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(Stroke. 1995;26:1553-1557.)
© 1995 American Heart Association, Inc.

Articles

Causes of Morbidity and Mortality After Ruptured Aneurysm Surgery in a Series of 230 Patients

The Importance of Control Angiography

F. Proust, MD; D. Hannequin, MD; O. Langlois, MD; P. Freger, MD P. Creissard, MD

From the Department of Neurosurgery, Centre Hospitalier Universitaire, Rouen, France.

Correspondence to Dr F. Proust, Department of Neurosurgery, Centre Hospitalier Universitaire, Rue de Germont, 76031 Rouen Cedex, France.

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Background and Purpose The purpose of this study was to determine the causes of morbidity and mortality after surgery for ruptured aneurysms.

Methods Two hundred thirty consecutive patients were studied. Initial hemorrhage volume and vasospasm were evaluated preoperatively with CT, transcranial Doppler ultrasonography, and angiography. Nimodipine infusion was started before surgery. Preoperative clinical status was evaluated according to Hunt and Hess grading criteria. Surgery was performed early in 186 patients (81%). Control angiography, transcranial Doppler ultrasonography, and CT were performed routinely after surgery. Hypodense areas revealed by control CT were related to intracerebral initial hematoma, vasospasm, postoperative thrombosis, or spatula hyperpressure.

Results Clinical outcome was excellent or good (Glasgow Outcome Scale [GOS] scores of 1 or 2) in 176 patients (77%), 17 (7%) were disabled (GOS score of 3), and 37 (16%) were vegetative or dead. In patients in good condition (grades I to III) preoperatively (n=200), 38 had an unfavorable outcome (GOS score of 2, 3, 4, or 5). The major cause of complication was postoperative thrombosis (42%). In patients in poor condition (grade IV or V) (n=30), 27 had an unfavorable outcome. The major cause of complication was initial bleeding (66%). Vasospasm was responsible for delayed ischemic deficit in 9 patients (3.9% of the total population).

Conclusions Systematic angiography remains by far the best means for determining the cause of a poor postoperative course.

Key Words: aneurysm • angiography • morbidity • mortality • surgery

	Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The management of SAH has considerably modified the incidence and causes of morbidity and mortality. In series including patients regardless of clinical condition or surgical timing,^{1 2 3 4 5} 44% to 62% could return to their previous occupation. The leading causes of disability and death were initial or recurrent hemorrhage and vasospasm.^{4 5 6} Recently published series of early aneurysm surgery combined with administration of a calcium channel blocker have shown that the outcome is excellent in 74% to 89% of patients in Hunt and Hess neurological grades I to III.^{7 8 9 10} This approach eliminates recurrent bleeding and reduced delayed ischemic deficit, but morbidity and mortality are still present.

Three procedures are routinely available to determine the cause of morbidity and mortality after aneurysm surgery: CT, TCD, and angiography. On CT scan, hematomas, hypodense areas, and hydrocephalus are easily identified. Conversely, the origin of new postoperative hypodense areas may be difficult to determine in the absence of further investigation. TCD is helpful in the determination of vasospasm in the MCA trunk.^{11 12 13} However, it may fail to reliably reveal vasospasm restricted to the anterior cerebral artery, the pericallosal artery, or the distal branches of the MCA.^{14 15} Moreover, postoperative TCD may misdiagnose parent artery thrombosis.

We describe a series of patients who underwent control CT scan and angiography, which allowed us to define more precisely the role of initial bleeding, vasospasm, and surgery in morbidity and mortality after aneurysm surgery.

	Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
From July 1987 to July 1993, 230 consecutive patients with ruptured aneurysms were admitted to our department. Patients ranged in age from 17 to 72 years, and the average age was 46. The ratio of females to males was 0.87:1.

Preoperative Diagnostic and Therapeutic Methods
The diagnosis of SAH was established on preoperative CT scan, particularly initial bleeding and acute hydrocephalus (Table 1). Acute hydrocephalus was noted in 12 patients (5%), and preoperative hypodense areas were observed in 7 patients. As soon as a diagnosis of SAH was established, nimodipine infusion (2 mg · h^-1) was started and continued until control angiography was performed. It was continued for at least 15 days when vasospasm was demonstrated on angiography but was stopped when there was no vasospasm.

View this table: [in this window] [in a new window]   Table 1. Observations on Preoperative CT Scan in 230 Patients

A TCD examination via the transtemporal approach was conducted 1 to 4 hours before angiography in a subgroup of 85 patients. Velocity values from the proximal MCA (M1) were used in the determination of vasospasm.^{11 12 13} The diagnosis of vasospasm was retained when mean velocity in M1 was greater than 120 cm · s^-1.

Panangiography via the femoral route was performed during the 24 hours after patient admission and showed aneurysm location (Table 2), associated aneurysms, and vasospasm compared with the contralateral side in the absence of intracerebral hematoma. The preoperative vasospasm was determined angiographically in 17 patients and on TCD in 11. It was diffuse and severe (defined as >50% of caliber reduction) in 12 patients. Angiography and surgical treatment were performed on the same day in 187 cases.

View this table: [in this window] [in a new window]   Table 2. Aneurysm Location on Angiography in 230 Patients

External ventricular drainage was performed before surgery in 25 cases: in 8 patients with symptomatic vasospasm, 12 with acute hydrocephalus, and 5 with discrepancy between a poor clinical status and moderate bleeding on CT scan. This ventricular drainage resulted in dramatic neurological improvement in 17 of the 25 patients.

Operation
Immediate preoperative clinical status was graded according to the Hunt and Hess classification.¹⁶ Patients in grades I through III were considered in preoperative good condition and patients in grades IV and V in preoperative poor condition. The distribution was as follows: 25 patients were grade I (11%), 115 grade II (50%), 60 grade III (26%), 18 grade IV (8%), and 12 grade V (5%). Surgery was performed within 24 to 36 hours of admission. One hundred eighty-six patients (81%) underwent early operation (within 72 hours after SAH). Emergency intervention was performed in patients with major intracerebral hematoma. For aneurysms located in the anterior part of the circle of Willis, a pterional approach was used. For anterior communicating artery aneurysms, a right-sided approach was systematically used except in patients with a right hypoplastic cerebral anterior artery. For vertebral aneurysms, a suboccipital trepanation was used. For the only basilar artery aneurysm, a pterional approach was used. Even in the absence of intracerebral hematoma after dural opening, initial brain swelling was noted in almost all cases of early operation. Ventricular drainage via the frontal horn was routinely performed and allowed a reduction of brain volume. Mannitol (250 mL of mannitol 10%) infusion was used to reach the basal cisterns in three patients because of brain swelling despite cephalospinal fluid drainage. The aneurysm was dissected according to microsurgical principles^{17 18} and clipped, and then the aneurysmal sac was opened. Temporary clipping was used in 15 patients (during no longer than 5 minutes), and hypotension was induced with sodium nitroprusside in 6 cases for the control of premature intraoperative rupture and in 10 cases of difficult dissection. Premature ruptures occurred in 20% of operations. At the end of operation the cisterns were irrigated systematically with in situ nimodipine.

Postoperative Treatment
Postoperative medical treatment included prophylactic anticonvulsives, nimodipine infusion, and hypervolemia with albumin solution under control of central venous pressure (>14 mm Hg). At the first sign of clinical vasospasm or when velocity was greater than 120 cm · s^-1, a Swan-Ganz catheter was placed and hypervolemia was more aggressive (increased quantity of albumin solution). Ventricular drainage systems were used in 35 patients, and intracranial pressure was monitored in 8.

Postoperative Outcome, CT Scan, TCD, and Angiography
The neurological outcome based on the GOS score¹⁹ was determined in a follow-up period ranging from 6 to 12 months after surgery.

Control CT scan and control angiography were systematically conducted 10 days after surgery and earlier in cases of clinical worsening. An additional control CT was performed 2 months later. TCD was performed in 110 patients.

Causes of Postoperative Hypodense Areas
Different types of hypodensity were demonstrated on the postoperative CT scans. Hypodensity was considered secondary to intracerebral hematoma when its size and location corresponded to the previous intracerebral hematoma. Another cause was suspected when the hypodense area was larger than expected or located in unexpected territory. Control angiography determined the cause to be either thrombosis or vasospasm. Finally, some hypodensities in particular areas were related to spatula hyperpressure when control angiography was normal.

Delayed ischemic deficit or so-called clinical vasospasm was defined according to the criteria of Kassell et al²⁰ : insidious onset, usually 4 to 9 days after SAH, characterized by decreased level of consciousness preceding focal deficit, and exclusion of other causes (rebleeding, intracerebral hematoma, hydrocephalus, metabolic disturbance, surgical complications). Vasospasm was considered responsible for infarction when a hypodensity appeared secondarily on control CT scan.

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Of 230 patients, 165 (72%) had a GOS score of 1, 11 (5%) had a GOS score of 2, 17 (7%) were disabled (GOS score of 3), and 37 (16%) were vegetative or dead (GOS score of 4 or 5) (Table 3). There were no complications due to control angiography.

View this table: [in this window] [in a new window]   Table 3. Clinical Outcome (Glasgow Outcome Scale Score) According to Preoperative Clinical Status (Hunt and Hess Grade) in 230 Patients

Patients in Good Condition Preoperatively (n=200)
Three patients had a preoperative incident responsible for death. Control CT scan was conducted in 197 patients and was normal in 118. In this latter group, control angiography revealed major-vessel occlusion in 2 and vasospasm in 35. TCD performed in 63 patients demonstrated vasospasm in 15.

Control CT scan was abnormal in 79 patients (42 had TCD). One patient demonstrated hemorrhage by rebleeding, and 9 revealed hydrocephalus. The cause of the hypodense area was only determined by CT scan in 24 patients (initial bleeding in 22 patients and abscess in 2). For the 45 others, the cause was determined by control angiography, which showed thrombosis in 18 and vasospasm in 11. Among these 11 patients, TCD was performed in 6 and demonstrated vasospasm in 5. Finally, hypodense area was related to spatula hyperpressure in 16 patients. The hypodense area on CT scan was clearly patent at 24 hours and disappeared at days 10 to 30. The location of the hypodense area was along the sylvian fissure for MCA aneurysm and near the caudate nucleus or frontal lobe for anterior communicating artery and internal carotid artery aneurysms.

One hundred sixty-two patients (81%) made a good recovery (GOS score of 1), and 38 patients (19%) had an unfavorable outcome (Table 4): 10 retained a GOS score of 2, 10 had a poor outcome (GOS score of 3), 1 became vegetative (GOS score of 4), and 17 died during hospitalization.

View this table: [in this window] [in a new window]   Table 4. Glasgow Outcome Scale Scores of 200 Patients in Good Condition Preoperatively

The principal cause of complication was thrombosis. Among 20 patients with postoperative thrombosis, 4 remained asymptomatic and 16 had an unfavorable outcome. Neurological deterioration was observed on the first postoperative day, and a hypodense area on CT scan was visible as early as 24 hours. These hypodense areas persisted as sequelae infarctions. Thromboses of the pericallosal artery in one patient and of the internal carotid artery in another were determined during the surgical procedure and accounted for the death of those patients.

Clinical vasospasm was observed in 11 patients and was responsible for poor outcome in 6 of them. It was preoperative in 3 patients admitted at days 8, 14, and 15. In 4 patients who underwent surgery for communicating anterior artery aneurysm, the clinical manifestation of postoperative vasospasm was immediate obnubilation. Four other patients developed delayed symptoms. Among these 11 patients, the intracranial pressure was greater than 20 mm Hg on admission in 4 patients and returned to normal after ventricular drainage.

Spatula hyperpressure was the cause of hypodense areas in 16 patients. Nine patients developed immediate postoperative deterioration, but their outcome was excellent with the exception of 1 patient with a hemorrhagic infarction secondary to spatula hyperpressure (GOS score of 2).

Preoperative incidents occurred in 3 patients: sliding of the aneurysmal clip, acute postoperative subdural hematoma, and rupture of the aneurysm during opening of the dura. Medical complications were responsible for unfavorable outcome in 4 patients (septic problems and pulmonary embolism). Initial bleeding caused the morbidity of 5 patients (pericallosal artery aneurysm in 2 and anterior communicating artery aneurysm in 3). In these cases, hematoma was localized in the hypothalamus or in the internal part of the dominant frontal lobe. Rebleeding occurred in 1 patient with multiple aneurysms subsequent to rupture of a giant aneurysm contralateral to the aneurysm that had been treated.

Patients in Poor Condition Preoperatively (n=30)
Of 30 patients in poor condition, 3 made a good recovery (GOS score of 1), 8 had a poor outcome (GOS scores of 2 and 3), and 19 died early.

Control CT scan was normal in 1 patient, but TCD and angiography demonstrated a preoperative vasospasm. Control CT scan was abnormal in 29 patients. A hypodense area was observed in 28 and generalized edema in 1. In 20 patients the hypodense area was secondary to initial bleeding. In the other 8 patients, control angiography showed thrombosis in 5 and vasospasm in 3. TCD was performed in 5 patients.

Twenty-seven patients had an unfavorable outcome (Table 5). The 5 cases of thrombosis occurred after emergency surgery for intracerebral hematoma (4 patients with aneurysm located on the MCA and 1 on the anterior communicating artery). In 1 patient thrombosis occurred during surgery for an aneurysm located on the anterior communicating artery. Vasospasm, preoperative in all 4 cases demonstrated by TCD, became complicated in 3. On admission these 4 patients had an intracranial pressure greater than 20 mm Hg, which became normal after ventricular drainage. Initial bleeding was the main cause of unfavorable outcome. Finally, postoperative generalized edema related to prolonged temporary clipping and preoperative hypotension occurred in 1 patient.

View this table: [in this window] [in a new window]   Table 5. Glasgow Outcome Scale Scores of 30 Patients in Poor Condition Preoperatively

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
We observed neurological deterioration essentially in the immediate postoperative period. The postoperative deterioration in the group of patients in good preoperative condition was clearly related to vascular occlusion (42.1%) and vasospasm (15.8%), with surgical trauma by spatula accounting for only 2.6%.

Vasospasm, which involves induction of delayed ischemic deficit,²¹ is considered to be a leading cause of morbidity and mortality after SAH.^{6 20 22 23} The incidence and severity of angiographic vasospasm are not obviously reduced by the introduction of anticalcic treatment,^{24 25} although a report of the Cooperative Aneurysm Study suggests that intravenous nicardipine reduces the incidence of clinical vasospasm in patients with aneurysmal SAH.²⁶ Some series find a decrease of delayed ischemic deficit when nimodipine is combined with early surgery.^{3 7 27 28} The incidence of delayed ischemic deficit ranges from 1% to 7%.^{9 10} In our series morbidity and mortality were due to delayed ischemic deficit in only 9 patients (Tables 4 and 5).

Postoperative thrombosis was rarely reported as an important agent of disability, possibly because control angiography was not routinely performed. For example, the incidence of postoperative thrombosis was only 3.1% in the International Cooperative Study on the Timing of Aneurysm Surgery.²³ Gilsbach et al²⁹ report 9 major-vessel occlusions after surgery in a series of 150 patients, but control angiography was not routinely performed in this study either. The role of thrombosis has been more precisely evaluated by systematic control angiography. Creissard et al³⁰ report a thrombosis incidence of 11% in a series of 100 subjects, Macdonald et al³¹ report a thrombosis incidence of 12% in a series of 66 patients, and Karhunen³² reports an incidence of major occlusions in 11% of 63 patients who died after aneurysm surgery. These data reveal the interest in performing postoperative angiography despite the cost. We suggest that in the absence of control angiography, thrombosis as the cause of hypodense areas might be underestimated.

The exact meaning of delayed ischemic deficit has been deduced from observation of the natural time course of SAH.^{21 33} Because of early surgical intervention for aneurysm, it is problematic to determine the cause of a new neurological deficit from clinical, TCD, and CT data. Our results show that symptoms of thrombosis and surgical trauma are generally immediately postoperative, whereas vasospasm symptoms are delayed. Early surgical intervention exposes patients to infarction after pressure of the self-retaining retractor. This is probably due to the lower tolerance of the brain during the acute stage of SAH⁹ or the disregulation of cerebral blood flow secondary to recent SAH.^{34 35} The outcome of these surgical traumas is generally favorable.

Surgical trauma may be difficult to diagnose in the presence of postoperative deterioration, particularly for anterior communicating aneurysm.⁸ It is possible that vasospasm and surgical trauma were combined in 4 cases of anterior communicating artery aneurysm. Moreover, it is sometimes difficult to detect and label clinical worsening in patients with preoperative intracerebral hematoma who undergo surgery in poor clinical condition. Therefore, it seems risky to speak of delayed ischemic deficit after early surgery when a diagnosis of thrombosis has not been made and a diagnosis of vasospasm has not been reliably established on clinical and angiographic grounds. Indeed, like Auer,²⁸ we believe that the importance of delayed ischemic deficit has been overestimated in the earlier literature. Only control angiography is able to diagnose the cause of ischemia in all cases.

It is likely that in the near future preoperative Doppler and angiography, as well as improved TCD techniques, will reduce the interest in control angiography as a means of diagnosing thrombosis and vasospasm.^{31 36 37}

Conclusion
Most of the causes of morbidity and mortality after aneurysm surgery are determined when both control CT and control angiography are performed. The leading cause of morbidity and mortality remains initial bleeding, and the second main cause is postoperative thrombosis; in contrast, the role of vasospasm appears to be insignificant in patients who undergo surgery early and receive nimodipine treatment. Therefore, we believe that angiography is still the best means to determine the cause of complications that occur after aneurysm surgery.

	Selected Abbreviations and Acronyms

 

GOS = Glasgow Outcome Scale MCA = middle cerebral artery SAH = subarachnoid hemorrhage TCD = transcranial Dopper ultrasonography

	Footnotes

 
¹ Deceased.

Received April 6, 1995; revision received May 23, 1995; accepted June 1, 1995.

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