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Bilateral carotid artery occlusion: clinical presentation and outcome
Bilateral carotid artery occlusion: clinical presentation and outcome R. Verhaeghe,
J. Naert, and J. Vermylen*
Introduction
Summary
Clinical events in patients with cerebrosvascular disease are not strictly related to the degree of obstruction of the major arteries supplying the brain’. In autopsy and angiographical studies, a fatal or disabling stroke is the expected incident that leads to the detection of rare cases of bilateral carotid artery occlusion2x3. We wondered whether patients identified with non-invasive techniques in the vascular laboratory would have the same presenting symptoms and the same clinical outcome.
In a 4-year period, 17 patients were diagnosed as having bilateral carotid artery obstruction on ultrasonic duplex examination. Twelve had been referred because of recent neurological symptoms and the remaining 5 during cardiac or peripheral vascular work-up. Three patients had a completely silent occlusion of their two carotid arteries. Cardiac and/or peripheral vascular symptoms were present in 11 subjects. Mean follow-up was 28 months. No further strokes occurred. The 3-year cumulative stroke-free survival by life-table analysis was 75%. Myocardial infarction was the cause of death in 2 of 4 patients. For some patients with bilateral carotid artery occlusion, the clinical outcome is better than anticipated.
Methods
The files with all ultrasound duplex examinations of the carotid arteries carried out from 1985 through 1988 at the vascular laboratory of our institute were searched for patients with a total bilateral occlusion of the carotid artery. The total population (n = 7757) referred to the vascular laboratory for carotid duplex consists of 64% males and 36% females. Focal neurological symptoms are the reason for referral in 43%) 30% are screened for asymptomatic cervical bruits or because of cardiac disease or peripheral vascular disease and the remaining 27% have rather aspecific complaints. All duplex scans were performed by the same three experienced technicians and all were classified according to the criteria proposed by the University of
Key words: Carotid artery diseases, carotid artery thrombosis; cerebrosvascular disorders. L
Washington School of Medicine4. Next, the clinical records of all patients with a bilateral occlusion of the carotid arteries were analyzed retrospectively for their past history, the reason for their referral and their subsequent clinical follow-up. In addition, all patients were contacted in the summer of 1989 and again in January 1990, either personally or via their attending physician to ascertain their current clinical status.
* Center for Thrombosis and Vascular Research, Universiry of Leuven, Belgium Address for correspondence 3000 Leuven, Belgium
and reprint requests: R. Verhaeghe,
Center for Thrombosis and Vascular Research, Herestraat 49,
Accepted 13.9.90 Clin Neural Neurosurg 1991. Vol. 93-2
123
The search of all duplex protocols yielded 17 recordings of a bilateral carotid occlusion. Sixteen patients had an occlusion of the two internal carotid arteries. All but one were males and their age ranged from 52 to 82 years (mean: 66 years). A 34-year-old man with severe renovascular hypertension had an occlusion of the left internal carotid and the left vertebral artery together with a total obstruction of the right common carotid artery distal to a tight stenosis of the innominate artery. Fifteen patients were heavy cigarette smokers and 4 had an elevated serum cholesterol (> 6.4 mmoY1); 8 were treated for hypertension and 4 were diabetics, only one of whom received insulin. Cervical bruits were noted in 10 patients (3 uniand 7 bilaterally). The flow direction in the ophthalmic artery determined with a continuous wave doppler was reversed on both sides in 11 patients and on one side only in all 6 others. Oculoplethysmography was available in 9 patients and showed a decrease in ophthalmic systolic pressure in all (3 uni- and 6 bilaterally). Ten of the 17 patients underwent angiography, at the discretion of their attending physician, and in all 10 the duplex findings were confirmed. Computed tomography of the brain showed an infarcted area in one hemisphere in 9 out of 11 available scans. The reason for referral to the vascular laboratory was a recent neurological event in 12 patients,
Brain
Heart
Limbs Fig. 1. Venn-diagram showing the number of patients with a history of neurological, cardiac or peripheral vascular symptoms or a combination of any of these.
124
Fig. 2. Cumulative stroke-free survival by life-table analysis.
either a stroke (n=7) or a transient ischaemic attack (TIA; n=5; in 2 patients after a previous stroke). The five others had a check-up for cardiac and/or peripheral vascular symptoms; they had their duplex ordered because of an earlier stroke (n=2), the finding of a cervical bruit (n=2) or evaluation of repeated syncopes (n= 1). The episodes of cerebral ischemia were presumably of a hemodynamic nature in 2 patients and were presumably thrombo-embolic events in the remaining 12. The clinical severity of the atherosclerotic disease in these 17 patients is illustrated in Table 1 and Figure 1. Two patients had cardiac as well as peripheral vascular problems in addition to their neurological features and 9 others had clinical symptoms in two vascular territories. Three patients had two strokes in the same hemisphere, and only three patients had no history at all of a neurological event. The follow-up period ranged from 1 to 60 months (mean: 28 months). No further strokes occurred and only one subject had two episodes with a feeling of faintness and visual blurring. Partial or complete recovery of the neurological deficit present at the time of initial evaluation occurred in all but 2 patients. Four patients died during follow-up, from either a myocardial infarction (n=2), a bronchial carcinoma (n=l), and a rapidly evolving dementia (n=l). The cumulative stroke free survival rate at 2 and at 3 years was 75% (the 95% confidence intervals being 54-96 and 45-105, respectively) (Fig. 2). Four patients underwent surgical therapy for their extracranial arterial disease. One subject received a bilateral extraeranial- intracranial ar-
Table 1. Clinical features of atherosclerotic disease. 11 3
Brain:
-
stroke TIA
Heart
-
infarction angina chronic heart failure
4* 2* 2
Limbs
-
amputation vascular surgery intermittent claudication
1 3 4
-
* 3 of these 6 had coronary bypass surgery.
terial bypass in another institute, the vertebral artery was reimplanted into the common carotid artery in two others because of an associated stenosis of the origin of the vertebral artery and the 34-year-old patient underwent an endarterectomy of the innominate artery together with a venous bypass to the right internal carotid artery but this bypass reoccluded without symptoms in the early postoperative period. Unstable angina and/or deteriorating leg ischemia became manifest in three patients. Discussion
Bilateral carotid artery occlusion was rather rarely reported until fairly recently. Studies on the natural history of (mainly unilateral) carotid occlusion occasionally mention a small number of patients with both their carotids obstructed5,h. The largest series are found in the two wellknown multicentre studies on surgery and carotid artery disease: 43 patients in the Joint Study of Extracranial Arterial Occlusion’ and 74 in the Cooperative Study of Extracranial-Intracranial Arterial Anastomoses (the EC/IC Bypass Study)‘.“. The patients in the present report were collected over a 4 year period in a single vascular laboratory; the question is whether patients surviving with this pattern of carotid artery occlusion may be more common than is usually thought and whether a systematic use of accurate non-invasive diagnostic techniques in all cardiovascular patients might lead to a more frequent detection of these lesions. The clinical features with which patients with a
bilateral carotid occlusion present is biased by the method of preselection and the way of referral. Early autopsy and angiography studies are almost invariably based on patients with serious neurological deficits and one can hardly expect patients in neurological series to present with anything else than cerebral symptoms. On the other hand, Wortzman er ~1.” noted as long as twenty years ago that many have no history or findings to indicate bilateral severe disease. The group of patients reported here are neurologically hardly different from patients with less severe degrees of occlusive disease. For instance, the 64% incidence of stroke at the initial evaluation is only slightly higher than the 52% in a larger duplex series with mainly unilateral occlusion”, and the 15% totally asymptomatic patients fall within the limits of published rates for unilateral occlusion (from 7 to 22%). Three patients in the present series occluded both their carotids without any symptoms at all, an unreported finding as far as we were able to trace. In addition, none of the patients had a stroke in both hemispheres, which indicates a sufficient collateral blood supply to maintain a normal function in at least one hemisphere. The Joint Study already observed that the neurological deficit that occurs with occlusion of a single carotid is less severe when the contralateral artery is diseased as well, presumably as a result of collateral development’. Another greater marked feature of the present population is the widespread and severe atherosclerotic disease which compromises the coronary and the peripheral circulation as well as the blood supply to the brain; this again may be influenced to some extent by the particular preselection of this study. A few early reports describe the fate of patients with bilateral carotid artery occlusion as poor and dismal because of a high incidence of permanent and often fatal neurological deficits”. Therefore this pattern of carotid disease was initially considered incompatible with a prolonged normal function of the brain. Gradually, however, the importance of an adequate collateral circulation for survival and functional prognosis was better appreciated13. Recently, Nicholls et al. found no significant difference in mortality and stroke rates between patients with bilateral occlusion and a large series of concom125
itantly followed patients with unilateral occlusion”. In addition, death from stroke was no longer the chief cause of mortality. In the present study as well, the clinical outcome is determined by the occurrence of increasing cardiac or peripheral vascular disease rather than by new neurological events. Recurrent stroke is found uncommonly in patients with bilateral carotid occlusion and symptoms of cerebral ischaemia are restricted to one hemisphere, whereas bilateral involvement or unilateral symptoms plus involvement of the posterior circulation is a clinical predictor for delayed stroke’. Thus a welldeveloped collateral circulation may be a determining factor for the absence of further stroke. It summary, patients with bilateral carotid artery occlusion do not constitute a homogenous clinical entity but represent a whole spectrum of clinical features between two extremes: those who do not survive the initial stroke because of an inadequate collateral circulation and those with a much better clinical outcome than anticipated. The latter group closely follows the clinical course of patients with unilateral occlusion, in whom the prognosis is largely determined by the extent and severity of coronary impairment.
126
References DYKEN ML. KLATTE E,KoLAR C)J,SPURGEONC. Complete occlusion of common and internal carotid arteries. Clinical Significance. Arch. Neural. 1974; 30:343-O. BERGUEK K,MCCAFFREYJF,BAUERRB. Bilateralinternal carotid artery occlusion. Its surgical management. Arch. Surg. 1980; 115:840-3. FRIEDMAN SC. Current management of the patient with carotid artery occlusion. Eur. J. Vast. Surg. 1989; 3:97101. ROEDERERGO,LANGLOISYE,JAGERKA~~~~. The natural history of carotid arterial disease in asymptomatic patients with cervical bruits. Stroke 1984; 15606-13. FURLAN AJ,WHISNANTJP,BAKER HL. Long-termprognosis after carotid artery occlusion. Neurology 1980; 30:986-8. SACQUEGNA T, DE CAROLS P, PAZAGLIA I',el al. The clinical course and prognosis of carotid artery occlusion. J. Neural. Neurosurg. Psychiatry 1982; 45:1037-9. FIELDS ws. Joint Study of Extracranial Arterial Occlusion. X. Internal carotid artery occlusion. JAMA 1976; 235~2734-8. The EC/K Bypass Study Group. Failure of extracranialintracranial arterial bypass to reduce the risk of ischemic stroke. N. Et@ J. Med. 1985; 313:1191-1200. WADE
JPH, WONG
W, BARNElT
HIM, VANDERVOORT
P.
Bilateral occlusion of the internal carotid arteries. Brain 1987; 110667-82. WORTZMAN G,BARNETT HIM, LONGHEED WM. Bilateral internal carotid occlusion. Can. Med. Ass. J. 1968; 99:1186-96. NICHOLLS SC, KOHLER
TR, BERGELIN RO, PRIMOZICH IF,
DE. Carotid artery occlusion: Natural history. J. Vast. Surg. 1986; 4:479-85. CLARKE EC, HARRISON cv. Bilateral carotid artery obstruction. Neurology (Minneapolis) 1956; 6:705-U. FIELDS WS,EDWARDSWH,CRAWFORDES. Bilateralcarotid artery thrombosis. Arch. Neural. 1961; 4:369-83. LAWRENCE
RL, STRANDNESS
J. Naert, and J. Vermylen*
Introduction
Summary
Clinical events in patients with cerebrosvascular disease are not strictly related to the degree of obstruction of the major arteries supplying the brain’. In autopsy and angiographical studies, a fatal or disabling stroke is the expected incident that leads to the detection of rare cases of bilateral carotid artery occlusion2x3. We wondered whether patients identified with non-invasive techniques in the vascular laboratory would have the same presenting symptoms and the same clinical outcome.
In a 4-year period, 17 patients were diagnosed as having bilateral carotid artery obstruction on ultrasonic duplex examination. Twelve had been referred because of recent neurological symptoms and the remaining 5 during cardiac or peripheral vascular work-up. Three patients had a completely silent occlusion of their two carotid arteries. Cardiac and/or peripheral vascular symptoms were present in 11 subjects. Mean follow-up was 28 months. No further strokes occurred. The 3-year cumulative stroke-free survival by life-table analysis was 75%. Myocardial infarction was the cause of death in 2 of 4 patients. For some patients with bilateral carotid artery occlusion, the clinical outcome is better than anticipated.
Methods
The files with all ultrasound duplex examinations of the carotid arteries carried out from 1985 through 1988 at the vascular laboratory of our institute were searched for patients with a total bilateral occlusion of the carotid artery. The total population (n = 7757) referred to the vascular laboratory for carotid duplex consists of 64% males and 36% females. Focal neurological symptoms are the reason for referral in 43%) 30% are screened for asymptomatic cervical bruits or because of cardiac disease or peripheral vascular disease and the remaining 27% have rather aspecific complaints. All duplex scans were performed by the same three experienced technicians and all were classified according to the criteria proposed by the University of
Key words: Carotid artery diseases, carotid artery thrombosis; cerebrosvascular disorders. L
Washington School of Medicine4. Next, the clinical records of all patients with a bilateral occlusion of the carotid arteries were analyzed retrospectively for their past history, the reason for their referral and their subsequent clinical follow-up. In addition, all patients were contacted in the summer of 1989 and again in January 1990, either personally or via their attending physician to ascertain their current clinical status.
* Center for Thrombosis and Vascular Research, Universiry of Leuven, Belgium Address for correspondence 3000 Leuven, Belgium
and reprint requests: R. Verhaeghe,
Center for Thrombosis and Vascular Research, Herestraat 49,
Accepted 13.9.90 Clin Neural Neurosurg 1991. Vol. 93-2
123
The search of all duplex protocols yielded 17 recordings of a bilateral carotid occlusion. Sixteen patients had an occlusion of the two internal carotid arteries. All but one were males and their age ranged from 52 to 82 years (mean: 66 years). A 34-year-old man with severe renovascular hypertension had an occlusion of the left internal carotid and the left vertebral artery together with a total obstruction of the right common carotid artery distal to a tight stenosis of the innominate artery. Fifteen patients were heavy cigarette smokers and 4 had an elevated serum cholesterol (> 6.4 mmoY1); 8 were treated for hypertension and 4 were diabetics, only one of whom received insulin. Cervical bruits were noted in 10 patients (3 uniand 7 bilaterally). The flow direction in the ophthalmic artery determined with a continuous wave doppler was reversed on both sides in 11 patients and on one side only in all 6 others. Oculoplethysmography was available in 9 patients and showed a decrease in ophthalmic systolic pressure in all (3 uni- and 6 bilaterally). Ten of the 17 patients underwent angiography, at the discretion of their attending physician, and in all 10 the duplex findings were confirmed. Computed tomography of the brain showed an infarcted area in one hemisphere in 9 out of 11 available scans. The reason for referral to the vascular laboratory was a recent neurological event in 12 patients,
Brain
Heart
Limbs Fig. 1. Venn-diagram showing the number of patients with a history of neurological, cardiac or peripheral vascular symptoms or a combination of any of these.
124
Fig. 2. Cumulative stroke-free survival by life-table analysis.
either a stroke (n=7) or a transient ischaemic attack (TIA; n=5; in 2 patients after a previous stroke). The five others had a check-up for cardiac and/or peripheral vascular symptoms; they had their duplex ordered because of an earlier stroke (n=2), the finding of a cervical bruit (n=2) or evaluation of repeated syncopes (n= 1). The episodes of cerebral ischemia were presumably of a hemodynamic nature in 2 patients and were presumably thrombo-embolic events in the remaining 12. The clinical severity of the atherosclerotic disease in these 17 patients is illustrated in Table 1 and Figure 1. Two patients had cardiac as well as peripheral vascular problems in addition to their neurological features and 9 others had clinical symptoms in two vascular territories. Three patients had two strokes in the same hemisphere, and only three patients had no history at all of a neurological event. The follow-up period ranged from 1 to 60 months (mean: 28 months). No further strokes occurred and only one subject had two episodes with a feeling of faintness and visual blurring. Partial or complete recovery of the neurological deficit present at the time of initial evaluation occurred in all but 2 patients. Four patients died during follow-up, from either a myocardial infarction (n=2), a bronchial carcinoma (n=l), and a rapidly evolving dementia (n=l). The cumulative stroke free survival rate at 2 and at 3 years was 75% (the 95% confidence intervals being 54-96 and 45-105, respectively) (Fig. 2). Four patients underwent surgical therapy for their extracranial arterial disease. One subject received a bilateral extraeranial- intracranial ar-
Table 1. Clinical features of atherosclerotic disease. 11 3
Brain:
-
stroke TIA
Heart
-
infarction angina chronic heart failure
4* 2* 2
Limbs
-
amputation vascular surgery intermittent claudication
1 3 4
-
* 3 of these 6 had coronary bypass surgery.
terial bypass in another institute, the vertebral artery was reimplanted into the common carotid artery in two others because of an associated stenosis of the origin of the vertebral artery and the 34-year-old patient underwent an endarterectomy of the innominate artery together with a venous bypass to the right internal carotid artery but this bypass reoccluded without symptoms in the early postoperative period. Unstable angina and/or deteriorating leg ischemia became manifest in three patients. Discussion
Bilateral carotid artery occlusion was rather rarely reported until fairly recently. Studies on the natural history of (mainly unilateral) carotid occlusion occasionally mention a small number of patients with both their carotids obstructed5,h. The largest series are found in the two wellknown multicentre studies on surgery and carotid artery disease: 43 patients in the Joint Study of Extracranial Arterial Occlusion’ and 74 in the Cooperative Study of Extracranial-Intracranial Arterial Anastomoses (the EC/IC Bypass Study)‘.“. The patients in the present report were collected over a 4 year period in a single vascular laboratory; the question is whether patients surviving with this pattern of carotid artery occlusion may be more common than is usually thought and whether a systematic use of accurate non-invasive diagnostic techniques in all cardiovascular patients might lead to a more frequent detection of these lesions. The clinical features with which patients with a
bilateral carotid occlusion present is biased by the method of preselection and the way of referral. Early autopsy and angiography studies are almost invariably based on patients with serious neurological deficits and one can hardly expect patients in neurological series to present with anything else than cerebral symptoms. On the other hand, Wortzman er ~1.” noted as long as twenty years ago that many have no history or findings to indicate bilateral severe disease. The group of patients reported here are neurologically hardly different from patients with less severe degrees of occlusive disease. For instance, the 64% incidence of stroke at the initial evaluation is only slightly higher than the 52% in a larger duplex series with mainly unilateral occlusion”, and the 15% totally asymptomatic patients fall within the limits of published rates for unilateral occlusion (from 7 to 22%). Three patients in the present series occluded both their carotids without any symptoms at all, an unreported finding as far as we were able to trace. In addition, none of the patients had a stroke in both hemispheres, which indicates a sufficient collateral blood supply to maintain a normal function in at least one hemisphere. The Joint Study already observed that the neurological deficit that occurs with occlusion of a single carotid is less severe when the contralateral artery is diseased as well, presumably as a result of collateral development’. Another greater marked feature of the present population is the widespread and severe atherosclerotic disease which compromises the coronary and the peripheral circulation as well as the blood supply to the brain; this again may be influenced to some extent by the particular preselection of this study. A few early reports describe the fate of patients with bilateral carotid artery occlusion as poor and dismal because of a high incidence of permanent and often fatal neurological deficits”. Therefore this pattern of carotid disease was initially considered incompatible with a prolonged normal function of the brain. Gradually, however, the importance of an adequate collateral circulation for survival and functional prognosis was better appreciated13. Recently, Nicholls et al. found no significant difference in mortality and stroke rates between patients with bilateral occlusion and a large series of concom125
itantly followed patients with unilateral occlusion”. In addition, death from stroke was no longer the chief cause of mortality. In the present study as well, the clinical outcome is determined by the occurrence of increasing cardiac or peripheral vascular disease rather than by new neurological events. Recurrent stroke is found uncommonly in patients with bilateral carotid occlusion and symptoms of cerebral ischaemia are restricted to one hemisphere, whereas bilateral involvement or unilateral symptoms plus involvement of the posterior circulation is a clinical predictor for delayed stroke’. Thus a welldeveloped collateral circulation may be a determining factor for the absence of further stroke. It summary, patients with bilateral carotid artery occlusion do not constitute a homogenous clinical entity but represent a whole spectrum of clinical features between two extremes: those who do not survive the initial stroke because of an inadequate collateral circulation and those with a much better clinical outcome than anticipated. The latter group closely follows the clinical course of patients with unilateral occlusion, in whom the prognosis is largely determined by the extent and severity of coronary impairment.
126
References DYKEN ML. KLATTE E,KoLAR C)J,SPURGEONC. Complete occlusion of common and internal carotid arteries. Clinical Significance. Arch. Neural. 1974; 30:343-O. BERGUEK K,MCCAFFREYJF,BAUERRB. Bilateralinternal carotid artery occlusion. Its surgical management. Arch. Surg. 1980; 115:840-3. FRIEDMAN SC. Current management of the patient with carotid artery occlusion. Eur. J. Vast. Surg. 1989; 3:97101. ROEDERERGO,LANGLOISYE,JAGERKA~~~~. The natural history of carotid arterial disease in asymptomatic patients with cervical bruits. Stroke 1984; 15606-13. FURLAN AJ,WHISNANTJP,BAKER HL. Long-termprognosis after carotid artery occlusion. Neurology 1980; 30:986-8. SACQUEGNA T, DE CAROLS P, PAZAGLIA I',el al. The clinical course and prognosis of carotid artery occlusion. J. Neural. Neurosurg. Psychiatry 1982; 45:1037-9. FIELDS ws. Joint Study of Extracranial Arterial Occlusion. X. Internal carotid artery occlusion. JAMA 1976; 235~2734-8. The EC/K Bypass Study Group. Failure of extracranialintracranial arterial bypass to reduce the risk of ischemic stroke. N. Et@ J. Med. 1985; 313:1191-1200. WADE
JPH, WONG
W, BARNElT
HIM, VANDERVOORT
P.
Bilateral occlusion of the internal carotid arteries. Brain 1987; 110667-82. WORTZMAN G,BARNETT HIM, LONGHEED WM. Bilateral internal carotid occlusion. Can. Med. Ass. J. 1968; 99:1186-96. NICHOLLS SC, KOHLER
TR, BERGELIN RO, PRIMOZICH IF,
DE. Carotid artery occlusion: Natural history. J. Vast. Surg. 1986; 4:479-85. CLARKE EC, HARRISON cv. Bilateral carotid artery obstruction. Neurology (Minneapolis) 1956; 6:705-U. FIELDS WS,EDWARDSWH,CRAWFORDES. Bilateralcarotid artery thrombosis. Arch. Neural. 1961; 4:369-83. LAWRENCE
RL, STRANDNESS