Thalamic Iron Differentiates Primary-Progressive and Relapsing-Remitting Multiple Sclerosis

References

1. 1.↵
   2. Raz E,
   3. Branson B,
   4. Jensen JH, et al

   . Relationship between iron accumulation and white matter injury in multiple sclerosis: a case-control study. J Neurol 2015;262:402–09 doi:10.1007/s00415-014-7569-3 pmid:25416468

   CrossRefPubMed
2. 2.↵
   2. Cobzas D,
   3. Sun H,
   4. Walsh AJ, et al

   . Subcortical gray matter segmentation and voxel-based analysis using transverse relaxation and quantitative susceptibility mapping with application to multiple sclerosis. J Magn Reson Imaging 2015;42:1601–10 doi:10.1002/jmri.24951 pmid:25980643

   CrossRefPubMed
3. 3.↵
   2. Stankiewicz JM,
   3. Neema M,
   4. Ceccarelli A

   . Iron and multiple sclerosis. Neurobiol Aging 2014;35(suppl 2):S51–58 doi:10.1016/j.neurobiolaging.2014.03.039 pmid:24929968

   CrossRefPubMed
4. 4.↵
   2. Ropele S,
   3. Kilsdonk ID,
   4. Wattjes MP, et al

   . Determinants of iron accumulation in deep grey matter of multiple sclerosis patients. Mult Scler 2014;20:1692–98 doi:10.1177/1352458514531085 pmid:24787429

   CrossRefPubMed
5. 5.↵
   2. Ropele S,
   3. de Graaf W,
   4. Khalil M, et al

   . MRI assessment of iron deposition in multiple sclerosis. J Magn Reson Imaging 2011;34:13–21 doi:10.1002/jmri.22590 pmid:21698703

   CrossRefPubMed
6. 6.↵
   2. Khalil M,
   3. Langkammer C,
   4. Ropele S, et al

   . Determinants of brain iron in multiple sclerosis: a quantitative 3T MRI study. Neurology 2011;77:1691–97 doi:10.1212/WNL.0b013e318236ef0e pmid:21975210

   Abstract/FREE Full Text
7. 7.↵
   2. Burgetova A,
   3. Seidl Z,
   4. Krasensky J, et al

   . Multiple sclerosis and the accumulation of iron in the basal ganglia: quantitative assessment of brain iron using MRI t(2) relaxometry. Eur Neurol 2010;63:136–43 doi:10.1159/000279305 pmid:20130410

   CrossRefPubMed
8. 8.↵
   2. Ge Y,
   3. Jensen JH,
   4. Lu H, et al

   . Quantitative assessment of iron accumulation in the deep gray matter of multiple sclerosis by magnetic field correlation imaging. AJNR Am J Neuroradiol 2007;28:1639–44 doi:10.3174/ajnr.A0646 pmid:17893225

   Abstract/FREE Full Text
9. 9.↵
   2. Haider L,
   3. Simeonidou C,
   4. Steinberger G, et al

   . Multiple sclerosis deep grey matter: the relation between demyelination, neurodegeneration, inflammation and iron. J Neurol Neurosurg Psychiatry 2014;85:1386–95 doi:10.1136/jnnp-2014-307712 pmid:24899728

   Abstract/FREE Full Text
10. 10.↵
    2. Hametner S,
    3. Wimmer I,
    4. Haider L, et al

    . Iron and neurodegeneration in the multiple sclerosis brain. Ann Neurol 2013;74:848–61 doi:10.1002/ana.23974 pmid:23868451

    CrossRefPubMed
11. 11.↵
    2. Khalil M,
    3. Langkammer C,
    4. Pichler A, et al

    . Dynamics of brain iron levels in multiple sclerosis: a longitudinal 3T MRI study. Neurology 2015;84:2396–402 doi:10.1212/WNL.0000000000001679 pmid:25979698

    CrossRefPubMed
12. 12.↵
    2. Antel J,
    3. Antel S,
    4. Caramanos Z, et al

    . Primary progressive multiple sclerosis: part of the MS disease spectrum or separate disease entity? Acta Neuropathol 2012;123:627–38 doi:10.1007/s00401-012-0953-0 pmid:22327362

    CrossRefPubMedWeb of Science
13. 13.↵
    2. Dusek P,
    3. Dezortova M,
    4. Wuerfel J

    . Imaging of iron. Int Rev Neurobiol 2013;110:195–239 doi:10.1016/B978-0-12-410502-7.00010-7 pmid:24209440

    CrossRefPubMed
14. 14.↵
    2. Langkammer C,
    3. Schweser F,
    4. Krebs N, et al

    . Quantitative susceptibility mapping (QSM) as a means to measure brain iron? A post mortem validation study. Neuroimage 2012;62:1593–99 doi:10.1016/j.neuroimage.2012.05.049 pmid:22634862

    CrossRefPubMed
15. 15.↵
    2. Schmalbrock P,
    3. Prakash RS,
    4. Schirda B, et al

    . Basal ganglia iron in patients with multiple sclerosis measured with 7T quantitative susceptibility mapping correlates with inhibitory control. AJNR Am J Neuroradiol 2016;37:439–46 doi:10.3174/ajnr.A4599 pmid:26611996

    Abstract/FREE Full Text
16. 16.↵
    2. Al-Radaideh AM,
    3. Wharton SJ,
    4. Lim SY, et al

    . Increased iron accumulation occurs in the earliest stages of demyelinating disease: an ultra-high field susceptibility mapping study in clinically isolated syndrome. Mult Scler 2013;19:896–903 doi:10.1177/1352458512465135 pmid:23139386

    CrossRefPubMed
17. 17.↵
    2. Wang Y,
    3. Liu T

    . Quantitative susceptibility mapping (QSM): decoding MRI data for a tissue magnetic biomarker. Magn Reson Med 2015;73:82–101 doi:10.1002/mrm.25358 pmid:25044035

    CrossRefPubMed
18. 18.↵
    2. Schweser F,
    3. Deistung A,
    4. Lehr BW, et al

    . Differentiation between diamagnetic and paramagnetic cerebral lesions based on magnetic susceptibility mapping. Med Phys 2010;37:5165–78 doi:10.1118/1.3481505 pmid:21089750

    CrossRefPubMed
19. 19.↵
    2. Lublin FD,
    3. Reingold SC,
    4. Cohen JA, et al

    . Defining the clinical course of multiple sclerosis: the 2013 revisions. Neurology 2014;83:278–86 doi:10.1212/WNL.0000000000000560 pmid:24871874

    CrossRefPubMed
20. 20.↵
    2. Ho DE,
    3. Imai K,
    4. King G, et al

    . MatchIt: nonparametric preprocessing for parametric causal inference. J Stat Soft 2011;42:1–28
21. 21.↵
    2. Horakova D,
    3. Kalincik T,
    4. Dolezal O, et al

    . Early predictors of non-response to interferon in multiple sclerosis. Acta Neurol Scand 2012;126:390–97 doi:10.1111/j.1600-0404.2012.01662.x pmid:22428845

    CrossRefPubMedWeb of Science
22. 22.↵
    2. Kalincik T,
    3. Vaneckova M,
    4. Tyblova M, et al

    . Volumetric MRI markers and predictors of disease activity in early multiple sclerosis: a longitudinal cohort study. PLoS One 2012;7:e50101 doi:10.1371/journal.pone.0050101 pmid:23166826

    CrossRefPubMedWeb of Science
23. 23.↵
    2. Vaneckova M,
    3. Kalincik T,
    4. Krasensky J, et al

    . Corpus callosum atrophy: a simple predictor of multiple sclerosis progression—a longitudinal 9-year study. Eur Neurol 2012;68:23–27 doi:10.1159/000337683 pmid:22677920

    CrossRefPubMed
24. 24.↵
    2. Langkammer C,
    3. Bredies K,
    4. Poser BA, et al

    . Fast quantitative susceptibility mapping using 3D EPI and total generalized variation. Neuroimage 2015;111:622–30 doi:10.1016/j.neuroimage.2015.02.041 pmid:25731991

    CrossRefPubMed
25. 25.↵
    2. Yushkevich PA,
    3. Piven J,
    4. Hazlett HC, et al

    . User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 2006;31:1116–28 doi:10.1016/j.neuroimage.2006.01.015 pmid:16545965

    CrossRefPubMedWeb of Science
26. 26.↵
    2. Hallgren B,
    3. Sourander P

    . The effect of age on the non-haemin iron in the human brain. J Neurochem 1958;3:41–51 doi:10.1111/j.1471-4159.1958.tb12607.x pmid:13611557

    CrossRefPubMedWeb of Science
27. 27.↵
    2. Kuchling J,
    3. Ramien C,
    4. Bozin I, et al

    . Identical lesion morphology in primary progressive and relapsing-remitting MS: an ultrahigh field MRI study. Mult Scler 2014;20:1866–71 doi:10.1177/1352458514531084 pmid:24781284

    CrossRefPubMed
28. 28.↵
    2. Jonkman LE,
    3. Rosenthal DM,
    4. Sormani MP, et al

    . Gray matter correlates of cognitive performance differ between relapsing-remitting and primary-progressive multiple sclerosis. PLoS One 2015;10:e0129380 doi:10.1371/journal.pone.0129380 pmid:26485710

    CrossRefPubMed
29. 29.↵
    2. Galego O,
    3. Gouveia A,
    4. Batista S, et al

    . Brain atrophy and physical disability in primary progressive multiple sclerosis: a volumetric study. Neuroradiol J 2015;28:354–58 doi:10.1177/1971400915594984 pmid:26246109

    CrossRefPubMed
30. 30.↵
    2. Nijeholt GJ,
    3. van Walderveen MA,
    4. Castelijns JA, et al

    . Brain and spinal cord abnormalities in multiple sclerosis: correlation between MRI parameters, clinical subtypes and symptoms. Brain 1998;121(pt 4):687–97 doi:10.1093/brain/121.4.687 pmid:9577394

    Abstract/FREE Full Text
31. 31.↵
    2. Hagemeier J,
    3. Heininen-Brown M,
    4. Poloni GU, et al

    . Iron deposition in multiple sclerosis lesions measured by susceptibility-weighted imaging filtered phase: a case control study. J Magn Reson Imaging 2012;36:73–83 doi:10.1002/jmri.23603 pmid:22407571

    CrossRefPubMed
32. 32.↵
    2. Quinn MP,
    3. Gati JS,
    4. Klassen ML, et al

    . Increased deep gray matter iron is present in clinically isolated syndromes. Mult Scler Relat Disord 2014;3:194–202 doi:10.1016/j.msard.2013.06.017 pmid:25878007

    CrossRefPubMed
33. 33.↵
    2. Hammond KE,
    3. Metcalf M,
    4. Carvajal L, et al

    . Quantitative in vivo magnetic resonance imaging of multiple sclerosis at 7 Tesla with sensitivity to iron. Ann Neurol 2008;64:707–13 doi:10.1002/ana.21582 pmid:19107998

    CrossRefPubMedWeb of Science
34. 34.↵
    2. Khalil M,
    3. Enzinger C,
    4. Langkammer C, et al

    . Quantitative assessment of brain iron by R(2)* relaxometry in patients with clinically isolated syndrome and relapsing-remitting multiple sclerosis. Mult Scler 2009;15:1048–54 doi:10.1177/1352458509106609 pmid:19556316

    CrossRefPubMedWeb of Science
35. 35.↵
    2. Zivadinov R,
    3. Heininen-Brown M,
    4. Schirda CV, et al

    . Abnormal subcortical deep-gray matter susceptibility-weighted imaging filtered phase measurements in patients with multiple sclerosis: a case-control study. Neuroimage 2012;59:331–39 doi:10.1016/j.neuroimage.2011.07.045 pmid:21820063

    CrossRefPubMedWeb of Science
36. 36.↵
    2. Du S,
    3. Sah SK,
    4. Zeng C, et al

    . Iron deposition in the gray matter in patients with relapse-remitting multiple sclerosis: a longitudinal study using three-dimensional (3D)-enhanced T2*-weighted angiography (ESWAN). Eur J Radiol 2015;84:1325–32 doi:10.1016/j.ejrad.2015.04.013 pmid:25959392

    CrossRefPubMed
37. 37.↵
    2. Hagemeier J,
    3. Yeh EA,
    4. Brown MH, et al

    . Iron content of the pulvinar nucleus of the thalamus is increased in adolescent multiple sclerosis. Mult Scler 2013;19:567–76 doi:10.1177/1352458512459289 pmid:22968543

    CrossRefPubMed
38. 38.↵
    2. Modica CM,
    3. Zivadinov R,
    4. Dwyer MG, et al

    . Iron and volume in the deep gray matter: association with cognitive impairment in multiple sclerosis. AJNR Am J Neuroradiol 2015;36:57–62 doi:10.3174/ajnr.A3998 pmid:24948507

    Abstract/FREE Full Text
39. 39.↵
    2. Morris CM,
    3. Candy JM,
    4. Oakley AE, et al

    . Histochemical distribution of non-haem iron in the human brain. Acta Anat (Basel) 1992;144:235–57 doi:10.1159/000147312 pmid:1529678

    CrossRefPubMedWeb of Science
40. 40.↵
    2. Acosta-Cabronero J,
    3. Betts MJ,
    4. Cardenas-Blanco A, et al

    . In vivo MRI mapping of brain iron deposition across the adult lifespan. J Neurosci 2016;36:364–74 doi:10.1523/JNEUROSCI.1907-15.2016 pmid:26758829

    Abstract/FREE Full Text
41. 41.↵
    2. Fukunaga M,
    3. Li TQ,
    4. van Gelderen P, et al

    . Layer-specific variation of iron content in cerebral cortex as a source of MRI contrast. Proc Natl Acad Sci U S A 2010;107:3834–39 doi:10.1073/pnas.0911177107 pmid:20133720

    Abstract/FREE Full Text
42. 42.↵
    2. Truyen L,
    3. van Waesberghe JH,
    4. van Walderveen MA, et al

    . Accumulation of hypointense lesions (“black holes”) on T1 spin-echo MRI correlates with disease progression in multiple sclerosis. Neurology 1996;47:1469–76 doi:10.1212/WNL.47.6.1469 pmid:8960729

    Abstract/FREE Full Text
43. 43.↵
    2. Di Perri C,
    3. Battaglini M,
    4. Stromillo ML, et al

    . Voxel-based assessment of differences in damage and distribution of white matter lesions between patients with primary progressive and relapsing-remitting multiple sclerosis. Arch Neurol 2008;65:236–43 pmid:18268194

    CrossRefPubMedWeb of Science
44. 44.↵
    2. Miller DH,
    3. Leary SM

    . Primary-progressive multiple sclerosis. Lancet Neurol 2007;6:903–12 doi:10.1016/S1474-4422(07)70243-0 pmid:17884680

    CrossRefPubMedWeb of Science
45. 45.↵
    2. Stevenson VL,
    3. Miller DH,
    4. Rovaris M, et al

    . Primary and transitional progressive MS: a clinical and MRI cross-sectional study. Neurology 1999;52:839–45 doi:10.1212/WNL.52.4.839 pmid:10078736

    Abstract/FREE Full Text
46. 46.↵
    2. Thompson AJ,
    3. Montalban X,
    4. Barkhof F, et al

    . Diagnostic criteria for primary progressive multiple sclerosis: a position paper. Ann Neurol 2000;47:831–35 pmid:10852554

    CrossRefPubMedWeb of Science
47. 47.↵
    2. Zhang Y,
    3. Metz LM,
    4. Yong VW, et al

    . 3T deep gray matter T2 hypointensity correlates with disability over time in stable relapsing-remitting multiple sclerosis: a 3-year pilot study. J Neurol Sci 2010;297:76–81 doi:10.1016/j.jns.2010.07.014 pmid:20708201

    CrossRefPubMed
48. 48.↵
    2. Tjoa CW,
    3. Benedict RH,
    4. Weinstock-Guttman B, et al

    . MRI T2 hypointensity of the dentate nucleus is related to ambulatory impairment in multiple sclerosis. J Neurol Sci 2005;234:17–24 doi:10.1016/j.jns.2005.02.009 pmid:15993137

    CrossRefPubMedWeb of Science
49. 49.↵
    2. Ruggieri S,
    3. Petracca M,
    4. Miller A, et al

    . Association of deep gray matter damage with cortical and spinal cord degeneration in primary progressive multiple sclerosis. JAMA Neurol 2015;72:1466–74 doi:10.1001/jamaneurol.2015.1897 pmid:26457955

    CrossRefPubMed
50. 50.↵
    2. Bergsland N,
    3. Horakova D,
    4. Dwyer MG, et al

    . Subcortical and cortical gray matter atrophy in a large sample of patients with clinically isolated syndrome and early relapsing-remitting multiple sclerosis. AJNR Am J Neuroradiol 2012;33:1573–78 doi:10.3174/ajnr.A3086 pmid:22499842

    Abstract/FREE Full Text
51. 51.↵
    2. Bermel RA,
    3. Bakshi R

    . The measurement and clinical relevance of brain atrophy in multiple sclerosis. Lancet Neurol 2006;5:158–70 doi:10.1016/S1474-4422(06)70349-0 pmid:16426992

    CrossRefPubMedWeb of Science
52. 52.↵
    2. Bodini B,
    3. Battaglini M,
    4. De Stefano N, et al

    . T2 lesion location really matters: a 10-year follow-up study in primary progressive multiple sclerosis. J Neurol Neurosurg Psychiatry 2011;82:72–77 doi:10.1136/jnnp.2009.201574 pmid:20627965

    Abstract/FREE Full Text
53. 53.↵
    2. Ciccarelli O,
    3. Brex PA,
    4. Thompson AJ, et al

    . Disability and lesion load in MS: a reassessment with MS functional composite score and 3D fast FLAIR. J Neurol 2002;249:18–24 doi:10.1007/PL00007843 pmid:11954864

    CrossRefPubMedWeb of Science
54. 54.↵
    2. Kearney H,
    3. Rocca MA,
    4. Valsasina P, et al

    . Magnetic resonance imaging correlates of physical disability in relapse onset multiple sclerosis of long disease duration. Mult Scler 2014;20:72–80 doi:10.1177/1352458513492245 pmid:23812283

    CrossRefPubMed
55. 55.↵
    2. Zivadinov R,
    3. Stosic M,
    4. Cox JL, et al

    . The place of conventional MRI and newly emerging MRI techniques in monitoring different aspects of treatment outcome. J Neurol 2008;255(suppl 1):61–74 doi:10.1007/s00415-008-1009-1 pmid:18317678

    CrossRefPubMed