link.springer.com

An updated histological classification system for multiple sclerosis lesions - Acta Neuropathologica

  • ️Lassmann, Hans
  • ️Sat Dec 17 2016

References

  1. Absinta M, Nair G, Sati P, Cortese IC, Filippi M, Reich DS (2015) Direct MRI detection of impending plaque development in multiple sclerosis. Neurol Neuroimmunol Neuroinflamm 2:e145

    Article  PubMed  PubMed Central  Google Scholar 

  2. Albert M, Antel J, Bruck W, Stadelmann C (2007) Extensive cortical remyelination in patients with chronic multiple sclerosis. Brain Pathol 17:129–138

    Article  PubMed  Google Scholar 

  3. Alvarez JI, Saint-Laurent O, Godschalk A, Terouz S, Briels C, Larouche S, Bourbonniere L, Larochelle C, Prat A (2015) Focal disturbances in the blood-brain barrier are associated with formation of neuroinflammatory lesions. Neurobiol Dis 74:14–24

    Article  CAS  PubMed  Google Scholar 

  4. Barnett MH, Prineas JW (2004) Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann Neurol 55:458–468

    Article  PubMed  Google Scholar 

  5. Bo L, Mork S, Kong PA, Nyland H, Pardo CA, Trapp BD (1994) Detection of MHC class II-antigens on macrophages and microglia, but not on astrocytes and endothelia in active multiple sclerosis lesions. J Neuroimmunol 51:135–146

    Article  CAS  PubMed  Google Scholar 

  6. Bo L, Vedeler CA, Nyland H, Trapp BD, Mork SJ (2003) Intracortical multiple sclerosis lesions are not associated with increased lymphocyte infiltration. Mult Scler 9:323–331

    Article  CAS  PubMed  Google Scholar 

  7. Bo L, Vedeler CA, Nyland HI, Trapp BD, Mork SJ (2003) Subpial demyelination in the cerebral cortex of multiple sclerosis patients. J Neuropathol Exp Neurol 62:723–732

    Article  PubMed  Google Scholar 

  8. Bogie JF, Stinissen P, Hendriks JJ (2014) Macrophage subsets and microglia in multiple sclerosis. Acta Neuropathol 128:191–213

    Article  CAS  PubMed  Google Scholar 

  9. Bramow S, Frischer JM, Lassmann H, Koch-Henriksen N, Lucchinetti CF, Sorensen PS, Laursen H (2010) Demyelination versus remyelination in progressive multiple sclerosis. Brain 133:2983–2998

    Article  PubMed  Google Scholar 

  10. Brink BP, Veerhuis R, Breij EC, van der Valk P, Dijkstra CD, Bö L (2005) The pathology of multiple sclerosis is location-dependent: no significant complement activation is detected in purely cortical lesions. J Neuropathol Exp Neurol 64: 147–155

    Article  CAS  PubMed  Google Scholar 

  11. Brück W, Porada P, Poser S, Rieckmann P, Hanefeld F, Kretzschmar HA, Lassmann H (1995) Monocyte/macrophage differentiation in early multiple sclerosis lesions. Ann Neurol 38:788–796

    Article  PubMed  Google Scholar 

  12. Buss A, Brook GA, Kakulas B, Martin D, Franzen R, Schoenen J, Noth J, Schmitt AB (2004) Gradual loss of myelin and formation of an astrocytic scar during Wallerian degeneration in the human spinal cord. Brain 127:34–44

    Article  CAS  PubMed  Google Scholar 

  13. Butovsky O, Jedrychowski MP, Moore CS, Cialic R, Lanser AJ, Gabriely G, Koeglsperger T, Dake B, Wu PM, Doykan CE et al (2014) Identification of a unique TGF-beta-dependent molecular and functional signature in microglia. Nat Neurosci 17:131–143

    Article  CAS  PubMed  Google Scholar 

  14. Calabrese M, Magliozzi R, Ciccarelli O, Geurts JJ, Reynolds R, Martin R (2015) Exploring the origins of grey matter damage in multiple sclerosis. Nat Rev Neurosci 16:147–158. doi:10.1038/nrn3900

    Article  CAS  PubMed  Google Scholar 

  15. Campbell Z, Sahm D, Donohue K, Jamison J, Davis M, Pellicano C, Auh S, Ohayon J, Frank JA, Richert N et al (2012) Characterizing contrast-enhancing and re-enhancing lesions in multiple sclerosis. Neurology 78:1493–1499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Davie CA, Hawkins CP, Barker GJ, Brennan A, Tofts PS, Miller DH, McDonald WI (1994) Serial proton magnetic resonance spectroscopy in acute multiple sclerosis lesions. Brain 117:49–58

    Article  PubMed  Google Scholar 

  17. De Groot CJA, Bergers E, Kamphorst W, Ravid R, Polman CH, Barkhof F, van der Valk P (2001) Post-mortem MRI-guided sampling of multiple sclerosis brain lesions. Increased yield of active demyelinating and (p)reactive lesions. Brain 124:1635–1645

    Article  PubMed  Google Scholar 

  18. Dendrou CA, Fugger L, Friese MA (2015) Immunopathology of multiple sclerosis. Nat Rev Immunol 15:545–558. doi:10.1038/nri3871

    Article  CAS  PubMed  Google Scholar 

  19. Dziedzic T, Metz I, Dallenga T, Konig FB, Muller S, Stadelmann C, Bruck W (2010) Wallerian degeneration: a major component of early axonal pathology in multiple sclerosis. Brain Pathol 20:976–985

    PubMed  Google Scholar 

  20. Filippi M, Rocca MA, Martino G, Horsfield MA, Comi G (1998) Magnetization transfer changes in the normal appearing white matter precede the appearance of enhancing lesions in patients with multiple sclerosis. Ann Neurol 43:809–814

    Article  CAS  PubMed  Google Scholar 

  21. Fischer MT, Wimmer I, Hoftberger R, Gerlach S, Haider L, Zrzavy T, Hametner S, Mahad D, Binder CJ, Krumbholz M et al (2013) Disease-specific molecular events in cortical multiple sclerosis lesions. Brain 136:1799–1815. doi:10.1093/brain/awt110

    Article  PubMed  PubMed Central  Google Scholar 

  22. Frischer JM, Bramow S, Dal-Bianco A, Lucchinetti CF, Rauschka H, Schmidbauer M, Laursen H, Sorensen PS, Lassmann H (2009) The relation between inflammation and neurodegeneration in multiple sclerosis brains. Brain 132:1175–1189

    Article  PubMed  PubMed Central  Google Scholar 

  23. Frischer JM, Weigand SD, Guo Y, Kale N, Parisi JE, Pirko I, Mandrekar J, Bramow S, Metz I, Bruck W et al (2015) Clinical and pathological insights into the dynamic nature of the white matter multiple sclerosis plaque. Ann Neurol. 78:710–721

    Article  PubMed  PubMed Central  Google Scholar 

  24. Goldschmidt T, Antel J, Konig FB, Brück W, Kuhlmann T (2009) Remyelination capacity of the MS brain decreases with disease chronicity. Neurology 72:1914–1921

    Article  CAS  PubMed  Google Scholar 

  25. Hametner S, Wimmer I, Haider L, Pfeifenbring S, Bruck W, Lassmann H (2013) Iron and neurodegeneration in the multiple sclerosis brain. Ann Neurol 74:848–861. doi:10.1002/ana.23974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Harris JO, Frank JA, Patronas N, McFarlin DE, McFarland HF (1991) Serial gadolinium-enhancing magnetic resonance imaging scans in patients with early, relapsing-remitting multiple sclerosis: implications for clinical trials and natural history. Ann Neurol 29:548–555

    Article  CAS  PubMed  Google Scholar 

  27. Hoftberger R, Fink S, Aboul-Enein F, Botond G, Olah J, Berki T, Ovadi J, Lassmann H, Budka H, Kovacs GG (2010) Tubulin polymerization promoting protein (TPPP/p25) as a marker for oligodendroglial changes in multiple sclerosis. Glia 58:1847–1857. doi:10.1002/glia.21054

    Article  PubMed  Google Scholar 

  28. Kuhlmann T, Miron V, Cui Q, Wegner C, Antel J, Brück W (2008) Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 131:1749–1758

    Article  CAS  PubMed  Google Scholar 

  29. Kuhlmann T, Remington L, Maruschak B, Owens T, Bruck W (2007) Nogo-A is a reliable oligodendroglial marker in adult human and mouse CNS and in demyelinated lesions. J Neuropathol Exp Neurol 66:238–246

    Article  CAS  PubMed  Google Scholar 

  30. Kutzelnigg A, Lucchinetti CF, Stadelmann C, Brück W, Rauschka H, Bergmann M, Schmidbauer M, Parisi JE, Lassmann H (2005) Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain 128:2705–2712

    Article  PubMed  Google Scholar 

  31. Lassmann H, Bruck W, Lucchinetti CF (2007) The immunopathology of multiple sclerosis: an overview. Brain Pathol 17:210–218. doi:10.1111/j.1750-3639.2007.00064.x

    Article  PubMed  Google Scholar 

  32. Lassmann H, Raine CS, Antel J, Prineas JW (1998) Immunopathology of multiple sclerosis: report on an international meeting held at the Institute of Neurology of the University of Vienna. J Neuroimmunol 86:213–217

    Article  CAS  PubMed  Google Scholar 

  33. Lucchinetti C, Brück W, Parisi J, Scheithauer B, Rodriguez M, Lassmann H (2000) Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination. Ann Neurol 47:707–717

    Article  CAS  PubMed  Google Scholar 

  34. Ludwin SK (2000) The neuropathology of multiple sclerosis. Neuroimaging Clin N Am 10:625–648

    CAS  PubMed  Google Scholar 

  35. Ludwin SK (2006) The pathogenesis of multiple sclerosis: relating human pathology to experimental studies. J Neuropathol Exp Neurol 65:305–318

    Article  PubMed  Google Scholar 

  36. Maggi P, Macri SM, Gaitan MI, Leibovitch E, Wholer JE, Knight HL, Ellis M, Wu T, Silva AC, Massacesi L et al (2014) The formation of inflammatory demyelinated lesions in cerebral white matter. Ann Neurol 76:594–608

    Article  PubMed  PubMed Central  Google Scholar 

  37. Mahad DH, Trapp BD, Lassmann H (2015) Pathological mechanisms in progressive multiple sclerosis. Lancet Neurol 14:183–193

    Article  CAS  PubMed  Google Scholar 

  38. Manrique-Hoyos N, Jurgens T, Gronborg M, Kreutzfeldt M, Schedensack M, Kuhlmann T, Schrick C, Bruck W, Urlaub H, Simons M et al (2012) Late motor decline after accomplished remyelination: impact for progressive multiple sclerosis. Ann Neurol 71:227–244

    Article  PubMed  Google Scholar 

  39. Marik C, Felts PA, Bauer J, Lassmann H, Smith KJ (2007) Lesion genesis in a subset of patients with multiple sclerosis: a role for innate immunity? Brain 130:2800–2815. doi:10.1093/brain/awm236

    Article  PubMed  PubMed Central  Google Scholar 

  40. Mews I, Bergmann M, Bunkowski S, Gullotta F, Brück W (1998) Oligodendrocyte and axon pathology in clinically silent multiple sclerosis lesions. Mult Scler 4:55–62

    Article  CAS  PubMed  Google Scholar 

  41. Moll NM, Rietsch AM, Ransohoff AJ, Cossoy MB, Huang D, Eichler FS, Trapp BD, Ransohoff RM (2008) Cortical demyelination in PML and MS: similarities and differences. Neurology 70:336–343. doi:10.1212/01.WNL.0000284601.54436.e4

    Article  CAS  PubMed  Google Scholar 

  42. Moore CS, Ase AR, Kinsara A, Rao VT, Michell-Robinson M, Leong SY, Butovsky O, Ludwin SK, Seguela P, Bar-Or A et al (2015) P2Y12 expression and function in alternatively activated human microglia. Neurol Neuroimmunol Neuroinflamm 2:e80

    Article  PubMed  PubMed Central  Google Scholar 

  43. Patani R, Balaratnam M, Vora A, Reynolds R (2007) Remyelination can be extensive in multiple sclerosis despite a long disease course. Neuropathol Appl Neurobiol 33:277–287

    Article  CAS  PubMed  Google Scholar 

  44. Patrikios P, Stadelmann C, Kutzelnigg A, Rauschka H, Schmidtbauer M, Laursen H, Sorensen P, Brück W, Lucchinetti C, Lassmann H (2006) Remyelination is extensive in a subset of multiple sclerosis patients. Brain 129:3165–3172

    Article  PubMed  Google Scholar 

  45. Peterson JW, Bö L, Mörk S, Chang A, Trapp BD (2001) Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann Neurol 50:389–400

    Article  CAS  PubMed  Google Scholar 

  46. Prineas JW (1985) The neuropathology of multiple sclerosis. In: Koetsier JC (ed) Demyelinating Diseases. Elsevier Science Publishers, Amsterdam, pp 213–257

  47. Prineas JW, Barnard RO, Kwon EE, Sharer LR, Cho ES (1993) Multiple Sclerosis: remyelination of nascent lesions. Ann Neurol 33:137–151

    Article  CAS  PubMed  Google Scholar 

  48. Prineas JW, Connell F (1979) Remyelination in multiple sclerosis. Ann Neurol 5:22–31

    Article  CAS  PubMed  Google Scholar 

  49. Prineas JW, Kwon EE, Cho E-S, Sharer LR, Barnett MH, Oleszak EL, Hoffman B, Morgan BP (2001) Immunopathology of secondary-progressive multiple sclerosis. Ann Neurol 50:646–657

    Article  CAS  PubMed  Google Scholar 

  50. Prineas JW, Kwon EE, Cho ES, Sharer LR (1984) Continual breakdown and regeneration of myelin in progressive multiple sclerosis plaques. Ann N Y Acad Sci 436:11–32

    Article  CAS  PubMed  Google Scholar 

  51. Prineas JW, McDonald I, Franklin RJM (2002) Demyelinating diseases. In: Graham D, Lantos PL (eds) Greenfield’s Neuropathology, 7th edn. Arnold, London, p 527–528

  52. Reynolds R, Roncaroli F, Nicholas R, Radotra B, Gveric D, Howell O (2011) The neuropathological basis of clinical progression in multiple sclerosis. Acta Neuropathol 122:155–170. doi:10.1007/s00401-011-0840-0

    Article  PubMed  Google Scholar 

  53. Singh S, Metz I, Amor S, van der Valk P, Stadelmann C, Brück W (2013) Microglial nodules in early multiple sclerosis white matter are associated with degenerating axons. Acta Neuropathol 125:595–608

    Article  Google Scholar 

  54. Thompson AJ, Kermode AG, Wicks D, MacManus DG, Kendall BE, Kingsley DP, McDonald WI (1991) Major differences in the dynamics of primary and secondary progressive multiple sclerosis. Ann Neurol 29:53–62

    Article  CAS  PubMed  Google Scholar 

  55. Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mork S, Bo L (1998) Axonal transection in the lesions of multiple sclerosis. New Engl J Med 338:278–285

    Article  CAS  PubMed  Google Scholar 

  56. van der Goes A, Boorsma W, Hoekstra K, Montagne L, De Groot CJ, Dijkstra CD (2005) Determination of the sequential degradation of myelin proteins by macrophages. J Neuroimmunol 161:12–20

    Article  PubMed  Google Scholar 

  57. van der Valk P, De Groot CJA (2000) Review. Staging of multiple sclerosis (MS) lesions: pathology of the time frame of MS. Neuropathol Appl Neurobiol 26:2–10

    Article  PubMed  Google Scholar 

  58. van Horssen J, Singh S, van der Pol S, Kipp M, Lim JL, Peferoen L, Gerritsen W, Kooi EJ, Witte ME, Geurts JJ et al (2012) Clusters of activated microglia in normal-appearing white matter show signs of innate immune activation. J Neuroinflammation 9:156. doi:10.1186/1742-2094-9-156

    PubMed  PubMed Central  Google Scholar 

  59. van Waesberghe JHTM, Kamphorst W, De Groot CJA, van Walderveen MAA, Castelijns JA, Ravid R, van der Valk P, Polman CH, Thompson AJ, Barkhof F (1999) Axonal loss in multiple sclerosis lesions: magnetic resonance imaging insights into substrates of disability. Ann Neurol 46:747–754

    Article  PubMed  Google Scholar 

  60. Yamasaki R, Lu H, Butovsky O, Ohno N, Rietsch AM, Cialic R, Wu PM, Doykan CE, Lin J, Cotleur AC et al (2014) Differential roles of microglia and monocytes in the inflamed central nervous system. J Exp Med 211:1533–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references