Advances and outlook for lupus retinopathy

References

• Lubon W, Lubon M, Kotyla P, et al. Understanding ocular findings and manifestations of systemic lupus erythematosus: update review of the literature. Int J Mol Sci. 2022 Oct 14;23(20):12264. doi: 10.3390/ijms232012264
   PubMed Web of Science ®Google Scholar
• Palejwala NV, Walia HS, Yeh S. Ocular manifestations of systemic lupus erythematosus: a review of the literature. Autoimmune Dis. 2012;2012:1–9. doi: 10.1155/2012/290898
   Google Scholar
• Davies JB, Rao PK. Ocular manifestations of systemic lupus erythematosus. Curr Opin Ophthalmology. 2008 Nov;19(6):512–518. doi: 10.1097/ICU.0b013e3283126d34
   PubMed Web of Science ®Google Scholar
• Sivaraj RR, Durrani OM, Denniston AK, et al. Ocular manifestations of systemic lupus erythematosus. Rheumatology (Oxford). 2007, Dec;46(12):1757–1762.
   PubMed Web of Science ®Google Scholar
• Tian J, Zhang D, Yao X, et al. Global epidemiology of systemic lupus erythematosus: a comprehensive systematic analysis and modelling study. Ann Rheum Dis. 2023, Mar;82(3):351–356.
   PubMed Web of Science ®Google Scholar
• Gawdat G, El-Fayoumi D, Marzouk H, et al. Ocular manifestations in children with juvenile-onset systemic lupus erythematosus. Semin Ophthalmol. 2018;33(4):470–476. doi: 10.1080/08820538.2017.1301497
   PubMed Web of Science ®Google Scholar
• Silpa-Archa S, Lee JJ, Foster CS. Ocular manifestations in systemic lupus erythematosus. Br J Ophthalmology. 2016 Jan;100(1):135–141. doi: 10.1136/bjophthalmol-2015-306629
   PubMed Web of Science ®Google Scholar
• Peponis V, Kyttaris VC, Tyradellis C, et al. Ocular manifestations of systemic lupus erythematosus: a clinical review. Lupus. 2006;15(1):3–12. doi: 10.1191/0961203306lu2250rr
   PubMed Web of Science ®Google Scholar
• Seth G, Chengappa KG, Misra DP, et al. Lupus retinopathy: a marker of active systemic lupus erythematosus. Rheumatol Int. 2018, Aug;38(8):1495–1501.
   PubMed Web of Science ®Google Scholar
• Dias-Santos A, Tavares Ferreira J, Pinheiro S, et al. Ocular involvement in systemic lupus erythematosus patients: a paradigm shift based on the experience of a tertiary referral center. Lupus. 2020, Mar;29(3):283–289.
   PubMed Web of Science ®Google Scholar
• Hysa E, Cutolo CA, Gotelli E, et al. Ocular microvascular damage in autoimmune rheumatic diseases: The pathophysiological role of the immune system. Autoimmun Rev. 2021 May;20(5):102796.
   PubMed Web of Science ®Google Scholar
• Lee I, Zickuhr L, Hassman L. Update on ophthalmic manifestations of systemic lupus erythematosus: pathogenesis and precision medicine. Curr Opin Ophthalmology. 2021 Nov 1;32(6):583–589. doi: 10.1097/ICU.0000000000000810
   PubMed Web of Science ®Google Scholar
• Cao X, Bishop RJ, Forooghian F, et al. Autoimmune retinopathy in systemic lupus erythematosus: histopathologic features. Open Ophthalmol J. 2009 Apr 28;3(1):20–25. doi: 10.2174/1874364100903010020
   PubMedGoogle Scholar
• Shah D, Mahajan N, Sah S, et al. Oxidative stress and its biomarkers in systemic lupus erythematosus. J Biomed Sci. 2014 Mar 17;21(1):23. doi: 10.1186/1423-0127-21-23
   PubMedGoogle Scholar
• Moschetti L, Piantoni S, Vizzardi E, et al. Endothelial dysfunction in systemic lupus erythematosus and systemic sclerosis: a common trigger for different microvascular diseases. Front Med. 2022;9:849086. doi: 10.3389/fmed.2022.849086
   Web of Science ®Google Scholar
• Ushiyama O, Ushiyama K, Koarada S, et al. Retinal disease in patients with systemic lupus erythematosus. Ann Rheum Dis. 2000, Sep;59(9):705–708.
   PubMed Web of Science ®Google Scholar
• Graham EM, Spalton DJ, Barnard RO, et al. Cerebral and retinal vascular changes in systemic lupus erythematosus. Ophthalmology. 1985, Mar;92(3):444–448.
   PubMed Web of Science ®Google Scholar
• Kharel Sitaula R, Shah DN, Singh D. Role of lupus retinopathy in systemic lupus erythematosus. J Ophthalmic Inflamm Infect. 2016 Dec;6(1):15. doi: 10.1186/s12348-016-0081-4
   PubMedGoogle Scholar
• Stafford-Brady FJ, Urowitz MB, Gladman DD, et al. Lupus retinopathy. Patterns, associations, and prognosis. Arthritis Rheum. 1988, Sep;31(9):1105–10.
   PubMedGoogle Scholar
• Marmor MF, Kellner U, Lai TY, et al. Revised recommendations on screening for chloroquine and hydroxychloroquine retinopathy. Ophthalmology. 2011, Feb;118(2):415–422.
   PubMed Web of Science ®Google Scholar
• Yusuf IH, Foot B, Lotery AJ. The Royal college of ophthalmologists recommendations on monitoring for hydroxychloroquine and chloroquine users in the United Kingdom (2020 revision): executive summary. Eye (Lond). 2021 Jan 9;35(6):1532–1537.
   PubMed Web of Science ®Google Scholar
• Manoussakis MN, Georgopoulou C, Zintzaras E, et al. Sjogren’s syndrome associated with systemic lupus erythematosus: clinical and laboratory profiles and comparison with primary Sjogren’s syndrome. Arthritis Rheum. 2004, Mar;50(3):882–891.
   PubMedGoogle Scholar
• Papagiannuli E, Rhodes B, Wallace GR, et al. Systemic lupus erythematosus: an update for ophthalmologists. Surv Ophthalmology. 2016, Jan;61(1):65–82.
   PubMed Web of Science ®Google Scholar
• Thong B, Olsen NJ. Systemic lupus erythematosus diagnosis and management. Rheumatology (Oxford). 2017 Apr 1;56(suppl_1):i3–i13. doi: 10.1093/rheumatology/kew401
   PubMedGoogle Scholar
• Conigliaro P, Cesareo M, Chimenti MS, et al. Take a look at the eyes in systemic lupus erythematosus: a novel point of view. Autoimmun Rev. 2019, Mar;18(3):247–254.
   PubMed Web of Science ®Google Scholar
• Gatto M, Iaccarino L, Ghirardello A, et al. Clinical and pathologic considerations of the qualitative and quantitative aspects of lupus nephritogenic autoantibodies: a comprehensive review. J Autoimmun. 2016 May;69:1–11.
   PubMed Web of Science ®Google Scholar
• Aringer M, Costenbader K, Daikh D, et al. 2019 European League Against Rheumatism/American College of Rheumatology Classification Criteria for Systemic Lupus Erythematosus. Arthritis & rheumat. 2019, Sep;71(9):1400–1412.
   PubMed Web of Science ®Google Scholar
• Mimier-Janczak MK, Kaczmarek D, Proc K, et al. Subclinical retinopathy in systemic lupus erythematosus patients - optical coherence tomography study. Reumatologia. 2023;61(3):161–168. doi: 10.5114/reum/166296
   PubMed Web of Science ®Google Scholar
• Fouad SA, Esmat Mahmoud Ali SM, Rezk Alnaggar ARL, et al. Structural retinal assessment using optical coherence tomography and fundus fluorescein angiography in systemic lupus erythematosus patients. J Clin Rheumatol. 2021 Jan 1;27(1):34–39. doi: 10.1097/RHU.0000000000001162
   PubMed Web of Science ®Google Scholar
• Ross JE, Bron AJ, Reeves BC, et al. Detection of optic nerve damage in ocular hypertension. Br J Ophthalmol. 1985, Dec;69(12):897–903.
   PubMed Web of Science ®Google Scholar
• Moschos MM, Tagaris G, Markopoulos L, et al. Morphologic changes and functional retinal impairment in patients with Parkinson disease without visual loss. Eur J Ophthalmol. 2011;21(1):24–29. doi: 10.5301/EJO.2010.1318
   PubMed Web of Science ®Google Scholar
• Garcia-Soler E, Martinez-Rubio C, De Smet MD, et al. Systemic lupus erythematosus purtscher like retinopathy: optical coherence tomography angiography assessment implications. Eur J Ophthalmology. 2022 Apr 25;100(S275):11206721231171705. doi: 10.1111/j.1755-3768.2022.0486
   Google Scholar
• Ermurat S, Koyuncu K. Evaluation of subclinical retinal microvascular changes in systemic lupus erythematosus patients using optical coherence tomography angiography and its relationship with disease activity. Lupus. 2022 Apr;31(5):541–554. doi: 10.1177/09612033221084222
   PubMed Web of Science ®Google Scholar
• Shi WQ, Han T, Liu R, et al. Retinal microvasculature and conjunctival vessel alterations in patients with systemic lupus erythematosus-an optical coherence tomography angiography study. Front Med. 2021;8:724283. doi: 10.3389/fmed.2021.724283
   Web of Science ®Google Scholar
• Mimier-Janczak M, Kaczmarek D, Janczak D, et al. Optical coherence tomography angiography as a new tool for evaluation of the subclinical retinal involvement in patients with systemic lupus erythematosus—A review. J Clin Med. 2021 Jun 29;10(13):2887. doi: 10.3390/jcm10132887
   PubMed Web of Science ®Google Scholar
• Mihailovic N, Leclaire MD, Eter N, et al. Altered microvascular density in patients with systemic lupus erythematosus treated with hydroxychloroquine-an optical coherence tomography angiography study. Graefes Arch Clin Exp Ophthalmology. 2020, Oct;258(10):2263–2269.
   PubMed Web of Science ®Google Scholar
• Pichi F, Woodstock E, Hay S, et al. Optical coherence tomography angiography findings in systemic lupus erythematosus patients with no ocular disease. Int Ophthalmology. 2020, Aug;40(8):2111–2118.
   PubMed Web of Science ®Google Scholar
• An Q, Gao J, Liu L, et al. Analysis of Foveal Microvascular Abnormalities in Patients with Systemic Lupus Erythematosus Using Optical Coherence Tomography Angiography. Ocul Immunol Inflamm. 2021 Nov 17;29(7–8):1392–1397. doi: 10.1080/09273948.2020.1735452
   PubMed Web of Science ®Google Scholar
• Arfeen SA, Bahgat N, Adel N, et al. Assessment of superficial and deep retinal vessel density in systemic lupus erythematosus patients using optical coherence tomography angiography. Graefes Arch Clin Exp Ophthalmology. 2020, Jun;258(6):1261–1268.
   PubMed Web of Science ®Google Scholar
• Conigliaro P, Cesareo M, Chimenti MS, et al. Evaluation of retinal microvascular density in patients affected by systemic lupus erythematosus: an optical coherence tomography angiography study. Ann Rheum Dis. 2019 Feb;78(2):287–289.
   PubMed Web of Science ®Google Scholar
• Bao L, Zhou R, Wu Y, et al. Unique changes in the retinal microvasculature reveal subclinical retinal impairment in patients with systemic lupus erythematosus. Microvasc Res. 2020 May;129:103957.
   PubMed Web of Science ®Google Scholar
• Marmor MF. Comparison of screening procedures in hydroxychloroquine toxicity. Arch Ophthalmology. 2012 Apr;130(4):461–469. doi: 10.1001/archophthalmol.2011.371
   PubMedGoogle Scholar
• Lee JH, Kim SS, Kim GT. Microvascular findings in patients with systemic lupus erythematosus assessed by fundus photography with fluorescein angiography. Clin Exp Rheumatol. 2013 Nov;31(6):871–6.
   PubMed Web of Science ®Google Scholar
• Dhingra S, Stavrou P. Indocyanine green angiography in systemic lupus erythematosus-associated uveitis. Ocul Immunol Inflamm. 2004 Mar;12(1):69–73. doi: 10.1076/ocii.12.1.69.28068
   PubMed Web of Science ®Google Scholar
• Meng P-P, Lin C-J, Hsia N-Y, et al. Use of ultra-widefield fluorescein angiography to guide the treatment to idiopathic retinal vasculitis, aneurysms, and neuroretinitis—case report and literature review. Medicina. 2022;58(10):1467. doi: 10.3390/medicina58101467
   PubMedGoogle Scholar
• Shoughy SS, Tabbara KF. Ocular findings in systemic lupus erythematosus. Saudi J Ophthalmology. 2016 Apr;30(2):117–121. doi: 10.1016/j.sjopt.2016.02.001
   PubMedGoogle Scholar
• Fanouriakis A, Kostopoulou M, Alunno A, et al. 2019 update of the EULAR recommendations for the management of systemic lupus erythematosus. Ann Rheum Dis. 2019, Jun;78(6):736–745.
   PubMed Web of Science ®Google Scholar
• Marmor MF, Kellner U, Lai TY, et al. Recommendations on screening for chloroquine and hydroxychloroquine retinopathy (2016 revision). Ophthalmology. 2016, Jun;123(6):1386–1394.
   PubMed Web of Science ®Google Scholar
• Kim KE, Ryu SJ, Kim YH, et al. Visual field examinations using different strategies in Asian patients taking hydroxychloroquine. Sci Rep. 2022 Aug 30;12(1):14778. doi: 10.1038/s41598-022-19048-0
   PubMed Web of Science ®Google Scholar
• Muthiah MN, Gias C, Chen FK, et al. Cone photoreceptor definition on adaptive optics retinal imaging. Br J Ophthalmology. 2014, Aug;98(8):1073–1079.
   PubMed Web of Science ®Google Scholar
• Mahendradas P, Vala R, Kawali A, et al. Adaptive Optics Imaging in Retinal Vasculitis. Ocul Immunol Inflamm. 2018;26(5):760–766. doi: 10.1080/09273948.2016.1263341
   PubMed Web of Science ®Google Scholar
• Hasanreisoglu M, Gulpinar Ikiz GD, Kucuk H, et al. Acute lupus choroidopathy: multimodal imaging and differential diagnosis from central serous chorioretinopathy. Int Ophthalmology. 2018, Feb;38(1):369–374.
   PubMed Web of Science ®Google Scholar
• Agarwal A, Afridi R, Agrawal R, et al. Multimodal Imaging in Retinal Vasculitis. Ocul Immunol Inflamm. 2017, Jun;25(3):424–433.
   PubMed Web of Science ®Google Scholar
• Ahn SJ, Joung J, Lee BR. En face optical coherence tomography imaging of the photoreceptor layers in hydroxychloroquine retinopathy. Am J Ophthalmology. 2019 Mar;199: 71–81. doi: 10.1016/j.ajo.2018.11.003
   PubMed Web of Science ®Google Scholar
• Mauget-Faysse M, Sukkarieh G, Jebrane H, et al. “En face” spectral-domain optical coherence tomography versus multifocal electroretinogram in hydroxychloroquine retinopathy screening. Ophthalmologica. 2023;246(1):14–23. doi: 10.1159/000528146
   PubMed Web of Science ®Google Scholar
• Tsuboi K, Mazloumi M, Guo Y, et al. Utility of en face OCT for the detection of clinically unsuspected retinal neovascularization in patients with diabetic retinopathy. Ophthalmology Retina. 2023 Mar 12;7(8):683–691. doi: 10.1016/j.oret.2023.03.002
   PubMedGoogle Scholar
• Bansal A, Hamli H, Lee WW, et al. En Face OCT in Diagnosis of Persistent Subretinal Fluid and Outer Retinal Folds after Rhegmatogenous Retinal Detachment Repair. Ophthalmology Retina. 2023, Jun;7(6):496–502.
   PubMedGoogle Scholar
• Lehmann M, Wolff B, Vasseur V, et al. Retinal and choroidal changes observed with ‘en face’ enhanced-depth imaging OCT in central serous chorioretinopathy. Br J Ophthalmology. 2013, Sep;97(9):1181–1186.
   PubMed Web of Science ®Google Scholar
• Ferrara D, Mohler KJ, Waheed N, et al. En face enhanced-depth swept-source optical coherence tomography features of chronic central serous chorioretinopathy. Ophthalmology. 2014, Mar;121(3):719–726.
   PubMed Web of Science ®Google Scholar
• Tan G, Baby B, Zhou Y, et al. Emerging molecular markers towards potential diagnostic panels for lupus. Front Immunol. 2021;12:808839. doi: 10.3389/fimmu.2021.808839
   PubMed Web of Science ®Google Scholar
• Bassi A, Krance SH, Pucchio A, et al. The application of artificial intelligence in the analysis of biomarkers for diagnosis and management of uveitis and Uveal Melanoma: a systematic review. Clin Ophthalmology. 2022;16:2895–2908. doi: 10.2147/OPTH.S377358
   PubMed Web of Science ®Google Scholar
• Sorkhabi MA, Potapenko IO, Ilginis T, et al. Assessment of anterior uveitis through anterior-segment optical coherence tomography and artificial intelligence-based image analyses. Transl Vis Sci Technol. 2022 Apr 1;11(4):7. doi: 10.1167/tvst.11.4.7
   PubMed Web of Science ®Google Scholar
• Nakayama LF, Ribeiro LZ, Dychiao RG, et al. Artificial intelligence in uveitis: A comprehensive review. Surv Ophthalmology. 2023, Jul;68(4):669–677.
   PubMed Web of Science ®Google Scholar
• So H, Chow E, Cheng IT, et al. Use of telemedicine for follow-up of lupus nephritis in the COVID-19 outbreak: the 6-month results of a randomized controlled trial. Lupus. 2022, Apr;31(4):488–494.
   PubMed Web of Science ®Google Scholar
• Ahn SJ, Joung J, Lee BR. Evaluation of hydroxychloroquine retinopathy using ultra-widefield fundus autofluorescence: peripheral findings in the retinopathy. Am J Ophthalmology. 2020 Sep 14;209:35–44. doi: 10.1016/j.ajo.2019.09.008
   PubMed Web of Science ®Google Scholar
• Ahn SJ, Joung J, Lim HW, et al. Optical coherence tomography protocols for screening of hydroxychloroquine retinopathy in Asian patients. Am J Ophthalmol. 2017 Dec;184:11–18.
   PubMed Web of Science ®Google Scholar
• Ahn SJ, Lee SU, Lee SH, et al. Evaluation of Retromode Imaging for Use in Hydroxychloroquine Retinopathy. Am J Ophthalmology. 2018 Dec;196:44–52.
   PubMed Web of Science ®Google Scholar
• Ahn SJ, Ryu SJ, Lim HW, et al. Toxic effects of hydroxychloroquine on the choroid: evidence from multimodal imaging. Retina (Philadelphia, Pa). 2019, May;39(5):1016–1026.
   PubMed Web of Science ®Google Scholar
• Kim KE, Ahn SJ, Woo SJ, et al. Use of optical coherence tomography retinal thickness deviation map for hydroxychloroquine retinopathy screening. Ophthalmology. 2021 Jun 15;128(1):110–119. doi: 10.1016/j.ophtha.2020.06.021
   PubMed Web of Science ®Google Scholar
• Yoon YH, Cho KS, Hwang JJ, et al. Induction of lysosomal dilatation, arrested autophagy, and cell death by chloroquine in cultured ARPE-19 cells. Invest Ophthalmology Visual Sci. 2010, Nov;51(11):6030–7.
   PubMed Web of Science ®Google Scholar
• Yusuf IH, Charbel Issa P, Ahn SJ. Novel imaging techniques for hydroxychloroquine retinopathy. Front Med. 2022;9:1026934. doi: 10.3389/fmed.2022.1026934
   Web of Science ®Google Scholar
• Kim KE, Kim YH, Kim J, et al. Macular ganglion cell complex and peripapillary retinal nerve fiber layer thicknesses in hydroxychloroquine retinopathy. Am J Ophthalmology. 2023 Jan;245:70–80.
   PubMed Web of Science ®Google Scholar
• Ahn SJ, Seo EJ, Kim KE, et al. Long-term progression of pericentral hydroxychloroquine retinopathy. Ophthalmology. 2021, Jun;128(6):889–898.
   PubMed Web of Science ®Google Scholar
• Buchman AL. Side effects of corticosteroid therapy. J Clin Gastroenterol. 2001 Oct;33(4):289–294. doi: 10.1097/00004836-200110000-00006
   PubMed Web of Science ®Google Scholar
• Fung AT, Tran T, Lim LL, et al. Local delivery of corticosteroids in clinical ophthalmology: a review. Clin Exp Ophthalmol. 2020, Apr;48(3):366–401.
   PubMed Web of Science ®Google Scholar
• Jones R 3rd, Rhee DJ. Corticosteroid-induced ocular hypertension and glaucoma: a brief review and update of the literature. Curr Opin Ophthalmology. 2006 Apr;17(2):163–167. doi: 10.1097/01.icu.0000193079.55240.18
   PubMed Web of Science ®Google Scholar
• Kersey JP, Broadway DC. Corticosteroid-induced glaucoma: a review of the literature. Eye (Lond). 2006 Apr;20(4):407–416. doi: 10.1038/sj.eye.6701895
   PubMed Web of Science ®Google Scholar
• Carli L, Tani C, Querci F, et al. Analysis of the prevalence of cataracts and glaucoma in systemic lupus erythematosus and evaluation of the rheumatologists’ practice for the monitoring of glucocorticoid eye toxicity. Clin Rheumatol. 2013, Jul;32(7):1071–3.
   PubMed Web of Science ®Google Scholar
• Cunningham ET Jr., Alfred PR, Irvine AR. Central serous chorioretinopathy in patients with systemic lupus erythematosus. Ophthalmology. 1996 Dec;103(12):2081–2090. doi: 10.1016/S0161-6420(96)30385-0
   PubMed Web of Science ®Google Scholar
• Semeraro F, Morescalchi F, Russo A, et al. Central serous chorioretinopathy: pathogenesis and management. Clin Ophthalmology. 2019;13:2341–2352. doi: 10.2147/OPTH.S220845
   PubMed Web of Science ®Google Scholar
• van der Goes MC, Jacobs JW, Boers M, et al. Monitoring adverse events of low-dose glucocorticoid therapy: EULAR recommendations for clinical trials and daily practice. Ann Rheum Dis. 2010, Nov;69(11):1913–1919.
   PubMed Web of Science ®Google Scholar
• Hong-Kee N, Mei-Fong C, Azhany Y, et al. Antiphospholipid syndrome in lupus retinopathy. Clin Ophthalmology. 2014;8:2359–2363. doi: 10.2147/OPTH.S71712
   PubMedGoogle Scholar
• Ikic Matijasevic M, Kilic P, Ikic L, et al. Rituximab, intravitreal bevacizumab and laser photocoagulation for treatment of macrophage activation syndrome and retinal vasculitis in lupus: a case report. Int J Mol Sci. 2023 Jan 30;24(3):2594. doi: 10.3390/ijms24032594
   PubMed Web of Science ®Google Scholar
• Katarzyna PB, Wiktor S, Ewa D, et al. Current treatment of systemic lupus erythematosus: a clinician’s perspective. Rheumatol Int. 2023, Aug;43(8):1395–1407.
   PubMed Web of Science ®Google Scholar
• Tah V, Orlans HO, Hyer J, et al. Anti-VEGF therapy and the Retina: an update. J Ophthalmol. 2015;2015:1–13. doi: 10.1155/2015/627674
   Web of Science ®Google Scholar
• Sciascia S, Radin M, Yazdany J, et al. Efficacy of belimumab on renal outcomes in patients with systemic lupus erythematosus: a systematic review. Autoimmun Rev. 2017, Mar;16(3):287–293.
   PubMed Web of Science ®Google Scholar
• Ramos-Casals M, Soto MJ, Cuadrado MJ, et al. Rituximab in systemic lupus erythematosus: a systematic review of off-label use in 188 cases. Lupus. 2009, Aug;18(9):767–776.
   PubMed Web of Science ®Google Scholar
• Li M, Jin Y, He J. Purtscher-like retinopathy associated with systemic lupus erythematosus treated with rituximab plus low-dose interleukin-2: a case report. Int J Rheum Dis. 2023 Feb 20;26(7):1373–1376. doi: 10.1111/1756-185X.14623
   PubMed Web of Science ®Google Scholar
• Liossis SN, Staveri C. What’s new in the treatment of systemic lupus erythematosus. Front Med. 2021;8:655100. doi: 10.3389/fmed.2021.655100
   PubMed Web of Science ®Google Scholar