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Ocular Ischemic Syndrome: A Brief Review

Hyder J. Almosawy, OD; Joseph V. Mega, OD; Paul B. Greenberg, MD, MPH; Claire Messina, OD; Amanda M. Hunter, OD

Abstract pupillary response to light on the affected side corresponding We review the etiology, characteristics and management of the stenosis.1 Notable anterior segment findings include ocular ischemic syndrome (OIS). Ocular ischemic syndrome neovascularization of the (NVI) (Fig. 1) [present in up to 90% is a visual-threatening condition closely linked to advanced of cases],1,2,4 neovascularization of the angle (NVA), iris atrophy, cardiovascular disease. Patients with OIS are at risk for ocular low grade , and hypotony.1,2 neovascularization and . Diagnostic testing to confirm the diagnosis of OIS must be done in order The most common posterior segment finding in OIS is mid- to properly determine treatment and management options for peripheral retinal hemorrhages (Fig. 2), which are present these patients as the risk for permanent visual loss is greater in 80% of cases.1,2,5,6 Other posterior segment findings with higher levels of and advanced cardiovascular include attenuation of retinal arteries, dilated retinal veins, disease. Coordination of care with the patient’s primary care microaneurysms, and posterior segment neovascularization. provider is necessary to optimize the patient’s cardiovascular Cystoid (CME) is present in 17% of OIS cases.1 risk factors and determine the most appropriate medical and/ or surgical treatment. Diagnostic Testing When a patient is suspected of having OIS, several ophthalmic Introduction diagnostic tests are helpful. Formal visual field testing can Ocular ischemic syndrome (OIS) is an uncommon but sight- uncover deficits due to retinal ischemia. The visual fields can threatening condition caused by the atherosclerotic occlusion range from normal to severe restriction and can serve as a of the common or internal carotid arteries or less commonly baseline for future change.1 (FA) can the .1,2 Ocular ischemic syndrome typically point to the presence of carotid stenosis and assess the degree occurs in the elderly—mean age is 65—and is an important of retinal ischemia. In a normal patient, the arm-to- time marker of cardio- and cerebrovascular disease,1,2 given that up in FA is normally five seconds; this can increase to one minute to 3% of this this age group have carotid artery disease.3 Herein, in OIS patients due to carotid artery occlusion.1,2,5 In addition we review the key characteristics and management of patients to demonstrating retinal hypoperfusion in OIS, FA can show with OIS. leakage from neovascularization, microaneurysms or CME.1,2

Characteristics Ocular ischemic syndrome presents unilaterally in 80% of cases.1,2 Vision loss can be gradual over several months to minutes, with patients presenting with a visual acuity ranged from 20/50 to counting fingers.1,2 Patients may have a sluggish

Hyder J. Almosawy, OD; Joseph V. Mega, OD; Paul B. Greenberg, MD, MPH; Claire Messina; Amanda M. Hunter, OD, Eye Clinic, Providence VA Medical Center Correspondence to: Amanda M. Hunter, OD, Eye Clinic, Providence VA Medical Center, 830 Chalkstone Ave., Providence, RI 02908 E-mail: [email protected] The authors have no financial or proprietary interest in any material or method mentioned in this article. This article has been peer reviewed. Disclaimer: The views expressed here are those of the authors and do not Figure 1. Neovascularization of the iris (NVI) corresponding to advanced necessarily reflect the position or the policy of the US Department of Veterans retinal ischemia. (Courtesy, North American Neuro- Society). Affairs or the US government

Ocular Ischemic Syndrome: A Brief Review 201 Systemic disease The systemic treatment of OIS can involve both medical and surgical therapy. Ocular ischemic syndrome is an important marker of cardiovascular disease.1,2 To this end, it is important to work with the patient’s PCP to manage any risk factors for cardiovascular disease. This includes treatment of , hypercholesterolemia or mellitus, smoking cessation and weight loss through diet and exercise.1,2 Additional subspecialty consultation with cardiology or neurology may also be needed.2 Anti-platelet agents and statins are effective in treating patients with less than 70% carotid artery stenosis but can also be used in a concerted effort with surgical intervention.9

The most effective surgical intervention is the carotid artery endarterectomy (CEA), which lowers the risks of in patients with 70-99% of carotid stenosis.1,2,8,10-12 A CEA is often effective in preventing progression and reversing signs of Figure 2. Retinal hemorrhages in the mid-periphery, commonly seen in OIS by increasing blood flow to ocular tissues.10,12 For these patients with ocular ischemic syndrome (Courtesy, Dr. Joseph Sowka, OD) . reasons, patients with significant carotid artery stenosis should be referred to vascular surgeons to consider CEA.

Not all OIS patients with this degree of stenosis may benefit With the assistance of the patient’s primary care provider (PCP), from CEA: a CEA is considered a high-risk procedure for suspected carotid artery stenosis can be verified with carotid perioperative stroke in patients over the age of 80 or who ultrasound, also known as the carotid duplex.1,2 Patients with suffer congestive heart failure, chronic obstructive pulmonary OIS typically have 75% stenosis of the carotid artery.1 Carotid disorder, recent coronary artery bypass graft or with complete duplex, with a sensitivity of up to 89% and a specificity of up occlusion of the contralateral carotid artery.9-11 Carotid artery to 84%,2,7,8 is a reliable diagnostic tool in patients with 70 to stenting (CAS), which involves inserting a stent into the stenotic 90% carotid stenosis. A carotid duplex may not detect stenosis lumen of an atherosclerotic carotid artery, is an alternative if it occurs higher up on the carotid artery.7 Indeed, for those treatment for higher risk patients.9,10 suspected OIS patients without significant stenosis on carotid ultrasound testing, a magnetic resonance angiogram (MRA) or Prognosis computed tomography angiography (CTA) may be helpful.1,2,8 The majority of OIS patients (58%) will have counting For detecting 70-99% carotid artery stenosis, the MRA and CTA fingers vision or worse visual acuity (VA) one year following have a sensitivities and specificities of up to 95% and 90% and diagnosis, irrespective of their presenting vision.1,2,6 If NVI is up to 91.6% and 97.4%,7,8 respectively. Unlike CTA, MRA does present at the time of diagnosis, 97% of patients will have a not expose patients to radiation but it would generally preclude VA of counting fingers or worse after 1 year.6 Systemically, patients with claustrophobia, pacemakers or other metallic patients presenting with OIS have a 40% mortality rate at five implantable devices in the body.7 years.1,2,4 The most common causes of death in OIS patients are myocardial infarction (67%) and cerebrovascular accident Management (19%).1,2,4 Educating patients on OIS and its ocular and systemic Ocular disease manifestations is not only critical in terms of preserving vision The ocular treatment of patients with OIS depends on the but also in reducing the risk for cardiovascular complications. presenting signs. Neovascularization of the anterior or posterior segment is typically treated with laser pan-retinal Conclusion photocoagulation or intravitreal injection of anti-vascular In sum, OIS is closely linked to a patient’s ocular and systemic endothelial growth factor (VEGF) agents.1 In patients with health. It is important that eye providers work closely with the CME, the main course of treatment is intravitreal anti-VEGF PCP to optimize the health outcomes of this high-risk patient therapy.1,2 For patients without ocular NV or CME, continued cohort. Due to the high mortality rate (40%) of patients with a observation with undilated gonioscopy and dilated fundus diagnosis of OIS, it is imperative that eyecare providers perform exams is necessary to monitor for these complications. The a thorough dilated eye examination on every patient annually. ocular follow-up plan for OIS patients will be based on their exam findings: patients with ocular neovascularization who Acknowledgements require treatment will need closer follow-up than patients We thank Dr. Joseph Sowka, OD for providing the fundus without ocular neovascularization. photograph for this manuscript.

202 Clinical & Refractive Optometry 31.2, 2020 References 9. Koelemay MJ, Nederkoorn PJ, Reitsma JB, Majoie 1. Terelak-Borys B, Skonieczna K, Grabska-Liberek I. Ocular CB. Systematic Review of Computed Tomographic ischemic syndrome - a systematic review. Med Sci Monit. Angiography for Assessment of Carotid Artery Disease. 2012;18(8):RA138–RA144. doi:10.12659/msm.883260 Stroke. 2004;35(10):2306-2312. doi:10.1161/01. 2. Sharma S, Brown GC. Ocular Ischemic Syndrome. . str.0000141426.63959.cc. 2006:1491-1502. doi:10.1016/b978-0-323-02598-0.50090-2. 10. Park J-H, Lee J-H. Carotid Artery Stenting. Korean Circulation 3. Eslami MOH, Pounds LC. Carotid Artery Disease. Carotid Journal. 2018;48(2):97. doi:10.4070/kcj.2017.0208s Artery Disease | Society for Vascular Surgery. https://vascular. 11. Haynes RB. Prevention of functional impairment by org/patient-resources/vascular-conditions/carotid-artery- endarterectomy for symptomatic high-grade carotid stenosis. disease. Accessed November 19, 2019. North American Symptomatic Carotid Endarterectomy 4. Sharma S, Brown GC. Ocular Ischemic Syndrome. Retina. Trial Collaborators. JAMA: The Journal of the American 2006:1491-1502. doi:10.1016/b978-0-323-02598-0.50090-2. Medical Association. 1994;271(16):1256-1259. doi:10.1001/ 5. Hung JH, Chang YS. Ocular ischemic syndrome. CMAJ. jama.271.16.1256. 2017;189(23):E804. doi:10.1503/cmaj.160459 12. White CJ. Stroke prevention: carotid stenting versus carotid 6. Brown GC, Magargal LE. The ocular ischemic syndrome. endarterectomy. F1000 Medicine Reports. 2010. doi:10.3410/ International Ophthalmology. 1988;11(4):239-251. m2-24. doi:10.1007/bf00131023. 13. Gee W. Regarding “Assessment of ocular perfusion after 7. Sivalingam A, Brown GC, Magargal LE. The ocular ischemic carotid endarterectomy with color-flow duplex scanning.” syndrome. III. Visual prognosis and the effect of treatment. Journal of Vascular Surgery. 1999;30(5):960. doi:10.1016/ International Ophthalmology. 1991;15(1):15-20. doi:10.1007/ s0741-5214(99)70026-1. bf00150974. 8. Adla T, Adlova R. Multimodality Imaging of Carotid Stenosis. Int J Angiol. 2015;24(3):179–184. doi:10.1055/s-0035-1556056

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Ocular Ischemic Syndrome: A Brief Review 203 INSTRUCTIONS FOR 1 HOUR OF COPE CE CREDIT

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POST-COURSE TEST

Ocular Ischemic Syndrome: A Brief Review

1. Ocular Ischemic Syndrome (OIS) is caused by of which artery? Common carotid Internal carotid Ophthalmic artery All of the above

2. What is Ocular Ischemic Syndrome (OIS) an important marker of? Frontal lobe tumour Diabetes Cardio- and cerebrovascular disease Extraocular muscle Palsy

3. According to the article, which of the following notable anterior segment finding is found in 90% of OIS cases? Neovascularization of the Iris (NVI) Sluggish pupillary response Iris atrophy Low grade uveitis COPE ACCREDITED POST-COURSE TEST POST-COURSE ACCREDITED COPE

4. According to the article, what is the most common posterior segment findings in OIS? Cystoid macula oedema Mid-peripheral retinal hemorrhages Dilated retinal veins Posterior segment neovascularization

204 Clinical & Refractive Optometry 31.2, 2020 5. According to the article, which ophthalmic diagnostic tests are helpful in patients suspected of having OIS? and Fluorescein angiography Optical Coherence Tomography (OCT) and red desaturation test Ocular surface staining and corneal pachymetry Fundus photography and corneal topography

6. According to the article, which systemic diagnostic tests are NOT noted to be helpful in patients suspected of having OIS? Carotid ultrasound also known as carotid duplex Magnetic resonance angiogram (MRA) Computed tomography angiography (CTA) Carotid artery biopsy

7. Which of the following ocular management plans are INCORRECT? Patients without ocular NV or CME are to be continually observed with undilated gonioscopy and dilated fundus exams Patients with CME (cystoid macula edema) are treated with intravitreal anti-VEGF therapy Patients without ocular neovascularization need closer follow-up than patients that do Neovascularization of the anterior or posterior segment is treated with laser pan-retinal photocoagulation or intravitreal anti-VEGF injections

8. Which of the following systemic management plans are INCORRECT? The most effective surgical intervention is the carotid artery endarterectomy (CEA) Anti-platelet agents and statins are ineffective in treating patients with less than 70% carotid artery stenosis Treat underlying hypertension, hypercholesterolemia or diabetes as well as smoking cessation and weight loss through diet and exercise Carotid artery stenting (CAS) is an alternative for patients with high risk for perioperative stroke

9. According to the article, if NVI is present, what percentage of patients will have VA of counting fingers or worse after 1 year? 19% 58% 80% 97%

10. What are the most common causes of death in OIS patients? Myocardial Infarction Cerebrovascular accident Perioperative stroke Both B and C COPE ACCREDITED POST-COURSE TEST POST-COURSE ACCREDITED COPE

Ocular Ischemic Syndrome: A Brief Review 205