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January 28, 2020; 94 (4) Article

Longitudinal optic neuritis-unrelated visual evoked potential changes in NMO spectrum disorders

Marius Ringelstein, Jens Harmel, Hanna Zimmermann, View ORCID ProfileAlexander U. Brandt, Friedemann Paul, Axel Haarmann, Mathias Buttmann, Martin W. Hümmert, Corinna Trebst, Christoph Schroeder, Ilya Ayzenberg, View ORCID ProfileIngo Kleiter, Kerstin Hellwig, Joachim Havla, Tania Kümpfel, Sven Jarius, Brigitte Wildemann, Paulus Rommer, Martin S. Weber, Hannah Pellkofer, Luise Röpke, Christian Geis, Nele Retzlaff, Uwe Zettl, Michael Deppe, Luisa Klotz, Kim Young, Jan-Patrick Stellmann, Matthias Kaste, Pawel Kermer, Wael Marouf, Florian Lauda, Hayrettin Tumani, View ORCID ProfileJonas Graf, Alexander Klistorner, Hans-Peter Hartung, Orhan Aktas, View ORCID ProfilePhilipp Albrecht, on behalf of the Neuromyelitis Optica Study Group (NEMOS)
First published December 3, 2019, DOI: https://doi.org/10.1212/WNL.0000000000008684
Marius Ringelstein
From the Department of Neurology, Medical Faculty (M.R., J. Harmel, J.G., H.-P.H., O.A., P.A.), and Department of Neurology, Center for Neurology and Neuropsychiatry, LVR-Klinikum (M.R.), Heinrich Heine University Düsseldorf; NeuroCure Clinical Research Center and Experimental and Clinical Research Center (H.Z., A.U.B., F.P.), Charité Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin Institute of Health, and Max Delbrueck Center for Molecular Medicine, Germany; Department of Neurology (A.U.B.), University of California Irvine; Department of Neurology (A.H., M.B.), University of Würzburg; Department of Neurology (M.B.), Caritas Hospital, Bad Mergentheim; Clinical Neuroimmunology and Neurochemistry (M.W.H.), Department of Neurology (C.T.), Hannover Medical School; Department of Neurology (C.S., I.A., I.K., K.H.), St. Josef Hospital, Ruhr University Bochum, Germany; Department of Neurology (I.A.), Sechenov First Moscow State Medical University, Moscow, Russia; Marianne-Strauß-Klinik (I.K.), Behandlungszentrum Kempfenhausen für Multiple Sklerose Kranke, Berg; Institute of Clinical Neuroimmunology (J. Halva, T.K., H.P.), University Hospital, Ludwig-Maximilians University, Munich; Molecular Neuroimmunology Group, Department of Neurology (S.J., B.W.), University of Heidelberg, Germany; Department of Neurology (P.R.), Medical University of Vienna, Austria; Institute of Neuropathology (M.S.W.) and Department of Neurology (M.S.W., H.P., P.K.), University Medical Center Göttingen; Department of Neurology (L.R., C.G.), Jena University Hospital; Neuroimmunological Section, Department of Neurology (N.R., U.Z.), University of Rostock; Department of Neurology (M.D., L.K.), University of Münster; Department of Neurology and Institute of Neuroimmunology and MS (K.Y., J.-P.S.), University Medical Center Hamburg-Eppendorf; Department of Neurology (M.K., P.K.), Nordwest-Hospital Sanderbusch, Sande; Department of Neurology (W.M.), Helios Hanseklinikum Stralsund; Department of Neurology (F.L., H.T.), University of Ulm, Germany; and Faculty of Medicine and Health Sciences (A.K.), Macquarie University, Sydney, New South Wales, Australia.
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Jens Harmel
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Hanna Zimmermann
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Alexander U. Brandt
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Friedemann Paul
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Axel Haarmann
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Mathias Buttmann
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Martin W. Hümmert
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Corinna Trebst
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Christoph Schroeder
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Ilya Ayzenberg
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Ingo Kleiter
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Kerstin Hellwig
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Joachim Havla
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Tania Kümpfel
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Sven Jarius
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Brigitte Wildemann
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Paulus Rommer
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Martin S. Weber
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Hannah Pellkofer
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Luise Röpke
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Christian Geis
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Nele Retzlaff
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Uwe Zettl
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Michael Deppe
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Luisa Klotz
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Kim Young
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Jan-Patrick Stellmann
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Matthias Kaste
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Pawel Kermer
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Wael Marouf
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Florian Lauda
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Hayrettin Tumani
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Jonas Graf
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Alexander Klistorner
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Hans-Peter Hartung
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Orhan Aktas
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Philipp Albrecht
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Longitudinal optic neuritis-unrelated visual evoked potential changes in NMO spectrum disorders
Marius Ringelstein, Jens Harmel, Hanna Zimmermann, Alexander U. Brandt, Friedemann Paul, Axel Haarmann, Mathias Buttmann, Martin W. Hümmert, Corinna Trebst, Christoph Schroeder, Ilya Ayzenberg, Ingo Kleiter, Kerstin Hellwig, Joachim Havla, Tania Kümpfel, Sven Jarius, Brigitte Wildemann, Paulus Rommer, Martin S. Weber, Hannah Pellkofer, Luise Röpke, Christian Geis, Nele Retzlaff, Uwe Zettl, Michael Deppe, Luisa Klotz, Kim Young, Jan-Patrick Stellmann, Matthias Kaste, Pawel Kermer, Wael Marouf, Florian Lauda, Hayrettin Tumani, Jonas Graf, Alexander Klistorner, Hans-Peter Hartung, Orhan Aktas, Philipp Albrecht, on behalf of the Neuromyelitis Optica Study Group (NEMOS)
Neurology Jan 2020, 94 (4) e407-e418; DOI: 10.1212/WNL.0000000000008684

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Abstract

Objective To investigate if patients with neuromyelitis optica spectrum disorder (NMOSD) develop subclinical visual pathway impairment independent of acute attacks.

Methods A total of 548 longitudinally assessed full-field visual evoked potentials (VEP) of 167 patients with NMOSD from 16 centers were retrospectively evaluated for changes of P100 latencies and P100-N140 amplitudes. Rates of change in latencies (RCL) and amplitudes (RCA) over time were analyzed for each individual eye using linear regression and compared using generalized estimating equation models.

Results The rates of change in the absence of optic neuritis (ON) for minimal VEP intervals of ≥3 months between baseline and last follow-up were +1.951 ms/y (n = 101 eyes; SD = 6.274; p = 0.012) for the P100 latencies and −2.149 µV/y (n = 64 eyes; SD = 5.013; p = 0.005) for the P100-N140 amplitudes. For minimal VEP intervals of ≥12 months, the RCL was +1.768 ms/y (n = 59 eyes; SD = 4.558; p = 0.024) and the RCA was −0.527 µV/y (n = 44 eyes; SD = 2.123; p = 0.111). The history of a previous ON >6 months before baseline VEP had no influence on RCL and RCA. ONs during the observational period led to mean RCL and RCA of +11.689 ms/y (n = 16 eyes; SD = 17.593; p = 0.003) and −1.238 µV/y (n = 11 eyes; SD = 3.708; p = 0.308), respectively.

Conclusion This first longitudinal VEP study of patients with NMOSD provides evidence of progressive VEP latency delay occurring independently of acute ON. Prospective longitudinal studies are needed to corroborate these findings and help to interpret the clinical relevance.

Glossary

AQP4-Ab=
antibodies against aquaporin-4;
ffVEP=
full-field visual evoked potentials;
HON-eyes=
eyes that had optic neuritis >6 months before baseline visual evoked potential;
IQR=
interquartile range;
MOG=
myelin oligodendrocyte glycoprotein;
MS=
multiple sclerosis;
NEMOS=
Neuromyelitis Optica Study Group;
NMOSD=
neuromyelitis optica spectrum disorders;
no-HON-eyes=
eyes that never had optic neuritis;
ON=
optic neuritis;
OP=
observational period;
RCA=
rate of change in amplitudes;
RCL=
rate of change in latencies;
SD-OCT=
spectral-domain optical coherence tomography;
SR=
stimulation response;
VEP=
visual evoked potential;
VEP1=
baseline visual evoked potential;
vrQoL=
vision-related quality of life

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • ↵* These authors contributed equally to this work.

  • Coinvestigators are listed at links.lww.com/WNL/B22.

  • Received February 11, 2019.
  • Accepted in final form July 22, 2019.
  • © 2019 American Academy of Neurology
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Disputes & Debates: Rapid online correspondence

  • Author response: Longitudinal optic neuritis-unrelated visual evoked potential changes in NMO spectrum disorders
    • Marius Ringelstein, Neurologist, Department of Neurology, Medical Faculty, Heinrich Heine University Düsseldorf, (Düsseldorf, Germany)
    • Jens Harmel, Neurologist, Heinrich Heine University (Düsseldorf, Germany)
    • Hanna Zimmermann, Scientist, Charité Universitätsmedizin (Berlin, Germany)
    • Alexander U. Brandt, Neurologist, Charité Universitätsmedizin (Berlin, Germany)
    • Friedemann Paul, Neurologist, Charité Universitätsmedizin (Berlin, Germany)
    • Axel Haarmann, Neurologist, University Hospital (Würzburg, Germany)
    • Mathias Buttmann, Neurologist, Caritas Hospital (Bad Mergentheim, Germany)
    • Martin W. Hümmert, Neurologist, Hannover Medical School (Hannover, Germany)
    • Corinna Trebst, Neurologist, Hannover Medical School (Hannover, Germany)
    • Christoph Schroeder, Neurologist, Ruhr University (Bochum, Germany)
    • Ilya Ayzenberg, Neurologist, Ruhr University (Bochum, Germany)
    • Ingo Kleiter, Neurologist, Ruhr University (Bochum, Germany)
    • Kerstin Hellwig, Neurologist, Ruhr University (Bochum, Germany)
    • Joachim Havla, Neurologist, Ludwig-Maximilians University (Munich, Germany)
    • Tania Kümpfel, Neurologist, Ludwig-Maximilians University (Munich, Germany)
    • Sven Jarius, Neurologist, University of Heidelberg (Heidelberg, Germany)
    • Brigitte Wildemann, Neurologist, University of Heidelberg (Heidelberg, Germany)
    • Paulus Rommer, Neurologist, Medical University of Vienna (Vienna, Austria)
    • Martin Weber, Neurologist, University Medical Center Göttingen (Göttingen, Germany)
    • Hannah Pellkofer, Neurologist, Ludwig-Maximilians University (Munich, Germany)
    • Luise Röpke, Neurologist, University Hospital (Jena, Germany)
    • Christian Geis, Neurologist, University Hospital (Jena, Germany)
    • Nele Retzlaff, Neurologist, University Hospital (Rostock, Germany)
    • Uwe Zettl, Neurologist, University Hospital (Rostock, Germany)
    • Michael Deppe, Scientist, University Hospital (Münster, Germany)
    • Luisa Klotz, Neurologist, University Hospital (Münster, Germany)
    • Kim Young, Neurologist, University Medical Center (Hamburg-Eppendorf, Germany)
    • Jan-Patrick Stellmann, Neurologist, University Medical Center (Hamburg-Eppendorf, Germany)
    • Matthias Kaste, Neurologist, Nordwest-Hospital Sanderbusch (Sande, Germany)
    • Pawel Kermer, Neurologist, Nordwest-Hospital Sanderbusch (Sande, Germany)
    • Wael Marouf, Neurologist, Helios Hanseklinikum Stralsund, Germany
    • Florian Lauda, Neurologist, University Hospital (Ulm, Germany)
    • Hayrettin Tumani, Neurologist, University Hospital (Ulm, Germany)
    • Jonas Graf, Neurologist, Heinrich Heine University (Düsseldorf, Germany)
    • Sasha Klistorner, Neurologist, Macquarie University (Sydney, Australia)
    • Hans-Peter Hartung, Neurologist, Heinrich Heine University (Düsseldorf, Germany)
    • Orhan Aktas, Neurologist, Heinrich Heine University (Düsseldorf, Germany)
    • Philipp Albrecht, Neurologist, Heinrich Heine University (Düsseldorf, Germany)
    Submitted December 09, 2019
  • Reader response: Longitudinal optic neuritis-unrelated visual evoked potential changes in NMO spectrum disorders
    • John J. Chen, MD, PhD, Departments of Ophthalmology and Neurology, Mayo Clinic (Rochester, MN)
    Submitted December 03, 2019
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