Retinal Optical Coherence Tomography Features Associated With Incident and Prevalent Parkinson Disease

doi:10.1212/WNL.0000000000207727

. 2023 Oct 17;101(16):e1581-e1593.

doi: 10.1212/WNL.0000000000207727. Epub 2023 Aug 21.

Retinal Optical Coherence Tomography Features Associated With Incident and Prevalent Parkinson Disease

Siegfried Karl Wagner¹, David Romero-Bascones², Mario Cortina-Borja², Dominic J Williamson², Robbert R Struyven², Yukun Zhou², Salil Patel², Rimona S Weil², Chrystalina A Antoniades², Eric J Topol², Edward Korot², Paul J Foster², Konstantinos Balaskas², Unai Ayala², Maitane Barrenechea², Iñigo Gabilondo², Anthony H V Schapira², Anthony P Khawaja², Praveen J Patel², Jugnoo S Rahi², Alastair K Denniston², Axel Petzold², Pearse Andrew Keane²; for UK Biobank Eye & Vision Consortium

Collaborators, Affiliations

Collaborators

for UK Biobank Eye & Vision Consortium:
Naomi Allen, Tariq Aslam, Denize Atan, Sarah Barman, Jenny H Barrett, Paul Bishop, Graeme Black, Tasanee Braithwaite, Roxana O Carare, Usha Chakravarthy, Michelle Chan, Sharon Yl Chua, Alexander Day, Parul Desai, Bal Dhillon, Andrew D Dick, Alexander Doney, Cathy Egan, Sarah Ennis, Marcus Fruttiger, John Ej Gallacher, David F Garway-Heath, Jane Gibson, Jeremy A Guggeinheim, Chris J Hammond, Alison Hardcastle, Simon P Harding, Ruth E Hogg, Pirro Hysi, Sir Peng T Khaw, Gerassimos Lascaratos, Thomas Littlejohns, Andrew J Lotery, Robert Luben, Phil Luthert, Tom Macgillivray, Sarah Mackie, Bernadette McGuiness, Gareth J McKay, Marin McKibbin, Tony Moore, James E Morgan, Eoin O'Sullivan, Richard Oram, Chris G Owen, Euan Paterson, Tunde Peto, Alicja R Rudnicka, Naveed Sattar, Jay Self, Panagiotis Sergouniotis, Sobha Sivaprasad, David Steel, Irene Stratton, Nicholas Strouthidis, Cathie Sudlow, Zihan Sun, Robyn Tapp, Dhanes Thomas, Emanuele Trucco, Adnan Tufail, Veronique Vitart, Ananth C Viswanathan, Mike Weedon, Cathy Williams, Katie Williams, Jayne V Woodside, MaxM Yates, Jennifer Yip, Yalin Zheng

Affiliations

¹ From the Institute of Ophthalmology (S.K.W., D.J.W., R.R.S., Y.Z., P.J.F., K.B., A.P.K., P.J.P., J.S.R., A.P., P.A.K.), University College London; NIHR Biomedical Research Centre at Moorfields Eye Hospital and UCL Institute of Ophthalmology (S.K.W., D.R.-B., D.J.W., R.R.S., Y.Z., E.K., P.J.F., K.B., A.P.K., P.J.P., J.S.R., A.K.D., A.P., P.A.K.), London, United Kingdom; Biomedical Engineering Department (D.R.-B., E.K., U.A., M.B.), Faculty of Engineering (MU-ENG), Mondragon Unibertsitatea, Spain; Great Ormond Street Institute of Child Health (M.C.-B., J.S.R.), and Centre for Medical Image Computing (D.J.W., R.R.S., Y.Z.), Department of Computer Science, University College London; NeuroMetrology Lab (S.P., C.A.A.), Nuffield Department of Clinical Neurosciences, University of Oxford; Dementia Research Centre (R.S.W.), University College London, United Kingdom; Department of Molecular Medicine (E.J.T.), Scripps Research, La Jolla, CA; Byers Eye Institute (E.K.), Stanford University, Palo Alto, CA; Biocruces Bizkaia Health Research Institute (I.G.), Barakaldo; IKERBASQUE: The Basque Foundation for Science (I.G.), Bilbao, Spain; Department of Clinical and Movement Neurosciences (A.H.V.S.), UCL Queen Square Institute of Neurology; Great Ormond Street Hospital NHS Foundation Trust (J.S.R.); Ulverscroft Vision Research Group (J.S.R.), University College London; NIHR Biomedical Research Centre at UCL Great Ormond Street Institute of Child Health and Great Ormond Street Hospital (J.S.R.), London; University of Birmingham (A.K.D.); University Hospitals Birmingham NHS Foundation Trust (A.K.D.); NIHR Birmingham Biomedical Research Centre (A.K.D.), University of Birmingham; and Queen Square Institute of Neurology (A.P.), University College London, United Kingdom. s.wagner@ucl.ac.uk.
² From the Institute of Ophthalmology (S.K.W., D.J.W., R.R.S., Y.Z., P.J.F., K.B., A.P.K., P.J.P., J.S.R., A.P., P.A.K.), University College London; NIHR Biomedical Research Centre at Moorfields Eye Hospital and UCL Institute of Ophthalmology (S.K.W., D.R.-B., D.J.W., R.R.S., Y.Z., E.K., P.J.F., K.B., A.P.K., P.J.P., J.S.R., A.K.D., A.P., P.A.K.), London, United Kingdom; Biomedical Engineering Department (D.R.-B., E.K., U.A., M.B.), Faculty of Engineering (MU-ENG), Mondragon Unibertsitatea, Spain; Great Ormond Street Institute of Child Health (M.C.-B., J.S.R.), and Centre for Medical Image Computing (D.J.W., R.R.S., Y.Z.), Department of Computer Science, University College London; NeuroMetrology Lab (S.P., C.A.A.), Nuffield Department of Clinical Neurosciences, University of Oxford; Dementia Research Centre (R.S.W.), University College London, United Kingdom; Department of Molecular Medicine (E.J.T.), Scripps Research, La Jolla, CA; Byers Eye Institute (E.K.), Stanford University, Palo Alto, CA; Biocruces Bizkaia Health Research Institute (I.G.), Barakaldo; IKERBASQUE: The Basque Foundation for Science (I.G.), Bilbao, Spain; Department of Clinical and Movement Neurosciences (A.H.V.S.), UCL Queen Square Institute of Neurology; Great Ormond Street Hospital NHS Foundation Trust (J.S.R.); Ulverscroft Vision Research Group (J.S.R.), University College London; NIHR Biomedical Research Centre at UCL Great Ormond Street Institute of Child Health and Great Ormond Street Hospital (J.S.R.), London; University of Birmingham (A.K.D.); University Hospitals Birmingham NHS Foundation Trust (A.K.D.); NIHR Birmingham Biomedical Research Centre (A.K.D.), University of Birmingham; and Queen Square Institute of Neurology (A.P.), University College London, United Kingdom.

PMID: 37604659
PMCID: PMC10585674
DOI: 10.1212/WNL.0000000000207727

Retinal Optical Coherence Tomography Features Associated With Incident and Prevalent Parkinson Disease

Siegfried Karl Wagner et al. Neurology. 2023.

. 2023 Oct 17;101(16):e1581-e1593.

doi: 10.1212/WNL.0000000000207727. Epub 2023 Aug 21.

Authors

Collaborators

for UK Biobank Eye & Vision Consortium:
Naomi Allen, Tariq Aslam, Denize Atan, Sarah Barman, Jenny H Barrett, Paul Bishop, Graeme Black, Tasanee Braithwaite, Roxana O Carare, Usha Chakravarthy, Michelle Chan, Sharon Yl Chua, Alexander Day, Parul Desai, Bal Dhillon, Andrew D Dick, Alexander Doney, Cathy Egan, Sarah Ennis, Marcus Fruttiger, John Ej Gallacher, David F Garway-Heath, Jane Gibson, Jeremy A Guggeinheim, Chris J Hammond, Alison Hardcastle, Simon P Harding, Ruth E Hogg, Pirro Hysi, Sir Peng T Khaw, Gerassimos Lascaratos, Thomas Littlejohns, Andrew J Lotery, Robert Luben, Phil Luthert, Tom Macgillivray, Sarah Mackie, Bernadette McGuiness, Gareth J McKay, Marin McKibbin, Tony Moore, James E Morgan, Eoin O'Sullivan, Richard Oram, Chris G Owen, Euan Paterson, Tunde Peto, Alicja R Rudnicka, Naveed Sattar, Jay Self, Panagiotis Sergouniotis, Sobha Sivaprasad, David Steel, Irene Stratton, Nicholas Strouthidis, Cathie Sudlow, Zihan Sun, Robyn Tapp, Dhanes Thomas, Emanuele Trucco, Adnan Tufail, Veronique Vitart, Ananth C Viswanathan, Mike Weedon, Cathy Williams, Katie Williams, Jayne V Woodside, MaxM Yates, Jennifer Yip, Yalin Zheng

Affiliations

¹ From the Institute of Ophthalmology (S.K.W., D.J.W., R.R.S., Y.Z., P.J.F., K.B., A.P.K., P.J.P., J.S.R., A.P., P.A.K.), University College London; NIHR Biomedical Research Centre at Moorfields Eye Hospital and UCL Institute of Ophthalmology (S.K.W., D.R.-B., D.J.W., R.R.S., Y.Z., E.K., P.J.F., K.B., A.P.K., P.J.P., J.S.R., A.K.D., A.P., P.A.K.), London, United Kingdom; Biomedical Engineering Department (D.R.-B., E.K., U.A., M.B.), Faculty of Engineering (MU-ENG), Mondragon Unibertsitatea, Spain; Great Ormond Street Institute of Child Health (M.C.-B., J.S.R.), and Centre for Medical Image Computing (D.J.W., R.R.S., Y.Z.), Department of Computer Science, University College London; NeuroMetrology Lab (S.P., C.A.A.), Nuffield Department of Clinical Neurosciences, University of Oxford; Dementia Research Centre (R.S.W.), University College London, United Kingdom; Department of Molecular Medicine (E.J.T.), Scripps Research, La Jolla, CA; Byers Eye Institute (E.K.), Stanford University, Palo Alto, CA; Biocruces Bizkaia Health Research Institute (I.G.), Barakaldo; IKERBASQUE: The Basque Foundation for Science (I.G.), Bilbao, Spain; Department of Clinical and Movement Neurosciences (A.H.V.S.), UCL Queen Square Institute of Neurology; Great Ormond Street Hospital NHS Foundation Trust (J.S.R.); Ulverscroft Vision Research Group (J.S.R.), University College London; NIHR Biomedical Research Centre at UCL Great Ormond Street Institute of Child Health and Great Ormond Street Hospital (J.S.R.), London; University of Birmingham (A.K.D.); University Hospitals Birmingham NHS Foundation Trust (A.K.D.); NIHR Birmingham Biomedical Research Centre (A.K.D.), University of Birmingham; and Queen Square Institute of Neurology (A.P.), University College London, United Kingdom. s.wagner@ucl.ac.uk.
² From the Institute of Ophthalmology (S.K.W., D.J.W., R.R.S., Y.Z., P.J.F., K.B., A.P.K., P.J.P., J.S.R., A.P., P.A.K.), University College London; NIHR Biomedical Research Centre at Moorfields Eye Hospital and UCL Institute of Ophthalmology (S.K.W., D.R.-B., D.J.W., R.R.S., Y.Z., E.K., P.J.F., K.B., A.P.K., P.J.P., J.S.R., A.K.D., A.P., P.A.K.), London, United Kingdom; Biomedical Engineering Department (D.R.-B., E.K., U.A., M.B.), Faculty of Engineering (MU-ENG), Mondragon Unibertsitatea, Spain; Great Ormond Street Institute of Child Health (M.C.-B., J.S.R.), and Centre for Medical Image Computing (D.J.W., R.R.S., Y.Z.), Department of Computer Science, University College London; NeuroMetrology Lab (S.P., C.A.A.), Nuffield Department of Clinical Neurosciences, University of Oxford; Dementia Research Centre (R.S.W.), University College London, United Kingdom; Department of Molecular Medicine (E.J.T.), Scripps Research, La Jolla, CA; Byers Eye Institute (E.K.), Stanford University, Palo Alto, CA; Biocruces Bizkaia Health Research Institute (I.G.), Barakaldo; IKERBASQUE: The Basque Foundation for Science (I.G.), Bilbao, Spain; Department of Clinical and Movement Neurosciences (A.H.V.S.), UCL Queen Square Institute of Neurology; Great Ormond Street Hospital NHS Foundation Trust (J.S.R.); Ulverscroft Vision Research Group (J.S.R.), University College London; NIHR Biomedical Research Centre at UCL Great Ormond Street Institute of Child Health and Great Ormond Street Hospital (J.S.R.), London; University of Birmingham (A.K.D.); University Hospitals Birmingham NHS Foundation Trust (A.K.D.); NIHR Birmingham Biomedical Research Centre (A.K.D.), University of Birmingham; and Queen Square Institute of Neurology (A.P.), University College London, United Kingdom.

PMID: 37604659
PMCID: PMC10585674
DOI: 10.1212/WNL.0000000000207727

Abstract

Background and objectives: Cadaveric studies have shown disease-related neurodegeneration and other morphological abnormalities in the retina of individuals with Parkinson disease (PD); however, it remains unclear whether this can be reliably detected with in vivo imaging. We investigated inner retinal anatomy, measured using optical coherence tomography (OCT), in prevalent PD and subsequently assessed the association of these markers with the development of PD using a prospective research cohort.

Methods: This cross-sectional analysis used data from 2 studies. For the detection of retinal markers in prevalent PD, we used data from AlzEye, a retrospective cohort of 154,830 patients aged 40 years and older attending secondary care ophthalmic hospitals in London, United Kingdom, between 2008 and 2018. For the evaluation of retinal markers in incident PD, we used data from UK Biobank, a prospective population-based cohort where 67,311 volunteers aged 40-69 years were recruited between 2006 and 2010 and underwent retinal imaging. Macular retinal nerve fiber layer (mRNFL), ganglion cell-inner plexiform layer (GCIPL), and inner nuclear layer (INL) thicknesses were extracted from fovea-centered OCT. Linear mixed-effects models were fitted to examine the association between prevalent PD and retinal thicknesses. Hazard ratios for the association between time to PD diagnosis and retinal thicknesses were estimated using frailty models.

Results: Within the AlzEye cohort, there were 700 individuals with prevalent PD and 105,770 controls (mean age 65.5 ± 13.5 years, 51.7% female). Individuals with prevalent PD had thinner GCIPL (-2.12 μm, 95% CI -3.17 to -1.07, p = 8.2 × 10^-5) and INL (-0.99 μm, 95% CI -1.52 to -0.47, p = 2.1 × 10^-4). The UK Biobank included 50,405 participants (mean age 56.1 ± 8.2 years, 54.7% female), of whom 53 developed PD at a mean of 2,653 ± 851 days. Thinner GCIPL (hazard ratio [HR] 0.62 per SD increase, 95% CI 0.46-0.84, p = 0.002) and thinner INL (HR 0.70, 95% CI 0.51-0.96, p = 0.026) were also associated with incident PD.

Discussion: Individuals with PD have reduced thickness of the INL and GCIPL of the retina. Involvement of these layers several years before clinical presentation highlight a potential role for retinal imaging for at-risk stratification of PD.

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Conflict of interest statement

S.K. Wagner is funded by the Medical Research Council (MR/TR000953/1) and the Rank Prize. D. Romero-Bascones received funding from the Basque Health Department (2022333011). M. Cortina-Borja, D.J. Williamson, R.R. Struyven, Y. Zhou, and S. Patel report no disclosures. R.S. Weil is supported by a Wellcome Clinical Research Career Development Fellowship (205167/Z/16/Z). C.A. Antoniades receives funding from the NIHR, Biomedical Research Centre (BRC), UCB-OXford collaborative grant, and Merck. E.J. Topol and E. Korot report no disclosures. P.J. Foster receives salary support from NIHR through a grant to the Biomedical Research Centre at Moorfields Eye Hospital and UCL Institute of Ophthalmology. K. Balaskas reports no disclosures. U. Ayala receives funding from the Basque Health Department (2022333011). M. Barrenechea receives funding from the Basque Health Department (2022333011). I. Gabilondo receives funding from the Basque Health Department (2022333011). A.H.V. Schapira reports no disclosures. A.P. Khawaja is supported by a UK Research & Innovation Future Leaders Fellowship (MR/T040912/1), an Alcon Research Institute Young Investigator Award and a Lister Institute Fellowship. A.P. Khawaja receives salary support from NIHR through a grant to the Biomedical Research Centre at Moorfields Eye Hospital and UCL Institute of Ophthalmology. P.J. Patel, J.S. Rahi, and A.K. Denniston report no disclosures. A. Petzold receives salary support from NIHR through a grant to the Biomedical Research Centre at Moorfields Eye Hospital and UCL Institute of Ophthalmology. P.A. Keane is supported by a UK Research & Innovation Future Leaders Fellowship (MR/T019050/1). P.A. Keane receives salary support from NIHR through a grant to the Biomedical Research Centre at Moorfields Eye Hospital and UCL Institute of Ophthalmology. Additional support was from the NIHR Birmingham, Great Ormond Street, Moorfields, Oxford, and University College London Hospitals Biomedical Research Centres. Go to Neurology.org/N for full disclosures.

Figures

**Figure 1. Flowchart Detailing Inclusion and Exclusion of Participants in Both AlzEye and UK Biobank**
PD = Parkinson disease.

**Figure 2. Distribution of Retinal Sublayer Thicknesses in AlzEye and UK Biobank**
Raincloud plots consisting of a density, box-whisker, and scatter plots for AlzEye (A–C) and UK Biobank (D–F) for individual retinal sublayers. Scatter points represent the mean of both eyes (where available) per participant. To improve visibility, a random 2% of control participants are illustrated.

**Figure 3. Summary of Findings for Prevalent and Incident Parkinson Disease**
Values are shown per parafoveal region and for the average of all inner segments (small donut). The effect measure corresponds to a color scale with warm colors indicating lower numbers. GCIPL = macular ganglion cell–inner plexiform layer; II = inner inferior; IN = inner nasal; INL = inner nuclear layer; IS = inner superior; IT = inner temporal; mRNFL = macular retinal nerve fiber layer.

**Figure 4. Illustration of Cell Type Distribution in the Retina**
An example optical coherence tomography scan of the nasal macula adjacent to schematic detailing interactions with dopaminergic amacrine cells. Dopaminergic cells (1) have dense plexi positioned throughout the inner plexiform and inner nuclear layers. They are presynaptic to amacrine AII cells (2), and some dopaminergic processes project toward the photoreceptor layer where they interact with horizontal cells (3). They are postsynaptic to bipolar cells (4). Previous work has demonstrated aggregation of proteins, including α synuclein, within the inner nuclear layer (5), which could result in impairment of nearby ganglion cells. GCIPL = macular ganglion cell–inner plexiform layer; INL = inner nuclear layer; PRL = photoreceptor layer; RNFL = retinal nerve fiber layer; RPE = retinal pigment epithelium.

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References

1. Biondetti E, Santin MD, Valabrègue R, et al. . The spatiotemporal changes in dopamine, neuromelanin and iron characterizing Parkinson's disease. Brain. 2021;144(10):3114-3125. doi:10.1093/brain/awab191 - DOI - PMC - PubMed
1. Morrish PK, Sawle GV, Brooks DJ. An [18F]dopa-PET and clinical study of the rate of progression in Parkinson's disease. Brain. 1996;119(2):585-591. doi:10.1093/brain/119.2.585 - DOI - PubMed
1. Sun J, Lai Z, Ma J, et al. . Quantitative evaluation of iron content in idiopathic rapid eye movement sleep behavior disorder. Mov Disord. 2020;35(3):478-485. doi:10.1002/mds.27929 - DOI - PubMed
1. Iranzo A, Valldeoriola F, Lomeña F, et al. . Serial dopamine transporter imaging of nigrostriatal function in patients with idiopathic rapid-eye-movement sleep behaviour disorder: a prospective study. Lancet Neurol. 2011;10(9):797-805. doi:10.1016/s1474-4422(11)70152-1 - DOI - PubMed
1. Lee JY, Martin-Bastida A, Murueta-Goyena A, et al. . Multimodal brain and retinal imaging of dopaminergic degeneration in Parkinson disease. Nat Rev Neurol. 2022;18(4):203-220. doi:10.1038/s41582-022-00618-9 - DOI - PubMed

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[1] Biondetti E, Santin MD, Valabrègue R, et al. . The spatiotemporal changes in dopamine, neuromelanin and iron characterizing Parkinson's disease. Brain. 2021;144(10):3114-3125. doi:10.1093/brain/awab191 - DOI - PMC - PubMed

[2] Biondetti E, Santin MD, Valabrègue R, et al. . The spatiotemporal changes in dopamine, neuromelanin and iron characterizing Parkinson's disease. Brain. 2021;144(10):3114-3125. doi:10.1093/brain/awab191 - DOI - PMC - PubMed

[3] Morrish PK, Sawle GV, Brooks DJ. An [18F]dopa-PET and clinical study of the rate of progression in Parkinson's disease. Brain. 1996;119(2):585-591. doi:10.1093/brain/119.2.585 - DOI - PubMed

[4] Morrish PK, Sawle GV, Brooks DJ. An [18F]dopa-PET and clinical study of the rate of progression in Parkinson's disease. Brain. 1996;119(2):585-591. doi:10.1093/brain/119.2.585 - DOI - PubMed

[5] Sun J, Lai Z, Ma J, et al. . Quantitative evaluation of iron content in idiopathic rapid eye movement sleep behavior disorder. Mov Disord. 2020;35(3):478-485. doi:10.1002/mds.27929 - DOI - PubMed

[6] Sun J, Lai Z, Ma J, et al. . Quantitative evaluation of iron content in idiopathic rapid eye movement sleep behavior disorder. Mov Disord. 2020;35(3):478-485. doi:10.1002/mds.27929 - DOI - PubMed

[7] Iranzo A, Valldeoriola F, Lomeña F, et al. . Serial dopamine transporter imaging of nigrostriatal function in patients with idiopathic rapid-eye-movement sleep behaviour disorder: a prospective study. Lancet Neurol. 2011;10(9):797-805. doi:10.1016/s1474-4422(11)70152-1 - DOI - PubMed

[8] Iranzo A, Valldeoriola F, Lomeña F, et al. . Serial dopamine transporter imaging of nigrostriatal function in patients with idiopathic rapid-eye-movement sleep behaviour disorder: a prospective study. Lancet Neurol. 2011;10(9):797-805. doi:10.1016/s1474-4422(11)70152-1 - DOI - PubMed

[9] Lee JY, Martin-Bastida A, Murueta-Goyena A, et al. . Multimodal brain and retinal imaging of dopaminergic degeneration in Parkinson disease. Nat Rev Neurol. 2022;18(4):203-220. doi:10.1038/s41582-022-00618-9 - DOI - PubMed

[10] Lee JY, Martin-Bastida A, Murueta-Goyena A, et al. . Multimodal brain and retinal imaging of dopaminergic degeneration in Parkinson disease. Nat Rev Neurol. 2022;18(4):203-220. doi:10.1038/s41582-022-00618-9 - DOI - PubMed

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Retinal Optical Coherence Tomography Features Associated With Incident and Prevalent Parkinson Disease

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Retinal Optical Coherence Tomography Features Associated With Incident and Prevalent Parkinson Disease

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