Michael T. Lawton, M.D.,and Robert F. Spetzler, M.D.

Internal Carotid Artery Sacrifice

for Radical Resection

of Skull Base Tumors

Anterior skull base tumors frequently encase theinternal carotid artery (ICA).1-8 Because complete resec-

tion is the objective of most tumor operations, the surgeonmust decide how to manage this artery. Some tumors can

be dissected cleanly from the artery and resected com-

pletely with carotid preservation.' Other tumors, how-ever, adhere to or invade the artery and cannot be resectedtotally without injuring it.3'5-8 The choice between pre-

serving the ICA and resecting a tumor subtotally or sacri-ficing the ICA to obtain a complete resection is difficultand controversial. Furthermore, the issue of whether toreconstruct the ICA after sacrifice is also controversial.We review our experience with ICA sacrifice and presentour strategy for managing the ICA in the radical resectionof anterior skull base lesions.

MATERIALS AND METHODS

In an experience with more than 300 anterior skullbase tumors treated between 1988 and 1994, the ICA was

sacrificed and revascularized in 10 patients. There were

five women and five men with an average age of 48 years

(range, 31 to 72 years).Four patients presented with untreated tumors. Six

patients sought treatment for recurrent tumor after beingtreated elsewhere. All six of these patients previouslyunderwent surgical resection of their tumors, with multi-ple resections in four patients. Five patients receivedradiation therapy, and none received chemotherapy.

Five patients presented with symptoms of mass ef-

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Skull Base Surgery, Volume 6, Number 2, April 1996 Division of Neurological Surgery, Barrow Neurological Institute, St. Joseph's Hospital andMedical Center, Phoenix, Arizona. Reprint requests: Dr. Spetzler,% Neuroscience Publications, Barrow Neurological Institute, 350 West ThomasRoad, Phoenix, AZ 85013-4496. Copyright X) 1996 by Thieme Medical Publishers, Inc., 381 Park Avenue South, New York, NY 10016. All rightsreserved.

SKULL BASE SURGERYNOLUME 6, NUMBER 2 APRIL 1996

fect and neural compression. Two patients had progres-sively worsening pain, two had episodes of excessivenasopharyngeal bleeding, and one had transient ischemicattacks related to occlusion of the ICA by tumor. Cranialnerve (CN) deficits were present in all 10 patients andincluded two patients with decreased vision from opticnerve compression, nine patients with extraocular musclemovement abnormalities (CN III palsy, n = 9; CN IV palsy,n = 6; CN VI palsy, n = 7), seven patients with sensorydeficits in the trigeminal distributions, four patients withfacial paresis or palsy, one patient with hearing loss, andtwo patients with deficits related to the accessory nerve.The motor examination in all 10 patients was normal.Based on Glasgow Outcome Score (GOS) criteria,9 all 10patients had moderate preoperative disabilities (GOS 2).

Eight tumors were located in and around the cav-ernous sinus, and two were in the infratemporal fossa.Eight tumors were located on the right side and two wereon the left side. Angiography demonstrated encasementof the ICA with luminal narrowing in nine patients; onepatient had complete ICA occlusion.

Pathologic examination of tumor specimens re-vealed the following diagnoses: five squamous cell car-cinomas, two adenoid cystic carcinomas, one mucoepi-dermoid carcinoma, one malignant meningioma, and onebenign meningioma.

RESU LTS

All lesions were approached through a standardfrontotemporal craniotomy. Additional exposure wasgained through an infratemporal fossa approach in threepatients, through a radical neck dissection in two patients,and through a transfacial approach in one patient. Sixpatients underwent staged resections of tumor. The tu-mors were resected totally in five patients and subtotallyin five patients.

All 10 patients had their ICA sacrificed as part of aradical tumor resection; revascularization was performedin all patients. Five patients were bypassed before tumorresection during the same operation; five were bypassedfirst, followed by tumor resection in a second-stage opera-tion. Revascularization procedures included five cervicalICA-middle cerebral artery (MCA) saphenous bypasses(including one on the contralateral side for a complica-tion), one cervical-to-supraclinoid ICA saphenous by-pass, three petrous-to-supraclinoid (C3-C5) bypasses,and two bonnet bypasses (contralateral superficial tempo-ral artery-to-ipsilateral MCA).10

Postoperative GOS decreased by one point in fourpatients. One patient developed an orocutaneous fistula,and the pectoralis muscle flap used to obliterate the fistulanecrosed. A similar patient developed a wound infectionthat progressed to sepsis and vascular insufficiency to thelatissimus dorsi muscle flap, which then resulted in necro-

120 sis. Both patients had undergone previous radical neck

dissection for tumor resection and radiation therapy, mak-ing the tissues susceptible to complications associatedwith wound healing. Both patients were treated with de-bridement and reconstruction of the wound with addi-tional muscle flaps, and both patients recovered theirbaseline neurologic status before dying 1.5 and 1.3 yearsafter surgery, respectively.

Two patients suffered ischemic complications. A by-pass graft occlusion in one patient resulted in infarctionand new deficits despite immediate revision. This patientwas lost to follow-up 2 months after surgery. Anotherpatient ruptured a pseudoaneurysm that developed on theopposite cavernous ICA after a transfacial approach. Theepistaxis was tamponaded and a contralateral cervicalICA-MCA saphenous-vein bypass excluded the injuredsegment of ICA from the circulation. Although this pa-tient suffered a cerebral infarction, he functions indepen-dently and showed only moderate disabilities at his 2-yearfollow-up examination. His current GOS is at his pre-operative level.

One additional complication occurred without neu-rologic sequelae in a patient with a cerebrospinal fluidleak that resolved after placement of a lumboperitonealshunt. Overall, all except the patient described in theprevious paragraph (with only 2-months follow-up) re-turned to their preoperative neurologic status as deter-mined by GOS. Currently, two patients are alive, threepatients are dead, and five patients have been lost tofollow-up (mean duration, 1.7 years). None of the surviv-ing patients have symptoms or radiographic evidence oflocal recurrence. The additional death was caused bypneumonia 7 months after surgical resection of a squa-mous carcinoma.

DISCUSSION

This small experience with carotid sacrifice for radi-cal resection of skull base tumors reflects our practice ofpreserving the ICA whenever possible. Our protocol formanaging these lesions is derived from a review of theliterature and relates to the benignancy or malignancy ofthe tumor. We preserve the ICA with benign tumors be-cause they do not invade the artery, or they invade it to alimited extent. In contrast, we recommend radical tumorresection and sacrifice of the ICA with malignant tumorsbecause they directly threaten the integrity of the ICAand, thus, the patient's survival. The ICA should not beconsidered a limitation to radical tumor resection becauseit can be safely reconstructed with an appropriate bypassprocedure.

Benign Skull Base Tumors

The majority of anterior skull base neoplasms-.meningioma, nerve sheath tumors, pituitary adenoma,

INTERNAL CAROTID ARTERY SACRIFICE-LAWTON, SPETZLER

and juvenile angiofibroma-are benign.7 Many of thesetumors can be resected completely without sacrifice of theICA. DeMonte et al2 preserved the ICA in all 41 patientswith cavernous sinus meningiomas and achieved totalresection in 31 patients (76%). In his review of clinoidalmeningiomas, Al-Meftyl concluded that the presence ofan arachnoid membrane between the ICA and the tumordetermines whether dissection of the vessel from thetumor is possible; complete ICA encasement by the tumordoes not prevent total resection. However, this arachnoidlayer is absent in extradural or interdural spaces such asthe cavernous sinus, and it is also absent in patients whohave undergone previous operations or irradiation. Me-ningiomas that encase the ICA without this interveningarachnoidal layer adhere to the adventitia and cannot beresected completely without sacrificing the ICA. The76% total resection rate in DeMonte's series demonstratesthat a protective arachnoidal membrane is often presentaround meningiomas; therefore, the majority of thesebenign tumors can be resected completely while preserv-ing the ICA. Other benign tumors, such as pituitary ade-nomas, neurilemomas, and angiofibromas, are more likelythan meningiomas to be dissected free of the ICA.4

Residual benign tumor left around the ICA to pre-serve it could potentially invade the vessel wall and com-promise the integrity of the artery. However, benign tu-mors tend not to invade the ICA to such an extent.Kotapka et aP3 studied ICAs encased by cavernous sinusmeningiomas in 19 patients. Luminal narrowing was pre-sent in all but two. Eight of these patients' ICAs wereinfiltrated by tumors-to the outer adventitia in five pa-tients and to the media through adventitia in three pa-tients. Apparently, meningiomas invade the carotid wall,but only to a limited extent. Therefore, residual tumor onthe ICA after resection does not threaten the integrity ofthe vessel. Tumor debulking is often sufficient to restorelumenal patency.

Residual benign tumor around the ICA could poten-tially increase the incidence of tumor recurrence. Becausethe risk of tumor recurrence decreases with more exten-sive surgical resection,11 the recurrence rate should belower in patients whose carotid arteries are sacrificed thanin patients whose carotid arteries are preserved. However,two representative series of patients with cavernous sinusmeningiomas that were aggressively resected, eitherwith8 or without ICA resection,2 had recurrence rates thatwere strikingly similar. Sen and Sekhar8 treated 17 pa-tients with tumor and ICA resection, totally resecting thetumors of 76% of the patients. The symptomatic andradiographic recurrence rate was 8% after total tumorresection and 25% after subtotal tumor resection. In com-parison, DeMonte et a12 achieved the same gross totalresection rate in 41 patients without carotid resection. Inthis series, the rates of recurrence were 3% and 20% aftertotal and subtotal resections, respectively. Therefore, ICAresection in the treatment of meningiomas of the anterior

The lack of ICA invasion by residual tumor and thelack of improvement in the tumor recurrence rate withcarotid resection argue for preserving the ICA when deal-ing with benign skull base tumors. ICA preservation is thepractice at our institution. Furthermore, the risk of com-plication from elective ICA occlusion is 7% to 10% in ourexperience, even with revascularization.12 This risk can-not be justified in the treatment of benign lesions. Al-though total resection is the goal of this surgery, subtotalresection of a benign tumor is considered safe. Nonethe-less, patients with residual tumor are followed carefullyfor recurrence with serial neurologic and imaging exam-inations.

An exception to this protocol is a benign tumor thatcompletely occludes the ICA. One such patient in thisseries had a meningioma that completely occluded theICA and caused transient ischemic attacks. CompleteICA occlusion permits resection of the artery with thetumor, but the ischemic symptoms indicate that cere-brovascular reserve may be inadequate and necessitate abypass graft.

Malignant Skull Base Tumors

An ICA surrounded by a malignant tumor is man-aged differently from one surrounded by a benign tumor.First, because malignant tumors can invade adjacentstructures, metastasize, and cause death, oncological prin-ciples of radical resection with tumor-free margins mustbe followed more strictly. Second, the risks of ICA sacri-fice are justified when compared to the dismal prognosisof patients with malignant neoplasms.

Our treatment strategy is based on the invasive be-havior of malignant tumors. Unlike malignant neoplasmswhich tend to invade the ICA wall directly and can lead tofrank ICA rupture,13-16 benign neoplasms tend to invadethe ICA superficially and do not precipitate rupture. Be-cause ICA rupture can cause potentially life-threateninghemorrhage, an artery involved with a malignant tumor isbest resected. The risk of an ICA rupture invaded bymalignant intracranial tumor is unknown. However, it islikely to be similar to the risk of rupture of an ICAinvaded by malignant cervical tumor-which is around18%.13,14,17 Furthermore, most of these ICAs rupturewithin 6 months.13'14 Therefore, when dealing with malig-nant neoplasms, the risk of ICA preservation and subse-quent rupture exceeds the risk of ICA sacrifice with re-vascularization.

The effect of ICA resection on tumor recurrence andthe survival of patients is difficult to determine becauseno prospective, randomized studies have analyzed thisissue. Malignant tumors are more difficult to resect thanbenign tumors, with total resection rates of55% and 86%,respectively.7 Recurrence after total resection is also in-creased with malignant tumors (25% vs 6%). ICA sacri-fice permits en bloc resection of the cavernous sinus and, 121skull base does not appear to lower the rate of recuffence.

SKULL BASE SURGERYNOLUME 6, NUMBER 2 APRIL 1996

therefore, a better chance at disease-free margins of resec-tion.18 However, it is unclear whether aggressive resec-tion extends a patient's survival significantly.'9 At theleast, radical tumor resection should attempt to relievelocal symptoms and to decrease the rate of intracranialrecurrence.

Reconstruction of the ICA

ICA resection produces a risk of ischemic complica-tions. Morbidity from elective ICA resection without re-construction for neck carcinomas ranges from 0% to 45%,and mortality ranges from 0% to 31%.20 Consequently,the surgeon must determine that the patient has either thecollateral circulation to tolerate ICA sacrifice, or the sur-geon must restore cerebral blood flow with a bypass graft.Diagnostic studies such as the balloon occlusion test withxenon computed tomographic-cerebral blood flow (XeCT-CBF) identify patients who are unlikely to tolerateICA sacrifice and who will require revascularization.5'6'8These provocative tests may cause temporary or perma-nent ischemic deficits ranging from 0.7% to 7%,21,22 andtheir false negative rates range from 2% to 22%.8,22-24 Inaddition, such tests do not predict the risk of delayedischemic complications or de novo aneurysm formation.Therefore, there is considerable cumulative risk from aballoon occlusion test, immediate ischemic complica-tions, delayed ischemic complications, and de novo aneu-rysm formation. We tend to revascularize patients whoseICA has been sacrificed because this approach has asurgical morbidity rate between 7% and 10% and a smalldelayed stroke risk from symptomatic graft failure.12 Theindications for revascularization remain controversial.

The revascularization procedure is performed imme-diately before the tumor is resected or in a precedingsurgical stage. Intraoperative somatosensory evoked po-tentials (SSEPs) are used routinely during the anastomo-sis. Changes in SSEPs alert the surgeon that the patient isnot tolerating the temporary ICA occlusion, and ICAperfusion should be maintained during proximal anasto-mosis by suturing the bypass graft to the external carotidartery.

Vascular complications occurred in 20% of the pa-tients in this series, a value similar to the stroke ratefollowing ICA occlusion.22 Although this similarity mightsuggest that the bypass provided no benefit, the bypassesin these two patients likely protected them from devastat-ing complications. The one patient who developed aninfarction after occlusion of the graft was dependent on itand would not have tolerated ICA sacrifice without it. Theother patient who developed an infarction after pseu-doaneurysm rupture would probably have developed bi-lateral infarctions from bilateral carotid occlusions anddied had it not been for the revascularization performedprior to tumor resection. Instead, he returned to his pre-operative level of function. The ischemic complications

in these patients would have been more devastating with-out revascularization, and revascularization contributedto the recovery in the second patient.

Limitations of the Current Study

The protocol at this institution for managing tumorsthat encase the ICA favors conservation rather than sacri-fice of the vessel. This series of patients is therefore small,and unfortunately does not lend itself to statisticallymeaningful conclusions about the efficacy of treatment.

The impact of ICA sacrifice on local recurrence andpatient survival is a difficult and controversial topic. Thisstudy is retrospective and did not include a control groupof patients with malignant tumors resected without ICAsacrifice for comparison. Furthermore, follow-up is lim-ited. A randomized, prospective study would generaterecurrence rates and survival data for patients whose tu-mors were resected with and without ICA sacrifice. Thatonly 10 patients underwent ICA sacrifice at this institutionin 6 years indicates that a multicenter study would berequired to obtain enough patients for a robust statisticalanalysis. The current study does not resolve this contro-versial issue, but it does present an approach to treatmentand results, as well as justification based on a review ofthe literature.

Regarding the literature review, the analysis reliedheavily on several articles.2,3'68 Unfortunately, few arti-cles provide data relevant to this issue. Many authorsdiscuss recurrence rates and survival after tumor resec-tion,11'25-28 but these studies include tumors in diverselocations that do not relate to the carotid artery. The verylimitations of this study emphasize the need for furtherinvestigations or for a prospective, randomized trial toprovide definitive answers to whether the ICA should bepreserved or sacrificed in patients with tumors.

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