Correlation between systemic immune inflammation index and diabetic epiretinal membranes_Chinese Journal of Ocular Fundus Diseases

Authors：

Zhou Daiying ¹ , Chen Jing ¹ , Lu Cuicui ² ,  Lyu Zhigang ¹

1. Department of Ophthalmology, Affiliated Jinhua Hospital of Zhejiang University of Medicine School, Jinhua 321000, China;
2. Department of Ophthalmology, Dongyang Red Cross Hospital, Jinhua 322100, China;

Corresponding author：

Lyu Zhigang, Email: jhyylzg@163.com

Keywords：

Diabetes mellitus; Macular epiretinal membrane; Systemic immune inflammation index

DOI：

10.3760/cma.j.cn511434-20240329-00127

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To investigate the correlation between systemic immune inflammatory index (SII) and other metabolic indicators and diabetic epiretinal membranes (dERM). Methods A retrospective case-control study. From March 2022 to July 2023, 81 patients (81 eyes) with dERM in Department of Ophthalmology, Affiliated Jinhua Hospital of Zhejiang University of Medicine School diagnosed by fundus screening were included in the study. A total of 81 patients (81 eyes) with diabetes who were matched in age, gender, and duration of diabetes and had no dERM or diabetic macular edema in both eyes during fundus screening were selected as the control group. All patients underwent optical coherence tomography (OCT) examination and laboratory tests for peripheral blood neutrophil, lymphocyte, platelet counts, serum albumin, blood lipids, uric acid, and glycosylated hemoglobin (HbA1c). SII was calculated. Random urine samples were collected for urinary albumin/creatinine ratio (ACR) testing. The OCT device's own analysis software obtained the macular volume coefficient, including central foveal thickness (CMT), macular volume, and average macular thickness. The macular volume coefficient, SII, serum albumin, blood lipids, uric acid, HbA1c, and ACR between the two groups were compared using paired t tests or Mann-Whitney U tests. Conditional logistic regression analysis was performed to evaluate the risk factors for dERM; Spearman correlation test was used to analyze the correlation between CMT, SII, ACR, disorganization of retinal inner layers (DRIL), intraretinal cyst (IRC), and hyper-reflective foci (HRF) in patients with dERM. Results There were significant differences in CMT, macular volume, average macular thickness, SII, serum albumin, and ACR between the dERM group and the control group (Z=−7.234, −6.306, −6.400, −3.063, −2.631, −3.868; P＜0.05). Conditional logistics regression analysis showed that high SII [odds ratio (OR)= 3.919, 95% confidence interval (CI) 1.591-9.654, P=0.003] and ACR (OR=4.432, 95%CI 1.885-10.420, P=0.001) were risk factors for dERM. Spearman correlation analysis showed that HRF, IRC, DRIL were positively correlated with CMT (Rs=0.234, 0.330, 0.248; P=0.036, 0.003, 0.026); HRF was positively correlated with SII and ACR (Rs=0.233, 0.278; P=0.036, 0.012). Conclusion Elevated SII and ACR are independent risk factors for the occurrence of dERM.

Citation： Zhou Daiying, Chen Jing, Lu Cuicui, Lyu Zhigang. Correlation between systemic immune inflammation index and diabetic epiretinal membranes. Chinese Journal of Ocular Fundus Diseases, 2024, 40(9): 699-705. doi: 10.3760/cma.j.cn511434-20240329-00127 Copy

1.	Sivalingam A, Eagle RC Jr, Duker JS, et al. Visual prognosis correlated with the presence of internal-limiting membrane in histopathologic specimens obtained from epiretinal membrane surgery[J]. Ophthalmology, 1990, 97(11): 1549-1552. DOI: 10.3389/fendo.2023.1160615.
2.	Romano MR, Ilardi G, Ferrara M, et al. Intraretinal changes in idiopathic versus diabetic epiretinal membranes after macular peeling[J/OL]. PLoS One, 2018, 13(5): e0197065[2018-05-08]. https://pubmed.ncbi.nlm.nih.gov/29738569/. DOI: 10.1371/journal.pone.0197065.
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8.	Bolz M, Schmidt-Erfurth U, Deak G, et al. Optical coherence tomographic hyperreflective foci: a morphologic sign of lipid extravasation in diabetic macular edema[J]. Ophthalmology, 2009, 116(5): 914-920. DOI: 10.1016/j.ophtha.2008.12.039.
9.	蒋婧文, 陈长征. 糖尿病黄斑水肿中光相干断层扫描生物学标志物研究进展[J]. 中华实验眼科杂志, 2021, 39(1): 89-92. DOI: 10.3760/cma.j.cn115989-20190617-00264.Jiang JW, Chen CZ. Research progress in biomarkers of diabetic macular edema on optical coherence tomography[J]. Chin J Exp Ophthalmol, 2021, 39(1): 89-92. DOI: 10.3760/cma.j.cn115989-20190617-00264.
10.	中国肥胖问题工作组. 中国成人超重和肥胖症预防与控制指南(节录)[J]. 营养学报, 2004, 26(1): 1-4. DOI: 10.13325/j.cnki.acta.nutr.sin.2004.01.001.The Working Group on obesity in China. Guidelines for prevention and control of overweight and obesity in Chinese adults[J]. Acta Nutrimenta Sinica, 2004, 26(1): 1-4. DOI: 10.13325/j.cnki.acta.nutr.sin.2004.01.001.
11.	Ng CH, Cheung N, Wang JJ, et al. Prevalence and risk factors for epiretinal membranes in a multi-ethnic United States population[J]. Ophthalmology, 2011, 118(4): 694-699. DOI: 10.1016/j.ophtha.2010.08.009.
12.	Dupas B, Tadayoni R, Gaudric A. Les membranes épirétiniennes maculaires[J]. J Fr Ophtalmol, 2015, 38(9): 861-875. DOI: 10.1016/j.jfo.2015.08.004.
13.	徐敏, 冯姝颖, 华欣. 特发性与糖尿病性黄斑前膜患者手术前后黄斑区微循环的比较[J]. 国际眼科杂志, 2021, 21(11): 1942-1947. DOI: 10.3980/j.issn.1672-5123.2021.11.22.Xu M, Feng SY, Hua X. Comparison of macular microcirculation in eyes with idiopathic and diabetic macular epiretinal membrane before and after surgery[J]. Int Eye Sci, 2021, 21(11): 1942-1947. DOI: 10.3980/j.issn.1672-5123.2021.11.22.
14.	冯姝颖. 特发性黄斑前膜与糖尿病性黄斑前膜黄斑区形态和微循环的对比研究[D]. 江苏: 扬州大学, 2022.Feng SY. Comparative study of morphology and microcirculation of macular area between idiopathic and diabetic macular epiretinal membrane[D]. Jiangsu: Yangzhou Univeristy, 2022.
15.	Vishwakarma S, Gupta RK, Jakati S, et al. Molecular assessment of epiretinal membrane: activated microglia, oxidative stress and inflammation[J]. Antioxidants (Basel), 2020, 9(8): 654. DOI: 10.3390/antiox9080654.
16.	徐佳琪, 孙大卫. 黄斑前膜的形成机制研究[J]. 国际眼科纵览, 2019, 43(2): 118-122. DOI: 10.3760/cma.j.issn.1673-5803.2019.02.009.Xu JQ, Sun DW. Formation mechanism of preretinal macular membrane[J]. Int Rev Ophthalmol, 2019, 43(2): 118-122. DOI: 10.3760/cma.j.issn.1673-5803.2019.02.009.
17.	冯姝颖, 解正高. 内界膜的组织病理学研究进展[J]. 中华实验眼科杂志, 2023, 41(1): 84-87. DOI: 10.3760/cma.j.cn115989-20190620-00270.Feng SY, Xie ZG. Advance in the histopathological research of internal limiting membrane[J]. Chin J Exp Ophthalmol, 2023, 41(1): 84-87. DOI: 10.3760/cma.j.cn115989-20190620-00270.
18.	Zhou J, Song S, Zhang Y, et al. OCT-based biomarkers are associated with systemic inflammation in patients with treatment-naive diabetic macular edema[J]. Ophthalmol Ther, 2022, 11(6): 2153-2167. DOI: 10.1007/s40123-022-00576-x.
19.	Elbeyli A, Kurtul BE, Ozcan SC, et al. The diagnostic value of systemic immune-inflammation index in diabetic macular oedema[J]. Clin Exp Optom, 2022, 105(8): 831-835. DOI: 10.1080/08164622.2021.1994337.
20.	Özata Gündoğdu K, Doğan E, Çelik E, et al. Serum inflammatory marker levels in serous macular detachment secondary to diabetic macular edema[J]. Eur J Ophthalmol, 2022, 32(6): 3637-3643. DOI: 10.1177/11206721221083465.
21.	Arroyo V, García-Martinez R, Salvatella X. Human serum albumin, systemic inflammation, and cirrhosis[J]. J Hepatol, 2014, 61(2): 396-407. DOI: 10.1016/j.jhep.2014.04.012.
22.	Eckart A, Struja T, Kutz A, et al. Relationship of nutritional status, inflammation, and serum albumin levels during acute illness: a prospective study[J]. Am J Med, 2020, 133(6): 713-722. DOI: 10.1016/j.amjmed.2019.10.031.
23.	van Hecke MV, Dekker JM, Nijpels G, et al. Inflammation and endothelial dysfunction are associated with retinopathy: the Hoorn study[J]. Diabetologia, 2005, 48(7): 1300-1306. DOI: 10.1007/s00125-005-1799-y.
24.	陈雪, 赵松青, 陆卫平, 等. 尿白蛋白/肌酐比值对2型糖尿病视网膜病变的影响及其截断值的判定[J]. 中华内分泌代谢杂志, 2022, 38(12): 1046-1051. DOI: 10.3760/cma.j.cn311282-20220524-00333.Chen X, Zhao SQ, Lu WP, et al. Effect of urinary albumin/creatinine ratio on type 2 diabetic retinopathy and its cut-off value for early diabetic retinopathy diagnosis[J]. Chin J Endocrinol Metab, 2022, 38(12): 1046-1051. DOI: 10.3760/cma.j.cn311282-20220524-00333.
25.	Benitez-Aguirre PZ, Marcovecchio ML, Chiesa ST, et al. Urinary albumin/creatinine ratio tertiles predict risk of diabetic retinopathy progression: a natural history study from the Adolescent Cardio-Renal Intervention Trial (AdDIT) observational cohort[J]. Diabetologia, 2022, 65(5): 872-878. DOI: 10.1007/s00125-022-05661-1.
26.	Qin S, Zhang C, Qin H, et al. Hyperreflective foci and subretinal fluid are potential imaging biomarkers to evaluate anti-VEGF effect in diabetic macular edema[J/OL]. Front Physiol, 2021, 12: 791442[2021-12-23]. https://pubmed.ncbi.nlm.nih.gov/35002773/. DOI: 10.3389/fphys.2021.791442.

1. Sivalingam A, Eagle RC Jr, Duker JS, et al. Visual prognosis correlated with the presence of internal-limiting membrane in histopathologic specimens obtained from epiretinal membrane surgery[J]. Ophthalmology, 1990, 97(11): 1549-1552. DOI: 10.3389/fendo.2023.1160615.
2. Romano MR, Ilardi G, Ferrara M, et al. Intraretinal changes in idiopathic versus diabetic epiretinal membranes after macular peeling[J/OL]. PLoS One, 2018, 13(5): e0197065[2018-05-08]. https://pubmed.ncbi.nlm.nih.gov/29738569/. DOI: 10.1371/journal.pone.0197065.
3. Hu B, Yang XR, Xu Y, et al. Systemic immune-inflammation index predicts prognosis of patients after curative resection for hepatocellular carcinoma[J]. Clin Cancer Res, 2014, 20(23): 6212-6222. DOI: 10.1158/1078-0432.CCR-14-0442.
4. 世界华人检验与病理医师协会. 血脂异常疾病检验诊断报告模式专家共识[J]. 中华医学杂志, 2018, 98(22): 1739-1742. DOI: 10.3760/cma.j.issn.0376-2491.2018.22.004.World Association of Chinese Clinical Pathologists and Anatomical Pathologists. Expert consensus on diagnostic report mode for dyslipidemia disease[J]. Natl Med J China, 2018, 98(22): 1739-1742. DOI: 10.3760/cma.j.issn.0376-2491.2018.22.004.
5. 中国成人血脂异常防治指南修订联合委员会. 中国成人血脂异常防治指南(2016年修订版)[J]. 中华心血管病杂志, 2016, 44(10): 833-853. DOI: 10.3760/cma.j.issn.0253-3758.2016.10.005.Joint Committee Issued Chinese Guideline for the Management of Dyslipidemia in Adults. 2016 Chinese guideline for the management of dyslipidemia in adults[J]. Chin J Cardiol, 2016, 44(10): 833-853. DOI: 10.3760/cma.j.issn.0253-3758.2016.10.005.
6. 中华医学会内分泌学分会. 中国高尿酸血症与痛风诊疗指南(2019)[J]. 中华内分泌代谢杂志, 2020, 36(1): 1-13. DOI: 10.3760/cma.j.issn.1000-6699.2020.01.001.Chinese Society of Endocrinology, Chinese Medical Association. Guideline for the diagnosis and management of hyperuricemia and gout in China (2019)[J]. Chin J Endocrinol Metab, 2020, 36(1): 1-13. DOI: 10.3760/cma.j.issn.1000-6699.2020.01.001.
7. Vujosevic S, Bini S, Torresin T, et al. Hyperreflective retinal spots in normal and diabetic eyes: B-scan and en face spectral domain optical coherence tomography evaluation[J]. Retina, 2017, 37(6): 1092-1103. DOI: 10.1097/IAE.0000000000001304.
8. Bolz M, Schmidt-Erfurth U, Deak G, et al. Optical coherence tomographic hyperreflective foci: a morphologic sign of lipid extravasation in diabetic macular edema[J]. Ophthalmology, 2009, 116(5): 914-920. DOI: 10.1016/j.ophtha.2008.12.039.
9. 蒋婧文, 陈长征. 糖尿病黄斑水肿中光相干断层扫描生物学标志物研究进展[J]. 中华实验眼科杂志, 2021, 39(1): 89-92. DOI: 10.3760/cma.j.cn115989-20190617-00264.Jiang JW, Chen CZ. Research progress in biomarkers of diabetic macular edema on optical coherence tomography[J]. Chin J Exp Ophthalmol, 2021, 39(1): 89-92. DOI: 10.3760/cma.j.cn115989-20190617-00264.
10. 中国肥胖问题工作组. 中国成人超重和肥胖症预防与控制指南(节录)[J]. 营养学报, 2004, 26(1): 1-4. DOI: 10.13325/j.cnki.acta.nutr.sin.2004.01.001.The Working Group on obesity in China. Guidelines for prevention and control of overweight and obesity in Chinese adults[J]. Acta Nutrimenta Sinica, 2004, 26(1): 1-4. DOI: 10.13325/j.cnki.acta.nutr.sin.2004.01.001.
11. Ng CH, Cheung N, Wang JJ, et al. Prevalence and risk factors for epiretinal membranes in a multi-ethnic United States population[J]. Ophthalmology, 2011, 118(4): 694-699. DOI: 10.1016/j.ophtha.2010.08.009.
12. Dupas B, Tadayoni R, Gaudric A. Les membranes épirétiniennes maculaires[J]. J Fr Ophtalmol, 2015, 38(9): 861-875. DOI: 10.1016/j.jfo.2015.08.004.
13. 徐敏, 冯姝颖, 华欣. 特发性与糖尿病性黄斑前膜患者手术前后黄斑区微循环的比较[J]. 国际眼科杂志, 2021, 21(11): 1942-1947. DOI: 10.3980/j.issn.1672-5123.2021.11.22.Xu M, Feng SY, Hua X. Comparison of macular microcirculation in eyes with idiopathic and diabetic macular epiretinal membrane before and after surgery[J]. Int Eye Sci, 2021, 21(11): 1942-1947. DOI: 10.3980/j.issn.1672-5123.2021.11.22.
14. 冯姝颖. 特发性黄斑前膜与糖尿病性黄斑前膜黄斑区形态和微循环的对比研究[D]. 江苏: 扬州大学, 2022.Feng SY. Comparative study of morphology and microcirculation of macular area between idiopathic and diabetic macular epiretinal membrane[D]. Jiangsu: Yangzhou Univeristy, 2022.
15. Vishwakarma S, Gupta RK, Jakati S, et al. Molecular assessment of epiretinal membrane: activated microglia, oxidative stress and inflammation[J]. Antioxidants (Basel), 2020, 9(8): 654. DOI: 10.3390/antiox9080654.
16. 徐佳琪, 孙大卫. 黄斑前膜的形成机制研究[J]. 国际眼科纵览, 2019, 43(2): 118-122. DOI: 10.3760/cma.j.issn.1673-5803.2019.02.009.Xu JQ, Sun DW. Formation mechanism of preretinal macular membrane[J]. Int Rev Ophthalmol, 2019, 43(2): 118-122. DOI: 10.3760/cma.j.issn.1673-5803.2019.02.009.
17. 冯姝颖, 解正高. 内界膜的组织病理学研究进展[J]. 中华实验眼科杂志, 2023, 41(1): 84-87. DOI: 10.3760/cma.j.cn115989-20190620-00270.Feng SY, Xie ZG. Advance in the histopathological research of internal limiting membrane[J]. Chin J Exp Ophthalmol, 2023, 41(1): 84-87. DOI: 10.3760/cma.j.cn115989-20190620-00270.
18. Zhou J, Song S, Zhang Y, et al. OCT-based biomarkers are associated with systemic inflammation in patients with treatment-naive diabetic macular edema[J]. Ophthalmol Ther, 2022, 11(6): 2153-2167. DOI: 10.1007/s40123-022-00576-x.
19. Elbeyli A, Kurtul BE, Ozcan SC, et al. The diagnostic value of systemic immune-inflammation index in diabetic macular oedema[J]. Clin Exp Optom, 2022, 105(8): 831-835. DOI: 10.1080/08164622.2021.1994337.
20. Özata Gündoğdu K, Doğan E, Çelik E, et al. Serum inflammatory marker levels in serous macular detachment secondary to diabetic macular edema[J]. Eur J Ophthalmol, 2022, 32(6): 3637-3643. DOI: 10.1177/11206721221083465.
21. Arroyo V, García-Martinez R, Salvatella X. Human serum albumin, systemic inflammation, and cirrhosis[J]. J Hepatol, 2014, 61(2): 396-407. DOI: 10.1016/j.jhep.2014.04.012.
22. Eckart A, Struja T, Kutz A, et al. Relationship of nutritional status, inflammation, and serum albumin levels during acute illness: a prospective study[J]. Am J Med, 2020, 133(6): 713-722. DOI: 10.1016/j.amjmed.2019.10.031.
23. van Hecke MV, Dekker JM, Nijpels G, et al. Inflammation and endothelial dysfunction are associated with retinopathy: the Hoorn study[J]. Diabetologia, 2005, 48(7): 1300-1306. DOI: 10.1007/s00125-005-1799-y.
24. 陈雪, 赵松青, 陆卫平, 等. 尿白蛋白/肌酐比值对2型糖尿病视网膜病变的影响及其截断值的判定[J]. 中华内分泌代谢杂志, 2022, 38(12): 1046-1051. DOI: 10.3760/cma.j.cn311282-20220524-00333.Chen X, Zhao SQ, Lu WP, et al. Effect of urinary albumin/creatinine ratio on type 2 diabetic retinopathy and its cut-off value for early diabetic retinopathy diagnosis[J]. Chin J Endocrinol Metab, 2022, 38(12): 1046-1051. DOI: 10.3760/cma.j.cn311282-20220524-00333.
25. Benitez-Aguirre PZ, Marcovecchio ML, Chiesa ST, et al. Urinary albumin/creatinine ratio tertiles predict risk of diabetic retinopathy progression: a natural history study from the Adolescent Cardio-Renal Intervention Trial (AdDIT) observational cohort[J]. Diabetologia, 2022, 65(5): 872-878. DOI: 10.1007/s00125-022-05661-1.
26. Qin S, Zhang C, Qin H, et al. Hyperreflective foci and subretinal fluid are potential imaging biomarkers to evaluate anti-VEGF effect in diabetic macular edema[J/OL]. Front Physiol, 2021, 12: 791442[2021-12-23]. https://pubmed.ncbi.nlm.nih.gov/35002773/. DOI: 10.3389/fphys.2021.791442.

Chinese Journal of Ocular Fundus Diseases

Correlation between systemic immune inflammation index and diabetic epiretinal membranes

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