Research progress in prevention and cure of glucagon-like peptide-1 receptor agonists-1 receptor agonists for diabetic retinopathy_Chinese Journal of Ocular Fundus Diseases

Authors：

Wu Cenyi ¹ , Li Xiaoxia ² , Shen Yu ² ,  Wu Miaoqin ²

1. The Seond Clinical Medical College of Zhejiang Chinese Medical University, Hangzhou 310053, China;
2. Department of Ophthalmology, Zhejiang Provincial People's Hospital, People's Hospital of Hangzhou Medical College, Hangzhou 310014, China;

Corresponding?author：

Wu Miaoqin, Email: eyewmq@126.com

Keywords：

Diabetic retinopathy; Glucagon-like peptide-1 receptor agonist; Semaglutide; Review

DOI：

10.3760/cma.j.cn511434-20230424-00184

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Diabetic retinopathy (DR) is one of the most frequent complications of diabetes (T2DM), which is the main eye disease causing blindness in adults in recent years. At present, glucagon-like peptide-1 receptor agonists (GLP-1RA) have become the main drugs used in the treatment of diabetes due to its superior hypoglycemic, lipid-lowering, hypertensive and cardiovascular effects. A large number of studies have shown that GLP-1RA drugs can protect retinal microvascular and optic nerves in the treatment of diabetes through various ways, but some studies have found that GLP-1RA drugs represented by semaglutide may lead to the progress of DR. Therefore, GLP-1RA should be used cautiously for patients who with severe non-proliferative DR or proliferative DR. Regardless of whether T2DM patients are complicated with DR, the fundus retinal condition should be monitored regularly after the use of GLP-1RA drugs, and timely countermeasures should be taken when DR occurs and develops. The benefits of GLP-1RA used by diabetes patients are obvious to all, and scientific and rational drug use can prevent the occurrence and progress of DR, which can better benefit DR Patients.

Citation： Wu Cenyi, Li Xiaoxia, Shen Yu, Wu Miaoqin. Research progress in prevention and cure of glucagon-like peptide-1 receptor agonists-1 receptor agonists for diabetic retinopathy. Chinese Journal of Ocular Fundus Diseases, 2024, 40(2): 153-158. doi: 10.3760/cma.j.cn511434-20230424-00184 Copy

1.	中華醫學會眼科學分會眼底病學組, 中國醫師協會眼科醫師分會眼底病學組. 我國糖尿病視網膜病變臨床診療指南(2022年)[J]. 中華眼底病雜志, 2023, 39(2): 99-124. DOI: 10.3760/cma.j.cn511434-20230110-00018.Fundus Disease Group of Ophthalmological Society of Chinese Medical Association, Fundus Disease Group of Ophthalmologist Branch of Chinese Medical Doctor Association. Evidence-based guidelines for diagnosis and treatment of diabetic retinopathy in China (2022)[J]. Chin J Ocul Fundus Dis, 2023, 39(2): 99-124. DOI: 10.3760/cma.j.cn511434-20230110-00018.
2.	Klein R, Klein BE, Moss SE, et al. The wisconsin epidemiologic study of diabetic retinopathy. Ⅱ. Prevalence and risk of diabetic retinopathy when age at diagnosis is less than 30 years[J]. Arch Ophthalmol, 1984, 102(4): 520-526. DOI: 10.1001/archopht.1984.01040030398010.
3.	Klein R, Klein BE, 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[J]. Arch Ophthalmol, 1984, 102(4): 527-532. DOI: 10.1001/archopht.1984.01040030405011.
4.	Palmer SC, Tendal B, Mustafa RA, et al. Sodium-glucose cotransporter protein-2 (SGLT-2) inhibitors and glucagon-like peptide-1 (GLP-1) receptor agonists for type 2 diabetes: systematic review and network meta-analysis of randomised controlled trials[J/OL]. BMJ, 2021, 372: m4573[2021-01-13].https://pubmed.ncbi.nlm.nih.gov/33441402/. DOI: 10.1136/bmj.m4573.
5.	American Diabetes Association Professional Practice Committee. Cardiovascular disease and risk management: standards of medical care in diabetes-2022[J]. Diabetes Care, 2022, 45(Suppl 1): S144-174. DOI: 10.2337/dc22-S010.
6.	中華醫學會糖尿病學分會, 中華醫學會內分泌學分會. 中國成人2型糖尿病合并心腎疾病患者降糖藥物臨床應用專家共識[J]. 中華糖尿病雜志, 2020, 12(6): 369-381. DOI: 10.3760/cma.j.cn115791-20200419-00233.Chinese Diabetes Society, Chinese Society of Endocrinology. Expert consensus on glucose-lowering pharmacotherapies in Chinese adults with type 2 diabetes and cardiovascular disease or chronic kidney disease[J]. Chin J Diabetes Mellitus, 2020, 12(6): 369-381. DOI: 10.3760/cma.j.cn115791-20200419-00233.
7.	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.
8.	Armstrong MJ, Hull D, Guo K, et al. Glucagon-like peptide 1 decreases lipotoxicity in non-alcoholic steatohepatitis[J]. J Hepatol, 2016, 64(2): 399-408. DOI: 10.1016/j.jhep.2015.08.038.
9.	Gilbert MP, Pratley RE. GLP-1 analogs and DPP-4 inhibitors in type 2 diabetes therapy: review of head-to-head clinical trials[J/OL]. Front Endocrinol (Lausanne), 2020, 11: 178[2020-04-03].https://pubmed.ncbi.nlm.nih.gov/32308645/. DOI: 10.3389/fendo.2020.00178.
10.	H?lscher C. Central effects of GLP-1: new opportunities for treatments of neurodegenerative diseases[J]. J Endocrinol, 2014, 221(1): 31-41. DOI: 10.1530/JOE-13-0221.
11.	Ma X, Liu Z, Ilyas I, et al. GLP-1 receptor agonists (GLP-1RAs): cardiovascular actions and therapeutic potential[J]. Int J Biol Sci, 2021, 17(8): 2050-2068. DOI: 10.7150/ijbs.59965.
12.	蔣王艷, 劉少華, 郭潔茹, 等. 基于美國FAERS數據庫的司美格魯肽不良事件信號挖掘[J]. 藥物流行病學雜志, 2022, 31(3): 167-172. DOI: 10.19960/j.cnki.issn1005-0698.2022.03.005.Jiang WY, Liu SH, Guo JR, et al. Data mining for adverse drug events of semaglutide based on FAERS database[J]. Chin J Pharmacoepidemiol, 2022, 31(3): 167-172. DOI: 10.19960/j.cnki.issn1005-0698.2022.03.005.
13.	Mohamed Q, Gillies MC, Wong TY. Management of diabetic retinopathy: a systematic review[J]. JAMA, 2007, 298(8): 902-916. DOI: 10.1001/jama.298.8.902.
14.	Wang L, Peng W, Zhao Z, et al. Prevalence and treatment of diabetes in China, 2013-2018[J]. JAMA, 2021, 326(24): 2498-2506. DOI: 10.1001/jama.2021.22208.
15.	Ahrén B, Masmiquel L, Kumar H, et al. Efficacy and safety of once-weekly semaglutide versus once-daily sitagliptin as an add-on to metformin, thiazolidinediones, or both, in patients with type 2 diabetes (SUSTAIN 2): a 56-week, double-blind, phase 3a, randomised trial[J]. Lancet Diabetes Endocrinol, 2017, 5(5): 341-354. DOI: 10.1016/S2213-8587(17)30092-X.
16.	Ahmann AJ, Capehorn M, Charpentier G, et al. Efficacy and safety of once-weekly semaglutide versus exenatide ER in subjects with type 2 diabetes (SUSTAIN 3): a 56-week, open-label, randomized clinical trial[J]. Diabetes Care, 2018, 41(2): 258-266. DOI: 10.2337/dc17-0417.
17.	Pratley RE, Aroda VR, Lingvay I, et al. Semaglutide versus dulaglutide once weekly in patients with type 2 diabetes (SUSTAIN 7): a randomised, open-label, phase 3b trial[J]. Lancet Diabetes Endocrinol, 2018, 6(4): 275-286. DOI: 10.1016/S2213-8587(18)30024-X.
18.	Lingvay I, Catarig AM, Frias JP, et al. Efficacy and safety of once-weekly semaglutide versus daily canagliflozin as add-on to metformin in patients with type 2 diabetes (SUSTAIN 8): a double-blind, phase 3b, randomised controlled trial[J]. Lancet Diabetes Endocrinol, 2019, 7(11): 834-844. DOI: 10.1016/S2213-8587(19)30311-0.
19.	Zinman B, Bhosekar V, Busch R, et al. Semaglutide once weekly as add-on to SGLT-2 inhibitor therapy in type 2 diabetes (SUSTAIN 9): a randomised, placebo-controlled trial[J]. Lancet Diabetes Endocrinol, 2019, 7(5): 356-367. DOI: 10.1016/S2213-8587(19)30066-X.
20.	Shi L X, Liu XM, Shi YQ, et al. Efficacy and safety of dulaglutide monotherapy compared with glimepiride in Chinese patients with type 2 diabetes: post-hoc analyses of a randomized, double-blind, phase Ⅲ study[J]. J Diabetes Investig, 2020, 11(1): 142-150. DOI: 10.1111/jdi.13075.
21.	Dziedziak J, Zaleska-?mijewska A, Szaflik JP, et al. Impact of arterial hypertension on the eye: a review of the pathogenesis, diagnostic methods, and treatment of hypertensive retinopathy[J/OL]. Med Sci Monit, 2022, 28: e935135[2022-01-20]. https://pubmed.ncbi.nlm.nih.gov/35046380/. DOI: 10.12659/MSM.935135.
22.	Wong TY, Cheung CMG, 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.
23.	Helmst?dter J, Frenis K, Filippou K, et al. Endothelial GLP-1 (glucagon-like peptide-1) receptor mediates cardiovascular protection by liraglutide in mice with experimental arterial hypertension[J]. Arterioscler Thromb Vasc Biol, 2020, 40(1): 145-158. DOI: 10.1161/atv.0000615456.97862.30.
24.	Kim M, Platt MJ, Shibasaki T, et al. GLP-1 receptor activation and Epac2 link atrial natriuretic peptide secretion to control of blood pressure[J]. Nat Med, 2013, 19(5): 567-575. DOI: 10.1038/nm.3128.
25.	肖誠, 于淼. 胰高糖素樣肽-1受體激動劑在2型糖尿病合并動脈粥樣硬化性心血管疾病或高危風險人群中的可能機制及循證證據[J]. 中華糖尿病雜志, 2022, 14(12): 1348-1354. DOI: 10.3760/cma.j.cn115791-20220802-00373.Xiao C, Yu M. Mechanisms and evidence of glucagon-like peptide-1 receptor agonist in type 2 diabetes mellitus complicated with atherosclerosis cardiovascular diseases or its high-risk population[J]. Chin J Diabetes Mellitus, 2022, 14(12): 1348-1354. DOI: 10.3760/cma.j.cn115791-20220802-00373.
26.	Klein BE, Moss SE, Klein R, et al. The wisconsin epidemiologic study of diabetic retinopathy. XIII. Relationship of serum cholesterol to retinopathy and hard exudate[J]. Ophthalmology, 1991, 98(8): 1261-1265. DOI: 10.1016/s0161-6420(91)32145-6.
27.	Benarous R, Sasongko MB, Qureshi S, et al. Differential association of serum lipids with diabetic retinopathy and diabetic macular edema[J]. Invest Ophthalmol Vis Sci, 2011, 52(10): 7464-7469. DOI: 10.1167/iovs.11-7598.
28.	Chou Y, Ma J, Su X, et al. Emerging insights into the relationship between hyperlipidemia and the risk of diabetic retinopathy[J]. Lipids Health Dis, 2020, 19(1): 241. DOI: 10.1186/s12944-020-01415-3.
29.	Sasongko MB, Wong TY, Nguyen TT, et al. Serum apolipoprotein AI and B are stronger biomarkers of diabetic retinopathy than traditional lipids[J]. Diabetes Care, 2011, 34(2): 474-479. DOI: 10.2337/dc10-0793.
30.	Moosaie F, Davatgari RM, Firouzabadi FD, et al. Lipoprotein(a) and apolipoproteins as predictors for diabetic retinopathy and its severity in adults with type 2 diabetes: a case-cohort study[J]. Can J Diabetes, 2020, 44(5): 414-421. DOI: 10.1016/j.jcjd.2020.01.007.
31.	馬玉梅, 傅松波, 金生祿, 等. GLP-1類似物改善糖尿病大鼠胰島素敏感性的研究[J]. 國際內分泌代謝雜志, 2021, 41(4): 313-317. DOI: 10.3760/cma.j.cn121383-20210313-03033.Ma YM, Fu SB, Jin SL, et al. Glucagon-like peptide-1 analogue improves insulin sensitivity in diabetic rats[J]. Int J Endocrinol & Metabol, 2021, 41(4): 313-317. DOI: 10.3760/cma.j.cn121383-20210313-03033.
32.	Anholm C, Kumarathurai P, Pedersen LR, et al. Liraglutide in combination with metformin may improve the atherogenic lipid profile and decrease C-reactive protein level in statin treated obese patients with coronary artery disease and newly diagnosed type 2 diabetes: a randomized trial[J]. Atherosclerosis, 2019, 288: 60-66. DOI: 10.1016/j.atherosclerosis.2019.07.007.
33.	Liu Y, Jiang X, Chen X. Liraglutide and metformin alone or combined therapy for type 2 diabetes patients complicated with coronary artery disease[J]. Lipids Health Dis, 2017, 16(1): 227. DOI: 10.1186/s12944-017-0609-0.
34.	Xu L, Yu SQ, Gao L, et al. Effects of incretin-based therapies on weight-related indicators among patients with type 2 diabetes: a network meta-analysis[J]. Biomed Environ Sci, 2020, 33(1): 37-47. DOI: 10.3967/bes2020.005.
35.	Hernández C, Bogdanov P, Corraliza L, et al. Topical administration of GLP-1 receptor agonists prevents retinal neurodegeneration in experimental diabetes[J]. Diabetes, 2016, 65(1): 172-187. DOI: 10.2337/db15-0443.
36.	Zhai R, Xu H, Hu F, et al. Exendin-4, a GLP-1 receptor agonist regulates retinal capillary tone and restores microvascular patency after ischaemia-reperfusion injury[J]. Br J Pharmacol, 2020, 177(15): 3389-3402. DOI: 10.1111/bph.15059.
37.	Hebsgaard JB, Pyke C, Yildirim E, et al. Glucagon-like peptide-1 receptor expression in the human eye[J]. Diabetes Obes Metab, 2018, 20(9): 2304-2308. DOI: 10.1111/dom.13339.
38.	Gon?alves A, Lin C-M, Muthusamy A, et al. Protective effect of a GLP-1 analog on ischemia-reperfusion induced blood-retinal barrier breakdown and inflammation[J]. Invest Ophthalmol Vis Sci, 2016, 57(6): 2584-2592. DOI: 10.1167/iovs.15-19006.
39.	Fan Y, Liu K, Wang Q, et al. Exendin-4 alleviates retinal vascular leakage by protecting the blood-retinal barrier and reducing retinal vascular permeability in diabetic Goto-Kakizaki rats[J]. Exp Eye Res, 2014, 127: 104-116. DOI: 10.1016/j.exer.2014.05.004.
40.	Wei L, Mo W, Lan S, et al. GLP-1 RA improves diabetic retinopathy by protecting the blood-retinal barrier through GLP-1R-ROCK-p-MLC signaling pathway[J/OL]. J Diabetes Res, 2022, 2022: 1861940[2022-11-03]. https://pubmed.ncbi.nlm.nih.gov/36387940/. DOI: 10.1155/2022/1861940.
41.	Lieth E, Gardner TW, Barber AJ, et al. Retinal neurodegeneration: early pathology in diabetes[J]. Clin Exp Ophthalmol, 2000, 28(1): 3-8. DOI: 10.1046/j.1442-9071.2000.00222.x.
42.	Grieco M, Giorgi A, Gentile MC, et al. Glucagon-like peptide-1: a focus on neurodegenerative diseases[J/OL]. Front Neurosci, 2019, 13: 1112[2019-10-18]. https://pubmed.ncbi.nlm.nih.gov/31680842/. DOI: 10.3389/fnins.2019.01112.
43.	Ferrari F, Moretti A, Villa RF. Incretin-based drugs as potential therapy for neurodegenerative diseases: current status and perspectives[J/OL]. Pharmacol Ther, 2022, 239: 108277[2022-09-03]. https://pubmed.ncbi.nlm.nih.gov/36064147/. DOI: 10.1016/j.pharmthera.2022.108277.
44.	葉小珍, 邵加慶. 司美格魯肽的臨床應用研究進展[J]. 中華糖尿病雜志, 2022, 14(Z1): 1-8. DOI: 10.3760/cma.j.cn115791-20220721-00353.Ye XZ, Shao JQ. Research progress of long‐acting glucagon‐like peptide‐1 receptor agonist semaglutide[J]. Chin J Diabetes Mellitus, 2022, 14(Z1): 1-8. DOI: 10.3760/cma.j.cn115791-20220721-00353.
45.	Mahapatra MK, Karuppasamy M, Sahoo BM. Therapeutic potential of semaglutide, a newer GLP-1 receptor agonist, in abating obesity, non-alcoholic steatohepatitis and neurodegenerative diseases: a narrative review[J]. Pharm Res, 2022, 39(6): 1233-1248. DOI: 10.1007/s11095-022-03302-1.
46.	張茸, 徐亮, 劉玉軍, 等. 胰高血糖素類肽-1緩釋珠對大鼠視網膜神經節細胞的保護作用[J]. 眼科, 2009, 18(6): 414-418.Zhang R, Xu L, Liu YJ, et al. Neuroprotective effect of intravitreal glucagon-like peptide-1 production in the optic nerve crush model[J]. Ophthalmol CHN, 2009, 18(6): 414-418.
47.	Green JB, Hernandez AF, D'agostino RB, et al. Harmony outcomes: a randomized, double-blind, placebo-controlled trial of the effect of albiglutide on major cardiovascular events in patients with type 2 diabetes mellitus-rationale, design, and baseline characteristics[J]. Am Heart J, 2018, 203: 30-38. DOI: 10.1016/j.ahj.2018.03.030.
48.	Yoshida Y, Joshi P, Barri S, et al. Progression of retinopathy with glucagon-like peptide-1 receptor agonists with cardiovascular benefits in type 2 diabetes-a systematic review and meta-analysis[J/OL]. J Diabetes Complications, 2022, 36(8): 108255[2022-07-05]. https://pubmed.ncbi.nlm.nih.gov/35817678/. DOI: 10.1016/j.jdiacomp.2022.108255.
49.	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.
50.	楊文健, 龔宇, 李鳴一, 等. 利拉魯肽對糖尿病視網膜病變患者的臨床療效及作用機制研究[J]. 臨床和實驗醫學雜志, 2019, 18(14): 1541-1545. DOI: 10.3969/j.issn.1671-4695.2019.14.025.Yang WJ, Gong Y, Li MY, et al. Study on the effect and mechanism of liraglutide in diabetic retinopathy[J]. Journal of Clinical and Experimental Medicine, 2019, 18(14): 1541-1545. DOI: 10.3969/j.issn.1671-4695.2019.14.025.
51.	A research study to look at how semaglutide compared to placebo affects diabetic eye disease in people with type 2 diabetes (FOCUS)[EB/OL]. (2019-12-01)[2022-04-24]. https://clinicaltrials.gov/ct2/show/NCT03811561.
52.	郭艷瓊, 彭晶, 李慶德, 等. 基于OpenFDA數據挖掘和分析司美格魯肽的不良事件報告信號[J]. 中國藥師, 2022, 25(3): 475-478. DOI: 10.19962/j.cnki.issn1008-049X.2022.03.016.Guo YQ, Peng J, Li QD, et al. Adverse drug events signal mining and analysis of semaglutide based on OpenFDA[J]. China Pharmacist, 2022, 25(3): 475-478. DOI: 10.19962/j.cnki.issn1008-049X.2022.03.016.
53.	Varadhan L, Humphreys T, Walker AB, et al. The impact of improved glycaemic control with GLP-1 receptor agonist therapy on diabetic retinopathy[J/OL]. Diabetes Res Clin Pract, 2014, 103(3): e37-e39[2014-01-06]. https://pubmed.ncbi.nlm.nih.gov/24456992/. DOI: 10.1016/j.diabres.2013.12.041.
54.	Bain SC, Klufas MA, Ho A, et al. Worsening of diabetic retinopathy with rapid improvement in systemic glucose control: a review[J]. Diabetes Obes Metab, 2019, 21(3): 454-466. DOI: 10.1111/dom.13538.
55.	Wysham CH, Macconell LA, Maggs DG, et al. Five-year efficacy and safety data of exenatide once weekly: long-term results from the DURATION-1 randomized clinical trial[J]. Mayo Clin Proc, 2015, 90(3): 356-365. DOI: 10.1016/j.mayocp.2015.01.008.
56.	Jingi AM, Tankeu AT, Ateba NA, et al. Mechanism of worsening diabetic retinopathy with rapid lowering of blood glucose: the synergistic hypothesis[J]. BMC Endocr Disord, 2017, 17(1): 63. DOI: 10.1186/s12902-017-0213-3.
57.	Kennedy A, Frank RN. The influence of glucose concentration and hypoxia on VEGF secretion by cultured retinal cells[J]. Curr Eye Res, 2011, 36(2): 168-177. DOI: 10.3109/02713683.2010.521968.
58.	Henricsson M, Berntorp K, Fernlund P, et al. Progression of retinopathy in insulin-treated type 2 diabetic patients[J]. Diabetes Care, 2002, 25(2): 381-385. DOI: 10.2337/diacare.25.2.381.
59.	Casson RJ, Wood JPM, Osborne NN. Hypoglycaemia exacerbates ischaemic retinal injury in rats[J]. Br J Ophthalmol, 2004, 88(6): 816-820. DOI: 10.1136/bjo.2003.024661.
60.	陳燕鳳. T2DM患者血清胰高血糖素樣肽-1水平與糖尿病視網膜病變的相關性及其影響因素的分析[D]. 福州: 福建醫科大學, 2021.Chen YF. An analysis of correlation and it’s impacting factors between the serum glucagon-like peptide 1 level and diabetic retinopathy in patients with T2DM[D]. Fuzhou: Fujian Medical University, 2021.
61.	Xu G, Kaneto H, Laybutt DR, et al. Downregulation of GLP-1 and GIP receptor expression by hyperglycemia: possible contribution to impaired incretin effects in diabetes[J]. Diabetes, 2007, 56(6): 1551-1558. DOI: 10.2337/db06-1033.

1. 中華醫學會眼科學分會眼底病學組, 中國醫師協會眼科醫師分會眼底病學組. 我國糖尿病視網膜病變臨床診療指南(2022年)[J]. 中華眼底病雜志, 2023, 39(2): 99-124. DOI: 10.3760/cma.j.cn511434-20230110-00018.Fundus Disease Group of Ophthalmological Society of Chinese Medical Association, Fundus Disease Group of Ophthalmologist Branch of Chinese Medical Doctor Association. Evidence-based guidelines for diagnosis and treatment of diabetic retinopathy in China (2022)[J]. Chin J Ocul Fundus Dis, 2023, 39(2): 99-124. DOI: 10.3760/cma.j.cn511434-20230110-00018.
2. Klein R, Klein BE, Moss SE, et al. The wisconsin epidemiologic study of diabetic retinopathy. Ⅱ. Prevalence and risk of diabetic retinopathy when age at diagnosis is less than 30 years[J]. Arch Ophthalmol, 1984, 102(4): 520-526. DOI: 10.1001/archopht.1984.01040030398010.
3. Klein R, Klein BE, 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[J]. Arch Ophthalmol, 1984, 102(4): 527-532. DOI: 10.1001/archopht.1984.01040030405011.
4. Palmer SC, Tendal B, Mustafa RA, et al. Sodium-glucose cotransporter protein-2 (SGLT-2) inhibitors and glucagon-like peptide-1 (GLP-1) receptor agonists for type 2 diabetes: systematic review and network meta-analysis of randomised controlled trials[J/OL]. BMJ, 2021, 372: m4573[2021-01-13].https://pubmed.ncbi.nlm.nih.gov/33441402/. DOI: 10.1136/bmj.m4573.
5. American Diabetes Association Professional Practice Committee. Cardiovascular disease and risk management: standards of medical care in diabetes-2022[J]. Diabetes Care, 2022, 45(Suppl 1): S144-174. DOI: 10.2337/dc22-S010.
6. 中華醫學會糖尿病學分會, 中華醫學會內分泌學分會. 中國成人2型糖尿病合并心腎疾病患者降糖藥物臨床應用專家共識[J]. 中華糖尿病雜志, 2020, 12(6): 369-381. DOI: 10.3760/cma.j.cn115791-20200419-00233.Chinese Diabetes Society, Chinese Society of Endocrinology. Expert consensus on glucose-lowering pharmacotherapies in Chinese adults with type 2 diabetes and cardiovascular disease or chronic kidney disease[J]. Chin J Diabetes Mellitus, 2020, 12(6): 369-381. DOI: 10.3760/cma.j.cn115791-20200419-00233.
7. 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.
8. Armstrong MJ, Hull D, Guo K, et al. Glucagon-like peptide 1 decreases lipotoxicity in non-alcoholic steatohepatitis[J]. J Hepatol, 2016, 64(2): 399-408. DOI: 10.1016/j.jhep.2015.08.038.
9. Gilbert MP, Pratley RE. GLP-1 analogs and DPP-4 inhibitors in type 2 diabetes therapy: review of head-to-head clinical trials[J/OL]. Front Endocrinol (Lausanne), 2020, 11: 178[2020-04-03].https://pubmed.ncbi.nlm.nih.gov/32308645/. DOI: 10.3389/fendo.2020.00178.
10. H?lscher C. Central effects of GLP-1: new opportunities for treatments of neurodegenerative diseases[J]. J Endocrinol, 2014, 221(1): 31-41. DOI: 10.1530/JOE-13-0221.
11. Ma X, Liu Z, Ilyas I, et al. GLP-1 receptor agonists (GLP-1RAs): cardiovascular actions and therapeutic potential[J]. Int J Biol Sci, 2021, 17(8): 2050-2068. DOI: 10.7150/ijbs.59965.
12. 蔣王艷, 劉少華, 郭潔茹, 等. 基于美國FAERS數據庫的司美格魯肽不良事件信號挖掘[J]. 藥物流行病學雜志, 2022, 31(3): 167-172. DOI: 10.19960/j.cnki.issn1005-0698.2022.03.005.Jiang WY, Liu SH, Guo JR, et al. Data mining for adverse drug events of semaglutide based on FAERS database[J]. Chin J Pharmacoepidemiol, 2022, 31(3): 167-172. DOI: 10.19960/j.cnki.issn1005-0698.2022.03.005.
13. Mohamed Q, Gillies MC, Wong TY. Management of diabetic retinopathy: a systematic review[J]. JAMA, 2007, 298(8): 902-916. DOI: 10.1001/jama.298.8.902.
14. Wang L, Peng W, Zhao Z, et al. Prevalence and treatment of diabetes in China, 2013-2018[J]. JAMA, 2021, 326(24): 2498-2506. DOI: 10.1001/jama.2021.22208.
15. Ahrén B, Masmiquel L, Kumar H, et al. Efficacy and safety of once-weekly semaglutide versus once-daily sitagliptin as an add-on to metformin, thiazolidinediones, or both, in patients with type 2 diabetes (SUSTAIN 2): a 56-week, double-blind, phase 3a, randomised trial[J]. Lancet Diabetes Endocrinol, 2017, 5(5): 341-354. DOI: 10.1016/S2213-8587(17)30092-X.
16. Ahmann AJ, Capehorn M, Charpentier G, et al. Efficacy and safety of once-weekly semaglutide versus exenatide ER in subjects with type 2 diabetes (SUSTAIN 3): a 56-week, open-label, randomized clinical trial[J]. Diabetes Care, 2018, 41(2): 258-266. DOI: 10.2337/dc17-0417.
17. Pratley RE, Aroda VR, Lingvay I, et al. Semaglutide versus dulaglutide once weekly in patients with type 2 diabetes (SUSTAIN 7): a randomised, open-label, phase 3b trial[J]. Lancet Diabetes Endocrinol, 2018, 6(4): 275-286. DOI: 10.1016/S2213-8587(18)30024-X.
18. Lingvay I, Catarig AM, Frias JP, et al. Efficacy and safety of once-weekly semaglutide versus daily canagliflozin as add-on to metformin in patients with type 2 diabetes (SUSTAIN 8): a double-blind, phase 3b, randomised controlled trial[J]. Lancet Diabetes Endocrinol, 2019, 7(11): 834-844. DOI: 10.1016/S2213-8587(19)30311-0.
19. Zinman B, Bhosekar V, Busch R, et al. Semaglutide once weekly as add-on to SGLT-2 inhibitor therapy in type 2 diabetes (SUSTAIN 9): a randomised, placebo-controlled trial[J]. Lancet Diabetes Endocrinol, 2019, 7(5): 356-367. DOI: 10.1016/S2213-8587(19)30066-X.
20. Shi L X, Liu XM, Shi YQ, et al. Efficacy and safety of dulaglutide monotherapy compared with glimepiride in Chinese patients with type 2 diabetes: post-hoc analyses of a randomized, double-blind, phase Ⅲ study[J]. J Diabetes Investig, 2020, 11(1): 142-150. DOI: 10.1111/jdi.13075.
21. Dziedziak J, Zaleska-?mijewska A, Szaflik JP, et al. Impact of arterial hypertension on the eye: a review of the pathogenesis, diagnostic methods, and treatment of hypertensive retinopathy[J/OL]. Med Sci Monit, 2022, 28: e935135[2022-01-20]. https://pubmed.ncbi.nlm.nih.gov/35046380/. DOI: 10.12659/MSM.935135.
22. Wong TY, Cheung CMG, 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.
23. Helmst?dter J, Frenis K, Filippou K, et al. Endothelial GLP-1 (glucagon-like peptide-1) receptor mediates cardiovascular protection by liraglutide in mice with experimental arterial hypertension[J]. Arterioscler Thromb Vasc Biol, 2020, 40(1): 145-158. DOI: 10.1161/atv.0000615456.97862.30.
24. Kim M, Platt MJ, Shibasaki T, et al. GLP-1 receptor activation and Epac2 link atrial natriuretic peptide secretion to control of blood pressure[J]. Nat Med, 2013, 19(5): 567-575. DOI: 10.1038/nm.3128.
25. 肖誠, 于淼. 胰高糖素樣肽-1受體激動劑在2型糖尿病合并動脈粥樣硬化性心血管疾病或高危風險人群中的可能機制及循證證據[J]. 中華糖尿病雜志, 2022, 14(12): 1348-1354. DOI: 10.3760/cma.j.cn115791-20220802-00373.Xiao C, Yu M. Mechanisms and evidence of glucagon-like peptide-1 receptor agonist in type 2 diabetes mellitus complicated with atherosclerosis cardiovascular diseases or its high-risk population[J]. Chin J Diabetes Mellitus, 2022, 14(12): 1348-1354. DOI: 10.3760/cma.j.cn115791-20220802-00373.
26. Klein BE, Moss SE, Klein R, et al. The wisconsin epidemiologic study of diabetic retinopathy. XIII. Relationship of serum cholesterol to retinopathy and hard exudate[J]. Ophthalmology, 1991, 98(8): 1261-1265. DOI: 10.1016/s0161-6420(91)32145-6.
27. Benarous R, Sasongko MB, Qureshi S, et al. Differential association of serum lipids with diabetic retinopathy and diabetic macular edema[J]. Invest Ophthalmol Vis Sci, 2011, 52(10): 7464-7469. DOI: 10.1167/iovs.11-7598.
28. Chou Y, Ma J, Su X, et al. Emerging insights into the relationship between hyperlipidemia and the risk of diabetic retinopathy[J]. Lipids Health Dis, 2020, 19(1): 241. DOI: 10.1186/s12944-020-01415-3.
29. Sasongko MB, Wong TY, Nguyen TT, et al. Serum apolipoprotein AI and B are stronger biomarkers of diabetic retinopathy than traditional lipids[J]. Diabetes Care, 2011, 34(2): 474-479. DOI: 10.2337/dc10-0793.
30. Moosaie F, Davatgari RM, Firouzabadi FD, et al. Lipoprotein(a) and apolipoproteins as predictors for diabetic retinopathy and its severity in adults with type 2 diabetes: a case-cohort study[J]. Can J Diabetes, 2020, 44(5): 414-421. DOI: 10.1016/j.jcjd.2020.01.007.
31. 馬玉梅, 傅松波, 金生祿, 等. GLP-1類似物改善糖尿病大鼠胰島素敏感性的研究[J]. 國際內分泌代謝雜志, 2021, 41(4): 313-317. DOI: 10.3760/cma.j.cn121383-20210313-03033.Ma YM, Fu SB, Jin SL, et al. Glucagon-like peptide-1 analogue improves insulin sensitivity in diabetic rats[J]. Int J Endocrinol & Metabol, 2021, 41(4): 313-317. DOI: 10.3760/cma.j.cn121383-20210313-03033.
32. Anholm C, Kumarathurai P, Pedersen LR, et al. Liraglutide in combination with metformin may improve the atherogenic lipid profile and decrease C-reactive protein level in statin treated obese patients with coronary artery disease and newly diagnosed type 2 diabetes: a randomized trial[J]. Atherosclerosis, 2019, 288: 60-66. DOI: 10.1016/j.atherosclerosis.2019.07.007.
33. Liu Y, Jiang X, Chen X. Liraglutide and metformin alone or combined therapy for type 2 diabetes patients complicated with coronary artery disease[J]. Lipids Health Dis, 2017, 16(1): 227. DOI: 10.1186/s12944-017-0609-0.
34. Xu L, Yu SQ, Gao L, et al. Effects of incretin-based therapies on weight-related indicators among patients with type 2 diabetes: a network meta-analysis[J]. Biomed Environ Sci, 2020, 33(1): 37-47. DOI: 10.3967/bes2020.005.
35. Hernández C, Bogdanov P, Corraliza L, et al. Topical administration of GLP-1 receptor agonists prevents retinal neurodegeneration in experimental diabetes[J]. Diabetes, 2016, 65(1): 172-187. DOI: 10.2337/db15-0443.
36. Zhai R, Xu H, Hu F, et al. Exendin-4, a GLP-1 receptor agonist regulates retinal capillary tone and restores microvascular patency after ischaemia-reperfusion injury[J]. Br J Pharmacol, 2020, 177(15): 3389-3402. DOI: 10.1111/bph.15059.
37. Hebsgaard JB, Pyke C, Yildirim E, et al. Glucagon-like peptide-1 receptor expression in the human eye[J]. Diabetes Obes Metab, 2018, 20(9): 2304-2308. DOI: 10.1111/dom.13339.
38. Gon?alves A, Lin C-M, Muthusamy A, et al. Protective effect of a GLP-1 analog on ischemia-reperfusion induced blood-retinal barrier breakdown and inflammation[J]. Invest Ophthalmol Vis Sci, 2016, 57(6): 2584-2592. DOI: 10.1167/iovs.15-19006.
39. Fan Y, Liu K, Wang Q, et al. Exendin-4 alleviates retinal vascular leakage by protecting the blood-retinal barrier and reducing retinal vascular permeability in diabetic Goto-Kakizaki rats[J]. Exp Eye Res, 2014, 127: 104-116. DOI: 10.1016/j.exer.2014.05.004.
40. Wei L, Mo W, Lan S, et al. GLP-1 RA improves diabetic retinopathy by protecting the blood-retinal barrier through GLP-1R-ROCK-p-MLC signaling pathway[J/OL]. J Diabetes Res, 2022, 2022: 1861940[2022-11-03]. https://pubmed.ncbi.nlm.nih.gov/36387940/. DOI: 10.1155/2022/1861940.
41. Lieth E, Gardner TW, Barber AJ, et al. Retinal neurodegeneration: early pathology in diabetes[J]. Clin Exp Ophthalmol, 2000, 28(1): 3-8. DOI: 10.1046/j.1442-9071.2000.00222.x.
42. Grieco M, Giorgi A, Gentile MC, et al. Glucagon-like peptide-1: a focus on neurodegenerative diseases[J/OL]. Front Neurosci, 2019, 13: 1112[2019-10-18]. https://pubmed.ncbi.nlm.nih.gov/31680842/. DOI: 10.3389/fnins.2019.01112.
43. Ferrari F, Moretti A, Villa RF. Incretin-based drugs as potential therapy for neurodegenerative diseases: current status and perspectives[J/OL]. Pharmacol Ther, 2022, 239: 108277[2022-09-03]. https://pubmed.ncbi.nlm.nih.gov/36064147/. DOI: 10.1016/j.pharmthera.2022.108277.
44. 葉小珍, 邵加慶. 司美格魯肽的臨床應用研究進展[J]. 中華糖尿病雜志, 2022, 14(Z1): 1-8. DOI: 10.3760/cma.j.cn115791-20220721-00353.Ye XZ, Shao JQ. Research progress of long‐acting glucagon‐like peptide‐1 receptor agonist semaglutide[J]. Chin J Diabetes Mellitus, 2022, 14(Z1): 1-8. DOI: 10.3760/cma.j.cn115791-20220721-00353.
45. Mahapatra MK, Karuppasamy M, Sahoo BM. Therapeutic potential of semaglutide, a newer GLP-1 receptor agonist, in abating obesity, non-alcoholic steatohepatitis and neurodegenerative diseases: a narrative review[J]. Pharm Res, 2022, 39(6): 1233-1248. DOI: 10.1007/s11095-022-03302-1.
46. 張茸, 徐亮, 劉玉軍, 等. 胰高血糖素類肽-1緩釋珠對大鼠視網膜神經節細胞的保護作用[J]. 眼科, 2009, 18(6): 414-418.Zhang R, Xu L, Liu YJ, et al. Neuroprotective effect of intravitreal glucagon-like peptide-1 production in the optic nerve crush model[J]. Ophthalmol CHN, 2009, 18(6): 414-418.
47. Green JB, Hernandez AF, D'agostino RB, et al. Harmony outcomes: a randomized, double-blind, placebo-controlled trial of the effect of albiglutide on major cardiovascular events in patients with type 2 diabetes mellitus-rationale, design, and baseline characteristics[J]. Am Heart J, 2018, 203: 30-38. DOI: 10.1016/j.ahj.2018.03.030.
48. Yoshida Y, Joshi P, Barri S, et al. Progression of retinopathy with glucagon-like peptide-1 receptor agonists with cardiovascular benefits in type 2 diabetes-a systematic review and meta-analysis[J/OL]. J Diabetes Complications, 2022, 36(8): 108255[2022-07-05]. https://pubmed.ncbi.nlm.nih.gov/35817678/. DOI: 10.1016/j.jdiacomp.2022.108255.
49. 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.
50. 楊文健, 龔宇, 李鳴一, 等. 利拉魯肽對糖尿病視網膜病變患者的臨床療效及作用機制研究[J]. 臨床和實驗醫學雜志, 2019, 18(14): 1541-1545. DOI: 10.3969/j.issn.1671-4695.2019.14.025.Yang WJ, Gong Y, Li MY, et al. Study on the effect and mechanism of liraglutide in diabetic retinopathy[J]. Journal of Clinical and Experimental Medicine, 2019, 18(14): 1541-1545. DOI: 10.3969/j.issn.1671-4695.2019.14.025.
51. A research study to look at how semaglutide compared to placebo affects diabetic eye disease in people with type 2 diabetes (FOCUS)[EB/OL]. (2019-12-01)[2022-04-24]. https://clinicaltrials.gov/ct2/show/NCT03811561.
52. 郭艷瓊, 彭晶, 李慶德, 等. 基于OpenFDA數據挖掘和分析司美格魯肽的不良事件報告信號[J]. 中國藥師, 2022, 25(3): 475-478. DOI: 10.19962/j.cnki.issn1008-049X.2022.03.016.Guo YQ, Peng J, Li QD, et al. Adverse drug events signal mining and analysis of semaglutide based on OpenFDA[J]. China Pharmacist, 2022, 25(3): 475-478. DOI: 10.19962/j.cnki.issn1008-049X.2022.03.016.
53. Varadhan L, Humphreys T, Walker AB, et al. The impact of improved glycaemic control with GLP-1 receptor agonist therapy on diabetic retinopathy[J/OL]. Diabetes Res Clin Pract, 2014, 103(3): e37-e39[2014-01-06]. https://pubmed.ncbi.nlm.nih.gov/24456992/. DOI: 10.1016/j.diabres.2013.12.041.
54. Bain SC, Klufas MA, Ho A, et al. Worsening of diabetic retinopathy with rapid improvement in systemic glucose control: a review[J]. Diabetes Obes Metab, 2019, 21(3): 454-466. DOI: 10.1111/dom.13538.
55. Wysham CH, Macconell LA, Maggs DG, et al. Five-year efficacy and safety data of exenatide once weekly: long-term results from the DURATION-1 randomized clinical trial[J]. Mayo Clin Proc, 2015, 90(3): 356-365. DOI: 10.1016/j.mayocp.2015.01.008.
56. Jingi AM, Tankeu AT, Ateba NA, et al. Mechanism of worsening diabetic retinopathy with rapid lowering of blood glucose: the synergistic hypothesis[J]. BMC Endocr Disord, 2017, 17(1): 63. DOI: 10.1186/s12902-017-0213-3.
57. Kennedy A, Frank RN. The influence of glucose concentration and hypoxia on VEGF secretion by cultured retinal cells[J]. Curr Eye Res, 2011, 36(2): 168-177. DOI: 10.3109/02713683.2010.521968.
58. Henricsson M, Berntorp K, Fernlund P, et al. Progression of retinopathy in insulin-treated type 2 diabetic patients[J]. Diabetes Care, 2002, 25(2): 381-385. DOI: 10.2337/diacare.25.2.381.
59. Casson RJ, Wood JPM, Osborne NN. Hypoglycaemia exacerbates ischaemic retinal injury in rats[J]. Br J Ophthalmol, 2004, 88(6): 816-820. DOI: 10.1136/bjo.2003.024661.
60. 陳燕鳳. T2DM患者血清胰高血糖素樣肽-1水平與糖尿病視網膜病變的相關性及其影響因素的分析[D]. 福州: 福建醫科大學, 2021.Chen YF. An analysis of correlation and it’s impacting factors between the serum glucagon-like peptide 1 level and diabetic retinopathy in patients with T2DM[D]. Fuzhou: Fujian Medical University, 2021.
61. Xu G, Kaneto H, Laybutt DR, et al. Downregulation of GLP-1 and GIP receptor expression by hyperglycemia: possible contribution to impaired incretin effects in diabetes[J]. Diabetes, 2007, 56(6): 1551-1558. DOI: 10.2337/db06-1033.

Previous Article
急性滲出性多形性卵黃樣黃斑病變1例
Next Article
Research progress on the bidirectional effect of autophagy on retinal neurovascular unit cells in diabetic retinopathy

Chinese Journal of Ocular Fundus Diseases

Research progress in prevention and cure of glucagon-like peptide-1 receptor agonists-1 receptor agonists for diabetic retinopathy

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content