Low hemoglobin levels are associated with increased risk of diabetic retinopathy in type 2 diabetes_Chinese Journal of Ocular Fundus Diseases

Authors：

Fu Lingli ¹ , Li Wenjun ¹ , Su Long ² ,  Sun Bei ¹

1. NHC Key Laboratory of Hormones and Development, Tianjin Key Laboratory of Metabolic Diseases, Chu Hsien-I Memorial Hospital & Tianjin Medical University, Tianjin Institute of Endocrinology, Tianjin Medical University, Tianjin 300134, China;
2. Department of Ophthalmology, The Second Hospital of Tianjin Medical University, Tianjin Institute of Orbital Disease, Tianjin 300211, China;
Su Long and Sun Bei are contributed equally to the article;

Corresponding?author：

Sun Bei, Email: sun_peipei220@hotmail.com

Keywords：

Diabetic retinopathy; Hemoglobins; Diabetes mellitus, type 2

DOI：

10.3760/cma.j.cn511434-20201204-00604

Video：

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Objective To assess the association of hemoglobin (Hb) levels with the prevalence of diabetic retinopathy (DR) in patients with type 2 diabetes mellitus (T2DM).Methods A cross-sectional study. From January 2017 to December 2018, 707 patients with T2DM who were hospitalized in the Department of Internal Medicine of Chu Hsien-I Memorial Hospital & Tianjin Medical University, were included in the study. All patients underwent color photography of the fundus of both eyes with dilated pupils. According to DR diagnostic criteria, patients were divided into DR group and non-DR (NDR) group, with 210 and 497 cases, respectively; DR group was further divided into non-proliferative DR group (NPDR) group and proliferative DR (PDR) group, about 186, 24 cases, respectively. Hb level was detected, single factor analysis of its correlation with DR; logistic regression analysis was used to evaluate the relationship between Hb level and DR risk.Results The Hb levels of the patients in the NDR group and the DR group were 140.58±17.26 and 132.35±23.48 g/dl; compared with the NDR group, the Hb level of the DR group was significantly lower, and the difference was statistically significant (t=5.107, P=0.000). In the NDR group, NPDR group, and PDR group, Hb levels of male patients were 149.3±1.01, 142.6±2.35, 132.9±8.44 g/dl, respectively; Hb levels of female patients were 131.7±0.90, 124.0±2.09, 116.8±5.23 g/dl. With the progress of DR, Hb levels of different sexes decreased significantly, and the difference was statistically significant (P＜0.000 1). The results of correlation analysis showed that Hb reduction was an independent risk factor for DR (odds ratio=4.437, 95% confidence interval 2.590-7.603, P＜0.000 1).Conclusion The reduction of Hb in T2DM patients is positively correlated with the severity of DR.

Citation： Fu Lingli, Li Wenjun, Su Long, Sun Bei. Low hemoglobin levels are associated with increased risk of diabetic retinopathy in type 2 diabetes. Chinese Journal of Ocular Fundus Diseases, 2021, 37(7): 528-532. doi: 10.3760/cma.j.cn511434-20201204-00604 Copy

1.	Zheng Y, He M, Congdon N. The worldwide epidemic of diabetic retinopathy[J]. Indian J Ophthalmol, 2012, 60(5): 428-431. DOI: 10.4103/0301-4738.100542.
2.	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): e016280[2017-09-01]. https://pubmed.ncbi.nlm.nih.gov/28864696/. DOI: 10.1136/bmjopen-2017-016280.
3.	Furuyama K, Kaneko K, Vargas PD. Heme as a magnificent molecule with multiple missions: heme determines its own fate and governs cellular homeostasis[J]. Tohoku J Exp Med, 2007, 213(1): 1-16. DOI: 10.1620/tjem.213.1.
4.	Dunst J, Becker A, Lautenschl?ger C, et al. Anemia and elevated systemic levels of vascular endothelial growth factor (VEGF)[J]. Strahlenther Onkol, 2002, 178(8): 436-441. DOI: 10.1007/s00066-002-0925-8.
5.	王敏, 汲寶蘭, 班博, 等. 2型糖尿病患者血紅蛋白水平與視網膜病變風險的相關研究[J]. 中華內分泌代謝雜志, 2019, 35(5): 387-390. DOI: 10.3760/cma.j.issn.1000-6699.2019.02.007.Wang M, Ji BL, Ban B, et al. Association between hemoglobin levels and diabetic retinopathy risk in type 2 diabetes mellitus[J]. Chin J Endocrinol Metab, 2019, 35(5): 387-390. DOI: 10.3760/cma.j.issn.1000-6699.2019.02.007.
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8.	Early Treatment Diabetic Retinopathy Study Research Group. Grading diabetic retinopathy from stereoscopic color fundus photographs--an extension of the modified Airlie house classification. ETDRS report number 10[J]. Ophthalmology, 1991, 98(5 Suppl): 786-806.
9.	Vujosevic S, Aldington SJ, Silva P, et al. Screening for diabetic retinopathy: new perspectives and challenges[J]. Lancet Diabetes Endocrinol, 2020, 8(4): 337-347. DOI: 10.1016/S2213-8587(19)30411-5.
10.	Flaxel CJ, Adelman RA, Bailey ST, et al. Diabetic retinopathy preferred practice pattern^?[J]. Ophthalmology, 2020, 127(1): P66-P145. DOI: 10.1016/j.ophtha.2019.09.025.
11.	Yau JW, Rogers SL, Kawasaki R, et al. Global prevalence and major risk factors of diabetic retinopathy[J]. Diabetes Care, 2012, 35(3): 556-564. DOI: 10.2337/dc11-1909.
12.	李筱榮, 楊千惠. 美國眼科學會《糖尿病視網膜病變臨床指南》解讀[J]. 中華實驗眼科雜志, 2020, 38(9): 795-798. DOI: 10.3760/cma.j.cn115989-20200518-00350.Li XR, Yang QH. Interpretation of diabetic retionpathy preferred practice pattern^?[J]. Chin J Exp Ophthalmol, 2020, 38(9): 795-798. DOI: 10.3760/cma.j.cn115989-20200518-00350.
13.	Hosseini MS, Rostami Z, Saadat A, et al. Anemia and microvascular complications in patients with type 2 diabetes mellitus[J/OL]. Nephrourol Mon, 2014, 6(4): e19976[2014-07-05]. https://pubmed.ncbi.nlm.nih.gov/25695026/. DOI: 10.5812/numonthly.19976.
14.	Sepúlveda FJ, Pérez P, Medinilla MG, et al. Anemia as a factor related to the progression of proliferative diabetic retinopathy afer photocoagulation[J]. Diabetes Complications, 2012, 26(5): 454-457. DOI: 10.1016/j.jdiacomp.2012.04.013.
15.	Chung JO, Park SY, Chung DJ, et al. Relationship between anemia, serum bilirubin concentrations and diabetic retinopathy in individuals with type 2 diabetes[J/OL]. Medicine (Baltimore), 2019, 98(43): e17693[2019-10-25]. https://pubmed.ncbi.nlm.nih.gov/31651899/. DOI: 10.1097/MD.0000000000017693.
16.	Traveset A, Rubinat E, Ortega E, et al. Lower hemoglobin concentration is associated with retinal ischemia and the severity of diabetic retinopathy in type 2 diabetes[J/OL]. J Diabetes Res, 2016, 3674946[2016-04-20]. https://pubmed.ncbi.nlm.nih.gov/27200379/. DOI: 10.1155/2016/3674946.
17.	Ajoy Mohan VK, Nithyanandam S, Idiculla J. Microalbuminuria and low hemoglobin as risk factors for the occurrence and increasing severity of diabetic retinopathy[J]. Indian J Ophthalmol, 2011, 59(3): 207-210. DOI: 10.4103/0301-4738.81029.
18.	Davis MD, Fisher MR, Gagnon RE, et al. Risk factors for high risk proliferative diabetic retinopathy and severe visual loss: early treatment diabetic retinopathy study report 18[J]. Invest Ophthalmol Vis Sci, 1998, 39: 233-252.
19.	Kajihara T, Uchino S, Suzuki M, et al. Human chorionic gonadotropin confers resistance to oxidative stress-induced apoptosis in decidualizing human endometrial stromal cells[J]. Fertil Steril, 2011, 95(4): 1302-1307. DOI: 10.1016/j.fertnstert.2010.05.048.
20.	Rajabian F, Mohri M, Heidarpour M. Relationships between oxidative stress, haematology and iron profile in anaemic and non-anaemic calves[J/OL]. Vet Rec, 2017, 181(10): 265[2017-09-09]. https://pubmed.ncbi.nlm.nih.gov/28774940/. DOI: 10.1136/vr.104179.
21.	DeNiro M, Al-Mohanna FA. Erythropoietin and anemia: biological markers that cannot be ignored in diabetic retinopathy[J]. Med Hypotheses, 2012, 78: 555-556. DOI: 10.1016/j.mehy.2012.01.026.
22.	Bahar A, Kashi Z, Ahmadzadeh Amiri A, et al. Association between diabetic retinopathy and hemoglobin level[J]. Caspian J Intern Med, 2013, 4(4): 759-762.
23.	Thomas MC. Anemia in diabetes: marker or mediator of microvascular disease?[J]. Nat Clin Pract Nephrol, 2007, 3: 20-30. DOI: 10.1038/ncpneph0378.

1. Zheng Y, He M, Congdon N. The worldwide epidemic of diabetic retinopathy[J]. Indian J Ophthalmol, 2012, 60(5): 428-431. DOI: 10.4103/0301-4738.100542.
2. 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): e016280[2017-09-01]. https://pubmed.ncbi.nlm.nih.gov/28864696/. DOI: 10.1136/bmjopen-2017-016280.
3. Furuyama K, Kaneko K, Vargas PD. Heme as a magnificent molecule with multiple missions: heme determines its own fate and governs cellular homeostasis[J]. Tohoku J Exp Med, 2007, 213(1): 1-16. DOI: 10.1620/tjem.213.1.
4. Dunst J, Becker A, Lautenschl?ger C, et al. Anemia and elevated systemic levels of vascular endothelial growth factor (VEGF)[J]. Strahlenther Onkol, 2002, 178(8): 436-441. DOI: 10.1007/s00066-002-0925-8.
5. 王敏, 汲寶蘭, 班博, 等. 2型糖尿病患者血紅蛋白水平與視網膜病變風險的相關研究[J]. 中華內分泌代謝雜志, 2019, 35(5): 387-390. DOI: 10.3760/cma.j.issn.1000-6699.2019.02.007.Wang M, Ji BL, Ban B, et al. Association between hemoglobin levels and diabetic retinopathy risk in type 2 diabetes mellitus[J]. Chin J Endocrinol Metab, 2019, 35(5): 387-390. DOI: 10.3760/cma.j.issn.1000-6699.2019.02.007.
6. Lee M, Han K, Lee J, et al. High hemoglobin levels are associated with decreased risk of diabetic retinopathy in Korean type 2 diabetes[J/OL]. Sci Rep, 2018, 8(1): 5538[2018-04-03]. https://pubmed.ncbi.nlm.nih.gov/29615813/. DOI: 10.1038/s41598-018-23905-2.
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.Diabetes Branch of Chinese Medical Association. Guidelines for the prevention and control of type 2 diabetes in China (2017 Edition)[J]. Chin J Diabetes Mellitus, 2018, 10(1): 4-67. DOI: 10.3760/cma.j.issn.1674-5809.2018.01.003.
8. Early Treatment Diabetic Retinopathy Study Research Group. Grading diabetic retinopathy from stereoscopic color fundus photographs--an extension of the modified Airlie house classification. ETDRS report number 10[J]. Ophthalmology, 1991, 98(5 Suppl): 786-806.
9. Vujosevic S, Aldington SJ, Silva P, et al. Screening for diabetic retinopathy: new perspectives and challenges[J]. Lancet Diabetes Endocrinol, 2020, 8(4): 337-347. DOI: 10.1016/S2213-8587(19)30411-5.
10. Flaxel CJ, Adelman RA, Bailey ST, et al. Diabetic retinopathy preferred practice pattern^?[J]. Ophthalmology, 2020, 127(1): P66-P145. DOI: 10.1016/j.ophtha.2019.09.025.
11. Yau JW, Rogers SL, Kawasaki R, et al. Global prevalence and major risk factors of diabetic retinopathy[J]. Diabetes Care, 2012, 35(3): 556-564. DOI: 10.2337/dc11-1909.
12. 李筱榮, 楊千惠. 美國眼科學會《糖尿病視網膜病變臨床指南》解讀[J]. 中華實驗眼科雜志, 2020, 38(9): 795-798. DOI: 10.3760/cma.j.cn115989-20200518-00350.Li XR, Yang QH. Interpretation of diabetic retionpathy preferred practice pattern^?[J]. Chin J Exp Ophthalmol, 2020, 38(9): 795-798. DOI: 10.3760/cma.j.cn115989-20200518-00350.
13. Hosseini MS, Rostami Z, Saadat A, et al. Anemia and microvascular complications in patients with type 2 diabetes mellitus[J/OL]. Nephrourol Mon, 2014, 6(4): e19976[2014-07-05]. https://pubmed.ncbi.nlm.nih.gov/25695026/. DOI: 10.5812/numonthly.19976.
14. Sepúlveda FJ, Pérez P, Medinilla MG, et al. Anemia as a factor related to the progression of proliferative diabetic retinopathy afer photocoagulation[J]. Diabetes Complications, 2012, 26(5): 454-457. DOI: 10.1016/j.jdiacomp.2012.04.013.
15. Chung JO, Park SY, Chung DJ, et al. Relationship between anemia, serum bilirubin concentrations and diabetic retinopathy in individuals with type 2 diabetes[J/OL]. Medicine (Baltimore), 2019, 98(43): e17693[2019-10-25]. https://pubmed.ncbi.nlm.nih.gov/31651899/. DOI: 10.1097/MD.0000000000017693.
16. Traveset A, Rubinat E, Ortega E, et al. Lower hemoglobin concentration is associated with retinal ischemia and the severity of diabetic retinopathy in type 2 diabetes[J/OL]. J Diabetes Res, 2016, 3674946[2016-04-20]. https://pubmed.ncbi.nlm.nih.gov/27200379/. DOI: 10.1155/2016/3674946.
17. Ajoy Mohan VK, Nithyanandam S, Idiculla J. Microalbuminuria and low hemoglobin as risk factors for the occurrence and increasing severity of diabetic retinopathy[J]. Indian J Ophthalmol, 2011, 59(3): 207-210. DOI: 10.4103/0301-4738.81029.
18. Davis MD, Fisher MR, Gagnon RE, et al. Risk factors for high risk proliferative diabetic retinopathy and severe visual loss: early treatment diabetic retinopathy study report 18[J]. Invest Ophthalmol Vis Sci, 1998, 39: 233-252.
19. Kajihara T, Uchino S, Suzuki M, et al. Human chorionic gonadotropin confers resistance to oxidative stress-induced apoptosis in decidualizing human endometrial stromal cells[J]. Fertil Steril, 2011, 95(4): 1302-1307. DOI: 10.1016/j.fertnstert.2010.05.048.
20. Rajabian F, Mohri M, Heidarpour M. Relationships between oxidative stress, haematology and iron profile in anaemic and non-anaemic calves[J/OL]. Vet Rec, 2017, 181(10): 265[2017-09-09]. https://pubmed.ncbi.nlm.nih.gov/28774940/. DOI: 10.1136/vr.104179.
21. DeNiro M, Al-Mohanna FA. Erythropoietin and anemia: biological markers that cannot be ignored in diabetic retinopathy[J]. Med Hypotheses, 2012, 78: 555-556. DOI: 10.1016/j.mehy.2012.01.026.
22. Bahar A, Kashi Z, Ahmadzadeh Amiri A, et al. Association between diabetic retinopathy and hemoglobin level[J]. Caspian J Intern Med, 2013, 4(4): 759-762.
23. Thomas MC. Anemia in diabetes: marker or mediator of microvascular disease?[J]. Nat Clin Pract Nephrol, 2007, 3: 20-30. DOI: 10.1038/ncpneph0378.

Chinese Journal of Ocular Fundus Diseases

Low hemoglobin levels are associated with increased risk of diabetic retinopathy in type 2 diabetes

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