Defining and scoring response to IFN-β in multiple sclerosis

Nature Reviews Neurology

Volumn 9, Issue 9, 2013, Pages 504-512

  Sormani, Maria Pia ^a   De Stefano, Nicola ^b  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF SIENA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; BETA INTERFERON ANTIBODY; BIOLOGICAL MARKER; FINGOLIMOD; GADOLINIUM; GLATIRAMER; NATALIZUMAB; NEUTRALIZING ANTIBODY; PLACEBO; UNCLASSIFIED DRUG;

DISABILITY; DISEASE ACTIVITY; DISEASE EXACERBATION; DRUG RESPONSE; EXPANDED DISABILITY STATUS SCALE; HUMAN; LONG TERM CARE; MODIFIED RIO SCORE; MULTIPLE SCLEROSIS; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROGNOSIS; REVIEW; RIO SCORE; SCORING SYSTEM;

BIOMARKERS, PHARMACOLOGICAL; HUMANS; INTERFERON-BETA; MAGNETIC RESONANCE IMAGING; MULTIPLE SCLEROSIS; TREATMENT OUTCOME;

EID: 84883739704     PISSN: 17594758     EISSN: 17594766     Source Type: Journal    
DOI: 10.1038/nrneurol.2013.146     Document Type: Review

References (71)

1. Compston, A. & Coles, A. Multiple sclerosis. Lancet 359, 1221-1231 (2002). (Pubitemid 34304266)
2. Baksi, R. The new era of multiple sclerosis therapeutics. Neurotherapeutics 10, 1 (2013).
3. Castro-Borrero, W. et al. Current and emerging therapies in multiple sclerosis: a systematic review. Ther. Adv. Neurol. Disord. 5, 205-220 (2012).
4. McGraw, C. A. & Lublin, F. D. Interferon beta and glatiramer acetate therapy. Neurotherapeutics 10, 2-18 (2013).
5. Paty, D. W. & Li, D. K. Interferon beta-1b is effective in relapsing-remitting multiple sclerosis. II. MRI analysis results of a multicenter, randomized, double-blind, placebo-controlled trial. UBC MS/MRI Study Group and the IFNB Multiple Sclerosis Study Group. Neurology 43, 662-667 (1993). (Pubitemid 23121952)
6. [No authors listed] Interferon beta-1b is effective in relapsing-remitting multiple sclerosis. I. Clinical results of a multicenter, randomized, double-blind, placebo-controlled trial. The IFNB Multiple Sclerosis Study Group. Neurology 43, 655-661 (1993).
7. Jacobs, L. D. et al. Intramuscular interferon beta-1a for disease progression in relapsing multiple sclerosis. The Multiple Sclerosis Collaborative Research Group (MSCRG). Ann. Neurol. 39, 285-294 (1996). (Pubitemid 26100751)
8. [No authors listed] Randomised double-blind placebo-controlled study of interferon β-1a in relapsing/remitting multiple sclerosis. PRISMS (Prevention of Relapses and Disability by Interferon β-1a Subcutaneously in Multiple Sclerosis) Study Group. Lancet 352, 1498-1504 (1998).
9. Polman, C. H. et al. A randomized, placebo-controlled trial of natalizumab for relapsing multiple sclerosis. N. Engl. J. Med. 354, 899-910 (2006).
10. Chataway, J. & Miller, D. H. Natalizumab therapy for multiple sclerosis. Neurotherapeutics 10, 19-28 (2013).
11. Kappos, L. et al. A placebo-controlled trial of oral fingolimod in relapsing multiple sclerosis. N. Engl. J. Med. 362, 387-401 (2010).
12. Cohen, J. A. et al. Oral fingolimod or intramuscular interferon for relapsing multiple sclerosis. N. Engl. J. Med. 362, 402-415 (2010).
13. Visser, F., Wattjes, M. P., Pouwels, P. J., Linssen, W. H. & van Oosten, B. W. Tumefactive multiple sclerosis lesions under fingolimod treatment. Neurology 79, 2000-2003 (2012).
14. Bourdette, D. & Gilden, D. Fingolimod and multiple sclerosis: four cautionary tales. Neurology 79, 1942-1943 (2012).
15. O'Connor, P. W. et al. A Phase II study of the safety and efficacy of teriflunomide in multiple sclerosis with relapses. Neurology 66, 894-900 (2006). (Pubitemid 43739766)
16. O'Connor, P. et al. Randomized trial of oral teriflunomide for relapsing multiple sclerosis. N. Engl. J. Med. 365, 1293-1303 (2011).
17. Gold, R. et al. Placebo-controlled phase 3 study of oral BG-12 for relapsing multiple sclerosis. N. Engl. J. Med. 367, 1098-1107 (2012).
18. Fox, R. J. et al. Placebo-controlled phase 3 study of oral BG-12 or glatiramer in multiple sclerosis. N. Engl. J. Med. 367, 1087-1097 (2012).
19. Gold, R. et al. Daclizumab high-yield process in relapsing-remitting multiple sclerosis (SELECT): a randomised, double-blind, placebo-controlled trial. Lancet 381, 2167-2175 (2013).
20. Comi, G. et al. Placebo-controlled trial of oral laquinimod for multiple sclerosis. N. Engl. J. Med. 366, 1000-1009 (2012).
21. Cohen, J. A. et al. Alemtuzumab versus interferon beta 1a as first-line treatment for patients with relapsing-remitting multiple sclerosis, a randomised controlled phase 3 trial. Lancet 380, 1819-1828 (2012).
22. Coles, A. J. et al. Alemtuzumab for patients with relapsing multiple sclerosis after disease-modifying therapy, a randomised controlled phase 3 trial. Lancet 380, 1829-1839 (2012).
23. Kurtzke, J. F. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 33, 1444-1452 (1983). (Pubitemid 14237132)
24. Poser, C. M. et al. New diagnostic criteria for multiple sclerosis: guidelines for research protocols. Ann. Neurol. 13, 227-231 (1983). (Pubitemid 13158528)
25. Barkhof, F. et al. Strategies for optimizing MRI techniques aimed at monitoring disease activity in multiple sclerosis treatment trials. J. Neurol. 244, 76-84 (1997). (Pubitemid 27057951)
26. Durelli, L. et al. MRI activity and neutralizing antibody as predictors of response to interferon β treatment in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 79, 646-651 (2008). (Pubitemid 351829435)
27. Cadavid, D. et al. Clinical consequences of MRI activity in treated multiple sclerosis. Mult. Scler. 17, 1113-1121 (2011).
28. Río, J. et al. Relationship between MRI lesion activity and response to IFN-β in relapsing-remitting multiple sclerosis patients. Mult. Scler. 14, 479-484 (2008). (Pubitemid 351943860)
29. Prosperini, L. et al. One-year MRI scan predicts clinical response to interferon β in multiple sclerosis. Eur. J. Neurol. 16, 1202-1209 (2009).
30. Sormani, M. et al. Scoring treatment response in patients with relapsing multiple sclerosis. Mult. Scler. 19, 605-612 (2013).
31. Tomassini, V. et al. Predictors of long-term clinical response to interferon beta therapy in relapsing multiple sclerosis. J. Neurol. 253, 287-293 (2006).
32. Bermel, R. et al. Predictors of long-term outcome in multiple sclerosis patients treated with interferon β. Ann. Neurol. 73, 95-103 (2013).
33. Goodin, D. et al. Relationship between early clinical characteristics and long term disability outcomes: 16 year cohort study (follow-up) of the pivotal interferon β-1b trial in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 83, 282-287 (2012).
34. Romeo, M. et al. Clinical and MRI predictors of response to interferon-beta and glatiramer acetate in relapsing-remitting multiple sclerosis patients. Eur. J. Neurol. 20, 1060-1067 (2013).
35. Mezei, Z. et al. Can a physician predict the clinical response to first-line immunomodulatory treatment in relapsing-remitting multiple sclerosis? Neuropsychiatr. Dis. Treat. 8, 465-473 (2012).
36. Waubant, E. et al. Clinical characteristics of responders to interferon therapy for relapsing MS. Neurology 61, 184-189 (2003). (Pubitemid 36875298)
37. Portaccio, E., Zipoli, V., Siracusa, G., Sorbi, S. & Amato, M. P. Response to interferon-beta therapy in relapsing-remitting multiple sclerosis, a comparison of different clinical criteria. Mult. Scler. 12, 281-286 (2006). (Pubitemid 43827182)
38. Fromont, A. et al. Clinical parameters to predict response to interferon in relapsing multiple sclerosis. Neuroepidemiology 31, 150-156 (2008).
39. Romeo, M. et al. Rio Score and Modified Rio Score validation in an Italian cohort of relapsing-remitting multiple sclerosis patients (abstract P549). Presented at the 28th Congress of the European Committee for Treatment and Research in Multiple Sclerosis, 10-13 October 2012.
40. Freedman, M. et al. Recognizing and treating suboptimally controlled multiple sclerosis, steps toward regaining command. Curr. Med. Res. Opin. 10, 2459-2470 (2009).
41. Río, J. et al. Assessment of different treatment failure criteria in a cohort of relapsing-remitting multiple sclerosis patients treated with interferon β: implications for clinical trials. Ann. Neurol. 52, 400-406 (2002).
42. Río, J. et al. Defining the response to interferon-β in relapsing-remitting multiple sclerosis patients. Ann. Neurol. 59, 344-352 (2006). (Pubitemid 43202488)
43. Río, J., Comabella, M. & Montalban, X. Predicting responders to therapies for multiple sclerosis. Nat. Rev. Neurol. 5, 553-560 (2009).
44. Polman, C. et al. Subgroups of the BENEFIT study, risk of developing MS and treatment effect of interferon beta-1b. J. Neurol. 255, 480-487 (2008).
45. O'Connor, P., Kinkel, R. P. & Kremenchutzky, M. Efficacy of intramuscular interferon beta-1a in patients with clinically isolated syndrome, analysis of subgroups based on new risk criteria. Mult. Scler. 15, 728-734 (2009).
46. Barkhof, F. et al. Validation of diagnostic magnetic resonance imaging criteria for multiple sclerosis and response to interferon β1a. Ann. Neurol. 53, 718-724 (2003). (Pubitemid 36622508)
47. Comi, G. et al. Comparison of two dosing frequencies of subcutaneous interferon beta-1a in patients with a first clinical demyelinating event suggestive of multiple sclerosis (REFLEX): a phase 3 randomised controlled trial. Lancet Neurol. 11, 33-41 (2012).
48. Martínez-Yélamos, S. et al. Regression to the mean in multiple sclerosis. Mult. Scler. 12, 826-829 (2006). (Pubitemid 46111778)
49. Prentice, R. L. Surrogate endpoints in clinical trials, definition and operational criteria. Stat. Med. 8, 431-440 (1989). (Pubitemid 19105891)
50. Sormani, M. P., Bruzzi, P., Comi, G. & Filippi, M. MRI metrics as surrogate markers for clinical relapse rate in relapsing-remitting MS patients. Neurology 58, 417-421 (2002). (Pubitemid 34150916)
51. Sormani, M. P. et al. MRI metrics as surrogate endpoints for EDSS progression in SPMS patients treated with IFN β-1b. Neurology 60, 1462-1466 (2003). (Pubitemid 36554807)
52. Sormani, M. P. et al. Magnetic resonance active lesions as individual-level surrogate for relapses in multiple sclerosis. Mult. Scler. 17, 541-549 (2011).
53. Sormani, M. P. et al. Combined MRI lesions and relapses as a perfect surrogate for disability in multiple sclerosis. Neurology 77, 1684-1690 (2011).
54. Wang, Y. C., Sandrock, A., Richert, J. R., Meyerson, L. & Miao, X. Short-term relapse quantitation as a fully surrogate endpoint for long-term sustained progression of disability in RRMS patients treated with natalizumab. Neurol. Res. Int. 2011, 195831 (2001).
55. Rudick, R., Lee, J., Simon, J., Ransohoff, R. M. & Fisher, E. Defining interferon β response status in multiple sclerosis patients. Ann. Neurol. 56, 548-555 (2004). (Pubitemid 39319345)
56. Inusah, S. et al. Assessing changes in relapse rates in multiple sclerosis. Mult. Scler. 16, 1414-1421 (2010).
57. Miller, D. H. et al. Serial gadolinium enhanced magnetic resonance imaging in multiple sclerosis. Brain 111, 927-939 (1988).
58. Freedman, M. S. et al. Treatment optimization in MS: Canadian MS Working Group updated recommendations. Can. J. Neurol. Sci. 40, 307-323 (2013).
59. Freedman, M. S. & Forrestal, F. G. Canadian treatment optimization recommendations (TOR) as a predictor of disease breakthrough in patients with multiple sclerosis treated with interferon β-1a: analysis of the PRISMS study. Mult. Scler. 14, 1234-1241 (2008).
60. Sormani, M., Signori, A., Stromillo, M. & De Stefano, N. Refining response to treatment as defined by the Modified Rio Score. Mult. Scler. http://dx.doi.org/10.1177/1352458513483892.
61. Kalincik, T. et al. Volumetric MRI markers and predictors of disease activity in early multiple sclerosis: a longitudinal cohort study. PLoS ONE 7, e50101 (2012).
62. Barkhof, F. et al. MRI monitoring of immunomodulation in relapse-onset multiple sclerosis trials. Nat. Rev. Neurol. 8, 13-21 (2011).
63. Barkhof, F. et al. Imaging outcomes for neuroprotection and repair in multiple sclerosis trials. Nat. Rev. Neurol. 5, 256-266 (2009).
64. Comabella, M. & Martin, R. Genomics in multiple sclerosis-current state and future directions. J. Neuroimmunol. 187, 1-8 (2007). (Pubitemid 47001533)
65. Singh, M. K. et al. Gene expression changes in peripheral blood mononuclear cells from multiple sclerosis patients undergoing β-interferon therapy. J. Neurol. Sci. 258, 52-59 (2007). (Pubitemid 46874477)
66. van Baarsen, L. G. et al. Pharmacogenomics of interferon β therapy in multiple sclerosis: baseline IFN signature determines pharmacological differences between patients. PLoS ONE 3, e1927 (2008).
67. Villoslada, P. et al. The HLA locus and multiple sclerosis in Spain. Role in disease susceptibility, clinical course and response to interferon β. J. Neuroimmunol. 130, 194-201 (2002). (Pubitemid 35240007)
68. Killestein, J. & Polman, C. H. Determinants of interferon β efficacy in patients with multiple sclerosis. Nat. Rev. Neurol. 7, 221-228 (2011).
69. Axtell, R. C. et al. T helper type 1 and 17 cells determine efficacy of interferon-β in multiple sclerosis and experimental encephalomyelitis. Nat. Med. 16, 406-412 (2010).
70. Hartung, H. P. et al. Interleukin 17F level and interferon beta response in patients with multiple sclerosis. JAMA Neurol. http://dx.doi.org/10.1001/ jamaneurol.2013.192.
71. Bushnell, S. E. et al. Serum IL-17F does not predict poor response to IM IFNβ-1a in relapsing-remitting MS. Neurology. 79, 531-537 (2012).