The status and progress of relationship between dyslipidemia and diabetic retinopathy_Chinese Journal of Ocular Fundus Diseases

Authors：

HanChangjing ,  ZhengZhi

Department of Ophthalmology, The First People′s Hospital of Shanghai, Shanghai JiaoTong University, Shanghai 200080, China;

Corresponding author：

ZhengZhi, Email: zhengzhi139@163.com

Keywords：

Diabetic retinopathy/etiology; Dyslipidemias; Review

DOI：

10.3760/cma.j.issn.1005-1015.2016.02.025

Video：

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Dyslipidemia plays an important role in the pathogenesis of diabetic retinopathy (DR).Apreliminary study found that low-density lipoprotein cholesterol, apolipoprotein (Apo)Band ApoB/ Apo A1 ratio were positively correlated with DR, while high-density lipoprotein cholesterol, Apo A1 was negatively correlated with DR and proliferative DR. Reducing the blood fats to be helpful to DR control. However, the mechanism of hyperlipidemia in the pathogenesis of DR, the reason of dyslipidemia in diabetic patients and the interaction between hyperglycemia and hyperlipidemia in DR are not clear yet. Moreover, there is no predictive indicators related to blood lipid for DR. Understanding the relationship between dyslipidemia and DR can provide definite evidence for fat-reducing therapy for DR control.

Citation： HanChangjing, ZhengZhi. The status and progress of relationship between dyslipidemia and diabetic retinopathy. Chinese Journal of Ocular Fundus Diseases, 2016, 32(2): 210-212. doi: 10.3760/cma.j.issn.1005-1015.2016.02.025 Copy

1.	Ozer PA,Unlu N,Demir MN,et al.Serum lipid profile in diabetic macular edema[J].JDiabetes Complications, 2009, 23(4):244-248.DOI:10.1016/j.jdiacomp.2007.12.004.
2.	Sun CY，Lee CC, Hsieh MF, et al. Clinical association of circulating VEGF-B levels with hyperlipidemia and target organ damage in type 2 diabetic patients[J].JBiol Regul Homeost Agents, 2014, 28(2):225-236.
3.	Lim LS, Wong TY. Lipids and diabetic retinopathy[J]. Expert Opin Biol Ther, 2012, 12(1):93-105. DOI: 10.1517/14712598.2012.641531.
4.	Benarous R, Sasongko MB, Qureshi S, et al. Differential association of serum lipids with diabetic retinopathy and diabetic macular edema[J]. Invest Ophthalmol Vis Sc, 2011, 52(10):7464-7469. DOI: 10.1167/iovs.11-7598.
5.	Jrgensen JS, Jrgensen TM, Green A, et al. Long-term associations between serum lipids and panretinal photocoagulation in type 1 diabetes[J]. Curr Eye Res, 2013, 38(8):889-893. DOI: 10.3109/02713683.2013.786094.
6.	Chowdhury TA, Hopkins D, Dodson PM, et al. The role of serum lipids in exudative diabetic maculopathy: is thereaplace for lipid lowering therapy? [J].Eye (Lond), 2002, 16(6):689-693.
7.	Hu A, Luo Y, Li T, et al. Low serum apolipoprotein A1/B ratio is associated with proliferative diabetic retinopathy in type 2 diabetes[J]. Graefe′s Arch Clin Exp Ophthalmol, 2012, 250(7):957-962. DOI: 10.1007/s00417-011-1855-x.
8.	Miljanovic B, Glynn RJ, Nathan DM, et al.A prospective study of serum lipids and risk of diabetic macular edema in type 1 diabetes[J]. Diabetes, 2004, 53(11):2883-2892.
9.	Chang YC, Wu WC. Dyslipidemia and diabetic retinopathy[J]. Rev Diabet Stud, 2013,10(2-3):121-132. DOI: 10.1900/RDS.2013.10.121. Epub 2013 Aug 10.
10.	Klein R, Marino EK, Kuller LH, et al. The relation of atherosclerotic cardiovascular disease to retinopathy in people with diabetes in the Cardiovascular Health Study[J]. BrJOphthalmol, 2002, 86(1):84-90.
11.	Wong TY, Cheung N, Tay WT, et al. Prevalence and risk factors for diabetic retinopathy: the Singapore Malay Eye Study[J]. Ophthalmology, 2008, 115(11):1869-1875. DOI: 10.1016/j.ophtha.2008.05.014.
12.	Chew EY, Klein ML, Ferris FL 3rd, et al. Association of elevated serum lipid levels with retinal hard exudate in diabetic retinopathy. Early Treatment Diabetic Retinopathy Study (ETDRS) Report 22[J]. Arch Ophthalmol, 1996, 114(9):1079-1084.
13.	Van Leiden HA, Dekker JM, Moll AC, et al. Blood pressure, lipids, and obesity are associated with retinopathy: the Hoorn Study[J]. Diabetes Care, 2002, 25(8):1320-1325.
14.	Rema M, Srivastava BK, Anitha B, et al. Association of serum lipids with diabetic retinopathy in urban South Indians - the Chennai Urban Rural Epidemiology Study (CURES) Eye Study-2[J]. Diabet Med, 2006, 23(9):1029-1036.
15.	Sasaki M, Kawashima M, Kawasaki R, et al. Association of serum lipids with macular thickness and volume in type 2 diabetes without diabetic macular edema[J]. Invest Ophthalmol Vis Sci, 2014, 55(3):1749-1753. DOI: 10.1167/iovs.13-13035.
16.	Mohan R, Mohan V, Susheela L, et al. Increased LDL cholesterol in non-insulin-dependent diabetics with maculopathy[J]. Acta Diabetol Lat, 1984, 21(1):85-89.
17.	Sasaki M, Kawasaki R, Noonan JE, et al. Quantitative measurement of hard exudates in patients with diabetes and their associations with serum lipid levels.[J]. Invest Ophthalmol Vis Sci, 2013, 54(8):5544-5550. DOI: 10.1167/iovs.13-11849.
18.	Morton J, Zoungas S, Li Q, et al. Low HDL cholesterol and the risk of diabetic nephropathy and retinopathy: results of the ADVANCE study[J]. Diabetes Care, 2012, 35(11):2201-2206. DOI: 10.2337/dc12-0306.
19.	Toth PP, Simko RJ, Palli SR, et al. The impact of serum lipids on risk for microangiopathy in patients with type 2 diabetes mellitus[J]. Cardiovasc Diabetol, 2012, 11:109. DOI:10.1186/1475-2840-11-109.
20.	Kawai S, Nakajima T, Hokari S, et al. Apolipoprotein A-I concentration in tears in diabetic retinopathy[J]. Ann Clin Biochem, 2002, 39(Pt 1):56-61.
21.	Klein RL, McHenry MB, Lok KH,et al. Apolipoprotein C-Ⅲ protein concentrations and gene polymorphisms in type 1 diabetes: associations with microvascular disease complications in the DCCT/EDIC cohort[J].JDiabetes Complications, 2005, 19(1):18-25.
22.	Santos A, Salguero ML, Gurrola C, et al. The epsilon4 allele of apolipoproteinEgene isapotential risk factor for the severity of macular edema in type 2 diabetic Mexican patients[J]. Ophthalmic Genet, 2002, 23(1):13-19.
23.	Simo R, Higuera M, Garcia-Ramirez M, et al. Elevation of apolipoprotein A-I and apolipoproteinHlevels in the vitreous fluid and overexpression in the retina of diabetic patients[J]. Arch Ophthalmol, 2008, 126(8):1076-1081. DOI: 10.1001/archopht.126.8.1076.
24.	Sasongko MB, Wong TY, Nguyen TT, et al. Serum apolipoprotein AI andBare stronger biomarkers of diabetic retinopathy than traditional lipids[J]. Diabetes Care, 2011, 34(2):474-479. DOI: 10.2337/dc10-0793.
25.	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.
26.	McKeage K, Keating GM. Fenofibrate:areview of its use in dyslipidaemia[J]. Drugs, 2011,71(14): 1917-1946. DOI: 10.2165/11208090-000000000-00000.
27.	Simo R, Hemandez C. Prevention and treatment of diabetic retinopathy：evidence from large，randomized trials. The emerging role of fenofibrate[J]. Rev Recent Clin Trials, 2012,7(1): 71-80.
28.	Keech AC, Mitchell P, Summanen PA, et al. Effect of fenofibrate on the need for laser treatment for diabetic retinopathy(FIELD study):a randomised controlled trial[J]. Lancet, 2007, 370(9600):1687-1697.
29.	Miranda S, Gonzalez-Rodrtguez A, Garcia-Ramirez M, et al. Beneficial effects of fenofibrate in retinal pigment epithelium by the modulation of stress and survival signaling under diabetic conditions[J].JCell Physiol,2012,227(6):2352-2362. DOI: 10.1002/jcp.22970.
30.	Baynes JW, Thorpe SR. Glycoxidation and lipoxidation in atherogenesis[J]. Free Radic Biol Med, 2000, 28(12):1708-1716.
31.	Klein R, Klein BE. Are individuals with diabetes seeing better?-along- term epidemiological perspective[J]. Diabetes, 2010, 59(8):1853-1860. DOI: 10.2337/db09-1904.
32.	Shah PK, Kaul S, Nilsson J, et al. Exploiting the vascular protective effects of high-density lipoprotein and its apolipoproteins: an idea whose time for testing is coming, part Ⅱ [J]. Circulation, 2001, 104(20):2498-2502.
33.	Davidson MH. Apolipoprotein measurements: is more widespread use clinically indicated? [J].Clin Cardiol, 2009, 32(9):482-486. DOI: 10.1002/clc.20559.
34.	Hill SA, McQueen MJ. Reverse cholesterol transport-a review of the process and its clinical implications[J]. Clin Biochem, 1997, 30(7):517-525.
35.	McQueen MJ, Hawken S, Wang X, et al. Lipids, lipoproteins, and apolipoproteins as risk markers of myocardial infarction in 52 countries (the INTERHEART study):acase-control study[J]. Lancet, 2008, 372(9634):224-233. DOI: 10.1016/S0140-6736(08)61076-4.
36.	Marcovina S, Packard CJ. Measurement and meaning of apolipoprotein AI and apolipoproteinBplasma levels[J].JIntern Med, 2006, 259(5):437-446.

1. Ozer PA,Unlu N,Demir MN,et al.Serum lipid profile in diabetic macular edema[J].JDiabetes Complications, 2009, 23(4):244-248.DOI:10.1016/j.jdiacomp.2007.12.004.
2. Sun CY，Lee CC, Hsieh MF, et al. Clinical association of circulating VEGF-B levels with hyperlipidemia and target organ damage in type 2 diabetic patients[J].JBiol Regul Homeost Agents, 2014, 28(2):225-236.
3. Lim LS, Wong TY. Lipids and diabetic retinopathy[J]. Expert Opin Biol Ther, 2012, 12(1):93-105. DOI: 10.1517/14712598.2012.641531.
4. Benarous R, Sasongko MB, Qureshi S, et al. Differential association of serum lipids with diabetic retinopathy and diabetic macular edema[J]. Invest Ophthalmol Vis Sc, 2011, 52(10):7464-7469. DOI: 10.1167/iovs.11-7598.
5. Jrgensen JS, Jrgensen TM, Green A, et al. Long-term associations between serum lipids and panretinal photocoagulation in type 1 diabetes[J]. Curr Eye Res, 2013, 38(8):889-893. DOI: 10.3109/02713683.2013.786094.
6. Chowdhury TA, Hopkins D, Dodson PM, et al. The role of serum lipids in exudative diabetic maculopathy: is thereaplace for lipid lowering therapy? [J].Eye (Lond), 2002, 16(6):689-693.
7. Hu A, Luo Y, Li T, et al. Low serum apolipoprotein A1/B ratio is associated with proliferative diabetic retinopathy in type 2 diabetes[J]. Graefe′s Arch Clin Exp Ophthalmol, 2012, 250(7):957-962. DOI: 10.1007/s00417-011-1855-x.
8. Miljanovic B, Glynn RJ, Nathan DM, et al.A prospective study of serum lipids and risk of diabetic macular edema in type 1 diabetes[J]. Diabetes, 2004, 53(11):2883-2892.
9. Chang YC, Wu WC. Dyslipidemia and diabetic retinopathy[J]. Rev Diabet Stud, 2013,10(2-3):121-132. DOI: 10.1900/RDS.2013.10.121. Epub 2013 Aug 10.
10. Klein R, Marino EK, Kuller LH, et al. The relation of atherosclerotic cardiovascular disease to retinopathy in people with diabetes in the Cardiovascular Health Study[J]. BrJOphthalmol, 2002, 86(1):84-90.
11. Wong TY, Cheung N, Tay WT, et al. Prevalence and risk factors for diabetic retinopathy: the Singapore Malay Eye Study[J]. Ophthalmology, 2008, 115(11):1869-1875. DOI: 10.1016/j.ophtha.2008.05.014.
12. Chew EY, Klein ML, Ferris FL 3rd, et al. Association of elevated serum lipid levels with retinal hard exudate in diabetic retinopathy. Early Treatment Diabetic Retinopathy Study (ETDRS) Report 22[J]. Arch Ophthalmol, 1996, 114(9):1079-1084.
13. Van Leiden HA, Dekker JM, Moll AC, et al. Blood pressure, lipids, and obesity are associated with retinopathy: the Hoorn Study[J]. Diabetes Care, 2002, 25(8):1320-1325.
14. Rema M, Srivastava BK, Anitha B, et al. Association of serum lipids with diabetic retinopathy in urban South Indians - the Chennai Urban Rural Epidemiology Study (CURES) Eye Study-2[J]. Diabet Med, 2006, 23(9):1029-1036.
15. Sasaki M, Kawashima M, Kawasaki R, et al. Association of serum lipids with macular thickness and volume in type 2 diabetes without diabetic macular edema[J]. Invest Ophthalmol Vis Sci, 2014, 55(3):1749-1753. DOI: 10.1167/iovs.13-13035.
16. Mohan R, Mohan V, Susheela L, et al. Increased LDL cholesterol in non-insulin-dependent diabetics with maculopathy[J]. Acta Diabetol Lat, 1984, 21(1):85-89.
17. Sasaki M, Kawasaki R, Noonan JE, et al. Quantitative measurement of hard exudates in patients with diabetes and their associations with serum lipid levels.[J]. Invest Ophthalmol Vis Sci, 2013, 54(8):5544-5550. DOI: 10.1167/iovs.13-11849.
18. Morton J, Zoungas S, Li Q, et al. Low HDL cholesterol and the risk of diabetic nephropathy and retinopathy: results of the ADVANCE study[J]. Diabetes Care, 2012, 35(11):2201-2206. DOI: 10.2337/dc12-0306.
19. Toth PP, Simko RJ, Palli SR, et al. The impact of serum lipids on risk for microangiopathy in patients with type 2 diabetes mellitus[J]. Cardiovasc Diabetol, 2012, 11:109. DOI:10.1186/1475-2840-11-109.
20. Kawai S, Nakajima T, Hokari S, et al. Apolipoprotein A-I concentration in tears in diabetic retinopathy[J]. Ann Clin Biochem, 2002, 39(Pt 1):56-61.
21. Klein RL, McHenry MB, Lok KH,et al. Apolipoprotein C-Ⅲ protein concentrations and gene polymorphisms in type 1 diabetes: associations with microvascular disease complications in the DCCT/EDIC cohort[J].JDiabetes Complications, 2005, 19(1):18-25.
22. Santos A, Salguero ML, Gurrola C, et al. The epsilon4 allele of apolipoproteinEgene isapotential risk factor for the severity of macular edema in type 2 diabetic Mexican patients[J]. Ophthalmic Genet, 2002, 23(1):13-19.
23. Simo R, Higuera M, Garcia-Ramirez M, et al. Elevation of apolipoprotein A-I and apolipoproteinHlevels in the vitreous fluid and overexpression in the retina of diabetic patients[J]. Arch Ophthalmol, 2008, 126(8):1076-1081. DOI: 10.1001/archopht.126.8.1076.
24. Sasongko MB, Wong TY, Nguyen TT, et al. Serum apolipoprotein AI andBare stronger biomarkers of diabetic retinopathy than traditional lipids[J]. Diabetes Care, 2011, 34(2):474-479. DOI: 10.2337/dc10-0793.
25. 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.
26. McKeage K, Keating GM. Fenofibrate:areview of its use in dyslipidaemia[J]. Drugs, 2011,71(14): 1917-1946. DOI: 10.2165/11208090-000000000-00000.
27. Simo R, Hemandez C. Prevention and treatment of diabetic retinopathy：evidence from large，randomized trials. The emerging role of fenofibrate[J]. Rev Recent Clin Trials, 2012,7(1): 71-80.
28. Keech AC, Mitchell P, Summanen PA, et al. Effect of fenofibrate on the need for laser treatment for diabetic retinopathy(FIELD study):a randomised controlled trial[J]. Lancet, 2007, 370(9600):1687-1697.
29. Miranda S, Gonzalez-Rodrtguez A, Garcia-Ramirez M, et al. Beneficial effects of fenofibrate in retinal pigment epithelium by the modulation of stress and survival signaling under diabetic conditions[J].JCell Physiol,2012,227(6):2352-2362. DOI: 10.1002/jcp.22970.
30. Baynes JW, Thorpe SR. Glycoxidation and lipoxidation in atherogenesis[J]. Free Radic Biol Med, 2000, 28(12):1708-1716.
31. Klein R, Klein BE. Are individuals with diabetes seeing better?-along- term epidemiological perspective[J]. Diabetes, 2010, 59(8):1853-1860. DOI: 10.2337/db09-1904.
32. Shah PK, Kaul S, Nilsson J, et al. Exploiting the vascular protective effects of high-density lipoprotein and its apolipoproteins: an idea whose time for testing is coming, part Ⅱ [J]. Circulation, 2001, 104(20):2498-2502.
33. Davidson MH. Apolipoprotein measurements: is more widespread use clinically indicated? [J].Clin Cardiol, 2009, 32(9):482-486. DOI: 10.1002/clc.20559.
34. Hill SA, McQueen MJ. Reverse cholesterol transport-a review of the process and its clinical implications[J]. Clin Biochem, 1997, 30(7):517-525.
35. McQueen MJ, Hawken S, Wang X, et al. Lipids, lipoproteins, and apolipoproteins as risk markers of myocardial infarction in 52 countries (the INTERHEART study):acase-control study[J]. Lancet, 2008, 372(9634):224-233. DOI: 10.1016/S0140-6736(08)61076-4.
36. Marcovina S, Packard CJ. Measurement and meaning of apolipoprotein AI and apolipoproteinBplasma levels[J].JIntern Med, 2006, 259(5):437-446.

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