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中华眼科医学杂志(电子版) ›› 2023, Vol. 13 ›› Issue (05) : 301 -305. doi: 10.3877/cma.j.issn.2095-2007.2023.05.009

综述

血脂异常与糖尿病视网膜病变的相关性研究进展
刘涵, 方晏红, 张蓝月, 李新星()   
  1. 402260 重庆大学附属江津医院眼科
  • 收稿日期:2023-09-01 出版日期:2023-10-28
  • 通信作者: 李新星
  • 基金资助:
    重庆市自然科学基金项目(cstc2020jcyj-msxmX0698、CSTB2023NSCQ-MSX0639); 重庆市江津区科学技术局项目(Y2023016)

Research progress of the correlation between dyslipidemia and diabetic retinopathy

Han Liu, Yanhong Fang, Lanyue Zhang, Xinxing Li()   

  1. Department of Ophthalmology, Chongqing University Jiangjin Hospital, Chongqing 402260, China
  • Received:2023-09-01 Published:2023-10-28
  • Corresponding author: Xinxing Li
引用本文:

刘涵, 方晏红, 张蓝月, 李新星. 血脂异常与糖尿病视网膜病变的相关性研究进展[J/OL]. 中华眼科医学杂志(电子版), 2023, 13(05): 301-305.

Han Liu, Yanhong Fang, Lanyue Zhang, Xinxing Li. Research progress of the correlation between dyslipidemia and diabetic retinopathy[J/OL]. Chinese Journal of Ophthalmologic Medicine(Electronic Edition), 2023, 13(05): 301-305.

糖尿病会引起糖尿病视网膜病变(DR)和糖尿病性黄斑水肿(DME)。两者均是成人失明和低视力的重要原因。血脂异常与DR及DME密切相关。传统血脂中,胆固醇、甘油三酯、极低密度脂蛋白及低密度脂蛋白可能是DR的危险因素,而高密度脂蛋白可能是其保护因素。非传统血脂中,载脂蛋白B、载脂蛋白C、载脂蛋白E、小而密低密度脂蛋白胆固醇及脂蛋白a可能是DR的危险因素,载脂蛋白A可能是其保护因素。血脂平衡和其比值有助于判断DR的发生与发展状态。多不饱和脂肪酸及其比值可能与DR的发病机制有关。他汀类和贝特类降脂药物均能在高糖环境下保护视网膜,并在抑制DR方面发挥潜在作用。本文中笔者对血脂异常与糖尿病视网膜病变的相关性研究进展进行综述。

Diabetes causes diabetic retinopathy (DR) and diabetic macular edema (DME), which are important causes of blindness and low vision in adults. The dyslipidemia is closely associated with DR and DME.Traditional blood lipids such as cholesterol, triglyceride, very low density lipoprotein and low-density lipoprotein may be risk factors for DR, while high-density lipoprotein may be protective. For non-traditional blood lipids, apolipoprotein B, C, E, small and dense low-density lipoprotein cholesterol and lipoprotein a may be risk factors for DR, while apolipoprotein A may be protective. Lipid balance/ratio is more helpful to determine the occurrence and progress of DR. Polyunsaturated fatty acids and their ratios may be related to the pathogenesis of DR. Lipid-lowering drugs statins and fibrates both protect the retina in high glucose environment and have a potential role in inhibiting DR.The correlation between blood lipids and DR was reviewed, aiming to provide a new strategy for DR integrated treatment.

表1 传统血脂、载脂蛋白及血脂平衡与糖尿病视网膜病变相关性的文献汇总表
类别 相关性 发表年份(年) 研究方法 病例数(例) 文献序号
传统血脂          
总胆固醇、高密度脂蛋白胆固醇 有关 2022 Meta分析 [8]
甘油三酯 有关 2022 横断面研究 131 [9]
低密度脂蛋白胆固醇 有关 2020 前瞻性病例对照研究 111例(176只眼) [10]
低密度脂蛋白胆固醇 有关 2020 病例对照研究 42 [11]
中间密度脂蛋白和极低密度脂蛋白 有关 2022 横断面研究 573 [12]
甘油三酯、总胆固醇和高密度脂蛋白胆固醇 无关 2018 Meta分析 [13]
整体血脂水平 无关 2013 回顾性研究 191 [14]
高密度脂蛋白、甘油三酯 无关 2022 临床随机试验 2468 [15]
低密度脂蛋白胆固醇 无关 2019 单样本随机对照试验 116 419 [7]
载脂蛋白          
载脂蛋白A-Ⅰ 负相关 2021 横断面研究 1027 [20]
载脂蛋白A-Ⅱ 负相关 2022 病例对照研究 157 [21]
载脂蛋白B 正相关 2021 病例对照研究 148 [22]
载脂蛋白C-Ⅰ 正相关 2018 蛋白质组学 [23]
载脂蛋白C-Ⅱ和C-Ⅲ 正相关 2023 蛋白质组学 [24]
载脂蛋白E 正相关 2017 动物实验 [26]
载脂蛋白E 正相关 2022 病例对照研究 667 [27]
血脂平衡/比值          
总胆固醇/低密度脂蛋白胆固醇、甘油三酯/高密度脂蛋白胆 固醇 危险因素 2017 横断面研究 1425 [37]
甘油三酯/高密度脂蛋白胆固醇 独立危险因素 2021 横断面研究 400 [38]
甘油三酯/高密度脂蛋白胆固醇 独立危险因素 2022 队列研究 420 [39]
载脂蛋白C-Ⅲ/载脂蛋白A-Ⅰ、载脂蛋白E/载脂蛋白A-Ⅰ 危险因素 2018 队列研究 1023 [40]
载脂蛋白B/载脂蛋白A-Ⅰ、载脂蛋白E/载脂蛋白C-Ⅱ、载 脂蛋白B/非高密度脂蛋白胆固醇 存在一定联系 2020 队列研究 1057 [29]
[1]
史雪辉,张丛,魏文斌. 关注糖尿病黄斑水肿的光学相干断层扫描分型及相关影像特征[J]. 中华眼科医学杂志(电子版)202111(1):1-7.
[2]
Mehta RK, Koirala P, Mallick RL, et al. Dyslipidemia in patients with type 2 diabetes mellitus in a tertiary care centre: a descriptive cross-sectional study[J]. JNMA J Nepal Med Assoc, 2021, 59(236): 305-309.
[3]
Kinuthia UM, Wolf A, Langmann T. Microglia and inflammatory responses in diabetic retinopathy[J]. Front Immunol, 2020, 11: 564077.
[4]
Busik JV. Lipid metabolism dysregulation in diabetic retinopathy[J]. J Lipid Res, 2021, 62: 100017.
[5]
Sasso FC, Pafundi PC, Gelso A, et al. High HDL cholesterol: A risk factor for diabetic retinopathy? Findings from NO BLIND study[J]. Diabetes Res Clin Pract, 2019, 150: 236-244.
[6]
中国血脂管理指南修订联合专家委员会. 中国血脂管理指南(2023年)[J]. 中国循环杂志202338(3):237-271.
[7]
Xuan J, Wang L, Fan L, et al. Systematic review and meta-analysis of the related factors for diabetic retinopathy[J]. Ann Palliat Med, 2022, 11(7): 2368-2381.
[8]
Wei Q, Qiu W, Liu Q, et al. Relationship between risk factors and macular thickness in patients with early diabetic retinopathy[J]. Int J Gen Med, 2022, 15: 6021-6029.
[9]
王凯悦,张新媛,聂瑶,等.脂类代谢异常与糖尿病视网膜微血管病变及神经元退行性改变的相关性研究[J]. 中华眼科医学杂志(电子版)202010(4):212-218.
[10]
Gungel H, Aral H, Erdenen F, et al. Central macular thickness in diabetic macular edema[J]. Acta Endocrinol (Buchar), 2020, 16(4): 417-425.
[11]
Julve J, Rossell J, Correig E, et al. Predictive value of the advanced lipoprotein profile and glycated proteins on diabetic retinopathy[J]. Nutrients, 2022, 14(19): 3932.
[12]
Zhou Y, Wang C, Shi K, et al. Relationship between dyslipidemia and diabetic retinopathy: A systematic review and meta-analysis[J]. Medicine (Baltimore), 2018, 97(36): e12283.
[13]
Cetin EN, Bulgu Y, Ozdemir S, et al. Association of serum lipid levels with diabetic retinopathy[J]. Int J Ophthalmol, 2013, 6(3): 346-349.
[14]
Hukportie DN, Li FR, Zhou R, et al. Lipid variability and risk of microvascular complications in Action to Control Cardiovascular Risk in Diabetes (ACCORD) trial: A post hoc analysis[J]. J Diabetes, 2022, 14(6): 365-376.
[15]
Emanuelsson F, Nordestgaard BG, Tybjerg-Hansen A, et al. Impact of LDL cholesterol on microvascular versus macrovascular disease: a mendelian randomization study[J]. J Am Coll Cardiol, 2019, 74(11): 1465-1476.
[16]
Mehta A, Shapiro MD. Apolipoproteins in vascular biology and atherosclerotic disease[J]. Nat Rev Cardiol, 2022, 19(3): 168-179.
[17]
Bhattacharjee PS, Huq TS, Potter V, et al. High-glucose-induced endothelial cell injury is inhibited by a Peptide derived from human apolipoprotein E[J]. PLoS One, 2012, 7(12): e52152.
[18]
Saucedo L, Pfister IB, Schild C, et al. Aqueous humor apolipoprotein concentration and severity of diabetic retinopathy in type 2 diabetes[J]. Mediators Inflamm, 2022, PMID: 2406322.
[19]
Van-Der-Vorst EPC. High-density lipoproteins and apolipoprotein A1[J]. Subcell Biochem, 2020, 94: 399-420.
[20]
Gao L, Zhang Y, Wang X, et al. Association of apolipoproteins A1 and B with type 2 diabetes and fasting blood glucose: a cross-sectional study[J]. BMC Endocr Disord, 2021, 21(1): 59.
[21]
Zhang X, Nie Y, Gong Z, et al. Plasma apolipoproteins predicting the occurrence and severity of diabetic retinopathy in patients with type 2 diabetes mellitus[J]. Front Endocrinol (Lausanne), 2022, 13: 915575.
[22]
Shi R, Lu Y, Liu D, et al. Association of serum apolipoprotein B with retinal neurovascular structural alterations in patients with type 2 diabetes: an optical coherence tomography angiography study[J]. Acta Diabetol, 2021, 58(12): 1673-1681.
[23]
Zou C, Han C, Zhao M, et al. Change of ranibizumab-induced human vitreous protein profile in patients with proliferative diabetic retinopathy based on proteomics analysis[J]. Clin Proteomics, 2018, 15: 12.
[24]
Kurooka N, Eguchi J, Wada J. Role of glycosylpho-sphatidylinositol-anchored high-density lipoprotein binding protein 1 in hypertriglyceridemia and diabetes[J].J Diabetes Investig, 2023, 14(10): 1148-1156.
[25]
Overgaard M, Ravnsborg T, Lohse Z, et al. Apolipoprotein D and transthyretin are reduced in female adolescent offspring of women with type 1 diabetes: The EPICOM study[J]. Diabet Med, 2022, 39(7): e14776.
[26]
Masuda T, Shimazawa M, Hashimoto Y, et al. Apolipoprotein E2 and E3, but not E4, promote retinal pathologic neovascularization[J]. Invest Ophthalmol Vis Sci, 2017, 58(2): 1208-1217.
[27]
Liu Z, Shao M, Ren J, et al. Association between increased lipid profiles and risk of diabetic retinopathy in a population-based case-control study[J]. J Inflamm Res, 2022, 15: 3433-3446.
[28]
Cegla J, Neely RDG, France M, et al. HEART UK consensus statement on Lipoprotein(a): A call to action [J]. Atherosclerosis, 2019, 291: 62-70.
[29]
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.
[30]
Tu WJ, Liu H, Liu Q, et al. Association between serum lipoprotein(a)and diabetic retinopathy in han Chinese patients with type 2 diabetes[J]. J Clin Endocrinol Metab, 2017, 102(7): 2525-2532.
[31]
Nishikura T, Koba S, Yokota Y, et al. Elevated small dense low-density lipoprotein cholesterol as a predictor for future cardiovascular events in patients with stable coronary artery disease[J]. J Atheroscler Thromb, 2014, 21(8): 755-67.
[32]
Nakayama A, Morita H, Sato T, et al. Small dense low-density lipoprotein cholesterol is a potential marker for predicting laser treatment for retinopathy in diabetic patients[J]. J Atheroscler Thromb, 2022, 29(5): 678-691.
[33]
Eid S, Sas KM, Abcouwer SF, et al. New insights into the mechanisms of diabetic complications: role of lipids and lipid metabolism[J]. Diabetologia, 2019, 62(9): 1539-1549.
[34]
Gong Y, Fu Z, Liegl R, et al. ω-3 and ω-6 long-chain PUFAs and their enzymatic metabolites in neovascular eye diseases[J]. Am J Clin Nutr, 2017, 106(1): 16-26.
[35]
Sala-Vila A, Díaz-López A, Valls-Pedret C, et al. Dietary marine ω-3 fatty acids and incident sight-threatening retinopathy in middle-aged and older individuals with type 2 diabetes: prospective investigation from the PREDIMED trial[J]. JAMA Ophthalmol, 2016, 134(10): 1142-1149.
[36]
Zhao S, Jin D, Wang S, et al. Serum ω-6/ω-3 polyunsaturated fatty acids ratio and diabetic retinopathy: A propensity score matching based case-control study in China[J]. EClinical Medicine, 2021, 39: 101089.
[37]
Raman R, Ganesan S, Pal SS, et al. Incidence and progression of diabetic retinopathy in urban india: sankara nethralaya-diabetic retinopathy epidemiology and molecular genetics study (SN-DREAMS Ⅱ), Report 1[J]. Ophthalmic Epidemiol, 2017, 24(5): 294-302.
[38]
王夏叶,刘莹,徐丽霞. 血脂指标比值对2型糖尿病视网膜病变的预测价值[J]. 中国卫生检验杂志202131(7):859-861,865.
[39]
胡邵宁,朱书渊,魏燕斌. 血清脂蛋白a水平及三酰甘油与高密度脂蛋白胆固醇比值与2型糖尿病视网膜病变的相关性研究[J]. 中国卫生检验杂志202232(2):205-208.
[40]
Zhang Q, Hu J, Hu Y, et al. Relationship between serum apolipoproteins levels and retinopathy risk in subjects with type 2 diabetes mellitus[J]. Acta Diabetol, 2018, 55(7): 681-689.
[41]
Kang EY, Chen TH, Garg SJ, et al. Association of statin therapy with prevention of vision-threatening diabetic retinopathy[J]. JAMA Ophthalmol, 2019, 137(4): 363-371.
[42]
Nielsen SF, Nordestgaard BG. Statin use before diabetes diagnosis and risk of microvascular disease: a nationwide nested matched study[J]. Lancet Diabetes Endocrinol, 2014, 2(11): 894-900.
[43]
Chatziralli IP. The role of dyslipidemia control in the progression of diabetic retinopathy in patients with type 2 diabetes mellitus[J]. Diabetes Ther, 2017, 8(2): 209-212.
[44]
Tuuminen R, Sahanne S, Loukovaara S. Low intravitreal angiopoietin-2 and VEGF levels in vitrectomized diabetic patients with simvastatin treatment[J]. Acta Ophthalmol, 2014, 92(7): 675-681.
[45]
Pranata R, Vania R, Victor AA. Statin reduces the incidence of diabetic retinopathy and its need for intervention: A systematic review and meta-analysis[J]. Eur J Ophthalmol, 2021, 31(3): 1216-1224.
[46]
Pearsall EA, Cheng R, Matsuzaki S, et al. Neuroprotective effects of PPARα in retinopathy of type 1 diabetes[J]. PLoS One, 2019, 14(2): e0208399.
[47]
Ruan Y, Jiang S, Musayeva A, et al. Oxidative stress and vascular dysfunction in the retina: therapeutic strategies[J]. Antioxidants (Basel), 2020, 9(8): 761.
[48]
Tomita Y, Lee D, Tsubota K, et al. PPARα agonist oral therapy in diabetic retinopathy[J]. Biomedicines, 2020, 8(10): 433.
[49]
Action to Control Cardiovascular Risk in Diabetes Follow-On (ACCORDION) Eye Study Group and the Action to Control Cardiovascular Risk in Diabetes Follow-On (ACCORDION) Study Group. Persistent effects of intensive glycemic control on retinopathy in type 2 diabetes in the action to control cardiovascular risk in diabetes (ACCORD) Follow-On Study[J]. Diabetes Care, 2016, 39(7): 1089-100.
[50]
Keech A, Simes RJ, Barter P, et al. Effects of long-term fenofibrate therapy on cardiovascular events in 9795 people with type 2 diabetes mellitus (the FIELD study): randomised controlled trial[J]. Lancet, 2005, 366(9500): 1849-1861.
[51]
Zhou X, Ai S, Chen Z, et al. Probucol promotes high glucose-induced proliferation and inhibits apoptosis by reducing reactive oxygen species generation in Müller cells[J]. Int Ophthalmol, 2019, 39(12): 2833-2842.
[52]
Liu HW, Luo Y, Zhou YF, et al. Probucol prevents diabetes-induced retinal neuronal degeneration through upregulating Nrf2[J]. Biomed Res Int, 2022, PMID: 32149102.
[53]
Liu H, Cai M. Effect of probucol on hemodynamics, rheology and blood lipid of diabetic retinopathy[J]. Exp Ther Med, 2018, 15(4): 3809-3814.
[54]
Mazzoli V, Zhong LH, Dang VT, et al. Characterization of retinal microvascular complications and the effects of endoplasmic reticulum stress in mouse models of diabetic atherosclerosis[J]. Invest Ophthalmol Vis Sci, 2020, 61(10): 49.
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