A case report of carotid body tumor

ELSEVIER

Auris Nasus Larynx 24 (1997) 21 I-216

Case report

A case report of carotid body tumor Shizuo Kojya ‘,*, Tetsuo Itokazu a, Tatsuhito Oowa ‘, Yutaka Noda a, Takayoshi Toda b, Al Muktafi Sadi b, Masaya Kiyuna b il Depurtment b Department

of Otorhinolarl;ngolog~, of Clinical

Laboratory

Schoo/ Me&&,

qf Medic,ine, Linioersity of the Ryukyus , 207 Uehara. Nishihura-cho, Okinawa 903-01, Japan Scl~ool of’ Medicine, University of the RJukJvs. Okinawa. Japun

Received 6 December 1995; received m revised form 18 October 1996: accepted 18 November 1996

Abstract A case of left carotid body tumor is presented. A 47-year-old female patient consulted our otorhinolaryngological clinic with a neck swelling that had persisted for 5 months. On physical examination, a movable and pulsating hard mass measuring 2 x 2.5 cm in size was found on the left side of her neck, near the angle of the mandible. Computed tomography, magnetic resonance image and angiography all demonstrated a well-circumscribed tumor mass showing high vascularity and located at the bifurcation of the left carotid artery. The tumor involved the left carot!ld artery, but the patency of the artery was preserved. The patient showed satisfactory temporary balloon occlusion test results without neurological complications. Since the tumor was strongly adherent to the carotid arterial wall. the tumor was resected together with the carotid artery. Histologically, the tumor was composed of organoid clusters of round cells with eosinophilic granular cytoplasm. Involvement of tumor cells was seen to the adventitia of the carotid artery, but only slight cellular atypia was seen. Ultrastructurally, two types of cells were observed in the central and marginal portion of the tumor; these were round chief cells with few cytoplasmic neurosecretory granules and spindle-shaped sustentacular cells. Immunohistochemically, the chief cells and sustentacular cells showed positive reaction for neuron-specific enolase and S-100. respectively. The ultrastructural findings suggested the benign nature of the tumor. e 1997 Elsevier Science Ireland Ltd. Keywords:

Carotid

body tumor;

Sustentacular

cell

-

* Corresponding author. Tel.: + 81 98 8953331, ext. 2495; fax: + 81 98 8952243. 0385~8146:97~$17.00 8 1997 Elsevier Science Ireland Ltd. All rights reserved PII SO385-8146(96)00029-6

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1. Introduction Extra-adrenal paraganglioma is a rare neuroendocrine neoplasm, usually occurring in various sites in the paraganglion system [I]. According to the site of origin, the tumors are known as paraganglioma of the carotid body, of the aortic body, and so on [2]. Among the paraganglioma of the head and neck region, carotid body tumors are most common, but they are rare surgical problems in this region [3]. In this paper a rare case of carotid body tumor is reported, that histologically showed adventitial involvement, but immunohistochemically and ultrastructurally had benign character.

2. Case report A 47-year-old woman consulted the Otorhinolaryngological Clinic of Ryukyu University Hospital with a neck mass that had persisted for 5 months. She had developed hypertension 1 year previously, for which she had been taking antihypertensive drugs. Seventeen years prior to this consultation she had undergone a hysterectomy. For the last 3 years she had suffered from rhinitis. Her family history included nothing contributory. On physical examination, a hard, movable and pulsating mass was observed on the left side of the neck. Otorhinolaryngological and neurological examination of the head and neck revealed no abnormal findings, and the results of other systemic examination were normal. Her blood pressure was 16OilOO mmHg. Routine blood study results and serum catecholamine levels were within normal limits. The electroencephalography findings were normal, but electrocardiography disclosed abnormal T unaccompanied by any symptoms. Enhanced computed tomography (CT) revealed a 3 x 3 cm mass showing marked enhancement at the level of the tongue root and the lower margin of the first cervical vertebra (Fig. 1). The jugular vein was compressed by the tumor and location of the carotid artery was unclear. Magnetic resonance image (MRI) revealed a 3 x 2.5 cm tumor mass at the bifurcation of the left carotid artery. The tumor involved the carotid arterial wall without disturbing its patency. An-

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giography also disclosed a highly vascular tumor at the site of left carotid artery bifurcation causing displacement of the internal carotid artery. No lymph node metastasis was detected using CT or MRI. The diagnosis of carotid body tumor was made. The patient showed satisfactory balloon occlusion test results, and no neurological complication was observed. The patient underwent operation under general anesthesia. The sympathetic, vagal and hypoglossal nerves that course along the carotid artery were intraoperatively found to be involved with the tumor. contrary to preoperative evaluation. These nerves were injured during separation, and they could not be well preserved except for the sympathetic nerve. The tumor could not be separated from the carotid artery due to strong adhesion. The tumor together with the carotid artery was resected without any complication after ligation of the resected arteries. Because the tumor was located at the carotid artery bifurcation, all of the common, external, and internal carotid arteryhad to be resected. The patient’s blood pressure showed no change on the 10th posl:-operative

Fig. tion

I. CT scan of neck reveales of the left carotid artery.

a tumor

mass at the bifurca-

S. Kojya

Fig. 2. Organoid stain x 400).

arrangement

of neoplastic

et 01. / Auris

chief

cells,

Nasus Larynx

(HE

day, suggesting that there was no relation between the hypertension and the tumor. Partial palsy of the left hypoglossal and recurrent nerve and Horner’s symptom were recognized postoperatively. The pathological examination of the resected tumor included light and electron microscopy and immunohistochemistry. 2.1. Light microscopy The histological sections were stained with hematoxylin eosin (HE), Mallory Azan, silver impregnation, elastica van Gieson, periodic acid Schiff and Grimelius methods. Routine HE preparations showed clusters of round tumors cells with eosinophilic granular cytoplasm (Fig. 2). The nuclei of the tumor cells were uniform in size and were located centrally. Nuclear atypia and mitotic figures were not seen. Characteristic Zellballen pattern was observed by silver staining (Fig. 3). Grimelius stain did not demonstrate any positive reaction. The tumor cells showed slight atypia, and involvement with tumor cells was seen to the adventitia of the carotid artery.

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Fig. 3. The characteristic stain x 200).

213

Zellballen

pattern

is shown

(silver

bodies against neuron-specific enolase (NSE), S100 protein and glial fibrillary acidic protein (GFAP) were used. The tumor cells showed strong positive reaction for NSE (Fig. 4) and S-lOO-positive cells were seen around the chief cells in both central and marginal portions of the tumor (Fig. 5) but these cells showed negative reaction for GFAP.

2.3. Electron microscopy Ultrastructural sections from the central portion of the tumor presented two types of cells

2.2. Immunohistochemistry Immunohistochemical examination was done by avidin-biotin-peroxidase complex (ABC) methods described by Hsu et al. [4] Primary anti-

Fig. 4. Chief ceils showing (ABC x 400).

strong

positive

reaction

for

NSE.

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tures were seen in the chief cells in the: specimen taken from the marginal portion of the tumor, but spindle-shaped sustentacular-like cells were only occasionally seen in the tumor margin.

3. Discussion

Fig. 5. Note the S-IOO-positive cells in the peripheral portion

spindle-shaped sustentacular of the tumor. (ABC x 400).

(Fig. 6). The chief cells showed centrally located nuclei with slight indentation of the nuclear membrane. Mitochondria, rough endoplasmic reticulum, free and attached ribosomes are seen in considerable amount in the cytoplasm. A few membrane-bound dense-cored granules, suggesting neurosecretory granules, were also seen. The cells showed desmosome-like cell junctions. Around the chief cells spindle-shaped sustentacular-like cells were seen. From these cells slender processes extended between the chief cells. They had abundant cytoplasmic organellae but no neurosecretory granules. Similar ultrastructural fea-

Fig. 6. Closely apposed chief cells (C) contarn a few neurosecretory granules (N). Spindle-shaped sustentacular cell (S) extend slender process between chief cells. (Bar 1 ltm).

The carotid body tumor can occur ‘on one or both sides [5]. There is no gender predominance and the tumor usually occurs in adults between 25-75 years, although occurrence in children has also been reported [6]. A familial tendency has been documented in about 10% of the patients [7]. The incidence of this tumor in persons living at high altitude is ten times greater thaln that in those living at sea level [8]. Recently K;atori et al. [9]. described that the carotid body tumors reported in Japan since 1924 amounted to 132 cases. Carotid body paragangliomas are usually non-functional [lo]. Functional carotid body tumors can be assessed based on a history of hypertension and a high level of serum catecholamine. The patient in the present case had a history of hypertension. but her serum catecholamine level was within the normal range. The patient’s continued high blood pressure post-operatively also suggested that the hypertension was not associated with the tumor. Non-functioning tumors might be confused with other common neck tumors such as parotid or other salivtary gland tumors, schwannoma, metastatic tumor, or lymphoma [I 11. However, the image-based diagnosis of carotid body tumor using CT, MRI and especially angiography has become easier [ 121. Although there are possible risks of vascular and neurological complications, surgical resection is the treatment of choice. Shamblin et al. [13] proposed a surgical classification of carotid body tumor, as follows: group I, easily removable small tumors with minimal attachment to tbe adjacent vessels; group II. relatively larger tumors having intimate attachment to the carotid arterial wall but that can be resected free; and group III, tumors with firm attachment to the carotid artery. The present tumor was categorized as a group III tumor, and surgical resection of the carotid artery together with the tumor was necessary.

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The carotid body, like other paraganglial structures, is composed of two distinct cell populations originated from primitive neural precursor cells. The chief, or type I cells originate from neuroectoderm, and are characterized histologically by closely-arranged round cells with cytoplasmic eosinophilic granular material and ultrastructurally by membrane-bound dense-cored neurosecretory granules. The type II cells, known as sustentacular cells, are homologous to the satellite cells of autonomic ganglia. These spindle-shaped cells are rarely recognized by light microscopic examination, but they can be seen ultrastructurally and are clearly recognized by immunohistochemical method [14]. Immunohistochemically, the chief cells are invariably positive for NSE, but not for S- 100 [ 14- 161. Sustentacular cell,s can be recognized by their positive reaction for S-100 protein and GFAP [15,17]. In the present case it was also observed that the chief cells were positive for NSE while the cells located peripherally to the chief cells showed positive reaction for S-100 protein. Ultrastructurally, the chief cells showed a few neurosecretory granules in the cytoplasm. Spindle-shaped cells, from which extended slender processes surrounding the chief cells without neurosecretory granules, were recognized as sustentacular cells. Carotid body tumors rarely show malignant change, and the histological diagnosis of malignant carotid body tumor is very difficult [18]. Only a few reports of malignant carotid body tumor have been published previously [19,20]. According to these reports definite metastatic foci, and vascular invasion of tumor cells, can also be documented as evidence of the malignant nature of the tumor. Histologically, an extremely large Zellballen pattern composed of pleomorphic cells showing mitotic figures can be considered as a sign of malignant change, but these findings should not be interpreted as sufficient evidence for malignancy [21]. As reported by many authors, the presence of sustentacular cells is one of the important criteria pointing to the benign character of a carotid body tumor [10,22,23]. Sustentacular cells homologous to the satellite cells of autonomic ganglia are usually not seen in malignant carotid body tumors [16]. The benign nature

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of the present tumor was suggested by the presence of sustentacular cells as demonstratfed both immunohistochemically and ultrastructurally. However, careful follow-up of the patient was pursued due to the marginal involvement of tumor cells noted histologically.

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