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Clinical-Angiographic Correlations in Amaurosis Fugax
CLINICAL-ANGIOGRAPHIC CORRELATIONS AMAUROSIS FUGAX B U R T O N A.
S A N D O K , M.D., L A S S E P A S , M.D., O.
J A M E S C. T R A U T M A N N , M.D., T H O R A L F M.
MANUEL RAMIREZ-
S U N D T , J R . , M.D.,
W A Y N E HOUSER,
IN
AND
M.D.
Rochester. Minnesota Amaurosis fugax is a term that has been used to describe various periodic recurrent episodes of loss of vision. 1 I n 1952, Fisher 2 denned it more specifically as "periodic blind ness in which the principal derangement is an interruption of the retinal blood flow, usually of one eye only." Typically, this more restricted unilateral visual loss is de scribed by patients as a dark curtain coming across the vision of one eye, slowly closing in from the outside, or down from above, or in the reverse directions. Complete blindness follows in a matter of seconds, and the eye generally remains blind for one to ten min utes. T h e vision then returns to normal, often by a reverse sequence. T h e term "amaurosis fugax" should be re served for this type of visual loss, even though it literally means "fleeting blindness" and might be applied to transient blindness of diverse cause. Differentiated from amau rosis fugax would be unilateral or bilateral transient homonymous hemianopia, visual obscurations associated with chronic papilledema, and various nondescript momentary episodes of unilateral or bilateral blindness that are of functional origin. Restricting the term "amaurosis fugax" in this way makes it possible to identify a pathophysiologic mechanism for this type of transient blind ness. From the Clinical Cerebrovascular Research Center (Dr. Ramirez-Lassepas), and the Depart ments of Neurology (Dr. Sandok), Ophthalmology (Dr. Trautmann), Neurosurgery (Dr. Sundt), and Diagnostic Roentgenology (Dr. Houser), Mayo Clinic and Mayo Foundation, Rochester, Minnesota. This study was supported in part by Public Health Service research grant NS-6663 from the National Institutes of Health. Reprint requests to Burton A. Sandok, M.D., Clinical Cerebrovascular Research Center, Mayo Clinic, Rochester, MN 55901.
Amaurosis fugax is an important symp tom in patients with occlusive disease of the extracranial portion of the carotid artery. 3 ' 1 T h e risk in patients with recurrent episodes of amaurosis fugax of developing permanent visual loss is not fully known. Fisher 2 re corded permanent residual loss of vision in 4 2 % of 138 cases he collected from the lit e r a t u r e ; however, our clinical experience with this symptom suggests that the actual incidence of permanent visual loss is sub stantially lower. I n contrast, however, Fisher emphasized that amaurosis fugax may pre cede the development of a contralateral hemiplegia due to a thrombotic process of the internal carotid artery ("as a sort of warn ing that disaster threatened"). 2 O u r clinical experience is in accord with his observations and suggests that there is an appreciable risk of subsequent permanent cerebral ischemic events when amaurosis fugax occurs in asso ciation with other transient cerebral isch emic attacks, carotid bruit, reduced retinal artery pressures, or retinal embolic phe nomena such as cholesterol emboli, arteriole occlusion, or venous stasis retinopathy. Some of these patients may have surgically cor rectable stenotic lesions of the carotid artery and may benefit from further neurovascular investigative studies in an effort to define the extent of the responsible lesion. Patients with either normal or totally occluded in ternal carotid arteries probably benefit little from such procedures, 5 and endarterectomy is not generally performed in these situa tions.
137
A group of patients with amaurosis fugax as one of their symptoms was studied by cerebral angiography to determine whether there was any clinical-angiographic correla tion and whether the severity of disease in
138
AMERICAN JOURNAL OF OPHTHALMOLOGY
the ipsilateral carotid artery could be pre dicted on the basis of clinical findings.
JULY, 1974
The clinical records of all patients who had cerebral angiography in the 25-month period from January 1970 through February 1972 were reviewed (1,080 patients). This represents the same group of patients re viewed in an earlier report.6 Selected from this large group were 43 patients who met the following criteria: (1) 50 years old or older; (2) symptoms of unilateral amau rosis fugax, with or without additional symptoms or signs of ischemic disease re ferable to the ipsilateral carotid system; (3) neuro-ophthalmic examination with particu lar attention to retinal artery pressures and ophthalmoscopic observation for the pres ence of retinal emboli or evidence of isch emic retinopathy; and (4) neurovascular ex amination with particular attention to a history of cerebral transient ischemic symp toms or signs of residual neurologic deficit and presence or absence of carotid bruits.
therefore we included an additional 16 pa tients who had permanent neurologic deficits as well as amaurosis fugax (Table 1). The study group is a select group of pa tients with amaurosis fugax who were of an age in which atheromatous disease of the carotid arteries was likely and in whom carot id angiography was performed. Many other patients were seen during the period covered by the study who probably met the criteria for selection but in whom carotid angiogra phy was not performed. No patient was in cluded who had amaurosis fugax without other symptoms or signs of cerebral ischemic attacks or signs on neurovascular examina tion of a carotid bruit, reduced retinal ar tery pressure, retinal emboli, or ischemic retinopathy. Thus, the group reflects the clinical bias of our practice during the 25month period. During that interval, carotid angiography was not performed on a pa tient if amaurosis fugax was the only symp tom and no other evidence of carotid occlusive disease was found on the neuro-ophthal mic or neurovascular examination.
The patients included in this study, there fore, differ from those in the earlier report. The previous report dealt only with patients who experienced transient episodes of uni lateral carotid system ischemic disease and included patients with cerebral transient ischemic attacks as well as 27 patients with amaurosis fugax. In the present report, we studied amaurosis fugax specifically, and
From the cerebral angiograms, the extracranial portion of the carotid artery was analyzed and classified into three groups: (1) normal—no evidence of disease in the extracranial portion of the carotid artery; (2) stenosis—evidence of disease and nar rowing of either the common carotid or the extracranial (or both) portion of the in ternal carotid artery, with or without ulcera-
MATERIAL AND METHODS
TABLE 1 COMPARISON OF SYMPTOMS WITH ANGIOGRAPHIC ABNORMALITY OF IPSILATERAL CAROTID ARTERY IN 4 3 PATIENTS WITH AMAUROSIS FUGAX
Ipsilateral Carotid Findings Symptoms Amaurosis fugax (AF) AF, transient cerebral ischemic attacks AF, stroke AF, transient cerebral ischemic attacks, stroke
Total
Normal
Stenosis
Occlusion
1 0 0 0
13 7 3 7
2 4 3 3
16 11 6 10
30
12
43
139
AMAUROSIS FUGAX
VOL. 79, NO 1
tion; and (3) occlusion—total occlusion of the extracranial portion of the internal carot id artery. The angiographic findings were then cor related with the symptoms given by the patients as well as with the clinical findings observed on the neurovascular and ophthalmoscopic examinations. A well-localized bruit of any intensity in the region of the carotid bifurcation, below the angle of the jaw, was regarded as significant. A differ ence of 10% in the retinal artery pressures of the two eyes was considered significant and reported as a decrease in retinal artery pressure. Cholesterol emboli, platelet-fibrin emboli, venous stasis retinopathy, and ar terial occlusions of the retina were con sidered embolic events. RESULTS
Only one patient had a normal carotid artery on the side ipsilateral to the symptoms or clinical findings; the remaining 42 pa tients either had stenosis (30 patients) or total occlusion (12 patients) of the ipsilateral common carotid or extracranial (or both) portion of the internal carotid artery. Thirty-seven of the 43 patients had arteriographic procedures in which both carotid arteries were visualized (Table 2 ) . Thirteen patients had a normal carotid artery on the side opposite the site of symptoms and clini cal findings. Importantly, 24 of these pa tients had evidence of occlusive disease of the contralateral carotid artery even though it produced no apparent ill effects.
Patients with amaurosis fugax in associa tion with either transient or permanent cerebral symptoms (transient ischemic at tacks or stroke) had a greater incidence of ipsilateral carotid arterial disease than did patients whose only symptom was amaurosis fugax. Five patients had no clinical findings of carotid occlusive disease on examination, but these five had other symptoms of cerebrovascular disease in addition to amaurosis fugax (Table 3). Four of the five patients had stenosis of the common carotid or extra cranial (or both) portion of the internal carotid artery, and one patient had a total occlusion of the extracranial portion of the carotid artery. Carotid bruits were documented in 31 patients, reduced retinal artery pressure in 30 patients, and retinal embolic events in 18 patients. Most of the patients (72%), how ever, had more than one clinical finding in dicative of carotid occlusive disease in addi tion to their symptoms. Fourteen patients had a combination of a carotid bruit and reduced retinal artery pressure, and an addi tional 12 patients had a carotid bruit and reduced retinal artery pressure, in addition to evidence of retinal embolic events. One patient with amaurosis fugax alone, on ex amination, had reduced retinal artery pres sure, retinal emboli, and a carotid bruit al though the carotid artery was radiographically normal. In this series, no single finding or com bination of findings allowed accurate predic-
TABLE 2 COMPARISON OF ANGIOGRAPHIC ABNORMALITY OF THE SYMPTOMATIC (IPSILATERAL) VESSEL WITH THAT I N THE CONTRALATERAL VESSEL
Carotid Vascular Findings Normal
Ipsilateral Contralateral
Stenosis
Occlusion
Total
No.
%
No.
%
No.
%
1 13
2 35
30 22
70 60
12 2
28 5
43 37
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AMERICAN JOURNAL OF OPHTHALMOLOGY
J U L Y , 197A
TABLE 3 COMPARISON OF CLINICAL FINDINGS WITH ANGIOGRAPHIC ABNORMALITY OF IPSILATERAL CAROTID ARTERY IN 4 3 PATIENTS WITH AMAUROSIS FUGAX
Ipsilateral Carotid Abnormality Findings None Reduced RAP* alone Emboli alone Bruit alone Reduced RAP and emboli Reduced RAP and bruit Emboli and bruit Reduced RAP, emboli, and bruit Total
Total
Normal
Stenosis
0 0 0 0 0 0 0 1
4 1 2 1 2 13 2 5
1 1 1 1 0 1 1 6
5 2 3 2 2 14 3 12
1
30
12
43
Occlusion
* Retinal artery pressure.
tion of the degree of patency of the ipsi lateral carotid artery, and a distinction be tween ipsilateral carotid stenosis and occlu sion could not be made on the basis of the clinical examination. DISCUSSION 2
Fisher has classified the presumed cause of amaurosis fugax into seven groups: (1) cases in the older age group in which athero sclerosis was probably a factor; (2) cases in the younger age group without apparent cause; (3) cases associated with migraine; (4) cases associated with Raynaud's syn drome ; (5) cases associated with heart dis ease; (6) cases of reflex amaurosis; and (7) miscellaneous cases. The cause and prognosis of amaurosis fugax encountered in younger patients, es pecially those without associated evidence of cerebrovascular disease, are not known. However, the condition may run an appar ently benign course and need not be due to retinal embolism from thrombosis in the ipsilateral internal carotid artery, as sug gested by Eadie, Sutherland, and Tyrer 7 in their report on 12 patients whose ages ranged from 14 to 51 years (mean 29.5 years). Reflection on our clinical experience in an older group of patients (50 years old or older) suggests that, except for the occa
sional patient with amaurosis fugax as a part of the syndrome of cranial arteritis, 8 most cases of amaurosis fugax (as sug gested in 1951 by Behrman 9 ) are related to carotid occlusive disease. Localized bruits, suggesting turbulent blood flow, were heard over the carotid bi furcation in 72% of our patients. In most instances, the bruit arises from the internal carotid artery and suggests stenotic patency of that vessel. Our case material suggests that a carotid bifurcation bruit can be ob served even though total occlusion of the internal carotid artery is present; and in this situation, the bruit likely arises from the ex ternal carotid. The presence of a carotid bruit, therefore, does not invariably imply internal carotid artery patency, and similarly its absence in these patients cannot be used" as invariable evidence of occlusion. Ipsilateral reduction in retinal artery pres sure was noted in 70% of our patients. A reduced retinal artery pressure was seldom found in the absence of severe narrowing or total occlusion of the ipsilateral carotid artery, and this may be interpreted as sug gesting the presence of a lesion capable of reducing distal carotid-ophthalmic artery blood flow. Whether the symptom of amaurosis fugax arises solely because of a total reduction in
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AMAUROSIS FUGAX
ophthalmic artery blood flow is not clear; this may happen in some patients. Angiographic visualization of ulceration within the carotid artery is difficult10'11 but was noted in approximately 50% of our patients in the present study. At surgery, ulcer craters in the atheromatous tissue removed during carotid endarterectomy were noted in most patients with significant stenosis, even though they were not suspected from the angiographic study; this would suggest a possible microembolic origin for amaurosis fugax in many patients. The high incidence of retinal embolic events noted in this group of patients (42%) tends to support this theory. Atheromatous ulcerative stenosis and oc clusion of the extracranial carotid artery probably are the principal pathologic condi tions responsible for the amaurosis fugax encountered in an elderly population. It is these same pathologic conditions that have been postulated12 and shown13'14 to be re sponsible for most cerebral transient isch emic attacks involving the carotid system. Approximately one third of patients with cerebral transient ischemic attacks, if un treated, will develop a cerebral infarct.15 Although the precise incidence of patients with amaurosis fugax who will experience cerebral ischemic episodes is not known, amaurosis fugax is associated with a greater incidence and degree of atheromatous extra cranial carotid arterial disease than perhaps are seen in transient cerebral ischemic at tacks alone.6 Patients with symptomatic uni lateral atheromatous stenosis of the ipsilateral carotid artery probably benefit from carotid arterial surgery 5,16 ; patients with complete occlusion of the ipsilateral carotid artery are not generally considered suitable candidates for such surgery. The distinction between carotid arterial stenosis and occlu sion cannot be made with certainty on the basis of the clinical findings. We believe that proximal stenotic lesions of the extracranial carotid artery associated with microembolization and symptoms of
141
retinal ischemia may carry an increased risk of subsequent cerebral ischemic events. We therefore recommend that patients with amaurosis fugax, especially if it is associated with other transient or permanent cerebral symptoms or signs, ipsilateral carotid bruit, reduced retinal artery pressure, or evidence of retinal embolic events, who are otherwise suitable surgical candidates, should undergo cervical-cranial angiography to delineate the nature and extent of the responsible lesion. Since evidence suggests that the risk of cere bral infarction is greatest during the first several weeks after an episode of transient ischemia,15 the management of such patients is an emergent one. Currently, we hospitalize such patients and, if no contraindications exist, begin anticoagulant therapy with heparin, which has been shown to improve sig nificantly the prognosis in patients with symptomatic carotid atheromatous disease.17 At the earliest moment after complete medi cal, neurologic, and ophthalmic evaluations, angiography is performed and definitive therapy is planned on the basis of the clinical-angiographic findings. SUMMARY
Of 1,080 patients studied by carotid an giography, 43 experienced unilateral amau rosis fugax. Of these 43 patients, 42 had significant occlusive disease of the ipsilateral common carotid or extracranial (or both) portion of the internal carotid artery; 12 (28%) had complete occlusion, and 30 (70%) had significant stenosis. Amaurosis fugax is a significant symptom of carotid occlusive disease affecting the extracranial portion of the carotid artery when it occurs in patients 50 years old or older in associa tion with either transient or permanent cerebral symptoms or signs, carotid bruit, reduced retinal artery pressures, or retinal embolic signs. Microembolization from an atheromatous plaque within this vessel is postulated as the pathophysiologic mecha nism for amaurosis fugax in most of these patients.
142
AMERICAN JOURNAL OF OPHTHALMOLOGY REFERENCES
1. Wagener, H. P . : Amaurosis fugax. Am. J. Med. Sci. 224:229, 1952. 2. Fisher, M.: Transient monocular blindness associated with hemiplegia. Arch. Ophthalmol. 47: 167, 1952. 3. Hollenhorst, R. W . : Ocular manifestations of insufficiency or thrombosis of the internal carotid artery. Am. J. Ophthalmol. 47:753, 1959. 4. Fisher, M.: Occlusion of the internal carotid artery. Arch. Neurol. Psychiatry 65 :346, 1951. 5. Fields, W. S., Maslenikov, V., Meyer, J. S., Hass, W. K., Remington, R. D., and Macdonald, M.: Joint study of extracranial arterial occlusion. 5. Progress report of prognosis following surgery or nonsurgical treatment for transient cerebral ischemic attacks and cervical carotid artery lessons. T.A.M.A. 211:1993,1970. 6. Ramirez-Lassepas, M., Sandok, B. A., and Burton, R. C.: Clinical indicators of extracranial Carotid artery disease in patients with transient symp toms. Stroke 4:537, 1973. 7. Eadie, M. J., Sutherland, J. M., and Tyrer, J. H . : Recurrent monocular blindness of uncertain cause. Lancet 1:319, 1968. 8. Hollenhorst, R. W., Brown, J. R., Wagener, H. P., and Shick, R. M.: Neurologic aspects of temporal arteritis. Neurology 10:490, 1960. 9. Behrman, S.: Amaurosis fugax et amaurosis fulminans. Arch. Ophthalmol. 45 :458, 1951. 10. Gomensoro, J. B., Maslenikov, V., Azambuja, N., Fields, W. S., and Lemak, N. A.: Joint study
J U L Y , 1974
of extracranial arterial occlusion. 8. Clinicalradiographic correlation of carotid bifurcation lesions in 177 patients with transient cerebral ischemic attacks. J.A.M.A. 224:985, 1973. 11. Gomensoro, J. B., Maslenikov, V., De Boni, J. A., Laguardia de Perez, G., Purriel, J., Medoc, J., Rodriguez Barrios, R., Abo, J. C , Tenyi, A., and Azambuja, N . : Ulcerated atheromatous plaques of the carotid artery bifurcation. Stroke 4:912, 1973. 12. Millikan, C. H., and Siekert, R. G.: Studies in cerebrovascular disease. 4. The syndrome of inter mittent insufficiency of the carotid arterial system. Mayo Clin. Proc. 30 :186, 1955. 13. Drake, W. E., Jr., and Drake, M. A. L . : Clinical and angiographic correlates of cerebro vascular insufficiency. Am. J. Med. 45 :253, 1968. 14. David, T. E., Humphries, A- W., Young, J. R., and Beven, E. G.: A correlation of neck bruits and arteriosclerotic carotid arteries. Arch. Surg. 107: 729, 1973. 15. Whisnant, J. P., Matsumoto, N., and Elveback, L. R.: Transient cerebral ischemic attacks in a community: Rochester, Minnesota, 1955 through 1969. Mayo Clin. Proc. 48:194, 1973. 16. Murphey, F., and Maccubbin, D. A . : Carotid endarterecfomy. A long-term follow-up study. J. Neurosurg. 23:156, 1965. 17. Millikan, C. H., Siekert, R. G., and Shick, R. M.: Studies in cerebrovascular disease. 5. The use of anticoagulant drugs in the treatment of inter mittent insufficiency of the internal carotid arterial system. Mayo Clin. Proc. 30:578, 1955.
S A N D O K , M.D., L A S S E P A S , M.D., O.
J A M E S C. T R A U T M A N N , M.D., T H O R A L F M.
MANUEL RAMIREZ-
S U N D T , J R . , M.D.,
W A Y N E HOUSER,
IN
AND
M.D.
Rochester. Minnesota Amaurosis fugax is a term that has been used to describe various periodic recurrent episodes of loss of vision. 1 I n 1952, Fisher 2 denned it more specifically as "periodic blind ness in which the principal derangement is an interruption of the retinal blood flow, usually of one eye only." Typically, this more restricted unilateral visual loss is de scribed by patients as a dark curtain coming across the vision of one eye, slowly closing in from the outside, or down from above, or in the reverse directions. Complete blindness follows in a matter of seconds, and the eye generally remains blind for one to ten min utes. T h e vision then returns to normal, often by a reverse sequence. T h e term "amaurosis fugax" should be re served for this type of visual loss, even though it literally means "fleeting blindness" and might be applied to transient blindness of diverse cause. Differentiated from amau rosis fugax would be unilateral or bilateral transient homonymous hemianopia, visual obscurations associated with chronic papilledema, and various nondescript momentary episodes of unilateral or bilateral blindness that are of functional origin. Restricting the term "amaurosis fugax" in this way makes it possible to identify a pathophysiologic mechanism for this type of transient blind ness. From the Clinical Cerebrovascular Research Center (Dr. Ramirez-Lassepas), and the Depart ments of Neurology (Dr. Sandok), Ophthalmology (Dr. Trautmann), Neurosurgery (Dr. Sundt), and Diagnostic Roentgenology (Dr. Houser), Mayo Clinic and Mayo Foundation, Rochester, Minnesota. This study was supported in part by Public Health Service research grant NS-6663 from the National Institutes of Health. Reprint requests to Burton A. Sandok, M.D., Clinical Cerebrovascular Research Center, Mayo Clinic, Rochester, MN 55901.
Amaurosis fugax is an important symp tom in patients with occlusive disease of the extracranial portion of the carotid artery. 3 ' 1 T h e risk in patients with recurrent episodes of amaurosis fugax of developing permanent visual loss is not fully known. Fisher 2 re corded permanent residual loss of vision in 4 2 % of 138 cases he collected from the lit e r a t u r e ; however, our clinical experience with this symptom suggests that the actual incidence of permanent visual loss is sub stantially lower. I n contrast, however, Fisher emphasized that amaurosis fugax may pre cede the development of a contralateral hemiplegia due to a thrombotic process of the internal carotid artery ("as a sort of warn ing that disaster threatened"). 2 O u r clinical experience is in accord with his observations and suggests that there is an appreciable risk of subsequent permanent cerebral ischemic events when amaurosis fugax occurs in asso ciation with other transient cerebral isch emic attacks, carotid bruit, reduced retinal artery pressures, or retinal embolic phe nomena such as cholesterol emboli, arteriole occlusion, or venous stasis retinopathy. Some of these patients may have surgically cor rectable stenotic lesions of the carotid artery and may benefit from further neurovascular investigative studies in an effort to define the extent of the responsible lesion. Patients with either normal or totally occluded in ternal carotid arteries probably benefit little from such procedures, 5 and endarterectomy is not generally performed in these situa tions.
137
A group of patients with amaurosis fugax as one of their symptoms was studied by cerebral angiography to determine whether there was any clinical-angiographic correla tion and whether the severity of disease in
138
AMERICAN JOURNAL OF OPHTHALMOLOGY
the ipsilateral carotid artery could be pre dicted on the basis of clinical findings.
JULY, 1974
The clinical records of all patients who had cerebral angiography in the 25-month period from January 1970 through February 1972 were reviewed (1,080 patients). This represents the same group of patients re viewed in an earlier report.6 Selected from this large group were 43 patients who met the following criteria: (1) 50 years old or older; (2) symptoms of unilateral amau rosis fugax, with or without additional symptoms or signs of ischemic disease re ferable to the ipsilateral carotid system; (3) neuro-ophthalmic examination with particu lar attention to retinal artery pressures and ophthalmoscopic observation for the pres ence of retinal emboli or evidence of isch emic retinopathy; and (4) neurovascular ex amination with particular attention to a history of cerebral transient ischemic symp toms or signs of residual neurologic deficit and presence or absence of carotid bruits.
therefore we included an additional 16 pa tients who had permanent neurologic deficits as well as amaurosis fugax (Table 1). The study group is a select group of pa tients with amaurosis fugax who were of an age in which atheromatous disease of the carotid arteries was likely and in whom carot id angiography was performed. Many other patients were seen during the period covered by the study who probably met the criteria for selection but in whom carotid angiogra phy was not performed. No patient was in cluded who had amaurosis fugax without other symptoms or signs of cerebral ischemic attacks or signs on neurovascular examina tion of a carotid bruit, reduced retinal ar tery pressure, retinal emboli, or ischemic retinopathy. Thus, the group reflects the clinical bias of our practice during the 25month period. During that interval, carotid angiography was not performed on a pa tient if amaurosis fugax was the only symp tom and no other evidence of carotid occlusive disease was found on the neuro-ophthal mic or neurovascular examination.
The patients included in this study, there fore, differ from those in the earlier report. The previous report dealt only with patients who experienced transient episodes of uni lateral carotid system ischemic disease and included patients with cerebral transient ischemic attacks as well as 27 patients with amaurosis fugax. In the present report, we studied amaurosis fugax specifically, and
From the cerebral angiograms, the extracranial portion of the carotid artery was analyzed and classified into three groups: (1) normal—no evidence of disease in the extracranial portion of the carotid artery; (2) stenosis—evidence of disease and nar rowing of either the common carotid or the extracranial (or both) portion of the in ternal carotid artery, with or without ulcera-
MATERIAL AND METHODS
TABLE 1 COMPARISON OF SYMPTOMS WITH ANGIOGRAPHIC ABNORMALITY OF IPSILATERAL CAROTID ARTERY IN 4 3 PATIENTS WITH AMAUROSIS FUGAX
Ipsilateral Carotid Findings Symptoms Amaurosis fugax (AF) AF, transient cerebral ischemic attacks AF, stroke AF, transient cerebral ischemic attacks, stroke
Total
Normal
Stenosis
Occlusion
1 0 0 0
13 7 3 7
2 4 3 3
16 11 6 10
30
12
43
139
AMAUROSIS FUGAX
VOL. 79, NO 1
tion; and (3) occlusion—total occlusion of the extracranial portion of the internal carot id artery. The angiographic findings were then cor related with the symptoms given by the patients as well as with the clinical findings observed on the neurovascular and ophthalmoscopic examinations. A well-localized bruit of any intensity in the region of the carotid bifurcation, below the angle of the jaw, was regarded as significant. A differ ence of 10% in the retinal artery pressures of the two eyes was considered significant and reported as a decrease in retinal artery pressure. Cholesterol emboli, platelet-fibrin emboli, venous stasis retinopathy, and ar terial occlusions of the retina were con sidered embolic events. RESULTS
Only one patient had a normal carotid artery on the side ipsilateral to the symptoms or clinical findings; the remaining 42 pa tients either had stenosis (30 patients) or total occlusion (12 patients) of the ipsilateral common carotid or extracranial (or both) portion of the internal carotid artery. Thirty-seven of the 43 patients had arteriographic procedures in which both carotid arteries were visualized (Table 2 ) . Thirteen patients had a normal carotid artery on the side opposite the site of symptoms and clini cal findings. Importantly, 24 of these pa tients had evidence of occlusive disease of the contralateral carotid artery even though it produced no apparent ill effects.
Patients with amaurosis fugax in associa tion with either transient or permanent cerebral symptoms (transient ischemic at tacks or stroke) had a greater incidence of ipsilateral carotid arterial disease than did patients whose only symptom was amaurosis fugax. Five patients had no clinical findings of carotid occlusive disease on examination, but these five had other symptoms of cerebrovascular disease in addition to amaurosis fugax (Table 3). Four of the five patients had stenosis of the common carotid or extra cranial (or both) portion of the internal carotid artery, and one patient had a total occlusion of the extracranial portion of the carotid artery. Carotid bruits were documented in 31 patients, reduced retinal artery pressure in 30 patients, and retinal embolic events in 18 patients. Most of the patients (72%), how ever, had more than one clinical finding in dicative of carotid occlusive disease in addi tion to their symptoms. Fourteen patients had a combination of a carotid bruit and reduced retinal artery pressure, and an addi tional 12 patients had a carotid bruit and reduced retinal artery pressure, in addition to evidence of retinal embolic events. One patient with amaurosis fugax alone, on ex amination, had reduced retinal artery pres sure, retinal emboli, and a carotid bruit al though the carotid artery was radiographically normal. In this series, no single finding or com bination of findings allowed accurate predic-
TABLE 2 COMPARISON OF ANGIOGRAPHIC ABNORMALITY OF THE SYMPTOMATIC (IPSILATERAL) VESSEL WITH THAT I N THE CONTRALATERAL VESSEL
Carotid Vascular Findings Normal
Ipsilateral Contralateral
Stenosis
Occlusion
Total
No.
%
No.
%
No.
%
1 13
2 35
30 22
70 60
12 2
28 5
43 37
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J U L Y , 197A
TABLE 3 COMPARISON OF CLINICAL FINDINGS WITH ANGIOGRAPHIC ABNORMALITY OF IPSILATERAL CAROTID ARTERY IN 4 3 PATIENTS WITH AMAUROSIS FUGAX
Ipsilateral Carotid Abnormality Findings None Reduced RAP* alone Emboli alone Bruit alone Reduced RAP and emboli Reduced RAP and bruit Emboli and bruit Reduced RAP, emboli, and bruit Total
Total
Normal
Stenosis
0 0 0 0 0 0 0 1
4 1 2 1 2 13 2 5
1 1 1 1 0 1 1 6
5 2 3 2 2 14 3 12
1
30
12
43
Occlusion
* Retinal artery pressure.
tion of the degree of patency of the ipsi lateral carotid artery, and a distinction be tween ipsilateral carotid stenosis and occlu sion could not be made on the basis of the clinical examination. DISCUSSION 2
Fisher has classified the presumed cause of amaurosis fugax into seven groups: (1) cases in the older age group in which athero sclerosis was probably a factor; (2) cases in the younger age group without apparent cause; (3) cases associated with migraine; (4) cases associated with Raynaud's syn drome ; (5) cases associated with heart dis ease; (6) cases of reflex amaurosis; and (7) miscellaneous cases. The cause and prognosis of amaurosis fugax encountered in younger patients, es pecially those without associated evidence of cerebrovascular disease, are not known. However, the condition may run an appar ently benign course and need not be due to retinal embolism from thrombosis in the ipsilateral internal carotid artery, as sug gested by Eadie, Sutherland, and Tyrer 7 in their report on 12 patients whose ages ranged from 14 to 51 years (mean 29.5 years). Reflection on our clinical experience in an older group of patients (50 years old or older) suggests that, except for the occa
sional patient with amaurosis fugax as a part of the syndrome of cranial arteritis, 8 most cases of amaurosis fugax (as sug gested in 1951 by Behrman 9 ) are related to carotid occlusive disease. Localized bruits, suggesting turbulent blood flow, were heard over the carotid bi furcation in 72% of our patients. In most instances, the bruit arises from the internal carotid artery and suggests stenotic patency of that vessel. Our case material suggests that a carotid bifurcation bruit can be ob served even though total occlusion of the internal carotid artery is present; and in this situation, the bruit likely arises from the ex ternal carotid. The presence of a carotid bruit, therefore, does not invariably imply internal carotid artery patency, and similarly its absence in these patients cannot be used" as invariable evidence of occlusion. Ipsilateral reduction in retinal artery pres sure was noted in 70% of our patients. A reduced retinal artery pressure was seldom found in the absence of severe narrowing or total occlusion of the ipsilateral carotid artery, and this may be interpreted as sug gesting the presence of a lesion capable of reducing distal carotid-ophthalmic artery blood flow. Whether the symptom of amaurosis fugax arises solely because of a total reduction in
VOL. 79, NO 1
AMAUROSIS FUGAX
ophthalmic artery blood flow is not clear; this may happen in some patients. Angiographic visualization of ulceration within the carotid artery is difficult10'11 but was noted in approximately 50% of our patients in the present study. At surgery, ulcer craters in the atheromatous tissue removed during carotid endarterectomy were noted in most patients with significant stenosis, even though they were not suspected from the angiographic study; this would suggest a possible microembolic origin for amaurosis fugax in many patients. The high incidence of retinal embolic events noted in this group of patients (42%) tends to support this theory. Atheromatous ulcerative stenosis and oc clusion of the extracranial carotid artery probably are the principal pathologic condi tions responsible for the amaurosis fugax encountered in an elderly population. It is these same pathologic conditions that have been postulated12 and shown13'14 to be re sponsible for most cerebral transient isch emic attacks involving the carotid system. Approximately one third of patients with cerebral transient ischemic attacks, if un treated, will develop a cerebral infarct.15 Although the precise incidence of patients with amaurosis fugax who will experience cerebral ischemic episodes is not known, amaurosis fugax is associated with a greater incidence and degree of atheromatous extra cranial carotid arterial disease than perhaps are seen in transient cerebral ischemic at tacks alone.6 Patients with symptomatic uni lateral atheromatous stenosis of the ipsilateral carotid artery probably benefit from carotid arterial surgery 5,16 ; patients with complete occlusion of the ipsilateral carotid artery are not generally considered suitable candidates for such surgery. The distinction between carotid arterial stenosis and occlu sion cannot be made with certainty on the basis of the clinical findings. We believe that proximal stenotic lesions of the extracranial carotid artery associated with microembolization and symptoms of
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retinal ischemia may carry an increased risk of subsequent cerebral ischemic events. We therefore recommend that patients with amaurosis fugax, especially if it is associated with other transient or permanent cerebral symptoms or signs, ipsilateral carotid bruit, reduced retinal artery pressure, or evidence of retinal embolic events, who are otherwise suitable surgical candidates, should undergo cervical-cranial angiography to delineate the nature and extent of the responsible lesion. Since evidence suggests that the risk of cere bral infarction is greatest during the first several weeks after an episode of transient ischemia,15 the management of such patients is an emergent one. Currently, we hospitalize such patients and, if no contraindications exist, begin anticoagulant therapy with heparin, which has been shown to improve sig nificantly the prognosis in patients with symptomatic carotid atheromatous disease.17 At the earliest moment after complete medi cal, neurologic, and ophthalmic evaluations, angiography is performed and definitive therapy is planned on the basis of the clinical-angiographic findings. SUMMARY
Of 1,080 patients studied by carotid an giography, 43 experienced unilateral amau rosis fugax. Of these 43 patients, 42 had significant occlusive disease of the ipsilateral common carotid or extracranial (or both) portion of the internal carotid artery; 12 (28%) had complete occlusion, and 30 (70%) had significant stenosis. Amaurosis fugax is a significant symptom of carotid occlusive disease affecting the extracranial portion of the carotid artery when it occurs in patients 50 years old or older in associa tion with either transient or permanent cerebral symptoms or signs, carotid bruit, reduced retinal artery pressures, or retinal embolic signs. Microembolization from an atheromatous plaque within this vessel is postulated as the pathophysiologic mecha nism for amaurosis fugax in most of these patients.
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AMERICAN JOURNAL OF OPHTHALMOLOGY REFERENCES
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