Офтальмологические проявления системной красной волчанки: влияние аутоиммунного воспаления

   Системная красная волчанка (СКВ) – мультисистемное аутоиммунное заболевание неустановленной этиологии с гетерогенными клиническими проявлениями. До трети больных СКВ имеют различные офтальмологические симптомы. Поражения глаз могут быть начальными признаками СКВ и приводить к тяжелым осложнениям, включая потерю зрения. Офтальмологические проявления часто связаны со степенью активности системного воспаления. Сухой кератоконъюнктивит, или вторичный синдром Шегрена, является наиболее частым поражением глаз при СКВ. Эписклерит и склерит встречаются реже, однако они могут быть первыми признаками заболевания. Односторонняя или чаще двусторонняя ретинопатия, связанная с васкулитом сосудов сетчатки, может являться причиной утраты зрения различной степени тяжести. На фоне длительного применения препаратов, используемых в настоящее время для лечения СКВ, возникает ряд нежелательных офтальмологических явлений: задняя субкапсулярная катаракта и вторичная открытоугольная глаукома при использовании глюкокортикостероидов, ретинопатии – в случаях продолжительного приема гидроксихлорохина. Побочные эффекты других иммуносупрессивных и генно-инженерных биологических препаратов до сих пор плохо изучены. Всем пациентам с СКВ рекомендуется проводить регулярные офтальмологические осмотры.

1. Hysa E, Cutolo CA, Gotelli E, Paolino S, Cimmino MA, Pacini G, Pizzorni C, Sulli A, Smith V, Cutolo M. Ocular microvascular damage in autoimmune rheumatic diseases: The pathophysiological role of the immune system. Autoimmun Rev. 2021 May; 20 (5): 102796. DOI: 10.1016/j.autrev.2021.102796

2. Luboń W, Luboń M, Kotyla P, Mrukwa-Kominek E. 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

3. Silpa-archa S, Lee JJ, Foster CS. Ocular manifestations in systemic lupus erythematosus. British Journal of Ophthalmology. 2016; 100: 135–141.

4. McMenamin PG. The distribution of immune cells in the uveal tract of the normal eye. Eye (Lond) 1997; 11 (Pt 2): 183–93.

5. Keino H, Horie S, Sugita S. Immune privilege and eye-derived T-regulatory cells. J. Immunol Res. 2018 May 20; 2018: 1679197. doi: 10.1155/2018/1679197

6. Lisnevskaia L, Murphy G, Isenberg D. Systemic lupus erythematosus. Lancet 2014; 384: 1878–1888.

7. Talat L, Lightman S, Tomkins-Netzer O. Ischemic retinal vasculitis and its management. J. Ophthalmol. 2014; 2014: 197675.

8. Yen YC, Weng SF, Chen HA, Lin YS. Risk of retinal vein occlusion in patients with systemic lupus erythematosis: a population-based cohort study. Br. J. Ophthalmol. 2013; 97: 1192–1196.

9. Sandhu V, Quan M. SLE and serum complement: causative, concomitant or coincidental? Open Rheumatol J. 2018 Sep 18; 12: 171. doi: 10.2174/1874312901812010171

10. D’Cruz DP, Houssiau FA, Ramirez G, Baguley E, McCutcheon J, Vianna J. et al. Antibodies to endothelial cells in systemic lupus erythematosus: a potential marker for nephritis and vasculitis. Clin Exp Immunol. 1991 Aug; 85 (2): 254–61. doi: 10.1111/j.1365–2249.1991.tb05714.x

11. Renaudineau Y, Dugu´e C, Dueymes M, Youinou P. Antiendothelial cell antibodies in systemic lupus erythematosus. Autoimmun Rev 2002 Dec; 1 (6): 365–72. doi: 10.1016/s1568-9972(02)00063-0.12848993

12. Atehortúa L, Rojas M, V´ asquez GM, Castano ˜ D. Endothelial alterations in systemic lupus erythematosus and rheumatoid arthritis: potential effect of monocyte interaction. Mediat Inflamm. 2017; 2017: 9680729. doi: 10.1155/2017/9680729

13. Erkan D, Salmon JE. The role of complement inhibition in thrombotic angiopathies and antiphospholipid syndrome. Turk. J. Haematol. 2016 Mar 5; 33 (1): 1–7. doi: 10.4274/tjh.2015.0197

14. Niewold TB, Clark DN, Salloum R, Poole BD. Interferon alpha in systemic lupus erythematosus. J. Biomed. Biotechnol. 2010; 2010: 948364. doi: 10.1155/2010/948364

15. Jones Buie JN, Oates JC. Role of interferon alpha in endothelial dysfunction: insights into endothelial nitric oxide synthase-related mechanisms. Am. J. Med. Sci. 2014 Aug; 348 (2): 168–75. doi: 10.1097/MAJ.0000000000000284

16. Knight JS, Kaplan MJ. Lupus neutrophils: ‘NET’ gain in understanding lupus pathogenesis. Curr. Opin. Rheumatol. 2012 Sep; 24 (5): 441–50. doi: 10.1097/BOR.0b013e3283546703.22617827

17. Hakkim A, Fürnrohr BG, Amann K, Laube B, Abed UA, Brinkmann V, et al. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc. Natl. Acad. Sci. U S A. 2010 May 25; 107 (21): 9813–8. doi: 10.1073/pnas.0909927107

18. Kaplan MJ. Neutrophils in the pathogenesis and manifestations of SLE. Nat Rev Rheumatol. 2011 Sep 27; 7 (12): 691–9. doi: 10.1038/nrrheum.2011.132

19. Carmona-Rivera C, Kaplan MJ. Low-density granulocytes: a distinct class of neutrophils in systemic autoimmunity. Semin Immunopathol. 2013 Jul; 35 (4): 455–63. DOI: 10.1007/s00281-013-0375-7

20. Villanueva E, Yalavarthi S, Berthier CC, Hodgin JB, Khandpur R, Lin AM, et al. Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J. Immunol. 2011 Jul 1; 187 (1): 538–52. doi: 10.4049/jimmunol.1100450

21. Skaggs BJ, Hahn BH, McMahon M. Accelerated atherosclerosis in patients with SLE – Mechanisms and management. Nat. Rev. Rheumatol. 2012 Feb 14; 8 (4): 214–23. doi: 10.1038/nrrheum.2012.14

22. Chang PC, Chen WS, Lin HY, Lee HM, Chen SJ. Combined central retinal artery and vein occlusion in a patient with systemic lupus erythematosus and antiphospholipid syndrome. Lupus. 2010 Feb; 19 (2): 206–9. doi: 10.1177/0961203309345751

23. Wu C, Dai R, Dong F, Wang Q. Purtscher-like retinopathy in systemic lupus erythematosus. Am. J. Ophthalmol. 2014 Dec; 158 (6): 1335–41. doi: 10.1016/j.ajo.2014.09.001

24. Munguia-Realpozo P, Mendoza-Pinto C, Sierra Benito C, Escarcega RO, GarciaCarrasco M, Mendez Martinez S, et al. Systemic lupus erythematosus and hypertension. Autoimmun. Rev. 2019 Oct; 18 (10): 102371. doi: 10.1016/j.autrev.2019.102371

25. Kono S, Takashima H, Suzuki D, Terada T, Konishi T, Miyajima H. Orbital myositis associated with discoid lupus erythematosus. Lupus. 2014 Feb; 23 (2): 220–2. DOI: 10.1177/0961203313517156

26. Stavrou P, Murray PI, Batta K, Gordon C. Acute ocular ischaemia and orbital inflammation associated with systemic lupus erythematosus. Br. J. Ophthalmol. 2002 Apr; 86 (4): 474–5. DOI: 10.1136/bjo.86.4.474

27. Mseddi M, Marrekchi S, Meziou TJ, Sellami D, Kammoun B, Feki J, Zahaf A, Turki H. Lupus érythémateux discoïde et paupière. Une série de 9 patients [Discoid lupus erythematosus with eyelid involvement. A series of nine patients]. J. Fr. Ophtalmol. 2007 Mar; 30 (3): 247–9. French. DOI: 10.1016/s01815512(07)89585-4

28. Lo Y, Jee SH, Cheng YP. Periorbital heliotrope edema as an uncommon manifestation of juvenile-onset systemic lupus erythematosus. Kaohsiung J. Med. Sci. 2020 Sep; 36 (9): 759–760. DOI: 10.1002/kjm2.12254

29. Mullaaziz D., Maden S., Deren O., Özkayalar H. Periorbital lupus erythematosus profundus: A case report and review of the literature. Turkderm. 2020; 54: 114–116.

30. Darjani A, Rafiei R, Mesbah A, Golmohammadi R, Rafiee B, Movaseghi M. Discoid Lupus Erythematosus Presenting as Upper Eyelid Edema and Erythema. Acta Med. Iran. 2017 Jul; 55 (7): 474–476.

31. Theisen E, Tiao J, Fedeles F. Periorbital discoid lupus erythematosus: A retrospective study. JAAD Case Rep. 2022 Jun 2; 25: 78–82. DOI: 10.1016/j.jdcr.2022.05.024

32. Kemeny-Beke A, Szodoray P. Ocular manifestations of rheumatic diseases. Int Ophthalmol. 2020 Feb; 40 (2): 503–510. DOI: 10.1007/s10792-019-01183-9

33. Wang L, Xie Y, Deng Y. Prevalence of dry eye in patients with systemic lupus erythematosus: a meta-analysis. BMJ Open. 2021 Sep 29; 11 (9): e047081. DOI: 10.1136/bmjopen-2020–047081

34. Schonberg S, Stokkermans TJ. Episcleritis. 2023 Aug 7. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2024 Jan.

35. Dutta Majumder P, Agrawal R, McCluskey P, Biswas J. Current Approach for the Diagnosis and Management of Noninfective Scleritis. Asia Pac J. Ophthalmol (Phila). 2020 Dec 7; 10 (2): 212–223. DOI: 10.1097/APO.0000000000000341

36. Messmer EM, Foster CS. Vasculitic peripheral ulcerative keratitis. Surv Ophthalmol. 1999 Mar-Apr; 43 (5): 379–96. DOI: 10.1016/s0039-6257(98)00051-4

37. Cao Y, Zhang W, Wu J, Zhang H, Zhou H. Peripheral Ulcerative Keratitis Associated with Autoimmune Disease: Pathogenesis and Treatment. J Ophthalmol. 2017; 2017: 7298026. DOI: 10.1155/2017/7298026. Epub 2017 Jul 13.

38. Lally L, Sammaritano LR. Vasculitis in antiphospholipid syndrome. Rheum Dis Clin. North. Am. 2015; 41 (1): 109–23, ix. DOI: 10.1016/j.rdc.2014.09.009

39. Montehermoso A, Cervera R, Font J, Ramos-Casals M, García-carrasco M, Formiga F, Callejas JL, Jorfán M, Griñó MC, Ingelmo M. Association of antiphospholipid antibodies with retinal vascular disease in systemic lupus erythematosus. Semin Arthritis Rheum. 1999 Apr; 28 (5): 326–32. DOI: 10.1016/s0049–0172(99)80017-1

40. Liu R, Wang Y, Xia Q, Xu T, Han T, Cai S, Luo SL, Wu R, Shao Y. Retinal thickness and microvascular alterations in the diagnosis of systemic lupus erythematosus: a new approach. Quant Imaging Med. Surg. 2022 Jan; 12 (1): 823–837. DOI: 10.21037/qims-21–359

41. Radosavljević A, Karadžić J, Kovačević I, Ljikar J, Devečerski G. Severe vaso-occlusive retinopathy associated with systemic lupus erythematosus. Vojnosanit Pregl. 2016 Dec; 73 (12): 1164–7. DOI: 10.2298/VSP150605136R

42. Leone P, Prete M, Malerba E, Bray A, Susca N, Ingravallo G, Racanelli V. Lupus Vasculitis : An Overview. Biomedicines. 2021 Nov 5; 9 (11): 1626. DOI: 10.3390/biomedicines9111626

43. Dias-Santos A, Tavares Ferreira J, Pinheiro S, Cunha JP, Alves M, Papoila AL, Moraes-Fontes MF, Proença R. Choroidal thickness changes in systemic lupus erythematosus patients. Clin Ophthalmol. 2019 Aug 20; 13: 1567–1578. DOI: 10.2147/OPTH.S219347

44. Arevalo JF, Lowder CY, Muci-Mendoza R. Ocular manifestations of systemic lupus erythematosus. Curr Opin Ophthalmol. 2002 Dec; 13 (6): 404–10. DOI: 10.1097/00055735-200212000-00011

45. Zink JM, Singh-Parikshak R, Johnson CS, Zacks DN. Hypopyon uveitis associated with systemic lupus erythematosus and antiphospholipid antibody syndrome. Graefes Arch Clin Exp Ophthalmol. 2005 Apr; 243 (4): 386–8. DOI: 10.1007/s00417-004-1022-8

46. Man BL, Mok CC, Fu YP. Neuro-ophthalmologic manifestations of systemic lupus erythematosus : a systematic review. Int J. Rheum Dis. 2014 Jun; 17 (5): 494–501. DOI: 10.1111/1756-185X.12337

47. de Andrade FA, Guimarães Moreira Balbi G, Bortoloti de Azevedo LG, Provenzano Sá G, Vieira de Moraes Junior H, Mendes Klumb E, Abramino Levy R. Neuro-ophthalmologic manifestations in systemic lupus erythematosus. Lupus. 2017 Apr; 26 (5): 522–528. DOI: 10.1177/0961203316683265

48. Jimenez-Vega A, Herencia-Anaya K, Palacios-Sánchez C, Cáceres-Del-Carpio J. Choroidopathy and optic neuropathy in systemic lupus erythematosus, a case report. Arch Soc Esp Oftalmol (Engl Ed). 2022 Jan; 97 (1): 34–39. DOI: 10.1016/j.oftale.2021.12.001

49. Nakamagoe K, Yanagiha H, Miyake Z, Kondo Y, Hiyama T, Ishii A, Kaji Y, Oshika T, Sumida T, Tamaoka A. Monocular Oculomotor Nerve Disorder Manifesting as Cranial Neuropathy in Systemic Lupus Erythematosus. Intern Med. 2018 Dec 1; 57 (23): 3445–3449. DOI: 10.2169/internalmedicine.1106-18

50. Conigliaro P, Cesareo M, Chimenti MS, Triggianese P, Canofari C, Barbato C, Giannini C, Salandri AG, Nucci C, Perricone R. Take a look at the eyes in Systemic Lupus Erythematosus: A novel point of view. Autoimmun Rev. 2019 Mar; 18 (3): 247–254. DOI: 10.1016/j.autrev.2018.09.011

51. Yusuf IH, Sharma S, Luqmani R, Downes SM. Hydroxychloroquine retinopathy. Eye (Lond). 2017 Jun; 31 (6): 828–845. DOI: 10.1038/eye.2016.298

52. Apostolopoulos D, Morand EF. It hasn't gone away: the problem of glucocorticoid use in lupus remains. Rheumatology (Oxford). 2017 Apr 1; 56 (suppl_1): i114–i122. DOI: 10.1093/rheumatology/kew406