Bilateral Severe Carotid Stenosis or Occlusion and Computed Tomographic Scan Positive Hemispheric Stroke with Neurologic Deficit: Immediate Contralateral Carotid Endarterectomy Nicholas A. Sannella, MD, N o r t h Andover, M a s s a c h u s e t t s
In the last 10 years, 13 patients presented with acute, hemispheric, computed tomographic scan-positive stroke; neuroiogic deficit; and bilateral carotid stenosis greater than 90% (N = 9) or ipsilateral occlusion with contralateral stenosis greater than 90% (N = 4). To improve ipsilateral flow without elevation of pressure to levels causing hemorrhagic infarction, all patients underwent carotid endarterectomy on the side contralateral to the hemispheric stroke from two to 10 days (average 6.6 days) from onset of symptoms. Those with fluctuating deficits stabilized to the initial fixed deficit and all 13 improved over the next six months. Four patients with ipsilateral internal carotid occlusion and one with ipsilateral severe siphon stenosis were discharged on antiplatelet therapy; of the remaining eight patients, seven underwent subsequent ipsilateral carotid endarterectomy from 42 to 111 days (average 58.4 days) from onset of symptoms. Mortality and stroke rate were 0. The four patients with internal carotid occlusion and the one with severe siphon stenosis filled both hemispheres from the contralateral carotid artery arteriographically in four and by oculoplethysmography in one. One patient demonstrated preferential flow from contralateral to the ipsilaterai hemisphere, but not the reverse; one patient demonstrated pericallosal collaterals. Immediate endarterectomy of the severely diseased carotid artery contralateral to a hemisphere with a computed tomographic scan-positive stroke causing neurologic deficit resulting from a severe carotid stenosis is a safe treatment option and may be beneficial in those with fluctuating neurologic deficits. (Ann Vasc Surg 1992;6:252-257). KEY WORDS:
Carotid artery stenosis; stroke; carotid endarterectomy.
The timing of ipsilateral carotid endarterectomy for severe stenosis following acute stroke remains controversial; early reports identified increased risk of hemorrhagic infarction with high mortality in a neurologically unstable group of patients [1,2]. Subsequently, Goldstone and Moore [3], in the prePresented at the New England Society for Vascular Surgery, September 14, 1990, Newport, Rhode Island. Reprint requests: N.A. Sannella, MD, 198 Massachusetts Avenue, North Andover, Massachusetts 01844.
computed tomographic (CT) scan era, recommended urgent evaluation and ipsilateral surgery for neurologically unstable patients with severely stenotic disease in the hopes of averting infarction or its progression. More precise identification of patient groups and neurologic deficits, use of CT scanning and a greater familiarity with carotid endarterectomy have all contributed to substantial decreases in morbidity and mortality in the ensuing decades [4]. However, recent critical reappraisal of this problem has not resulted in resolution. In252
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253
TABLE I. Case Age/sex 1 56 Male
Arteriography CT RICO L99% R. parietal
Collateral By OPG both hemispheres
RICO L90%
AC patent
2
74 Male
3 4
73 Female R90% L ICO 50 Male R95% L95%
5
77 Male
R95% L95%
6
62 Male
R90% SS L99%
7
64 Male
R99% L95%
8
49 Male
R90% L90%
9
75 Male
R95% L95%
10
76 Female R90% L90%
11 12
69 Male R95% L95% 59 Female R99% L95%
13
55 Male
R ICO L98%
Deficit Fluctuating left arm from paralysis to mild weakness R. occipitoparietal Left hand numbness, weakness, mild L. temporoparietal Right arm face weakness Right hand clumsiness, L. parietal weakness
Follow-up Died, cardiac disease 61 months A&W 30 months
AC patent A&W 72 months Ant comm right A&W 62 months to left but not left to right L. occipitoparietal Fluctuating aphasia, right Leptomeningeal A&W 24 months arm and hand weakness to paralysis R. parietal Right arm weakness Right anterior A&W 5 months fluctuating from mild to cerebral from severe left internal carotid R. occipitoparietal Left arm weakness A&W 25 months hemianopsia L. parietal Expressive aphasia, A&W 65 months severe L. occipitoparietal Right arm and hand A&W 13 months weakness, expressive aphasia L. occipitoparietal Expressive aphasia, right Died, cardiac 18 months arm weakness R. frontal Left arm weakness A&W 80 months L. occipoparietal Right homonymous A&W 37 months hemianopsia R. parietal Left arm and hand AC patent A&W 64 months weakness, numbness
C T - c o m p u t e d t o m o g r a p h i c s c a n ; R - right; L - left; I C O - i n t e r n a l c a r o t i d o c c l u s i o n ; O P G - o c u l o p l e t h y s m o g r a p h y ;
AC - anterior communicating;
A&W - alive
and w e l l ; S S - s i p h o n stenosis
creased risk of stroke has been reported in patients with progressive neurologic deficit, positive CT scan and e n d a r t e r e c t o m y [5], surgery within five weeks of acute stroke [6], urgent ipsilateral endarterectomy and positive CT scan [7]. H o w e v e r , endarterectomy has been advised in patients with small, fixed neurologic deficits without any interval surgical delay [8] or as long as a plateau of neurologic recovery has been achieved [9]. Further compounding this issue is the risk of new stroke or extension of the original stroke in the interval between an initial presentation and surgery four to six weeks later. Dosick and associates [4] reported this to be as high as 21% in an initial group and 9.5% in a subsequent group with no mention of the contralateral artery. The subset of patients with neurologic deficit, hemispheric infarction by CT scan, ipsilateral stenosis greater than 90%, or occlusion and contralateral 90% stenosis or bilateral stenosis greater than 90% are particularly compromised. Contralateral endarterectomy to improve ipsilateral flow for maintenance of viability and neurologic stability without sufficient increase of pressure to cause hemorrhagic infarction was accomplished in this group and is the subject of this study.
METHODS In the last 10 years, patients who presented with transient ischemic attacks (TIAs) or mild-to-moderate neurologic deficit underwent initial diagnostic and therapeutic modalities consisting of CT scanning, heparin therapy where appropriate, and arteriography. Patients with severe deficit or decreased level of consciousness were not immediately studied. In those with ipsilateral surgical lesions, if CT scanning were positive for ischemic stroke and if neurologic examination were normal or the deficit minor and fixed, immediate ipsilateral endarterectomy was performed. A subset of 13 patients was identified with significant stable or fluctuating neurologic deficit, CT scans demonstrating hemispheric infarction, and ipsilateral severe carotid stenosis or occlusion with contralateral severe stenosis or bilateral severe stenosis (Table I). All 13 patients had a fixed deficit; in eight it was improving, but in five there was a c o m p o n e n t that fluctuated, then worsened to a baseline deficit. At the discretion of the radiologist, arteriographic study was limited in some patients to digital subtraction arteriographic (DSA) studies of the neck without cerebral visualization. H o w e v e r , there was demonstration of interhemispheric flow in some
254
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patients. In four with internal carotid occlusion and one with severe siphon stenosis, both hemispheres filled arteriographically from the contralateral carotid artery and by oculoplethysmography (OPG) in one. One patient demonstrated preferential flow contralateral to the ipsilateral CT scan positive hemisphere, but not the reverse; one patient demonstrated pericallosal (leptomeningeal) collaterals. No statement could be made referable to intracranial collaterals in the other six patients. All patients had cortical stroke without return of function within three weeks, no previous symptoms, both appropriate and inappropriate lesions, and appropriate cortical infarction by CT scanning, defined as C4b H O A3a Tli by the C H A T system [10]. All patients underwent carotid endarterectomy on the side contralateral to the hemispheric stroke from two to I0 days (average 6.6 days) from onset of symptoms. Seven of the remaining eight patients with ipsilateral stenosis underwent subsequent ipsilateral carotid e n d a r t e r e c t o m y from 42 to I11 days (average 58.4 days) from onset o f symptoms. General, endotracheal, normotensive anesthesia with systemic heparinization and indwelling shunt were e m p l o y e d in all cases; rigorous attention to perioperative and postoperative maintenance of normotension was accomplished with systolic pressures being kept below 160 and above 100 with agents consisting of phenylephrine, dopamine and nitroprusside. Tacking sutures were employed where necessary; no patches were incorporated into arterial closure.
RESULTS This subset of 13 patients is from a total group o f 615 patients who underwent 662 carotid endarterectomies. Thirty day mortality for the entire group was I%; postoperative neurologic deficits occurred in 2.3%. For this subset, mortality and stroke rate was 0%. The five patients with deficits fluctuating from mild to moderate or severe stabilized with persistence of a mild deficit which subsequently improved. The eight patients with stable deficits showed continuing improvement in the ensuing months as well. There was no incidence of neurologic worsening. Of the eight patients with severe ipsilateral carotid stenosis, seven subsequently underwent an unremarkable ipsilateral carotid e n d a r t e r e c t o m y , following interval Coumadin or antiplatelet therapy with no further neurologic sequelae. One patient declined ipsilateral e n d a r t e r e c t o m y and continues to be well 37 months later, with his condition unchanged on ultrasound. No subsequent neurologic deficits have been recorded in these patients. T h e r e have been no interval or subsequent internal
ANNALS OF
VASCULARSURGERY
Fig. 1. Patient No. 1: Computed tomographic scan demonstrating right parietal infarction.
carotid occlusions. In follow-up there have been no neurologic events requiring CT scans.
CASE REPORTS Patient No. 1
A 56-year-old white man, a fireman with a history of coronary artery disease and bilateral carotid bruits, was admitted with left arm and hand weakness. Computed tomographic scan revealed right parietal infarction (Fig. 1), and heparin therapy was initiated. In the next 48 hours, three episodes of progression of left arm and hand weakness to complete paralysis occurred, with resolution back to mild-to-moderate weakness. Arteriography revealed a right internal carotid occlusion and a severe left sided stenosis (Fig. 2). Immediate left carotid endarterectomy was accomplished unremarkably with stabilization of his deficit to the original weakness and subsequent complete clearing in the ensuing three months. Pre- and postoperative OPG findings demonstrated bilateral hemispheric increase in pressures. The patient continued to be well with no further neurologic difficulties, until he died of cardiac disease 61 months later. Patient No. 2
A 77-year-old man was admitted with right arm and hand weakness and expressive aphasia. Heparin therapy was commenced with resolution of his aphasia, but persistence of right arm weakness. Two further episodes in the ensuing 72 hours consisted of progression to almost complete paralysis of the arm with return of function to its original weakness. Computed tomographic scan demonstrated occipitoparietal infarction on the left side (Fig.
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Fig. 4. Patient No. 2: Arteriography revealing bilateral severe carotid stenosis.
3); arteriography revealed bilateral 95% stenosis (Fig. 4) with left hemispheric filling from right leptomeningeal collaterals, with the anterior communicating vessel not patent. Immediate right carotid endarterectomy was performed unremarkably with stabilization of function and no further episodes. His arm weakness resolved within the next two months and left carotid endarterectomy was subsequently accomplished unremarkably. He continues neurologically intact two years later.
DISCUSSION Fig. 2. Patient No. 1: Aortic arch arteriogram demonstrating right internal carotid occlusion and severe left-sided stenosis.
Fig. 3, Patient No. 2: Computed tomographic scan demonstrating left-sided occipitoparietal infarction.
Sachs [11] reported relief of symptoms in both hemispheres with endarterectomy of stenotic carotids associated with contralateral occlusion; Piotrowski and colleagues [9] noted that 12 of 129 patients with "acute stroke" (9.3%) had ipsitateral occlusion and severe contralateral stenosis, with subsequent contralateral endarterectomy, the timing of contralateral endarterectomy not specifically being mentioned. However, this group included patients with retinal strokes, and CT scanning was accomplished in only 77% of the entire group, with findings of not only appropriate cortical infarcts, but also lacunar infarcts or no infarcts. However, the value of immediate contralateral endarterectomy in prevention of interval extension of stroke by increasing collateral flow, as well as improving the safety of subsequent ipsilateral endarterectomy, has not been examined. The extent of revascularization of the CT scanpositive hemisphere with the initial contralateral endarterectomy is unique to the individual patient. Arteriographic definition of the potential anatomic collateral hemispheric flow has been limited in this study, as in others, by considerations of safety and practicality. Digital subtraction arteriography and ultrasound have resulted in less need for the extensive arteriography performed in previous years [12]. The ideal of a second arteriogram following initial
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contralateral carotid endarterectomy to define improved areas of perfusion after correction of a greater than 90% contralateral stenosis for study purposes is obvious, but not clinically indicated. Nonetheless, we were able to demonstrate patency of the Circle of Willis arteriographically in four patients and by OPG in one patient. Post-Willisian leptomeningeal vessels were demonstrated in one further patient. Physiologic definition of collateral hemispheric potential in patients with severe carotid stenosis has been studied with various techniques. Increased bilateral Doppler ophthalmic artery pressure has been identified following unilateral carotid endarterectomy in the presence of significant bilateral occlusive disease [13]. Eikelboom [14] using OPG and collateral ophthalmic artery pressure data noted a correlation which implies decreased collateral flow to the opposite hemisphere from the side of a severe ipsilateral stenosis. Also noted was no certainty of collateral flow as measured by OPG even when anterior or posterior communicating arteries were arteriographically visualized. Increased systolic and diastolic velocities for ipsilateral disease in the presence of severe contralaterat disease has been reported [15]. Transcranial Doppler and carotid compression in 55 patients with unilateral carotid occlusion identified five patients with total and 24 with partial dependence of the contralateral patent carotid vessel for middle cerebral artery flow [16]. Sundt and coworkers [17] measured cerebral blood flow using Xenon 133 and found cerebral blood flow to be increased after correction of carotid lesions greater than 90%; this has been noted to be bihemispheric with initial marked increase in hemispheric flow, but a more moderate global hyperemia as well [18]. The disparity between areas of CT scan positive stroke and symptomatology (such as the patient with occipital infarct with both visual and motor symptoms) can be explained by a zone of neuronal tissue still viable, but nonfunctional, the so-called "ischemic penumbra" [19]. Prompt revascularization in this clinical setting might well afford salvage of these regions. Discrepancies with Xenon 133 between low flow areas on cerebral blood flow tomograms and hypodense areas of infarction on CT scanning have been identified, suggesting these areas are viable, but nonfunctional neuronal tissue [20]. Intracranial hemorrhage following carotid endarterectomy would appear to be multifactorial in origin. The initial report of Wylie and associates [1] has prompted continuing caution with ipsilateral endarterectomy in the face of acute stroke in the hopes of avoiding conversion of an ischemic stroke to intracranial hemorrhage. Correction of an ipsilateral high grade carotid stenosis associated with loss of cerebral autoregulation caused by long-standing severe chronic cerebral ischemia has been noted to
ANNALS OF VASCULAR SURGERY
result in hyperperfusion, theoretically increasing the odds of intracerebral hemorrhage. Pomposelli and colleagues [22] reported postoperative hemorrhage in 11 (0.7%) of 1,500 carotid endarterectomy patients; all had normal coagulation studies; six of 11 patients were normotensive postoperatively. However, postoperative maintenance of normotension has obviously been recommended [23]. The initial contralateral endarterectomy in our patients would place the normal contralateral hemisphere at the normal, low risk for hemorrhage and the abnormal, ipsilateral, CT scan positive hemisphere at uncertain risk. The dampening effect of collateral patterns on pressure and the vigorous maintenance of normotension undoubtedly serve to protect against postoperative hemorrhage. Hafner and coworkers [24] suggested that involvement of multiple extracranial cerebral vessels may increase the risk of postendarterectomy hemorrhage, although only two of 10 of his patients had severe (>90%) bilateral disease. The coexistence of bilateral severe carotid disease has been suggested as a "necessary factor" by Pomposelli [22]. However, contralateral endarterectomy as initial operation has not been suggested prior to the present report for protection from intracranial hemorrhage as well as preservation of viable neurologic tissue. Although it is not possible to differentiate flowrelated stroke from embolic stroke in these patients, the predominant distribution of infarction in our patients to what has been paradoxically referred to as "watershed" areas [25]--and the marked degrees of stenosis--would support a primary flow etiology rather than an embolic one. Postmortem study [26] has identified the crucial role of collateral flow in patterns of hemispheric stroke as it relates to bilateral occlusive carotid disease and the integrity of the Circle of Willis. Torvic and Jorgensen [27] also correlate the size and depth of infarction with the presence and size of Willisian collaterals. The stabilization of our patients with marked neurologic instability, especially those with ipsilateral occlusion, would clinically support revascularization of both hemispheres. This applies beyond doubt in our patient with OPG data. The benign course of those with stable deficits and immediate contralateral endarterectomy and subsequent ipsilateral endarterectomy would also tend to confirm this revascularization as well. This subset of patients, presenting with ipsilateral stroke and bilateral severe carotid occlusive disease, is at high-risk of complications from medical [4] as well as surgical therapy [28]. The surgeon's responsibility extends not only to avoidance of operative complications but to offering relief to patients even if they are in a high risk group. Ipsilateral endarterectomy best restores flow and eliminates an embolic source but in the opinion of
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this author, these potentially beneficial effects are achieved at the prohibitive price of intracerebral hemorrhage and extension of infarction. We believe immediate contralateral endarterectomy improves ipsilateral flow, as evidenced by the neurologic stabilization of our 13 patients as well as by the subsequent safety of ipsilateral endarterectomy. Although the amount of flow through collateral hemispheric patterns is not predictable with present technology, this limitation should not preclude consideration of operation in this high-risk subset of patients.
REFERENCES 1. WYLIE EJ, HEIN MR, ADAMS JR. Intracranial hemorrhage following surgical revascularization for treatment of acute stroke. J Neurosurg 1964;21:212-215. 2. ROB CG. Operation for acute completed stroke due to thrombosis of internal carotid artery. Surgery 1969;65:852-855. 3. GOLDSTONE J, MOORE WS. Emergency carotid artery surgery in neurologically unstable patients. Arch Surg 1976; 111:1284--1291. 4. DOSICK SM, WHALEN RC, GALE SS, et al. Carotid endarterectomy in the stroke patient: computerized axial tomography to determine timing. J Vasc Surg 1985;2:214-219. 5. LITTLE JR, MOUFARRIJ NA, FURLAN AJ. Early carotid endarterectomy after cerebral infarction. Neurosurgery 1989;24:334-338. 6. GIORDANO JM, TROUT HH, KOZLOFF L, et al. Timing of carotid artery endarterectomy after stroke. J Vasc Surg 1985 ;2:250-254. 7. RICOTTA J, OURIEL K, GREEN RM, et al. Use of computerized cerebral tomography in selection of patients for elective and urgent carotid endarterectomy. Ann Surg 1985;202:783-787. 8. WHITTEMORE AD, RUBY ST, COUCH NP, et al. Early carotid endarterectomy in patients with small, fixed neurologic deficits. J Vasc Surg 1984;12:795-799. 9. PIOTROWSKI J J, BERNHARD VM, RUBIN JR, et at. Timing of carotid endarterectomy after acute stroke. J l/asc Surg 1990;11:45-52. 10. BERNSTEIN EF, BROWSE NL. The CHAT classification of stroke. Ann Surg 1989;209:242-248. 11. SACHS SM, FULENWIDER JT, SMITH RB, et al. Does contralateral carotid occlusion influence neurologic fate of carotid endarterectomy? Surgery 1989;96:839-844. 12. RICOTTA J J, HOLEN J, SCHENK. Is routine angiography
nmm
257
necessary prior to carotid endarterectomy? J Vasc Surg 1984;1:96-102. 13. STRAUSS AL, REIGER H. Variability of Doppler ophthalmic pressure index with occlusive carotid artery disease. J Vasc Surg 1990;12:50-55. 14. EIKELBOOM BC. Physiologic principles of ocular pneumoplethysmography. In: BERNSTEIN EF (ed). Noninvasive diagnostic techniques in vascular disease. 3rd ed. St. Louis: C.V. Mosby, 1985: pp 91-96. 15. SPADONE DP, BARKMEIER LD, HODGSON KJ, et al. Contralateral internal carotid artery stenosis or occlusion: pitfall of correct ipsilateral classification--a study performed with color-flow imaging, J Vasc Surg 1990;11:642--649. 16. NORRIS JW, KRAJEWSKI A, BORNSTEIN NM. The clinical role of the cerebral collateral circulation in carotid occlusion. J Vasc Surg 1990;12:113-118. 17. SUNDT TM, SHARBROUGH FW, PIEPGRAS DG, et al. Correlation of cerebral blood flow and electroencephalographic changes during carotid endarterectomy. Mayo Ctin Proc 1981 ;56:533-543. 18. SCHROEDER T, SILLESEN H, SORENSEN O, et al. Cerebral hyperperfusion following endarterectomy. J Neurosurg 1987;66:824--829. 19. ASTRUP J, SIESJO BK, SMYON L. Thresholds in cerebral ischemia--the ischemic penumbra. Stroke 1981;12:723-725. 20. LASSEN NA, HENRIKSEN L, PAULSON O. Regional cerebral blood flow in stroke: xenon inhalation and emission tomography. Stroke 1981;12:184-188. 21. REIGEL MM, HOLLIER LH, SUNDT TM, et al. Cerebral hyperperfusion syndrome: a cause of neurologic dysfunction after carotid endarterectomy. J Vasc Surg 1987;5:628--634. 22. POMPOSELLI FB, LAMPARELLO PJ, RILES TS, et al. Intracranial hemorrhage after carotid endarterectomy. J Vasc Surg 1988;7:248-255. 23. PEIPGRAS DG, MORGAN MK, SUNDT TM, et al. Intracranial hemorrhage after carotid endarterectomy. J Neurosurg 1988;68:532-536. 24. HAFNER DH, SMITH RB, KING OW, et al. Massive intracerebral hemorrhage following carotid endarterectomy. Arch Surg 1987;122:305-307. 25. FISHER M. Occlusion of the carotid arteries. A M A Arch Neurol Psychiat 1954;72:187-204. 26. RODDA RA. The arterial patterns associated with internal carotid disease and cerebral infarcts. Stroke 1986;17:69-79. 27. TORVIC A, JORGENSEN L. Thrombotic occlusions of the carotid arteries in an autopsy series. J Neurol Sci 1966;3: 410--432. 28. GRABER JN, VOLLMAN RW, JOHNSON WV, et at. Stroke after carotid endarterectomy: risk as predicted by preoperative computerized tomography. A m J Surg 1984 ;147:492~196.
In the last 10 years, 13 patients presented with acute, hemispheric, computed tomographic scan-positive stroke; neuroiogic deficit; and bilateral carotid stenosis greater than 90% (N = 9) or ipsilateral occlusion with contralateral stenosis greater than 90% (N = 4). To improve ipsilateral flow without elevation of pressure to levels causing hemorrhagic infarction, all patients underwent carotid endarterectomy on the side contralateral to the hemispheric stroke from two to 10 days (average 6.6 days) from onset of symptoms. Those with fluctuating deficits stabilized to the initial fixed deficit and all 13 improved over the next six months. Four patients with ipsilateral internal carotid occlusion and one with ipsilateral severe siphon stenosis were discharged on antiplatelet therapy; of the remaining eight patients, seven underwent subsequent ipsilateral carotid endarterectomy from 42 to 111 days (average 58.4 days) from onset of symptoms. Mortality and stroke rate were 0. The four patients with internal carotid occlusion and the one with severe siphon stenosis filled both hemispheres from the contralateral carotid artery arteriographically in four and by oculoplethysmography in one. One patient demonstrated preferential flow from contralateral to the ipsilaterai hemisphere, but not the reverse; one patient demonstrated pericallosal collaterals. Immediate endarterectomy of the severely diseased carotid artery contralateral to a hemisphere with a computed tomographic scan-positive stroke causing neurologic deficit resulting from a severe carotid stenosis is a safe treatment option and may be beneficial in those with fluctuating neurologic deficits. (Ann Vasc Surg 1992;6:252-257). KEY WORDS:
Carotid artery stenosis; stroke; carotid endarterectomy.
The timing of ipsilateral carotid endarterectomy for severe stenosis following acute stroke remains controversial; early reports identified increased risk of hemorrhagic infarction with high mortality in a neurologically unstable group of patients [1,2]. Subsequently, Goldstone and Moore [3], in the prePresented at the New England Society for Vascular Surgery, September 14, 1990, Newport, Rhode Island. Reprint requests: N.A. Sannella, MD, 198 Massachusetts Avenue, North Andover, Massachusetts 01844.
computed tomographic (CT) scan era, recommended urgent evaluation and ipsilateral surgery for neurologically unstable patients with severely stenotic disease in the hopes of averting infarction or its progression. More precise identification of patient groups and neurologic deficits, use of CT scanning and a greater familiarity with carotid endarterectomy have all contributed to substantial decreases in morbidity and mortality in the ensuing decades [4]. However, recent critical reappraisal of this problem has not resulted in resolution. In252
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253
TABLE I. Case Age/sex 1 56 Male
Arteriography CT RICO L99% R. parietal
Collateral By OPG both hemispheres
RICO L90%
AC patent
2
74 Male
3 4
73 Female R90% L ICO 50 Male R95% L95%
5
77 Male
R95% L95%
6
62 Male
R90% SS L99%
7
64 Male
R99% L95%
8
49 Male
R90% L90%
9
75 Male
R95% L95%
10
76 Female R90% L90%
11 12
69 Male R95% L95% 59 Female R99% L95%
13
55 Male
R ICO L98%
Deficit Fluctuating left arm from paralysis to mild weakness R. occipitoparietal Left hand numbness, weakness, mild L. temporoparietal Right arm face weakness Right hand clumsiness, L. parietal weakness
Follow-up Died, cardiac disease 61 months A&W 30 months
AC patent A&W 72 months Ant comm right A&W 62 months to left but not left to right L. occipitoparietal Fluctuating aphasia, right Leptomeningeal A&W 24 months arm and hand weakness to paralysis R. parietal Right arm weakness Right anterior A&W 5 months fluctuating from mild to cerebral from severe left internal carotid R. occipitoparietal Left arm weakness A&W 25 months hemianopsia L. parietal Expressive aphasia, A&W 65 months severe L. occipitoparietal Right arm and hand A&W 13 months weakness, expressive aphasia L. occipitoparietal Expressive aphasia, right Died, cardiac 18 months arm weakness R. frontal Left arm weakness A&W 80 months L. occipoparietal Right homonymous A&W 37 months hemianopsia R. parietal Left arm and hand AC patent A&W 64 months weakness, numbness
C T - c o m p u t e d t o m o g r a p h i c s c a n ; R - right; L - left; I C O - i n t e r n a l c a r o t i d o c c l u s i o n ; O P G - o c u l o p l e t h y s m o g r a p h y ;
AC - anterior communicating;
A&W - alive
and w e l l ; S S - s i p h o n stenosis
creased risk of stroke has been reported in patients with progressive neurologic deficit, positive CT scan and e n d a r t e r e c t o m y [5], surgery within five weeks of acute stroke [6], urgent ipsilateral endarterectomy and positive CT scan [7]. H o w e v e r , endarterectomy has been advised in patients with small, fixed neurologic deficits without any interval surgical delay [8] or as long as a plateau of neurologic recovery has been achieved [9]. Further compounding this issue is the risk of new stroke or extension of the original stroke in the interval between an initial presentation and surgery four to six weeks later. Dosick and associates [4] reported this to be as high as 21% in an initial group and 9.5% in a subsequent group with no mention of the contralateral artery. The subset of patients with neurologic deficit, hemispheric infarction by CT scan, ipsilateral stenosis greater than 90%, or occlusion and contralateral 90% stenosis or bilateral stenosis greater than 90% are particularly compromised. Contralateral endarterectomy to improve ipsilateral flow for maintenance of viability and neurologic stability without sufficient increase of pressure to cause hemorrhagic infarction was accomplished in this group and is the subject of this study.
METHODS In the last 10 years, patients who presented with transient ischemic attacks (TIAs) or mild-to-moderate neurologic deficit underwent initial diagnostic and therapeutic modalities consisting of CT scanning, heparin therapy where appropriate, and arteriography. Patients with severe deficit or decreased level of consciousness were not immediately studied. In those with ipsilateral surgical lesions, if CT scanning were positive for ischemic stroke and if neurologic examination were normal or the deficit minor and fixed, immediate ipsilateral endarterectomy was performed. A subset of 13 patients was identified with significant stable or fluctuating neurologic deficit, CT scans demonstrating hemispheric infarction, and ipsilateral severe carotid stenosis or occlusion with contralateral severe stenosis or bilateral severe stenosis (Table I). All 13 patients had a fixed deficit; in eight it was improving, but in five there was a c o m p o n e n t that fluctuated, then worsened to a baseline deficit. At the discretion of the radiologist, arteriographic study was limited in some patients to digital subtraction arteriographic (DSA) studies of the neck without cerebral visualization. H o w e v e r , there was demonstration of interhemispheric flow in some
254
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patients. In four with internal carotid occlusion and one with severe siphon stenosis, both hemispheres filled arteriographically from the contralateral carotid artery and by oculoplethysmography (OPG) in one. One patient demonstrated preferential flow contralateral to the ipsilateral CT scan positive hemisphere, but not the reverse; one patient demonstrated pericallosal (leptomeningeal) collaterals. No statement could be made referable to intracranial collaterals in the other six patients. All patients had cortical stroke without return of function within three weeks, no previous symptoms, both appropriate and inappropriate lesions, and appropriate cortical infarction by CT scanning, defined as C4b H O A3a Tli by the C H A T system [10]. All patients underwent carotid endarterectomy on the side contralateral to the hemispheric stroke from two to I0 days (average 6.6 days) from onset of symptoms. Seven of the remaining eight patients with ipsilateral stenosis underwent subsequent ipsilateral carotid e n d a r t e r e c t o m y from 42 to I11 days (average 58.4 days) from onset o f symptoms. General, endotracheal, normotensive anesthesia with systemic heparinization and indwelling shunt were e m p l o y e d in all cases; rigorous attention to perioperative and postoperative maintenance of normotension was accomplished with systolic pressures being kept below 160 and above 100 with agents consisting of phenylephrine, dopamine and nitroprusside. Tacking sutures were employed where necessary; no patches were incorporated into arterial closure.
RESULTS This subset of 13 patients is from a total group o f 615 patients who underwent 662 carotid endarterectomies. Thirty day mortality for the entire group was I%; postoperative neurologic deficits occurred in 2.3%. For this subset, mortality and stroke rate was 0%. The five patients with deficits fluctuating from mild to moderate or severe stabilized with persistence of a mild deficit which subsequently improved. The eight patients with stable deficits showed continuing improvement in the ensuing months as well. There was no incidence of neurologic worsening. Of the eight patients with severe ipsilateral carotid stenosis, seven subsequently underwent an unremarkable ipsilateral carotid e n d a r t e r e c t o m y , following interval Coumadin or antiplatelet therapy with no further neurologic sequelae. One patient declined ipsilateral e n d a r t e r e c t o m y and continues to be well 37 months later, with his condition unchanged on ultrasound. No subsequent neurologic deficits have been recorded in these patients. T h e r e have been no interval or subsequent internal
ANNALS OF
VASCULARSURGERY
Fig. 1. Patient No. 1: Computed tomographic scan demonstrating right parietal infarction.
carotid occlusions. In follow-up there have been no neurologic events requiring CT scans.
CASE REPORTS Patient No. 1
A 56-year-old white man, a fireman with a history of coronary artery disease and bilateral carotid bruits, was admitted with left arm and hand weakness. Computed tomographic scan revealed right parietal infarction (Fig. 1), and heparin therapy was initiated. In the next 48 hours, three episodes of progression of left arm and hand weakness to complete paralysis occurred, with resolution back to mild-to-moderate weakness. Arteriography revealed a right internal carotid occlusion and a severe left sided stenosis (Fig. 2). Immediate left carotid endarterectomy was accomplished unremarkably with stabilization of his deficit to the original weakness and subsequent complete clearing in the ensuing three months. Pre- and postoperative OPG findings demonstrated bilateral hemispheric increase in pressures. The patient continued to be well with no further neurologic difficulties, until he died of cardiac disease 61 months later. Patient No. 2
A 77-year-old man was admitted with right arm and hand weakness and expressive aphasia. Heparin therapy was commenced with resolution of his aphasia, but persistence of right arm weakness. Two further episodes in the ensuing 72 hours consisted of progression to almost complete paralysis of the arm with return of function to its original weakness. Computed tomographic scan demonstrated occipitoparietal infarction on the left side (Fig.
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Fig. 4. Patient No. 2: Arteriography revealing bilateral severe carotid stenosis.
3); arteriography revealed bilateral 95% stenosis (Fig. 4) with left hemispheric filling from right leptomeningeal collaterals, with the anterior communicating vessel not patent. Immediate right carotid endarterectomy was performed unremarkably with stabilization of function and no further episodes. His arm weakness resolved within the next two months and left carotid endarterectomy was subsequently accomplished unremarkably. He continues neurologically intact two years later.
DISCUSSION Fig. 2. Patient No. 1: Aortic arch arteriogram demonstrating right internal carotid occlusion and severe left-sided stenosis.
Fig. 3, Patient No. 2: Computed tomographic scan demonstrating left-sided occipitoparietal infarction.
Sachs [11] reported relief of symptoms in both hemispheres with endarterectomy of stenotic carotids associated with contralateral occlusion; Piotrowski and colleagues [9] noted that 12 of 129 patients with "acute stroke" (9.3%) had ipsitateral occlusion and severe contralateral stenosis, with subsequent contralateral endarterectomy, the timing of contralateral endarterectomy not specifically being mentioned. However, this group included patients with retinal strokes, and CT scanning was accomplished in only 77% of the entire group, with findings of not only appropriate cortical infarcts, but also lacunar infarcts or no infarcts. However, the value of immediate contralateral endarterectomy in prevention of interval extension of stroke by increasing collateral flow, as well as improving the safety of subsequent ipsilateral endarterectomy, has not been examined. The extent of revascularization of the CT scanpositive hemisphere with the initial contralateral endarterectomy is unique to the individual patient. Arteriographic definition of the potential anatomic collateral hemispheric flow has been limited in this study, as in others, by considerations of safety and practicality. Digital subtraction arteriography and ultrasound have resulted in less need for the extensive arteriography performed in previous years [12]. The ideal of a second arteriogram following initial
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contralateral carotid endarterectomy to define improved areas of perfusion after correction of a greater than 90% contralateral stenosis for study purposes is obvious, but not clinically indicated. Nonetheless, we were able to demonstrate patency of the Circle of Willis arteriographically in four patients and by OPG in one patient. Post-Willisian leptomeningeal vessels were demonstrated in one further patient. Physiologic definition of collateral hemispheric potential in patients with severe carotid stenosis has been studied with various techniques. Increased bilateral Doppler ophthalmic artery pressure has been identified following unilateral carotid endarterectomy in the presence of significant bilateral occlusive disease [13]. Eikelboom [14] using OPG and collateral ophthalmic artery pressure data noted a correlation which implies decreased collateral flow to the opposite hemisphere from the side of a severe ipsilateral stenosis. Also noted was no certainty of collateral flow as measured by OPG even when anterior or posterior communicating arteries were arteriographically visualized. Increased systolic and diastolic velocities for ipsilateral disease in the presence of severe contralaterat disease has been reported [15]. Transcranial Doppler and carotid compression in 55 patients with unilateral carotid occlusion identified five patients with total and 24 with partial dependence of the contralateral patent carotid vessel for middle cerebral artery flow [16]. Sundt and coworkers [17] measured cerebral blood flow using Xenon 133 and found cerebral blood flow to be increased after correction of carotid lesions greater than 90%; this has been noted to be bihemispheric with initial marked increase in hemispheric flow, but a more moderate global hyperemia as well [18]. The disparity between areas of CT scan positive stroke and symptomatology (such as the patient with occipital infarct with both visual and motor symptoms) can be explained by a zone of neuronal tissue still viable, but nonfunctional, the so-called "ischemic penumbra" [19]. Prompt revascularization in this clinical setting might well afford salvage of these regions. Discrepancies with Xenon 133 between low flow areas on cerebral blood flow tomograms and hypodense areas of infarction on CT scanning have been identified, suggesting these areas are viable, but nonfunctional neuronal tissue [20]. Intracranial hemorrhage following carotid endarterectomy would appear to be multifactorial in origin. The initial report of Wylie and associates [1] has prompted continuing caution with ipsilateral endarterectomy in the face of acute stroke in the hopes of avoiding conversion of an ischemic stroke to intracranial hemorrhage. Correction of an ipsilateral high grade carotid stenosis associated with loss of cerebral autoregulation caused by long-standing severe chronic cerebral ischemia has been noted to
ANNALS OF VASCULAR SURGERY
result in hyperperfusion, theoretically increasing the odds of intracerebral hemorrhage. Pomposelli and colleagues [22] reported postoperative hemorrhage in 11 (0.7%) of 1,500 carotid endarterectomy patients; all had normal coagulation studies; six of 11 patients were normotensive postoperatively. However, postoperative maintenance of normotension has obviously been recommended [23]. The initial contralateral endarterectomy in our patients would place the normal contralateral hemisphere at the normal, low risk for hemorrhage and the abnormal, ipsilateral, CT scan positive hemisphere at uncertain risk. The dampening effect of collateral patterns on pressure and the vigorous maintenance of normotension undoubtedly serve to protect against postoperative hemorrhage. Hafner and coworkers [24] suggested that involvement of multiple extracranial cerebral vessels may increase the risk of postendarterectomy hemorrhage, although only two of 10 of his patients had severe (>90%) bilateral disease. The coexistence of bilateral severe carotid disease has been suggested as a "necessary factor" by Pomposelli [22]. However, contralateral endarterectomy as initial operation has not been suggested prior to the present report for protection from intracranial hemorrhage as well as preservation of viable neurologic tissue. Although it is not possible to differentiate flowrelated stroke from embolic stroke in these patients, the predominant distribution of infarction in our patients to what has been paradoxically referred to as "watershed" areas [25]--and the marked degrees of stenosis--would support a primary flow etiology rather than an embolic one. Postmortem study [26] has identified the crucial role of collateral flow in patterns of hemispheric stroke as it relates to bilateral occlusive carotid disease and the integrity of the Circle of Willis. Torvic and Jorgensen [27] also correlate the size and depth of infarction with the presence and size of Willisian collaterals. The stabilization of our patients with marked neurologic instability, especially those with ipsilateral occlusion, would clinically support revascularization of both hemispheres. This applies beyond doubt in our patient with OPG data. The benign course of those with stable deficits and immediate contralateral endarterectomy and subsequent ipsilateral endarterectomy would also tend to confirm this revascularization as well. This subset of patients, presenting with ipsilateral stroke and bilateral severe carotid occlusive disease, is at high-risk of complications from medical [4] as well as surgical therapy [28]. The surgeon's responsibility extends not only to avoidance of operative complications but to offering relief to patients even if they are in a high risk group. Ipsilateral endarterectomy best restores flow and eliminates an embolic source but in the opinion of
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this author, these potentially beneficial effects are achieved at the prohibitive price of intracerebral hemorrhage and extension of infarction. We believe immediate contralateral endarterectomy improves ipsilateral flow, as evidenced by the neurologic stabilization of our 13 patients as well as by the subsequent safety of ipsilateral endarterectomy. Although the amount of flow through collateral hemispheric patterns is not predictable with present technology, this limitation should not preclude consideration of operation in this high-risk subset of patients.
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