Skull base resection with cervical-to-petrous carotid artery bypass to facilitate repair of distal internal carotid artery lesions

PII: S0967-2109(01)00109-0

Cardiovascular Surgery, Vol. 10, No. 1, pp. 31–37, 2002  2002 The International Society for Cardiovascular Surgery Published by Elsevier Science Ltd. All rights reserved 0967-2109/02 $22.00

www.elsevier.com/locate/cardiosur

Skull base resection with cervical-to-petrous carotid artery bypass to facilitate repair of distal internal carotid artery lesions Jonathan L. Eliason, James L. Netterville, Raul J. Guzman, Marc A. Passman and Thomas C. Naslund Division of Vascular Surgery and the Department of Otolaryngology, Vanderbilt University Medical Center, 1161 22nd Avenue South, Nashville, TN 37232, USA Purpose: To demonstrate a direct operative approach to vascular lesions of the internal carotid artery (ICA) at the level of the skull base. Methods: Between January 1993 and October 1999, five patients underwent lateral skull base resection with cervical-to-petrous carotid artery saphenous vein bypass for repair of distal ICA lesions. This report describes operative methods, morbidity, graft patency, and long-term outcome with this experience. Results: Of the five patients with skull base ICA lesions, all had aneurysmal disease. Three were atherosclerotic and two were dysplastic. Preoperative neurologic symptoms including transient ischemic attacks (2) and Horner’s syndrome with vascular headaches (1) were completely resolved after operation. Preoperative dysphagia (2) was resolved in one patient and clinically improved in the other. Postoperative complications included transient paresis in the cranial nerve (CN) VII distribution, as well as permanent loss of the eustachian tube and chorda tympani nerve in all five patients. One patient had lasting paresis in the CN XI distribution as well as a mild stroke resulting in arm weakness. No residual arm weakness was detected at one year. There were no graft occlusions by duplex ultrasound at 45.8 months mean objective follow-up, and no ipsilateral stroke or mortality at 51.2 months mean clinical follow-up. Conclusions: Saphenous vein bypass from the cervical-to-petrous ICA is technically feasible and provides a valuable reconstruction option for patients with skull base ICA lesions.  2002 The International Society for Cardiovascular Surgery. Published by Elsevier Science Ltd. All rights reserved Keywords: carotid artery, aneurysm, skull base, bypass, petrous

Introduction The boundaries of what internal carotid artery lesion is “too high” to be surgically accessible have been changing. Historically, lesions in the portion of the artery above the level of a line drawn between the angle of the mandible and the tip of the mastoid pro-

Correspondence to: Thomas C. Naslund, M.D. Tel.: +1-615-3222343; Fax: +1-615-343-4251; e-mail: [email protected]

CARDIOVASCULAR SURGERY

FEBRUARY 2002 VOL 10 NO 1

cess (Blaisdell line) had been considered inaccessible by standard surgical techniques [1]. Since that time many maneuvers have been employed to allow exposure of the more distal portions of the extracranial ICA using a cervical approach. Division of the digastric muscle, mandibular manipulations such as anterior translational movement, subluxation or lateral mandibulotomy, division of the styloid processassociated musculature or resection of the styloid process itself have all been used toward this end. Despite these techniques, visualizing ICA of satisfactory quality to accomplish repair can be trouble31

Skull base resection: J. L. Eliason et al.

some, even after the use of endoluminal vascular control. A cadaver study has demonstrated that the last centimeter of the ICA before it enters the carotid canal cannot be reached without resection of the mastoid process at the skull base [2]. Surgical exposures of the skull base traditionally used in the resection of head and neck tumors can provide access to the ICA at this level. The purpose of this article is to demonstrate the use of skull base resection in the treatment of isolated vascular lesions at the base of the skull.

Patients and methods Between January 1993 and October 1999, five patients with symptomatic lesions of the distal extracranial ICA were treated with bypass using reversed saphenous vein graft (RSVG) from the cervical-topetrous ICA after skull base resection. The operative team consisted of a vascular surgeon and an otolaryngologist with expertise in skull base exposures. A summary of the five cases is shown in Table 1, and the case reports are outlined below. Case 1: A 53-yr-old male with Von Recklinghausen’s neurofibromatosis and a remote history of rhabdomyosarcoma of the right thigh presented with six weeks of progressive dysphagia and weight loss. Head and neck exam revealed a bulging mass in the left oropharynx, paralyzed left vocal cord and palate asymmetry. The possibility of a tumor recurrence was considered. However, a CT scan with IV contrast revealed a 4.5 cm ICA aneurysm extending to the base of the skull (Figure 1). Arteriogram confirmed a large ICAA with invasion of the skull base (Figure 2). Due to the patient’s extremely debilitated state, a feeding tube was placed and six weeks of enteral nutrition was given prior to his operative repair. At operation, the aneurysm was not resected due to its size and adherence to adjacent structures. After skull base exposure, a cervical-to-petrous Table 1

Figure 1 Head CT. Arrows demarcate skull base ICA aneurysm

carotid artery bypass using RSVG was performed. Cultures of the aneurysm wall showed no growth. The patient had an uneventful recovery. Although his swallowing is improved, he continues to have mild aspiration. He has had medialization of his true vocal cord and recently underwent palatal adhesion to further improve his swallowing function. Case 2: A 51-yr-old male had a six-month history of severe right retro-orbital and temporal headaches. His initial medical treatment for cluster headaches did not relieve his symptoms, and he subsequently developed a right-sided Horner’s syndrome. A head

Summary of casesa

Patient

Age

Sex

Sign/symptom

Type of lesion

Surgical treatment

Outcome

1.

53

M

Nonspecific aneurysm

2.

51

M

Dysphagia, vocal cord paralysis Horner’s Syndrome

Nonspecific aneurysm

Skull base resection and RSVG bypass Skull base resection and RSVG bypass

3.

68

F

TIA

Nonspecific aneurysm

4.

80

F

Dysphagia, neck mass

Dysplastic aneurysm

5.

66

F

Amaurosis fugax

Dysplastic aneurysm with stenosis and coil

Vocal cord paralysis*, deficit CN IX* Mild CVA, deficit CN XI, required myringotomy tube No permanent CN deficit No permanent CN deficit, required myringotomy tube No permanent CN deficit

Skull base resection and RSVG bypass Skull base resection and RSVG bypass Skull base resection and RSVG bypass

a TIA, transient ischemic attack; FMD, fibromuscular dysplasia; RSVG, reversed saphenous vein graft; CN, cranial nerve. *Deficit was present pre-operatively

32

CARDIOVASCULAR SURGERY

FEBRUARY 2002 VOL 10 NO 1

Skull base resection: J. L. Eliason et al.

Figure 2 (A) Left carotid arteriogram showing ICA aneurysm. (B) Magnified view of left ICA aneurysm

CT was obtained which revealed an aneurysm of the distal right ICA. Arteriography helped characterize a 3 cm ICAA abutting the skull base (Figure 3). The patient underwent a skull base resection and bypass of his carotid artery aneurysm using vein graft. Post-

Figure 3 Right carotid arteriogram showing ICA aneurysm

CARDIOVASCULAR SURGERY

FEBRUARY 2002 VOL 10 NO 1

operatively he was noted to have left upper extremity weakness as well as weakness in the CN XI distribution on the right. A right parietal infarct was demonstrated on CT scan. The patient was anticoagulated with coumadin and spent several weeks in a rehabilitation facility. He made a rapid recovery and six months later was back at work as a truck driver. At his one year follow-up there was no residual left arm weakness. His CN XI deficit was permanent. Case 3: A 68-yr-old female with recurrent transient right arm weakness and numbness was evaluated by arteriography and shown to have a 75% stenosis at the origin of the left ICA and an aneurysm just proximal to the artery’s entrance into the skull base. She was treated with aneurysm resection and RSVG bypass to the petrous carotid artery following skull base resection. The patient has done well in her 5yr follow-up. Case 4: An 80-yr-old female had episodic difficulty swallowing solid food and a high right-sided neck mass. Her evaluation included a head CT and arteriogram. These revealed a large right-sided ICAA with its distal margin extending to the skull base. Although initially it was felt that adequate exposure could be obtained through an extended cervical incision, inadequate visualization of the distal neck of the aneurysm led to a lateral skull base resection with bypass to the petrous portion of the ICA. Postoperatively the patient required myringotomy tube placement for serous otitis media. She also had temporary dysfunction CN IX resulting in palate asymmetry that resolved in six months. Case 5: A 66-yr-old female had three episodes of right sided amaurosis fugax within 48 h. Arteriogram showed a complex lesion of the high cervical ICA with a 95% right ICA stenosis at the level of the styloid process and an associated 360° coil. There was also aneurysmal change consistent with fibromuscular dysplasia (FMD) at the skull base. In order to expose normal artery distal to the FMD and coil, the patient underwent skull base resection with exposure of the petrous ICA followed by cervical-topetrous ICA bypass using RSVG. She had no neurologic deficits at 5-yr follow-up. Operative technique: The patient is positioned supine with the head turned contralateral to the operative site and the neck extended. Pre-incision marks are placed on the skin to outline the potential incision for a skull base resection if required. Cervical exposure is accomplished first using a curvilinear incision within a skin crease extending up to the posterior aspect of the earlobe. The jugular vein, ICA and CNs X–XII are all isolated. The posterior belly of the digastric muscle is then resected along with level II jugular nodes to widen exposure in this portion of the neck. CN IX is identified and preserved if possible. Excision of the stylohyoid and stylopharyngeus muscles is performed with resection of 33

Skull base resection: J. L. Eliason et al.

the styloid process. The ICA can now be exposed up to the skull base. If the pathology of the ICA can then be managed within the confines of the neck, vascular repair is undertaken. If more distal exposure of the ICA is required, the incision is extended for exposure of the lateral skull base. The cervical incision is brought around the earlobe, anterior to the ear, up into the temporal region and forward to the hairline (Figure 4). A temporal flap is then developed and the zygomatic arch is identified. The deep temporal fascia is incised to preserve the temporal branch of CN VII. The remainder of CN VII is left intact with its surrounding soft tissues in place. The articular surface of the temporo-mandibular joint is bluntly mobilized forward out of its fossa and a self-retaining retractor is used to provide anterior traction on the mandible allowing exposure of the glenoid fossa. The operative microscope allows medial and slight posterior resection of the glenoid to expose the first vertical portion of the petrous ICA. The second portion of the intrapetrous ICA is horizontal and can also be fully mobilized (Figure 5). If the entire petrous carotid artery is exposed, the skull base resection is extended to the dura. The chorda tympany nerve and eustachian tube are divided as the artery is drilled free. Once the ICA is fully mobilized, there is easy communication between the lateral skull base resection and the cervical exposure below.

Figure 4 Incision for lateral skull base resection for petrous carotid exposure

34

Figure 5 Exposure after temporal flap has been raised and mandible retracted anteriorly

Reversed saphenous vein graft harvested from the groin is used for bypass. Following systemic heparinization, the graft is anastomosed to the origin of the ICA with spatulation onto the common carotid artery (Figure 6). If the distal anastomosis is made to the proximal vertical portion of the petrous ICA, it may be feasible to accomplish through the cervical

Figure 6 Skull base resection complete and reversed saphenous vein graft (RSVG) repair completed

CARDIOVASCULAR SURGERY

FEBRUARY 2002 VOL 10 NO 1

Skull base resection: J. L. Eliason et al.

incision using inferior distraction of the artery. When the horizontal portion of the petrous ICA is used, the anastomosis is conducted through the small opening in the lateral skull base (Figure 7). No shunt is utilized during the carotid reconstruction and interrupted sutures are preferred for the distal anastomosis. Cephalic hypertension is maintained while the artery is occluded. Completion arteriography is used to demonstrate the distal anastomosis. If a hemodynamically significant lesion is identified, repair can be accomplished at the time of the original operation. Post-operative observation is accomplished in the intensive care unit. With a high risk for hematoma formation, closed-suction drains are routinely used in the cervical as well as temporal portions of the incision.

Results The mean age at operation was 63.2 yr (range 51– 80 yr). All patients had aneurysmal changes. Three of the ICAAs were nonspecific “atherosclerotic” and two were dysplastic as defined by the suggested standards for reporting on arterial aneurysms [3]. One patient also had a critical stenosis secondary to fibromuscular dysplasia (FMD). The mean operative time was 7.2 h (range 3.6–9.1) with an average ICU and hospital length of stay of 2.2 days (range 1–3) and 5.6 days (range 4–7), respectively. Preoperative neurologic symptoms including transient ischemic attack (2) and Horner’s syndrome with vascular headaches (1) were completely resolved after operation. Preoperative dysphagia (2) was resolved in one patient and clinically improved in the other. Post-

operative complications included clinically evident paresis in the distributions of CN VII (5), IX (3), X (1) and XI (2). Two of the deficits (vocal cord paralysis from CN X involvement and palate asymmetry from CN IX) had been present pre-operatively. Of the deficits that occurred as a result of the operation, all but CN XI from case 2 were transient, lasting between 3 and 12 months. Each patient also had permanent loss of the eustachian tube resulting in a mild conductive hearing loss and two patients required myringotomy tube placement for serous otitis. Loss of the chorda tympani nerve caused subjective alteration in taste for one patient. One patient had a minor intraoperative stroke resulting in arm weakness and seizures. There was no residual deficit at one year and seizures did not occur outside of the perioperative period. All patients were followed with duplex ultrasonography of the carotid arteries with a mean objective follow-up of 45.8 months (range 6–65). No graft occlusions or significant stenosis were noted. No ipsilateral strokes occurred within a mean clinical follow-up of 51.2 months (range 8–87). There were no perioperative or late mortalities.

Discussion The management of ICA lesions at the base of the skull is controversial. Safe and effective treatment strategies have been difficult to attain. Options available for lesions too high to reach through a cervical approach include non-operative treatment, carotid ligation, EC–IC bypass followed by ICA occlusion, endovascular treatment or direct operative repair. Many feel the morbidity of surgical exposure and the

Figure 7 (A) Magnified view of petrous ICA exposure. (B) Operative exposure with cervical-to-petrous carotid artery bypass using RSVG. Arrow identification: *→ denotes distal anastomosis; †→ denotes saphenous vein graft; ‡→ denotes CN VII within surrounding soft tissue

CARDIOVASCULAR SURGERY

FEBRUARY 2002 VOL 10 NO 1

35

Skull base resection: J. L. Eliason et al.

time required for direct repair of this arterial segment is not warranted. Those that favor a direct operative approach feel that the morbidity of the operation is outweighed by the durability of the repair and the reduced risk of neurological sequelae. We feel that our results support the use of skull base resection combined with vein graft reconstruction for the treatment of these lesions. Non-operative management and carotid ligation are undesirable treatment options for distal extracranial ICA lesions due to their high risk of stroke. Carotid ligation has been shown to carry a 24% incidence of ischemic complications when used in the treatment of arterial aneurysms filling from the carotid artery [4]. EC–IC bypass followed by carotid occlusion came about in an attempt to lower this stroke risk. This technique may have utility for certain intracranial ICA lesions. It is now typically performed using endovascular carotid occlusion [5]. Its application to ICA lesions at the skull base seems inferior to a direct approach, however. The effectiveness of EC–IC bypass in reducing risk of ischemic stroke is not well demonstrated [6]. In addition, this technique does not definitively exclude a thromboembolic event from the occluded artery [7]. Endoluminal solutions provide another treatment option. Their roles in these situations are still in the early stages of being defined. Successful balloon angioplasty and stenting of stenotic ICA lesions at the base of the skull or within the petrous carotid artery have been reported [8]. We have performed two such procedures without complication (unreported). However, no intermediate or longterm follow-up in significant numbers has been published to define the safety and utility of these types of interventions. Arterial dissection, stent fracture, intimal hyperplasia at transition zones, and air embolism during deployment of endovascular grafts/covered stents are all potential risks associated with these techniques. As stents become lower profile and their flexibility improves, the risks of dissection and stent fracture from motion in multiple planes may be reduced. However, the virtual inoperability of such lesions after endovascular treatment, or in case of failure of the endovascular procedure, would suggest that cautious evaluation is needed prior to considering an endoluminal solution. One report of endovascular exclusion of an ICA aneurysm with stroke and early endograft occlusion highlights the risk of thromboembolic complications that can occur with these techniques [9]. For direct operative exposure of the ICA at the skull base there are several options. The majority of these have been used when arterial reconstruction is required in association with tumor resection. Fisch et al. described a posterior approach with radical mastoidectomy and obliteration of the middle ear 36

[10]. Glasscock et al. reported using an anterior infratemporal fossa approach to the intrapetrous ICA [11]. Other reports of using vein graft bypasses from the cervical-to-petrous carotid artery then followed [12, 13]. Some used a subcutaneously tunneled graft in combination with a cervical incision and a temporal craniotomy for exposure of the petrous ICA [14, 15]. Candon et al. used a similar technique, but tunneled the vein graft within the intact ICA [16, 17]. A recent report by Rosset et al. outlined the use of the first vertical portion of the intrapetrous ICA as the distal target for bypass in the treatment of 10 patients with skull base ICAAs [18]. Although the petrous ICA can be exposed in several ways, we favor an anterior approach with infratemporal fossa and lateral skull base exposure. This prevents the profound conductive hearing loss associated with a posterior approach. There is also no need for a craniotomy. Drilling free both the vertical and horizontal portions of the petrous carotid artery allows the removal of bone around 270° of the artery. This allows excellent mobility of the artery for bypass [19]. Cervical-to-petrous ICA bypass provides definitive exclusion of emboli from the lesion and the anterior cerebral circulation is restored through a high flow conduit. Patients with vascular lesions extending into the skull base can still be considered candidates for direct arterial reconstruction with this approach. Graft patency in this small group of patients appears to be excellent. The morbidity from this type of skull base resection results primarily from cranial nerve dysfunction. Patients with ICAAs not high enough to require special techniques for exposure of the skull base are reported to have a 20–23% incidence of transient cranial nerve dysfunction postoperatively [20, 21]. With an infratemporal fossa and lateral skull base exposure, all patients have temporary paresis of the facial nerve. Other cranial nerve deficits can also occur, but permanent cranial nerve injuries are uncommon. Other morbidities with this approach are eustachian tube dysfunction and loss of the chorda tympany nerve. The serous otitis that develops with the obliteration of the eustachian tube can be treated with the placement of a myringotomy tube if significant symptoms develop. Only two of our five patients felt the mild conductive hearing loss associated with serous otitis warranted tube placement. Only one felt the alteration in taste from loss of the chorda tympany nerve was significant. Vascular surgeons will rarely encounter ICA lesions requiring skull base resections in practice. If this type of approach is needed, a surgeon with substantial experience in exposing the base of the skull is required. Therefore a team approach and the ability to work closely with such an expert is necessary. In spite of the additional expertise in the operating room, these reconstructions remain subCARDIOVASCULAR SURGERY

FEBRUARY 2002 VOL 10 NO 1

Skull base resection: J. L. Eliason et al.

stantially challenging, yet gratifying in their longterm outcome. Although rarely necessary, we find the direct approach to the petrous carotid a useful and mandatory component of the armamentarium in the management of patients with large ICAAs or other symptomatic carotid artery lesions at the base of the skull. As expertise in skull base exposure continues to populate major medical centers, wider use of this technique is anticipated.

References 1. Blaisdell, W. F., Clauss, R. H., Galbraith, J. G. et al., Joint study of extracranial arterial occlusion. Journal of the American Medical Association, 1969, 209, 1889–1895. 2. Mock, C. N., Lilly, M. P., McRae, R. G. et al., Selection of the approach to the distal internal carotid artery from the second cervical vertebra to the base of the skull. Journal of Vascular Surgery, 1991, 13, 846–853. 3. Johnston, K. W., Rutherford, R. B., Tilson, M. D. et al., Suggested standards for reporting on arterial aneurysms. Journal of Vascular Surgery, 1991, 13, 452–458. 4. Landolt, A. M. and Millikan, C. H., Pathogenesis of cerebral infarction secondary to mechanical carotid artery occlusion. Stroke, 1970, 1, 52–62. 5. Hacein-Bey, L., Connolly, E. S. Jr., Doung, H. et al., Treatment of inoperable carotid aneurysms with endovascular carotid occlusion after extracranial–intracranial bypass surgery. Neurosurgery, 1997, 41, 1225–1234. 6. The EC/IC Bypass Study Group, Failure of extracranial–intracranial arterial bypass to reduce the risk of ischemic stroke. New England Journal of Medicine, 1985, 313, 1191–1200. 7. Heros, R. C., Thromboembolic complications after combined internal carotid ligation and extra-t-intracranial bypass. Surgical Neurology, 1984, 21, 75–79. 8. Mencken, G. S., Wholey, M. H. and Eles, G. R., Use of coronary artery stents in the treatment of internal carotid artery stenosis at the base of the skull. Catheterization and Cardiovascular Diagnosis, 1998, 45, 434–438. 9. May, J., White, G. H., Waugh, R. et al., Endoluminal repair of internal carotid artery aneurysm: a feasible but hazardous procedure. Journal of Vascular Surgery, 1997, 26, 1055–1060.

CARDIOVASCULAR SURGERY

FEBRUARY 2002 VOL 10 NO 1

10. Fisch, U. P., Oldring, D. J. and Senning, A., Surgical therapy of internal carotid artery lesions of the skull base and temporal bone. Otolaryngology Head and Neck Surgery, 1980, 88, 548–554. 11. Glasscock, M. E., Smith III, P. G., Whitaker, S. R. et al., Management of aneurysms of the petrous portion of the internal carotid artery by resection and primary anastomosis. Laryngoscope, 1983, 93, 1445–1453. 12. Sekhar, L. N., Schramm, V. L. Jr., Jones, N. F. et al., Operative exposure and management of the petrous and upper cervical internal carotid artery. Neurosurgery, 1986, 19, 967–982. 13. Miyazaki, S., Fukushima, T. and Fujimaki, T., Resection of high-cervical paraganglioma with cervical-to-petrous internal carotid artery saphenous vein bypass. Journal of Neurosurgery, 1990, 73, 141–146. 14. Fitzpatrick, B. C., Spetzler, R. F., Ballard, J. L. et al., Cervicalto-petrous internal carotid artery bypass procedure. Journal of Neurosurgery, 1993, 79, 138–141. 15. Newell, D. W., Grady, S. M. and Nichols, S. C., Cervical carotid to petrous carotid bypass for lesions of the upper cervical carotid artery. Annals of Vascular Surgery, 1996, 10, 76–87. 16. Candon, E., Mart-Ane, C., Pieuchot, P. et al., Cervical-to-petrous internal carotid artery saphenous vein in situ bypass for the treatment of high cervical dissecting aneurysm: technical case report. Neurosurgery, 1996, 39, 863–866. 17. Candon, E., Canovas, J., Kabbaj, J. et al., Anatomic basis for the treatment of aneurysms of the upper cervical segment of the internal carotid artery by extra-intracranial cervico-petrous bypass with inverted “in situ” saphenous vein graft. Surgical and Radiologic Anatomy, 1998, 19, 1–6. 18. Rosset, E., Albertini, J., Magnan, P. E. et al., Surgical treatment of extracranial internal carotid artery aneurysms. Journal of Vascular Surgery, 2000, 31, 713–723. 19. Dew, L. A., Shelton, C., Harnsberger, H. R. et al., Surgical exposure of the petrous internal carotid artery: practical application for skull base surgery. Laryngoscope, 1997, 107, 967–976. 20. Moreau, P., Albat, B. and The´ venet, A., Surgical treatment of extracranial internal carotid artery aneurysm. Annals of Vascular Surgery, 1994, 8, 409–416. 21. Faggioli, G., Freyrie, A., Stella, A. et al., Extracranial internal carotid artery aneurysms: results of a surgical series with longterm folow-up. Journal of Vascular Surgery, 1996, 23, 587–595. Paper accepted 17 May 2001

37