJ, Veer IM, Steup-Beekman GM et al (2010) Tract-based spatial statistics on diffusion tensor imaging in systemic lupus erythematosus reveals localized involvement of white matter tracts. Arthritis Rheum 62:3716–3721CrossRefPubMed Emmer BJ, Veer IM, Steup-Beekman GM et al (2010) Tract-based spatial statistics on diffusion tensor imaging in systemic lupus erythematosus reveals localized involvement of white matter tracts. Arthritis Rheum 62:3716–3721CrossRefPubMed
19.
go back to reference Jung RE, Chavez RS, Flores RA et al (2012) White matter correlates of neuropsychological dysfunction in systemic lupus erythematosus. PLoS ONE 7:e28373CrossRefPubMedPubMedCentral Jung RE, Chavez RS, Flores RA et al (2012) White matter correlates of neuropsychological dysfunction in systemic lupus erythematosus. PLoS ONE 7:e28373CrossRefPubMedPubMedCentral
20.
go back to reference Schmidt-Wilcke T, Cagnoli P, Wang P et al (2014) Diminished white matter integrity in patients with systemic lupus erythematosus. Neuroimage Clin 5:291–297CrossRefPubMedPubMedCentral Schmidt-Wilcke T, Cagnoli P, Wang P et al (2014) Diminished white matter integrity in patients with systemic lupus erythematosus. Neuroimage Clin 5:291–297CrossRefPubMedPubMedCentral
21.
go back to reference Ercan E, Ingo C, Tritanon O et al (2015) A multimodal MRI approach to identify and characterize microstructural brain changes in neuropsychiatric systemic lupus erythematosus. Neuroimage Clin 8:337–344CrossRefPubMedPubMedCentral Ercan E, Ingo C, Tritanon O et al (2015) A multimodal MRI approach to identify and characterize microstructural brain changes in neuropsychiatric systemic lupus erythematosus. Neuroimage Clin 8:337–344CrossRefPubMedPubMedCentral
22.
go back to reference Sundgren PC, Dong Q, Gómez-Hassan D, Mukherji SK, Maly P, Welsh R (2004) Diffusion tensor imaging of the brain: review of clinical applications. Neuroradiology 46(5):339–350CrossRefPubMed Sundgren PC, Dong Q, Gómez-Hassan D, Mukherji SK, Maly P, Welsh R (2004) Diffusion tensor imaging of the brain: review of clinical applications. Neuroradiology 46(5):339–350CrossRefPubMed
23.
go back to reference Smith SM, Jenkinson M, Johansen-Berg H et al (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage 31:1487–1505CrossRefPubMed Smith SM, Jenkinson M, Johansen-Berg H et al (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage 31:1487–1505CrossRefPubMed
24.
go back to reference Qiu D, Tan LH, Zhou K et al (2008) Diffusion tensor imaging of normal white matter maturation from late childhood to young adulthood: voxel-wise evaluation of mean diffusivity, fractional anisotropy, radial and axial diffusivities, and correlation with reading development. NeuroImage 41:223–232CrossRefPubMed Qiu D, Tan LH, Zhou K et al (2008) Diffusion tensor imaging of normal white matter maturation from late childhood to young adulthood: voxel-wise evaluation of mean diffusivity, fractional anisotropy, radial and axial diffusivities, and correlation with reading development. NeuroImage 41:223–232CrossRefPubMed
25.
go back to reference Nived O, Sturfelt G, Liang MH et al (2003) ACR nomenclature for CNS lupus revisited. Lupus 12:872–876CrossRefPubMed Nived O, Sturfelt G, Liang MH et al (2003) ACR nomenclature for CNS lupus revisited. Lupus 12:872–876CrossRefPubMed
26.
go back to reference Smith SM, Jenkinson M, Woolrich MW et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:208–219CrossRef Smith SM, Jenkinson M, Woolrich MW et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:208–219CrossRef
27.
go back to reference Zivadinov R, Shucard JL, Hussein S et al (2013) Multimodal imaging in systemic lupus erythematosus patients with diffuse neuropsychiatric involvement. Lupus 22:675–683CrossRefPubMed Zivadinov R, Shucard JL, Hussein S et al (2013) Multimodal imaging in systemic lupus erythematosus patients with diffuse neuropsychiatric involvement. Lupus 22:675–683CrossRefPubMed
28.
go back to reference Cesar B, Dwyer MG, Shucard JL et al (2015) Cognitive and white matter tract differences in MS and diffuse neuropsychiatric systemic lupus erythematosus. AJNR Am J Neuroradiol 36:1874–1883CrossRefPubMed Cesar B, Dwyer MG, Shucard JL et al (2015) Cognitive and white matter tract differences in MS and diffuse neuropsychiatric systemic lupus erythematosus. AJNR Am J Neuroradiol 36:1874–1883CrossRefPubMed
29.
go back to reference Song SK, Sun SW, Ramsbottom MJ et al (2002) Demyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17:1429–1436CrossRefPubMed Song SK, Sun SW, Ramsbottom MJ et al (2002) Demyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17:1429–1436CrossRefPubMed
30.
go back to reference Sun SW, Liang HF, Trinkaus K et al (2006) Noninvasive detection of cuprizone induced axonal damage and demyelination in the mouse corpus callosum. Magn Reson Med 55:302–308CrossRefPubMed Sun SW, Liang HF, Trinkaus K et al (2006) Noninvasive detection of cuprizone induced axonal damage and demyelination in the mouse corpus callosum. Magn Reson Med 55:302–308CrossRefPubMed
31.
go back to reference Acosta-Cabronero J, Williams GB, Pengas G et al (2010) Absolute diffusivities define the landscape of white matter degeneration in Alzheimer’s disease. Brain 133:529–539CrossRefPubMed Acosta-Cabronero J, Williams GB, Pengas G et al (2010) Absolute diffusivities define the landscape of white matter degeneration in Alzheimer’s disease. Brain 133:529–539CrossRefPubMed
32.
go back to reference Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system—a technical review. NMR Biomed 15:435–555CrossRefPubMed Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system—a technical review. NMR Biomed 15:435–555CrossRefPubMed
33.
go back to reference Agosta F, Pievani M, Sala S et al (2011) White matter damage in Alzheimer disease and its relationship to gray matter atrophy. Radiology 258:853–863CrossRefPubMed Agosta F, Pievani M, Sala S et al (2011) White matter damage in Alzheimer disease and its relationship to gray matter atrophy. Radiology 258:853–863CrossRefPubMed
34.
go back to reference Efthimiou P, Blanco B (2009) Pathogenesis of neuropsychiatric systemic lupus erythematosus and potential biomarkers. Mod Rheumatol 19:457–468CrossRefPubMed Efthimiou P, Blanco B (2009) Pathogenesis of neuropsychiatric systemic lupus erythematosus and potential biomarkers. Mod Rheumatol 19:457–468CrossRefPubMed
Metadata
Title
Evaluation of white matter integrity in systemic lupus erythematosus by diffusion tensor magnetic resonance imaging: a study using tract-based spatial statistics
Authors
Diogo Goulart Corrêa
Nicolle Zimmermann
Denis Batista Pereira
Thomas M. Doring
Tania Maria Netto
Nina Ventura
Rochele Paz Fonseca
Emerson Leandro Gasparetto
Publication date
01-08-2016
Publisher
Springer Berlin Heidelberg
Published in
Neuroradiology / Issue 8/2016
Print ISSN: 0028-3940
Electronic ISSN: 1432-1920
DOI
https://doi.org/10.1007/s00234-016-1688-8

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