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Author: Devraj B Basu, MD, PhD, Clinical Fellow and Lecturer, Department of Otorhinolaryngology-Head and Neck Surgery, University of Pennsylvania Health System

Devraj B Basu is a member of the following medical societies: American Academy of Otolaryngology-Head and Neck Surgery and American Medical Student Association/Foundation

Coauthor(s): 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; Gregory S Weinstein, MD, FACS, Professor and Vice-Chairman, Codirector for the Center for Head and Neck Cancer, Department of Otorhinolaryngology-Head and Neck Surgery, University of Pennsylvania Hospital

Editors: 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; Francisco Talavera, PharmD, PhD, Senior Pharmacy Editor, eMedicine; Nader Sadeghi, MD, FRCS(C), Associate Professor of Surgery, Director of Head and Neck Surgery, Department of Surgery, Division of Otolaryngology, George Washington University; Christopher L Slack, MD, Otolaryngology-Facial Plastic Surgery, Private Practice, Associated Coastal ENT; Medical Director, Treasure Coast Sleep Disorders; Arlen D Meyers, MD, MBA, Professor, Department of Otolaryngology-Head and Neck Surgery, University of Colorado School of Medicine

Author and Editor Disclosure

Synonyms and related keywords: 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

Malignant invasion of the carotid artery presents the head and neck surgeon with difficult dilemmas in regard to both diagnosis and treatment. When resection of the artery as part of a cancer surgery is considered, preoperative evaluation is necessary to discern which patients are at greatest risk of ischemic stroke and thus likely to benefit from carotid reconstruction. Unfortunately, individuals undergoing carotid resection, either with or without reconstruction, still bear significant risk for 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 often considered a contraindication to primary surgical therapy because of the risk of stroke with carotid resection. 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 (Huvos, 1973; McCready, 1989).

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

Carotid wall invasion usually arises from either direct extension from a malignant tumor, commonly of the nasopharynx or oropharynx, or advanced jugular chain nodal metastasis with extracapsular spread. As noted, such individuals are most often considered for carotid resection as part of a surgical salvage attempt after prior radiotherapy and chemotherapy have failed. Occasionally, benign tumors of the lateral skull base, such as glomus jugulare tumors and schwannomas, as well as various skull base malignancies, may also necessitate planned carotid resection (Sanna, 2004).

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 strongly suggests invasion but, as noted, can be deceiving in the postradiation salvage setting. Similarly, involvement of greater or less than 180° of the carotid circumference on CT scan was not significantly predictive of histologic invasion (Yoo, 2000). If elective surgery is contemplated and carotid invasion is deemed possible based on clinical and radiographic impression, further preoperative planning with angiography is necessary.

Occasionally, in cases of carotid rupture, emergent carotid ligation or resection is warranted without preoperative testing or even the opportunity for reconstruction. More often, however, sentinel bleeding is controlled with conservative measures without radical intervention, 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 (Konno, 1981), no difference was noted in complications associated with the reason for ligation, which included cancer infiltration, impending rupture, and acute rupture. 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 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 20 7 0 7 3 4 2
Konno, et al 156 53 6 47 24 . . . . . .
Razack and Sako 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 (Jones, 1981). 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 (Ehrnefeld, 1983). 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 (Kelly, 1979).



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, the availability of any nonsurgical therapies, and the patient's level of enthusiasm for surgery given the risk of severe neurologic sequelae or even death.



Imaging Studies

  • Angiography: The initial assessment for feasibility of resection without reconstruction consists of 4-vessel angiography, which establishes the patency of the vessels and the potential availability of collateral flow through the circle of Willis if one carotid is occluded.
  • Trial balloon occlusion
    • When collateral flow is present based on angiography findings, temporary preoperative occlusion provides physiologic information on the patient's ability to tolerate occlusion of the carotid to be resected. The original diagnostic trials of carotid occlusion were performed intraoperatively on the common carotid artery using umbilical tape under local anesthesia (James, 1971). Trial balloon occlusion (TBO) performed during angiography has replaced operative trial occlusion. The patient is heparinized while the balloon catheter is placed under angiographic guidance. It is inflated in the internal carotid artery for up to 15-30 minutes while the patient is monitored for development of neurologic signs and symptoms.
    • For multiple reasons, even when the patient tolerates TBO, a cerebral vascular accident (CVA) may still develop if operative ligation is ultimately performed. First, thrombus may develop in the carotid stump and embolization may occur. Second, intraoperative blood loss and decreased systemic blood pressure under general anesthesia may decrease regional cerebral blood flow (CBF) more than balloon occlusion or ligation alone. For this reason, a hypotensive challenge during TBO may improve the predictive value of the test (Standard, 1995) but is not routinely performed at most centers.
  • Flow Scanning
    • Single-photon emission computed tomography scanning
      • Because of the inadequacy of predicting cerebral ischemia with TBO alone, CBF studies during carotid occlusion have been developed. Single-photon emission computed tomography (SPECT) imaging using technetium-99m hexamethylpropyleneamine oxime (Tc-99m HMPAO) provides a semiquantitative comparison of blood flow to each hemisphere. After the patient has tolerated TBO, Tc-99m is injected intravenously, with the balloon kept inflated for an additional 15-30 minutes. Tc-99m is converted to a hydrophilic form inside the brain that is retained for hours. Because the half-life of Tc-99m is 6 hours, SPECT scanning can be delayed until after completion of angiography and TBO.
      • Tc-99m SPECT scanning does not provide an exact measurement of regional CBF. Rather, it is evaluated based on differences in tracer retention between the 2 sides, and adequate CBF is defined as less than a 10% difference between hemispheres.
    • Xenon flow scanning
      • During TBO, CBF may rise or fall in either hemisphere, resulting in a significant difference in CBF between hemispheres. Thus, determination of the absolute CBF may be helpful in overcoming this ambiguity inherent in interpretation of SPECT scans. Xenon-133 scans offer a more quantitative measurement of regional CBF (Andersen, 1988) but are technically more difficult than SPECT when used in conjunction with TBO. While the carotid is occluded, the patient must inhale xenon gas and, unlike with SPECT, undergo simultaneous nuclear medicine scanning because xenon is rapidly absorbed and discharged.

        The primary difficulty with this technique lies in the need to take the patient from the angiography suite to the nuclear medicine scanner with the certainty that the balloon is still in place. In order to perform this procedure optimally, the nuclear medicine scanner needs to be present in the angiography suite. With this technique, adequate CBF is defined as greater than 30 mL/100g/min, although some require a threshold of as high as 40 mL/100g/min to be considered low risk (Erba, 1988).

      • Regional CBF may also be measured using stable xenon as a CT contrast agent. This method requires transferring the patient to the CT scanning unit with a catheter in place and with the same considerations as in xenon flow scans. The quantitative results from this method have been shown to prevent frequent misinterpretation of flow asymmetries between hemispheres (Witt, 1994) that may lead to a false-positive reading of a SPECT scan.



Surgical therapy

Permanent balloon occlusion

When carotid reconstruction is not desirable or technically feasible in a patient who has passed TBO and flow testing, permanent balloon occlusion is a preoperative intervention that may reduce cerebral vascular accident (CVA) incidence over simple ligation (Adams, 1999). The underlying principle is that high embolization of the carotid eliminates the standing column of blood present after ligation that later serves as a source of stump emboli. The method involves angiographic placement of permanent balloons or coils in the carotid siphon region just 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 (Eckard, 1992).

However, the application of this technique have been associated with neurologic complications and with protracted intraoperative hypotension; in one case, migration of a balloon was reported (Freeman, 2004). 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 (Gonzalez, 1990).

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:

  • High risk - Failed TBO, no cerebral blood flow (CBF) scans obtained
  • Moderate risk - Passed TBO, inadequate CBF scan
  • Low risk - Passed TBO, adequate CBF scan

Moderate- and high-risk patients usually undergo reconstruction if carotid resection is performed, while the best management of low-risk patients using available treatment methods is less clear. Inevitably, a few patients in the low-risk category 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 (Meleca, 1994; Wright, 1996; Freeman, 2004). However, although unusual, these complications may still occur in the face of vein grafting, even in low-risk patients (de Vries, 1990; Segal, 1995). 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 (Nishioka, 1966; Gonzalez, 1990; Youmans, 1967; Konno, 1981).

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 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 (Nishioka, 1966). 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 (Barnett, 1978).

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, 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 very poor in cases of malignant carotid involvement, although no universal statement can be made about all tumors, and each patient merits careful consideration within their clinical context. However, early local recurrence is the norm, and rapid presentation with distant metastatic disease is common. Patients require extensive preoperative counseling and must contemplate salvage surgeries, bearing in mind substantial risks, including those of devastating neurologic sequelae. This risk can be managed significantly, but adverse neurologic outcomes from carotid resection cannot yet be prevented altogether.



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Management of the Neck With Carotid Artery Involvement excerpt

Article Last Updated: Sep 5, 2006