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Radiological Evaluation of Paragangliomas of the Head and Neck 1 Andrew W. Duncan, M.D.,2 Ernest E. Lack, M.D.,3 and Michael F. Deck, M.D. Paragangliomas can be differentiated angiographically from most other tumors in the head and neck by their profuse vascularity; specific classification is based on their position and displacement of adjacent vessels. Subtraction usually aids in diagnosis. In most cases, bilateral carotid angiography should be performed, since the ipsilateral carotid artery may have to be ligated and an asymptomatic contralateral tumor may also be found during surgery. Studies of multiple vessels will often show an additional blood supply. Computed tomography can demonstrate the tumor's vascular nature and position and is valuable in follow-up after radiation therapy. INDEX TERMS: Cerebral angiography, indications • Head, neoplasms • Neck, neoplasms • Paraganglioma (Carotid bifurcation, paraganglioma, 1[7] .3642; Cerebral vessel, paraganglioma, 1[72] .3642)

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have followed the recommendation of Glennerand Grimley, who advocate classification according to the site of origin rather than relying solely upon the "chromaffin" or "nonchromaffin" status of the tumor (13). Six selected cases are illustrated in Figures 1-6.

ARAGANGLIOMA S of the head and neck are slowly growing, hypervascular tumors which can originate in various sites; of these the most common is the carotid artery bifurcation, followed by the middle ear and the ganglion nodosum of the vagus nerve (24). Less common locations include the larynx (1), orbit (10), nose (15), and aortic arch (25). Regardless of the location, the correct preoperative diagnosis is seldom made; all too often, the true nature of the tumor is established at the time of attempted biopsy or surgical resection, sometimes with disastrous consequences. At Memorial Hospital, for example, the surgical mortality rate among patients undergoing resection of a carotid body paraganglioma prior to 1945 was approximately 50 %, due mainly to ligation of the major cranial vessels (9). Since then, the results of surgical treatment of paragangliomas of the head and neck have been vastly improved. This change can be attributed to advanced techniques of vascular surgery, increased clinical awareness of these tumors, and the increasing use of preoperative selective angiography. Recently we have also used computed tomography (CT) in evaluating these tumors. We have reviewed those cases studied at Memorial Hospital in the past 40 years to determine the value of these contrast procedures in preoperative localization and diagnosis.

P

DISCUSSION

Paragangliomas of the head and neck are rare; at Memorial Hospital they accounted for less than 0.012 % of all specimens seen over a 40-year period (24). Their clinical importance outweighs their rarity, however, since these tumors must be considered in the evaluation of any lateral neck mass, even one located far from the carotid bifurcation. Paragangliomas originate from dispersed paraganglia, closely associated with branchial arch mesodermal derivatives such as the carotid arteries and aortic arch (26). Aorto-pulmonary and carotid body paraganglia have been shown to respond physiologically to changes in blood pH, P02' and pC0 2 (8). This homeostatic chemoreceptor role is reflected morphologically in (a) the hyperplasia of the carotid body (2, 22) and recently vagal body paraganglia (23) noted under hypoxic conditions and (b) the tenfold increase in carotid body paragangliomas among patients living at high altitudes (33). Among paragangliomas of the head and neck, those derived from the carotid body are perhaps the most familiar to radiologists and surgeons alike. Idbohrn in 1951 is credited with the first preoperative angiographicstudy of such tumors (17). Clinically, a carotid body paraganglioma characteristically presents as a slowly growing, painless mass in the side of the neck, near the angle of the mandible (Fig. 1, a and b). CT scans can be useful in delineating both the location and extent of these tumors; moreover,

CASE MATERIAL

From 1937 to 1977, 72 patients with paragangliomas of the head and neck were treated or seen in consultation at Memorial Hospital. Selective angiography was performed in 10 cases (12 tumors), and 4 patients were also studied with CT. More detailed clinical information for 69 of these 72 patients was publlshed previously (24). We

-- 1 From the Departmentsof Radiology (A.W.D., M.F.D.)and Pathology (E.EL), Memorial Sloan-Kettering Cancer Center, New York, N.Y. Received Oct. 13, 1978; accepted and revision requested Jan. 19, 1979; revision received Feb. 12. 2 Present address: Department of Radiology, Peter Bent Brigham Hospital, Boston, Mass. 02115. 3 Present address: Pathology Department, Children's Hospital Medical Center;"300 Longwood Ave., Boston, Mass. 02115. sjh

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Fig . 1. CASE I. Painless mass in a 72-year-old man with a strong family history of carotid body paragangliomas. a. Right common carotid angiogram (lateral projection) shows marked separation of the branches of the internal and external carotid arteries. Hypertrophic nutrient vessels are stretched around the tumor and ramify within it. b. The frontal projection demonstrates a persistent homogeneous tumor blush with residual contrast material outlining the walls of the carotid arteries. Note the slight lateral deviation of the bifurcation. c. CT scan shows an isodense soft-tissue mass lateral to the oropharynx and adjacent to the mandible. The anterior and posterior extent of tumor are demonstrated by arrows. The resected carotid body paraganglioma measured 3.2 cm in diameter.

Fig. 2. CASE II. This 65-year-old woman had a nontender mass in the right neck which was biopsied elsewhere. a. Right carotid angiogram demonstrates the site of ligation of the external carotid artery. Only a few nutrient tumor vessels are apparent. There is marked posterior bowing of the internal carotid artery by tumor . b. Right vertebral angiogram (lateral projection) shows the main residual vascular supply from the vertebral artery branches, which cap the tumor . c. CT scan shows the enhanced tumor in the right retromand ibular region , with medial extension encroaching upon the oropharynx and vertebral body. A 4.0-cm carotid body paraganglioma was resected, but the internal carotid artery was preserved .

because of their vascular nature, marked contrast enhancement can be expected (Fig. 1, c). Carotid body paragangliomas are occasionally associated with the carotid sinus syndrome and if large enough can produce dysphagia (24) . These tumors usually demonstrate some degree of lateral mobility on physical examination; in addition, because of their vascular nature, they may be pulsatile , with a detectable thrill or bruit. Due to their location, both carotid and vagal body paragangliomas must be considered in the differential diagnosis of a lateral neck mass, which includes enlarged lymph nodes due to infectious etiology, malignant lymphoma or metastatic tumor, branchial cleft cyst, carotid artery aneurysm, and neurogenic and salivary gland tumors (24, 27, 34).

Since the carotid body is normally located on the medial aspect of the common carotid artery bifurcation (22), angiography characteristically shows lateral displacement by tumor, with separation of both external and internal branches. Much less commonly, the tumor can displace the bifurcation both anteriorly and medially. Although the major blood supply is from the proximal external carotid artery, the tumor can also be supplied by small adventitial vessels from the internal and external branches. During biopsy or resection, it is sometimes necessary to ligate the external carotid artery (Fig. 2, a). Angiography can demonstrate nutrient vessels arising from the ipsilateral subclavian or vertebral arteries if the tumor has not been completely resected (Fig. 2, b). CT will show displace-

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Fig. 3. CASE III. There was no family history of parangangliomas in this middle-aged man with bilateral neck masses. a. Right carotid angiogram (late arterial phase) shows opac ification of a carotid body tumor and separation of the branches of the internal and external carotid arteries. b. Left common carot id angiogram (early arterial phase) demonstrates a contralateral carotid body paraganglioma containing tortuous nutrient vessels. The patient refused biopsy or resection and was subsequently lost to follow-up .

ment rather than invasion of the soft tissues (Fig. 2, c). In general, the angiographic diagnosis of paraganglioma is established by the profuse vascularity of the tumor;

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tortuous, well-defined nutrient vessels of relatively uniform caliber are seen in the arterial phase and a dense, nonhomogeneous tumor blush or stain in the capillary phase. Tumor vascularity is never as intense or homogeneous as that seen during opacification of an aneurysm , which in any case characteristically washes out during the early capillary phase . A neurogenic tumor, such as a neurilemmoma, can occasionally simulate a paraganglioma and even cause displacement of the bifurcation and separation of the internal and external carotid artery branches; however, these tumors are usually much less vascular, as are enlarged lymph nodes and branchial cleft cysts. The contralateral carotid artery should also be studied angiographically, not only to ensure good cross-flow in case the major ipsilateral vessel has to be I.igated at surgery, but also to detect an asymptomatic contralateral paraganglioma (5) (Fig. 3). Paragangliomas tend to be multiple or bilateral if there is a family history of tumor (18). The familial occurrence of carotid body paragangliomas was first noted by Chase in 1933 (7) and has since been shown to be associated with multiple tumors in 25-33 % of cases (29, 32). Familial paragangliomas other than the carotid body type have also been described (24) . The first angiographic study of a vagal body paraganglioma that we know of was reported by King (21) in 1955, 20 years after the first description of the pathological findings by Stout (36). As arteriography characteristically shows anterior and medial displacement of the external and internal carotid arteries without involvement of the bifurcation (Fig. 4), these tumors tend not to directly involve major vascular structures of the carotid system (3, 38).

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Fig. 4. CASE IV. This 69-year-Old woman presented with progressive hoarseness and a slowly enlarging left neck mass. a. Left common carotid angiogram (lateral projection) shows anterior displacement of the branches of the carotid artery by a hypervascular tumor supplied by hypertrophic nutrient vessels from the external carotid artery. b. Late arterial phase (lateral projection) shows a persistent nonhomogeneous tumor stain without involvement of the carotid bifurcation. c. Frontal view shows lateral bowing of the carotid vessels and early opacification of the nutrient vessels. The branches of the carotid artery are displaced anteriorly and laterally. The resected vagal body paraganglioma measured 4.0 cm in diameter.

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Fig. 5. CASE V. This 56-year-old woman had multiple familial paragangliomas . a. Tomograms of the base of the skull show erosion and widen ing of the jugular foramen on the right (R) due to a jugulotympanic paraganglioma. The adjacent bone shows sclerotic change. A contralateral vagal body paraganglioma is present . but the left jugular foram en is not involved. A carotid body tumor had been exci sed from the left side of the nec k 28 years earlier. b. Right carotid angiogram (lateral view . early arterial phase) using subtraction. Tortuous nutrient vessel s. emanating mainly from the occ ipital arter y. supply a jugulotympanic paragangliom a. An ipsilateral vertebra l angiogram showed additional supply from the meningeal and muscular branche s. c. Front al view. early arte rial phase. The tumo r is local ized to the tymp anomastoid reg ion. d. Left vertebral angiogram (arterial phase) shows tortuous feeding vessels supplying a vagal body paraganglioma . The tumor had been present for 20 years and recent ly produced clinical symptoms of vertigo due to shunting of blood from the vert ebrob asilar artery system . e. CT scan shows an enhanc ed jugulotympanic paragang lioma near the base of the skull on the right. f. CT scan taken at a lower level show s a soft -t issue density in the left ret romandibular area . encroaching on the nasopharyn x. g. After intravenous con trast infusion, there is marked enhancement of the tumor, indicati ng its vasc ular nature .

In our series, the tumor blush was less homogeneous than that of carotid body and jugulotympanic paragangliomas , possibly reflecting the greater degree of sclerosis noted in some vagal body tumors (24). The blood supply is almost exclusively from the external carotid artery; and. unl ike jugulotympanic tumors, vagal body paragangliomas rarely cause erosion or widening of the jugular foramen, although they too can compress the internal jugular vein . This characteristic lack of structural alteration of the

foramen is one of the important findings which distinguish these tumors from jugulotympanic paragangliomas. Late in the course of some vagal body paragangliomas, however, intracranial infiltration via the jugular foramen can prove fatal (24). Vagal body paraganglia normally develop at or just below the ganglion nodosum of the vagus nerve on each side (23). It must be emphasized that the term " vagal body" is a misnomer, since it is composed of multiple paraganglia

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Fig. 6. CASE VI. This 64-year-old woman presented with orbital pain and pulsatile exophthalmos. a. Frontal view shows destruction of the innominate (Bull's) line and the lesser wing of the sphenoid. Biopsy of the orbital mass revealed a nonchromaffin paraganglioma. b. Lateral view (late arterial phase) shows a hypervascular tumor within the orbit, with posterior extension into the middle cranial fossa. Radiation therapy produced a marked decrease in the exophthalmos. c. CT scan through the orbit taken three years later shows residual exophthalmos and a retro-orbital tumor extending into the anterior and middle cranial fossae. The patient is currently alive four years after the initial diagnosis.

distributed at various levels along the cephalic portion of the vagus nerve, usually beneath the perineural sheath. Some paraganglia are located within the jugular foramen, adjacent to the jugular ganglion (23). In contrast to carotid body paragangliomas, therefore, vagal body paragangliomas tend to be located farther cephalad in the neck, near the base of the skull, with medial protrusion into the oropharynx. These tumors are also more frequently associated with cranial nerve palsy and secondary vocal cord paralysis due to involvement of branches of the recurrent laryngeal nerve. By contrast, jugulotympanic paraganglia are found within the adventitia of the bulb of the internal jugular vein and within the middle ear (14). Tumors originating from these paraganglia can elicit a variety of signs and symptoms depending upon their size and location. Those invading the tympanic area can present as a polypoid mass in the middle ear or external auditory canal, causing progressive hearing loss and/or tinnitus (24, 28). If the tumor involves the jugular fossa, several types of cranial nerve palsy can result. Finally, if the tumor extends into the middle cranial fossa from the petrous portion of the temporal bone, the fifth (trigeminal) or sixth (abducens) cranial nerves can be affected. Jugulotympanic paragangliomas can be very difficult to diagnose radiographically, particularly when they are small (30,31). Findings on plain skull radiographs depend on the size and location of the tumor. The jugular foramen may be enlarged or eroded, as shown in one of our patients with multiple familial paragangliomas (Fig. 5, a). The tumor can also involve the middle ear or external auditory canal, causing erosion of the apex of the petrous bone due to

extension into the middle cranial fossa. Care must be taken in interpretation of the plain radiographs, since mastoid air cells and large venous lakes in the petrous apex can mimic a destructive lesion . Normal variation in the size, shape, and symmetry of the jugular foramen may also cause difficulty in interpretation (20,37). In the sigmoid sinus , the shape may be modified by the retromastoid emissary vein, best seen on transoral and oblique views; however, the irregular margins and enlargement of the jugular foramen and destruction of the inferior petrous pyramid (37) leave little doubt as to the pathological nature of the lesion. Hypocycloidal tomography in the frontal projection usually gives valuable information; Stenver's projection may occasionally be necessary to show erosion of the foramen . If the tumor is large, lateral tomograms may show destruction of the corticojugular spine, a spicule of bone common to the anterior margin of the jugular foramen and the posterior margin of the carotid canal. Carotid angiography in jugulotympanic paragangliomas shows the same tumor hypervascularity as at other sites (Fig. 5, b and c) but may be difficult to interpret when the tumor is small (31) . In most cases, the angiographic findings are sufficiently characteristic to make a definitive diagnosis; moreover, this procedure provides accurate information regarding tumor size and position, particularly when intracranial extension is present. Subtraction is helpful in eliminating bony densities. The tympanic branch of the ascending pharyngeal artery and the meningeal branches of the external carotid artery supply the tumor and are often hypertrophic. Selective external injections will demonstrate this vascular supply to best advantage. An additional blood

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supply may arise from the internal carotid and vertebral arteries, along with the meningeal and muscular branches; therefore these vessels should be studied selectively. Again, as with all other tumors deriving their blood supply from one carotid artery, the contralateral vessel should be studied, preferably with cross-compression, in order to detect multiple tumors and demonstrate adequate crossflow in the event that the ipsilateral vessel has to be ligated during surgery (4) (Fig. 5, d). Arteriovenous shunting and retrograde filling of the sigmoid sinus are sometimes seen during the arterial phase and will invariably be shown by subtraction even when the shunt is very small. Large tumors with intracranial extension can displace the anterior inferior cerebellar artery and ipsilateral cerebellopontine angle vessels. Finally, there is usually sufficient opacification of the venous system from the arterial injection to demonstrate compression of the internal jugular vein or even complete occlusion by tumor; but if this is not conclusive, retrograde jugular phlebography can be performed (12). CT scans in our patient with multiple familial paragangliomas showed a markedly enhanced jugulotympanic tumor on the right (Fig. 5, e) and a vagal body paraganglioma on the left (Fig. 5, f and g). In our experience, the orbit is a distinctly uncommon site for a paraganglioma, with the important differential diagnosis on angiography being a metastatic vascular tumor (11). We saw one patient with an orbital paraganglioma (Fig. 6, a and b) who had no other known primary tumor but did have long-standing thyroid enlargement due to nodular goiter. It would be extremely unlikely to have such a large secondary orbital deposit for so long a time (now four years later) without regional lymphadenopathy if the thyroid were indeed the primary site. In this case, CT following radiation therapy obviated repeat cerebral angiography with its attendant risks (Fig. 6, c). These tumors presumably originate from paraganglia located in the vicinity of the ciliary ganglion. Botar and Pribek have described a paraganglionic structure in the orbit of the chimpanzee (6), but very little is currently known about either the existence or location of this tissue in man. Since too few cases of orbital paraganglioma have been reported in the literature, it is premature to speculate meaningfully on prognosis or optimal therapy; however, radiotherapy had a beneficial effect in our patient. Complete surgical resection is the preferred treatment of paragangliomas of the head and neck. While this is feasible with most carotid or vagal body paragangliomas (24), jugulotympanic paragangliomas are extremely difficult to eradicate by surgery alone; Hatfield et al. have advocated a combined approach, consisting of radical mastoidectomy followed by external irradiation (16). The reported malignant potential for jugulotympanic paragangliomas is approximately 4 % (19), but the most important factor in prognosis is the distinct tendency for local recurrence, sometimes after a long period of time. Adjunctive radiation therapy may also be useful in incompletely resected paragangliomas, such as vagal body tumors which tenaciously involve the base of the skull. In a recent

July 1979

review by Kahn, 16 % of vagal body paragangliomas were found to be malignant, with local and/or distant metastases (19). By contrast, the incidence of malignant behavior in carotid body paragangliomas ranges from 2 to 9% (24,34), with Staats et al. reporting a 6 % incidence in their review of 500 tumors (35). With currently available angiographic techniques for accurate preoperative diagnosis, the risk of attempted surgical extirpation of most paragangliomas is minimal compared to their malignant potential. ACKNOWLEDGMENT: We wish to thank Marie DiNitto for typing the manuscript.

REFERENCES 1. Andrews AH Jr: Glomus tumors (nonchromaffin paragangliomas) of the larynx. Case report. Ann Otol Rhinol Laryngol 64: 1034-1036, Dec 1955 2. Arias-Stella J, Valcarcel J: Chief cell hyperplasia in the human carotid body at high altitudes. Physiologic and pathologic significance. Hum Pathol 7:361-373, Jul 1976 3. Bateson EM, Bull T: Two unusual tumours of the chemoreceptor system with angiographic demonstration. Br J Radiol 40: 120-124, Feb 1967 4. van der Borden J: Bilateral non-chromaffin tympano-jugular paraganglioma. J Laryngol Otol 81:445-448, Apr 1967 5. Bosniak MA, Seidenberg B, Rubin IC, et al: Angiographic demonstration of bilateral carotid body tumors. Am J Roentgenol 92:850-854, Oct 1964 6. Botar J, Pribek L: Corpuscule paraganglionnaire dans l'orbite (note prellmlnaire). Ann Anat Pathol 12:227-228, Feb 1935 7. Chase WH: Famial and bilateral tumours of the carotid body. J Pathol Bacteriol 36: 1-12, Jan 1933 8. Dripps RD Jr, Comroe JH Jr: The clinical significance of the carotid and aortic bodies. Am J Med Sci 208:681-694, Nov 1944 9. Farr HW: Carotid body tumors. A thirty year experience at Memorial Hospital. Am J Surg 114:614-619, Oct 1967 10. Fisher ER, Hazard JB: Nonchromaffin paraganglioma of the orbit. Cancer 5:521-524, May 1952 11. Font RL, Ferry AP: Carcinoma metastatic to the eye and orbit. III. A clinicopathologic study of 28 cases metastatic to the orbit. Cancer 38:1326-1335, Sep 1976 12. Gejrot T, Lauren T: Retrograde jugularography in diagnosis of glomus tumours in the jugular region. Acta OtolaryngoI58:191-207, Aug-Sep 1964 13. Glenner GG, Grimley PM: Tumors of the Extra-adrenal Paraganglion System (Including Chemoreceptors). Atlas of Tumor Pathology, Series 2, Fasc 9. Washington DC, AFIP, 1974 14. Guild SR: The glomus jugulare, a nonchromaffin paraganglion, in man. Ann Otol Rhinol Laryngol 62:1045-1071, Dec 1953 15. Harkins WB: Nonchromaffin paraganglioma of the nasal sinuses. Laryngoscope 67:246-259, Mar 1957 16. Hatfield PM, James AE, Schulz MD: Chemodectomas of the glomus jugulare. Cancer 30: 1164-1168, Nov 1972 17. Idbohrn H: Angiographical diagnosis of carotid body tumours. Acta Radiol 35: 115-123, Feb-Mar 1951 18. Jacobs JB, Chretien PB, Sugarbaker E, et al: Arteriographic discovery of a small contralateral carotid body tumor. Radiology 93:837-838, Oct 1969 19. Kahn LB: Vagal body tumor (nonchromaffin paraganglioma, chemodectoma, and carotid body-like tumor) with cervical lymph node metastasis and familial association. Ultrastructural study and review. Cancer 38:2367-2377, Dec 1976 20. Kim SK, Capp MP: Jugular foramen and early roentgen diagnosis of glomus jugulare tumor. Am J Roentgenol 97:597-600, Jul 1966 21. King AB: Successful removal of a nonchromaffin paraganglioma of a vagus nerve. Am Surg 21:170-176, Feb 1955 22. Lack EE: Carotid body hypertrophy in patients with cystic fi-

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brosis and cyanotic congenital heart disease. Hum Pathol 8:39-51, Jan 1977 23. Lack EE: Hyperplasia of vagal and carotid body paraganglia in patients with chronic hypoxemia. Am J Pathol 91:497-516, Jun

1978 24.

Lack EE, Cubilla AL, Woodruff JM, et al: Paragangliomas of the head and neck region: a clinical study of 69 patients. Cancer 39:397-409, Feb 1977 25. Lack EE, Stillinger RA, Colvin DB, et al: Aortico-pulmonary paraganglioma. Report of a case with ultrastructural study and review of the literature. Cancer 43:269-278, Jan 1979 26. Lattes R: Nonchromaffin paraganglioma of ganglion nodosum, carotid body, and aortic-arch bodies. Cancer 3:667-694, Jul 1950 27. Medellin H, Wallace S: Angiography in neoplasms of the head and neck. Radiol Clin North Am 8:307-321, Dec 1970 28. Oberman HA, Holtz F, Sheffer LA, et al: Chemodectomas (nonchromaffin paragangliomas) of the head and neck. A clinicopathologic study. Cancer 21:838-851, May 1968 29. Pratt LW: Familial carotid body tumors. Arch Otolaryngol 97:334-336, April 1973 30. Rice RP, Holman CB: Roentgenographic manifestations of tumors of the glomus jugulare (chemodectoma). Am J Roentgenol 89:1201-1208, Jun 1963

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31. Rucker TN: Radiology of glomus jugulare tumors in the temporal bone. Radiology 81:807-816, Nov 1963 32. Rush BF Jr: Familial bilateral carotid body tumors. Ann Surg 157:633-636, Apr 1963 33. Saldana MJ, Salem LE, Travezan R: High altitude hypoxia and chemodectomas. Hum Pathol 4:251-263, Jun 1973 34. Shamblin WR, ReMine WH, Sheps SG, et al: Carotid body tumor (chemodectoma). Clinicopathologic analysis of ninety cases. Am J Surg 122:732-739, Dec 1971 35. Staats EF, Brown RL, Smith RR: Carotid body tumors, benign and malignant. Laryngoscope 76:907-916, May 1966 36. Stout AP: The malignant tumors of the peripheral nerves. Am J Cancer 25:1-36, Sep 1935 37. Strickler JM: New and simple techniques for demonstration of the jugular foramen. Am J Roentgenol 97:601-606, Jul 1966 38. Westbury H: Glomus intravagale tumour. Br J Radiol 40: 148-150, Feb 1967 Ernest E. Lack, MD. Pathology Department Children's Hospital Medical Center 300 Longwood Ave. Boston, Mass. 02115