Abstract
Purpose
To evaluate the retinal vascular plexus and choriocapillaris structures in patients with non-ocular Behçet’s disease (BD) using optical coherence tomography angiography (OCTA).
Methods
The study included 42 eyes of non-ocular BD patients (study group) and 40 eyes of 20 healthy subjects (control group). Flow area (mm2), mean vascular density (VD) (%) and foveal avascular zone (FAZ) (mm2) were measured using OCTA (Optovue Inc., Fremont, CA, USA). Subfoveal choroidal thickness (CT) (μm) and central macular thickness (CMT) (μm) measurements were also performed.
Results
The mean superficial capillary plexus, deep capillary plexus and choriocapillaris flow area values were found to be significantly lower in the study group than in the control group (p < 0.001, p < 0.001, p = 0.008, respectively). In respect of mean VD, a statistically significant difference was determined between the study and control groups in both superficial and deep VD (p < 0.001). No statistically significant difference was found out between the groups in respect of superficial FAZ, deep FAZ and CMT (p = 0.165, p = 0.477, p = 0.457, respectively). The subfoveal CT was also measured to be significantly thicker in the study group than in the control group (p < 0.001).
Conclusion
The results obtained with OCTA revealed that there could be both retinal and choroidal involvement in non-ocular BD patients before the emergence of evident clinical findings.
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References
Ozyazgan Y, Ucar D, Hatemi G, Yazici Y (2015) Ocular involvement of Behçet’s syndrome: a comprehensive review. Clin Rev Allergy Immunol 49(3):298–306
Behçet H (1937) Über rezidivierende aphthöse, durch ein Virus verursachte Geschwüre am Mund, am Auge und an den Genitalien. Dermatol Monatsschr 105:1152–1157
Mishima S, Masuda K, Izawa Y, Mochizuki M, Namba K (1979) The eighth Frederick H. Verhoeff Lecture. presented by saiichi mishima, MD Behcet’s disease in Japan: ophthalmologic aspects. Trans Am Ophthalmol Soc 77:225–279
Yazıcı H, Tüzün Y, Pazarlı H, Yurdakul S, Ozyazgan Y, Ozdoğan H et al (1984) Influence of age of onset and patient’s sex on the prevalence and severity of manifestation of Behçet’s syndrome. Ann Rheum Dis 43(6):783–789
Tugal-Tutkun I, Onal S, Altan-Yaycioglu R, Huseyin Altunbas H, Urgancioğlu M et al (2004) Uveitis in Behçet disease: an analysis of 880 patients. Am J Ophthalmol 138:373–380
Atmaca LS (1989) Fundus changes associated with Behçet’s disease. Graefe’s Arch Clin Exp Ophthalmol 227:340–344
Tugal-Tutkun I (2009) Behçet’s uveitis. Middle East Afr J Ophthalmol 16:219–224
Chalam KV, Sambhav K (2016) Optical coherence tomography angiography in retinal diseases. J Ophthalmic Vis Res 11(1):84–89
de Carlo TE, Romano A, Waheed NK, Duker JS (2015) A review of optical coherence tomography angiography (OCTA). Int J Retina Vitreous 1:5
Takase N, Nozaki M, Kato A, Ozeki H, Yoshida M, Ogura Y et al (2015) Enlargement of foveal avascular zone in diabetic eyes evaluated by en face optical coherence tomography angiography. Retina 35:2377–2383
Khairallah M, Abroug N, Khochtali S, Mahmoud A, Jelliti B, Coscas G et al (2017) Optical coherence tomography angiography in patients with Behçet uveitis. Retina 37:1678–1691
Raafat KA, Allam RSHM, Medhat BM (2018) Optical coherence tomography angiography findings in patients with nonocular Behçet disease. Retina. https://doi.org/10.1097/IAE.0000000000002177
Tunç R, Uluhan A, Melikoğlu M, Ozyazgan Y, Ozdoğan H, Yazici H (2001) A reassessment of the International Study Group criteria for the diagnosis (classification) of Behçet’s syndrome. Clin Exp Rheumatol 19(5 Suppl 24):45–47
Karti O, Zengin MO, Kerci SG, Ayhan Z, Kusbeci T (2018) Acute effect of caffeine on macular microcirculation in healthy subjects: an optical coherence tomography angiography study. Retina. https://doi.org/10.1097/IAE.0000000000002058
Choi W, Mohler KJ, Potsaid B, Lu CD, Liu JJ, Jayaraman V et al (2013) Choriocapillaris and choroidal microvasculature imaging with ultrahigh speed OCT angiography. PLoS ONE 8(12):e81499
Jia Y, Wei E, Wang X, Zang X, Morrison JC, Parikh M et al (2014) Optical coherence tomography angiography of optic disc perfusion in glaucoma. Ophthalmology 121(7):1322–1332
Bandello F, Corbelli E, Carnevali A, Pierro L, Querques G (2016) Optical coherence tomography angiography of diabetic retinopathy. Dev Ophthalmol 56:107–112
Kim AY, Chu Z, Shahidzadeh A, Wang RK, Puliafito CA, Kashani AH (2016) Quantifying microvascular density and morphology in diabetic retinopathy using spectral-domain optical coherence tomography angiography. Invest Ophthalmol Vis Sci 57(9):OCT362–OCT370
Somkijrungroj T, Vongkulsiri S, Kongwattananon W, Chotcomwongse P, Luangpitakchumpol S, Jaisuekul K (2017) Assessment of vascular change using swept source optical coherence tomography angiography: a new theory explains central visual loss in Behcet’s disease. Ophthalmology 2017:2180723
Scarinci F, Picconi F, Giorno P, Boccassini B, De Geronimo D, Varano M et al (2018) Deep capillary plexus impairment in patients with type 1 diabetes mellitus with no signs of diabetic retinopathy revealed using optical coherence tomography angiography. Acta Ophthalmol 96(2):264–265
de Carlo TE, Chin AT, BoniniFilho MA, Adhi M, Branchini L, Salz DA et al (2015) Detection of microvascular changes in eyes of patients with diabetes but not clinical diabetic retinopathy using optical coherence tomography angiography. Retina 35:2364–2370
Mullaney J, Collum LM (1985) Ocular vasculitis in Behcet’s disease. Apathological and immunohistochemical study. Int Ophthalmol 7:183–191
George RK, Chan CC, Whitcup SM, Nussenblatt RB (1997) Ocular immunopathology of Behcet’s disease. Surv Ophthalmol 42:157–162
Atmaca LS, Sonmez PA (2003) Fluorescein and indocyanine green angiography findings in Behcet’s disease. Br J Ophthalmol 87:1466–1468
Bozzoni-Pantaleoni F, Gharbiya M, Pirraglia MP, Accorinti M, Pivetti-Pezzi P (2001) Indocyanine green angiographic findings in Behcet disease. Retina 21:230–236
Kim M, Kim H, Kwon HJ, Kim SS, Koh HJ, Lee SC (2013) Choroidal thickness in Behcet’s üveitis: an enhanced depth imaging optical coherence tomography and its association with angiographic changes. Invest Ophthalmol Vis Sci 54(9):6033–6039
Ataş M, Yuvacı I, Demircan S, Güler E, Altunel O, Pangal E et al (2014) Evaluation of the macular, peripapillary nerve fiber layer and choroid thickness changes in Behçet’s disease with spectral-domain OCT. J Ophthalmol 2014:865394
Chams H, Mohtasham N, Davatchi F, Shahram F, Naji A, Aalami Harandi Z et al (2015) Ophthalmic findings in Behçet's disease: cases without apparent ocular signs. J Curr Ophthalmol 27(1–2):46–50
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Çömez, A., Beyoğlu, A. & Karaküçük, Y. Quantitative analysis of retinal microcirculation in optical coherence tomography angiography in cases with Behçet’s disease without ocular involvement. Int Ophthalmol 39, 2213–2221 (2019). https://doi.org/10.1007/s10792-018-1059-z
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DOI: https://doi.org/10.1007/s10792-018-1059-z