Abstract
The purpose of this study was to evaluate optic nerve head (ONH) differences of the patients with Alzheimer’s disease (AD) measured by confocal scanning laser tomography [Heidelberg Retina Tomograph (HRT) III] and compare with glaucoma and control subjects. Eighty-four patients were enrolled into the study: 44 eyes of 24 patients with mild to moderate AD (Group 1), 68 eyes of 35 patients with glaucoma (Group 2), and 49 eyes of 25 heathy volunteers as a control (Group 3). A complete ophthalmologic examination as well as a confocal scanning laser ophthalmoscopic assessment with HRT III were performed on all patients. Mean values of the ONH topographic parameters such as rim area (RA), rim volume (RV), height variation contour, linear cup/disc ratio, cup shape measure, and retinal nerve fiber layer (RNFL) were recorded. Mean values of RNFL thickness was 0.23 ± 0.07 in AD, 0.22 ± 0.09 in glaucoma and 0.24 ± 0.07 in the control group (p = 0.323). RA and RV were significantly lower, and linear C/D ratio was significantly higher in the glaucoma group when compared to AD and control (p < 0.05). There was no statistically significant difference between AD and control for the optic disc parameters tested (p > 0.05). We observed a negative correlation of the age with RNFL in all of the groups (p < 0.005). Age was the most important parameter affecting RNFL. Our results suggest that HRT does not demonstrate ONH differences between AD and control group, while it successfully differentiates glaucoma from AD and control cases of older age.
Similar content being viewed by others
References
Guo L, Duggan J, Cordeiro MF (2010) Alzheimer’s disease and retinal neurodegeneration. Curr Alzheimer Res 7(1):3–14
Holroyd S, Shepherd ML (2001) Alzheimer’s disease: a review for the ophthalmologist. Surv Ophthalmol 45:516–524
Pache M, Flammer J (2006) A sick eye in a sick body? Systemic findings in patients with primary open-angle glaucoma. Surv Ophthalmol 51:179–212
Gupta N, Yucel YH (2007) What changes can we expect in the brain of glaucoma patients? Surv Ophthalmol 52:122–126
Wostyn P, Audenaert K, De Deyn PP (2008) Alzheimer’s disease-related changes in diseases characterized by elevation of intracranial or intraocular pressure. Clin Neurol Neurosurg 110(2):101–109
Quigley HA (1999) Neuronal death in glaucoma. Prog Retin Eye Res 18:39–57
Tezel G (2006) Oxidative stress in glaucomatous neurodegeneration: mechanisms and consequences. Prog Retin Eye Res 25:490–513
Kirby E, Bandelow S, Hogervorst E (2010) Visual impairment in Alzheimer’s disease: a critical review. J Alzheimers Dis 21(1):15–34
McKinnon SJ (2012) The cell and molecular biology of glaucoma: common neurodegenerative pathways and relevance to glaucoma. Invest Ophthalmol Vis Sci 53(5):2485–2487
Parisi V (2003) Correlation between morphological and functional retinal impairment in patients affected by ocular hypertension, glaucoma, demyelinating optic neuritis and Alzheimer’s disease. Semin Ophthalmol 18:50–57
Kallenbach K, Frederiksen J (2007) Optical coherence tomography in optic neuritis and multiple sclerosis: a review. Eur J Neurol 14(8):841–849
Kirbas S, Turkyilmaz K, Anlar O, Tufekci A, Durmus M (2013) Retinal nerve fiber layer thickness in Parkinson disease. J Neuroophthalmol 33(1):62–65
Jindahra P, Hedges TR, Mendoza-Santiesteban CE, Plant GT (2010) Optical coherence tomography of the retina: applications in neurology. Curr Opin Neurol 23(1):16–23
Ikram MK, Cheung CY, Wong TY, Chen CP (2012) Retinal pathology as biomarker for cognitive impairment and Alzheimer’s disease. J Neurol Neurosurg Psychiatry 83(9):917–922
Frost S, Martins RN, Kanagasingam Y (2010) Ocular biomarkers for early detection of Alzheimer’s disease. J Alzheimers Dis 22(1):1–16
Badalà F, Nouri-Mahdavi K, Raoof DA, Leeprechanon N, Law SK, Caprioli J (2007) Optic disk and nerve fiber layer imaging to detect glaucoma. Am J Ophthalmol 144(5):724–732
Klamann MK, Grünert A, Maier AK, Gonnermann J, Joussen AM, Huber KK (2013) Comparison of functional and morphological diagnostics in glaucoma patients and healthy subjects. Ophthalmic Res 49(4):192–198
Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198
Hodapp E, Parrish RK II, Anderson DR (1993) Clinical decisions in glaucoma. The C.V. Mosby Co., St. Louis
Pei JJ, Sjogren M, Winblad B (2008) Neurofibrillary degeneration in Alzheimer’s disease: from molecular mechanisms to identification of drug targets. Curr Opin Psychiatry 21:555–561
Blanks JC, Hinton DR, Sadun AA, Miller CA (1989) Retinal ganglion cell degeneration in Alzheimer’s disease. Brain Res 501:364–372
Sadun A, Bassi C (1990) Optic nerve damage in Alzheimer’s disease. Ophthalmology 97:9–17
Hinton DR, Sadun AA, Blanks JC, Miller CA (1986) Optic-nerve degeneration in Alzheimer’s disease. N Engl J Med 315:485–487
Syed AB, Armstrong RA, Smith CU (2005) A quantitative analysis of optic nerve axons in elderly control subjects and patients with Alzheimer’s disease. Folia Neuropathol 43(1):1–6
Cuzzo LM, Ross-Cisneros FN, Yee KM, Wang MY, Sadun AA (2011) Low density lipoprotein receptor-related protein (LRP) is decreased in optic neuropathy of Alzheimer’s disease. J Neuroophthalmol 31(2):139–146
Davies DC, McCoubrie P, McDonald B, Jobst KA (1995) Myelinated axon number in the optic nerve is unaffected by Alzheimer’s disease. Br J Ophthalmol 79:596–600
Risacher SL, Wudunn D, Pepin SM, MaGee TR, McDonald BC, Flashman LA, Wishart HA, Pixley HS, Rabin LA, Paré N, Englert JJ, Schwartz E, Curtain JR, West JD, O’Neill DP, Santulli RB, Newman RW, Saykin AJ (2013) Visual contrast sensitivity in Alzheimer’s disease, mild cognitive impairment, and older adults with cognitive complaints. Neurobiol Aging 34(4):1133–1144
Pache M, Smeets CH, Gasio PF, Savaskan E, Flammer J, Wirz-Justice A, Kaiser HJ (2003) Colour vision deficiencies in Alzheimer’s disease. Age Ageing 32:422–426
Krasodomska K, Lubiński W, Potemkowski A, Jobst KA (2010) Pattern electroretinogram (PERG) and pattern visual evoked potential (PVEP) in the early stages of Alzheimer’s disease. Doc Ophthalmol 121(2):111–121
Wostyn P, Audenaert K, De Deyn PP (2009) Alzheimer’s disease and glaucoma is there a causal relationship? Br J Ophthalmol 93(12):1557–1559
Trick GL, Calotti FY, Skarf B (2006) Advances in imaging of the optic disc and retinal nerve fiber layer. J Neuroophthalmol 26(4):284–295
Hoffmann EM, Miglior S, Zeyen T, Torri V, Rulli E, Aliyeva S, Floriani I, Cunha-Vaz J, Pfeiffer N (2013) The Heidelberg retina tomograph ancillary study to the European Glaucoma Prevention Study: study design and baseline factors. Acta Ophthalmol 91(8):e612–e619
Kamal DS, Viswanathan AC, Garway-Heath DF et al (1999) Detection of optic disc change with the Heidelberg retina tomograph before confirmed visual field change in ocular hypertensives converting to early glaucoma. Br J Ophthalmol 83:290–294
Toledo J, Sepulcre J, Salinas-Alaman A, García-Layana A, Murie-Fernandez M, Bejarano B, Villoslada P (2008) Retinal nerve fiber layer atrophy is associated with physical and cognitive disability in multiple sclerosis. Mult Scler 14(7):906–912
Trip SA, Schlottmann PG, Jones SJ, Garway-Heath DF, Thompson AJ, Plant GT, Miller DH (2006) Quantification of optic nerve head topography in optic neuritis: a pilot study. Br J Ophthalmol 90(9):1128–1131
Danesh-Meyer HV, Birch H, Ku JY, Carroll S, Gamble G (2006) Reduction of optic nerve fibers in patients with Alzheimer disease identified by laser imaging. Neurology 67(10):1852–1854
Kergoat H, Kergoat MJ, Justino L, Chertkow H, Robillard A, Bergman H (2001) An evaluation of the retinal nerve fiber layer thickness by scanning laser polarimetry in individuals with dementia of the Alzheimer type. Acta Ophthalmol Scand 79(2):187–191
Berisha F, Feke GT, Trempe CL, McMeel JW, Schepens CL (2006) Localized retinal nerve fiber layer thinning in patients with early glaucoma or Alzheimer’s disease. Investig Ophthalmol Vis Sci 47:18–24
Parisi V (2001) Morphological and functional retinal impairment in Alzheimer’s disease patients. Clin Neurophysiol 112:1860–1867
Iseri PK, Altinas O, Tokay T, Yuksel N (2006) Relationship between cognitive impairment and retinal morphological and visual functional abnormalities in Alzheimer’s disease. J Neuro-ophthalmol 26:18–24
He XF, Liu YT, Peng C, Zhang F, Zhuang S, Zhang JS (2012) Optical coherence tomography assessed retinal nerve fiber layer thickness in patients with Alzheimer’s disease: a meta-analysis. Int J Ophthalmol 5(3):401–405
Kirbas S, Turkyilmaz K, Anlar O et al (2013) Retinal nerve fiber layer thickness in patients with Alzheimer disease. Neuroophthalmology 33(1):58–61
Kergoat H, Kergoat MJ, Justino L, Robillard A, Bergman H, Chertkow H (2001) Normal optic nerve head topography in the early stages of dementia of the Alzheimer type. Dement Geriatr Cogn Disord 12(6):359–363
Zangwill LM, Bowd C (2006) Retinal nerve fiber layer analysis in the diagnosis of glaucoma. Curr Opin Ophthalmol 17:120–131
Kesler A, Vakhapova V, Korczyn AD, Naftaliev E, Neudorfer M (2011) Retinal thickness in patients with mild cognitive impairment and Alzheimer’s disease. Clin Neurol Neurosurg 113(7):523–526
Paquet C, Boissonnot M, Roger F, Dighiero P, Gil R, Hugon J (2007) Abnormal retinal thickness in patients with mild cognitive impairment and Alzheimer’s disease. Neurosci Lett 420(2):97–99
Coops A, Henson DB, Kwartz AJ, Artes PH (2006) Automated analysis of heidelberg retina tomograph optic disc images by glaucoma probability score. Invest Ophthalmol Vis Sci 47:5348–5355
Alasil T, Wang K, Keane PA, Lee H, Baniasadi N, de Boer JF, Chen TC (2013) Analysis of normal retinal nerve fiber layer thickness by age, sex, and race using spectral domain optical coherence tomography. J Glaucoma 22(7):532–541
Khawaja AP, Chan MP, Broadway DC, Garway-Heath DF, Luben R, Yip JL, Hayat S, Khaw KT, Foster PJ (2013) Laser scanning tomography in the EPIC-Norfolk eye study: principal components and associations. Invest Ophthalmol Vis Sci 54(10):6638–6645
Conflict of interest
The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kurna, S.A., Akar, G., Altun, A. et al. Confocal scanning laser tomography of the optic nerve head on the patients with Alzheimer’s disease compared to glaucoma and control. Int Ophthalmol 34, 1203–1211 (2014). https://doi.org/10.1007/s10792-014-0004-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10792-014-0004-z