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Published in: Journal of Ophthalmic Inflammation and Infection 1/2014

Open Access 01-12-2014 | Original research

Choroidal atrophy and loss of choriocapillaris in convalescent stage of Vogt-Koyanagi-Harada disease: in vivo documentation

Authors: Hossein Nazari, Amirhossein Hariri, Zhihong Hu, Yanwei Ouyang, SiriniVas Sadda, Narsing A Rao

Published in: Journal of Ophthalmic Inflammation and Infection | Issue 1/2014

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Abstract

Background

The aim of this study was to determine the clinical significance of posterior choroidal thickness and vascular changes in the convalescent stage of Vogt-Koyanagi-Harada disease (VKH). Macular spectral domain optical coherence tomography (SD-OCT) images of 22 eyes of 13 consecutive patients with VKH at the convalescent stage were compared to 17 eyes of 9 age/sex/refraction-matched normal subjects. The choriocapillaris layer, medium choroidal vessels (Sattler's layer), and large choroidal vessels (Haller's layer) were assessed in foveal SD-OCT scans. The presence and the extent of disruption of outer retinal structures were also noted. Inner and outer choroid boundaries were manually drawn on horizontal raster SD-OCT scans, and choroidal thickness and volume maps were generated. Correlation analysis was run to assess the association of the above parameters in the VKH patients compared to the normal subjects.

Results

In the eyes with convalescent stage of VKH, mean choroidal thickness in the foveal central subfield (200 ± 60 μm) was lower than in matched controls (288 ± 40 μm) (P < 0.0001). A thinner sub-macular choroid correlated with a lower visual acuity in uveitis eyes (Pearson correlation, r = -0.5089, P = 0.005). While the choriocapillaris layer was continuous and intact in all control eyes, various degrees of choriocapillaris loss were observed in 11 eyes (50%) with VKH (P < 0.0001). In these patients, the presence of outer retinal disruption was associated with a lower visual acuity (Spearman correlation, P < 0.001).

Conclusions

The choroid is significantly thinner and the choriocapillaris layer is disrupted in the eyes with convalescent stage of VKH. Evaluation of the choriocapillaris in SD-OCT scans may be a useful surrogate marker for visual function in the convalescent stage of VKH.
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Literature
1.
go back to reference Moorthy RS, Inomata H, Rao NA: Vogt-Koyanagi-Harada syndrome. Surv Ophthalmol 1995, 39: 265–292. 10.1016/S0039-6257(05)80105-5CrossRefPubMed Moorthy RS, Inomata H, Rao NA: Vogt-Koyanagi-Harada syndrome. Surv Ophthalmol 1995, 39: 265–292. 10.1016/S0039-6257(05)80105-5CrossRefPubMed
2.
go back to reference Rao NA, Gupta A, Dustin L, Chee SP, Okada AA, Khairallah M, Bodaghi B, Lehoang P, Rao NA, Gupta A, Dustin L, Chee SP, Okada AA, Khairallah M, Bodaghi B, Lehoang P, Accorinti M, Mochizuki M, Prabriputaloong T, Read RW: Frequency of distinguishing clinical features in Vogt-Koyanagi-Harada disease. Ophthalmology 2010, 117: 591–599. 9 e1 10.1016/j.ophtha.2009.08.030PubMedCentralCrossRefPubMed Rao NA, Gupta A, Dustin L, Chee SP, Okada AA, Khairallah M, Bodaghi B, Lehoang P, Rao NA, Gupta A, Dustin L, Chee SP, Okada AA, Khairallah M, Bodaghi B, Lehoang P, Accorinti M, Mochizuki M, Prabriputaloong T, Read RW: Frequency of distinguishing clinical features in Vogt-Koyanagi-Harada disease. Ophthalmology 2010, 117: 591–599. 9 e1 10.1016/j.ophtha.2009.08.030PubMedCentralCrossRefPubMed
3.
go back to reference Rao NA: Pathology of Vogt-Koyanagi-Harada disease. Int Ophthalmol 2007, 27: 81–85. 10.1007/s10792-006-9029-2CrossRefPubMed Rao NA: Pathology of Vogt-Koyanagi-Harada disease. Int Ophthalmol 2007, 27: 81–85. 10.1007/s10792-006-9029-2CrossRefPubMed
4.
go back to reference Takahashi H, Takase H, Ishizuka A, Miyanaga M, Kawaguchi T, Ohno-Matsui K, Mochizuki M: Choroidal thickness in convalescent Vogt-Koyanagi-Harada disease. Retina 2013. [Epublication ahead of print] Takahashi H, Takase H, Ishizuka A, Miyanaga M, Kawaguchi T, Ohno-Matsui K, Mochizuki M: Choroidal thickness in convalescent Vogt-Koyanagi-Harada disease. Retina 2013. [Epublication ahead of print]
5.
go back to reference Forster DJ, Cano MR, Green RL, Rao NA: Echographic features of the Vogt-Koyanagi-Harada syndrome. Arch Ophthalmol 1990, 108: 1421–1426. 10.1001/archopht.1990.01070120069031CrossRefPubMed Forster DJ, Cano MR, Green RL, Rao NA: Echographic features of the Vogt-Koyanagi-Harada syndrome. Arch Ophthalmol 1990, 108: 1421–1426. 10.1001/archopht.1990.01070120069031CrossRefPubMed
6.
go back to reference Inomata H, Rao NA: Depigmented atrophic lesions in sunset glow fundi of Vogt-Koyanagi-Harada disease. Am J Ophthalmol 2001, 131: 607–614. 10.1016/S0002-9394(00)00851-5CrossRefPubMed Inomata H, Rao NA: Depigmented atrophic lesions in sunset glow fundi of Vogt-Koyanagi-Harada disease. Am J Ophthalmol 2001, 131: 607–614. 10.1016/S0002-9394(00)00851-5CrossRefPubMed
7.
go back to reference Agawa T, Miura M, Ikuno Y, Makita S, Fabritius T, Iwasaki T, Goto H, Nishida K, Yasuno Y: Choroidal thickness measurement in healthy Japanese subjects by three-dimensional high-penetration optical coherence tomography. Graefes Arch Clin Exp Ophthalmol 2011, 249: 1485–1492. 10.1007/s00417-011-1708-7CrossRefPubMed Agawa T, Miura M, Ikuno Y, Makita S, Fabritius T, Iwasaki T, Goto H, Nishida K, Yasuno Y: Choroidal thickness measurement in healthy Japanese subjects by three-dimensional high-penetration optical coherence tomography. Graefes Arch Clin Exp Ophthalmol 2011, 249: 1485–1492. 10.1007/s00417-011-1708-7CrossRefPubMed
8.
go back to reference Branchini L, Regatieri CV, Flores-Moreno I, Baumann B, Fujimoto JG, Duker JS: Reproducibility of choroidal thickness measurements across three spectral domain optical coherence tomography systems. Ophthalmology 2012, 119: 119–123. 10.1016/j.ophtha.2011.07.002PubMedCentralCrossRefPubMed Branchini L, Regatieri CV, Flores-Moreno I, Baumann B, Fujimoto JG, Duker JS: Reproducibility of choroidal thickness measurements across three spectral domain optical coherence tomography systems. Ophthalmology 2012, 119: 119–123. 10.1016/j.ophtha.2011.07.002PubMedCentralCrossRefPubMed
9.
go back to reference Imamura Y, Fujiwara T, Margolis R, Spaide RF: Enhanced depth imaging optical coherence tomography of the choroid in central serous chorioretinopathy. Retina 2009, 29: 1469–1473. 10.1097/IAE.0b013e3181be0a83CrossRefPubMed Imamura Y, Fujiwara T, Margolis R, Spaide RF: Enhanced depth imaging optical coherence tomography of the choroid in central serous chorioretinopathy. Retina 2009, 29: 1469–1473. 10.1097/IAE.0b013e3181be0a83CrossRefPubMed
10.
go back to reference Keane PA, Ruiz-Garcia H, Sadda SR: Clinical applications of long-wavelength (1,000-nm) optical coherence tomography. Ophthalmic Surg Lasers Imaging 2011,42(Suppl):S67-S74.CrossRefPubMed Keane PA, Ruiz-Garcia H, Sadda SR: Clinical applications of long-wavelength (1,000-nm) optical coherence tomography. Ophthalmic Surg Lasers Imaging 2011,42(Suppl):S67-S74.CrossRefPubMed
11.
go back to reference Zhang L, Lee K, Niemeijer M, Mullins RF, Sonka M, Abramoff MD: Automated segmentation of the choroid from clinical SD-OCT. Invest Ophthalmol Vis Sci 2012, 53: 7510–7519. 10.1167/iovs.12-10311PubMedCentralCrossRefPubMed Zhang L, Lee K, Niemeijer M, Mullins RF, Sonka M, Abramoff MD: Automated segmentation of the choroid from clinical SD-OCT. Invest Ophthalmol Vis Sci 2012, 53: 7510–7519. 10.1167/iovs.12-10311PubMedCentralCrossRefPubMed
12.
go back to reference Motaghiannezam R, Schwartz DM, Fraser SE: In vivo human choroidal vascular pattern visualization using high-speed swept-source optical coherence tomography at 1060 nm. Invest Ophthalmol Vis Sci 2012, 53: 2337–2348. 10.1167/iovs.11-7823CrossRefPubMed Motaghiannezam R, Schwartz DM, Fraser SE: In vivo human choroidal vascular pattern visualization using high-speed swept-source optical coherence tomography at 1060 nm. Invest Ophthalmol Vis Sci 2012, 53: 2337–2348. 10.1167/iovs.11-7823CrossRefPubMed
13.
go back to reference Sohrab M, Wu K, Fawzi AA: A pilot study of morphometric analysis of choroidal vasculature in vivo, using en face optical coherence tomography. PLoS One 2012, 7: e48631. 10.1371/journal.pone.0048631PubMedCentralCrossRefPubMed Sohrab M, Wu K, Fawzi AA: A pilot study of morphometric analysis of choroidal vasculature in vivo, using en face optical coherence tomography. PLoS One 2012, 7: e48631. 10.1371/journal.pone.0048631PubMedCentralCrossRefPubMed
14.
go back to reference Fong AH, Li KK, Wong D: Choroidal evaluation using enhanced depth imaging spectral-domain optical coherence tomography in Vogt-Koyanagi-Harada disease. Retina 2011, 31: 502–509. 10.1097/IAE.0b013e3182083bebCrossRefPubMed Fong AH, Li KK, Wong D: Choroidal evaluation using enhanced depth imaging spectral-domain optical coherence tomography in Vogt-Koyanagi-Harada disease. Retina 2011, 31: 502–509. 10.1097/IAE.0b013e3182083bebCrossRefPubMed
15.
go back to reference Maruko I, Iida T, Sugano Y, Oyamada H, Sekiryu T, Fujiwara T, Spaide RF: Subfoveal choroidal thickness after treatment of Vogt-Koyanagi-Harada disease. Retina 2011, 31: 510–517. 10.1097/IAE.0b013e3181eef053CrossRefPubMed Maruko I, Iida T, Sugano Y, Oyamada H, Sekiryu T, Fujiwara T, Spaide RF: Subfoveal choroidal thickness after treatment of Vogt-Koyanagi-Harada disease. Retina 2011, 31: 510–517. 10.1097/IAE.0b013e3181eef053CrossRefPubMed
16.
go back to reference Nazari H, Rao NA: Resolution of subretinal fluid with systemic corticosteroid treatment in acute Vogt-Koyanagi-Harada disease. Br J Ophthalmol 2012, 96: 1410–1414. 10.1136/bjophthalmol-2012-301857CrossRefPubMed Nazari H, Rao NA: Resolution of subretinal fluid with systemic corticosteroid treatment in acute Vogt-Koyanagi-Harada disease. Br J Ophthalmol 2012, 96: 1410–1414. 10.1136/bjophthalmol-2012-301857CrossRefPubMed
17.
go back to reference Parc C, Guenoun JM, Dhote R, Brezin A: Optical coherence tomography in the acute and chronic phases of Vogt-Koyanagi-Harada disease. Ocul Immunol Inflamm 2005, 13: 225–227. 10.1080/09273940490912416CrossRefPubMed Parc C, Guenoun JM, Dhote R, Brezin A: Optical coherence tomography in the acute and chronic phases of Vogt-Koyanagi-Harada disease. Ocul Immunol Inflamm 2005, 13: 225–227. 10.1080/09273940490912416CrossRefPubMed
18.
go back to reference Nakai K, Gomi F, Ikuno Y, Yasuno Y, Nouchi T, Ohguro N, Nishida K: Choroidal observations in Vogt-Koyanagi-Harada disease using high-penetration optical coherence tomography. Graefes Arch Clin Exp Ophthalmol 2012, 250: 1089–1095. 10.1007/s00417-011-1910-7CrossRefPubMed Nakai K, Gomi F, Ikuno Y, Yasuno Y, Nouchi T, Ohguro N, Nishida K: Choroidal observations in Vogt-Koyanagi-Harada disease using high-penetration optical coherence tomography. Graefes Arch Clin Exp Ophthalmol 2012, 250: 1089–1095. 10.1007/s00417-011-1910-7CrossRefPubMed
19.
go back to reference Damico FM, Kiss S, Young LH: Vogt-Koyanagi-Harada disease. Semin Ophthalmol 2005, 20: 183–190. 10.1080/08820530500232126CrossRefPubMed Damico FM, Kiss S, Young LH: Vogt-Koyanagi-Harada disease. Semin Ophthalmol 2005, 20: 183–190. 10.1080/08820530500232126CrossRefPubMed
20.
go back to reference Read RW, Holland GN, Rao NA, Tabbara KF, Ohno S, Arellanes-Garcia L, Pivetti-Pezzi P, Tessler HH, Usui M: Revised diagnostic criteria for Vogt-Koyanagi-Harada disease: report of an international committee on nomenclature. Am J Ophthalmol 2001, 131: 647–652. 10.1016/S0002-9394(01)00925-4CrossRefPubMed Read RW, Holland GN, Rao NA, Tabbara KF, Ohno S, Arellanes-Garcia L, Pivetti-Pezzi P, Tessler HH, Usui M: Revised diagnostic criteria for Vogt-Koyanagi-Harada disease: report of an international committee on nomenclature. Am J Ophthalmol 2001, 131: 647–652. 10.1016/S0002-9394(01)00925-4CrossRefPubMed
21.
go back to reference Nazari H, Dustin L, Heussen FM, Sadda S, Rao NA: Morphometric spectral-domain optical coherence tomography features of epiretinal membrane correlate with visual acuity in patients with uveitis. Am J Ophthalmol 2012, 154: 78–86. e1 10.1016/j.ajo.2012.01.032PubMedCentralCrossRefPubMed Nazari H, Dustin L, Heussen FM, Sadda S, Rao NA: Morphometric spectral-domain optical coherence tomography features of epiretinal membrane correlate with visual acuity in patients with uveitis. Am J Ophthalmol 2012, 154: 78–86. e1 10.1016/j.ajo.2012.01.032PubMedCentralCrossRefPubMed
22.
go back to reference Nazari H, Rao N: Longitudinal morphometric analysis of epiretinal membrane in patients with uveitis. Ocul Immunol Inflamm 2013, 21: 2–7. 10.3109/09273948.2012.714044CrossRefPubMed Nazari H, Rao N: Longitudinal morphometric analysis of epiretinal membrane in patients with uveitis. Ocul Immunol Inflamm 2013, 21: 2–7. 10.3109/09273948.2012.714044CrossRefPubMed
23.
go back to reference Shin JW, Shin YU, Cho HY, Lee BR: Measurement of choroidal thickness in normal eyes using 3D OCT-1000 spectral domain optical coherence tomography. Korean J Ophthalmol 2012, 26: 255–259. 10.3341/kjo.2012.26.4.255PubMedCentralCrossRefPubMed Shin JW, Shin YU, Cho HY, Lee BR: Measurement of choroidal thickness in normal eyes using 3D OCT-1000 spectral domain optical coherence tomography. Korean J Ophthalmol 2012, 26: 255–259. 10.3341/kjo.2012.26.4.255PubMedCentralCrossRefPubMed
24.
go back to reference Kuroda S, Ikuno Y, Yasuno Y, Nakai K, Usui S, Sawa M, Tsujikawa M, Gomi F, Nishida K: Choroidal thickness in central serous chorioretinopathy. Retina 2013, 33: 302–308. 10.1097/IAE.0b013e318263d11fCrossRefPubMed Kuroda S, Ikuno Y, Yasuno Y, Nakai K, Usui S, Sawa M, Tsujikawa M, Gomi F, Nishida K: Choroidal thickness in central serous chorioretinopathy. Retina 2013, 33: 302–308. 10.1097/IAE.0b013e318263d11fCrossRefPubMed
25.
go back to reference Margolis R, Spaide RF: A pilot study of enhanced depth imaging optical coherence tomography of the choroid in normal eyes. Am J Ophthalmol 2009, 147: 811–815. 10.1016/j.ajo.2008.12.008CrossRefPubMed Margolis R, Spaide RF: A pilot study of enhanced depth imaging optical coherence tomography of the choroid in normal eyes. Am J Ophthalmol 2009, 147: 811–815. 10.1016/j.ajo.2008.12.008CrossRefPubMed
26.
go back to reference Shin JW, Shin YU, Lee BR: Choroidal thickness and volume mapping by a six radial scan protocol on spectral-domain optical coherence tomography. Ophthalmology 2012, 119: 1017–1023. 10.1016/j.ophtha.2011.10.029CrossRefPubMed Shin JW, Shin YU, Lee BR: Choroidal thickness and volume mapping by a six radial scan protocol on spectral-domain optical coherence tomography. Ophthalmology 2012, 119: 1017–1023. 10.1016/j.ophtha.2011.10.029CrossRefPubMed
27.
go back to reference Jirarattanasopa P, Ooto S, Nakata I, Tsujikawa A, Yamashiro K, Oishi A, Yoshimura N: Choroidal thickness, vascular hyperpermeability, and complement factor H in age-related macular degeneration and polypoidal choroidal vasculopathy. Invest Ophthalmol Vis Sci 2012, 53: 3663–3672. 10.1167/iovs.12-9619CrossRefPubMed Jirarattanasopa P, Ooto S, Nakata I, Tsujikawa A, Yamashiro K, Oishi A, Yoshimura N: Choroidal thickness, vascular hyperpermeability, and complement factor H in age-related macular degeneration and polypoidal choroidal vasculopathy. Invest Ophthalmol Vis Sci 2012, 53: 3663–3672. 10.1167/iovs.12-9619CrossRefPubMed
28.
go back to reference Wirostko WJ, Nordgren RN, Dubis AM: Topographical choroidal thickness change following PDT for CSC: an OCT case report. J Ophthalmol 2012, 2012: 347206.PubMedCentralCrossRefPubMed Wirostko WJ, Nordgren RN, Dubis AM: Topographical choroidal thickness change following PDT for CSC: an OCT case report. J Ophthalmol 2012, 2012: 347206.PubMedCentralCrossRefPubMed
29.
go back to reference Koizumi H, Yamagishi T, Yamazaki T, Kawasaki R, Kinoshita S: Subfoveal choroidal thickness in typical age-related macular degeneration and polypoidal choroidal vasculopathy. Graefes Arch Clin Exp Ophthalmol 2011, 249: 1123–1128. 10.1007/s00417-011-1620-1CrossRefPubMed Koizumi H, Yamagishi T, Yamazaki T, Kawasaki R, Kinoshita S: Subfoveal choroidal thickness in typical age-related macular degeneration and polypoidal choroidal vasculopathy. Graefes Arch Clin Exp Ophthalmol 2011, 249: 1123–1128. 10.1007/s00417-011-1620-1CrossRefPubMed
30.
go back to reference Reibaldi M, Boscia F, Avitabile T, Uva MG, Russo V, Zagari M, Bonfiglio V, Reibaldi A, Longo A: Enhanced depth imaging optical coherence tomography of the choroid in idiopathic macular hole: a cross-sectional prospective study. Am J Ophthalmol 2011, 151: 112–117. e2 10.1016/j.ajo.2010.07.004CrossRefPubMed Reibaldi M, Boscia F, Avitabile T, Uva MG, Russo V, Zagari M, Bonfiglio V, Reibaldi A, Longo A: Enhanced depth imaging optical coherence tomography of the choroid in idiopathic macular hole: a cross-sectional prospective study. Am J Ophthalmol 2011, 151: 112–117. e2 10.1016/j.ajo.2010.07.004CrossRefPubMed
31.
go back to reference MacDonald IM, Russell L, Chan CC: Choroideremia: new findings from ocular pathology and review of recent literature. Surv Ophthalmol 2009, 54: 401–407. 10.1016/j.survophthal.2009.02.008PubMedCentralCrossRefPubMed MacDonald IM, Russell L, Chan CC: Choroideremia: new findings from ocular pathology and review of recent literature. Surv Ophthalmol 2009, 54: 401–407. 10.1016/j.survophthal.2009.02.008PubMedCentralCrossRefPubMed
32.
go back to reference Forooghian F, Yeh S, Faia LJ, Nussenblatt RB: Uveitic foveal atrophy: clinical features and associations. Arch Ophthalmol 2009, 127: 179–186. 10.1001/archophthalmol.2008.564PubMedCentralCrossRefPubMed Forooghian F, Yeh S, Faia LJ, Nussenblatt RB: Uveitic foveal atrophy: clinical features and associations. Arch Ophthalmol 2009, 127: 179–186. 10.1001/archophthalmol.2008.564PubMedCentralCrossRefPubMed
33.
go back to reference Ikewaki J, Kimoto K, Choshi T, Nagata M, Motomura Y, Tamura K, Shinoda K, Nakatsuka K: Optical coherence tomographic assessment of dynamic macular changes in patients with Vogt-Koyanagi-Harada disease. Int Ophthalmol 2011, 31: 9–13. 10.1007/s10792-010-9412-xCrossRefPubMed Ikewaki J, Kimoto K, Choshi T, Nagata M, Motomura Y, Tamura K, Shinoda K, Nakatsuka K: Optical coherence tomographic assessment of dynamic macular changes in patients with Vogt-Koyanagi-Harada disease. Int Ophthalmol 2011, 31: 9–13. 10.1007/s10792-010-9412-xCrossRefPubMed
34.
go back to reference Mullins RF, Johnson MN, Faidley EA, Skeie JM, Huang J: Choriocapillaris vascular dropout related to density of drusen in human eyes with early age-related macular degeneration. Invest Ophthalmol Vis Sci 2011, 52: 1606–1612. 10.1167/iovs.10-6476PubMedCentralCrossRefPubMed Mullins RF, Johnson MN, Faidley EA, Skeie JM, Huang J: Choriocapillaris vascular dropout related to density of drusen in human eyes with early age-related macular degeneration. Invest Ophthalmol Vis Sci 2011, 52: 1606–1612. 10.1167/iovs.10-6476PubMedCentralCrossRefPubMed
35.
go back to reference Wu T, Handa JT, Gottsch JD: Light-induced oxidative stress in choroidal endothelial cells in mice. Invest Ophthalmol Vis Sci 2005, 46: 1117–1123. 10.1167/iovs.04-0517CrossRefPubMed Wu T, Handa JT, Gottsch JD: Light-induced oxidative stress in choroidal endothelial cells in mice. Invest Ophthalmol Vis Sci 2005, 46: 1117–1123. 10.1167/iovs.04-0517CrossRefPubMed
Metadata
Title
Choroidal atrophy and loss of choriocapillaris in convalescent stage of Vogt-Koyanagi-Harada disease: in vivo documentation
Authors
Hossein Nazari
Amirhossein Hariri
Zhihong Hu
Yanwei Ouyang
SiriniVas Sadda
Narsing A Rao
Publication date
01-12-2014
Publisher
Springer Berlin Heidelberg
Published in
Journal of Ophthalmic Inflammation and Infection / Issue 1/2014
Electronic ISSN: 1869-5760
DOI
https://doi.org/10.1186/1869-5760-4-9

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