Effect of mild anemia on prognosis of proliferative diabetic retinopathy after pars plana vitrectomy_Chinese Journal of Ocular Fundus Diseases

Authors：

Zhong Qiqi ¹ , Zhang Chenguang ¹ ,  Lin Tiezhu ²

1. Department of Ophthalmology, Zhejiang Provincial People's Hospital, Hangzhou 310014, China;
2. Department of Ophthalmology, Shenyang He Eye Hospital, Shenyang 110002, China;

Corresponding author：

Lin Tiezhu, Email: 360970814@qq.com

Keywords：

Pars plana vitrectomy; Anemia; Proliferative diabetic retinopathy; Visual prognosis

DOI：

10.3760/cma.j.cn511434-20220926-00362

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To observe the effect of mild anemia on prognosis of hyperplastic diabetic retinopathy (PDR) treated by pars plana vitrectomy (PPV). Methods A retrospective case-control study. From January 2021 to December 2022, 147 PDR patients with 147 eyes who received PPV treatment at Shenyang He Eye Hospital were included in the study. There were 147 eyes in 147 cases, 82 eyes in 82 males and 65 eyes in 65 females. Age was 25-79 (53.54±12.74) years old. A hemoglobin (Hb) of 90 to 120 g/L in men and 90 to 110 g/L in women was defined as mild anemia. According to Hb results, the patients were divided into mild anemia group and non-anemia group, with 39 cases (39 eyes) and 108 cases (108 eyes), respectively. The best corrected visual acuity (BCVA) test was performed using the international standard logarithmic visual acuity scale before and after the surgery, which was statistically converted to minimum resolved logarithmic (logMAR) visual acuity. The logMAR BCVA of the affected eye was 0.2-2.5 (1.60±0.62) before surgery. According to whether the BCVA improved by more than 3 lines 6 months after surgery, the affected eyes were divided into BCVA improved by more than 3 lines and BCVA improved by less than 3 lines, 117 eyes and 30 eyes, respectively. The patient's body mass index (BMI), BCVA at 6 months after surgery, and the occurrence of neovascular glaucoma (NVG) and recurrence of vitreous hemorrhage (RVH) were recorded. Independent sample t test was used for comparison between groups. Multivariate logistic regression analysis was performed to analyze the influencing factors of increased BCVA ≥3 rows after surgery. Results Six months after surgery, the logMAR BCVA of patients in mild anemia group and non-anemia group were 0.97±0.87 and 0.68±0.63, respectively. BCVA increased ≥3 in 26 (66.7%, 26/39) and 91 (84.3%, 91/108) eyes, respectively. logMAR BCVA (t=2.234) and BCVA increased by ≥3 rows of eyes (χ²=5.460) between the two groups, the differences were statistically significant (P=0.027, 0.019). Logistic regression analysis showed that baseline logMAR BCVA [odds ratio (OR) =4.291, 95% confidence interval (CI) 1.918-9.600, P＜0.001)], BMI (OR=1.248, 95%CI 1.057-1.472, P=0.009), the number of retinal laser photocoagulation during surgery (OR=1.001, 95%CI 1.000-1.002, P=0.038), mild anemia (OR=0.360, 95%CI 0.131-0.993, P=0.048), postoperative NVG (OR=0.156, 95%CI 0.033-0.726, P=0.018) and RVH (OR=0.264, 95%CI 0.086-0.808, P=0.020) were independent factors for BCVA improvement ≥3 lines after PPV. Conclusions Mild anemia has a certain effect on BCVA improvement after PPV of PDR. Mild anemia, post-operative NVG and RVH were independent risk factors for increasing BCVA ≥3 lines after PPV in PDR patients.

1.	Teo ZL, Tham YC, Yu M, et al. Global prevalence of diabetic retinopathy and projection of burden through 2045: systematic review and meta-analysis[J]. Ophthalmology, 2021, 128(11): 1580-1591. DOI: 10.1016/j.ophtha.2021.04.027.
2.	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.
3.	Romero-Aroca P, Baget-Bernaldiz M, Pareja-Rios A, et al. Diabetic macular edema pathophysiology: vasogenic versus inflammatory[J/OL]. J Diabetes Res, 2016, 2016: 2156273[2016-09-28]. https://pubmed.ncbi.nlm.nih.gov/27761468/. DOI: 10.1155/2016/2156273.
4.	Thomas M, Tsalamandris C, MacIsaac R, et al. Anaemia in diabetes: an emerging complication of microvascular disease[J]. Curr Diabetes Rev, 2005, 1(1): 107-126. DOI: 10.2174/1573399052952587.
5.	Bonakdaran S, Gharebaghi M, Vahedian M. Prevalence of anemia in type 2 diabetes and role of renal involvement[J]. Saudi J Kidney Dis Transpl, 2011, 22(2): 286-290.
6.	Keane WF, Zhang Z, Lyle PA, et al. Risk scores for predicting outcomes in patients with type 2 diabetes and nephropathy: the RENAAL study[J]. Clin J Am Soc Nephrol, 2006, 1(4): 761-767. DOI: 10.2215/CJN.01381005.
7.	冯帅, 王天龙. 围手术期贫血与患者血液管理新进展[J]. 国际麻醉学与复苏杂志, 2022, 43(5): 514-517. DOI: 10.3760/cma.j.cn321761-20210413-00549.Feng S, Wang TL. Research advances on perioperative anemia and patients' blood supply management[J]. Int J Anesth Resus, 2022, 43(5): 514-517. DOI: 10.3760/cma.j.cn321761-20210413-00549.
8.	Musallam KM, Tamim HM, Richards T, et al. Preoperative anaemia and postoperative outcomes in non-cardiac surgery: a retrospective cohort study[J]. Lancet, 2011, 378(9800): 1396-1407. DOI: 10.1016/S0140-6736(11)61381-0.
9.	Lee MK, Han KD, Lee JH, 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.
10.	李雪景, 王坤, 姚一民, 等. 慢性肾衰竭患者增生型糖尿病视网膜病变玻璃体切割手术疗效观察及预后影响因素分析[J]. 中华眼底病杂志, 2023, 39(2): 145-152. DOI: 10.3760/cma.j.cn511434-20221030-00564.Li XJ, Wang K, Yao YM, et al. Therapeutic effect and prognostic factors of vitrectomy for proliferative diabetic retinopathy in patients with chronic renal failure[J]. Chin J Ocul Fundus Dis, 2023, 39(2): 145-152. DOI: 10.3760/cma.j.cn511434-20221030-00564.
11.	中华医学会眼科学分会眼底病学组, 中国医师协会眼科医师分会眼底病学组. 我国糖尿病视网膜病变临床诊疗指南(2022年)——基于循证医学修订[J]. 中华眼底病杂志, 2023, 39(2): 91-94. DOI: 10.3760/cma.j.cn511434-20230208-00055.Fundus Disease Group of Ophthalmological Society of Chinese Medical Association, Fundus Disease Group of Ophthalmologist Branch of Chinese Medical Doctor Association. Guidelines for clinical diagnosis and treatment of diabetic retinopathy in China (2022)[J]. Chin J Ocul Fundus Dis, 2023, 39(2): 91-94. DOI: 10.3760/cma.j.cn511434-20230208-00055.
12.	Yuzurihara D, Iijima H. Visual outcome in central retinal and branch retinal artery occlusion[J]. Jpn J Ophthalmol, 2004, 48(5): 490-492. DOI: 10.1007/s10384-004-0102-y.
13.	吴东, 陈嘉林. 贫血(一)[J]. 中华全科医师杂志, 2012, 11(5): 332-333. DOI: 10.3760/cma.j.issn.1671-7368.2012.05.007.Wu D, Chen JL. Anemia(1)[J]. Chin J Gen Pract, 2012, 11(5): 332-333. DOI: 10.3760/cma.j.issn.1671-7368.2012.05.007.
14.	传丰宁, 高幼垣, 田文青, 等. 糖尿病伴发贫血的原因分析[J]. 中华糖尿病杂志, 2016, 8(3): 181-183. DOI: 10.3760/cma.j.issn.1674-5809.2016.03.013.Chuan FN, Gao YY, Tian WQ, et al. Analysis of causes of anemia associated with diabetes mellitus[J]. Chin J Diabetes Mellitus, 2016, 8(3): 181-183. DOI: 10.3760/cma.j.issn.1674-5809.2016.03.013.
15.	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, 2016: 3674946[2016-04-20]. https://pubmed.ncbi.nlm.nih.gov/27200379/. DOI: 10.1155/2016/3674946.
16.	Li Y, Yu Y, VanderBeek BL. Anaemia and the risk of progression from non-proliferative diabetic retinopathy to vision threatening diabetic retinopathy[J]. Eye (Lond), 2020, 34(5): 934-941. DOI: 10.1038/s41433-019-0617-6. DOI: 10.1038/s41433-019-0617-6.
17.	汤芳丽, 邢丽丽, 汪文俊, 等. 2型糖尿病患者血红蛋白水平与糖尿病视网膜病变的相关性研究[J]. 中华内分泌代谢杂志, 2023, 39(7): 560-564. DOI: 10.3760/cma.j.cn311282-20230221-00080.Tang FL, Xing LL, Wang WJ, et al. Correlation between hemoglobin level and diabetic retinopathy in patients with type 2 diabetes mellitus[J]. China J Endocrinal Metab, 2023, 39(7): 560-564. DOI: 10.3760/cma.j.cn311282-20230221-00080.
18.	王敏, 汲宝兰, 班博, 等. 2型糖尿病患者血红蛋白水平与视网膜病变风险的相关研究[J]. 中华内分泌代谢杂志, 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]. China J Endocrinal Metab, 2019, 35(5): 387-390. DOI: 10.3760/cma.j.issn.1000-6699.2019.02.007.
19.	中华医学会外科学分会, 中华外科杂志编辑委员会. 普通外科围手术期缺铁性贫血管理多学科专家共识[J]. 中华外科杂志, 2020, 58(4): 252-256. DOI: 10.3760/cma.j.cn112139-20200210-00073.Chinese Surgical Society, Editorial Board of Chinese Journal of Surgery. Multidisciplinary expert^,s consensus on the management of perioperative iron deficency anemia in patients accepting general surgery[J]. Chin J Surg, 2020, 58(4): 252-256. DOI: 10.3760/cma.j.cn112139-20200210-00073.
20.	Ratnarajan G, Mellington F, Saldanha M, et al. Long-term visual and retinopathy outcomes in a predominately type 2 diabetic patient population undergoing early vitrectomy and endolaser for severe vitreous haemorrhage[J]. Eye (Lond), 2011, 25(6): 704-709. DOI: 10.1038/eye.2011.65.
21.	Lin TZ, Kong Y, Shi C, et al. Prognosis value of Chinese Ocular Fundus Diseases Society classification for proliferative diabetic retinopathy on postoperative visual acuity after pars plana vitrectomy in type 2 diabetes[J]. Int J Ophthalmol, 2022, 15(10): 1627-1633. DOI: 10.18240/ijo.2022.10.10.
22.	翟敏, 王春芳. 增殖型糖尿病视网膜病变玻璃体切除术后虹膜新生血管的危险因素分析[J]. 中国医师杂志, 2017, 19(6): 901-902. DOI: 10.3760/cma.j.issn.1008-1372.2017.06.028.Zhai M, Wang CF. Iris neovascularization after vitrectomy for proliferative diabetic retinopathy Risk factor analysis[J], Journal of Chinese Physician, 2017, 19(6): 901-902. DOI: 10.3760/cma.j.issn.1008-1372.2017.06.028.
23.	祖雪, 代光政, 林铁柱. 增生性糖尿病视网膜病变行玻璃体切割术后发生新生血管性青光眼的风险因素[J]. 国际眼科杂志, 2023, 23(5): 808-812. DOI: 10.3980/j.issn.1672-5123.2023.5.18.Zu X, Dai GZ, Lin TZ. Risk factors associated with neovascular glaucoma after vitrectomy for proliferative diabetic retinopathy[J]. Int Eye Sci, 2023, 23(5): 808-812. DOI: 10.3980/j.issn.1672-5123.2023.5.18.
24.	Nišić F, Pidro A, Lepara O, et al. Effect of pan-retinal laser photocoagulation on intravitreal vascular endothelial growth factor concentration in proliferative diabetic retinopathy[J]. Rom J Ophthalmol, 2022, 66(3): 265-270. DOI: 10.22336/rjo.2022.49.
25.	DeNiro M, Al-Mohanna FA. Erythropoietin and anemia: biological markers that cannot be ignored in diabetic retinopathy[J]. Med Hypotheses, 2012, 78(4): 555-556. DOI: 10.1016/j.mehy.2012.01.026.
26.	Baget-Bernaldiz M, Romero-Aroca P, Mira-Puerto A, et al. Risk factors for recurrent vitreous hemorrhage in type 2 diabetes mellitus patients after posterior vitrectomy[J/OL]. J Clin Med, 2023, 12(8): 2989[2023-04-20]. https://pubmed.ncbi.nlm.nih.gov/37109325/. DOI: 10.3390/jcm12082989.

1. Teo ZL, Tham YC, Yu M, et al. Global prevalence of diabetic retinopathy and projection of burden through 2045: systematic review and meta-analysis[J]. Ophthalmology, 2021, 128(11): 1580-1591. DOI: 10.1016/j.ophtha.2021.04.027.
2. 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.
3. Romero-Aroca P, Baget-Bernaldiz M, Pareja-Rios A, et al. Diabetic macular edema pathophysiology: vasogenic versus inflammatory[J/OL]. J Diabetes Res, 2016, 2016: 2156273[2016-09-28]. https://pubmed.ncbi.nlm.nih.gov/27761468/. DOI: 10.1155/2016/2156273.
4. Thomas M, Tsalamandris C, MacIsaac R, et al. Anaemia in diabetes: an emerging complication of microvascular disease[J]. Curr Diabetes Rev, 2005, 1(1): 107-126. DOI: 10.2174/1573399052952587.
5. Bonakdaran S, Gharebaghi M, Vahedian M. Prevalence of anemia in type 2 diabetes and role of renal involvement[J]. Saudi J Kidney Dis Transpl, 2011, 22(2): 286-290.
6. Keane WF, Zhang Z, Lyle PA, et al. Risk scores for predicting outcomes in patients with type 2 diabetes and nephropathy: the RENAAL study[J]. Clin J Am Soc Nephrol, 2006, 1(4): 761-767. DOI: 10.2215/CJN.01381005.
7. 冯帅, 王天龙. 围手术期贫血与患者血液管理新进展[J]. 国际麻醉学与复苏杂志, 2022, 43(5): 514-517. DOI: 10.3760/cma.j.cn321761-20210413-00549.Feng S, Wang TL. Research advances on perioperative anemia and patients' blood supply management[J]. Int J Anesth Resus, 2022, 43(5): 514-517. DOI: 10.3760/cma.j.cn321761-20210413-00549.
8. Musallam KM, Tamim HM, Richards T, et al. Preoperative anaemia and postoperative outcomes in non-cardiac surgery: a retrospective cohort study[J]. Lancet, 2011, 378(9800): 1396-1407. DOI: 10.1016/S0140-6736(11)61381-0.
9. Lee MK, Han KD, Lee JH, 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.
10. 李雪景, 王坤, 姚一民, 等. 慢性肾衰竭患者增生型糖尿病视网膜病变玻璃体切割手术疗效观察及预后影响因素分析[J]. 中华眼底病杂志, 2023, 39(2): 145-152. DOI: 10.3760/cma.j.cn511434-20221030-00564.Li XJ, Wang K, Yao YM, et al. Therapeutic effect and prognostic factors of vitrectomy for proliferative diabetic retinopathy in patients with chronic renal failure[J]. Chin J Ocul Fundus Dis, 2023, 39(2): 145-152. DOI: 10.3760/cma.j.cn511434-20221030-00564.
11. 中华医学会眼科学分会眼底病学组, 中国医师协会眼科医师分会眼底病学组. 我国糖尿病视网膜病变临床诊疗指南(2022年)——基于循证医学修订[J]. 中华眼底病杂志, 2023, 39(2): 91-94. DOI: 10.3760/cma.j.cn511434-20230208-00055.Fundus Disease Group of Ophthalmological Society of Chinese Medical Association, Fundus Disease Group of Ophthalmologist Branch of Chinese Medical Doctor Association. Guidelines for clinical diagnosis and treatment of diabetic retinopathy in China (2022)[J]. Chin J Ocul Fundus Dis, 2023, 39(2): 91-94. DOI: 10.3760/cma.j.cn511434-20230208-00055.
12. Yuzurihara D, Iijima H. Visual outcome in central retinal and branch retinal artery occlusion[J]. Jpn J Ophthalmol, 2004, 48(5): 490-492. DOI: 10.1007/s10384-004-0102-y.
13. 吴东, 陈嘉林. 贫血(一)[J]. 中华全科医师杂志, 2012, 11(5): 332-333. DOI: 10.3760/cma.j.issn.1671-7368.2012.05.007.Wu D, Chen JL. Anemia(1)[J]. Chin J Gen Pract, 2012, 11(5): 332-333. DOI: 10.3760/cma.j.issn.1671-7368.2012.05.007.
14. 传丰宁, 高幼垣, 田文青, 等. 糖尿病伴发贫血的原因分析[J]. 中华糖尿病杂志, 2016, 8(3): 181-183. DOI: 10.3760/cma.j.issn.1674-5809.2016.03.013.Chuan FN, Gao YY, Tian WQ, et al. Analysis of causes of anemia associated with diabetes mellitus[J]. Chin J Diabetes Mellitus, 2016, 8(3): 181-183. DOI: 10.3760/cma.j.issn.1674-5809.2016.03.013.
15. 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, 2016: 3674946[2016-04-20]. https://pubmed.ncbi.nlm.nih.gov/27200379/. DOI: 10.1155/2016/3674946.
16. Li Y, Yu Y, VanderBeek BL. Anaemia and the risk of progression from non-proliferative diabetic retinopathy to vision threatening diabetic retinopathy[J]. Eye (Lond), 2020, 34(5): 934-941. DOI: 10.1038/s41433-019-0617-6. DOI: 10.1038/s41433-019-0617-6.
17. 汤芳丽, 邢丽丽, 汪文俊, 等. 2型糖尿病患者血红蛋白水平与糖尿病视网膜病变的相关性研究[J]. 中华内分泌代谢杂志, 2023, 39(7): 560-564. DOI: 10.3760/cma.j.cn311282-20230221-00080.Tang FL, Xing LL, Wang WJ, et al. Correlation between hemoglobin level and diabetic retinopathy in patients with type 2 diabetes mellitus[J]. China J Endocrinal Metab, 2023, 39(7): 560-564. DOI: 10.3760/cma.j.cn311282-20230221-00080.
18. 王敏, 汲宝兰, 班博, 等. 2型糖尿病患者血红蛋白水平与视网膜病变风险的相关研究[J]. 中华内分泌代谢杂志, 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]. China J Endocrinal Metab, 2019, 35(5): 387-390. DOI: 10.3760/cma.j.issn.1000-6699.2019.02.007.
19. 中华医学会外科学分会, 中华外科杂志编辑委员会. 普通外科围手术期缺铁性贫血管理多学科专家共识[J]. 中华外科杂志, 2020, 58(4): 252-256. DOI: 10.3760/cma.j.cn112139-20200210-00073.Chinese Surgical Society, Editorial Board of Chinese Journal of Surgery. Multidisciplinary expert^,s consensus on the management of perioperative iron deficency anemia in patients accepting general surgery[J]. Chin J Surg, 2020, 58(4): 252-256. DOI: 10.3760/cma.j.cn112139-20200210-00073.
20. Ratnarajan G, Mellington F, Saldanha M, et al. Long-term visual and retinopathy outcomes in a predominately type 2 diabetic patient population undergoing early vitrectomy and endolaser for severe vitreous haemorrhage[J]. Eye (Lond), 2011, 25(6): 704-709. DOI: 10.1038/eye.2011.65.
21. Lin TZ, Kong Y, Shi C, et al. Prognosis value of Chinese Ocular Fundus Diseases Society classification for proliferative diabetic retinopathy on postoperative visual acuity after pars plana vitrectomy in type 2 diabetes[J]. Int J Ophthalmol, 2022, 15(10): 1627-1633. DOI: 10.18240/ijo.2022.10.10.
22. 翟敏, 王春芳. 增殖型糖尿病视网膜病变玻璃体切除术后虹膜新生血管的危险因素分析[J]. 中国医师杂志, 2017, 19(6): 901-902. DOI: 10.3760/cma.j.issn.1008-1372.2017.06.028.Zhai M, Wang CF. Iris neovascularization after vitrectomy for proliferative diabetic retinopathy Risk factor analysis[J], Journal of Chinese Physician, 2017, 19(6): 901-902. DOI: 10.3760/cma.j.issn.1008-1372.2017.06.028.
23. 祖雪, 代光政, 林铁柱. 增生性糖尿病视网膜病变行玻璃体切割术后发生新生血管性青光眼的风险因素[J]. 国际眼科杂志, 2023, 23(5): 808-812. DOI: 10.3980/j.issn.1672-5123.2023.5.18.Zu X, Dai GZ, Lin TZ. Risk factors associated with neovascular glaucoma after vitrectomy for proliferative diabetic retinopathy[J]. Int Eye Sci, 2023, 23(5): 808-812. DOI: 10.3980/j.issn.1672-5123.2023.5.18.
24. Nišić F, Pidro A, Lepara O, et al. Effect of pan-retinal laser photocoagulation on intravitreal vascular endothelial growth factor concentration in proliferative diabetic retinopathy[J]. Rom J Ophthalmol, 2022, 66(3): 265-270. DOI: 10.22336/rjo.2022.49.
25. DeNiro M, Al-Mohanna FA. Erythropoietin and anemia: biological markers that cannot be ignored in diabetic retinopathy[J]. Med Hypotheses, 2012, 78(4): 555-556. DOI: 10.1016/j.mehy.2012.01.026.
26. Baget-Bernaldiz M, Romero-Aroca P, Mira-Puerto A, et al. Risk factors for recurrent vitreous hemorrhage in type 2 diabetes mellitus patients after posterior vitrectomy[J/OL]. J Clin Med, 2023, 12(8): 2989[2023-04-20]. https://pubmed.ncbi.nlm.nih.gov/37109325/. DOI: 10.3390/jcm12082989.

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Latest ArticlesEffect of mild anemia on prognosis of proliferative diabetic retinopathy after pars plana vitrectomy

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