Advances in the risk relationship between glucagon-like peptide-1 receptor agonists and diabetic retinopathy_Chinese Journal of Ocular Fundus Diseases

Authors：

Tan Huiwen ¹ , Li Danting ¹ ,  Zhang Meixia ²

1. Department of Endocrinology and Metabolism, West China Hospital, Sichuan University, Chengdu 610041, China;
2. Department of Ophthalmology, West China Hospital, Sichuan University, Chengdu 610041, China;

Corresponding author：

Zhang Meixia, Email: meixiazhang@foxmail.com

Keywords：

Diabetic retinopathy; Glucagon-like peptide-1 receptor agonist; Multi-effect protection; Risk; Review

DOI：

10.3760/cma.j.cn511434-20211217-00707

Video：

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Abstract Full text Figures/Tables Video References Cited by

Diabetic retinopathy (DR) is one of the most serious complications of diabetes mellitus. Severe diabetic macular edema or proliferative retinopathy may lead to impaired vision or even blindness in diabetic patients. The glucagon-like peptide-1 receptor agonist (GLP-1RA) is now commonly used as novel glucose-lowering agents in the clinical management of type 2 diabetes, but the rapid glycaemic changes associated with the use of the GLP-1RA may aggravate the risk of an increase in the occurrence of short-term potential DR. Potential effects and mechanisms of DR include oxidative stress, vascular endothelial growth factor, inflammation, retinal neurodegeneration, and other cytokines.Whether GLP-1RA leads to the increased risk of DR remains controversial. More basic and clinical studies are needed with the aim of further clarifying the correlation between GLP-1RA and DR risk.

Citation： Tan Huiwen, Li Danting, Zhang Meixia. Advances in the risk relationship between glucagon-like peptide-1 receptor agonists and diabetic retinopathy. Chinese Journal of Ocular Fundus Diseases, 2023, 39(11): 943-948. doi: 10.3760/cma.j.cn511434-20211217-00707 Copy

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3.	Pan CW, Wang S, Qian DJ, et al. Prevalence, awareness, and risk factors of diabetic retinopathy among adults with known type 2 diabetes mellitus in an urban community in China[J]. Ophthalmic Epidemiol, 2017, 24(3): 188-194. DOI: 10.1080/09286586.2016.1264612.
4.	Cheung N, Mitchell P, Wong TY. Diabetic retinopathy[J]. Lancet, 2010, 376(9735): 124-136. DOI: 10.1016/s0140-6736(09)62124-3.
5.	Pang B, Zhou H, Kuang H. The potential benefits of glucagon-like peptide-1 receptor agonists for diabetic retinopathy[J]. Peptides, 2018, 100: 123-126. DOI: 10.1016/j.peptides.2017.08.003.
6.	Huang YL, Xu XZ, Liu J, et al. Effects of new hypoglycemic drugs on cardiac remodeling: a systematic review and network meta-analysis[J]. BMC Cardiovasc Disord, 2023, 23(1): 293. DOI: 10.1186/s12872-023-03324-6.
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26.	Kowluru RA. Retinopathy in a diet-induced type 2 diabetic rat model and role of epigenetic modifications[J]. Diabetes, 2020, 69(4): 689-698. DOI: 10.2337/db19-1009.
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29.	Mudaliar S, Hupfeld C, Chao DL. SGLT2 inhibitor-induced low-grade ketonemia ameliorates retinal hypoxia in diabetic retinopathy-a novel hypothesis[J]. J Clin Endocrinol Metab, 2021, 106(5): 1235-1244. DOI: 10.1210/clinem/dgab050.
30.	丁国龙, 谢安明, 雷剑琴, 等. 增生型糖尿病视网膜病变患者玻璃体内注射贝伐单抗后房水中细胞因子的变化及其相关性分析[J]. 眼科新进展, 2017, 37(4): 4. DOI: 10.13389/j.cnki.rao.2017.0091.Ding GL, Xie AM, Lei JQ, et al. Changes of cytokines in aqueous humor of patients with proliferative diabetic retinopathy after intravitreal bevacizumab and their correlation analysis[J]. Rec Adv Ophthalmol, 2017, 37(4): 4. DOI: 10.13389/j.cnki.rao.2017.0091.
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1. Wong TY, Cheung CM, Larsen M, et al. Diabetic retinopathy[J/OL]. Nat Rev Dis Primers, 2016, 2: 16012[2016-03-17]. https://pubmed.ncbi.nlm.nih.gov/27159554/. DOI: 10.1038/nrdp.2016.12.
2. 邓宇轩, 叶雯青, 孙艳婷, 等. 中国糖尿病视网膜病变患病率的荟萃分析[J]. 中华医学杂志, 2020, 100(48): 3846-3852. DOI: 10.3760/ cma.j.cn112137-20200925-02720.Deng YX, Ye WQ, Sun YT, et al. A meta-analysis of prevalence of diabetic retinopathy in China[J]. Natl Med J China, 2020, 100(48): 3846-3852. DOI: 10.3760/cma.j.cn112137-20200925-02720.
3. Pan CW, Wang S, Qian DJ, et al. Prevalence, awareness, and risk factors of diabetic retinopathy among adults with known type 2 diabetes mellitus in an urban community in China[J]. Ophthalmic Epidemiol, 2017, 24(3): 188-194. DOI: 10.1080/09286586.2016.1264612.
4. Cheung N, Mitchell P, Wong TY. Diabetic retinopathy[J]. Lancet, 2010, 376(9735): 124-136. DOI: 10.1016/s0140-6736(09)62124-3.
5. Pang B, Zhou H, Kuang H. The potential benefits of glucagon-like peptide-1 receptor agonists for diabetic retinopathy[J]. Peptides, 2018, 100: 123-126. DOI: 10.1016/j.peptides.2017.08.003.
6. Huang YL, Xu XZ, Liu J, et al. Effects of new hypoglycemic drugs on cardiac remodeling: a systematic review and network meta-analysis[J]. BMC Cardiovasc Disord, 2023, 23(1): 293. DOI: 10.1186/s12872-023-03324-6.
7. Marso SP, Daniels GH, Brown-Frandsen K, et al. Liraglutide and cardiovascular outcomes in type 2 diabetes[J]. N Engl J Med, 2016, 375(4): 311-322. DOI: 10.1056/NEJMoa1603827.
8. Simó R, Hernández C. GLP-1R as a target for the treatment of diabetic retinopathy: friend or foe?[J]. Diabetes, 2017, 66(6): 1453-1460. DOI: 10.2337/db16-1364.
9. Douros A, Filion KB, Yin H, et al. Glucagon-like peptide 1 receptor agonists and the risk of incident diabetic retinopathy[J]. Diabetes Care, 2018, 41(11): 2330-2338. DOI: 10.2337/dc17-2280.
10. Holst JJ. The physiology of glucagon-like peptide 1[J]. Physiol Rev, 2007, 87(4): 1409-1439. DOI: 10.1152/physrev.00034.2006.
11. Gribble FM, Reimann F. Metabolic messengers: glucagon-like peptide 1[J]. Nat Metab, 2021, 3(2): 142-148. DOI: 10.1038/s42255-020-00327-x.
12. Gilbert MP, Pratley RE. GLP-1 analogs and DPP-4 inhibitors in type 2 diabetes therapy: review of head-to-head clinical trials[J]. Front Endocrinol (Lausanne), 2020, 11: 178. DOI: 10.3389/fendo.2020.00178.
13. Pratley R, Amod A, Hoff ST, et al. Oral semaglutide versus subcutaneous liraglutide and placebo in type 2 diabetes (PIONEER 4): a randomised, double-blind, phase 3a trial[J]. Lancet, 2019, 394(10192): 39-50. DOI: 10.1016/s0140-6736(19)31271-1.
14. Trujillo JM, Nuffer W. GLP-1 receptor agonists for type 2 diabetes mellitus: recent developments and emerging agents[J]. Pharmacotherapy, 2014, 34(11): 1174-1186. DOI: 10.1002/phar.1507.
15. Brunton SA, Wysham CH. GLP-1 receptor agonists in the treatment of type 2 diabetes: role and clinical experience to date[J]. Postgrad Med, 2020, 132(sup2): 3-14. DOI: 10.1080/00325481.2020.1798099.
16. Yang CT, Yang CY, Ou HT, et al. Comparative cardiovascular safety of GLP-1 receptor agonists versus other glucose-lowering agents in real-world patients with type 2 diabetes: a nationwide population-based cohort study[J]. Cardiovasc Diabetol, 2020, 19(1): 83. DOI: 10.1186/s12933-020-01053-0.
17. Husain M, Birkenfeld AL, Donsmark M, et al. Oral semaglutide and cardiovascular outcomes in patients with type 2 diabetes[J]. N Engl J Med, 2019, 381(9): 841-851. DOI: 10.1056/NEJMoa1901118.
18. Hernandez AF, Green JB, Janmohamed S, et al. Albiglutide and cardiovascular outcomes in patients with type 2 diabetes and cardiovascular disease (harmony outcomes): a double-blind, randomised placebo-controlled trial[J]. Lancet, 2018, 392(10157): 1519-1529. DOI: 10.1016/S0140-6736(18)32261-X.
19. Gerstein HC, Colhoun HM, Dagenais GR, et al. Dulaglutide and cardiovascular outcomes in type 2 diabetes (REWIND): a double-blind, randomised placebo-controlled trial[J]. Lancet, 2019, 394(10193): 121-130. DOI: 10.1016/s0140-6736(19)31149-3.
20. Marso SP, Bain SC, Consoli A, et al. Semaglutide and cardiovascular outcomes in patients with type 2 diabetes[J]. N Engl J Med, 2016, 375(19): 1834-1844. DOI: 10.1056/NEJMoa1607141.
21. Song SJ, Wong TY. Current concepts in diabetic retinopathy[J]. Diabetes Metab J, 2014, 38(6): 416-425. DOI: 10.4093/dmj.2014.38.6.416.
22. Wang W, Lo ACY. Diabetic retinopathy: pathophysiology and treatments[J/OL]. Int J Mol Sci, 2018, 19(6): 1816[2018-06-20]. https://pubmed.ncbi.nlm.nih.gov/29925789/. DOI: 10.3390/ijms19061816.
23. Zafar S, Sachdeva M, Frankfort BJ, et al. Retinal neurodegeneration as an early manifestation of diabetic eye disease and potential neuroprotective therapies[J]. Curr Diab Rep, 2019, 19(4): 17. DOI: 10.1007/s11892-019-1134-5.
24. Kang Q, Yang C. Oxidative stress and diabetic retinopathy: molecular mechanisms, pathogenetic role and therapeutic implications[J/OL]. Redox Biol, 2020, 37: 101799[2020-11-13]. https://pubmed.ncbi.nlm.nih.gov/33248932/. DOI: 10.1016/j.redox.2020.101799.
25. Hammes HP. Diabetic retinopathy: hyperglycaemia, oxidative stress and beyond[J]. Diabetologia, 2018, 61(1): 29-38. DOI: 10.1007/s00125-017-4435-8.
26. Kowluru RA. Retinopathy in a diet-induced type 2 diabetic rat model and role of epigenetic modifications[J]. Diabetes, 2020, 69(4): 689-698. DOI: 10.2337/db19-1009.
27. Sui A, Chen X, Demetriades AM, et al. Inhibiting NF-κB signaling activation reduces retinal neovascularization by promoting a polarization shift in macrophages[J]. Invest Ophthalmol Vis Sci, 2020, 61(6): 4. DOI: 10.1167/iovs.61.6.4.
28. Brownlee M. Biochemistry and molecular cell biology of diabetic complications[J]. Nature, 2001, 414(6865): 813-820. DOI: 10.1038/414813a.
29. Mudaliar S, Hupfeld C, Chao DL. SGLT2 inhibitor-induced low-grade ketonemia ameliorates retinal hypoxia in diabetic retinopathy-a novel hypothesis[J]. J Clin Endocrinol Metab, 2021, 106(5): 1235-1244. DOI: 10.1210/clinem/dgab050.
30. 丁国龙, 谢安明, 雷剑琴, 等. 增生型糖尿病视网膜病变患者玻璃体内注射贝伐单抗后房水中细胞因子的变化及其相关性分析[J]. 眼科新进展, 2017, 37(4): 4. DOI: 10.13389/j.cnki.rao.2017.0091.Ding GL, Xie AM, Lei JQ, et al. Changes of cytokines in aqueous humor of patients with proliferative diabetic retinopathy after intravitreal bevacizumab and their correlation analysis[J]. Rec Adv Ophthalmol, 2017, 37(4): 4. DOI: 10.13389/j.cnki.rao.2017.0091.
31. Capitão M, Soares R. Angiogenesis and inflammation crosstalk in diabetic retinopathy[J]. J Cell Biochem, 2016, 117(11): 2443-2453. DOI: 10.1002/jcb.25575.
32. Rübsam A, Parikh S, Fort PE. Role of inflammation in diabetic retinopathy[J]. Int J Mol Sci, 2018, 19(4): 942. DOI: 10.3390/ijms19040942.
33. Barber AJ, Lieth E, Khin SA, et al. Neural apoptosis in the retina during experimental and human diabetes. Early onset and effect of insulin[J]. J Clin Invest, 1998, 102(4): 783-791. DOI: 10.1172/jci2425.
34. Carrasco E, Hernández C, Miralles A, et al. Lower somatostatin expression is an early event in diabetic retinopathy and is associated with retinal neurodegeneration[J]. Diabetes Care, 2007, 30(11): 2902-2908. DOI: 10.2337/dc07-0332.
35. Garcia-Ramírez M, Hernández C, Villarroel M, et al. Interphotoreceptor retinoid-binding protein (IRBP) is downregulated at early stages of diabetic retinopathy[J]. Diabetologia, 2009, 52(12): 2633-2641. DOI: 10.1007/s00125-009-1548-8.
36. Sohn EH, van Dijk HW, Jiao C, et al. Retinal neurodegeneration may precede microvascular changes characteristic of diabetic retinopathy in diabetes mellitus[J/OL]. Proc Natl Acad Sci USA, 2016, 113(19): E2655-2664[2016-05-10]. https://pubmed.ncbi.nlm.nih.gov/27114552/. DOI: 10.1073/pnas.1522014113.
37. Masser DR, Otalora L, Clark NW, et al. Functional changes in the neural retina occur in the absence of mitochondrial dysfunction in a rodent model of diabetic retinopathy[J]. J Neurochem, 2017, 143(5): 595-608. DOI: 10.1111/jnc.14216.
38. Santos AR, Ribeiro L, Bandello F, et al. Functional and structural findings of neurodegeneration in early stages of diabetic retinopathy: cross-sectional analyses of baseline aata of the EUROCONDOR project[J]. Diabetes, 2017, 66(9): 2503-2510. DOI: 10.2337/db16-1453.
39. Chen H, Zhang X, Liao N, et al. Decreased expression of glucagon-like peptide-1 receptor and sodium-glucose co-transporter 2 in patients with proliferative diabetic retinopathy[J/OL]. Front Endocrinol (Lausanne), 2022, 13: 1020252[2022-11-17]. https://pubmed.ncbi.nlm.nih.gov/36465606/. DOI: 10.3389/fendo.2022.1020252.
40. Zhang Y, Zhang J, Wang Q, et al. Intravitreal injection of exendin-4 analogue protects retinal cells in early diabetic rats[J]. Invest Ophthalmol Vis Sci, 2011, 52(1): 278-285. DOI: 10.1167/iovs.09-4727.
41. Zeng Y, Yang K, Wang F, et al. The glucagon like peptide 1 analogue, exendin-4, attenuates oxidative stress-induced retinal cell death in early diabetic rats through promoting Sirt1 and Sirt3 expression[J]. Exp Eye Res, 2016, 151: 203-211. DOI: 10.1016/j.exer.2016.05.002.
42. Cai X, Li J, Wang M, et al. GLP-1 Treatment improves diabetic retinopathy by alleviating autophagy through GLP-1R-ERK1/2-HDAC6 signaling pathway[J]. Int J Med Sci, 2017, 14(12): 1203-1212. DOI: 10.7150/ijms.20962.
43. Yasuda H, Ohashi A, Nishida S, et al. Exendin-4 induces extracellular-superoxide dismutase through histone H3 acetylation in human retinal endothelial cells[J]. J Clin Biochem Nutr, 2016, 59(3): 174-181. DOI: 10.3164/jcbn.16-26.
44. Pfeffer MA, Claggett B, Diaz R, et al. Lixisenatide in patients with type 2 diabetes and acute coronary syndrome[J]. N Engl J Med, 2015, 373(23): 2247-2257. DOI: 10.1056/NEJMoa1509225.
45. Holman RR, Bethel MA, Mentz RJ, et al. Effects of once-weekly exenatide on cardiovascular outcomes in type 2 diabetes[J]. N Engl J Med, 2017, 377(13): 1228-1239. DOI: 10.1056/NEJMoa1612917.
46. Buse JB, Wexler DJ, Tsapas A, et al. 2019 update to: management of hyperglycaemia in type 2 diabetes, 2018. A consensus report by the American Diabetes Association (ADA) and the European Association for the Study of Diabetes (EASD)[J]. Diabetologia, 2020, 63(2): 221-228. DOI: 10.1007/s00125-019-05039-w.
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Chinese Journal of Ocular Fundus Diseases

Advances in the risk relationship between glucagon-like peptide-1 receptor agonists and diabetic retinopathy

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