Correlations between macular microvascular parameters in patients with type 2 diabetes mellitus and urinary albumin creatinine ratio_Chinese Journal of Ocular Fundus Diseases

Authors：

Liu Yalu , Feng Ruifang , Liu Haiyang , Guan Lina , Qiao Lei , Xu Qing , Gong Chaoju ,  Li Suyan

Department of Ophthalmology, The Affiliated Xuzhou Municipal Hospital of Xuzhou Medical University, Xuzhou First People’s Hospital, Institute of Eye Disease Prevention and Treatment of Xuzhou, Xuzhou 221002, China;

Corresponding author：

Li Suyan, Email: lisuyan1226@126.com

Keywords：

Diabetes mellitus, type 2; Regional blood flow; Tomography, optical coherence; Diabetic nephropathies; Diabetic angiopathies

DOI：

10.3760/cma.j.cn511434-20210518-00256

Video：

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Objective To observe and analyze the correlation between macular microvascular parameters and urinary albumin to creatinine ratio (UACR) in patients with type 2 diabetes mellitus (T2DM). Methods A cross-sectional study. From October 2017 to April 2018, 100 eyes of 100 patients (T2DM) and 27 eyes of 27 healthy controls (the control group) were enrolled in Xuzhou First People’s Hospital. All subjects underwent anterior segment examination via slit-lamp biomicroscopy, dilated fundus examination, 7-field fundus photographs, OCT angiography (OCTA), the fasting glucose test, glycosylated hemoglobin (HbA1c), urinary albumin, urinary creatinine and UACR levels determination. Height and weight measurement were taken for calculating body mass index (BMI). Diabetic retinopathy was ruled out by fundoscopic examinations and 7-field fundus photographs in T2DM patients. According to the UACR, patients in the T2DM group were subdivided into A1 group (UACR< 30 mg/g), A2 group (UACR 30-300 mg/g), and A3 group (UACR>300 mg/g), with 38 cases and 38 eyes respectively , 40 cases with 40 eyes, 22 cases with 22 eyes. A 6 mm×6 mm scanning area centered on the macular fovea were scanned for right eye using a frequency domain OCTA instrument, which were divided into three concentric circles centered on the macular fovea by the software automatically. The foveal zone was defined as a circular area measuring 1 mm in diameter, the parafoveal zone was described as a middle circle area measuring 1-3 mm in diameter, and the perifoveal zone was an outer circle area measuring 3-6 mm in diameter. The vessel density of superficial capillary plexus (SCP) and deep capillary plexus (DCP), foveal avascular area (FAZ) and perimeter (PERIM), non-circularity index (AI) were measured. The correlation between the macular vessel density, FAZ and UACR was analyzed by Spearman correlation analysis. Results A1 group, A2 group, A3 group, and normal control group. The macular area SCP and DCP (F=13.722, 5.644), foveal area (F=4.607, 4.719), parafoveal area (H=23.142, F=2.904), the blood flow density of the area around the fovea (F=12.292, H=10.946), the difference was statistically significant (P＜0.05); with the increase of UACR, the blood flow density of each area of SCP and DCP showed a downward trend. The results of correlation analysis showed that the blood flow density of the whole SCP, parafoveal area, and surrounding area of T2DM patients was negatively correlated with UACR (r=－0.376, －0.240, －0.364, －0.347, P＜0.05). There were no correlation among fasting plasma glucose, HbAlc and UACR (r=0.179, 0.085, P＞0.05). There were no correlation among blood flow density in BMI, SCP foveal area, DCP and UACR (|r|＜0.3, P＞0.05). Conclusion The whole, parafovea and perifovea vessel density values of SCP in T2DM eyes without DR are negatively correlated with UACR.

Citation： Liu Yalu, Feng Ruifang, Liu Haiyang, Guan Lina, Qiao Lei, Xu Qing, Gong Chaoju, Li Suyan. Correlations between macular microvascular parameters in patients with type 2 diabetes mellitus and urinary albumin creatinine ratio. Chinese Journal of Ocular Fundus Diseases, 2022, 38(4): 297-303. doi: 10.3760/cma.j.cn511434-20210518-00256 Copy

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6.	American Diabetes Association. 11. Microvascular complications and foot care: standards of medical care in diabetes-2020[J]. Diabetes Care, 2020, 43(Suppl 1): S135-151. DOI: 10.2337/dc20-S011.
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8.	Campbell JP, Zhang M, Hwang TS, et al. Detailed cascular anatomy of the human retina by projection-resolved optical coherence tomography angiography[J/OL]. Sci Rep, 2017, 7: 42201[2017-02-10]. https://pubmed.ncbi.nlm.nih.gov/28186181/. DOI: 10.1038/srep42201.
9.	李琳, 李全民. 糖尿病肾病美国糖尿病协会指南更新要点及治疗进展[J]. 中华糖尿病杂志, 2020, 12(6): 424-428. DOI: 10.3760/cma.j.cn115791-20200320-00166.Li L, Li QM. Update and progress of American Diabetes Association guidelines for diabetic kidney disease[J]. Chin J of Diabetes Mellitus, 2020, 12(6): 424-428. DOI: 10.3760/cma.j.cn115791-20200320-00166.
10.	El-Asrar AM, Al-Rubeaan KA, Al-Amro SA, et al. Retinopathy as a predictor of other diabetic complications[J]. Int Ophthalmol, 2001, 24(1): 1-11. DOI: 10.1023/a:1014409829614.
11.	Hsing SC, Lee CC, Lin C, et al. The severity of diabetic retinopathy is an independent factor for the progression of diabetic nephropathy[J]. J Clin Med, 2020, 10(1): 3. DOI: 10.3390/jcm10010003.
12.	Martín-Merino E, Fortuny J, Rivero-Ferrer E, et al. Incidence of retinal complications in a cohort of newly diagnosed diabetic patients[J/OL]. PLoS One, 2014, 9(6): e100283[2014-06-25]. https://pubmed.ncbi.nlm.nih.gov/24963628/. DOI: 10.1371/journal.pone.0100283.
13.	Cankurtaran V, Inanc M, Tekin K, et al. Retinal microcirculation in predicting diabetic nephropathy in type 2 diabetic patients without retinopathy[J]. Ophthalmologica, 2020, 243(4): 271-279. DOI: 10.1159/000504943.
14.	Lou J, Jing L, Yang H, et al. Risk factors for diabetic nephropathy complications in community patients with type 2 diabetes mellitus in Shanghai: logistic regression and classification tree model analysis[J]. Int J Health Plann Manage, 2019, 34(3): 1013-1024. DOI: 10.1002/hpm.2871.
15.	Blair NP, Wanek J, Felder AE, et al. Retinal oximetry and vessel diameter measurements with a commercially available scanning laser ophthalmoscope in diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 2017, 58(12): 5556-5563. DOI: 10.1167/iovs.17-21934.
16.	Fondi K, Wozniak PA, Howorka K, et al. Retinal oxygen extraction in individuals with type 1 diabetes with no or mild diabetic retinopathy[J]. Diabetologia, 2017, 60(8): 1534-1540. DOI: 10.1007/s00125-017-4309-0.
17.	滕娟, 余海跃, 陈志萍, 等. 2型糖尿病患者尿微量白蛋白含量与黄斑区视网膜微循环相关性分析[J]. 眼科新进展, 2020, 40(10): 952-956. DOI: 10.13389/j.cnki.rao.2020.0214.Teng J, Yu HY, Chen ZP, et al. Correlation analysis between microalbumin changes and macular retinal microcirculation in type 2 diabetic patients[J]. Rec Adv in Ophthalmol, 2020, 40(10): 952-956. DOI: 10.13389/j.cnki.rao.2020.0214.
18.	Sasso FC, Pafundi PC, Gelso A, et al. Relationship between albuminuric CKD and diabetic retinopathy in a real-world setting of type 2 diabetes: findings from no blind study[J]. Nutr Metab Cardiovasc Dis, 2019, 29(9): 923-930. DOI: 10.1016/j.numecd.2019.05.065.
19.	Kaewput W, Thongprayoon C, Rangsin R, et al. Associations of renal function with diabetic retinopathy and visual impairment in type 2 diabetes: a multicenter nationwide cross-sectional study[J]. World J Nephrol, 2019, 8(2): 33-43. DOI: 10.5527/wjn.v8.i2.33.
20.	Jiang S, Yu T, Zhang Z, et al. Diagnostic performance of retinopathy in the detection of diabetic nephropathy in type 2 diabetes: a systematic review and meta-analysis of 45 studies[J]. Ophthalmic Res, 2019, 62(2): 68-79. DOI: 10.1159/000500833.
21.	曾运考, 杨大卫, 曹丹, 等. 早期不同分期糖尿病视网膜病变黄斑区血流密度及血管结构改变[J]. 中华实验眼科杂志, 2020, 38(9): 783-787. DOI: 10.3760/cma.j.cn115989-20200715-00497.Zeng YK, Yang DW, Cao D, et al. Changes of macular vessel density and structures in different early stages of diabetic retinopathy[J]. Chin J Exp Ophthalmol, 2020, 38(9): 783-787. DOI: 10.3760/cma.j.cn115989-20200715-00497.
22.	Khatri A, Pradhan E, Kc BK, et al. Detection, localization, and characterization of vision-threatening features of microaneurysms using optical coherence tomography angiography in diabetic maculopathy[J]. Eur J Ophthalmol, 2021, 31(3): 1208-1215. DOI: 10.1177/1120672120924609.
23.	DaCosta J, Bhatia D, Talks J. The use of optical coherence tomography angiography and optical coherence tomography to predict visual acuity in diabetic retinopathy[J]. Eye (Lond), 2020, 34(5): 942-947. DOI: 10.1038/s41433-019-0606-9.
24.	中华医学会糖尿病学分会微血管并发症学组. 中国糖尿病肾脏疾病防治临床指南[J]. 中华糖尿病杂志, 2019, 11(1): 15-28. DOI: 10.3760/cma.j.issn.1674-5809.2019.01.004.Microvascular Complications Group, Diabetes Society, Chinese Medical Association. Chinese clinical practice guideline of diabetic kidney disease[J]. Chin J of Diabetes Mellitus, 2019, 11(1): 15-28. DOI: 10.3760/cma.j.issn.1674-5809.2019.01.004.
25.	Ashimatey BS, Green KM, Chu Z, et al. Impaired retinal vascular reactivity in diabetic retinopathy as assessed by optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2019, 60(7): 2468-2473. DOI: 10.1167/iovs.18-26417.
26.	Lee H, Lee M, Chung H, et al. Quantification of retinal vessel tortuosity in diabetic retinopathy using optical coherence tomography angiography[J]. Retina, 2018, 38(5): 976-985. DOI: 10.1097/iae.0000000000001618.
27.	Sousa DC, Leal I, Moreira S, et al. A protocol to evaluate retinal vascular response using optical coherence tomography angiography[J]. Front Neurosci, 2019, 13: 566. DOI: 10.3389/fnins.2019.00566.

1. 杨文英. 中国糖尿病的流行特点及变化趋势[J]. 中国科学(生命科学), 2018, 48(8): 812-819. DOI: 10.1360/N052018-00005.Yang WY. Epidemiology and trends in diabetes in China[J]. Science in China (Series C), 2018, 48(8): 812-819. DOI: 10.1360/N052018-00005.
2. Weng JP, Bi Y. Epidemiological status of chronic diabetic complications in China[J]. Chin Med J (Engl), 2015, 128(24): 3267-3269. DOI: 10.4103/0366-6999.171350.
3. 中华医学会糖尿病学分会糖尿病慢性并发症调查组. 全国住院糖尿病患者慢性并发症及其相关危险因素10年回顾性调查分析[J]. 中国糖尿病杂志, 2003, 11(4): 232-237. DOI: 10.3321/j.issn:1006-6187.2003.04.002.Investigation Group of Chronic Complications of Diabetes, Chinese Diabetes Society of Chinese Medical Association. Chronic diabetic complications and related macro-vascular diseases of in-patients with diabetes in mainland of China: a national retrospective analysis in recent 10 years[J]. Chin J Diabetes, 2003, 11(4): 232-237. DOI: 10.3321/j.issn:1006-6187.2003.04.002.
4. Spaide RF, Fujimoto JG, Waheed NK, et al. Optical coherence tomography angiography[J]. Prog Retin Eye Res, 2018, 64: 1-55. DOI: 10.1016/j.preteyeres.2017.11.003.
5. Um T, Seo EJ, Kim YJ, et al. Optical coherence tomography angiography findings of type 1 diabetic patients with diabetic retinopathy, in comparison with type 2 patients[J]. Graefe's Arch Clin Exp Ophthalmol, 2020, 258(2): 281-288. DOI: 10.1007/s00417-019-04517-6.
6. American Diabetes Association. 11. Microvascular complications and foot care: standards of medical care in diabetes-2020[J]. Diabetes Care, 2020, 43(Suppl 1): S135-151. DOI: 10.2337/dc20-S011.
7. 中华医学会眼科学会眼底病学组. 我国糖尿病视网膜病变临床诊疗指南(2014年)[J]. 中华眼科杂志, 2014, 50(11): 851-865. DOI: 10.3760/cma.j.issn.0412-4081.2014.11.014.Ocular Fundus Diseases Group of Ophthalmological Society of Chinese Medical Association. Guidelines for clinical diagnosis and treatment of diabetic retinopathy in China(2014)[J]. Chin J Ophthalmol, 2014, 50(11): 851-865. DOI: 10.3760/cma.j.issn.0412-4081.2014.11.014.
8. Campbell JP, Zhang M, Hwang TS, et al. Detailed cascular anatomy of the human retina by projection-resolved optical coherence tomography angiography[J/OL]. Sci Rep, 2017, 7: 42201[2017-02-10]. https://pubmed.ncbi.nlm.nih.gov/28186181/. DOI: 10.1038/srep42201.
9. 李琳, 李全民. 糖尿病肾病美国糖尿病协会指南更新要点及治疗进展[J]. 中华糖尿病杂志, 2020, 12(6): 424-428. DOI: 10.3760/cma.j.cn115791-20200320-00166.Li L, Li QM. Update and progress of American Diabetes Association guidelines for diabetic kidney disease[J]. Chin J of Diabetes Mellitus, 2020, 12(6): 424-428. DOI: 10.3760/cma.j.cn115791-20200320-00166.
10. El-Asrar AM, Al-Rubeaan KA, Al-Amro SA, et al. Retinopathy as a predictor of other diabetic complications[J]. Int Ophthalmol, 2001, 24(1): 1-11. DOI: 10.1023/a:1014409829614.
11. Hsing SC, Lee CC, Lin C, et al. The severity of diabetic retinopathy is an independent factor for the progression of diabetic nephropathy[J]. J Clin Med, 2020, 10(1): 3. DOI: 10.3390/jcm10010003.
12. Martín-Merino E, Fortuny J, Rivero-Ferrer E, et al. Incidence of retinal complications in a cohort of newly diagnosed diabetic patients[J/OL]. PLoS One, 2014, 9(6): e100283[2014-06-25]. https://pubmed.ncbi.nlm.nih.gov/24963628/. DOI: 10.1371/journal.pone.0100283.
13. Cankurtaran V, Inanc M, Tekin K, et al. Retinal microcirculation in predicting diabetic nephropathy in type 2 diabetic patients without retinopathy[J]. Ophthalmologica, 2020, 243(4): 271-279. DOI: 10.1159/000504943.
14. Lou J, Jing L, Yang H, et al. Risk factors for diabetic nephropathy complications in community patients with type 2 diabetes mellitus in Shanghai: logistic regression and classification tree model analysis[J]. Int J Health Plann Manage, 2019, 34(3): 1013-1024. DOI: 10.1002/hpm.2871.
15. Blair NP, Wanek J, Felder AE, et al. Retinal oximetry and vessel diameter measurements with a commercially available scanning laser ophthalmoscope in diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 2017, 58(12): 5556-5563. DOI: 10.1167/iovs.17-21934.
16. Fondi K, Wozniak PA, Howorka K, et al. Retinal oxygen extraction in individuals with type 1 diabetes with no or mild diabetic retinopathy[J]. Diabetologia, 2017, 60(8): 1534-1540. DOI: 10.1007/s00125-017-4309-0.
17. 滕娟, 余海跃, 陈志萍, 等. 2型糖尿病患者尿微量白蛋白含量与黄斑区视网膜微循环相关性分析[J]. 眼科新进展, 2020, 40(10): 952-956. DOI: 10.13389/j.cnki.rao.2020.0214.Teng J, Yu HY, Chen ZP, et al. Correlation analysis between microalbumin changes and macular retinal microcirculation in type 2 diabetic patients[J]. Rec Adv in Ophthalmol, 2020, 40(10): 952-956. DOI: 10.13389/j.cnki.rao.2020.0214.
18. Sasso FC, Pafundi PC, Gelso A, et al. Relationship between albuminuric CKD and diabetic retinopathy in a real-world setting of type 2 diabetes: findings from no blind study[J]. Nutr Metab Cardiovasc Dis, 2019, 29(9): 923-930. DOI: 10.1016/j.numecd.2019.05.065.
19. Kaewput W, Thongprayoon C, Rangsin R, et al. Associations of renal function with diabetic retinopathy and visual impairment in type 2 diabetes: a multicenter nationwide cross-sectional study[J]. World J Nephrol, 2019, 8(2): 33-43. DOI: 10.5527/wjn.v8.i2.33.
20. Jiang S, Yu T, Zhang Z, et al. Diagnostic performance of retinopathy in the detection of diabetic nephropathy in type 2 diabetes: a systematic review and meta-analysis of 45 studies[J]. Ophthalmic Res, 2019, 62(2): 68-79. DOI: 10.1159/000500833.
21. 曾运考, 杨大卫, 曹丹, 等. 早期不同分期糖尿病视网膜病变黄斑区血流密度及血管结构改变[J]. 中华实验眼科杂志, 2020, 38(9): 783-787. DOI: 10.3760/cma.j.cn115989-20200715-00497.Zeng YK, Yang DW, Cao D, et al. Changes of macular vessel density and structures in different early stages of diabetic retinopathy[J]. Chin J Exp Ophthalmol, 2020, 38(9): 783-787. DOI: 10.3760/cma.j.cn115989-20200715-00497.
22. Khatri A, Pradhan E, Kc BK, et al. Detection, localization, and characterization of vision-threatening features of microaneurysms using optical coherence tomography angiography in diabetic maculopathy[J]. Eur J Ophthalmol, 2021, 31(3): 1208-1215. DOI: 10.1177/1120672120924609.
23. DaCosta J, Bhatia D, Talks J. The use of optical coherence tomography angiography and optical coherence tomography to predict visual acuity in diabetic retinopathy[J]. Eye (Lond), 2020, 34(5): 942-947. DOI: 10.1038/s41433-019-0606-9.
24. 中华医学会糖尿病学分会微血管并发症学组. 中国糖尿病肾脏疾病防治临床指南[J]. 中华糖尿病杂志, 2019, 11(1): 15-28. DOI: 10.3760/cma.j.issn.1674-5809.2019.01.004.Microvascular Complications Group, Diabetes Society, Chinese Medical Association. Chinese clinical practice guideline of diabetic kidney disease[J]. Chin J of Diabetes Mellitus, 2019, 11(1): 15-28. DOI: 10.3760/cma.j.issn.1674-5809.2019.01.004.
25. Ashimatey BS, Green KM, Chu Z, et al. Impaired retinal vascular reactivity in diabetic retinopathy as assessed by optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2019, 60(7): 2468-2473. DOI: 10.1167/iovs.18-26417.
26. Lee H, Lee M, Chung H, et al. Quantification of retinal vessel tortuosity in diabetic retinopathy using optical coherence tomography angiography[J]. Retina, 2018, 38(5): 976-985. DOI: 10.1097/iae.0000000000001618.
27. Sousa DC, Leal I, Moreira S, et al. A protocol to evaluate retinal vascular response using optical coherence tomography angiography[J]. Front Neurosci, 2019, 13: 566. DOI: 10.3389/fnins.2019.00566.

Chinese Journal of Ocular Fundus Diseases

Correlations between macular microvascular parameters in patients with type 2 diabetes mellitus and urinary albumin creatinine ratio

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