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February 2020; 10 (1) ResearchOpen Access

Visual tests predict dementia risk in Parkinson disease

Louise-Ann Leyland, Fion D. Bremner, Ribeya Mahmood, View ORCID ProfileSam Hewitt, Marion Durteste, Molly R.E. Cartlidge, Michelle M.-M. Lai, Luke E. Miller, Ayse P. Saygin, Pearse A. Keane, Anette E. Schrag, Rimona S. Weil
First published September 18, 2019, DOI: https://doi.org/10.1212/CPJ.0000000000000719
Louise-Ann Leyland
Dementia Research Centre (L-AL, RM, RSW), Institute of Neurology, University College London, United Kingdom; Neuro-ophthalmology (FDB, MM-ML), National Hospital for Neurology and Neurosurgery, University College London Hospitals, London, United Kingdom; Institute of Neurology (SH, MD, MREC), University College London, UCL, United Kingdom; School of Biomedical Sciences (MREC), Biological Sciences, Leeds University, United Kingdom; ImpAct (LEM), Lyon Neuroscience Research Center, France; Department of Cognitive Science (APS), University of California, San Diego; Kavli Institute for Brain and Mind (APS), University of California, San Diego; Institute of Ophthalmology (PAK), UCL, United Kingdom; Moorfields Eye Hospital (PAK), London, United Kingdom; Department of Clinical Neuroscience (AES), Institute of Neurology, UCL Hampstead Campus, London, United Kingdom; Movement Disorders Consortium (AES, RSW), UCL, United Kingdom; and The Wellcome Centre for Human Neuroimaging (RSW), Institute of Neurology, University College London, United Kingdom.
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Fion D. Bremner
Dementia Research Centre (L-AL, RM, RSW), Institute of Neurology, University College London, United Kingdom; Neuro-ophthalmology (FDB, MM-ML), National Hospital for Neurology and Neurosurgery, University College London Hospitals, London, United Kingdom; Institute of Neurology (SH, MD, MREC), University College London, UCL, United Kingdom; School of Biomedical Sciences (MREC), Biological Sciences, Leeds University, United Kingdom; ImpAct (LEM), Lyon Neuroscience Research Center, France; Department of Cognitive Science (APS), University of California, San Diego; Kavli Institute for Brain and Mind (APS), University of California, San Diego; Institute of Ophthalmology (PAK), UCL, United Kingdom; Moorfields Eye Hospital (PAK), London, United Kingdom; Department of Clinical Neuroscience (AES), Institute of Neurology, UCL Hampstead Campus, London, United Kingdom; Movement Disorders Consortium (AES, RSW), UCL, United Kingdom; and The Wellcome Centre for Human Neuroimaging (RSW), Institute of Neurology, University College London, United Kingdom.
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Ribeya Mahmood
Dementia Research Centre (L-AL, RM, RSW), Institute of Neurology, University College London, United Kingdom; Neuro-ophthalmology (FDB, MM-ML), National Hospital for Neurology and Neurosurgery, University College London Hospitals, London, United Kingdom; Institute of Neurology (SH, MD, MREC), University College London, UCL, United Kingdom; School of Biomedical Sciences (MREC), Biological Sciences, Leeds University, United Kingdom; ImpAct (LEM), Lyon Neuroscience Research Center, France; Department of Cognitive Science (APS), University of California, San Diego; Kavli Institute for Brain and Mind (APS), University of California, San Diego; Institute of Ophthalmology (PAK), UCL, United Kingdom; Moorfields Eye Hospital (PAK), London, United Kingdom; Department of Clinical Neuroscience (AES), Institute of Neurology, UCL Hampstead Campus, London, United Kingdom; Movement Disorders Consortium (AES, RSW), UCL, United Kingdom; and The Wellcome Centre for Human Neuroimaging (RSW), Institute of Neurology, University College London, United Kingdom.
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Sam Hewitt
Dementia Research Centre (L-AL, RM, RSW), Institute of Neurology, University College London, United Kingdom; Neuro-ophthalmology (FDB, MM-ML), National Hospital for Neurology and Neurosurgery, University College London Hospitals, London, United Kingdom; Institute of Neurology (SH, MD, MREC), University College London, UCL, United Kingdom; School of Biomedical Sciences (MREC), Biological Sciences, Leeds University, United Kingdom; ImpAct (LEM), Lyon Neuroscience Research Center, France; Department of Cognitive Science (APS), University of California, San Diego; Kavli Institute for Brain and Mind (APS), University of California, San Diego; Institute of Ophthalmology (PAK), UCL, United Kingdom; Moorfields Eye Hospital (PAK), London, United Kingdom; Department of Clinical Neuroscience (AES), Institute of Neurology, UCL Hampstead Campus, London, United Kingdom; Movement Disorders Consortium (AES, RSW), UCL, United Kingdom; and The Wellcome Centre for Human Neuroimaging (RSW), Institute of Neurology, University College London, United Kingdom.
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Marion Durteste
Dementia Research Centre (L-AL, RM, RSW), Institute of Neurology, University College London, United Kingdom; Neuro-ophthalmology (FDB, MM-ML), National Hospital for Neurology and Neurosurgery, University College London Hospitals, London, United Kingdom; Institute of Neurology (SH, MD, MREC), University College London, UCL, United Kingdom; School of Biomedical Sciences (MREC), Biological Sciences, Leeds University, United Kingdom; ImpAct (LEM), Lyon Neuroscience Research Center, France; Department of Cognitive Science (APS), University of California, San Diego; Kavli Institute for Brain and Mind (APS), University of California, San Diego; Institute of Ophthalmology (PAK), UCL, United Kingdom; Moorfields Eye Hospital (PAK), London, United Kingdom; Department of Clinical Neuroscience (AES), Institute of Neurology, UCL Hampstead Campus, London, United Kingdom; Movement Disorders Consortium (AES, RSW), UCL, United Kingdom; and The Wellcome Centre for Human Neuroimaging (RSW), Institute of Neurology, University College London, United Kingdom.
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Molly R.E. Cartlidge
Dementia Research Centre (L-AL, RM, RSW), Institute of Neurology, University College London, United Kingdom; Neuro-ophthalmology (FDB, MM-ML), National Hospital for Neurology and Neurosurgery, University College London Hospitals, London, United Kingdom; Institute of Neurology (SH, MD, MREC), University College London, UCL, United Kingdom; School of Biomedical Sciences (MREC), Biological Sciences, Leeds University, United Kingdom; ImpAct (LEM), Lyon Neuroscience Research Center, France; Department of Cognitive Science (APS), University of California, San Diego; Kavli Institute for Brain and Mind (APS), University of California, San Diego; Institute of Ophthalmology (PAK), UCL, United Kingdom; Moorfields Eye Hospital (PAK), London, United Kingdom; Department of Clinical Neuroscience (AES), Institute of Neurology, UCL Hampstead Campus, London, United Kingdom; Movement Disorders Consortium (AES, RSW), UCL, United Kingdom; and The Wellcome Centre for Human Neuroimaging (RSW), Institute of Neurology, University College London, United Kingdom.
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Michelle M.-M. Lai
Dementia Research Centre (L-AL, RM, RSW), Institute of Neurology, University College London, United Kingdom; Neuro-ophthalmology (FDB, MM-ML), National Hospital for Neurology and Neurosurgery, University College London Hospitals, London, United Kingdom; Institute of Neurology (SH, MD, MREC), University College London, UCL, United Kingdom; School of Biomedical Sciences (MREC), Biological Sciences, Leeds University, United Kingdom; ImpAct (LEM), Lyon Neuroscience Research Center, France; Department of Cognitive Science (APS), University of California, San Diego; Kavli Institute for Brain and Mind (APS), University of California, San Diego; Institute of Ophthalmology (PAK), UCL, United Kingdom; Moorfields Eye Hospital (PAK), London, United Kingdom; Department of Clinical Neuroscience (AES), Institute of Neurology, UCL Hampstead Campus, London, United Kingdom; Movement Disorders Consortium (AES, RSW), UCL, United Kingdom; and The Wellcome Centre for Human Neuroimaging (RSW), Institute of Neurology, University College London, United Kingdom.
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Luke E. Miller
Dementia Research Centre (L-AL, RM, RSW), Institute of Neurology, University College London, United Kingdom; Neuro-ophthalmology (FDB, MM-ML), National Hospital for Neurology and Neurosurgery, University College London Hospitals, London, United Kingdom; Institute of Neurology (SH, MD, MREC), University College London, UCL, United Kingdom; School of Biomedical Sciences (MREC), Biological Sciences, Leeds University, United Kingdom; ImpAct (LEM), Lyon Neuroscience Research Center, France; Department of Cognitive Science (APS), University of California, San Diego; Kavli Institute for Brain and Mind (APS), University of California, San Diego; Institute of Ophthalmology (PAK), UCL, United Kingdom; Moorfields Eye Hospital (PAK), London, United Kingdom; Department of Clinical Neuroscience (AES), Institute of Neurology, UCL Hampstead Campus, London, United Kingdom; Movement Disorders Consortium (AES, RSW), UCL, United Kingdom; and The Wellcome Centre for Human Neuroimaging (RSW), Institute of Neurology, University College London, United Kingdom.
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Ayse P. Saygin
Dementia Research Centre (L-AL, RM, RSW), Institute of Neurology, University College London, United Kingdom; Neuro-ophthalmology (FDB, MM-ML), National Hospital for Neurology and Neurosurgery, University College London Hospitals, London, United Kingdom; Institute of Neurology (SH, MD, MREC), University College London, UCL, United Kingdom; School of Biomedical Sciences (MREC), Biological Sciences, Leeds University, United Kingdom; ImpAct (LEM), Lyon Neuroscience Research Center, France; Department of Cognitive Science (APS), University of California, San Diego; Kavli Institute for Brain and Mind (APS), University of California, San Diego; Institute of Ophthalmology (PAK), UCL, United Kingdom; Moorfields Eye Hospital (PAK), London, United Kingdom; Department of Clinical Neuroscience (AES), Institute of Neurology, UCL Hampstead Campus, London, United Kingdom; Movement Disorders Consortium (AES, RSW), UCL, United Kingdom; and The Wellcome Centre for Human Neuroimaging (RSW), Institute of Neurology, University College London, United Kingdom.
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Pearse A. Keane
Dementia Research Centre (L-AL, RM, RSW), Institute of Neurology, University College London, United Kingdom; Neuro-ophthalmology (FDB, MM-ML), National Hospital for Neurology and Neurosurgery, University College London Hospitals, London, United Kingdom; Institute of Neurology (SH, MD, MREC), University College London, UCL, United Kingdom; School of Biomedical Sciences (MREC), Biological Sciences, Leeds University, United Kingdom; ImpAct (LEM), Lyon Neuroscience Research Center, France; Department of Cognitive Science (APS), University of California, San Diego; Kavli Institute for Brain and Mind (APS), University of California, San Diego; Institute of Ophthalmology (PAK), UCL, United Kingdom; Moorfields Eye Hospital (PAK), London, United Kingdom; Department of Clinical Neuroscience (AES), Institute of Neurology, UCL Hampstead Campus, London, United Kingdom; Movement Disorders Consortium (AES, RSW), UCL, United Kingdom; and The Wellcome Centre for Human Neuroimaging (RSW), Institute of Neurology, University College London, United Kingdom.
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Anette E. Schrag
Dementia Research Centre (L-AL, RM, RSW), Institute of Neurology, University College London, United Kingdom; Neuro-ophthalmology (FDB, MM-ML), National Hospital for Neurology and Neurosurgery, University College London Hospitals, London, United Kingdom; Institute of Neurology (SH, MD, MREC), University College London, UCL, United Kingdom; School of Biomedical Sciences (MREC), Biological Sciences, Leeds University, United Kingdom; ImpAct (LEM), Lyon Neuroscience Research Center, France; Department of Cognitive Science (APS), University of California, San Diego; Kavli Institute for Brain and Mind (APS), University of California, San Diego; Institute of Ophthalmology (PAK), UCL, United Kingdom; Moorfields Eye Hospital (PAK), London, United Kingdom; Department of Clinical Neuroscience (AES), Institute of Neurology, UCL Hampstead Campus, London, United Kingdom; Movement Disorders Consortium (AES, RSW), UCL, United Kingdom; and The Wellcome Centre for Human Neuroimaging (RSW), Institute of Neurology, University College London, United Kingdom.
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Rimona S. Weil
Dementia Research Centre (L-AL, RM, RSW), Institute of Neurology, University College London, United Kingdom; Neuro-ophthalmology (FDB, MM-ML), National Hospital for Neurology and Neurosurgery, University College London Hospitals, London, United Kingdom; Institute of Neurology (SH, MD, MREC), University College London, UCL, United Kingdom; School of Biomedical Sciences (MREC), Biological Sciences, Leeds University, United Kingdom; ImpAct (LEM), Lyon Neuroscience Research Center, France; Department of Cognitive Science (APS), University of California, San Diego; Kavli Institute for Brain and Mind (APS), University of California, San Diego; Institute of Ophthalmology (PAK), UCL, United Kingdom; Moorfields Eye Hospital (PAK), London, United Kingdom; Department of Clinical Neuroscience (AES), Institute of Neurology, UCL Hampstead Campus, London, United Kingdom; Movement Disorders Consortium (AES, RSW), UCL, United Kingdom; and The Wellcome Centre for Human Neuroimaging (RSW), Institute of Neurology, University College London, United Kingdom.
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Citation
Visual tests predict dementia risk in Parkinson disease
Louise-Ann Leyland, Fion D. Bremner, Ribeya Mahmood, Sam Hewitt, Marion Durteste, Molly R.E. Cartlidge, Michelle M.-M. Lai, Luke E. Miller, Ayse P. Saygin, Pearse A. Keane, Anette E. Schrag, Rimona S. Weil
Neurol Clin Pract Feb 2020, 10 (1) 29-39; DOI: 10.1212/CPJ.0000000000000719

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Abstract

Objective To assess the role of visual measures and retinal volume to predict the risk of Parkinson disease (PD) dementia.

Methods In this cohort study, we collected visual, cognitive, and motor data in people with PD. Participants underwent ophthalmic examination, retinal imaging using optical coherence tomography, and visual assessment including acuity and contrast sensitivity and high-level visuoperception measures of skew tolerance and biological motion. We assessed the risk of PD dementia using a recently described algorithm that combines age at onset, sex, depression, motor scores, and baseline cognition.

Results One hundred forty-six people were included in the study (112 with PD and 34 age-matched controls). The mean disease duration was 4.1 (±2·5) years. None of these participants had dementia. Higher risk of dementia was associated with poorer performance in visual measures (acuity: ρ = 0.29, p = 0.0024; contrast sensitivity: ρ = −0.37, p < 0.0001; skew tolerance: ρ = −0.25, p = 0.0073; and biological motion: ρ = −0.26, p = 0.0054). In addition, higher risk of PD dementia was associated with thinner retinal structure in layers containing dopaminergic cells, measured as ganglion cell layer (GCL) and inner plexiform layer (IPL) thinning (ρ = −0.29, p = 0.0021; ρ = −0.33, p = 0.00044). These relationships were not seen for the retinal nerve fiber layer that does not contain dopaminergic cells and were not seen in unaffected controls.

Conclusion Visual measures and retinal structure in dopaminergic layers were related to risk of PD dementia. Our findings suggest that visual measures and retinal GCL and IPL volumes may be useful to predict the risk of dementia in PD.

Footnotes

  • Funding information and disclosures are provided at the end of the article. Full disclosure form information provided by the authors is available with the full text of this article at Neurology.org/cp.

  • The Article Processing Charge was funded by Wellcome Trust.

  • Received April 9, 2019.
  • Accepted June 7, 2019.
  • Copyright © 2019 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 License 4.0 (CC BY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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