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Macular and peripapillary vessel density alterations in a large series of patients with systemic lupus erythematosus without ocular involvement

  • Retinal Disorders
  • Published:
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Abstract

Purpose

The aim of this study was to investigate changes in both macular and peripapillary retinal microcirculation in the subclinical period of systemic lupus erythematosus (SLE) patients and to assess the relationship of these changes with disease activity, damage index, renal involvement, and use of hydroxychloroquine (HCQ).

Methods

Sixty eyes of 60 SLE patients and 60 age-matched, healthy controls were evaluated with optical coherence tomography angiography (OCTA). Vessel densities, structural parameters, and foveal avascular zone (FAZ) assesments were made.

Results

There was no significant correlation between activity and damage index and all regions of both superficial (SCP-VD) and deep capillary plexus vessel densities (DCP-VD) in the SLE group. There were no significant difference between groups in terms of FAZ, structural parameters, and radial peripapillary capillary vessel densities (RPC-VD). The mean SCP-VD and DCP-VD of most regions showed a significant decrease in the SLE group, except for parafovea superior and parafovea temporal. The decrease in vessel density (VD) in the perifoveal regions of DCP-VD in SLE patients was remarkable. DCP-VD showed good specifity and sensitivity in detecting vascular changes in SLE patients with whole image area under the curve (AUC) = 0.671, p < 0.001, odds ratio (OR) = 0.909, p = 0.009, and perifovea AUC = 0.671, p < 0.001, OR = 0.918, p = 0.012. Similarly, the SCP-VD whole image AUC = 0.609, p = 0.037, and OR = 0.825, p = 0.018 and perifovea AUC = 0.608, p = 0.037, and OR = 0.918, p = 0.012. The DCP-VD of perifovea superior showed a diagnostic accuracy for discrimination between SLE patients with and without nephritis (AUC = 0.671, p = 0.016). The SCP-VD and cumulative dose of HCQ demonstrated significant negative correlation in the SLE group (whole image, r =  − 0.332, p = 0.010).

Conclusions

SLE patients without ocular involvement had vascular changes that were particularly evident in the DCP and primarily in the perifovea. The perifovea superior of DCP had diagnostic utility in patients with nephropathy.

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Data availability

The data that support the findings of this study are available from the corresponding author, (S. S.), upon reasonable request.

Code availability

Not applicable.

References

  1. Sitaula R, Shah DN, Singh D (2011) The spectrum of ocular involvement in systemic lupus erythematosus in a tertiary eye care center in Nepal. Ocul Immunol Inflamm 19:422–425. https://doi.org/10.3109/09273948.2011.610023

    Article  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 15:3–12. https://doi.org/10.1191/0961203306lu2250rr

    Article  CAS  PubMed  Google Scholar 

  3. Palejwala NV, Walia HS, Yeh S (2012) Ocular manifestations of systemic lupus erythematosus: a review of the literature. Autoimmune Dis 2012:290898. https://doi.org/10.1155/2012/290898

    Article  PubMed  PubMed Central  Google Scholar 

  4. Giorgi D, Pace F, Giorgi A, Bonomo L, Gabrieli CB (1999) Retinopathy in systemic lupus erythematosus: pathogenesis and approach to therapy. Hum Immunol 60:688–696. https://doi.org/10.1016/S0198-8859(99)00035-X

    Article  CAS  PubMed  Google Scholar 

  5. Nangia PV, Viswanathan L, Kharel R, Biswas J (2017) Retinal involvement in systemic lupus erythematosus. Lupus Open Access 2:2–5. https://doi.org/10.35248/2684-1630.17.2.129

    Article  Google Scholar 

  6. Stafford-Brady FJ, Urowitz MB, Gladman DD, Easterbrook M (1988) Lupus retinopathy. Patterns, associations, and prognosis. Arthritis Rheum 31:1105–1110. https://doi.org/10.1002/art.1780310904

    Article  CAS  PubMed  Google Scholar 

  7. Chalam KV, Sambhav K (2016) Optical coherence tomography angiography in retinal diseases. J Ophthalmic Vis Res 11:84–92. https://doi.org/10.4103/2008-322X.180709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  9. Marmor MF, Kellner U, Lai TY, Melles RB, Mieler WF (2016) American Academy of Ophthalmology. Recommendations on screening for chloroquine and hydroxychloroquine retinopathy (2016 Revision). Ophthalmology 123:1386–1394. https://doi.org/10.1016/j.ophtha.2016.01.058

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  11. Cook RJ, Gladman DD, Pericak D, Urowitz MB (2000) Prediction of short term mortality in systemic lupus erythematosus with time dependent measures of disease activity. J Rheumatol 27:1892–1895

    CAS  PubMed  Google Scholar 

  12. Gladman D, Ginzler E, Goldsmith C, Fortin P, Liang M, Urowitz M, Bacon P, Bombardieri S, Hanly J, Hay E (1992) Systemic lupus international collaborative clinics: development of a damage index in systemic lupus erythematosus. J Rheumatol 19:1820–1821

    CAS  PubMed  Google Scholar 

  13. Dammacco R (2018) Systemic lupus erythematosus and ocular involvement: an overview. Clin Exp Med 18:135–149. https://doi.org/10.1007/s10238-017-0479-97

    Article  CAS  PubMed  Google Scholar 

  14. Lee JH, Kim SS, Kim GT (2013) Microvascular findings in patients with systemic lupus erythematosus assessed by fundus photography with fluorescein angiography. Clin Exp Rheumatol 31(871–876):5

    Google Scholar 

  15. Conigliaro P, Cesareo M, Chimenti MS, Triggianese P, Canofari C, Aloe G, Nucci C, Perricone R (2019) Evaluation of retinal microvascular density in patients affected by systemic lupus erythematosus: an optical coherence tomography angiography study. Ann Rheum Dis 78:287–289. https://doi.org/10.1136/annrheumdis-2018-214235

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  17. 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 29:1392–1397. https://doi.org/10.1080/09273948.2020.1735452

    Article  PubMed  Google Scholar 

  18. Arfeen SA, Nermeen B, Nehal A, Mervat E, Khafagy MM (2020) Assessment of superficial and deep retinal vessel density in systemic lupus erythematosus patients using optical coherence tomography angiography. Graefe’s Arch Clin Exp Ophthalmol 258:1261–1268. https://doi.org/10.1007/s00417-020-04626-7

    Article  Google Scholar 

  19. Pichi F, Woodstock E, Hay S, Neri P (2020) Optical coherence tomography angiography findings in systemic lupus erythematosus patients with no ocular disease. Int Ophthalmol 40:2111–2118. https://doi.org/10.1007/s10792-020-01388-3

    Article  PubMed  Google Scholar 

  20. Işık MU, Akmaz B, Akay F, Güven YZ, Solmaz D, Gercik Ö, Kabadayı G, Kurut İ, Akar S (2021) Evaluation of subclinical retinopathy and angiopathy with OCT and OCTA in patients with systemic lupus erythematosus. Int Ophthalmol 41:143–150. https://doi.org/10.1007/s10792-020-01561-8

    Article  PubMed  Google Scholar 

  21. Forte R, Haulani H, Dyrda A, Jürgens I (2021) Swept source optical coherence tomography angiography in patients treated with hydroxychloroquine: correlation with morphological and functional tests. Br J Ophthalmol 105:1297–1301. https://doi.org/10.1136/bjophthalmol-2018-313679

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. School of Medicine, Department of Ophthalmology, Kocaeli University, Kocaeli, Turkey

    Sevgi Subasi

  2. Derince Training and Research Hospital, University of Health Sciences, Kocaeli, Turkey

    Kubra Demirci Kucuk & Ecem Onder Tokuc

  3. School of Medicine, Department of Internal Medicine, Division of Rheumatology, Kocaeli University, Kocaeli, Turkey

    Senar San, Ayse Cefle & Ayten Yazici

  4. School of Medicine, Department of Biostatistics and Medical Informatics, Kocaeli University, Kocaeli, Turkey

    Sibel Balci

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  1. Sevgi Subasi
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Correspondence to Sevgi Subasi.

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Ethics approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards (GOKAEK-2020/08.06 220/68).

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Informed consent was obtained from all individual participants included in the study. Approval was obtained from the ethics committee of Kocaeli University. The procedures used in this study adhere to the tenets of the Declaration of Helsinki.

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The authors declare no competing interests.

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Subasi, S., Kucuk, K.D., San, S. et al. Macular and peripapillary vessel density alterations in a large series of patients with systemic lupus erythematosus without ocular involvement. Graefes Arch Clin Exp Ophthalmol 260, 3543–3552 (2022). https://doi.org/10.1007/s00417-022-05742-2

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  • DOI: https://doi.org/10.1007/s00417-022-05742-2

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