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.
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.	世界華人檢驗與病理醫師協會. 血脂異常疾病檢驗診斷報告模式專家共識[J]. 中華醫學雜志, 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.	中國成人血脂異常防治指南修訂聯合委員會. 中國成人血脂異常防治指南(2016年修訂版)[J]. 中華心血管病雜志, 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.	中華醫學會內分泌學分會. 中國高尿酸血癥與痛風診療指南(2019)[J]. 中華內分泌代謝雜志, 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.	蔣婧文, 陳長征. 糖尿病黃斑水腫中光相干斷層掃描生物學標志物研究進展[J]. 中華實驗眼科雜志, 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.	中國肥胖問題工作組. 中國成人超重和肥胖癥預防與控制指南(節錄)[J]. 營養學報, 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, 馮姝穎, 華欣. 特發性與糖尿病性黃斑前膜患者手術前后黃斑區微循環的比較[J]. 國際眼科雜志, 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.	馮姝穎. 特發性黃斑前膜與糖尿病性黃斑前膜黃斑區形態和微循環的對比研究[D]. 江蘇: 揚州大學, 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, 孫大衛. 黃斑前膜的形成機制研究[J]. 國際眼科縱覽, 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.	馮姝穎, 解正高. 內界膜的組織病理學研究進展[J]. 中華實驗眼科雜志, 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.	?zata Gündo?du K, Do?an E, ?elik 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.	陳雪, 趙松青, 陸衛平, 等. 尿白蛋白/肌酐比值對2型糖尿病視網膜病變的影響及其截斷值的判定[J]. 中華內分泌代謝雜志, 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. 世界華人檢驗與病理醫師協會. 血脂異常疾病檢驗診斷報告模式專家共識[J]. 中華醫學雜志, 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. 中國成人血脂異常防治指南修訂聯合委員會. 中國成人血脂異常防治指南(2016年修訂版)[J]. 中華心血管病雜志, 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. 中華醫學會內分泌學分會. 中國高尿酸血癥與痛風診療指南(2019)[J]. 中華內分泌代謝雜志, 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. 蔣婧文, 陳長征. 糖尿病黃斑水腫中光相干斷層掃描生物學標志物研究進展[J]. 中華實驗眼科雜志, 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. 中國肥胖問題工作組. 中國成人超重和肥胖癥預防與控制指南(節錄)[J]. 營養學報, 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, 馮姝穎, 華欣. 特發性與糖尿病性黃斑前膜患者手術前后黃斑區微循環的比較[J]. 國際眼科雜志, 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. 馮姝穎. 特發性黃斑前膜與糖尿病性黃斑前膜黃斑區形態和微循環的對比研究[D]. 江蘇: 揚州大學, 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, 孫大衛. 黃斑前膜的形成機制研究[J]. 國際眼科縱覽, 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. 馮姝穎, 解正高. 內界膜的組織病理學研究進展[J]. 中華實驗眼科雜志, 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. ?zata Gündo?du K, Do?an E, ?elik 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. 陳雪, 趙松青, 陸衛平, 等. 尿白蛋白/肌酐比值對2型糖尿病視網膜病變的影響及其截斷值的判定[J]. 中華內分泌代謝雜志, 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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