The role of oxidative stress in retinal diseases Review article
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Published:
Oct 3, 2024
Keywords:
stres oksydacyjny, antyoksydanty, siatkówka, zwyrodnienie plamki związane z wiekiem, retinopatia cukrzycowa
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Abstract
Oxidative stress plays a key role in the pathogenesis of many diseases associated with aging, including atherosclerosis, neurodegenerative diseases, diabetes, and retinal diseases. The retina is a tissue that is particularly susceptible to the adverse effects of oxidative stress, as it is characterized by high metabolic rate and high oxygen consumption compared to other body tissues. This review article discusses the relationship between the cellular mechanisms of impaired prooxidant-antioxidant homeostasis and the development of age-related macular degeneration and diabetic retinopathy. Natural defense mechanisms of maintaining redox homeostasis and therapeutic strategies based on the use of antioxidants are also described.
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1.
Nowińska A. The role of oxidative stress in retinal diseases. Ophthatherapy [Internet]. 2024Oct.3 [cited 2024Oct.26];11(2):160-8. Available from: https://journalsmededu.pl/index.php/ophthatherapy/article/view/3122
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Address reprint requests to: Medical Education, Marcin Kuźma (marcin.kuzma@mededu.pl)
References
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4. Guymer RH, Campbell TG. Age-related macular degeneration. Lancet. 2023; 401: 1459-72. https://doi.org/10.1016/S0140-6736(22)02609-5.
5. Jomova K, Alomar SY, Alwasel SH et al. Several lines of antioxidant defense against oxidative stress: antioxidant enzymes, nanomaterials with multiple enzyme-mimicking activities, and low-molecular-weight antioxidants. Arch Toxicol. 2024; 98: 1323-67. https://doi.org/10.1007/s00204-024-03696-4.
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7. Zamora-Ros R, Forouhi NG, Sharp SJ et al. The association between dietary flavonoid and lignan intakes and incident type 2 diabetes in European populations: the EPIC-InterAct study. Diabetes Care. 2013; 36: 3961-70. https://doi.org/10.2337/dc13-0877.
8. Kaulmann A, Bohn T. Carotenoids, inflammation, and oxidative stress – implications of cellular signaling pathways and relation to chronic disease prevention. Nutr Res. 2014; 34: 907-29. https://doi.org/10.1016/j.nutres.2014.07.010.
9. Sung L-C, Chao H-H, Chen C-H et al. Lycopene inhibits cyclic strain-induced endothelin-1 expression through the suppression of reactive oxygen species generation and induction of heme oxygenase-1 in human umbilical vein endothelial cells. Clin Exp Pharmacol Physiol. 2015; 42: 632-9. https://doi.org/10.1111/1440-1681.12412.
10. Krinsky NI, Landrum JT, Bone RA. Biologic mechanisms of the protective role of lutein and zeaxanthin in the eye. Annu Rev Nutr. 2003; 23: 171-201. https://doi.org/10.1146/annurev.nutr.23.011702.073307.
11. Wei D, Qu C, Zhao N et al. The significance of precisely regulating heme oxygenase-1 expression: Another avenue for treating age-related ocular disease? Ageing Res Rev. 2024; 97: 102308. https://doi.org/10.1016/j.arr.2024.102308.
12. Vyawahare H, Shinde P. Age-Related Macular Degeneration: Epidemiology, Pathophysiology, Diagnosis, and Treatment. Cureus. 2022; 14(9): e29583. https://doi.org/10.7759/cureus.29583.
13. Wong WL, Su X, Li X et al. Global prevalence of age-related macular degeneration and disease burden projection for 2020 and 2040: a systematic review and meta-analysis. Lancet Glob Heal. 2014; 2: e106-16. https://doi.org/10.1016/S2214-109X(13)70145-1.
14. Deng Y, Qiao L, Du M et al. Age-related macular degeneration: Epidemiology, genetics, pathophysiology, diagnosis, and targeted therapy. Genes Dis. 2022; 9: 62-79. https://doi.org/10.1016/j.gendis.2021.02.009.
15. Teo ZL, Tham YC, Yu M et al. Global Prevalence of Diabetic Retinopathy and Projection of Burden through 2045: Systematic Review and Meta-analysis. Ophthalmology. 2021 ;128: 1580-91. https://doi.org/10.1016/j.ophtha.2021.04.027.
16. Klein R, Klein BEK, Moss SE et al. The Wisconsin Epidemiologic Study of Diabetic Retinopathy: XIV. Ten-Year Incidence and Progression of Diabetic Retinopathy. Arch Ophthalmol. 1994; 112: 1217-28. https://doi.org/10.1001/archopht.1994.01090210105023.
17. Klein R, Klein BEK, Moss SE et al. The Wisconsin Epidemiologic Study of Diabetic Retinopathy: III. Prevalence and Risk of Diabetic Retinopathy When Age at Diagnosis is 30 or More Years. Arch Ophthalmol. 1984; 102: 527-32. https://doi.org/10.1001/archopht.1984.01040030405011.
18. Mohamed Q, Gillies MC, Wong TY. Management of Diabetic Retinopathy. JAMA. 2007; 298: 902. https://doi.org/10.1001/jama.298.8.902.
19. Datta S, Cano M, Ebrahimi K et al. The impact of oxidative stress and inflammation on RPE degeneration in non-neovascular AMD. Prog Retin Eye Res. 2017; 60: 201-18. https://doi.org/10.1016/j.preteyeres.2017.03.002.
20. Liu D, Liu Z, Liao H et al. Ferroptosis as a potential therapeutic target for age-related macular degeneration. Drug Discov Today. 2024; 29: 103920. https://doi.org/10.1016/j.drudis.2024.103920.
21. Tang D, Chen X, Kang R et al. Ferroptosis: molecular mechanisms and health implications. Cell Res. 2021; 31: 107-25. https://doi.org/10.1038/s41422-020-00441-1.
22. Feher J, Kovacs I, Artico M et al. Mitochondrial alterations of retinal pigment epithelium in age-related macular degeneration. Neurobiol Aging. 2006; 27: 983-93. https://doi.org/10.1016/j.neurobiolaging.2005.05.012.
23. Somasundaran S, Constable IJ, Mellough CB et al. Retinal pigment epithelium and age-related macular degeneration: A review of major disease mechanisms. Clin Experiment Ophthalmol. 2020; 48: 1043-56. https://doi.org/10.1111/ceo.13834.
24. Karunadharma PP, Nordgaard CL, Olsen TW et al. Mitochondrial DNA damage as a potential mechanism for age-related macular degeneration. Invest Ophthalmol Vis Sci. 2010; 51: 5470-9. https://doi.org/10.1167/iovs.10-5429.
25. Haydinger CD, Oliver GF, Ashander LM et al. Oxidative Stress and Its Regulation in Diabetic Retinopathy. Antioxidants. 2023; 12. https://doi.org/10.3390/antiox12081649.
26. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature. 2001; 414: 813-20. https://doi.org/10.1038/414813a .
27. Feng Y, von Hagen F, Lin J et al. Incipient diabetic retinopathy - insights from an experimental model. Ophthalmol J Int d’ophtalmologie Int J Ophthalmol Zeitschrift Fur Augenheilkd. 2007; 221: 269-74. https://doi.org/10.1159/000101930.
28. Tang Q, Buonfiglio F, Böhm EW et al. Diabetic Retinopathy: New Treatment Approaches Targeting Redox and Immune Mechanisms. Antioxidants. 2024; 13. https://doi.org/10.3390/antiox13050594.
29. Dong H, Sun Y, Nie L et al. Metabolic memory: mechanisms and diseases. Signal Transduct Target Ther. 2024; 9: 38. https://doi.org/10.1038/s41392-024-01755-x .
30. White NH, Sun W, Cleary PA et al. Prolonged effect of intensive therapy on the risk of retinopathy complications in patients with type 1 diabetes mellitus: 10 years after the Diabetes Control and Complications Trial. Arch Ophthalmol. 2008; 126: 1707-15. https://doi.org/10.1001/archopht.126.12.1707.
31. Age-Related Eye Disease Study Research Group. Risk factors associated with age-related macular degeneration. Ophthalmology. 2000; 107: 2224-32. https://doi.org/10.1016/S0161-6420(00)00409-7.
32. Sangiovanni JP, Agrón E, Meleth AD et al. {omega}-3 Long-chain polyunsaturated fatty acid intake and 12-y incidence of neovascular age-related macular degeneration and central geographic atrophy: AREDS report 30, a prospective cohort study from the Age-Related Eye Disease Study. Am J Clin Nutr. 2009; 90: 1601-7. https://doi.org/10.3945/ajcn.2009.27594.
33. Evans JR, Lawrenson JG. Antioxidant vitamin and mineral supplements for slowing the progression of age-related macular degeneration. Cochrane Database Syst Rev. 2017; 7: CD000254. https://doi.org/10.1002/14651858.CD000254.pub4.
34. Evans JR, Lawrenson JG. Antioxidant vitamin and mineral supplements for slowing the progression of age-related macular degeneration. Cochrane Database Syst Rev. 2023; 2023: CD000254. https://doi.org/10.1002/14651858.CD000254.pub5.
35. Christen WG, Glynn RJ, Chew EY et al. Folic acid, pyridoxine, and cyanocobalamin combination treatment and age-related macular degeneration in women: the Women’s Antioxidant and Folic Acid Cardiovascular Study. Arch Intern Med. 2009; 169: 335-41. https://doi.org/10.1001/archinternmed.2008.574.
36. Parekh N, Voland RP, Moeller SM et al. Association between dietary fat intake and age-related macular degeneration in the Carotenoids in Age-Related Eye Disease Study (CAREDS): an ancillary study of the Women’s Health Initiative. Arch Ophthalmol. 2009; 127: 1483-93. https://doi.org/10.1001/archophthalmol.2009.130.
37. Meyers KJ, Mares JA, Igo RPJ et al. Genetic evidence for role of carotenoids in age-related macular degeneration in the Carotenoids in Age-Related Eye Disease Study (CAREDS). Invest Ophthalmol Vis Sci. 2014; 55: 587-99. https://doi.org/10.1167/iovs.13-13216.
38. Moeller SM, Parekh N, Tinker L et al. Associations between intermediate age-related macular degeneration and lutein and zeaxanthin in the Carotenoids in Age-related Eye Disease Study (CAREDS): ancillary study of the Women’s Health Initiative. Arch Ophthalmol. 2006; 124: 1151-62. https://doi.org/10.1001/archopht.124.8.1151.
39. Bryl A, Falkowski M, Zorena K et al. The Role of Resveratrol in Eye Diseases-A Review of the Literature. Nutrients. 2022; 14. https://doi.org/10.3390/nu14142974.
40. Kabiesz A. Resveratrol and curcumin against diabetic retinopathy. Better together than apart. OphthaTherapy. 2023; 10: 284-8. https://doi.org/10.24292/01.OT.211223.
41. Popescu M, Bogdan C, Pintea A et al. Antiangiogenic cytokines as potential new therapeutic targets for resveratrol in diabetic retinopathy. Drug Des Devel Ther. 2018; 12: 1985-96. https://doi.org/10.2147/DDDT.S156941.
42. Fanaro GB, Marques MR, Calaza K da C et al. New Insights on Dietary Polyphenols for the Management of Oxidative Stress and Neuroinflammation in Diabetic Retinopathy. Antioxidants. 2023; 12. https://doi.org/10.3390/antiox12061237.
43. Bucolo C, Drago F, Maisto R et al. Curcumin prevents high glucose damage in retinal pigment epithelial cells through ERK1/2-mediated activation of the Nrf2/HO-1 pathway. J Cell Physiol. 2019; 234: 17295-304. https://doi.org/10.1002/jcp.28347.
44. Alfonso-Muñoz EA, Burggraaf-Sánchez de Las Matas R, Mataix Boronat J et al. Role of Oral Antioxidant Supplementation in the Current Management of Diabetic Retinopathy. Int J Mol Sci. 2021; 22. https://doi.org/10.3390/ijms22084020.
45. Inchingolo AD, Inchingolo AM, Malcangi G et al. Effects of Resveratrol, Curcumin and Quercetin Supplementation on Bone Metabolism- A Systematic Review. Nutrients. 2022; 14. https://doi.org/10.3390/nu14173519.
46. Rugină D, Ghiman R, Focșan M et al. Resveratrol-delivery vehicle with anti-VEGF activity carried to human retinal pigmented epithelial cells exposed to high-glucose induced conditions. Colloids Surf B Biointerfaces. 2019; 181: 66-75. https://doi.org/10.1016/j.colsurfb.2019.04.022.
47. Dong Y, Wan G, Yan P et al. Fabrication of resveratrol coated gold nanoparticles and investigation of their effect on diabetic retinopathy in streptozotocin induced diabetic rats. J Photochem Photobiol B. 2019; 195: 51-7. https://doi.org/10.1016/j.jphotobiol.2019.04.012.
48. Robles-Rivera RR, Castellanos-González JA, Olvera-Montaño C et al. Adjuvant Therapies in Diabetic Retinopathy as an Early Approach to Delay Its Progression: The Importance of Oxidative Stress and Inflammation. Oxid Med Cell Longev. 2020; 2020: 3096470. https://doi.org/10.1155/2020/3096470.
49. Garcia-Medina JJ, Pinazo-Duran MD, Garcia-Medina M et al. A 5-year follow-up of antioxidant supplementation in type 2 diabetic retinopathy. Eur J Ophthalmol. 2011; 21: 637-43. https://doi.org/10.5301/EJO.2010.6212.
50. Chous AP, Richer SP, Gerson JD et al. The Diabetes Visual Function Supplement Study (DiVFuSS). Br J Ophthalmol. 2016; 100: 227-34. https://doi.org/10.1136/bjophthalmol-2014-306534.
51. Lafuente M, Ortín L, Argente M et al. Three-year outcomes in a randomized single-blind controlled trial of intravitreal ranibizumab and oral supplementation with docosahexaenoic acid and antioxidants for diabetic macular edema. Retina. 2019; 39: 1083-90. https://doi.org/10.1097/IAE.0000000000002114.
2. Igielska-Kalwat J, Gościańska J, Nowak I. Carotenoids as natural antioxidants. Postepy Hig Med Dosw. 2015; 69: 418-28. https://doi.org/10.5604/17322693.1148335.
3. Kushwah N, Bora K, Maurya M et al. Oxidative Stress and Antioxidants in Age-Related Macular Degeneration. Antioxidants. 2023; 12. https://doi.org/10.3390/antiox12071379.
4. Guymer RH, Campbell TG. Age-related macular degeneration. Lancet. 2023; 401: 1459-72. https://doi.org/10.1016/S0140-6736(22)02609-5.
5. Jomova K, Alomar SY, Alwasel SH et al. Several lines of antioxidant defense against oxidative stress: antioxidant enzymes, nanomaterials with multiple enzyme-mimicking activities, and low-molecular-weight antioxidants. Arch Toxicol. 2024; 98: 1323-67. https://doi.org/10.1007/s00204-024-03696-4.
6. Jarosz M, Rychlik E, Stoś K et al. (ed). Normy żywienia dla populacji Polski i ich zastosowanie. Narodowy Instytut Zdrowia Publicznego, Warszawa 2020.
7. Zamora-Ros R, Forouhi NG, Sharp SJ et al. The association between dietary flavonoid and lignan intakes and incident type 2 diabetes in European populations: the EPIC-InterAct study. Diabetes Care. 2013; 36: 3961-70. https://doi.org/10.2337/dc13-0877.
8. Kaulmann A, Bohn T. Carotenoids, inflammation, and oxidative stress – implications of cellular signaling pathways and relation to chronic disease prevention. Nutr Res. 2014; 34: 907-29. https://doi.org/10.1016/j.nutres.2014.07.010.
9. Sung L-C, Chao H-H, Chen C-H et al. Lycopene inhibits cyclic strain-induced endothelin-1 expression through the suppression of reactive oxygen species generation and induction of heme oxygenase-1 in human umbilical vein endothelial cells. Clin Exp Pharmacol Physiol. 2015; 42: 632-9. https://doi.org/10.1111/1440-1681.12412.
10. Krinsky NI, Landrum JT, Bone RA. Biologic mechanisms of the protective role of lutein and zeaxanthin in the eye. Annu Rev Nutr. 2003; 23: 171-201. https://doi.org/10.1146/annurev.nutr.23.011702.073307.
11. Wei D, Qu C, Zhao N et al. The significance of precisely regulating heme oxygenase-1 expression: Another avenue for treating age-related ocular disease? Ageing Res Rev. 2024; 97: 102308. https://doi.org/10.1016/j.arr.2024.102308.
12. Vyawahare H, Shinde P. Age-Related Macular Degeneration: Epidemiology, Pathophysiology, Diagnosis, and Treatment. Cureus. 2022; 14(9): e29583. https://doi.org/10.7759/cureus.29583.
13. Wong WL, Su X, Li X et al. Global prevalence of age-related macular degeneration and disease burden projection for 2020 and 2040: a systematic review and meta-analysis. Lancet Glob Heal. 2014; 2: e106-16. https://doi.org/10.1016/S2214-109X(13)70145-1.
14. Deng Y, Qiao L, Du M et al. Age-related macular degeneration: Epidemiology, genetics, pathophysiology, diagnosis, and targeted therapy. Genes Dis. 2022; 9: 62-79. https://doi.org/10.1016/j.gendis.2021.02.009.
15. Teo ZL, Tham YC, Yu M et al. Global Prevalence of Diabetic Retinopathy and Projection of Burden through 2045: Systematic Review and Meta-analysis. Ophthalmology. 2021 ;128: 1580-91. https://doi.org/10.1016/j.ophtha.2021.04.027.
16. Klein R, Klein BEK, Moss SE et al. The Wisconsin Epidemiologic Study of Diabetic Retinopathy: XIV. Ten-Year Incidence and Progression of Diabetic Retinopathy. Arch Ophthalmol. 1994; 112: 1217-28. https://doi.org/10.1001/archopht.1994.01090210105023.
17. Klein R, Klein BEK, Moss SE et al. The Wisconsin Epidemiologic Study of Diabetic Retinopathy: III. Prevalence and Risk of Diabetic Retinopathy When Age at Diagnosis is 30 or More Years. Arch Ophthalmol. 1984; 102: 527-32. https://doi.org/10.1001/archopht.1984.01040030405011.
18. Mohamed Q, Gillies MC, Wong TY. Management of Diabetic Retinopathy. JAMA. 2007; 298: 902. https://doi.org/10.1001/jama.298.8.902.
19. Datta S, Cano M, Ebrahimi K et al. The impact of oxidative stress and inflammation on RPE degeneration in non-neovascular AMD. Prog Retin Eye Res. 2017; 60: 201-18. https://doi.org/10.1016/j.preteyeres.2017.03.002.
20. Liu D, Liu Z, Liao H et al. Ferroptosis as a potential therapeutic target for age-related macular degeneration. Drug Discov Today. 2024; 29: 103920. https://doi.org/10.1016/j.drudis.2024.103920.
21. Tang D, Chen X, Kang R et al. Ferroptosis: molecular mechanisms and health implications. Cell Res. 2021; 31: 107-25. https://doi.org/10.1038/s41422-020-00441-1.
22. Feher J, Kovacs I, Artico M et al. Mitochondrial alterations of retinal pigment epithelium in age-related macular degeneration. Neurobiol Aging. 2006; 27: 983-93. https://doi.org/10.1016/j.neurobiolaging.2005.05.012.
23. Somasundaran S, Constable IJ, Mellough CB et al. Retinal pigment epithelium and age-related macular degeneration: A review of major disease mechanisms. Clin Experiment Ophthalmol. 2020; 48: 1043-56. https://doi.org/10.1111/ceo.13834.
24. Karunadharma PP, Nordgaard CL, Olsen TW et al. Mitochondrial DNA damage as a potential mechanism for age-related macular degeneration. Invest Ophthalmol Vis Sci. 2010; 51: 5470-9. https://doi.org/10.1167/iovs.10-5429.
25. Haydinger CD, Oliver GF, Ashander LM et al. Oxidative Stress and Its Regulation in Diabetic Retinopathy. Antioxidants. 2023; 12. https://doi.org/10.3390/antiox12081649.
26. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature. 2001; 414: 813-20. https://doi.org/10.1038/414813a .
27. Feng Y, von Hagen F, Lin J et al. Incipient diabetic retinopathy - insights from an experimental model. Ophthalmol J Int d’ophtalmologie Int J Ophthalmol Zeitschrift Fur Augenheilkd. 2007; 221: 269-74. https://doi.org/10.1159/000101930.
28. Tang Q, Buonfiglio F, Böhm EW et al. Diabetic Retinopathy: New Treatment Approaches Targeting Redox and Immune Mechanisms. Antioxidants. 2024; 13. https://doi.org/10.3390/antiox13050594.
29. Dong H, Sun Y, Nie L et al. Metabolic memory: mechanisms and diseases. Signal Transduct Target Ther. 2024; 9: 38. https://doi.org/10.1038/s41392-024-01755-x .
30. White NH, Sun W, Cleary PA et al. Prolonged effect of intensive therapy on the risk of retinopathy complications in patients with type 1 diabetes mellitus: 10 years after the Diabetes Control and Complications Trial. Arch Ophthalmol. 2008; 126: 1707-15. https://doi.org/10.1001/archopht.126.12.1707.
31. Age-Related Eye Disease Study Research Group. Risk factors associated with age-related macular degeneration. Ophthalmology. 2000; 107: 2224-32. https://doi.org/10.1016/S0161-6420(00)00409-7.
32. Sangiovanni JP, Agrón E, Meleth AD et al. {omega}-3 Long-chain polyunsaturated fatty acid intake and 12-y incidence of neovascular age-related macular degeneration and central geographic atrophy: AREDS report 30, a prospective cohort study from the Age-Related Eye Disease Study. Am J Clin Nutr. 2009; 90: 1601-7. https://doi.org/10.3945/ajcn.2009.27594.
33. Evans JR, Lawrenson JG. Antioxidant vitamin and mineral supplements for slowing the progression of age-related macular degeneration. Cochrane Database Syst Rev. 2017; 7: CD000254. https://doi.org/10.1002/14651858.CD000254.pub4.
34. Evans JR, Lawrenson JG. Antioxidant vitamin and mineral supplements for slowing the progression of age-related macular degeneration. Cochrane Database Syst Rev. 2023; 2023: CD000254. https://doi.org/10.1002/14651858.CD000254.pub5.
35. Christen WG, Glynn RJ, Chew EY et al. Folic acid, pyridoxine, and cyanocobalamin combination treatment and age-related macular degeneration in women: the Women’s Antioxidant and Folic Acid Cardiovascular Study. Arch Intern Med. 2009; 169: 335-41. https://doi.org/10.1001/archinternmed.2008.574.
36. Parekh N, Voland RP, Moeller SM et al. Association between dietary fat intake and age-related macular degeneration in the Carotenoids in Age-Related Eye Disease Study (CAREDS): an ancillary study of the Women’s Health Initiative. Arch Ophthalmol. 2009; 127: 1483-93. https://doi.org/10.1001/archophthalmol.2009.130.
37. Meyers KJ, Mares JA, Igo RPJ et al. Genetic evidence for role of carotenoids in age-related macular degeneration in the Carotenoids in Age-Related Eye Disease Study (CAREDS). Invest Ophthalmol Vis Sci. 2014; 55: 587-99. https://doi.org/10.1167/iovs.13-13216.
38. Moeller SM, Parekh N, Tinker L et al. Associations between intermediate age-related macular degeneration and lutein and zeaxanthin in the Carotenoids in Age-related Eye Disease Study (CAREDS): ancillary study of the Women’s Health Initiative. Arch Ophthalmol. 2006; 124: 1151-62. https://doi.org/10.1001/archopht.124.8.1151.
39. Bryl A, Falkowski M, Zorena K et al. The Role of Resveratrol in Eye Diseases-A Review of the Literature. Nutrients. 2022; 14. https://doi.org/10.3390/nu14142974.
40. Kabiesz A. Resveratrol and curcumin against diabetic retinopathy. Better together than apart. OphthaTherapy. 2023; 10: 284-8. https://doi.org/10.24292/01.OT.211223.
41. Popescu M, Bogdan C, Pintea A et al. Antiangiogenic cytokines as potential new therapeutic targets for resveratrol in diabetic retinopathy. Drug Des Devel Ther. 2018; 12: 1985-96. https://doi.org/10.2147/DDDT.S156941.
42. Fanaro GB, Marques MR, Calaza K da C et al. New Insights on Dietary Polyphenols for the Management of Oxidative Stress and Neuroinflammation in Diabetic Retinopathy. Antioxidants. 2023; 12. https://doi.org/10.3390/antiox12061237.
43. Bucolo C, Drago F, Maisto R et al. Curcumin prevents high glucose damage in retinal pigment epithelial cells through ERK1/2-mediated activation of the Nrf2/HO-1 pathway. J Cell Physiol. 2019; 234: 17295-304. https://doi.org/10.1002/jcp.28347.
44. Alfonso-Muñoz EA, Burggraaf-Sánchez de Las Matas R, Mataix Boronat J et al. Role of Oral Antioxidant Supplementation in the Current Management of Diabetic Retinopathy. Int J Mol Sci. 2021; 22. https://doi.org/10.3390/ijms22084020.
45. Inchingolo AD, Inchingolo AM, Malcangi G et al. Effects of Resveratrol, Curcumin and Quercetin Supplementation on Bone Metabolism- A Systematic Review. Nutrients. 2022; 14. https://doi.org/10.3390/nu14173519.
46. Rugină D, Ghiman R, Focșan M et al. Resveratrol-delivery vehicle with anti-VEGF activity carried to human retinal pigmented epithelial cells exposed to high-glucose induced conditions. Colloids Surf B Biointerfaces. 2019; 181: 66-75. https://doi.org/10.1016/j.colsurfb.2019.04.022.
47. Dong Y, Wan G, Yan P et al. Fabrication of resveratrol coated gold nanoparticles and investigation of their effect on diabetic retinopathy in streptozotocin induced diabetic rats. J Photochem Photobiol B. 2019; 195: 51-7. https://doi.org/10.1016/j.jphotobiol.2019.04.012.
48. Robles-Rivera RR, Castellanos-González JA, Olvera-Montaño C et al. Adjuvant Therapies in Diabetic Retinopathy as an Early Approach to Delay Its Progression: The Importance of Oxidative Stress and Inflammation. Oxid Med Cell Longev. 2020; 2020: 3096470. https://doi.org/10.1155/2020/3096470.
49. Garcia-Medina JJ, Pinazo-Duran MD, Garcia-Medina M et al. A 5-year follow-up of antioxidant supplementation in type 2 diabetic retinopathy. Eur J Ophthalmol. 2011; 21: 637-43. https://doi.org/10.5301/EJO.2010.6212.
50. Chous AP, Richer SP, Gerson JD et al. The Diabetes Visual Function Supplement Study (DiVFuSS). Br J Ophthalmol. 2016; 100: 227-34. https://doi.org/10.1136/bjophthalmol-2014-306534.
51. Lafuente M, Ortín L, Argente M et al. Three-year outcomes in a randomized single-blind controlled trial of intravitreal ranibizumab and oral supplementation with docosahexaenoic acid and antioxidants for diabetic macular edema. Retina. 2019; 39: 1083-90. https://doi.org/10.1097/IAE.0000000000002114.