Recovery of macular cone photoreceptors in Vogt-Koyanagi-Harada disease

  • Tomoko Nakamura
  • Atsushi Hayashi
  • Toshihiko Oiwake
Inflammatory Disorders

Abstract

Purpose

Our purpose was to study changes in macular cone photoreceptors in Vogt-Koyanagi-Harada (VKH) disease patients after high-dose corticosteroid treatment using an adaptive optics (AO) fundus camera.

Methods

We retrospectively analyzed 16 eyes of eight patients with new-onset acute VKH disease that were studied retrospectively. After serous retinal detachment (SRD) had resolved, AO images were obtained using the rtx1™ AO fundus camera over a 12-month course. Cone counting was performed in the nasal, temporal, superior and inferior areas of the macula 0.75 mm from the foveal center. A control group of 30 eyes of 30 healthy subjects was established for comparison.

Results

In the eyes with VKH disease, the mean cone densities 0.75 mm from the foveal center were 11,847 at baseline (resolution of SRD), and 15,218, 16,684 and 17,686 cones/mm2, at 3, 6, and 12 months later, respectively. The mean cone densities at 3, 6, and 12 months were significantly increased compared to those of baseline (p = 0.007, p < 0.001, and p < 0.001, respectively); however, they were significantly lower than that of the healthy control eyes (p < 0.001). The mean cone densities at areas with a previous presence of cystoid spaces were significantly lower than those without cystoid spaces at the baseline, and at 3, 6, and 12 months (p < 0.001, p = 0.007, p < 0.001, and p = 0.008, respectively).

Conclusions

Cone densities were gradually increased after the resolution of SRD in the eyes of VKH disease patients. The presence of cystoid spaces might be a marker of severe damage to cone photoreceptors.

Keywords

Adaptive optics Cone density Cystoid space Photoreceptor Serous retinal detachment Vogt-Koyanagi-Harada disease 

Notes

Compliance with ethical standards

Conflicts of interest

All authors have no financial interest in the subject matter or materials disucussed in this manuscript.

Ethical approval

All procedures performed in this study involving human participants were in accordance with the ethical standards of the institutional and the national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

For this type of study, formal consent is not required.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. 1.
    Moorthy RS, Inomata H, Rao NA (1995) Vogt-Koyanagi-Harada syndrome. Surv Ophthalmol 39:265–292CrossRefPubMedGoogle Scholar
  2. 2.
    Read RW, Holland GN, Rao NA, Tabbara KF, Ohno S, Arellanes-Garcia L, Pivetti-Pezzi P, Tessler HH, Usui M (2001) Revised diagnostic criteria for Vogt-Koyanagi-Harada disease: report of an international committee on nomenclature. Am J Ophthalmol 131:647–652CrossRefPubMedGoogle Scholar
  3. 3.
    Maruyama Y, Kishi S (2004) Tomographic features of serous retinal detachment in Vogt-Koyanagi-Harada syndrome. Ophthalmic Surg Lasers Imaging 35:239–242PubMedGoogle Scholar
  4. 4.
    Ooto S, Hangai M, Sakamoto A, Tsujikawa A, Yamashiro K, Ojima Y, Yamada Y, Mukai H, Oshima S, Inoue T, Yoshimura N (2010) High-resolution imaging of resolved central serous chorioretinopathy using adaptive optics scanning laser ophthalmoscopy. Ophthalmology 117(1800-1809):1809 e1-2.  https://doi.org/10.1016/j.ophtha.2010.01.042 Google Scholar
  5. 5.
    Nakamura T, Ueda-Consolvo T, Oiwake T, Hayashi A (2016) Correlation between outer retinal layer thickness and cone density in patients with resolved central serous chorioretinopathy. Graefes Arch Clin Exp Ophthalmol 254:2347–2354.  https://doi.org/10.1007/s00417-016-3403-1 CrossRefPubMedGoogle Scholar
  6. 6.
    Zitova B, Flusser J (2003) Image registration methods: a survey. Image Vis Comput 21:977–1000.  https://doi.org/10.1016/S0262-8856(03)00137-9 CrossRefGoogle Scholar
  7. 7.
    Bennett AG, Rudnicka AR, Edgar DF (1994) Improvements on Littmann's method of determining the size of retinal features by fundus photography. Graefes Arch Clin Exp Ophthalmol 232:361–367CrossRefPubMedGoogle Scholar
  8. 8.
    Spaide RF, Curcio CA (2011) Anatomical correlates to the bands seen in the outer retina by optical coherence tomography: literature review and model. Retina 31:1609–1619.  https://doi.org/10.1097/IAE.0b013e3182247535 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Yamaki K, Kondo I, Nakamura H, Miyano M, Konno S, Sakuragi S (2000) Ocular and extraocular inflammation induced by immunization of tyrosinase related protein 1 and 2 in Lewis rats. Exp Eye Res 71:361–369.  https://doi.org/10.1006/exer.2000.0893 CrossRefPubMedGoogle Scholar
  10. 10.
    Hayakawa K, Ishikawa M, Yamaki K (2004) Ultrastructural changes in rat eyes with experimental Vogt-Koyanagi-Harada disease. Jpn J Ophthalmol 48:222–227.  https://doi.org/10.1007/s10384-003-0061-8 CrossRefPubMedGoogle Scholar
  11. 11.
    Sakai T, Calderone JB, Lewis GP, Linberg KA, Fisher SK, Jacobs GH (2003) Cone photoreceptor recovery after experimental detachment and reattachment: an immunocytochemical, morphological, and electrophysiological study. Invest Ophthalmol Vis Sci 44:416–425CrossRefPubMedGoogle Scholar
  12. 12.
    Saleh M, Debellemaniere G, Meillat M, Tumahai P, Bidaut Garnier M, Flores M, Schwartz C, Delbosc B (2014) Quantification of cone loss after surgery for retinal detachment involving the macula using adaptive optics. Br J Ophthalmol 98:1343–1348.  https://doi.org/10.1136/bjophthalmol-2013-304813 CrossRefPubMedGoogle Scholar
  13. 13.
    Tsujikawa A, Yamashiro K, Yamamoto K, Nonaka A, Fujihara M, Kurimoto Y (2005) Retinal cystoid spaces in acute Vogt-Koyanagi-Harada syndrome. Am J Ophthalmol 139:670–677.  https://doi.org/10.1016/j.ajo.2004.11.053 CrossRefPubMedGoogle Scholar
  14. 14.
    Yamaguchi Y, Otani T, Kishi S (2007) Tomographic features of serous retinal detachment with multilobular dye pooling in acute Vogt-Koyanagi-Harada disease. Am J Ophthalmol 144:260–265.  https://doi.org/10.1016/j.ajo.2007.04.007 CrossRefPubMedGoogle Scholar
  15. 15.
    Ishihara K, Hangai M, Kita M, Yoshimura N (2009) Acute Vogt-Koyanagi-Harada disease in enhanced spectral-domain optical coherence tomography. Ophthalmology 116:1799–1807.  https://doi.org/10.1016/j.ophtha.2009.04.002 CrossRefPubMedGoogle Scholar
  16. 16.
    Lee JE, Park SW, Lee JK, Choi HY, Oum BS, Kim HW (2009) Edema of the photoreceptor layer in Vogt-Koyanagi-Harada disease observed using high-resolution optical coherence tomography. Korean J Ophthalmol 23:74–79.  https://doi.org/10.3341/kjo.2009.23.2.74 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Bae SS, Forooghian F (2016) Optical coherence tomography-based quantification of photoreceptor injury and recovery in Vogt-Koyanagi-Harada uveitis. Ocul Immunol Inflamm 25.  https://doi.org/10.3109/09273948.2015.1125510
  18. 18.
    Doi E, Gauthier JL, Field GD, Shlens J, Sher A, Greschner M, Machado TA, Jepson LH, Mathieson K, Gunning DE, Litke AM, Paninski L, Chichilnisky EJ, Simoncelli EP (2012) Efficient coding of spatial information in the primate retina. J Neurosci 32:16256–16264.  https://doi.org/10.1523/JNEUROSCI.4036-12.2012 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Maruko I, Iida T, Sugano Y, Oyamada H, Sekiryu T, Fujiwara T, Spaide RF (2011) Subfoveal choroidal thickness after treatment of Vogt-Koyanagi-Harada disease. Retina 31:510–517.  https://doi.org/10.1097/IAE.0b013e3181eef053 CrossRefPubMedGoogle Scholar
  20. 20.
    Nakayama M, Keino H, Okada AA, Watanabe T, Taki W, Inoue M, Hirakata A (2012) Enhanced depth imaging optical coherence tomography of the choroid in Vogt-Koyanagi-Harada disease. Retina 32:2061–2069.  https://doi.org/10.1097/IAE.0b013e318256205a CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Tomoko Nakamura
    • 1
  • Atsushi Hayashi
    • 1
  • Toshihiko Oiwake
    • 1
  1. 1.Department of Ophthalmology, Graduate School of Medicine and Pharmaceutical SciencesUniversity of ToyamaToyamaJapan

Personalised recommendations