Advertisement

Neuroradiology

, Volume 58, Issue 8, pp 819–825 | Cite as

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

  • Diogo Goulart CorrêaEmail author
  • Nicolle Zimmermann
  • Denis Batista Pereira
  • Thomas M. Doring
  • Tania Maria Netto
  • Nina Ventura
  • Rochele Paz Fonseca
  • Emerson Leandro Gasparetto
Functional Neuroradiology

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.

Keywords

Systemic lupus erythematosus Magnetic resonance imaging Diffusion tensor imaging Wallerian degeneration Demyelination 

Notes

Compliance with ethical standards

We declare that all human and animals studies have been approved by the ethical review board of the Clementino Fraga Filho University Hospital and have therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. We declare that all patients gave informed consent prior to inclusion in this study.

Conflict of interest

We declare that we have no conflict of interest.

References

  1. 1.
    Unterman A, Nolte JE, Boaz M et al (2010) Neuropsychiatric syndromes in systemic lupus erythematosus: a meta-analysis. Semin Arthritis Rheum 30:985–992Google Scholar
  2. 2.
    Huizinga TWJ, Diamond B (2008) Lupus and the central nervous system. Lupus 17:376–379CrossRefPubMedGoogle Scholar
  3. 3.
    ACR Ad hoc Committee on Neuropsychiatric Lupus Nomenclature (1999) The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 42:599–608CrossRefGoogle Scholar
  4. 4.
    Muscal E, Brey RL (2010) Neurologic manifestations of systemic lupus erythematosus in children and adults. Neurol Clin 28:61–73CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Luyendijk J, Steens SCA, Ouwendijk WJN et al (2011) Neuropsychiatric systemic lupus erythematosus lessons learned from magnetic resonance imaging. Arthritis Rheum 63:722–732CrossRefPubMedGoogle Scholar
  6. 6.
    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 46:15–21CrossRefPubMedGoogle Scholar
  7. 7.
    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 64:635–643CrossRefGoogle Scholar
  8. 8.
    Lee KL, Mok CC (2004) Role of neuroimaging in the management of neuropsychiatric lupus. Hong Kong Bull Rheum Dis 4:26–30Google Scholar
  9. 9.
    Sibbitt WL Jr, Brooks WM, Kornfeld M et al (2009) Magnetic resonance imaging and brain histopathology in neuropsychiatric systemic lupus erythematosus. Semin Arthritis Rheum 40:32–52CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Brooks WM, Sibbitt WL Jr, Kornfeld M et al (2010) The histopathologic associates of neurometabolite abnormalities in fatal neuropsychiatric systemic lupus erythematosus. Arthritis Rheum 62:2055–2063PubMedPubMedCentralGoogle Scholar
  11. 11.
    Appenzeller S, Li LM, Costallat LT et al (2005) Evidence of reversible axonal dysfunction in systemic lupus erythematosus: a proton MRS study. Brain 128:2933–2940CrossRefPubMedGoogle Scholar
  12. 12.
    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 18:159–162CrossRefPubMedGoogle Scholar
  13. 13.
    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 24:812–816CrossRefPubMedGoogle Scholar
  14. 14.
    Zhang L, Harrison M, Heier LA et al (2007) Diffusion changes in patients with systemic lupus erythematosus. Magn Reson Imaging 25:399–405CrossRefPubMedGoogle Scholar
  15. 15.
    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 26:541–551CrossRefPubMedGoogle Scholar
  16. 16.
    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 48:213–222CrossRefPubMedGoogle Scholar
  17. 17.
    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 62:3716–3721CrossRefPubMedGoogle Scholar
  18. 18.
    Jung RE, Caprihan A, Chavez RS et al (2010) Diffusion tensor imaging in neuropsychiatric systemic lupus erythematosus. BMC Neurol 10:65CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Jung RE, Chavez RS, Flores RA et al (2012) White matter correlates of neuropsychological dysfunction in systemic lupus erythematosus. PLoS ONE 7:e28373CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Schmidt-Wilcke T, Cagnoli P, Wang P et al (2014) Diminished white matter integrity in patients with systemic lupus erythematosus. Neuroimage Clin 5:291–297CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    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 8:337–344CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    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):339–350CrossRefPubMedGoogle Scholar
  23. 23.
    Smith SM, Jenkinson M, Johansen-Berg H et al (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage 31:1487–1505CrossRefPubMedGoogle Scholar
  24. 24.
    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 41:223–232CrossRefPubMedGoogle Scholar
  25. 25.
    Nived O, Sturfelt G, Liang MH et al (2003) ACR nomenclature for CNS lupus revisited. Lupus 12:872–876CrossRefPubMedGoogle Scholar
  26. 26.
    Smith SM, Jenkinson M, Woolrich MW et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:208–219CrossRefGoogle Scholar
  27. 27.
    Zivadinov R, Shucard JL, Hussein S et al (2013) Multimodal imaging in systemic lupus erythematosus patients with diffuse neuropsychiatric involvement. Lupus 22:675–683CrossRefPubMedGoogle Scholar
  28. 28.
    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 36:1874–1883CrossRefPubMedGoogle Scholar
  29. 29.
    Song SK, Sun SW, Ramsbottom MJ et al (2002) Demyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17:1429–1436CrossRefPubMedGoogle Scholar
  30. 30.
    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 55:302–308CrossRefPubMedGoogle Scholar
  31. 31.
    Acosta-Cabronero J, Williams GB, Pengas G et al (2010) Absolute diffusivities define the landscape of white matter degeneration in Alzheimer’s disease. Brain 133:529–539CrossRefPubMedGoogle Scholar
  32. 32.
    Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system—a technical review. NMR Biomed 15:435–555CrossRefPubMedGoogle Scholar
  33. 33.
    Agosta F, Pievani M, Sala S et al (2011) White matter damage in Alzheimer disease and its relationship to gray matter atrophy. Radiology 258:853–863CrossRefPubMedGoogle Scholar
  34. 34.
    Efthimiou P, Blanco B (2009) Pathogenesis of neuropsychiatric systemic lupus erythematosus and potential biomarkers. Mod Rheumatol 19:457–468CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Diogo Goulart Corrêa
    • 1
    • 2
    Email author
  • Nicolle Zimmermann
    • 1
    • 3
  • Denis Batista Pereira
    • 1
  • Thomas M. Doring
    • 2
  • Tania Maria Netto
    • 1
  • Nina Ventura
    • 1
    • 2
  • Rochele Paz Fonseca
    • 1
    • 3
  • Emerson Leandro Gasparetto
    • 1
    • 2
  1. 1.Department of Radiology, Hospital Universitário Clementino Fraga FilhoFederal University of Rio de JaneiroRio de JaneiroBrazil
  2. 2.Clínica de Diagnóstico por Imagem (CDPI)Rio de JaneiroBrazil
  3. 3.Department of PsychologyPontifical Catholic University of Rio Grande do SulPorto AlegreBrazil

Personalised recommendations