Journal of Neural Transmission

, Volume 121, Issue 11, pp 1367–1376 | Cite as

Application of an OCT data-based mathematical model of the foveal pit in Parkinson disease

  • Yin Ding
  • Brian Spund
  • Sofya Glazman
  • Eric M. Shrier
  • Shahnaz Miri
  • Ivan Selesnick
  • Ivan Bodis-Wollner
Neurology and Preclinical Neurological Studies - Original Article

Abstract

Spectral-domain Optical coherence tomography (OCT) has shown remarkable utility in the study of retinal disease and has helped to characterize the fovea in Parkinson disease (PD) patients. We developed a detailed mathematical model based on raw OCT data to allow differentiation of foveae of PD patients from healthy controls. Of the various models we tested, a difference of a Gaussian and a polynomial was found to have “the best fit”. Decision was based on mathematical evaluation of the fit of the model to the data of 45 control eyes versus 50 PD eyes. We compared the model parameters in the two groups using receiver-operating characteristics (ROC). A single parameter discriminated 70 % of PD eyes from controls, while using seven of the eight parameters of the model allowed 76 % to be discriminated. The future clinical utility of mathematical modeling in study of diffuse neurodegenerative conditions that also affect the fovea is discussed.

Keywords

Fovea Retinal imaging Optical coherence tomography (OCT) Parkinson disease (PD) Mathematical modeling 

References

  1. Adam CR, Shrier E, Ding A, Bodis-Wollner I, Glazman S (2013) Correlation of inner retinal thickness evaluated by spectral-domain optical coherence tomography and contrast sensitivity in Parkinson disease. J Neuroophthalmol 33(2):137–142PubMedCrossRefGoogle Scholar
  2. Altintas O, Iseri P, Ozkan B, Caglar Y (2008) Correlation between retinal morphological and functional findings and clinical severity in Parkinsons disease. Doc Ophthalmol 116(2):137–146PubMedCrossRefGoogle Scholar
  3. Bagci AM, Shahidi M, Ansari R, Blair M, Blair NP, Zelkha R (2008) Thickness profiles of retinal layers by optical coherence tomography image segmentation. Am J Ophthalmol 146(5):679–687PubMedCrossRefPubMedCentralGoogle Scholar
  4. Bishop CM (2006) Pattern recognition and machine learning. Springer, New YorkGoogle Scholar
  5. Bodis-Wollner I (2013) Foveal vision is impaired in Parkinson’s disease. Parkinsonism Relat Disord 19(1):1–14PubMedCrossRefGoogle Scholar
  6. Bodis-Wollner I, Yahr MD (1978) Measurements of visual evoked potentials in Parkinson’s disease. Brain 101(4):661–671PubMedCrossRefGoogle Scholar
  7. Bodis-Wollner I, Glazman S, Yerram S (2013) Fovea and foveation in Parkinson’s disease. Behav Neurosci 127(2):139–150PubMedCrossRefGoogle Scholar
  8. Bodis-Wollner I, Miri S, Glazman S (2014) Venturing into the no-man’s land of the retina in Parkinson’s disease. Mov Disord 29(1):15–22PubMedCrossRefGoogle Scholar
  9. Brandt AU, Oberwahrenbrock T, Ringelstein M, Young KL, Tiede M, Hartung HP et al (2011) Primary retinal pathology in multiple sclerosis as detected by optical coherence tomography. Brain 134(11):e193–e193PubMedCrossRefGoogle Scholar
  10. Budenz DL, Fredette MJ, Feuer WJ, Anderson DR (2008) Reproducibility of peripapillary retinal nerve fiber thickness measurements with stratus OCT in glaucomatous eyes. Ophthalmology 115(4):661–666PubMedCrossRefGoogle Scholar
  11. Cubo E, Tedejo RP, Rodriguez Mendez V, Lopez Pena MJ, Trejo Gabriel Y, Galan JM (2010) Retinal thickness in Parkinson’s disease and essential tremor. Mov Disord 25:2461–2462PubMedCrossRefGoogle Scholar
  12. Djamgoz MBA, Hankins MW, Hirano J, Archer SN (1997) Neurobiology of retinal dopamine in relation to degenerative states of the tissue. Vision Res 37(24):3509–3529PubMedCrossRefGoogle Scholar
  13. Drexler W, Fujimoto JG (2008) State-of-the-art retinal optical coherence tomography. Prog retin eye res 27(1):45–88PubMedCrossRefGoogle Scholar
  14. Dubis AM, McAllister JT, Carroll J (2009) Reconstructing foveal pit morphology from optical coherence tomography imaging. Br J Ophthalmol 93(9):1223–1227PubMedCrossRefPubMedCentralGoogle Scholar
  15. Dubis AM, Costakos DM, Subramaniam CD, Godara P, Wirostko WJ, Carroll J, Provis JM (2012) Evaluation of normal human foveal development using optical coherence tomography and histologic examination. Arch Ophthalmol 130(10):1291–1300PubMedCrossRefPubMedCentralGoogle Scholar
  16. Dubis AM, Subramaniam CD, Godara P, Carroll J, Costakos DM (2013) Subclinical macular findings in infants screened for retinopathy of prematurity with spectral-domain optical coherence tomography. Ophthalmology 120(8):1665–1671PubMedCrossRefPubMedCentralGoogle Scholar
  17. Forooghian F, Cukras C, Meyerle CB, Chew EY, Wong WT (2008) Evaluation of time domain and spectral domain optical coherence tomography in the measurement of diabetic macular edema. Invest Ophthalmol Vis Sci 49(10):4290–4296PubMedCrossRefPubMedCentralGoogle Scholar
  18. Fortune B, Burgoyne CF, Cull G, Reynaud J, Wang L (2013) Onset and progression of peripapillary retinal nerve fiber layer (RNFL) retardance changes occur earlier than RNFL thickness changes in experimental glaucoma. Invest Ophthalmol Vis Sci 54(8):5653–5661PubMedCrossRefPubMedCentralGoogle Scholar
  19. Guo L, Duggan J, Cordeiro MF (2010) Alzheimer’s disease and retinal neurodegeneration. Curr Alzheimer Res 7(1):3–14PubMedCrossRefGoogle Scholar
  20. Hajee M, March W, Lazzaro D, Wolintz A, Shrier E, Glazman S, Bodis-Wollner I (2009) Inner retinal layer thinning in Parkinson disease. Arch Ophthalmol 127(6):737–741PubMedCrossRefGoogle Scholar
  21. Hanley JA, McNeil BJ (1982) The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143(1):29–36PubMedCrossRefGoogle Scholar
  22. Hirsch J, Curcio CA (1989) The spatial resolution capacity of human foveal retina. Vision Res 29(9):1095–1101PubMedCrossRefGoogle Scholar
  23. Huang D, Swanson EA, Lin CP, Schuman JS, Stinson WG (1991) Optical coherence tomography. Science 254(5035):1178–1181PubMedCrossRefGoogle Scholar
  24. Ikeda H, Head GM, Ellis CJ (1994) Electrophysiological signs of retinal dopamine deficiency in recently diagnosed Parkinson’s disease and a follow up study. Vision Res 34(19):2629–2638PubMedCrossRefGoogle Scholar
  25. Inzelberg R, Ramirez JA, Nisipeanu P, Ophir A (2004) Retinal nerve fiber layer thinning in Parkinson disease. Vision Res 44(24):2793–2797PubMedCrossRefGoogle Scholar
  26. Kashani AH, Zimmer-Galler IE, Shah SM, Dustin L, Do DV (2010) Retinal thickness analysis by race, gender, and age using Stratus OCT. Am J Ophthalmol 149(3):496–502PubMedCrossRefPubMedCentralGoogle Scholar
  27. Kirbas S, Turkyilmaz K, Anlar O, Tufekci A, Durmus M (2013) Retinal nerve fiber layer thickness in patients with Alzheimer disease. J Neuroophthalmol 33(1):58–61PubMedCrossRefGoogle Scholar
  28. Kromer R, Serbecic N, Hausner L, Froelich L, Aboul-Enein F, Beutelspacher SC (2014) Detection of retinal nerve fiber layer defects in Alzheimer’s disease using SD-OCT. Front Psychiatry 5:22. doi:10.3389/fpsyt.2014.00022 (Epub ahead of print)PubMedCrossRefPubMedCentralGoogle Scholar
  29. Leruez S, Annweiler C, Etcharry-Bouyx F, Verny C, Beauchet O, Milea D (2012) Alzheimer’s disease and visual impairment. J Fr Ophtalmol 35(4):308–311PubMedCrossRefGoogle Scholar
  30. Loduca AL, Zhang C, Zelkha R, Shahidi M (2010) Thickness mapping of retinal layers with spectral-domain optical coherence tomography. Am J Ophthalmol 150(6):849855CrossRefGoogle Scholar
  31. Matlab Statistics Toolbox Release (2011) The MathWorks Inc. Natick, Massachusetts 2011Google Scholar
  32. Moreno-Ramos T, Benito-León J, Villarejo A, Bermejo-Pareja F (2013) Retinal nerve fiber layer thinning in dementia associated with Parkinson’s disease, dementia with lewy bodies, and Alzheimer’s disease. J Alzheimers Dis 34(3):659–664PubMedGoogle Scholar
  33. Moschos MM, Tagaris G, Markopoulos I, Margetis I, Tsapakis S, Kanakis M, Koutsandrea C (2010) Morphologic changes and functional retinal impairment in patients with Parkinson disease without visual loss. Eur J Ophthalmol 21:24–29CrossRefGoogle Scholar
  34. Nguyen-Legros J (1988) Functional neuroarchitecture of the retina: hypothesis on the dysfunction of retinal dopaminergic circuitry in Parkinson’s disease. Surg Radiol Anat 10(2):137–144PubMedCrossRefGoogle Scholar
  35. Parisi V, Restuccia R, Fattapposta F, Mina C, Bucci MG, Pierelli F (2001) Morphological and functional retinal impairment in Alzheimer’s disease patients. Clin Neurophysiol 112(10):1860–1867PubMedCrossRefGoogle Scholar
  36. Provis JM, Hendrickson AE (2008) The foveal avascular region of developing human retina. Arch Ophthalmol 126(4):507–511PubMedCrossRefGoogle Scholar
  37. Provis JM, Diaz CM, Dreher B (1998) Ontogeny of the primate fovea: a central issue in retinal development. Prog Neurobiol 54(5):549–580PubMedCrossRefGoogle Scholar
  38. Pulicken M, Gordon-Lipkin E, Balcer LJ, Frohman E, Cutter G, Calabresi PA (2007) Optical coherence tomography and disease subtype in multiple sclerosis. Neurology 69(22):2085–2092PubMedCrossRefGoogle Scholar
  39. Sakata LM, Deleon-Ortega J, Sakata V, Girkin CA (2009) Optical coherence tomography of the retina and optic nerve—a review. Clin Experiment Ophthalmol 37(1):90–99PubMedCrossRefGoogle Scholar
  40. Scheibe P, Lazareva A, Braumann UD, Reichenbach A, Wiedemann P, Francke M, Rauscher FG (2014) Parametric model for the 3D reconstruction of individual fovea shape from OCT data. Exp Eye Res 119:19–26PubMedCrossRefGoogle Scholar
  41. Shrier EM, Adam CR, Spund B, Glazman S, Bodis-Wollner I (2012) Interocular asymmetry of foveal thickness in Parkinson disease. J Ophthalmol 2012:728457PubMedPubMedCentralGoogle Scholar
  42. Sikorski BL, Malukiewicz G, Stafiej J, Lesiewska-Junk H, Raczynska D (2013) The diagnostic function of OCT in diabetic maculopathy. Mediators Inflamm 2013:434560PubMedCrossRefPubMedCentralGoogle Scholar
  43. Song WK, Lee SC, Lee ES, Kim CY, Kim SS (2010) Macular thickness variations with sex, age, and axial length in healthy subjects: a spectral domain-optical coherence tomography study. Invest Ophthalmol Vis Sci 51(8):3913–3918PubMedCrossRefGoogle Scholar
  44. Spund BS, Ding Y, Liu T, Selesnick I, Glazman S, Shrier EM, Bodis-Wollner I (2013) Remodeling of the fovea in Parkinson disease. J. Neural Transm 120(5):745–753PubMedCrossRefGoogle Scholar
  45. Stanzione P, Fattapposta F, Tagliati M, D’Alessio C, Marciani MG, Foti A, Amabile G (1990) Dopaminergic pharmacological manipulations in normal humans confirm the specificity of the visual (PERG-VEP) and cognitive (P300) electrophysiological alterations in Parkinson’s disease. Electroencephalogr Clin Neurophysiol Suppl 41:216–220PubMedGoogle Scholar
  46. Sung KR, Kim DY, Park SB, Kook MS (2009) Comparison of retinal nerve fiber layer thickness measured by Cirrus HD and Stratus optical coherence tomography. Ophthalmology 116(7):1264–1270PubMedCrossRefGoogle Scholar
  47. Tick S, Rossant F, Ghorbel I, Gaudric A, Sahel JA (2011) Foveal shape and structure in a normal population. Invest Ophthalmol Vis Sci 52(8):5105–5110PubMedCrossRefGoogle Scholar
  48. Tomlins PH, Wang RK (2005) Theory, developments and applications of optical coherence tomography. J Physics D Appl Phys 38(15):2519CrossRefGoogle Scholar
  49. Tzekov R, Mullan M (2013) Vision function abnormalities in Alzheimer disease. Surv Ophthalmol. doi:10.1016/j.survophthal.2013.10.002 (Epub ahead of print)PubMedGoogle Scholar
  50. Wagner-Schuman M, Dubis AM, Nordgren RN, Lei Y, Odell D, Chiao H, Weh E, Fischer W, Sulai Y, Dubra A, Carroll J (2011) Race-and sex-related differences in retinal thickness and foveal pit morphology. Invest Ophthalmol Vis Sci 52(1):625–634PubMedCrossRefPubMedCentralGoogle Scholar
  51. Witkovsky P (2004) Dopamine and retinal function. Documenta ophthalmologica 108(1):17–39PubMedCrossRefGoogle Scholar
  52. Wolf-Schnurrbusch UE, Ceklic L, Brinkmann CK (2009) Macular thickness measurements in healthy eyes using six different optical coherence tomography instruments. Invest Ophthalmol Vis Sci 50(7):3432–3437PubMedCrossRefGoogle Scholar
  53. Wollstein G, Ishikawa H, Wang J, Beaton SA, Schuman JS (2005) Comparison of three optical coherence tomography scanning areas for detection of glaucomatous damage. Am J Ophthalmol 139(1):39–43PubMedCrossRefGoogle Scholar
  54. Young KL, Brandt AU, Petzold A, Reitz LY, Lintze F, Paul F et al (2013) Loss of retinal nerve fibre layer axons indicates white but not grey matter damage in early multiple sclerosis. Eur J Neurol 20(5):803–811PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2014

Authors and Affiliations

  • Yin Ding
    • 1
  • Brian Spund
    • 2
  • Sofya Glazman
    • 3
  • Eric M. Shrier
    • 4
    • 5
  • Shahnaz Miri
    • 3
  • Ivan Selesnick
    • 1
    • 6
  • Ivan Bodis-Wollner
    • 3
    • 4
    • 5
    • 6
  1. 1.Department of Electrical and Computer EngineeringPolytechnic Institute of New York UniversityBrooklynUSA
  2. 2.North Shore University HospitalManhassetUSA
  3. 3.Department of NeurologySUNY Downstate Medical CenterBrooklynUSA
  4. 4.Department of OphthalmologySUNY Downstate Medical CenterBrooklynUSA
  5. 5.SUNY Eye InstituteAlbanyNY
  6. 6.The School of Graduate StudiesSUNY Downstate Medical CenterBrooklynUSA

Personalised recommendations