Skip to main content

Advertisement

SpringerLink
Log in

Hyperpigmented spots after treatment for submacular hemorrhage secondary to polypoidal choroidal vasculopathy

  • Retinal Disorders
  • Published:
Graefe's Archive for Clinical and Experimental Ophthalmology Aims and scope Submit manuscript

Abstract

Purpose

To investigate the characteristics and clinical course of hyperpigmented spots after submacular hemorrhage secondary to polypoidal choroidal vasculopathy (PCV).

Methods

This retrospective, observational study included 87 eyes initially treated with three anti-vascular endothelial growth factor (VEGF) injections for submacular hemorrhage secondary to PCV. Patients were divided into two groups according to the presence of multiple small, dark-gray or black, pigmented lesions after initial treatment: the hyperpigmented spots group and no-hyperpigmented spots group. Baseline characteristics and re-activation of the lesion were compared between the two groups.

Results

The mean follow-up period was 30.6 ± 12.9 months, and 41 eyes (47.1%) were included in the hyperpigmented spots group. The hyperpigmented spots group exhibited greater extent of hemorrhage (P < 0.001) and greater central foveal thickness (P = 0.045) than did the no-hyperpigmented spots group. In the hyperpigmented spots group, re-activation of the lesion was noted in 17 eyes (41.5%) at a mean duration of 15.4 ± 12.7 months after the third anti-VEGF injection. In the no-hyperpigmented spots group, re-activation was noted in 28 eyes (60.9%) at a mean duration of 6.4 ± 4.0 months after the third injection. Kaplan–Meier analysis with log-rank test revealed a significant difference in the re-activation of the lesion between the two groups (P = 0.006).

Conclusions

Hyperpigmented spots were associated with a large amount of submacular hemorrhage in PCV. The low incidence of re-activation and late re-activation of the lesion in eyes with hyperpigmented spots suggest that a novel follow-up and treatment strategy is required for this condition.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Uyama M, Wada M, Nagai Y, Matsubara T, Matsunaga H, Fukushima I, Takahashi K, Matsumura M (2002) Polypoidal choroidal vasculopathy: natural history. Am J Ophthalmol 133:639–648

    Article  PubMed  Google Scholar 

  2. Kim JH, Chang YS, Kim JW, Kim CG (2017) Characteristics of submacular hemorrhages in age-related macular degeneration. Optom Vis Sci 94:556–563

    Article  PubMed  Google Scholar 

  3. Glatt H, Machemer R (1982) Experimental subretinal hemorrhage in rabbits. Am J Ophthalmol 94:762–773

    Article  CAS  PubMed  Google Scholar 

  4. Toth CA, Morse LS, Hjelmeland LM, Landers MB 3rd (1991) Fibrin directs early retinal damage after experimental subretinal hemorrhage. Arch Ophthalmol 109:723–729

    Article  CAS  PubMed  Google Scholar 

  5. Bhisitkul RB, Winn BJ, Lee OT, Wong J, Pereira Dde S, Porco TC, He X, Hahn P, Dunaief JL (2008) Neuroprotective effect of intravitreal triamcinolone acetonide against photoreceptor apoptosis in a rabbit model of subretinal hemorrhage. Invest Ophthalmol Vis Sci 49:4071–4077

    Article  PubMed  Google Scholar 

  6. Notomi S, Hisatomi T, Murakami Y, Terasaki H, Sonoda S, Asato R, Takeda A, Ikeda Y, Enaida H, Sakamoto T, Ishibashi T (2013) Dynamic increase in extracellular ATP accelerates photoreceptor cell apoptosis via ligation of P2RX7 in subretinal hemorrhage. PLoS One 8:e53338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Kim JH, Chang YS, Kim JW, Kim CG, Lee DW (2017) Submacular hemorrhage and grape-like polyp clusters: factors associated with reactivation of the lesion in polypoidal choroidal vasculopathy. Eye (Lond) Jul 14 {Epub ahead of print]

  8. Kim JH, Chang YS, Kim JW, Kim CG, Yoo SJ, Cho HJ (2014) Intravitreal anti-vascular endothelial growth factor for submacular hemorrhage from choroidal neovascularization. Ophthalmology 121:926–935

    Article  PubMed  Google Scholar 

  9. Shin JY, Lee JM, Byeon SH (2015) Anti-vascular endothelial growth factor with or without pneumatic displacement for submacular hemorrhage. Am J Ophthalmol 159:904–914 e901

    Article  CAS  PubMed  Google Scholar 

  10. Sasahara M, Tsujikawa A, Musashi K, Gotoh N, Otani A, Mandai M, Yoshimura N (2006) Polypoidal choroidal vasculopathy with choroidal vascular hyperpermeability. Am J Ophthalmol 142:601–607

    Article  PubMed  Google Scholar 

  11. Kim YM, Kim JH, Koh HJ (2012) Improvement of photoreceptor integrity and associated visual outcome in neovascular age-related macular degeneration. Am J Ophthalmol 154:164.e1–173.e1

    Article  Google Scholar 

  12. Anderson DH, Guerin CJ, Erickson PA, Stern WH, Fisher SK (1986) Morphological recovery in the reattached retina. Invest Ophthalmol Vis Sci 27:168–183

    CAS  PubMed  Google Scholar 

  13. Anderson DH, Stern WH, Fisher SK, Erickson PA, Borgula GA (1983) Retinal detachment in the cat: the pigment epithelial–photoreceptor interface. Invest Ophthalmol Vis Sci 24:906–926

    CAS  PubMed  Google Scholar 

  14. Fisher SK, Lewis GP, Linberg KA, Verardo MR (2005) Cellular remodeling in mammalian retina: results from studies of experimental retinal detachment. Prog Retin Eye Res 24:395–431

    Article  PubMed  Google Scholar 

  15. Fazekas F, Kleinert R, Roob G, Kleinert G, Kapeller P, Schmidt R, Hartung HP (1999) Histopathologic analysis of foci of signal loss on gradient-echo T2*-weighted MR images in patients with spontaneous intracerebral hemorrhage: evidence of microangiopathy-related microbleeds. AJNR Am J Neuroradiol 20:637–642

    CAS  PubMed  Google Scholar 

  16. Stafanous SN, Matthew M (2009) An unusual case of recurrent subconjunctival haemorrhage causing yellow-brown discolouration due to haemosiderin deposition. Orbit 28:179–180

    Article  PubMed  Google Scholar 

  17. Emerson MV, Jakobs E, Green WR (2007) Ocular autopsy and histopathologic features of child abuse. Ophthalmology 114:1384–1394

    Article  PubMed  Google Scholar 

  18. Fujii K, Hao H, Shibuya M, Imanaka T, Fukunaga M, Miki K, Tamaru H, Sawada H, Naito Y, Ohyanagi M, Hirota S, Masuyama T (2015) Accuracy of OCT, grayscale IVUS, and their combination for the diagnosis of coronary TCFA: an ex vivo validation study. JACC Cardiovasc Imaging 8:451–460

    Article  PubMed  Google Scholar 

  19. Avery RL, Fekrat S, Hawkins BS, Bressler NM (1996) Natural history of subfoveal subretinal hemorrhage in age-related macular degeneration. Retina 16:183–189

    Article  CAS  PubMed  Google Scholar 

  20. Cheung CM, Bhargava M, Xiang L, Mathur R, Mun CC, Wong D, Wong TY (2013) Six-month visual prognosis in eyes with submacular hemorrhage secondary to age-related macular degeneration or polypoidal choroidal vasculopathy. Graefes Arch Clin Exp Ophthalmol 251:19–25

    Article  PubMed  Google Scholar 

  21. Mathew R, Richardson M, Sivaprasad S (2013) Predictive value of spectral-domain optical coherence tomography features in assessment of visual prognosis in eyes with neovascular age-related macular degeneration treated with ranibizumab. Am J Ophthalmol 155:720–726, 726.e1

    Article  CAS  PubMed  Google Scholar 

  22. Hayashi H, Yamashiro K, Tsujikawa A, Ota M, Otani A, Yoshimura N (2009) Association between foveal photoreceptor integrity and visual outcome in neovascular age-related macular degeneration. Am J Ophthalmol 148:83.e1–89.e1

    Google Scholar 

  23. Kitagawa Y, Shimada H, Mori R, Tanaka K, Yuzawa M (2016) Intravitreal tissue plasminogen activator, ranibizumab, and gas injection for submacular hemorrhage in polypoidal choroidal vasculopathy. Ophthalmology 123:1278–1286

    Article  PubMed  Google Scholar 

  24. Holz FG, Tadayoni R, Beatty S, Berger A, Cereda MG, Cortez R, Hoyng CB, Hykin P, Staurenghi G, Heldner S, Bogumil T, Heah T, Sivaprasad S (2015) Multi-country real-life experience of anti-vascular endothelial growth factor therapy for wet age-related macular degeneration. Br J Ophthalmol 99:220–226

    Article  PubMed  Google Scholar 

  25. Writing Committee for the UK Age-Related Macular Degeneration EMR Users Group (2014) The neovascular age-related macular degeneration database: multicenter study of 92,976 ranibizumab injections: report 1: visual acuity. Ophthalmology 121:1092–1101

  26. Brown DM, Kaiser PK, Michels M, Soubrane G, Heier JS, Kim RY, Sy JP, Schneider S (2006) Ranibizumab versus verteporfin for neovascular age-related macular degeneration. N Engl J Med 355:1432–1444

    Article  CAS  PubMed  Google Scholar 

  27. Rosenfeld PJ, Brown DM, Heier JS, Boyer DS, Kaiser PK, Chung CY, Kim RY (2006) Ranibizumab for neovascular age-related macular degeneration. N Engl J Med 355:1419–1431

    Article  CAS  PubMed  Google Scholar 

  28. Campochiaro PA (2015) Molecular pathogenesis of retinal and choroidal vascular diseases. Prog Retin Eye Res 49:67–81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Fung AE, Lalwani GA, Rosenfeld PJ, Dubovy SR, Michels S, Feuer WJ, Puliafito CA, Davis JL, Flynn HW Jr, Esquiabro M (2007) An optical coherence tomography-guided, variable dosing regimen with intravitreal ranibizumab (Lucentis) for neovascular age-related macular degeneration. Am J Ophthalmol 143:566–583

    Article  CAS  PubMed  Google Scholar 

  30. Kuroda Y, Yamashiro K, Miyake M, Yoshikawa M, Nakanishi H, Oishi A, Tamura H, Ooto S, Tsujikawa A, Yoshimura N (2015) Factors associated with recurrence of age-related macular degeneration after anti-vascular endothelial growth factor treatment: a retrospective cohort study. Ophthalmology 122:2303–2310

    Article  PubMed  Google Scholar 

  31. Kim JH, Chang YS, Lee DW, Kim CG, Kim JW (2017) Incidence and timing of the first recurrence in neovascular age-related macular degeneration: comparison between ranibizumab and aflibercept. J Ocul Pharmacol Ther 33:445–451

    Article  CAS  PubMed  Google Scholar 

  32. Inoue M, Yamane S, Sato S, Sakamaki K, Arakawa A, Kadonosono K (2016) Comparison of time to retreatment and visual function between ranibizumab and aflibercept in age-related macular degeneration. Am J Ophthalmol 169:95–103

    Article  PubMed  Google Scholar 

  33. Chin-Yee D, Eck T, Fowler S, Hardi A, Apte RS (2016) A systematic review of as needed versus treat and extend ranibizumab or bevacizumab treatment regimens for neovascular age-related macular degeneration. Br J Ophthalmol 100:914–917

    Article  PubMed  Google Scholar 

Download references

Funding

Kim’s Eye Hospital (Seoul, South Korea) provided financial support in the form of funding for English editing support. The sponsor had no role in the design or conduct of this research.

Author information

Authors and Affiliations

  1. Department of Ophthalmology, Kim’s Eye Hospital, Konyang University College of Medicine, #156 Youngdeungpo-dong 4ga, Youngdeungpo-gu, Seoul, 150-034, South Korea

    Jae Hui Kim, Chul Gu Kim, Dong Won Lee & Jung Il Han

  2. Department of Ophthalmology, Konyang University College of Medicine, Daejeon, South Korea

    Young Suk Chang

Authors
  1. Jae Hui Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Young Suk Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chul Gu Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dong Won Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jung Il Han
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jae Hui Kim.

Ethics declarations

Conflict of interest

All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest, or non-financial interest in the subject matter or materials discussed in this manuscript.

Ethical approval

The study was approved by the institutional review board of Kim’s Eye Hospital (Seoul, South Korea). This study was conducted in accordance with the tenets of the Declaration of Helsinki.

Informed consent

Informed consent was not obtained in this study. Identifying information about participants was not presented in this study.

Financial support

This study was supported by Kim’s Eye Hospital Research Center.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, J.H., Chang, Y.S., Kim, C.G. et al. Hyperpigmented spots after treatment for submacular hemorrhage secondary to polypoidal choroidal vasculopathy. Graefes Arch Clin Exp Ophthalmol 256, 469–477 (2018). https://doi.org/10.1007/s00417-017-3877-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00417-017-3877-5

Keywords

Search

Navigation