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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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.	中華醫學會糖尿病學分會糖尿病慢性并發癥調查組. 全國住院糖尿病患者慢性并發癥及其相關危險因素10年回顧性調查分析[J]. 中國糖尿病雜志, 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.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. 糖尿病腎病美國糖尿病協會指南更新要點及治療進展[J]. 中華糖尿病雜志, 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, 余海躍, 陳志萍, 等. 2型糖尿病患者尿微量白蛋白含量與黃斑區視網膜微循環相關性分析[J]. 眼科新進展, 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.	曾運考, 楊大衛, 曹丹, 等. 早期不同分期糖尿病視網膜病變黃斑區血流密度及血管結構改變[J]. 中華實驗眼科雜志, 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.	中華醫學會糖尿病學分會微血管并發癥學組. 中國糖尿病腎臟疾病防治臨床指南[J]. 中華糖尿病雜志, 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. 楊文英. 中國糖尿病的流行特點及變化趨勢[J]. 中國科學(生命科學), 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. 中華醫學會糖尿病學分會糖尿病慢性并發癥調查組. 全國住院糖尿病患者慢性并發癥及其相關危險因素10年回顧性調查分析[J]. 中國糖尿病雜志, 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.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. 糖尿病腎病美國糖尿病協會指南更新要點及治療進展[J]. 中華糖尿病雜志, 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, 余海躍, 陳志萍, 等. 2型糖尿病患者尿微量白蛋白含量與黃斑區視網膜微循環相關性分析[J]. 眼科新進展, 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. 曾運考, 楊大衛, 曹丹, 等. 早期不同分期糖尿病視網膜病變黃斑區血流密度及血管結構改變[J]. 中華實驗眼科雜志, 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. 中華醫學會糖尿病學分會微血管并發癥學組. 中國糖尿病腎臟疾病防治臨床指南[J]. 中華糖尿病雜志, 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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