Metastatic Intravagal Paraganglioma Case Report and Review of the Literature
MICHAEL C. HEINRICH, M.D.* ANTHONY E. HARRIS, M.D. WILLIAM R. BELL, M.D.
Intravagal paragangliomas are rare tumors of neural crest origin. These tumors are usually benign with few reports of metastases or aggressive behavior. One case of Intravagal paraganglloma metastatic to a regional lymph node is described and the diagnosis and management of these tumors are discussed. The reports of 14 other cases with regional or distal metastases are reviewed. Paraganglionic cells originate from the neural crest [ 1] and are thought to be modified neurons . These cells embryologically migrate in close association with ganglion cells of the autonomic nervous system. Certain macroscopic bodies of paraganglion cells have known physiologic importance, such as the carotid and aortic bodies (which function as chemoreceptors) and the adrenal medulla (which functions as a neuroendocrine organ). Other paraganglionic bodies, including the vagal body, have no known function. Tumors originating from paraganglionic cells are referred to as paragangliomas, except for tumors of the adrenal medulla, which are known as pheochromocytomas. In the past, these tumors have been referred to as chemodectomas (tumors of chemoreceptor organs), glomus tumors (tumors of glomoid or vascular origin), and nonchromaffin paragangliomas. In this report, we use the classification of Glenner and Grimley [ 1] and refer to tumors of the vagal body as intravagal paragangliomas. Intravagal paragangliomas are rare, usually benign tumors with few reports of metastatic or malignant behavior. We describe a patient with a regionally metastatic intravagal paraganglioma.
From the Division of Hematology, Department of Medicine, and the Department of Otolaryngology and Heed and Neck Surgery, The Johns Hopkins University School of Medicine and Hospital, Baltimore, Maryland. This work was supported in part by Research Grants 5R01 HL01601, 5T32 HL07377, and 5T35 AM07384 from the National Heart, Lung, and Blood Institute, National Institutes of Health (Bethesda, Maryland)and by the Whitehall Foundation (Palm Beach, Florida). Dr. Bell is a Hubert E. and Anne E. Rogers Scholar in Academic Medicine. Requests for reprints should be addressed to Dr. Anthony E. Harris, Department of Otolaryngology and Head and Neck Surgery, The Johns Hopkins University School of Medicine and Hospital, Baltimore, Maryland 21205. Manuscript accepted May 4, 1984. * Current address: Department of Medicine, Oregon Health Sciences University, 3181 S.W. Sam Jackson Park Road, Portland, Oregon 97201.
CASE REPORT A 23-year-old black man was first seen at The Johns Hopkins Hospital on September 29, 1983 with a complaint of hoarseness and a painful left upper neck mass. The patient had been aware of the left neck mass for over one year with gradual progression in size over the past six months. The patient also noted hoarseness of two months' duration, characterized by breathiness and loss of volume. The patient also admitted to a 10-pound weight loss over the past six months. The patient consulted his family physician and was initially treated with antibiotics for suspected pharyngitis. When his symptoms persisted, he was referred to the Otolaryngology-Head and Neck Surgery Department for further evaluation. The patient denied hypertension, headaches, fever, or chills. There was no family history of a similar illness. On physical examination, the pulse was 72 beats per minute, blood pressure 118/70 mm Hg, and the oral temperature was 37°C. Results of otologic and nasal examinations were normal. Oral examination revealed a mucosally covered mass in the left oropharynx displacing the tonsil and soft palate medially (Figure 1). The mass extended superiorly to the naso-
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METASTATIC INTRAVAGALPARAGANGLIOMA--HEINRICHET AL
Figure 1 (left). Intraoral view demons~rating medial disp~ernent of uvu/a, soft palate, and tonsil. Figure 2 (right). neck.
pharynx and inferiorly to the pyriform sinus. Laryngeal examination demonstrated a paralyzed left vocal cord in the midline position. A 2 by 5 cm firm, poorly mobile, nontender and nonpulsatile mass was palpated in the left upper neck (Figure 2). A separate group of lymph nodes, 2 by 3 cm in aggregate size, were palpated directly over the mass anteriorly. The carotid system was displaced anteriorly. The remainder of the neck examination showed unremarkable findings. Results of neurologic examination were normal except for the absence of left 10th nerve function. Laboratory studies were remarkable for a hematocrit value of 32.1 percent, hemoglobin level of 9.8 g/dl, mean corpuscular volume of 67.5 fl, mean corpuscular hemoglobin of 20.8 pg, and mean corpuscular hemoglobin concentration of 31.3 g/dl. The white blood call count was 6,100/mm 3 and the differential count was normal. The platelet count was 561,000/mm 3. The reticulocyte count was 0.4 percent. Chemical values were notable only for an albumin of 2.9 g/dl and a total protein of 8.9 g/dl. Serum protein electrophoresis showed a stair-stop increase in globulins with ~-3' bridging and a broad-based elevation of gammaglobulin. Serum and urine immunoelectrophoresis did not demonstrate any monoclonal protein. Bone marrow examination revealed normal cellularity and cell line maturation with abundant stainable iron. Urinary catecholamine levels were within normal limits. Computed tomography of the neck showed a well-circumscribed hypervascular mass extending from the base of the skull to the level of the pyriform sinus on the left-hand side (Figure 3). Carotid angiography showed a hypervascular mass originating above the carotid bifurcation and displacing the carotid system anteriorly (Figure 4). There was no widening of the carotid bifurcation. Chest radiography showed a 7 mm radiodensity in the left upper lobe near the anterior portion of the left second rib.
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Mass in left upper
Computed chest tomography showed the lesion to be small without definition or calcification. Clinical impression was that of paraganglioma, probably of vagal origin. With the presence of adanopathy, weight loss, and anemia, the possibility of malignancy was considered. Open biopsy of the neck mass was performed with inclusion of the overlying adenopathy. Histologic and electron microscopic examination of the mass and the lymph node demonsVated tissue diagnostic of a paraganglioma (Flguru 5 and 6). The patient declined to undergo percutaneous needle biopsy of the left upper lobe lesion. With a malignant pareganglioma diagnosed on the basis of lymph node metastases, excision of the mass with radical neck dissection was recommended. Due to the extension to the skull base and circumferential involvement of the internal carotid artery, complete excision of the entire carotid system was advised. To facilitate excision, the internal carotid artery was occluded in the region of the carotid syphon with a balloon catheter, The patient had no neurologic sequelae over a 30-minute period of total occlusion and therefore the balloon was detached and left in position. A second balloon was placed in the internal carotid artery just above the bifurcation. One week later, the patient underwent left radical neck dissection with excision of the tumor and sacrifice of left cranial nerves 9, 10, 11, and 12, as well as the entire carotid system and cervical sympathetic chain. The intracranial carotid occlusion allowed transsecUon at the skull base. Although all gross neoplasm was resected, a satisfactory surgical margin at the skull base was not possible. All 23 lymph nodes included in the specimen were free from tumor. The patient had a postoperative pharyngocutaneous fistula that closed spontaneously. Postresection computed tomographic scanning did not demonstrate any gross tumor in the area of the jugular foramen. Postoperative swallowing and speech were not impaired, and shoulder function was mini-
METASTATIC INTRAVAGAL PARAGANGLIOMA--HEINRICH ET AL
Figure 3. mass.
Computed tomographic scan of parapharyngeal
Figure 4. Carotid angiogram wilh arrow confirming anterior displacement of carotid system.
Figuro 5. Intravagal paraganglioma with typical zellballen (arrow) (hematoxylin and eosin stain; original magnification X 300, reduced by 10 percent).
Figure 6. Lymph node with metastatic paraganglioma (hematoxylin and eosin stain; original magnification X 120, reduced by 10 percent).
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mally decreased. A course of postoperativeradiotherapy was recommended followed by close observation and serial computed tomographic scanning. COMMENTS
Head and neck paragangliomas are rare, with the Sloan-Kettering Cancer Center Pathology Department reporting only 69 cases in over 600,000 patients examined between 1937 and 1975 . Lawson  reported 2,000 cases of head and neck paragangliomas in the literature, about 5 percent of which were intravagal paragangliomas. In order to understand the clinical presentation and behavior of intravagal paragangliomas, knowledge of the anatomy of the parapharyngeal space in which these tumors arise is necessary. The parapharyngeal space is bounded by the base of the skull superiorly, the mandible laterally, and the vertebral bodies posteriorly . These bony structures force neoplasms to grow medially and inferiorly. Growth medially of the tumor causes displacement of the soft palate, lateral nasopharynx, and lateral pharyngeal wall. The pharyngeal constrictor musculature and fascia are present between the pharyngeal mucosa and any parapharyngeal neoplasm and prevent the neoplasm from ulcerating into the pharynx, nasopharynx, or palate mucosa . Growth inferiorly results in a mass appearing below the angle of the mandible. The parapharyngeal space contains many vital structures, including the internal carotid artery, internal jugular vein, cranial nerves 9 through 12, and the cervical sympathetic chain . Neoplastic growth can cause symptoms by impinging on or invading any or all of these structures. The vagus nerve exits the base of the skull through the jugular foramen and has three ganglia (superior, middle, and inferior) within its first several centimeters of extracranial course, all of which are above the carotid bifurcation . The behavior of an intravagal paraganglioma varies depending upon from which ganglia it arises. Tumors arising from the inferior ganglion are usually spindle-shaped and have the least frequency of intracranial extension. Tumors arising from the middle ganglion are usually cone-shaped with the base attached to the skull. Tumors arising from the superior ganglion are usually dumbbell-shaped with both intracranial and cervical components. Tumors arising from the two rostral-most ganglia are the type of intravagal paraganglioma most likely to produce intracranial infiltration and multiple cranial nerve palsies . Intravagal paragangliomas most often present with a painless cervical mass below the mandible. On examination, 83 percent of patients will have a palpable neck mass, 46 percent will have both a neck mass and an intraoral mass, and 16 percent will have an intraoral
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mass alone . The mass may have direct or transmitted vascular pulsations and occasionally may have a bruit . Fifty percent of patients will have one or more cranial nerve palsies, with the vagus nerve being the most frequently involved. Thus, patients will often complain of hoarseness or dysphagia . Cranial nerve palsies may precede or follow the appearance of the mass . Rarely, patients may present with carotid sinus syndrome or Horner's syndrome. Intravagal paragangliomas are slow-growing, with four years as the average length of symptoms before diagnosis . The average age at time of diagnosis is 48 years. This tumor is more frequent in women than in men (ratio 2.7 to 1) and occurs slightly more often on the right side . All paragangliomas produce and store catecholamines [ 1] and thus are capable of producing symptoms by releasing these products. Unlike pheochromocytomas, intravagal paragangliomas are rarely functional, with only four reported cases in the literature [9-12]. Paragangliomas are sometimes multicentric and/or familial, Familial paragangliomas tend to have an increased frequency of multicentricity. Lawson  reported that about 20 percent of intravagal paragangliomas are associated with either a contralateral intravagal paraganglioma and/or a paraganglioma at an extravagal site. Histologically, all paragangliomas (including pheochromocytoma) are similar. Paragangliomas are highly vascular tumors with nests of cells (zellballen) lining vascular sinuses. These nests of cells are composed of chief cells, which contain catecholamine granules and the supporting sustentacular cells [ 1]. Lack et al  indicate that malignant paragangliomas can be differentiated histologically from benign paragangliomas by the presence of central necrosis of zellballen, invasion of vascular spaces, and presence of mitotic figures. However, most authors state that there is no histologic difference between benign and malignant paragangliomas . The differential diagnosis of intravagal paraganglioma is that of an upper anterolateral neck mass and includes branchial cleft cyst, paraganglioma, metastatic squamous cell carcinoma, thyroid cancer, lymphoma, neurofibroma, schwannoma, ganglioneuroma, and salivary gland neoplasms [ 14]. Diagnosis is often possible with the use of carotid angiography, which characteristically reveals a highly vascular tumor displacing the external and internal carotid arteries anteriorly without widening of the carotid bifurcation . Evaluation of a known paraganglioma should include measurement of urinary metanephrines to assess if the paraganglioma is functional and if pharmacologic intervention is needed before surgery [ 16]. Evaluation should also consider
METASTATIC INTRAVAGAL PARAGANGLIOMA--HEINRICH ET AL
the possibility that multicentric paragangliomas are present. Treatment of intravagal paragangliomas is primarily surgical. Although the tumors are usually benign and slow-growing, significant symptoms will result solely from the mass effect of the tumor, given enough time . Because the vagus nerve usually enters the tumor or is fixed to it, it is almost always impossible to spare the vagus nerve in resecting the tumor . Other frequent neurologic deficits after surgery include Horner's syndrome and ipsilateral loss of hypoglossal nerve function . The degree of neurologic deficit frequently decreases with time. Intravagal paragangliomas, which are fixed to the skull or have intracranial extension, may be only partially resectable. In one study [ 13], 17 percent of surgically resected intravagal paragangliomas recurred. The use of radiation therapy in the treatment of intravagal paragangliomas is controversial. Spector et ars  study of the use of 4,000 to 6,000 rads tumor dose to jugular paragangliomas showed that 45 percent of the tumors were no longer detectable after radiation, 20 percent of the tumors were persistent and smaller to unchanged after more than 10 years, and 35 percent of the tumors recurred within three years. In our review of the literature, we were able to discover only 14 cases of metastatic intravagal paraganglioma (Table I). Several other cases have been cited as being metastatic, but we do not believe that there is sufficient evidence to accept these cases. Kahn  has cited Case 13 of Smetana and Scott  as an intravagal paraganglioma metastatic to the lungs, heart, and brain. The only evidence that this case was an intravagal paraganglioma is the authors' statement that the tumor was located in the "posterior triangle of the neck." In the original article of Smetana and Scott , no anatomic origin is assigned to Case 13 even though the authors did classify another case (Case 14) as an intravagal paraganglioma. Druck et al  have cited Case 2 of Lattes  as an intravagal paraganglioma metastatic to bone. We believe that there is clear evidence that the spread of the tumor to the mastoid and occipital bones and first cervical vertebral body was due to direct extension and not distant metastasis. Several authors [17,23] have cited Case 2 of Murphy et al  as an intravagal paraganglioma metastatic to an adjacent lymph node. In the original article, Murphy et al could not decide if the tumor reached the lymph node by metastasis or direct extension. Besides the 15 cases in Table I, we are aware of one other possible metastatic intravagal paraganglioma. Conley and Clairmont  have reported a case of intravagal paraganglioma associated with five cervical lymph nodes containing metastatic paraganglioma.
However, the patient had a carotid body paraganglioma on the same side of the neck as his vagal tumor, so it is unclear from which tumor the metastases originated. It should be noted that we are including in our series the metastatic paraganglioma reported by Burman . The diagnosis of paraganglioma was made by biopsy of an occipital bone metastasis, with the diagnosis of intravagal paraganglioma made on the basis of clinical history rather than on the basis of pathologic and anatomic examination. However, we believe that the clinical history is classic for intravagal paraganglioma and would be extremely atypical for any other type of cervical paraganglioma. The demographic characteristics of the 15 patients with metastatic intravagal paraganglioma are similar to those of patients with nonmetastatic intravagal paragangliomas. Eight of 14 were female and the average age at the time of diagnosis was 50 (range 23 to 72). Determining the average length of symptoms before diagnosis is complicated by the uncertain history in one of the patients. In the report of Mahe et al , the patient recalled having a lateral cervical mass that was treated with x-ray therapy when she was 28. The mass disappeared only to reappear at the same location 40 years later when it was surgically diagnosed as an intravagal paraganglioma. Without this case, the average length of symptoms before diagnosis was 3.7 years (range six months to 16 years). When Mahe et al's case is included, the average length of symptoms was 6.3 years. Information on the nature of the symptoms was available for 14 of the 15 patients. Seventy-one percent of the patients complained of a neck mass and 36 percent complained of pain and a neck mass. Sixty-four percent of the patients complained of symptoms that were possibly due to cranial nerve dysfunction, with two patients complaining of vasovagal syncope, three complaining of changes in their voice, and four complaining of dysphagia. On physical examination, eight of 14 tumors were located on the right side, keeping with the slight predilection of the tumor for that side. Twelve of the 13 patients for whom data were available had a palpable neck mass (92 percent), eight had a neck mass and an oral mass (62 percent), and one had an oral mass without a neck mass (8 percent). Seven of the 13 had a demonstrable cranial nerve palsy (54 percent). The most frequently involved cranial nerves were 10 (seven patients), 9 (six patients), and 12 (three patients). None of the 14 patients had Homer's syndrome. The presence or absence of certain cranial nerve palsies is useful in predicting whether metastases exist in a given patient. The frequency of metastases among intravagal paragangliomas is 10 percent . A patient
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Fifteen Patients with Metastatic Intravagal Paraganglloma
9uratlonof Symptoms (before diagnosis)
6 months 6 months
5 years 6 months
[ 13] 
? 40 years
 Present report
2 years 1 year
2 years Not stated
Right neck mass, Bone,lungs right oral mass, 6th, 8th through 10th, and 12th cranial nerves Mass,pain, Left neck mass, Lymphnode syncope left oral mass, 9th and 10th cranial nerves Mass,headache Rightneck mass, Lymphnode 5th and 8th through 1lth cranial nerves Mass,voice Right neck mass Lymphnode change, dysphagia Mass Right neck mass Lymphn o d e Dysphagia Left neck mass, Lymphnode left oral mass Mass, pain, Left neck mass, Lung syncope, left oral voice mass, 9th through 12th change cranial nerves Pain,dysphagia Left oral mass, 9th, Lymph node, 10th, and 12th bone, lung cranial nerves Mass Right neck mass Lymphn o d e Mass Right neck mass, Lymphnode right oral mass Not stated Tumor on right side Lymph node Mass Not stated Liver, b o n e , brain Dysphagia
Right neck mass, 9th and 10th cranial nerves Mass,pain Left neck mass Mass,pain, Left neck mass, voice change left oral mass, 10th cranial nerve
who presents with an isolated 10th cranial nerve palsy has the same 10 percent chance of having a metastatic tumor. A patient with two or more cranial nerve palsies has a 20 percent chance of having a metastatic tumor. A patient who presents with a solitary 9th cranial nerve palsy has a 36 percent chance of having a metastatic tumor . As might be expected from a series of patients spanning 30 years, the methods used to make the di-
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Alive at 8 years
Died preoperatively 13 years after first operation
Radicalexcision Tumor unresectable
Alive at 1 week Dead7 days after open biopsy
Tumor partially resected
Alive at 2 years
T u m o runresectable
Deadafter 2 years
Radicalexcision Local excision
Lost to follow-up Alive at 2 years Alive at 7 years Dead after 2 years
Local excision Surgery, radiotherapy, chemotherapy Partial resection
Lung Lymphnode, ? lung
Local excision Tumor partially resected
Alive at 3 years Alive at 3 months
Alive at 10 days
agnosis were extremely varied. Several conclusions, however, are possible. Closed biopsy almost always was nondiagnostic and on one occasion resulted in severe arterial hemorrhage necessitating emergency surgery. Angiography was performed in five cases and showed a hypervascular mass displacing the internal carotid artery anteriorly and no widening of the carotid bifurcation in all cases [ 17,21,28,29]. This pattern is diagnostic of intravagal paraganglioma. Other than by
viously. In three of the 15 cases, the tumor histologically showed the presence of mitotic figures and two of those showed central necrosis [ 13,26,30]. In one additional case, Poster et al  reported the tumor as histologically "malignant." To our knowledge, mitotic figures have never been reported in any nonmetastatic intravagal paraganglioma. The prognosis for these metastatic tumors appears to be somewhat worse than for those intravagal paragangliomas that are nonmetastatic. Aggressive behavior was observed more frequently in these 15 tumors than is usual with this type of neoplasm. One patient died preoperatively of his tumor and two others died within two years after diagnosis. In two patients, the tumor was nonresectable and in two other patients only portions of the tumor were resectable. In summary, we are aware of 141 cases of intravagal paraganglioma in the English literature, 15 of which were metastatic (10.6 percent). This frequency of metastatic tumors is much lower than that reported by Druck et al , but is similar to that reported by Lawson . Because there is no registry for these tumors, it is difficult to be certain of the true frequency of metastatic tumors of this type. From our review, there appears to be no clinical difference between metastatic and nonmetastatic intravagal paragangliomas at the time of presentation. Diagnosis is best made by angiography and/or open biopsy. Surgical removal is indicated for these tumors. The role of radiation and/or chemotherapy as primary or adjuvant therapy for these tumors is unclear. Histologically, a minority of metastatic intravagal paragangliomas are recognized to have mitotic figures. From our review, it appears that these metastatic tumors have a worse prognosis than nonmetastatic intravagal paragangliomas.
angiography, the diagnosis was most often made by open biopsy or exploratory surgery. Cervical lymph nodes were the most common site of metastasis and were involved in 11 of 15 cases (73 percent). Cervical node involvement alone was seen in 10 of 15 cases (67 percent). Cervical node involvement and distant metastasis were seen in one case (7 percent). Distant metastasis alone was seen in four of 15 cases (27 percent). The lungs were the site of a metastatic lesion in four cases (27 percent) and were associated with distant bone metastases in two of those cases (13 percent). There was one case of liver metastasis associated with bone and brain metastases. The sites of these metastases suggest that these tumors are capable of both lymphangitic and hematogenous spread. In 10 of the 11 patients with lymph node involvement, the nodes demonstrated tumor at the time of diagnosis (91 percent). The other patient was found to have nodal involvement one year after the time of original diagnosis. Of the patients with lung metastases, all metastases were detected within three years (range one and a half to three years). Of the three patients with bone metastases, metastases appeared within two years after diagnosis in two patients and four years after the appearance of the neck mass in the other patient. It appears that the distant metastases of intravagal paragangliomas appear sooner than those of carotid body paragangliomas. Kahn [ 17] has reported that in 20 cases of carotid body paragangliomas with distant metastases, the distant lesions were detected an average of 9.8 years after diagnosis of the original tumor (range 20 months to 20 years). All of the tumors exhibited the classic histologic features of intravagal paragangliomas described pre-
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