Skip to main content

Advertisement

Log in

Choroidal vascular alterations evaluated by ultra-widefield indocyanine green angiography in central serous chorioretinopathy

Graefe's Archive for Clinical and Experimental Ophthalmology Aims and scope Submit manuscript

Abstract

Purpose

This study aims to evaluate choroidal vascular alterations in patients with central serous chorioretinopathy (CSC) using ultra-widefield (UWF) indocyanine green angiography (ICGA).

Methods

This was a retrospective case–control study conducted at a single tertiary eye center. In total, 36 eyes in patients with either unilateral (24 patients) or bilateral (six patients) treatment-naïve CSC and 30 eyes in 24 age-matched controls were evaluated. The number of quadrants with vortex vein engorgement on UWF ICGA was evaluated. Dilated choroidal vessels affecting the macula were regarded as extended vortex vein engorgement. Choroidal vascular hyperpermeability (CVH) area on late-phase ICGA was quantified using stereographic projection. The parameters were compared with clinical and optical coherence tomographic findings.

Results

Eyes with CSC had larger CVH area, thicker choroid, and more quadrants with vortex vein engorgement and extended vortex vein engorgement compared with control eyes (all P < 0.001). In patients with unilateral CSC, affected eyes had larger CVH area, thicker choroid, and more extended vortex vein engorgements compared with unaffected fellow eyes (all P < 0.001), but vortex vein engorgement did not significantly differ. CVH was significantly correlated with extended vortex vein engorgement (P < 0.001) and subfoveal choroidal thickness (P = 0.007).

Conclusions

The increased number and binocular symmetry of engorged vortex veins suggest an anatomical predisposition for CSC. CVH area and extended vortex vein engorgement were indicators of choroidal outflow congestion. These parameters may serve as diagnostic clues or predictors of disease development in eyes with CSC.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price includes VAT (France)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Data availability

Data are available upon reasonable request.

Code availability

Not applicable.

References

  1. Menchini U, Virgili G, Lanzetta P, Ferrari E (1997) Indocyanine green angiography in central serous chorioretinopathy ICG angiography in CSC. Int Ophthalmol 21:57–69

    Article  CAS  Google Scholar 

  2. Pang CE, Shah VP, Sarraf D, Freund KB (2014) Ultra-widefield imaging with autofluorescence and indocyanine green angiography in central serous chorioretinopathy. Am J Ophthalmol 158:362-371.e362. https://doi.org/10.1016/j.ajo.2014.04.021

    Article  PubMed  Google Scholar 

  3. Yannuzzi LA, Shakin JL, Fisher YL, Altomonte MA (1984) Peripheral retinal detachments and retinal pigment epithelial atrophic tracts secondary to central serous pigment epitheliopathy. Ophthalmology 91:1554–1572

    Article  CAS  Google Scholar 

  4. Gass JD (1967) Pathogenesis of disciform detachment of the neuroepithelium. Am J Ophthalmol 63(Suppl):1–139

    Google Scholar 

  5. Marmor MF (1988) New hypotheses on the pathogenesis and treatment of serous retinal detachment. Graefes Arch Clin Exp Ophthalmol 226:548–552. https://doi.org/10.1007/bf02169203

    Article  CAS  PubMed  Google Scholar 

  6. Spaide RF, Hall L, Haas A, Campeas L, Yannuzzi LA, Fisher YL, Guyer DR, Slakter JS, Sorenson JA, Orlock DA (1996) Indocyanine green videoangiography of older patients with central serous chorioretinopathy. Retina 16:203–213. https://doi.org/10.1097/00006982-199616030-00004

    Article  CAS  PubMed  Google Scholar 

  7. Prunte C, Flammer J (1996) Choroidal capillary and venous congestion in central serous chorioretinopathy. Am J Ophthalmol 121:26–34. https://doi.org/10.1016/s0002-9394(14)70531-8

    Article  CAS  PubMed  Google Scholar 

  8. Prunte C (1995) Indocyanine green angiographic findings in central serous chorioretinopathy. Int Ophthalmol 19:77–82

    Article  CAS  Google Scholar 

  9. Jirarattanasopa P, Ooto S, Tsujikawa A, Yamashiro K, Hangai M, Hirata M, Matsumoto A, Yoshimura N (2012) Assessment of macular choroidal thickness by optical coherence tomography and angiographic changes in central serous chorioretinopathy. Ophthalmology 119:1666–1678. https://doi.org/10.1016/j.ophtha.2012.02.021

    Article  PubMed  Google Scholar 

  10. Tsujikawa A, Ojima Y, Yamashiro K, Ooto S, Tamura H, Nakagawa S, Yoshimura N (2010) Punctate hyperfluorescent spots associated with central serous chorioretinopathy as seen on indocyanine green angiography. Retina 30:801–809. https://doi.org/10.1097/IAE.0b013e3181c72068

    Article  PubMed  Google Scholar 

  11. Yannuzzi LA, Slakter JS, Gross NE, Spaide RF, Costa D, Huang SJ, Klancnik JM Jr, Aizman A (2003) Indocyanine green angiography-guided photodynamic therapy for treatment of chronic central serous chorioretinopathy: a pilot study. Retina 23:288–298. https://doi.org/10.1097/00006982-200306000-00002

    Article  PubMed  Google Scholar 

  12. Hirahara S, Yasukawa T, Kominami A, Nozaki M, Ogura Y (2016) Densitometry of choroidal vessels in eyes with and without central serous chorioretinopathy by wide-field indocyanine green angiography. Am J Ophthalmol 166:103–111. https://doi.org/10.1016/j.ajo.2016.03.040

    Article  PubMed  Google Scholar 

  13. Imamura Y, Fujiwara T, Spaide RF (2011) Fundus autofluorescence and visual acuity in central serous chorioretinopathy. Ophthalmology 118:700–705. https://doi.org/10.1016/j.ophtha.2010.08.017

    Article  PubMed  Google Scholar 

  14. Kitaya N, Nagaoka T, Hikichi T, Sugawara R, Fukui K, Ishiko S, Yoshida A (2003) Features of abnormal choroidal circulation in central serous chorioretinopathy. Br J Ophthalmol 87:709–712

    Article  CAS  Google Scholar 

  15. Warrow DJ, Hoang QV, Freund KB (2013) Pachychoroid pigment epitheliopathy. Retina 33:1659–1672. https://doi.org/10.1097/IAE.0b013e3182953df4

    Article  PubMed  Google Scholar 

  16. Dansingani KK, Balaratnasingam C, Naysan J, Freund KB (2016) En face imaging of pachychoroid spectrum disorders with swept-source optical coherence tomography. Retina 36:499–516. https://doi.org/10.1097/iae.0000000000000742

    Article  PubMed  Google Scholar 

  17. Spaide RF, Ledesma-Gil G, Gemmy Cheung CM (2020) Intervortex venous anastomosis in pachychoroid-related disorders. Retina. https://doi.org/10.1097/iae.0000000000003004

    Article  PubMed  PubMed Central  Google Scholar 

  18. Matsumoto H, Hoshino J, Mukai R, Nakamura K, Kikuchi Y, Kishi S, Akiyama H (2020) Vortex vein anastomosis at the watershed in pachychoroid spectrum diseases. Ophthalmology Retina 4:938–945. https://doi.org/10.1016/j.oret.2020.03.024

    Article  PubMed  Google Scholar 

  19. Sagong M, van Hemert J, Olmos de Koo LC, Barnett C, Sadda SR (2015) Assessment of accuracy and precision of quantification of ultra-widefield images. Ophthalmology 122:864–866. https://doi.org/10.1016/j.ophtha.2014.11.016

    Article  PubMed  Google Scholar 

  20. Spaide RF (2011) Peripheral areas of nonperfusion in treated central retinal vein occlusion as imaged by wide-field fluorescein angiography. Retina 31:829–837. https://doi.org/10.1097/IAE.0b013e31820c841e

    Article  PubMed  Google Scholar 

  21. Cakir B, Reich M, Lang S, Bühler A, Ehlken C, Grundel B, Stech M, Reichl S, Stahl A, Böhringer D, Agostini H, Lange C (2019) OCT angiography of the choriocapillaris in central serous chorioretinopathy: a quantitative subgroup analysis. Ophthalmol Ther 8:75–86. https://doi.org/10.1007/s40123-018-0159-1

    Article  PubMed  PubMed Central  Google Scholar 

  22. Jung JJ, Yu DJG, Ito K, Rofagha S, Lee SS, Hoang QV (2020) Quantitative assessment of asymmetric choroidal outflow in pachychoroid eyes on ultra-widefield indocyanine green angiography. Invest Ophthalmol Vis Sci 61:50. https://doi.org/10.1167/iovs.61.8.50

    Article  PubMed  PubMed Central  Google Scholar 

  23. Jeong A, Lim J, Sagong M (2021) Choroidal vascular abnormalities by ultra-widefield indocyanine green angiography in polypoidal choroidal vasculopathy. Invest Ophthalmol Vis Sci 62:29. https://doi.org/10.1167/iovs.62.2.29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Singer M, Sagong M, van Hemert J, Kuehlewein L, Bell D, Sadda SR (2016) Ultra-widefield imaging of the peripheral retinal vasculature in normal subjects. Ophthalmology 123:1053–1059. https://doi.org/10.1016/j.ophtha.2016.01.022

    Article  PubMed  Google Scholar 

  25. Uyama M, Matsunaga H, Matsubara T, Fukushima I, Takahashi K, Nishimura T (1999) Indocyanine green angiography and pathophysiology of multifocal posterior pigment epitheliopathy. Retina 19:12–21. https://doi.org/10.1097/00006982-199901000-00003

    Article  CAS  PubMed  Google Scholar 

  26. Guyer DR, Yannuzzi LA, Slakter JS, Sorenson JA, Ho A, Orlock D (1994) Digital indocyanine green videoangiography of central serous chorioretinopathy. Arch Ophthalmol 112:1057–1062. https://doi.org/10.1001/archopht.1994.01090200063023

    Article  CAS  PubMed  Google Scholar 

  27. Nishiyama Y, Mori K, Murayama K, Yoneya S (2001) Quantitative analysis of indocyanine green angiographic image in central serous chorioretinopathy. Jpn J Ophthalmol 45:116. https://doi.org/10.1016/s0021-5155(00)00309-9

    Article  CAS  PubMed  Google Scholar 

  28. Hiroe T, Kishi S (2018) Dilatation of asymmetric vortex vein in central serous chorioretinopathy. Ophthalmol Retina 2:152–161. https://doi.org/10.1016/j.oret.2017.05.013

    Article  PubMed  Google Scholar 

  29. Yang L, Jonas JB, Wei W (2013) Choroidal vessel diameter in central serous chorioretinopathy. Acta Ophthalmol 91:e358-362. https://doi.org/10.1111/aos.12059

    Article  PubMed  Google Scholar 

  30. Imamura Y, Fujiwara T, Margolis R, Spaide RF (2009) Enhanced depth imaging optical coherence tomography of the choroid in central serous chorioretinopathy. Retina 29:1469–1473. https://doi.org/10.1097/IAE.0b013e3181be0a83

    Article  PubMed  Google Scholar 

  31. Izumi T, Maruko I (2021) Morphological differences of choroid in central serous chorioretinopathy determined by ultra-widefield optical coherence tomography. https://doi.org/10.1007/s00417-021-05380-0

  32. Chung YR, Kim JW, Kim SW, Lee K (2016) Choroidal thickness in patients with central serous chorioretinopathy: assessment of Haller and Sattler layers. Retina 36:1652–1657. https://doi.org/10.1097/iae.0000000000000998

    Article  PubMed  Google Scholar 

  33. Yang L, Jonas JB, Wei W (2013) Optical coherence tomography-assisted enhanced depth imaging of central serous chorioretinopathy. Invest Ophthalmol Vis Sci 54:4659–4665. https://doi.org/10.1167/iovs.12-10991

    Article  PubMed  Google Scholar 

  34. Spaide RF, Gemmy Cheung CM, Matsumoto H, Kishi S, Boon CJF, van Dijk EHC, Mauget-Faysse M, Behar-Cohen F, Hartnett ME, Sivaprasad S, Iida T, Brown DM, Chhablani J, Maloca PM (2021) Venous overload choroidopathy: a hypothetical framework for central serous chorioretinopathy and allied disorders. Prog Retin Eye Res 100973. https://doi.org/10.1016/j.preteyeres.2021.100973

  35. Hanumunthadu D, van Dijk EHC, Dumpala S, Rajesh B, Jabeen A, Jabeen A, Ansari M, Mehta P, Shah S, Sarvaiya C, Meyerle C, Wu L, Banker A, Boon CJ, Chhablani J (2019) Evaluation of choroidal layer thickness in central serous chorioretinopathy. J Ophthalmic Vis Res 14:164–170. https://doi.org/10.4103/jovr.jovr_152_17

    Article  PubMed  PubMed Central  Google Scholar 

  36. Ma DJ, Park UC, Kim ET, Yu HG (2018) Choroidal vascularity changes in idiopathic central serous chorioretinopathy after half-fluence photodynamic therapy. PLoS ONE 13:e0202930. https://doi.org/10.1371/journal.pone.0202930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Daruich A, Matet A, Dirani A, Bousquet E, Zhao M, Farman N, Jaisser F, Behar-Cohen F (2015) Central serous chorioretinopathy: recent findings and new physiopathology hypothesis. Prog Retin Eye Res 48:82–118. https://doi.org/10.1016/j.preteyeres.2015.05.003

    Article  CAS  PubMed  Google Scholar 

  38. Lee H, Lee J, Chung H, Kim HC (2016) Baseline spectral domain optical coherence tomographic hyperreflective foci as a predictor of visual outcome and recurrence for central serous chorioretinopathy. Retina 36:1372–1380. https://doi.org/10.1097/iae.0000000000000929

    Article  CAS  PubMed  Google Scholar 

  39. van Velthoven ME, Verbraak FD, Garcia PM, Schlingemann RO, Rosen RB, de Smet MD (2005) Evaluation of central serous retinopathy with en face optical coherence tomography. Br J Ophthalmol 89:1483–1488. https://doi.org/10.1136/bjo.2005.073056

    Article  PubMed  PubMed Central  Google Scholar 

  40. Yu J, Jiang C, Xu G (2019) Correlations between changes in photoreceptor layer and other clinical characteristics in central serous chorioretinopathy. Retina 39:1110–1116. https://doi.org/10.1097/iae.0000000000002092

    Article  PubMed  Google Scholar 

  41. Hanumunthadu D, Matet A, Rasheed MA, Goud A, Vuppurabina KK, Chhablani J (2019) Evaluation of choroidal hyperreflective dots in acute and chronic central serous chorioretinopathy. Indian J Ophthalmol 67:1850–1854. https://doi.org/10.4103/ijo.IJO_2030_18

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by a 2020 Yeungnam University research grant. The funding organization had no role in this study including design, collection, analysis, interpretation of data, or approval of manuscript.

Author information

Authors and Affiliations

Authors

Contributions

Design and conduct of the study, MS; collection and management of data SJ, WK, DN, JH, and MS; analysis and interpretation of data, SJ, WK, DN, and MS; and preparation, review, and approval of the manuscript, SJ, WK, DN, JV, and MS.

Corresponding author

Correspondence to Min Sagong.

Ethics declarations

Ethics approval

The study protocol was approved by the Institutional Review Board of Yeungnam University Hospital.

Consent to participate

Written informed consent was obtained from all participants.

Consent for publication

Not applicable.

Competing interests

S. Jeong, none; W Kang, none; D Noh, none; and M. Sagong, none. J.v.H. is the research director at Optos, a Nikon Company (Employment) and held patents (Improvement in and relating to Imaging of the Eye) pending to Optos PLC.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jeong, S., Kang, W., Noh, D. et al. Choroidal vascular alterations evaluated by ultra-widefield indocyanine green angiography in central serous chorioretinopathy. Graefes Arch Clin Exp Ophthalmol 260, 1887–1898 (2022). https://doi.org/10.1007/s00417-021-05461-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00417-021-05461-0

Keywords

Navigation