Retinal thickness as a biomarker of cognitive impairment in manifest Huntington's disease.


Journal

Journal of neurology
ISSN: 1432-1459
Titre abrégé: J Neurol
Pays: Germany
ID NLM: 0423161

Informations de publication

Date de publication:
Aug 2023
Historique:
received: 05 03 2023
accepted: 07 04 2023
revised: 06 04 2023
medline: 17 7 2023
pubmed: 20 4 2023
entrez: 20 04 2023
Statut: ppublish

Résumé

Cognitive decline has been reported in premanifest and manifest Huntington's disease but reliable biomarkers are lacking. Inner retinal layer thickness seems to be a good biomarker of cognition in other neurodegenerative diseases. To explore the relationship between optical coherence tomography-derived metrics and global cognition in Huntington's Disease. Thirty-six patients with Huntington's disease (16 premanifest and 20 manifest) and 36 controls matched by age, sex, smoking status, and hypertension status underwent macular volumetric and peripapillary optical coherence tomography scans. Disease duration, motor status, global cognition and CAG repeats were recorded in patients. Group differences in imaging parameters and their association with clinical outcomes were analyzed using linear mixed-effect models. Premanifest and manifest Huntington's disease patients presented thinner retinal external limiting membrane-Bruch's membrane complex, and manifest patients had thinner temporal peripapillary retinal nerve fiber layer compared to controls. In manifest Huntington's disease, macular thickness was significantly associated with MoCA scores, inner nuclear layer showing the largest regression coefficients. This relationship was consistent after adjusting for age, sex, and education and p-value correction with False Discovery Rate. None of the retinal variables were related to Unified Huntington's Disease Rating Scale score, disease duration, or disease burden. Premanifest patients did not show a significant association between OCT-derived parameters and clinical outcomes in corrected models. In line with other neurodegenerative diseases, OCT is a potential biomarker of cognitive status in manifest HD. Future prospective studies are needed to evaluate OCT as a potential surrogate marker of cognitive decline in HD.

Sections du résumé

BACKGROUND BACKGROUND
Cognitive decline has been reported in premanifest and manifest Huntington's disease but reliable biomarkers are lacking. Inner retinal layer thickness seems to be a good biomarker of cognition in other neurodegenerative diseases.
OBJECTIVE OBJECTIVE
To explore the relationship between optical coherence tomography-derived metrics and global cognition in Huntington's Disease.
METHODS METHODS
Thirty-six patients with Huntington's disease (16 premanifest and 20 manifest) and 36 controls matched by age, sex, smoking status, and hypertension status underwent macular volumetric and peripapillary optical coherence tomography scans. Disease duration, motor status, global cognition and CAG repeats were recorded in patients. Group differences in imaging parameters and their association with clinical outcomes were analyzed using linear mixed-effect models.
RESULTS RESULTS
Premanifest and manifest Huntington's disease patients presented thinner retinal external limiting membrane-Bruch's membrane complex, and manifest patients had thinner temporal peripapillary retinal nerve fiber layer compared to controls. In manifest Huntington's disease, macular thickness was significantly associated with MoCA scores, inner nuclear layer showing the largest regression coefficients. This relationship was consistent after adjusting for age, sex, and education and p-value correction with False Discovery Rate. None of the retinal variables were related to Unified Huntington's Disease Rating Scale score, disease duration, or disease burden. Premanifest patients did not show a significant association between OCT-derived parameters and clinical outcomes in corrected models.
CONCLUSIONS CONCLUSIONS
In line with other neurodegenerative diseases, OCT is a potential biomarker of cognitive status in manifest HD. Future prospective studies are needed to evaluate OCT as a potential surrogate marker of cognitive decline in HD.

Identifiants

pubmed: 37079031
doi: 10.1007/s00415-023-11720-3
pii: 10.1007/s00415-023-11720-3
pmc: PMC10345164
doi:

Substances chimiques

Biomarkers 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

3821-3829

Subventions

Organisme : EITB Maratoia
ID : BIO17/ND/009
Organisme : Osasun Saila, Eusko Jaurlaritzako
ID : 2019111004

Informations de copyright

© 2023. The Author(s).

Références

Penney JB Jr et al (1997) CAG repeat number governs the development rate of pathology in Huntington’s disease. Ann Neurol 41(5):689–692
doi: 10.1002/ana.410410521 pubmed: 9153534
Purdon SE et al (1994) Huntington’s disease: pathogenesis, diagnosis and treatment. J Psychiatry Neurosci 19(5):359–367
pubmed: 7528535 pmcid: 1188625
Dhalla A, Pallikadavath S, Hutchinson CV (2019) Visual Dysfunction in Huntington’s Disease: A Systematic Review. J Huntingtons Dis 8(2):233–242
doi: 10.3233/JHD-180340 pubmed: 30932892
Petzold A et al (2010) Optical coherence tomography in multiple sclerosis: a systematic review and meta-analysis. Lancet Neurol 9(9):921–932
doi: 10.1016/S1474-4422(10)70168-X pubmed: 20723847
Murueta-Goyena A et al (2021) Retinal thickness predicts the risk of cognitive decline in Parkinson disease. Ann Neurol 89(1):165–176
doi: 10.1002/ana.25944 pubmed: 33098308
Murueta-Goyena A et al (2019) Parafoveal thinning of inner retina is associated with visual dysfunction in Lewy body diseases. Mov Disord. https://doi.org/10.1002/mds.27728
doi: 10.1002/mds.27728 pubmed: 31769091 pmcid: 6790692
Cheung CY et al (2021) Retinal imaging in Alzheimer’s disease. J Neurol Neurosurg Psychiatry 92(9):983–994
doi: 10.1136/jnnp-2020-325347 pubmed: 34108266
Kersten HM et al (2015) Optical coherence tomography findings in Huntington’s disease: a potential biomarker of disease progression. J Neurol 262(11):2457–2465
doi: 10.1007/s00415-015-7869-2 pubmed: 26233693
Gatto E et al (2018) Optical coherence tomography (OCT) study in Argentinean Huntington’s disease patients. Int J Neurosci 128(12):1157–1162
doi: 10.1080/00207454.2018.1489807 pubmed: 29912591
Gulmez Sevim D et al (2019) Retinal single-layer analysis with optical coherence tomography shows inner retinal layer thinning in Huntington’s disease as a potential biomarker. Int Ophthalmol 39(3):611–621
doi: 10.1007/s10792-018-0857-7 pubmed: 29435796
Amini E et al (2022) Huntington’s disease and neurovascular structure of retina. Neurol Sci 43(10):5933–5941
doi: 10.1007/s10072-022-06232-3 pubmed: 35771295
Andrade C et al (2016) Spectral-domain optical coherence tomography as a potential biomarker in Huntington’s disease. Mov Disord 31(3):377–383
doi: 10.1002/mds.26486 pubmed: 26853218
Schmid RD et al (2022) No optical coherence tomography changes in premanifest Huntington’s disease mutation carriers far from disease onset. Brain Behav 12(6):e2592
doi: 10.1002/brb3.2592 pubmed: 35511084 pmcid: 9226796
Mazur-Michałek I et al (2022) Structural abnormalities of the optic nerve and retina in Huntington’s disease pre-clinical and clinical settings. Int J Mol Sci 23(10):5450
doi: 10.3390/ijms23105450 pubmed: 35628260 pmcid: 9141007
Stout JC, Andrews SC, Glikmann-Johnston Y (2017) Cognitive assessment in Huntington disease clinical drug trials. Handb Clin Neurol 144:227–244
doi: 10.1016/B978-0-12-801893-4.00019-5 pubmed: 28947120
Ojeda N et al (2016) Montreal cognitive assessment test: normalization and standardization for Spanish population. Rev Neurol 63(11):488–496
pubmed: 27874165
Tewarie P et al (2012) The OSCAR-IB consensus criteria for retinal OCT quality assessment. PLoS ONE 7(4):e34823
doi: 10.1371/journal.pone.0034823 pubmed: 22536333 pmcid: 3334941
Murueta-Goyena A et al (2021) Foveal remodeling of retinal microvasculature in Parkinson’s disease. Front Neurosci 15:708700
doi: 10.3389/fnins.2021.708700 pubmed: 34321998 pmcid: 8311167
Helmlinger D et al (2002) Progressive retinal degeneration and dysfunction in R6 Huntington’s disease mice. Hum Mol Genet 11(26):3351–3359
doi: 10.1093/hmg/11.26.3351 pubmed: 12471061
Ragauskas S et al (2014) Early retinal function deficit without prominent morphological changes in the R6/2 mouse model of Huntington’s disease. PLoS ONE 9(12):e113317
doi: 10.1371/journal.pone.0113317 pubmed: 25469887 pmcid: 4254453
Batcha AH et al (2012) Retinal dysfunction, photoreceptor protein dysregulation and neuronal remodelling in the R6/1 mouse model of Huntington’s disease. Neurobiol Dis 45(3):887–896
doi: 10.1016/j.nbd.2011.12.004 pubmed: 22198376
Duda M et al (2017) EPR studies on the properties of model photoreceptor membranes made of natural and synthetic lipids. Cell Biochem Biophys 75(3–4):433–442
doi: 10.1007/s12013-017-0795-4 pubmed: 28413858 pmcid: 5691102
Lee J et al (2011) Modulation of lipid peroxidation and mitochondrial function improves neuropathology in Huntington’s disease mice. Acta Neuropathol 121(4):487–498
doi: 10.1007/s00401-010-0788-5 pubmed: 21161248
Teberik K (2019) The effect of smoking on macular, choroidal, and retina nerve fiber layer thickness. Turk J Ophthalmol 49(1):20–24
doi: 10.4274/tjo.galenos.2018.80588 pubmed: 30829021 pmcid: 6416485
Cui B et al (2021) Association of cigarette smoking with retinal thickness and vascular structure in an elderly Chinese population. Photodiagnosis Photodynamic Therapy 36:102481
doi: 10.1016/j.pdpdt.2021.102481 pubmed: 34403826
Liew SH et al (2007) The role of heredity in determining central retinal thickness. Br J Ophthalmol 91(9):1143–1147
doi: 10.1136/bjo.2007.114215 pubmed: 17360735 pmcid: 1954930
Lee WH et al (2020) Longitudinal changes in the thickness of the ganglion cell-inner plexiform layer in patients with hypertension: a 4-year prospective observational study. Acta Ophthalmol 98(4):e479–e486
doi: 10.1111/aos.14291 pubmed: 31658412
Sánchez-Tocino H et al (2002) Retinal thickness study with optical coherence tomography in patients with diabetes. Invest Ophthalmol Vis Sci 43(5):1588–1594
pubmed: 11980878
Duff K et al (2010) Mild cognitive impairment in prediagnosed Huntington disease. Neurology 75(6):500–507
doi: 10.1212/WNL.0b013e3181eccfa2 pubmed: 20610833 pmcid: 2918475
Julayanont P, McFarland NR, Heilman KM (2020) Mild cognitive impairment and dementia in motor manifest Huntington’s disease: classification and prevalence. J Neurol Sci 408:116523
doi: 10.1016/j.jns.2019.116523 pubmed: 31678902

Auteurs

Ane Murueta-Goyena (A)

Neurodegenerative Diseases Group, Biocruces Bizkaia Health Research Institute, Barakaldo, Spain. ane.muruetagoyena@ehu.eus.
Department of Neurosciences, Faculty of Medicine and Nursery, University of the Basque Country (UPV/EHU), 48930, Leioa, Spain. ane.muruetagoyena@ehu.eus.

Rocío Del Pino (R)

Neurodegenerative Diseases Group, Biocruces Bizkaia Health Research Institute, Barakaldo, Spain.

Marian Acera (M)

Neurodegenerative Diseases Group, Biocruces Bizkaia Health Research Institute, Barakaldo, Spain.

Sara Teijeira-Portas (S)

Neurodegenerative Diseases Group, Biocruces Bizkaia Health Research Institute, Barakaldo, Spain.

David Romero (D)

Biomedical Engineering Department, Faculty of Engineering, Mondragon University, Mondragon, Spain.

Unai Ayala (U)

Biomedical Engineering Department, Faculty of Engineering, Mondragon University, Mondragon, Spain.

Tamara Fernández-Valle (T)

Neurodegenerative Diseases Group, Biocruces Bizkaia Health Research Institute, Barakaldo, Spain.
Department of Neurosciences, Faculty of Medicine and Nursery, University of the Basque Country (UPV/EHU), 48930, Leioa, Spain.
Neurology Department, Cruces University Hospital, Osakidetza, Barakaldo, Spain.

Beatriz Tijero (B)

Neurodegenerative Diseases Group, Biocruces Bizkaia Health Research Institute, Barakaldo, Spain.
Neurology Department, Cruces University Hospital, Osakidetza, Barakaldo, Spain.

Iñigo Gabilondo (I)

Neurodegenerative Diseases Group, Biocruces Bizkaia Health Research Institute, Barakaldo, Spain.
IKERBASQUE, The Basque Foundation for Science, Bilbao, Spain.

Juan Carlos Gómez Esteban (JC)

Neurodegenerative Diseases Group, Biocruces Bizkaia Health Research Institute, Barakaldo, Spain.
Department of Neurosciences, Faculty of Medicine and Nursery, University of the Basque Country (UPV/EHU), 48930, Leioa, Spain.
Neurology Department, Cruces University Hospital, Osakidetza, Barakaldo, Spain.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH