Article | Published:

Changes in volume of various retinal layers over time in early and intermediate age-related macular degeneration

Eyevolume 33pages428434 (2019) | Download Citation

Abstract

Purpose

To evaluate longitudinally volume changes in inner and outer retinal layers in early and intermediate age-related macular degeneration (AMD) compared to healthy control eyes using optical coherence tomography (OCT).

Methods

71 eyes with AMD and 31 control eyes were imaged at two time points: baseline and after 2 years. Automated OCT layer segmentation was performed using OrionTM. This software is able to measure volumes of retinal layers with distinct boundaries including Retinal Nerve Fibre Layer (RNFL), Ganglion Cell-Inner Plexiform Layer (GCIPL), Inner Nuclear Layer (INL), Outer Plexiform Layer (OPL), Outer Nuclear Layer (ONL), Photoreceptors (PR) and Retinal Pigment Epithelium–Bruch’s Membrane complex (RPE-BM). The mean retinal layer volumes and volume changes at 2 years were compared between groups.

Results

Mean GCIPL and INL volumes were lower, while PR and RPE-BM volumes were higher in AMD eyes than controls at baseline (all P < 0.05) and year 2 (all P < 0.05). In AMD eyes, RNFL and ONL volumes decreased by 0.0232 (P = 0.033) and 0.0851 (P = 0.001), respectively. In contrast, OPL and RPE-BM volumes increased in AMD eyes by 0.0391 (P = 0.000) and 0.0209 (P = 0.000) respectively. Moreover, there were significant differences in longitudinal volume change of OPL (P = 0.02), ONL (P = 0.008) and RPE-BM (P = 0.02) between AMD eyes and controls.

Conclusions

There were abnormal retinal layer volumes and volume changes in eyes with early and intermediate AMD.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    van Leeuwen R, Klaver CC, Vingerling JR, Hofman A, de Jong PT. Epidemiology of age-related maculopathy: a review. Eur J Epidemiol. 2003;18:845–54.

  2. 2.

    Friedman DS, O’Colmain BJ, Munoz B, Tomany SC, McCarty C, de Jong PT, et al. Prevalence of age-related macular degeneration in the United States. Arch Ophthalmol. 2004;122:564–72.

  3. 3.

    Resnikoff S, Pascolini D, Etya’ale D, Kocur I, Pararajasegaram R, Pokharel GP, et al. Global data on visual impairment in the year 2002. Bull World Health Organ. 2004;82:844–51.

  4. 4.

    Ferris FL 3rd, Wilkinson CP, Bird A, Chakravarthy U, Chew E, Csaky K, et al. Clinical classification of age-related macular degeneration. Ophthalmology. 2013;120:844–51.

  5. 5.

    Ferris FL 3rd, Fine SL, Hyman L. Age-related macular degeneration and blindness due to neovascular maculopathy. Arch Ophthalmol. 1984;102:1640–2.

  6. 6.

    Green WR, Enger C. Age-related macular degeneration histopathologic studies. The 1992 Lorenz E. Zimmerman Lecture. Ophthalmology. 1993;100:1519–35.

  7. 7.

    Campochiaro PA, Soloway P, Ryan SJ, Miller JW. The pathogenesis of choroidal neovascularization in patients with age-related macular degeneration. Mol Vis. 1999;5:34.

  8. 8.

    Curcio CA, Medeiros NE, Millican CL. Photoreceptor loss in age-related macular degeneration. Invest Ophthalmol Vis Sci. 1996;37:1236–49.

  9. 9.

    Jackson GR, Owsley C, Curcio CA. Photoreceptor degeneration and dysfunction in aging and age-related maculopathy. Ageing Res Rev. 2002;1:381–96.

  10. 10.

    Medeiros NE, Curcio CA. Preservation of ganglion cell layer neurons in age-related macular degeneration. Invest Ophthalmol Vis Sci. 2001;42:795–803.

  11. 11.

    Schuman SG, Koreishi AF, Farsiu S, Jung SH, Izatt JA, Toth CA. Photoreceptor layer thinning over drusen in eyes with age-related macular degeneration imaged in vivo with spectral-domain optical coherence tomography. Ophthalmology. 2009;116:488–96.e2.

  12. 12.

    Hartmann KI, Gomez ML, Bartsch DU, Schuster AK, Freeman WR. Effect of change in drusen evolution on photoreceptor inner segment/outer segment junction. Retina. 2012;32:1492–9.

  13. 13.

    Sadigh S, Cideciyan AV, Sumaroka A, Huang WC, Luo X, Swider M, et al. Abnormal thickening as well as thinning of the photoreceptor layer in intermediate age-related macular degeneration. Invest Ophthalmol Vis Sci. 2013;54:1603–12.

  14. 14.

    Sadigh S, Luo X, Cideciyan AV, Sumaroka A, Boxley SL, Hall LM, et al. Drusen and photoreceptor abnormalities in African-Americans with intermediate non-neovascular age-related macular degeneration. Curr Eye Res. 2015;40:398–406.

  15. 15.

    Tan J, Yang Y, Jiang H, Liu C, Deng Z, Lam BL, et al. The measurement repeatability using different partition methods of intraretinal tomographic thickness maps in healthy human subjects. Clin Ophthalmol. 2016;10:2403–15.

  16. 16.

    Terry L, Cassels N, Lu K, Acton JH, Margrain TH, North RV, et al. Automated retinal layer segmentation using spectral domain optical coherence tomography: evaluation of inter-session repeatability and agreement between devices. PLoS ONE. 2016;11:e0162001.

  17. 17.

    Savastano MC, Minnella AM, Tamburrino A, Giovinco G, Ventre S, Falsini B. Differential vulnerability of retinal layers to early age-related macular degeneration: evidence by SD-OCT segmentation analysis. Invest Ophthalmol Vis Sci. 2014;55:560–6.

  18. 18.

    Lee EK, Yu HG. Ganglion cell-inner plexiform layer and peripapillary retinal nerve fiber layer thicknesses in age-related macular degeneration. Invest Ophthalmol Vis Sci. 2015;56:3976–83.

  19. 19.

    Yenice E, Sengun A, Soyugelen Demirok G, Turacli E. Ganglion cell complex thickness in nonexudative age-related macular degeneration. Eye. 2015;29:1076–80.

  20. 20.

    Zucchiatti I, Parodi MB, Pierro L, Cicinelli MV, Gagliardi M, Castellino N, et al. Macular ganglion cell complex and retinal nerve fiber layer comparison in different stages of age-related macular degeneration. Am J Ophthalmol. 2015;160:602–7.e1.

  21. 21.

    Muftuoglu IK, Ramkumar HL, Bartsch DU, Meshi A, Gaber R, Freeman WR. Quantitative analysis of the inner retinal layer thicknesses in age-related macular degeneration using corrected optical coherence tomography segmentation. Retina. 2017;38:1478–84.

  22. 22.

    Borrelli E, Abdelfattah NS, Uji A, Nittala MG, Boyer DS, Sadda SR. Postreceptor neuronal loss in intermediate age-related macular degeneration. Am J Ophthalmol. 2017;181:1–11.

  23. 23.

    Camacho P, Dutra-Medeiros M, Paris L. Ganglion cell complex in early and intermediate age-related macular degeneration: evidence by SD-OCT manual segmentation. Ophthalmologica. 2017;238:31–43.

  24. 24.

    Villegas-Perez MP, Lawrence JM, Vidal-Sanz M, Lavail MM, Lund RD. Ganglion cell loss in RCS rat retina: a result of compression of axons by contracting intraretinal vessels linked to the pigment epithelium. J Comp Neurol. 1998;392:58–77.

  25. 25.

    Feigl B, Brown B, Lovie-Kitchin J, Swann P. Functional loss in early age-related maculopathy: the ischaemia postreceptoral hypothesis. Eye. 2007;21:689–96.

  26. 26.

    Toto L, Borrelli E, Di Antonio L, Carpineto P, Mastropasqua R. Retinal vascular plexuses’ changes in dry age-related macular degeneration, evaluated by means of optical coherence tomography angiography. Retina. 2016;36:1566–72.

  27. 27.

    Toto L, Borrelli E, Mastropasqua R, Di Antonio L, Doronzo E, Carpineto P, et al. Association between outer retinal alterations and microvascular changes in intermediate stage age-related macular degeneration: an optical coherence tomography angiography study. Br J Ophthalmol. 2017;101:774–9.

  28. 28.

    Strettoi E, Porciatti V, Falsini B, Pignatelli V, Rossi C. Morphological and functional abnormalities in the inner retina of the rd/rd mouse. J Neurosci: Off J Soc Neurosci. 2002;22:5492–504.

  29. 29.

    Gartner S, Henkind P. Aging and degeneration of the human macula. 1. Outer nuclear layer and photoreceptors. Br J Ophthalmol. 1981;65:23–8.

  30. 30.

    Machida S, Kondo M, Jamison JA, Khan NW, Kononen LT, Sugawara T, et al. P23H rhodopsin transgenic rat: correlation of retinal function with histopathology. Invest Ophthalmol Vis Sci. 2000;41:3200–9.

  31. 31.

    Shelley EJ, Madigan MC, Natoli R, Penfold PL, Provis JM. Cone degeneration in aging and age-related macular degeneration. Arch Ophthalmol. 2009;127:483–92.

  32. 32.

    Behbehani R, Abu Al-Hassan A, Al-Salahat A, Sriraman D, Oakley JD, Alroughani R. Optical coherence tomography segmentation analysis in relapsing remitting versus progressive multiple sclerosis. PLoS ONE. 2017;12:e0172120.

  33. 33.

    Ferrara D, Silver RE, Louzada RN, Novais EA, Collins GK, Seddon JM. Optical coherence tomography features preceding the onset of advanced age-related macular degeneration. Invest Ophthalmol Vis Sci. 2017;58:3519–29.

Download references

Acknowledgements

The research was supported by the National Institute for Health Research (NIHR) Biomedical Research Centre based at Moorfields Eye Hospital NHS Foundation Trust and UCL Institute of Ophthalmology. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR or the Department of Health.

Author information

Affiliations

  1. NIHR Moorfields Biomedical Research Centre, Moorfields Eye Hospital NHS Foundation Trust, London, UK

    • Ali Lamin
    • , Adam M. Dubis
    •  & Sobha Sivaprasad
  2. UCL Institute of Ophthalmology, London, UK

    • Ali Lamin
    • , Adam M. Dubis
    •  & Sobha Sivaprasad
  3. Voxeleron LLC, Pleasanton, CA, USA

    • Jonathan D. Oakley
    •  & Daniel B. Russakoff

Authors

  1. Search for Ali Lamin in:

  2. Search for Jonathan D. Oakley in:

  3. Search for Adam M. Dubis in:

  4. Search for Daniel B. Russakoff in:

  5. Search for Sobha Sivaprasad in:

Conflict of interest

The authors declare that they have no conflict of interest.

Corresponding author

Correspondence to Sobha Sivaprasad.

About this article

Publication history

Received

Accepted

Published

Issue Date

DOI

https://doi.org/10.1038/s41433-018-0234-9