Annals of Vascular Surgery
Volume 23, Issue 5 , Pages 616-620, September 2009

Management of Carotid Body Tumors and Familial Paragangliomas: Review of 30 Years' Experience

Department of Cardiovascular Surgery, Faculty of Medicine, Atatürk University, Erzurum, Turkey

Article Outline

Background

Carotid body tumors (CBTs), especially familial paragangliomas, are rare benign neoplasms, accounting for <0.5% of all tumors; and they are the most common extra-adrenal paraganglioma.

Methods

In this study, CBTs were clinically suspected in 31 patients but diagnosed by histopathology in 28 between 1977 and 2007 at our department. All but one was operated upon. The ages of the 30 surgically treated patients ranged 17–73 years. A mass in the neck was the common symptom in all patients. Two of the 28 patients with CBTs had a familial paraganglioma history of CBT.

Results

Twenty-eight of these 30 surgically treated patients had confirmed CBT by histopathology; the diagnoses of other two patients were neurofibroma in one and tuberculosis lymphadenitis in one. These two patients were excluded from the study. CBTs were resected without a shunt procedure. UltraCision was used in five patients for tumor resection; the surgical results of these patients were excellent (easy dissection, minimal hemorrhage and time operation). Twenty patients underwent total resection, six had resection and saphenous vein interposition, one had partial resection, and one had carotid artery ligation with no resultant neurological deficit. One case of hypoglossal paralysis and one benign recurrence were detected. No mortality or malignant course was observed.

Conclusion

CBTs are infrequent neoplasms; their surgical treatment is highly dependent on the ability and experience of the surgeon. The diagnostic and therapeutic relevance reside in making a timely diagnosis to propose a surgical treatment aimed at preventing complications and neurological damage. Surgical resection is usually definitive therapy for these lesions.

 

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Introduction 

Carotid body tumors (CBTs) are rare benign neoplasms, accounting for <0.5% of all tumors; and they are the most common extra-adrenal paraganglioma.1 They develop from epithelioid cells derived from the neural crest. The normal carotid body is a small mass of neurovascular tissue located bilaterally in the medial valley of the carotid artery bifurcation. The fetal carotid body develops within the arterial wall between the medial and adventitial layers. The carotid body is usually a minute oval structure of 1–5mm in diameter located on the posterior aspect of the carotid bifurcation. The blood supply is mostly via a small vessel from the carotid bifurcation and branches of the external carotid artery. The carotid body is innervated by afferent branches of the glossopharyngeal and vagus nerves and the cervical sympathetic ganglia.2, 3 The carotid body has extremely high blood flow and oxygen consumption.4 CBTs usually result in symptoms related to their mass and compression on adjacent structures in the relatively confined space of the carotid sheath. The tumor is usually discovered on routine examination and noted to be pulsatile but not expansible. Biopsy is contraindicated because of the risks of bleeding and pseudoaneurysm.1, 2, 3 Approximately 10% of patients have bilateral lesions. The prevalence of local recurrence and local invasion is estimated at about 10% for CBTs.5

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Patients and Methods 

In this study, CBTs were clinically suspected in 31 patients (24 females, 7 males) between 1977 and 2007 at the Department of Cardiovascular Surgery, Atatürk University Research Hospital, Erzurum, Turkey. A mass in the neck was the common symptom in all patients (Table I). The site and size of each of these tumors were established by imaging studies including color-flow duplex sonography in 19 (Fig. 1), computed tomography (CT) in 29, magnetic resonance imaging (MRI) in 16 (Fig. 2), selective angiography (before 1990) in 22 (Fig. 3), and digital subtraction angiography (DSA, after 1990) in nine. Clinical and laboratory studies were done to exclude hormonally active tumors in all patients. Functioning CBTs produce clinical manifestations such as hypertension, headaches, palpitations, and tachycardia. Contributory laboratory data include urinary elevated 24hr metanephrine and vanillylmandelic acid levels and serum catecholamine glucose level screening tests. In our study, no hormonally active tumor was detected on the basis of clinical and laboratory studies. Thirty patients agreed to undergo surgical treatment. The CBTs were resected without a shunt procedure.

Table I. General characteristics
Classification (according to Shamblin et al.6)Patients (n)Age (years)SexSymptomsDiagnosisTreatmentComplicationFollow-up
I417FCervical massSA+ CTTR—14 years
26MCervical massSA+ CTTR—10 years
50FCervical massCT+DSA+CFDS+MRITR—9 years
56FCervical massCT+CFDS+SATR—2 years
II1538FCervical massSATR—21 years
50FCervical massSATRRecurrence17 years
30FCervical massSA+CTTRHP15 years
55FCervical massSA+ CTTR—13 years
43MCervical massSA+ CTTRRecurrencea13 years
36MCervical massSA+ CTTR+SVI—11 years
31FCervical massSA+ CTLigation—12 years
52FCervical massCT+ DSATR+SVI—12 years
65FCervical massCT+ DSATR+SVI—12 years
55FCervical massCT+DSA+CFDSTR+SVI—8 years
58FCervical massCT+CFDS+SA+MRITR—5 years
62FCervical massCT+CFDS+SA+MRITR—4 years
52FCervical massCT+CFDS+SATR—3 years
60FCervical massCT+CFDS+SA+MRITR—18 months
50FCervical massCT+CFDS+SA+MRITR—9 months
III965FCervical massCT+DSA+CFDS+MRITR+SVI—13 years
35FCervical massCT+DSA+CFDS+MRITR+SVI—13 years
53MCervical massCT+DSA+CFDS+MRIPR—12 years
42FCervical massCT+CFDS+SA+MRITR—6 years
71FCervical massCT+CFDS+SA+MRITR—5 years
64FCervical massCT+CFDS+SA+MRITR—3 years
73FCervical massCT+CFDS+SA+MRITR—7 months
57FCervical massCT+CFDS+SA+MRITR—6 months
71MCervical massCT+CFDS+SA+MRITR—9 months

SA, selective angiography; CT, computed tomography; DSA, digital subtraction angiography; CFDS, color-flow duplex sonography; MRI, magnetic resonance imaging; TR, total resection; PR, partial resection; SVI, saphenous vein interposition; HP, hypoglossal paralysis.

aOn the other side of the neck.

  • View full-size image.
  • Fig. 3 

    Selective angiography shows a carotid bifurcation involved with a CBT. Note the splaying of the internal and external branches and the dense vascularity of the tumor mass.

Patients diagnosed with CBT were given a medical and family history questionnaire. We established a family who exhibited familial paragangliomas. Two of our 28 patients with CBTs had a familial history of paragangliomas, one in the mother (age 73) and the other in a daughter (age 57). They were members of the same family.

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Results 

In 28 of the 30 surgically treated cases, a CBT was confirmed by histopathology. One case was found to be a neurofibroma, and another was diagnosed as tuberculosis lymphadenitis; these two patients were excluded from the study. There was no history of tuberculosis in the patient with tuberculosis lymphadenitis, and clinical signs in the lung or other organs could not be established. The patient with tuberculosis lymphadenitis had a mass located in the carotid body. CT and DSA imaging were done on this patient preoperatively.

According to the classification of Shamblin et al.,6 four patients had a type I CBT, 15 had type II, and nine had type III (Table I). Total resection was performed in 20 patients, a further six had total resection and saphenous vein interposition, one had partial resection, and one underwent carotid artery ligation. In our study, partial resection for tumor was done in only one case because an artery was invaded. The external carotid artery was ligated due to this artery being invaded and stenotic. Also, the ligation procedure facilitated the resection of the very large tumor.

No shunt procedures were employed. UltraCision (Harmonic Scalpel; Ethicon, Cincinnati, OH) was used in five patients for tumor resection; the surgical results of these patients were excellent. The tumor resection with UltraCision was easier than electrocautery dissection. In our five cases mean blood loss was 500mL and operation time was 4hr.

Regional lymph node was detected in three cases during the operation. Histopathological diagnosis was nonchromaffin paraganglioma in all 28 patients. Two patients of these 28 had familial paraganglioma. One case of hypoglossal paralysis and one benign recurrence were detected (Table I). No patient died, and no malignant course was observed.

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Discussion 

Although the term “tumor” has historically been assigned to these masses, they are not carcinomas; and the neoplastic process is actually hypertrophy of the carotid body tissue. Carotid body hypertrophy has been associated with chronic hypoxia and familial predisposition.7 A history of parents or siblings with asynchronous or remote history of a paraganglioma is a clear indicator of familial disease. A family tendency for paragangliomas occurred in <10% of the cases. All of our patients lived in a particular area at an altitude of 1,800 meters, and two patients had familial paraganglioma.

A CBT can be diagnosed by ultrasound, technetium isotope scintigraphy, CT, or MRI. Color-flow duplex sonography can easily delineate a hypervascular mass nestled in the carotid bifurcation, which differentiates it from a relatively nonvascular mass and is now the most widely utilized noninvasive method.8 In addition, this technique can provide information on the tumor dimensions and demonstrate any coexistent carotid occlusive disease.2, 8 Duplex scan is effective at making the diagnosis, but angiography and CT or MRI are helpful to plan surgery. Angiography is also very sensitive in the detection of small lesions. In our opinion, the definitive diagnostic procedure for CBT evaluation is carotid angiography, which provides more information about the primary tumor, which may help in preoperative planning. Preoperative planning requires a selective carotid arteriogram to provide a record of the arterial anatomy and the relation of the CBT to the carotid bifurcation.

It is still essential to identify those large tumors that may be easily embolized as a preparatory step for surgical excision.2, 9, 10 We did not perform preoperative embolization on any of the CBTs in our series.

A CBT must be differentiated from bronchial cyst, parotid gland tumor, carotid artery aneurysm, lateral aberrant thyroid gland, malignant lymphoma, neurofibroma, tuberculosis lymphadenitis, and metastatic carcinoma.

Tachycardia, hypertension, and tremors may also indicate possible endocrine activity. Carotid body paragangliomas are usually nonfunctional. We found no functional CBT in our cases.

Shamblin and colleagues6 classified CBTs according to their gross relationship with the carotid vessels. Type I tumors account for 26% of cases and are localized masses that are easily removed. Type II tumors are adherent and partially surround the carotid vessels; they make up 46% of such tumors and are removed with moderate difficulty. Type III tumors (27%) are adherent and completely surround the carotid vessels; they are removed with extreme difficulty and generally require resection of the internal carotid with vein graft interposition.11 Type III tumors are associated with a high complication rate (perioperative stroke and cranial nerve dysfunction). Of the 28 CBTs found in our cases, four were type I, 15 type II, and nine type III (Table I).

Several methods of treating CBTs have been proposed. The role of preoperative embolization of highly vascular CBTs is controversial. Preoperative percutanous catheter embolization of the lesion might be effective at reducing vascularity and improving the safety of surgical excision, with lower operative blood loss and decreased technical difficulties. However, percutanous embolization may produce thrombosis in the internal carotid artery or cerebral embolization. Therefore, this method should be used only as an adjunct to operative resection.2, 12, 13 Schick and colleagues14 performed arterial embolization and showed by arteriogram that the size of the tumor decreased 30–90%. Operation time and blood loss are generally longer in the literature. For Schick et al.'s patients, the blood loss was 4,000mL and operation time was 12hr.14 Surgical resection of the lesion by UltraCision might be effective at improving the safety of surgical excision, with lower operative blood loss, decreased technical difficulties, and shorter operation. Surgical resection results of these tumors might be excellent via UltraCision. In our series, this procedure was performed in five cases.

Once a paraganglioma is discovered, surgical excision is the treatment of choice unless the patient has a specific contraindication such as terminal illness, advanced age, or high anesthetic or operative risk.15 This tumor is radioresistant; thus, adjuvant radiotherapy after partial resection is of questionable benefit, and most tumors subsequently demonstrate progressive enlargement.16, 17 The lesion is considered to be malignant if there is infiltration of the paraganglionic tissue into adjacent lymph nodes or distant metastasis, and approximately 10% of reported cases meet this definition of malignancy. In follow-up studies at the Memorial Cancer Center, malignancy was detected in 9% of 43 patients over a 20-year period.12, 13, 14 No malignant course was observed in our study.

The external carotid artery should be ligated only if it is invaded.2, 3, 13 As in our single case, Padberg and colleagues18 ligated the carotid arteries in three patients without causing any neurological deficit, although abrupt obstruction of the carotid arteries caused paralysis in 30%. Chronic narrowing of the internal carotid artery may not produce paralysis due to collateral circulation.19 However, Chamorro Sanchez and colleagues20 reported transient ischemic attacks in a patient with bilateral CBTs. Cowley21 reported 12% mortality and a 30% incidence of paralysis after carotid ligation. A donor saphenous vein site should be prepared as complicated arterial reconstruction is required in approximately 25% of cases.13, 21 Carotid shunts should also be available because clamping of the internal carotid artery may be necessary.

In conclusion, CBTs are infrequent neoplasms; CT and MRI are recommended for early screening and contribute additional information about the tumor extension and definitive treatment in patients with CBTs and familial paraganglioma. Selective carotid angiography is very sensitive in the detection of small lesions. Surgery is mandatory to obtain disease-free survival with low morbidity and mortality.

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References 

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 Presented at the 3rd International Clinical Vascular Biology Congress, Antalya, Turkey, Nisan 25–29 2007, and at the 9th National Congress of the Turkish Association of Cardiovascular Surgery, Antalya, Turkey, November 1–5, 2006.

PII: S0890-5096(09)00131-9

doi:10.1016/j.avsg.2009.06.014

Annals of Vascular Surgery
Volume 23, Issue 5 , Pages 616-620, September 2009

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