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Retina

Reduced Retinal Microvascular Density Related to Activity Status and Serum Antibodies in Patients with Graves’ Ophthalmopathy

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Pages 576-584 | Received 16 May 2019, Accepted 23 Sep 2019, Published online: 09 Oct 2019

References

  • Brain R. Pathogenesis and treatment of endocrine exophthalmos. Lancet. 1959;1(7064):109–15. doi:10.1016/s0140-6736(59)90001-7.
  • Gorman CA. Temporal relationship between onset of Graves’ ophthalmopathy and diagnosis of thyrotoxicosis. Mayo Clin Proc. 1983;58(8):515–19.
  • Lim SL, Lim AK, Mumtaz M, Hussein E, Wan Bebakar WM, Khir AS. Prevalence, risk factors, and clinical features of thyroid-associated ophthalmopathy in multiethnic Malaysian patients with Graves’ disease. Thyroid. 2008;18(12):1297–301. doi:10.1089/thy.2008.0044.
  • Mourits MP, Prummel MF, Wiersinga WM, Koornneef L. Clinical activity score as a guide in the management of patients with Graves’ ophthalmopathy. Clin Endocrinol (Oxf). 1997;47(1):9–14. doi:10.1046/j.1365-2265.1997.2331047.x.
  • Danesh-Meyer HV, Carroll SC, Foroozan R, Savino PJ, Fan J, Jiang Y, Vander Hoorn S. Relationship between retinal nerve fiber layer and visual field sensitivity as measured by optical coherence tomography in chiasmal compression. Invest Ophthalmol Vis Sci. 2006;47(11):4827–35. doi:10.1167/iovs.06-0327.
  • Bartalena L, Pinchera A, Marcocci C. Management of Graves’ ophthalmopathy: reality and perspectives. Endocr Rev. 2000;21(2):168–99. doi:10.1210/edrv.21.2.0393.
  • Verity DH, Rose GE. Acute thyroid eye disease (TED): principles of medical and surgical management. Eye (Lond). 2013;27(3):308–19. doi:10.1038/eye.2012.284.
  • Bartley GB. The epidemiologic characteristics and clinical course of ophthalmopathy associated with autoimmune thyroid disease in Olmsted County, Minnesota. Trans Am Ophthalmol Soc. 1994;92:477–588.
  • Neigel JM, Rootman J, Belkin RI, Nugent RA, Drance SM, Beattie CW, Spinelli JA. Dysthyroid optic neuropathy. The crowded orbital apex syndrome. Ophthalmology. 1988;95(11):1515–21. doi:10.1016/s0161-6420(88)32978-7.
  • Yanik B, Conkbayir I, Acaroglu G, Hekimoglu B. Graves’ ophthalmopathy: comparison of the Doppler sonography parameters with the clinical activity score. J Clin Ultrasound. 2005;33(8):375–80. doi:10.1002/jcu.20154.
  • Alp MN, Ozgen A, Can I, Cakar P, Gunalp I. Colour Doppler imaging of the orbital vasculature in Graves’ disease with computed tomographic correlation. Br J Ophthalmol. 2000;84(9):1027–30. doi:10.1136/bjo.84.9.1027.
  • Pérez-López M, Sales-Sanz M, Rebolleda G, Casas-Llera P, González-Gordaliza C, Jarrín E, Muñoz-Negrete FJ. Retrobulbar ocular blood flow changes after orbital decompression in Graves’ ophthalmopathy measured by color Doppler imaging. Invest Ophthalmol Vis Sci. 2011;52(8):5612–17. doi:10.1167/iovs.10-6907.
  • Alford EL, Soparkar CNS. Management of the ‘tight orbit’ and associated visual loss. Curr Opin Otolaryngol Head Neck Surg. 2013;21(4):417–22. doi:10.1097/MOO.0b013e32836312a1.
  • Jorge R, Scott IU, Akaishi PM, Velasco Cruz AA, Flynn HW Jr. Resolution of choroidal folds and improvement in visual acuity after orbital decompression for graves orbitopathy. Retina. 2003;23(4):563–65. doi:10.1097/00006982-200308000-00025.
  • Konuk O, Onaran Z, Ozhan Oktar S, Yucel C, Unal M. Intraocular pressure and superior ophthalmic vein blood flow velocity in Graves’ orbitopathy: relation with the clinical features. Graefes Arch Clin Exp Ophthalmol. 2009;247(11):1555–59. doi:10.1007/s00417-009-1144-0.
  • Kawagishi T, Nishizawa Y, Emoto M, Konishi T, Maekawa K, Hagiwara S, Okuno Y, Inada H, Isshiki G, Morii H. Impaired retinal artery blood flow in IDDM patients before clinical manifestations of diabetic retinopathy. Diabetes Care. 1995;18(12):1544–49. doi:10.2337/diacare.18.12.1544.
  • Lieb WE, Cohen SM, Merton DA, Shields JA, Mitchell DG, Goldberg BB. Color Doppler imaging of the eye and orbit. Technique and normal vascular anatomy. Arch Ophthalmol. 1991;109(4):527–31. doi:10.1001/archopht.1991.01080040095036.
  • Dong J, Jia YD, Wu Q, Zhang S, Jia Y, Huang D, Wang X. Interchangeability and reliability of macular perfusion parameter measurements using optical coherence tomography angiography. Br J Ophthalmol. 2017;101(11):1542–49. doi:10.1136/bjophthalmol-2016-309441.
  • Ye L, Zhou SS, Yang WL, Bao J, Jiang N, Min YL, Yuan Q, Tan G, Shen M, Shao Y. Retinal microvasculature alteration in active thyroid-associated ophthalmopathy. Endocr Pract. 2018;24(7):658–67. doi:10.4158/EP-2017-0229.
  • Vestergaard P. Smoking and thyroid disorders–a meta-analysis. Eur J Endocrinol. 2002;146(2):153–61. doi:10.1530/eje.0.1460153.
  • Eckstein AK, Plicht M, Lax H, Neuhã¤User M, Mann K, Lederbogen S, Heckmann C, Esser J, Morgenthaler NG. Thyrotropin receptor autoantibodies are independent risk factors for Graves’ ophthalmopathy and help to predict severity and outcome of the disease. J Clin Endocrinol Metab. 2006;91(9):3464–70. doi:10.1210/jc.2005-2813.
  • Bartalena L, Marcocci C, Bogazzi F, Panicucci M, Lepri A, Pinchera A. Use of corticosteroids to prevent progression of Graves’ ophthalmopathy after radioiodine therapy for hyperthyroidism. N Engl J Med. 1989;321(20):1349–52. doi:10.1056/NEJM198911163212001.
  • Bartley GB. Evolution of classification systems for Graves’ ophthalmopathy. Ophthalmic Plast Reconstr Surg. 1995;11(4):229–37. doi:10.1097/00002341-199512000-00001.
  • Kwapong WR, Ye H, Peng C, Zhuang X, Wang J, Shen M, Lu F. Retinal microvascular impairment in the early stages of Parkinson’s disease. Invest Ophthalmol Vis Sci. 2018;59(10):4115–22. doi:10.1167/iovs.17-23230.
  • Van SL, Hooijkaas H, Paridaens D, Wa VDB, Kuijpers RW, Drexhage HA, van Hagen PM, Dik WA. PDGF enhances orbital fibroblast responses to TSHR stimulating autoantibodies in Graves’ ophthalmopathy patients. J Clin Endocrinol Metab. 2012;97(6):E944. doi:10.1210/jc.2012-1020.
  • Blum Meirovitch S, Leibovitch I, Kesler A, Varssano D, Rosenblatt A, Neudorfer M. Retina and nerve fiber layer thickness in eyes with thyroid-associated ophthalmopathy. Isr Med Assoc J. 2017;19:277–81.
  • Dosso A, Safran AB, Sunaric G, Burger A. Anterior ischemic optic neuropathy in Graves’ disease. J Neuroophthalmol. 1994;14:170–74.
  • Kurioka Y, Inaba M, Kawagishi T, Emoto M, Kumeda Y, Inoue Y, Morii H, Nishizawa Y. Increased retinal blood flow in patients with Graves’ disease: influence of thyroid function and ophthalmopathy. Eur J Endocrinol. 2001;144(2):99–107. doi:10.1530/eje.0.1440099.
  • Nakase Y, Osanai T, Yoshikawa K, Inoue Y. Color Doppler imaging of orbital venous flow in dysthyroid optic neuropathy. Jpn J Ophthalmol. 1994;38:80–86.
  • Nielsen CH, Brix TH, Leslie RG, Hegedüs L. A role for autoantibodies in enhancement of pro-inflammatory cytokine responses to a self-antigen, thyroid peroxidase. Clin Immunol. 2009;133(2):218–27. doi:10.1016/j.clim.2009.07.014.
  • Chu CH, Lee JK, Keng HM, Chuang MJ, Lu CC, Wang MC, Sun CC, Wei MC, Lam HC. Hyperthyroidism is associated with higher plasma endothelin-1 concentrations. Exp Biol Med. 2006;231:1040–43.
  • Sayın O, Yeter V, Arıtürk N. Optic disc, macula, and retinal nerve fiber layer measurements obtained by OCT in thyroid-associated ophthalmopathy. J Ophthalmol. 2016 2016,(2016-7-17);2016(8):1–7. doi:10.1155/2016/9452687.
  • Alimgil ML, Benian O, Esgin H, Erda S. Ocular pulse amplitude in patients with Graves’ disease: a preliminary study. Acta Ophthalmol Scand. 2009;77(6):694–96. doi:10.1034/j.1600-0420.1999.770618.x.
  • Chang R, Chu Z, Burkemper B, Lee GC, Fard A, Durbin MK, Reznik A, Xu BY, Kashani A, Varma R, et al. Effect of scan size on glaucoma diagnostic performance using OCT angiography en face images of the radial peripapillary capillaries. J Glaucoma. 2019;28(5):465–472. doi:10.1097/IJG.0000000000001216.
  • Manalastas PIC, Zangwill LM, Saunders LJ, Mansouri K, Belghith A, Suh MH, Yarmohammadi A, Penteado RC, Akagi T, Shoji T, et al. Reproducibility of optical coherence tomography angiography macular and optic nerve head vascular density in glaucoma and healthy eyes. J Glaucoma. 2017;26(10):851–59. doi:10.1097/IJG.0000000000000768.
  • Lei J, Durbin MK, Shi Y, Uji A, Balasubramanian S, Baghdasaryan E, Al-Sheikh M, Sadda SR. Repeatability and reproducibility of superficial macular retinal vessel density measurements using optical coherence tomography angiography en face images. JAMA Ophthalmol. 2017;135(10):1092–98. doi:10.1001/jamaophthalmol.2017.3431.
  • Wei Y, Jiang H, Shi Y, Qu D, Gregori G, Zheng F, Rundek T, Wang J. Age-related alterations in the retinal microvasculature, microcirculation, and microstructure. Invest Ophthalmol Vis Sci. 2017;58(9):3804–17. doi:10.1167/iovs.17-21460.
  • Yang Y, Wang J, Jiang H, Yang X, Feng L, Hu L, Wang L, Lu F, Shen M. Retinal microvasculature alteration in high myopia. Invest Ophthalmol Vis Sci. 2016;57(14):6020–30. doi:10.1167/iovs.16-19542.
  • Jiang H, Wei Y, Shi Y, Wright CB, Sun X, Gregori G, Zheng F, Vanner EA, Lam BL. Rundek T and others. Altered macular microvasculature in mild cognitive impairment and Alzheimer disease. J Neuroophthalmol. 2018;38(3):292–98. doi:10.1097/WNO.0000000000000580.
  • Zhang T, Xiao W, Ye H, Chen R, Mao Y, Peripapillary YH. Macular vessel density in dysthyroid optic neuropathy: an optical coherence tomography angiography study. Invest Ophthalmol Vis Sci. 2019;60(6):1863–69. doi:10.1167/iovs.18-25941.
  • Browning DJ, Glassman AR, Aiello LP, Beck RW, Brown DM, Fong DS, Bressler NM, Danis RP, Kinyoun JL. Nguyen QD and others. Relationship between optical coherence tomography-measured central retinal thickness and visual acuity in diabetic macular edema. Ophthalmology. 2007;114(3):525–36. doi:10.1016/j.ophtha.2006.06.052.
  • Falsini B, Riva CE, Logean E. Flicker-evoked changes in human optic nerve blood flow: relationship with retinal neural activity. Invest Ophthalmol Vis Sci. 2002;43(7):2309–16.
  • Tani T, Nagaoka T, Nakabayashi S, Yoshioka T, Yoshida A. Autoregulation of retinal blood flow in response to decreased ocular perfusion pressure in cats: comparison of the effects of increased intraocular pressure and systemic hypotension. Invest Ophthalmol Vis Sci. 2014;55(1):360–67. doi:10.1167/iovs.13-12591.
  • Novaes P, Grisolia ABD, Smith TJ. Update on thyroid-associated Ophthalmopathy with a special emphasis on the ocular surface. Clin Diabetes Endocrinol. 2016;2(1):19. doi:10.1186/s40842-016-0037-5.
  • Feucht N, Maier M, Lepennetier G, Pettenkofer M, Wetzlmair C, Daltrozzo T, Scherm P, Zimmer C, Hoshi MM, Hemmer B. Optical coherence tomography angiography indicates associations of the retinal vascular network and disease activity in multiple sclerosis. Mult Scler. 2019;25(2):224–34.
  • Delaey C. Van De Voorde J. Regulatory mechanisms in the retinal and choroidal circulation. Ophthalmic Res. 2000;32(6):249–56. doi:10.1159/000055622.
  • Paolo P, Claudio C, Ciro C, Carlo I, Sergio DA, Adolfo S. Increased retinal blood flow in patients with active Graves’ ophthalmopathy. Curr Eye Res. 2007;32(11):985–90. doi:10.1080/02713680701689773.
  • Morikawa Y, Morikawa A, Makino I. Relationship of thyroid states and serum thrombomodulin (TM) levels in patients with Graves’ disease: TM, a possible new marker of the peripheral activity of thyroid hormones. J Clin Endocrinol Metab. 1993;76(3):609–14.
  • Takano S, Kimura S, Ohdama S, Aoki N. Plasma thrombomodulin in health and diseases. Blood. 1990;76:2024.
  • Yang QC, Sun X, Wang YM, Wu Q, Feng J, Chen BY. Systematic and endothelial inflammation and endothelial progenitor cell levels in emphysematous rats exposed to intermittent hypoxia. Respir Care. 2015;60(2):279–89. doi:10.4187/respcare.03492.

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