Carotid
Body Tumors
Dennis H. Kraus, MD; Bruce M. Sterman, MD; Albert G. Hakaim, MD; Edwin G. Howard L. Levine, MD; Benjamin G. Wood, MD; Harvey M. Tucker, MD
\s=b\ The surgical management of carotid body tumors requires identification and preservation of neural and vascular structures without compromising resection of the neoplasm. Fifteen patients were examined and treated for carotid body tumors at the Cleveland (Ohio) Clinic Foundation from 1979 through 1987. The benchmark of diagnosis is bilateral carotid angiography. When neural structures are free of tumor, meticulous dissection facilitates their preservation. Large tumor size
increases risk for arterial resection necessitating reconstruction. The use of a vascular shunt minimizes the risk of cerebral ischemia. Postoperative intravenous digital subtraction angiography allows for evaluation of arterial repair. A retrospective review of 15 carotid body tumor resections performed in 14 patients revealed no evidence of tumor recurrence, no mortality associated with surgical intervention, no postoperative cerebrovascular accident, and limited morbidity associated with unavoidable sacrifice of neural elements. (Arch Otolaryngol Head Neck Surg.
1990;116:1384-1387)
Carotid bodyparagangliomas arising
tumors are nonchromaffin at the bifurcation of the common ca¬ rotid artery. The causes of carotid body tumors in high-altitude dwellers who have hyperplasia of the
chemosensory organ secondary to chronic hypoxia have been well described.1-2 No satisfactory explana¬ tion exists for the
occurrence
of these
tumors at lower elevations. It is gen¬ erally accepted that surgery is the pri-
Accepted for publication June 2,1990. From the Departments of Otolaryngology and
Communicative Disorders (Drs Kraus, Sterman, Levine, Wood, and Tucker) and Vascular Surgery (Drs Hakaim and Beven), The Cleveland (Ohio) Clinic Foundation. Presented at the 1989 Annual Meeting of the American Society of Head and Neck Surgeons, San Francisco, Calif, April 6, 1989. Reprint requests to Department of Otolaryngology and Communicative Disorders, The Cleveland Clinic Foundation, 9500 Euclid Ave, Cleveland, OH 44195-5034 (Dr Tucker).
mary mode of
Beven, MD;
therapy; however,
sev¬
eral studies describe the use of radia¬ tion therapy for these benign
neoplasms.34 Preoperative angio¬ graphie evaluation, surgical manage¬ ment of arterial and neurologic struc¬ tures during tumor resection, and sur¬ gical complications are examined retrospectively in this report. PATIENTS AND METHODS From June 1979 through June 1987, 15 patients were treated for carotid body tu¬ mors at the Cleveland (Ohio) Clinic Foun¬ dation. Three patients were referred for treatment of a second carotid body tumor after resection of the contralateral side performed at another institution. All 15 patients underwent complete head and neck examination and digital subtraction an¬ giography (either intra-arterial or intrave¬ nous
study).
Fourteen of these patients were treated surgically, and one patient was given radi¬ ation therapy (45 Gy) because he had un¬ dergone incomplete resection of his tumor before referral to the Cleveland Clinic Foundation and was found to have a second carotid body tumor, as well as an inopera¬ ble mediastinal chemodectoma. A similar operative approach was used in all patients. The common, internal, and ex¬ ternal carotid arteries and the hypoglossal and vagus nerves were identified and con¬ trolled prior to the resection of the carotid body tumor. Transection of the external carotid artery improved access to large tu¬ mors, and subadventitial dissection facili¬ tated removal of carotid body tumors. How¬ ever, it resulted in an increased risk of in¬ advertent entry into the carotid artery. Management of a simple arterial laceration consisted of controlling the bleeding by gentle direct finger pressure over the open¬ ing while the patient was given 7500 U of sodium heparin. After the temporary ap¬ plication of atraumatic vascular clamps, the laceration was primarily repaired. More extensive arterial injuries required saphenous vein graft replacement, using an indwelling Heyer-Schulte-Sundt shunt to maintain cerebral perfusion. Postoperative intravenous digital subtraction angiogra-
Downloaded From: http://archotol.jamanetwork.com/ by a New York University User on 06/09/2015
phy
was
used to evaluate arterial repair. also examined for post¬
patients were operative cranial The
nerve
deficit
or
cere-
brovascular accident.
RESULTS
The patients ranged in age from 24 to 72 years (mean age, 45 years). There were 11 women and four men. Four¬ teen were white, and one was Hispanic (the only case from a high-altitude
geographic location). Multiple paragangliomas were found in seven pa¬ tients (Table 1). Symptoms included neck mass (all 15 patients), tenderness (two patients), and dysphagia with as¬ piration (one patient). On physical ex¬ amination, there were two patients with neck bruits, two patients with cranial nerve deficits, and one patient with lateral pharyngeal wall displace¬ ment.
Angiography showed preoperative tumor-induced occlusion of the exter¬ nal carotid artery in one patient and increased widening between the inter¬ nal and external carotid arteries in four patients. In the three patients re¬ ferred to the Cleveland Clinic Founda¬ tion after resection of a carotid body tumor, an occlusion of the internal ca¬ rotid artery was found on the previ¬ ously operated on side. Fifteen carotid body tumors were resected in 14 patients (one patient had staged bilateral surgery). One patient also required a modified radical neck dissection for resection of a recurrent carotid body tumor (previous excision was performed 12 years earlier). Com¬ plete excision of the tumor was felt to have been accomplished in all cases. In one patient with bilateral carotid body tumors, the contralateral tumor was not operated on after the initial proce¬ dure required ligation of the internal carotid artery due to uncontrolled bleeding at the skull base. The other patient, treated nonsurgically, re¬ ceived radiation therapy (45 Gy). None
of the
surgical patients has had tumor within a mean follow-up period of 36 months (range, 8 to 85 months).
Table
recurrence
Vascular or neural structures were sacrificed either completely or in part in 10 of the 15 procedures to accom¬ plish complete tumor resection. Resec¬ tion and ligation of the internal ca¬ rotid artery were required in one case. Primary closure of an inadvertent in¬ ternal carotid arteriotomy was accom¬ plished in three cases, while three oth¬ ers required saphenous vein interposi¬ tion grafts to repair the internal carotid resection. The external carotid artery was resected and ligated in six cases. Surgical treatment of vascular and neural structures around the ca¬ rotid body tumors and postoperative assessment of the carotid arterial sys¬ tem are summarized in Tables 2 and 3. Two of the three arteries repaired with saphenous vein interposition grafts oc¬ cluded postoperatively. There were no postoperative cerebrovascular acci¬ dents among the 15 patients who had undergone surgeries. However, two of the patients referred after operations elsewhere had suffered postoperative cerebrovascular accidents. Both pa¬ tients' neurologic deficits resolved prior to treatment at the Cleveland Clinic Foundation. Two of four patients were treated for vagus nerve paralysis with true vocalcord Teflon injection. Voice was im¬ proved in those patients, and there was no evidence of aspiration. One patient did not require treatment as the con¬ tralateral vocal cord provided ade¬ quate compensation. The only patient to present with preoperative vocal cord paralysis had adequate compensation in the immediate postoperative period. That patient, however, developed a hoarse voice, dysphagia, and aspira¬ tion with pneumonia over time and is presently being examined for addi¬ tional treatment. COMMENT
High index of suspicion is important in the diagnosis of carotid body tumor. Incorrect diagnoses include tubercu¬ lous adenitis, thyroid carcinoma mé¬ tastases, branchial cysts, tonsillar neoplasms, or parotid gland tumors.5 The onset of symptoms is often insid-
1.—Multiple Paragangliomas*
Carotid Body Tumor Glomus
Patient No.
Unilateral
Bilateral
Tympanicum
Other Sites Mediastinal Intratracheal
Aryepiglottic
fold
14
indicates íesion shown at head of table column is present in
Table 2. —
patient.
Involvement of Vascular and Neural Structures in Carotid Body Tumor Surgery
External Carotid Patient
No.
Artery Resection and
Internal Carotid
Ligation*
Cranial Nerve
Artery Surgery
Sacrifice
Resection with
IX,t X.t Xllt
Other Cervical sympathetic trunk, modified radical neck dissection
IX. X, Xllt
Cervical sympathetic
saphenous vein interposition graft
(preoperatlvely)
Arteriotomy with primary closure Resection with
8
saphenous vein interposition graft Arteriotomy with primary closure
Li
w
Resection with saphenous vein
interposition graft Internal carotid resection and ligation
9
10
trunkt X, XII
indicates resection and
fPreoperative
cranial
nerve
Arteriotomy with primary closure ligation performed. deficit.
^Patient with staged bilateral carotid body tumor surgery. L and R indicate left and right, respectively. Table
3.—Postoperative Carotid Vessel Patency* Internal Carotid Artery
Patient No.
Secondary
External Carotid Artery Occlusion
Surgery
(preoperatlvely)
Resection with saphenoid vein interposition graft
Occlusion
Occlusion Prior to Surgery
Radiation
Arteriotomy with primary closure Resection with saphenoid vein interposition graft
8Lt
Rt
Arteriotomy with primary closure Resection with saphenoid vein
interposition graft
Resection and ligation
15
Arteriotomy with primary closure
*x indicates occlusion present. tPatient with staged bilateral carotid body
tumor surgery. L and R indicate left and
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right, respectively.
-DiagnosisCarotid Body Tumors Bilateral
Unilateral
I
Small/Moderate/Large
Small/Moderate Small/Moderate
Small/Moderate
Large
Large Large
Staged Surgery
Staged Surgery
Staged Surgery
Surgery
vs
Radiation Treatment algorithm.
ious and
typically consists of a pain¬ less, pulsatile neck mass at the angle of the mandible. Medial displacement of the lateral pharyngeal wall and cra¬ nial nerve deficits are seen later in the disease. Headache, excessive perspira¬ tion, palpitations, pallor, and nausea
suggest
a
catecholamine-secreting ca¬
rotid body,6 and when these symptoms are present, the levels of urine vanillylmandelic acid should be tested. The reported incidence of multicentric paragangliomas varies from 10% in the nonfamilial type to as high as 50% in the familial variety.7 Multiple tumors occurred in this series in 47%; only one of the seven patients had a family history of paragangliomas. Many patients, however, were referred for management of bilateral carotid body tumors after diagnosis else¬ where. Patients are commonly examined initially with a contrast-enhanced
computed tomographic scan or mag¬ netic resonance imaging. Fine-needle aspiration is not useful in the evalua¬ tion of suspected vascular tumors, and
further evaluation should include bi¬ lateral carotid angiography. Widening of the carotid bifurcation with a welldefined tumor blush is virtually pathognomonic. Bilateral studies al¬ low detection of multicentric disease.8 In this study, intra-arterial and intra¬ venous digital subtraction angiogra¬ phies were equally reliable in the di¬ agnosis of vascular tumors. However, intra-arterial studies carry a risk of transient ischemie event.5 Attempts at classification of tumor size and involvement of surrounding
neurovascular structures have been based on the pathologic specimens.9·10 Such classification systems predict morbidity on the basis of surgical find¬ ings, but preoperatlvely they do not predict the likelihood of vascular in¬ volvement. A more recently proposed classification predicts surgical out¬ come on the basis of angiography as follows: stage I, no evidence of carotid stenosis; stage II, narrowing of the ex¬ ternal carotid artery; and stage III, stenosis of the internal carotid artery.5 In this study, the classification scheme was not effective, because angiography failed to predict vessel stenosis or invasion documented at surgery. It is generally accepted that small carotid body tumors should be resect¬ ed. Those lesions not encircling the ca¬ rotid artery are not firmly adherent and can be resected with minimal mor¬ bidity or mortality.8 Early interven¬ tion in carotid body tumors can pre¬ vent neurovascular complications as¬ sociated with long-standing disease.8 Radiation therapy has been reported to yield excellent control for large ca¬ rotid body tumors,3'4 and even if it fails to eradicate the tumor, there is no symptomatic progression of disease.4 Other authors8 argue against the use of radiation therapy, because paragan¬ gliomas are biologically radioresistant and because significant morbidity is associated with radiation therapy. The use of radiation therapy for benign le¬ sions must be questioned when surgi¬ cal options with low morbidity exist. In the one patient in this series treated with radiation therapy for a carotid body tumor and an unresectable medi-
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astinal chemodectoma, no evidence of disease progression was found at 10 months. The rare malignant variants have regional or distant metastatic disease that necessitates postopera¬ tive radiation therapy." A systematic surgical approach has been described by Lees et al9 and Shamblin et al,10 including wide surgi¬ cal exposure; proximal and distal vascular control; identification and preservation of neural structures; subadventitial tumor dissection; pre¬ servation of the common and internal carotid arteries with external carotid sacrifice, if necessary; and vascular shunting during grafting, if necessary. Neural structures are resected only when they are encased in tumor. An uncontrolled hemorrhage may result from intratumor dissection. Meticu¬ lous subadventitial resection facili¬ tates tumor removal.912 Ligation and division of the external carotid artery facilitates resection in large lesions. Similarly, advanced lesions with oblit¬ eration of adventitial planes place the common and internal carotid arteries at risk of injury. When possible, a simple arteriotomy should be repaired primarily. If internal carotid artery resection is necessary, the use of a shunt decreases the risk of cerebral infarction. Primary anastomosis is performed when no tension exists at the anastomosis site. Larger resection requires vascular grafting, in which a saphenous vein interposition graft is preferred over synthetic material. Intravenous digital subtraction an¬ giography was employed to determine the patency of the carotid artery anas¬ tomosis in the postoperative period, and if its quality is good, sensitivity and specificity for stenosis or occlusion are greater than 90% when compared with those achieved by standard angiography.1314 In addition, intrave¬ nous digital subtraction angiography is less expensive and less invasive than standard arteriography. More re¬ cently, duplex scanning has been found to be very reliable in determin¬ ing carotid patency noninvasively. All patients with primary repair had patent carotid arteries; however, two of the three saphenous vein interposi¬ tion grafts used were occluded. One additional patient had ligation of the
internal carotid artery at the skull base. There were no symptoms of cere¬ bral ischemia in any patient. Patency of the circle of Willis obviously pro¬ vided compensation for the inter¬ rupted carotid blood flow. Patients with bilateral carotid body tumors who have had carotid thrombosis as a result of the initial unilateral resec¬ tion are potentially at high risk for ce¬ rebral ischemia during the operation for the remaining contralateral tumor. In two of the three patients referred with this entity, the carotid arterial
system was carefully preserved during the resection of the second tumor. The third patient received radiation ther¬ apy.
Neural structures that are at risk include the glossopharyngeal, vagus, and hypoglossal nerves, the cervical sympathetic nerves, and the marginal mandibular branch of the facial nerve. Only in those rare circumstances when a radical neck dissection is performed as a part of an en bloc resection is the accessory nerve at risk. Preoperative paresis or paralysis of cranial nerves suggests direct tumor invasion. These structures are at high risk for sacrifice during resection. Postoperative pare¬ sis or paralysis typically resolves if the nerve is preserved during surgery.9 The major morbidity is associated with vocal cord dysfunction and the subsequent risk of aspiration second¬ ary to vagus
or
recurrent
laryngeal
damage. In some instances, tem¬ porary (Gelfoam) or permanent (Te¬ flon) vocal cord injection will be neces¬ sary for the improvement of voice or control of aspiration.15 The following treatment algorithm for carotid body tumors is suggested by these data (Figure). A patient with nerve
unilateral lesion and without serious associated risk factors should be con¬ sidered a surgical candidate, regard¬ less of tumor size. However, tumor size determines management in bilateral disease. With bilateral, small tumors, staged operations should be performed a few weeks apart. Careful evaluation for postoperative cranial nerve deficits and for carotid artery patency is es¬ sential prior to the operation for the second contralateral tumor, as detec¬ tion of any of these complications should dictate a more conservative apa
to the second side. Two approaches exist when there is a difference in size between the tu¬ mors, and each case must be individu¬ alized since good arguments can be made for approaching either the smaller or the larger tumor first. Re¬ section of the smaller tumor first is probably the safest approach since it can be performed with minimal com¬ plications. However, in the unlikely occurrence of carotid thrombosis or major cranial nerve deficit, only nonoperative management of the second large tumor would permit the avoid¬ ance of the serious risk of bilateral ca¬ rotid or cranial nerve complications. Some of the larger tumors, however, are symptomatic from their bulk alone and, therefore, a "forced" conservative approach in this setting makes this al¬ ternative less acceptable. The other approach entails the resection of the larger tumor first, which generally is associated with a higher incidence of carotid and cranial nerve complica¬ tions. Although carotid thrombosis or cranial nerve deficits on the side of the larger lesion do not preclude resection of the contralateral smaller lesion, they make the small-percent risk much more significant. Bilateral large tumors place both carotid arteries and cranial nerves at higher risk. In elderly patients who are
proach
operative candidates, radiation therapy should be considered. In younger patients, surgery should be performed on the side of the carotid artery supplying the nondominant ce¬ rebral cortex. Thus, should carotid poor
thrombosis occur, the dominant arte¬ rial supply may be treated with radia¬ tion therapy. In summary, surgical management of carotid body tumors remains the preferred treatment. A high index of suspicion is essential in early diagno¬ sis; a pulsatile, solitary mass at the angle of the j aw is suggestive of a ca¬ rotid body tumor. Delayed diagnosis allows tumor enlargement with in¬ creased risk to neurovascular struc¬ tures. Contrast-enhanced computed
tomography or magnetic resonance imaging identifies a vascular tumor, and bilateral angiography is used for preoperative evaluation. A multidisci¬ plinary approach with cooperation be-
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tween otolaryngology-head and neck surgeons and vascular surgeons helps to minimize complications. Surgical
management includes identification
and preservation of vascular and neu¬ ral structures adjacent to the carotid body tumor, and dissection in the sub¬ adventitial plane facilitates tumor re¬ section. Primary repair of arteriotomies or shunting with saphenous vein grafts is preferred when carotid arte¬ riotomy is unavoidable, and postoper¬ ative intravenous digital subtraction angiography assesses the carotid ar¬ tery patency. Small or moderate tu¬ mors can be resected with little mor¬ bidity, and large tumors place neu¬ rovascular structures at greater, but acceptable, risk. References 1. Saldana MJ, Salem LE, Travezan R. High altitude hypoxia and chemodectomas. Hum
Physiol. 1973;4:251-263. 2. Arias-Stella J, Valcarcei J. Chief cell hyperplasia in the human carotid body at high altitudes. Hum Physiol. 1976;7:361-373. 3. Million RR, Cassisi NJ. Chemodectomas (glomus body tumors). In: Million RR, Cassisi NJ, eds. Management of Head and Neck Cancer: A Multidisciplinary Approach. Philadelphia, Pa: JB Lipincott Co; 1985. 4. Lybeert MLM, Van Andrei JG, Eijkeboom WMH, DeJong PC, Knegt P. Radiotherapy of paragangliomas. Clin Otolaryngol. 1984;9:105-109. 5. Rodriguez-Cuevas H, Lau I, Rodriguez HP. High-altitude paragangliomas: diagnostic and therapeutic considerations. Cancer. 1986;57:672\x=req-\ 676. 6. Schwaber MK, Glasscock ME, Nissen AJ, Jackson CG, Smith PG. Diagnosis and management of catecholamine secreting glomus tumors.
Laryngoscope. 1984;94:1008-1015. 7. Van Baars F, Van den Broek P, Cremers C,
Veldman J. Familial non-chromaffinic paragan-
gliomas (glomus tumors): clinical aspects. Laryngoscope. 1981;91:988-996. 8. Sykes JM, Ossoff RH. Paragangliomas of the head and neck. Otolaryngol Clin North Am. 1986;19:755-766.
9. Lees CD, Levine HL, Beven EG, Tucker HM. Tumors of the carotid body. Am J Surg. 1981; 142:362-365. 10. Shamblin WR, Remine WH, Sheps SG, Harrison SSG. Carotid body tumors. Am J Surg.
1971;122:732-739. 11. Zbaren P, Lehmann W. Carotid body paraganglioma with metastases. Laryngoscope. 1985;95:450-454. 12. Sobol SM, Freeman R, Thawley S, Little J, Beven E. Management of inadvertent injury to the carotid artery during head and neck surgery. Head Neck Surg. 1982;4:475-482. 13. Paushter DM, LaValley A, Rosenbloom SA. Radiologic evaluation of the asymptomatic carotid bruit. Cleve Clin Q. 1986;53:367-372. 14. Buonocore E, Meany TF, Borkowski GP.
Digital subtraction angiography of the abdominal Radiology. 1981;139:281\x=req-\
aorta and renal arteries.
286. 15. Tucker HM.
Laryngeal paralysis: etiology
and management. In: English GM, ed. Otolaryngology. Hagerstown, Md: Harper & Row Inc; 1981.
Body Tumors
Dennis H. Kraus, MD; Bruce M. Sterman, MD; Albert G. Hakaim, MD; Edwin G. Howard L. Levine, MD; Benjamin G. Wood, MD; Harvey M. Tucker, MD
\s=b\ The surgical management of carotid body tumors requires identification and preservation of neural and vascular structures without compromising resection of the neoplasm. Fifteen patients were examined and treated for carotid body tumors at the Cleveland (Ohio) Clinic Foundation from 1979 through 1987. The benchmark of diagnosis is bilateral carotid angiography. When neural structures are free of tumor, meticulous dissection facilitates their preservation. Large tumor size
increases risk for arterial resection necessitating reconstruction. The use of a vascular shunt minimizes the risk of cerebral ischemia. Postoperative intravenous digital subtraction angiography allows for evaluation of arterial repair. A retrospective review of 15 carotid body tumor resections performed in 14 patients revealed no evidence of tumor recurrence, no mortality associated with surgical intervention, no postoperative cerebrovascular accident, and limited morbidity associated with unavoidable sacrifice of neural elements. (Arch Otolaryngol Head Neck Surg.
1990;116:1384-1387)
Carotid bodyparagangliomas arising
tumors are nonchromaffin at the bifurcation of the common ca¬ rotid artery. The causes of carotid body tumors in high-altitude dwellers who have hyperplasia of the
chemosensory organ secondary to chronic hypoxia have been well described.1-2 No satisfactory explana¬ tion exists for the
occurrence
of these
tumors at lower elevations. It is gen¬ erally accepted that surgery is the pri-
Accepted for publication June 2,1990. From the Departments of Otolaryngology and
Communicative Disorders (Drs Kraus, Sterman, Levine, Wood, and Tucker) and Vascular Surgery (Drs Hakaim and Beven), The Cleveland (Ohio) Clinic Foundation. Presented at the 1989 Annual Meeting of the American Society of Head and Neck Surgeons, San Francisco, Calif, April 6, 1989. Reprint requests to Department of Otolaryngology and Communicative Disorders, The Cleveland Clinic Foundation, 9500 Euclid Ave, Cleveland, OH 44195-5034 (Dr Tucker).
mary mode of
Beven, MD;
therapy; however,
sev¬
eral studies describe the use of radia¬ tion therapy for these benign
neoplasms.34 Preoperative angio¬ graphie evaluation, surgical manage¬ ment of arterial and neurologic struc¬ tures during tumor resection, and sur¬ gical complications are examined retrospectively in this report. PATIENTS AND METHODS From June 1979 through June 1987, 15 patients were treated for carotid body tu¬ mors at the Cleveland (Ohio) Clinic Foun¬ dation. Three patients were referred for treatment of a second carotid body tumor after resection of the contralateral side performed at another institution. All 15 patients underwent complete head and neck examination and digital subtraction an¬ giography (either intra-arterial or intrave¬ nous
study).
Fourteen of these patients were treated surgically, and one patient was given radi¬ ation therapy (45 Gy) because he had un¬ dergone incomplete resection of his tumor before referral to the Cleveland Clinic Foundation and was found to have a second carotid body tumor, as well as an inopera¬ ble mediastinal chemodectoma. A similar operative approach was used in all patients. The common, internal, and ex¬ ternal carotid arteries and the hypoglossal and vagus nerves were identified and con¬ trolled prior to the resection of the carotid body tumor. Transection of the external carotid artery improved access to large tu¬ mors, and subadventitial dissection facili¬ tated removal of carotid body tumors. How¬ ever, it resulted in an increased risk of in¬ advertent entry into the carotid artery. Management of a simple arterial laceration consisted of controlling the bleeding by gentle direct finger pressure over the open¬ ing while the patient was given 7500 U of sodium heparin. After the temporary ap¬ plication of atraumatic vascular clamps, the laceration was primarily repaired. More extensive arterial injuries required saphenous vein graft replacement, using an indwelling Heyer-Schulte-Sundt shunt to maintain cerebral perfusion. Postoperative intravenous digital subtraction angiogra-
Downloaded From: http://archotol.jamanetwork.com/ by a New York University User on 06/09/2015
phy
was
used to evaluate arterial repair. also examined for post¬
patients were operative cranial The
nerve
deficit
or
cere-
brovascular accident.
RESULTS
The patients ranged in age from 24 to 72 years (mean age, 45 years). There were 11 women and four men. Four¬ teen were white, and one was Hispanic (the only case from a high-altitude
geographic location). Multiple paragangliomas were found in seven pa¬ tients (Table 1). Symptoms included neck mass (all 15 patients), tenderness (two patients), and dysphagia with as¬ piration (one patient). On physical ex¬ amination, there were two patients with neck bruits, two patients with cranial nerve deficits, and one patient with lateral pharyngeal wall displace¬ ment.
Angiography showed preoperative tumor-induced occlusion of the exter¬ nal carotid artery in one patient and increased widening between the inter¬ nal and external carotid arteries in four patients. In the three patients re¬ ferred to the Cleveland Clinic Founda¬ tion after resection of a carotid body tumor, an occlusion of the internal ca¬ rotid artery was found on the previ¬ ously operated on side. Fifteen carotid body tumors were resected in 14 patients (one patient had staged bilateral surgery). One patient also required a modified radical neck dissection for resection of a recurrent carotid body tumor (previous excision was performed 12 years earlier). Com¬ plete excision of the tumor was felt to have been accomplished in all cases. In one patient with bilateral carotid body tumors, the contralateral tumor was not operated on after the initial proce¬ dure required ligation of the internal carotid artery due to uncontrolled bleeding at the skull base. The other patient, treated nonsurgically, re¬ ceived radiation therapy (45 Gy). None
of the
surgical patients has had tumor within a mean follow-up period of 36 months (range, 8 to 85 months).
Table
recurrence
Vascular or neural structures were sacrificed either completely or in part in 10 of the 15 procedures to accom¬ plish complete tumor resection. Resec¬ tion and ligation of the internal ca¬ rotid artery were required in one case. Primary closure of an inadvertent in¬ ternal carotid arteriotomy was accom¬ plished in three cases, while three oth¬ ers required saphenous vein interposi¬ tion grafts to repair the internal carotid resection. The external carotid artery was resected and ligated in six cases. Surgical treatment of vascular and neural structures around the ca¬ rotid body tumors and postoperative assessment of the carotid arterial sys¬ tem are summarized in Tables 2 and 3. Two of the three arteries repaired with saphenous vein interposition grafts oc¬ cluded postoperatively. There were no postoperative cerebrovascular acci¬ dents among the 15 patients who had undergone surgeries. However, two of the patients referred after operations elsewhere had suffered postoperative cerebrovascular accidents. Both pa¬ tients' neurologic deficits resolved prior to treatment at the Cleveland Clinic Foundation. Two of four patients were treated for vagus nerve paralysis with true vocalcord Teflon injection. Voice was im¬ proved in those patients, and there was no evidence of aspiration. One patient did not require treatment as the con¬ tralateral vocal cord provided ade¬ quate compensation. The only patient to present with preoperative vocal cord paralysis had adequate compensation in the immediate postoperative period. That patient, however, developed a hoarse voice, dysphagia, and aspira¬ tion with pneumonia over time and is presently being examined for addi¬ tional treatment. COMMENT
High index of suspicion is important in the diagnosis of carotid body tumor. Incorrect diagnoses include tubercu¬ lous adenitis, thyroid carcinoma mé¬ tastases, branchial cysts, tonsillar neoplasms, or parotid gland tumors.5 The onset of symptoms is often insid-
1.—Multiple Paragangliomas*
Carotid Body Tumor Glomus
Patient No.
Unilateral
Bilateral
Tympanicum
Other Sites Mediastinal Intratracheal
Aryepiglottic
fold
14
indicates íesion shown at head of table column is present in
Table 2. —
patient.
Involvement of Vascular and Neural Structures in Carotid Body Tumor Surgery
External Carotid Patient
No.
Artery Resection and
Internal Carotid
Ligation*
Cranial Nerve
Artery Surgery
Sacrifice
Resection with
IX,t X.t Xllt
Other Cervical sympathetic trunk, modified radical neck dissection
IX. X, Xllt
Cervical sympathetic
saphenous vein interposition graft
(preoperatlvely)
Arteriotomy with primary closure Resection with
8
saphenous vein interposition graft Arteriotomy with primary closure
Li
w
Resection with saphenous vein
interposition graft Internal carotid resection and ligation
9
10
trunkt X, XII
indicates resection and
fPreoperative
cranial
nerve
Arteriotomy with primary closure ligation performed. deficit.
^Patient with staged bilateral carotid body tumor surgery. L and R indicate left and right, respectively. Table
3.—Postoperative Carotid Vessel Patency* Internal Carotid Artery
Patient No.
Secondary
External Carotid Artery Occlusion
Surgery
(preoperatlvely)
Resection with saphenoid vein interposition graft
Occlusion
Occlusion Prior to Surgery
Radiation
Arteriotomy with primary closure Resection with saphenoid vein interposition graft
8Lt
Rt
Arteriotomy with primary closure Resection with saphenoid vein
interposition graft
Resection and ligation
15
Arteriotomy with primary closure
*x indicates occlusion present. tPatient with staged bilateral carotid body
tumor surgery. L and R indicate left and
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right, respectively.
-DiagnosisCarotid Body Tumors Bilateral
Unilateral
I
Small/Moderate/Large
Small/Moderate Small/Moderate
Small/Moderate
Large
Large Large
Staged Surgery
Staged Surgery
Staged Surgery
Surgery
vs
Radiation Treatment algorithm.
ious and
typically consists of a pain¬ less, pulsatile neck mass at the angle of the mandible. Medial displacement of the lateral pharyngeal wall and cra¬ nial nerve deficits are seen later in the disease. Headache, excessive perspira¬ tion, palpitations, pallor, and nausea
suggest
a
catecholamine-secreting ca¬
rotid body,6 and when these symptoms are present, the levels of urine vanillylmandelic acid should be tested. The reported incidence of multicentric paragangliomas varies from 10% in the nonfamilial type to as high as 50% in the familial variety.7 Multiple tumors occurred in this series in 47%; only one of the seven patients had a family history of paragangliomas. Many patients, however, were referred for management of bilateral carotid body tumors after diagnosis else¬ where. Patients are commonly examined initially with a contrast-enhanced
computed tomographic scan or mag¬ netic resonance imaging. Fine-needle aspiration is not useful in the evalua¬ tion of suspected vascular tumors, and
further evaluation should include bi¬ lateral carotid angiography. Widening of the carotid bifurcation with a welldefined tumor blush is virtually pathognomonic. Bilateral studies al¬ low detection of multicentric disease.8 In this study, intra-arterial and intra¬ venous digital subtraction angiogra¬ phies were equally reliable in the di¬ agnosis of vascular tumors. However, intra-arterial studies carry a risk of transient ischemie event.5 Attempts at classification of tumor size and involvement of surrounding
neurovascular structures have been based on the pathologic specimens.9·10 Such classification systems predict morbidity on the basis of surgical find¬ ings, but preoperatlvely they do not predict the likelihood of vascular in¬ volvement. A more recently proposed classification predicts surgical out¬ come on the basis of angiography as follows: stage I, no evidence of carotid stenosis; stage II, narrowing of the ex¬ ternal carotid artery; and stage III, stenosis of the internal carotid artery.5 In this study, the classification scheme was not effective, because angiography failed to predict vessel stenosis or invasion documented at surgery. It is generally accepted that small carotid body tumors should be resect¬ ed. Those lesions not encircling the ca¬ rotid artery are not firmly adherent and can be resected with minimal mor¬ bidity or mortality.8 Early interven¬ tion in carotid body tumors can pre¬ vent neurovascular complications as¬ sociated with long-standing disease.8 Radiation therapy has been reported to yield excellent control for large ca¬ rotid body tumors,3'4 and even if it fails to eradicate the tumor, there is no symptomatic progression of disease.4 Other authors8 argue against the use of radiation therapy, because paragan¬ gliomas are biologically radioresistant and because significant morbidity is associated with radiation therapy. The use of radiation therapy for benign le¬ sions must be questioned when surgi¬ cal options with low morbidity exist. In the one patient in this series treated with radiation therapy for a carotid body tumor and an unresectable medi-
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astinal chemodectoma, no evidence of disease progression was found at 10 months. The rare malignant variants have regional or distant metastatic disease that necessitates postopera¬ tive radiation therapy." A systematic surgical approach has been described by Lees et al9 and Shamblin et al,10 including wide surgi¬ cal exposure; proximal and distal vascular control; identification and preservation of neural structures; subadventitial tumor dissection; pre¬ servation of the common and internal carotid arteries with external carotid sacrifice, if necessary; and vascular shunting during grafting, if necessary. Neural structures are resected only when they are encased in tumor. An uncontrolled hemorrhage may result from intratumor dissection. Meticu¬ lous subadventitial resection facili¬ tates tumor removal.912 Ligation and division of the external carotid artery facilitates resection in large lesions. Similarly, advanced lesions with oblit¬ eration of adventitial planes place the common and internal carotid arteries at risk of injury. When possible, a simple arteriotomy should be repaired primarily. If internal carotid artery resection is necessary, the use of a shunt decreases the risk of cerebral infarction. Primary anastomosis is performed when no tension exists at the anastomosis site. Larger resection requires vascular grafting, in which a saphenous vein interposition graft is preferred over synthetic material. Intravenous digital subtraction an¬ giography was employed to determine the patency of the carotid artery anas¬ tomosis in the postoperative period, and if its quality is good, sensitivity and specificity for stenosis or occlusion are greater than 90% when compared with those achieved by standard angiography.1314 In addition, intrave¬ nous digital subtraction angiography is less expensive and less invasive than standard arteriography. More re¬ cently, duplex scanning has been found to be very reliable in determin¬ ing carotid patency noninvasively. All patients with primary repair had patent carotid arteries; however, two of the three saphenous vein interposi¬ tion grafts used were occluded. One additional patient had ligation of the
internal carotid artery at the skull base. There were no symptoms of cere¬ bral ischemia in any patient. Patency of the circle of Willis obviously pro¬ vided compensation for the inter¬ rupted carotid blood flow. Patients with bilateral carotid body tumors who have had carotid thrombosis as a result of the initial unilateral resec¬ tion are potentially at high risk for ce¬ rebral ischemia during the operation for the remaining contralateral tumor. In two of the three patients referred with this entity, the carotid arterial
system was carefully preserved during the resection of the second tumor. The third patient received radiation ther¬ apy.
Neural structures that are at risk include the glossopharyngeal, vagus, and hypoglossal nerves, the cervical sympathetic nerves, and the marginal mandibular branch of the facial nerve. Only in those rare circumstances when a radical neck dissection is performed as a part of an en bloc resection is the accessory nerve at risk. Preoperative paresis or paralysis of cranial nerves suggests direct tumor invasion. These structures are at high risk for sacrifice during resection. Postoperative pare¬ sis or paralysis typically resolves if the nerve is preserved during surgery.9 The major morbidity is associated with vocal cord dysfunction and the subsequent risk of aspiration second¬ ary to vagus
or
recurrent
laryngeal
damage. In some instances, tem¬ porary (Gelfoam) or permanent (Te¬ flon) vocal cord injection will be neces¬ sary for the improvement of voice or control of aspiration.15 The following treatment algorithm for carotid body tumors is suggested by these data (Figure). A patient with nerve
unilateral lesion and without serious associated risk factors should be con¬ sidered a surgical candidate, regard¬ less of tumor size. However, tumor size determines management in bilateral disease. With bilateral, small tumors, staged operations should be performed a few weeks apart. Careful evaluation for postoperative cranial nerve deficits and for carotid artery patency is es¬ sential prior to the operation for the second contralateral tumor, as detec¬ tion of any of these complications should dictate a more conservative apa
to the second side. Two approaches exist when there is a difference in size between the tu¬ mors, and each case must be individu¬ alized since good arguments can be made for approaching either the smaller or the larger tumor first. Re¬ section of the smaller tumor first is probably the safest approach since it can be performed with minimal com¬ plications. However, in the unlikely occurrence of carotid thrombosis or major cranial nerve deficit, only nonoperative management of the second large tumor would permit the avoid¬ ance of the serious risk of bilateral ca¬ rotid or cranial nerve complications. Some of the larger tumors, however, are symptomatic from their bulk alone and, therefore, a "forced" conservative approach in this setting makes this al¬ ternative less acceptable. The other approach entails the resection of the larger tumor first, which generally is associated with a higher incidence of carotid and cranial nerve complica¬ tions. Although carotid thrombosis or cranial nerve deficits on the side of the larger lesion do not preclude resection of the contralateral smaller lesion, they make the small-percent risk much more significant. Bilateral large tumors place both carotid arteries and cranial nerves at higher risk. In elderly patients who are
proach
operative candidates, radiation therapy should be considered. In younger patients, surgery should be performed on the side of the carotid artery supplying the nondominant ce¬ rebral cortex. Thus, should carotid poor
thrombosis occur, the dominant arte¬ rial supply may be treated with radia¬ tion therapy. In summary, surgical management of carotid body tumors remains the preferred treatment. A high index of suspicion is essential in early diagno¬ sis; a pulsatile, solitary mass at the angle of the j aw is suggestive of a ca¬ rotid body tumor. Delayed diagnosis allows tumor enlargement with in¬ creased risk to neurovascular struc¬ tures. Contrast-enhanced computed
tomography or magnetic resonance imaging identifies a vascular tumor, and bilateral angiography is used for preoperative evaluation. A multidisci¬ plinary approach with cooperation be-
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tween otolaryngology-head and neck surgeons and vascular surgeons helps to minimize complications. Surgical
management includes identification
and preservation of vascular and neu¬ ral structures adjacent to the carotid body tumor, and dissection in the sub¬ adventitial plane facilitates tumor re¬ section. Primary repair of arteriotomies or shunting with saphenous vein grafts is preferred when carotid arte¬ riotomy is unavoidable, and postoper¬ ative intravenous digital subtraction angiography assesses the carotid ar¬ tery patency. Small or moderate tu¬ mors can be resected with little mor¬ bidity, and large tumors place neu¬ rovascular structures at greater, but acceptable, risk. References 1. Saldana MJ, Salem LE, Travezan R. High altitude hypoxia and chemodectomas. Hum
Physiol. 1973;4:251-263. 2. Arias-Stella J, Valcarcei J. Chief cell hyperplasia in the human carotid body at high altitudes. Hum Physiol. 1976;7:361-373. 3. Million RR, Cassisi NJ. Chemodectomas (glomus body tumors). In: Million RR, Cassisi NJ, eds. Management of Head and Neck Cancer: A Multidisciplinary Approach. Philadelphia, Pa: JB Lipincott Co; 1985. 4. Lybeert MLM, Van Andrei JG, Eijkeboom WMH, DeJong PC, Knegt P. Radiotherapy of paragangliomas. Clin Otolaryngol. 1984;9:105-109. 5. Rodriguez-Cuevas H, Lau I, Rodriguez HP. High-altitude paragangliomas: diagnostic and therapeutic considerations. Cancer. 1986;57:672\x=req-\ 676. 6. Schwaber MK, Glasscock ME, Nissen AJ, Jackson CG, Smith PG. Diagnosis and management of catecholamine secreting glomus tumors.
Laryngoscope. 1984;94:1008-1015. 7. Van Baars F, Van den Broek P, Cremers C,
Veldman J. Familial non-chromaffinic paragan-
gliomas (glomus tumors): clinical aspects. Laryngoscope. 1981;91:988-996. 8. Sykes JM, Ossoff RH. Paragangliomas of the head and neck. Otolaryngol Clin North Am. 1986;19:755-766.
9. Lees CD, Levine HL, Beven EG, Tucker HM. Tumors of the carotid body. Am J Surg. 1981; 142:362-365. 10. Shamblin WR, Remine WH, Sheps SG, Harrison SSG. Carotid body tumors. Am J Surg.
1971;122:732-739. 11. Zbaren P, Lehmann W. Carotid body paraganglioma with metastases. Laryngoscope. 1985;95:450-454. 12. Sobol SM, Freeman R, Thawley S, Little J, Beven E. Management of inadvertent injury to the carotid artery during head and neck surgery. Head Neck Surg. 1982;4:475-482. 13. Paushter DM, LaValley A, Rosenbloom SA. Radiologic evaluation of the asymptomatic carotid bruit. Cleve Clin Q. 1986;53:367-372. 14. Buonocore E, Meany TF, Borkowski GP.
Digital subtraction angiography of the abdominal Radiology. 1981;139:281\x=req-\
aorta and renal arteries.
286. 15. Tucker HM.
Laryngeal paralysis: etiology
and management. In: English GM, ed. Otolaryngology. Hagerstown, Md: Harper & Row Inc; 1981.
