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Quantitative evaluation of retinal and choroidal vascularity in systemic lupus erythematosus by SS-OCT/OCTA

  • Retinal Disorders
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Abstract

Purpose

To evaluate changes in retinal and choroidal vascularity using swept-source optical coherence tomography (SS-OCT) and optical coherence tomography angiography (OCTA) in patients with systemic lupus erythematosus (SLE).

Methods

In this prospective, cross-sectional study, 48 SLE patients and 40 healthy control (group HC) participants were included. The SLE patients were divided into two subgroups: patients with SLE with no ocular disease (group I) and patients with SLE with signs of retinopathy (group II). The superficial vessel density (SVD), deep vessel density (DVD), peripapillary retinal vessel densities (pRVD), choroidal thickness (ChT), and choroidal vascularity including total choroidal area (TCA), luminal area (LA), stromal area (SA), and choroidal vascularity index (CVI) were measured using SS-OCT/OCTA. Physical and ophthalmic examinations as well as the assessments of immunological markers were performed. The results of SS-OCT/OCTA were compared between group I, group II, and group HC, while the correlations among the parameters were analyzed.

Results

The SVD, DVD, and pRVD were found to be significantly lower in SLE patients than group HC, especially in SLE patients with signs of retinopathy. ChT were found to be significantly higher in group II. CVI was positively correlated with SVD and DVD in the fovea, as well as the foveal and parafoveal thickness. A significant decrease in SVD and DVD in the fovea among subjects positive for anti-dsDNA antibodies was noted.

Conclusions

The application of OCTA in the evaluation of microvasculature may be useful in subclinical changes. Retinal microvascular density decreased in patients with SLE with greater severity of SLE. Disturbed retinal circulation was related to SLE disease activity, disease duration, CVI, and being positive for anti-dsDNA antibodies. The study results also suggest that SLE with signs of retinopathy may affect the choroid with increases in LA, SA, TCA, and ChT.

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References

  1. Danchenko N, Satia JA, Anthony MS (2006) Epidemiology of systemic lupus erythematosus: a comparison of worldwide disease burden. Lupus 15(5):308–318. https://doi.org/10.1191/0961203306lu2305xx

    Article  CAS  PubMed  Google Scholar 

  2. Peponis V, Kyttaris VC, Tyradellis C, Vergados I, Sitaras NM (2006) Ocular manifestations of systemic lupus erythematosus: a clinical review. Lupus 15(1):3–12. https://doi.org/10.1191/0961203306lu2250rr

    Article  CAS  PubMed  Google Scholar 

  3. Read RW (2004) Clinical mini-review: systemic lupus erythematosus and the eye. Ocul Immunol Inflamm 12(2):87–99. https://doi.org/10.1080/09273940490895308

    Article  PubMed  Google Scholar 

  4. Nag TC, Wadhwa S (2006) Vascular changes of the retina and choroid in systemic lupus erythematosus: pathology and pathogenesis. Curr Neurovasc Res 3(2):159–168. https://doi.org/10.2174/156720206776875821

    Article  PubMed  Google Scholar 

  5. Jia Y, Morrison JC, Tokayer J, Tan O, Lombardi L, Baumann B, Lu CD, Choi W, Fujimoto JG, Huang D (2012) Quantitative OCT angiography of optic nerve head blood flow. Biomed Opt Express 3(12):3127–3137. https://doi.org/10.1364/BOE.3.003127

    Article  PubMed  PubMed Central  Google Scholar 

  6. Jia Y, Wei E, Wang X, Zhang X, Morrison JC, Parikh M, Lombardi LH, Gattey DM, Armour RL, Edmunds B, Kraus MF, Fujimoto JG, Huang D (2014) Optical coherence tomography angiography of optic disc perfusion in glaucoma. Ophthalmology 121(7):1322–1332. https://doi.org/10.1016/j.ophtha.2014.01.021

    Article  PubMed  Google Scholar 

  7. An Q, Gao J, Liu L, Liao R, Shuai Z (2021) Analysis of foveal microvascular abnormalities in patients with systemic lupus erythematosus using optical coherence tomography angiography. Ocul Immunol Inflamm 29(7–8):1392–1397. https://doi.org/10.1080/09273948.2020.1735452

    Article  PubMed  Google Scholar 

  8. Arfeen SA, Bahgat N, Adel N, Eissa M, Khafagy MM (2020) Assessment of superficial and deep retinal vessel density in systemic lupus erythematosus patients using optical coherence tomography angiography. Graefes Arch Clin Exp Ophthalmol 258(6):1261–1268. https://doi.org/10.1007/s00417-020-04626-7

    Article  PubMed  Google Scholar 

  9. Mihailovic N, Leclaire MD, Eter N, Brucher VC (2020) Altered microvascular density in patients with systemic lupus erythematosus treated with hydroxychloroquine-an optical coherence tomography angiography study. Graefes Arch Clin Exp Ophthalmol 258(10):2263–2269. https://doi.org/10.1007/s00417-020-04788-4

    Article  PubMed  PubMed Central  Google Scholar 

  10. Borrelli E, Gabela MC, Sacconi R, Querques L, Vella G, Zuccaro B, Gelormini F, Bandello F, Querques G (2021) Choroidal luminal and stromal areas and choriocapillaris perfusion are characterised by a non-linear quadratic relation in healthy eyes. Br J Ophthalmol 105(4):567–572. https://doi.org/10.1136/bjophthalmol-2020-316479

    Article  PubMed  Google Scholar 

  11. Iovino C, Pellegrini M, Bernabei F, Borrelli E, Sacconi R, Govetto A, Vagge A, Di Zazzo A, Forlini M, Finocchio L, Carnevali A, Triolo G, Giannaccare G (2020) Choroidal vascularity index: an in-depth analysis of this novel optical coherence tomography parameter. J Clin Med 9(2):595. https://doi.org/10.3390/jcm9020595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Sonoda S, Sakamoto T, Yamashita T, Shirasawa M, Uchino E, Terasaki H, Tomita M (2014) Choroidal structure in normal eyes and after photodynamic therapy determined by binarization of optical coherence tomographic images. Invest Ophthalmol Vis Sci 55(6):3893–3899. https://doi.org/10.1167/iovs.14-14447

    Article  PubMed  Google Scholar 

  13. Singh SR, Invernizzi A, Rasheed MA, Cagini C, Goud A, Vupparaboina KK, Cozzi M, Lupidi M, Chhablani J (2018) Wide-field choroidal vascularity in healthy eyes. Am J Ophthalmol 193:100–105. https://doi.org/10.1016/j.ajo.2018.06.016

    Article  PubMed  Google Scholar 

  14. Tan KA, Laude A, Yip V, Loo E, Wong EP, Agrawal R (2016) Choroidal vascularity index - a novel optical coherence tomography parameter for disease monitoring in diabetes mellitus? Acta Ophthalmol 94(7):e612–e616. https://doi.org/10.1111/aos.13044

    Article  PubMed  Google Scholar 

  15. Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40(9):1725. https://doi.org/10.1002/art.1780400928

    Article  CAS  PubMed  Google Scholar 

  16. Gladman DD, Ibanez D, Urowitz MB (2002) Systemic lupus erythematosus disease activity index 2000. Rheumatol 29(2):288–291

    Google Scholar 

  17. Agrawal R, Wei X, Goud A, Vupparaboina KK, Jana S, Chhablani J (2017) Influence of scanning area on choroidal vascularity index measurement using optical coherence tomography. Acta Ophthalmol 95(8):e770–e775. https://doi.org/10.1111/aos.13442

    Article  PubMed  Google Scholar 

  18. Sonoda S, Sakamoto T, Yamashita T, Uchino E, Kawano H, Yoshihara N, Terasaki H, Shirasawa M, Tomita M, Ishibashi T (2015) Luminal and stromal areas of choroid determined by binarization method of optical coherence tomographic images. Am J Ophthalmol 159(6):1123-1131.e1. https://doi.org/10.1016/j.ajo.2015.03.005

    Article  PubMed  Google Scholar 

  19. Giannaccare G, Pellegrini M, Sebastiani S, Bernabei F, Moscardelli F, Iovino C, Napoli PE, Campos E (2020) Choroidal vascularity index quantification in geographic atrophy using binarization of enhanced-depth imaging optical coherence tomographic scans. Retina 40(5):960–965. https://doi.org/10.1097/IAE.0000000000002459

    Article  PubMed  Google Scholar 

  20. Zhang Q, Zheng F, Motulsky EH, Gregori G, Chu Z, Chen CL, Li C, de Sisternes L, Durbin M, Rosenfeld PJ, Wang RK (2018) A novel strategy for quantifying choriocapillaris flow voids using swept-source OCT angiography. Invest Ophthalmol Vis Sci 59(1):203–211. https://doi.org/10.1167/iovs.17-22953

    Article  PubMed  PubMed Central  Google Scholar 

  21. Saygin D, Highland KB, Tonelli AR (2019) Microvascular involvement in systemic sclerosis and systemic lupus erythematosus. Microcirculation 26(3):e12440. https://doi.org/10.1111/micc.12440

    Article  PubMed  PubMed Central  Google Scholar 

  22. de Larrinoa IRFF (2015) What is new in systemic lupus erythematosus. Reumatol Clin 11(1):27–32. https://doi.org/10.1016/j.reuma.2014.09.004

    Article  Google Scholar 

  23. Liu GY, Utset TO, Bernard JT (2015) Retinal nerve fiber layer and macular thinning in systemic lupus erythematosus: an optical coherence tomography study comparing SLE and neuropsychiatric SLE. Lupus 24(1):1169–1176. https://doi.org/10.1177/0961203315582285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Karpik AG, Schwartz MM, Dickey LE, Streeten BW, Roberts JL (1985) Ocular immune reactants in patients dying with systemic lupus erythematosus. Clin Immunol Immunopathol 35(3):295–312. https://doi.org/10.1016/0090-1229(85)90091-1

    Article  CAS  PubMed  Google Scholar 

  25. Altinkaynak H, Duru N, Uysal BS, Erten S, Kurkcuoglu PZ, Yuksel N, Duru Z, Cagil N (2016) Choroidal thickness in patients with systemic lupus erythematosus analyzed by spectral-domain optical coherence tomography. Ocul Immunol Inflamm 24(3):254–260. https://doi.org/10.3109/09273948.2015.1006790

    Article  CAS  PubMed  Google Scholar 

  26. Agin A, Kadayifcilar S, Sonmez HE, Baytaroglu A, Demir S, Sag E, Ozen S, Eldem B (2019) Evaluation of choroidal thickness, choroidal vascularity index and peripapillary retinal nerve fiber layer in patients with juvenile systemic lupus erythematosus. Lupus 28(1):44–50. https://doi.org/10.1177/0961203318814196

    Article  CAS  PubMed  Google Scholar 

  27. Bao L, Zhou R, Wu Y, Wang J, Shen M, Lu F, Wang H, Chen Q (2020) Unique changes in the retinal microvasculature reveal subclinical retinal impairment in patients with systemic lupus erythematosus. Microvasc Res 129:103957. https://doi.org/10.1016/j.mvr.2019.103957

    Article  CAS  PubMed  Google Scholar 

  28. Kim M, Kim SS, Kwon HJ, Koh HJ, Lee SC (2012) Association between choroidal thickness and ocular perfusion pressure in young, healthy subjects: enhanced depth imaging optical coherence tomography study. Invest Ophthalmol Vis Sci 53(12):7710–7717. https://doi.org/10.1167/iovs.12-10464

    Article  PubMed  Google Scholar 

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Funding

Project supported by the Science and Technology Commission of Shanghai Municipality, China (Grant No. 20Y11911200).

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Author notes

  1. Tingting Guo and Yihua Jin contributed equally to this article.

Authors and Affiliations

  1. Department of Ophthalmology and Shanghai Key Laboratory of Visual Impairment and Restoration, Eye, Ear, Nose, and Throat Hospital of Fudan University, Shanghai, China

    Tingting Guo, Yihua Jin, Min Zhou, Boya Lei & Kang Xue

  2. Department of Rheumatology, School of Medicine, Renji Hospital, Shanghai Jiao Tong University, Shanghai, China

    Linlin Huang & Sheng Chen

Authors
  1. Tingting Guo
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  2. Yihua Jin
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  3. Min Zhou
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  4. Boya Lei
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  5. Linlin Huang
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  6. Sheng Chen
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  7. Kang Xue
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Corresponding authors

Correspondence to Sheng Chen or Kang Xue.

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Ethics approval and consent to participate

All procedures performed on human participants followed the 1964 Declaration of Helsinki and its later amendments after receiving proper approval from the Human Research Ethics Committee of the Eye & ENT Hospital of Fudan University (No. 2021005–1). Informed consent was obtained from all participants.

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Guo, T., Jin, Y., Zhou, M. et al. Quantitative evaluation of retinal and choroidal vascularity in systemic lupus erythematosus by SS-OCT/OCTA. Graefes Arch Clin Exp Ophthalmol 261, 3385–3393 (2023). https://doi.org/10.1007/s00417-023-06155-5

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