Abstract
Objective: Carotid resection for head and neck cancer is rare, and serious complications may arise since such cancer is frequently detected in advanced stages. The objective is to describe nine cases of carotid artery resection and reconstruction due to tumor invasion. Methods: The clinical records of nine patients who underwent carotid resection and reconstruction at our hospital were retrospectively reviewed. Carotid body tumors were evaluated with the aid of a vascular team in case carotid resection was necessary at the time of surgery. CT angiography to determine the status of the circle of Willis was performed in all patients who might undergo carotid resection and reconstruction in case of failure to restore cerebral blood flow and thus reduce possible sequelae due to ligation. Results: Of nine patients, 6 had carotid body tumors, 1 had a thyroid tumor of conglomerate lymph nodes, 1 had a larynx tumor of conglomerate lymph nodes, and 1 had a myofibroblastic tumor. There were no intraoperative cerebrovascular accidents. One patient (11.1%) had a cerebrovascular accident secondary to carotid hematoma in the intermediate postoperative period that required vascular graft removal. One patient (11.1%) died seven days after surgery following an ischemic cerebrovascular accident. Eight patients remain asymptomatic, and 1 patient with recurrence and metastasis. Conclusions: Carotid resection remains a controversial issue in the treatment of advanced head and neck cancer. However, carotid resection and reconstruction are required for disease control, and complications such as thrombosis or vascular accidents may arise. Fortunately, this is a rare condition. We recommend carotid reconstruction for all patients in whom resection is required for tumor control. Ligation should be a last resort, as seen in the management of one of our patients.
Keywords: Carotid resection, Carotid ligation, Reconstruction, Head and neck tumors
Introduction
In 1552 in France, Ambroise Paré became the first surgeon to ligate a carotid artery while he treated a patient with a sword thrust to the throat. The patient survived the operation but later suffered a cerebrovascular accident (CVA) that resulted in left hemiplegia and aphasia [1]. In the late 18th century at St. Bartholomew’s Hospital, London, John Abernethy presented the first complete report of carotid ligation to stop bleeding, but without explaining the causes [2, 3].
There are two instances where carotid ligation or resection is necessary. Ligation is elective when tumors are infiltrating or intimately attached to the artery. Resection is nonelective when, whatever the cause, an artery bleeds [4, 5]. Elective carotid artery resection is still a controversial treatment regarding the management of advanced head and neck cancer due to the complexity of the procedure and its risks of neurological sequelae.
New procedures have been studied and developed to assess and select patients who could tolerate carotid resection and thus minimize the risks of cerebrovascular accidents. Moreover, artery reconstruction techniques have improved using synthetic grafts, whose sequelae and mortality rates are lower than allografts or ligation [6, 7]. We describe nine cases of carotid artery resection and reconstruction due to tumor invasion.
Materials and Methods
The records of nine patients who underwent carotid resection and reconstruction at our hospital were retrospectively reviewed. Carotid body tumors are evaluated with the aid of a vascular team in case carotid resection is necessary at the time of surgery. CT angiography to determine the status of the circle of Willis is performed in all patients who might undergo carotid resection and reconstruction in case of failure to restore cerebral blood flow and thus reduce possible sequelae due to ligation.
Case Reports
Case 1
A 57-year-old male presented with a history of progressive tumor growth at cervical level III for 3 years. Papillary thyroid carcinoma was diagnosed after performing a fine needle aspiration biopsy. CT imaging showed compromised vessels and cartilage invasion, for which total thyroidectomy with right-sided and central selective neck dissection were performed. During surgery a spontaneous rupture of the compromised artery was replaced with a Dacron graft. No postoperative neurological deficit was observed. The histopathological report showed a tumor of 8 × 5 cm, 5/51 nodes with papillary thyroid cancer, and capsule rupture (Fig. 1). A cumulative dose of 400 mCi of I-131 was administered. The patient also received 66.6 Gy of radiotherapy. At 4-year follow-up, biochemical testing and PET scan revealed stable disease due to pulmonary metastasis.
Fig. 1.
(a) Carcinoma papilar of the thyroid N3 metastasis to the left neck, (b) Surgical specimen containing the tumor and external carotid artery, (c) Carotid artery reconstruction
Case 2
A 32-year-old female presented with an 11-month history of a pulsatile tumor in the left neck. TC scan reveled a carotid body tumor Shamblin III. Segmental resection at the carotid bifurcation and reconstruction of the common artery to internal carotid artery using a Gore-Tex graft were performed and ligation of the external carotid artery. The histopathological report showed a carotid body paraganglioma measuring 4 × 2.5 × 2.5 cm, a portion of the carotid artery, and 10 nodes with no evidence of neoplasia. The patient was discharged three days after surgery and received phoniatric rehabilitation. Follow-up lasted for a year and was discontinued because the patient did not develop any major complications. Seven years after surgery the patient remained asymptomatic.
Case 3
A 27-year-old female diagnosed with bilateral carotid body tumor was referred to our hospital. TC scan revealed a 6 × 4 cm lesion in the left carotid bifurcation and a contrast-enhanced node of 1.5 cm on the right side. During resection of the left carotid body tumor, a 4 × 4 cm lesion infiltrating and fully encasing the carotid artery was found. A partial resected of the carotid artery with ligation of the external carotid artry along with the vagus nerve, and a Gore-Tex graft was placed. The histopathological report described a vagal paraganglioma measuring 1.7 × 1.4 × 1 cm, a left carotid body tumor measuring 3.7 × 3 × 2 cm, and 13/13 nodes of mixed hyperplasia. Six days after surgery the patient presented swelling on the left side of the neck. USG revealed soft tissue edema without signs of a hematoma. However, a few hours later the patient was operated on for carotid bleeding. A tracheostomy was performed, the hematoma was drained (100 cc), and the internal carotid artery and jugular vein were ligated. NMR and CT scan found multiple cerebral strokes in the left hemisphere around the second and third frontal gyri with a hyperintense appearance and internal carotid artery thrombosis. In addition, a chest x-ray revealed left pneumothorax that required a drain tube. The patient recovered well. Hoarseness and slight upper limb motor impairment were observed after decannulation. At 10-year follow-up the patient remains asymptomatic (Fig. 2).
Fig. 2.
(a) CT scan show a carotid body tumor Shambln III, (b) Resection of tumor attached to the wall at the carotid bifurcation, (c) Carotid artery reconstruction
Case 4
A 54-year-old female diagnosed with carotid body tumor. A partial resection of the common carotid artry was done. Nerves and jugular vein were preserved, and reconstruction was accomplished by placing a Gore-Tex graft. During follow-up the patient did not show neurological deficit; carotid Doppler ultrasound found no evidence of stenosis nor atheroma, and blood flow was normal. At 10-year follow-up the patient remains asymptomatic (Fig. 3).
Fig. 3.
(a) Angio-CT scan showing a carotid body tumor, (b) Resection of tumor attached to the wall at the external carotid artery, (c) External carotid artery vascular graft
Case 5
A 43-year-old male with a 1-year history of supraglottic squamous cell carcinoma with left lymph node metastasis. Tomography showed vessel involvement due to a left conglomerate mass invading the pyriform sinus (T3N3M0). Since the tumor was deemed unresectable at the time, the patient received concomitant treatment. Poor response to radiation (72 Gy) and gemcitabine was due to bulky disease. Treatment was switched to 10 Gy electron boost. CT scan revealed poor clinical response (< 50%) and persistence of the conglomerate mass with a fixed size of 5 × 3 cm. Even though palliative care was considered, salvage surgery was provided. Left neck dissection was performed, and segmental resection at the level of the bifurcation with a goretex vascular prosthesis graft, from the common to the internal carotid, the external carotid artery was ligated, and the spinal and hypoglossal nerves were sacrificed.The pathology report indicated squamous cell carcinoma infiltrating the middle and outer layers of the carotid artery bifurcation. At follow-up the patient showed symptomatic improvement with decreased neck stiffness and greater head and neck mobility. The patient was followed up for 6 months and remained asymptomatic with stable disease, then was lost to follow-up with disease, and, finally, two years after treatment was reported dead of other cause.
Case 6
A 53-year-old male who had undergone superficial parotidectomy 10 years earlier and had a benign report presented with a 5-year history of a pulsatile tumor in the left neck, which was diagnosed as carotid body tumor. CT scan showed a heterogeneous mass on the left side of the carotid space that displaced the vascular structures, with hypodense areas after contrast injection in relation to the carotid body. The patient underwent stent placement following a two-step hybrid surgical procedure for carotid body tumors as described by Hurtado Lopez et al. [8]. Resecting the external carotid artery could not be achieved due to the diameter of the common carotid artery. After a close 8-month follow-up, tumor resection + reconstruction using a vascular graft + suture of the left external carotid artery were performed. The Shamblin IIIa carotid body tumor extended from the common carotid artery to the skull base. No neurological deficit in the postoperative period was observed. At 10-year follow-up, the patient noticed a swelling at the lesion site. Ultrasound showed a level IIa cervical nodule. CT scan demonstrated a recurrent vascular tumor measuring 6 × 5 cm at the graft site with prosthetic material, bilateral pulmonary nodules, and a solid lesion in the left scapula, which was biopsied and reported as metastasis. The patient was referred to palliative care, received a total of 35 Gy radiotherapy, and showed a partial clinical response. Chemotherapy was proposed, but the patient preferred to remain under monitoring.
Case 7
A 48-year-old male presented with a 6-month history of a left cervical tumor measuring 4 × 4 cm and dysphonia. Nasofibroscopy showed left cord paralysis. CT scan revealed a tumor with carotid wall involvement. No biopsy was performed. During surgery, the left internal jugular vein and external carotid artery were ligated, the internal carotid artery was resected, and a PTFE vascular graft was placed. The histopathological report described an inflammatory myofibroblastic tumor measuring 9 × 5.5 × 5 cm and 5/5 lymph nodes with follicular hyperplasia. At 6-month follow-up, Doppler ultrasound detected appropriate and continuous blood flow. At 5-year follow-up, no tumor activity was observed, and the patient maintained an adequate quality of life (Fig. 4).
Fig. 4.
(a) Inflammatory pseudotumor firmly attached to the sternocleidomastoid muscle with carotid involvement, (b) En bloc resection of internal carotid artery with tumor, (c) Carotid artery vascular graft
Case 8
A 42-year-old female with an 8-month history of a left cervical pulsatile tumor showing a progressive increase in volume. Contrast-enhanced CT revealed a 36 × 37 × 40 mm Shamblin IIIB carotid body tumor. During surgery it was found that the tumor was encasing the internal and external carotid arteries and extended above the digastric muscle. The external carotid artery was cut, clamped, and ligated. The internal carotid artery had a punctiform perforation for which a 5 − 0 Prolene suture was placed, with ischemia time of 5 min. The pathology report was chemodectoma measuring 7 × 5 × 1 cm with fibrosis and infiltrating the tunica adventitia. The patient evolved without complications during the postoperative period and remained without tumor activity for 4 years. After this time a recurrences was achieved at the level II tumor on the left side of the neck. CT angiography showed a recurrence of carotid body tumor Shamblin III. During surgery the tumor was found to be attached to the extracranial portion of the internal carotid artery. A segmental resection of the most distal portion of the carotid artery was performed 2 cm before reaching the skull. En bloc resection of the internal carotid artery with a ~ 6 cm tumor was performed and a 4-cm Dacron graft was placed. Patency and hermeticity were verified. The pathology report indicated a 4 × 3 × 2.2 cm carotid body tumor with free edges adhered to the artery. At 7-year follow-up the patient remained asymptomatic with no tumor activity.
Case 9
A 29-year-old female with a 4-year history of a carotid body tumor with progressive growth. CT scan demonstrated a Shamblin III carotid body tumor of 55 × 38 × 73 mm. During surgery a non-chromaffin paraganglioma of 7 × 7 × 2 cm was found. It was resected without complications and with minimal bleeding. The histopathological report showed free margins. However, it was found that 2 cm away from the skull base the internal carotid artery wall had a circumferential involvement of 180 degrees with bleeding. During reconstruction of the internal carotid artery, a difference in the diameter of the synthetic bridge was found, and transposition with end-to-end external to internal carotid artery anastomosis was performed, with 1500 cc of blood loss. The patient was transferred to the ICU with a high risk of CVA. The patient responded poorly within the 5 postoperative days, having intracranial hypertension, cerebral edema, and malignant ischemic stroke, as shown by CT angiography. Since the patient was unsuitable for surgery, she received palliative care until her death on the 7th postoperative day.
Discussion
Carotid artery ligation is not a new procedure. In fact, it was common in the 19th century when surgery professors recommended it in cases of bleeding (from either the artery or its branches), tumors, aneurysms, epilepsy, trigeminal neuralgia, psychosis, hemiplegia, and even headaches [3]. There are currently two indications for carotid resection: (1) when tumors are invading or intimately attached to the artery, this is an elective and uncommon procedure; (2) artery bleeding, which is an emergency condition requiring immediate reconstruction to avoid neurological sequelae; however, sometimes these sequelae are of secondary importance to life preservation.
Peeling the tumor off the arterial wall instead of resecting the carotid artery results in positive margins R1 or R2. Up to 40% of pathological specimens have microscopic wall invasion, which can eventually lead to rupture and subsequent mortal bleeding. In the present series we describe both benign and malignant tumors partially or totally involving the wall circumference that required partial or total resection [5]. In Mexico, and particularly in our clinical specialty, 75% of tumors are detected in advanced stages; nevertheless, carotid artery infiltration is uncommon. One-year and two-year disease-free survival for patients with malignant tumors are, respectively, 44% and 22%. Despite poor survival rates, locoregional control of the disease is achieved, and the quality of life improves [6–9].
One problem of vascular resection and reconstruction is carotid kinking, as the result of reduced blood flow, which can trigger a stroke. Measuring the balloon-occluded intra-arterial stump pressure is the most valuable indicator to assess the risk of thrombosis and stenosis after carotid resection. Some authors believe that a stump pressure of 55–60 mm Hg allows safe ligation with no major neurological sequelae, [1] whereas others recommend a stump pressure greater than 70 mm Hg as a cutoff threshold [4]. Setting a threshold of > 50 mm Hg, Meleca et al. [5] found that the risk of neurological complications was higher when performing ligation alone than reconstruction.
CT angiography is performed to determine the status of the circle of Willis in all patients who might undergo carotid resection and reconstruction. Other promising tests have been described in the literature to assess collateral flow, such as inflating a balloon inside the common carotid artery for 20 min with neurological monitoring. If there are no changes in brain function, a single-photon emission CT is performed. If this CT finds any abnormalities, the resected carotid artery must be reconstructed. In a study conducted by de Vries et al., [4] 136 patients underwent temporary balloon occlusion of the internal carotid artery and were monitored for neurological changes by EEG for 15 min. If no changes occurred, balloon occlusion was performed again but this time to measure blood flow. Those patients who completed the test and had normal blood flow were classified as low risk for neurological complications (in case the internal carotid artery had to be resected). The authors concluded that, despite the positive results, a larger sample size was needed to be statistically significant [10–12].
CT angiography provides detailed anatomical information and functional status on both carotid arteries and the circle of Willis. Ligation is contraindicated in the absence of a patent circle of Willis. In our hospital only CT angiography is available for such surgical planning, since we lack the material or trained personnel to perform the procedures described in the most recent literature. There is currently no sufficiently reliable test to predict which patients can undergo ligation without risk of suffering major neurological complications; therefore, we believe reconstruction is better than ligation alone, unless it is absolutely necessary.8,10−12
The hybrid surgical procedure described by Hurtado-Lopez et al. [8] is a promising technique we also use (Case 6), with which the risk of arterial collapse is reduced by placing a stent and performing a two-step arterial resection and reconstruction. It also facilitates reconstruction by maintaining patency during graft-artery anastomosis. In case 9, a Shamblin III carotid body tumor infiltrating the arterial wall led to a long ischemic time, blood loss of 1500 cc, and the patient’s death secondary to ischemic stroke and neurological compromise. We believe that the hybrid procedure with stent placement would have avoided arterial reconstruction since the stent would have protected the artery even if there was a partial loss of the carotid wall. The risk of bleeding can be reduced by having the stent as an arterial bridge while reconstruction is achieved, as mentioned by Gustavo Fink et al. [13].
As we published before, [14] infiltration must be confirmed clinically or histologically to avoid biases of vascular damage due to surgical deficiencies and to diminish subjective aspects or lessen their value. In case 9 no injury was caused during resection; we noticed the infiltration once the tumor had been removed. Moreover, the tumor distance to the skull base was 1 cm, which results in a 1.8 times increase in > 250 ml of blood loss, as we have already reported alongside Kim GY et al. [15]. Therefore, elective procedures should not be limited to malignant tumors, since benign tumors can grow to the point where resection poses a high risk of artery laceration because it is impossible to find a resection plane between the artery and benign tumor. Additionally, if the artery is weakened during resection and the arterial wall exhibits marked muscular atrophy, blood loss could occur in the postoperative period and result in an emergency procedure [13–15].
In the case of paragangliomas, they sometimes are bulky tumors making resection difficult, or the carotid artery, either the common or internal carotid artery, is fully surrounded by the tumor. Furthermore, as Luna-Ortiz et al. explained, [14] the resection plane along the white line might be lost due to fibrosis and clear artery infiltration, which would require carotid resection, as in many of our cases. Hence, identifying affected arteries is the first step in patient assessment for proper procedure planning, which most of the time is only determined during surgery [16–18].
Most authors recommend autologous tissues for vascular reconstruction, [19, 20] such as the great saphenous vein or superficial femoral artery, or transposition of the external to the internal carotid artery when the common carotid artery is preserved [19] because they last longer and have a lower risk of infection. However, synthetic grafts have improved in recent years, allowing adequate permeability in the middle and long term [20–22]. Therefore, using synthetic materials is recommended for patients likely to undergo neck radiation since these materials remain permeable despite fibrosis and scarring [22, 23].
In an English case series review of 148 patients, Katsuno et al. [24] evaluated the safety of carotid reconstruction and reported major neuromorbidity of 4.7%, operative mortality of 6.8%, and combined major neuromorbidity with mortality of 10.1%. These findings are similar to the ones observed in our series, where one patient had a CVA and recovered almost entirely. Reports on resection without reconstruction show higher rates: mortality ranging from 20 to 29% and neuromorbidity of 25 to 29%.23,24 However, reconstruction also carries a high risk of complications such as thrombosis or bleeding, which could lead to death.
Conclusions
Carotid resection remains a controversial issue in the treatment of advanced head and neck cancer. However, in such instances carotid resection and reconstruction are required for disease control, and complications such as thrombosis or vascular accidents may arise. Fortunately, this is a rare condition. Ligation should not be a likely option. We recommend carotid reconstruction for all patients in whom resection is required for tumor control. Ligation could be a last resort, as seen in the management of one of our patients. Reconstruction also carries a high risk of complications such as thrombosis or bleeding, which can lead to death.
Funding
No funds, grants, or other support was received.
Declarations
Conflict of Interest
None.
Non-financial Interests
None.
This is an observational study. The National Cancer Institute Ethics Committee has confirmed that no ethical approval is required.
Verbal informed consent was obtained.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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