VASCULAR Clinical Study
SURGICAL TREATMENT OF GIANT INTRACRANIAL ANEURYSMS: CURRENT VIEWPOINT Giampaolo Cantore, M.D. Department of Neurological Sciences, Istituto Neurologico Mediterraneo Neuromed, Istituto di Ricovero e Cura a Carattere Scientifico, Pozzilli, Italy
Antonio Santoro, M.D. Department of Neurosciences, Neurosurgery Unit, University of Rome Sapienza, Rome, Italy
Giulio Guidetti, M.D. Department of Radiological Sciences, University of Rome Sapienza, Rome, Italy
Catia P. Delfinis, M.D. Department of Neurosciences, Neurosurgery Unit, University of Rome Sapienza, Rome, Italy
Claudio Colonnese, M.D. Department of Neurological Sciences, Istituto Neurologico Mediterraneo Neuromed, Istituto di Ricovero e Cura a Carattere Scientifico, Pozzilli, Italy
Emiliano Passacantilli, M.D. Department of Neurosciences, Neurosurgery Unit, University of Rome Sapienza, Rome, Italy Reprint requests: Emiliano Passacantilli, M.D., via A. Nibby 5/A, 00161 Rome, Italy. Email:
[email protected] Received, June 28, 2007. Accepted, April 30, 2008.
OBJECTIVE: Despite new endovascular techniques and technological advances in microsurgery, the treatment of giant intracranial aneurysms is still a daunting neurosurgical task. Many of these aneurysms have a large, calcified neck, directly involve parent and collateral branches, and are partly thrombosed. In this retrospective review, we focused our analysis on the indications for high-flow, extracranial-intracranial (ECIC) bypass surgery using a saphenous vein graft. METHODS: A series of 130 patients were treated between 1990 and 2004; 31 patients were managed endovascularly, and 99 patients were treated microsurgically (surgical clipping in 58 patients and high-flow EC-IC bypass followed by aneurysm trapping in 41 patients). We examined the patients’ clinical records and pre- and postoperative case notes for cerebral angiographic examinations. Graft patency was verified with cerebral angiography, computed tomographic angiography, Doppler ultrasound, or graft palpation. RESULTS: The high-flow EC-IC bypass was used for all surgically treated prepetrous aneurysms (3 patients), intracavernous aneurysms (1 patient), intracavernous aneurysms with subarachnoid extension (23 patients), as well as for some supraclinoid aneurysms (12 of the 32 patients). It was also used for 1 of the 9 aneurysms located in the carotid bifurcation and 2 of 5 vertebrobasilar circulation aneurysms. Of the 58 patients managed by surgical clipping, 4 (6.9%) died, and 51 (94.4%) improved. Of the 41 patients managed with high-flow EC-IC bypass, 4 (9.8%) died and 34 (91.9%) improved. Graft patency at the follow-up examination was 92.7%. CONCLUSION: The “gold standard” for the treatment of giant aneurysms remains surgical clipping. When direct surgical clipping or endovascular repair is contraindicated, the high-flow EC-IC bypass is a viable surgical option. KEY WORDS: Extracranial-intracranial bypass, Giant aneurysm, Saphenous vein graft, Unclippable aneurysm, Uncoilable aneurysm Neurosurgery 63[ONS Suppl 2]:ONS279–ONS290, 2008
E
ven today, treatment of a patient with a giant intracranial aneurysm remains, to most neurosurgeons, a daunting and challenging task. Choosing the management strategy likely to guarantee the best possible clinical outcome has become even harder, owing to the various new techniques and refined strategies now available. Among the most effective therapeutic options for giant aneurysms are the newer endovascular techniques, including
DOI: 10.1227/01.NEU.0000313122.58694.91
intracranial stents to reconstruct the parent arterial wall and biologically active coils that allow intra-aneurysmal thrombosis (12, 13, 21, 22, 24, 27, 28, 41, 46, 52, 62, 63, 79). The promising outcomes achieved by endovascular therapy for small aneurysms nevertheless remain unconfirmed for giant aneurysms; the larger case series report high rates of recanalization and low percentages of complete closure (6, 12, 13, 21, 22, 47, 53, 57, 62, 79).
ABBREVIATIONS: AComA, anterior communicating artery; BOT, balloon occlusion test; CT, computed tomographic; ECA, external carotid artery; EC-IC, extracranial-intracranial; EEG, electroencephalogram; FT, frontotemporal; ICA, internal carotid artery; MCA, middle cerebral artery; MRI, magnetic resonance imaging; mRS, modified Rankin Scale; SAH, subarachnoid hemorrhage
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Although proximal parent vessel occlusion, Hunterian ligation, is a viable therapeutic option for aneurysms in the anterior circulation, no safe and codified tests exist for determining tolerance to vessel closure (17, 34, 42, 80). Hence, the current treatment of choice remains surgical clipping (4, 8, 15, 16, 18, 30, 48, 72, 78, 87), a procedure that guarantees complete exclusion of the aneurysm from the circulation and parent vessel patency. The complex anatomy of these aneurysms, the presence of a severely diseased parent vessel or perforating vessels within the aneurysm sac itself, and their development in anatomically complex sites nevertheless renders many aneurysms notoriously difficult to clip (22, 44, 49, 64, 72). In this setting of rapidly changing practice patterns, a widely known technique in the treatment of complex aneurysms and cranial base tumors is high-flow extracranial-intracranial (EC-IC) bypass surgery (5, 8, 20, 22, 29, 31, 32, 60, 64, 68–70, 74, 83, 89). More information on the indications for direct surgical clipping or high-flow EC-IC bypass surgery in the management of patients with giant intracranial aneurysms is needed from large series with long follow-up periods (⬎5 yr). We designed this retrospective study to review our experience in a series of patients treated in our academic center over the past 15 years for giant intracranial aneurysms, focusing our attention on patients whose aneurysms were managed with high-flow EC-IC bypass surgery. To find out whether the indications we used in this series for surgical clipping or high-flow EC-IC bypass were appropriate, we analyzed the indications, complications, and advantages of surgical clipping and highflow EC-IC bypass.
TABLE 1. Demographic and clinical characteristics of the 99 patients whose giant intracranial aneurysms were treated surgically (1990–2004)a No.
High-flow Direct EC-IC bypass clipping
Total series
99
41
58
Female
54
27
27
Male
45
23
22
Average age (yr)
48
46
50
Ruptured aneurysms
26
10
16
8
12
Hunt and Hess grade ⱕII ⬎II
2
4
73
31
42
43
20
23
41
18
23
2
2
Subarachnoid hemorrhage
26
10
16
Transient ischemic attack
14
5
9
Seizure disorder
11
4
7
5
2
3
Unruptured aneurysms Clinical presentation
Mass effect With cranial neuropathy With hemiparesis
Headache a
EC-IC, extracranial-intracranial.
A consecutive series of 130 patients underwent treatment for giant intracranial aneurysms in the Neurosurgical Unit at the University Sapienza, Rome, Italy, and the affiliated Neurosurgical Unit at Neuromed, Pozzilli, Italy, from January 1990 to December 2004 (15 years) (7). Of these 130 patients, 31 were treated endovascularly and 99 (45 men and 54 women; mean age, 48 years) were treated surgically; 58 patients underwent surgical clipping, and 41 patients underwent a high-flow EC-IC bypass using a saphenous vein graft followed by aneurysmal trapping. In 1 patient, the bypass served to prepare the aneurysmal neck for clipping, and in another patient, who has already been described elsewhere (65), a double bypass was constructed before endovascular treatment. In our series, 73 patients harbored unruptured giant aneurysms, and 26 patients had ruptured aneurysms. Twenty patients were in Hunt and Hess Grades I and II. The presenting clinical symptoms of the 99 patients studied are summarized in Table 1. The shape and, often, the large-sized neck makes giant aneurysms hard to classify according to site; therefore, we distinguished them according to the arterial segment involved by the neck. Of the 99 surgically treated giant intracranial aneurysms, 3 were located in the prepetrous segment of the internal carotid artery (ICA), 1 was an intracavernous aneurysm, 23 were intracavernous aneurysms with subarachnoid extension, 32 involved the supraclinoid segment of the ICA, 9 involved the ICA bifurcation, 11 involved the anterior communicating artery (AComA), 15 involved the middle cerebral artery (MCA) bifurcation, and 5 involved the vertebrobasilar circulation (Table 2).
All patients underwent computed tomographic (CT) brain scanning and magnetic resonance imaging (MRI). Patients treated from 2000 on also underwent 3-dimensional CT angiography to study the patent and thrombosed aneurysmal segments. All patients also had cerebral digital subtraction angiography with the balloon occlusion test (BOT) when appropriate. The findings from diagnostic imaging were assessed by an interventional neuroradiologist, and patients whose aneurysms were deemed suitable for coil embolization or intracranial stent placement, or both procedures, were scheduled for endovascular treatment as the primary choice (31 of 130 patients). In this study, we defined aneurysms as unclippable or difficult to clip on the basis of the findings on MRI, CT angiography, and cerebral angiography, according to the following criteria: location of the aneurysm, neck dimension, fusiform parent artery dilation, and calcified neck. Patients whose aneurysms involved the supraclinoid tract or the ICA bifurcation first underwent surgical exploration to evaluate the feasibility of direct microsurgical clipping. If clipping proved unusually difficult, they underwent high-flow EC-IC bypass followed by aneurysm trapping in the same operative session. When selecting patients for high-flow EC-IC bypass, we considered 2 groups. Patients younger than 70 years (an arbitrary cutoff line derived from our experience and the increased risk of concomitant medical illnesses in elderly patients) whose general condition was good (American Society of Anesthesiologists scale status classification ⱕII) (3, 19, 36), in whom we anticipated sacrifice of a major vessel, underwent high-flow EC-IC bypass. Patients in poor clinical condition (American Society of Anesthesiologists scale ⬎II) and those older than 70 years underwent preoperative BOT. All patients who failed BOT were treated with high-flow EC-IC bypass, regardless of their
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PATIENTS AND METHODS
GIANT ANEURYSM EXTRACRANIAL-INTRACRANIAL BYPASS
TABLE 2. Summary of aneurysm locations and treatment approachesa Aneurysm location
No. of patients (%)
High-flow EC-IC bypass
Direct clipping
Surgical approach
Prepetrous A.
3 (3%)
ICA-ICA, 1 ECA-MCA, 2
FTOZ, 1 FT, 2
Intracavernous A.
1 (1%)
ICA-MCA, 1
FT, 1
Intracavernous A. with subarachnoid extension
23 (23.2%)
ICA-MCA, 16
32 (32.3%)
ICA-MCA, 9 ECA-MCA, 3
9 (9.1%)
ECA-MCA, 1
ECA-MCA, 7 Supraclinoid A. A. involving the ICA bifurcation
FT, 23 20
FTOZ, 20 FT, 12
8
FT, 9
A. of the AComA
11 (11.1%)
11
FT, 11
A. of the MCA
15 (15.2%)
15
FT, 15
1
FTOZ, 1
True PComA A.
1 (1%)
ECA-MCA + coiling, 1
A. of the upper third of the BA
1 (1%)
ECA-MCA (ICA occluded, collateral flow from BA)
FT, 1
A. of the vertebrobasilar junction
1 (1%)
1
TS, 1
PICA
1 (1%)
1
PLA, 1
AICA
1 (1%)
1
RS, 1
Total
99 (100%)
58
99
41
a EC-IC, extracranial-intracranial; A., aneurysm; ICA, internal carotid artery; ECA, external carotid artery; MCA, middle cerebral artery; FTOZ, frontotemporo-orbitozygomatic; FT, frontotemporal; AComA, anterior communicating artery; PComA, posterior communicating artery; BA, basilar artery; TS, transsigmoidal; PICA, posteroinferior cerebellar artery; PLA, posterolateral approach; AICA, anteroinferior cerebellar artery; RS, retrosigmoidal.
clinical condition and age. Patients who tolerated BOT underwent ICA closure (Fig. 1). The indications for the type of bypass used changed as the series progressed. Patients treated early (1990–1997; 19 cases) underwent a preoperative BOT consisting of a 30-minute parent vessel closure in hypotension and during electroencephalogram (EEG) monitoring. Patients who failed BOT had a bypass using the external carotid artery (ECA) as the donor vessel; otherwise, the ICA was used. Graft patency was evaluated with intraoperative angiography, and to verify graft patency with greater certainty, the parent vessel was closed endovascularly 1 or 2 weeks after the procedure. Abnormalities that we observed in intraoperative EEG activity and somatosensory evoked potentials in patients who tolerated preoperative BOT subsequently induced us to change our clinical practice pattern. Later in the series (1997–2004; 22 cases), we used an intraoperative occlusion test alone; that is, we closed the ICA, ECA, and common carotid artery for 15 minutes during EEG recording under normotensive conditions and pharmacologically induced brain protection (burst suppression). If the patient failed the intraoperative occlusion test, we constructed the bypass with the ECA as the donor vessel and closed the ICA intraoperatively after verifying graft patency with intraoperative angiography and, from 2001 on, with an intraoperative flowmeter (Transonic Systems, Inc., Ithaca, NY). All surviving patients in this retrospective study were followed in the outpatient clinic, and their clinical records and radiological notes were studied. Of the 99 patients studied, 86 underwent CT or MRI scans at 1 and 6 months and annually thereafter. To evaluate the functional health of our patients, we analyzed the preoperative scores on the modified Rankin Scale (mRS) (Table 3) (81); the same mRS scale was used at discharge and during follow-up at the same time from January
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to March 2007. We defined patients with a favorable functional outcome as those with an mRS score equal to or higher than the preoperative mRS score. In patients treated with high-flow EC-IC, bypass graft patency was assessed with Doppler ultrasound, CT angiography, and MRI angiography and, in 3 patients who declined follow-up at the beginning of this retrospective study, bypass graft patency was assessed by evaluating graft pulsation at the zygomatic root during a telephone interview (60).
Surgical Technique for High-flow EC-IC Bypass The patient lay supine with a small pad under the shoulder on the operative side, the head turned to the opposite side at about 45 degrees, and the neck slightly extended. Neurophysiological monitoring to identify possible cerebral ischemic damage during temporary clipping consisted of an EEG and somatosensory evoked potentials. The saphenous vein was then exposed, beginning from the medial malleolus to the knee. If this segment was unsuitable in caliber, the vein was exposed up to the mid-third of the thigh. Collateral veins were closed with 5–0 sutures at about 1 mm away from their origin. When exposure ended, the vein was covered with papaverine hydrochloride-soaked cottonoids. The carotid bifurcation was then exposed at the neck. The common carotid artery, ICA, and ECA were then clamped for 15 minutes while we decided on the type of lower anastomosis according to the aforementioned rationale used in the second part of our series (1997–2004). Through a frontotemporal (FT) craniotomy, the sylvian fissure was then opened widely to expose the temporal or frontal branch of the MCA. At this stage, the superficial aspect of the exposed saphenous vein was marked in situ with an ink line (the Garret line) to avoid inadvertent twisting and kinking of the graft during final posi-
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Giant aneurysm
TABLE 3. Modified Rankin Scale
Amenable to endovascular treatment?
yes
Embolization
Score
Description
0
No symptoms at all
1
No significant disability despite symptoms; able to carry out all usual duties and activities
2
Slight disability; unable to carry out all previous activities, but able to look after affairs without assistance
3
Moderate disability; requiring some help, but able to walk without assistance
4
Moderately severe disability; unable to walk without assistance and unable to attend to bodily needs without assistance
5
Severe disability; bedridden, incontinent, and requiring constant nursing care and attention
6
Dead
no
Clippable aneurysm?
yes
Clipping
no
ASA ⱕ II age ⱕ 70 yr
no
yes
BOT
No deficit
Neurological deficit
Parent vessel sacrifice without high-flow EC-IC bypass
High-flow EC-IC bypass
IOT
Tolerated
Not tolerated
M2-ICA ICA-ICA
M2-ECA
FIGURE 1. Algorithm for the surgical treatment of giant intracranial aneurysms, according to the American Society of Anesthesiologists (ASA) classification system (Class 1, patient has no organic, physiological, psychiatric, or biochemical disturbance; in other words, the patient has no system disease and is considered a healthy patient. Class 2, mild to moderate disturbances, such as anemia, obesity, diabetes, hypertension, or bronchitis). BOT, balloon occlusion test; EC-IC, extracranial-intracranial; IOT, intraoperative occlusion test; M2, M2 portion of the middle cerebral artery; ICA, internal carotid artery; ECA, external carotid artery (adapted from Dripps RD, Lamont A, Eckenhoff JE: The role of anesthesia in surgical morbidity. JAMA 178:261–266, 1961 [19]).
tioning, thus preserving the natural direction of flow. The vein was removed, connected to a pressure transducer, and distended at a constant pressure of 120 to 150 mm Hg with heparinized solution. The saphenous vein graft was then tunneled in front of the tragus. Before construction of the proximal anastomosis began, the patient was given 3000 IU of heparin and 10 mg of dexamethasone intravenously. Before transient clipping of the M2 segment of the MCA, the patient also received a barbiturate (thiopental sodium) by intravenous infusion at a dose sufficient to obtain burst suppression in the intraoperative EEG. The distal anastomosis was constructed first with 8–0 polypropylene sutures (Prolene; Ethicon, Inc., Somerville, NJ). Once suturing ended, before the MCA clips were removed, a temporary clip was placed on the graft as close as possible to the end-to-side anastomosis to avoid thrombosis as a result of blood reflux, while continuing to keep the graft distended and irrigated in heparinized saline. The proximal anastomosis was constructed and sutured end-to-end to the ICA or ECA with 7–0 Prolene sutures. When the series began, graft patency was assessed intraoperatively with angiography or real-time micro-Doppler ultrasonography. In the 4 years before the study ended, graft patency was assessed by measuring graft flow with an intraoperative flowmeter. If flow in an ECAMCA bypass exceeded 50 mL/min, the ICA was closed at the neck. Whenever possible, the aneurysm was trapped distally by closing the ICA before the origin of the posterior communicating artery.
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All patients began receiving 1 g per day of hydrocortisone (Flebocortid; Janssen-Cilag N.V., Berchem, Belgium) immediately after the operation and for a week thereafter, as well as aspirin (acetylsalicylic acid) for 1 year.
Anatomic Location and Choice of Treatment
Prepetrous Aneurysms Of the 3 patients with prepetrous aneurysms treated, 1 underwent an ICA-ICA bypass and 2 underwent an ECA-MCA bypass. None of these patients tolerated the carotid BOT. All operations preceded the advent of intracranial stents. In all 3 cases, the aneurysm was trapped and completely occluded from the circulation. For the ICA-ICA bypass, we used a frontotemporo-orbitozygomatic approach, and in the other 2 cases, we used an FT approach.
Intracavernous Aneurysms One patient who presented with an intracavernous aneurysm also had an asymptomatic contralateral intracavernous aneurysm that precluded closure of the ICA at the neck. This patient, treated later in the series, tolerated the intraoperative BOT and therefore had an ICAMCA bypass via an FT approach. The use of a high-flow EC-IC bypass was planned preoperatively according to the location of the aneurysm.
Intracavernous Aneurysms with Subarachnoid Extension The 23 patients who presented with these aneurysms all underwent high-flow EC-IC bypass. The subarachnoid extension was assessed on coronal MRI scans and other radiological images (Fig. 2). In all cases, the decision to use a high-flow EC-IC bypass was made preoperatively, after assessing the location of the neck below the anterior clinoid process. All aneurysms were exposed via an FT approach. In 15 patients (65.2%), the aneurysm was a fusiform dilation of the ICA. The first 15 patients treated when the series began all underwent preoperative BOT; of these 15 patients, 10 tolerated BOT and underwent an ICA-MCA bypass, and 5 failed BOT and had an ECA-MCA bypass. In these cases, the carotid artery was closed endovascularly 15 days later, after a new BOT had verified graft patency. In 2 of the 15 patients, spontaneous thrombosis developed in the aneurysm after bypass sur-
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GIANT ANEURYSM EXTRACRANIAL-INTRACRANIAL BYPASS
A
B
D C
E
Supraclinoid Aneurysms Of the 99 patients in this series, 32 had supraclinoid aneurysms. Of these 32 aneurysms, 15 were partially thrombosed. In all 32 cases, except 2 in whom preoperative radiological imaging showed a fusiform ICA dilation, direct clipping was attempted after exposing the carotid artery at the neck and completing an extradural clinoidectomy. Of the 32 patients who had supraclinoid aneurysms, 20 underwent direct clipping. In only 12 of the 20 patients, the ICA was temporarily closed at the neck. Arterial patency after clipping was assessed intraoperatively by transcranial micro-Doppler ultrasonography until 2001, and from then on with an intraoperative flowmeter. All patients had postoperative angiography to confirm complete obliteration. Of the 32 patients with supraclinoid aneurysms, 12 received highflow EC-IC bypasses, in 10 associated with trapping and in 2 with proximal closure of the ICA at the neck. Of these 32 aneurysms, 2 consisted of a fusiform ICA dilation, 6 had a calcified neck that measured more than 2 cm in diameter, and 2 had been previously coiled and then recanalized. In 10 of the 12 patients who received a high-flow ECIC bypass, the bypass procedure was converted during the same operative session after verifying that clipping would be unduly difficult. Of these 12 patients, 6 were patients treated early in our series who underwent preoperative BOT; 5 of them (ICA-MCA bypasses) tolerated BOT, and 1 (ECA-MCA bypass) did not. Of the 6 patients treated later in the series who underwent intraoperative BOT, 4 tolerated BOT (ICA-MCA bypass) and 2 did not (ECA-MCA bypass). The parent artery was closed with the procedure described in the previous section. Overall, in 20 patients, a frontotemporo-orbitozygomatic approach was used, and in 12, an FT approach was used (10 of these patients were treated in the second part of the series, 1997–2004).
Aneurysms Involving the ICA Bifurcation FIGURE 2. A 67-year-old woman presented with a 2-month history of headache, vomiting, right Cranial Nerve II and IV paresis, weakness, and temporospatial disorientation caused by a giant (2.8 ⫻ 3 cm in diameter) right intracavernous aneurysm with subarachnoid extension. A, preoperative anteroposterior digital subtraction angiogram of the right internal carotid artery (ICA), revealing a giant aneurysm originating from the intracavernous portion of the ICA. The 2 anterior cerebral arteries are supplied by the right ICA. B, coronal T1-weighted magnetic resonance imaging scan showing an isointensehypointense lesion located in the right sellar and suprasellar medianparamedian region that dislocates the surrounding structures. C, 3-dimensional computed tomographic (CT) angiogram showing the relationship of the giant aneurysm to the bone structures and the circle of Willis and hypoplasia of the left A1 tract (arrow). D, intraoperative photograph taken after extracranial-intracranial (EC-IC) bypass and aneurysm trapping, showing the subarachnoid component of the aneurysm (AN) and its relationship to the optic nerves (*). The clip can be seen on the right ICA (arrowhead) before the origin of the posterior communicating artery. E, completion CT angiogram showing the graft end-to-side anastomosis on the M2 portion of the right middle cerebral artery (arrow) and exclusion of the aneurysm from the circulation. gery. The remaining 8 patients, treated later in the series, underwent BOT intraoperatively; 6 of these patients tolerated BOT and underwent an ICA-MCA bypass, and 2 patients failed BOT and had an ECAMCA bypass. The ICA was closed intraoperatively after graft patency had been verified.
NEUROSURGERY
Of the 99 patients in the series, 9 had ICA bifurcation aneurysms; 8 patients underwent direct clipping, and 1 had a high-flow EC-IC bypass with aneurysm trapping. All aneurysms were exposed via an FT approach.
Aneurysms of the AComA In total, 11 patients’ aneurysms were treated with direct clipping via an FT approach. In 7 patients, no proper neck could be discerned, and in 5 patients, the A2 tracts were patent and the AComA was closed. In 5 patients, more than 3 clips were needed to reconstruct the neck and exclude the aneurysm from the circulation. Vessel patency was verified intraoperatively with transcranial micro-Doppler ultrasonography and, from 2001 on, by intraoperative transonic flow. All patients underwent postoperative angiography.
Aneurysms of the MCA MCA aneurysms were treated in all 15 patients with direct clipping via an FT approach. In all cases, given the location, we planned direct treatment preoperatively. Of these 15 aneurysms, 6 had a calcified neck and 4 were partly thrombosed. In all 15 cases, vessel patency was assessed by intraoperative Doppler ultrasonography or flowmeter. In 5 cases, 2 clips were used, and in 5 patients, more than 3 clips were used for reconstructing the aneurysm neck. All patients underwent postoperative angiography.
Vertebrobasilar Aneurysms Only 5 of the 99 patients presented with vertebrobasilar aneurysms. Of these 5 patients, 3 were treated by direct clipping. The first patient had a vertebral aneurysm at the junction of the vertebrobasilar artery,
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Of the 99 patients whose giant intracranial aneurysms were treated during the 15 years studied, 8 patients (4 who received high-flow EC-IC bypass and who had 4 direct clippings) died after undergoing direct microsurgery or high-flow EC-IC bypass, accounting for a treatment mortality rate of 8%. Of the 99 patients treated, 13 had infarctions on postoperative MRI or CT scans; 3 patients died because of infarction. In 7 patients, the vasospasm-related ischemia provoked a transient neurological deficit, which improved during the followup period. In another 3 patients, the symptoms related to ischemia were neurologically important and did not regress over time. Of the 99 patients treated, 1 patient died 10 days after the operation because of ischemia in the MCA territory; this patient had an intracavernous aneurysm with subdural extension and was operated on during the first part of our series (1990–1997). Because the preoperative BOT led to the onset of neurological deficits, an ECA-MCA bypass was constructed. During the postoperative course, the ICA remained patent. Cerebral angiography at 24 hours showed a patent graft, and the BOT at 30 minutes induced no neurological or EEG changes. The ICA was therefore closed endovascularly. Twelve hours after the procedure, the patient became hemiplegic and comatose and died 9 days later. A cranial CT scan on the third postoperative day revealed widespread ischemia in the MCA territory, and Doppler ultrasonography confirmed the presence of blood flow within the graft. The probable cause of ischemia was spread of intra-aneurysmal thrombosis to MCA branches. Another patient, operated on early in the series, died of subarachnoid hemorrhage (SAH). This patient had a supraclinoid aneurysm intraoperatively judged to be nonclippable and had undergone an ECA-MCA bypass. The postoperative angiogram showed graft patency and a marked contrast medium pooling within the aneurysm; hence, it was decided not to close the ICA and to wait for the
aneurysm to close spontaneously through the reversed flow mechanisms obtained with the high-flow EC-IC bypass (9, 66, 86). On postoperative Day 14, the patient died of SAH owing to aneurysm rupture. A third patient died on postoperative Day 20 of massive gastric bleeding with immediate hypovolemic shock followed by cardiocirculatory arrest. This was an obese patient with diabetes who had an intracavernous aneurysm with subarachnoid extension; the patient was treated in the second part of the series (1997–2004) with an ICA-MCA bypass. A patient with a giant intracavernous aneurysm with subarachnoid extension died on postoperative Day 25 of massive SAH after being discharged on Day 14 in excellent neurological condition. The patient underwent high-flow EC-IC bypass and ICA closure at its exit from the cavernous sinus. The follow-up angiogram documented complete exclusion of the aneurysm from the circulation. The autopsy study showed complete thromboembolization of the aneurysm and no new malformations. One patient who had a ruptured giant MCA aneurysm and was in Hunt and Hess Grade III when admitted underwent direct clipping and died of a severe vasospasm followed by an MCA infarction. Another patient with a ruptured supraclinoid aneurysm underwent direct microsurgical clipping and died of vasospasm-related ischemia 9 days after the SAH. A patient with a giant AComA aneurysm treated by direct surgical clipping and reconstruction using 5 clips of the arterial walls died on postoperative Day 15 of hypothalamic ischemia. A patient who underwent successful clipping of a supraclinoid ICA aneurysm died of pulmonary thromboembolism during the late postoperative course. Of the 99 patients, 22 patients (15 treated by high-flow ECIC bypass, 7 treated by direct clipping) worsened during the postoperative course (0–30 days after the intervention), with the onset of hemiparesis, dysphasia, and/or cranial nerve deficits that were not present preoperatively, accounting for a temporary neurological morbidity rate of 22.2%. In 19 of the 22 patients (13 who underwent high-flow EC-IC bypass and 6 who had direct clipping), neurological symptoms had completely regressed at follow-up; in 7 of these patients, transient neurological worsening was provoked by a graft vasospasm documented on Doppler ultrasonography and cerebral angiography (2 cases). In 3 of the 22 patients, neurological deficits persisted at follow-up, yielding a permanent treatment-associated neurological morbidity rate of 3%. In 1 of these 3 patients, a patient in whom a double bypass was used to treat a bilateral cavernous sinus aneurysm, hydrocephalus necessitated a ventriculoperitoneal shunt, and graft vasospasm-related hemiparesis developed after the second operation. Even though the vasospasm resolved, the vasospasm-related symptoms only partly regressed during the follow-up period. In another case, a 72-year-old patient who had an intracavernous aneurysm with subarachnoid extension, an ICA-MCA bypass resulted in a capsular hemorrhagic infarction, probably reflecting a “breakthrough phenomenon.” This patient became hemiplegic and disoriented, symptoms that only partly regressed during the follow-up period. In a
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exposed through the transsigmoidal approach. Another patient had an anteroinferior cerebellar artery aneurysm that was exposed through a retrosigmoidal approach. The third patient had a giant aneurysm of the posteroinferior cerebellar artery that had been previously embolized and recanalized and was exposed through a posterolateral (far lateral) approach at the craniospinal junction. In all 3 cases, afferent vessel patency was assessed with intraoperative microDoppler ultrasonography and confirmed by postoperative digital subtraction angiography. A high-flow EC-IC bypass was used in 2 of these 5 patients; 1 was the patient who had a true posterior communicating artery aneurysm already described in a previously published case report (65). The second patient had an aneurysm involving the upper third of the basilar artery and with a coexisting occluded right ICA. Because the carotid artery territory was fed by the posterior communicating artery, we envisaged aneurysm trapping and performed an ECA-MCA bypass. Ten days after the bypass and when patency was verified, the aneurysm was clipped through a frontotemporoorbitozygomatic approach.
RESULTS Patients’ Outcomes: Mortality and Morbidity
GIANT ANEURYSM EXTRACRANIAL-INTRACRANIAL BYPASS
TABLE 4. Surgical outcome and global outcomea Outcome Death Favorable
High-flow EC-IC bypass 4 (9.8%)
Direct clipping 4 (6.9%)b
c
At discharge
22 (53.6%)
47 (81%)
At follow-upd
35 (85.4%)
53 (91.4%)
a
EC-IC, extracranial-intracranial. One patient died 4 years after aneurysm treatment for reasons unrelated to the surgical procedure. c Score equal to or higher than preoperative modified Rankin Scale score. d Median follow-up period, 8.5 years (range, 2–15 yr). b
patient who presented with seizures and had a giant aneurysm involving the ICA bifurcation that was treated with direct clipping, ischemia developed in the MCA territory during the postoperative course, resulting in moderate hemiparesis that remained unchanged during follow-up. In 2 patients, a lymph collection formed at the saphenous vein harvesting site but regressed with elastic bandaging at 3 months. In 2 patients, the neck scar reopened because of a hematoma involving the operative field. In 1 patient, a cerebral abscess formed but responded to medical therapy. The median clinical follow-up period was 8.5 years (range, 2–15 years). At follow-up, of the 99 patients treated, 85 (85.86%) had a favorable outcome (Table 4). One patient died 4 years after aneurysm treatment for reasons unrelated to the surgical procedure.
Graft Patency Of the 41 saphenous vein grafts, 3 (7.3%) occluded, 1 during the early postoperative course (within 72 hours after the operation) and 2 (4.9%) during the late course (6 months and 2 years after the operation). In all cases, graft closure was asymptomatic. The graft blood flow velocity in these 41 patients was 15 to 20 cm/s, as measured by Doppler ultrasound.
Global Clinical Outcome Of the 41 patients treated with high-flow EC-IC bypass, assessment at discharge showed that 22 patients had a favorable outcome (53.6%). The mortality rate in this group was 9.8% (4 patients). At the time of the follow-up assessment (3–15 years), 35 patients had a favorable outcome (85.4%). Of the 58 patients treated with direct clipping, assessment at discharge showed that 47 patients (81%) had a favorable outcome. The mortality rate in this group was 6.9% (4 patients). At the time of the follow-up assessment, 53 patients (91.4%) had a favorable outcome.
DISCUSSION In this large series of patients treated in our academic center over the past 15 years for giant intracranial aneurysms, the complications related to direct clipping and to high-flow EC-IC
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bypass overlap those described in similar published series of patients treated with the various microsurgical techniques (4, 10, 15, 16, 18, 26, 30, 35, 40, 43, 45, 48, 67, 72, 73, 75, 85, 86).
Choice of Microsurgical Treatment (Clipping versus High-flow EC-IC Bypass) The good outcome of the patients in the series we reviewed suggest that the indications we used in this series for surgical clipping or high-flow EC-IC bypass were appropriate. Our review emphasizes that these criteria for the surgical treatment of giant intracranial aneurysms still hinge on the anatomic location of the aneurysm, the size of the neck, and the presence of a calcified neck or a fusiform dilation in the parent artery (2, 10, 87). By integrating these data obtained from the preoperative neuroimaging workup, we were able to plan surgical aneurysmal repair to foresee problems that might arise and assess the possible advantages or disadvantages of each treatment. Only 26 cases were ruptured aneurysms; of these, 20 were in Hunt and Hess Grades I and II. In our series, SAHs with good Hunt and Hess grades did not significantly influence the choice of treatment or the outcome. Our decision to distinguish giant aneurysms according to the arterial segment involved by the neck seems to be helpful because it avoided exposing patients with prepetrous aneurysms, intracavernous aneurysms, and intracavernous aneurysms with subarachnoid extension to the known risks of direct clipping. Direct clipping of intracavernous aneurysms using a microsurgical cranial base approach, first proposed by Dolenc (15, 16) and Sindou et al. (71), also found favor with others from the late 1980s onward (4, 14, 48, 59). These earlier reports notwithstanding, most investigators, including our own neurovascular team—encouraged by published results similar to and sometimes even better than those obtained with direct clipping, especially for cranial nerve deficits (11, 20, 25, 32, 46)— deemed it safer and less laborious to manage these aneurysms with other available modalities, namely EC-IC bypass. When deciding whether supraclinoid aneurysms should be treated by direct clipping, in addition to considering the anatomic location documented on the neuroimaging workup, we relied on intraoperative exploration using extradural clinoidectomy. This procedure provides excellent exposure of the clinoid ICA segment, thereby facilitating clipping (26, 37, 54, 55, 76, 87, 88). Accordingly, none of the patients in our series had aneurysmal rupture or optic nerve deficits related to extradural clinoidectomy. These encouraging results notwithstanding, our experience again stresses that for supraclinoid aneurysms, even more than for intracavernous aneurysms, the choice of treatment plan (direct clipping or high-flow EC-IC bypass plus trapping) fundamentally depends on the surgeon’s experience and the presence of other concomitant anatomic factors (size of the neck, calcified neck, and fusiform dilation).
Indications for High-flow EC-IC Bypass In this series, when deciding which patients should undergo high-flow EC-IC bypass, we invariably used a modified uni-
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versal approach to cerebral revascularization. Unlike the customarily reported universal approach to cerebral revascularization, which envisages constructing a bypass whenever sacrifice of a major vessel is anticipated (33, 45), the modified universal approach we used envisaged the high-flow EC-IC bypass only for patients younger than 70 years of age who were in good clinical condition (American Society of Anesthesiologists scale score ⱕII). Therefore, we reserved recourse to Hunterian ligation in patients at high surgical risk who failed to meet these criteria but tolerated BOT (Fig. 1). This modified approach has several advantages over selective revascularization, a procedure that entails using carotid BOT to identify a group of patients at risk for closure of a major artery (the ICA) and performing cerebral revascularization in this group of patients alone (11, 25, 32, 38, 58, 70, 74, 82). First, it eliminates the risk related to carotid BOT (range, 1.7–7%) (33, 45, 51, 57, 77) and the potential risk of early ischemia (range, 2–22.7%) (45, 57) and late ischemia (0–1.9%/yr) (34, 45, 56, 61), even in patients who tolerate BOT. It also eliminates the low yet well-documented risk of new aneurysms caused by changes in blood flow dynamics after vessel closure without bypass (33, 38, 42, 50, 84). A further possible disadvantage of selective cerebral revascularization is that even patients in whom no neurological deficits or EEG changes develop after BOT may exhibit MRI-documented delayed first-pass transit of contrast material through the affected cerebral hemisphere, indicative of altered perfusion without concurrent changes in cerebral blood flow or blood volume (23). By avoiding cerebral revascularization in patients at high surgical risk related to age and concomitant medical illness, the modified universal approach we used reduces early and late risks and improves overall outcome. In an attempt to reduce the complications linked to cerebral revascularization, we used staged revascularization and aneurysm occlusion in the early years (1990–1997), whereas in more recent years (1997–2004), we used single-stage combined revascularization and closure of the aneurysm. The staged revascularization strategy including a second, postoperative ICA test occlusion had a twofold aim: it angiographically verified bypass patency, and it postoperatively confirmed adequate clinical adaptation to the improved flow (25, 46). In a small series of 9 patients selected according to this rationale, 5 superficial temporary artery-MCA bypasses and 4 high-flow EC-IC bypasses (ECA-MCA), high-flow revascularization led to no major neurological complications, the aneurysms were all thrombosed, and in 1 case, the bypass and the ICA were closed without major complications (25). The good results obtained by Hacein-Bey et al. (25) and later by Lawton et al. (46), using a strategy of staged revascularization and occlusion, were not confirmed in our series. In the first part of our series, 1 patient died of SAH while we awaited spontaneous closure, and another patient died of cerebral ischemia related to graft vasospasm after the postoperative BOT. Therefore, we advise against delayed parent vessel occlusion. After we eliminated pre- and postoperative BOT, gained more experi-
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ence, and used a 1-step bypass technique, we had no further cases of aneurysm rebleeding and no graft closure as a result of lack of flow demand. These markedly improved results in the second part of the series suggest that closing the ICA immediately after bypass surgery (1-stage procedure) is a valid strategy for reducing some of the complications linked to cerebral revascularization. Although we have emphasized saphenous vein grafts in this review, vascular neurosurgeons are increasing their use of radial artery grafts. Radial artery grafts are appealing because they have arterial architecture, are easily harvested, provide intermediate to high flow, and improve overall patency rates. The most serious disadvantage of radial artery graft is the presence of arterial spasms, while a potential disadvantage includes endothelial injury caused by denervation or disruption of the vasa vasorum (39). The long-term patency rate for radial artery grafts has not been reported in the neurosurgery literature. Therefore, while radial artery grafts may improve these numbers, the expected patency with saphenous vein grafts is still sufficiently high.
Minimizing Complications In our series, the most important cause of complication after direct surgical clipping of a giant intracranial aneurysm was closure or subocclusion of an afferent or efferent vessel, or both (4, 18, 26, 30, 35, 40, 43, 45, 72, 75, 85). To circumvent this problem, we used various clipping techniques on a case-bycase basis, including combined clipping using straight or fenestrated clips, tandem clipping, and dome clipping for aneurysms that had a thick-walled neck. As our experience increased, we found ways of minimizing some of these complications. For example, we used clips of various types, including ultralong, fenestrated, and booster clips, and tried to make our intraoperative surgical strategy as flexible as possible (35, 72). Our experience in this large series confirms that a crucial point in managing giant intracranial aneurysms is meticulous intraoperative control of vessel patency during direct surgical clipping and during high-flow EC-IC bypass surgery. We therefore agree with others in highlighting the importance of intraoperative angiography, micro-Doppler ultrasonography, and a flowmeter (1, 47). In the early part of the series, we used intraoperative angiography for follow-up after direct clipping and also to check intraoperative graft patency. Intraoperative micro-Doppler ultrasonography provided useful information, had a low risk of complications, and was comparatively simple to use. We made ample use of the intraoperative flowmeter to check patency after direct clipping and to measure blood flow within the graft. Although values exceeding 60 mL/min seem good predictors of graft success, these data need to be confirmed in larger series with longer follow-up. The limitation of all currently available intraoperative imaging techniques is that none of them verify the patency of the perforating arteries, an outcome currently guaranteed only by a meticulous surgical technique.
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CONCLUSIONS
1. Akdemir H, Oktem IS, Tucer B, Menkü A, Bas¸ aslan K, Günaldi O: Intraoperative microvascular Doppler sonography in aneurysm surgery. Minim Invasive Neurosurg 49:312–316, 2006. 2. Anson JA, Lawton MT, Spetzler RF: Characteristics and surgical treatment of dolichoectatic and fusiform aneurysms. J Neurosurg 84:185–193, 1996. 3. ASA Committee on Clinical Anesthesia Study Commissions: ASA House of Delegates-1962 Session. 501–1.1/page 1: www.asahq.org. Accessed 9/14/2008. 4. Ausman JI, Diaz FG, Sadasivan B, Gonzeles-Portillo M Jr, Malik GM, Deopujari CE: Giant intracranial aneurysm surgery: The role of microvascular reconstruction. Surg Neurol 34:8–15, 1990. 5. Brambilla G, Paoletti P, Rodriguez y Baena R: Extracranial-intracranial arterial bypass in the treatment of inoperable giant aneurysms of the internal carotid artery. Report of a case. Acta Neurochir (Wien) 60:63–69, 1982. 6. Braun IF, Battey PM, Fulenwider JT, Per-Lee JH: Transcatheter carotid occlusion: An alternative to the surgical treatment of cervical carotid aneurysms. J Vasc Surg 4:229–302, 1986. 7. Cantore G: Management of giant aneurysms. Presented at the meeting of the World Federation of Neurosurgical Societies, Marrakech, June 19–24, 2005. 8. Cantore GP, Santoro A: Treatment of aneurysms unsuitable for clipping or endovascular therapy. J Neurosurg Sci 42 [Suppl 1]:71–75, 1998. 9. Cantore G, Santoro A, De Pian R: Spontaneous occlusion of supraclinoid aneurysms after the creation of extra-intracranial bypasses using long grafts: Reports of two cases. Neurosurgery 44:216–220, 1999. 10. Caramia F, Santoro A, Pantano P, Passacantilli E, Guidetti G, Pierallini A, Fantozzi LM, Cantore GP, Bozzao L: Cerebral hemodynamics on MRI perfusion images before and after bypass surgery in patients with giant intracranial aneurysms. AJNR Am J Neuroradiol 22:1704–1710, 2001. 11. Carter BS, Ogilvy CS, Putman C, Ojemann RG: Selective use of extracranialintracranial bypass as an adjunct to therapeutic internal carotid artery occlusion. Clin Neurosurg 46:351–362, 2000. 12. Cognard C, Weill A, Castaings L, Rey A, Moret J: Intracranial berry aneurysms: Angiographic and clinical results after endovascular treatment. Radiology 206:499–510, 1998. 13. Cognard C, Weill A, Spelle L, Piotin M, Castaings L, Rey A, Moret J: Long term angiographic follow-up of 169 intracranial berry aneurysms occluded with detachable coils. Radiology 212:348–356, 1999. 14. Diaz FG, Ohaegbulam S, Dujovny M, Ausman JI: Surgical alternatives in the treatment of cavernous sinus aneurysms. J Neurosurg 71:846–853, 1989. 15. Dolenc V: Direct microsurgical repair of intracavernous vascular lesions. J Neurosurg 58:824–831, 1983. 16. Dolenc VV: Extradural approach to intracavernous ICA aneurysms. Acta Neurochir Suppl 72:99–106, 1999. 17. Drake CG, Peerless SJ, Ferguson GG: Hunterian proximal arterial occlusion for giant aneurysms of the carotid circulation. J Neurosurg 81:656–665, 1994. 18. Drake CG, Peerless SJ: Giant fusiform intracranial aneurysms: Review of 120 patients treated surgically from 1965 to 1992. J Neurosurg 87:141–162, 1997.
19. Dripps RD, Lamont A, Eckenhoff JE: The role of anesthesia in surgical morbidity. JAMA 178:261–266, 1961. 20. Gelber BR, Sund TM: Treatment of intracavernous and giant carotid aneurysms by combined internal carotid ligation and extra- to intracranial bypass. J Neurosurg 52:1–10, 1980. 21. Goddard AJ, Annesley-Williams D, Gholkar A: Endovascular management of unruptured intracranial aneurysms: Does outcome justify treatment? J Neurol Neurosurg Psychiatry 72:485–490, 2002. 22. Gonzalez NR, Duckwiler G, Jahan R, Murayama Y, Viñuela F: Challenges in the endovascular treatment of giant intracranial aneurysms. Neurosurgery 59 [Suppl 3]:S113–S124, 2006. 23. Griffiths PD, Wilkinson ID, Mitchell P, Patel MC, Paley MN, Romanowski CA, Powell T, Hodgson TJ, Hoggard N, Jellinek D: Multimodality MR imaging depiction of hemodynamic changes and cerebral ischemia in subarachnoid hemorrhage. AJNR Am J Neuroradiol 22:1690–1697, 2001. 24. Gruber A, Killer M, Bavinzski G, Richling B: Clinical and angiographic results of endosaccular coiling treatment of giant and very large intracranial aneurysms: A 7-year, single center experience. Neurosurgery 45:793–804, 1999. 25. Hacein-Bey L, Connolly ES Jr, Duong H, Vang MC, Lazar RM, Marshall RS, Young WL, Solomon RA, Pile-Spellman J: Treatment of inoperable carotid aneurisms with endovascular carotid occlusion after extracranial-intracranial bypass surgery. Neurosurgery 41:1225–1234, 1997. 26. Heros RC, Nelson PB, Ojemann RG, Crowell RM, DeBrun G: Large and giant paraclinoid aneurysms: Surgical techniques, complications, and results. Neurosurgery 12:153–163, 1983. 27. Higashida RT, Halbach VV, Dowd C, Barnwell SL, Dormandy B, Bell J, Hieshima GB: Endovascular detachable balloon embolization therapy of cavernous carotid artery aneurysms: Results in 87 cases. J Neurosurg 72:857–863, 1990. 28. Higashida RT, Smith W, Gress D, Urwin R, Dowd CF, Balousek PA, Halbach VV: Intravascular stent and endovascular coil placement for a ruptured fusiform aneurysm of the basilar artery. Case report and review of the literature. J Neurosurg 87:944–949, 1997. 29. Hoit DA, Malek AM: Fusion of three-dimensional calcium rendering with rotational angiography to guide the treatment of a giant intracranial aneurysm: Technical case report. Neurosurgery 58:ONS-E173, 2006. 30. Hosobuchi Y: Direct surgical treatment of giant intracranial aneurysms. J Neurosurg 51:743–756, 1979. 31. Inoue T, Tsutsumi K, Ohno H, Shinozaki M: Revascularization of the anterior cerebral artery with an A3-A3 anastomosis and a superficial temporal artery bypass using an A3-radial artery graft to trap a giant anterior communicating artery aneurysm: Technical case report. Neurosurgery 57: E207, 2005. 32. Jafar JJ, Russel SM, Woo HH: Treatment of giant intracranial aneurisms with saphenous vein extracranial-to-intracranial bypass grafting: Indications, operative technique, and results in 29 patients. Neurosurgery 51:138–146, 2002. 33. Javedan SP, Deshmukh VR, Spetzler RF, Zabramski JM: The role of cerebral revascularization in patients with intracranial aneurysms. Neurosurg Clin N Am 36:541–555, 2001. 34. Kak VK, Taylor AR, Gordon DS: Proximal carotid ligation for internal carotid aneurysms: A long-term follow-up study. J Neurosurg 39:503–513, 1973. 35. Kato Y, Sano H, Imizu S, Yoneda M, Viral M, Nagata J, Kanno T: Surgical strategies for treatment of giant or large intracranial aneurisms: Our experience with 139 cases. Minim Invasive Neurosurg 46:339–343, 2003. 36. Keats AS: The ASA classification of physical status—A recapitulation. Anesthesiology 49:233–236, 1978. 37. Khan N, Yoshimura S, Roth P, Cesnulis E, Koenue-Leblebicioglu D, Curcic M, Imhof HG, Yonekawa Y: Conventional microsurgical treatment of paraclinoid aneurysms: State of the art with the use of the selective extradural anterior clinoidectomy SEAC. Acta Neurochir (Wien) Suppl 94:23–29, 2005. 38. Klemme WM: Hemorrhage from a previously undemonstrated intracranial aneurysm as a late complication of carotid artery ligation. Case report. J Neurosurg 46:654–658, 1977.
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Surgery still has a predominant role in the treatment of giant intracranial aneurysms. An especially exacting task for the neurosurgeon is choosing the most appropriate management strategy, above all one that puts the patient at lower risk. The reference standard for the treatment of giant aneurysms remains direct surgical clipping. Modern neurosurgeons managing intracranial aneurysms should have expertise in high-flow ECIC bypass, a technique that will resolve many complex cases, thus leaving recourse to Hunterian ligation only for patients at high surgical risk.
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Acknowledgment This work is dedicated to the memory of Antonino Agrillo, M.D., colleague and friend.
COMMENTS
D
espite advances in endovascular treatment for intracranial aneurysms, microsurgery plays the predominant role in the treatment of giant aneurysms. Cantore et al. retrospectively reviewed their 15-year experience treating 130 patients with giant aneurysms (mean duration of clinical follow-up 6.8 years) of whom 99 were treated with microsurgery (58 surgical clipping and 41 with high-flow extracranialintracranial bypass and trapping or proximal ligation). In patients who were younger than 70 years and healthy (American Society of Anesthesiologists Class ⬍II), bypass was performed if vessel sacrifice was planned. In patients who were older than 70 years or in poor clinical condition (American Society of Anesthesiologists Class ⬎II) a balloon occlusion test was performed (intraoperatively later in the series [1997–2004]) to determine the need for bypass. The one-stage procedure was felt by Cantore et al. to decrease the risk of the treatment. All patients with prepetrous aneurysms, intracavernous aneurysms, and intracavernous aneurysms with subarachnoid extension underwent bypass procedures. The treatment mortality was 8% and morbidity was 22.2% (19 of 22 patients showed complete symptom regression at a late follow-up examination). Early in the microsurgical era the idea of a Hunterian strategy being used was considered a failure. The early neurovascular surgeons went to extreme lengths to reconstruct even the most difficult lesions perfectly. Over time it has been recognized that in many situations the acute and long-term risks of reconstruction can be higher than the ischemic and thrombotic risks associated with proximal vessel occlusion. The goal should always be a perfect patient rather than a perfect angiogram. The technique of trial balloon occlusion has allowed us not only to identify which patients need revascularization but also to quantify how much additional flow is needed. For example, if a patient clinically tolerates trial balloon occlusion but develops a minor electrophysiological abnormality during hypotension, we recommend a low-flow (superficial temporal artery) bypass. In contrast, if a dense neurological deficit develops shortly after balloon occlusion, we typically recommend a high-flow graft. Over time we have migrated away from the saphenous vein as a donor in favor of
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the radial artery. This vessel has a significantly better size match up with M2, M3, and P3 vessels. The successful treatment of giant intracranial aneurysms remains difficult and requires that the surgeon have a clear understanding of the patient’s cerebrovascular anatomy and the unique characteristics of the aneurysm. The use of high-flow bypass, as demonstrated by Cantore et al., plays a vital role in managing this disease and allowing the successful elimination of the giant aneurysm from the circulation. Daniel Surdell H. Hunt Batjer Chicago, Illinois
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antore et al. presented 130 patients with giant intracranial aneurysms treated over a 1-year span. Of these patients, 99 were treated surgically, and the remaining 31 patients underwent endovascular therapy. Surgical clipping was accomplished in 58 patients. The other 41 surgically treated patients underwent placement of a highflow bypass using a saphenous vein graft. Cantore et al. used a treatment decision algorithm that relied on a balloon test occlusion as well as intraoperative determination of the suitability of aneurysm clipping. They advocated a high-flow bypass for all unclippable giant aneurysms. We follow a similar protocol for patients in whom balloon test occlusion fails. In patients with a giant aneurysm that tolerates balloon test occlusion, we tend to perform a low-flow bypass in the form of a superficial temporal artery-to-middle cerebral artery bypass. We agree with the authors that flow reversal, with or without trapping, is an effective way to obliterate the aneurysm. Regarding giant aneurysms involving the posterior circulation, in addition to flow reversal, we have, in appropriate patients, use hypothermic cardiac arrest with direct aneurysm clipping and have obtained good results. We find it interesting that Cantore et al. managed 31 of 130 aneurysms with endovascular treatment, especially because they demonstrated considerable expertise in clipping aneurysms or performing a vascular bypass for the rest of their patients. At our institution, we consider giant aneurysms for endovascular therapy only if direct surgical treatment fails. Even with stent and balloon remodeling technologies, complete endovascular obliteration is rare and associated with significant recanalization rates. We believe that giant aneurysms should primarily be treated by direct clipping when feasible and by a bypass procedure when clipping is untenable. Certainly combined endovascular and revascularization procedures have provided new solutions for particularly difficult aneurysms. In summary, Cantore et al. have presented a rational approach to this very difficult neurosurgical condition as well as their patients’ excellent outcomes Shervin R. Dashti Robert F. Spetzler Phoenix, Arizona
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antore et al. presented a series of 99 giant aneurysms treated surgically between 1990 and 2004. They experienced a favorable outcome at discharge (defined as a modified Rankin Scale [mRS] score equal to or better than the patient’s preprocedure mRS score) in 70% of patients. With this modern comparative surgical series, Cantore et al. have presented an excellent explanation of their decision-making algorithm guiding the use of extracranial-intracranial bypass that will doubtlessly be of aid to many in the neurosurgical community.
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However, we, as reviewers, must also take a moment to state our disappointment that such an overall strong article would fail to have outcome data presented with a standardized accepted assessment tool. Although Cantore et al. make reference to the mRS (one such standardized assessment tool), they do not actually report the patients’ actual mRS scores, but rather they substitute “favorable” and “unfavorable” and base the designation on the patient’s premorbid state. Although these data are also interesting, a true objective functional assessment would greatly improve comparability and substantially improve the reader’s true understanding of the patients’ outcomes— knowledge that is critical in both decision-making and preprocedure patient education. In conclusion, we feel that the neurosurgical community will benefit from this addition to our literature. However, in the current age of evidence-based medicine and disseminated knowledge of the fundamentals of epidemiology, we must frown upon the authors’ lack of reporting patient results with an accepted outcome assessment tool. We hope future efforts will include such standardized tools.
Cantore et al. have demonstrated their significant experience in reporting their data in an honest and critical fashion. Robert H. Rosenwasser Philadelphia, Pennsylvania
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antore et al. analyzed 130 patients with giant aneurysms treated by coil embolization, direct clipping, and high-flow bypass with parent artery occlusion. They showed a unique algorithm used in determining therapeutic modalities based on their experiences. In the surgical treatment with high-flow bypass, they added high-flow bypass in all aneurysms treated by trapping when patients were younger than 70 years old. They treated some patients older than 70 years without bypass. There is no clear evidence for this cutoff line. However, the number of patients is sufficient, and the clinical result of their series seems excellent. These facts might indicate the feasibility of their algorithm. I think this article is of much clinical value for the management of giant intracranial aneurysms. Ken-ichiro Kikuta Kyoto, Japan
J Mocco L. Nelson Hopkins Buffalo, New York
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antore et al. described their experience in the management of 130 patients treated between 1990 and 2004. Of this group, 31 were managed endovascularly and 99 microsurgically. There is no question that in this day and age surgical management still has a very important role for giant aneurysms, and, in fact, for most aneurysms that cannot be treated with an endovascular approach. With the exception of a deconstructive procedure with and without bypass, direct surgical intervention is generally the preferred methodology. These are difficult lesions and at the current time require significant decision-making and technical skills to deal with either from an endovascular standpoint or a surgical standpoint. With covered stents now being available, many paraclinoid lesions perhaps will be dealt with quite effectively. However, in more distal lesions in which efferent vessels are important, direct surgical reconstruction with or without bypass is still the mainstream treatment.
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Nobuo Hashimoto Osaka, Japan
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n this article, Cantore et al. reported their experience with 99 giant intracranial aneurysms, 41 being treated by high-flow bypass and occlusion and 58 being treated by clipping. The results were very good overall, with 85% of the patients doing well at follow-up examination. Any series of giant aneurysms such as this is likely to contain a large number of intracavernous aneurysms, a fact that must be taken into account when one is comparing results with those of other series, because they generally have a good prognosis, if a good-quality bypass is performed. In the next 10 years, newer stent technology such as the “pipeline stent” will have a major impact on the treatment of giant aneurysms, obviating the need for open surgery. This article should be considered a benchmark, as Cantore et al. have demonstrated excellent results and provided a thoughtful publication. Laligam N. Sekhar Seattle, Washington
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