Carotid endarterectomy as stroke prophylaxis

EurJVascSurgl, 371 380(1987)

REVIEW ARTICLE C a r o t i d E n d a r t e r e c t o m y as S t r o k e Prophylaxis Rabbe T a k o l a n d e r and David Bergqvist

Department of Surgerg, University of Lund, General Hospital, MalmS, Sweden

"Because a surgeon tells you he has operated o n a large n u m b e r of patients with a certain rate of success does not necessarily m e a n his choice of treatment was therefore the best choice ..."1 This sentence was quoted by Allan D. Callow in his presidential address to the American Society for Vascular Surgery at its Fourtieth A n n u a l Meeting. 2 In this address was also discussed h o w m a n y problems that trouble us have been solved during the 30 years which have lapsed since the first carotid endarterectomy. The truth is that m a n y crucial questions concerning carotid artery surgery have yet to be answered. However, some lessons have been learnt and this review puts special emphasi s o n indications, techniques and results of carotid artery surgery. Carotid endarterectomy is an attractive therapeutic alternative in patients with transient ischaemic attacks (TIA) since stenoses and occlusions in the internal carotid arteries seem to be a major factor in occlusions of the vascular territory of the middle cerebral artery. 3 There is also evidence that the majority of carotid TIAs are due to atherothromboembolism from the bifurcation of the carotid artery. 4,s Some 50% of patients w h o develop ischaemic strokes have had TIA, 4'6 data varying considerably. 7.8 In patients with carotid TIA a n g i o g r a p h y reveals pathological alterations in the ipsilateral carotid bifurcation in at least 50%. 9,1° In patients with amaurosis fugax the percentage of a b n o r m a l arteriograms is reported even higher. ")'~ In patients with fixed neurological deficits intracerebral arterial lesions seem to be more c o m m o n t h a n in TIA patients. 12 Please address all correspondence to: Rabbe Takolander, Department of Surgery Maim5 General Hospital S 214 01 Malm6, Sweden 0950 821X/87/060371 + 10 $03.00/0 © 1987 Gmne & StrattonLtd

A r o u n d 1 O0 0 0 0 carotid endarterectomies were pertormed in the U.S. during 1984, giving a rate of 4 3 5 endarterectomies/million inhabitants/year. The corresponding frequency for England and Ireland was 2 3 ~3 and for Sweden 37 during 1983.14 In Sweden there are, h o w ever, large variations between different parts of the country. Thus the n u m b e r performed at our hospital during 1983 corresponds to 203 operations/million inhabitants/year, in Great Britain and Ireland endarterectomy because of a carotid bruit in an asymptomatic patient is rare, ~3 as it also is in Sweden. In the U.S. on the other hand, endarterectomy of asymptomatic patients, is m a y in part explain t h e h i g h frequency of operations. It m u s t be emphasised that carotid endarterectomy is a prophylactic form of surgery and the reason for performing it is to remove the source of the embolus, an ulcerated plaque or a tight stenosis. For the individual patient this does not m e a n an improvement but that the risk for potential and statistically calculated neurological events is diminished. Four justifications motivate a carotid endarterectomy: ~6 (1) The lesion at the origin of the internal carotid artery probably caused the preceding TIA, usually by an embolus, occasionally by reduction in the volume blood flow; (2) No other lesion or general disorder should be as likely or more likely to have caused the focal cerebral dis-order; (3) The lesion is likely to cause further TIA or cerebral infarction; (4) The long-term risk of stroke without surgery is

372

Rabbe Takolander and David Bergqvist

higher than the long-term risk with surgery added to the risk of angiography. Although carotid endarterectomy has been performed tbr more than 30 years we still lack the ultimate evaluation of how surgery stands in relation to other methods of stroke prophylaxis after TIA. It is difficult to compare non-surgically and surgically treated patients on the basis of existing publications. In pharmacologically treated series all patients are not subjected to angiography and in most series patients with normal angiograms are included. The conclusion is that pharmacological treatment more often is instituted because of the syndrome TIA while surgical treatment is performed because of a distinct and removable lesion at the carotid artery bifurcation, thought to be the origin of emboli causing TIA. Another difficulty is to establish the natural course after TIA. Whisnant et a1.17 reported a stroke risk of 15% during the first year after TIA and 5%/year thereafter. That study is old and does not necessarily give the present risk situation. Moreover, it is probably impossible to obtain the true natural course today as many patients are treating themselves or are treated by physicians with acetylsalicylic acid and/or dipyridamole in various doses. The use of oral anticoagulants as prophylaxis can be seriously questioned because of the risk for severe haemorrhagic complications, is According to a survey by Jonas 1~ only one randomised study and six non-controlled studies give useful data to review surgical results after carotid endarterectomy in patients with TIA or minor stroke. The reason is the way of reporting surgical series as well as the fact that the series are not "clean", i.e. they include asymptomatic patients as well as patients with TIA or minor stroke. In that part of the joint study which concerned TIA patients 43% had experienced vertebro-basilar ischemia exclusively. 2° There are only 21 published patients with TIA and relevant carotid lesions to compare with. These patients were subjected to angiography and randomised to pharmacological treatment, 21 the patient population being too small to draw valid conclusions. Thus today it is not possible to decide whether surgical or pharmacological prophylaxis should be recommended. Many authors have therefore proposed a new randomised trial in order to settle the question. Such a study is now in progress in Europe. The European Carotid Surgery Trial will randomise around 1000 patients to one group where carotid artery surgery is performed as soon as possible and another group where surgery is avoided as long as possible, thus a rather pragmatic attitude. During follow-up, deaths, cerebrovascular events and myocardial infarctions will be registered. = However, during the years which have lapsed since 1954, when the endarterectomy of the internal carotid EurJ VascSurg Vol 1, December1987

artery giving the greatest impetus tbr this kind of surgery was reported, 23 some facts have accumulated about the risks of the operation and the effects on patients during follow-up. The ideal candidate for carotid endarterectomy seems to be the symptomatic patient with little or no permanent deficit, who is otherwise in good health, has a carotid artery stenosis of at least 5 0 - 6 0 % or an ulcerated plaque in the appropriate artery and minimal other atherosclerotic manifestations. 24 However, as atherosclerosis is a universal disease patients undergoing carotid artery surgery often have several signs of arteriosclerosis. Some 60% are hypertensive, 40% suffer from coronary artery disease and bilateral carotid artery lesions are common.

Definitions One great difficulty when analyzing publications on prophylaxis and treatment of patients with TIA or minor stroke is the variations in and sometimes lack of definitions. It is of great importance to use uniform definitions concerning symptoms, pathological findings, details of treatment and the time course. Courbier 2s suggested a classification based on symptomatology: The term TIA should be restricted to symptoms disappearing within 2 4 h . Reversible transient stroke describes the condition which lasts more than 2 4 h but is totally reversible within 3 weeks. Symptoms lasting longer are classified as established stroke. An abrupt increase in frequency or severity of TIA is called a crescendo TIA (CTIA). 26 A progressing stroke is a stroke that either progresses over a period of at least 24 h without waxing and waning but with a gradual increase in deficit which is called a stroke in evolution, or a neurological deficit that temporarily may improve but never clears completely with a pattern of waxing and waning signs called a fluctuating stroke. 2~' As for postoperative complications the time for their occurrence and the exact symptomatology and cause are important to document.

Indications Patients with amaurosis fugax and carotid territory TIA comprise the largest and best characterised group where carotid endarterectomy can be recommended. Patients with minor established strokes may be operated upon after a free interval of 3-6 weeks, 27 2~ but in cases where no signs of infarction on a cerebral CT can be

Carotid Endarterectomy

shown, the operation may be performed earlier after the stroke. 30 As mentioned elsewhere carotid endarterectomy in patients with previous stroke is not as successful as in non-stroke patients and the merit of surgery in these patients remains controversial. In patients with CTIA or progressing stroke there is no consensus on indications for surgical intervention. Good results have been reported by several authors but the need for controlled trials evaluating the role of surgery is great. Carotid thrombendarterectomy for vertebrobasilar ischaemia (VBI) is also controversial. 31-34 The role of carotid endarterectomy in asymptomatic patients has not been clarified and new clinical trials have been welcomed, is

The nature of t h e plaque Intraplaque haemorrhage, which can be detected with ultrasound scanning, seems to be an important manifestation of significant carotid artery disease. Reilly et al. 3s found that a plaque appeared heterogeneous in 80% of cases with haemorrhage and fibrous plaques showed a more homogeneous structure. Riles et al.36 and Lusby et al. 37 showed a significantly higher frequency of recent haemorrhage in the plaques in symptomatic than in asymptomatic patients and theretbre Lusby et al. 37 claimed it was possible to differentiate between dangerous and less dangerous plaques. Persson 3s did not find the same striking difference in intraplaque h a e m o r r h a g e between symptomatic and asymptomatic patients. Among the asymptomatic plaques, however, only 5 of 62 had a connection between h a e m o r r h a g e and the arterial lumen compared with 66 of 98 among the symptomatic plaques. Duplex scanning, originally thought to be an adjunct to angiography which is the gold standard in the diagnosis of carotid artery lesions, has developed into a highly accurate tool. It has been shown, retrospectively, that angiography did not add any significant information in the preoperative evaluation of the patient.S9 Furthermore it has been proposed that angiography is not necessary or is unwarranted under certain circumstances before carotid endarterectomy when high quality ultrasonographic imaging combined with Doppler analysis is available. 4° Haemorrhage ha a plaque, which seems to be a risk factor, is difficult to treat pharmacologically and surgery is therefore a rational alternative. Acetylsalicylic acid (in doses from 3 2 5 - 1 3 0 0 rag/day) m a y allow carotid artery disease to progress to a dangerous state by diminishing symptoms of progressive atherosclerosis, possibly by inhibition of arterial prostacyclin. 41 Whether or not drugs

373

which influence the haemostatic mechanism increase the risk for intraplaque haemorrhage is not k n o w n and can only be speculated on. The sign of plaque rupture is ulceration, which m a y be recognised on ultrasound scanning or angiogram. Ulceration is, however, notoriously difficult to demonstrate. Eikelboom et al., 42 comparing angiogram with surgical specimens, found an overall accuracy of the angiogram of 6 7%. Ulcers as found on surgical specimens were retrospectively detectable on angiography in only 2 5%.4s Ultrasound scanning seems better than angiography to demonstrate ulcerations. 39,44 Symptoms of focal cerebral ischaemia are more likely to be related to ulceration with thromboembolism than to hemodynamicafly significant lesions. 45,46 In order to symptomatically reduce cerebral blood flow, neglecting any collateral cerebral circulation a stenosis greater than 75% of the diameter or 94% of the area m a y be necessary. 47 The risk of stroke seems enhanced when there is also an intracerebral siphon lesion or anatomical anomalies of the circle of Willis'. 12 Intracranial physiology can be evaluated with the intracranial Doppler.

O p e r a t i v e risks In speciafised centres carotid endarterectomy can be performed with a mortality of 1-2% and a frequency of operative permanent deficits of 3-5%. In their survey of 16 reports of carotid endarterectomy West et al. 48 found an operative mortality of 3.4 (0-11.2%) and a frequency of operative permanent deficits of 5.7% (0.8 27) among 3820 operations performed on 3233 patients during the period 1 9 6 8 - 1 9 7 7 . It has generally been claimed that the more experienced the surgical team becomes in treating patients undergoing carotid endarterectomy the better are the results. 21,49 Carotid artery surgery performed by occasional vascular surgeons m a y subject patients to extraordinary risks,S°,whereas others have stated that the frequency of operations does not seem to influence the outcome, sl,52 In centres with a low frequency of operations one may speculate that only the worst cases are referred to surgery. Units with a larger number of operations probably get a selection of easier cases. This situation is, however, very difficult to define. There is also a trend towards better results in the compilation of 21 series during the years 1 9 7 5 - 1 9 8 5 shown in Table 1 (none included in the material of West et al.). The m e a n operative pro-cedure mortality was 1.8% and the frequency of operative strokes 3.1%. Our operative mortality during the years 1 9 7 1 1982 was 2.9% with a trend towards better results. DurEurj VascSurg Vol l. December1987

374

Rabbe Takolander and David Bergqvist

Table 1.

No. of operations

Transient deficit

Stroke

Patient mortality

Procedure mortality

No. of patients

No.

%

No.

No.

%

No.

%

10

9.6

6

5.7

8

9

8

9

3.5

4

2.0

12

2

2.5

0

%

Author

Year

(53)

Lindberg et al.

1975

104

9(1

(54)

Nunn

1975

234

188

(11)

Mungas et al.

1977

8(1

80

(55)

Cornell

1978

122

100

3

2.4

2

1.6

4

(56)

Stanfordetal.

1978

187

154

5

3

4

*

0

(57)

Dukeetal.

1979

157

134

6

3.8

5

3.2

2

1.5

2

1.3

(58)

Haynesetal.

1979

276

232

4

1.4

3

1.3

3

1.0

(59)

Rfickert et al.

1979

100

90

3

3

0

0

(60)

Owensetal.

1980

121

113

5

4.1

0

0

(61)

Lyeetal.

1980

186

161

10

5.3

1

0.6

1

0.5

(62)

Watson

1981

140

140

8

5.7

1

0.7

l

0.7

(63)

Eriksson et al.

1981

88

88

2

2.2

2

2.2

2

2.2

(64)

WhiteetaL

1981

118

104

1

1

1

0.8

(65)

Lees etal.

1981

390

335

(66)

Bernstein et al.

1983

456

(67)

Whisnant et al.

1983

(68)

Tuchmann et al.

(51)

3

5.1

0 4.0

4

3.2

0

5.3

4

1.8

4

1.5

370

15

3.3

4

1.0

4

0.8

15l

151

5

3

1

0.6

1

0.6

1984

186

142

4

4

2

7

4,9

7

3.8

Slavishetal.

1984

743

743

26

(69)

Bunt et al.

1985

200

200

(70)

Raithel et al.t

1985

244

244

(71)

Hertzeretal.

1985

335

335

4618

4194

7

2.3

12

21

Totally

9

1.6

6.3

2 3.5

2.8

145

13

1.8

20

2.7

20

2.7

3

1.5

3

1.5

3

1.5

8

3.3

5

2.0

5

2.0

21

6.3

6

1.8

6

1.8

3.1

84

2.0

84

1.8

*Stroke 13%, TIA 1.3% "~Allpatients with contralateral occlusion of the carotid artery.

ins the years 1983-1985 it w a s 0 . 8 % . N o n - f a t a l n e u r o l o g i c a l deficits i n c o n n e c t i o n w i t h t h e o p e r a t i o n o c c u r r e d in 4.8% 1971-1982. T h e series c o m p i l e d b y W e s t et al. a n d i n T a b l e 1 a r e not homogeneous as to t h e i n d i c a t i o n s for s u r g e r y . G e n e r a l l y TIA p a t i e n t s fare b e t t e r b o t h c o n c e r n i n g o p e r a tive m o r t a l i t y a n d m o r b i d i t y . I n t h e l a r g e series r e p o r t e d b y T h o m p s o n 72 w i t h 1 2 5 9 o p e r a t i o n s p e r f o r m e d i n 1 0 0 0 patients (1978) the TIA patients had an operative mort a l i t y of 0 , 8 % , w h i l e t h o s e w i t h a p r e o p e r a t i v e n e u r o l o g i c a l deficit h a d a n o p e r a t i v e m o r t a l i t y of 5 . 7 % . S t a n f o r d et al. s6 s h o w e d a s t r o k e f r e q u e n c y of 1 . 3 % i n T I A EurJ Vasc Surg Vol 1, December 1987

patients and 13% in patients with preoperative neurol o g i c a l deficits. I n t h e m a t e r i a l f r o m o u r h o s p i t a l ( 1 9 7 1 1 9 8 2 ) t h e s t r o k e p a t i e n t s h a d a m o r t a l i t y of 5 . 9 % a n d t h e s a m e f r e q u e n c y of p e r m a n e n t o p e r a t i v e n e u r o l o g i c a l deficits. T h e T I A p a t i e n t s h a d a m o r t a l i t y of 1 . 4 % a n d a freq u e n c y of o p e r a t i v e p e r m a n e n t deficits of 3 . 9 % . Patients with bilateral carotid artery stenoses have b e e n r e p o r t e d to h a v e a h i g h e r r i s k of o p e r a t i v e s t r o k e s . 22,s4,ss'73 S o m e a u t h o r s , h o w e v e r , a r e of t h e o p i n i o n t h a t t h e d e g r e e of p a t h o l o g i c a l i n v o l v e m e n t of t h e c o n t r a l a t e r a l a r t e r y d o e s n o t h a v e a n y i m p l i c a t i o n for p o s t o p e r a t i v e p r o b l e m s b u t t h a t t h e c l i n i c a l c o n d i t i o n of

Carotid Endarterectorny

the patient has, i.e. the presence of permanent neurological deficits preoperatively. 74 it has been shown that patients with a totally occluded contralateral carotid artery m a y undergo a carotid endarterectomy with a morbidity and mortality comparable with that in patients without a contralateral occlusion. 75-77 In patients with stenosis on one side and occlusion on the contralateral, carotid endarterectomy of the stenotic side should be performed first since most of the patients are then relieved of symptoms. Only in cases remaining symptomatic should an extracranialintracranial (EC/IC) bypass should be considered.7S'77 The risks of surgery (myocardial infarction excluded) mainly consist of peroperative embolisation and postoperative occlusion with or without concomitant embolisation. Cerebral infarction due to a low perfusion because of temporary clamping seems to be rare. The majority of problems in connection with the operation are due to embolisation, no relation between the duration of clamping and the occurrence of operative neurological deficits being found. 43 In order to protect the brain during carotid artery clamping an intraluminal shunt is the method of choice. The shunt is always used by some surgeons, never by some, and in a selective way by most, and good results have been claimed by all. One reason is probably that surgeons do best with the technique they are most used to. Another reason m a y be that a shunt is in reality only rarely indicated. In order to selectively use the shunt, some surgeons perform the endarterectomy under local anaesthesia. The development of neurologic deficits with carotid clamping in the conscious patient appears to be a reliable indicator for the selection of patients needing a shunt.78,79 Carotid endarterectomy under local anaesthesia m a y be a stress factor, shown by higher cathecolamine levels in the blood during the operation, s° which may be responsible for significantly higher blood pressures in the local anaesthesia group. 80.al Peroperative embolisation is avoided by a meticulous technique. In order to check the anatomical and physiological result of the endarterectomy intraoperative angiography, Doppler spectrum analysis, duplex scanning and electromagnetic flow measurements have been employed. With intraoperative angiography or Doppler spectrum analysis both mortality and stroke rates have been reduced, sx s4 With duplex scanning both morphological and functional problems in the operative field can be evaluated. 8s-s7 Ocular pneumoplethysmography has been used to detect immediate postoperative occlusions, ss When patients develop neurological symptoms after an interval in the immediate postoperative period an aggressive surgical approach with emergency re-exploration has given good results. Prompt thrombectomy (within 4 h ) can

375

totally restore more than 50% of these patients, s9-92 In cases with fluctuating neurology angiography, if performed immediately, m a y be of value in the decision to reoperate.

Possible benefits f r o m surgery After carotid endarterectomy the m e a n stroke frequency varies between 1 and 1.7%/year on the operated s i d e . f'6'67'71'9~'94 Among patients operated on at our hospital the mean stroke frequency was 2.5%/year on the ipsilateral side, operative deficits included. Twenty-eight percent of the patients in this series had preoperative permanent neurological deficits. The stroke frequency from 6 months up to 8 years postoperatively was l % / y e a r ipsilaterally and 0.4% on the non-operated side. Thus the first 6 months postoperatively carries the highest risk for development of new neurological deficits. The cause is multifactorial and every measure must be taken to diminish the frequency. One way may be pharmacological prophylaxis, for instance with platelet inhibitors. Surgery for CTIA or progressing stroke demands great efforts by a team of neurologists, radiologists, and surgeons to cope with the challenge to stop the progress of a stroke. No comparative studies between surgery and conservative treatment have been performed and only historical controls can be used. Thus, in a series of 204 conservatively treated patients with progressing strokes 69% became hemiplegic, 14% died and only 12% returned to normal 14 days after the onset. 9s In the series reported by Greenhalgh et al. 26 progression of stroke was arrested in all 15 patients after surgery and in the CTIA group good results were seen in 6 out of 7 patients. One patient in the latter group died. In the series reported by Gotdstone and Moore 96 each of 26 patients (8 with CTIA and 18 with progressing stroke) made a "dramatic and complete" neurological recovery after operation. Mentzer et al. 97 reported 55 cases with fluctuating neurological deficits 24 of w h o m were operated on and 31 treated non-operatively. Seventy percent improved in the surgical group compared with 11% in the nonoperated group (P < 0.01). From the literature, Mentzer e t al. compiled 190 operated cases with progressing strokes and found that 55% recovered compared with 23% in a group of 263 cases with progressing stroke treated nonsurgically. Although no controlled randomised trial has been performed regarding this very special group of patients it seems possible that surgical intervention in cases with CTIA and progressing stroke might be of value. To be considered for surgery the patient has to have a mild deficit, no infarction on CT scan and a patent internal carotid artery. After a minor stroke surgery m a y Eur ] VascSm'gVol l, December1987

376

Rabbe Takolander and David Bergqvist

be a good choice since survivors of stroke have a high rate of recurrent stroke and the mortality rate with subsequent stroke is higher than with the initial stroke. 98'99 Furthermore, after minor stroke the risks with long-term anticoagulant therapy makes this kind of treatment doubtful. ~8 In a retrospective study McCullough et al. ~°° have shown that patients operated on after established stroke fared better than those treated conservatively. Follow-up to 6 years revealed that all of the surgically treated patients remained free from new deficits compared with 58% of the medically treated group. However, none of the medically treated patients had undergone angiography. In a review of 474 patients with established strokes treated with carotid endarterectomy McCullough ~°° found an operative mortality of 6.3% and 4.9% incidence of operative neurologic defects. During follow-up (6 m o n t h s - 1 3 years) neurologic deficits were found in 9.2%. For comparison 1472 patients treated pharmacologically were collected from the literature. During a follow-up of 6 - 1 5 years there was a 25% frequency of fatal recurrent strokes and a 35% overall frequency of recurrent neurological deficits. In our material of 3 52 patients the yearly stroke frequencies on the endarterectomised side were similar in patients with and without preoperative stroke. According to Thompson 72 it appears that endarterectomy lowers the frequency of recurrent strokes in patients with mild, stable strokes. Good results with carotid endarterectomy for vertebro-basilar ischaemia have been described by several authors. However, it seems as if patients with vertebro-basilar ischaemia (VBI) and arteriographic evidence of intracranial disease are at higher risk for cerebral ischaemia during endarterectomy. 3s The use of an intraoperative shunt has frequently been advocated in these patients. A prerequisite for successful surgical results in patients with VBI and carotid lesion seems to be the visualisation of the posterior communicating artery. ~°~ Moreover, oculoplethysmography (OPG) m a y be a useful test to determine which patients with VBI benefit from carotid endarterectomy. 702 In non-operated asymptomatic patients with a carotid bruit the stroke risk seems to be between 1.7 and 2.3% per year. 1°s'1°4 In addition to a slightly increased stroke risk, these patients have a significantly increased cardiac risk. In one series 30% of patients with an asymptomatic bruit died during a 3-year period, mostly from myocardial infarction, l°s The stroke risk does not warrant surgery but an expectant attitude with operation if the patient becomes symptomatic. When a bruit is accompanied by a 50% stenosis a higher risk of TIA and stroke has been found. 1°6'1°7 In order to be included among truly asymptomatic patients a clear CT scan EurJ VascSurg Vol 1, December1987

seems to be obligatory since a high frequency (19%) of silent infarcts has been recorded in a prospective study, lO8 Most silent infarcts in an inappropriate hemisphere were accompanied by severe atheroma of the carotid artery supplying that hemisphere. "~8 If a high-risk group of patients with a spontaneous stroke risk of over 5%/year can be identified surgery might be beneficial 1°9 provided the surgical unit can document a low peroperative complication rate. There is some evidence that patients with a stenosis of over 75% develop ischaemic symptoms at a rate higher than 5%/year.ll°.11~ But to justify surgical intervention on asymptomatic patients optimal results must be achieved. 112 In patients with symptoms of embolisation, with occlusion of the ipsilateral internal carotid artery and stenosis or ulceration of the external carotid artery, reconstruction of the external carotid artery is indicated. In these cases the external carotid artery constitutes a major pathway for the cerebral circulation as well as for embolisation. Reconstruction of the ulcerated external carotid artery or oversewing of the blind stump has been shown to inhibit the TIA.113-119 It has also been established that low flow syndromes m a y disappear and the need for a planned extracranial-intracranial (EC/IC) bypass m a y be eliminated. 120

A

contralateral

asymptornatic side

non-operated

Risk factors for the development of symptoms on the side contralateral to endarterectomy seems to be hypertension, a stenosis of more t h a n 80% or a large ulcer, 121-~23 but the bad prognosis for the contralateral ulcerated carotid artery has been questioned. T M It must be observed though, that the contradictory studies are not entirely comparable since the study with the more favourable outcome seems to have included patients with more benign lesions.

Recurrences It has previously been suggested that the value of surgery is decreased in patients with lesions in the petrous or cavernous portion of the internal carotid artery. The relief of symptoms, however, is similar in patients with and without tandem lesions, and there is no relation between the severity of siphon disease and recurrent symptoms following bifurcation endarterectomy. 125,126 There is also some evidence that siphon stenosis m a y be of embolic ori-

Carotid Endarterectomy

gin and may disappear after bifurcation endarterectomy. 127 Female gender, hypertension, symptoms at an early age and postoperative smoking are risk factors for recurrence. ~2s'129 The true incidence of recurrence has yet to be determined. It is, however, clear that there is no correlation between anatomic and symptomatic recurrence. 130,131 Depending on which non-invasive method is used asymptomatic recurrent disease may be detected in 6.7-19%. 132-14o Symptomatic recurrence has been reported in 0 . 6 - - 3 % . 141-t44 Early (2 years) recurrence seems to be the result of neo-intimal hyperplasia whereas later recurrences more often show the features of atherosclerosis, indicating probable recurrence. 14s The wellbeing of the patient suggests a conservative approach in asymptomatic patients as long as the stenosis is not greater than 75~/o. 136

Survival Myocardial infarction is the dominating long-term cause of death in patients with TIA independent of whether treatment has been surgical or pharmacological. Endarterectomy does not prolong the life of the patient. The presence of coronary artery disease gives a significantly lower survival after carotid endarterectomy and the difference is significant in comparison with patients who do not have signs of coronary artery disease at the time of operation. 43 In our material the survival of patients without coronary artery disease was comparable with the survival of an age and sex matched normal population. Bilateral carotid artery lesions indicate a more advanced arteriosclerotic disease, also in the coronary arteries, and this is reflected in a significantly lower survival (Unpublished observations Malm6 General Hospital 1986).

Conclusions Carotid endarterectomy in patients with TIA from the relevant vascular territory is an effective way to prevent stroke in the long run, provided the operation can be performed with a low combined mortality and neurological morbidity. Surgery can be performed with a mortality around 1% and a morbidity below 3% with a total yearly stroke frequency during the postoperative follow up of less than 2%/year and on the ipsilateral side between 1 1.7%/year. With such results surgery seems an acceptable prophylactic method. The place for surgery in relation to pharmacological treatment is not possible to

377

establish today, and only a prospective randomised comparison between the two alternatives can give an adequate answer. The natural course of a symptomatic carotid artery stenosis may never be possible to establish. To leave patients without prophylaxis after the diagnosis of a symptomatic carotid artery stenosis seems unethical today since good results have been reported both with pharmacology and surgery. The maximal acceptable rate of peroperative complications to justify surgery is very difficult to establish by analysing various retrospective series. Hass and Jonas 146 estimated this rate to be below 3%. Quinones-Baldrich and Moore m47 mentioned the limits as a mortality of 1% and a morbidity of 3%. However, Hass and Jonas 146 admitted that "had no postoperative deaths or strokes occurred, surgical treatment would be clearly superior to medical treatment". To conclude, if surgery is considered it should be performed in centres with surgeons familiar with the problems concerning carotid artery surgery to minimise the risks of the procedure.

References 1 SALZMANEW. Is surgery worthwhile? Arch Surtl 1 9 8 5 ; 1 2 0 : 7 7 1 776. 2 CALLOWAD. Presidential address: The microcosm of the arterial w a l l - - A plea for research. J Vasc Surg 1987;5:1-18. 3 L'HERMITTE F, GAUTIERJC, DEROUESNEC. Nature of occlusions of the middle cerebral artery. Neurology 1 9 7 0 ; 2 0 : 8 2 - 8 8 . 4 BARNETT HJM. Progress towards stroke prevention. Robert Wartenberg Lecture. Neurology 1 9 8 0 ; 3 0 : 1 2 1 2 - 1 2 2 5 . 5 HARRISON MJG. Pathogenesis. In: Warlow C, Morris PJ, eds Transient Ischemic Attacks. New York: Dekker, 1 9 8 2 ; 2 1 4 6 . 6 PESSIN MS, MINTON RC, DAVIS KR, et aI. Mechanisms of acute carotid stroke. Ann Neurol 1 9 7 9 ; 6 : 2 4 5 - 2 5 2 . 7 BARNETTHJM. Transient cerebral ischemia-pathogenesis, prognosis and m a n a g e m e n t . Ann R Coll Ph!ts Surg Can 1 9 7 4 ; 7 : 1 5 3 - 1 7 3 . 8 WmSNANT JP. The decline of stroke. Stroke 1 9 8 4 ; 1 5 : 1 6 0 - 1 6 8 . 9 HARRISONMJG, MARSHALLJ. Indications for angiography and surgery in carotid artery disease. Br IViedJ 1975; 1:616-617. 10 EISENEERC RL, NEMZFJ~WR, MOOREWS, MANI RL. Relationship of transient ischemic attacks and angiographically demonstrable lesions of the carotid artery. Stroke 1 9 7 7 ; 8 : 4 8 3 - 4 8 6 . 11 MUNOAS JE, BAKER WH. Amaurosis fngax. Stroke 1977;8:232 235. 12 THIELE BL, YOUNG JV, CHIKOS PM, HlaSCH JH, 8TRANDNESSDE. Correlation of arteriographic findings and symptoms in cerebrovascular disease. Neurology 1 9 8 0 ; 3 0 : 1 0 4 1 - 1 0 4 6 . 13 MuruE JA, MORRISP]. Carotid endarterectomy in Great Britain and Ireland. Br J Surg 1 9 8 6 : 7 3 : 8 6 7 - 8 7 0 . 14 BERGQVIST D. Enkfit om svensk kfirlkirurgi 1983: Antalet operationer b a r 6kat m a r k a n t m e n ~innu ~ir behovet troligen inte tiickt Lfikartidn 1 9 8 5 ; 8 2 : 3 4 9 0 - 3 4 9 1 . 15 BARNETT HJM, PLUM F, WALTONJN. Carotid e n d a r t e r e c t o m y - - a n expression of concern. Stroke 1 9 8 4 ; 1 5 : 9 4 1 - 9 4 3 . 16 WaRLOW CH. Carotid endarterectomy: Does it work? Stroke 1984; 15:1068-1076. 17 WHISNANT JP, MATSUMOTON, ELVEBACKLR. Transient cerebral ischemic attacks in a community, Rochester, Minnesota, 1955 t h r o u g h 1969. Mayo Clin Proc 1973;48:] 9 4 - 1 9 8 .

Eurl VascSurg Vol 1, December 1987

378

Rabbe Takolander and David Bergqvist

18 LEVINEM, HIRSH J. Hemorrhagic complications of long-term anticoagulant therapy for ischemic cerebral vascular disease. Stroke 1986;17:111-116. 19 JONAS8. IMPS (Intact m o n t h s of patient survival): An analysis of the results of carotid endarterectomy. Stroke 1 9 8 6 ; 1 7 : 1 3 2 9 1334. 20 FIELDS WS, MASLENIKOV V, MEYER JS, HASS WJ, REMINGTON RD, McDONALD M. Joint study of extracranial arterial occlusion. V. Progress report of prognosis following surgery or non-surgical treatment for transient cerebral ischemic attacks and cervical carotid artery lesions. JAMB 1970;211:1933-2 O03. 21 SHAWDA, VENABLESGS, CARTLIDGENEF, BATESD, DICKINSONPH. Carotid endarterectomy in patients with transient cerebral ischemia. ] Neurol Sci 1 9 8 4 ; 6 4 : 4 5 - 5 3 . 22 European Carotid Surgical Trial. Protocol, June 1985. 23 EASTCOTTHHG, PICKERING GW, ROB CH G. Reconstruction of internal carotid artery in a patient with intermittent attacks of hemiplegia. Lancet 1 9 5 4 ; 2 : 9 9 4 - 9 9 6 . 24 BYERJA, EASTONJ1). Therapy of ischemic cerebrovascular disease. Ann lnt Med 1 9 8 0 ; 9 3 : 7 4 2 - 7 5 6 . 25 CotmmEg R. Basis for a n international classification of cerebral arterial diseases. ] Vase Surg 1 9 8 6 ; 4 : 1 7 9 - 1 8 3 . 26 GREENHALGHRM, McCoLLUM CN, BOURKEBM, DAIN R, PERKIN GD, ROSE FC. Emergency carotid endarterectomy. In: Bergan J, Yao ] eds Vascular Surgical Emergencies. Grune & Stratton, 1987;139 151. 27 WYLIE El, EHRENFELDWK. Surgical indications and contraindications. In: Wylie EJ ed. Extracranial Occlusive Cerebrovascular Disease. Philadelphia: Saunders, 1 9 7 0 : 1 2 1 - I 29. 28 ROB C. The origin and development of surgery for occlusive disease of the carotid arteries. Rev Surg 1972;29:1-6. 29 FIELDS WS. Selection of patients with cerebrovascular disease for arterial surgery. World] Surg 1 9 7 9 ; 3 : 1 4 7 - 1 5 4 . 30 DOSICKSM, WHALEN RC, GALE SS, BROWNOW. Carotid endarterectomy in the stroke patient: Computerized axial tomography to determine timing. ] Vase Surg ] 9 8 5 ; 2 : 2 1 4 - 2 1 9 . 31 MCNAMARAJO, HEYMAN A, SILVER D, MANDEL ME. The value of carotid endarterectomy in treating transient cerebral ischemia of the posterior circulation. Neurologg 1977;27:682-684. 32 BARDINJA, BERNSTEINEF, HUMBERPB, et al. Is carotid endarterectomy beneficial in prevention of recurrent stroke? Arch Surg 1982; 117:1401 1407. 33 FORD ]], BAKER WH, EHRENItAFT JL. Carotid endarterectomy for nonhemispheric transient ischemic attacks. Arch Surg 1975;110: 1314-1317. 34 ROSENTAHLD, COSSMAND, LEDIG B, CALLOWAD. Results of carotid endarterectomy for vertebrobasilar insufficiency. Arch Surg 1978; 113:1361-1364. 35 REILLYLM, LUSBYRJ, HUGHESL, FERRELLLD, STONEYR], EHRENFELD WK. Carotid plaque histology using real-time ultrasonography clinical and therapeutic implications. Am ] Surg 1 9 8 3 ; 1 4 6 : 1 8 8 193. 36 RILES TS, BAUMANNFG, MINTZE~ R, IMPARATOAM. The significance of intramural hemorrhage in the carotid bifurcation plaque. (Abstract). Stroke 1982;13:124. 37 LESBY RJ, FERRELL LD, EHF,ENFELD WK, STONEY RJ, WYLIE EI. Carotid plaque haemorrhage. Its role in production of cerebral ischemia. Arch Surg 1 9 8 2 ; 1 1 7 : 1 4 7 9 - 1 4 8 8 . 38 PERSSON AV. Intraplaque hemorrhage. Surg Clin N Am 1986;66: 415-420. 39 WALSHJ, MARKOWlTZI, KERSTEINMD. Carotid endarterectomy for amaurosis fugax without angiography. Am J Surg 1986; 152:172174. 40 CREWJR, DEAN M, JOIINSON IM, KNIGHTOND, BASHOURTT, ELLERTSOND, HANNA ES. Carotid surgery without angiography. Am ] Surg 1984;148:217-220. 41 CARSON SN, DEMLING RH, ESO_UIVELCO. Aspirin failure in symptomatic atherosclerotic carotid artery disease. Surgery 1981;90: 1084-1092, 42 EIKELBOOMBC, RILES TR, MINTZER R, et al. Inaccuracy of angiography in the diagnosis of carotid ulceration. Stroke 1983;14: 882-885. EurJ Vase Surg Vol 1, Decenlber 1987

43 TAKOLANDERR], ERICSSONBF, BERGENTZS-E. Reconstruction of the carotid artery. A review of 167 operations. Acta Chit Scand 1981; 147:173-178. 44 BORNMYRS, ]UNGQVISTG,, OLIVECRONAH, TAKOLANDERR, BF~GQVIST D, LINDELLS-E. Ulcerations in the carotid bifurcation. A diagnostic problem. Acta Chir Scand 1 9 8 6 ; 1 5 2 : 4 9 9 - 5 0 1 . 45 MOOREWS, HALL AD. Importance of emboli from carotid bifurcation in pathogenesis of cerebral ischemic attacks. Arch Surg 1970; 101:708-716. 46 BARTYNSKIWS, DARBOUZEP, NEMIS P JR. Significance of ulcerated plaque in transient cerebral ischemta. Am J Surg 1981 ;141: 353. 47 ARCHIE]P, FELDTMANRW. Critical stenosis of the internal carotid artery. Surgery 1981;89:67-72. 48 WESTH, BURTONR, ROONAJ, MALONEJM, GOLDSTONEJ, MDOREW8. Comparative risk of operation and expectant m a n a g e m e n t for carotid artery disease. Stroke 1979;10:117 121. 49 FODEN, SUNDTTM, ROBERTSONIT, PEERLESS SJ, SHIELDS CB. Multicenter retrospective review of results and complications of carotid endarterectomy in 1981. Stroke 1 9 8 6 ; 1 7 : 3 7 0 - 3 7 6 . 50 EASTON JD, SHERMAN DG. Stroke and mortality rate in carotid endartereetomy: 228 conservative operations. Stroke 1977;8: 565-568. 51 SLAvlss LG, NtCHOLAsCG, GEEW. Review of a community hospital experience with carotid endarterectomy. Stroke 1 9 8 4 ; 1 5 : 9 5 6 959. 52 KEMPCZINSKIRF, BROTTTG, LABUTTAR]. The influence of surgical specialty and caseload on the results of carotid endarterectomy. ] Vase Surg 1 9 8 6 ; 3 : 9 1 1 - 9 1 6 . 53 LINDBERGB, NORBJi.CKB, NVENDSENP, SYNCKV. Carotid endarterectomy: A review of 104 operations. ] Cardiovasc Surg 1 9 7 5 ; 1 6 : 1 6 1 170. 54 NUNN DB. Carotid endarterectomy: An analysis of 234 operative cases. Ann Surg 1975;182:733-738, 55 CORNELL WP. Carotid endarterectomy: Results in 100 patients. Ann Thoracic Surg 1 9 7 8 ; 2 5 : 1 2 2 - 1 2 6 . 56 STANFORDJR, LUBOWM, VASKOIS. Prevention of stroke by carotid endarterectomy. Surgery 1 9 7 8 ; 8 3 : 2 5 9 - 2 6 3 . 5 7 DUKELJ, SLAYMAKEREE, LAMBERTWC, WRIGHT CB. Carotid arterial reconstruction: Ten-year experience. Am Surg 1979;45:281 288. 58 HAYNESCD, DEMVSEYRL. Carotid endarterectomy. Review of 276 cases in a c o m m u n i t y hospital. Ann Surg 1979;189:758-762. 59 R0CKERT U, ALSTAEDT F, SCHELD F, TREDE M. Ergebnisse nach Carotis-Rekonstruktion. Deutsch Med Wochenschrift 1979;104: 428-431. 60 OWENSML, ATKINSON]B, WILSON SE. Recurrent transient ischemic attacks after carotid endarterectomy. Arch Surg 1 9 8 0 ; 1 1 5 : 4 8 2 486. 61 LYE CH R, DOWNSAR. Carotid endarterectomy: Early and late results in 171 patients. Can J Surg 1 9 8 0 ; 2 3 : 5 3 6 - 5 4 0 . 62 WATSONMR. Carotid endarterectomy in a small c o m m u n i t y hospital. Am ] Surg 1981 ; 1 4 1 : 5 4 3 - 5 4 5 . 63 ERIKSSONS-E, LINKH, ALlVlA, R~.DBERGC, KOSTULASV. Results from 88 consecutive prophylactic carotid endarterectomies in cerebral infarction and transitory ischemic attacks. Acta Neurol Scand 1981 ;63:209-219. 64 WHITE JS, SIRINEKKR, Roo'r D, RODGERSW. Morbidity and mortality of carotid endarterectomy. Rates of occurrence in asymptomatic and symptomatic patients. Arch Surg 1981;116:409 412. 65 LEES CD, lrIERTZER NR. Postoperative stroke and late neurologic complications after carotid endarterectomy. Arch Surg 1981 ; 116: 1561-1568. 66 BERNSTEIN EF, HUMBER PB, COLLINS GM, DILLEY RB, DEWN JB, STUART SH. Life expectancy and late stroke following carotid endarterectomy. Ann Surg 1 9 8 3 ; 1 9 8 : 8 0 - 8 6 . 67 WHISNANT ]P, SANDOKBA, SUNDTTH M. Carotid endarterectomy for unilateral carotid system transient cerebral ischemia. Mayo Clin Proc 1983;58:171 175. 68 TUCHMANN A, STRASSER K, AXENKOPF G, SP~tTERGEBNISSE NACH CAROTISENDARTERIEKTOMIE.Langenbecks Arch Chit 1984;363:111~ 119.

Carotid Endarterectorny

69 BUNTT], HAYNESJL. Carotid endarterectomy. One solution to the stroke problem. Am Surg 1985;51:61-69. 70 RAITHELD, NOPPENEVTH, SCHWEIDERH, WILD R, SEITZ B. Frfih u n d Spfitergebnisse nach 244 Rekonstruktionen der Arteria Carotis Interna bei kontralateralem Interna-Verschluss. Langenbecks Arch Chir 1985:366:341. 71 HERTZERNR. ARISON R. Cumulative stroke and survival ten years after carotid endarterectomy. 1 Vasc Surg 1985 ;2: 6 6 1 - 6 6 8 . 72 THOMPSONlE, PATMAN RD, TALKINGTONCM. Carotid endarterectomy for cerebrovascular insufficiency, Comp Ther 1978 ;4:31-37. 73 VAN DEN AKKER PJ, VAN SCHIFFCAARDER, TERPSTRAJL. Operative and late results of surgery for obstructive carotid artery disease. In: Greenhalgh RM, Rose FC, eds Progress in Stroke Research 2. Great Britain: Pitman, Bath, 1983:465~!,79. 74 MOORE D], Morn JR, FINCH WT, SUMNER DS. Influence of the contralateral carotid artery on neurologic complications following carotid endarterectomy. 1 gasc Surg 1984;1:409 414. 75 HAMMACHERER, EIKELBOOMBC, BAST TJ, DEGEEST R, VERMEULEN FEE. Surgical treatment of patients with a carotid artery occlusion and a contralateral stenosis. J Cardiovasc Surg 1 9 8 4 ; 2 5 : 5 1 3 - 5 1 7 . 76 SACHS SM, FULENWIDERJT, SMITH RB, DARDEN WA, SALAM AA, PERDUE GD. l)oes contralateral carotid occlusion influence neurologic fate of carotid endarterectomy? Surgery 1 9 8 4 ; 9 6 : 8 3 9 - 8 4 4 . 77 GEE W, McDONALD KM, KouPP HA, CELANI BJ; BAST RG. Carotid stenosis plus occlusion: Endarterectomy or by-pass. Arch Surg 1980;115:183 187. 78 CONNOLLYJE. Carotid endarterectomy in the awake patient. Am J Surg 1 9 8 5 ; 1 5 0 : 1 5 9 - 1 6 5 . 79 EVANSWE, HAVES]P, WALTKEEA, VERMILIONBD. Optimal cerebral monitoring during carotid endarterectomy: Neurologic response under local anaesthesia. ] Vasc Surg 1985;2:775 777. 80 TAKOLANDEP,R, BERGOVISTD, KATZMANP, HULTHI~NJOHANSSONA. Local anaesthesia as a stress factor in carotid artery surgery. Poster 23.2. 2nd International Vascular symposium, London 1986. 81 GABELMANCG, GANN DS, ASHWORTHCJ, CARNEYWJ. One hundred consecutive carotid reconstructions: Local versus general anesthesia. Am J Surg 1 9 8 3 ; 1 4 5 : 4 7 7 - 4 8 1 . 82 SCOTTSM, SETm GK, BmD(~MANNAH. Perioperative stroke during carotid endarterectomy: The value of intraoperative angiography. J Cardiovasc Surg 1 9 8 2 ; 2 3 : 3 5 3 - 3 5 8 . 83 COURBIERR, JAUSSERANJ-M, REGGI M, FORMICHI M, FERDANI M. Routine intraoperative carotid angiography: Its impact on operative morbidity and carotid restenosis. J Vasc Surg 1 9 8 6 ; 3 : 3 4 3 350. 84 SANDMANN W, KNIEMEYER H, PERONNEAU P. Carotid bifurcation Doppler spectrum analysis at surgery. In: Greenhalgh RM, ed.

Diagnostic Techniques and Assessment Procedures in Vascular Surgery. London, Grune & Stratton 1 9 8 5 : 1 2 3 - 1 2 7 . 85 LANERJ, AePLEB~C, M. Real-time intraoperative angiosonography after carotid endarterectomy. Surgery 1982;92:5 9. 86 KLOTTERH-J, GAMST)iLLERG, GRONN1NGERJ, ROCKERTK, KUnN FP. Intraoperative sonographie n a c h Endarterectomie der Arteria Carotis. Chirurg 1 9 8 4 ; 5 5 : 3 3 9 - 3 4 2 . 87 ZIERLERRE, BANDYK DF, THIELE BL. lntraoperative assessment of carotid endarterectomy, l Vasc Surg 1984; 1: 73-84. 88 ORTEGAG, GEE W, KAUPPHA, McDONALDKM. Postendarterectomy carotid occlusion. Surgery 1981;90:1093 1098. 89 KWAANJHM, CONNOLLYJE, NHAREFKINJB. Successful m a n a g e m e n t of early stroke after carotid endarterectomy. Ann Surg 1979; 190: 676-678. 90 LINBBERG B. Acute carotid occlusion. Indication for surgery? J Cardiovasc Surg 1 9 8 0 ; 2 1 : 3 1 5 - 3 2 0 . 91 TREIMAN RL, COSSMAN DV, COHEN JL, FORAN RE, LEWN PM. M a n a g e m e n t of postoperative stroke after carotid endarterectomy. Am J Surg 1 9 8 1 ; 1 4 2 : 2 3 6 - 2 3 8 . 92 TAKOLANDERR, BERGENTZS-E, BERGQVISTD, PERSSONNH. Managem e n t of early neurologic deficits after carotid thrombendarterectomy. Eur J Vasc Surg 1987;1:67-71. 93 AC~
379

progression, mortality and recurrent

neurological episodes.

] Cardiovasc Surg 1 9 8 6 ; 2 7 : 4 1 8 - 4 2 5 . 94 STEWARTG, ROSS-R~JSSELLRW, BROWSENL. The long-term results of carotid endarterectomy for transient ischemic attacks. J Vasc Surg 1 9 8 7 ; 4 : 6 0 0 - 6 0 5 . 95 MILLIKAN CH. Clinical m a n a g e m e n t of cerebral ischemia. In: McDowell FH, Brennan RW eds. Cerebral Vascular Disease. Eighth Conference. New York, Grune and Stratton 1973:209. 96 GOLDSTONE1, MOOREWS. A new look at emergency carotid artery operations for the treatment of cerebrovascular insufficiency. Stroke 1 9 7 8 ; 9 : 5 9 9 - 6 0 2 . 97 MENTZERRM, FINKELMEIERBA, CROSBYIK, WELLONSJR HA. Emergency carotid endarterectomy tbr fluctuating neurologic deficits. Surgery 1 9 8 1 ; 8 9 : 6 0 - 6 6 98 BAKERRN, SCHWARTZWS, RAMSEYER]C. Prognosis a m o n g survivors of ischemic stroke. Neurology 1968; 1 8 : 9 3 3 - 9 4 1 . 99 MATSUMOTON, WtnSNANT ]P, KURLANDLT, OKAZAKIH. Natural history of stroke in Rochester, Minnesota 1955 through 1969. An extension of a previous study 1945 through 1954. Stroke 1973;4: 20 29. 100 McCULLOUGHJL, MENTZERRM, HARMAN PK, KAISER DL, KRON IL, CROSBY 1K. Carotid endarterectomy after a completed stroke: Reduction in long-term neurologic deterioration. J Vasc Surg 1985;2:7 14. 101 HARWARDTRS, WICKBOMIG, OTIS SM, BERNSTEIN EF, DILLEY RB. Posterior communicating artery visualization in predicting results of carotid endarterectomy for vertebrobasilar insufficiency. Am J Surg 1984;148:43 50. 102 Otm1EL K, RICOTTAJl, GREEN RM, DEWEESBJA. Carotid endarterectomy for nonhemispheric cerebral symptoms: Patient selection with ocular pneumoplethysmography. ]Vasc Surg 1 9 8 6 ; 4 : 1 1 5 118. 103 HEYMANA, WILKINSONW, HEYI)EN S, et al. Risk of stroke in asymptomatie persons with cervical arterial bruits. N Engl ] Med 1980; 302:838-841. 104 WOLF PA, KANNEL w g , 8ORLIE P, MCNAMARAP. Asymptomatic carotid bruit and risk of stroke--The Fratningham Study. lAMA 1981;245:1442-1445. 105 GREENHALGHRM, ELLIS M. Waiting for symptouls in patients with asymptomatic carotid bruit. In: Greenhalgh RM, Rose FC eds. Progress in Stroke Research 2 Bath, Great Britain, Pitman 1983: 247-253. 106 KARTCHNERMM, MCRAE LP. Noninvasive evaluation and management of the asymptomatic carotid bruit. Surgery 1 9 7 7 ; 8 2 : 8 4 0 847, 107 BUSUTTILRW, BAKER ]D, DAVIDSON RK, MACHLEDER Hi. Carotid artery s t e n o s i s - - h e m o d y n a m i c significance and clinical course. lAMA 1 9 8 1 ; 2 4 5 : 1 4 3 8 - 1 4 4 1 . 108 BERGUERR, SIEGGREEN MY, LAZO A, HODAKOWSKIGT. The silent brain inthrct in carotid surgery. J Vasc Surg 1 9 8 6 : 3 : 4 4 2 ~ t 4 7 . 109 CHAMBERSBR, NORRIS ]W. The case against surgery for asymptomatic carotid stenosis. Stroke 1984; 15: 964- 967. 110 ROEDERERGO, LANGLOISYE, JAGER KA, PRIMOZICHJF, BEACHKW, PHILLIPS DJ, STRANDNESSJR DE. The natural history of carotid arterial disease in a s y m p t o m a t i c patients with cervical bruits. Stroke 1 9 8 4 ; 1 5 : 6 0 5 - 6 1 3 . 1 l I BAIRD RN, ALDOORIHI, BENVENISTE GL, HOBROCKSM. Asymptomatic carotid m u r m u r - - U l t r a s o n i c factors influencing outcome. Presented at the Fortieth A n n u a l Meeting of the Society for Vascular Surgery, New Orleans, La., June 9-1 O, 1986. 112 THOMPSONJE. Don't throw out the baby with the bath water. A perspective on carotid endarterectomy, l Vasc Surg 1 9 8 6 ; 4 : 5 4 3 545, 113 CONNOLLYJE, STEMMEREA. Endarterectomy of the external carotid artery. Arch Surg 1973;106:799 802. 114 CLAYSON KR, FalWARDS WH. Importance of the external carotid artery in extracranial cerebrovascular occlusive disease. South Med J 1977; 7 0 : 9 0 4 - 9 0 9 . 115 BARNETTHJM, PEERLESS SJ, KAUFMANNJCE. "Stump" of internal carotid artery. A source for further cerebral embolic ischemia. Stroke 1 9 7 8 ; 9 : 4 4 8 ~ t 5 6 . 116 COUNTEERW, VIJAYANATHANT. External carotid artery in internal EurJ Vasc Surg Vot 1, December 1987

380

Rabbe Takolander and David Bergqvist

carotid artery occlusion. Angiographic, therapeutic and prognostic considerations. Stroke 1979;10:450 460. 117 HERTZERNR. External carotid endarterectomy. Sur,q Gynecol Obstet

1981;153:186-190. 118 LAMBERTH WC. External carotid endarterectomy: Indications, operative technique and results. Su r`qery 1983; 93: 57-63. l 19 TAKOLANDERR, BERGOVIST l), BERGENTZS-E, ERICSSONBF. Reconstruction of the external carotid artery. Acta Chir Stand 1985; 151: 647-650. 120 SCHULERII, FLANIGAN PF, DEBoRD J-R, RYAN TJ, CASTRONUOWOJJ, LIM LT. The treatment of cerebral ischemia by external carotid artery revascularization. Arch Sury 1983; 118: 5 6 7 - 572. 121 MOORE WS, BOREN C, MALONE JM et aL Natural history of nonstenotic, asymptomatic ulcerative lesions of the carotid artery. Arch Sur,q 1 9 7 8 : 1 1 3 : 1 3 5 2 - 1 3 5 9 . 122 ROEDERER GO, LANGLOIS YE, LOSIANI L e t al. Natural history of carotid artery disease on the side contralateral to endarterectomy. ]Vasc Sur,q 1984:1:62-72. 123 NOBEL M, IMPARAII) AM, RILES TS, MINTZER R. Contralateral neurologic symptoms after carotid surgery: A nine-year follow-up. ]Vasc Sur,q 1986;3:623 628. 124 HARWARDTRS, KROENERJM, WIC•BOM JG, BERNSTEINEF. Natural history of asymptomatic ulcerative plaques of the carotid bifurcation. Am ] Sur,q 1 9 8 3 ; 1 4 6 : 2 0 8 - 2 1 2 . 125 SCHULER JJ, FLANmAN DP, LIM LT, KEWER T, WILLIAMS LR, BEHREND AJ. The effect of carotid siphon stenosis on stroke rate, death and relief of symptoms following elective carotid endarterectomy. Surgery 1 9 8 2 ; 9 2 : 1 0 5 8 - 1 0 6 7 . 126 ROEDERERGO, LANGLOISYE, CHAN ARW, CmKos PM, THIELE BL, STRANI)NESSDE. Is siphon disease important in predicting outcome of carotid endarterectomy? Arch Su~q 1 9 8 3 ; 1 1 8 : 1 1 7 7 - 1 1 8 1 . 127 DAY AL, RHOTON AL, QUISLINC RG. Resolving siphon stenosis following endarterectomy. Stroke 1 9 8 0 ; 1 1 : 2 7 8 - 2 8 1 . 128 COSSMAND, CALLOWAD, STEIN A, MATSUMOTOG. Early restenosis after carotid endarterectomy. Arch Sur,q 1978; 1 1 3 : 2 7 5 - 2 7 8 . 129 CEAGETTGP, RICH NM, McDONALD PT, et al. Etiologic factors for recurrent carotid artery stenosis. Sur,qery 1 9 8 3 ; 9 3 : 3 1 3 - 3 1 8 . ] 30 AUKLANDA, KURLOWRA, HAMER JD. Carotid artery occlusion following endarterectomy: evaluation by spectral analysis of Doppler ultrasound signals. Br J Sur,q 1982 ;69:45-47. 131 BODILY KC, ZIRLER RE, MARINELLI MR, THIELE BL, GREENE FM, STRANDNESS DE. Flow disturbances following carotid endarterectomy. Sur,q Gynecol Obstet 1980; 141: 77-80. 132 KREMENJE, GEE W, KAUPPHA, McDONAEDKM. Restenosis or occlusion after carotid endarterectomy. Arch Surq 1 9 7 9 : 1 1 4 : 7 0 8 - 7 1 0 .

EurJ Vasc Surg Vol 1, December 1987

133 TURNIPSEED WD, BERKOFF HA, CRUMMEYA. Postoperative occlusion after carotid endarterectomy. Arch Surq 1 9 8 0 ; 1 1 5 : 5 7 3 3 5734. 134 CANTELMONL, CUTLERBS, WHEELERHB, HERRMANNJB, CARDULLO PA. Noninvasive detection of carotid stenosis following endarterectomy. Arch Surq 1981;116:1005 1008. 135 ZmLER RE, BANDYK DF, THIELE BL, STRANDNESSJR DE. Carotid artery stenosis following endarterectomy. Arch Surg 1982:117: 1408-1415. 136 BAKER WH, HAYES AC, MAULER D, LITTOOV FN. Durability of carotid endarterectomy. Surgery 1 9 8 3 ; 9 4 : 1 1 2 - 1 1 5 . 137 SALVlAN A, BAKERJD, MACHLEDERHI, BUSUTTILRW, BARKERWF, MOORE WS. Cause and noninvasive detection of restenosis after carotid endarterectomy. Am J Surg 1983; 1 4 6 : 2 9 - 3 4 . 138 PIERCE GE, ILIOPOUEOSII, HOLCOMBMA, RIEDER CF, HERMRECKAS, THOMASJH. Incidence of recurrent stenosis after carotid endarterectomy determined by digital subtraction angiography. Am ] Surg 1984;148:848-854. 139 RAITHEL D, SCHWEIGER H, GENTSCH HH, SEYFERT W, ZEITLER E. Digital transvenous angiography in follow-up examinations after carotid reconstruction: Early results. ] Cardiovasc Surg 1984;25: 400-403. ] 40 THOMASM, OTIS SM, RUSH M, ZYROFF], DIELEY RB, BERNSTEINEF. Recurrent carotid artery stenosis following endarterectomy. Ann Surg 1 9 8 4 ; 2 0 0 : 7 4 - 7 9 . 141 STONEYRJ, STRING ST. Recurrent carotid stenosis. Surgery 1976; 80:705-710. 142 THOMPSONJE, TALKINGTONCM. Carotid endarterectomy. Ann Surg 1976;184:1-15. 143 HERTZER NR, MARTINEZ BD, BENJAMIN SP, BEVEN EG. Recurrent stenosis after carotid endarterectomy. Sur,q G!lnecol Obstet 1979; 149:360-364. 144 CROSSMAND, CALLOWAD, STEIN A, MATSUMOTOG. Early restenosis after carotid endarterectomy. Arch Suroo l 9 7 8 ; 1 1 3 : 2 7 5 - 2 7 8 . 145 CEAGETTGP, ROBINOWITZM, YOUKEYJR et al. Morphogenesis and clinicopathologic characteristics of recurrent carotid disease. ] Vasc Sury 1986;3:10-23. 146 HASS WK, JONAS S. Caution falling rock zone: An analysis of the medical and surgical m a n a g e m e n t of threatened stroke. Proc Inst Med Chap t 980;33:80 84. 147 QUINONES-BALDRICHWJ, MOOREWS. Results of medical and surgical therapy for extracranial arterial occlusive disease. In: Rutherford RB, ed. Vascular Sur,qery. Philadelphia: Saunders 1 9 8 4 : 1 3 2 2 1328.

Received 5 March 1987