Research progress of serum anti-retinal autoantibodies in retinal diseases_Chinese Journal of Ocular Fundus Diseases

Authors：

Wang Zilin ,  Sun Xiaodong

Department of Ophthalmology, Shanghai General Hospital, Shanghai Jiao Tong University, National Clinical Research Center for Eye Diseases, Shanghai Key Laboratory of Ocular Fundus Diseases, Shanghai Engineering Center for Visual Science and Photomedicine, Shanghai 200080, China;

Corresponding author：

Sun Xiaodong, Email: xdsun@sjtu.edu.cn

Keywords：

Autoimmune; Anti-retinal autoantibody; Retinal disease; Review

DOI：

10.3760/cma.j.cn511434-20220420-00230

Video：

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Abstract Full text Figures/Tables Video References Cited by

Serum anti-retinal autoantibodies (ARA) are a group of autoantibodies that bind to retinal auto-antigens with significant biological importance in pathological processes such as retinal degeneration, inflammatory microenvironment formation, and tissue destruction. In recent years, the expression of serum anti-retinal antibodies has been found to be upregulated in patients with various blinding retinal diseases such as age-related macular degeneration, autoimmune retinopathy, and retinitis pigmentosa, closely correlated with the progression of diseases. However, current researches on ARA are incomplete, lacking animal experiments and large randomized controlled clinical trials. As a result, the exact mechanism of ARA is not well understood. Although several studies have demonstrated that serum ARA has an important diagnostic value in hereditary, autoimmune, and degenerative retinal diseases, there still lacks recognized laboratory tests and laboratory indicators with high specificity and sensitivity. Clinical symptoms should be considered when making definitive diagnosis of the diseases. Therefore, clarifying the mechanisms of ARA in retinal dystrophies provides new ideas in early diagnosis and treatments of retinal diseases, which is clinically and scientifically important for the maintenance of visual functions.

Citation： Wang Zilin, Sun Xiaodong. Research progress of serum anti-retinal autoantibodies in retinal diseases. Chinese Journal of Ocular Fundus Diseases, 2023, 39(9): 779-783. doi: 10.3760/cma.j.cn511434-20220420-00230 Copy

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2.	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.
3.	Ten Berge JC, Fazil Z, van den Born I, et al. Intraocular cytokine profile and autoimmune reactions in retinitis pigmentosa, age-related macular degeneration, glaucoma and cataract[J]. Acta Ophthalmologica, 2019, 97(2): 185-192. DOI: 10.1111/aos.13899.
4.	Wildner G. Tumors, tumor therapies, autoimmunity and the eye[J/OL]. Autoimmun Rev, 2021, 20(9): 102892[2021-07-13]. https://pubmed.ncbi.nlm.nih.gov/34229046/. DOI: 10.1016/j.autrev.2021.102892.
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6.	Chen M, Luo C, Zhao J, et al. Immune regulation in the aging retina[J]. Prog Retin Eye Res, 2019, 69: 159-172. DOI: 10.1016/j.preteyeres.2018.10.003.
7.	Morohoshi K, Goodwin AM, Ohbayashi M, et al. Autoimmunity in retinal degeneration: autoimmune retinopathy and age-related macular degeneration[J]. J Autoimmun, 2009, 33(3-4): 247-254. DOI: 10.1016/j.jaut.2009.09.003.
8.	McMurtrey JJ, Tso MOM. A review of the immunologic findings observed in retinitis pigmentosa[J]. Surv Ophthalmol, 2018, 63(6): 769-781. DOI: 10.1016/j.survophthal.2018.03.002.
9.	Rojas M, Restrepo-Jiménez P, Monsalve DM, et al. Molecular mimicry and autoimmunity[J]. J Autoimmun, 2018, 95: 100-123. DOI: 10.1016/j.jaut.2018.10.012.
10.	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.
11.	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.
12.	Adamus G. Latest updates on antiretinal autoantibodies associated with vision loss and breast cancer[J]. Invest Ophthalmol Vis Sci, 2015, 56(3): 1680-1688. DOI: 10.1167/iovs.14-15739.
13.	Hara M, Martinez-Hernandez E, Ariño H, et al. Clinical and pathogenic significance of IgG, IgA, and IgM antibodies against the NMDA receptor[J/OL]. Neurology, 2018, 90(16): e1386-e1394[2018-03-16]. https://pubmed.ncbi.nlm.nih.gov/29549218/. DOI: 10.1212/WNL.0000000000005329.
14.	Adamus G, Karren L. Autoimmunity against carbonic anhydrase II affects retinal cell functions in autoimmune retinopathy[J]. J Autoimmun, 2009, 32(2): 133-139. DOI: 10.1016/j.jaut.2009.02.001.
15.	Ladewig G, Reinhold U, Thirkill CE, et al. Incidence of antiretinal antibodies in melanoma: screening of 77 serum samples from 51 patients with American Joint Committee on cancer stage I-IV[J]. Br J Dermatol, 2005, 152(5): 931-938. DOI: 10.1111/j.1365-2133.2005.06480.x.
16.	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.
17.	Angeletti A, Migliorini P, Bruschi M, et al. Anti-alpha enolase multi-antibody specificity in human diseases. Clinical significance and molecular mechanisms[J/OL]. Autoimmun Rev, 2021, 20(12): 102977[2021-10-27]. https://pubmed.ncbi.nlm.nih.gov/34718161/. DOI: 10.1016/j.autrev.2021.102977.
18.	Przeździecka-Dołyk J, Brzecka A, Ejma M, et al. Ocular paraneoplastic syndromes[J/OL]. Biomedicines, 2020, 8(11): 490[2020-11-10]. https://pubmed.ncbi.nlm.nih.gov/33182708/. DOI: 10.3390/biomedicines8110490.
19.
20.	Chen JJ, McKeon A, Greenwood TM, et al. Clinical utility of antiretinal antibody testing[J]. JAMA Ophthalmol, 2021, 139(6): 658-662. DOI: 10.1001/jamaophthalmol.2021.0651.
21.	Nikoopour E, Lin CM, Sheskey S, et al. Immune cell infiltration into the eye is controlled by IL-10 in recoverin-Induced autoimmune retinopathy[J]. J Immunol, 2019, 202(4): 1057-1068. DOI: 10.4049/jimmunol.1800574.
22.	Sen HN, Grange L, Akanda M, et al. Autoimmune retinopathy: current concepts and practices (an American ophthalmological society thesis)[J/OL]. Trans Am Ophthalmol Soc, 2018, 115: T8[2017-03-08]. https://pubmed.ncbi.nlm.nih.gov/29576753/.
23.	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.
24.	Adamus G. Autoantibody targets and their cancer relationship in the pathogenicity of paraneoplastic retinopathy[J]. Autoimmun Rev, 2009, 8(5): 410-414. DOI: 10.1016/j.autrev.2009.01.002.
25.	Safadi K, Chowers I, Banin E, et al. Autoimmune retinopathy: clinical, electrophysiological, and immunological features in nine patients with long-term follow-up[J]. Graefe's Arch Clin Exp Ophthalmol, 2022, 260(3): 975-991. DOI: 10.1007/s00417-021-05409-4.
26.	Pawestri AR, Arjkongharn N, Suvannaboon R, et al. Autoantibody profiles and clinical association in Thai patients with autoimmune retinopathy[J/OL]. Sci Rep, 2021, 11(1): 15047[2021-07-22]. https://pubmed.ncbi.nlm.nih.gov/34294798/. DOI: 10.1038/s41598-021-94377-0.
27.	Haapasalo J, Nordfors K, Haapasalo H, et al. The expression of carbonic anhydrases Ⅱ, Ⅸ and Ⅻ in brain tumors[J//OL]. Cancers (Basel), 2020, 12(7): 1723[2020-06-29]. https://pubmed.ncbi.nlm.nih.gov/32610540/. DOI: 10.3390/cancers12071723.
28.	Davoudi S, Ebrahimiadib N, Yasa C, et al. Outcomes in autoimmune retinopathy patients treated with Rituximab[J]. Am J Ophthalmol, 2017, 180: 124-132. DOI: 10.1016/j.ajo.2017.04.019.
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.	Fleckenstein M, Keenan TDL, Guymer RH, et al. Age-related macular degeneration[J]. Nat Rev Dis Primers, 2021, 7(1): 31. DOI: 10.1038/s41572-021-00265-2.
31.	Allingham MJ, Loksztejn A, Cousins SW, et al. Immunological aspects of age-related macular degeneration[J]. Adv Exp Med Biol, 2021, 1256: 143-189. DOI: 10.1007/978-3-030-66014-7_6.
32.	Kubicka-Trząska A, Wilańska J, Romanowska-Dixon B, et al. Circulating anti-retinal antibodies in response to anti-angiogenic therapy in exudative age-related macular degeneration[J/OL]. Acta Ophthalmol, 2014, 92(8): e610-e614[2014-05-06].https://pubmed.ncbi.nlm.nih.gov/24802549/. DOI: 10.1111/aos.12435.
33.	Liu Y, Bell BA, Song Y, et al. Deuterated docosahexaenoic acid protects against oxidative stress and geographic atrophy-like retinal degeneration in a mouse model with iron overload[J/OL]. Aging Cell, 2022: e13579[2022-03-08].https://pubmed.ncbi.nlm.nih.gov/35257475/. DOI: 10.1111/acel.13579.
34.	Gu J, Pauer GJ, Yue X, et al. Assessing susceptibility to age-related macular degeneration with proteomic and genomic biomarkers[J]. Mol Cell Proteomics, 2009, 8(6): 1338-1349. DOI: 10.1074/mcp.M800453-MCP200.
35.	Hollyfield JG, Perez VL, Salomon RG. A hapten generated from an oxidation fragment of docosahexaenoic acid is sufficient to initiate age-related macular degeneration[J]. Mol Neurobiol, 2010, 41(2-3): 290-298. DOI: 10.1007/s12035-010-8110-z.
36.	Morohoshi K, Patel N, Ohbayashi M, et al. Serum autoantibody biomarkers for age-related macular degeneration and possible regulators of neovascularization[J]. Exp Mol Pathol, 2012, 92(1): 64-73. DOI: 10.1016/j.yexmp.2011.09.017.
37.	Adamus G. Can innate and autoimmune reactivity forecast early and advance stages of age-related macular degeneration?[J]. Autoimmun Rev, 2017, 16(3): 231-236. DOI: 10.1016/j.autrev.2017.01.005.
38.	刘红丽, 吴继红. 视网膜色素变性的诊断和治疗进展[J]. 中华眼底病杂志, 2021, 37(11): 896-900. DOI: 10.3760/cma.j.cn511434-20210319-00147.Liu HL, Wu JH. Progress in diagnosis and treatment of retinitis pigmentosa[J]. Chin J Ocul Fundus Dis, 2021, 37(11): 896-900. DOI: 10.3760/cma.j.cn511434-20210319-00147.
39.	Sato T, Nishiguchi KM, Fujita K, et al. Serum anti-recoverin antibodies is found in elderly patients with retinitis pigmentosa and cancer[J/OL]. Acta Ophthalmol, 2020, 98(6): e722-e729[2020-02-11]. https://pubmed.ncbi.nlm.nih.gov/32043815/. DOI: 10.1111/aos.14373.
40.	Heckenlively JR, Jordan BL, Aptsiauri N. Association of antiretinal antibodies and cystoid macular edema in patients with retinitis pigmentosa[J]. Am J Ophthalmol, 1999, 127(5): 565-573. DOI: 10.1016/s0002-9394(98)00446-2.

1. Adamus G. Importance of autoimmune responses in progression of retinal degeneration initiated by gene mutations[J/OL]. Front Med (Lausanne), 2021, 8: 672444[2021-12-02]. https://pubmed.ncbi.nlm.nih.gov/34926479/. DOI: 10.3389/fmed.2021.672444.
2. 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.
3. Ten Berge JC, Fazil Z, van den Born I, et al. Intraocular cytokine profile and autoimmune reactions in retinitis pigmentosa, age-related macular degeneration, glaucoma and cataract[J]. Acta Ophthalmologica, 2019, 97(2): 185-192. DOI: 10.1111/aos.13899.
4. Wildner G. Tumors, tumor therapies, autoimmunity and the eye[J/OL]. Autoimmun Rev, 2021, 20(9): 102892[2021-07-13]. https://pubmed.ncbi.nlm.nih.gov/34229046/. DOI: 10.1016/j.autrev.2021.102892.
5. 陈玥, 姜利斌. 自身免疫性视网膜病变的临床特征与研究进展[J]. 中华眼底病杂志, 2021, 37(11): 901-905. DOI: 10.3760/cma.j.cn511434-20201112-00547.Chen Y, Jiang LB. Clinical features and research progress of autoimmune retinopathy[J]. Chin J Ocul Fundus Dis, 2021, 37(11): 901-905. DOI: 10.3760/cma.j.cn511434-20201112-00547.
6. Chen M, Luo C, Zhao J, et al. Immune regulation in the aging retina[J]. Prog Retin Eye Res, 2019, 69: 159-172. DOI: 10.1016/j.preteyeres.2018.10.003.
7. Morohoshi K, Goodwin AM, Ohbayashi M, et al. Autoimmunity in retinal degeneration: autoimmune retinopathy and age-related macular degeneration[J]. J Autoimmun, 2009, 33(3-4): 247-254. DOI: 10.1016/j.jaut.2009.09.003.
8. McMurtrey JJ, Tso MOM. A review of the immunologic findings observed in retinitis pigmentosa[J]. Surv Ophthalmol, 2018, 63(6): 769-781. DOI: 10.1016/j.survophthal.2018.03.002.
9. Rojas M, Restrepo-Jiménez P, Monsalve DM, et al. Molecular mimicry and autoimmunity[J]. J Autoimmun, 2018, 95: 100-123. DOI: 10.1016/j.jaut.2018.10.012.
10. 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.
11. 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.
12. Adamus G. Latest updates on antiretinal autoantibodies associated with vision loss and breast cancer[J]. Invest Ophthalmol Vis Sci, 2015, 56(3): 1680-1688. DOI: 10.1167/iovs.14-15739.
13. Hara M, Martinez-Hernandez E, Ariño H, et al. Clinical and pathogenic significance of IgG, IgA, and IgM antibodies against the NMDA receptor[J/OL]. Neurology, 2018, 90(16): e1386-e1394[2018-03-16]. https://pubmed.ncbi.nlm.nih.gov/29549218/. DOI: 10.1212/WNL.0000000000005329.
14. Adamus G, Karren L. Autoimmunity against carbonic anhydrase II affects retinal cell functions in autoimmune retinopathy[J]. J Autoimmun, 2009, 32(2): 133-139. DOI: 10.1016/j.jaut.2009.02.001.
15. Ladewig G, Reinhold U, Thirkill CE, et al. Incidence of antiretinal antibodies in melanoma: screening of 77 serum samples from 51 patients with American Joint Committee on cancer stage I-IV[J]. Br J Dermatol, 2005, 152(5): 931-938. DOI: 10.1111/j.1365-2133.2005.06480.x.
16. 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.
17. Angeletti A, Migliorini P, Bruschi M, et al. Anti-alpha enolase multi-antibody specificity in human diseases. Clinical significance and molecular mechanisms[J/OL]. Autoimmun Rev, 2021, 20(12): 102977[2021-10-27]. https://pubmed.ncbi.nlm.nih.gov/34718161/. DOI: 10.1016/j.autrev.2021.102977.
18. Przeździecka-Dołyk J, Brzecka A, Ejma M, et al. Ocular paraneoplastic syndromes[J/OL]. Biomedicines, 2020, 8(11): 490[2020-11-10]. https://pubmed.ncbi.nlm.nih.gov/33182708/. DOI: 10.3390/biomedicines8110490.
19. 10.1016/j.survophthal.2012.09.001.
20. Chen JJ, McKeon A, Greenwood TM, et al. Clinical utility of antiretinal antibody testing[J]. JAMA Ophthalmol, 2021, 139(6): 658-662. DOI: 10.1001/jamaophthalmol.2021.0651.
21. Nikoopour E, Lin CM, Sheskey S, et al. Immune cell infiltration into the eye is controlled by IL-10 in recoverin-Induced autoimmune retinopathy[J]. J Immunol, 2019, 202(4): 1057-1068. DOI: 10.4049/jimmunol.1800574.
22. Sen HN, Grange L, Akanda M, et al. Autoimmune retinopathy: current concepts and practices (an American ophthalmological society thesis)[J/OL]. Trans Am Ophthalmol Soc, 2018, 115: T8[2017-03-08]. https://pubmed.ncbi.nlm.nih.gov/29576753/.
23. 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.
24. Adamus G. Autoantibody targets and their cancer relationship in the pathogenicity of paraneoplastic retinopathy[J]. Autoimmun Rev, 2009, 8(5): 410-414. DOI: 10.1016/j.autrev.2009.01.002.
25. Safadi K, Chowers I, Banin E, et al. Autoimmune retinopathy: clinical, electrophysiological, and immunological features in nine patients with long-term follow-up[J]. Graefe's Arch Clin Exp Ophthalmol, 2022, 260(3): 975-991. DOI: 10.1007/s00417-021-05409-4.
26. Pawestri AR, Arjkongharn N, Suvannaboon R, et al. Autoantibody profiles and clinical association in Thai patients with autoimmune retinopathy[J/OL]. Sci Rep, 2021, 11(1): 15047[2021-07-22]. https://pubmed.ncbi.nlm.nih.gov/34294798/. DOI: 10.1038/s41598-021-94377-0.
27. Haapasalo J, Nordfors K, Haapasalo H, et al. The expression of carbonic anhydrases Ⅱ, Ⅸ and Ⅻ in brain tumors[J//OL]. Cancers (Basel), 2020, 12(7): 1723[2020-06-29]. https://pubmed.ncbi.nlm.nih.gov/32610540/. DOI: 10.3390/cancers12071723.
28. Davoudi S, Ebrahimiadib N, Yasa C, et al. Outcomes in autoimmune retinopathy patients treated with Rituximab[J]. Am J Ophthalmol, 2017, 180: 124-132. DOI: 10.1016/j.ajo.2017.04.019.
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. Fleckenstein M, Keenan TDL, Guymer RH, et al. Age-related macular degeneration[J]. Nat Rev Dis Primers, 2021, 7(1): 31. DOI: 10.1038/s41572-021-00265-2.
31. Allingham MJ, Loksztejn A, Cousins SW, et al. Immunological aspects of age-related macular degeneration[J]. Adv Exp Med Biol, 2021, 1256: 143-189. DOI: 10.1007/978-3-030-66014-7_6.
32. Kubicka-Trząska A, Wilańska J, Romanowska-Dixon B, et al. Circulating anti-retinal antibodies in response to anti-angiogenic therapy in exudative age-related macular degeneration[J/OL]. Acta Ophthalmol, 2014, 92(8): e610-e614[2014-05-06].https://pubmed.ncbi.nlm.nih.gov/24802549/. DOI: 10.1111/aos.12435.
33. Liu Y, Bell BA, Song Y, et al. Deuterated docosahexaenoic acid protects against oxidative stress and geographic atrophy-like retinal degeneration in a mouse model with iron overload[J/OL]. Aging Cell, 2022: e13579[2022-03-08].https://pubmed.ncbi.nlm.nih.gov/35257475/. DOI: 10.1111/acel.13579.
34. Gu J, Pauer GJ, Yue X, et al. Assessing susceptibility to age-related macular degeneration with proteomic and genomic biomarkers[J]. Mol Cell Proteomics, 2009, 8(6): 1338-1349. DOI: 10.1074/mcp.M800453-MCP200.
35. Hollyfield JG, Perez VL, Salomon RG. A hapten generated from an oxidation fragment of docosahexaenoic acid is sufficient to initiate age-related macular degeneration[J]. Mol Neurobiol, 2010, 41(2-3): 290-298. DOI: 10.1007/s12035-010-8110-z.
36. Morohoshi K, Patel N, Ohbayashi M, et al. Serum autoantibody biomarkers for age-related macular degeneration and possible regulators of neovascularization[J]. Exp Mol Pathol, 2012, 92(1): 64-73. DOI: 10.1016/j.yexmp.2011.09.017.
37. Adamus G. Can innate and autoimmune reactivity forecast early and advance stages of age-related macular degeneration?[J]. Autoimmun Rev, 2017, 16(3): 231-236. DOI: 10.1016/j.autrev.2017.01.005.
38. 刘红丽, 吴继红. 视网膜色素变性的诊断和治疗进展[J]. 中华眼底病杂志, 2021, 37(11): 896-900. DOI: 10.3760/cma.j.cn511434-20210319-00147.Liu HL, Wu JH. Progress in diagnosis and treatment of retinitis pigmentosa[J]. Chin J Ocul Fundus Dis, 2021, 37(11): 896-900. DOI: 10.3760/cma.j.cn511434-20210319-00147.
39. Sato T, Nishiguchi KM, Fujita K, et al. Serum anti-recoverin antibodies is found in elderly patients with retinitis pigmentosa and cancer[J/OL]. Acta Ophthalmol, 2020, 98(6): e722-e729[2020-02-11]. https://pubmed.ncbi.nlm.nih.gov/32043815/. DOI: 10.1111/aos.14373.
40. Heckenlively JR, Jordan BL, Aptsiauri N. Association of antiretinal antibodies and cystoid macular edema in patients with retinitis pigmentosa[J]. Am J Ophthalmol, 1999, 127(5): 565-573. DOI: 10.1016/s0002-9394(98)00446-2.

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