Epidemiology of Progressive Multiple Sclerosis

Chapter

Abstract

Since the earliest clinical descriptions of multiple sclerosis (MS), it has been recognised that a minority of patients experience slow accumulation, or progression of disability from onset of disease [1]: this phenotype is now commonly termed primary progressive MS (PPMS). However, more commonly patients go on to develop progression only following an initial period of relapses; this is referred to as secondary progressive disease (SPMS) [2]. These two distinct phases of relapses and progression are now thought to reflect the dual pathological processes of neuroinflammation and neurodegeneration which, in part, give rise to the wide clinical phenotype of MS [3]. Although our understanding of MS has made significant advances in recent years, there remains no single definitive diagnostic test or biomarker which accurately reflects the underlying disease process or biology, and as a result our ability to identify and quantify disease progression remains limited [2]. As we enter a new treatment era for MS, including the advent of clinical trials in progressive disease, epidemiological studies remain important in providing insights into the biology and evolution of disability in primary and secondary MS and are also key to the planning of successful interventional studies.

References

  1. 1.
    Charcot J. Lectures on the diseases of the nervous system (chapter). In: Disseminated sclerosis: its symptomatology. London: New Sydenham Society; 1877. p. 209–17.Google Scholar
  2. 2.
    Lublin FD, Reingold SC, Cohen JA, et al. Defining the clinical course of multiple sclerosis: the 2013 revisions. Neurology. 2014;83(3):278–86.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Compston A, Coles A. Multiple sclerosis. Lancet. 2008;372(9648):1502–17.CrossRefPubMedGoogle Scholar
  4. 4.
    Andersson PB, Waubant E, Gee L, Goodkin DE. Multiple sclerosis that is progressive from the time of onset: clinical characteristics and progression of disability. Arch Neurol. 1999;56(9):1138–42.CrossRefPubMedGoogle Scholar
  5. 5.
    Leray E, Yaouanq J, Le Page E, et al. Evidence for a two-stage disability progression in multiple sclerosis. Brain. 2010;133(7):1900–13.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Minderhoud JM, van der Hoeven JH, Prange AJ. Course and prognosis of chronic progressive multiple sclerosis. Results of an epidemiological study. Acta Neurol Scand. 1988;78(1):10–5.CrossRefPubMedGoogle Scholar
  7. 7.
    Phadke JG. Clinical aspects of multiple sclerosis in north-east Scotland with particular reference to its course and prognosis. Brain. 1990;113(6):1597–628.CrossRefPubMedGoogle Scholar
  8. 8.
    Runmarker B, Andersen O. Prognostic factors in a multiple sclerosis incidence cohort with twenty-five years of follow-up. Brain. 1993;116(1):117–34.CrossRefPubMedGoogle Scholar
  9. 9.
    McDonnell G, Hawkins S. An epidemiologic study of multiple sclerosis in Northern Ireland. Neurology. 1998;50(2):423–8.CrossRefPubMedGoogle Scholar
  10. 10.
    Cottrell DA, Kremenchutzky M, Rice GP, et al. The natural history of multiple sclerosis: a geographically based study. 5. The clinical features and natural history of primary progressive multiple sclerosis. Brain. 1999;122(4):625–39.CrossRefPubMedGoogle Scholar
  11. 11.
    Tremlett H, Paty D, Devonshire V. The natural history of primary progressive MS in British Columbia, Canada. Neurology. 2005;65(12):1919–23.CrossRefPubMedGoogle Scholar
  12. 12.
    Confavreux C, Vukusic S. Natural history of multiple sclerosis: a unifying concept. Brain. 2006;129(3):606–16.CrossRefPubMedGoogle Scholar
  13. 13.
    Debouverie M, Louis S, Pittion-Vouyovitch S, Roederer T, Vespignani H. Multiple sclerosis with a progressive course from onset in Lorraine-Eastern France. J Neurol. 2007;254(10):1370–5.CrossRefPubMedGoogle Scholar
  14. 14.
    Koch M, Mostert J, Heersema D, De Keyser J. Progression in multiple sclerosis: further evidence of an age dependent process. J Neurol Sci. 2007;255(1–2):35–41.CrossRefPubMedGoogle Scholar
  15. 15.
    Maghzi AH, Etemadifar M, Saadatnia M. Clinical and demographical characteristics of primary progressive multiple sclerosis in Isfahan, Iran. Eur J Neurol. 2007;14(4):403–7.CrossRefPubMedGoogle Scholar
  16. 16.
    Koch M, Kingwell E, Rieckmann P, Tremlett H. The natural history of primary progressive multiple sclerosis. Neurology. 2009;73(23):1996–2002.CrossRefPubMedGoogle Scholar
  17. 17.
    Harding KE, Wardle M, Moore P, et al. Modelling the natural history of primary progressive multiple sclerosis. J Neurol Neurosurg Psychiatry. 2014;86(1):13–9.CrossRefPubMedGoogle Scholar
  18. 18.
    Jena S, Alexander M, Aaron S, et al. Natural history of multiple sclerosis from the Indian perspective: experience from a tertiary care hospital. Neurol India. 2015;63:866–73.CrossRefPubMedGoogle Scholar
  19. 19.
    Piccolo L, Kumar G, Nakashima I, et al. Multiple sclerosis in Japan appears to be a milder disease compared to the UK. J Neurol. 2015;262(4):831–6.CrossRefPubMedGoogle Scholar
  20. 20.
    Lublin FD, Reingold SC. Defining the clinical course of multiple sclerosis: results of an international survey. National Multiple Sclerosis Society (USA) advisory committee on clinical trials of new agents in multiple sclerosis. Neurology. 1996;46(4):907–11.CrossRefPubMedGoogle Scholar
  21. 21.
    Debouverie M, Laforest L, Van Ganse E, Guillemin F. Earlier disability of the patients followed in multiple sclerosis centers compared to outpatients. Mult Scler. 2008;15(2):251–7.CrossRefGoogle Scholar
  22. 22.
    Weinshenker BG, Bass B, Rice GP, et al. The natural history of multiple sclerosis: a geographically based study. 1. Clinical course and disability. Brain. 1989;112(1):133–46.CrossRefPubMedGoogle Scholar
  23. 23.
    Stankoff B, Mrejen S, Tourbah A, et al. Age at onset determines the occurrence of the progressive phase of multiple sclerosis. Neurology. 2007;68(10):779–81.CrossRefPubMedGoogle Scholar
  24. 24.
    McDonnell G, Hawkins S. Clinical study of primary progressive multiple sclerosis in Northern Ireland. J Neurol Neurosurg Psychiatry. 1998;64(4):451–4.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Ribbons KA, McElduff P, Boz C, et al. Male sex is independently associated with faster disability accumulation in relapse-onset MS but not in primary progressive MS. PLoS One. 2015;10(6):e0122,686. published online. http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0122686 CrossRefGoogle Scholar
  26. 26.
    Simone IL, Carrara D, Tortorella C, et al. Course and prognosis in early-onset MS: comparison with adult-onset forms. Neurology. 2002;59(12):1922–8.CrossRefPubMedGoogle Scholar
  27. 27.
    Boiko A, Vorobeychik G, Paty D, Devonshire V, Sadovnick D, University of British Columbia MS Clinic Neurologists. Early onset multiple sclerosis: a longitudinal study. Neurology. 2002;59(7):1006–10.CrossRefPubMedGoogle Scholar
  28. 28.
    Harding KE, Liang K, Cossburn MD, et al. Long-term outcome of paediatric-onset multiple sclerosis: a population-based study. J Neurol Neurosurg Psychiatry. 2013;84(2):141–7.CrossRefPubMedGoogle Scholar
  29. 29.
    Renoux C, Vukusic S, Mikaeloff Y, et al. Natural history of multiple sclerosis with childhood onset. N Engl J Med. 2007;356(25):2603–13.CrossRefPubMedGoogle Scholar
  30. 30.
    Delalande S, Seze JD, Ferriby D, Stojkovic T, Vermersch P. Late onset multiple sclerosis. Rev Neurol (Paris). 2002;158(11):1082–7.Google Scholar
  31. 31.
    Tremlett H, Devonshire V. Is late-onset multiple sclerosis associated with a worse outcome? Neurology. 2006;67(6):954–9.CrossRefPubMedGoogle Scholar
  32. 32.
    Cossburn M, Ingram G, Hirst C, Ben-Shlomo Y, Pickersgill T, Robertson N. Age at onset as a determinant of presenting phenotype and initial relapse recovery in multiple sclerosis. Mult Scler J. 2012;18(1):45–54.CrossRefGoogle Scholar
  33. 33.
    Kremenchutzky M, Cottrell D, Rice G, et al. The natural history of multiple sclerosis: a geographically based study 7. Progressive-relapsing and relapsing-progressive multiple sclerosis: a re-evaluation. Brain. 1999;122(10):1941–50.CrossRefPubMedGoogle Scholar
  34. 34.
    Confavreux C, Vukusic S. Age at disability milestones in multiple sclerosis. Brain. 2006;129(3):595–605.CrossRefPubMedGoogle Scholar
  35. 35.
    Phadke JG. Survival pattern and cause of death in patients with multiple sclerosis: results from an epidemiological survey in north east Scotland. J Neurol Neurosurg Psychiatry. 1987;50(5):523–31.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Leray E, Morrissey S, Yaouanq J, et al. Long-term survival of patients with multiple sclerosis in west France. Mult Scler J. 2007;13(7):865–74.CrossRefGoogle Scholar
  37. 37.
    Grytten Torkildsen N, Lie S, Aarseth J, Nyland H, Myhr K. Survival and cause of death in multiple sclerosis: results from a 50-year follow-up in western Norway. Mult Scler J. 2008;14(9):1191–8.CrossRefGoogle Scholar
  38. 38.
    Smestad C, Sandvik L, Celius E. Excess mortality and cause of death in a cohort of Norwegian multiple sclerosis patients. Mult Scler. 2009;15(11):1263–70.CrossRefPubMedGoogle Scholar
  39. 39.
    Hader WJ. Disability and survival of multiple sclerosis in Saskatoon, Saskatchewan. Can J Neurol Sci. 2010;37(1):28–35.CrossRefPubMedGoogle Scholar
  40. 40.
    Kingwell E, van der Kop M, Zhao Y, et al. Relative mortality and survival in multiple sclerosis: findings from British Columbia, Canada. J Neurol Neurosurg Psychiatry. 2012;83(1):61–6.CrossRefPubMedGoogle Scholar
  41. 41.
    Leray E, Vukusic S, Debouverie M, et al., 2015, Excess mortality in patients with multiple sclerosis starts at 20 years from clinical onset: data from a large-scale French observational study. PLoS One, 10(7): e0132,033. Published online.  10.1371/journal.pone.0132033
  42. 42.
    Jick SS, Li L, Falcone GJ, Vassilev ZP, Wallander MA. Epidemiology of multiple sclerosis: results from a large observational study in the UK. J Neurol. 2015;262(9):2033–41.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Sandi D, Zsiros V, Fvesi J, et al. Mortality in Hungarian patients with multiple sclerosis between 1993 and 2013. J Neurol Sci. 2016;367:329–32.CrossRefPubMedGoogle Scholar
  44. 44.
    Koch MW, Greenfield J, Javizian O, Deighton S, Wall W, Metz LM. The natural history of early versus late disability accumulation in primary progressive MS. J Neurol Neurosurg Psychiatry. 2014;86(6):615–21.CrossRefPubMedGoogle Scholar
  45. 45.
    Bergamaschi R, Berzuini C, Romani A, Cosi V. Predicting secondary progression in relapsing-remitting multiple sclerosis: a Bayesian analysis. J Neurol Sci. 2001;189(1–2):13–21.CrossRefPubMedGoogle Scholar
  46. 46.
    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 J. 2003;9(3):260–74.CrossRefGoogle Scholar
  47. 47.
    Kremenchutzky M, Rice GPA, Baskerville J, Wingerchuk DM, Ebers GC. The natural history of multiple sclerosis: a geographically based study 9: observations on the progressive phase of the disease. Brain. 2006;129(3):584–94.CrossRefPubMedGoogle Scholar
  48. 48.
    Koch M, De Keyser J, Tremlett H. Timing of birth and disease progression in multiple sclerosis. Mult Scler. 2008;14(6):793–8.CrossRefPubMedGoogle Scholar
  49. 49.
    Tedeholm H, Skoog B, Lisovskaja V, Runmarker B, Nerman O, Andersen O. The outcome spectrum of multiple sclerosis: disability, mortality, and a cluster of predictors from onset. J Neurol. 2015;262(5):1148–63.CrossRefPubMedGoogle Scholar
  50. 50.
    Manouchehrinia A, Beiki O, Hillert J. Clinical course of multiple sclerosis: a nationwide cohort study. Mult Scler J. 2016:1352458516681197. doi: 10.1177/1352458516681197. [Epub ahead of print]
  51. 51.
    Vukusic S, Confavreux C. Prognostic factors for progression of disability in the secondary progressive phase of multiple sclerosis. J Neurol Sci. 2003;206(2):135–7.CrossRefPubMedGoogle Scholar
  52. 52.
    Lorscheider J, Buzzard K, Jokubaitis V, et al. Defining secondary progressive multiple sclerosis. Brain. 2016;139(9):2395–405.CrossRefPubMedGoogle Scholar
  53. 53.
    Tremlett H, Zhao Y, Devonshire V. Natural history of secondary-progressive multiple sclerosis. Mult Scler J. 2008;14(3):314–24.CrossRefGoogle Scholar
  54. 54.
    Skoog B, Tedeholm H, Runmarker B, Odn A, Andersen O. Continuous prediction of secondary progression in the individual course of multiple sclerosis. Mult Scler Rel Disord. 2014;3(5):584–92.CrossRefGoogle Scholar
  55. 55.
    Tremlett H, Yousefi M, Devonshire V, Rieckmann P, Zhao Y. Impact of multiple sclerosis relapses on progression diminishes with time. Neurology. 2009;73(20):1616–23.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Tremlett H, Zhao Y, Devonshire V. Natural history comparisons of primary and secondary progressive multiple sclerosis reveals differences and similarities. J Neurol. 2009;256(3):374–81.CrossRefPubMedGoogle Scholar
  57. 57.
    Scalfari A, Lederer C, Daumer M, Nicholas R, Ebers G, Muraro P. The relationship of age with the clinical phenotype in multiple sclerosis. Mult Scler J. 2016;22(13):1750–8.CrossRefGoogle Scholar
  58. 58.
    Robertson NP, Clayton D, Fraser M, Deans J, Compston DA. Clinical concordance in sibling pairs with multiple sclerosis. Neurology. 1996;47(2):347–52.CrossRefPubMedGoogle Scholar
  59. 59.
    Oturai AB, Ryder LP, Fredrikson S, et al. Concordance for disease course and age of onset in Scandinavian multiple sclerosis coaffected sib pairs. Mult Scler. 2004;10(1):5–8.PubMedGoogle Scholar
  60. 60.
    Hensiek AE, Seaman SR, Barcellos LF, et al. Familial effects on the clinical course of multiple sclerosis. Neurology. 2007;68(5):376–83.CrossRefPubMedGoogle Scholar
  61. 61.
    Koch M, Zhao Y, Yee I, et al. Disease onset in familial and sporadic primary progressive multiple sclerosis. Mult Scler J. 2010;16(6):694–700.CrossRefGoogle Scholar
  62. 62.
    Koch M, Uyttenboogaart M, Heerings M, Heersema D, Mostert J, De Keyser J. Progression in familial and nonfamilial MS. Mult Scler J. 2008;14(3):300–6.CrossRefGoogle Scholar
  63. 63.
    Ebers GC, Koopman WJ, Hader W, et al. The natural history of multiple sclerosis: a geographically based study. 8. Familial multiple sclerosis. Brain. 2000;123(3):641–9.CrossRefPubMedGoogle Scholar
  64. 64.
    IMSGC. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature. 2011;476(7359):214–9.CrossRefGoogle Scholar
  65. 65.
    Montalban X, Hauser SL, Kappos L, et al. Ocrelizumab versus placebo in primary progressive multiple sclerosis. N Engl J Med. 2017;376(3):209–20.CrossRefPubMedGoogle Scholar
  66. 66.
    CAMMS223 Trial Investigators, Coles AJ, Compston DAS, et al. Alemtuzumab vs. interferon beta-1a in early multiple sclerosis. N Engl J Med. 2008;359(17):1786–801.CrossRefGoogle Scholar
  67. 67.
    Cottrell DA, Kremenchutzky M, Rice GP, Hader W, Baskerville J, Ebers GC. The natural history of multiple sclerosis: a geographically based study. 6. Applications to planning and interpretation of clinical therapeutic trials in primary progressive multiple sclerosis. Brain. 1999;122(4):641–7.CrossRefPubMedGoogle Scholar
  68. 68.
    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. 2013;12:857–65.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  1. 1.Institute of Psychological Medicine and Clinical NeuroscienceCardiff University, University Hospital of WalesCardiffUK

Personalised recommendations