. 2015 Mar;14(2).
doi: 10.1016/S1474-4422(14)70264-9.

Clinical trials in progressive multiple sclerosis: lessons learned and future perspectives

Daniel Ontaneda 1 Robert J Fox 2 Jeremy Chataway 3 
  • PMID: 25772899
  •     141 References
  •     64 citations


Progressive multiple sclerosis is characterised clinically by the gradual accrual of disability independent of relapses and can occur with disease onset (primary progressive) or can be preceded by a relapsing disease course (secondary progressive). An effective disease-modifying treatment for progressive multiple sclerosis has not yet been identified, and so far the results of clinical trials have generally been disappointing. Ongoing advances in the knowledge of pathogenesis, in the identification of novel targets for neuroprotection, and in improved outcome measures could lead to effective treatments for progressive multiple sclerosis. In this Series paper, we summarise the lessons learned from completed clinical trials and perspectives from trials in progress in progressive multiple sclerosis. We review promising clinical, imaging, and biological markers, along with novel designs, for clinical trials. The use of more refined outcomes and truly neuroprotective drugs, coupled with more efficient trial design, has the capacity to deliver a new era of therapeutic discovery in this challenging area.

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Neurology, 2010 Mar 05; 74(13). PMID: 20200338
Effect of high-dose simvastatin on brain atrophy and disability in secondary progressive multiple sclerosis (MS-STAT): a randomised, placebo-controlled, phase 2 trial.
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Lancet, 2014 Mar 25; 383(9936). PMID: 24655729
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The Multiple Sclerosis Impact Scale (MSIS-29): a new patient-based outcome measure.
J Hobart, D Lamping, +2 authors, A Thompson.
Brain, 2001 May 04; 124(Pt 5). PMID: 11335698
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Cortical surface-based analysis. I. Segmentation and surface reconstruction.
A M Dale, B Fischl, M I Sereno.
Neuroimage, 1999 Feb 05; 9(2). PMID: 9931268
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Treatment of secondary progressive multiple sclerosis with the immunomodulator linomide: a double-blind, placebo-controlled pilot study with monthly magnetic resonance imaging evaluation.
D M Karussis, Z Meiner, +4 authors, O Abramsky.
Neurology, 1996 Aug 01; 47(2). PMID: 8757002
Markers for different glial cell responses in multiple sclerosis: clinical and pathological correlations.
A Petzold, M J Eikelenboom, +8 authors, G Giovannoni.
Brain, 2002 Jun 22; 125(Pt 7). PMID: 12076997
The multiple sclerosis functional composite: a new clinical outcome measure for multiple sderosis trials.
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Mult Scler, 2002 Oct 03; 8(5). PMID: 12356200
Revisiting brain atrophy and its relationship to disability in multiple sclerosis.
Navid Shiee, Pierre-Louis Bazin, +8 authors, Daniel S Reich.
PLoS One, 2012 May 23; 7(5). PMID: 22615886    Free PMC article.
Comorbidity, socioeconomic status and multiple sclerosis.
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Mult Scler, 2008 Aug 30; 14(8). PMID: 18728060
Development of biomarkers for multiple sclerosis as a neurodegenerative disorder.
Ulf Ziemann, Mathias Wahl, Elke Hattingen, Hayrettin Tumani.
Prog Neurobiol, 2011 Apr 29; 95(4). PMID: 21524682
A comparison of health utility measures for the evaluation of multiple sclerosis treatments.
J D Fisk, M G Brown, +3 authors, K J Stadnyk.
J Neurol Neurosurg Psychiatry, 2004 Dec 21; 76(1). PMID: 15607996    Free PMC article.
Intravenous synthetic peptide MBP8298 delayed disease progression in an HLA Class II-defined cohort of patients with progressive multiple sclerosis: results of a 24-month double-blind placebo-controlled clinical trial and 5 years of follow-up treatment.
K G Warren, I Catz, L Z Ferenczi, M J Krantz.
Eur J Neurol, 2006 Aug 02; 13(8). PMID: 16879301
More multiarm randomised trials of superiority are needed.
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Lancet, 2014 Jul 30; 384(9940). PMID: 25066148
Outcome measures for multiple sclerosis clinical trials: relative measurement precision of the Expanded Disability Status Scale and Multiple Sclerosis Functional Composite.
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Mult Scler, 2004 Feb 06; 10(1). PMID: 14760951
Retinal nerve fiber layer thickness, brain atrophy, and disability in multiple sclerosis patients.
Jose Manuel Abalo-Lojo, Carmen Carollo Limeres, +4 authors, Francisco Gonzalez.
J Neuroophthalmol, 2013 Oct 29; 34(1). PMID: 24162258
Longitudinal changes in diffusion tensor-based quantitative MRI in multiple sclerosis.
D M Harrison, B S Caffo, +6 authors, D S Reich.
Neurology, 2011 Jan 12; 76(2). PMID: 21220722    Free PMC article.
Relationship between brain atrophy and disability: an 8-year follow-up study of multiple sclerosis patients.
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Mult Scler, 2001 Feb 24; 6(6). PMID: 11212131
Differential diagnosis of suspected multiple sclerosis: a consensus approach.
D H Miller, B G Weinshenker, +15 authors, C H Polman.
Mult Scler, 2008 Sep 23; 14(9). PMID: 18805839    Free PMC article.
Highly Cited.
Cortical atrophy is relevant in multiple sclerosis at clinical onset.
Massimiliano Calabrese, Matteo Atzori, +9 authors, Paolo Gallo.
J Neurol, 2007 Mar 16; 254(9). PMID: 17361339
Gaps Between Aims and Achievements in Therapeutic Modification of Neuronal Damage ("Neuroprotection").
Heinz Wiendl, Christian Elger, +4 authors, Stefan Schwab.
Neurotherapeutics, 2015 Mar 17; 12(2). PMID: 25773662    Free PMC article.
The immunogenetics of multiple sclerosis: A comprehensive review.
Jill A Hollenbach, Jorge R Oksenberg.
J Autoimmun, 2015 Jul 05; 64. PMID: 26142251    Free PMC article.
Highly Cited. Review.
Risk Mitigation Strategies for Adverse Reactions Associated with the Disease-Modifying Drugs in Multiple Sclerosis.
Adnan M Subei, Daniel Ontaneda.
CNS Drugs, 2015 Sep 27; 29(9). PMID: 26407624    Free PMC article.
Sharing data from MS clinical trials: Opportunities, challenges, and future directions.
Timothy Coetzee.
Mult Scler, 2015 Oct 07; 21(11). PMID: 26438302    Free PMC article.
Synaptopathy connects inflammation and neurodegeneration in multiple sclerosis.
Georgia Mandolesi, Antonietta Gentile, +6 authors, Diego Centonze.
Nat Rev Neurol, 2015 Nov 21; 11(12). PMID: 26585978
Brain and cord myelin water imaging: a progressive multiple sclerosis biomarker.
Shannon Kolind, Arshia Seddigh, +9 authors, Peter A Brex.
Neuroimage Clin, 2015 Nov 26; 9. PMID: 26594633    Free PMC article.
Therapeutic Advances and Future Prospects in Progressive Forms of Multiple Sclerosis.
Afsaneh Shirani, Darin T Okuda, Olaf Stüve.
Neurotherapeutics, 2016 Jan 06; 13(1). PMID: 26729332    Free PMC article.
Exploring potential mechanisms of action of natalizumab in secondary progressive multiple sclerosis.
Finn Sellebjerg, Diego Cadavid, +3 authors, Daniel Mikol.
Ther Adv Neurol Disord, 2016 Jan 21; 9(1). PMID: 26788129    Free PMC article.
Multiple sclerosis: Fingolimod failure in progressive MS INFORMS future trials.
Andrew L Smith, Jeffrey A Cohen.
Nat Rev Neurol, 2016 Mar 30; 12(5). PMID: 27020561
Decision making under uncertainty, therapeutic inertia, and physicians' risk preferences in the management of multiple sclerosis (DIScUTIR MS).
Gustavo Saposnik, Angel Perez Sempere, +3 authors, Jorge Maurino.
BMC Neurol, 2016 May 06; 16. PMID: 27146451    Free PMC article.
Secondary Progressive Multiple Sclerosis: Definition and Measurement.
Domenico Plantone, Floriana De Angelis, Anisha Doshi, Jeremy Chataway.
CNS Drugs, 2016 May 12; 30(6). PMID: 27166830
Development of a Sensitive Outcome for Economical Drug Screening for Progressive Multiple Sclerosis Treatment.
Peter Kosa, Danish Ghazali, +11 authors, Bibiana Bielekova.
Front Neurol, 2016 Aug 31; 7. PMID: 27574516    Free PMC article.
Measuring Brain Tissue Integrity during 4 Years Using Diffusion Tensor Imaging.
D Ontaneda, K Sakaie, +4 authors, R J Fox.
AJNR Am J Neuroradiol, 2016 Sep 24; 38(1). PMID: 27659189    Free PMC article.
A Personalized Approach in Progressive Multiple Sclerosis: The Current Status of Disease Modifying Therapies (DMTs) and Future Perspectives.
Emanuele D'Amico, Francesco Patti, Aurora Zanghì, Mario Zappia.
Int J Mol Sci, 2016 Oct 21; 17(10). PMID: 27763513    Free PMC article.
Free serum haemoglobin is associated with brain atrophy in secondary progressive multiple sclerosis.
Alex Lewin, Shea Hamilton, +4 authors, Charles R M Bangham.
Wellcome Open Res, 2016 Dec 21; 1. PMID: 27996064    Free PMC article.
Nogo-A Antibodies for Progressive Multiple Sclerosis.
Benjamin V Ineichen, Patricia S Plattner, +3 authors, Martin E Schwab.
CNS Drugs, 2017 Jan 21; 31(3). PMID: 28105588
Pharmacological Approaches to the Management of Secondary Progressive Multiple Sclerosis.
A Nandoskar, J Raffel, +2 authors, R S Nicholas.
Drugs, 2017 Apr 22; 77(8). PMID: 28429241
Cerebellar volume as imaging outcome in progressive multiple sclerosis.
Matilde Inglese, Maria Petracca, +8 authors, Maria Pia Sormani.
PLoS One, 2017 Apr 25; 12(4). PMID: 28437430    Free PMC article.
Volume versus surface-based cortical thickness measurements: A comparative study with healthy controls and multiple sclerosis patients.
R Righart, P Schmidt, +8 authors, M Mühlau.
PLoS One, 2017 Jul 07; 12(7). PMID: 28683072    Free PMC article.
Patient-reported outcomes and survival in multiple sclerosis: A 10-year retrospective cohort study using the Multiple Sclerosis Impact Scale-29.
Joel Raffel, Alison Wallace, +3 authors, Richard Nicholas.
PLoS Med, 2017 Jul 12; 14(7). PMID: 28692670    Free PMC article.
Neuroprotection by eIF2α-CHOP inhibition and XBP-1 activation in EAE/optic neuritiss.
Haoliang Huang, Linqing Miao, +8 authors, Yang Hu.
Cell Death Dis, 2017 Jul 21; 8(7). PMID: 28726788    Free PMC article.
Anti-inflammatory disease-modifying treatment and short-term disability progression in SPMS.
Johannes Lorscheider, Vilija G Jokubaitis, +26 authors, MSBase Study Group.
Neurology, 2017 Aug 11; 89(10). PMID: 28794248    Free PMC article.
Organotypic Cultures from the Adult CNS: A Novel Model to Study Demyelination and Remyelination Ex Vivo.
Glaiza A Tan, Kendra L Furber, +3 authors, Adil J Nazarali.
Cell Mol Neurobiol, 2017 Aug 11; 38(1). PMID: 28795301
Automated segmentation of cerebral deep gray matter from MRI scans: effect of field strength on sensitivity and reliability.
Renxin Chu, Shelley Hurwitz, Shahamat Tauhid, Rohit Bakshi.
BMC Neurol, 2017 Sep 07; 17(1). PMID: 28874119    Free PMC article.
Advancing trial design in progressive multiple sclerosis.
Robert J Fox, Jeremy Chataway.
Mult Scler, 2017 Oct 19; 23(12). PMID: 29041871    Free PMC article.
Spotlight on siponimod and its potential in the treatment of secondary progressive multiple sclerosis: the evidence to date.
Alberto Gajofatto.
Drug Des Devel Ther, 2017 Nov 16; 11. PMID: 29138536    Free PMC article.
Discriminative ability of quality of life measures in multiple sclerosis.
Kirsten M Fiest, Jamie Greenfield, +3 authors, Ruth Ann Marrie.
Health Qual Life Outcomes, 2017 Dec 23; 15(1). PMID: 29268750    Free PMC article.
Cognitive phenotypes in multiple sclerosis.
Victoria M Leavitt, Gabriella Tosto, Claire S Riley.
J Neurol, 2018 Jan 23; 265(3). PMID: 29356970
Sleep-Disordered Breathing in People with Multiple Sclerosis: Prevalence, Pathophysiological Mechanisms, and Disease Consequences.
Hanna A Hensen, Arun V Krishnan, Danny J Eckert.
Front Neurol, 2018 Jan 31; 8. PMID: 29379466    Free PMC article.
Progressive multiple sclerosis, cognitive function, and quality of life.
Helene Højsgaard Chow, Karen Schreiber, +6 authors, Finn Sellebjerg.
Brain Behav, 2018 Feb 28; 8(2). PMID: 29484253    Free PMC article.
Therapeutic Inertia in the New Landscape of Multiple Sclerosis Care.
Gustavo Saposnik, Xavier Montalban.
Front Neurol, 2018 Apr 05; 9. PMID: 29615967    Free PMC article.
Disease-Modifying Treatment in Progressive Multiple Sclerosis.
John Robert Ciotti, Anne Haney Cross.
Curr Treat Options Neurol, 2018 Apr 09; 20(5). PMID: 29627873
Identification of brain antigens recognized by autoantibodies in experimental autoimmune encephalomyelitis-induced animals treated with etomoxir or interferon-β.
Anne Skøttrup Mørkholt, Kenneth Kastaniegaard, +6 authors, John Dirk Nieland.
Sci Rep, 2018 May 08; 8(1). PMID: 29728570    Free PMC article.
CSF inflammatory biomarkers responsive to treatment in progressive multiple sclerosis capture residual inflammation associated with axonal damage.
Jeppe Romme Christensen, Mika Komori, +4 authors, Finn Sellebjerg.
Mult Scler, 2018 May 19; 25(7). PMID: 29775134    Free PMC article.
Pharmacotherapy in Secondary Progressive Multiple Sclerosis: An Overview.
Floriana De Angelis, Domenico Plantone, Jeremy Chataway.
CNS Drugs, 2018 Jul 04; 32(6). PMID: 29968175
Modeling Approaches in Cost-Effectiveness Analysis of Disease-Modifying Therapies for Relapsing-Remitting Multiple Sclerosis: An Updated Systematic Review and Recommendations for Future Economic Evaluations.
Luis Hernandez, Malinda O'Donnell, Maarten Postma.
Pharmacoeconomics, 2018 Jul 05; 36(10). PMID: 29971666
Systematic Review.
Multiple Sclerosis-Secondary Progressive Multi-Arm Randomisation Trial (MS-SMART): a multiarm phase IIb randomised, double-blind, placebo-controlled clinical trial comparing the efficacy of three neuroprotective drugs in secondary progressive multiple sclerosis.
Peter Connick, Floriana De Angelis, +22 authors, UK Multiple Sclerosis Society Clinical Trials Network.
BMJ Open, 2018 Sep 01; 8(8). PMID: 30166303    Free PMC article.
Targeting phosphocreatine metabolism in relapsing-remitting multiple sclerosis: evaluation with brain MRI, 1H and 31P MRS, and clinical and cognitive testing.
Melissa Cambron, Tatjana Reynders, +4 authors, Guy Laureys.
J Neurol, 2018 Sep 07; 265(11). PMID: 30187159
Short-term disability progression in two multiethnic multiple sclerosis centers in the treatment era.
Ilya Kister, Tamar E Bacon, Gary R Cutter.
Ther Adv Neurol Disord, 2018 Sep 15; 11. PMID: 30214486    Free PMC article.
Connexin 30 Deficiency Attenuates Chronic but Not Acute Phases of Experimental Autoimmune Encephalomyelitis Through Induction of Neuroprotective Microglia.
Mei Fang, Ryo Yamasaki, +5 authors, Jun-Ichi Kira.
Front Immunol, 2018 Nov 23; 9. PMID: 30464764    Free PMC article.
Two Sides to Every Story: Perspectives from Four Patients and a Healthcare Professional on Multiple Sclerosis Disease Progression.
Jeri Burtchell, Kristen Fetty, +2 authors, Daniel Kantor.
Neurol Ther, 2019 Jul 06; 8(2). PMID: 31273563    Free PMC article.
Diagnosis and Management of Progressive Multiple Sclerosis.
Gabrielle Macaron, Daniel Ontaneda.
Biomedicines, 2019 Aug 01; 7(3). PMID: 31362384    Free PMC article.
Suggestions for improving the design of clinical trials in multiple sclerosis-results of a systematic analysis of completed phase III trials.
Sinje Gehr, Thomas Kaiser, +2 authors, Friedemann Paul.
EPMA J, 2019 Dec 14; 10(4). PMID: 31832116    Free PMC article.
Clinical and MRI efficacy of sc IFN β-1a tiw in patients with relapsing MS appearing to transition to secondary progressive MS: post hoc analyses of PRISMS and SPECTRIMS.
Mark S Freedman, Staley Brod, +4 authors, Patricia K Coyle.
J Neurol, 2019 Sep 29; 267(1). PMID: 31559532    Free PMC article.
Efficacy of three neuroprotective drugs in secondary progressive multiple sclerosis (MS-SMART): a phase 2b, multiarm, double-blind, randomised placebo-controlled trial.
Jeremy Chataway, Floriana De Angelis, +22 authors, MS-SMART Investigators.
Lancet Neurol, 2020 Jan 26; 19(3). PMID: 31981516    Free PMC article.
Biochemical Differences in Cerebrospinal Fluid between Secondary Progressive and Relapsing⁻Remitting Multiple Sclerosis.
Stephanie Herman, Torbjörn Åkerfeldt, +2 authors, Kim Kultima.
Cells, 2019 Jan 27; 8(2). PMID: 30678351    Free PMC article.
The Enigmatic Role of Viruses in Multiple Sclerosis: Molecular Mimicry or Disturbed Immune Surveillance?
Jens Geginat, Moira Paroni, +4 authors, Sergio Abrignani.
Trends Immunol, 2017 May 28; 38(7). PMID: 28549714    Free PMC article.
Is It Possible to Conduct a Multi-Arm Multi-Stage Platform Trial in Parkinson's Disease: Lessons Learned from Other Neurodegenerative Disorders and Cancer.
Marie-Louise Zeissler, Vivien Li, Mahesh K B Parmar, Camille Buchholz Carroll.
J Parkinsons Dis, 2020 Mar 03; 10(2). PMID: 32116263    Free PMC article.
Is Exercise Training Beneficial in Progressive Multiple Sclerosis?
Lara A Pilutti, Thomas A Edwards.
Int J MS Care, 2017 Mar 01; 19(2). PMID: 32607069    Free PMC article.
Gaining First Insights on Secondary Progressive Multiple Sclerosis Patients Treated With Siponimod in Clinical Routine: Protocol of the Noninterventional Study AMASIA.
Tjalf Ziemssen, Olaf Hoffmann, +3 authors, Benedict Rauser.
JMIR Res Protoc, 2020 Jun 06; 9(7). PMID: 32499214    Free PMC article.
Single-cell mass cytometry reveals complex myeloid cell composition in active lesions of progressive multiple sclerosis.
Chotima Böttcher, Marlijn van der Poel, +10 authors, Josef Priller.
Acta Neuropathol Commun, 2020 Aug 20; 8(1). PMID: 32811567    Free PMC article.
Use and cost of disease-modifying therapies by Sonya Slifka Study participants: has anything really changed since 2000 and 2009?
Sarah L Minden, R Philip Kinkel, +3 authors, Lisa I Iezzoni.
Mult Scler J Exp Transl Clin, 2019 Mar 01; 5(1). PMID: 30815276    Free PMC article.
Glial Activation Markers in CSF and Serum From Patients With Primary Progressive Multiple Sclerosis: Potential of Serum GFAP as Disease Severity Marker?
Ahmed Abdelhak, Tilman Hottenrott, +8 authors, André Huss.
Front Neurol, 2019 Apr 12; 10. PMID: 30972011    Free PMC article.
Can We Treat Secondary Progressive Multiple Sclerosis Now?
Rohit Bhatia, Nishita Singh.
Ann Indian Acad Neurol, 2019 Apr 23; 22(2). PMID: 31007422    Free PMC article.
Dietary Therapy in Secondary Progressive Multiple Sclerosis: A Case Report.
Janak Nathan, Dhanashri Khedekar Kale, +2 authors, Sonal Bailur.
Cureus, 2019 Aug 21; 11(8). PMID: 31428547    Free PMC article.
Use of a symptom-based questionnaire to screen for the presence of significant voiding dysfunction in patients with multiple sclerosis and lower urinary tract symptoms: a pilot study.
Vivien Li, Jalesh N Panicker, Collette Haslam, Jeremy Chataway.
J Neurol, 2020 Jul 17; 267(12). PMID: 32671529    Free PMC article.
Multiple sclerosis, a treatable disease.
Anisha Doshi, Jeremy Chataway.
Clin Med (Lond), 2016 Dec 14; 16(Suppl 6). PMID: 27956442    Free PMC article.
Multiple sclerosis, a treatable disease .
Anisha Doshi, Jeremy Chataway.
Clin Med (Lond), 2017 Dec 03; 17(6). PMID: 29196354    Free PMC article.
Response to ibudilast treatment according to progressive multiple sclerosis disease phenotype.
Andrew D Goodman, Janel K Fedler, +10 authors, SPRINT-MS Investigators.
Ann Clin Transl Neurol, 2021 Jan 19; 8(1). PMID: 33460301    Free PMC article.
Predictors of Health Utility in Relapsing-Remitting and Secondary-Progressive Multiple Sclerosis: Implications for Future Economic Models of Disease-Modifying Therapies.
Luis Hernandez, Malinda O'Donnell, Maarten Postma, for MSOAC.
Pharmacoeconomics, 2020 Sep 30; 39(2). PMID: 32989685    Free PMC article.
Purinergic Receptors on Oligodendrocyte Progenitors: Promising Targets for Myelin Repair in Multiple Sclerosis?
Davide Lecca, Maria P Abbracchio, Marta Fumagalli.
Front Pharmacol, 2021 Feb 16; 11. PMID: 33584312    Free PMC article.
Cuprizone-Induced Neurotoxicity in Human Neural Cell Lines Is Mediated by a Reversible Mitochondrial Dysfunction: Relevance for Demyelination Models.
Eva Martínez-Pinilla, Núria Rubio-Sardón, +5 authors, Ana Navarro.
Brain Sci, 2021 Mar 07; 11(2). PMID: 33671675    Free PMC article.
Optical coherence tomography outcomes from SPRINT-MS, a multicenter, randomized, double-blind trial of ibudilast in progressive multiple sclerosis.
Robert A Bermel, Janel K Fedler, +12 authors, Robert J Fox.
Mult Scler, 2020 Oct 16;. PMID: 33054533    Free PMC article.
Deciphering Multiple Sclerosis Progression.
Virginia Meca-Lallana, Leticia Berenguer-Ruiz, +7 authors, Francisco Carlos Pérez-Miralles.
Front Neurol, 2021 Apr 27; 12. PMID: 33897583    Free PMC article.