Experts forum

Advances in clinical diagnosis of secondary progressive multiple sclerosis

Expand
  • Department of Neurology, Tianjin Medical University General Hospital, Tianjin 300052, China

Received date: 2022-10-03

  Online published: 2023-04-23

Abstract

Multiple sclerosis(MS) is a chronic inflammatory disease of the central nervous system that involves demyelination and axonal degeneration. Usually, MS begins with a relapsing-remitting MS (RRMS) course, and approxi mately will develop into secondary progressive multiple sclerosis (SPMS). At present, the pathogenesis of SPMS is not completely clear, but studies have shown that the occurrence of SPMS is related to the slowly expanding lesions in the central nervous system, leptomeningeal follicle-like structure, chronic inflammation and brain atrophy. In clinical practice, the diagnosis of SPMS is often delayed and retrospective. Up to two-thirds of patients with insidious worsening of disability are still considered to have RRMS. These patients may continue to receive disease-modifying therapies for RRMS, which may not be effective for slowing SPMS. Therefore, early identification and diagnosis of SPMS are essential for their treatment.

Cite this article

ZHANG Chao, GAO Xue . Advances in clinical diagnosis of secondary progressive multiple sclerosis[J]. Journal of Diagnostics Concepts & Practice, 2022 , 21(06) : 669 -676 . DOI: 10.16150/j.1671-2870.2022.06.002

References

[1] Inojosa H, Proschmann U, Akgün K, et al. A focus on secondary progressive multiple sclerosis (SPMS): challenges in diagnosis and definition[J]. J Neurol, 2021, 268(4):1210-1221.
[2] Weinshenker B G, Bass B, Rice G P, et al. The natural history of multiple sclerosis: a geographically based study. I. Clinical course and disability[J]. Brain, 1989, 112 (Pt 1):133-146.
[3] Healy L M, Stratton J A, Kuhlmann T, et al. The role of glial cells in multiple sclerosis disease progression[J]. Nat Rev Neurol, 2022, 18(4):237-248.
[4] Yong H Y F, Yong V W. Mechanism-based criteria to improve therapeutic outcomes in progressive multiple sclerosis[J]. Nat Rev Neurol, 2022, 18(1):40-55.
[5] Lassmann H, van Horssen J, Mahad D. Progressive multiple sclerosis: pathology and pathogenesis[J]. Nat Rev Neurol, 2012, 8(11):647-656.
[6] Correale J, Gaitán M I, Ysrraelit M C, et al. Progressive multiple sclerosis: from pathogenic mechanisms to treatment[J]. Brain, 2017, 140(3):527-546.
[7] Oki S. Eomes-expressing T-helper cells as potential target of therapy in chronic neuroinflammation[J]. Neurochem Int, 2019, 130:104348.
[8] Peruzzotti-Jametti L, Willis C M, Hamel R, et al. Metabolic Control of Smoldering Neuroinflammation[J]. Front Immunol, 2021, 12:705920.
[9] J?ckle K, Zeis T, Schaeren-Wiemers N, et al. Molecular signature of slowly expanding lesions in progressive multiple sclerosis[J]. Brain, 2020, 143(7):2073-2088.
[10] Dal-Bianco A, Grabner G, Kronnerwetter C, et al. Slow expansion of multiple sclerosis iron rim lesions: pathology and 7 T magnetic resonance imaging[J]. Acta Neuropathol, 2017, 133(1):25-42.
[11] Gillen K M, Mubarak M, Nguyen T D, et al. Significance and In Vivo Detection of Iron-Laden Microglia in White Matter Multiple Sclerosis Lesions[J]. Front Immunol, 2018, 9:255.
[12] Mehta V, Pei W, Yang G, et al. Iron is a sensitive biomarker for inflammation in multiple sclerosis lesions[J]. PLoS One, 2013, 8(3):e57573.
[13] Popescu B F, Frischer J M, Webb S M, et al. Pathogenic implications of distinct patterns of iron and zinc in chronic MS lesions[J]. Acta Neuropathol, 2017, 134(1):45-64.
[14] Lassmann H. Targets of therapy in progressive MS[J]. Mult Scler, 2017, 23(12):1593-1599.
[15] Choi I Y, Lee P, Adany P, et al. In vivo evidence of oxi-dative stress in brains of patients with progressive multiple sclerosis[J]. Mult Scler, 2018, 24(8):1029-1038.
[16] Rawji K S, Gonzalez Martinez G A, Sharma A, et al. The Role of Astrocytes in Remyelination[J]. Trends Neurosci, 2020, 43(8):596-607.
[17] Faissner S, Plemel J R, Gold R, et al. Progressive multiple sclerosis: from pathophysiology to therapeutic strategies[J]. Nat Rev Drug Discov, 2019, 18(12):905-922.
[18] Reali C, Magliozzi R, Roncaroli F, et al. B cell rich meningeal inflammation associates with increased spinal cord pathology in multiple sclerosis[J]. Brain Pathol, 2020, 30(4):779-793.
[19] Lassmann H. Pathogenic Mechanisms Associated With Different Clinical Courses of Multiple Sclerosis[J]. Front Immunol, 2019, 9:3116.
[20] Magliozzi R, Howell O, Vora A, et al. Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology[J]. Brain, 2007, 130(Pt 4):1089-1104.
[21] Serafini B, Rosicarelli B, Magliozzi R, et al. Detection of ectopic B-cell follicles with germinal centers in the meninges of patients with secondary progressive multiple sclerosis[J]. Brain Pathol, 2004, 14(2):164-174.
[22] Aloisi F, Serafini B, Magliozzi R, et al. Detection of Epstein-Barr virus and B-cell follicles in the multiple sclerosis brain: what you find depends on how and where you look[J]. Brain, 2010, 133(Pt 12):e157.
[23] Moccia M, Haider L, Eshaghi A, et al. B Cells in the CNS at Postmortem Are Associated With Worse Outcome and Cell Types in Multiple Sclerosis[J]. Neurol Neuroimmunol Neuroinflamm, 2021, 9(1):e1108.
[24] Gardner C, Magliozzi R, Durrenberger P F, et al. Cortical grey matter demyelination can be induced by elevated pro-inflammatory cytokines in the subarachnoid space of MOG-immunized rats[J]. Brain, 2013, 136(Pt 12):3596-3608.
[25] Raveney B J E, Sato W, Takewaki D, et al. Involvement of cytotoxic Eomes-expressing CD4+ T cells in secondary progressive multiple sclerosis[J]. Proc Natl Acad Sci U S A, 2021, 118(11):e2021818118.
[26] Raveney B J, Oki S, Hohjoh H, et al. Eomesodermin-expressing T-helper cells are essential for chronic neuroinflammation[J]. Nat Commun, 2015, 6:8437.
[27] Levite M. Glutamate, T cells and multiple sclerosis[J]. J Neural Transm (Vienna), 2017, 124(7):775-798.
[28] Scalfari A, Neuhaus A, Daumer M, et al. Onset of secondary progressive phase and long-term evolution of multiple sclerosis[J]. J Neurol Neurosurg Psychiatry, 2014, 85(1):67-75.
[29] Ciron J, Gueguen A, Al K A, et al. Secondary progressive multiple sclerosis: A national consensus paper on diagnostic criteria[J]. Rev Neurol (Paris), 2022.
[30] Katz S I, Krieger S, Farrell C, et al. Diagnostic uncertainty during the transition to secondary progressive multiple sclerosis[J]. Mult Scler, 2014, 20(12):1654-1657.
[31] Rojas J I, Patrucco L, Alonso R, et al. Diagnostic uncertainty during the transition to secondary progressive multiple sclerosis: Multicenter study in Argentina[J]. Mult Scler, 2021, 27(4):579-584.
[32] Cree B, Hollenbach J A, Bove R, et al. Silent progression in disease activity-free relapsing multiple sclerosis[J]. Ann Neurol, 2019, 85(5):653-666.
[33] Lorscheider J, Buzzard K, Jokubaitis V, et al. Defining secondary progressive multiple sclerosis[J]. Brain, 2016, 139(Pt 9):2395-2405.
[34] Filippi M, Preziosa P, Langdon D, et al. Identifying Progression in Multiple Sclerosis: New Perspectives[J]. Ann Neurol, 2020, 88(3):438-452.
[35] Magliozzi R, Fadda G, Brown R A, et al. "Ependymal-in" Gradient of Thalamic Damage in Progressive Multiple Sclerosis[J]. Ann Neurol, 2022, 92(4):670-685.
[36] Kapoor R, Smith K E, Allegretta M, et al. Serum neurofilament light as a biomarker in progressive multiple sclerosis[J]. Neurology, 2020, 95(10):436-444.
[37] H?gel H, Rissanen E, Barro C, et al. Serum glial fibrillary acidic protein correlates with multiple sclerosis disease severity[J]. Mult Scler, 2020, 26(2):210-219.
[38] Filippi M, Preziosa P, Barkhof F, et al. Diagnosis of Progressive Multiple Sclerosis From the Imaging Perspective: A Review[J]. JAMA Neurol, 2021, 78(3):351-364.
[39] Klineova S, Lublin F D. Clinical Course of Multiple Sclerosis[J]. Cold Spring Harb Perspect Med, 2018, 8(9).
[40] Preziosa P, Pagani E, Meani A, et al. Slowly Expanding Lesions Predict 9-Year Multiple Sclerosis Disease Progression[J]. Neurol Neuroimmunol Neuroinflamm, 2022, 9(2).
[41] Dal-Bianco A, Grabner G, Kronnerwetter C, et al. Long-term evolution of multiple sclerosis iron rim lesions in 7 T MRI[J]. Brain, 2021, 144(3):833-847.
[42] Ontaneda D. Progressive Multiple Sclerosis[J]. Continuum (Minneap Minn), 2019, 25(3):736-752.
[43] Genovese A V, Hagemeier J, Bergsland N, et al. Atrophied Brain T2 Lesion Volume at MRI Is Associated with Disability Progression and Conversion to Secondary Progressive Multiple Sclerosis[J]. Radiology, 2019, 293(2):424-433.
[44] Sucksdorff M, Matilainen M, Tuisku J, et al. Brain TSPO-PET predicts later disease progression independent of relapses in multiple sclerosis[J]. Brain, 2020, 143(11):3318-3330.
[45] Cree B, Arnold D L, Chataway J, et al. Secondary Progressive Multiple Sclerosis: New Insights[J]. Neurology, 2021, 97(8):378-388.
[46] Nylund M, Sucksdorff M, Matilainen M, et al. Phenotyping of multiple sclerosis lesions according to innate immune cell activation using 18 kDa translocator protein-PET[J]. Brain Commun, 2022, 4(1):b301.
[47] Varhaug K N, Torkildsen ?, Myhr K M, et al. Neurofilament Light Chain as a Biomarker in Multiple Sclerosis[J]. Front Neurol, 2019, 10:338.
[48] Kuhle J, Barro C, Andreasson U, et al. Comparison of three analytical platforms for quantification of the neurofilament light chain in blood samples: ELISA, electrochemiluminescence immunoassay and Simoa[J]. Clin Chem Lab Med, 2016, 54(10):1655-1661.
[49] Comabella M, Sastre-Garriga J, Carbonell-Mirabent P, et al. Serum neurofilament light chain levels predict long-term disability progression in patients with progressive multiple sclerosis[J]. J Neurol Neurosurg Psychiatry, 2022.
[50] Edwards K R, Kamath A, Button J, et al. A pharmacokinetic and biomarker study of delayed-release dimethyl fumarate in subjects with secondary progressive multiple sclerosis: evaluation of cerebrospinal fluid penetration and the effects on exploratory biomarkers[J]. Mult Scler Relat Disord, 2021, 51:102861.
[51] Barro C, Benkert P, Disanto G, et al. Serum neurofilament as a predictor of disease worsening and brain and spinal cord atrophy in multiple sclerosis[J]. Brain, 2018, 141(8):2382-2391.
[52] Salzer J, Svenningsson A, Sundstr?m P. Neurofilament light as a prognostic marker in multiple sclerosis[J]. Mult Scler, 2010, 16(3):287-292.
[53] Sun M, Liu N, Xie Q, et al. A candidate biomarker of glial fibrillary acidic protein in CSF and blood in differentiating multiple sclerosis and its subtypes: A systematic review and meta-analysis[J]. Mult Scler Relat Disord, 2021, 51:102870.
[54] Groen K, Lechner-Scott J, Pohl D, et al. Can serum glial fibrillary acidic protein(GFAP) solve the longstanding problem of diagnosis and monitoring progressive multiple sclerosis[J]. Mult Scler Relat Disord, 2021, 50:102931.
[55] Saraste M, Bezukladova S, Matilainen M, et al. Increased serum glial fibrillary acidic protein associates with microstructural white matter damage in multiple sclerosis: GFAP and DTI[J]. Mult Scler Relat Disord, 2021, 50:102810.
[56] Choi I Y, Lee P, Hughes A J, et al. Longitudinal changes of cerebral glutathione(GSH) levels associated with the clinical course of disease progression in patients with secondary progressive multiple sclerosis[J]. Mult Scler, 2017, 23(7):956-962.
[57] Cristofanilli M, Gratch D, Pagano B, et al. Transglutaminase-6 is an autoantigen in progressive multiple sclerosis and is upregulated in reactive astrocytes[J]. Mult Scler, 2017, 23(13):1707-1715.
Outlines

/