Eye (1991) 5, 226-238

Ophthalmologic Manifestations of Carotid Occlusive Disease

J. D. DUGAN, Jr. and W. R. GREEN Baltimore, Maryland, USA.

Summary Amaurosis fugax is perhaps the best known ocular symptom of carotid vascular disease. An understanding of the symptoms and an ability to recognise the character­ istic changes of hypotensive retinopathy and the ocular ischaemic syndrome should be familiar to ophthalmologists. In patients with known cerebrovascular disease a careful ophthalmologic examination should be per:formed to evaluate for the pres­ ence of ocular involvement related to emboli and hypoperfusion. Once identified a variety of non-invasive and invasive techniques may be employed to determine the degree of stenosis and an individual treatment plan initiated. Early recognition and treatment of patients with carotid occlusive disease may prevent more serious complications.

Stenosis and occlusion of the carotid arteries in 30% to 40% of patients with ipsilateral car­ are an important source of morbidity and otid atherosclerotic occlusive disease.1-7 At mortality despite current education about the the time of its initial description by Moore in hazards of cigarette smoking and elevated 1922,8 amaurosis fugax was thought to repre­ serum cholesterol levels. Patients with carotid sent benign angiospasm of the retinal vas­ artery disease may be seen by ophthal­ culature. It was not until 1952, when Fisher9 mologists during routine examination or reported on six patients with transient epi­ referred with symptoms related to ocular sodes of monocular blindness who later devel­ ischaemia. An understanding of the spectrum oped contralateral hemiplegia, that our of ocular manifestations and an ability to present understanding of the importance of recognise the ocular signs and symptoms ipsilateral carotid artery disease began. related to carotid occlusive disease is there­ Today, when a patient describes episodes of fore important. The manifestations of carotid monocular visual loss lasting between seconds insufficiency encompass a spectrum including to several minutes with return of normal vision frequently described as a 'curtain being transient episodes of monocular blindness raised' , carotid vascular disease leads the dif­ (amaurosis fugax), venous stasis retinopathy, ferential diagnosis. and the ocular ischaemic syndrome with If the retina is observed in patients with rubeosis irides and the development of neo­ these symptoms, one may frequently see vascular glaucoma. bright yellow or orange, irregular shaped Amaurosis Fugax cholesterol emboli at branch points in the ret­ Amaurosis fugax or transient blindness occurs inal arteries as initially described by Hollen-

From: The Eye Pathology Laboratory and Department of Pathology, the Johns Hopkins Medical Institutions, Baltimore, MD, USA.

Correspondence to: W. Richard Green, MD., Eye Pathology Laboratory, Johns Hopkins Hospital, 600 North Wolfe Street, Baltimore, Maryland 21205, USA. OPHTHALMOLOGIC MANIFESTATIONS OF CAROTID OCCLUSIVE DISEASE 227

horseD and confirmed histologically by David fugax in his left eye during the year before his and associates. II The appearance of these death was unremarkable by routine light emboli is sometimes facilitated by light digital microscopy. Trypsin digestion of the retina, pressure on the eye. Less frequently observed however, disclosed numerous capillary micro­ are grayish white platelet-fibrin emboli as anuerysms, loss of overall cellularity, and par­ described by Fisherl2 which can be seen pas­ ticular loss of pericytes in the equator and sing through the retinal vasculature during periphery (Fig. 1). episodes of visual loss. These emboli tend to Other causes of amaurosis fugax include cause transient occlusion and fragment at ret­ retinal migraine/o,21 postprandial systemic inal artery bifurcations. The source of both hypoperfusion,22 temporal arteritis,zl pseudo­ emboli are most frequently from ulcerative tumour cerebri,21 structural cardiac defects,23 plaques of the ipsilateral carotid artery. ophthalmic artery stenosis,24 ocular hyper­ Occasionally, larger yellowish white calcific tension,21 and hyperviscosity syndromes.25,26 emboli may be found within retina vessels, Rare cases have also been described as the most frequently at the disc margin, and should result of arteriovenous maiformations,27,28 suggest aortic valve disease as an aetiol­ intraorbital tumours/9 Moyamoya disease30 ogy.13,14 Another hypothesis, recently sug­ and spontaneous anterior chamber gested as an aetiology in certain patients with haemorrhage. 31 carotid stenosis implicates increased red cell aggregation, decreased red cell deformity and Venous Stasis Retinopathy subsequent increase in viscosity secondary to Although less frequent than acute embolic lowered velocity as a cause in some cases of events, carotid arterial disease may progress amaurosis fugax.15 to include characteristic posterior retinal An interesting form of amaurosis fugax changes due to relative hypoperfusion. In occurring after exposure to bright light has 1962, Hedges6 described retinal changes also been described in patients with carotid which included dilation of the retinal veins insufficiency. In 1979, Furlan et at. 16 described with or without a 'sausage shaped' appear­ five such patients with severe extracranial car­ ance and peripheral haemorrhages in associ­ otid disease. In one of these patients with ation with carotid occlusive disease. severe internal carotid occlusion, endarterec­ Impressed by the venous tortuosity and dila­ tomy was followed by subsequent resolution tion with mid peripheral retinal, dot-and-blot of his symptoms. Brigham et at. 17 reported on haemorrhages, superficial flame-shaped two patients with complete occulsion of the nerve fibre layer haemorrhages and micro­ ipsilateral carotid artery whose symptoms of aneurysms, Kearns and Hollenhorst,32 called bright light amaurosis fugax were relieved by the condition venous stasis retinopathy. This extensive endarterectomy of the distal com­ retinopathy is not due to outflow obstruction mon and the external carotid arteries. Jacobs as seen in central retinal vein occlusions et at. 18 reported the features of four patients (CRVO) but rather is the result of decreased with carotid disease who experienced positive arterial perfusion pressure and is more cor­ after images after bright light exposure. Don­ rectly termed hypotensive retinopathy. Hypo­ nan et at. 19 examined four patients with blur­ tensive retinopathy usually results from ring of vision on exposure to bright light using prolonged ischaemia and is most frequently visual evoked potentials and found decrease related to either total occlusion of the internal in the visual evoked response in six of eight carotid or stenosis of greater than 90% symptomatic eyes. All of these authors sug­ (Fig. 2).33 Kearns et al. found this retinopathy 5% gest that the increased metabolic demands of 'in of their patients with unilateral and the retina upon exposure to bright light is not 17% of their patients with bilateral carotid provided in these patients with compromised occulsion.32 ocular blood flow. While it is possible that venous stasis ret­ Histopathologic evaluation of an eye of a inopathy may be confused with the non­ patient with carotid occlusive disease and a ischaemic, incomplete form of central retinal history of numerous episodes of amaurosis vein occlusion (CRVO) and diabetic retino- 228 J. D. DUGAN, JR. AND W. R. GREEN

Fig la. Fig lb.

Fig Ie.

Fig. 1 A, retinal trypsin digest preparation discloses numerous capillary microanuerysms in periphery (arrow), B, Higher power view of peripheral area with microanuerysm (arrow) and overall reduced Fig. 2. Portion of the right internal carotid just distal cellularity, to the bifurcation shows severe atherosclerosis with C, Capillaries in posterior pole have a normal one·to· several smali lumens of recanalisation (arrowhead) anti one ratio of pericytes and endothelial celis, (Periodic one area of recent thrombosis (arrow) (hematoxylin· acid·Schiff: A, x12; Band C, x520), (From: eosin, x12), (From: Kahn M, Green WR, Knox DL, Michelson PE, Knox DL, Green WR, Ischaemic Miller NR: Ocular features of carotid occlusive disease, ocular inflammation, A Clinicopathologic case report. Retina 19 86 , 6: 239-52), Arch Optha11971, 86: 274-80. OPHTHALMOLOGIC MANIFESTATIONS OF CAROTID OCCLUSIVE DISEASE 229

Fig3a. Fig3b.

Fig. 3. A, Gross internal view of the left eye from a 69·year·old woman with hypotensive retinopathy shows multiple intraretinal haemorrhages and microaneurysms in the equatorial and mid·peripheral areas. B, Superficial mid-peripheral retinal haemorrhage (arrow) (hematoxylin-eosin, x 350). (From: Kahn M, Green WR, Knox DL, Miller NR: Ocular features of carotid occlusive disease. Retina 1986, 6: 239-252).

Fig4a. Fig4b.

Fig. 4. A, Retinal trypsin digestion preparation of same eye as in Figure 3 reveals numerous capillary microaneurysms in the periphery. Only rare pericytes are present and the endothelial cells appear to have migrated toward and proliferated with microaneurysms (arrows) (periodic acid-Schiff, xl OO). E, No microaneurysms are present in the posterior pole and there are an equal number of pericytes and endothelial cells (hematoxylin-eosin, periodic acid-Schiff:A, xlOO; B, x190). (From: Kahn M, Green WR, Knox DL, Miller NR: Ocular features of carotid occlusive disease. Retina 1986, 6: 239-252). 230 J. D. DUGAN, JR. AND W. R. GREEN pathy, a number of features should allow a ocular structures supplied by the ophthalmic correct diagnosis. The main clinical manifes­ artery. Anterior segment findings include: tation differentiating incomplete CRVO and dilated episcleral veins (Fig.5a); corneal the retinopathy of carotid disease is the low oedema; anterior chamber cells and flare; a retinal arterial pressure of the latter as mid-dilated and poorly reactive pupil; catar­ measured by ophthalmodynamometry or ocu­ actous changes and iris atrophy (Fig. 6); and lopneumoplethysmography.34 Indeed sponta­ rubeosis iridis with secondary neovascular neous or easily induced pulsation of the glaucoma.18 ,40-46 The posterior changes retinal artery may be seen. Similarly, the ret­ irtclude vascular dilatation and tortuosity, inal artery pressure is normal in patients with peripheral retinal haemorrhages and micro­ diabetic retinopathy. In addition, diabetic ret­ anuerysms (Fig. 5b) and cobblestone degen­ inopathy is usually bilateral and symmetric eration. The retinal changes are similar to with haemorrhages and microaneurysms those seen in hypotensive retinopathy and located throughout the fundus as compared represent a progression of this disease to with the predominantly mid-peripheral include ischaemic changes in both the inner location in carotid occlusive disease. Since and outer layers of the retina, narrowing of diabetic patients often have accelerated athe­ the retinal arterioles, choroidal perfusion rosclerotic vessel disease including involve­ defects, macular oedema and neovascularisa­ ment of the carotid arteries, marked tion of the disc and the retina in some asymmetry between the two eyes should sug­ instances.4,18,47-52 Intraocular pressure is gest ipsilateral carotid artery disease on the usually elevated in those patients with rubeo­ side with greater involvement.35 sis irides, but may be normal or decreased, Other conditions which may show similar reflecting decreased production of aqueous retinal changes as seen in the retinopathy of humour by an ischaemic ciliary body. That carotid occlusive disease include; Takayasu's this is indeed the case, is suggested by the ele­ disease36,37 the aortic arch syndromes ,38 hyper­ vation of pressure following surgical re-estab­ viscosity syndromes, haemoglobinopathy, lishment of orbital blood flow.32,53 The leukaemia, and conditions with elevations of presence of dull, aching orbital pain in the PC02 such as emphysema, extreme obes­ patients with normal intraocular pressure is ity and fibrocystic disease. the result of ischaemia and was identified in Histopathologic examination of eyes 5% of patients in one series.32 afflicted with hypotensive retinopathy The histopathologic study of eyes with the demonstrate characteristic features resulting ocular ischaemic syndrome have disclosed from prolonged ischaemic. These features involvement of nearly all ocular structures. include retinal haemorrhages and capillary The posterior segment findings may include mircoaneurysms (Fig. 3).39 The posterior pole outer retinal ischaemic atrophy as evidenced is usually without recognisable pathology. by the presence of extensive cobblestone The predominance of changes peripherally degeneration (Fig. 7) and wedge-shaped suggests that the observed changes are related areas of retinal pigment epithelial atrophy to a higher degree of ischaemia in these (Fig. 8), diffuse inner retinal ischaemic atro­ regions. Trypsin digest preparations demon­ phy (Figs. 9, 10), equatorial and mid-peri­ strate the numerous microaneurysms and loss pheral haemorrhages disc neovascularisation of pericytes compared to endothelial cells in and dense proteinaceous material in the vit­ the peripheral retina (Fig. 4). reous. Retinal trypsin digest preparations reveal marked capillary acellularity Ocular Ischaemic Syndrome (Fig. lOb). Microscopic examination of In certain cases with more severe chronic pan­ anterior segment discloses dense proteina­ ocular vascular compromise, the posterior ceous material in the anterior and posterior findings may progress to include anterior chambers, partial atrophy of the iris changes of the ocular ischaemia syndrome as (Fig. 11a), lflS neovascularisation first described by Knox.4O Panocular ischae­ (Fig. 11b, 12) and peripheral anterior syne­ mia may lead to pathologic changes in all chiae (Fig. 11b, 12a), partial atrophy of the OPHTHALMOLOGIC MANIFESTATIONS OF CAROTID OCCLUSIVE DISEASE 231

Fig. Sa Fig. 5b

Fig. 5. A, External appearance with episcleral vascular congestion of the right eye of a 69 -year-old man with the ischaemic ocular inflammatory syndrome at initial presentation. B, Ophthalmoloscopic appearance of peripheral retinal haemorrhages, microanuerysms and venous congestion. (From: Michelson PE, Knox DL, Green WR. lschaemic ocular inflammation.A Clinicopathologic case report. Arch Ophthalmol 197 1, 86: 27�O).

Fig. 6. Appearance four months later of the same patient as illustrated in Figure 5, shows the evolution to a mature cataract, partial iris atrophy and rubeosis irides. (From: Michelson PE, Knox DL, Green WR. Ischaemic ocular inflammation. A Clinicopathologic case report. Arch Opthalmol1971, 86: 27�O). 232 J. D. DUGAN, JR. AND W. R. GREEN

Fig.7a. Fig.7b.

Fig.7. A, Gross appearance of extensive cobblestone degeneration extending to the mid-periphery in an eye of a 53-year-old man with the ocular ischaemic syndrome. B, Margin of cobblestone lesion (left of arrow) with loss of the retinal pigment epithelium and outer retinal layers up to and including the outer aspect of the inner nuclear layer. (Haematoxylin and eosin x185) (From: Michelson PE, Knox DL, Green WR. Ischaemic ocular inflammation. A clinicopathologic case report. Arch Ophthalmol1971, S6: 27�O).

Fig. Sa. Fig. Sb.

Fig. S. A, Gross appearance of extensive peripheral outer retinal ischaemic atrophy in eye of a 53-year-old mall with carotid occlusive disease and ocular ischaemic changes. B, In some areas the atrophy has a wedge-shaped configuration. (From: Kahn M, Green WR, Knox DL, Miller NR: Ocular features of carotid occlusive disease. Retina 1986, 6: 239-52). OPHTHALMOLOGIC MANIFESTATIONS OF CAROTID OCCLUSIVE DISEASE 233

Fig. 9a. Fig. 9b.

Fig. 9. Microscopic examination from the patient in Figure 8. A, Inner retinal ischaemic atrophy in the macular area (haematoxylin·eosin, x210). B, Mid·peripheral area shows inner retinal and partial outer retina ischaemic atrophy (periodic acid-Schiff, x 300). C, Equatorial retina is reduced to a thin nearly acellular strand (between arrowheads) in an area of inner and outer retinal ischaemic atrophy (periodic acid·Schiff, x 300). (From Kahn M, Green WR, Knox DL, Miller NR: Ocular features of carotid occlusive disease. Retina Fig. 9c. 1986, 6: 239- 252).

ciliary body (Fig. 12c), and cataractous cant flow obstruction as indicated by delay in changes.39,52 appearance of dye in the choroidal and retinal The progression from hypotensive retino­ circulation as well as indicating structural pathy to the ocular ischaemic syndrome may, abnormalities of the ocular vasculature. in part, be mediated by the release of angio­ When bilateral simultaneous fluorescein genic factors from ischaemic retina. These angiography is performed, delayed or dispar­ factors are thought to be responsible for the ate arm to retina circulation time as well as neovascularisation of the posterior pole and delayed ciliary circulation at the disc were diffusion of these substances to the anterior found to correlate with carotid occlusion.55 segment lead to the development of iris neo­ Fluorescein angiographic features in patients vascularisation and secondary glaucoma. with carotid occlusive disease include: patchy, delay.ed, irregular choroidal filling; areas of Fluorescein Angiography retinal non-perfusion; microaneurysms and Sarkies et al.54 using fluorescein angiography venous beading; diffuse late leakage from ret­ to evaluate patients with carotid occlusion or inal vessels; leakage at arterial bifurcations stenosis, found abnormalities in 67% of cases. suggesting emboli damage; and leakage from - The test can be used to demonstrate signifi- retinal neovascularisation. 4,18,48,54 59 234 J. D. DUGAN. JR. AND W. R. GREEN

..

Fig. l0. Ocular ischaemic syndrome. A, Mid-peripheral retina with inner retinal ischaemic atrophy with loss of the mner retmal layers down to the inner portion of the inner nuclear layer. Capillaris (arrows) are acellular. (Periodic acid-Schiff, x525). B, Trypsin digest preparation discloses only occasional pericytes (periodic acid. Schiff, x160). (From Kahn M, Green WR, Knox DL. Miller NR: Ocular features of carotid occlusive disease. Retina 1986, 6: 239-52).

'.. ...

A

Fig. 11. Anterior segment changes in the ocular ischaemic syndrome. A, Pupillary portion of iris disclosed partial ischaemic necrosis with loss of the pigment epithelium and dilator muscle and partial acellulariiy of the stroma. Only a small portion of the sphincter muscle (arrow) remains. B, The angle is closed by peripheral anterior synechia and new blood vessels (asterisk) are present on the anterior surface of the iris. Endothelium (arrowheads) with basement membrane extends across the false angle and onto the anterior surface of the iris. (Haematoxylin and eosin: A and B. x 17 0). (From: Michelson PE. Knox DL, Green WR: lschaemic ocular inflammation.A Clinicopathogic case report. Arch OphthalmoI 19 71,86: 274-80). OPHTHALMOLOGIC MANIFESTATIONS OF CAROTID OCCLUSIVE DISEASE 235

Fig. 12a. Fig. 12b.

Fig. 12. A, Area shows temporal peripheral anterior synechia with new vessels (asterisk) on the anterior surface of the iris and partial iris atrophy with dispersion of free pigment and pigmented macrophages (arrow) (periodic acid-Schiff, xJ80). B, Nasal iris leaflet showsperipheral anterior synechia with endothelialisation and descemetisation of the false angle and anterior surface of the iris (arrows), rubeosis iridis (asterisk), and pigmented macrophages in the anterior chamber (periodic acid-Schiff, x 300). C, Microscopic view reveals partial atrophy of the ciliary body with loss of the non-pigmented epithelium (arrow) and rounding up of pigment (asterisk) (hematoxylin-eosin, x 120). (From: Kahn M, Green WR, Knox DL, Miller NR: Ocular features of carotid occlusive disease. Retina 1986, 6: 239- 52).

Diagnostic Evaluation recently, intra-arterial digital subtraction Evaluation of patients with suspected occlu­ angiography has replaced conventional sion or stenosis of the carotid arteries includes angiography in the assessment of patients in a variety of invasive and non-invasive tests. many institutions. While angiography is The 'gold standard' for evaluation of the car­ usually performed in most patients preparing ptid arteries has historically been selective for surgical intervention, it is associated with a 60 mtra-arterial carotid angiography. More small but definite morbidity and mortality. A 236 J. D. DUGAN, JR. AND W. R. GREEN

number of non-invasive techniques, there­ and disc neovascularisation after carotid fore, are usually used in initial diagnostic eval­ endarterectomy. Resolution of hypotensive uations and for screening purposes. retinopathy was also reported by Kearns et Assessment of orbital blood flowto indicate ai.71 in one case following ST-MCA bypass more proximal stenosis of the cervical vas­ and resulted in 'some decrease in retinopathy' 13 culature is accomplished with opthalmo­ in patients following carotid bypass sur­ dynamometry, oculophlethysmography, ocu­ gery?2 Edwards et ai. reported72 one patient lopneumoplethysmography, and periorbital with the ocular ischaemic syndrome whose Doppler ultrasound. The sensitivity and ophthalmic disease reversed following ST­ specificityof these tests have been reported by MCA bypass. On the other hand, Sarkies et several authors.61-65 These tests are capable of al.56 demonstrated improved microcirculation indicating stenosis and a reduction of orbital in four patients treated with endarterectomy perfusion, but give no information regarding alone in one patient treated with endarterec­ the anatomic location of the responsible tomy and extracranial-intracranial bypass but lesion. Another shortcoming of these tests is saw no improvement in two patients after their inability to detect ulcerative lesions of extracranial-intracranial bypass alone or in the carotid arteries which may be responsible three patients managed medically. Iris neo­ vascularisation resolved and neovascular for significant morbidity, and for this reason glaucoma was prevented in one patient their use as screening tests are limited. treated by goniophotocoagulation and carotid Duplex ultrasonography, on the other endarterectomy.73 Indeed regression of neo­ hand, provides both an anatomical picture of vascular glaucoma has been observed follow­ the carotid arteries and a pulse Doppler signal ing intracranial-extracranial bypass74 as well at selected points within the displayed seg­ as in three cases treated with peripheral ment. This allows visualisation of possible cryoablation, cyclocryotherapy of the ciliary ulcerative plaques as well as an indication of body and cerebrovascular surgery.58,75 More the haemodynamic consequences of a stenotic recently Johnston et al. 57 used a multidisci­ region based on quantificationof peak systolic plinary approach involving pametinal photo­ and end diastolic velocity. Duplex sonography coagulation or cryoablation and cerebro­ is therefore an excellent screening and diag­ vascular surgery in combination with nostic tool and has been advocated as a highly anti-platelet therapy on thirteen eyes with accurate technique in evaluation of patients stabilisation of vision and regression of neo­ with carotid occlusive disease.66,67 vascularisation in all but one patient. Ocular ischaemic pain has also lessened following , ,76 Treatment extracranial-intracranial bypass.32 69 The indicat�.::ms for surgical intervention for Despite the foregoing reports, the decision carotid occlusive disease is a matter of debate for surgical intervention is not without associ­ at present, but it is clearly a multifactorial ated morbidity and mortality and the decision decision based on the patients operative risk to proceed is based on an individual approach and symptomatology. Ophthalmological to each patient. In a prospective series of 252 intervention, in the form of pametinal photo­ consecutive patients who underwent 282 car­ coagulation, has been reported to result in otid endarterectomies, Sundt et al. 77 noted a regression of iris neovascularisation and, one per cent operative minor morbidity, a when performed prior to closure of the angle, 0.7% mortality, asymptomatic restenosis in may help prevent the development of neovas­ 10% and severe stenosis or occlusion in 3%. cular glaucoma.57,68,69 In those patients with Actuarial analysis indicated that the cumula­ ocular manifestations of carotid occlusive tive probability of ipsilateral stroke, transient disease who have undergone carotid endarte­ ischaemic attack, or reversible ischaemic neu­ 4% 8% rectomy or superficial temporal artery to rologic deficitwas at one month and at middle cerebral artery (ST-MCA) bypass, five years.77 improvement of their ophthalmic disease has Key words: Amaurosis fugax, Atherosclerosis, Car­ , been reported.32 7O-72 Neupert et ai.70 demon­ otid occlusive disease, Ocular ischaemic syndrome, strated resolution of hypotensive retinopathy Venous stasis retinopathy. OPHTHALMOLOGIC MANIFESTATIONS OF CAROTID OCCLUSIVE DISEASE 237

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