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      Retinal arterial occlusion with multiple retinal emboli and carotid artery occlusion disease. Haemodynamic changes and pathways of embolism

      research-article
      1 , 2 , 3 , 1 , , 4 , 5
      BMJ Open Ophthalmology
      BMJ Publishing Group
      retina, imaging

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          Abstract

          Objective

          To introduce a special subgroup, retinal artery occlusion (RAO) with multiple emboli, which is highly associated with ipsilateral carotid artery occlusion disease (CAOD).

          Methods and analysis

          This is a cohort study. Cases of RAO with multiple retinal emboli were consecutively enrolled. All patients underwent at least one of the carotid/cerebral evaluations: carotid arteriography, orbital/carotid colour Doppler ultrasonography and CT angiography to demonstrate haemodynamic changes and to discuss possible mechanisms and pathways of the emboli.

          Results

          Among 208 RAO eyes, 12 eyes (5.7%) in 11 patients had multiple emboli were recruited in this study. Eleven eyes (91.6%) had ipsilateral carotid plaques and atherosclerosis with high-grade stenosis; among them, five were total carotid occlusion. Haemodynamic changes were found in nine patients with RAO (81.8%) with carotid stenosis 60% or greater. Most compensatory intracranial circulations were re-established via the circle of Willi with antegrade ophthalmic flows, but the direction of ophthalmic flow reversed in three eyes indicating the recruitment of external collaterals. Two cases underwent carotid stent successfully.

          Conclusion

          RAOs with multiple emboli are rare but highly associated with severe CAOD with haemodynamic flow changes, warning critical condition in carotid/cerebral circulations. Either direct embolism from the carotid or cardiac lesions or indirect embolism via the collateral pathways is the mechanism of pathogenesis. Immediate action should start to manage these patients to prevent further deterioration.

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          Most cited references29

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          Acute retinal arterial occlusive disorders.

          The initial section deals with basic sciences; among the various topics briefly discussed are the anatomical features of ophthalmic, central retinal and cilioretinal arteries which may play a role in acute retinal arterial ischemic disorders. Crucial information required in the management of central retinal artery occlusion (CRAO) is the length of time the retina can survive following that. An experimental study shows that CRAO for 97min produces no detectable permanent retinal damage but there is a progressive ischemic damage thereafter, and by 4h the retina has suffered irreversible damage. In the clinical section, I discuss at length various controversies on acute retinal arterial ischemic disorders. Classification of acute retinal arterial ischemic disorders: These are of 4 types: CRAO, branch retinal artery occlusion (BRAO), cotton wool spots and amaurosis fugax. Both CRAO and BRAO further comprise multiple clinical entities. Contrary to the universal belief, pathogenetically, clinically and for management, CRAO is not one clinical entity but 4 distinct clinical entities - non-arteritic CRAO, non-arteritic CRAO with cilioretinal artery sparing, arteritic CRAO associated with giant cell arteritis (GCA) and transient non-arteritic CRAO. Similarly, BRAO comprises permanent BRAO, transient BRAO and cilioretinal artery occlusion (CLRAO), and the latter further consists of 3 distinct clinical entities - non-arteritic CLRAO alone, non-arteritic CLRAO associated with central retinal vein occlusion and arteritic CLRAO associated with GCA. Understanding these classifications is essential to comprehend fully various aspects of these disorders. Central retinal artery occlusion: The pathogeneses, clinical features and management of the various types of CRAO are discussed in detail. Contrary to the prevalent belief, spontaneous improvement in both visual acuity and visual fields does occur, mainly during the first 7 days. The incidence of spontaneous visual acuity improvement during the first 7 days differs significantly (p<0.001) among the 4 types of CRAO; among them, in eyes with initial visual acuity of counting finger or worse, visual acuity improved, remained stable or deteriorated in non-arteritic CRAO in 22%, 66% and 12% respectively; in non-arteritic CRAO with cilioretinal artery sparing in 67%, 33% and none respectively; and in transient non-arteritic CRAO in 82%, 18% and none respectively. Arteritic CRAO shows no change. Recent studies have shown that administration of local intra-arterial thrombolytic agent not only has no beneficial effect but also can be harmful. Prevalent multiple misconceptions on CRAO are discussed. Branch retinal artery occlusion: Pathogeneses, clinical features and management of various types of BRAO are discussed at length. The natural history of visual acuity outcome shows a final visual acuity of 20/40 or better in 89% of permanent BRAO cases, 100% of transient BRAO and 100% of non-arteritic CLRAO alone. Cotton wools spots: These are common, non-specific acute focal retinal ischemic lesions, seen in many retinopathies. Their pathogenesis and clinical features are discussed in detail. Amaurosis fugax: Its pathogenesis, clinical features and management are described.
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            Retinal artery occlusion: associated systemic and ophthalmic abnormalities.

            To investigate systematically the various associated systemic and ophthalmic abnormalities in different types of retinal artery occlusion (RAO). Cohort study. We included 439 consecutive untreated patients (499 eyes) with RAO first seen in our clinic from 1973 to 2000. At first visit, all patients underwent detailed ophthalmic and medical history, and comprehensive ophthalmic evaluation. Visual evaluation was done by recording visual acuity, using the Snellen visual acuity chart, and visual fields with a Goldmann perimeter. Initially they also had carotid Doppler/angiography and echocardiography. The same ophthalmic evaluation was performed at each follow-up visit. Demographic features, associated systemic and ophthalmic abnormalities, and sources of emboli in various types of RAO. We classified RAO into central (CRAO) and branch (BRAO) artery occlusion. In both nonarteritic (NA) CRAO and BRAO, the prevalence of diabetes mellitus, arterial hypertension, ischemic heart disease, and cerebrovascular accidents were significantly higher compared with the prevalence of these conditions in the matched US population (all P or =50% stenosis in 31% of NA-CRAO patients and 30% of BRAO, and plaques in 71% of NA-CRAO and 66% of BRAO. An abnormal echocardiogram with an embolic source was seen in 52% of NA-CRAO and 42% of BRAO. Neovascular glaucoma developed in only 2.5% of NA-CRAO eyes. This study showed that, in CRAO as well as BRAO, the prevalence of various cardiovascular diseases and smoking was significantly higher compared with the prevalence of these conditions in the matched US population. Embolism is the most common cause of CRAO and BRAO; plaque in the carotid artery is usually the source of embolism and less commonly the aortic and/or mitral valve. The presence of plaques in the carotid artery is generally of much greater importance than the degree of stenosis in the artery. Contrary to the prevalent misconception, we found no cause-and-effect relationship between CRAO and neovascular glaucoma.
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              Pattern of collaterals, type of infarcts, and haemodynamic impairment in carotid artery occlusion.

              In internal carotid artery (ICA) occlusion, increased oxygen extraction fraction (OEF) indicates inadequate collateral blood flow distal to the occlusion, which may be caused by poor function of collateral pathways. In ICA occlusion, the circle of Willis may be the major collateral pathway, while the collaterals through the ophthalmic artery and leptomeningeal vessels may be recruited when collateral flow through the circle of Willis is inadequate. Conversely, ischaemic lesions may affect the adequacy of collateral blood flow by reducing the metabolic demand of the brain. To determine whether the pattern of collateral pathways and the type of infarcts are independent predictors of OEF in ICA occlusion. We studied 42 patients with symptomatic ICA occlusion. The presence of Willisian, ophthalmic, or leptomeningeal collaterals was evaluated by conventional four vessel angiography. The infarcts on magnetic resonance imaging were categorised as territorial, border zone (external or internal), striatocapsular, lacunar, and other white matter infarcts. The value of OEF in the affected hemisphere was measured with positron emission tomography as an index of haemodynamic impairment. Using multivariate analysis, the presence of any ophthalmic or leptomeningeal collaterals and the absence of striatocapsular infarcts were significant and independent predictors of increased OEF. In patients with symptomatic ICA occlusion, the supply of collateral flow, which is affected by the pattern of collateral pathways, and the metabolic demand of the brain, which is affected by the type of infarct, may be important factors determining the severity of haemodynamic impairment.
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                Author and article information

                Journal
                BMJ Open Ophthalmol
                BMJ Open Ophthalmol
                bmjophth
                bmjophth
                BMJ Open Ophthalmology
                BMJ Publishing Group (BMA House, Tavistock Square, London, WC1H 9JR )
                2397-3269
                2020
                27 July 2020
                : 5
                : 1
                : e000467
                Affiliations
                [1 ]departmentDepartment of Ophthalmology , Changhua Christian Medical Foundation Changhua Christian Hospital , Changhua, Taiwan
                [2 ]departmentSchool of Medicine , Chung Shan Medical University , Changhua, Taiwan
                [3 ]departmentDepartment of Optometry , College of Nursing and Health Sciences, Da-Yeh University , Changhua, Taiwan
                [4 ]departmentCentre for Neuroscience Studies , Queen's University , Kingston, Ontario, Canada
                [5 ]departmentDepartment of Neurology , Changhua Christian Medical Foundation Changhua Christian Hospital , Changhua City, Taiwan
                Author notes
                [Correspondence to ] Dr Jiunn-Feng Hwang; hwangjf@ 123456cch.org.tw
                Author information
                http://orcid.org/0000-0002-4191-7136
                http://orcid.org/0000-0002-7423-6353
                Article
                bmjophth-2020-000467
                10.1136/bmjophth-2020-000467
                7390230
                b31da758-befd-40af-9b05-207cc86e04ae
                © Author(s) (or their employer(s)) 2020. Re-use permitted under CC BY-NC. No commercial re-use. See rights and permissions. Published by BMJ.

                This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See:  http://creativecommons.org/licenses/by-nc/4.0/.

                History
                : 19 March 2020
                : 22 June 2020
                : 10 July 2020
                Categories
                Original Research
                1506
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                retina,imaging
                retina, imaging

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