Investigating the choriocapillaris and choroidal vasculature with new optical coherence tomography technologies

https://doi.org/10.1016/j.preteyeres.2015.10.002Get rights and content

Abstract

The body of knowledge of in vivo investigation of the choroid has been markedly enhanced by recent technological advances in optical coherence tomography (OCT). New insights elucidating the morphological features of the choriocapillaris and choroidal vasculature, in both physiological and pathological conditions, indicate that the choroid plays a pivotal role in many posterior segment diseases. In this article, a review of the histological characteristics of the choroid, which must be considered for the proper interpretation of in vivo imaging, is followed by a comprehensive discussion of fundamental principles of the current state-of-the-art in OCT, including cross-sectional OCT, en face OCT, and OCT angiography using both spectral domain OCT and swept source OCT technologies. A detailed review of the tomographic features of the choroid in the normal eye is followed by relevant findings in prevalent chorioretinal diseases, focusing on major causes of vision loss such as typical early and advanced age-related macular degeneration, polypoidal choroidal vasculopathy, central serous chorioretinopathy, pachychoroid spectrum disorders, diabetic choroidopathy, and myopia.

Section snippets

Basic histology of the choroid in normal eyes

The morphological features of the Bruch membrane/choriocapillaris complex and choroidal vasculature on ex-vivo histology, described herein, are relevant for the proper interpretation of the optical reconstruction of the tissue through in vivo fundus imaging.

Basic principles of Fourier domain optical coherence tomography

Optical coherence tomography is based on the physical principle of interferometry; a Michaelson interferometer uses the wavelength of the light as its own timing standard. The micron-scale resolution is obtained by comparison between the time of flight of the sample reflection and the known time of delay of a reference reflection, by looking for phase differences in the light interference. Coherence of light is conceptualized as a measure of how two waves of light are correlated to each other

Total choroidal thickness

Technological advances on Fourier domain OCT that took place in the last few years, including acquisition techniques and post-acquisition processing methods, greatly contributed to a better visualization of deeper structures such as the choroid on cross-sectional OCT. The total choroidal thickness could be more precisely assessed, either at the subfoveal region or throughout the length of the cross-sectional scan, because the choroidal-scleral interface became easier to identify (Adhi et al.,

Typical age-related macular degeneration

Studies with cross-sectional OCT show somewhat discordant results related to subfoveal total choroidal thickness measurements in AMD. Discrepant results may be related to wide variability of choroidal morphology in the population, as well as to limitations of quantitative and qualitative assessment of the choroid on cross-sectional OCT. In addition, discordance across studies may be related to different disease stages and specific clinical features, such as the sub-type of choroidal

Future directions

Tridimensional, dense volumetric datasets acquired with faster and deeper OCT scans are currently a valuable tool to investigate the posterior segment of the eye, from the vitreous cavity to the choroidal scleral interface. New advances on OCT have dramatically increased our understanding of the morphology and function of chorioretinal tissues. Emerging advances on spectral domain OCT and swept source OCT, including en face OCT and OCT angiography, are definitive game changers in the research

Conflicts of interest

Jay S. Duker receives research support from Carl Zeiss Meditech, Inc. and Optovue, Inc. Daniela Ferrara is an employee at Genentech, Inc. and receives stock/stock options from Roche.

Acknowledgments

We acknowledge support from NIH (R01-EY011289-27, R01-EY013178-12, R01-EY018184-05, R44EY022864-01, R01-CA075289-16, R01-NS057476-05, R44-EY022864-01); AFOSR (FA9550-10-1-0551 and FA9550-10-1-0063); Massachusetts Lions Club; German Science Foundation DFG (DFG-GSC80-SAOT). The funding organizations had no role in the design or conduct of this research.

References (288)

  • S.E. Chung et al.

    Choroidal thickness in polypoidal choroidal vasculopathy and exudative age-related macular degeneration

    Ophthalmology

    (2011)
  • S.W. Cousins et al.

    The role of aging, high fat diet and blue light exposure in an experimental mouse model for basal laminar deposit formation

    Exp. Eye Res.

    (2002)
  • T.E. de Carlo et al.

    Spectral-domain optical coherence tomography angiography of choroidal neovascularization

    Ophthalmology

    (2015)
  • J.R. Evans

    Risk factors for age-related macular degeneration

    Prog. Retin Eye Res.

    (2001)
  • L. Feeney-Burns et al.

    Age-related macular changes in humans over 90 years old

    Am. J. Ophthalmol.

    (1990)
  • D. Ferrara et al.

    En face enhanced-depth swept-source optical coherence tomography features of chronic central serous chorioretinopathy

    Ophthalmology

    (2014)
  • T. Fujiwara et al.

    Enhanced depth imaging optical coherence tomography of the choroid in highly myopic eyes

    Am. J. Ophthalmol.

    (2009)
  • J. Gong et al.

    Effects of extracellular matrix and neighboring cells on induction of human embryonic stem cells into retinal pigment epithelial progenitors

    Exp. Eye Res.

    (2008)
  • G.S. Hageman et al.

    An integrated hypothesis that considers drusen as biomarkers of immune-mediated processes at the RPE-Bruch membrane interface in aging and age-related macular degeneration

    Prog. Retin Eye Res.

    (2001)
  • A.A. Hidayat et al.

    Diabetic choroidopathy. Light and electron microscopic obervations of seven cases

    Ophthalmology

    (1985)
  • J. Ho et al.

    Analysis of normal peripapillary choroidal thickness via spectral domain optical coherence tomography

    Ophthalmology

    (2011)
  • M. Adhi et al.

    Optical coherence tomography – current and future applications

    Curr. Opin. Ophthalmol.

    (2013)
  • M. Adhi et al.

    Analysis of morphological features and vascular layers of choroid in diabetic retinopathy using spectral-domain optical coherence tomography

    JAMA Ophthalmol.

    (2013)
  • M. Adhi et al.

    Enhanced visualization of the choroido-scleral interface using swept-source OCT

    Ophthalmic Surg. Lasers Imaging Retina

    (2013)
  • M. Adhi et al.

    Choroidal analysis in healthy eyes using swept-spirce optical coherence tomography compared to spectral domain optical coherence tomography

    Am. J. Ophthalmol.

    (2014)
  • M. Adhi et al.

    Characterization of choroidal layers in normal aging eyes using enface swept-source optical coherence tomography

    PLoS One

    (2015)
  • T. Agawa et al.

    Choroidal thickness measurement in healthy Japanese subjects by three-dimensional high-penetration optical coherence tomography

    Graefes Arch. Clin. Exp. Ophthalmol.

    (2011)
  • T. Alasil et al.

    En face imaging of the choroid in polypoidal choroidal vasculopathy using swept-source optical coherence tomography

    Am. J. Ophthalmol.

    (2015)
  • A. Alm et al.

    Ocular and optic nerve blood flow at normal and increased intraocular pressures in monkeys (Macaca irus): a study with radioactively labelled microspheres including flow determinations in brain and someother tissues

    Exp. Eye Res.

    (1973)
  • A. Benavente-Perez et al.

    Reproducibility-repeatability of choroidal thickness calculation using optical coherence tomography

    Optom. Vis. Sci.

    (2010)
  • J. Bergamnson

    The ophthalmic innervation of the uvea in monkeys

    Exp. Eye Res.

    (1977)
  • A. Bindewald et al.

    Classification of abnormal fundus autofluorescence patterns in the junctional zone of geographic atrophy in patients with age-related macular degeneration

    Br. J. Ophthalmol.

    (2005)
  • A.C. Bird

    Therapeutic targets in age-related macular disease

    J. Clin. Invest

    (2010)
  • M.A. Bonini Filho et al.

    Association of choroidal neovascularization and central serous chorioretinopathy with optical coherence tomography angiography

    JAMA Ophthalmol.

    (2015 May)
  • N.S. Bora et al.

    Differential expression of the complement regulatory proteins in the human eye

    Invest Ophthalmol. Vis. Sci.

    (1993)
  • C. Brandl et al.

    Choroidal thickness measurements during central serous chorioretinopathy treatment

    Int. Ophthalmol.

    (2014)
  • R.D. Braun et al.

    Quantification of erythrocyte flow in the choroid of the albino rat

    Am. J. Physiol.

    (1997)
  • A.J. Bron et al.

    Wolff's Anatomy of the Eye and Orbit

    (1997)
  • J.S. Brown et al.

    In vivo human choroidal thickness measurements: evidence for diurnal fluctuations

    Invest Ophthalmol. Vis. Sci.

    (2009)
  • E. Buschini et al.

    Recent developments in the management of dry-age related macular degeneration

    Clin. Ophthalmol.

    (2015)
  • V. Caillaux et al.

    Morphologic characterization of dome-shaped macula in myopic eyes with serous macular detachment

    Am. J. Ophthalmol.

    (2013)
  • P. Carrai et al.

    Wide-field spectral domain-optical coherence tomography in central serous chorioretinopathy

    Int. Ophthalmol.

    (2015)
  • R. Chakraborty et al.

    Diurnal variations in axial length, choroidal thickness, intraocular pressure, and ocular biometrics

    Invest Ophthalmol. Vis. Sci.

    (2011)
  • T. Chassine et al.

    How can we prevent myopia progression?

    Eur. J. Ophthalmol.

    (2015)
  • Q. Chen et al.

    Automated choroid segmentation based on gradual intensity distance in HD-OCT images

    Opt. Express

    (2015)
  • S.R. Chinn et al.

    Optical coherence tomography using a frequency-tunable optical source

    Opt. Lett.

    (1997)
  • W. Choi et al.

    Choriocapillaris and choroidal microvasculature imaging with ultrahigh speed OCT angiography

    PLoS One

    (2013)
  • M. Choma et al.

    Sensitivity advantage of swept source and Fourier domain optical coherence tomography

    Opt. Express

    (2003)
  • M.V. Cicinelli et al.

    Optical coherence tomography and pathological myopia: an update of the literature

    Int. Ophthalmol

    (2015)
  • S. Copete et al.

    Direct comparison of spectral-domain and swept-source OCT in the measurement of choroidal thickness in normal eyes

    Br. J. Ophthalmol.

    (2014)
  • Cited by (219)

    View all citing articles on Scopus
    View full text