Clinical features and research progress of autoimmune retinopathy_Chinese Journal of Ocular Fundus Diseases

Authors：

Chen Yue ,  Jiang Libin

Beijing Tongren Eye Center, Beijing Tongren Hospital, Capital Medical University, Beijing 100730, China;

Corresponding author：

Jiang Libin, Email: jlbjlb@sina.com

Keywords：

Retinal diseases; Immune system diseases; Review

DOI：

10.3760/cma.j.cn511434-20201112-00547

Video：

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Autoimmune retinopathy (AIR) is an umbrella term for a group of rare autoimmune retinal degenerative disease presumably caused by cross-reactivity of serum autoantibodies directed against ratinal antigens, and include cancer-associated retinopathy, melanoma-associated retinopathy and non-paraneoplastic autoimmune retinopathy. Common feature of AIR include progressively painless vision loss with abnormal electrophysiology responses associated with positive anti-retinal antibodies. They present a clinical diagnosis challenge on account of the rare incidence, unobvious clinical symptoms and lack of specific and sensitive biological markers. Early diagnosis and treatment may play a critical role to avoid the irreversible immunological retinal damage.

Citation： Chen Yue, Jiang Libin. Clinical features and research progress of autoimmune retinopathy. Chinese Journal of Ocular Fundus Diseases, 2021, 37(11): 901-905. doi: 10.3760/cma.j.cn511434-20201112-00547 Copy

1.	Grange L, Dalal M, Nussenblatt RB, et al. Autoimmune retinopathy[J]. Am J Ophthalmol, 2014, 157(2): 266-272. DOI: 10.1016/j.ajo.2013.09.019.
2.	Grewal DS, Fishman GA, Jampol LM. Autoimmune retinopathy and antiretinal antibodies: a review[J]. Retina, 2014, 34(5): 827-845. DOI: 10.1097/IAE.0000000000000119.
3.	Comlekoglu DU, Thompson IA, Sen HN. Autoimmune retinopathy[J]. Curr Opin Ophthalmol, 2013, 24(6): 598-605. DOI: 10.1097/ICU.0b013e3283654e1e.
4.	Zeng HY, Liu Q, Peng XY, et al. Detection of serum anti-retinal antibodies in the Chinese patients with presumed autoimmune retinopathy[J]. Graefe's Arch Clin Exp Ophthalmol, 2019, 257(8): 1759-1764. DOI: 10.1007/s00417-019-04359-2.
5.	Patel N, Ohbayashi M, Nugent AK, et al. Circulating anti-retinal antibodies as immune markers in age-related macular degeneration[J]. Immunology, 2005, 115(3): 422-430. DOI: 10.1111/j.1365-2567.2005.02173.x.
6.	Shimazaki K, Jirawuthiworavong GV, Heckenlively JR, et al. Frequency of anti-retinal antibodies in normal human serum[J]. J Neuroophthalmol, 2008, 28(1): 5-11. DOI: 10.1097/WNO.0b013e318167549f.
7.	Thirkill CE, Roth AM, Keltner JL. Cancer-associated retinopathy[J]. Arch Ophthalmol, 1987, 105(3): 372-375. DOI: 10.1001/archopht.1987.01060030092033.
8.	Maeda T, Maeda A, Maruyama I, et al. Mechanisms of photoreceptor cell death in cancer-associated retinopathy[J]. Invest Ophthalmol Vis Sci, 2001, 42(3): 705-712.
9.	Adamus G, Champaigne R, Yang S. Occurrence of major anti-retinal autoantibodies associated with paraneoplastic autoimmune retinopathy[J/OL]. Clin Immunol, 2020, 210: 108317[2019-11-23].https://pubmed.ncbi.nlm.nih.gov/31770612/. DOI: 10.1016/j.clim.2019.108317.
10.	Ohguro H, Maruyama I, Nakazawa M, et al. Antirecoverin antibody in the aqueous humor of a patient with cancer-associated retinopathy[J]. Am J Oph thalm ol, 2002, 134(4): 605-607. DOI: 10.1016/s0002-9394(02)01633-1.
11.	Adamus G, Machnicki M, Elerding H, et al. Antibodies to recoverin induce apoptosis of photoreceptor and bipolar cells in vivo[J]. J Autoimmun, 1998, 11(5): 523-533. DOI: 10.1006/jaut.1998.0221.
12.	Adamus G. Antirecoverin antibodies and autoimmune retinopathy[J]. Arch Ophthalmol, 2000, 118(11): 1577-1578. DOI: 10.1001/archopht.118.11.1577.
13.	Adamus G. Impact of autoantibodies against glycolytic enzymes on pathogenicity of autoimmune retinopathy and other autoimmune disorders[J/OL]. Front Immunol, 2017, 8: 505[2017-04-28].https://pubmed.ncbi.nlm.nih.gov/28503176/. DOI: 10.3389/fimmu.2017.00505.
14.	Adamus G. Autoantibody targets and their cancer relationship in the pathogenicity of paraneoplastic retinopathy[J]. Autoimmun Rev, 2009, 8: 410-414. DOI: 10.1016/j.autrev.2009.01.002.
15.	Adamus G, Brown L, Weleber RG. Molecular biomarkers for autoimmune retinopathies: significance of anti-transducin-alpha autoantibodies[J]. Exp Mol Pathol, 2009, 87: 195-203. DOI: 10.1016/j.yexmp.2009.08.003.
16.	Adamus G, Yang S, Weleber RG. Unique epitopes for carbonic anhydrase Ⅱ autoantibodies related to autoimmune retinopathy and cancer-associated retinopathy[J]. Exp Eye Res, 2016, 147: 161-168. DOI: 10.1016/j.exer.2016.05.012.
17.	Braithwaite T, Holder GE, Lee RW, et al. Diagnostic features of the autoimmune retinopathies[J]. Autoimmun Rev, 2014, 13(4-5): 534-538. DOI: 10.1016/j.autrev.2014.01.039.
18.	Dutta Majumder P, Marchese A, Pichi F, et al. An update on autoimmune retinopathy[J]. Indian J Ophthalmol, 2020, 68(9): 1829-1837. DOI: 10.4103/ijo.IJO_786_20.
19.	Spaide R. Autofluorescence from the outer retina and subretinal space: hypothesis and review[J]. Retina, 2008, 28(1): 5-35. DOI: 10.1097/IAE.0b013e318158eca4.
20.	Honnorat J. Onconeural antibodies are essential to diagnose paraneoplastic neurological syndromes[J]. Acta Neurol Scand Suppl, 2006, 183: 64-68. DOI: 10.1111/j.1600-0404.2006.00620.x.
21.	Rahimy E, Sarraf D. Paraneoplastic and non-paraneoplastic retinopathy and optic neuropathy: evaluation and management[J]. Surv Ophthalmol, 2013, 58(5): 430-458. DOI: 10.1016/j.survophthal.2012.09.001.
22.	Sawyer RA, Selhorst JB, Zimmerman LE, et al. Blindness caused by photoreceptor degeneration as a remote effect of cancer[J]. Am J Ophthalmol, 1976, 81(5): 606-613. DOI: 10.1016/0002-9394(76)90125-2.
23.	Klingele TG, Burde RM, Rappazzo JA, et al. Paraneoplastic retinopathy[J]. J Clin Neuroophthalmol, 1984, 4(4): 239-245.
24.	Berson EL, Lessell S. Paraneoplastic night blindness with malignant melanoma[J]. Am J Ophthalmol, 1988, 106(3): 307-311. DOI: 10.1016/0002-9394(88)90366-2.
25.	Keltner JL, Roth AM, Chang RS. Photoreceptor degeneration. Possible autoimmune disorder[J]. Arch Ophthalmol, 1983, 101(4): 564-569. DOI: 10.1001/archopht.1983.01040010564006.
26.	Finn AP, Thomas AS, Stinnett SS, et al. The role of cystoid macular edema as a marker in the progression of non-paraneoplastic autoimmune retinopathy[J]. Graefe's Arch Clin Exp Ophthalmol, 2018, 256(10): 1867-1873. DOI: 10.1007/s00417-018-4084-8.
27.	Heckenlively JR, Ferreyra HA. Autoimmune retinopathy: a review and summary[J]. Semin Immunopathol, 2008, 30(2): 127-134. DOI: 10.1007/s00281-008-0114-7.
28.	Saito W, Kase S, Ohguro H, et al. Slowly progressive cancer-associated retinopathy[J]. Arch Ophthalmol, 2007, 125(10): 1431-1433. DOI: 10.1001/archopht.125.10.1431.
29.	Fox AR, Gordon LK, Heckenlively JR, et al. Consensus on the diagnosis and management of nonparaneoplastic autoimmune retinopathy using a modified delphi approach[J]. Am J Ophthalmol, 2016, 168: 183-190. DOI: 10.1016/j.ajo.2016.05.013.
30.	Hajali M, Fishman GA. The prevalence of cystoid macular oedema on optical coherence tomography in retinitis pigmentosa patients without cystic changes on fundus examination[J]. Eye (Lond), 2009, 23(4): 915-919. DOI: 10.1038/eye.2008.110.
31.	Tsang SH, Sharma T. Acute zonal occult outer retinopathy (AZOOR) and related diseases[J]. Adv Exp Med Biol, 2018, 1085: 233-237. DOI: 10.1007/978-3-319-95046-4.
32.	Monson DM, Smith JR. Acute zonal occult outer retinopathy[J]. Surv Ophthalmol, 2011, 56(1): 23-35. DOI: 10.1016/j.survophthal.2010.07.004.
33.	Ferreyra HA, Jayasundera T, Khan NW, et al. Management of autoimmune retinopathies with immunosuppression[J]. Arch Ophthalmol, 2009, 127(4): 390-397. DOI: 10.1001/archophthalmol.2009.24.
34.	Guy J, Aptsiauri N. Treatment of paraneoplastic visual loss with intravenous immunoglobulin: report of 3 cases[J]. Arch Ophthalmol, 1999, 117(4): 471-477. DOI: 10.1001/archopht.117.4.471.
35.	Murphy MA, Thirkill CE, Hart WM Jr. Paraneoplastic retinopathy: a novel autoantibody reaction associated with small-cell lung carcinoma[J]. J Neuroophthalmol, 1997, 17(2): 77-83.
36.	Kasongole D, Raval V, Mruthyunjaya P, et al. Multimodal imaging in non-paraneoplastic autoimmune retinopathy[J]. Indian J Ophthalmol, 2019, 67(7): 1171-1173. DOI: 10.4103/ijo.IJO_1416_18.
37.	Maleki A, Lamba N, Ma L, et al. Rituximab as a monotherapy or in combination therapy for the treatment of non-paraneoplastic autoimmune retinopathy[J]. Clin Ophthalmol, 2017, 11: 377-385. DOI: 10.2147/OPTH.S120162.
38.	Boudreault K, Justus S, Sengillo JD, et al. Efficacy of rituximab in non-paraneoplastic autoimmune retinopathy[J/OL]. Orphanet J Rare Dis, 2017, 12(1): 129[2017-07-15]. https://pubmed.ncbi.nlm.nih.gov/28709429/. DOI: 10.1186/s13023-017-0680-7.
39.	Espandar L, O'Brien S, Thirkill C, et al. Successful treatment of cancer-associated retinopathy with alemtuzumab[J]. J Neurooncol, 2007, 83(3): 295-302. DOI: 10.1007/s11060-006-9326-7.
40.	Link B, Schlötzer-Schrehardt U, Jünemann A. Carcinoma-associated retinopathy-an electrophysiological and immunohistochemical correlation[J]. Retina, 2009, 29(1): 69-72. DOI: 10.1097/IAE.0b013e3181853d06.

1. Grange L, Dalal M, Nussenblatt RB, et al. Autoimmune retinopathy[J]. Am J Ophthalmol, 2014, 157(2): 266-272. DOI: 10.1016/j.ajo.2013.09.019.
2. Grewal DS, Fishman GA, Jampol LM. Autoimmune retinopathy and antiretinal antibodies: a review[J]. Retina, 2014, 34(5): 827-845. DOI: 10.1097/IAE.0000000000000119.
3. Comlekoglu DU, Thompson IA, Sen HN. Autoimmune retinopathy[J]. Curr Opin Ophthalmol, 2013, 24(6): 598-605. DOI: 10.1097/ICU.0b013e3283654e1e.
4. Zeng HY, Liu Q, Peng XY, et al. Detection of serum anti-retinal antibodies in the Chinese patients with presumed autoimmune retinopathy[J]. Graefe's Arch Clin Exp Ophthalmol, 2019, 257(8): 1759-1764. DOI: 10.1007/s00417-019-04359-2.
5. Patel N, Ohbayashi M, Nugent AK, et al. Circulating anti-retinal antibodies as immune markers in age-related macular degeneration[J]. Immunology, 2005, 115(3): 422-430. DOI: 10.1111/j.1365-2567.2005.02173.x.
6. Shimazaki K, Jirawuthiworavong GV, Heckenlively JR, et al. Frequency of anti-retinal antibodies in normal human serum[J]. J Neuroophthalmol, 2008, 28(1): 5-11. DOI: 10.1097/WNO.0b013e318167549f.
7. Thirkill CE, Roth AM, Keltner JL. Cancer-associated retinopathy[J]. Arch Ophthalmol, 1987, 105(3): 372-375. DOI: 10.1001/archopht.1987.01060030092033.
8. Maeda T, Maeda A, Maruyama I, et al. Mechanisms of photoreceptor cell death in cancer-associated retinopathy[J]. Invest Ophthalmol Vis Sci, 2001, 42(3): 705-712.
9. Adamus G, Champaigne R, Yang S. Occurrence of major anti-retinal autoantibodies associated with paraneoplastic autoimmune retinopathy[J/OL]. Clin Immunol, 2020, 210: 108317[2019-11-23].https://pubmed.ncbi.nlm.nih.gov/31770612/. DOI: 10.1016/j.clim.2019.108317.
10. Ohguro H, Maruyama I, Nakazawa M, et al. Antirecoverin antibody in the aqueous humor of a patient with cancer-associated retinopathy[J]. Am J Oph thalm ol, 2002, 134(4): 605-607. DOI: 10.1016/s0002-9394(02)01633-1.
11. Adamus G, Machnicki M, Elerding H, et al. Antibodies to recoverin induce apoptosis of photoreceptor and bipolar cells in vivo[J]. J Autoimmun, 1998, 11(5): 523-533. DOI: 10.1006/jaut.1998.0221.
12. Adamus G. Antirecoverin antibodies and autoimmune retinopathy[J]. Arch Ophthalmol, 2000, 118(11): 1577-1578. DOI: 10.1001/archopht.118.11.1577.
13. Adamus G. Impact of autoantibodies against glycolytic enzymes on pathogenicity of autoimmune retinopathy and other autoimmune disorders[J/OL]. Front Immunol, 2017, 8: 505[2017-04-28].https://pubmed.ncbi.nlm.nih.gov/28503176/. DOI: 10.3389/fimmu.2017.00505.
14. Adamus G. Autoantibody targets and their cancer relationship in the pathogenicity of paraneoplastic retinopathy[J]. Autoimmun Rev, 2009, 8: 410-414. DOI: 10.1016/j.autrev.2009.01.002.
15. Adamus G, Brown L, Weleber RG. Molecular biomarkers for autoimmune retinopathies: significance of anti-transducin-alpha autoantibodies[J]. Exp Mol Pathol, 2009, 87: 195-203. DOI: 10.1016/j.yexmp.2009.08.003.
16. Adamus G, Yang S, Weleber RG. Unique epitopes for carbonic anhydrase Ⅱ autoantibodies related to autoimmune retinopathy and cancer-associated retinopathy[J]. Exp Eye Res, 2016, 147: 161-168. DOI: 10.1016/j.exer.2016.05.012.
17. Braithwaite T, Holder GE, Lee RW, et al. Diagnostic features of the autoimmune retinopathies[J]. Autoimmun Rev, 2014, 13(4-5): 534-538. DOI: 10.1016/j.autrev.2014.01.039.
18. Dutta Majumder P, Marchese A, Pichi F, et al. An update on autoimmune retinopathy[J]. Indian J Ophthalmol, 2020, 68(9): 1829-1837. DOI: 10.4103/ijo.IJO_786_20.
19. Spaide R. Autofluorescence from the outer retina and subretinal space: hypothesis and review[J]. Retina, 2008, 28(1): 5-35. DOI: 10.1097/IAE.0b013e318158eca4.
20. Honnorat J. Onconeural antibodies are essential to diagnose paraneoplastic neurological syndromes[J]. Acta Neurol Scand Suppl, 2006, 183: 64-68. DOI: 10.1111/j.1600-0404.2006.00620.x.
21. Rahimy E, Sarraf D. Paraneoplastic and non-paraneoplastic retinopathy and optic neuropathy: evaluation and management[J]. Surv Ophthalmol, 2013, 58(5): 430-458. DOI: 10.1016/j.survophthal.2012.09.001.
22. Sawyer RA, Selhorst JB, Zimmerman LE, et al. Blindness caused by photoreceptor degeneration as a remote effect of cancer[J]. Am J Ophthalmol, 1976, 81(5): 606-613. DOI: 10.1016/0002-9394(76)90125-2.
23. Klingele TG, Burde RM, Rappazzo JA, et al. Paraneoplastic retinopathy[J]. J Clin Neuroophthalmol, 1984, 4(4): 239-245.
24. Berson EL, Lessell S. Paraneoplastic night blindness with malignant melanoma[J]. Am J Ophthalmol, 1988, 106(3): 307-311. DOI: 10.1016/0002-9394(88)90366-2.
25. Keltner JL, Roth AM, Chang RS. Photoreceptor degeneration. Possible autoimmune disorder[J]. Arch Ophthalmol, 1983, 101(4): 564-569. DOI: 10.1001/archopht.1983.01040010564006.
26. Finn AP, Thomas AS, Stinnett SS, et al. The role of cystoid macular edema as a marker in the progression of non-paraneoplastic autoimmune retinopathy[J]. Graefe's Arch Clin Exp Ophthalmol, 2018, 256(10): 1867-1873. DOI: 10.1007/s00417-018-4084-8.
27. Heckenlively JR, Ferreyra HA. Autoimmune retinopathy: a review and summary[J]. Semin Immunopathol, 2008, 30(2): 127-134. DOI: 10.1007/s00281-008-0114-7.
28. Saito W, Kase S, Ohguro H, et al. Slowly progressive cancer-associated retinopathy[J]. Arch Ophthalmol, 2007, 125(10): 1431-1433. DOI: 10.1001/archopht.125.10.1431.
29. Fox AR, Gordon LK, Heckenlively JR, et al. Consensus on the diagnosis and management of nonparaneoplastic autoimmune retinopathy using a modified delphi approach[J]. Am J Ophthalmol, 2016, 168: 183-190. DOI: 10.1016/j.ajo.2016.05.013.
30. Hajali M, Fishman GA. The prevalence of cystoid macular oedema on optical coherence tomography in retinitis pigmentosa patients without cystic changes on fundus examination[J]. Eye (Lond), 2009, 23(4): 915-919. DOI: 10.1038/eye.2008.110.
31. Tsang SH, Sharma T. Acute zonal occult outer retinopathy (AZOOR) and related diseases[J]. Adv Exp Med Biol, 2018, 1085: 233-237. DOI: 10.1007/978-3-319-95046-4.
32. Monson DM, Smith JR. Acute zonal occult outer retinopathy[J]. Surv Ophthalmol, 2011, 56(1): 23-35. DOI: 10.1016/j.survophthal.2010.07.004.
33. Ferreyra HA, Jayasundera T, Khan NW, et al. Management of autoimmune retinopathies with immunosuppression[J]. Arch Ophthalmol, 2009, 127(4): 390-397. DOI: 10.1001/archophthalmol.2009.24.
34. Guy J, Aptsiauri N. Treatment of paraneoplastic visual loss with intravenous immunoglobulin: report of 3 cases[J]. Arch Ophthalmol, 1999, 117(4): 471-477. DOI: 10.1001/archopht.117.4.471.
35. Murphy MA, Thirkill CE, Hart WM Jr. Paraneoplastic retinopathy: a novel autoantibody reaction associated with small-cell lung carcinoma[J]. J Neuroophthalmol, 1997, 17(2): 77-83.
36. Kasongole D, Raval V, Mruthyunjaya P, et al. Multimodal imaging in non-paraneoplastic autoimmune retinopathy[J]. Indian J Ophthalmol, 2019, 67(7): 1171-1173. DOI: 10.4103/ijo.IJO_1416_18.
37. Maleki A, Lamba N, Ma L, et al. Rituximab as a monotherapy or in combination therapy for the treatment of non-paraneoplastic autoimmune retinopathy[J]. Clin Ophthalmol, 2017, 11: 377-385. DOI: 10.2147/OPTH.S120162.
38. Boudreault K, Justus S, Sengillo JD, et al. Efficacy of rituximab in non-paraneoplastic autoimmune retinopathy[J/OL]. Orphanet J Rare Dis, 2017, 12(1): 129[2017-07-15]. https://pubmed.ncbi.nlm.nih.gov/28709429/. DOI: 10.1186/s13023-017-0680-7.
39. Espandar L, O'Brien S, Thirkill C, et al. Successful treatment of cancer-associated retinopathy with alemtuzumab[J]. J Neurooncol, 2007, 83(3): 295-302. DOI: 10.1007/s11060-006-9326-7.
40. Link B, Schlötzer-Schrehardt U, Jünemann A. Carcinoma-associated retinopathy-an electrophysiological and immunohistochemical correlation[J]. Retina, 2009, 29(1): 69-72. DOI: 10.1097/IAE.0b013e3181853d06.

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