Evaluation and Comparison of Choroidal Thickness in Patients with Behçet Disease with versus without Ocular Involvement

Abstract

Purpose: To assess the subfoveal choroidal thickness (SFCT) in patients with Behçet disease (BD) and compare the SFCT in patients with and without ocular BD (OBD) and between patients with active and quiescent phases of the Behçet’s posterior uveitis.


Method: This prospective cross-sectional study was conducted on patients with BD (n = 51) between October 2016 and October 2018. Complete ocular examinations including slit lamp biomicroscopy and fundus examination with dilated pupils were performed for all patients. The SFCT values were compared between patients with and without OBD. Enhanced depth imaging optical coherence tomography (EDI–OCT) was done to measure the SFCT, and wide field fundus fluorescein angiography (WF–FAG) was performed to evaluate the ocular involvement and determine the active or quiescent phases of the Behçet’s posterior uveitis. The correlation between the changes of SFCT and the WF-FAG scores was assessed.


Results: One hundred and two eyes of 51 patients with BD, aged 29 to 52 years were studied. Of these, 23 patients were male. The mean age ± standard deviation in patients with OBD and patients without ocular involvement was 38.71 ± 7.8 and 36.22 ± 10.59 years (P = 0.259) respectively. The mean SFCT in patients with OBD was significantly greater than in patients without OBD (364.17 ± 93.34 vs 320.43 ± 56.70 μm; P = 0.008). The difference of mean SFCT between the active compared to quiescent phase was not statistically significant when only WF-FAG criteria were considered for activity (368.12 ± 104.591 vs 354.57 ± 58.701 μm, P = 0.579). However, when the disease activity was considered based on both WF-FAG and ocular exam findings, SFCT in the active group was higher than the inactive group (393.04 ± 94.88 vs 351.65 ± 58.63 μm, P = 0.060). This difference did not reach statistical significance, but it was clinically relevant.


Conclusion: Choroidal thickness was significantly increased in BD patients with ocular involvement; therefore, EDI-OCT could be a noninvasive test for evaluation of ocular involvement in patients with BD. The increased SFCT was not an indicative of activity in OBD; however, it could predict possible ocular involvement throughout the disease course.

Keywords:

Behçet’s Disease, Behçet’s Uveitis, Choroidal Thickness, Enhanced Depth Imaging Optical Coherence Tomography (EDI–OCT), Ocular Behçet, Wide Field Fluorescein Angiography

References
1. France R, Buchanan RN, Wilson MW, Sheldon MB Jr. Relapsing iritis with recurrent ulcers of the mouth and genitalia (Behcet’s syndrome). Review: with report of additional case. Medicine 1951;30:335–355.

2. Deuter CM, Kötter I, Wallace GR, Murray PI, Stübiger N, Zierhut M. Behçet’s disease: ocular effects and treatment. Prog Retin Eye Res 2008;27:111–136.

3. Emre S, Güven-Yılmaz S, Ulusoy MO, Ateş H. Optical coherence tomography angiography findings in Behcet patients. Int Ophthalmol 2019;39:1–9.

4. Tugal-Tutkun I. Imaging in the diagnosis and management of Behçet disease. Int Ophthalmol Clin 2012;52:183–190.

5. Akkoç N. Update on the epidemiology, risk factors and disease outcomes of Behçet’s disease. Best Pract Res Clin Rheumatol 2018;321–310.

6. Kim M, Kim H, Kwon HJ, Kim SS, Koh HJ, Lee SC. Choroidal thickness in Behcet’s uveitis: an enhanced depth imagingoptical coherence tomography and its association with angiographic changes. Invest Ophthalmol Vis Sci 2013;54:6033–6039.

7. Khairallah M, Abroug N, Khochtali S, Mahmoud A, Jelliti B, Coscas G, et al. Optical coherence tomography angiography in patients with Behcet uveitis. Retina 2017;37:1678–1691.

8. Onal S, Uludag G, Oray M, Mengi E, Herbort CP, Akman M, et al. Quantitative analysis of structural alterations in the choroid of patients with active Behçet uveitis. Retina 2018;38:828–840.

9. Tugal-Tutkun I, Ozdal PC, Oray M, Onal S. Review for diagnostics of the year: multimodal imaging in Behçet uveitis. Ocul Immunol Inflamm 2017;25:7–19.

10. Tugal-Tutkun I, Onal S, Altan-Yaycioglu R, Altunbas HH, Urgancioglu M. Uveitis in Behçet disease: an analysis of 880 patients. Am J Ophthalmol 2004;138:373–380.

11. Tugal-Tutkun I. Behçet’s uveitis. Middle East Afr J Ophthalmol 2009;16:219–224.

12. Atmaca LS. Fundus changes associated with Behçet’s disease. Graefes Arch Clin Exp Ophthalmol 1989;227:340–344.

13. Özdal P, Ortac S, Taşkintuna I, Firat E. Posterior segment involvement in ocular Behçet’s disease. Eur J Ophthalmol 2002;12:424–431.

14. Coskun E, Gurler B, Pehlivan Y, Kisacik B, Okumus S, Yayuspayı R, et al. Enhanced depth imaging optical coherence tomography findings in Behcet disease. Ocul Immunol Inflamm 2013;21:440–445.

15. Hassenstein A, Meyer CH. Clinical use and research applications of Heidelberg retinal angiography and spectral−domain optical coherence tomography–a review. Clin Experiment Ophthalmol 2009;37:130–143.

16. Atmaca L, Sonmez P. Fluorescein and indocyanine green angiography findings in Behçet’s disease. Br J Ophthalmol 2003;87:1466–1468.

17. Ishikawa S, Taguchi M, Muraoka T, Sakurai Y, Kanda T, Takeuchi M. Changes in subfoveal choroidal thickness associated with uveitis activity in patients with Behcet’s disease. Br J Ophthalmol 2014;98:1508–1513.

18. Ataş M, Yuvacı İ, Demircan S, Güler E, Altunel O, Pangal E, et al. Evaluation of the macular, peripapillary nerve fiber layer and choroid thickness changes in Behçet’s disease with spectral-domain OCT. J Ophthalmol 2014:865394.

19. Tugal-Tutkun I, Herbort CP, Khairallah M, Group ASfUW. Scoring of dual fluorescein and ICG inflammatory angiographic signs for the grading of posterior segment inflammation (dual fluorescein and ICG angiographic scoring system for uveitis). Int Ophthalmol 2010;30:539–552.

20. Charteris D, Barton K, McCartney A, Lightman S. CD4+ Lymphocyte involvement in ocular Behclet’s disease. Autoimmunity 1992;12:201–206.

21. George RK, Chan C-C, Whitcup SM, Nussenblatt RB. Ocular immunopathology of Behçet’s disease. Surv Ophthalmol 1997;42:157–162.

22. Mullaney J, Collum LM. Ocular vasculitis in Behcet’s disease. A pathological and immunohistochemical study. Int Ophthalmol 1985;7:183–191.

23. Branchini LA, Adhi M, Regatieri CV, Nandakumar N, Liu JJ, Laver N, et al. Analysis of choroidal morphologic features and vasculature in healthy eyes using spectraldomain optical coherence tomography. Ophthalmology 2013;120:1901–1908.

24. Invernizzi A, Mapelli C, Viola F, Cigada M, Cimino L, Ratiglia R, et al. Choroidal granulomas visualized by enhanced depth imaging optical coherence tomography. Retina 2015;35:525–531.

25. Kang HM, Lee SC. Long-term progression of retinal vasculitis in Behçet patients using a fluorescein angiography scoring system. Graefes Arch Clin Exp Ophthalmol 2014;252:1001–1008.

26. Moon SW, Kim BH, Park UC, Yu HG. Inter-observer variability in scoring ultra-wide-field fluorescein angiography in patients with Behçet retinal vasculitis. Ocul Immunol Inflamm 2017;25:20–28.