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November 2021; 8 (6) ArticleOpen Access

Retinal Optical Coherence Tomography in Neuromyelitis Optica

Frederike Cosima Oertel, Svenja Specovius, Hanna G. Zimmermann, View ORCID ProfileClaudia Chien, Seyedamirhosein Motamedi, Charlotte Bereuter, Lawrence Cook, Marco Aurélio Lana Peixoto, Mariana Andrade Fontanelle, View ORCID ProfileHo Jin Kim, View ORCID ProfileJae-Won Hyun, Jacqueline Palace, Adriana Roca-Fernandez, Maria Isabel Leite, Srilakshmi Sharma, Fereshteh Ashtari, Rahele Kafieh, Alireza Dehghani, Mohsen Pourazizi, Lekha Pandit, Anitha D'Cunha, View ORCID ProfileOrhan Aktas, Marius Ringelstein, View ORCID ProfilePhilipp Albrecht, Eugene May, Caryl Tongco, Letizia Leocani, Marco Pisa, Marta Radaelli, View ORCID ProfileElena H. Martinez-Lapiscina, View ORCID ProfileHadas Stiebel-Kalish, Sasitorn Siritho, Jérome de Seze, Thomas Senger, View ORCID ProfileJoachim Havla, Romain Marignier, Alvaro Cobo Calvo, Denis Bichuetti, View ORCID ProfileIvan Maynart Tavares, Nasrin Asgari, Kerstin Soelberg, Ayse Altintas, Rengin Yildirim, View ORCID ProfileUygur Tanriverdi, Anu Jacob, Saif Huda, Zoe Rimler, Allyson Reid, Yang Mao-Draayer, Ibis Soto de Castillo, View ORCID ProfileAxel Petzold, Ari J. Green, View ORCID ProfileMichael R. Yeaman, Terry Smith, View ORCID ProfileAlexander U. Brandt, Friedemann Paul
First published September 15, 2021, DOI: https://doi.org/10.1212/NXI.0000000000001068
Frederike Cosima Oertel
From the Experimental and Clinical Research Center (F.C.O., Svenja Specovius, H.G.Z., C.C., S.M., C.B., A.U.B., F.P.), Max Delbrück Center for Molecular Medicine and Charité–Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Germany: NeuroCure Clinical Research Center (F.C.O., Svenja Specovius, H.G.Z., C.C., S.M., C.B., A.U.B., F.P.), Charité–Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Germany; Department of Neurology (F.C.O., A.J.G.), University of California San Francisco, CA; Department of Pediatrics (L.C.), University of Utah, Salt Lake City; CIEM MS Research Center (M.A.L.P., M.A.F.), University of Minas Gerais, Medical School, Belo Horizonte, Brazil; Department of Neurology (H.J.K., J.-W.H.), National Cancer Center, Goyang, Republic of Korea; Department of Neurology (J.P., A.R.-F., M.I.L.), and Department of Ophthalmology (Srilakshmi Sharma), and Department of Ophthalmology (Srilakshmi Sharma), Oxford University Hospitals, National Health Service Trust, UK; Kashani MS Center (F.A.), School of Advanced Technologies in Medicine and Medical Image and Signal Processing Research Center (R.K.), Department of Ophthalmology, Isfahan Eye Research Center (A.D., Mohsen Pourazizi), Isfahan University of Medical Sciences, Iran; Department of Neurology (L.P., A.D'C.), KS Hegde Medical Academy, Nitte University, Mangalore, India; Department of Neurology (O.A., Marius Ringelstein, P.A.), Medical Faculty, Heinrich Heine University Düsseldorf, Germany; Swedish Neuroscience Institute Neuro-Ophthalmology (E.M., C.T.), Seattle, WA; Experimental Neurophysiology Unit (L.L., Marco Pisa, Marta Radaelli), Institute of Experimental Neurology (INSPE) Scientific Institute Hospital San Raffaele and University Vita-Salute San Raffaele, Milan, Italy; Hospital Clinic of Barcelona-Institut d'Investigacions (E.H.M.-L.), Biomèdiques August Pi Sunyer, (IDIBAPS), Spain; Sackler School of Medicine (H.S.-K.), Tel Aviv University, Israel; Neuro-Ophthalmology Division (H.S.-K.), Department of Ophthalmology, Rabin Medical Center, Petah Tikva, Israel; Division of Neurology (Sasitorn Siritho), Department of Medicine, Siriraj Hospital and Bumrungrad International Hospital, Bangkok, Thailand; Neurology Service (J.d.S., Thomas Senger), University Hospital of Strasbourg, France; Institute of Clinical Neuroimmunology (J.H.), Biomedical Center and University Hospital, Ludwig-Maximilians Universitaet Muenchen, Munich, Germany; Neurology (R.M., A.C.C.), Multiple Sclerosis, Myelin Disorders and Neuroinflammation, Pierre Wertheimer Neurological Hospital, Hospices Civils de Lyon, France; Centre d'Esclerosi Múltiple de Catalunya (Cemcat) (A.C.C.), Department of Neurology/Neuroimmunology, Hospital Universitari Vall d'Hebron, Universitat Autònoma de Barcelona, Spain; Department of Neurology and Neurosurgery (D.B., I.M.T.), Escola Paulista de Medicina, Universidade Federal de São Paulo, Brazil; Departments of Neurology (N.A.), Slagelse Hospitals, Institute of Regional Health Research, University of Southern Denmark, Odense; Institute of Regional Health Research (N.A., K.S.), University of Southern Denmark, Odense; Department of Neurology (A.A., U.T.), and Department of Ophthalmology (R.Y.), Cerrahpasa Medical Faculty, Istanbul University, Turkey; The Walton Centre for Neurology and Neurosurgery (A.J., S.H.), Liverpool, UK; The Cleveland Clinic Abu Dhabi (A.J.), United Arab Emirates; NYU Multiple Sclerosis Comprehensive Care Center (Z.R., A.R.), Department of Neurology, NYU School of Medicine, New York; Department of Neurology (Y.M.-D.), University of Michigan Medical School, Ann Arbor; Department of Neurology (I.S.C.), Hospital Clínico de Maracaibo, Venezuela; Moorfield's Eye Hospital (A.P.), University College London, UK; Department of Medicine (M.R.Y.), Los Angeles Biomedical Research Institute at Harbor-University of California at Los Angeles (UCLA) Medical Center, Torrance, CA, United States of America; Department of Medicine (M.R.Y.), David Geffen School of Medicine at UCLA, Los Angeles, CA, United States of America; Departments of Ophthalmology and Visual Sciences (Terry Smith), Kellogg Eye Center, University of Michigan Medical School, Ann Arbor, United States of America; Division of Metabolism (Terry Smith), Endocrine and Diabetes, Department of Internal Medicine, University of Michigan Medical School, Ann Arbor; Department of Neurology (A.U.B.), University of California, Irvine; and Department of Neurology (F.P.), Charité–Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Germany.
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Svenja Specovius
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Full PDF
Citation
Retinal Optical Coherence Tomography in Neuromyelitis Optica
Frederike Cosima Oertel, Svenja Specovius, Hanna G. Zimmermann, Claudia Chien, Seyedamirhosein Motamedi, Charlotte Bereuter, Lawrence Cook, Marco Aurélio Lana Peixoto, Mariana Andrade Fontanelle, Ho Jin Kim, Jae-Won Hyun, Jacqueline Palace, Adriana Roca-Fernandez, Maria Isabel Leite, Srilakshmi Sharma, Fereshteh Ashtari, Rahele Kafieh, Alireza Dehghani, Mohsen Pourazizi, Lekha Pandit, Anitha D'Cunha, Orhan Aktas, Marius Ringelstein, Philipp Albrecht, Eugene May, Caryl Tongco, Letizia Leocani, Marco Pisa, Marta Radaelli, Elena H. Martinez-Lapiscina, Hadas Stiebel-Kalish, Sasitorn Siritho, Jérome de Seze, Thomas Senger, Joachim Havla, Romain Marignier, Alvaro Cobo Calvo, Denis Bichuetti, Ivan Maynart Tavares, Nasrin Asgari, Kerstin Soelberg, Ayse Altintas, Rengin Yildirim, Uygur Tanriverdi, Anu Jacob, Saif Huda, Zoe Rimler, Allyson Reid, Yang Mao-Draayer, Ibis Soto de Castillo, Axel Petzold, Ari J. Green, Michael R. Yeaman, Terry Smith, Alexander U. Brandt, Friedemann Paul
Neurol Neuroimmunol Neuroinflamm Nov 2021, 8 (6) e1068; DOI: 10.1212/NXI.0000000000001068

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This article has a correction. Please see:

  • Errata - March 01, 2022
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Abstract

Background and Objectives To determine optic nerve and retinal damage in aquaporin-4 antibody (AQP4-IgG)-seropositive neuromyelitis optica spectrum disorders (NMOSD) in a large international cohort after previous studies have been limited by small and heterogeneous cohorts.

Methods The cross-sectional Collaborative Retrospective Study on retinal optical coherence tomography (OCT) in neuromyelitis optica collected retrospective data from 22 centers. Of 653 screened participants, we included 283 AQP4-IgG–seropositive patients with NMOSD and 72 healthy controls (HCs). Participants underwent OCT with central reading including quality control and intraretinal segmentation. The primary outcome was thickness of combined ganglion cell and inner plexiform (GCIP) layer; secondary outcomes were thickness of peripapillary retinal nerve fiber layer (pRNFL) and visual acuity (VA).

Results Eyes with ON (NMOSD-ON, N = 260) or without ON (NMOSD-NON, N = 241) were assessed compared with HCs (N = 136). In NMOSD-ON, GCIP layer (57.4 ± 12.2 μm) was reduced compared with HC (GCIP layer: 81.4 ± 5.7 μm, p < 0.001). GCIP layer loss (−22.7 μm) after the first ON was higher than after the next (−3.5 μm) and subsequent episodes. pRNFL observations were similar. NMOSD-NON exhibited reduced GCIP layer but not pRNFL compared with HC. VA was greatly reduced in NMOSD-ON compared with HC eyes, but did not differ between NMOSD-NON and HC.

Discussion Our results emphasize that attack prevention is key to avoid severe neuroaxonal damage and vision loss caused by ON in NMOSD. Therapies ameliorating attack-related damage, especially during a first attack, are an unmet clinical need. Mild signs of neuroaxonal changes without apparent vision loss in ON-unaffected eyes might be solely due to contralateral ON attacks and do not suggest clinically relevant progression but need further investigation.

Glossary

AQP4-IgG=
aquaporin-4 IgG;
CROCTINO=
Collaborative Retrospective Study on retinal OCT in Neuromyelitis Optica;
EDSS=
Expanded Disability Status Scale;
GCIP=
ganglion cell and inner plexiform;
HC=
healthy control;
HC-VA=
high-contrast visual acuity;
INL=
inner nuclear layer;
MME=
microcystic macular edema;
MS=
multiple sclerosis;
MOG-IgG=
myelin oligodendrocyte glycoprotein IgG;
NMOSD=
neuromyelitis optica spectrum disorder;
NMOSD-NON=
NMOSD eyes without a history of ON;
OCT=
optical coherence tomography;
ON=
optic neuritis;
pRNFL=
peripapillary retinal nerve fiber layer;
SE=
standard error;
VA=
visual acuity;
VEP=
visually evoked potential

Footnotes

  • Go to Neurology.org/NN for full disclosures. Funding information is provided at the end of the article.

  • ↵* These authors contributed equally to this work.

  • The Article Processing Charge was funded by the authors.

  • Received March 23, 2021.
  • Accepted in final form June 15, 2021.
  • Copyright © 2021 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND), which permits downloading and sharing the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

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