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June 17, 2014; 82 (24) Article

Axonal loss of retinal neurons in multiple sclerosis associated with optic radiation lesions

Alexander Klistorner, Prima Sriram, Nikitha Vootakuru, Chenyu Wang, Michael H. Barnett, Raymond Garrick, John Parratt, Netta Levin, Noa Raz, Anneke Van der Walt, Lynette Masters, Stuart L. Graham, Con Yiannikas
First published May 16, 2014, DOI: https://doi.org/10.1212/WNL.0000000000000522
Alexander Klistorner
From the Department of Ophthalmology (A.K., N.V.) and the Brain and Mind Institute (C.W., M.H.B., L.M.), University of Sydney; the Australian School of Advanced Medicine (A.K., P.S., S.L.G.), Macquarie University; St. Vincent Hospital (R.G.); North Shore Hospital (J.P.), Sydney, Australia; Hadassah Hebrew University Medical Center (N.L., N.R.), Jerusalem, Israel; the Department of Neurology (A.V.d.W.), Royal Melbourne Hospital; and Concord Hospital (C.Y.), Sydney, Australia.
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Prima Sriram
From the Department of Ophthalmology (A.K., N.V.) and the Brain and Mind Institute (C.W., M.H.B., L.M.), University of Sydney; the Australian School of Advanced Medicine (A.K., P.S., S.L.G.), Macquarie University; St. Vincent Hospital (R.G.); North Shore Hospital (J.P.), Sydney, Australia; Hadassah Hebrew University Medical Center (N.L., N.R.), Jerusalem, Israel; the Department of Neurology (A.V.d.W.), Royal Melbourne Hospital; and Concord Hospital (C.Y.), Sydney, Australia.
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Nikitha Vootakuru
From the Department of Ophthalmology (A.K., N.V.) and the Brain and Mind Institute (C.W., M.H.B., L.M.), University of Sydney; the Australian School of Advanced Medicine (A.K., P.S., S.L.G.), Macquarie University; St. Vincent Hospital (R.G.); North Shore Hospital (J.P.), Sydney, Australia; Hadassah Hebrew University Medical Center (N.L., N.R.), Jerusalem, Israel; the Department of Neurology (A.V.d.W.), Royal Melbourne Hospital; and Concord Hospital (C.Y.), Sydney, Australia.
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Chenyu Wang
From the Department of Ophthalmology (A.K., N.V.) and the Brain and Mind Institute (C.W., M.H.B., L.M.), University of Sydney; the Australian School of Advanced Medicine (A.K., P.S., S.L.G.), Macquarie University; St. Vincent Hospital (R.G.); North Shore Hospital (J.P.), Sydney, Australia; Hadassah Hebrew University Medical Center (N.L., N.R.), Jerusalem, Israel; the Department of Neurology (A.V.d.W.), Royal Melbourne Hospital; and Concord Hospital (C.Y.), Sydney, Australia.
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Michael H. Barnett
From the Department of Ophthalmology (A.K., N.V.) and the Brain and Mind Institute (C.W., M.H.B., L.M.), University of Sydney; the Australian School of Advanced Medicine (A.K., P.S., S.L.G.), Macquarie University; St. Vincent Hospital (R.G.); North Shore Hospital (J.P.), Sydney, Australia; Hadassah Hebrew University Medical Center (N.L., N.R.), Jerusalem, Israel; the Department of Neurology (A.V.d.W.), Royal Melbourne Hospital; and Concord Hospital (C.Y.), Sydney, Australia.
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Raymond Garrick
From the Department of Ophthalmology (A.K., N.V.) and the Brain and Mind Institute (C.W., M.H.B., L.M.), University of Sydney; the Australian School of Advanced Medicine (A.K., P.S., S.L.G.), Macquarie University; St. Vincent Hospital (R.G.); North Shore Hospital (J.P.), Sydney, Australia; Hadassah Hebrew University Medical Center (N.L., N.R.), Jerusalem, Israel; the Department of Neurology (A.V.d.W.), Royal Melbourne Hospital; and Concord Hospital (C.Y.), Sydney, Australia.
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John Parratt
From the Department of Ophthalmology (A.K., N.V.) and the Brain and Mind Institute (C.W., M.H.B., L.M.), University of Sydney; the Australian School of Advanced Medicine (A.K., P.S., S.L.G.), Macquarie University; St. Vincent Hospital (R.G.); North Shore Hospital (J.P.), Sydney, Australia; Hadassah Hebrew University Medical Center (N.L., N.R.), Jerusalem, Israel; the Department of Neurology (A.V.d.W.), Royal Melbourne Hospital; and Concord Hospital (C.Y.), Sydney, Australia.
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Netta Levin
From the Department of Ophthalmology (A.K., N.V.) and the Brain and Mind Institute (C.W., M.H.B., L.M.), University of Sydney; the Australian School of Advanced Medicine (A.K., P.S., S.L.G.), Macquarie University; St. Vincent Hospital (R.G.); North Shore Hospital (J.P.), Sydney, Australia; Hadassah Hebrew University Medical Center (N.L., N.R.), Jerusalem, Israel; the Department of Neurology (A.V.d.W.), Royal Melbourne Hospital; and Concord Hospital (C.Y.), Sydney, Australia.
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Noa Raz
From the Department of Ophthalmology (A.K., N.V.) and the Brain and Mind Institute (C.W., M.H.B., L.M.), University of Sydney; the Australian School of Advanced Medicine (A.K., P.S., S.L.G.), Macquarie University; St. Vincent Hospital (R.G.); North Shore Hospital (J.P.), Sydney, Australia; Hadassah Hebrew University Medical Center (N.L., N.R.), Jerusalem, Israel; the Department of Neurology (A.V.d.W.), Royal Melbourne Hospital; and Concord Hospital (C.Y.), Sydney, Australia.
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Anneke Van der Walt
From the Department of Ophthalmology (A.K., N.V.) and the Brain and Mind Institute (C.W., M.H.B., L.M.), University of Sydney; the Australian School of Advanced Medicine (A.K., P.S., S.L.G.), Macquarie University; St. Vincent Hospital (R.G.); North Shore Hospital (J.P.), Sydney, Australia; Hadassah Hebrew University Medical Center (N.L., N.R.), Jerusalem, Israel; the Department of Neurology (A.V.d.W.), Royal Melbourne Hospital; and Concord Hospital (C.Y.), Sydney, Australia.
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Lynette Masters
From the Department of Ophthalmology (A.K., N.V.) and the Brain and Mind Institute (C.W., M.H.B., L.M.), University of Sydney; the Australian School of Advanced Medicine (A.K., P.S., S.L.G.), Macquarie University; St. Vincent Hospital (R.G.); North Shore Hospital (J.P.), Sydney, Australia; Hadassah Hebrew University Medical Center (N.L., N.R.), Jerusalem, Israel; the Department of Neurology (A.V.d.W.), Royal Melbourne Hospital; and Concord Hospital (C.Y.), Sydney, Australia.
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Stuart L. Graham
From the Department of Ophthalmology (A.K., N.V.) and the Brain and Mind Institute (C.W., M.H.B., L.M.), University of Sydney; the Australian School of Advanced Medicine (A.K., P.S., S.L.G.), Macquarie University; St. Vincent Hospital (R.G.); North Shore Hospital (J.P.), Sydney, Australia; Hadassah Hebrew University Medical Center (N.L., N.R.), Jerusalem, Israel; the Department of Neurology (A.V.d.W.), Royal Melbourne Hospital; and Concord Hospital (C.Y.), Sydney, Australia.
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Con Yiannikas
From the Department of Ophthalmology (A.K., N.V.) and the Brain and Mind Institute (C.W., M.H.B., L.M.), University of Sydney; the Australian School of Advanced Medicine (A.K., P.S., S.L.G.), Macquarie University; St. Vincent Hospital (R.G.); North Shore Hospital (J.P.), Sydney, Australia; Hadassah Hebrew University Medical Center (N.L., N.R.), Jerusalem, Israel; the Department of Neurology (A.V.d.W.), Royal Melbourne Hospital; and Concord Hospital (C.Y.), Sydney, Australia.
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Full PDF
Citation
Axonal loss of retinal neurons in multiple sclerosis associated with optic radiation lesions
Alexander Klistorner, Prima Sriram, Nikitha Vootakuru, Chenyu Wang, Michael H. Barnett, Raymond Garrick, John Parratt, Netta Levin, Noa Raz, Anneke Van der Walt, Lynette Masters, Stuart L. Graham, Con Yiannikas
Neurology Jun 2014, 82 (24) 2165-2172; DOI: 10.1212/WNL.0000000000000522

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Abstract

Objective: To investigate the potential links between thinning of retinal ganglion cell axons in eyes of patients with multiple sclerosis (MS) without past optic neuritis (ON) and MS-related inflammatory damage of the posterior visual pathway.

Methods: Temporal retinal nerve fiber layer (tRNFL) thickness was analyzed in eyes with no history of ON (NON) from 53 patients with relapsing-remitting MS. Fifty normal age- and sex-matched controls were examined with optical coherence tomography. Low-contrast visual acuity charts were used for functional assessment of vision. The optic tract (OT) and optic radiation (OR) were identified using probabilistic tractography, and volume of T2 fluid-attenuated inversion recovery lesions and diffusion tensor imaging (DTI) indices were measured within both structures. Cross-sectional diameter of the OT was also calculated.

Results: tRNFL thickness was significantly reduced in NON eyes and was associated with reduced low-contrast visual acuity. Lesions within the OR were detected in the majority of patients. There was a significant correlation between thinning of the tRNFL and OR lesion volume (adjusted for non-OR lesion volume, age, sex, and disease duration). tRNFL thickness also correlated with OR DTI indices. No OT lesions were identified in any of the patients and no relationship between retinal nerve fiber layer loss and potential markers of OT lesions was found.

Conclusion: The results demonstrate a strong tract-specific association between loss of tRNFL fibers and MS-related inflammation within OR.

GLOSSARY

AD=
axial diffusivity;
ANOVA=
analysis of variance;
DTI=
diffusion tensor imaging;
FA=
fractional anisotropy;
FLAIR=
fluid-attenuated inversion recovery;
GCL=
ganglion cell layer;
gRNFL=
global retinal nerve fiber layer;
INL=
inner nuclear layer;
IPL=
inner plexiform layer;
LCLA=
low-contrast letter acuity;
MD=
mean diffusivity;
mfVEP=
multifocal visual evoked potentials;
MS=
multiple sclerosis;
NON=
no history of optic neuritis;
OCT=
optical coherence tomography;
ON=
optic neuritis;
ONL=
outer nuclear layer;
OPL=
outer plexiform layer;
OR=
optic radiations;
OT=
optic tracts;
PIS=
photoreceptor inner segment;
RD=
radial diffusivity;
RGC=
retinal ganglion cells;
RNFL=
retinal nerve fiber layer;
RRMS=
relapsing-remitting multiple sclerosis;
tRNFL=
temporal retinal nerve fiber layer;
VA=
visual acuity

Footnotes

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

  • Editorial, page 2152

  • Supplemental data at Neurology.org

  • Received October 23, 2013.
  • Accepted in final form February 3, 2014.
  • © 2014 American Academy of Neurology
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