Quantitative analysis of the effect of HbA1c level on macular microcirculation in patients with type 2 diabetes mellitus_Chinese Journal of Ocular Fundus Diseases

Authors：

Zhu Qiujian ¹ , Bi Mingchao ² , Zhao Ping ¹ , Xu Cailian ¹ , Wu Xue ¹ , Liang Juan ¹ , Zhu Manhui ¹ , Ma Lie ¹ ,  Song E ¹

1. Lixiang Eye Hospital of Soochow University, Suzhou 215021, China;
2. Department of Ophthalmology, Bethune First Hospital of Jilin University, Changchun 130021, China;

Corresponding author：

Song E, Email: songe23@163.com

Keywords：

Diabetes mellitus, type 2; Hemoglobin A, glycosylated; Microcirculation; Tomography, optical coherence

DOI：

10.3760/cma.j.issn.1005-1015.2019.01.003

Video：

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ObjectiveTo observe and analyze the effect of HbA1c level on macular microcirculation in patients with type 2 diabetes mellitus (T2DM).MethodsA cross-sectional study. One hundred and twenty-four T2DM patients (124 eyes) without diabetic retinopathy who diagnosed by the examination of fundus color photography in Lixiang Eye Hospital Of Soochow University during September to December 2017 were enrolled in this study. There were 59 males (59 eyes) and 65 females (65 eyes), with the mean age of 65.06±7.99 years old. All patients underwent BCVA, fundus color photography, and OCT angiography (OCTA). The history of diabetes, hypertension and dyslipidemia were recorded in detail. According to the HbA1c level, patients were divided into three groups, HbA1c ideal control group (group A, HbA1c ＜7%, 67 eyes), HbA1c control group (group B, 7%≤HbA1c≤9%, 44 eyes), and HbA1c poor control group (group C, HbA1c＞9%, 13 eyes), respectively. The 3 mm×3 mm range of the macular area was scanned by OCTA instrument. The vascular density (VD) and skeleton density (SD) of nonsegmented retinal layer (NRL), superficial retinal layer (SRL) and deep retinal layer (DRL) in the macular area and foveal avascular zone (FAZ) area, non-circularity index, axial rate (AR) of SRL were measured. The correlation between HbA1c, BCVA and VD, SD of NRL, SRL, DRL was analyzed statistically with Spearman correlation test. The correlation between systemic factors and the above indicators was analyzed statistically with linear regression analysis.ResultsThe results of linear regression analysis showed that HbA1c was significantly correlated with VD (t=−3.237, −3.156, −2.050) and SD (t=−0.3.45, −3.034, −2.248) of NRL, SRL and DRL (P＜0.05); but no correlation with FAZ, non-circularity index and AR (t=1.739, 0.429, 1.155; P＞0.05). The differences of VD (F=6.349, 5.981, 3.709), SD (F=7.275, 6.085, 1.904) and AR (F=0.027) of NRL, SRL and DRL in group A, B and C were statistically significant (P＜0.05); but the differences of FAZ (F=1.904), non-circularity index (F=0.280) was not statistically significant (P＞0.05). Significant differences (P＜0.05) of VD and SD of NRL were found between group A and B (t=1.987, 2.201), group A and C (t=3.365, 3.572), group B and C (t=2.010, 2.076). Significant differences (P＜0.05) of VD and SD of SRL were found between group A and B (t=2.087, 2.168), group A and C (t=3.197, 3.194). There were significant differences (P＜0.05) in SD of DRL between group A and B (t=2.239), group A and C (t=−2.519). There was significant difference in VD of DRL between group A and C (t=2.363). The results of Spearman correlation analysis showed that HbA1c was negatively correlated with VD (r=−0.273, −0.255, −0.222; P=0.002, 0.004, 0.013) and SD (r=−0.275, −0.236, −0.254; P＜0.05) of NRL, SRL, DRL; positively correlated with FAZ and BCVA (r=0.221, 0.183; P＜0.05). BCVA was negatively correlated with VD (r=−0.210, −0.190, −0.245) and SD (r=−0.239, −0.207, −0.296) of NRL, SRL, and DRL (P＜0.05), but not correlated with FAZ (r=0.099, P＞0.05).ConclusionThe decrease of macular perfusion and the morphological change of FAZ accompanied by HbA1c increased.

Citation： Zhu Qiujian, Bi Mingchao, Zhao Ping, Xu Cailian, Wu Xue, Liang Juan, Zhu Manhui, Ma Lie, Song E. Quantitative analysis of the effect of HbA1c level on macular microcirculation in patients with type 2 diabetes mellitus. Chinese Journal of Ocular Fundus Diseases, 2019, 35(1): 8-14. doi: 10.3760/cma.j.issn.1005-1015.2019.01.003 Copy

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2.	Kim AY, Chu Z, Shahidzadeh A, et al. Quantifying microvascular density and morphology in diabetic retinopathy using spectral-domain optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2016, 57(9): 362-370. DOI: 10.1167/iovs.15-18904.
3.	Durbin MK, An L, Shemonski ND, et al. Quantification of retinal microvascular density in optical coherence tomographic angiography images in diabetic retinopathy[J]. JAMA Ophthalmol, 2017, 135(4): 370-376. DOI: 10.1001/jamaophthalmol.2017.0080.
4.	Krawitz BD, Mo S, Geyman LS, et al. Acircularity index and axis ratio of the foveal avascular zone in diabetic eyes and healthy controls measured by optical coherence tomography angiography[J]. Vision Res, 2017, 139: 177-186. DOI: 10.1016/j.visres.2016.09.019.
5.	王健, 陈松, 何广辉, 等. 无明显糖尿病视网膜病变的2型糖尿病患者黄斑区微血管改变的光相干断层扫描血管成像观察[J]. 中华眼底病杂志, 2017, 33(1): 15-18. DOI: 10.3760/cma.j.issn.1005-1015.2017.01.005.Wang J, Chen S, He GH, et al. Observation of macular microvascular changes in eyes of patients of type 2 diabetes without clinical ;features of diabetic retinopathy by optical coherence tomography angiography[J]. Chin J Ocul Fundus Dis, 2017, 33(1): 15-18. DOI: 10.3760/cma.j.issn.1005-1015.2017.01.005.
6.	邬嘉蔚, 柯晓云, 符敏. 光相干断层扫描血管成像在糖尿病视网膜病变诊断中的应用研究进展[J]. 中华眼底病杂志, 2018, 34(1): 86-89. DOI: 10.3760/cma.j.issn.1005-1015.2018.01.026.Wu JW, Ke XY, Fu M, et al. The value of optical coherence tomography angiography in the diagnosis of diabetic retinopathy[J]. Chin J Ocul Fundus Dis, 2018, 34(1): 86-89. DOI: 10.3760/cma.j.issn.1005-1015.2018.01.026.
7.	Liu Y, Yang J, Tao L, et al. Risk factors of diabetic retinopathy and sight-threatening diabetic retinopathy: a cross-sectional study of 13473 patients with type 2 diabetes mellitus in mainland China[J/OL]. BMJ Open, 2017, 7(9): 016280[2017-09-01]. http://dx.doi.org/10.1136/bmjopen-2017-016280. DOI: 10.1136/bmjopen-2017-016280.
8.	Knudsen LL, Lervang HH, Lundbye-Christensen S, et al. The North Jutland County Diabetic Retinopathy Study (NCDRS) 2. Non-ophthalmic parameters and clinically significant macular oedema[J]. Br J Ophthalmol, 2007, 91(12): 1593-1595. DOI: 10.1136/bjo.2006.111872.
9.	Zhang X, Saaddine JB, Chou CF, et al. Prevalence of diabetic retinopathy in the United States, 2005-2008[J]. JAMA, 2010, 304(6): 649-656. DOI: 10.1001/jama.2010.1111.
10.	Nathan DM, McGee P, Steffes MW, et al. Relationship of glycated albumin to blood glucose and HbA1c values and to retinopathy, nephropathy, and cardiovascular outcomes in the DCCT/EDIC study[J]. Diabetes, 2014, 63(1): 282-290. DOI: 10.2337/db13-0782.
11.	Zhang A, Zhang Q, Chen CL, et al. Methods and algorithms for optical coherence tomography-based angiography: a review and comparison[J/OL]. J Biomed Opt, 2015, 20(10): 100901[2015-10-16]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4881033/. DOI: 10.1117/1.JBO.20.10.100901.
12.	Gao SS, Jia Y, Zhang M, et al. Optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2016, 57(9): 27-36. DOI: 10.1167/iovs.15-19043.
13.	陈沁, 喻晓兵, 戴虹. 糖尿病患者黄斑区视网膜毛细血管形态的光相干断层扫描血管成像观察[J]. 中华眼底病杂志, 2018, 34(4): 328-332. DOI: 10.3760/cma.j.issn.1005-1015.2018.04.004.Chen Q, Yu X, Dai H, et al. The macular capillary morphology in diabetic patients by optical coherence tomography angiography[J]. Chin J Ocul Fundus Dis, 2018, 34(4): 328-332. DOI: 10.3760/cma.j.issn.1005-1015.2018.04.004.
14.	中华医学会糖尿病学分会. 中国2型糖尿病防治指南(2017年版)[J]. 中华糖尿病杂志, 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 (2017)[J]. Chin J Diabetes Mellitus, 2018, 10(1): 4-67. DOI: 10.3760/cma.j.issn.1674-5809.2018.01.003.
15.	World Health Orgnization. Definition and diagnosis of diabetes mellitus and intermediate hyperglycemia: report of a WHO/IDF consultation, 2006[M]. Geneva: WHO Document Production Services, 2006.
16.	Kim AY, Rodger DC, Shahidzadeh A, et al. Quantifying retinal microvascular changes in uveitis using spectral-domain optical coherence tomography angiography[J]. Am J Ophthalmol, 2016, 171: 101-112. DOI: 10.1016/j.ajo.2016.08.035.
17.	Tan ACS, Tan GS, Denniston AK, et al. An overview of the clinical applications of optical coherence tomography angiography[J]. Eye (Lond), 2018, 32(2): 262-286. DOI: 10.1038/eye.2017.181.
18.	Ishibazawa A, Nagaoka T, Takahashi A, et al. optical coherence tomography angiography in diabetic retinopathy: a prospective pilot study[J]. Am J Ophthalmol, 2015, 160(1): 35-44. DOI: 10.1016/j.ajo.2015.04.021.
19.	Kashani AH, Chen CL, Gahm JK, et al. Optical coherence tomography angiography: a comprehensive review of current methods and clinical applications[J]. Prog Retin Eye Res, 2017, 60: 66-100. DOI: 10.1016/j.preteyeres.2017.07.002.
20.	Shahlaee A, Pefkianaki M, Hsu J, et al. Measurement of foveal avascular zone dimensions and its reliability in healthy eyes using optical coherence tomography angiography[J]. Am J Ophthalmol, 2016, 161: 50-55. DOI: 10.1016/j.ajo.2015.09.026.
21.	Rodríguez-Segade S, Rodríguez J, Paz JM, et al. Translating the A1C assay into estimated average glucose values: response to Nathan et al[J]. Diabetes Care, 2009, 32(1): 10-12. DOI: 10.2337/dc08-1214.
22.	Vieira-Potter VJ, Karamichos D, Lee DJ. Ocular complications of diabetes and therapeutic approaches[J/OL]. Biomed Res Int, 2016, 2016: 3801570[2016-03-28]. http://dx.doi.org/10.1155/2016/3801570. DOI: 10.1155/2016/3801570.
23.	Samara WA, Shahlaee A, Adam MK, et al. Quantification of diabetic macular ischemia using optical coherence tomography angiography and its relationship with visual acuity[J]. Ophthalmology, 2017, 124(2): 235-244. DOI: 10.1016/j.ophtha.2016.10.008.
24.	Nawy S, Jahr CE. Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells[J]. Nature, 1990, 346(6281): 269-271. DOI: 10.1038/346269a0.
25.	Chaya T, Matsumoto A, Sugita Y, et al. Versatile functional roles of horizontal cells in the retinal circuit[J/OL]. Sci Rep, 2017, 7(1): 5540[2017-07-17].https://www.nature.com/articles/s41598-017-05543-2. DOI: 10.1038/s41598-017-05543-2.
26.	Reif R, Qin J, An L, et al. Quantifying optical microangiography images obtained from a spectral domain optical coherence tomography system[J]. Int J Biomed Imaging. 2012, 2012: 509783[2012-06-26]. http://dx.doi.org/10.1155/2012/509783. DOI: 10.1155/2012/509783.
27.	Dimitrova G, Chihara E, Takahashi H, et al. Quantitative retinal optical coherence tomography angiography in patients with diabetes without diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 2017, 58(1): 190-196. DOI: 10.1167/iovs.16-20531.

1. Agemy SA,Scripsema NK,Shah CM, et al. Retinal vascular perfusion density mapping using optical coherence tomography angiography in normals and diabetic retinopathy patients[J]. Retina, 2015, 35(11): 2353-2363. DOI: 10.1097/iae.0000000000000862.
2. Kim AY, Chu Z, Shahidzadeh A, et al. Quantifying microvascular density and morphology in diabetic retinopathy using spectral-domain optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2016, 57(9): 362-370. DOI: 10.1167/iovs.15-18904.
3. Durbin MK, An L, Shemonski ND, et al. Quantification of retinal microvascular density in optical coherence tomographic angiography images in diabetic retinopathy[J]. JAMA Ophthalmol, 2017, 135(4): 370-376. DOI: 10.1001/jamaophthalmol.2017.0080.
4. Krawitz BD, Mo S, Geyman LS, et al. Acircularity index and axis ratio of the foveal avascular zone in diabetic eyes and healthy controls measured by optical coherence tomography angiography[J]. Vision Res, 2017, 139: 177-186. DOI: 10.1016/j.visres.2016.09.019.
5. 王健, 陈松, 何广辉, 等. 无明显糖尿病视网膜病变的2型糖尿病患者黄斑区微血管改变的光相干断层扫描血管成像观察[J]. 中华眼底病杂志, 2017, 33(1): 15-18. DOI: 10.3760/cma.j.issn.1005-1015.2017.01.005.Wang J, Chen S, He GH, et al. Observation of macular microvascular changes in eyes of patients of type 2 diabetes without clinical ;features of diabetic retinopathy by optical coherence tomography angiography[J]. Chin J Ocul Fundus Dis, 2017, 33(1): 15-18. DOI: 10.3760/cma.j.issn.1005-1015.2017.01.005.
6. 邬嘉蔚, 柯晓云, 符敏. 光相干断层扫描血管成像在糖尿病视网膜病变诊断中的应用研究进展[J]. 中华眼底病杂志, 2018, 34(1): 86-89. DOI: 10.3760/cma.j.issn.1005-1015.2018.01.026.Wu JW, Ke XY, Fu M, et al. The value of optical coherence tomography angiography in the diagnosis of diabetic retinopathy[J]. Chin J Ocul Fundus Dis, 2018, 34(1): 86-89. DOI: 10.3760/cma.j.issn.1005-1015.2018.01.026.
7. Liu Y, Yang J, Tao L, et al. Risk factors of diabetic retinopathy and sight-threatening diabetic retinopathy: a cross-sectional study of 13473 patients with type 2 diabetes mellitus in mainland China[J/OL]. BMJ Open, 2017, 7(9): 016280[2017-09-01]. http://dx.doi.org/10.1136/bmjopen-2017-016280. DOI: 10.1136/bmjopen-2017-016280.
8. Knudsen LL, Lervang HH, Lundbye-Christensen S, et al. The North Jutland County Diabetic Retinopathy Study (NCDRS) 2. Non-ophthalmic parameters and clinically significant macular oedema[J]. Br J Ophthalmol, 2007, 91(12): 1593-1595. DOI: 10.1136/bjo.2006.111872.
9. Zhang X, Saaddine JB, Chou CF, et al. Prevalence of diabetic retinopathy in the United States, 2005-2008[J]. JAMA, 2010, 304(6): 649-656. DOI: 10.1001/jama.2010.1111.
10. Nathan DM, McGee P, Steffes MW, et al. Relationship of glycated albumin to blood glucose and HbA1c values and to retinopathy, nephropathy, and cardiovascular outcomes in the DCCT/EDIC study[J]. Diabetes, 2014, 63(1): 282-290. DOI: 10.2337/db13-0782.
11. Zhang A, Zhang Q, Chen CL, et al. Methods and algorithms for optical coherence tomography-based angiography: a review and comparison[J/OL]. J Biomed Opt, 2015, 20(10): 100901[2015-10-16]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4881033/. DOI: 10.1117/1.JBO.20.10.100901.
12. Gao SS, Jia Y, Zhang M, et al. Optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2016, 57(9): 27-36. DOI: 10.1167/iovs.15-19043.
13. 陈沁, 喻晓兵, 戴虹. 糖尿病患者黄斑区视网膜毛细血管形态的光相干断层扫描血管成像观察[J]. 中华眼底病杂志, 2018, 34(4): 328-332. DOI: 10.3760/cma.j.issn.1005-1015.2018.04.004.Chen Q, Yu X, Dai H, et al. The macular capillary morphology in diabetic patients by optical coherence tomography angiography[J]. Chin J Ocul Fundus Dis, 2018, 34(4): 328-332. DOI: 10.3760/cma.j.issn.1005-1015.2018.04.004.
14. 中华医学会糖尿病学分会. 中国2型糖尿病防治指南(2017年版)[J]. 中华糖尿病杂志, 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 (2017)[J]. Chin J Diabetes Mellitus, 2018, 10(1): 4-67. DOI: 10.3760/cma.j.issn.1674-5809.2018.01.003.
15. World Health Orgnization. Definition and diagnosis of diabetes mellitus and intermediate hyperglycemia: report of a WHO/IDF consultation, 2006[M]. Geneva: WHO Document Production Services, 2006.
16. Kim AY, Rodger DC, Shahidzadeh A, et al. Quantifying retinal microvascular changes in uveitis using spectral-domain optical coherence tomography angiography[J]. Am J Ophthalmol, 2016, 171: 101-112. DOI: 10.1016/j.ajo.2016.08.035.
17. Tan ACS, Tan GS, Denniston AK, et al. An overview of the clinical applications of optical coherence tomography angiography[J]. Eye (Lond), 2018, 32(2): 262-286. DOI: 10.1038/eye.2017.181.
18. Ishibazawa A, Nagaoka T, Takahashi A, et al. optical coherence tomography angiography in diabetic retinopathy: a prospective pilot study[J]. Am J Ophthalmol, 2015, 160(1): 35-44. DOI: 10.1016/j.ajo.2015.04.021.
19. Kashani AH, Chen CL, Gahm JK, et al. Optical coherence tomography angiography: a comprehensive review of current methods and clinical applications[J]. Prog Retin Eye Res, 2017, 60: 66-100. DOI: 10.1016/j.preteyeres.2017.07.002.
20. Shahlaee A, Pefkianaki M, Hsu J, et al. Measurement of foveal avascular zone dimensions and its reliability in healthy eyes using optical coherence tomography angiography[J]. Am J Ophthalmol, 2016, 161: 50-55. DOI: 10.1016/j.ajo.2015.09.026.
21. Rodríguez-Segade S, Rodríguez J, Paz JM, et al. Translating the A1C assay into estimated average glucose values: response to Nathan et al[J]. Diabetes Care, 2009, 32(1): 10-12. DOI: 10.2337/dc08-1214.
22. Vieira-Potter VJ, Karamichos D, Lee DJ. Ocular complications of diabetes and therapeutic approaches[J/OL]. Biomed Res Int, 2016, 2016: 3801570[2016-03-28]. http://dx.doi.org/10.1155/2016/3801570. DOI: 10.1155/2016/3801570.
23. Samara WA, Shahlaee A, Adam MK, et al. Quantification of diabetic macular ischemia using optical coherence tomography angiography and its relationship with visual acuity[J]. Ophthalmology, 2017, 124(2): 235-244. DOI: 10.1016/j.ophtha.2016.10.008.
24. Nawy S, Jahr CE. Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells[J]. Nature, 1990, 346(6281): 269-271. DOI: 10.1038/346269a0.
25. Chaya T, Matsumoto A, Sugita Y, et al. Versatile functional roles of horizontal cells in the retinal circuit[J/OL]. Sci Rep, 2017, 7(1): 5540[2017-07-17].https://www.nature.com/articles/s41598-017-05543-2. DOI: 10.1038/s41598-017-05543-2.
26. Reif R, Qin J, An L, et al. Quantifying optical microangiography images obtained from a spectral domain optical coherence tomography system[J]. Int J Biomed Imaging. 2012, 2012: 509783[2012-06-26]. http://dx.doi.org/10.1155/2012/509783. DOI: 10.1155/2012/509783.
27. Dimitrova G, Chihara E, Takahashi H, et al. Quantitative retinal optical coherence tomography angiography in patients with diabetes without diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 2017, 58(1): 190-196. DOI: 10.1167/iovs.16-20531.

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Quantitative analysis of the effect of HbA1c level on macular microcirculation in patients with type 2 diabetes mellitus

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