T1 Recovery Is Predominantly Found in Black Holes and Is Associated with Clinical Improvement in Patients with Multiple Sclerosis

References

1. 1.↵
   2. MacKay A,
   3. Laule C,
   4. Vavasour I, et al

   . Insights into brain microstructure from the T2 distribution. Magn Reson Imaging 2006;24:515–25 doi:10.1016/j.mri.2005.12.037 pmid:16677958

   CrossRefPubMedWeb of Science
2. 2.↵
   2. Laule C,
   3. Leung E,
   4. Lis DK, et al

   . Myelin water imaging in multiple sclerosis: quantitative correlations with histopathology. Mult Scler 2006;12:747–53 doi:10.1177/1352458506070928 pmid:17263002

   Abstract/FREE Full Text
3. 3.↵
   2. De Groot CJ,
   3. Bergers E,
   4. Kamphorst W, et al

   . Post-mortem MRI-guided sampling of multiple sclerosis brain lesions: increased yield of active demyelinating and (p)reactive lesions. Brain 2001;124:1635–45 doi:10.1093/brain/124.8.1635 pmid:11459754

   Abstract/FREE Full Text
4. 4.↵
   2. van Walderveen MA,
   3. Kamphorst W,
   4. Scheltens P

   . Histopathologic correlate of hypointense lesions on T1-weighted spin-echo MRI in multiple sclerosis. Neurology 1998;50:1282–88 doi:10.1212/WNL.50.5.1282 pmid:9595975

   Abstract/FREE Full Text
5. 5.↵
   2. Bitsch A,
   3. Kuhlmann T,
   4. Stadelmann C, et al

   . A longitudinal MRI study of histopathologically defined hypointense multiple sclerosis lesions. Ann Neurol 2001;49:793–96 doi:10.1002/ana.1053 pmid:11409432

   CrossRefPubMedWeb of Science
6. 6.↵
   2. Faizy TD,
   3. Thaler C,
   4. Kumar D, et al

   . Heterogeneity of multiple sclerosis lesions in multislice myelin water imaging. PLoS One 2016;11:e0151496 doi:10.1371/journal.pone.0151496 pmid:26990645

   CrossRefPubMed
7. 7.↵
   2. Barkhof F,
   3. Bruck W,
   4. De Groot CJ, et al

   . Remyelinated lesions in multiple sclerosis: magnetic resonance image appearance. Arch Neurol 2003;60:1073–81 doi:10.1001/archneur.60.8.1073 pmid:12925362

   CrossRefPubMedWeb of Science
8. 8.↵
   2. Riva M,
   3. Ikonomidou VN,
   4. Ostuni JJ, et al

   . Tissue-specific imaging is a robust methodology to differentiate in vivo T1 black holes with advanced multiple sclerosis-induced damage. AJNR Am J Neuroradiol 2009;30:1394–401 doi:10.3174/ajnr.A1573 pmid:19406765

   Abstract/FREE Full Text
9. 9.↵
   2. Naruse S,
   3. Horikawa Y,
   4. Tanaka C, et al

   . Proton nuclear magnetic resonance studies on brain edema. J Neurosurg 1982;56:747–52 doi:10.3171/jns.1982.56.6.0747 pmid:6281400

   CrossRefPubMedWeb of Science
10. 10.↵
    2. Schmierer K,
    3. Scaravilli F,
    4. Altmann DR, et al

    . Magnetization transfer ratio and myelin in postmortem multiple sclerosis brain. Ann Neurol 2004;56:407–15 doi:10.1002/ana.20202 pmid:15349868

    CrossRefPubMedWeb of Science
11. 11.↵
    2. Schmierer K,
    3. Tozer DJ,
    4. Scaravilli F, et al

    . Quantitative magnetization transfer imaging in postmortem multiple sclerosis brain. J Magn Reson Imaging 2007;26:41–51 doi:10.1002/jmri.20984 pmid:17659567

    CrossRefPubMedWeb of Science
12. 12.↵
    2. Thaler C,
    3. Faizy T,
    4. Sedlacik J, et al

    . T1-thresholds in black holes increase clinical-radiological correlation in multiple sclerosis patients. PLoS One 2015 10:e0144693 doi:10.1371/journal.pone.0144693 pmid:26659852

    CrossRefPubMed
13. 13.↵
    2. Parry A,
    3. Clare S,
    4. Jenkinson M, et al

    . MRI brain T1 relaxation time changes in MS patients increase over time in both the white matter and the cortex. J Neuroimaging 2003;13:234–39 doi:10.1111/j.1552-6569.2003.tb00184.x pmid:12889170

    CrossRefPubMed
14. 14.↵
    2. Manfredonia F,
    3. Ciccarelli O,
    4. Khaleeli Z, et al

    . Normal-appearing brain T1 relaxation time predicts disability in early primary progressive multiple sclerosis. Arch Neurol 2007;64:411–15 doi:10.1001/archneur.64.3.411 pmid:17353385

    CrossRefPubMed
15. 15.↵
    2. Marques JP,
    3. Kober T,
    4. Krueger G, et al

    . MP2RAGE, a self bias-field corrected sequence for improved segmentation and T1-mapping at high field. Neuroimage 2010;49:1271–81 doi:10.1016/j.neuroimage.2009.10.002 pmid:19819338

    CrossRefPubMedWeb of Science
16. 16.↵
    2. Schmidt P,
    3. Gaser C,
    4. Arsic M, et al

    . An automated tool for detection of FLAIR-hyperintense white-matter lesions in multiple sclerosis. Neuroimage 2012;59:3774–83 doi:10.1016/j.neuroimage.2011.11.032 pmid:22119648

    CrossRefPubMed
17. 17.↵
    2. Kappos L,
    3. Lechner-Scott J,
    4. Lienert C

    . Neurostatus. Neurostatus training and documentation DVD for a standardized neurological examination and assessment of Kurtzke's functional systems and expanded disability status scale for MS patients. 2002, 2007, Basel, Switzerland. http://neurostatus.net. Accessed January 6, 2015; 2015.
18. 18.↵
    1. Helmuth J

    2. Smith A

    . The symbol-digit modalities test: a neuropsychologic test of learning and other cerebral disorders. In Helmuth J, ed. Learning Disorders. Seattle: Special Child Publications; 1968;83–91
19. 19.↵
    2. Jonckheere AR

    . A distribution-free K-sample test against ordered alternatives. Biometrika 1954;41:133–45 doi:10.2307/2333011

    FREE Full Text
20. 20.↵
    2. Miller DH,
    3. Altmann DR,
    4. Chard DT

    . Advances in imaging to support the development of novel therapies for multiple sclerosis. Clin Pharmacol Ther 2012;91:621–34 doi:10.1038/clpt.2011.349 pmid:22398971

    CrossRefPubMed
21. 21.↵
    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

    Abstract/FREE Full Text
22. 22.↵
    2. McFarland HF,
    3. Barkhof F,
    4. Antel J, et al

    . The role of MRI as a surrogate outcome measure in multiple sclerosis. Mult Scler 2002;8:40–51 doi:10.1191/1352458502ms767xx pmid:11936488

    Abstract/FREE Full Text
23. 23.↵
    2. Steenwijk MD,
    3. Vrenken H,
    4. Jonkman LE, et al

    . High-resolution T1-relaxation time mapping displays subtle, clinically relevant, gray matter damage in long-standing multiple sclerosis. Mult Scler 2016;22:1279–88 doi:10.1177/1352458515615953 pmid:26564997

    Abstract/FREE Full Text
24. 24.↵
    2. Simioni S,
    3. Amarù F,
    4. Bonnier G, et al

    . MP2RAGE provides new clinically-compatible correlates of mild cognitive deficits in relapsing-remitting multiple sclerosis. J Neurol 2014;261:1606–13 doi:10.1007/s00415-014-7398-4 pmid:24912471

    CrossRefPubMed
25. 25.↵
    2. Blystad I,
    3. Håkansson I,
    4. Tisell A, et al

    . Quantitative MRI for analysis of active multiple sclerosis lesions without gadolinium-based contrast agent. AJNR Am J Neuroradiol 2016;37:94–100 doi:10.3174/ajnr.A4501 pmid:26471751

    Abstract/FREE Full Text
26. 26.↵
    2. Filippi M,
    3. Rocca MA,
    4. Barkhof F, et al

    ; Attendees of the Correlation between Pathological MRI Findings in MS workshop. Association between pathological and MRI findings in multiple sclerosis. Lancet Neurol 2012;11:349–60 doi:10.1016/S1474-4422(12)70003-0 pmid:22441196

    CrossRefPubMedWeb of Science
27. 27.↵
    2. Bagnato F,
    3. Jeffries N,
    4. Richert ND, et al

    . Evolution of T1 black holes in patients with multiple sclerosis images monthly for 4 years. Brain 2003;126:1782–89 doi:10.1093/brain/awg182 pmid:12821527

    Abstract/FREE Full Text
28. 28.↵
    2. van Waesberghe JH,
    3. van Walderveen MA,
    4. Castelijns JA, et al

    . Patterns of lesion development in multiple sclerosis: longitudinal observations with T1-weighted spin-echo and magnetization transfer MR. AJNR Am J Neuroradiol 1998;19:675–83 pmid:9576653

    Abstract
29. 29.↵
    2. Rovira A,
    3. Alonso J,
    4. Cucurella G, et al

    . Evolution of multiple sclerosis lesions on serial contrast-enhanced T1-weighted and magnetization-transfer MR images. AJNR Am J Neuroradiol 1999;20:1939–45 pmid:10588122

    Abstract/FREE Full Text
30. 30.↵
    2. Raine CS,
    3. Wu E

    . Mutlitple sclerosis: remyelination in acute lesions. J Neuropathol Exp Neurol 1993;52:199–204 doi:10.1097/00005072-199305000-00003 pmid:7684075

    CrossRefPubMed
31. 31.↵
    2. Lassmann W,
    3. Brück W,
    4. Luchinetti C, et al

    . Remyelination in multiple sclerosis. Mult Scler 1997;3:133–36 doi:10.1177/135245859700300213 pmid:9291167

    Abstract/FREE Full Text
32. 32.↵
    2. Patrikios P,
    3. Stadelmann C,
    4. Kutzelnigg A, et al

    . Remyelination is extensive in a subset of multiple sclerosis patients. Brain 2006;129:3165–72 doi:10.1093/brain/awl217 pmid:16921173

    Abstract/FREE Full Text
33. 33.↵
    2. Fox RJ,
    3. Cronin T,
    4. Lin J, et al

    . Measuring myelin repair and axonal loss with diffusion tensor imaging. AJNR Am J Neuroradiol 2011;32:85–91 doi:10.3174/ajnr.A2238 pmid:20947644

    Abstract/FREE Full Text
34. 34.↵
    2. Jonkman LE,
    3. Soriano AL,
    4. Amor S, et al

    . Can MS lesion stages be distinguished with MRI? A postmortem MRI and histopathology study. J Neurol 2015;262:1074–80 doi:10.1007/s00415-015-7689-4 pmid:25761376

    CrossRefPubMed
35. 35.↵
    2. Gold R,
    3. Kappos L,
    4. Arnold DL, et al

    ; DEFINE Study Investigators. Placebo-controlled phase 3 study of oral BG-12 for relapsing multiple sclerosis. N Engl J Med 2012;367:1098–107 doi:10.1056/NEJMoa1114287 pmid:22992073

    CrossRefPubMedWeb of Science
36. 36.↵
    2. Bar-Or A,
    3. Gold R,
    4. Kappos L, et al

    . Clinical efficacy of BG-12 (dimethyl fumarate) in patients with relapsing-remitting multiple sclerosis: subgroup analyses of the DEFINE study. J Neurol 2013;260:2297–305 doi:10.1007/s00415-013-6954-7 pmid:23797999

    CrossRefPubMed
37. 37.↵
    2. Duncan ID,
    3. Brower A,
    4. Kondo Y, et al

    . Extensive remyelination of the CNS leads to functional recovery. Proc Natl Acad Sci U S A 2009;106:6832–36 doi:10.1073/pnas.0812500106 pmid:19342494

    Abstract/FREE Full Text
38. 38.↵
    2. Liebetanz D,
    3. Merkler D

    . Effects of commissural de- and remyelination on motor skill behaviour in the cuprizone mouse model of multiple sclerosis. Exp Neurol 2006;202:217–24 doi:10.1016/j.expneurol.2006.05.032 pmid:16857191

    CrossRefPubMedWeb of Science
39. 39.↵
    2. Murray PD,
    3. McGavern DB,
    4. Sathornsumetee S, et al

    . Spontaneous remyelination following extensive demyelination is associated with improved neurological function in a viral model of multiple sclerosis. Brain 2001;124(pt 7):1403–16 doi:10.1093/brain/124.7.1403 pmid:11408335

    Abstract/FREE Full Text
40. 40.↵
    2. Roosendaal SD,
    3. Moraal B,
    4. Pouwels PJ, et al

    . Accumulation of cortical lesions in MS: relation with cognitive impairment. Mult Scler 2009;15:708–14 doi:10.1177/1352458509102907 pmid:19435749

    Abstract/FREE Full Text
41. 41.↵
    2. Rovaris M,
    3. Filippi M,
    4. Minicucci L, et al

    . Cortical/subcortical disease burden and cognitive impairment in patients with multiple sclerosis. AJNR Am J Neuroradiol 2000;21:402–08 pmid:10696031

    Abstract/FREE Full Text