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September 11, 2018; 91 (11) Article

Retinal thinning associates with nigral dopaminergic loss in de novo Parkinson disease

Jeeyun Ahn, Jee-Young Lee, Tae Wan Kim, Eun Jin Yoon, Sohee Oh, Yu Kyeong Kim, Jong-Min Kim, Se Joon Woo, Ki Woong Kim, Beomseok Jeon
First published August 15, 2018, DOI: https://doi.org/10.1212/WNL.0000000000006157
Jeeyun Ahn
From the Departments of Ophthalmology (J.A., T.W.K.), Neurology (J.-Y.L.), Nuclear Medicine (E.J.Y., Y.K.K.), and Biomedical Statistics (S.O.), Seoul Metropolitan Government–Seoul National University Boramae Medical Center and Seoul National University College of Medicine; Departments of Neurology (J.M.K.), Ophthalmology (S.J.W.), and Psychiatry (K.W.K.), Seoul National University Bundang Hospital and Seoul National University College of Medicine; and Department of Neurology (B.J.), Seoul National University Hospital and Seoul National University College of Medicine, South Korea.
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Jee-Young Lee
From the Departments of Ophthalmology (J.A., T.W.K.), Neurology (J.-Y.L.), Nuclear Medicine (E.J.Y., Y.K.K.), and Biomedical Statistics (S.O.), Seoul Metropolitan Government–Seoul National University Boramae Medical Center and Seoul National University College of Medicine; Departments of Neurology (J.M.K.), Ophthalmology (S.J.W.), and Psychiatry (K.W.K.), Seoul National University Bundang Hospital and Seoul National University College of Medicine; and Department of Neurology (B.J.), Seoul National University Hospital and Seoul National University College of Medicine, South Korea.
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Tae Wan Kim
From the Departments of Ophthalmology (J.A., T.W.K.), Neurology (J.-Y.L.), Nuclear Medicine (E.J.Y., Y.K.K.), and Biomedical Statistics (S.O.), Seoul Metropolitan Government–Seoul National University Boramae Medical Center and Seoul National University College of Medicine; Departments of Neurology (J.M.K.), Ophthalmology (S.J.W.), and Psychiatry (K.W.K.), Seoul National University Bundang Hospital and Seoul National University College of Medicine; and Department of Neurology (B.J.), Seoul National University Hospital and Seoul National University College of Medicine, South Korea.
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Eun Jin Yoon
From the Departments of Ophthalmology (J.A., T.W.K.), Neurology (J.-Y.L.), Nuclear Medicine (E.J.Y., Y.K.K.), and Biomedical Statistics (S.O.), Seoul Metropolitan Government–Seoul National University Boramae Medical Center and Seoul National University College of Medicine; Departments of Neurology (J.M.K.), Ophthalmology (S.J.W.), and Psychiatry (K.W.K.), Seoul National University Bundang Hospital and Seoul National University College of Medicine; and Department of Neurology (B.J.), Seoul National University Hospital and Seoul National University College of Medicine, South Korea.
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Sohee Oh
From the Departments of Ophthalmology (J.A., T.W.K.), Neurology (J.-Y.L.), Nuclear Medicine (E.J.Y., Y.K.K.), and Biomedical Statistics (S.O.), Seoul Metropolitan Government–Seoul National University Boramae Medical Center and Seoul National University College of Medicine; Departments of Neurology (J.M.K.), Ophthalmology (S.J.W.), and Psychiatry (K.W.K.), Seoul National University Bundang Hospital and Seoul National University College of Medicine; and Department of Neurology (B.J.), Seoul National University Hospital and Seoul National University College of Medicine, South Korea.
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Yu Kyeong Kim
From the Departments of Ophthalmology (J.A., T.W.K.), Neurology (J.-Y.L.), Nuclear Medicine (E.J.Y., Y.K.K.), and Biomedical Statistics (S.O.), Seoul Metropolitan Government–Seoul National University Boramae Medical Center and Seoul National University College of Medicine; Departments of Neurology (J.M.K.), Ophthalmology (S.J.W.), and Psychiatry (K.W.K.), Seoul National University Bundang Hospital and Seoul National University College of Medicine; and Department of Neurology (B.J.), Seoul National University Hospital and Seoul National University College of Medicine, South Korea.
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Jong-Min Kim
From the Departments of Ophthalmology (J.A., T.W.K.), Neurology (J.-Y.L.), Nuclear Medicine (E.J.Y., Y.K.K.), and Biomedical Statistics (S.O.), Seoul Metropolitan Government–Seoul National University Boramae Medical Center and Seoul National University College of Medicine; Departments of Neurology (J.M.K.), Ophthalmology (S.J.W.), and Psychiatry (K.W.K.), Seoul National University Bundang Hospital and Seoul National University College of Medicine; and Department of Neurology (B.J.), Seoul National University Hospital and Seoul National University College of Medicine, South Korea.
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Se Joon Woo
From the Departments of Ophthalmology (J.A., T.W.K.), Neurology (J.-Y.L.), Nuclear Medicine (E.J.Y., Y.K.K.), and Biomedical Statistics (S.O.), Seoul Metropolitan Government–Seoul National University Boramae Medical Center and Seoul National University College of Medicine; Departments of Neurology (J.M.K.), Ophthalmology (S.J.W.), and Psychiatry (K.W.K.), Seoul National University Bundang Hospital and Seoul National University College of Medicine; and Department of Neurology (B.J.), Seoul National University Hospital and Seoul National University College of Medicine, South Korea.
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Ki Woong Kim
From the Departments of Ophthalmology (J.A., T.W.K.), Neurology (J.-Y.L.), Nuclear Medicine (E.J.Y., Y.K.K.), and Biomedical Statistics (S.O.), Seoul Metropolitan Government–Seoul National University Boramae Medical Center and Seoul National University College of Medicine; Departments of Neurology (J.M.K.), Ophthalmology (S.J.W.), and Psychiatry (K.W.K.), Seoul National University Bundang Hospital and Seoul National University College of Medicine; and Department of Neurology (B.J.), Seoul National University Hospital and Seoul National University College of Medicine, South Korea.
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Beomseok Jeon
From the Departments of Ophthalmology (J.A., T.W.K.), Neurology (J.-Y.L.), Nuclear Medicine (E.J.Y., Y.K.K.), and Biomedical Statistics (S.O.), Seoul Metropolitan Government–Seoul National University Boramae Medical Center and Seoul National University College of Medicine; Departments of Neurology (J.M.K.), Ophthalmology (S.J.W.), and Psychiatry (K.W.K.), Seoul National University Bundang Hospital and Seoul National University College of Medicine; and Department of Neurology (B.J.), Seoul National University Hospital and Seoul National University College of Medicine, South Korea.
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Citation
Retinal thinning associates with nigral dopaminergic loss in de novo Parkinson disease
Jeeyun Ahn, Jee-Young Lee, Tae Wan Kim, Eun Jin Yoon, Sohee Oh, Yu Kyeong Kim, Jong-Min Kim, Se Joon Woo, Ki Woong Kim, Beomseok Jeon
Neurology Sep 2018, 91 (11) e1003-e1012; DOI: 10.1212/WNL.0000000000006157

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Abstract

Objective To analyze the relationship between retinal thinning and nigral dopaminergic loss in de novo Parkinson disease (PD).

Methods Forty-nine patients with PD and 54 age-matched controls were analyzed. Ophthalmologic examination and macula optical coherence tomography scans were performed with additional microperimetry, N-(3-[18F]fluoropropyl)-2-carbomethoxy-3-(4-iodophenyl) nortropane PET, and 3T MRI scans were done in patients with PD only. Retinal layer thickness and volume were measured in subfields of the 1-, 2.22-, and 3.45-mm Early Treatment of Diabetic Retinopathy Study circle and compared in patients with PD and controls. Correlation of inner retinal layer thinning with microperimetric response was examined in patients with PD, and the relationships between retinal layer thickness and dopamine transporter densities in the ipsilateral caudate, anterior and posterior putamen, and substantia nigra were analyzed.

Results Retinal layer thinning was observed in the temporal and inferior 2.22-mm sectors (false discovery rate–adjusted p < 0.05) of drug-naive patients with PD, particularly the inner plexiform and ganglion cell layers. The thickness of these layers in the inferior 2.22-mm sector showed a negative correlation with the Hoehn and Yahr stage (p = 0.032 and 0.014, respectively). There was positive correlation between macular sensitivity and retinal layer thickness in all 3.45-mm sectors, the superior 2.22-mm sector, and 1-mm circle (p < 0.05 for all). There was an association between retinal thinning and dopaminergic loss in the left substantia nigra (false discovery rate–adjusted p < 0.001).

Conclusion Retinal thinning is present in the early stages of PD, correlates with disease severity, and may be linked to nigral dopaminergic degeneration. Retinal imaging may be useful for detection of pathologic changes occurring in early PD.

Glossary

DAT=
dopamine transporter;
ETDRS=
Early Treatment of Diabetic Retinopathy Study;
FDR=
false discovery rate;
18F-FP-CIT=
N-(3-[18F]fluoropropyl)-2-carbomethoxy-3-(4-iodophenyl) nortropane;
GCL=
ganglion cell layer;
GEE=
generalized estimating equation;
HY=
Hoehn and Yahr;
IPL=
inner plexiform layer;
KLoSHA=
Korean Longitudinal Study on Health and Aging;
LMM=
linear mixed-effects model;
MP=
microperimetry;
NFL=
nerve fiber layer;
OCT=
optical coherence tomography;
ONL=
outer nuclear layer;
PD=
Parkinson disease;
SD=
spectral domain;
WRL=
whole retinal layer

Footnotes

  • ↵* These authors equally contributed to this work.

  • 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.

  • Editorial, page 493

  • Received November 21, 2017.
  • Accepted in final form June 7, 2018.
  • © 2018 American Academy of Neurology
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