Significant changes of the choroid in patients with ocular ischemic syndrome and symptomatic carotid artery stenosis

Autoři: Hae Min Kang aff001;  Jeong Hoon Choi aff002;  Hyoung Jun Koh aff003;  Sung Chul Lee aff003
Působiště autorů: Department of Ophthalmology, Catholic Kwandong University College of Medicine, International St. Mary’s Hospital, Incheon, Republic of Korea aff001;  Choikang Eye Clinic, Seoul, Republic of Korea aff002;  Department of Ophthalmology, Yonsei University College of Medicine, Seoul, Republic of Korea aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article



To evaluated the changes in choroidal vasculature in patients with ocular ischemic syndrome (OIS) and in the ipsilateral eyes of patients with symptomatic carotid artery stenosis (CAS)


A total of 50 patients (15 patients with OIS, 10 patients with symptomatic CAS, 25 patients of age-and sex-matched control group) were included, and the medical records were retrospectively reviewed. The mean subfoveal choroidal thickness (SFCT) of each eye was measured, and binary images of the choroid were evaluated to compare the mean choroidal area and the luminal area.


The mean SFCT was 170.5±75.3 μm in the eyes with OIS, 154.8±62.9 μm in the ipsilateral eyes with symptomatic CAS, and 277.5±73.2 μm in the right eyes of the control group patients (P<0.001). The mean choroidal area was 494,478.6±181,846.2 μm2 in the eyes with OIS, 453,750.0±196,725.8 μm2 in the ipsilateral eyes with symptomatic CAS, and 720,520±281,319.5 μm2 in the control group eyes (P = 0.036). The mean luminal area was 333,185.7±112,665.9 μm2 in the eyes with OIS, 313,983.3±132,032.1 μm2 in the ipsilateral eyes with symptomatic CAS, and 480,325.0±185,112.6 μm2 in the control group eyes (P = 0.046). The mean SFCT, mean choroidal area, and mean luminal area were significantly smaller in the eyes with OIS (P = 0.017, P = 0.005, and P = 0.004, respectively), and those with symptomatic CAS (P = 0.020, P = 0.016, and P = 0.021, respectively) than in the unaffected contralateral eyes. There were no significant differences between the eyes in the control group (P = 0.984, P = 284, and P = 0.413, respectively).


The mean SFCT, mean choroidal area, and mean luminal area were significantly thinner in the eyes with OIS and the ipsilateral eyes with symptomatic CAS, compared with the control group eyes. The eyes with OIS and those with symptomatic CAS had significantly thinner SFCT, and smaller choroidal area and luminal area than the unaffected contralateral eyes. Choroid may reflect the vascular status of the carotid artery, indicated by choroidal thinning and decreasing choroidal area, especially luminal area.

Klíčová slova:

Blood flow – Carotid arteries – Eye diseases – Eyes – Ophthalmology – Stenosis – Tomography – Choroid


1. Grant MB, Lutty GA. Ryan’s Retina: Retinal and choroidal vasculature: retinal oxygenation. 6th ed. Elsevier; 2018

2. Nickla DL, Wallman J. The multifunctional choroid. Prog Retin Eye Res 2010;29(2):144–168 doi: 10.1016/j.preteyeres.2009.12.002 20044062

3. Biousse V. Carotid disease and the eye. Curr Opin Ophthalmol 1997;8(6):16–26 10176098

4. Dugan JD Jr, Green WR. Ophthalmologic manifestations of carotid occlusive disease. Eye 1991;5(Pr 1):226–238

5. Lawrence PF, Oderich GS. Ophthalmologic findings as predictors of carotid artery disease. Vasc Endovascular Surg 2002;36(6):415–424 doi: 10.1177/153857440203600602 12476231

6. Volkers EJ, Donders RC, Koudstaal PJ, van Gijn J, Algra A, Jaap Kappelle L. Transient monocular blindness and the risk of vascular complications according to subtype: a prospective cohort study. J Neurol 2016;263(9):1771–1777 doi: 10.1007/s00415-016-8189-x 27314958

7. Avery MB, Magal I, Kherani A, Mitha AP. Risk of stroke in patients with ocular arterial occlusive disorders: a retrospective Canadian study. J Am Heart Assoc 2019;8(3):3010509. doi: 10.1161/JAHA.118.010509 30712440

8. Hayreh SS, Zimmerman MB. Ocular arterial occlusive disorders and carotid artery disease. Ophthalmol Retina 2017;1(1):12–18 doi: 10.1016/j.oret.2016.08.003 28547004

9. Mendrinos E, Machinis TG, Pournaras CJ. Ocular ischemic syndrome. Surv Ophthalmol 2010;55(1):2–34 doi: 10.1016/j.survophthal.2009.02.024 19833366

10. Terelak-Borys B, Skonieczna K, Grabska-Liberek I. Ocular ischemic syndrome–a systematic review. Med Sci Monit 2012;18(8):RA138–144 doi: 10.12659/MSM.883260 22847215

11. Brown GC, Magargal LE. The ocular ischemic syndrome. Clinical, fluorescein angiographic and carotid angiographic features. Int Ophthalmol 1988;11(4):239–251 3182177

12. Mizener JB, Podhajsky P, Hayreh SS. Ocular ischemic syndrome. Ophthalmology 1997;104(5):859–864 doi: 10.1016/s0161-6420(97)30221-8 9160035

13. Kim YH, Sung MS, Park SW. Clinical features of ocular ischemic syndrome and risk factors for neovascular glaucoma. Korean J Ophthalmol 2017;31(4):343–350 doi: 10.3341/kjo.2016.0067 28682017

14. Luo J, Yan Z, Jia Y, Luo R. Clinical analysis of 42 cases of ocular ischemic syndrome. J Ophthalmol 2018;2018:2606147. doi: 10.1155/2018/2606147 eCollection 2018. 29713523

15. Sturrock GD, Mueller HR. Chronic ocular ischaemia. Br J Ophthalmol 1984;68(10):716–723 doi: 10.1136/bjo.68.10.716 6383463

16. Sivalingam A, Brown GC, Magargal LE. The ocular ischemic syndrome.Ⅲ. Visual prognosis and the effect of treatment. Int Ophthalmol 1991;15(1):15–20 2010264

17. Sivalingam A, Brown GC, Magargal LE, Menduke H. The ocular ischemic syndrome. Ⅱ. Mortality and systemic morbidity. Int Ophthalmol 1989;13(3):187–191 2793312

18. Kang HM, Lee CS, Lee SC. Thinner subfoveal choroidal thickness in eyes with ocular ischemic syndrome than in unaffected contralateral eyes. Graefes Arch Clin Exp Ophthalmol 2014;252(5):851–852 doi: 10.1007/s00417-014-2609-3 24687142

19. Kim DY, Joe SG, Lee JY, Kim JG, Yang SJ. Choroidal thickness in eyes with unilateral ocular ischemic syndrome. J Ophthalmol 2015;2015:620372. doi: 10.1155/2015/620372 26504596

20. Wang H, Wang Y, Li H. Multimodality imaging assessment of ocular ischemic syndrome. J Ophthalmol 2017;2017:4169135. doi: 10.1155/2017/4169135 29375911

21. Wang H, Wang Y, Li H. Subfoveal choroidal thickness and volume in severe internal carotid artery stenosis patients. Int J Ophthalmol 2017;10(12):1870–1876 doi: 10.18240/ijo.2017.12.13 29259906

22. Wabnitz AM, Turan TN. Symptomatic carotid artery stenosis: surgery, stenting, or medical therapy? Curr Treat Options Cardio Med 2017;19(6):62

23. Barnett HJ, Taylor DW, Eliasziw M, Fox AJ, Ferguson GG, Haynes RB, et al., Benefit of carotid endarterectomy in patients with symptomatic moderate or severe stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med 1998;339(20):1415–1425 doi: 10.1056/NEJM199811123392002 9811916

24. Moore WS, Barnett HJ, Beebe HG, Bernstein EF, Brener BJ, Brott T, et al., Guidelines for carotid endarterectomy. A multidisciplinary consensus statement from the ad hoc Committee, American Heart Association. Stoke 1995;26(1):188–201

25. Sonoda S, Sakamoto T, Yamashita T, Shirasawa M, Uchino E, Terasaki H et al., Choroidal structure in normal eyes and after photodynamic therapy determined by binarization of optical coherence tomographic images. Invest Ophthalmol Vis Sci 2014;55(6):3893–3899 doi: 10.1167/iovs.14-14447 24894395

26. Sonoda S, Sakamoto T, Yamashita T, Uchino E, Kawano H, Yoshihara N, et al., Luminal and stromal areas of choroid determined by binarization method of optical coherence tomographic images. Am J Ophthalmol 2015;159(6):1123–1131 doi: 10.1016/j.ajo.2015.03.005 25790737

27. Shinohara Y, Kashima T, Akiyama H, Shimoda Y, Li D, Kish S. Evaluation of fundus blood flow in normal individuals and patients with internal carotid artery obstruction using laser speckle flowgraphy. PLoS One. 2017;12(1):e0169596. doi: 10.1371/journal.pone.0169596 28056061

28. Kearns TP. Ophthalmology and the carotid artery. Am J Ophthalmol 1979;88(4):714–722 doi: 10.1016/0002-9394(79)90671-8 507143

29. Cohen R, Padilla J, Light D, Diller R. Carotid artery occlusive disease and ocular manifestations: Importance of identifying patients at risk. Optometry 2010;81(7):359–363 doi: 10.1016/j.optm.2009.10.013 20630374

30. Ma F, Su J, Shang Q, Ma J, Zhang T, Wang X, et al., Changes in ocular hemodynamics after carotid artery angioplasty and stenting (CAAS) in patients with different severity of ocular ischemic syndrome. Curr Eye Res 2018;43(2):266–272 doi: 10.1080/02713683.2017.1390771 29135355

31. Neroev VV, Kiseleva TN, Vlasov SK, Pak NV, Gavrilenko AV. Kuklin AV. Visual outcomes after carotid reconstructive surgery for ocular ischemia. Eye (Lond) 2012;26(10):1281–1287

32. Ishii M, Hayashi M, Yagi F, Sato K, Tomita G, Iwabuchi S. Relationship between the direction of ophthalmic artery blood flow and ocular microcirculation before and after carotid artery stenting. J Ophthalmol 2016;2016:2530914. doi: 10.1155/2016/2530914 28070413

33. Kawaguchi S, Iida J, Uchiyama Y. Ocular circulation and chronic ocular ischemic syndrome before and after carotid artery revascularization surgery. J Ophthalmol 2012;2012:350475. doi: 10.1155/2012/350475 23316337

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2019 Číslo 10
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