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March 2022; 9 (2) ArticleOpen Access

Optic Nerve Lesion Length at the Acute Phase of Optic Neuritis Is Predictive of Retinal Neuronal Loss

Mickael Denis, Jean-Philippe Woillez, View ORCID ProfileVasily M. Smirnov, View ORCID ProfileElodie Drumez, Julien Lannoy, Julie Boucher, Mickael Zedet, Jean-Pierre Pruvo, View ORCID ProfileJulien Labreuche, Helene Zephir, Xavier Leclerc, Olivier Outteryck
First published January 28, 2022, DOI: https://doi.org/10.1212/NXI.0000000000001135
Mickael Denis
From the Univ. Lille (M.D., J.-P.P., X.L., O.O.), Department of Neuroradiology, INSERM, CHU Lille, U1172—Lille Neurosciences Institute; Univ. Lille (J.-P.W., V.M.S.), Department of Visual Explorations and Neuro-Ophthalmology, Hôpital Roger Salengro, CHU Lille; Univ. Lille (E.D., Julien Labreuche), CHU Lille, EA 2694—Santé publique: épidémiologie et qualité des soins, Department of Biostatistics; and Univ. Lille (Julien Lannoy, J.B., M.Z., H.Z.), Department of Neurology, INSERM, CHU Lille, U1172–Lille Neurosciences Institute, France.
MD
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  • For correspondence: mickael-denis@hotmail.fr
Jean-Philippe Woillez
From the Univ. Lille (M.D., J.-P.P., X.L., O.O.), Department of Neuroradiology, INSERM, CHU Lille, U1172—Lille Neurosciences Institute; Univ. Lille (J.-P.W., V.M.S.), Department of Visual Explorations and Neuro-Ophthalmology, Hôpital Roger Salengro, CHU Lille; Univ. Lille (E.D., Julien Labreuche), CHU Lille, EA 2694—Santé publique: épidémiologie et qualité des soins, Department of Biostatistics; and Univ. Lille (Julien Lannoy, J.B., M.Z., H.Z.), Department of Neurology, INSERM, CHU Lille, U1172–Lille Neurosciences Institute, France.
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  • For correspondence: docteur.jp.woillez@wanadoo.fr
Vasily M. Smirnov
From the Univ. Lille (M.D., J.-P.P., X.L., O.O.), Department of Neuroradiology, INSERM, CHU Lille, U1172—Lille Neurosciences Institute; Univ. Lille (J.-P.W., V.M.S.), Department of Visual Explorations and Neuro-Ophthalmology, Hôpital Roger Salengro, CHU Lille; Univ. Lille (E.D., Julien Labreuche), CHU Lille, EA 2694—Santé publique: épidémiologie et qualité des soins, Department of Biostatistics; and Univ. Lille (Julien Lannoy, J.B., M.Z., H.Z.), Department of Neurology, INSERM, CHU Lille, U1172–Lille Neurosciences Institute, France.
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  • ORCID record for Vasily M. Smirnov
  • For correspondence: vasily.smirnov@chu-lille.fr
Elodie Drumez
From the Univ. Lille (M.D., J.-P.P., X.L., O.O.), Department of Neuroradiology, INSERM, CHU Lille, U1172—Lille Neurosciences Institute; Univ. Lille (J.-P.W., V.M.S.), Department of Visual Explorations and Neuro-Ophthalmology, Hôpital Roger Salengro, CHU Lille; Univ. Lille (E.D., Julien Labreuche), CHU Lille, EA 2694—Santé publique: épidémiologie et qualité des soins, Department of Biostatistics; and Univ. Lille (Julien Lannoy, J.B., M.Z., H.Z.), Department of Neurology, INSERM, CHU Lille, U1172–Lille Neurosciences Institute, France.
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  • For correspondence: edrumezchr@gmail.com
Julien Lannoy
From the Univ. Lille (M.D., J.-P.P., X.L., O.O.), Department of Neuroradiology, INSERM, CHU Lille, U1172—Lille Neurosciences Institute; Univ. Lille (J.-P.W., V.M.S.), Department of Visual Explorations and Neuro-Ophthalmology, Hôpital Roger Salengro, CHU Lille; Univ. Lille (E.D., Julien Labreuche), CHU Lille, EA 2694—Santé publique: épidémiologie et qualité des soins, Department of Biostatistics; and Univ. Lille (Julien Lannoy, J.B., M.Z., H.Z.), Department of Neurology, INSERM, CHU Lille, U1172–Lille Neurosciences Institute, France.
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Julie Boucher
From the Univ. Lille (M.D., J.-P.P., X.L., O.O.), Department of Neuroradiology, INSERM, CHU Lille, U1172—Lille Neurosciences Institute; Univ. Lille (J.-P.W., V.M.S.), Department of Visual Explorations and Neuro-Ophthalmology, Hôpital Roger Salengro, CHU Lille; Univ. Lille (E.D., Julien Labreuche), CHU Lille, EA 2694—Santé publique: épidémiologie et qualité des soins, Department of Biostatistics; and Univ. Lille (Julien Lannoy, J.B., M.Z., H.Z.), Department of Neurology, INSERM, CHU Lille, U1172–Lille Neurosciences Institute, France.
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  • For correspondence: julie.boucher@chru-lille.fr
Mickael Zedet
From the Univ. Lille (M.D., J.-P.P., X.L., O.O.), Department of Neuroradiology, INSERM, CHU Lille, U1172—Lille Neurosciences Institute; Univ. Lille (J.-P.W., V.M.S.), Department of Visual Explorations and Neuro-Ophthalmology, Hôpital Roger Salengro, CHU Lille; Univ. Lille (E.D., Julien Labreuche), CHU Lille, EA 2694—Santé publique: épidémiologie et qualité des soins, Department of Biostatistics; and Univ. Lille (Julien Lannoy, J.B., M.Z., H.Z.), Department of Neurology, INSERM, CHU Lille, U1172–Lille Neurosciences Institute, France.
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  • For correspondence: mickael.zedet@hotmail.fr
Jean-Pierre Pruvo
From the Univ. Lille (M.D., J.-P.P., X.L., O.O.), Department of Neuroradiology, INSERM, CHU Lille, U1172—Lille Neurosciences Institute; Univ. Lille (J.-P.W., V.M.S.), Department of Visual Explorations and Neuro-Ophthalmology, Hôpital Roger Salengro, CHU Lille; Univ. Lille (E.D., Julien Labreuche), CHU Lille, EA 2694—Santé publique: épidémiologie et qualité des soins, Department of Biostatistics; and Univ. Lille (Julien Lannoy, J.B., M.Z., H.Z.), Department of Neurology, INSERM, CHU Lille, U1172–Lille Neurosciences Institute, France.
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  • For correspondence: jppruvo@gmail.com
Julien Labreuche
From the Univ. Lille (M.D., J.-P.P., X.L., O.O.), Department of Neuroradiology, INSERM, CHU Lille, U1172—Lille Neurosciences Institute; Univ. Lille (J.-P.W., V.M.S.), Department of Visual Explorations and Neuro-Ophthalmology, Hôpital Roger Salengro, CHU Lille; Univ. Lille (E.D., Julien Labreuche), CHU Lille, EA 2694—Santé publique: épidémiologie et qualité des soins, Department of Biostatistics; and Univ. Lille (Julien Lannoy, J.B., M.Z., H.Z.), Department of Neurology, INSERM, CHU Lille, U1172–Lille Neurosciences Institute, France.
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Helene Zephir
From the Univ. Lille (M.D., J.-P.P., X.L., O.O.), Department of Neuroradiology, INSERM, CHU Lille, U1172—Lille Neurosciences Institute; Univ. Lille (J.-P.W., V.M.S.), Department of Visual Explorations and Neuro-Ophthalmology, Hôpital Roger Salengro, CHU Lille; Univ. Lille (E.D., Julien Labreuche), CHU Lille, EA 2694—Santé publique: épidémiologie et qualité des soins, Department of Biostatistics; and Univ. Lille (Julien Lannoy, J.B., M.Z., H.Z.), Department of Neurology, INSERM, CHU Lille, U1172–Lille Neurosciences Institute, France.
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  • For correspondence: helene.zephir@chru-lille.fr
Xavier Leclerc
From the Univ. Lille (M.D., J.-P.P., X.L., O.O.), Department of Neuroradiology, INSERM, CHU Lille, U1172—Lille Neurosciences Institute; Univ. Lille (J.-P.W., V.M.S.), Department of Visual Explorations and Neuro-Ophthalmology, Hôpital Roger Salengro, CHU Lille; Univ. Lille (E.D., Julien Labreuche), CHU Lille, EA 2694—Santé publique: épidémiologie et qualité des soins, Department of Biostatistics; and Univ. Lille (Julien Lannoy, J.B., M.Z., H.Z.), Department of Neurology, INSERM, CHU Lille, U1172–Lille Neurosciences Institute, France.
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  • For correspondence: xavier.leclerc@chru-lille.fr
Olivier Outteryck
From the Univ. Lille (M.D., J.-P.P., X.L., O.O.), Department of Neuroradiology, INSERM, CHU Lille, U1172—Lille Neurosciences Institute; Univ. Lille (J.-P.W., V.M.S.), Department of Visual Explorations and Neuro-Ophthalmology, Hôpital Roger Salengro, CHU Lille; Univ. Lille (E.D., Julien Labreuche), CHU Lille, EA 2694—Santé publique: épidémiologie et qualité des soins, Department of Biostatistics; and Univ. Lille (Julien Lannoy, J.B., M.Z., H.Z.), Department of Neurology, INSERM, CHU Lille, U1172–Lille Neurosciences Institute, France.
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Citation
Optic Nerve Lesion Length at the Acute Phase of Optic Neuritis Is Predictive of Retinal Neuronal Loss
Mickael Denis, Jean-Philippe Woillez, Vasily M. Smirnov, Elodie Drumez, Julien Lannoy, Julie Boucher, Mickael Zedet, Jean-Pierre Pruvo, Julien Labreuche, Helene Zephir, Xavier Leclerc, Olivier Outteryck
Neurol Neuroimmunol Neuroinflamm Mar 2022, 9 (2) e1135; DOI: 10.1212/NXI.0000000000001135

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Abstract

Background and Objectives Acute optic neuritis (ON) is a classical presenting symptom of multiple sclerosis (MS), neuromyelitis optica spectrum disorders (NMOSD), and anti–MOG-associated disorders. The resulting visual impairment is variable and can be severe. Clinicians are in need of predictive biomarkers to optimize the management of acute ON. In this longitudinal study (IRMANO, NCT03651662), we evaluated the ability of optic nerve lesion length measured on MRI at the acute phase of ON to predict retinal neuro-axonal loss and visual impairment at a chronic stage.

Methods We conducted a longitudinal study (IRMANO, NCT03651662) of patients who presented a clinical episode of ON (≤8 weeks). All patients underwent a retinal optical coherence tomography (OCT) and a brain/optic nerve MRI, including 3D double-inversion recovery (DIR) sequence at the acute phase of ON and 12 months later. Primary outcomes were optic nerve DIR hypersignal lesion length, macular ganglion cell–inner plexiform layer (GCIPL) volume measured on OCT, and low-contrast monocular visual acuity (LCMVA).

Results The study group included 51 patients (33 women, mean age of 32.4 years ± 7.9). We recruited patients with a clinically isolated syndrome (n = 20), a relapsing-remitting MS (n = 23), an isolated ON (n = 6), and a first clinical episode of NMOSD (n = 2). Optic nerve DIR hypersignal was observed in all but 1 symptomatic optic nerves. At inclusion, the mean optic nerve lesion length (in mm) was 12.35 ± 5.98. The mean GCIPL volume (in mm3) significantly decreased between inclusion (1.90 ± 0.18) and M12 (1.67 ± 0.21; p < 0.0001). Optic nerve lesion length at inclusion was significantly associated with GCIPL thinning (estimate ± SD; −0.012 ± 0.004; p = 0.0016) and LCMVA at M12 (0.016 ± 0.003; p < 0.001). Optic nerve lesion length significantly increased at M12 (15.76 ± 8.70; p = 0.0007). The increase in optic nerve lesion length was significantly associated with the GCIPL thinning between inclusion and M12 (−0.012 ± 0.003; p = 0.0011).

Discussion At the acute phase of ON, optic nerve lesion length is an imaging biomarker predictive of retinal neuro-axonal loss and chronic visual impairment, which can help to stratify future therapeutic strategies in acute ON.

Classification of Evidence This study provides Class I evidence that optic nerve lesion length measured on MRI during the acute phase of a first episode of ON is associated with long-term retinal neuro-axonal loss and visual impairment.

Glossary

3D-DIR=
3D double-inversion recovery;
Abs=
aquaporin 4 antibodies;
ANCOVA=
analysis of covariance;
CIS=
clinically isolated syndrome;
DMT=
disease-modifying therapy;
FU=
follow-up;
GCIPL=
ganglion-cells–inner plexiform layer;
IETD=
intereye retinal thickness difference;
INL=
inner nuclear layer;
LCMVA=
low-contrast monocular visual acuity;
MME=
microcystic macular edema;
MOGAD=
MOG-associated disorder;
MS=
multiple sclerosis;
NMOSD=
neuromyelitis optica spectrum disorder;
OCT=
optical coherence tomography;
ON=
optic neuritis;
pRNFL=
peripapillary retinal nerve fiber layer;
RRMS=
relapsing-remitting multiple sclerosis;
VF=
visual field

Footnotes

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

  • The Article Processing Charge was funded by the University Hospital of Lille (CHU Lille).

  • Received September 10, 2021.
  • Accepted in final form December 3, 2021.
  • Copyright © 2022 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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