Abstract
Purpose
To present characteristics of choriocapillaris layer imaging with swept-source optical coherence tomography angiography (SS-OCTA) in eyes with macular hole (MH).
Methods
Patients with MH were included. Vascular density of choriocapillaris (VDC) and central flow void areas were obtained using SS-OCTA. Data were compared with age- and gender-matched normal controls.
Results
Fifty-one patients with MH and 51 controls were included. Among the 51 patients with MH, 19 had lamellar MH (LMH) and 32 had full-thickness MH (FTMH). While VDC in LMH (79.26 ± 4.06%) was not significantly different from that seen in fellow eyes (79.88 ± 4.28%, P = 0.729) and normal controls (80.53 ± 4.21%, P = 1.000), VDC in surgically closed FTMH (74.60 ± 7.37%) was similar to that of fellow eyes (75.45 ± 7.39%, P = 0.400) but lower than that of controls (78.37 ± 7.13%, P = 0.011). On univariate analysis of 32 patients with unilateral sealed FTMH, VDC was not correlated with basal hole area (P = 0.797) or preoperative area of disrupted ellipsoid zone (P = 0.863). Central flow void was detected in 32 eyes. Mean central flow void area was 0.82 ± 0.84 mm2, which correlated with preoperative area of disrupted ellipsoid zone (P = 0.001).
Conclusions
Choriocapillaris layer imaging using SS-OCTA showed that choriocapillaris in both eyes of patients with unilateral FTMH had different characteristics from eyes with LMH or normal controls. These results suggest that variation in choriocapillaris layer flow is involved in the pathogenesis of MH.
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References
Ho AC, Guyer DR, Fine SL (1998) Macular hole. Surv Ophthalmol 42:393–416
Smiddy WE, Flynn HW Jr (2004) Pathogenesis of macular holes and therapeutic implications. Am J Ophthalmol 137:525–537. https://doi.org/10.1016/j.ajo.2003.12.011
McDonnell PJ, Fine SL, Hillis AI (1982) Clinical features of idiopathic macular cysts and holes. Am J Ophthalmol 93:777–786
Haouchine B, Massin P, Gaudric A (2001) Foveal pseudocyst as the first step in macular hole formation: a prospective study by optical coherence tomography. Ophthalmology 108:15–22
Spaide RF, Koizumi H, Pozzoni MC (2008) Enhanced depth imaging spectral-domain optical coherence tomography. Am J Ophthalmol 146:496–500. https://doi.org/10.1016/j.ajo.2008.05.032
Zhang P, Zhou M, Wu Y, Lu B, Li T, Zhao J, Wang F, Sun X (2017) Choroidal thickness in unilateral idiopathic macular hole: a cross-sectional study and meta-analysis. Retina 37:60–69. https://doi.org/10.1097/iae.0000000000001118
Zeng J, Li J, Liu R, Chen X, Pan J, Tang S, Ding X (2012) Choroidal thickness in both eyes of patients with unilateral idiopathic macular hole. Ophthalmology 119:2328–2333. https://doi.org/10.1016/j.ophtha.2012.06.008
Reibaldi M, Boscia F, Avitabile T, Uva MG, Russo V, Zagari M, Bonfiglio V, Reibaldi A, Longo A (2011) Enhanced depth imaging optical coherence tomography of the choroid in idiopathic macular hole: a cross-sectional prospective study. Am J Ophthalmol 151:112–117.e112. https://doi.org/10.1016/j.ajo.2010.07.004
Huang Y, Zhang Q, Thorell MR, An L, Durbin MK, Laron M, Sharma U, Gregori G, Rosenfeld PJ, Wang RK (2014) Swept-source OCT angiography of the retinal vasculature using intensity differentiation-based optical microangiography algorithms. Ophthalmic Surg Lasers Imaging Retina 45:382–389. https://doi.org/10.3928/23258160-20140909-08
Lane M, Moult EM, Novais EA, Louzada RN, Cole ED, Lee B, Husvogt L, Keane PA, Denniston AK, Witkin AJ, Baumal CR, Fujimoto JG, Duker JS, Waheed NK (2016) Visualizing the choriocapillaris under drusen: comparing 1050-nm swept-source versus 840-nm spectral-domain optical coherence tomography angiography. Invest Ophthalmol Vis Sci 57:OCT585–OCT590. https://doi.org/10.1167/iovs.15-18915
Moult EM, Waheed NK, Novais EA, Choi W, Lee B, Ploner SB, Cole ED, Louzada RN, Lu CD, Rosenfeld PJ, Duker JS, Fujimoto JG (2016) Swept-source optical coherence tomotraphy angiography reveals choriocapillaris alterations in eyes with nascent geographic atrophy and drusen-associated geographic atrophy. Retina 36(Suppl 1):S2–s11. https://doi.org/10.1097/iae.0000000000001287
Yannuzzi NA, Swaminathan SS, Zheng F, Miller A, Gregori G, Davis JL, Rosenfeld PJ (2017) Swept-source OCT angiography shows sparing of the choriocapillaris in multiple evanescent white dot syndrome. Ophthalmic Surg Lasers Imaging Retina 48:69–74. https://doi.org/10.3928/23258160-20161219-10
Moult E, Choi W, Waheed NK, Adhi M, Lee B, Lu CD, Jayaraman V, Potsaid B, Rosenfeld PJ, Duker JS, Fujimoto JG (2014) Ultrahigh-speed swept-source OCT angiography in exudative AMD. Ophthalmic Surg Lasers Imaging Retina 45:496–505. https://doi.org/10.3928/23258160-20141118-03
Choi W, Moult EM, Waheed NK, Adhi M, Lee B, Lu CD, de Carlo TE, Jayaraman V, Rosenfeld PJ, Duker JS, Fujimoto JG (2015) Ultrahigh-speed, swept-source optical coherence tomography angiography in nonexudative age-related macular degeneration with geographic atrophy. Ophthalmology 122:2532–2544. https://doi.org/10.1016/j.ophtha.2015.08.029
Zampedri E, Romanelli F, Semeraro F, Parolini B, Frisina R (2017) Spectral-domain optical coherence tomography findings in idiopathic lamellar macular hole. Graefes Arch Clin Exp Ophthalmol 255:699–707. https://doi.org/10.1007/s00417-016-3545-1
Takahashi H, Kishi S (2000) Tomographic features of a lamellar macular hole formation and a lamellar hole that progressed to a full-thickness macular hole. Am J Ophthalmol 130:677–679
Haouchine B, Massin P, Tadayoni R, Erginay A, Gaudric A (2004) Diagnosis of macular pseudoholes and lamellar macular holes by optical coherence tomography. Am J Ophthalmol 138:732–739. https://doi.org/10.1016/j.ajo.2004.06.088
Michalewska Z, Michalewski J, Cisiecki S, Adelman R, Nawrocki J (2008) Correlation between foveal structure and visual outcome following macular hole surgery: a spectral optical coherence tomography study. Graefes Arch Clin Exp Ophthalmol 246:823–830. https://doi.org/10.1007/s00417-007-0764-5
Theodossiadis PG, Grigoropoulos VG, Theodossiadis GP (2011) The significance of the external limiting membrane in the recovery of photoreceptor layer after successful macular hole closure: a study by spectral domain optical coherence tomography. Ophthalmologica 225:176–184. https://doi.org/10.1159/000323322
Gherghel D, Orgul S, Gugleta K, Gekkieva M, Flammer J (2000) Relationship between ocular perfusion pressure and retrobulbar blood flow in patients with glaucoma with progressive damage. Am J Ophthalmol 130:597–605
Copete S, Flores-Moreno I, Montero JA, Duker JS, Ruiz-Moreno JM (2014) Direct comparison of spectral-domain and swept-source OCT in the measurement of choroidal thickness in normal eyes. Br J Ophthalmol 98:334–338. https://doi.org/10.1136/bjophthalmol-2013-303904
Adhi M, Liu JJ, Qavi AH, Grulkowski I, Lu CD, Mohler KJ, Ferrara D, Kraus MF, Baumal CR, Witkin AJ, Waheed NK, Hornegger J, Fujimoto JG, Duker JS (2014) Choroidal analysis in healthy eyes using swept-source optical coherence tomography compared to spectral domain optical coherence tomography. Am J Ophthalmol 157:1272–1281.e1271. https://doi.org/10.1016/j.ajo.2014.02.034
Teng Y, Yu M, Wang Y, Liu X, You Q, Liu W (2017) OCT angiography quantifying choriocapillary circulation in idiopathic macular hole before and after surgery. Graefes Arch Clin Exp Ophthalmol 255:893–902. https://doi.org/10.1007/s00417-017-3586-0
Rymer J, Wildsoet CF (2005) The role of the retinal pigment epithelium in eye growth regulation and myopia: a review. Vis Neurosci 22:251–261. https://doi.org/10.1017/s0952523805223015
Nickla DL, Wallman J (2010) The multifunctional choroid. Prog Retin Eye Res 29:144–168. https://doi.org/10.1016/j.preteyeres.2009.12.002
Fryczkowski AW (1994) Anatomical and functional choroidal lobuli. Int Ophthalmol 18:131–141
Lovasik JV, Kergoat H (2012) Systemic determinants. In: Schmetterer L, Kiel JW (eds) Ocular blood flow. Springer, New York, pp 173–210
Chen FK, Viljoen RD, Bukowska DM (2016) Classification of image artefacts in optical coherence tomography angiography of the choroid in macular diseases. Clin Exp Ophthalmol 44:388–399. https://doi.org/10.1111/ceo.12683
Shinojima A, Kawamura A, Mori R, Fujita K, Yuzawa M (2016) Findings of optical coherence tomographic angiography at the choriocapillaris level in central serous chorioretinopathy. Ophthalmologica 236:108–113. https://doi.org/10.1159/000448436
Gass JD (1976) Lamellar macular hole: a complication of cystoid macular edema after cataract extraction. Arch Ophthalmol 94:793–800
Oh JH, Oh J (2015) Moment of cyst eruption captured by optical coherence tomography in diabetic macular edema. Retina 35:1283–1284. https://doi.org/10.1097/iae.0000000000000419
Govetto A, Dacquay Y, Farajzadeh M, Platner E, Hirabayashi K, Hosseini H, Schwartz SD, Hubschman JP (2016) Lamellar macular hole: two distinct clinical entities? Am J Ophthalmol 164:99–109. https://doi.org/10.1016/j.ajo.2016.02.008
Wangsa-Wirawan ND, Linsenmeier RA (2003) Retinal oxygen: fundamental and clinical aspects. Arch Ophthalmol 121:547–557. https://doi.org/10.1001/archopht.121.4.547
Riva CE, Titze P, Hero M, Petrig BL (1997) Effect of acute decreases of perfusion pressure on choroidal blood flow in humans. Invest Ophthalmol Vis Sci 38:1752–1760
Riva CE, Titze P, Hero M, Movaffaghy A, Petrig BL (1997) Choroidal blood flow during isometric exercises. Invest Ophthalmol Vis Sci 38:2338–2343
Yun C, Ahn J, Kim M, Hwang SY, Kim SW, Oh J (2016) Ocular perfusion pressure and choroidal thickness in early age-related macular degeneration patients with reticular pseudodrusen. Invest Ophthalmol Vis Sci 57:6604–6609. https://doi.org/10.1167/iovs.16-19989
Rishi P, Rishi E, Mathur G, Raval V (2013) Ocular perfusion pressure and choroidal thickness in eyes with polypoidal choroidal vasculopathy, wet-age-related macular degeneration, and normals. Eye (Lond) 27:1038–1043. https://doi.org/10.1038/eye.2013.106
Flower RW, Fryczkowski AW, McLeod DS (1995) Variability in choriocapillaris blood flow distribution. Invest Ophthalmol Vis Sci 36:1247–1258
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This manuscript is based upon work supported by the Ministry of Trade, Industry & Energy (MOTIE, Korea) under Industrial Technology Innovation (10063364).
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J.O. is a consultant of Topcon Corporation. Other authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers’ bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge, or beliefs) in the subject matter or materials discussed in this manuscript.
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Ahn, J., Yoo, G., Kim, J.T. et al. Choriocapillaris layer imaging with swept-source optical coherence tomography angiography in lamellar and full-thickness macular hole. Graefes Arch Clin Exp Ophthalmol 256, 11–21 (2018). https://doi.org/10.1007/s00417-017-3814-7
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DOI: https://doi.org/10.1007/s00417-017-3814-7