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Published in: BMC Endocrine Disorders 1/2024

Open Access 01-12-2024 | Diabetic Retinopathy | Research

Association between HDL cholesterol with diabetic retinopathy in diabetic patients: a cross-sectional retrospective study

Authors: Wuping Xu, Xuedong Xu, Min Zhang, Chiping Sun

Published in: BMC Endocrine Disorders | Issue 1/2024

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Abstract

Objective

Diabetic patients are often comorbid with dyslipidemia, however, the relationship between high-density lipoprotein cholesterol(HDL-C) and diabetic retinopathy (DR) in the adult diabetic population remains to be fully elucidated.The aim of this study is to evaluate the associations between HDL-C and DR in the United States adults with diabetes.

Methods

A total of 1708 participants from the National Health and Nutrition Examination Survey (NHANES) 2005–2008 were enrolled in the present study. Fundus images of all study subjects were captured and evaluated using a digital camera and an ophthalmic digital imaging system, and the diagnosis of DR was made by the severity scale of the Early Treatment Diabetic Retinopathy Study (ETDRS).Roche Diagnostics were used to measure serum HDL-C concentration. The relationship of DR with HDL-C was investigated using multivariable logistic regression. The potential non-line correlation was explored with smooth curve fitting approach.

Results

The fully-adjusted model showed that HDL-C positively correlated with DR(OR:1.69, 95%CI: 1.25–2.31).However, an inverted U-shaped association between them was observed by applying the smooth curve fitted method. The inflection point of HDL-C(1.99mmol/l) was calculated by utilizing the two-piecewise logistic regression model. In the subgroup analysis, the inverted U-shaped nonlinear correlation between HDL-C and DR was also found in female, Non-Hispanic White, and lower age groups.

Conclusion

Our study revealed an inverted U-shaped positive relationship between HDL-C and DR.The findings may provide us with a more comprehensive understanding of the association between HDL-C and DR.
Literature
2.
go back to reference Karaa A. A Goldstein 2015 The spectrum of clinical presentation, diagnosis, and management of mitochondrial forms of diabetes. Pediatr Diabetes 16 1 1–9 PMID:25330715.CrossRefPubMed Karaa A. A Goldstein 2015 The spectrum of clinical presentation, diagnosis, and management of mitochondrial forms of diabetes. Pediatr Diabetes 16 1 1–9 PMID:25330715.CrossRefPubMed
3.
go back to reference Ogurtsova K, da Rocha Fernandes JD, Huang Y, et al. IDF DiabetesAtlas: global estimates for the prevalence of diabetes for 2015 and2040. Diabetes Res Clin Pract. 2017;128:40. -50.PMID: 28437734.CrossRefPubMed Ogurtsova K, da Rocha Fernandes JD, Huang Y, et al. IDF DiabetesAtlas: global estimates for the prevalence of diabetes for 2015 and2040. Diabetes Res Clin Pract. 2017;128:40. -­50.PMID: 28437734.CrossRefPubMed
4.
go back to reference Costacou T, Evans RW, Orchard TJ. High-density lipoprotein cholesterol in diabetes: is higher always better? J Clin Lipidol. 2011;5(5):387–94. PMID: 21981840.CrossRefPubMedPubMedCentral Costacou T, Evans RW, Orchard TJ. High-density lipoprotein cholesterol in diabetes: is higher always better? J Clin Lipidol. 2011;5(5):387–94. PMID: 21981840.CrossRefPubMedPubMedCentral
5.
go back to reference Williams AN, Conway BN. Effect of high density lipoprotein cholesterol on the relationship of serum iron and hemoglobin with kidney function in diabetes. J Diabetes Complications. 2017;31(6):958–63. PMID: 28410926.CrossRefPubMedPubMedCentral Williams AN, Conway BN. Effect of high density lipoprotein cholesterol on the relationship of serum iron and hemoglobin with kidney function in diabetes. J Diabetes Complications. 2017;31(6):958–63. PMID: 28410926.CrossRefPubMedPubMedCentral
6.
go back to reference Wang W, Lo ACY. Diabetic Retinopathy: Pathophysiology and Treatments. Int J Mol Sci 2018, 19(6).PMID: 29925789. Wang W, Lo ACY. Diabetic Retinopathy: Pathophysiology and Treatments. Int J Mol Sci 2018, 19(6).PMID: 29925789.
7.
go back to reference Nagda D, Mitchell W, Zebardast N. The functional burden of diabetic retinopathy in the United States. Graefe’s Archiv Clin Exp Ophthalmol. 2021;259(10):2977. 2986.PMID: 33914161.CrossRef Nagda D, Mitchell W, Zebardast N. The functional burden of diabetic retinopathy in the United States. Graefe’s Archiv Clin Exp Ophthalmol. 2021;259(10):2977. ­2986.PMID: 33914161.CrossRef
8.
go back to reference Demir M, Oba E, Dirim B, Ozdal E, Can E. Retraction Note: Central macular thickness in patients with type 2 diabetes mellitus without clinical retinopathy. BMC ophthalmology 2015, 15:167.PMID: 26572602. Demir M, Oba E, Dirim B, Ozdal E, Can E. Retraction Note: Central macular thickness in patients with type 2 diabetes mellitus without clinical retinopathy. BMC ophthalmology 2015, 15:167.PMID: 26572602.
9.
go back to reference Rai BB, Morley MG, Bernstein PS, Maddess T. Pattern of vitreo-retinal diseases at the national referral hospital in Bhutan: a retrospective, hospital-based study. BMC ophthalmology 2020, 20(1):51.PMID: 32054472. Rai BB, Morley MG, Bernstein PS, Maddess T. Pattern of vitreo-retinal diseases at the national referral hospital in Bhutan: a retrospective, hospital-based study. BMC ophthalmology 2020, 20(1):51.PMID: 32054472.
10.
go back to reference Nittala MG, Keane PA, Zhang K, Sadda SR. Risk factors for proliferative diabetic retinopathy in a. Latino Am Popul Retina. 2014;34(8):1594–9. PMID:24662751. Nittala MG, Keane PA, Zhang K, Sadda SR. Risk factors for proliferative diabetic retinopathy in a. Latino Am Popul Retina. 2014;34(8):1594–9. PMID:24662751.
11.
go back to reference Chatziralli IP. The role of Dyslipidemia Control in the Progression of Diabetic Retinopathy in patients with type 2 diabetes Mellitus. Diabetes Ther. 2017;8(2):209–12. PMID: 28247336.CrossRefPubMedPubMedCentral Chatziralli IP. The role of Dyslipidemia Control in the Progression of Diabetic Retinopathy in patients with type 2 diabetes Mellitus. Diabetes Ther. 2017;8(2):209–12. PMID: 28247336.CrossRefPubMedPubMedCentral
12.
go back to reference Chen X, Meng Y, Li J, She H, Zhao L, Zhang J, Peng Y, Shang K, Zhang Y, Gu X et al. Serum uric acid concentration is associated with hypertensive retinopathy in hypertensive chinese adults. BMC ophthalmology : 2017, 17(1):83.PMID: 28577362. Chen X, Meng Y, Li J, She H, Zhao L, Zhang J, Peng Y, Shang K, Zhang Y, Gu X et al. Serum uric acid concentration is associated with hypertensive retinopathy in hypertensive chinese adults. BMC ophthalmology : 2017, 17(1):83.PMID: 28577362.
13.
go back to reference Kong X, Wang J, Gao G, Tan M, Ding B, Li H, Ma J. Association between free thyroxine levels and Diabetic Retinopathy in Euthyroid patients with type 2 diabetes Mellitus. Endocr Res. 2020;45(2):111–8. PMID: 31773995.CrossRefPubMed Kong X, Wang J, Gao G, Tan M, Ding B, Li H, Ma J. Association between free thyroxine levels and Diabetic Retinopathy in Euthyroid patients with type 2 diabetes Mellitus. Endocr Res. 2020;45(2):111–8. PMID: 31773995.CrossRefPubMed
14.
go back to reference Selvan H, Azad SV, Ramesh P, Bhakthaganesh K. Retinopathy in severe aplastic anaemia. BMJ case reports 2019, 12(10).PMID: 31615780. Selvan H, Azad SV, Ramesh P, Bhakthaganesh K. Retinopathy in severe aplastic anaemia. BMJ case reports 2019, 12(10).PMID: 31615780.
15.
go back to reference Moriya T, Tanaka S, Kawasaki R, Ohashi Y, Akanuma Y, Yamada N, Sone H, Yamashita H, Katayama S. Diabetic retinopathy and microalbuminuria can predict macroalbuminuria and renal function decline in Japanese type 2 diabetic patients: Japan Diabetes complications Study. Diabetes Care. 2013;36(9):2803–9. PMID: 23620478.CrossRefPubMedPubMedCentral Moriya T, Tanaka S, Kawasaki R, Ohashi Y, Akanuma Y, Yamada N, Sone H, Yamashita H, Katayama S. Diabetic retinopathy and microalbuminuria can predict macroalbuminuria and renal function decline in Japanese type 2 diabetic patients: Japan Diabetes complications Study. Diabetes Care. 2013;36(9):2803–9. PMID: 23620478.CrossRefPubMedPubMedCentral
16.
go back to reference Sen D, Ghosh S, Roy D. Correlation of C-reactive protein and body mass index with diabetic retinopathy in Indian population. Diabetes Metabolic Syndrome. 2015;9(1):28–9. PMID: 25470633.CrossRefPubMed Sen D, Ghosh S, Roy D. Correlation of C-reactive protein and body mass index with diabetic retinopathy in Indian population. Diabetes Metabolic Syndrome. 2015;9(1):28–9. PMID: 25470633.CrossRefPubMed
17.
go back to reference Wang X, Dong Y, Qi X, Huang C, Hou L. Cholesterol levels and risk of hemorrhagic stroke: a systematic review and meta-analysis. Stroke. 2013;44(7):1833–9. PMID: 23704101.CrossRefPubMed Wang X, Dong Y, Qi X, Huang C, Hou L. Cholesterol levels and risk of hemorrhagic stroke: a systematic review and meta-analysis. Stroke. 2013;44(7):1833–9. PMID: 23704101.CrossRefPubMed
18.
go back to reference Lee MY, Hsiao PJ, Huang JC, Hsu WH, Chen SC, Chang JM, Shin SJ, ASSOCIATIONS BETWEEN TRIGLYCERIDE/HIGH-DENSITY LIPOPROTEIN CHOLESTEROL RATIO AND MICRO- AND MACROANGIOPATHIES IN TYPE 2 DIABETES MELLITUS. Endocrine practice: official journal of the American College of Endocrinology and the American Association of Clinical Endocrinologists 2018, 24(7):615–21.PMID: 30048164. Lee MY, Hsiao PJ, Huang JC, Hsu WH, Chen SC, Chang JM, Shin SJ, ASSOCIATIONS BETWEEN TRIGLYCERIDE/HIGH-DENSITY LIPOPROTEIN CHOLESTEROL RATIO AND MICRO- AND MACROANGIOPATHIES IN TYPE 2 DIABETES MELLITUS. Endocrine practice: official journal of the American College of Endocrinology and the American Association of Clinical Endocrinologists 2018, 24(7):615–21.PMID: 30048164.
19.
go back to reference 2. Classification and Diagnosis of Diabetes: Standards of Medical Care in Diabetes-2019. Diabetes care 2019, 42(Suppl 1):S13-s28.PMID: 30559228. 2. Classification and Diagnosis of Diabetes: Standards of Medical Care in Diabetes-2019. Diabetes care 2019, 42(Suppl 1):S13-s28.PMID: 30559228.
20.
go back to reference Curtin LR, Mohadjer LK, Dohrmann SM, Montaquila JM, Kruszan-Moran D, Mirel LB, Carroll MD, Hirsch R, Schober S, Johnson CL. The National Health and Nutrition Examination Survey: Sample Design, 1999–2006. Vital and health statistics Series 2, Data Evaluation Methods Res 2012(155):1–39.PMID: 22788053. Curtin LR, Mohadjer LK, Dohrmann SM, Montaquila JM, Kruszan-Moran D, Mirel LB, Carroll MD, Hirsch R, Schober S, Johnson CL. The National Health and Nutrition Examination Survey: Sample Design, 1999–2006. Vital and health statistics Series 2, Data Evaluation Methods Res 2012(155):1–39.PMID: 22788053.
21.
go back to reference Blighe K, Gurudas S, Lee Y, Sivaprasad S. Diabetic Retinopathy Environment-Wide Association Study (EWAS) in NHANES 2005–2008. J Clin Med 2020, 9(11).PMID: 33198349. Blighe K, Gurudas S, Lee Y, Sivaprasad S. Diabetic Retinopathy Environment-Wide Association Study (EWAS) in NHANES 2005–2008. J Clin Med 2020, 9(11).PMID: 33198349.
22.
go back to reference Modjtahedi BS, Bose N, Papakostas TD, Morse L, Vavvas DG, Kishan AU. Lipids and Diabetic Retinopathy. Semin Ophthalmol. 2016;31(1–2):10–8. PMID: 26959124.CrossRefPubMed Modjtahedi BS, Bose N, Papakostas TD, Morse L, Vavvas DG, Kishan AU. Lipids and Diabetic Retinopathy. Semin Ophthalmol. 2016;31(1–2):10–8. PMID: 26959124.CrossRefPubMed
23.
go back to reference Jenkins AJ, Grant MB, Busik JV. Lipids, hyperreflective crystalline deposits and diabetic retinopathy: potential systemic and retinal-specific effect of lipid-lowering therapies. Diabetologia. 2022;65(4):587–603. PMID: 35149880.CrossRefPubMedPubMedCentral Jenkins AJ, Grant MB, Busik JV. Lipids, hyperreflective crystalline deposits and diabetic retinopathy: potential systemic and retinal-specific effect of lipid-lowering therapies. Diabetologia. 2022;65(4):587–603. PMID: 35149880.CrossRefPubMedPubMedCentral
24.
go back to reference Campbell S, Genest J. HDL-C: clinical equipoise and vascular endothelial function. Expert Rev Cardiovasc Ther. 2013;11(3):343–53. PMID: 23469914.CrossRefPubMed Campbell S, Genest J. HDL-C: clinical equipoise and vascular endothelial function. Expert Rev Cardiovasc Ther. 2013;11(3):343–53. PMID: 23469914.CrossRefPubMed
25.
go back to reference März W, Kleber ME, Scharnagl H, Speer T, Zewinger S, Ritsch A, Parhofer KG, von Eckardstein A, Landmesser U, Laufs U. Clin Res Cardiology: Official J German Cardiac Soc. 2017;106(9):663–75. PMID: 28342064.CrossRef März W, Kleber ME, Scharnagl H, Speer T, Zewinger S, Ritsch A, Parhofer KG, von Eckardstein A, Landmesser U, Laufs U. Clin Res Cardiology: Official J German Cardiac Soc. 2017;106(9):663–75. PMID: 28342064.CrossRef
26.
go back to reference Sumi M, Sata M, Miura S, Rye KA, Toya N, Kanaoka Y, Yanaga K, Ohki T, Saku K, Nagai R. Reconstituted high-density lipoprotein stimulates differentiation of endothelial progenitor cells and enhances ischemia-induced angiogenesis. Arterioscler Thromb Vasc Biol. 2007;27(4):813–8. PMID: 17272742.CrossRefPubMed Sumi M, Sata M, Miura S, Rye KA, Toya N, Kanaoka Y, Yanaga K, Ohki T, Saku K, Nagai R. Reconstituted high-density lipoprotein stimulates differentiation of endothelial progenitor cells and enhances ischemia-induced angiogenesis. Arterioscler Thromb Vasc Biol. 2007;27(4):813–8. PMID: 17272742.CrossRefPubMed
27.
go back to reference Feng Y, Jacobs F, Van Craeyveld E, Brunaud C, Snoeys J, Tjwa M, Van Linthout S, De Geest B. Human ApoA-I transfer attenuates transplant arteriosclerosis via enhanced incorporation of bone marrow-derived endothelial progenitor cells. Arterioscler Thromb Vasc Biol. 2008;28(2):278–83. PMID: 18063807.CrossRefPubMed Feng Y, Jacobs F, Van Craeyveld E, Brunaud C, Snoeys J, Tjwa M, Van Linthout S, De Geest B. Human ApoA-I transfer attenuates transplant arteriosclerosis via enhanced incorporation of bone marrow-derived endothelial progenitor cells. Arterioscler Thromb Vasc Biol. 2008;28(2):278–83. PMID: 18063807.CrossRefPubMed
28.
go back to reference Tabet F, Rye KA. High-density lipoproteins, inflammation and oxidative stress. Clinical science (London, England: 1979) 2009, 116(2):87–98.PMID: 19076062. Tabet F, Rye KA. High-density lipoproteins, inflammation and oxidative stress. Clinical science (London, England: 1979) 2009, 116(2):87–98.PMID: 19076062.
29.
go back to reference Morton J, Zoungas S, Li Q, Patel AA, Chalmers J, Woodward M, Celermajer DS, Beulens JW, Stolk RP, Glasziou P, et al. Low HDL cholesterol and the risk of diabetic nephropathy and retinopathy: results of the ADVANCE study. Diabetes Care. 2012;35(11):2201–6. PMID: 22891258.CrossRefPubMedPubMedCentral Morton J, Zoungas S, Li Q, Patel AA, Chalmers J, Woodward M, Celermajer DS, Beulens JW, Stolk RP, Glasziou P, et al. Low HDL cholesterol and the risk of diabetic nephropathy and retinopathy: results of the ADVANCE study. Diabetes Care. 2012;35(11):2201–6. PMID: 22891258.CrossRefPubMedPubMedCentral
30.
go back to reference Sacks FM, Hermans MP, Fioretto P, Valensi P, Davis T, Horton E, Wanner C, Al-Rubeaan K, Aronson R, Barzon I, et al. Association between plasma triglycerides and high-density lipoprotein cholesterol and microvascular kidney disease and retinopathy in type 2 diabetes mellitus: a global case-control study in 13 countries. Circulation. 2014;129(9):999–1008. PMID: 24352521.CrossRefPubMed Sacks FM, Hermans MP, Fioretto P, Valensi P, Davis T, Horton E, Wanner C, Al-Rubeaan K, Aronson R, Barzon I, et al. Association between plasma triglycerides and high-density lipoprotein cholesterol and microvascular kidney disease and retinopathy in type 2 diabetes mellitus: a global case-control study in 13 countries. Circulation. 2014;129(9):999–1008. PMID: 24352521.CrossRefPubMed
31.
go back to reference Benarous R, Sasongko MB, Qureshi S, Fenwick E, Dirani M, Wong TY, Lamoureux EL. Differential association of serum lipids with diabetic retinopathy and diabetic macular edema. Investig Ophthalmol Vis Sci. 2011;52(10):7464–9. PMID: 21862642.CrossRef Benarous R, Sasongko MB, Qureshi S, Fenwick E, Dirani M, Wong TY, Lamoureux EL. Differential association of serum lipids with diabetic retinopathy and diabetic macular edema. Investig Ophthalmol Vis Sci. 2011;52(10):7464–9. PMID: 21862642.CrossRef
32.
go back to reference Sasso FC, Pafundi PC, Gelso A, Bono V, Costagliola C, Marfella R, Sardu C, Rinaldi L, Galiero R, Acierno C et al. High HDL cholesterol: a risk factor for diabetic retinopathy? Findings from NO BLIND study. Diabetes research and clinical practice 2019, 150:236–44.PMID: 30904748. Sasso FC, Pafundi PC, Gelso A, Bono V, Costagliola C, Marfella R, Sardu C, Rinaldi L, Galiero R, Acierno C et al. High HDL cholesterol: a risk factor for diabetic retinopathy? Findings from NO BLIND study. Diabetes research and clinical practice 2019, 150:236–44.PMID: 30904748.
33.
go back to reference Kohner EM, Aldington SJ, Stratton IM, Manley SE, Holman RR, Matthews DR, Turner RC. United Kingdom Prospective Diabetes Study, 30: diabetic retinopathy at diagnosis of non-insulin-dependent diabetes mellitus and associated risk factors. Archives Ophthalmol (Chicago Ill:1960). 1998;116(3):297–303. PMID:9514482.CrossRef Kohner EM, Aldington SJ, Stratton IM, Manley SE, Holman RR, Matthews DR, Turner RC. United Kingdom Prospective Diabetes Study, 30: diabetic retinopathy at diagnosis of non-insulin-dependent diabetes mellitus and associated risk factors. Archives Ophthalmol (Chicago Ill:1960). 1998;116(3):297–303. PMID:9514482.CrossRef
34.
go back to reference Lyons TJ, Jenkins AJ, Zheng D, Lackland DT, McGee D, Garvey WT, Klein RL. Diabetic retinopathy and serum lipoprotein subclasses in the DCCT/EDIC cohort. Investig Ophthalmol Vis Sci. 2004;45(3):910–8. PMID: 14985310.CrossRef Lyons TJ, Jenkins AJ, Zheng D, Lackland DT, McGee D, Garvey WT, Klein RL. Diabetic retinopathy and serum lipoprotein subclasses in the DCCT/EDIC cohort. Investig Ophthalmol Vis Sci. 2004;45(3):910–8. PMID: 14985310.CrossRef
35.
go back to reference Popescu T, Moţa M. Dyslipidemia and hypertension in patients with type 2 diabetes and retinopathy. Romanian J Intern Med = Revue Roumaine de Med Interne. 2009;47(3):235–41. PMID: 20446438. Popescu T, Moţa M. Dyslipidemia and hypertension in patients with type 2 diabetes and retinopathy. Romanian J Intern Med = Revue Roumaine de Med Interne. 2009;47(3):235–41. PMID: 20446438.
36.
go back to reference von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP. The strengthening the reporting of Observational studies in Epidemiology (STROBE) Statement: guidelines for reporting observational studies. Int J Surg (London England). 2014;12(12):1495–9. PMID: 18064739.CrossRef von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP. The strengthening the reporting of Observational studies in Epidemiology (STROBE) Statement: guidelines for reporting observational studies. Int J Surg (London England). 2014;12(12):1495–9. PMID: 18064739.CrossRef
Metadata
Title
Association between HDL cholesterol with diabetic retinopathy in diabetic patients: a cross-sectional retrospective study
Authors
Wuping Xu
Xuedong Xu
Min Zhang
Chiping Sun
Publication date
01-12-2024
Publisher
BioMed Central
Published in
BMC Endocrine Disorders / Issue 1/2024
Electronic ISSN: 1472-6823
DOI
https://doi.org/10.1186/s12902-024-01599-0

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