Homocysteine and serum uric acid levels in type 2 diabetic retinopathy and their predictive value for disease_Chinese Journal of Ocular Fundus Diseases

Authors：

Wei Jing ,  Zhang Jincheng , Shi Yanan , Zhang Huiqin , Wu Yan

Department of Endocrinology, Cangzhou Central Hospital of Hebei Province, Cangzhou 061000, China;

Corresponding?author：

Zhang Jincheng, Email: zjcnfm@126.com

Keywords：

Homocysteine; Blood uric acid; Type 2 diabetes; Diabetic retinopathy; Predictive value

DOI：

10.3760/cma.j.cn511434-20220425-00248

Video：

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Objective To observe the correlation between homocysteine (Hcy) and serum uric acid (SUA) and retinopathy in type 2 diabetes mellitus (T2DM), preliminary study on its predictive value. Methods A retrospective study. From January 2020 to March 2021, a total of 324 T2DM patients hospitalized in Department of Endocrinology, Cangzhou Central Hospital of Hebei Province were included. Fasting blood glucose (FBG), glycated hemoglobin (HbA1C), triglycerides (TG), low density lipoprotein cholesterol (LDL-C), high density lipoprotein cholesterol (HDL-C), serum creatinine (Scr), blood urea nitrogen (BUN), Hcy, SUA, peripheral blood endothelial progenitor cells (EPC), circulating endothelial cells (CEC) were counted and homeostasis model assessment for insulin resistance (HOMA-IR) was calculated. According to the absence or presence of diabetic retinopathy (DR), the patients were divided into non DR (NDR) group and DR group with 100 and 214 cases, respectively. Clinical data and laboratory biochemical indexes of the two groups were compared and observed. The logistic regression was used to analyze the independent risk factors for DR in T2DM patients. Smooth curve fitting was used to analyze the curve relationship between Hcy, SUA and DR, and ROC area (AUC) of Hcy, SUA; their combined prediction of DR in T2DM patients was calculated by receiver operating characteristic curve (ROC curve), and the predictive value of Hcy and SUA for DR in T2DM patients was evaluated. Results Diabetic course (t=5.380), systolic blood pressure (t=2.935), hypertension (χ²=10.248), diabetic nephropathy (χ²=9.515), diabetic peripheral neuropathy (χ²=24.501), FBG (t=3.945), HbA1C (t=3.336) and TG in DR Group (t=2.898), LDL-C (t=3.986), Scr (t=2.139), SUA (t=7.138), HOMA-IR (t=3.237), BUN (t=3.609), Hcy (t=2.363) and CEC (t=19.396) were significantly higher than those in NDR group. The difference was statistically significant (P＜0.05). EPC (t=9.563) and CPC (t=7.684) levels were significantly lower than those of NDR group, and the difference was statistically significant (P＜0.05). Logistic regression analysis showed that diabetes course, SBP, hypertension, FBG, HbA1C, LDL-C, SUA, Hcy, EPC, CPC and CEC were all independent risk factors for developing DR in T2DM patients (P＜0.05). The smooth curve fitting analysis showed that Hcy and SUA were positively correlated with the occurrence of DR. After adjusting for confounding factors, when Hcy≥15 μmol/L, the risk of DR Increased by 14% for every 1 μmol/L increase in Hcy [odds ratio (OR)=0.92, 95% confidence interval (CI) 0.88-0.98, P＜0.05]. When Hcy＜15 μmol/L, there was no significant difference (OR=0.96, 95%CI 0.92-1.08, P＞0.05). When SUA≥304 μmol/L, the risk of DR increased by 17%, every 20 μmol/L SUA increased (OR=0.80, 95%CI 0.68-0.94, P＜0.05). When SUA＜304 μmol/L, the difference was not statistically significant (OR=0.83, 95%CI 0.72-0.95, P＞0.05). ROC curve analysis results showed that the AUC values of Hcy, SUA and Hcy combined with SUA in predicting the occurrence of DR in T2DM patients were 0.775 (95%CI 0.713-0.837, P＜0.001), 0.757 (95%CI 0.680-0.834, P＜0.001) and 0.827 (95%CI 0.786-0.868, P＜0.001). Hcy combined with SUA showed better predictive efficiency. Conclusions The abnormal increase of Hcy and SUA levels in T2DM patients are closely related to the occurrence of DR, they are independent risk factors for the occurrence of DR. Hcy combined with SUA has high predictive value for the occurrence of DR.

Citation： Wei Jing, Zhang Jincheng, Shi Yanan, Zhang Huiqin, Wu Yan. Homocysteine and serum uric acid levels in type 2 diabetic retinopathy and their predictive value for disease. Chinese Journal of Ocular Fundus Diseases, 2023, 39(2): 125-131. doi: 10.3760/cma.j.cn511434-20220425-00248 Copy

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2.	Li W, Jin L, Cui Y, et al. Bone marrow mesenchymal stem cells-induced exosomal microRNA-486-3p protects against diabetic retinopathy through TLR4/NF-κB axis repression[J]. J Endocrinol Invest, 2021, 44(6): 1193-1207. DOI: 10.1007/s40618-020-01405-3.
3.	Louie HH, Shome A, Kuo CY, et al. Connexin43 hemichannel block inhibits NLRP3 inflammasome activation in a human retinal explant model of diabetic retinopathy[J/OL]. Exp Eye Res, 2021, 202: 108384[2020-12-05]. https://pubmed.ncbi.nlm.nih.gov/33285185/. DOI: 10.1016/j.exer.2020.108384.
4.	Yu HS, Hong EH, Shin YU, et al. ATP-binding cassette subfamily A-1 (ABCA1) levels are increased in the aqueous humour of proliferative diabetic retinopathy patients[J/OL]. Acta Ophthalmol, 2021, 99(3): e442-443[2020-07-23]. https://pubmed.ncbi.nlm.nih.gov/32701222/. DOI: 10.1111/aos.14550.
5.	Rallidis LS, Kosmas N, Rallidi T, et al. Homocysteine is an independent predictor of long-term cardiac mortality in patients with stable coronary artery disease in the era of statins[J]. Coron Artery Dis, 2020, 31(2): 152-156. DOI: 10.1097/MCA.0000000000000800.
6.	Selvaraj S, Claggett BL, Pfeffer MA, et al. Serum uric acid, influence of sacubitril-valsartan, and cardiovascular outcomes in heart failure with preserved ejection fraction: PARAGON-HF[J]. Eur J Heart Fail, 2020, 22(11): 2093-2101. DOI: 10.1002/ejhf.1984.
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8.	中華醫學會眼科學會眼底病學組. 我國糖尿病視網膜病變臨床診療指南(2014年)[J]. 中華眼科雜志, 2014, 50(11): 851-865. DOI: 10.3760/cma.j.issn.0412-4081.2014.11.014.Fundus Diseases Group, Ophthalmology Society of Chinese Medical Association. Guidelines for clinical diagnosis and treatment of diabetes retinopathy in China (2014)[J]. Chin J Ophthalmol, 2014, 50(11): 851-865. DOI: 10.3760/cma.j.issn.0412-4081.2014.11.014.
9.	Dennis JM. Precision medicine in type 2 diabetes: using individualized prediction models to optimize selection of treatment[J]. Diabetes, 2020, 69(10): 2075-2085. DOI: 10.2337/dbi20-0002.
10.	Li X, Xie J, Zhang L, et al. Identifying microvascular and neural parameters related to the severity of diabetic retinopathy using optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2020, 61(5): 39. DOI: 10.1167/iovs.61.5.39.
11.	Lv X, Ran X, Chen X, et al. Early-onset type 2 diabetes: a high-risk factor for proliferative diabetic retinopathy (PDR) in patients with microalbuminuria[J/OL]. Medicine (Baltimore), 2020, 99(19): e20189[2020-05-01]. https://pubmed.ncbi.nlm.nih.gov/32384512/. DOI: 10.1097/MD.0000000000020189.
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13.	Ren Y, Gao L, Guo X, et al. Interactive effect of serum uric acid and total bilirubin for micro-vascular disease of type 2 diabetes in China[J]. J Diabetes Complications, 2018, 32(11): 1000-1005. DOI: 10.1016/j.jdiacomp.2018.09.002.
14.	項杰, 張曙光, 陳素英, 等. 血尿酸、胱抑素C和促代謝因子水平與糖尿病視網膜病變的相關性分析[J]. 現代藥物與臨床, 2020, 35(11): 2144-2148. DOI: 10.7501/j.issn.1674-5515.2020.11.006.Xiang J, Zhang SG, Chen SY, et al. Correlation between levels of serum uric acid, cystatin C, and betatrophin and diabetic retinopathy[J]. Drugs & Clinic, 2020, 35(11): 2144-2148. DOI: 10.7501/j.issn.1674-5515.2020.11.006.
15.	Zhu DD, Wang YZ, Zou C, et al. The role of uric acid in the pathogenesis of diabetic retinopathy based on Notch pathway[J]. Biochem Biophys Res Commun, 2018, 503(2): 921-929. DOI: 10.1016/j.bbrc.2018.06.097.
16.	劉韻, 郭皖北, 曹明艷, 等. 胰島素抗體陽性的2型糖尿病患者血清同型半胱氨酸水平變化的研究[J]. 中國糖尿病雜志, 2020, 28(1): 33-36. DOI: 10.3969/j.issn.1006-6187.2020.01.007.Liu Y, Guo WB, Cao MY, et al. Relationship between positive insulin antibody and serum homocysteine levels in patients with type 2 diabetes[J]. Chin J Diabetes, 2020, 28(1): 33-36. DOI: 10.3969/j.issn.1006-6187.2020.01.007.
17.	Gupta P, John D, Rebekah G, et al. Role of hyperhomocysteinemia in proliferative diabetic retinopathy: a case-control study[J]. Indian J Ophthalmol, 2018, 66(10): 1435-1440. DOI: 10.4103/ijo.IJO_350_18.
18.	鐘欣靜, 黃翠娟, 林蓓佑, 等. H型高血壓病人同型半胱氨酸與血壓變異性和血尿酸的相關性[J]. 中西醫結合心腦血管病雜志, 2020, 18(6): 948-951. DOI: 10.12102/j.issn.1672-1349.2020.06.021.Zhong XJ, Huang CJ, Lin BY, et al. Correlation between homocysteine and blood pressure variability and serum uric acid in patients with type H hypertension[J]. Chinese Journal of Integrative Medicine on Cardio/Cerebrovascular Disease, 2020, 18(6): 948-951. DOI: 10.12102/j.issn.1672-1349.2020.06.021.
19.	徐菲菲, 劉詠梅, 房振宇, 等. 原發性腎小球腎炎患者血漿高同型半胱氨酸水平的變化及與鈣磷乘積和血尿酸的相關性分析[J]. 現代生物醫學進展, 2020, 20(3): 558-560, 548. DOI: 10.13241/j.cnki.pmb.2020.03.034.Xu FF, Liu YM, Fang ZY, et al. Changes of plasma Hcy in patients with primary glomerulonephritis and its correlation with calcium-phosphorus product and blood uric acid[J]. Progress in Modern Biomedicine, 2020, 20(3): 558-560, 548. DOI: 10.13241/j.cnki.pmb.2020.03.034.
20.	Dong N, Shi H, Tang X. Plasma homocysteine levels are associated with macular thickness in type 2 diabetes without diabetic macular edema[J]. Int Ophthalmol, 2018, 38(2): 737-746. DOI: 10.1007/s10792-017-0528-0.
21.	龔杰, 周波. 同型半胱氨酸和糖化血紅蛋白水平與糖尿病視網膜病變的相關性[J]. 廣西醫學, 2019, 41(16): 2042-2044. DOI: 10.11675/j.issn.0253-4304.2019.16.09.Gong J, Zhou B. Correlation of homocysteine and hemoglobin A1 c levels with diabetic retinopathy[J]. Guangxi Medical Journal, 2019, 41(16): 2042-2044. DOI: 10.11675/j.issn.0253-4304.2019.16.09.
22.	李紅軍, 劉有婭, 譚芳. 2型糖尿病視網膜病變患者凝血功能及危險因素分析[J]. 血栓與止血學, 2020, 26(2): 190-192. DOI: 10.3969/j.issn.1009-6213.2020.02.004.Li HJ, Liu YY, Tan F. Analysison coagulation function and risk factors of patients with type 2 diabetic retinopathy[J]. Chinese Journal of Thrombosis and Hemostasis, 2020, 26(2): 190-192. DOI: 10.3969/j.issn.1009-6213.2020.02.004.
23.	朱夏媛, 吳浩, 葛彩英, 等. 社區2型糖尿病視網膜病變風險預測模型的構建與驗證[J]. 中國全科醫學, 2020, 23(6): 85-88. DOI: 10.12114/j.issn.1007-9572.2020.00.063.Zhu XY, Wu H, Ge CY, et al. Establishment and verification of a risk prediction model of diabetic retinopathy in patients with type 2 diabetes in the community[J]. Chinese General Practice, 2020, 23(6): 85-88. DOI: 10.12114/j.issn.1007-9572.2020.00.063.
24.	柳潔平, 付艷廣, 張俊廣, 等. 血清ICAM-1、VEGF水平與糖尿病視網膜病變患者微血管損傷的關系[J]. 山東醫藥, 2020, 60(16): 47-49. DOI: 10.3969/j.issn.1002-266X.2020.16.012.Liu JP, Fu YG, Zhang JG, et al. The relationship between serum ICAM-1, VEGF levels and microvascular injury in patients with diabetes retinopathy[J]. Shandong Medical Journal, 2020, 60(16): 47-49. DOI: 10.3969/j.issn.1002-266X.2020.16.012.

1. Bene BA, O'Connor S, Mastellos N, et al. Impact of mobile health applications on self-management in patients with type 2 diabetes mellitus: protocol of a systematic review[J/OL]. BMJ Open, 2019, 9(6): e025714[2019-06-25]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6597642/. DOI: 10.1136/bmjopen-2018-025714.
2. Li W, Jin L, Cui Y, et al. Bone marrow mesenchymal stem cells-induced exosomal microRNA-486-3p protects against diabetic retinopathy through TLR4/NF-κB axis repression[J]. J Endocrinol Invest, 2021, 44(6): 1193-1207. DOI: 10.1007/s40618-020-01405-3.
3. Louie HH, Shome A, Kuo CY, et al. Connexin43 hemichannel block inhibits NLRP3 inflammasome activation in a human retinal explant model of diabetic retinopathy[J/OL]. Exp Eye Res, 2021, 202: 108384[2020-12-05]. https://pubmed.ncbi.nlm.nih.gov/33285185/. DOI: 10.1016/j.exer.2020.108384.
4. Yu HS, Hong EH, Shin YU, et al. ATP-binding cassette subfamily A-1 (ABCA1) levels are increased in the aqueous humour of proliferative diabetic retinopathy patients[J/OL]. Acta Ophthalmol, 2021, 99(3): e442-443[2020-07-23]. https://pubmed.ncbi.nlm.nih.gov/32701222/. DOI: 10.1111/aos.14550.
5. Rallidis LS, Kosmas N, Rallidi T, et al. Homocysteine is an independent predictor of long-term cardiac mortality in patients with stable coronary artery disease in the era of statins[J]. Coron Artery Dis, 2020, 31(2): 152-156. DOI: 10.1097/MCA.0000000000000800.
6. Selvaraj S, Claggett BL, Pfeffer MA, et al. Serum uric acid, influence of sacubitril-valsartan, and cardiovascular outcomes in heart failure with preserved ejection fraction: PARAGON-HF[J]. Eur J Heart Fail, 2020, 22(11): 2093-2101. DOI: 10.1002/ejhf.1984.
7. 中華醫學會糖尿病學分會. 中國2型糖尿病防治指南(2017年版)[J]. 中華糖尿病雜志, 2018, 10(1): 4-67. DOI: 10.3760/cma.j.issn.1674-5809.2018.01.003.Chinese Diabetes Society, Chinese Medical Association. Standards of care for type 2 diabetes in China[J]. Chin J Diabetes Mellitus, 2018, 10(1): 4-67. DOI: 10.3760/cma.j.issn.1674-5809.2018.01.003.
8. 中華醫學會眼科學會眼底病學組. 我國糖尿病視網膜病變臨床診療指南(2014年)[J]. 中華眼科雜志, 2014, 50(11): 851-865. DOI: 10.3760/cma.j.issn.0412-4081.2014.11.014.Fundus Diseases Group, Ophthalmology Society of Chinese Medical Association. Guidelines for clinical diagnosis and treatment of diabetes retinopathy in China (2014)[J]. Chin J Ophthalmol, 2014, 50(11): 851-865. DOI: 10.3760/cma.j.issn.0412-4081.2014.11.014.
9. Dennis JM. Precision medicine in type 2 diabetes: using individualized prediction models to optimize selection of treatment[J]. Diabetes, 2020, 69(10): 2075-2085. DOI: 10.2337/dbi20-0002.
10. Li X, Xie J, Zhang L, et al. Identifying microvascular and neural parameters related to the severity of diabetic retinopathy using optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2020, 61(5): 39. DOI: 10.1167/iovs.61.5.39.
11. Lv X, Ran X, Chen X, et al. Early-onset type 2 diabetes: a high-risk factor for proliferative diabetic retinopathy (PDR) in patients with microalbuminuria[J/OL]. Medicine (Baltimore), 2020, 99(19): e20189[2020-05-01]. https://pubmed.ncbi.nlm.nih.gov/32384512/. DOI: 10.1097/MD.0000000000020189.
12. Seki H, Kaneko H, Morita H, et al. Relation of serum uric acid and cardiovascular events in young adults aged 20-49 years[J]. Am J Cardiol, 2021, 152: 150-157. DOI: 10.1016/j.amjcard.2021.05.007.
13. Ren Y, Gao L, Guo X, et al. Interactive effect of serum uric acid and total bilirubin for micro-vascular disease of type 2 diabetes in China[J]. J Diabetes Complications, 2018, 32(11): 1000-1005. DOI: 10.1016/j.jdiacomp.2018.09.002.
14. 項杰, 張曙光, 陳素英, 等. 血尿酸、胱抑素C和促代謝因子水平與糖尿病視網膜病變的相關性分析[J]. 現代藥物與臨床, 2020, 35(11): 2144-2148. DOI: 10.7501/j.issn.1674-5515.2020.11.006.Xiang J, Zhang SG, Chen SY, et al. Correlation between levels of serum uric acid, cystatin C, and betatrophin and diabetic retinopathy[J]. Drugs & Clinic, 2020, 35(11): 2144-2148. DOI: 10.7501/j.issn.1674-5515.2020.11.006.
15. Zhu DD, Wang YZ, Zou C, et al. The role of uric acid in the pathogenesis of diabetic retinopathy based on Notch pathway[J]. Biochem Biophys Res Commun, 2018, 503(2): 921-929. DOI: 10.1016/j.bbrc.2018.06.097.
16. 劉韻, 郭皖北, 曹明艷, 等. 胰島素抗體陽性的2型糖尿病患者血清同型半胱氨酸水平變化的研究[J]. 中國糖尿病雜志, 2020, 28(1): 33-36. DOI: 10.3969/j.issn.1006-6187.2020.01.007.Liu Y, Guo WB, Cao MY, et al. Relationship between positive insulin antibody and serum homocysteine levels in patients with type 2 diabetes[J]. Chin J Diabetes, 2020, 28(1): 33-36. DOI: 10.3969/j.issn.1006-6187.2020.01.007.
17. Gupta P, John D, Rebekah G, et al. Role of hyperhomocysteinemia in proliferative diabetic retinopathy: a case-control study[J]. Indian J Ophthalmol, 2018, 66(10): 1435-1440. DOI: 10.4103/ijo.IJO_350_18.
18. 鐘欣靜, 黃翠娟, 林蓓佑, 等. H型高血壓病人同型半胱氨酸與血壓變異性和血尿酸的相關性[J]. 中西醫結合心腦血管病雜志, 2020, 18(6): 948-951. DOI: 10.12102/j.issn.1672-1349.2020.06.021.Zhong XJ, Huang CJ, Lin BY, et al. Correlation between homocysteine and blood pressure variability and serum uric acid in patients with type H hypertension[J]. Chinese Journal of Integrative Medicine on Cardio/Cerebrovascular Disease, 2020, 18(6): 948-951. DOI: 10.12102/j.issn.1672-1349.2020.06.021.
19. 徐菲菲, 劉詠梅, 房振宇, 等. 原發性腎小球腎炎患者血漿高同型半胱氨酸水平的變化及與鈣磷乘積和血尿酸的相關性分析[J]. 現代生物醫學進展, 2020, 20(3): 558-560, 548. DOI: 10.13241/j.cnki.pmb.2020.03.034.Xu FF, Liu YM, Fang ZY, et al. Changes of plasma Hcy in patients with primary glomerulonephritis and its correlation with calcium-phosphorus product and blood uric acid[J]. Progress in Modern Biomedicine, 2020, 20(3): 558-560, 548. DOI: 10.13241/j.cnki.pmb.2020.03.034.
20. Dong N, Shi H, Tang X. Plasma homocysteine levels are associated with macular thickness in type 2 diabetes without diabetic macular edema[J]. Int Ophthalmol, 2018, 38(2): 737-746. DOI: 10.1007/s10792-017-0528-0.
21. 龔杰, 周波. 同型半胱氨酸和糖化血紅蛋白水平與糖尿病視網膜病變的相關性[J]. 廣西醫學, 2019, 41(16): 2042-2044. DOI: 10.11675/j.issn.0253-4304.2019.16.09.Gong J, Zhou B. Correlation of homocysteine and hemoglobin A1 c levels with diabetic retinopathy[J]. Guangxi Medical Journal, 2019, 41(16): 2042-2044. DOI: 10.11675/j.issn.0253-4304.2019.16.09.
22. 李紅軍, 劉有婭, 譚芳. 2型糖尿病視網膜病變患者凝血功能及危險因素分析[J]. 血栓與止血學, 2020, 26(2): 190-192. DOI: 10.3969/j.issn.1009-6213.2020.02.004.Li HJ, Liu YY, Tan F. Analysison coagulation function and risk factors of patients with type 2 diabetic retinopathy[J]. Chinese Journal of Thrombosis and Hemostasis, 2020, 26(2): 190-192. DOI: 10.3969/j.issn.1009-6213.2020.02.004.
23. 朱夏媛, 吳浩, 葛彩英, 等. 社區2型糖尿病視網膜病變風險預測模型的構建與驗證[J]. 中國全科醫學, 2020, 23(6): 85-88. DOI: 10.12114/j.issn.1007-9572.2020.00.063.Zhu XY, Wu H, Ge CY, et al. Establishment and verification of a risk prediction model of diabetic retinopathy in patients with type 2 diabetes in the community[J]. Chinese General Practice, 2020, 23(6): 85-88. DOI: 10.12114/j.issn.1007-9572.2020.00.063.
24. 柳潔平, 付艷廣, 張俊廣, 等. 血清ICAM-1、VEGF水平與糖尿病視網膜病變患者微血管損傷的關系[J]. 山東醫藥, 2020, 60(16): 47-49. DOI: 10.3969/j.issn.1002-266X.2020.16.012.Liu JP, Fu YG, Zhang JG, et al. The relationship between serum ICAM-1, VEGF levels and microvascular injury in patients with diabetes retinopathy[J]. Shandong Medical Journal, 2020, 60(16): 47-49. DOI: 10.3969/j.issn.1002-266X.2020.16.012.

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Homocysteine and serum uric acid levels in type 2 diabetic retinopathy and their predictive value for disease

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