The relationship between retinal layers and brain areas in asymptomatic first-degree relatives of sporadic forms of Alzheimer’s disease: an exploratory analysis

  1. López-Cuenca, Inés 12
  2. Marcos-Dolado, Alberto 234
  3. Yus-Fuertes, Miguel 25
  4. Salobrar-García, Elena 126
  5. Elvira-Hurtado, Lorena 1
  6. Fernández-Albarral, José A. 12
  7. Salazar, Juan J. 126
  8. Ramírez, Ana I. 126
  9. Sánchez-Puebla, Lidia 1
  10. Fuentes-Ferrer, Manuel Enrique 27
  11. Barabash, Ana 289
  12. Ramírez-Toraño, Federico 1011
  13. Gil-Martínez, Lidia 12
  14. Arrazola-García, Juan 2513
  15. Gil, Pedro 2314
  16. de Hoz, Rosa 126
  17. Ramírez, José M. 1215
  1. 1 Universidad Complutense de Madrid
    info

    Universidad Complutense de Madrid

    Madrid, España

    ROR 02p0gd045

  2. 2 Health Research Institute of the Hospital Clínico San Carlos (IdISSC)
  3. 3 Department of Medicine, School of Medicine, Complutense University of Madrid
  4. 4 Department of Neurology, Hospital Clínico San Carlos
  5. 5 Department of Diagnostic Imaging, Hospital Clínico San Carlos
  6. 6 Department of Immunology, Ophthalmology and ENT, Faculty of Optics and Optometry, Complutense University of Madrid
  7. 7 Preventive Medicine Service, Research Methodological Support Unit, Hospital Clínico San Carlos, Madrid
  8. 8 Department of Endocrinology and Nutrition, Hospital Clínico San Carlos, Madrid
  9. 9 Center for Biomedical Research Network on Diabetes and Associated Metabolic Diseases, Institute of Health Carlos III, Madrid
  10. 10 Laboratory of Cognitive and Computational Neuroscience, Center for Biomedical Technology, Technical University of Madrid
  11. 11 Department of Experimental Psychology, Complutense University of Madrid, Madrid
  12. 12 Foundation for Biomedical Research at Hospital Clínico San Carlos (FIBHCSC), Hospital Clínico San Carlos, Madrid
  13. 13 Department of Radiology, Rehabilitation and Radiation Therapy, School of Medicine, Complutense University of Madrid
  14. 14 Memory Unit, Geriatrics Service, Hospital Clínico San Carlos, Madrid
  15. 15 Department of Immunology, Ophthalmology and ENT, School of Medicine, Complutense University of Madrid
Erakutsi afiliazioak +
Aldizkaria:
Alzheimer's Research & Therapy

ISSN: 1758-9193

Argitalpen urtea: 2022

Alea: 14

Zenbakia: 1

Mota: Artikulua

DOI: 10.1186/S13195-022-01008-5 GOOGLE SCHOLAR lock_openSarbide irekia editor

Beste argitalpen batzuk: Alzheimer's Research & Therapy

€ Ikusi finantzaketa

Finantzaketari buruzko informazioa

Finantzatzaile

Erreferentzia bibliografikoak

  • Association A. 2017 Alzheimer’s disease facts and figures. Alzheimers Dement. 2017;13:325–73. https://doi.org/10.1016/J.JALZ.2017.02.001.
  • Jansen WJ, Ossenkoppele R, Knol DL, Tijms BM, Scheltens P, Verhey FRJ, et al. Prevalence of cerebral amyloid pathology in persons without dementia: a meta-analysis. JAMA. 2015;313:1924–38. https://doi.org/10.1001/jama.2015.4668.
  • Palmqvist S, Schöll M, Strandberg O, Mattsson N, Stomrud E, Zetterberg H, et al. Earliest accumulation of β-amyloid occurs within the default-mode network and concurrently affects brain connectivity. Nat Commun. 2017;8:1–13. https://doi.org/10.1038/s41467-017-01150-x.
  • Villeneuve S, Rabinovici GD, Cohn-Sheehy BI, Madison C, Ayakta N, Ghosh PM, et al. Existing Pittsburgh compound-B positron emission tomography thresholds are too high: statistical and pathological evaluation. Brain. 2015;138:2020–33. https://doi.org/10.1093/brain/awv112.
  • Guillozet AL, Weintraub S, Mash DC, Marsel Mesulam M. Neurofibrillary tangles, amyloid, and memory in aging and mild cognitive impairment. Arch Neurol. 2003;60:729–36. https://doi.org/10.1001/archneur.60.5.729.
  • Shi Z, Cao X, Hu J, Jiang L, Mei X, Zheng H, et al. Retinal nerve fiber layer thickness is associated with hippocampus and lingual gyrus volumes in nondemented older adults. Prog Neuro-Psychopharmacol Biol Psychiatry. 2020;99:109824. https://doi.org/10.1016/j.pnpbp.2019.109824.
  • London A, Benhar I, Schwartz M. The retina as a window to the brain - from eye research to CNS disorders. Nat Rev Neurol. 2013;9:44–53. https://doi.org/10.1038/nrneurol.2012.227.
  • Sivak JM. The aging eye: common degenerative mechanisms between the Alzheimer’s brain and retinal disease. Investig Ophthalmol Vis Sci. 2013;54:871–80. https://doi.org/10.1167/iovs.12-10827.
  • Koronyo-Hamaoui M, Koronyo Y, Ljubimov AV, Miller CA, Ko MK, Black KL, et al. Identification of amyloid plaques in retinas from Alzheimer’s patients and noninvasive in vivo optical imaging of retinal plaques in a mouse model. Neuroimage. 2011;54:S204–17. https://doi.org/10.1016/j.neuroimage.2010.06.020.
  • Ning A, Cui J, To E, Ashe K, Matsubara J. Amyloid-β deposits lead to retinal degeneration in a mouse model of Alzheimer disease. Investig Opthalmol Vis Sci. 2008;49:5136–43. https://doi.org/10.1167/iovs.08-1849.
  • Koronyo Y, Biggs D, Barron E, Boyer DS, Pearlman JA, Au WJ, et al. Retinal amyloid pathology and proof-of-concept imaging trial in Alzheimer’s disease. JCI insight. 2017;2:e93621. https://doi.org/10.1172/jci.insight.93621.
  • López-Cuenca I, de Hoz R, Salobrar-García E, Elvira-Hurtado L, Rojas P, Fernández-Albarral JA, et al. Macular thickness decrease in asymptomatic subjects at high genetic risk of developing Alzheimer’s disease: an OCT study. J Clin Med. 2020;9:1728. https://doi.org/10.3390/jcm9061728.
  • Jáñez-Escalada L, Jáñez-García L, Salobrar-García E, Santos-Mayo A, de Hoz R, Yubero R, et al. Spatial analysis of thickness changes in ten retinal layers of Alzheimer’s disease patients based on optical coherence tomography. Sci Rep. 2019;9:1–14. https://doi.org/10.1038/s41598-019-49353-0.
  • Garcia-Martin ES, Rojas B, Ramirez AI, de Hoz R, Salazar JJ, Yubero R, et al. Macular thickness as a potential biomarker of mild Alzheimer’s disease. Ophthalmology. 2014;121:1149–1151.e3. https://doi.org/10.1016/j.ophtha.2013.12.023.
  • Salobrar-García E, Hoyas I, Leal M, de Hoz R, Rojas B, Ramirez AI, et al. Analysis of retinal peripapillary segmentation in early Alzheimer’s disease patients. Biomed Res Int. 2015;2015:636548. https://doi.org/10.1155/2015/636548.
  • Salobrar-García E, de Hoz R, Ramírez AI, López-Cuenca I, Rojas P, Vazirani R, et al. Changes in visual function and retinal structure in the progression of Alzheimer’s disease. PLoS One. 2019;14:e0220535. https://doi.org/10.1371/journal.pone.0220535.
  • Casaletto KB, Ward ME, Baker NS, Bettcher BM, Gelfand JM, Li Y, et al. Retinal thinning is uniquely associated with medial temporal lobe atrophy in neurologically normal older adults. Neurobiol Aging. 2017;51:141–7. https://doi.org/10.1016/j.neurobiolaging.2016.12.011.
  • Donix M, Burggren AC, Suthana NA, Siddarth P, Ekstrom AD, Krupa AK, et al. Family history of Alzheimer’s disease and hippocampal structure in healthy people. Am J Psychiatry. 2010;167:1399–406. https://doi.org/10.1176/appi.ajp.2010.09111575.
  • E.T.D.R.S Group. Grading Diabetic Retinopathy from Stereoscopic Color Fundus Photographs—an extension of the modified Airlie House classification: ETDRS report number 10. Ophthalmology. 1991;98:786–806. https://doi.org/10.1016/S0161-6420(13)38012-9.
  • Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis: I. Segmentation and surface reconstruction. Neuroimage. 1999;9:179–94. https://doi.org/10.1006/nimg.1998.0395.
  • Fischl B, Sereno MI, Dale AM. Cortical surface-based analysis: II. Inflation, flattening, and a surface-based coordinate system. Neuroimage. 1999;9:195–207. https://doi.org/10.1006/nimg.1998.0396.
  • Ségonne F, Dale AM, Busa E, Glessner M, Salat D, Hahn HK, et al. A hybrid approach to the skull stripping problem in MRI. Neuroimage. 2004;22:1060–75. https://doi.org/10.1016/j.neuroimage.2004.03.032.
  • Ségonne F, Pacheco J, Fischl B. Geometrically accurate topology-correction of cortical surfaces using nonseparating loops. IEEE Trans Med Imaging. 2007;26:518–29. https://doi.org/10.1109/TMI.2006.887364.
  • Fischl B, Sereno MI, Tootell RBH, Dale AM. High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp. 1999;8:272–84.  https://doi.org/10.1002/(SICI)1097-0193(1999)8:4<272::AID-HBM10>3.0.CO;2-4.
  • Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage. 2006;31:968–80. https://doi.org/10.1016/j.neuroimage.2006.01.021.
  • Seltzer MM, Li LW. The dynamics of caregiving: transitions during a three-year prospective study. Gerontologist. 2000;40:165–78. https://doi.org/10.1093/geront/40.2.165.
  • Jefferson AL, Lambe S, Chaisson C, Palmisano J, Horvath KJ, Karlawish J. Clinical research participation among aging adults enrolled in an Alzheimer’s disease center research registry. J Alzheimers Dis. 2011;23:443–52. https://doi.org/10.3233/JAD-2010-101536.
  • Plassman BL, Welsh-Bohmer KA, Bigler ED, Johnson MA, Anderson CV, Helms MJ, et al. Apolipoprotein E epsilon 4 allele and hippocampal volume in twins with normal cognition. Neurology. 1997;48:985–9. https://doi.org/10.1212/WNL.48.4.985.
  • Reiman EM, Uecker A, Caselli RJ, Lewis S, Bandy D, De Leon MJ, et al. Hippocampal volumes in cognitively normal persons at genetic risk for Alzheimer’s disease. Ann Neurol. 1998;44:288–91. https://doi.org/10.1002/ana.410440226.
  • Schmidt H, Schmidt R, Fazekas F, Semmler J, Kapeller P, Reinhart B, et al. Apolipoprotein E4allele in the normal elderly: neuropsychologic and brain MRI correlates. Clin Genet. 1996;50:293–9. https://doi.org/10.1111/J.1399-0004.1996.TB02377.X.
  • Tohgi H, Takahashi S, Kato E, Homma A, Niina R, Sasaki K, et al. Reduced size of right hippocampus in 39- to 80-year-old normal subjects carrying the apolipoprotein E epsilon4 allele. Neurosci Lett. 1997;236:21–4. https://doi.org/10.1016/S0304-3940(97)00743-X.
  • de Flores R, La Joie R, Chételat G. Structural imaging of hippocampal subfields in healthy aging and Alzheimer’s disease. Neuroscience. 2015;309:29–50. https://doi.org/10.1016/J.NEUROSCIENCE.2015.08.033.
  • Burggren AC, Zeineh MM, Ekstrom AD, Braskie MN, Thompson PM, Small GW, et al. Reduced cortical thickness in hippocampal subregions among cognitively normal apolipoprotein E E4 carriers. Neuroimage. 2008;41:1177–83. https://doi.org/10.1016/J.NEUROIMAGE.2008.03.039.
  • Batzu L, Westman E, Pereira JB. Cerebrospinal fluid progranulin is associated with increased cortical thickness in early stages of Alzheimer’s disease. Neurobiol Aging. 2019;88:61–70. https://doi.org/10.1016/J.NEUROBIOLAGING.2019.12.012.
  • López-Sanz D, Bruña R, Garcés P, Martín-Buro MC, Walter S, Delgado ML, et al. Functional connectivity disruption in subjective cognitive decline and mild cognitive impairment: a common pattern of alterations. Front Aging Neurosci. 2017;9. https://doi.org/10.3389/fnagi.2017.00109.
  • Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991;82:239–59. https://doi.org/10.1007/BF00308809.
  • Salobrar-García E, López-Cuenca I, Sánchez-Puebla L, de Hoz R, Fernández-Albarral JA, Ramírez AI, et al. Retinal thickness changes over time in a murine AD model APPNL-F/NL-F. Front Aging Neurosci. 2021;12:625642. https://doi.org/10.3389/fnagi.2020.625642.
  • Shariflou S, Georgevsky D, Mansour H, Rezaeian M, Hosseini N, Gani F, et al. Diagnostic and prognostic potential of retinal biomarkers in early on-set Alzheimer’s disease. Curr Alzheimer Res. 2017;14:1000–7. https://doi.org/10.2174/1567205014666170329114445.
  • Masuzzo A, Dinet V, Cavanagh C, Mascarelli F, Krantic S. Amyloidosis in retinal neurodegenerative diseases. Front Neurol. 2016;7:127. https://doi.org/10.3389/fneur.2016.00127.
  • Jindahra P, Petrie A, Plant GT. Retrograde Trans-Synaptic Retinal Ganglion Cell Loss Identified by Optical Coherence Tomography. Brain. 2009;132:628–34. https://doi.org/10.1093/brain/awp001.
  • Criscuolo C, Cerri E, Fabiani C, Capsoni S, Cattaneo A, Domenici L. The retina as a window to early dysfunctions of Alzheimer’s disease following studies with a 5xFAD mouse model. Neurobiol Aging. 2018;67:181–8. https://doi.org/10.1016/j.neurobiolaging.2018.03.017.
  • Donix M, Wittig D, Hermann W, Haussmann R, Dittmer M, Bienert F, et al. Relation of retinal and hippocampal thickness in patients with amnestic mild cognitive impairment and healthy controls. Brain Behav. 2021:1–9. https://doi.org/10.1002/brb3.2035.
  • Méndez-Gómez JL, Pelletier A, Rougier MB, Korobelnik JF, Schweitzer C, Delyfer MN, et al. Association of retinal nerve fiber layer thickness with brain alterations in the visual and limbic networks in elderly adults without dementia. JAMA Netw Open. 2018;1. https://doi.org/10.1001/jamanetworkopen.2018.4406.
  • Shi Z, Zheng H, Hu J, Jiang L, Cao X, Chen Y, et al. Retinal nerve fiber layer thinning is associated with brain atrophy: a longitudinal study in nondemented older adults. Front Aging Neurosci. 2019;11:1–10. https://doi.org/10.3389/fnagi.2019.00069.
  • Lewis DA, Campbell MJ, Terry RD, Morrison JH. Laminar and regional distributions of neurofibrillary tangles and neuritic plaques in Alzheimer’s disease: a quantitative study of visual and auditory cortices. J Neurosci. 1987;7:1799–808. https://doi.org/10.1523/jneurosci.07-06-01799.1987.
  • Hof PR, Morrison JH. Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer’s disease: II. Primary and secondary visual cortex. J Comp Neurol. 1990;301:55–64. https://doi.org/10.1002/cne.903010106.
  • Ong YT, Hilal S, Cheung CY, Venketasubramanian N, Niessen WJ, Vrooman H, et al. Retinal neurodegeneration on optical coherence tomography and cerebral atrophy. Neurosci Lett. 2015;584:12–6. https://doi.org/10.1016/j.neulet.2014.10.010.
  • Mutlu U, Bonnemaijer PWM, Ikram MA, Colijn JM, Cremers LGM, Buitendijk GHS, et al. Retinal neurodegeneration and brain MRI markers: the Rotterdam study. Neurobiol Aging. 2017;60:183–91. https://doi.org/10.1016/j.neurobiolaging.2017.09.003.
  • Chua SY, Lascaratos G, Atan D, Zhang B, Reisman C, Khaw PT, et al. Relationships between retinal layer thickness and brain volumes in the UK Biobank cohort. Eur J Neurol. 2020. https://doi.org/10.1111/ene.14706.
  • Mejia-Vergara AJ, Karanjia R, Sadun AA. OCT parameters of the optic nerve head and the retina as surrogate markers of brain volume in a normal population, a pilot study. J Neurol Sci. 2021;420:117213. https://doi.org/10.1016/j.jns.2020.117213.
  • Donix M, Burggren AC, Scharf M, Marschner K, Suthana NA, Siddarth P, et al. APOE associated hemispheric asymmetry of entorhinal cortical thickness in aging and Alzheimer’s disease. Psychiatry Res Neuroimaging. 2013;214:212–20. https://doi.org/10.1016/j.pscychresns.2013.09.006.
  • Shaw P, Lerch JP, Pruessner JC, Taylor KN, Rose AB, Greenstein D, et al. Cortical morphology in children and adolescents with different apolipoprotein E gene polymorphisms: an observational study. Lancet Neurol. 2007;6:494–500. https://doi.org/10.1016/S1474-4422(07)70106-0.
  • Fillit H, Green A. Aducanumab and the FDA — where are we now? Nat Rev Neurol. 2021;17:129–30. https://doi.org/10.1038/s41582-020-00454-9.