CNS Involvement in Chronic Inflammatory Demyelinating Polyneuropathy: Subtle Retinal Changes in Optical Coherence Tomography
Language English Country United States Media electronic-print
Document type Journal Article
PubMed
34667130
PubMed Central
PMC8529418
DOI
10.1212/nxi.0000000000001099
PII: 9/1/e1099
Knihovny.cz E-resources
- MeSH
- Polyradiculoneuropathy, Chronic Inflammatory Demyelinating diagnostic imaging pathology physiopathology MeSH
- Adult MeSH
- Middle Aged MeSH
- Humans MeSH
- Neural Conduction physiology MeSH
- Tomography, Optical Coherence MeSH
- Prospective Studies MeSH
- Cross-Sectional Studies MeSH
- Retina diagnostic imaging pathology MeSH
- Aged MeSH
- Visual Pathways diagnostic imaging pathology MeSH
- Check Tag
- Adult MeSH
- Middle Aged MeSH
- Humans MeSH
- Male MeSH
- Aged MeSH
- Female MeSH
- Publication type
- Journal Article MeSH
BACKGROUND AND OBJECTIVES: Chronic inflammatory demyelinating polyneuropathy (CIDP) is an autoimmune disease primarily affecting the peripheral nervous system. However, several noncontrolled studies have suggested concomitant inflammatory CNS demyelination similar to multiple sclerosis. The aim of this study was to investigate an involvement of the visual pathway in patients with CIDP. METHODS: In this prospective cross-sectional study, we used high-resolution spectral-domain optical coherence tomography to compare the thickness of the peripapillary retinal nerve fiber layer and the deeper macular retinal layers as well as the total macular volume (TMV) in 22 patients with CIDP and 22 age-matched and sex-matched healthy control (HC) individuals. Retinal layers were semiautomatically segmented by the provided software and were correlated with clinical measures and nerve conduction studies. RESULTS: In patients with CIDP compared with healthy age-matched and sex-matched controls, we found slight but significant volume reductions of the ganglion cell/inner plexiform layer complex (CIDP 1.86 vs HC 1.95 mm3, p = 0.015), the retinal pigment epithelium (CIDP 0.38 vs HC 0.40 mm3, p = 0.02), and the TMV (CIDP 8.48 vs HC 8.75 mm3, p = 0.018). The ganglion cell layer volume and motor nerve conduction velocity were positively associated (B = 0.002, p = 0.02). DISCUSSION: Our data reveal subtle retinal neurodegeneration in patients with CIDP, providing evidence for visual pathway involvement, detectable by OCT. The results need corroboration in independent, larger cohorts.
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Lehmann HC, Burke D, Kuwabara S. Chronic inflammatory demyelinating polyneuropathy: update on diagnosis, immunopathogenesis and treatment. J Neurol Neurosurg Psychiatry. 2019;90(9):981-987. PubMed
Forrester C, Lascelles RG. Association between polyneuritis and multiple sclerosis. J Neurol Neurosurg Psychiatry. 1979;42(9):864-866. PubMed PMC
Thomas PK, Walker RW, Rudge P, et al. . Chronic demyelinating peripheral neuropathy associated with multifocal central nervous system demyelination. Brain. 1987;110(pt 1):53-76. PubMed
Mendell JR, Kolkin S, Kissel JT, Weiss KL, Chakeres DW, Rammohan KW. Evidence for central nervous system demyelination in chronic inflammatory demyelinating polyradiculoneuropathy. Neurology. 1987;37(8):1291-1294. PubMed
Ormerod IE, Waddy HM, Kermode AG, Murray NM, Thomas PK. Involvement of the central nervous system in chronic inflammatory demyelinating polyneuropathy: a clinical, electrophysiological and magnetic resonance imaging study. J Neurol Neurosurg Psychiatry. 1990;53(9):789-793. PubMed PMC
Ohtake T, Komori T, Hirose K, Tanabe H. CNS involvement in Japanese patients with chronic inflammatory demyelinating polyradiculoneuropathy. Acta Neurol Scand. 1990;81(2):108-112. PubMed
Hickman SJ, Allen JA, Baisre A, et al. . Neuro-ophthalmological complications of chronic inflammatory demyelinating polyradiculoneuropathy. Neuroophthalmology. 2013;37(4):146-156. PubMed PMC
Knopp M, Leese RJ, Martin-Lamb D, Rajabally YA. Optic and auditory pathway dysfunction in demyelinating neuropathies. Acta Neurol Scand. 2014;130(1):53-57. PubMed
Takeda M, Tachibana H, Tuda K, Wada S, Kasama S. CNS involvement in chronic inflammatory demyelinating polyneuropathy: a visual evoked potential study. J Neurol Neurophysiol. 2010;1:105-108.
Holtkamp M, Zschenderlein R, Brück W, Weber JR. Chronic inflammatory demyelinating polyradiculoneuropathy with histologically proven optic neuritis. Acta Neuropathol. 2001;101(5):529-531. PubMed
Ogata H, Matsuse D, Yamasaki R, et al. . A nationwide survey of combined central and peripheral demyelination in Japan. J Neurol Neurosurg Psychiatry. 2016;87(1):29-36. PubMed
Wang YQ, Chen H, Zhuang WP, Li HL. The clinical features of combined central and peripheral demyelination in Chinese patients. J Neuroimmunol. 2018;317:32-36. PubMed
Aktas O. Shifting borders, crossing boundaries: the case of combined central and peripheral demyelination. Mult Scler. 2018;24(4):550-551. PubMed
Graf J, Jansen L, Ingwersen J, et al. . Multifocal visual evoked potentials in chronic inflammatory demyelinating polyneuropathy. Ann Clin Transl Neurol. 2018;5(8):952-961. PubMed PMC
Dziadkowiak E, Ejma M, Wieczorek M, et al. . Abnormality of multimodal evoked potentials in chronic inflammatory demyelinating polyradiculoneuropathy (CIDP). Neurol Sci. 2020;41(9):2495-2501. PubMed PMC
Petzold A, Balcer LJ, Calabresi PA, et al. . Retinal layer segmentation in multiple sclerosis: a systematic review and meta-analysis. Lancet Neurol. 2017;16(10):797-812. PubMed
Sotirchos ES, Gonzalez Caldito N, Filippatou A, et al. . Progressive multiple sclerosis is associated with faster and specific retinal layer atrophy. Ann Neurol. 2020;87(6):885-896. PubMed PMC
Pisa M, Guerrieri S, Di Maggio G, et al. . No evidence of disease activity is associated with reduced rate of axonal retinal atrophy in MS. Neurology. 2017;89(24):2469-2475. PubMed
Schneider E, Zimmermann H, Oberwahrenbrock T, et al. . Optical coherence tomography reveals distinct patterns of retinal damage in neuromyelitis optica and multiple sclerosis. PLoS One. 2013;8(6):e66151. PubMed PMC
Cheung CY, Ong YT, Hilal S, et al. . Retinal ganglion cell analysis using high-definition optical coherence tomography in patients with mild cognitive impairment and Alzheimer's disease. J Alzheimers Dis. 2015;45(1):45-56. PubMed
Roth NM, Saidha S, Zimmermann H, et al. . Photoreceptor layer thinning in idiopathic Parkinson's disease. Mov Disord. 2014;29(9):1163-1170. PubMed
Ringelstein M, Albrecht P, Südmeyer M, et al. . Subtle retinal pathology in amyotrophic lateral sclerosis. Ann Clin Transl Neurol. 2014;1(4):290-297. PubMed PMC
Albrecht P, Müller AK, Ringelstein M, et al. . Retinal neurodegeneration in Wilson's disease revealed by spectral domain optical coherence tomography. PLoS One. 2012;7(11):e49825. PubMed PMC
Oertel FC, Havla J, Roca-Fernández A, et al. . Retinal ganglion cell loss in neuromyelitis optica: a longitudinal study. J Neurol Neurosurg Psychiatry. 2018;89(12):1259-1265. PubMed
Lambe J, Fitzgerald KC, Murphy OC, et al. . Association of spectral-domain OCT with long-term disability worsening in multiple sclerosis. Neurology. 2021;96(16):e2058-e2069. PubMed PMC
von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. J Clin Epidemiol. 2008;61(4):344-349. PubMed
Cruz-Herranz A, Balk LJ, Oberwahrenbrock T, et al. . The APOSTEL recommendations for reporting quantitative optical coherence tomography studies. Neurology. 2016;86(24):2303-2309. PubMed PMC
Lee JI, Gemerzki L, Boerker L, et al. . No alteration of optical coherence tomography and multifocal visual evoked potentials in eyes with symptomatic carotid artery disease. Front Neurol. 2019;10:741. PubMed PMC
Tewarie P, Balk L, Costello F, et al. . The OSCAR-IB consensus criteria for retinal OCT quality assessment. PLoS One. 2012;7(4):e34823. PubMed PMC
Balk LJ, Twisk JWR, Steenwijk MD, et al. . A dam for retrograde axonal degeneration in multiple sclerosis? J Neurol Neurosurg Psychiatry. 2014;85(7):782-789. PubMed
Albrecht P, Ringelstein M, Müller AK, et al. . Degeneration of retinal layers in multiple sclerosis subtypes quantified by optical coherence tomography. Mult Scler. 2012;18(10):1422-1429. PubMed
Syc SB, Saidha S, Newsome SD, et al. . Optical coherence tomography segmentation reveals ganglion cell layer pathology after optic neuritis. Brain. 2012;135(pt 2):521-533. PubMed PMC
Oberwahrenbrock T, Ringelstein M, Jentschke S, et al. . Retinal ganglion cell and inner plexiform layer thinning in clinically isolated syndrome. Mult Scler. 2013;19(14):1887-1895. PubMed
Motamedi S, Gawlik K, Ayadi N, et al. . Normative data and minimally detectable change for inner retinal layer thicknesses using a semi-automated OCT image segmentation pipeline. Front Neurol. 2019;10:1117. PubMed PMC
Kupersmith MJ, Garvin MK, Wang JK, Durbin M, Kardon R. Retinal ganglion cell layer thinning within one month of presentation for optic neuritis. Mult Scler. 2016;22(5):641-648. PubMed PMC
Gabilondo I, Martínez-Lapiscina EH, Fraga-Pumar E, et al. . Dynamics of retinal injury after acute optic neuritis. Ann Neurol. 2015;77(3):517-528. PubMed
Saidha S, Al-Louzi O, Ratchford JN, et al. . Optical coherence tomography reflects brain atrophy in multiple sclerosis: a four-year study. Ann Neurol. 2015;78(5):801-813. PubMed PMC
Nolan-Kenney RC, Liu M, Akhand O, et al. . Optimal intereye difference thresholds by optical coherence tomography in multiple sclerosis: an international study. Ann Neurol. 2019;85(5):618-629. PubMed
Aktas O, Hartung H-PCSI. Multiple sclerosis. Tracing optic nerve involvement by standardized optical coherence tomography. Ann Neurol. 2019;85(5):615-617. PubMed
Strauss O. The retinal pigment epithelium in visual function. Physiol Rev. 2005;85(3):845-881. PubMed
Horstmann L, Schmid H, Heinen AP, Kurschus FC, Dick HB, Joachim SC. Inflammatory demyelination induces glia alterations and ganglion cell loss in the retina of an experimental autoimmune encephalomyelitis model. J Neuroinflammation. 2013;10:120. PubMed PMC
Cruz-Herranz A, Dietrich M, Hilla AM, et al. . Monitoring retinal changes with optical coherence tomography predicts neuronal loss in experimental autoimmune encephalomyelitis. J Neuroinflammation. 2019;16:203. PubMed PMC
Manogaran P, Samardzija M, Schad AN, et al. . Retinal pathology in experimental optic neuritis is characterized by retrograde degeneration and gliosis. Acta Neuropathol Commun. 2019;7:116. PubMed PMC
Green AJ, McQuaid S, Hauser SL, Allen IV, Lyness R. Ocular pathology in multiple sclerosis: retinal atrophy and inflammation irrespective of disease duration. Brain. 2010;133(pt 6):1591-1601. PubMed PMC