Acute retinal arterial occlusive disorders

doi:10.1016/j.preteyeres.2011.05.001

Progress in Retinal and Eye Research

Volume 30, Issue 5, September 2011, Pages 359-394

https://doi.org/10.1016/j.preteyeres.2011.05.001 Get rights and content

Abstract

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 97 min produces no detectable permanent retinal damage but there is a progressive ischemic damage thereafter, and by 4 h 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.

Introduction

Central retinal artery occlusion (CRAO) results in sudden, catastrophic visual loss and is therefore one of the most important topics in ophthalmology. Similarly, branch retinal arteriolar occlusion (BRAO) causes sudden segmental visual loss and may recur to involve other branch retinal arterioles. Amaurosis fugax is a common transient acute retinal ischemic condition. Thus, acute retinal arterial occlusive disorders together comprise one of the major causes of acute visual loss. There is a voluminous literature on the subject, with conflicting findings. The subject has been and continues to be rife with misconceptions and mistaken theories. Recent studies have provided new data on various aspects of acute retinal arterial occlusive disorders.

Since 1955 I have investigated the subject comprehensively by doing basic, experimental and clinical studies. Those have revealed new information about the retinal arterial blood supply and its occlusive disorders, contradicting much of the conventional thinking. The objective of this review is to provide a comprehensive overview of this important subject, based on my studies combined with a review of the relevant literature.

The first essential for an in-depth understanding of the retinal arterial occlusive disorders is a good grasp of the relevant basic scientific facts about them; the basic sciences are the foundation of Medicine. Following is a brief discussion of some of those.

Section snippets

Blood supply of the retina

The retina is supplied by the central retinal artery (CRA) and in some eyes also by the cilioretinal artery. The primary source of blood supply to both the arteries is the ophthalmic artery. A brief account of the anatomy of these three arteries is essential to understanding the retinal arterial vascular disorders.

Nerve supply to retinal vessels

During its intraorbital and intraneural portion the CRA has adrenergic nerve supply by a sympathetic nerve called the nerve of Tiedemann (Hayreh and Vrabec, 1966); however, the retinal branches of the CRA have no adrenergic nerve supply. Therefore, there is no autonomic innervation of the retinal vascular bed.

Blood-retinal barrier

The blood-retinal barrier plays an important role in the regulation of the microenvironment in the retina. There are two types of blood-retinal barrier.

Autoregulation of retinal blood flow

The object of blood flow autoregulation is to maintain the blood flow in a tissue relatively constant during changes in its perfusion pressure. This is an important mechanism to regulate blood flow. The retinal circulation has efficient autoregulation. The exact mechanism and site of autoregulation are still unclear, except that it most probably operates by altering the vascular resistance. It is generally considered a feature of the terminal arterioles; with the rise or fall of perfusion

Retinal tolerance time to acute ischemia

Retinal tolerance to acute ischemia is key to understanding the retinal arterial occlusive disorders and their management. We investigated this experimentally in 38 elderly, atherosclerotic and hypertensive rhesus monkeys (mimicking patients with CRAO), producing transient occlusion of the CRA varying from 97 to 240 min, by temporarily clamping the CRA at its site of entry into the optic nerve (Hayreh et al., 2004b). The retinal circulation, function and changes were evaluated before and during

Causes of retinal arterial occlusion

In the management of a disease, the first essential requisite is to know what caused it; therefore the first necessary task is to find out the causes of retinal arterial occlusion. There is a colossal amount of literature about the association of retinal arterial occlusion with a large variety of systemic and hematological conditions. Most of that is based on anecdotal case reports, and, given that, it is not always possible to establish a true cause-and-effect relationship between the

Racial differences in the causes of retinal arterial occlusion

Ahuja et al. (1999), in a retrospective study of consecutive 29 African American and 17 Caucasian patients with a diagnosis of amaurosis fugax, CRAO, BRAO, or intra-arterial retinal plaques, evaluated the causes of retinal artery occlusion. They found that their African American patients had a mean age of 61 years (range, 30–77 years) and the Caucasian patients a mean age of 73 years (range, 56–94 years) (p = 0.003). There was no statistically significant difference between the 2 groups with

Evaluation of patients with acute retinal arterial occlusion

It is generally agreed that all patients with acute retinal arterial occlusion must be evaluated for the source of embolism, which is the commonest cause for its development.

A recent study evaluated the role of carotid Doppler/angiography and Echocardiography in a prospective study 249 CRAO and 190 BRAO patients (Hayreh et al., 2009b). It showed that the plaque in the carotid artery is the usual source of embolism and less commonly the aortic and/or mitral valve.

Central retinal artery occlusion

Von Graefe (1859) was the first to diagnose CRAO ophthalmoscopically, and he wrote a classical description of the appearance of the fundus which is still well worth reading. The sudden and catastrophic visual loss with CRAO is one of the most important topics in ophthalmology. That makes it an ophthalmic emergency. In spite of this clinical entity having been well known for 150 years, and a voluminous literature on its various aspects, there are still several controversial issues. My critical

Hemi-central retinal artery occlusion

This has recently been reported by Karagoz et al. (2009) in one patient due to thromboembolism and by Rishi et al. (2010) in 4 young adults aged between 22 and 36. Color Doppler examination of the CRA confirmed branching of the artery behind the lamina cribrosa. My anatomical studies of CRA showed two examples of two CRAs in the optic nerve (Fig. 2) (Hayreh, 1958). Thus, occlusion of one of those can cause hemi-CRAO. This clinical entity should not be confused with occlusion of one of the two

Branch retinal arteriolar occlusion

As discussed above, the so-called “branch retinal arteries” are in fact arterioles (Hogan et al., 1971). Therefore the universally used term of “branch retinal artery occlusion” is incorrect.

Cotton wool spots

Cotton wool spots (CWSs) are common, acute, non-specific retinal lesions, seen in retinopathies due to a whole host of conditions, including diabetic retinopathy, hypertensive retinopathy, retinal vein occlusion, GCA, systemic lupus erythematosus, Wegener’s granulomatosis, dermatomyositis, human immunodeficiency virus retinopathy, cytomegalovirus retinitis, Purtscher’s retinopathy, Bartonella henselae neuroretinitis, radiation retinopathy, bone marrow transplantation retinopathy,

Amaurosis fugax

Amaurosis fugax (AF), or transient visual loss in an eye, is conventionally described as due to transient acute retinal ischemia. While that is true in most cases, it is important to remember that it does also occur due to conditions not involving the retina. An important and well-documented example of the latter is the AF seen in GCA, which is due to transient acute ischemia of the optic nerve head only. I have seen patients who experienced episodes of transient blurring of vision due to acute

Conclusions and future directions

There has been great confusion and controversy on the various types of acute retinal arterial occlusive disorders. For example, there is a very common impression that CRAO has a dismal visual outcome and no successful treatment. The primary reason for all this has been describing CRAO as all one clinical entity; the same applies to BRAO. Recent studies have proven otherwise. They have shown that, based on their pathogeneses and clinical features, CRAO and BRAO each consist of multiple distinct

Acknowledgements

I owe a very great debt of gratitude to Mrs. Patricia Duffel, librarian of our department, for her invaluable help in researching the literature on the subject, formatting the references to the style of Journal and inserting them in the text. I am also grateful to my wife Shelagh for her editorial assistance. Supported by grants EY-1151 and 1576 from the National Institutes of Health, and in part by unrestricted grant from Research to Prevent Blindness, Inc., New York.

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Retinal Vascular Occlusion Risks in High Blood Pressure and the Benefits of Blood Pressure Control
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This study aimed to evaluate the association of retinal vascular occlusion, including retinal vein occlusion (RVO) and retinal artery occlusion (RAO), with stages of hypertension.
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Based on baseline blood pressure (BP) as defined by the 2017 American College of Cardiology/American Heart Association guideline, participants were categorized into 4 BP groups. For the BP change measurement, BP groups were defined based on the combination of baseline and follow-up BP categories. The composite retinal vascular occlusion events and hazard ratios (HRs) of retinal vascular occlusion according to BP groups were estimated.
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^☆: The author has no conflict of interest.

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Acute retinal arterial occlusive disorders☆

Abstract

Introduction

Section snippets

Blood supply of the retina

Nerve supply to retinal vessels

Blood-retinal barrier

Autoregulation of retinal blood flow

Retinal tolerance time to acute ischemia

Causes of retinal arterial occlusion

Racial differences in the causes of retinal arterial occlusion

Evaluation of patients with acute retinal arterial occlusion

Central retinal artery occlusion

Hemi-central retinal artery occlusion

Branch retinal arteriolar occlusion

Cotton wool spots

Amaurosis fugax

Conclusions and future directions

Acknowledgements

Ophthalmology

Lancet

Ophthalmology

Am. J. Ophthalmol.

Ophthalmology

Am. J. Ophthalmol.

Am. J. Ophthalmol.

Am. J. Ophthalmol.

Am. J. Ophthalmol.

Exp. Eye Res.

Prog. Retin. Eye Res.

Prog. Retin. Eye Res.

Am. J. Ophthalmol.

Ophthalmology

Am. J. Ophthalmol.

Ophthalmology

Ophthalmology

Ophthalmology

Ophthalmology

Ophthalmology

Exp. Eye Res.

Am. J. Ophthalmol.

Ophthalmology

Mechanisms of retinal arterial occlusive disease in African American and Caucasian patients

Stroke

Occurrence of hemispheric and retinal ischemia in atrial fibrillation compared with carotid stenosis

Stroke

Glaucoma, capillaries and pericytes. 1. Blood flow regulation

Ophthalmologica

Glaucoma, capillaries and pericytes. 2. Identification and characterization of retinal pericytes in culture

Ophthalmologica

Comparison of intra-arterial thrombolysis with conventional treatment in patients with acute central retinal artery occlusion

J. Neurol. Neurosurg. Psychiatry

The pathology of cotton wool spots and cytoid bodies in hypertensive retinopathy and other diseases

Trans. Ophthalmol. Soc. U.K.

Experimental occlusion of retinal arterioles: using graded glass ballotini

Br. J. Ophthalmol.

Anticardiolipin IgG antibody and homocysteine as possible risk factors for retinal vascular occlusive disease in Thai patients

Jpn. J. Ophthalmol.

Retinal ischemia and embolism. Etiologies and outcomes based on a prospective study

Cerebrovasc. Dis.

Urticaria in idiopathic bilateral recurrent branch retinal arterial occlusion

Acta Ophthalmol. Scand.

Local intra-arterial fibrinolysis for acute occlusion of the central retinal artery: a meta-analysis of the published data

Br. J. Ophthalmol.

Recurrent retinal artery obstruction as a presenting symptom of ophthalmic artery aneurysm: a case report

Graefes Arch. Clin. Exp. Ophthalmol.

Recurrent branch retinal infarcts in association with migraine

Headache

Cilioretinal arteries and retinal arterial occlusion

Arch. Ophthalmol.

Selective intraarterial fibrinolysis of acute central retinal artery occlusion

Acta Radiol.

Dual trunk central retinal vein incidence in clinical practice

Arch. Ophthalmol.

Obstruction of the central artery of the retina

R. London Ophthalmic Hosp. Rep.

Pathology of obstruction of the central artery of the retina

R. London Ophthalmic Hosp. Rep.

Frequénce des vaisseaux ciliorétiniens, leur rapport avec les ametropies, leur association avec d’autres anomalies du fond de l’oeil

Bull. Soc. Fr. Dermatol. Syphiligr.