Lateral geniculate nucleus volume changes after optic neuritis in neuromyelitis optica: A longitudinal study

Athina Papadopoulou; Frederike C Oertel; Claudia Chien; Joseph Kuchling; Hanna G Zimmermann; Nadja Siebert; Seyedamirhosein Motamedi; Marcus D' Souza; Susanna Asseyer; Judith Bellmann-Strobl; Klemens Ruprecht; M Mallar Chakravarty; Michael Scheel; Stefano Magon; Jens Wuerfel; Friedemann Paul; Alexander U Brandt

doi:10.1016/j.nicl.2021.102608

Lateral geniculate nucleus volume changes after optic neuritis in neuromyelitis optica: A longitudinal study

Neuroimage Clin. 2021:30:102608. doi: 10.1016/j.nicl.2021.102608. Epub 2021 Mar 4.

Authors

Athina Papadopoulou¹, Frederike C Oertel², Claudia Chien³, Joseph Kuchling³, Hanna G Zimmermann³, Nadja Siebert³, Seyedamirhosein Motamedi³, Marcus D' Souza¹, Susanna Asseyer³, Judith Bellmann-Strobl³, Klemens Ruprecht⁴, M Mallar Chakravarty⁵, Michael Scheel⁶, Stefano Magon⁷, Jens Wuerfel⁸, Friedemann Paul⁹, Alexander U Brandt¹⁰

Affiliations

¹ Experimental and Clinical Research Center, Max Delbrueck Center for Molecular Medicine and Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; NeuroCure Clinical Research Center, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; Neurologic Clinic and Policlinic, Department of Medicine, Clinical Research and Biomedicine University Hospital Basel, University of Basel, Basel, Switzerland.
² Experimental and Clinical Research Center, Max Delbrueck Center for Molecular Medicine and Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; NeuroCure Clinical Research Center, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; Department of Neurology, University of California San Francisco, CA, USA.
³ Experimental and Clinical Research Center, Max Delbrueck Center for Molecular Medicine and Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; NeuroCure Clinical Research Center, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.
⁴ Department of Neurology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.
⁵ Cerebral Imaging Centre, Douglas Mental Health University Institute, Montreal, Canada; McGill University, Department of Psychiatry and Department of Biomedical Engineering, Montreal, Canada.
⁶ Experimental and Clinical Research Center, Max Delbrueck Center for Molecular Medicine and Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; NeuroCure Clinical Research Center, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; Department of Neuroradiology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.
⁷ Neurologic Clinic and Policlinic, Department of Medicine, Clinical Research and Biomedicine University Hospital Basel, University of Basel, Basel, Switzerland; Pharma Research and Early Development, Roche Innovation Center Basel, F. Hoffmann-La Roche Ltd, Switzerland.
⁸ Medical Image Analysis Center (MIAC AG) and Department for Biomedical Engineering, Basel, Switzerland.
⁹ Experimental and Clinical Research Center, Max Delbrueck Center for Molecular Medicine and Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; NeuroCure Clinical Research Center, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; Department of Neurology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.
¹⁰ Experimental and Clinical Research Center, Max Delbrueck Center for Molecular Medicine and Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; NeuroCure Clinical Research Center, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; Department of Neurology, University of California Irvine, CA, USA. Electronic address: alexander.brandt@charite.de.

Abstract

Objectives: Lateral geniculate nucleus (LGN) volume is reduced after optic neuritis (ON) in neuromyelitis optica spectrum disorders (NMOSD). We aimed at a longitudinal assessment of LGN volume in NMOSD.

Methods: Twenty-nine patients with aquaporin 4-IgG seropositive NMOSD (age: 47.8 ± 14.6 years (y), female: n = 27, history of ON (NMO-ON): n = 17, median time since ON: 3[1.2-12.1]y) and 18 healthy controls (HC; age: 39.3 ± 15.8y; female: n = 13) were included. Median follow-up was 4.1[1.1-4.7]y for patients and 1.7[0.9-3.2]y for HC. LGN volume was measured using a multi-atlas-based approach of automated segmentation on 3 Tesla magnetic resonance images. Retinal optical coherence tomography and probabilistic tractography of the optic radiations (OR) were also performed.

Results: At baseline, NMO-ON patients had lower LGN volumes (395.4 ± 48.9 mm³) than patients without ON (NMO-NON: 450.7 ± 55.6 mm³; p = 0.049) and HC (444.5 ± 61.5 mm³, p = 0.025). LGN volume was associated with retinal neuroaxonal loss and microstructural OR damage. Longitudinally, there was no change in LGN volumes in the absence of ON, neither in all patients (B = -0.6, SE = 1.4, p = 0.670), nor in NMO-ON (B = -0.8, SE = 1.6, p = 0.617) and NMO-NON (B = 1.7, SE = 3.5, p = 0.650). However, in four patients with new ON during follow-up, LGN volume was reduced at last visit (median time since ON: 2.6 [1.8-3.9]y) compared to the measurement before ON (352 ± 52.7 vs. 371.1 ± 55.9 mm³; t = -3.6, p = 0.036).

Conclusion: Although LGN volume is reduced after ON in NMOSD, this volume loss is not progressive over longer follow-up or independent of ON. Thus, our findings -at least in this relatively small cohort- do not support occult neurodegeneration of the afferent visual pathway in NMOSD.

Keywords: Anterograde degeneration; NMOSD; Neurodegeneration; Thalamus.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adult
Female
Geniculate Bodies
Humans
Longitudinal Studies
Middle Aged
Nerve Fibers
Neuromyelitis Optica* / diagnostic imaging
Optic Neuritis* / diagnostic imaging
Young Adult