140
Views
3
CrossRef citations to date
0
Altmetric
Reviews

The challenges of measuring disability accumulation in relapsing–remitting multiple sclerosis: evidence from interferon beta treatments

References

  • Compston A, Coles A. Multiple sclerosis. Lancet 359(9313), 1221–1231 (2002).
  • Noseworthy JH, Lucchinetti C, Rodriguez M, Weinshenker BG. Multiple sclerosis. N. Engl. J. Med. 343(13), 938–952 (2000).
  • 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(5), 278–285 (1998).
  • Naci H, Fleurence R, Birt J, Duhig A. Economic burden of multiple sclerosis: a systematic review of the literature. Pharmacoeconomics 28(5), 363–379 (2010).
  • Hughes S, Spelman T, Trojano M et al. The Kurtzke EDSS rank stability increases 4 years after the onset of multiple sclerosis: results from the MSBase Registry. J. Neurol. Neurosurg. Psychiatry 83(3), 305–310 (2012).
  • Tremlett H, Paty D, Devonshire V. Disability progression in multiple sclerosis is slower than previously reported. Neurology 66(2), 172–177 (2006).
  • Weinshenker BG, Rice GP, Noseworthy JH, Carriere W, Baskerville J, Ebers GC. The natural history of multiple sclerosis: a geographically based study. 4. Applications to planning and interpretation of clinical therapeutic trials. Brain 114(Pt 2), 1057–1067 (1991).
  • Confavreux C, Vukusic S, Adeleine P. Early clinical predictors and progression of irreversible disability in multiple sclerosis: an amnesic process. Brain 126(Pt 4), 770–782 (2003).
  • Leray E, Yaouanq J, Le Page E et al. Evidence for a two-stage disability progression in multiple sclerosis. Brain 133(Pt 7), 1900–1913 (2010).
  • Jacobs LD, Cookfair DL, Rudick RA et al. Intramuscular interferon beta-1a for disease progression in relapsing multiple sclerosis. The Multiple Sclerosis Collaborative Research Group (MSCRG). Ann. Neurol. 39(3), 285–294 (1996).
  • Cohen JA, Reingold SC, Polman CH, Wolinsky JS. Disability outcome measures in multiple sclerosis clinical trials: current status and future prospects. Lancet Neurol. 11(5), 467–476 (2012).
  • Trojano M, Paolicelli D, Tortorella C et al. Natural history of multiple sclerosis: have available therapies impacted long-term prognosis? Neurol. Clin. 29(2), 309–321 (2011).
  • Frischer JM, Bramow S, Dal-Bianco A et al. The relation between inflammation and neurodegeneration in multiple sclerosis brains. Brain 132(Pt 5), 1175–1189 (2009).
  • Lublin FD, Baier M, Cutter G. Effect of relapses on development of residual deficit in multiple sclerosis. Neurology 61(11), 1528–1532 (2003).
  • Goodin DS, Traboulsee A, Knappertz V et al. Relationship between early clinical characteristics and long term disability outcomes: 16 year cohort study (follow-up) of the pivotal interferon beta-1b trial in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 83(3), 282–287 (2012).
  • Goodin DS, Reder AT, Ebers GC et al. Survival in MS: a randomized cohort study 21 years after the start of the pivotal IFNbeta-1b trial. Neurology 78(17), 1315–1322 (2012).
  • Shirani A, Zhao Y, Karim ME et al. Association between use of interferon beta and progression of disability in patients with relapsing-remitting multiple sclerosis. JAMA 308(3), 247–256 (2012).
  • Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 33(11), 1444–1452 (1983).
  • Weinshenker BG, Bass B, Rice GP et al. The natural history of multiple sclerosis: a geographically based study. 2. Predictive value of the early clinical course. Brain 112(Pt 6), 1419–1428 (1989).
  • Hyland M, Rudick RA. Challenges to clinical trials in multiple sclerosis: outcome measures in the era of disease-modifying drugs. Curr. Opin. Neurol. 24(3), 255–261 (2011).
  • Polman CH, Rudick RA. The multiple sclerosis functional composite: a clinically meaningful measure of disability. Neurology 74(Suppl. 3), S8–S15 (2010).
  • Healy BC, Engler D, Glanz B, Musallam A, Chitnis T. Assessment of definitions of sustained disease progression in relapsing-remitting multiple sclerosis. Mult. Scler. Int. 2013, 189–624 (2013).
  • Ellison GW, Myers LW, Leake BD et al. Design strategies in multiple sclerosis clinical trials. Ann. Neurol. 36(Suppl.), S108–S112 (1994).
  • Rudick RA, Lee JC, Cutter G et al. Disability progression in a clinical trial of relapsing-remitting multiple sclerosis: eight-year follow-up. Arch. Neurol. 67(11), 1329–1335 (2010).
  • Rio J, Nos C, Tintore M et al. Assessment of different treatment failure criteria in a cohort of relapsing-remitting multiple sclerosis patients treated with interferon beta: implications for clinical trials. Ann. Neurol. 52(4), 400–406 (2002).
  • Cutter GR, Baier ML, Rudick RA et al. Development of a multiple sclerosis functional composite as a clinical trial outcome measure. Brain 122(Pt 5), 871–882 (1999).
  • Rudick RA, Polman CH, Cohen JA et al. Assessing disability progression with the Multiple Sclerosis Functional Composite. Mult. Scler. 15(8), 984–997 (2009).
  • Schwid SR, Goodman AD, McDermott MP, Bever CF, Cook SD. Quantitative functional measures in MS: what is a reliable change? Neurology 58(8), 1294–1296 (2002).
  • Kragt JJ, van der Linden FA, Nielsen JM, Uitdehaag BM, Polman CH. Clinical impact of 20% worsening on Timed 25-Foot Walk and 9-Hole Peg Test in multiple sclerosis. Mult. Scler. 12(5), 594–598 (2006).
  • Graves J, Balcer LJ. Eye disorders in patients with multiple sclerosis: natural history and management. Clin. Ophthalmol. 41409–1422 (2010).
  • Ontaneda D, LaRocca N, Coetzee T, Rudick R. Revisiting the multiple sclerosis functional composite: proceedings from the National Multiple Sclerosis Society (NMSS) Task Force on Clinical Disability Measures. Mult. Scler. 18(8), 1074–1080 (2012).
  • Bermel RA, Weinstock-Guttman B, Bourdette D, Foulds P, You X, Rudick RA. Intramuscular interferon beta-1a therapy in patients with relapsing-remitting multiple sclerosis: a 15-year follow-up study. Mult. Scler. 16(5), 588–596 (2010).
  • Miller D, Weinstock-Guttman B, Bourdette D, You X, Foulds P, Rudick R. Change in quality of life in patients with relapsing-remitting multiple sclerosis over 2 years in relation to other clinical parameters: results from a trial of intramuscular interferon {beta}-1a. Mult. Scler. 17(6), 734–742 (2011).
  • Miller DM, Rudick RA, Baier M et al. Factors that predict health-related quality of life in patients with relapsing-remitting multiple sclerosis. Mult. Scler. 9(1), 1–5 (2003).
  • Jongen PJ, Sindic C, Carton H, Zwanikken C, Lemmens W, Borm G. Improvement of health-related quality of life in relapsing remitting multiple sclerosis patients after 2 years of treatment with intramuscular interferon-beta-1a. J. Neurol. 257(4), 584–589 (2010).
  • Putzki N, Fischer J, Gottwald K et al. Quality of life in 1000 patients with early relapsing-remitting multiple sclerosis. Eur. J. Neurol. 16(6), 713–720 (2009).
  • Vermersch P, de Seze J, Delisse B, Lemaire S, Stojkovic T. Quality of life in multiple sclerosis: influence of interferon-beta1 a (Avonex) treatment. Mult. Scler. 8(5), 377–381 (2002).
  • Hobart J, Lamping D, Fitzpatrick R, Riazi A, Thompson A. The Multiple Sclerosis Impact Scale (MSIS-29): a new patient-based outcome measure. Brain. 124(Pt 5), 962–973 (2001).
  • Renoux C. Natural history of multiple sclerosis: long-term prognostic factors. Neurol. Clin. 29(2), 293–308 (2011).
  • Berg-Hansen P, Smestad C, Sandvik L, Harbo HF, Celius EG. Increased disease severity in non-Western immigrants with multiple sclerosis in Oslo, Norway. Eur. J. Neurol. 20(12), 1546–1552 (2013).
  • Kister I, Chamot E, Bacon JH et al. Rapid disease course in African Americans with multiple sclerosis. Neurology 75(3), 217–223 (2010).
  • Kantarci O, Siva A, Eraksoy M et al. Survival and predictors of disability in Turkish MS patients. Turkish Multiple Sclerosis Study Group (TUMSSG). Neurology 51(3), 765–772 (1998).
  • Bergamaschi R, Berzuini C, Romani A, Cosi V. Predicting secondary progression in relapsing-remitting multiple sclerosis: a Bayesian analysis. J. Neurol. Sci. 189(1–2), 13–21 (2001).
  • Damasceno A, Von Glehn F, Brandão CO, Damasceno BP, Cendes F. Prognostic indicators for long-term disability in multiple sclerosis patients. J. Neurol. Sci. 324(1–2), 29–33 (2013).
  • Lević ZM, Dujmović I, Pekmezović T et al. Prognostic factors for survival in multiple sclerosis. Mult. Scler. 5(3), 171–178 (1999).
  • Eriksson M, Andersen O, Runmarker B. Long-term follow up of patients with clinically isolated syndromes, relapsing-remitting and secondary progressive multiple sclerosis. Mult. Scler. 9(3), 260–274 (2003).
  • Myhr KM, Riise T, Vedeler C et al. Disability and prognosis in multiple sclerosis: demographic and clinical variables important for the ability to walk and awarding of disability pension. Mult. Scler. 7(1), 59–65 (2001).
  • Riise T, Grønning M, Fernández O et al. Early prognostic factors for disability in multiple sclerosis, a European multicenter study. Acta Neurol. Scand. 85(3), 212–218 (1992).
  • Simone IL, Carrara D, Tortorella C et al. Course and prognosis in early-onset MS: comparison with adult-onset forms. Neurology 59(12), 1922–1928 (2002).
  • Trojano M, Avolio C, Manzari C et al. Multivariate analysis of predictive factors of multiple sclerosis course with a validated method to assess clinical events. J. Neurol. Neurosurg. Psychiatry 58(3), 300–306 (1995).
  • Amato MP, Ponziani G, Bartolozzi ML, Siracusa G. A prospective study on the natural history of multiple sclerosis: clues to the conduct and interpretation of clinical trials. J. Neurol. Sci. 168(2), 96–106 (1999).
  • Binquet C, Quantin C, Le Teuff G, Pagliano JF, Abrahamowicz M, Moreau T. The prognostic value of initial relapses on the evolution of disability in patients with relapsing-remitting multiple sclerosis. Neuroepidemiology 27(1), 45–54 (2006).
  • Hammond SR, McLeod JG, Macaskill P, English DR. Multiple sclerosis in Australia: prognostic factors. J. Clin. Neurosci. 7(1), 16–19 (2000).
  • Phadke JG. Clinical aspects of multiple sclerosis in north-east Scotland with particular reference to its course and prognosis. Brain 113(Pt. 6), 1597–1628 (1990).
  • Amato MP, Ponziani G. A prospective study on the prognosis of multiple sclerosis. Neurol. Sci. 21(4 Suppl. 2), S831–S838 (2000).
  • Uría DF, Menes BB, Calatayud MT, Arribas JM. [Prognostic factors in multiple sclerosis in a population-based series in Asturias]. Neurologia 9(5), 182–187 (1994) [ article in Spanish].
  • Tremlett H, Yousefi M, Devonshire V, Rieckmann P, Zhao Y; UBC Neurologists. Impact of multiple sclerosis relapses on progression diminishes with time. Neurology 73(20), 1616–1623 (2009).
  • Scalfari A, Neuhaus A, Daumer M, Muraro PA, Ebers GC. Onset of secondary progressive phase and long-term evolution of multiple sclerosis. J. Neurol. Neurosurg. Psychiatry doi:10.1136/jnnp-2012-304333 (2013) ( Epub ahead of print).
  • Langer-Gould A, Popat RA, Huang SM et al. Clinical and demographic predictors of long-term disability in patients with relapsing-remitting multiple sclerosis: a systematic review. Arch. Neurol. 63(12), 1686–1691 (2006).
  • Confavreux C, Vukusic S. Natural history of multiple sclerosis: a unifying concept. Brain 129(Pt 3), 606–616 (2006).
  • PRISMS (Prevention of Relapses and Disability by Interferon beta-1a Subcutaneously in Multiple Sclerosis) Study Group. Randomised double-blind placebo-controlled study of interferon beta-1a in relapsing/remitting multiple sclerosis. Lancet 352(9139), 1498–1504 (1998).
  • IFNB Multiple Sclerosis Study Group. Interferon beta-lb is effective in relapsing-remitting multiple sclerosis. I. Clinical results of a multicenter, randomized, double-blind, placebo-controlled trial. Neurology 57(12 Suppl 5), S3–S9 (2001).
  • O’Connor P, Filippi M, Arnason B et al. 250 microg or 500 microg interferon beta-1b versus 20 mg glatiramer acetate in relapsing-remitting multiple sclerosis: a prospective, randomised, multicentre study. Lancet Neurol. 8(10), 889–897 (2009).
  • Panitch H, Goodin DS, Francis G et al. Randomized, comparative study of interferon beta-1a treatment regimens in MS: the EVIDENCE trial. Neurology 59(10), 1496–1506 (2002).
  • Kappos L, Traboulsee A, Constantinescu C et al. Long-term subcutaneous interferon beta-1a therapy in patients with relapsing-remitting MS. Neurology 67(6), 944–953 (2006).
  • Uitdehaag BM, Constantinescu C, Cornelisse P et al. Impact of exposure to interferon beta-1a on outcomes in patients with relapsing-remitting multiple sclerosis: exploratory analyses from the PRISMS long-term follow-up study. Ther. Adv. Neurol. Disord. 4(1), 3–14 (2011).
  • Ebers GC, Traboulsee A, Li D et al.; Investigators of the 16-year Long-Term Follow-up Study. Analysis of clinical outcomes according to original treatment groups 16 years after the pivotal IFNB-1b trial. J. Neurol. Neurosurg. Psychiatry 81(8), 907–912 (2010).
  • Trojano M, Pellegrini F, Paolicelli D et al. Real-life impact of early interferon beta therapy in relapsing multiple sclerosis. Ann. Neurol. 66(4), 513–520 (2009).
  • Kinkel RP, Kollman C, O’Connor P et al.; CHAMPIONS Study Group. im. interferon beta-1a delays definite multiple sclerosis 5 years after a first demyelinating event. Neurology 66(5), 678–684 (2006).
  • Kinkel RP, Dontchev M, Kollman C, Skaramagas TT, O’Connor PW, Simon JH. Association between immediate initiation of intramuscular interferon beta-1a at the time of a clinically isolated syndrome and long-term outcomes: a 10-year follow-up of the Controlled High-Risk Avonex Multiple Sclerosis Prevention Study in Ongoing Neurological Surveillance. Arch. Neurol. 69(2), 183–190 (2012).
  • Kappos L, Freedman MS, Polman CH et al.; BENEFIT Study Group. Long-term effect of early treatment with interferon beta-1b after a first clinical event suggestive of multiple sclerosis: 5-year active treatment extension of the phase 3 BENEFIT trial. Lancet Neurol. 8(11), 987–997 (2009).
  • Goodin DS, Jones J, Li D et al. Establishing long-term efficacy in chronic disease: use of recursive partitioning and propensity score adjustment to estimate outcome in MS. PLoS ONE 6(11), e22444 (2011).
  • Bermel RA, You X, Foulds P et al. Predictors of long-term outcome in MS patients treated with interferon beta. Ann. Neurol. 73(1), 95–103 (2012).
  • Uitdehaag BM, Barkhof F, Coyle PK et al. The changing face of multiple sclerosis clinical trial populations. Curr. Med. Res. Opin. 27, 1529–1537 (2011).
  • Rice GPA, Incorvaia B, Munari LM et al. Interferon in relapsing-remitting multiple sclerosis. Cochrane Database Syst. Rev. (4), CD002002 (2001).
  • Gronseth GS, Ashman E. The AAN response to evidence-based medicine: promise and pitfalls. Mult. Scler. 18(7), 949–950 (2012).
  • Greenberg BM, Balcer L, Calabresi PA et al. Interferon beta use and disability prevention in relapsing-remitting multiple sclerosis. JAMA Neurol. 70(2)248251 (2013).
  • Derfuss T, Kappos L. Evaluating the potential benefit of interferon treatment in multiple sclerosis. JAMA 308(3), 290–291 (2012).
  • Goodin DS, Reder AT, Cutter G. Treatment with interferon beta for multiple sclerosis. JAMA 308(16), 1627–1628 (2012).
  • Farrell RA, Giovannoni G. Measuring and management of anti-interferon beta antibodies in subjects with multiple sclerosis. Mult. Scler. 13(5), 567–577 (2007).
  • Francis GS, Rice GP, Alsop JC; PRISMS Study Group. Interferon beta-1a in MS: results following development of neutralizing antibodies in PRISMS. Neurology 65(1), 48–55 (2005).
  • Kappos L, Clanet M, Sandberg-Wollheim M et al. European Interferon Beta-1a im. Dose-Comparison Study Investigators. Neutralizing antibodies and efficacy of interferon beta-1a: a 4-year controlled study. Neurology 65(1), 40–47 (2005).
  • Freedman MS, Francis GS, Sanders EA et al. University of British Columbia MS/MRI Research Group. Randomized study of once-weekly interferon beta-1la therapy in relapsing multiple sclerosis: three-year data from the OWIMS study. Mult. Scler. 11(1), 41–45 (2005).
  • Knobler RL, Greenstein JI, Johnson KP et al. Systemic recombinant human interferon-beta treatment of relapsing-remitting multiple sclerosis: pilot study analysis and six-year follow-up. J. Interferon Res. 13(5), 333–340 (1993).
  • Clerico M, Faggiano F, Palace J, Rice G, Tintorè M, Durelli L. Recombinant interferon beta or glatiramer acetate for delaying conversion of the first demyelinating event to multiple sclerosis. Cochrane Database Syst. Rev. (2), CD005278 (2008).
  • Rudick RA, Cutter G, Baier M et al. Use of the Multiple Sclerosis Functional Composite to predict disability in relapsing MS. Neurology 56(5), 1324–1330 (2001).
  • Bermel RA, You X, Foulds P et al. Predictors of long-term outcome in multiple sclerosis patients treated with interferon beta. Ann. Neurol. 73(1), 95–103 (2013).
  • Kragt JJ, Thompson AJ, Montalban X et al. Responsiveness and predictive value of EDSS and MSFC in primary progressive MS. Neurology 70(13 Pt. 2), 1084–1091 (2008).
  • Sormani MP, Bonzano L, Roccatagliata L, Mancardi GL, Uccelli A, Bruzzi P. Surrogate endpoints for EDSS worsening in multiple sclerosis. A meta-analytic approach. Neurology 75(4), 302–309 (2010).
  • Rudick RA, Kappos L. Measuring disability in relapsing-remitting MS. Neurology 75(4), 296–297 (2010).
  • Comi G. Shifting the paradigm toward earlier treatment of multiple sclerosis with interferon beta. Clin. Ther. 31(6), 1142–1157 (2009).
  • Richards RG, Sampson FC, Beard SM, Tappenden P. A review of the natural history and epidemiology of multiple sclerosis: implications for resource allocation and health economic models. Health Technol. Assess. 6(10), 1–73 (2002).
  • Grima DT, Torrance GW, Francis G, Rice G, Rosner AJ, Lafortune L. Cost and health related quality of life consequences of multiple sclerosis. Mult. Scler. 6(2), 91–98 (2000).
  • Fisher E, Rudick RA, Simon JH et al. Eight-year follow-up study of brain atrophy in patients with MS. Neurology 59(9), 1412–1420 (2002).
  • Cadavid D, Wolansky LJ, Skurnick J et al. Efficacy of treatment of MS with IFNbeta-1b or glatiramer acetate by monthly brain MRI in the BECOME study. Neurology 72(23), 1976–1983 (2009).
  • Lukas C, Minneboo A, de Groot V et al. Early central atrophy rate predicts 5 year clinical outcome in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 81(12), 1351–1356 (2010).
  • 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. 59(4), 597–605 (2006).
  • Río J, Castilló J, Rovira A et al. Measures in the first year of therapy predict the response to interferon beta in MS. Mult. Scler. 15(7), 848–853 (2009).
  • Horakova D, Kalincik T, Dolezal O et al. Early predictors of non-response to interferon in multiple sclerosis. Acta Neurol. Scand. 126(6), 390–397 (2012).
  • Sämann PG, Knop M, Golgor E, Messler S, Czisch M, Weber F. Brain volume and diffusion markers as predictors of disability and short-term disease evolution in multiple sclerosis. AJNR Am. J. Neuroradiol. 33(7), 1356–1362 (2012).
  • Giorgio A, Stromillo ML, Bartolozzi ML et al. Relevance of hypointense brain MRI lesions for long-term worsening of clinical disability in relapsing multiple sclerosis. Mult. Scler. doi:10.1177/1352458513494490 (2013) ( Epub ahead of print).
  • Lavorgna L, Bonavita S, Ippolito D et al. Clinical and magnetic resonance imaging predictors of disease progression in multiple sclerosis: a nine-year follow-up study. Mult. Scler. doi:10.1177/1352458513494958 (2013) ( Epub ahead of print).
  • Brex PA, Ciccarelli O, O’Riordan JI, Sailer M, Thompson AJ, Miller DH. A longitudinal study of abnormalities on MRI and disability from multiple sclerosis. N. Engl. J. Med. 346(3), 158–164 (2002).
  • Vaneckova M, Kalincik T, Krasensky J et al. Corpus callosum atrophy—a simple predictor of multiple sclerosis progression: a longitudinal 9-year study. Eur. Neurol. 68(1), 23–27 (2012).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.