Progressive multiple sclerosis: prospects for disease therapy, repair, and restoration of function

The Lancet

Volumn 389, Issue 10076, 2017, Pages 1357-1366

  Ontaneda, Daniel ^a   Thompson, Alan J ^b   Fox, Robert J ^a   Cohen, Jeffrey A ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFLAMMATORY AGENT; NEUROPROTECTIVE AGENT;

BRAIN SIZE; DISABILITY; DISEASE ACTIVITY; DISEASE CLASSIFICATION; GRAY MATTER; HUMAN; MULTIPLE SCLEROSIS; NEUROIMAGING; NEUROPROTECTION; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SPINAL CORD; CLASSIFICATION; DIAGNOSTIC IMAGING; PATHOLOGY;

ANTI-INFLAMMATORY AGENTS; DISABILITY EVALUATION; HUMANS; MULTIPLE SCLEROSIS, CHRONIC PROGRESSIVE; NEUROPROTECTIVE AGENTS;

EID: 85007240186     PISSN: 01406736     EISSN: 1474547X     Source Type: Journal    
DOI: 10.1016/S0140-6736(16)31320-4     Document Type: Review

References (86)

1. 1 Browne, P, Chandraratna, D, Angood, C, et al. Atlas of multiple sclerosis 2013: a growing global problem with widespread inequity. Neurology 83 (2014), 1022–1024.
2. 2 Fox, RJ, Thompson, A, Baker, D, et al. Setting a research agenda for progressive multiple sclerosis: the International Collaborative on Progressive MS. Mult Scler J 18 (2012), 1534–1540.
3. 3 Miller, DH, Leary, SM, Primary-progressive multiple sclerosis. Lancet Neurol 6 (2007), 903–912.
4. 4 Kantarci, OH, Lebrun, C, Siva, A, et al. Primary progressive multiple sclerosis evolving from radiologically isolated syndrome. Ann Neurol 79 (2016), 288–294.
5. 5 Lucchinetti, CF, Parisi, J, Bruck, W, The pathology of multiple sclerosis. Neurol Clin 23 (2005), 77–105.
6. 6 Lucchinetti, CF, Popescu, BFG, Bunyan, RF, et al. Inflammatory cortical demyelination in early multiple sclerosis. N Eng J Med 365 (2011), 2188–2197.
7. 7 Calabrese, M, Poretto, V, Favaretto, A, et al. Cortical lesion load associates with progression of disability in multiple sclerosis. Brain 135 (2012), 2952–2961.
8. 8 Peterson, JW, Bo, L, Mork, S, Chang, A, Trapp, BD, Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann Neurol 50 (2001), 389–400.
9. 9 Serafini, B, Rosicarelli, B, Magliozzi, R, Stigliano, E, Aloisi, F, Detection of ectopic B-cell follicles with germial centers in the meninges of patients with secondary progressive multiple sclerosis. Brain Pathol 14 (2004), 164–174.
10. 10 Howell, OW, Reeves, CA, Nicholas, R, et al. Meningeal inflammation is widespread and linked to cortical pathology in multiple sclerosis. Brain 134 (2011), 2755–2771.
11. 11 Mahad, DH, Trapp, BD, Lassmann, H, Progressive multiple sclerosis 1. Pathological mechanisms in progressive multiple sclerosis. Lancet Neurol 14 (2015), 183–193.
12. 12 Chang, A, Tourtellotte, WW, Rudick, RA, Trapp, BD, Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N Engl J Med 346 (2002), 165–173.
13. 13 Trapp, BD, Peterson, J, Ransohoff, RM, Rudick, R, Mork, S, Bo, L, Axonal transection in the lesions of multiple sclerosis. N Engl J Med 338 (1998), 278–285.
14. 14 Lublin, FD, Reingold, SC, Cohen, JA, et al. Defining the clinical course of multiple sclerosis: the 2013 revisions. Neurology 83 (2014), 278–286.
15. 15 Cohen, JA, Reingold, SC, Polman, CH, Wolinsky, JS, for the International Advisory Committee on Clinical Trials in Multiple Sclerosis. Disability outcome measures in multiple sclerosis trials: current status and future prospects. Lancet Neurol 11 (2012), 467–476.
16. 16 Rudick, RA, LaRocca, N, Hudson, LD, MSOAC. Multiple Sclerosis Outcome Assessments Consortium: Genesis and initial project plan. Mult Scler J 20 (2014), 12–17.
17. 17 Lublin, F, Miller, DH, Freedman, MS, et al. Oral fingolimod in primary progressive multiple sclerosis (INFORMS): a phase 3, randomised, double-blind, placebo-controlled trial. Lancet 387 (2016), 1075–1084.
18. 18 Rudick, RA, Miller, D, Bethoux, F, et al. The Multiple Sclerosis Performance test (MSPT): an iPad-based disability assessment tool. J Vis Exp, 30, 2014, e51318.
19. 19 Sormani, MP, Bruzzi, P, MRI lesions as a surrogate for relapses in multiple sclerosis: a meta-analysis of randomised trials. Lancet Neurol 12 (2013), 669–676.
20. 20 De Stefano, N, Giorgio, A, Battaglini, M, et al. Assessing brain atrophy rates in a large population of untreated multiple sclerosis subtypes. Neurology 74 (2010), 1868–1876.
21. 21 Zivadinov, R, Sepcic, J, Nasuelli, D, et al. A longitudinal study of brain atrophy and cognitive disturbances in the early phase of relapsing-remitting multiple sclerosis. J Neurol Neurosurg Psychiatry 70 (2001), 773–780.
22. 22 Sormani, MP, Arnold, DL, De Stefano, N, Treatment effect on brain atrophy correlates with treatment effect on disability in multiple sclerosis. Ann Neurol 75 (2014), 43–49.
23. 23 Altmann, DR, Jasperse, B, Barkhof, F, et al. Sample sizes for brain atrophy outcomes in trials for secondary progressive multiple sclerosis. Neurology 72 (2009), 595–601.
24. 24 Seewann, A, Kooi, EJ, Roosendaal, SD, et al. Postmortem verification of MS cortical lesion detection with 3D DIR. Neurology 78 (2012), 302–308.
25. 25 Mainero, C, Benner, T, Radding, A, et al. In vivo imaging of cortical pathology in multiple sclerosis using ultra-high field MRI. Neurology 73 (2009), 941–948.
26. 26 Fisher, E, Lee, J-C, Nakamura, K, Rudick, RA, Gray matter atrophy in multiple sclerosis: a longitudinal study. Ann Neurol 64 (2008), 255–265.
27. 27 Chen, JT, Narayanan, S, Collins, DL, Smith, SM, Matthews, PM, Arnold, DL, Relating neocortical pathology to disability progression in multiple sclerosis using MRI. Neuroimage 23 (2004), 1168–1175.
28. 28 Calabrese, M, Rinaldi, F, Grossi, P, Gallo, P, Cortical pathology and cognitive impairment in multiple sclerosis. Expert Rev Neurother 11 (2011), 425–432.
29. 29 Anderson, VM, Fisniku, LK, Khaleeli, Z, et al. Hippocampal atrophy in relapsing-remitting and primary progressive MS: a comparative study. Mult Scler 16 (2010), 1083–1090.
30. 30 Mesaros, S, Rocca, MA, Pagani, E, et al. Thalamic damage predicts the evolution of primary-progressive multiple sclerosis. AJNR Am J Neuroradiol 32 (2011), 1016–1020.
31. 31 Fox, RJ, Cronin, T, Lin, J, et al. Measuring myelin repair and axonal loss with diffusion tensor imaging. AJNR Am J Neuroradiol 32 (2011), 85–91.
32. 32 Fisniku, LK, Altmann, DG, Cercignani, M, et al. Magnetization transfer ratio abnormalities reflect clinically relevant grey matter damage in multiple sclerosis. Mult Scler 15 (2009), 668–677.
33. 33 MacMillan, EL, Tam, R, Zhao, Y, et al. Progressive multiple sclerosis exhibits decreasing glutamate and glutamine over two years. Mult Scler J 22 (2016), 112–116.
34. 34 Ma, D, Gulani, V, Seiberlich, N, et al. Magnetic resonance fingerprinting. Nature 495 (2013), 187–192.
35. 35 Bieniek, M, Altmann, DR, Davies, GR, et al. Cord atrophy separates early primary progressive and relapsing remitting multiple sclerosis. J Neurol Neurosurg Psychiatry 77 (2006), 1036–1039.
36. 36 von Meyenburg, J, Wilm, BJ, Weck, A, et al. Spinal cord diffusion-tensor imaging and motor-evoked potentials in multiple sclerosis patients: microstructural and functional asymmetry. Radiology 267 (2013), 869–879.
37. 37 Charil, A, Caputo, D, Cavarretta, R, Sormani, MP, Ferrante, P, Filippi, M, Cervical cord magnetization transfer ratio and clinical changes over 18 months in patients with relapsing-remitting multiple sclerosis: a preliminary study. Mult Scler 12 (2006), 662–665.
38. 38 Marliani, AF, Clementi, V, Albini Riccioli, L, et al. Quantitative cervical cord 3T proton MR spectroscopy in multiple sclerosis. AJNR Am J Neuroradiol 31 (2010), 180–184.
39. 39 Oh, U, Fujita, M, Ikonomidou, VN, et al. Translocator protein PET imaging for glial activation in multiple sclerosis. J Neuroimmune Pharmacol 6 (2011), 354–361.
40. 40 Wu, C, Zhu, J, Baeslack, J, et al. Longitudinal positron emission tomography imaging for monitoring myelin repair in the spinal cord. Ann Neurol 74 (2013), 688–698.
41. 41 Martinez-Lapiscina, EH, Arnow, S, Wilson, JA, et al. Retinal thickness measured with optical coherence tomography and risk of disability worsening in multiple sclerosis: a cohort study. Lancet Neurol 15 (2016), 574–584.
42. 42 Saidha, S, Al-Louzi, O, Ratchford, JN, et al. Optical coherence tomography reflects brain atrophy in multiple sclerosis: a four-year study. Ann Neurol 78 (2015), 801–813.
43. 43 Steiner D, Arnold D, Freedman M, et al. Natalizumab versus placebo in patients with secondary progressive multiple sclerosis (SPMS): results from ASCEND, a multicenter, double-blind, placebo-controlled, randomized phase 3 clinical trial. Annual Meeting of the American Academy of Neurology; April 15–21, 2016; Vancouver, BC, Canada. abstr ES1.009.
44. 44 Freedman, MS, Bar-Or, A, Oger, J, et al. A phase III study evaluating the efficacy and safety of MBP8298 in secondary progressive MS. Neurology 77 (2011), 1551–1560.
45. 45 Hawker, K, O'Connor, P, Freedman, MS, et al. Rituximab in patients with primary progressive multiple sclerosis. Results of a randomized double-blind placebo-controlled multicenter trial. Ann Neurol 66 (2009), 460–471.
46. 46 Montalban, X, Hemmer, B, Rammohan, K, et al. Efficacy and safety of ecrelizumab in primary progressive multiple sclerosis—results of the placebo-controlled, double-blind, phase III ORATORIO study (Abstract 228). Mult Scler J 23 (2015), 780–781.
47. 47 Wolinsky, JS, Narayana, PA, O'Connor, P, et al. Glatiramer acetate in primary progressive multiple sclerosis: results of a multinational, multicenter, double-blind, placebo-controlled trial. Ann Neurol 61 (2007), 14–24.
48. 48 Zajicek, J, Ball, S, Wright, D, et al. Effect of dronabinol on progression in progressive multiple sclerosis (CUPID): a randomised, placebo-controlled trial. Lancet Neurol 12 (2013), 857–865.
49. 49 Tourbah, A, Lebrun-Frenay, C, Edan, G, et al., for the MS-SPI study group. MD1003 (high-dose biotin) for the treatment of progressive multiple sclerosis: a randomised, double-blind, placebo-controlled study. Mult Scler, 2016, 10.1177/1352458516667568 published online Sept 1.
50. 50 European Study Group on Interferon β-1b in Secondary Progressive MS. Placebo-controlled multicentre randomised trial of interferon β-1b in treatment of secondary progressive multiple sclerosis. Lancet 352 (1998), 1491–1497.
51. 51 Cohen, JA, Cutter, GR, Fischer, JS, et al. Benefit of interferon β-1a on MSFC progression in secondary progressive MS. Neurology 59 (2002), 679–687.
52. 52 Secondary Progressive Efficacy Clinical Trial of Recombinant Interferon-beta-1a in MS (SPECTRIMS) Study Group. Randomized controlled trial of interferon-beta-1a in secondary progressive MS. Clinical results. Neurology 56 (2001), 1496–1504.
53. 53 The North American Study Group on Interferon Beta-1b in Secondary Progressive MS. Interferon beta-1b in secondary progressive MS: results from a three-year controlled study. Neurology 63 (2004), 1788–1795.
54. 54 Andersen, O, Elovaara, I, Farkkila, M, et al. Multicentre, randomised, double blind, placebo controlled, phase III study of weekly, low dose, subcutaneous interferon beta-1a in secondary progressive multiple sclerosis. J Neurol Neurosurg Psychiatry 75 (2004), 706–710.
55. 55 Kappos, L, Weinshenker, B, Pozzilli, C, et al. Interferon beta-1b in secondary progressive MS. A combined analysis of the two trials. Neurology 63 (2004), 1779–1787.
56. 56 Kappos, L, Radue, E-W, O'Connor, P, et al. A placebo-controlled trial of oral fingolimod in relapsing multiple sclerosis. N Engl J Med 362 (2010), 387–401.
57. 57 Cohen, JA, Barkhof, F, Comi, G, et al. Oral fingolimod or intramuscular interferon for relapsing multiple sclerosis. N Engl J Med 362 (2010), 402–415.
58. 58 Calabresi, PA, Radu, EW, Goodin, D, et al. Safety and efficacy of fingolimod in patients with relapsing-remitting multiple sclerosis (FREEDOMS II): a double-blind, randomised, placebo-controlled, phase 3 trial. Lancet Neurol 13 (2014), 545–556.
59. 59 Groves, A, Kihara, Y, Chun, J, Fingolimod: direct CNS effects of sphingosine 1-phosphate (S1P) receptor modulation and implications in multiple sclerosis therapy. J Neurol Sci 328 (2013), 9–18.
60. 60 McFarland, HF, The B cell—old player, new position on the team (editorial). N Engl J Med 358 (2008), 664–665.
61. 61 Wolinsky, JS, Arnold, D, Bar-Or, A, et al. Efficacy of ocrelizumab in patients with PPMS with and without T1 gadolinium-enhancing lesions at baseline in a phase III placebo-controlled trial (LB148). Mult Scler J 22 (2016), 67–68.
62. 62 Chataway, J, Schuerer, N, Alsanousi, A, et al. Effect of high-dose simvastatin on brain atrophy and disability in secondary progressive multiple sclerosis (MS-STAT): a randomised, placebo-controlled, phase 2 trial. Lancet 383 (2014), 2213–2221.
63. 63 Raftopoulos, R, Hickman, SJ, Toosy, A, et al. Phenytoin for neuroprotection in patients with acute optic neuritis: a randomised, placebo-controlled, phase 2 trial. Lancet Neurol 15 (2016), 259–269.
64. 64 Kapoor, R, Furby, J, Hayton, T, et al. Lamotrigine for neuroprotection in secondary progressive multiple sclerosis: a randomised, double-blind, placebo-controlled, parallel-group study. Lancet Neurol 9 (2010), 681–688.
65. 65 Sedel, F, Bernard, D, Mock, DM, Tourbah, A, Targeting demyelination and virtual hypoxia with high-dose biotin as a treatment for progressive multiple sclerosis. Neuropharmacology, 2015, 10.1016/j.neuropharm.2015.08.028 published online Sept 5.
66. 66 Mi, S, Pepinsky, RB, Cadavid, D, Blocking LINGO-1 as a therapy to promote CNS repair: from concept to the clinic. CNS Drugs 27 (2013), 493–503.
67. 67 Cadavid, D, Balcer, L, Galetta, S, et al. Efficacy analysis of the Anti-LINGO-1 monoclonal antibody BIIB033 in acute optic neuritis: the RENEW trial. Neurology, 84(suppl 14), 2015 P7.202.
68. 68 Cadavid, D, Edwards, KR, Hupperts, R, et al. Efficacy analysis of opicinumab in relapsing multiple sclerosis: the phase 2b SYNERGY trial (abstract 192). Mult Scler J, 22(suppl 3), 2016, 66.
69. 69 Windrem, MS, Schanz, SJ, Guo, M, et al. Neonatal chimerization with human glial progenitor cells can both remyelinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell 2 (2008), 553–565.
70. 70 Goodman, AD, Stem cell therapy for MS. Mult Scler J, 22(suppl 1), 2016, 8.
71. 71 Mei, F, Fancy, SPJ, Shen, Y-AA, et al. Micropillar arrays as a high-throughput screening platform for therapeutics in multiple sclerosis. Nat Med 20 (2014), 954–960.
72. 72 Najm, FJ, Madhavan, M, Zaremba, A, et al. Drug-based modulation of endogenous stem cells promotes functional remyelination in vivo. Nature 522 (2015), 216–220.
73. 73 Green A, Gelfand J, Cree B, et al. Positive phase II double-blind randomized placebo-controlled crossover trial of clemastine fumarate for remyelination of chronic optic neuropathy in MS. Annual Meeting of the American Academy of Neurology; April 15–21, 2016; Vancouver, BC, Canada. abstr ES1.008.
74. 74 Cohen, JA, Mesenchymal stem cell transplantation in multiple sclerosis. J Neurol Sci 333 (2013), 43–49.
75. 75 Heesen, C, Bohm, J, Reich, C, Kasper, J, Goebel, M, Gold, SM, Patient perception of bodily functions in multiple sclerosis: gait and visual function are the most valuable. Mult Scler 14 (2008), 988–991.
76. 76 Campbell, E, Coulter, EH, Mattison, PG, Miller, L, McFadyen, A, Paul, L, Physiotherapy rehabilitation for people with progressive multiple sclerosis: a systematic review. Arch Phys Med Rehabil 97 (2016), 141–151.
77. 77 Dalgas, U, Stenager, E, Exercise and disease progression in multiple sclerosis: can exercise slow down the progression of multiple sclerosis?. Ther Adv Neurol Disord 5 (2012), 81–95.
78. 78 Beier, M, Bombardier, CH, Hartoonian, N, Motl, RW, Kraft, GH, Improved physical fitness correlates with improved cognition in multiple sclerosis. Arch Phys Med Rehabil 95 (2014), 1328–1334.
79. 79 Briken, S, Gold, SM, Patra, S, et al. Effects of exercise on fitness and cognition in progressive MS: a randomized, controlled pilot trial. Mult Scler J 20 (2014), 382–390.
80. 80 Hupperts, R, Lycke, J, Short, C, et al. Prolonged-release fampridine and walking and balance in MS: randomised controlled MOBILE trial. Mult Scler J 22 (2016), 212–221.
81. 81 Feys, P, Potential of robot-assisted therapy for disabled persons with MS. Mult Scler J 22 (2016), 264–265.
82. 82 Tomassini, V, Matthews, PM, Thompson, AJ, et al. Neuroplasticity and functional recovery in multiple sclerosis. Nature Rev Neurol 8 (2012), 635–646.
83. 83 Weiss, S, Mori, F, Rossi, S, Centonze, D, Disability in multiple sclerosis: when synaptic long-term potentiation fails. Neurosci Biobehav Rev 43 (2014), 88–99.
84. 84 Marrie, RA, Cohen, J, Stuve, O, et al. A systematic review of the incidence and prevalence of comorbidity in multiple sclerosis: overview. Mult Scler J 21 (2015), 263–281.
85. 85 Nilsagard, Y, Gunn, H, Freeman, J, et al. Falls in people with MS—an individual data meta-analysis from studies from Australia, Sweden, United Kingdom and the United States. Mult Scler J 21 (2015), 92–100.
86. 86 Dunn, M, Bhargava, P, Kalb, R, Your patients with MS have set wellness as a high priority—and the National MS Society is responding. Multiple Sclerosis Special Report. US Neurology 11 (2015), 80–86.