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Retina

Interleukin-6 and Diabetic Retinopathy: A Systematic Review and Meta-Analysis

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Pages 564-574 | Received 27 Jul 2018, Accepted 04 Jan 2019, Published online: 04 Feb 2019

References

  • Abdulsalam S, Ibrahim A, Saidu H, Muazu M, Aliyu UT, Umar HI, Gezawa ID, Owolabi LF. Knowledge, attitude, and practice of diabetic retinopathy among physicians in Northwestern Nigeria. Niger J Clin Pract. 2018;21(4):478–83. doi:10.4103/njcp.njcp_266_17.
  • Li YY, Yang XF, Gu H, Senllingen T, Liu XP, Liu NP. The relationship between insulin resistance/β-cell dysfunction and diabetic retinopathy in Chinese patients with type 2 diabetes mellitus: the Desheng Diabetic Eye Study. Int J Ophthalmol. 2018;11(3):493–500. doi:10.18240/ijo.2018.03.21.
  • Karam T, Kamath YS, Rao LG, Rao KA, Shenoy SB, Bhandary SV. Diabetic retinopathy in patients with diabetic foot syndrome in South India. Indian J Ophthalmol. 2018;66(4):547–50. doi:10.4103/ijo.IJO_1000_17.
  • Tsai T, Kuehn S, Tsiampalis N, Vu MK, Kakkassery V, Stute G, Dick HB, Joachim SC. Anti-inflammatory cytokine and angiogenic factors levels in vitreous samples of diabetic retinopathy patients. PLoS One. 2018;13(3):e0194603. doi:10.1371/journal.pone.0194603.
  • Dumitrescu AG, Istrate SL, Labcu RC, Guta OM, Ciuluvica R, Voinea L. Retinal changes in diabetic patients without diabetic retinopathy. Rom J Ophthalmol. 2017;61:249–55.
  • Makwana T, Takkar B, Venkatesh P, Sharma JB, Gupta Y, Chawla R, Vohra R, Kriplani A, Tandon N. Prevalence, progression, and outcomes of diabetic retinopathy during pregnancy in Indian scenario. Indian J Ophthalmol. 2018;66(4):541–46. doi:10.4103/ijo.IJO_1062_17.
  • Sturrock BA, Rees G, Lamoureux EL, Wong TY, Holloway E, Fenwich EK. Individuals’ perspectives on coping with vision loss from diabetic retinopathy. Optom Vis Sci. 2018;95(4):362–72. doi:10.1097/OPX.0000000000001209.
  • Zhang W, Chen S, Liu ML. Pathogenic roles of microvesicles in diabetic retinopathy. Acta Pharmacol Sin. 2018 Jan;39(1):1–11. doi:10.1038/aps.2017.77.
  • Liu L, Zuo Z, Lu S, Liu A, Liu X. Naringin attenuates diabetic retinopathy by inhibiting inflammation, oxidative stress and NF-κB activation in vivo and in vitro. Iran J Basic Med Sci. 2017;20(7):813–21. doi:10.22038/IJBMS.2017.9017.
  • Rubsam A, Parikh S, Fort PE. Role of inflammation in diabetic retinopathy. Int J Mol Sci. 2018;19(4):e 924. doi:10.3390/ijms19040942.
  • Krick TW, Bressler NM. Recent clinically relevant highlights from the diabetic retinopathy clinical research network. Curr Opin Ophthalmol. 2018;29(3):199–205. doi:10.1097/ICU.0000000000000472.
  • Chandra S, Sheth J, Anantharaman G, Gopalakrishnan M. Ranibizumab-induced retinal reperfusion and regression of neovascularization in diabetic retinopathy: an angiographic illustration. Am J Ophthalmol Case Rep. 2018;9:41–44. doi:10.1016/j.ajoc.2018.01.006.
  • Arutyunov GP, Dragunov DO, Sokolova AV, Mitrokhin VM, Kamkin AG, Latyshev TV. Factors associated with levels of interleukins −18, −8, and −6 in hypertensive patients at high and very high cardiovascular risk. Kardiologiia. 2017;57:69–75.
  • Yu Y, Zhang J, Zhu R, Zhao R, Chen J, Jin J, Tian Y, Su SB. The profile of angiogenic factors in vitreous humor of the patients with proliferative diabetic retinopathy. Curr Mol Med. 2017;17(4):280–86. doi:10.2174/1566524017666171106111440.
  • Noma H, Mimura T, Yasuda K, Motohashi R, Kotake O, Shimura M. Aqueous humor levels of soluble vascular endothelial growth factor receptor and inflammatory factors in diabetic macular edema. Ophthalmologica. 2017;238(1–2):81–88. doi:10.1159/000475603.
  • Yoshimura T, Sonoda KH, Sugahara M, Mochizuki Y, Enaida H, Oshima Y, Ueno A, Hata Y, Yoshida H, Ishibashi T. Comprehensive analysis of inflammatory immune mediators in vitreoretinal diseases. PLoS One. 2009;4(12):e8158. doi:10.1371/journal.pone.0008158.
  • Mocan MC, Kadayifcilar S, Eldem B. Elevated intravitreal interleukin-6 levels in patients with proliferative diabetic retinopathy. Can J Ophthalmol. 2006;41(6):747–52. doi:10.3129/i06-070.
  • Chen H, Wen F, Zhang XZ, Su SB. Expression of T-helper-associated cytokines in patients with type 2 diabetes mellitus with retinopathy. Mol Vis. 2012;18:219–26.
  • Lee JH, Lee W, Kwon OH, Kim JH, Kwon OW, Kim KH, Lim JB. Cytokine profile of peripheral blood in type 2 diabetes mellitus patients with diabetic retinopathy. Ann Clin Lab Sci. 2008;38:361–67.
  • Joanna AM, JoIanta OM. Assessment of selected adhesion molecule and proinflammatory cytokine levels in the vitreous body of patients with type 2 diabetes — role of the inflammatory–immune process in the pathogenesis of proliferative diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol. 2008 Dec;246(12):1665–70. doi:10.1007/s00417-008-0868-6.
  • Afzal N, Zaman S, Shahzad F, Javaid K, Zafar A, Nagi AH. Immune mechanisms in type-2 diabetic retinopathy. J Pak Med Assoc. 2015;65:159–63.
  • Boss JD, Signgh PK, Pandya HK, Tosi J, Kim C, Tewari A, Juzych MS, Abrams GW, Kumar A. Assessment of neurotrophins and inflammatory mediators in vitreous of patients with diabetic retinopathy. Invest Ophthalmol Vis Sci. 2017;58(12):5594–603. doi:10.1167/iovs.17-21973.
  • Canataroglu H, Varinli I, Ozacn AA, Canataroglu A, Doran F, Varinli S. Interleukin (IL)-6, Interleukin (IL)-8 levels and cellular composition of the vitreous humor in proliferative diabetic retinopathy, proliferative vitreoretinopathy, and traumatic proliferative vitreoretinopathy. Ocul Immunol Inflamm. 2005;13:375–81.
  • Chen H, Wen F, Zhang X, Su SB. Expression of T-helper-associated cytokines in patients with type 2 diabetes mellitus with retinopathy. Mol Vis. 2012;18:219–26.
  • Chen H, Zhang X, Liao N, Wen F. Assessment of biomarkers using multiplex assays in aqueous humor of patients with diabetic retinopathy. BCM Opthalmol. 2017;17(1):176–85. doi:10.1186/s12886-017-0572-6.
  • Chernykh VV, Varvarinsky EV, Smirnov EV, Chernykh DV, Trunov AN. Proliferative and inflammatory factors in the vitreous of patients with proliferative diabetic retinopathy. Indian J Ophthalmol. 2015;63(1):33–36. doi:10.4103/0301-4738.151464.
  • Gustavsson C, Agardh CD, Agardh E. Profile of intraocular tumour necrosis factor-a and interleukin-6 in diabetic subjects with different degrees of diabetic retinopathy. Ata Ophthalmol. 2013;91:445–52. doi:10.1111/j.1755-3768.2012.02430.x.
  • Kawashima M, Shoji J, Masami Nakajima M, Kamura Y, Sato Y. Soluble IL-6 receptor in vitreous fluid of patients with proliferative diabetic retinopathy. Jpn J Ophthalmpl. 2007;51(2):100–04. doi:10.1007/s10384-006-0411-4.
  • Koleva-Georgieva DN, Sivkova NP, Terzieva D. Serum inflammatory cytokings IL-1β, IL-6, TNF-a and VEGF have influence on the development of diabetic retinopathy. Folia Med. 2011;53:44–50.
  • Koskela UE, Kuusisto SM, Nissinen AE, Savolainen AE, Liinamaa MJ. High Vitreous Concentration of IL-6 and IL-8, but not of adhesion molecules in relation to plasma concentrations in proliferative diabeticretinopathy. Ophthalmic Res. 2013;49(2):108–14. doi:10.1159/000342977.
  • Loukovaara S, Piippo N, Kinnunen K, Hytti M, Kaarniranta K, Kauppinen A. NLRP3 inflammasome activation is associated with proliferative diabetic retinopathy. Acta Ophthalmol. 2017 Dec;95(8):803–08. doi:10.1111/aos.13427.
  • Hernandez-Da Mota SE, Soto-Bahena JJ, Viveros-Sandoval ME. Cardiel-Rios. Pro-inflammatory serum cytokines in diabetic retinopathy. Cir Cir. 2015;83(2):100–06. doi:10.1016/j.circir.2015.04.003.
  • Mysliwiec M, Balcerska A, Zorena K, Mysliwska J, Lipowski P, Raczynska K. The role of vasclular endothelial factor alpha and interleukin-6 in pathogenesis of diabetic retinopathy. Diabetes Res Clin Pract. 2008;79(1):141–46. doi:10.1016/j.diabres.2007.07.011.
  • Nakamura N, Hasegawa G, Obayashi H, Yamazaki M, Ogata M, Nakano K, Yoshikawa T, Watanabe A, Kinoshita S, Fujianami A. Increased concentration of pentosidine, an advanced glycation end product, and interleukin-6 in the vitreous of patients with proliferative diabetic retinopathy. Diabetes Res Clin Pract. 2003;61:93–101.
  • Oh IK, Kim SW, Oh J, Lee TS, Hua H. Inflammatory and angiogenic factors in the aqueous humor and the relationship to diabetic retinopathy. Cur Eye Res. 2010;35(12):1116–27. doi:10.3109/02713683.2010.510257.
  • Suzuki Y, Nakazawa M, Suzuki K, Yamazaki H, Miyagawa Y. Expression profiles of cytokines and chemokines in vitreous fluid in diabetic retinopathy and central retinal vein occlusion. Jpn J Ophthalmol. 2011;55(3):256–63. doi:10.1007/s10384-011-0004-8.
  • Tasci E, Ozbek MN, Onenli-Mungan N, Temiz F, Topaloglu AK, Yuksel B. Low serum adiponectin levels in children and adolescents with diabetic retinopathy. Eurasian J Med. 2011;43(1):18–22. doi:10.5152/eajm.2011.04.
  • Yi X, Sun J, Li L, Wei Q, Qian Y, Chen X, Ma L. Research communication 1,25-Dihydroxyvi- tamin D3 deficiency is involved in the pathogenesis of diabetic retinopathy in the uygur population of China. IUBMB Life. 2016;68(6):445–51. doi:10.1002/iub.1501.
  • Yoshida S, Kubo Y, Kobayashi Y, Zhou Y, Nakama T, Yamaguchi M, Tachibana T, Ishikawa K, Arita R, Nakao S, et al. Increased vitreous concentrations of MCP-1 and IL-6 after vitrectomy in patients with proliferative diabetic retinopathy: possible association with postoperative macular oedema. Br J Ophthalmol. 2015;99(7):960–66. doi:10.1136/bjophthalmol-2014-306366.
  • Yuuki T, Kanda T, Kimura Y, Kootajima N, Tamura J, Kobayashi I, Kishi S. Inflammatory cytokines in vitreous fluid and serum of patients with diabetic vitreoretinopathy. J Diabetes Complications. 2001;15:257–59.
  • Tsai T, Kuehn S, Tsiampalis N, Vu MK, Kakkassery V, Stute G, Dick HB, Joachim SC. etAnti-inflammatory cytokine and angiogenic factors levels in vitreous samples of diabetic retinopathy patients. PLoS One. 2018;27(3):e0194603. doi:10.1371/journal.pone.0194603.
  • Funatsu H, Yamashita H, Shimizu E, Kojima R, Hori S. Relationship between vascular endothelial growth factor and interleukin-6 in diabetic retinopathy. Retina. 2001;21:469–77.
  • Kaviarasan K, Jithu M, Arif Mull M, Sharma T, Sivasankar S, Das UN, Angayarkanni N. Low blood and vitreal BDNF, LXA4 and altered Th1/Th2 cytokine balance are potential risk factors for diabetic retinopathy. Metabolism. 2015;64(9):958–66. doi:10.1016/j.metabol.2015.04.005.
  • Ma Y, Tao Y, Lu Q, Jiang YR. Intraocular expression of serum amyloid A and Interleukin-6 in proliferative diabetic retinopathy. Am J Ophthalmol. 2011;152(4):678–85. doi:10.1016/j.ajo.2011.03.007.
  • Scboenberher SD, Kim SJ, Sheng J, Rezaei KA, Lalezary M, Cherney E. Increased Prostaglandin E2 (PGE2) Levels in proliferativediabetic retinopathy, and correlation with VEGF and inflammatory cytokines. Invest Ophthalmol Vis Sci. 2012;53(9):5906–11. doi:10.1167/iovs.12-10410.
  • Xu Y, Cheng Q, Yang B, Yu S, Xu F, Lu L, Liang X. Increased sCD200 levels in vitreous of patients with proliferative diabetic retinopathy and its correlation with VEGF and proinflammatory cytokines. Invest Ophthalmol Vis Sci. 2015;56(11):6564–72. doi:10.1167/iovs.15-16854.
  • Zou HL, Wang Y, Gang Q, Zhang Y, Sun Y. Plasma level of miR-93 is associated with higher risk to develop type 2 diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol. 2017;255(6):1159–66. doi:10.1007/s00417-017-3638-5.
  • Hendrick AM, Gibson MV, Kulshreshtha A. Diabetic Retinopathy. Prim Care. 2015;42(3):451–64. doi:10.1016/j.pop.2015.05.005.
  • Ghaffar T, Marwat ZI, Ullah F, Khan S, Hassan Aamir AU. Association of serum total bilirubin level with diabetic retinopathy in type 2 diabetes mellitus. J Ayub Med Coll. 2016;28:537–41.
  • Barliya T, Dardik R, Nisqav Y, Dachbash M, Gaton D, Kenet G, Ehrlich R, Weinberger D, Libnat T. Possible involvement of NETosis in inflammatory processes in the eye: evidence from a small cohort of patients. Mol Vis. 2017;23:922–32.
  • Miller K, Fortun JA. Diabetic macular edema: current understanding, pharmacologic treatment options, and developing therapies. Asia Pac J Ophthalmol (Phila). 2018;7(1):28–35. doi:10.22608/APO.2017529.
  • Qiu AW, Bian Z, Mao PA, Liu QH. IL-17A exacerbates diabetic retinopathy by impairing Müller cell function via Act1 signaling. Exp Mol Med. 2016;16;48:e280.
  • Chen H, Zhang X, Liao N, Mi L, Peng Y, Liu B, Zhang S, Wen F. Enhanced expression of NLRP3 inflammasome-related inflammation in diabetic retinopathy. Invest Ophthalmol Vis Sci. 2018;59(2):978–85. doi:10.1167/iovs.17-22816.
  • Zorena K, Mysliwska J, Mysliwiec M, Balcerska A, Hak L, Lipowski P, Raczynska K. Serum TNF-Alpha level predicts nonproliferative diabetic retinopathy in children. Mediators Inflamm. 2007;2007:92196. doi:10.1155/2007/92196.
  • Yuuki T, Kanda T, Kimura Y, Kotajima N, Tamura J, Kobayashi I, Kishi S. Inflammatory cytokines in vitreous fluid and serum of patients with diabetic vitreoretinopathy. J Diabetes Complications. 2001;15:257–59.
  • Nakamura S, Iwasaki N, Funatsu H, Kitano S, Iwamoto Y. Impact of variants in the VEGF gene on progression of proliferative diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol. 2009;247(1):21–26. doi:10.1007/s00417-008-0915-3.
  • Sen A, Paine SK, Chowdhury IH, Mukherjee A, Choudhuri S, Saha A, Mandal LK, Bhattacharya B. Impact of interleukin-6 promoter polymorphis and serum interleukin-6 level on the acute inflammation and neovascularization stages of patients with Eales’ disease. Mol Vis. 2011;17:2552–63.
  • Aguilera E, Serra-Planas E, Granada ML, Pellitero S, Reverter J, Alonso N, Soldevila B, Mauricio D, Puig-Domingo M. Relationship of YKL-40 and adiponectin and subclinical atherosclerosis in asymptomatic patients with type 1 diabetes mellitus from a European Mediterranean population. Cardiovasc Diabetol. 2015;14:121. doi:10.1186/s12933-015-0287-z.
  • Yi X, Sun J, Li L, Wei Q, Qian Y, Chen X, Ma L. 1,25-Dihydroxyvitamin D3 deficiency is involved in the pathogenesis of diabetic retinopathy in the uygur population of China. IUBMB Life. 2016;68(6):445–51. doi:10.1002/iub.1501.

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