color doppler sonography of the neck in a patient with bilateral carotid body tumors

Color Doppler Sonography of the Neck in a Patient with Bilateral Carotid Body Tumors Hsin-Ju Cheng , Chih-Hsun Chu2, Chih-Chen Lu1, Po-Chin Wang3, Shyh-Jer Lin4, Chun-Chin Sun, Mei-Chun

R E P O R T

Introduction

Carotid body tumor (CBT) is the most common

paraganglioma of the head and neck Other

para-ganglioma in the head and neck include jugular,

vagal, nasal, orbital, laryngeal, and tympanic tumors

[1] Embryologically derived from neural crest cells

of the autonomic nervous system, paragangliomas

are similar to the pheochromocytomas histologically

But unlike pheochromocytoma, paragangliomas

are mainly nonfunctioning, and only 1–3% of para-gangliomas are hyperfunctioning [2] Symptoms and signs such as palpitations, tremors, tachycardia, and hypertension may indicate possible endocrine activ-ity of these tumors [3]

Paragangliomas grow along the parasympathetic nervous system CBT is a paraganglioma originating

in the chemoreceptors of the carotid body High altitude hypoxia-induced hyperplasia of chemore-ceptor tissues is assumed to be the cause of CBT

Color Doppler Sonography of the Neck in a

Patient with Bilateral Carotid Body Tumors

Hsin-Ju Cheng , Chih-Hsun Chu2, Chih-Chen Lu1, Po-Chin Wang3, Shyh-Jer Lin4, Chun-Chin Sun, Mei-Chun Wang, Jenn-Kuen Lee1,5, Ming-Ju Chuang ,

Han-Kai Tsai, Hing-Chung Lam1,6*

Paragangliomas are rare cases Carotid body tumor (CBT) is the most common glioma of the head and neck Embryologically derived from neural crest cells, paragan-glioma and pheochromocytoma are similar in histology But unlike pheochromocytoma, almost all paragangliomas are nonfunctional Duplex sonography is increasingly used as the first noninvasive diagnostic tool for neck mass However, for more detail of soft tissue nearby, magnetic resonance imaging (MRI) and computed tomography (CT) with 3D reconstruction are preferred Herein we report a patient having bilateral CBT concomi-tant with bilateral pheochromocytomas Duplex sonography clearly demonstrates the tumor and surrounding carotid arteries Compared with CT, duplex sonography is a more rapid, convenient, safe, and economic measurement for the first diagnostic step

KEY WORDS — carotid body tumor, paraganglioma, sonography, ultrasound

■ J Med Ultrasound 2009;17(2):114–119 ■

Received: September 17, 2008 Accepted: November 24, 2008 Division of Endocrinology and Metabolism, Kaohsiung Veterans General Hospital, 1National Yang-Ming University and 2Tzuhui Institute of Technology,3Department of Radiology, Kaohsiung Veterans General Hospital, 4Division of Hematology, Kaohsiung Veterans General Hospital, 5Laboratory of Biochemistry, Kaohsiung Veterans General Hospital, 6Yuh-Ing Junior College of Health Care & Management

*Address correspondence to: Prof Hing-Chung Lam, Division of Endocrinology and Metabolism, Department of

Internal Medicine, Kaohsiung Veterans General Hospital, No 386, Ta-Chung 1stRoad, Kaohsiung, Taiwan

E-mail: hclam@vghks.gov.tw

The prevalence of CBT at high altitude is ten times

more frequent than that at sea level [1] The weight

of a combined carotid body at sea level is around

20 mg, and that at high altitude is about 60 mg [4]

The female to male ratio of CBT is around 2:1 at

sea level, but elevated to 8:1 at high altitude [5] A

lower baseline hemoglobin level accounts for the

higher sensitivity of females to hypoxia Additionally,

genetic defects contributed to familial

paragan-gliomas have also been proposed [6] About 10–50%

of paragangliomas are familial type [7] and the

ge-netic defects may involve the oxygen-sensing and

signaling pathway [6] Furthermore,

neovasculariza-tion due to the hypoxia-activated vascular

endothe-lial growth factor may also be involved in the

pathogenesis of CBT [8] Contrastingly there are

some conflicts to the stance that low hemoglobin

levels or high altitude are related to hypersensitivity

of a carotid body Luna-Ortiz et al have shown that

there were no significant differences in the mean

hemoglobin and hematocrit between residents

liv-ing at high altitude or low altitude [9] Hence they

suggested that ethnicity may play a role

Though angiography was commonly performed

in the diagnosis of a carotid body tumor in the past

[3], the rapidity, convenience, and safety of color

duplex sonography means it is performed more

frequently as the first diagnostic tool Some papers

have mentioned sonography in the diagnosis of

carotid body tumors, but few have shown the

sono-graphic images [10,11] In this report we submit

images of carotid body tumors using 2D imaging,

duplex sonography, and multidetector computed

tomography (CT) with 3D reconstruction

Case Report

A 36-year-old man was referred to our institution

with a bilateral palpable neck mass and rapid body

weight loss He had found bilateral neck mass over

submandibular area 5 years beforehand However,

he felt two neck masses grow rapidly with a body

weight loss of about 5 kg in the last 2 months He

visited a local hospital where a series of imaging

studies including CT and MRI of the neck and CT

of the abdomen were performed However only tumors in bilateral carotid spaces as well as over bilateral adrenal glands were disclosed Biopsy of the left-sided neck mass was performed which revealed a pheochromocytoma-like tumor The level

of urine vanillylmandelic acid (VMA) of this patient

in 24 hours was 22.13 mg/day He was referred to our institution for further management

Physical examination disclosed a slim build with

a low body mass index (BMI) (height 178 cm, weight 51.2 kg, BMI 16.12 kg/m2), blood pressure of 115/

82 mmHg, a heart rate of 100 beats per minute, a respiratory rate of 18/min, and a body temperature

of 36.1°C A bilateral pulsatile and painless mass of about 3× 2 cm2in size was noted below the angle

of the mandible Otherwise, there were no significant findings and his blood pressure remained normal during hospitalization Endocrine tests including serum thyroid hormones, parathyroid hormones, prolactin, cortisol, adrenocorticotropin (ACTH), and aldosterone levels were unremarkable Neck sonog-raphy (Figs 1 and 2), neck to abdominal CT (Fig 3), and whole abdominal MRI (not shown) revealed only the presence of bilateral CBT concomitant bi-lateral adrenal tumors An otolaryngologist did not suggest surgical management of his carotid body tumors due to a high risk of neurological compli-cations The patient was referred to a urologist to consider adrenalectomy Six months after he was discharged from our hospital, he visited our clinic again There was no further body weight loss dur-ing the 6 months and he had still not decided to receive adrenalectomy

Discussion

Although some suggest that CBT is present more in people living at high altitude and in females with relatively low hemoglobin, our patient was a previ-ously healthy man who lived at sea level, and his hemoglobin was 13.2 g/dL on admission

A painless cervical mass may be the initial pres-entation of CBT [3,5,9] The duration of symptoms

may range from 1 to 5 years prior to the diagnosis

due to the slow progression of the tumor [5,7] This

patient noticed bilateral painless cervical masses 5

years beforehand but had paid no attention to it due

to a lack of initial symptoms Only 3% of

paragan-glioma may transform into malignancy [12] There

are no histological characteristics for distinguishing

malignant changes in paraganglioma Malignancy is

defined as paraganglioma with distant metastases

The most reported sites of metastases include the

liver, bone, kidney, lung, breast, pancreas,

retroperi-toneum and thyroid [13,14] Systemic symptoms

like malaise, weight loss or weakness may suggest

metastatic disease [3]

Although the patient had a weight loss of about

5 kg in 2 months, he did not report any other dis-comfort He visited our clinic again 6 months after discharge and we noticed that there was no further body weight loss during that period Image surveys and laboratory examinations during hospitaliza-tion favored bilateral CBT and bilateral pheochro-mocytomas without significant metastasis

Angiography was previously the preferred

meth-od for the diagnosis of carotid bmeth-ody tumors [3] As technology progressed, noninvasive procedures like MRI and CT offered 3D reconstruction and thus provided more information of soft nearby tissue [10,15] Nevertheless, color duplex sonography is

CBT

CBT

Fig 1.Neck sonography of the right-sided CBT (A) Right-sided neck mass, transverse view CBT was partially surrounded by inter-nal carotid artery (thick arrow) and exterinter-nal carotid artery (thin arrow), compatible with Shamblin class II tumor (B) Right-sided neck mass, transverse view with Doppler scan Blue confirmed these vessels were arteries, an internal (thick arrow) and an external (thin arrow) carotid artery Red confirmed the internal jugular vein (double arrow) (C) Right-sided neck mass, longitudinal view CBT presented as a mass lesion surrounded by the internal (thick arrow) and external (thin arrow) carotid artery (D) Right-sided neck mass, longitudinal view with Doppler scan.

Fig 2.Neck sonography of the left-sided carotid body tumor (CBT) scanning from upper to lower portion (A) Left-sided neck mass, transverse view, 2D image CBT between the internal (thick arrow) and external (thin arrow) carotid artery (B) The internal and external artery was partially embedded in the CBT, which is compatible with a Shamblin class II tumor (C) The internal and external arteries became closer together (D) The carotid artery bifurcation site.

Fig 3.Neck CT, 3D reconstruction, oblique sagittal view (A) Shows the patient’s left CBT, surrounded by an internal and external carotid artery (B) The right CBT.

still recommended as the first diagnostic step by

some authors [10], and a high diagnostic rate of

around 90% has been proposed by Jansen et al [16]

and Kapfer et al [17] This is due to the fact that

hypervascularity has been considered a specific

crite-rion for diagnosing a CBT by color duplex

sonogra-phy [18] and hence color Doppler studies are helpful

differential tools in patients with neck lesions that

are difficult to diagnose Nevertheless, MRI or CT

with 3D reconstruction are still necessary to provide

more information on soft nearby tissue for further

surgical planning

Treatment choices include surgical resection,

radiation, stereotactic radiosurgery, embolization,

131I-MIBG (metaiodobenzylguanidine) and

combi-nation therapy Surgical management is the first

choice if the tumor is resectable The therapeutic

goal of CBT is complete surgical resection of the

tumor with preservation of adjacent neurovascular

structures Incomplete excision is associated with a

significant local recurrence rate [3] However, the

size, extension, and localization of the tumor all

influence the possibility of tumor resection and

acceptable morbidity Shamblin et al proposed a

three-stage classification in 1971 to grade difficulty

of resection in CBT [19] Class I tumors are defined

as localized and easily resected tumors Class II

tumors are those partially surrounding the blood

vessels Class III tumors are those completely

en-cased the carotids Most cases are class II or class III

tumors when diagnosed [3,9,20] and the morbidity

related to the surgical resection increases for these

class II and class III tumors In order to avoid

neu-rological deficits, early surgical management for

class III tumors is recommended by Luna-Ortiz et al

[9] However, because of the high morbidity rate,

some authors have not suggested surgical treatment

for those over 60 years of age unless malignancy is

suspected [21] Our case had Shamblin class II CBT

tumors on both sides of the neck We consulted an

otolaryngologist, but surgical management was

not considered due to the high risk of neurological

complications

The use of radiotherapy is still controversial

for CBT management For unresectable tumors,

radiotherapy with fractionated doses of 1.8– 2.0 Gy/day (total dose 45 Gy) may be considered for local control [22–24] As well as the ablation of local tumor, radiotherapy could also be performed for distant metastases with good symptom control [13] Recently, stereotactic radiosurgery which al-lows cellular damage within a sharply defined treatment volume has been employed to stabilize tumor growth [25] 131I-MIBG, either used alone or

in combination therapy for metastatic paragan-gliomas, has been reported to result in clinical im-provement and complete remission, respectively [26,27] Finally, due to the rich vascular nature of these tumors, preoperative conventional endovas-cular transarterial embolization [28] and direct puncture embolization with cyanoacrylate glue or ethanol [29,30] have been described as useful adjuvants prior to surgery

How long should we leave it before we follow up imaging of a patient with CBT ? René van den Berg suggested a follow-up interval of approximately 2 years, or even more in stable paraganglioma [13]

Of course, this would depend on changes in the clin-ical situation of the patient In conclusion, CBT are rare tumors of the head and neck and color duplex sonography can be used as the first-line diagnostic tool for the detection of CBT

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