A multimodal MRI approach to identify and characterize microstructural brain changes in neuropsychiatric systemic lupus erythematosus

NeuroImage: Clinical

Volumn 8, Issue , 2015, Pages 337-344

  Ercan, Ece ^a   Ingo, Carson ^a   Tritanon, Oranan ^b   Magro Checa, Cesar ^a   Smith, Alex ^c,d   Smith, Seth ^c,e   Huizinga, Tom ^a   Van Buchem, Mark A ^a   Ronen, Itamar ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MAHIDOL UNIVERSITY   (Thailand)

^c VANDERBILT UNIVERSITY   (United States)

^d VANDERBILT UNIVERSITY   (United States)

^e VANDERBILT UNIVERSITY   (United States)

Author keywords

Diffusion tensor imaging; erythematosus; Magnetic resonance imaging; Magnetization transfer imaging; Neuropsychiatric systemic lupus; Normal appearing white matter; Systemic lupus erythematosus

Indexed keywords

ADULT; ARTICLE; BRAIN MAPPING; BRAIN REGION; CLINICAL ARTICLE; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; FEMALE; FRACTIONAL ANISOTROPY; GOLD STANDARD; HUMAN; MULTIMODAL IMAGING; NEUROPSYCHIATRY; NEURORADIOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SYSTEMIC LUPUS ERYTHEMATOSUS; WHITE MATTER; BRAIN VASCULITIS; MIDDLE AGED; PATHOLOGY; PROCEDURES;

ADULT; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; LUPUS VASCULITIS, CENTRAL NERVOUS SYSTEM; MAGNETIC RESONANCE IMAGING; MIDDLE AGED; MULTIMODAL IMAGING; WHITE MATTER;

EID: 84930661173     PISSN: None     EISSN: 22131582     Source Type: Journal    
DOI: 10.1016/j.nicl.2015.05.002     Document Type: Article

References (48)

1. Aja-Fernandez S., Alberola-Lopez C., and Westin C.F. Noise and signal estimation in magnitude MRI and Rician distributed images: a LMMSE approach I.E.E.E. Trans. Image Process. 17 8 2008 1383 1398 10.1109/TIP.2008.925382 18632347
2. American College Of Rheumatology The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes Arthritis Rheum. 42 4 1999 599 608 10.1002/1529-0131(199904)42:4<599::AID-ANR2>3.0.CO;2-F 10211873
3. Appenzeller S., Bonilha L., Rio P.A., Min Li L., Costallat L.T., and Cendes F. Longitudinal analysis of gray and white matter loss in patients with systemic lupus erythematosus Neuroimage 34 2 2007 694 701 10.1016/j.neuroimage.2006.09.029 17112740
4. Appenzeller S., Pike G.B., and Clarke A.E. Magnetic resonance imaging in the evaluation of central nervous system manifestations in systemic lupus erythematosus Clin. Rev. Allergy Immunol. 34 3 2008 361 366 10.1007/s12016-007-8060-z 18084729
5. Appenzeller S., Vasconcelos Faria A., Li L.M., Costallat L.T., and Cendes F. Quantitative magnetic resonance imaging analyses and clinical significance of hyperintense white matter lesions in systemic lupus erythematosus patients Ann. Neurol. 64 6 2008 635 643 10.1002/ana.21483 19107986
6. Bazin P.L., Cuzzocreo J.L., Yassa M.A., Gandler W., McAuliffe M.J., Bassett S.S., and Pham D.L. Volumetric neuroimage analysis extensions for the MIPAV software package J. Neurosci. Methods 165 1 2007 111 121 10.1016/j.jneumeth.2007.05.024 17604116
7. Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review N.M.R. Biomed. 15 7-8 2002 435 455 10.1002/nbm.782 12489094
8. Behrens T.E., Woolrich M.W., Jenkinson M., Johansen-Berg H., Nunes R.G., Clare S., Matthews P.M., Brady J.M., and Smith S.M. Characterization and propagation of uncertainty in diffusion-weighted MR imaging Magn. Reson. Med. 50 5 2003 1077 1088 10.1002/mrm.10609 14587019
9. Bertsias G.K., and Boumpas D.T. Pathogenesis, diagnosis and management of neuropsychiatric SLE manifestations Nat. Rev. Rheumatol. 6 6 2010 358 367 10.1038/nrrheum.2010.62 20458332
10. Bodini B., Cercignani M., Toosy A., De Stefano N., Miller D.H., Thompson A.J., and Ciccarelli O. A novel approach with "skeletonised MTR" measures tract-specific microstructural changes in early primary-progressive MS Hum. Brain Mapp. 35 2 2014 723 733 10.1002/hbm.22196 23616276
11. Bosma G.P., Huizinga T.W., Mooijaart S.P., and Van Buchem M.A. Abnormal brain diffusivity in patients with neuropsychiatric systemic lupus erythematosus A.J.N.R. Am. J. Neuroradiol. 24 5 2003 850 854 12748084
12. Bosma G.P., Rood M.J., Huizinga T.W., de Jong B.A., Bollen E.L., and van Buchem M.A. Detection of cerebral involvement in patients with active neuropsychiatric systemic lupus erythematosus by the use of volumetric magnetization transfer imaging Arthritis Rheum. 43 11 2000 2428 2436 10.1002/1529-0131(200011)43:11<2428::AID-ANR9>3.0.CO;2-H 11083265
13. Bosma G.P., Rood M.J., Zwinderman A.H., Huizinga T.W., and van Buchem M.A. Evidence of central nervous system damage in patients with neuropsychiatric systemic lupus erythematosus, demonstrated by magnetization transfer imaging Arthritis Rheum. 43 1 2000 48 54 10.1002/1529-0131(200001)43:1<48::AID-ANR7>3.0.CO;2-H 10643699
14. Bosma G.P., Steens S.C., Petropoulos H., Admiraal-Behloul F., van den Haak A., Doornbos J., Huizinga T.W., Brooks W.M., Harville A., Sibbitt W.L. Jr., and van Buchem M.A. Multisequence magnetic resonance imaging study of neuropsychiatric systemic lupus erythematosus Arthritis Rheum. 50 10 2004 3195 3202 10.1002/art.20512 15476212
15. Budde M.D., Xie M., Cross A.H., and Song S.K. Axial diffusivity is the primary correlate of axonal injury in the experimental autoimmune encephalomyelitis spinal cord: a quantitative pixelwise analysis J. Neurosci. 29 9 2009 2805 2813 10.1523/JNEUROSCI.4605-08.2009 19261876
16. Castellino G., Govoni M., Giacuzzo S., and Trotta F. Optimizing clinical monitoring of central nervous system involvement in SLE Autoimmun. Rev. 7 4 2008 297 304 10.1016/j.autrev.2007.11.022 18295733
17. Chiang C.W., Wang Y., Sun P., Lin T.H., Trinkaus K., Cross A.H., and Song S.K. Quantifying white matter tract diffusion parameters in the presence of increased extra-fiber cellularity and vasogenic edema Neuroimage 101 2014 310 319 10.1016/j.neuroimage.2014.06.064 25017446
18. Emmer B.J., Steens S.C., Steup-Beekman G.M., van der Grond J., Admiraal-Behloul F., Olofsen H., Bosma G.P., Ouwendijk W.J., Huizinga T.W., and van Buchem M.A. Detection of change in CNS involvement in neuropsychiatric SLE: a magnetization transfer study J. Magn. Reson. Imaging 24 4 2006 812 816 10.1002/jmri.20706 16941632
19. Emmer B.J., Steup-Beekman G.M., Steens S.C., Huizinga T.W., van Buchem M.A., and van der Grond J. Correlation of magnetization transfer ratio histogram parameters with neuropsychiatric systemic lupus erythematosus criteria and proton magnetic resonance spectroscopy: association of magnetization transfer ratio peak height with neuronal and cognitive dysfunction Arthritis Rheum. 58 5 2008 1451 1457 10.1002/art.23452 18438847
20. Emmer B.J., Veer I.M., Steup-Beekman G.M., Huizinga T.W., van der Grond J., and van Buchem M.A. Tract-based spatial statistics on diffusion tensor imaging in systemic lupus erythematosus reveals localized involvement of white matter tracts Arthritis Rheum. 62 12 2010 3716 3721 10.1002/art.27717 20722009
21. Hochberg M.C. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus Arthritis Rheum. 40 9 1997 1725 10.1002/1529-0131(199709)40:9 9324032
22. Hughes M., Sundgren P.C., Fan X., Foerster B., Nan B., Welsh R.C., Williamson J.A., Attwood J., Maly P.V., Chenevert T.L., McCune W., and Gebarski S. 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 2 2007 213 222 10.1080/02841850601105825 17354144
23. Ingo C., Magin R.L., Colon-Perez L., Triplett W., and Mareci T.H. On random walks and entropy in diffusion-weighted magnetic resonance imaging studies of neural tissue Magn. Reson. Med. 71 2014 617 627 10.1002/mrm.24706 23508765
24. Jeltsch-David H., and Muller S. Neuropsychiatric systemic lupus erythematosus: pathogenesis and biomarkers Nat. Rev. Neurol. 10 10 2014 579 596 10.1038/nrneurol.2014.148 25201240
25. Jenkinson M., Bannister P., Brady M., and Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images Neuroimage 17 2 2002 825 841 10.1006/nimg.2002.1132 12377157
26. Jenkinson M., and Smith S. A global optimisation method for robust affine registration of brain images Med. Image Anal. 5 2 2001 143 156 10.1016/S1361-8415(01)00036-6 11516708
27. Jung R.E., Caprihan A., Chavez R.S., Flores R.A., Sharrar J., Qualls C.R., Sibbitt W., and Roldan C.A. Diffusion tensor imaging in neuropsychiatric systemic lupus erythematosus B.M.C. Neurol. 10 2010 65 10.1186/1471-2377-10-65 20667115
28. Kozora E., and Filley C.M. Cognitive dysfunction and white matter abnormalities in systemic lupus erythematosus J. Int. Neuropsychol. Soc. 17 3 2011 385 392 10.1017/S1355617711000191 21338548
29. Lauvsnes M.B., and Omdal R. Systemic lupus erythematosus, the brain, and anti-NR2 antibodies J. Neurol. 259 4 2012 622 629 10.1007/s00415-011-6232-5 21909801
30. Luyendijk J., Steens S.C., Ouwendijk W.J., Steup-Beekman G.M., Bollen E.L., van der Grond J., Huizinga T.W., Emmer B.J., and van Buchem M.A. Neuropsychiatric systemic lupus erythematosus: lessons learned from magnetic resonance imaging Arthritis Rheum. 63 3 2011 722 732 10.1002/art.30157 21360502
31. McAuliffe M.J., Lalonde F.M., McGarry D., Gandler W., Csaky K., and Trus B.L. Medical Image Processing, Analysis and Visualization in Clinical Research 2001 Medical Systems. 14th IEEE Symposium on CBMS
32. Moll N.M., Rietsch A.M., Thomas S., Ransohoff A.J., Lee J.C., Fox R., Chang A., Ransohoff R.M., and Fisher E. Multiple sclerosis normal-appearing white matter: pathology-imaging correlations Ann. Neurol. 70 5 2011 764 773 10.1002/ana.22521 22162059
33. Price S.J., Tozer D.J., and Gillard J.H. Methodology of diffusion-weighted, diffusion tensor and magnetisation transfer imaging Br. J. Radiol. 84 Spec No 2 2011 S121 S126 10.1259/bjr/12789972 22433823
34. Schmidt-Wilcke T., Cagnoli P., Wang P., Schultz T., Lotz A., McCune W.J., and Sundgren P.C. Diminished white matter integrity in patients with systemic lupus erythematosus Neuroimage Clin. 5 2014 291 297 10.1016/j.nicl.2014.07.001 25161895
35. Sibbitt W.L. Jr., Brooks W.M., Kornfeld M., Hart B.L., Bankhurst A.D., and Roldan C.A. Magnetic resonance imaging and brain histopathology in neuropsychiatric systemic lupus erythematosus Semin. Arthritis Rheum. 40 1 2010 32 52 10.1016/j.semarthrit.2009.08.005 19880162
36. 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., and Behrens T.E. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data Neuroimage 31 4 2006 1487 1505 10.1016/j.neuroimage.2006.02.024 16624579
37. Song S.K., Yoshino J., Le T.Q., Lin S.J., Sun S.W., Cross A.H., and Armstrong R.C. Demyelination increases radial diffusivity in corpus callosum of mouse brain Neuroimage 26 1 2005 132 140 10.1016/j.neuroimage.2005.01.028 15862213
38. Steup-Beekman G.M., Zirkzee E.J., Cohen D., Gahrmann B.M., Emmer B.J., Steens S.C., Bollen E.L., van Buchem M.A., and Huizinga T.W. Neuropsychiatric manifestations in patients with systemic lupus erythematosus: epidemiology and radiology pointing to an immune-mediated cause Ann. Rheum. Dis. 72 Suppl. 2 2013 ii76 ii79 10.1136/annrheumdis-2012-202369 23253914
39. Stojanovich L., Zandman-Goddard G., Pavlovich S., and Sikanich N. Psychiatric manifestations in systemic lupus erythematosus Autoimmun. Rev. 6 6 2007 421 426 10.1016/j.autrev.2007.02.007 17537389
40. Tan E.M., Cohen A.S., Fries J.F., Masi A.T., McShane D.J., Rothfield N.F., Schaller J.G., Talal N., and Winchester R.J. The 1982 revised criteria for the classification of systemic lupus erythematosus Arthritis Rheum. 25 11 1982 1271 1277 10.1002/art.1780251101 7138600
41. Welsh R.C., Rahbar H., Foerster B., Thurnher M., and Sundgren P.C. Brain diffusivity in patients with neuropsychiatric systemic lupus erythematosus with new acute neurological symptoms J. Magn. Reson. Imaging 26 3 2007 541 551 10.1002/jmri.21036 17729344
42. Wheeler-Kingshott C.A., and Cercignani M. About "axial" and "radial" diffusivities Magn. Reson. Med. 61 5 2009 1255 1260 10.1002/mrm.21965 19253405
43. Winkler A.M., Ridgway G.R., Webster M.A., Smith S.M., and Nichols T.E. Permutation inference for the general linear model Neuroimage 92 2014 381 397 10.1016/j.neuroimage.2014.01.060 24530839
44. Wood E.T., Ronen I., Techawiboonwong A., Jones C.K., Barker P.B., Calabresi P., Harrison D., and Reich D.S. Investigating axonal damage in multiple sclerosis by diffusion tensor spectroscopy J. Neurosci. 32 19 2012 6665 6669 10.1523/JNEUROSCI.0044-12.2012 22573688
45. Zhang L., Harrison M., Heier L.A., Zimmerman R.D., Ravdin L., Lockshin M., and Uluʇ A.M. Diffusion changes in patients with systemic lupus erythematosus Magn. Reson. Imaging 25 3 2007 399 405 10.1016/j.mri.2006.09.037 17371731
46. Zimny A., Szmyrka-Kaczmarek M., Szewczyk P., Bladowska J., Pokryszko-Dragan A., Gruszka E., Wiland P., and Sasiadek M. In vivo evaluation of brain damage in the course of systemic lupus erythematosus using magnetic resonance spectroscopy, perfusion-weighted and diffusion-tensor imaging Lupus 23 1 2014 10 19 10.1177/0961203313511556 24192079
47. Zirkzee E.J., Steup-Beekman G.M., van der Mast R.C., Bollen E.L., van der Wee N.J., Baptist E., Slee T.M., Huisman M.V., Middelkoop H.A., Luyendijk J., van Buchem M.A., and Huizinga T.W. Prospective study of clinical phenotypes in neuropsychiatric systemic lupus erythematosus; multidisciplinary approach to diagnosis and therapy J. Rheumatol. 39 11 2012 2118 2126 10.3899/jrheum.120545 22984275
48. Zivadinov R., Shucard J.L., Hussein S., Durfee J., Cox J.L., Bergsland N., Dwyer M.G., Benedict R.H., Ambrus J., and Shucard D.W. Multimodal imaging in systemic lupus erythematosus patients with diffuse neuropsychiatric involvement Lupus 22 7 2013 675 683 10.1177/0961203313486193 23640981