Intracerebral haemorrhage after carotid endarterectomy

Eur J VascSurg 1, 51-60 (1987)

Intracerebral Haemorrhage After Carotid Endarterectomy T o r b e n S c h r o e d e r 1", H en r i k Sillesen 1, Jens Boesen 2, H e n n i n g Laursen 3, and Per S o e l b e r g Sore ns e n 4 1Departments of Vascular Surgery, 2Neuroradiology, 3Neuropathology, and 4Neurology, Rigshospitalet R K 2 1 0 1 , University Hospital, Blegdamsvej 9, DK 2 1 0 0 Copenhagen, Denmark (Received 16 October 1986, accepted in revisedform 24 November 1986) Among 662 consecutive carotid endarterectomies eight cases of postoperative ipsilateral intracerebral haemorrhage were identified, occurring into brain areas which, preoperatively were without infarction. As blood pressures across the stenosis were routinely measured during surgery, the internal carotid artery (/CA) perfusion pressure could be related to the occurrence of haemorrhage. In addition, cerebral blood flow (CBF) was studied with the intravenous xenon-133 technique in four patients and histopathologic examination of the brain was available in four patients who died subsequent to their haemorrhage. All eight patients had a high grade of ICA stenosis and a marked reduction of ICA perfusion pressure (average of 40%) which was significantly greater than that observed (average of 6%) in the other patients undergoing carotid surgery (P < 0.0001 ). Relative hyperperfusion of the ipsilateraI hemisphere was seen in the four patients studied postoperatively. In at least two cases the haematoma was preceded by an asymptomatic postoperative ischaemic infarct. Histologic examination did not confirm previous findings of changes resembling those seen in malignant hypertensive encephalopathy. These results substantiate the view, that patients at risk of haemorrhage after endarterectomy are those with a low preoperative cerebral perfusion pressure and postoperative hyperperfusion. Postoperative silent brain infarction is an additional risk factor.

Key Words: Carotid artery disease; Carotid endarterectomy; Intracerebral haemorrhage; Cerebralperfusion pressure.

Introduction lntracerebral haemorrhage is a rare, but devastating complication of carotid endarterectomy. The incidence is reported to be ½ to 1%. 1-6 Eventually more than 50% die, thus haemorrhage constitutes a major source of noncardiac perioperative mortality. 6 Risk factors have been variously attributed to recent cerebral infarction, severe hypertension and the use of systemic anticoagulants. 1-9 Recently attention has been drawn to a preoperative state of impaired cerebral haemodynamics with a severely reduced cerebral perfusion pressure. 2,s, 10Following reconstruction, perfusion pressure becomes normal and due to a loss of autoregulation hyperperfusion re*To whom all correspondenceshould be addressed. 0950-821X/87/010051 + 10 $03.00/0 © 1987 Grune & Stratton Ltd

suits. In some instances this may lead to cerebral edema and haemorrhage. During the last 6} years we have encountered eight cases of intracerebral haemorrhage after carotid endarterectomy. As the arterial blood pressures across the internal carotid artery (ICA) stenosis are routinely measured during surgery at our centre, the occurrence of haemorrhage could be related to the degree of reduction in perfusion pressure, Furthermore, cerebral blood flow (CBF) was measured in four of the patients before and after surgery, but before haemorrhage occurred. Four of the eight patients died following haemorrhage and tile brain was examined histologically. Specimens were particularly examined for vascular changes which might indicate the presence of malignant hypertensive changes, as recently reported by Bernstein et al. lo

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T. Schroeder e t al.

M e t h o d s and M a t e r i a l s

A total of 662 carotid endarterectomies were performed in 597 patients from January 1, 1980 to June 30, 1986. Arch arteriography and in most patients cerebral computed tomography (CT-scan) were performed preoperatively. All patients were evaluated by a neurologist before and after surgery.

asymmetry was calculated as the difference between CBF in the ipsilateral and the contralateral hemisphere in percentage of mean CBF. Reproducibility studies with this equipment have shown changes in hemispheric CBF from one study to another exceeding :t:gml/lOOg/min or changes in side-to-side asymmetry exceeding ± 7% to be significant at the 95% level. 11

Ultrasound Doppler studies Surgical procedures Endarterectomy was performed under general halothane anaesthesia keeping the PaCO2 at approximately 30mmHg. Blood pressures across the internal carotid artery (ICA) stenosis were measured before clamping through a 21 G cannula connected via manometer line to a pressure transducer. The ratio of the ICA mean pressure to common carotid artery mean pressure (ICA/CCA pressure ratio) served as an expression of the hemispheric perfusion pressure. After clamping, the distal mean pressure (stump pressure) was also recorded. Blood flow through the ICA was measured before and after reconstruction by an electromagnetic flowmeter (Nycotron 372). An intraluminal shunt was used if the stump pressure went below 40 mmHg or the continuously registered electroencephalogram (EEG) flattened during clamping of the artery. Until 1986 all patients received oral anticoagulant therapy with phenprocoumon, during the perioperative period. The dosage was adjusted according to the prothrombin-proconvertin (PP) concentration (therapeutic level 10-20%). When a diagnosis of cerebral haemorrhage was made the effect of anticoagulants was counteracted with phytonadione and further administration stopped. Heparin was used locally during surgery.

CBF measurements Cerebral blood flow has been measured since 1984, using the intravenous xenon-133 technique and a mobile unit (Novo Cerebrograph lOa), as previously described. 11 Following an i.v. bolus injection of 15 mCi xenon-133 in saline, the cerebral clearance was recorded for 11 rains, using five NaI detectors covering each middle cerebral artery territory. CBF was expressed as a noncompartmental flow index, calculated from the monoexponential slope between 30 and 90 s of the deconvoluted clearance curve. 12 The blood to tissue partition coefficient lambda, was set to 1.0 ml/g. The five regional flow values were averaged and the relative side-to-side EurJ VascSurg Vol 1, February 1987

Since 1985 patients have been evaluated by continuous and pulsed wave Doppler ultrasound technique. In this report we have included only the results of the Continuous Wave Doppler examination.13

Histologic brain examination In the four fatal cases tissue blocks were obtained from the frontal, parietal and occipital lobes and from the hippocampal gyrus, mesencephalon, pons and cerebellum for microscopical examination after paraformaldehyde fixation. In addition, blocks were prepared from any pathological tissue. Following dehydration and paraffin embedding, sections were stained with haematoxylineosin, van Gieson technique, Crystal violet, KlfiverBarrera, glial fibrillary acid protein peroxidaseantiperoxidase technique or the Martins, Scarlet, Blue technique for fibrin. In addition frozen sections were stained by the Bielschowsky technique for neurons.

Results

Eight cases of postoperative haemorrhage were identified, giving an incidence of 1.2% (95% confidence level: 0.4-2.2%). Eventually, four patients died. A total of seven patients died following endarterectomy, thus more than half of the perioperative mortality was caused by cerebral haemorrhage.

Case reports: Case I A 44-year-old woman with severe, but well controlled hypertension was admitted 3 months after a left hemispheric stroke. At the time of admission minor weakness and dyscoordination of the right arm was present. Arteriography showed an 80% stenosis of the left ICA. A left

Cerebral Haemorrhage After Endarterectomy

parietal infarct was demonstrated by CT-scan. Following a left endarterectomy the postoperative course was uneventful until the fourth postoperative day, w h e n she complained of severe left sided headache. The BP had remained stable about the preoperative level of 130/80. On the fifth day she experienced a grand real seizure and developed right sided hemiparesis. The BP increased to 2 2 0 / 1 3 0 and was treated with dihydralazine and diazepam. Emergency CT-scan demonstrated a well delineated 2 x 2 × 2 cm h a e m a t o m a in the left occipital region surrounded by oedema. The infarct seen on the preoperative CT-scan was unchanged. During the following weeks the neurological deficits gradually improved and one year later only minor weakness of the right hand remained.

Case 2

A 60-year-old man, with a history of mild hypertension, had for 6 months experienced daily posture related TIA's with weakness of the left side lasting for a few minutes. Neurological examination was normal. Arteriography revealed a high grade stenosis of the right ICA. During right sided endarterectomy, no flow could be recorded in the ICA, and pressure measurements were therefore omitted. Apart from a moderate right temporal and periorbital headache on the 2nd and 3rd day, the postoperative course was uneventful. In the evening on the 4th day, the BP suddenly increased to 2 0 0 / 9 0 and he developed increasing impairment of consciousness and a left sided hemiparesis. Severe hypertension of up to 3 0 0 / 1 4 0 was treated with dihydralazine. Over the course of 70 min he became comatose and died. At autopsy an 8 x 6 × 8 cm h a e m a t o m a was found in the right corpus striatum with rupture into the lateral ventricle. A fresh mural thrombus was seen in the right middle cerebral artery. Microscopically the h a e m a t o m a was sharply demarcated from the surrounding brain tissue. The adjacent tissue showed some oedema, swelling of the endothelium of a few arterioles and diapedetic haemorrhage. Fibrinoid necrosis or inflammatory infiltration was not observed.

Case 3

This 56-year-old normotensive m a n complained of a pulse-synchronous bruit in the left ear lasting for 4 months. He had never experienced focal neurologic symptoms and neurologic examination was normal. Arteriography showed a thread-like residual lumen in the left ICA. Following endarterectomy he complained of

53

episodes of left frontal headache not accompanied by an elevation of BP. Neurologic examination on the 4th day revealed a right lower quadrant-anopia. No other deficits could be demonstrated. CT scan revealed a well demarcated 3 x 3 x 3 cm h a e m a t o m a in the left occipital region. The further course was uneventful until the 13th day, when he experienced a new episode of left sided headache, this time followed by confusion and stupor. No pareses could be identified but the BP was 175/80. Emergency CT-scan showed that the occipital haemorrhage had extended to occupy the posterior part of the parietal lobe. He was intubated and hyperventilated to reduce intracranial pressure, and hypertension was treated with dihydralazine. After 3 days treatment he was comatose, with response to noxious stimuli in the left arm only. Repeated CT-scan showed a minor increase in the size of the haemorrhage and the oedema had grown to occupy the entire left cerebral hemisphere. Two days later, 18 days after endarterectomy, he died. Autopsy demonstrated a 5 x 5 x 5 cm h a e m a t o m a in the left occipital lobe and oedema of the entire left hemisphere. The arterial system was free of thrombosis. Histologically the tissue surrounding the haemorrhage was oedematous, monocytes and macrophages had invaded the edges, and the neurons were dead and disrupted. Swelling of capillary endothelium and fibrinoid exudation were obvious, but fibrinoid necrosis of the larger vessels was not seen.

Case 4

A 58-year-old normotensive m a n was admitted after two episodes of TIA from the left carotid territory. Neurologic examination and CT-scan were normal. The angiogram showed a high grade stenosis of the left ICA and 50% stenosis of the right. Blood pressure and neurologic function immediately after left endarterectomy was normal however 3 h later, he suddenly began to vomit and developed a right sided hemiparesis. Hypertension was controlled with dihydralazine, but he became increasingly comatose and died 9 h later. CT scan was not performed. Autopsy revealed a large recent h a e m a t o m a in the area of the left striatum. The h a e m a t o m a was sharply demarcated, and the adjacent tissue showed only oedematous swelling and perivascular haemorrhage.

Case 5

This 50-year-old m a n had a history of progressing cogniEur] Vasc Surg Vol 1, February 1987

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T. S c h r o e d e r e t al.

tive dysfunction, dysphasia and periodic disorientation over a 4 month period. Moderate hypertension was present. On admission he presented a left parietal lobe symptoms namely non-fluent aphasia and marked dyscoordination of the right hand. Arteriorgraphy revealed occlusion of the left ICA and a thread-like residual lumen of the right ICA. Endarterectomy of the right ICA was decided upon, but surgery was postponed for 6 weeks as a fresh infarction in the left parieto-occipital region was demonstrated by CT-scan. For 2 4 h after endarterectomy he remained intubated, and was hyperventilated in order to reduce the expected postoperative hyperaemia. BP was controlled with chlorpromazine. Shortly after extubation he became stuporous, developed seizures of the left side and was reintubated and ventilated. Concomitant hypertension was treated with dihydralazine. CT-scan revealed a small diffuse haemorrhage of the right occipital region surrounded by hypodensity. He remained unconscious for a week with severe generalised myoclonic seizures. On the 12th day, however, he began to wake up. Until the 17th day he presented temporary diabetes insipidus, responding to vasopressin. CT-scan at this time showed complete disappearance of the previously haemorrhagic area in the right occipital lobe. After one month he was discharged from hospital suffering from the aphasia and dyscoordination, which he had preoperatively. One year later a CBF tomography was performed using the xenon-133 inhalation technique and SPECT. 14 A low flow area was seen in the left occipital region, corresponding to the preoperative infarct, but flow in the right occipital region where the haematoma appeared postoperatively was normal.

Case 6

A 65-year-old normotensive woman presented with a history of TIA's followed by a minor stroke referred to the right cerebral hemisphere. She had experienced no further symptoms. Neurologic examination revealed mild finger paresis in the left hand. CT-scan showed right parietal infarct and arteriography revealed bilateral highgrade ICA stenoses. Doppler flow studies showed reversal of flow in the right periorbital arteries. Following right sided endarterectomy tile first 3 postoperative days were uneventful and the BP remained below 140/60. On the 4th day she suddenly experienced a severe, pounding headache in the right frontal region, BP increased to 180/80 and she developed generalized seizures. Afterwards no neurological deficits could be demonstrated and her BP was normal, During the next two days she experiEurJ VascSurg Vol 1, February 1987

enced several attacks of right frontal headache. A CTscan, performed on the 6th day showed a hypodense area in the right frontal lobe, suggesting a fresh infarct. The parietal infarct seen preoperatively was unchanged. Doppler examination showed the right carotid to be patent and that the periorbital flow direction was normal. On day 7, the headache suddenly worsened, followed by focal seizures in the left arm, left sided hemiparesis and coma. Emergency CT-scan showed a large haematoma in the right fronto-parietal region with penetration to the ventricular system and pronounced oedema. Without regaining consciousness she died 21 h later. Autopsy showed a 6 x 6 × 3 cm haematoma in the right fronto-parietal lobes with severe oedema of the adjacent tissues and pronounced cellular infiltration. Endothelial swelling and diapedetic haemorrhage were prominent in many capillaries. Endothelial proliferation, fibrinous exudates and fibrinoid degeneration were found in a number of larger vessels, but only in relation to the necrotic brain tissue. A mural thrombus was found in the right carotid bifurcation, but no thrombotic material could be demonstrated distally.

Case 7

This 42-year-old normotensive woman had experienced daily attacks of paraesthesia in the left hand during a period of 9 months. The last month before admission she had been free of symptoms. Neurologic examination, eye examination and CT-scan were normal. Arteriography and Doppler examination showed an 80% stenosis of the right ICA and periorbital flow on that side. Following right sided carotid endarterectomy she was normotensive, but complained of episodic right sided headache. On the 5th day, when 1 g of acetazolamide was given i.v. in association with a postoperative CBF study, she became uneasy, and the headache intensified. No focal neurotogic deficits were found and the BP was 160/100. One and a half hours later she had a grand real seizure followed by left sided hemiparesis. CT-scan performed 3 h later revealed haemorrhage in the right frontal lobe, but also oedema of most of the right cerebral hemisphere. Doppler examination showed the right bifurcation to be patent. During the following two days she gradually became comatose. Repeated CT-scans showed increasing compression of the ventricular system and the haematoma was evacuated on the 7th postoperative day. Thereafter she gradually regained consciousness and during the following weeks the hemiparesis markedly improved. At four weeks only a slight hand paresis and moderate dysphasia remained. CT-scan at t h i s time

Cerebral Haemorrhage After Endarterectomy

showed a hypodense lesion corresponding to the evacuated h a e m a t o m a in the frontal lobe.

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sure ratio was less t h a n O. 75. Thus, the incidence of postendarterectomy h a e m o r r h a g e among patients with ICA/ CCA pressure ratio below 0.75 was 8%.

Case 8 CBF results A 60-year-old normotensive w o m a n had suffered a left hemisphere minor stroke 1 year before admission. Numbness of the right a r m remained, but new neurologic episodes had not occurred. Neurologic examination showed weakness of the right arm and CT-scan demonstrated a left parietal infarct (Fig. 1). Angiography showed an 80% narrowing of the left ICA and the periorbital flow direction was reversed, as demonstrated by the Doppler technique. Following left sided endarterectomy she received no anticoagulant therapy. On the 3rd day she experienced a left sided frontal headache. CT-scan at this time [Fig. l(b)] showed a hypodense area, suggestive of a fresh infarct, in the left parieto-occipital region. The preoperative infarct was unchanged and positioned more anteriorly. The headache worsened the next day, and she developed expressive dysphasia. In no instance did the BP exceed 160/90. Repeated CT-scan showed that a 4 × 5 x 5 cm haemorrhage had occurred in the previously hypodense area [Fig. l(c)]. Oedema involved most of the left hemisphere. During the following days she developed right sided hemiparalysis and became unconscious. CTscan at this time revealed penetration of blood into the ventricular system and massive oedema [Fig. l(d)]. Hypertensive episodes were treated with a beta adrenergic blocking agent. For 3 days she was comatose, but on the 10th day she slowly regained consciousness. She had a pronounced global aphasia and right haemiplegia. Doppler examination showed the left bifurcation to be patent. Two months later partial remission of the aphasia and haerniplegia had occurred.

Intraoperative pressure measurements The m e a n blood pressure across the ICA stenosis was measured in seven of the patients. In all instances a major pressure gradient was found, resulting in a m e a n ICA/CCA pressure ratio of 0.6 (Table 2). Pressure results were available in 596 of the 662 cases (90%). The percentage distribution of patients according to ICA/CCA pressure ratios are shown in Figure 2. Patients who developed haemorrhage had on average a significantly lower ICA/CCA pressure ratio w h e n compared with the other patients operated on in this period: 0.60 vs. 0.94 (P < 0.0001). In 92 (16%) instances the ICA/CCA pres-

Baseline studies were performed before and one day after surgery in four patients. In three patients CBF was measured again 3 - 5 days postoperatively, to 1-2 days before the neurologic symptoms developed. In all patients a significant CBF increase ( > 9 m l / l O 0 g/min) was noted on the first day after surgery, whereas hemispheric CBF returned towards the preoperative level in the later studies (Fig. 3, upper part). Also the side-to-side asymmetry on the first day was improved significantly ( > 7%) in favour of the ipsilateral hemisphere. However, this improvement was further accentuated in the later studies (Fig. 3, lower part).

Summary of results The pre-, peri- and postoperative data are summarized in Tables 1-3. All patients presented a high degree of stenosis of the ICA and perfusion pressure was reduced by at least 2 5%. CBF measurements showed hyperaemia in the ipsitateral hemisphere relative to the contralateral hemisphere in the four patients studied (Cases 5-8). In patients, who had a history of stroke (Cases 1, 5, 6 and 8), at least 8 weeks had passed from the last symptoms to endarterectomy. None of the eight patients had preoperative clinical or radiographic evidence of cerebral infarction in the region of subsequent haemorrhage. In two patients (Cases 6 and 8), however, the haemorrhage was most probably preceded by a postoperative ischaemic infarction. In four patients (Cases 1, 2, 4 and 5) all the evidence suggested a primary haemorrhage, while in cases 3 and 7 it was impossible to determine whether the haemorrhage was secondary to regional ischaemia or the ischaemia was secondary to pressure exerted by the haematoma. None of the four patients examined showed definite histologic changes resembling those seen in malignant hypertensive encephalopathy.

Discussion intracerebral h a e m o r r h a g e into an area of previous infarction is a k n o w n complication of carotid endarterectomy, especially w h e n surgery is performed within days Euri VascSurg Vol ], February 1987

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Fig. 1. Preoperative (Fig. l(a)] and postoperative CT-scans performed 3 days [Fig. l(b)], 5 days [Fig. l(c)] and 7 days after carotid endarterectomy [Fig. 1(d)]. See case history for further details. (Case 8.)

Eur] Vasc Surg Vol 1, February 1987

Cerebral Haemorrhage After Endarterectomy

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50 m

changes analogous to hypertensive encephalopathy demonstrated in a fatal case, l° indicate that postendarterectomy haemorrhage in the normal brain is related to 40 a preoperative state of haemodynamic impairment. Distal to a high-grade ICA stenosis the hemispheric perfusion c 09 pressure may be severely reduced, if the collateral circu50 lation, supplied mainly through the circle of Willis, is im~6 paired as well. Under such circumstances, a state of o chronic hypoperfusion may exist, during which the resisE 20 tance vessels stay maximally dilated to ensure adequate blood flow. Restoration of normal perfusion pressure by io endarterectorny can result in cerebral hyperfusion, due to loss of autoregulation. This mechanism is probably equivalent to the normal perfusion pressure breakthrough de0"2 0.3 0"4 0.5 0.6 0.7 0"8 0-9 1.0 scribed by Spetzler et al. 1~ after resection of cerebral fCA/CCA pressure ratio arteriovenous malformations. Fig. 2. Percentage distribution of ratio of internal to common carotid A reversed periorbital flow, 1° as observed in three artery mean pressure (ICA/CCApressure ratio) determined in 596 caro- patients (Cases 6-8), or a decreased retinal artery prestid endarterectomies. The black circles represent the patients who exsure 2 provide indirect evidence of a reduced perfusion. perienced cerebral haemorrhage. Direct pressure measurements related to ICA endarterectomy have only been sporadically reported. 9 The present results support the theory that a low perfusion pressure is a major risk factor: all seven patients who had pressure 90 measurements performed belonged to a group, constitut~.E ing 16% of the whole series, in whom the ICA/CCA pres.~ ~ 70 sure ratio was below 0.75 (Fig. 2). [t should be Eo ~0 recognised, that the ICA/CCA pressure ratio, measured case 7 E 50 during halothane anaesthesia and hypocapnia, did not case 8 0 f j ~ / , ~ ~ reflect the pressure conditions at the arteriolar level in the oa~ case 6 ~ case 5 ~ ~ ~ 30 conscious patient, hence the true perfusion pressure ratio may well be grossly overestimated. On the other hand, as conditions were approximately equal for all patients, the pressure ratio, as here defined, provided a means of iden20 tifying those patients who were haemodynamically most compromised. case I0 The proposed haemodynarnic basis for developing postoperative haemorrhage was given further support by case the available CBF results. Although the number of studies ~3 bSE was limited, the consistency of the side-to-side asymcose case metry data clearly indicated hyperaemia of the ipsilateral -I0 hemisphere relative to the contralateral hemisphere (Fig. PRE Doy I Day 3--5 3, lower part). The occurrence of such hyperperfusion Fig. 3. Cerebralbloodflowstudied before, one and three to fivedays fol- after restoration of normal perfusion pressure suggests lowing carotid endarterectomyin 4 patients. Hemispheric mean flowis shown in the upper graph and side-to-side asymmetry, determined as impairment of autoregulation. The return to normal of the interhemispheric flowdifferencein percentage of mean flow, in the flow in the late studies (Fig. 3, upper part) may suggest lower graph. that autoregulatory control has been regained in the larger part of the brain, while focal autoregulation may still be absent. Methodological problems with the present CBF technique as well as biologic variability make comafter a major stroke or in patients with ICA occlusion, t, 7,8 parisons of hemispheric flow levels less reliable. As the Haemorrhage into an area of normal brain has however non-invasive xenon- 13 3 technique allows simultaneous only been reported infrequently. 2,5,~° The perioperative determination of CBF in both hemispheres, such global findings of marked hyperperfusion in patients who later variations can be minimised by considering the changes developed haemorrhage,2 together with histologic in side-to-side asymmetry, u Eur] VascSurg Vol 1, February I987

T. Schroeder e t al.

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Table 1. Preoperative neurologic history and examination

Age Sex

Neurologic history

1

44 F

L hsph stroke

2

60 M

R hsph TIA

3

56 M

-

4

59 M

L hsph TIA

5

50 M

6

Time from last symptom to operation

Degree of ICA stenosis on angiography

Neurologic examination

Infarction on CT-scan

3 months

Slight R UE paresis

L parietal

R: 20% L: 80%

L

2 days

Normal

Not performed

R: 80% L: 0

R

Normal

Not performed

R: 50% L: 90%

L

2 months

Normal

Normal

R: 40% L: 80%

L

L hsph stroke

8 weeks

Gerstmann, RUE slight paresis

L parietooccipital

R: 90% L: 100%

R

65 F

R hsph stroke

7 mont hs

L finger paresis

R parietal

R: 90% L: 80%

R

7

42 F

R hsph TIA

1 mont h

Normal

Normal

R: 80% L: 0

R

8

60 F

R hsph stroke

Slight L UE paresis

R parietal

R: 80% L: 0

R

Case

-

12 mont hs

Op side

Abbreviations: L = left; R = right; UE = upper extremity; ICA = internal carotid artery; hsph = hemispheric TIA = transient ischaemic attack.

Table 2. Pressure and flow measurements pedbrmed during carotid e n d a r t e r e c t o m y

Case

Mean pressure ICA/CCA gradient pressure mmHg ratio

Stumppressure mmHg

ICA flow ml/min --pre post

EEG changes during Shunt clamping used

1

35

0,69

40

70

180

-

-

-

-

312

-

2

3

55

0.37

20

132

500

-

4

25

0.71

50

168

216

-

5

69

0.39

28

100

312

+

6

21

0.74

40

72

168

-

7

35

0.60

43

155

96

8

39

0.56

30

66

186

+

+

+

Abbreviations: ICA = internal carotid artery; CCA = commo n carotid artery; EEG = electroencephalography.

Hyperperfusion has been associated also with posten-, darterectomy headache and seizures. 2,s'16q9 In the present study, all six patients, who developed haemorrhage later than the second postoperative day, complained of severe headache one to two days before the onset of neurologic symptoms. The headache was always unilateral and localised fronto-temporal or periorbital on EurJ Vasc Surg Vol 1, February 1987

the side ipsilateral to surgery. Although postoperative headache is common, j7 this type of severe headache occurring after surgery to a high-grade stenosis should probably be a sign of imminent cerebral haemorrhage. Three of our patients presented with the clinical triad of unilateral headache, seizures and h a e m o r r h a g e (Table 3), previously described in only one case. 1°

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Table 3. Timefromendarterectomyto postoperativeevents (days) and course Case

PP values %

Headache days

Seizures days

Haemorrhage days Course

1

29-36

4

5

5

Remission

2

32-22

1

-

4

Died 4th day

3

29-21

2

4

Died 18th day

4

18

-

1

Died 1st day

5

24-12

-

2

2

Remission

6

37-49

3

4

4

Died 8th day

7

44-26

3

5

5

Evacuation of hematoma, partial remission

4

Major deficit

8

3

Abbreviations: PP = prothrombine-proconvertineconcentration.

We have previously studied the sequential course of CBF following endarterectomy in a single case 2° and later in a series of uncomplicated patients. 21 These studies indicated marked hyperperfusion, lasting 1 to 4 days, in most patients with low perioperative pressures. While postendarterectomy hyperperfusion is associated with increased perioperative morbidity, 2's not all patients will suffer complications. In the present series all haematomas occurred into an area of brain which was preoperatively free of infarction. Yet, the possibility of peri- or postoperative embolism, causing ischaemic infarction prior to the haemorrhage, must be considered. In fact, two of the three late CBF studies were performed in the two patients (Cases 6 and 8) who postoperatively developed an infarct prior to the haemorrhage. As emboli commonly disintegrate, the enhanced hyperaemia in these patients could also reflect reperfusion, changing the ischaemic infarct into a hyperaemic infarct. 22 The histologic changes in the tissue adjacent to a haematoma of some days duration may be identical to those seen in an ischaemic infarct followed by secondary haemorrhage. Thus, a distinction may be impossible unless serial CT-scans are available. Moreover, the absence of neurologic symptoms provides no guarantee against infarct, since many brain areas lack clear somatic representation. The recent data of Berguer et al. 23 have indicated that silent postoperatively brain infarcts may occur more frequently than symptomatic infarcts. Two patients (Cases 6 and 8) developed silent infarcts before the haemorrhage, and a postoperative infarct might be considered in cases 3 and 7. Haemorrhage into an infarct may also explain the observation in this study as well as in other series that haemorrhage usually develops 4: to 7 days after surgery. 2'4's Primary haemorrhage seems to be the most likely

explanation in the majority of patients in the present series. We were, however, unable to find definite histologic evidence of malignant hypertensive encephalopathy. 1° In one patient (Case 6) we found fibrinoid degeneration but only in the ischaemic tissue adjacent to the haemorrhage. Although we can identify a subgroup of patients at increased risk of cerebral haemorrhage, following carotid endarterectomy, we cannot offer explanation why only some of these patients are affected. Several points should be considered. In some studies uncontrolled postoperative hypertension has been identified as the major cause of haemorrhage. 9 The frequency of postoperative hypertension is high 24-26 and hypertension is generally observed in patients who suffer cerebrovascular accidents, as was the case in six patients in this series. In the majority, however, the BP seemed well controlled until neurologic symptoms occurred. The onset of hypertensive episodes coincided with the appearance of a headache. However, as haemorrhage in most cases occurred several days after endarterectomy, when BP monitoring is less intensive, the possibility that hypertension may have contributed in some cases remains possible. In this study, dihydralazine was used in five patients to control postoperative hypertension. However, marked cerebral vasodilation in addition to increased intracranial pressure, 27,2s makes dihydralazine less suitable for treatment of hypertension in this situation. Although dihydralazine was not the precipitating factor, it may have contributed to deterioration in some instances. In one patient (Case 7) we administered the potent cerebral vasodilator acetazolamide for the purpose of investigating postoperative perfusion reserve. In a state of relative and probably uneven hyperperfusion the administration of acetazolamide may have been the last straw. On the EurJ VascSurg Vol 1, February 1987

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T. Schroeder e t al.

o t h e r h a n d o v e r 3 0 0 a c e t a z o l a m i d e studies h a v e b e e n p e r f o r m e d in this i n s t i t u t i o n i n c l u d i n g p o s t o p e r a t i v e studies a n d studies in p a t i e n t s w i t h a c u t e s t r o k e w i t h o u t i n c i d e n t . H o w e v e r , as t h e r e m a y be a r e l a t i o n s h i p , w e p r o p o s e to u s e c a r b o n d i o x i d e i n h a l a t i o n for p o s t o p e r a tive t e s t i n g of v a s o r e a c t i v i t y in future. T h e use of a n t i c o a g u l a n t s m a y h a v e b e e n i m p o r t a n t , as s e v e n of t h e e i g h t p a t i e n t s r e c e i v e d p e r i o p e r a t i v e t r e a t m e n t w i t h p h e n p r o c u m o n . O n l y t w o p a t i e n t s (Cases 4 a n d 5) h a d PP v a l u e s w i t h i n t h e t h e r a p e u t i c r a n g e at t h e t i m e of h a e m o r r h a g e , w h i l e in t h e r e m a i n i n g five p a t i e n t s P P w e r e a b o v e 0 . 2 (Table 3). T h i s m a k e s it less p r o b a b l e , t h a t a n t i c o a g u l a n t s p l a y e d a m a j o r role in t h e d e v e l o p m e n t of p o s t o p e r a t i v e h a e m o r r h a g e . The present study clearly indicates that patients at risk of d e v e l o p i n g p o s t e n d a r t e r e c t o m y h a e m o r r h a g e a r e t h o s e w h o p r e s e n t h i g h - g r a d e stenosis r e s u l t i n g in a s t a t e of r e d u c e d p e r f u s i o n p r e s s u r e . F o l l o w i n g r e c o n s t r u c t i o n h y p e r p e r f u s i o n will result, a n d in s o m e i n s t a n c e s this m a y l e a d to o e d e m a a n d h a e m o r r h a g e . T h e h i s t o p a t h o logic basis for t h i s m e c h a n i s m , h o w e v e r , c o u l d n o t be eluc i d a t e d by t h e p r e s e n t study. I n at least t w o p a t i e n t s a silent b r a i n i n f a r c t o c c u r r e d p o s t o p e r a t i v e l y , b u t b e f o r e t h e h a e m o r r h a g e d e v e l o p e d . T h i s s u g g e s t s t h a t posto p e r a t i v e silent i n f a r c t i o n , in p a t i e n t s w i t h p r e o p e r a t i v e h y p o p e r f u s i o n m a y be t h e p a t h o l o g i c basis fpr p o s t e n d a r t e r e c t o m y h a e m o r r h a g e in at least s o m e p a t i e n t s .

5 SOI,OMON t~k, LOrTUS CM, QUEST DO, CORRELLJW. Incidence and

etiology of intracerebral hemorrhage following carotid endarterectomy. J Neurosurg 1986; 64: 29-34. 6 SUNDTTM, EBERSOLDMJ, SHARBROUGHFW, PIEPGRASDG, MARSHWR, MESSICKJM. The risk-benefit ratio of intraoperative shunting during carotid endarterectomy. Relevancy to operative and postoperative results and complications. Ann Surtl 1986; 203:196-204. 7 WYLIEEl, HEIN ME, ADAMSJE. Intracranial hemorrhage following surgical revascularization for treatment of acute strokes. J Neurosurg 1964;21:212-215. 8 GONZALEZLL, LEWISCM. Cerebral hemorrhage following successful endarterectomy of the internal carotid artery. Surg Ggnecol Obstet 1977;122:773-777. 9 CAPLAN LR, SKILLMAN ], OJEMANN R, FIELDS WS. Intracerebral

10

lI

12

13 14

15 SPETZLERRF, WILSON CB, WEINSTEIN P, MEDHORN M, TOWNSENDJ,

16

17 Acknowledgements

Financial support was received from: Fondsborsvekselerer Henry Hansen og Hustrus Legat, P. Carl Pedersens Foundation, Vera and Carl Johan Michaelsens Foundation, the Danish Medical Research Council, The Danish Heart Foundation, Dagmar Marshalls Foundation, Fabrikant Einar Willumsens Mindelegat and Kong Christian den Tiendes Foundation.

18 19 20 21

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Eur ] Vasc Surg Vol 1, February 1987

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