Updated: Mar 5, 2009
Malignant invasion of the carotid artery presents the head and neck oncologist with both diagnostic and therapeutic challenges. When resection of the carotid artery as part of a cancer surgery is considered, preoperative evaluation can identify which patients are at greatest risk of neurologic sequelae, and carotid reconstruction must be considered whenever possible to decrease the risk of such complications.1 Unfortunately, even with reconstruction, patients still bear some risk of immediate and delayed neurologic sequelae from the procedure. Furthermore, long-term survival is generally poor in cases of malignant carotid involvement, even when the surgical resection of the carotid proceeds uneventfully.
In modern head and neck oncologic practice, high radiologic suspicion of carotid invasion is considered by some to be a contraindication to primary surgical therapy because of the risk of stroke with carotid resection.2 As a result, many individuals in whom carotid resection is considered have previously been treated with radiotherapy and have persistent or recurrent malignancy in an irradiated field.
Attempting surgical salvage in this population presents additional challenges. First, carotid invasion is more difficult to predict based on preoperative CT imaging or MRI in this population. Thus, the surgeon must entertain the possibility of invasion even in the absence of bulky disease or carotid encasement. At the same time, the radiographic or intraoperative appearance of carotid involvement can merely represent inflammatory changes and fibrosis in an irradiated field, mimicking invasion when none is present.
This unpredictability is highlighted by multiple pathologic series in which only a minority (37.5-42%) of resected carotid arteries are shown histologically to be invaded.3,4 Secondly, irradiated patients have arterial walls that are weakened because of adventitial fibrosis, destruction of the arterial elastic tissue, and accelerated atherosclerosis. Attempting to preserve such a carotid with subadventitial dissection can be unwise because occult tumor can easily be left behind. Furthermore, even if uninvolved with tumor, the arterial wall is easily further weakened by such dissection, resulting in either intraoperative rupture or high risk of postoperative rupture if wound complications prevent adequate protection of the vessel.
Carotid ligation/resection
Occasionally, benign tumors of the lateral skull base, such as glomus jugulare tumors and schwannomas, as well as various skull base malignancies, may necessitate planned carotid resection.5 However, carotid wall invasion most often arises either from direct extension of a primary head and neck squamous cell carcinoma of the pharynx or from bulky jugular chain lymph node metastasis with extracapsular extension. Although labeled "unresectable" by 2002 AJCC staging criteria, such individuals may be selectively considered for carotid resection as part of primary surgical therapy or a salvage attempt after prior radiotherapy and chemotherapy.
Some 2008 studies do advocate selective use of carotid resection as part of primary surgical therapy for head and neck carcinomas.6,7 These retrospective case series suggest better disease-free survival (20-30% range) from carotid resection than with nonsurgical therapy for previously untreated patients. This result is not surprising, as primary surgical resection remains the preferred mode of therapy, when deemed feasible, for the types of massive volume tumors that typically lead to carotid invasion. A further rationale for surgery in these untreated patients is that a high proportion of tumors suggested to invade the carotid wall radiographically can ultimately be removed without carotid resection.
Clinically, carotid invasion is suggested when a tumor that abuts the carotid sheath feels fixed or hypomobile, particularly in the vertical dimension. Radiographically, obliteration of tissue planes between the artery and the tumor on MRI suggests invasion but, as noted, can be deceiving in the postradiation salvage setting. Even in untreated patients, involvement of greater or less than 180° of the carotid circumference on CT scan is not significantly predictive of histologic invasion,8 with clinical assessment being of at least equal value. Only involvement of the artery 270o or more appears 100% predictive of the surgeon's inability to peel tumor off the artery.9 If elective surgery is contemplated and carotid invasion is deemed possible based on clinical and radiographic impression, further preoperative planning including angiography is necessary.
Occasionally, in cases of carotid rupture, emergent carotid resection may be needed without any preoperative testing. In this scenario, reconstruction is favorable whenever possible, although it may be impractical in a surgical field containing an uncontrolled fistula, which may have caused the rupture itself. Impending rupture is often signaled by minor sentinel bleeding, which can be controlled initially with conservative measures, allowing time for assessment with angiography and consideration of neuro-interventional versus open surgical approaches.
The 3 studies in the table below demonstrate the high morbidity and mortality associated with carotid ligation without reconstruction or preoperative testing. In the largest series, no difference was noted in complications associated with the reason for ligation, which included cancer infiltration, impending rupture, and acute rupture.10 The incidence of cerebral complications significantly decreased in patients whose common carotids were occluded gradually over 8 days or longer (5.3%), compared with patients with ligation for less than 7 days (30.6%) or those patients with abrupt ligation (42%).
Morbidity and Mortality Associated With Carotid Ligation Without Reconstruction or Preoperative Testing
| Study | Number of Patients | Number of Events | Temporary Ischemia | Permanent Cerebral Vascular Accident (CVA) | Deaths CNS | Total Deaths | Embolic Blindness |
| Maves et al 11 | 20 | 7 | 0 | 7 | 3 | 4 | 2 |
| Konno et al 10 | 156 | 53 | 6 | 47 | 24 | . . . | . . . |
| Razack and Sako 12 | 77 | 25 | 1 | 24 | 4 | . . . | . . . |
The physiology of carotid flow
Preoperative testing and perioperative management of hemodynamics after carotid resection are based on an understanding of cerebral blood flow (CBF) regulation. Under normal physiologic conditions, the average CBF is 50-55 mm/100 g/min, a range that is maintained by the autoregulation capacity of cerebral vasculature. However, in significant hypotension, autoregulation is lost and the CBF fluctuates with arterial blood pressure. Generally, CBF must decrease to 20-25 mL/100 g/min for brain dysfunction to occur. Management of systemic blood pressure can thus be critical for maintaining cerebral perfusion in individuals having undergone carotid resection, even in the absence of immediate posttreatment neurologic sequelae. Delayed onset symptoms and even a cerebral vascular accident (CVA) may develop in patients after carotid occlusion if systemic blood pressure drops.
The timing of permanent brain injury from ischemia has been well characterized in a primate model.13 Here, the neurologic symptoms that result from obstruction of the middle cerebral artery were partially reversible for up to 3 hours after occlusion. Microscopic infarcts were observed after 15-30 minutes and moderate-to-large infarction 2-3 hours later. After 3 hours, large permanent infarcts developed. With a regional CBF of less than 23 mL/100 g/min, reversible paralysis occurred. With a regional CBF of less than 10-12 mL/100 g/min for 2-3 hours or of less than 17-18 mL/100 g/min during permanent occlusion, the animals developed irreversible neurologic sequelae.
Stump pressure is an important concept for intraoperative decision making in managing cases of sudden rupture or unexpected carotid involvement.14 Brisk backflow from the distal carotid stump is a reflection of stump pressure, which is regarded as an indicator of adequate collateral blood flow when the carotid is occluded proximally. This value may even be measured intraoperatively with a strain gauge attached to a 19-gauge needle. Although stump pressures of more than 50-70 mm Hg are considered low risk, caution is still warranted because intraoperative electroencephalogram changes have been demonstrated at higher pressures.15
Contraindications to surgical management of the neck with carotid artery involvement are based on the patient's comorbidities and ability to tolerate surgery, as well as the technical feasibility of extirpating the tumor. Although few absolute contraindications exist, decision making is heavily influenced by the patient's overall functional status, the anticipated natural course of the tumor, consideration of nonsurgical options, and the patient's level of enthusiasm for surgery given the risk of severe neurologic sequelae or even death.
Preoperative carotid occlusion
Carotid reconstruction may not technically feasible in some patients, particularly individuals with the internal carotid artery involved close to the skull base. After normal trial balloon occlusion (TBO) and flow testing results, permanent balloon occlusion is a preoperative intervention that may reduce cerebral vascular accident (CVA) incidence over simple ligation in this clinical setting.21 The underlying principle is that high embolization of the carotid eliminates the standing column of blood present after ligation that is thought to serve as a later source of stump emboli. The method involves angiographic placement of permanent balloons or coils in the carotid siphon region proximal to the ophthalmic artery. Typically, the patient is heparinized, and hemodynamics are closely monitored for 72 hours.
Carotid resection is delayed by 2 weeks to allow for fixation of the coils and to avoid adverse hemodynamic effects from surgery during the vulnerable period immediately following occlusion. Additional advantages include avoiding the need for heparinization during a period of shunting prior to reconstruction, thus reducing intraoperative blood loss. In an early study of this technique, all 8 patients who underwent preoperative permanent balloon occlusion tolerated it without sequelae.22
However, the application of this technique has still been associated with neurologic complications with protracted intraoperative hypotension; in one case, migration of a balloon was also reported.2 A further disadvantage of this technique is that it must be applied preoperatively and may thus subject a patient to unnecessary risk if the carotid artery turns out to be uninvolved at the time of surgery.
Permanent balloon occlusion may also be performed without surgery to manage impending carotid rupture. In one series, 22 patients were treated by placing 2 permanent balloons just proximal to the ophthalmic artery and embolizing the internal carotid artery (ICA) down to the level of the carotid bifurcation with liquid biological adhesive (Histoacryl). None of the 22 patients had an immediate complication from the permanent occlusion, although 2 patients developed progressive hemiplegia that began 24 hours later.23
Surgical decision making
Although the type of preoperative scanning and precise technique used may vary, patients are generally placed into 3 categories based on trial balloon occlusion (TBO) and flow scanning results, as follows:
Moderate- and high-risk patients usually undergo reconstruction if carotid resection is performed. Although the best management of low-risk patients is less clear, these patients may also benefit from reconstruction whenever possible. A few patients in the low-risk category undergoing carotid ligation still experience neurologic sequelae, presumptively from inadequately sensitive flow scan workups, perioperative hypotension, or carotid stump emboli. This fact has led some authors to advocate vein graft reconstruction of the artery, when feasible.24,1,2
However, although unusual, these complications may still occur in the face of vein grafting, even in low-risk patients.25,26 Such events occur despite heparinization and placement of a temporary shunt to maintain cerebral perfusion during reconstruction, an essential step in moderate- and high-risk patients. A clot in the graft may be a potential source for an embolic CVA in some cases.
Other operative considerations include attention to the possibility of preserving the external carotid artery, which often requires resection in patients with head and neck cancer. Backflow from an intact external carotid can, in principle, both augment cerebral perfusion and prevent the development of stump emboli. Preservation of the external carotid is, not surprisingly, associated with an approximately 50% decrease in the CVA rate, as apparent from multiple reports.27,23,28,10
Lastly, whether or not to reconstruct the carotid must be decided in the larger context of the total resection and reconstruction to be performed. In previously irradiated patients, postoperative exposure of a carotid reconstruction from wound breakdown or contact with fistula drainage may risk lethal hemorrhage and instead bias one's management toward preoperative balloon occlusion. When reconstruction is performed, attention must be given to adequate protection of the carotid from pharyngeal secretions and coverage with well-vascularized tissue, using pedicled or free tissue transfer to accomplish these ends when necessary.
Neurologic complications
The early cerebral vascular accident (CVA) risk is well described and guides much of the perioperative evaluation and management efforts when carotid resection is considered. However, reports of long-term follow-up in patients with occluded carotid arteries demonstrate a delayed CVA rate as high as 25 times that of the general population. In a report of 814 cases of carotid occlusion performed for intracranial aneurysm, 233 patients developed ischemic symptoms after occlusion.27 Of these, 79% occurred within the first 48 hours and 10% occurred in the second 48 hours. However, 5 patients had ischemic symptoms at 6 months, 11 months, 12 months, 18 months, and 4 years, respectively. Late ischemic complications have also been confirmed in other reports.29
Nerve deficits
Resection of malignant disease that involves the carotid wall typically requires an en bloc resection of other adjacent involved structures, which often include the vagus nerve, the hypoglossal nerve, the spinal accessory nerve, and the cervical sympathetic chain. Particularly when compounded with other deficits, combined vagus and hypoglossal palsies may produce lasting postoperative dysphagia and aspiration, and patients must be apprised of the risks of such disabilities before surgery.
Long-term survival is generally poor in cases of malignant carotid involvement; early local recurrence is the norm, and rapid failure with distant metastatic disease is also common. Yet, no universal case against carotid resection can be made, and each patient merits careful consideration within his or her broad clinical context. In fact, recent data show significant numbers of long-term survivors among previously untreated patients undergoing carotid resection.6 These favorable surgical outcomes for very advanced tumors suggest that carotid resection does still have a limited role in the management of the head and neck cancer. Patients require extensive preoperative counseling and must contemplate surgery bearing in mind substantial risks, including those of devastating neurologic sequelae. This risk can be managed significantly by carotid reconstruction whenever possible, but adverse neurologic outcomes from carotid resection cannot be prevented altogether.
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Sanna M, Piazza P, Ditrapani G, Agarwal M. Management of the internal carotid artery in tumors of the lateral skull base: preoperative permanent balloon occlusion without reconstruction. Otol Neurotol. Nov 2004;25(6):998-1005. [Medline].
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Roh JL, Kim MR, Choi SH, et al. Can patients with head and neck cancers invading carotid artery gain survival benefit from surgery?. Acta Otolaryngol. 2008;128(12):1370-4. [Medline].
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Jones TH, Morawetz RB, Crowell RM, et al. Thresholds of focal cerebral ischemia in awake monkeys. J Neurosurg. Jun 1981;54(6):773-82. [Medline].
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Wright JG, Nicholson R, Schuller DE, Smead WL. Resection of the internal carotid artery and replacement with greater saphenous vein: a safe procedure for en bloc cancer resections with carotid involvement. J Vasc Surg. May 1996;23(5):775-80; discussion 781-2. [Medline].
management of the neck with carotid artery involvement, carotid artery, carotid involvement, malignant carotid invasion, malignant carotid involvement, carotid reconstruction, carotid artery reconstruction, carotid weakness, arterial wall weakness, arterial wall rupture, carotid artery rupture, carotid rupture, herald bleed, carotid ligation, sudden carotid rupture, carotid occlusion, CVA, cardiovascular accident, TBO, total balloon occlusion, xenon, Xe, carotid resection
Devraj Basu, MD, PhD, FACS, Assistant Professor, Department of Otorhinolaryngology-Head and Neck Surgery, University of Pennsylvania Health System
Devraj Basu, MD, PhD, FACS is a member of the following medical societies: American Academy of Otolaryngology-Head and Neck Surgery, American Association for Cancer Research, American College of Surgeons, and American Head and Neck Society
Disclosure: Nothing to disclose.
John M Truelson, MD, FACS, Chairman, Division of Head and Neck Surgery, Associate Professor, Department of Otorhinolaryngology, University of Texas Southwestern Medical Center at Dallas
John M Truelson, MD, FACS is a member of the following medical societies: American Academy of Otolaryngology-Head and Neck Surgery, American College of Surgeons, American Medical Association, American Society for Head and Neck Surgery, Phi Beta Kappa, and Texas Medical Association
Disclosure: Nothing to disclose.
Gregory S Weinstein, MD, FACS, Professor and Vice-Chairman, Department of Otorhinolaryngology-Head and Neck Surgery, Director of Division of Head and Neck Surgery, Director of Head and Oncology Fellowship, Director of Otorhinolaryngology-Head and Neck Clinic, Co-director of The Center for Head and Neck Surgery, University of Pennsylvania School of Medicine
Gregory S Weinstein, MD, FACS is a member of the following medical societies: American Academy of Otolaryngology-Head and Neck Surgery, American College of Surgeons, American Laryngological Association, American Laryngological Rhinological and Otological Society, American Medical Association, American Radium Society, American Society for Head and Neck Surgery, Pennsylvania Medical Society, Philadelphia County Medical Society, and Society of University Otolaryngologists-Head and Neck Surgeons
Disclosure: Nothing to disclose.
Richard V Smith, MD, Director of Clinical Affairs, Associate Professor, Department of Otolaryngology, Division of Head and Neck Surgery, Einstein College of Medicine, Montefiore Medical Center
Richard V Smith, MD is a member of the following medical societies: American Academy of Otolaryngology-Head and Neck Surgery, American College of Surgeons, American Head and Neck Society, American Laryngological Rhinological and Otological Society, American Medical Association, American Medical Student Association/Foundation, Medical Society of the District of Columbia, New York Academy of Medicine, and Vermont State Medical Society
Disclosure: Nothing to disclose.
Francisco Talavera, PharmD, PhD, Senior Pharmacy Editor, eMedicine
Disclosure: eMedicine Salary Employment
Nader Sadeghi, MD, FRCS(C), Associate Professor of Surgery, Director of Head and Neck Surgery, Division of Otolaryngology, George Washington University
Nader Sadeghi, MD, FRCS(C) is a member of the following medical societies: American Academy of Otolaryngology-Head and Neck Surgery, American Head and Neck Society, Federation of Medical Specialists in Quebec, and Royal College of Physicians and Surgeons of Canada
Disclosure: Nothing to disclose.
Christopher L Slack, MD, Otolaryngology-Facial Plastic Surgery, Private Practice, Associated Coastal ENT; Medical Director, Treasure Coast Sleep Disorders
Christopher L Slack, MD is a member of the following medical societies: Alpha Omega Alpha, American Academy of Facial Plastic and Reconstructive Surgery, American Academy of Otolaryngology-Head and Neck Surgery, and American Medical Association
Disclosure: Nothing to disclose.
Arlen D Meyers, MD, MBA, Professor, Department of Otolaryngology-Head and Neck Surgery, University of Colorado School of Medicine
Arlen D Meyers, MD, MBA is a member of the following medical societies: American Academy of Facial Plastic and Reconstructive Surgery, American Academy of Otolaryngology-Head and Neck Surgery, and American Head and Neck Society
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