Black holes in multiple sclerosis: Definition, evolution, and clinical correlations

Acta Neurologica Scandinavica

Volumn 122, Issue 1, 2010, Pages 1-8

  Sahraian, M A ^a   Radue, E W ^b   Haller, S ^b   Kappos, L ^b  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

Black hole; Hypointense lesion; Magnetic resonance imaging; Multiple sclerosis

Indexed keywords

BETA1A INTERFERON; GLATIRAMER; INTERFERON BETA SERINE; NATALIZUMAB; PLACEBO;

BRAIN EDEMA; CELL LOSS; CHRONIC DISEASE; CLINICAL ASSESSMENT; CLINICAL TRIAL; DISEASE ACTIVITY; DISEASE COURSE; ENCEPHALITIS; GLIOSIS; HUMAN; MULTIPLE SCLEROSIS; NERVE DEGENERATION; NERVE FIBER; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PATHOPHYSIOLOGY; PHYSICAL DISABILITY; RELAPSING REMITTING MULTIPLE SCLEROSIS; REVIEW; SECONARY PROGRESSIVE MULTIPLE SCLEROSIS; THERAPY EFFECT;

ADJUVANTS, IMMUNOLOGIC; BRAIN; HUMANS; INTERFERON-BETA; INTERFERONS; MAGNETIC RESONANCE IMAGING; MULTIPLE SCLEROSIS;

EID: 77953342126     PISSN: 00016314     EISSN: 16000404     Source Type: Journal    
DOI: 10.1111/j.1600-0404.2009.01221.x     Document Type: Review

References (72)

1. Barkhof F, Filippi M, Miller DH, Scheltens P, Campi A, Polman CH. Comparison of MRI criteria at first presentation to predict conversion to clinically definite multiple sclerosis. Brain 1997 120 : 2059 2069.
2. Miller DH, Grossman RI, Reingold SC, McFarland HF. The role of magnetic resonance techniques in understanding and managing multiple sclerosis. Brain 1998 121 : 3 24.
3. Polman C, Reingold SC, Edan G, Filippi M, Hartung HP, Kappos L. Diagnostic criteria for multiple sclerosis: 2005 revisions to the "McDonald Criteria". Ann Neurol 2005 58 : 840 846. (Pubitemid 41746873)
4. Simon JH, Li D, Traboulsee A, Coyle PK, Arnold DL. Standardized MR imaging protocol for multiple sclerosis: Consortium of MS Centers consensus guidelines. Am J Neuroradiol 2006 27 : 455 461.
5. Arnold DL, Matthews PM. MRI in the diagnosis and management of multiple sclerosis. Neurology 2002 58 (Suppl. 4 S23 31.
6. Moore GR, Leung E, Mackay AL, Vavasour IM, Whittall KP, Cover KS. A pathology-MRI study of the short-T2 component in formalin-fixed multiple sclerosis brain. Neurology 2000 55 : 1506 1510.
7. Barkhof F, van Walderveen M. Characterization of tissue damage in multiple sclerosis by nuclear magnetic resonance. Philos Trans R Soc Lond B Biol Sci 1999 354 : 1675 1686. (Pubitemid 29534433)
8. He J, Grossman RI, Ge Y, Mannon LJ. Enhancing patterns in multiple sclerosis: evolution and persistence. Am J Neuroradiol 2001 22 : 664 669.
9. Lai M, Hodgson T, Gawne-Cain M et al. A preliminary study into the sensitivity of disease activity detection by serial weekly magnetic resonance imaging in multiple sclerosis. J Neurol Neurosurg Psychiatry 1996 60 : 339 341.
10. Bakshi R, Hutton GJ, Miller JR, Radue EW. The use of magnetic resonance imaging in the diagnosis and long-term management of multiple sclerosis. Neurology 2004 63 (Suppl. 5 S3 11.
11. Barkhof F, McGowan JC, van Waesberghe JH, Grossman RI. Hypointense multiple sclerosis lesions on T1-weighted spin echo magnetic resonance images: their contribution in understanding multiple sclerosis evolution. J Neurol Neurosurg Psychiatry 1998 64 (Suppl. 1 S77 9.
12. Bagnato F, Jeffries N, Richert ND et al. Evolution of T1 black holes in patients with multiple sclerosis images monthly for 4 years. Brain 2003 126 : 1782 1789.
13. van Waesberghe JH, van Walderveen MA, Castelijns JA et al. Patterns of lesion development in multiple sclerosis: longitudinal observations with T1-weighted spin-echo and magnetization transfer MR. Am J Neuroradiol 1998 19 : 675 683.
14. Brex PA, Molyneux PD, Smiddy P, Barkhof F, Filippi M, Yousry TA. The effect of IFNbeta-1b on the evolution of enhancing lesions in secondary progressive MS. Neurology 2001 57 : 2185 2190.
15. Ciccarelli O, Giugni E, Paolillo A, Maniero C, Gasperini C, Bastianello S. Magnetic resonance outcome of new enhancing lesions in patients with relapsing-remitting multiple sclerosis. Eur J Neurol 1999 6 : 455 459.
16. Filippi M, Rovaris M, Rocca MA, Sormani MP, Wolinsky JS, Comi G. European/Canadian glatiramer acetate study group. Glatiramer acetate reduces the proportion of new MS lesions evolving into "black holes". Neurology 2001 57 : 731 733.
17. Dalton CM, Miszkiel KA, Barker GJ et al. Effect of natalizumab on conversion of gadolinium enhancing lesions to T1 hypointense lesions in relapsing multiple sclerosis. J Neurol 2004 251 : 407 413.
18. Barkhof F, Bruck W, De Groot CJ et al. Remyelinated lesions in multiple sclerosis: magnetic resonance image appearance. Arch Neurol 2003 60 : 1073 1081.
19. Wolinsky JS, Narayana PA, Noseworthy JH et al. Linomide in relapsing and secondary progressive MS: part II: MRI results. MRI Analysis Center of the University of Texas-Houston, Health Science Center, and the North American Linomide Investigators. Neurology 2000 54 : 1734 1741.
20. Filippi M, Wolinsky JS, Sormani MP, Comi G. European/Canadian glatiramer acetate study group. Enhancement frequency decreases with increasing age in relapsing-remitting multiple sclerosis. Neurology 2001 56 : 422 423.
21. Bakshi R, Minagar A, Jaisani Z, Wolinsky JS. Imaging of multiple sclerosis: role in neurotherapeutics. NeuroRx 2005 2 : 277 303. (Pubitemid 40471438)
22. Minneboo A, Uitdehaag BM, Ader HJ, Barkhof F, Polman CH, Castelijns JA. Patterns of enhancing lesion evolution in multiple sclerosis are uniform within patients. Neurology 2005 65 : 56 61.
23. Loevner LA, Grossman RI, McGowan JC, Ramer KN, Cohen JA. Characterization of multiple sclerosis plaques with T1-weighted MR and quantitative magnetization transfer. Am J Neuroradiol 1995 16 : 1473 1479.
24. Filippi M, Iannucci G, Tortorella C et al. Comparison of MS clinical phenotypes using conventional and magnetization transfer MRI. Neurology 1999 52 : 588 594. (Pubitemid 29075609)
25. Nijeholt GJ, van Walderveen MA, Castelijns JA et al. Brain and spinal cord abnormalities in multiple sclerosis. Correlation between MRI parameters, clinical subtypes and symptoms. Brain 1998 121 : 687 697.
26. Stevenson VL, Miller DH, Rovaris M et al. Primary and transitional progressive MS: a clinical and MRI cross-sectional study. Neurology 1999 52 : 839 845.
27. van Walderveen MA, Lycklama a Nijeholt GJ, Andèr HJ et al. Hypointense lesions on T1-weighted spin-echo magnetic resonance imaging: relation to clinical characteristics in subgroups of patients with multiple sclerosis. Arch Neurol 2001 58 : 76 81.
28. Koziol JA, Wagner S, Sobel DF et al. Predictive value of lesions for relapses in relapsing-remitting multiple sclerosis. Am J Neuroradiol 2001 22 : 284 291.
29. Fazekas F, Strasser-Fuchs S, Schmidt H et al. Apolipoprotein E genotype related differences in brain lesions of multiple sclerosis. J Neurol Neurosurg Psychiatry 2000 69 : 25 8.
30. Enzinger C, Ropele S, Smith S et al. Accelerated evolution of brain atrophy and "black holes" in MS patients with APOE-epsilon 4. Ann Neurol 2004 55 : 563.
31. Molyneux PD, Brex PA, Fogg C et al. The precision of T1 hypointense lesion volume quantification in multiple sclerosis treatment trials: a multicenter study. Mult Scler 2000 6 : 237 240.
32. Datta S, Sajja BR, He R, Wolinsky JS, Gupta RK, Narayana PA. Segmentation and quantification of black holes in multiple sclerosis. Neuroimage 2006 29 : 467 474.
33. Hiehle JF Jr., Grossman RI, Ramer KN, Gonzalez-Scarano F, Cohen JA. Magnetization transfer effects in MR-detected multiple sclerosis lesions: comparison with gadolinium-enhanced spin-echo images and nonenhanced T1-weighted images. Am J Neuroradiol 1995 16 : 69 77.
34. Laule C, Vavasour IM, Whittall KP et al. Evolution of focal and diffuse magnetisation transfer abnormalities in multiple sclerosis. J Neurol 2003 250 : 924 931.
35. Fazekas F, Ropele S, Enzinger C, Seifert T, Strasser-Fuchs S. Quantitative magnetization transfer imaging of pre-lesional white-matter changes in multiple sclerosis. Mult Scler 2002 8 : 479 484.
36. Barnes D, Munro PM, Youl BD, Prineas JW, McDonald WI. The longstanding MS lesion. A quantitative MRI and electron microscopic study. Brain 1991 114 : 1271 1280.
37. McDonald WI. Rachelle Fishman-Matthew Moore Lecture. The pathological and clinical dynamics of multiple sclerosis. J Neuropathol Exp Neurol 1994 53 : 338 343.
38. van Walderveen MA, Barkhof F, Pouwels PJ, van Schijndel RA, Polman CH, Castelijns JA. Neuronal damage in T1-hypointense multiple sclerosis lesions demonstrated in vivo using proton magnetic resonance spectroscopy. Ann Neurol 1999 46 : 79 87.
39. Bitsch A, Bruhn H, Vougioukas V et al. Inflammatory CNS demyelination: histopathologic correlation with in vivo quantitative proton MR spectroscopy. Am J Neuroradiol 1999 20 : 1619 1627.
40. Brex PA, Parker GJ, Leary SM et al. Lesion heterogeneity in multiple sclerosis: a study of the relations between appearances on T1 weighted images, T1 relaxation times, and metabolite concentrations. J Neurol Neurosurg Psychiatry 2000 68 : 627 632.
41. Bjartmar C, Trapp BD. Axonal and neuronal degeneration in multiple sclerosis: mechanisms and functional consequences. Curr Opin Neurol 2001 14 : 271 278.
42. Li BS, Regal J, Soher BJ, Mannon LJ, Grossman RI, Gonen O. Brain metabolite profiles of T1-hypointense lesions in relapsing-remitting multiple sclerosis. Am J Neuroradiol 2003 24 : 68 74.
43. Vavasour IM, Li DK, Laule C, Traboulsee AL, Moore GR, MacKay AL. Multi-parametric MR assessment of T(1) black holes in multiple sclerosis : evidence that myelin loss is not greater in hypointense versus isointense T(1) lesions. J Neurol 2007 254 : 1653 1659.
44. Pirko I, Nolan TK, Holland SK, Johnson AJ. Multiple sclerosis: pathogenesis and MR imaging features of T1 hypointensities in murine model. Radiology 2008 246 : 790 795.
45. Meier DS, Weiner HL, Khoury SJ, Guttmann CR. Magnetic resonance imaging surrogates of multiple sclerosis pathology and their relationship to central nervous system atrophy. J Neuroimaging 2004 14 (Suppl. 3 S46 53.
46. Bitsch A, Kuhlmann T, Stadelmann C, Lassmann H, Lucchinetti C, Bruck W. A longitudinal MRI study of histopathologically defined hypointense multiple sclerosis lesions. Ann Neurol 2001 49 : 793 796.
47. Bruck W, Bitsch A, Kolenda H, Bruck Y, Stiefel M, Lassmann H. Inflammatory central nervous system demyelination: correlation of magnetic resonance imaging findings with lesion pathology. Ann Neurol 1997 42 : 783 793.
48. van Walderveen MA, Kamphorst W, Scheltens P et al. Histopathologic correlate of hypointense lesions on T1-weighted spin-echo MRI in multiple sclerosis. Neurology 1998 50 : 1282 1288.
49. Nessler S, Boretius S, Stadelmann C et al. Early MRI changes in a mouse model of multiple sclerosis are predictive of severe inflammatory tissue damage. Brain 2007 130 : 2186 2198.
50. Bitsch A, Brück W. MRI-pathological correlates in MS. Int MSJ 2002 8 : 89 95.
51. Miki Y, Grossman RI, Udupa JK et al. Relapsing-remitting multiple sclerosis: longitudinal analysis of MR images - lack of correlation between changes in T2 lesion volume and clinical findings. Radiology 1999 213 : 395 399.
52. van Walderveen MA, Barkhof F, Hommes OR, Polman CH, Tobi H, Frequin ST. Correlating MRI and clinical disease activity in multiple sclerosis: relevance of hypointense lesions on short-TR/short-TE (T1-weighted) spin-echo images. Neurology 1995 45 : 1684 1690.
53. Kappos L. Multiple sclerosis trials. Lancet 1999 353 : 2242 2243.
54. Rovaris M, Comi G, Ladkani D, Wolinsky JS, Filippi M. European/Canadian Glatiramer acetate study group. Short-term correlations between clinical and MR imaging findings in relapsing-remitting multiple sclerosis. Am J Neuroradiol 2003 24 : 75 81.
55. Goodin DS. Magnetic resonance imaging as a surrogate outcome measure of disability in multiple sclerosis: Have we been overly harsh in our assessment? Ann Neurol 2006 59 : 597 605.
56. Truyen L, van Waesberghe JH, 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 1476.
57. Paolillo A, Coles AJ, Molyneux PD et al. Quantitative MRI in patients with secondary progressive MS treated with monoclonal antibody Campath 1H. Neurology 1999 53 : 751 757.
58. Giugni E, Pozzilli C, Bastianello S et al. MRI measures and their relations with clinical disability in relapsing-remitting and secondary progressive multiple sclerosis. Mult Scler 1997 3 : 221 225.
59. O'Riordan JI, Gawne Cain M, Coles A et al. T1 hypointense lesion load in secondary progressive multiple sclerosis: a comparison of pre versus post contrast loads and of manual versus semi automated threshold techniques for lesion segmentation. Mult Scler 1998 4 : 408 412.
60. Simon JH, Lull J, Jacobs LD, Rudick RA, Cookfair DL, Herndon RM. A longitudinal study of T1 hypointense lesions in relapsing MS: MSCRG trial of interferon beta-1a. Multiple Sclerosis Collaborative Research Group. Neurology 2000 55 : 185 192.
61. Koudriavtseva T, Thompson AJ, Fiorelli M et al. Gadolinium enhanced MRI predicts clinical and MRI disease activity in relapsing-remitting multiple sclerosis. J Neurol Neurosurg Psychiatry 1997 62 : 285 287.
62. van Walderveen MA, Truyen L, van Oosten BW et al. Development of hypointense lesions on T1-weighted spin-echo magnetic resonance images in multiple sclerosis: relation to inflammatory activity. Arch Neurol 1999 56 : 345 351.
63. Masek M, Vaneckova M, Krasensky J et al. Secondary-progressive form of multiple sclerosis: MRI changes versus clinical status. Neuro Endocrinol Lett 2008 29 : 461 466.
64. Bakshi R, Neema M, Healy BC et al. Predicting clinical progression in multiple sclerosis with the magnetic resonance disease severity scale. Arch Neurol 2008 65 : 1449 1453.
65. Cid C, Alcazar A, Regidor I, Masjuan J, Salinas M, Alvarez-Cermeno JC. Neuronal apoptosis induced by cerebrospinal fluid from multiple sclerosis patients correlates with hypointense lesions on T1 magnetic resonance imaging. J Neurol Sci 2002 193 : 103 109.
66. Radue EW, Sahraian MA, Pace A, Hyde R. The evaluation of black hole volume evolution as it relates to lesion load, extent of enhancement, and treatment with IM interferon-beta-1a in two relapsing-remitting multiple sclerosis studies. Mult Scler 2006 12 (Suppl. 1 Abstract).
67. Zivadinov R, Locatelli L, Cookfair D et al. Interferon beta-1a slows progression of brain atrophy in relapsing-remitting multiple sclerosis predominantly by reducing gray matter atrophy. Mult Scler. 2007 13 : 490 501.
68. Paolillo A, Bastianello S, Frontoni M et al. Magnetic resonance imaging outcome of new enhancing lesions in relapsing-remitting multiple sclerosis patients treated with interferon beta1a. J Neurol 1999 246 : 443 448. (Pubitemid 29326837)
69. Gasperini C, Pozzilli C, Bastianello S et al. Interferon-beta-1a in relapsing-remitting multiple sclerosis: effect on hypointense lesion volume on T1 weighted images. J Neurol Neurosurg Psychiatry 1999 67 : 579 584.
70. Bagnato F, Gupta S, Richert ND et al. Effects of interferon beta-1b on black holes in multiple sclerosis over a 6-year period with monthly evaluations. Arch Neurol 2005 62 : 1684 1688.
71. Miller DH, Soon D, Fernando KT et al. MRI outcomes in a placebo-controlled trial of natalizumab in relapsing MS. Neurology 2007 68 : 1390 1401.
72. Barkhof F, van Waesberghe JH, Filippi M et al. European Study Group on Interferon beta-1b in Secondary Progressive Multiple Sclerosis. T1 hypointense lesions in secondary progressive multiple sclerosis: effect of interferon beta-1b treatment. Brain 2001 124 : 1396 1402.