Clinical case Cir Cir 2014;82:273-278.
Carotid body paraganglioma in a teenager. Case report
María Elisa López-Vázquez1 Francisco Javier Llamas-Macías1 César Nuño-Escobar1 Alejandro González-Ojeda2 Clotilde Fuentes-Orozco2 Michel Dassaejv Macías-Amezcua2 Departamento de Angiología y Cirugía Vascular Unidad de Investigación Médica en Epidemiologia Clínica Unidad Médica de Alta Especialidad, Hospital de Especialidades del Centro Médico Nacional de Occidente, Instituto Mexicano del Seguro Social, Guadalajara, Jalisco, México.
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ABSTRACT Background: Paragangliomas of the head and neck are neuroendocrine tumors. They have a low incidence (0.6%), are generally benign, have a poorly defined etiology, and multiple factors have been associated with their origin. Humans and other species living at high altitudes (> 2000 m above sea level) are subjected to a relatively chronic hypoxia and there is a high prevalence of the development of carotid body hyperplasia and eventually paragangliomas. This disease is usually seen in patients in their 50s and in their 30s if there is a family history. Clinical case: We present the case of a 16-year-old female with acute pharyngitis and symptomless growing tumor located on the left side of the neck. A duplex Doppler ultrasound showed a solid nodular lesion on the left carotid bifurcation. A left lateral cervicotomy was performed, finding a highly vascularized tumor of 4 × 3 × 3 cm involving the common carotid from its middle third, the internal carotid up to the cranial base, and the external carotid to its upper third and intimately related to the trachea, esophagus and cervical spine. The tumor was completely resected and the histopathological analysis corroborated the presence of paragangliomas. Conclusions: The publication of this case is relevant and of clinical interest due to the uncommon age of presentation and the fact that it should be considered as a diagnostic possibility. Key words: paraganglioma, carotid body. www.amc.org.mx
Received: 2-27-2013 Accepted: 6-4-2013
Correspondence:
Clotilde Fuentes Orozco Calle Nebulosa 2975, Interior 6 C 44520, Guadalajara, Jalisco, México Tel: (33) 3618-9538 E-mail:
[email protected]
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BACKGROUND Paragangliomas are hypervascularized neuroendocrine tumors derived from chromaffin cells of the adrenal medulla or the paraganglia of the extra-adrenal system of the chest and abdomen, called pheochromocytomas or extra-adrenal paraganglioma.1-3 Paraganglioma of the head and neck are rare neoplasms that represent 0.6% of the tumors in the area and 0.03% of all neoplasms, with malignancy rates of up to 15%, with recurrence of 5%.1,4 They appear predominantly in the carotid body (65%) and its incidence is from 1:30,000/100,000 in the general population.1,5,6 There are two types of presentation: sporadic and familial. Familial paraganglioma are seen in 10-30% of the cases, are commonly bilateral and multicentric, whereas sporadic cases (70-80%) tend to be unilateral of left predominance (75%). They mainly affect the female gender (2:1) and particularly people who live at altitudes >2000 m above sea level.1,7,8 The purpose of this paper is to report the clinical behavior of a left carotid paraganglioma in a 16-year-old patient, a relatively uncommon situation in the practice of a vascular surgeon.
CLINICAL CASE The case of a 16-year-old female adolescent is reported. The patient is originally from and resident of Guadalajara, Jalisco, Mexico (mean altitude of 1,570 m above sea level) and reported that a year prior she had the appearance of a tumor on the left lateral side of the neck that grew gradually, without causing symptoms, after having pharyngitis that resolved without complications. The patient did not mention any relevant family medical history. On direct physical examination, a painless tumor of ~6 cm on the left lateral side of the neck was observed at the height of the mandibular angle.
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No murmurs or rubs were palpated. There was a transverse displacement found, which was limited to the manipulation (Fontaine sign). Neurological examination revealed no changes. Results of the arterial blood gases, serum electrolytes, coagulation studies and blood count were all normal. Duplex Doppler ultrasound of the neck revealed a solid nodular lesion over the left carotid bifurcation without velocity changes and structures with high velocity blood flow compatible with vascular formations, which caused a displacement in the soft tissues of the neck and carotid bulb. There were no contralateral tumors found. Helical computed tomography (CT) with contrast administration showed a well-defined ovoid tumor with increase in density localized on the left side of the neck from the hyoid and with extension in a cephalad direction, with maximum diameter of 4.3 × 2.8 cm on the superior maxilla, in relation to the internal border of the carotid vessels, which were laterally displaced (Figures 1-3). Three-dimension reconstruction revealed a tumor on the left carotid bifurcation that demonstrated uptake and concentration of the contrast media, displacing the internal and external carotid of 8.7 × 4.4 × 3.8 cm. It was classified as Shamblin type IIIb (Figures 4-6). After informed consent was obtained from the parents and pre-anesthesia evaluation, the patient was surgically intervened with a left lateral cervicotomy. The carotid sheath was infiltrated by the tumor. A vascularized tumor ~4 × 3 × 3 cm was observed affecting the common carotid from its mid-third, the internal carotid up to the base of the skull and the external carotid up to its superior third, with a close relationship with the trachea, esophagus and spinal cord, with areas of induration from the posterior extension to the angle of the mandible that involved the hypoglossal, glossopharyngeal and vagus nerves.
López-Vázquez ME et al. Carotid body paraganglioma
Figure 1. Glomus tumor (4.3 × 2.8 cm) in a 16-yearold adolescent in connection with the internal margins of the carotid vessels, with maximum diameter in the upper maxilla.
Figure 3. Axial cut showing a left lateral solid neck tumor with heterogeneous uptake.
Figure 2. Contrast computed tomography of the neck showing a highly vascularized tumor that causes an opening of the carotid bifurcation.
Figure 4. Third-dimension supra-aortic reconstruction where the classic characteristics of a tumor of the carotid body are highlighted.
The tumor was resected in totality although it was not able to be separated from the vagus and
glossopharyngeal nerves; therefore, they were dissected. The obtained specimen was sent for
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stroma (Zellballen pattern), confirming the diagnosis of paraganglioma of the carotid body. During the postoperative period the patient had left palpebral ptosis, anisocoria with left myosis and dysphonia for which rehabilitation therapy was initiated, noting clinical improvement by the third week.
DISCUSSION The carotid body is a chemoreceptor located at the bifurcation of the primitive carotid artery in the adventitial layer of posterior mid-face, which proceeds from the mesoderm in the third brachial arch and the neural ectoderm from the neural crest and subsequently differentiates in the precursors of the paralymphatic cells.9-11 Figure 5. Image showing involvement of the common carotid bifurcation by part of the glomus tumor (arrow).
Figure 6. Angiotac coronal cut of the supra-aortic trunk, which revealed an 87 × 44 × 38 mm tumor in which involvement of the skull base is observed.
histopathological study, which revealed the presence of accumulations of oval cells with uniform hyperchromatic nuclei surrounded by vascular
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The case described here is thought to be relevant and of clinical interest because it is very rare for this type of tumor to be diagnosed in a patient of this age as the average in familial cases is 30 years of age and in sporadic cases is 55 years of age. This could lead to late diagnosis because the suspicion in young patients may be underestimated.1,5,6 It has been reported that paragangliomas increase in incidence in a direct relationship with altitude above sea level (1/1000 at the median level of the ocean waters, 9/1000 between 2000 and 3000 m and 12/1000 between 3600 and 4000 m above sea level) where the atmospheric numbers of oxygen are reduced, causing chronic hypoxemia and stress in type 1 carotid cells. When lack of oxygen is attempted to be compensated, it creates hyperplasia and neoplasia of the cells.1,12,13 Another factor in the absence of the stimulus of chronic hypoxia suggests that paragangliomas are the result of a genetic predisposition. Paraganglioma with a clear genetic component has been linked to mutations in the germinal line of the cycle related with genes of the succinate
López-Vázquez ME et al. Carotid body paraganglioma
dehydrogenase complex (SDH), in its subunits SDHB, SDHC, SDHD and SDHAF2 with different tissue and functional origin. The sporadic form is the most common; however, the familial pattern of autosomal dominance is recognized in 30% of the cases.1-3,7,8 The morphology of these tumors is defined and demarcated. They have an elastic consistency and are of reddish-brown color. They are located on the posterior face of the common carotid artery bifurcation. As the tumor grows, the anatomic relationships on the carotid bifurcation are gradually distorted, tending to “separate” the walls of the internal and external carotid arteries. Histologically, carotid body tumors follow a characteristic organ growth pattern referred to as the Zellballen pattern in which the individual tumor cells (predominantly type I) are polygonal and are arranged in different cellular nests.1,2,14 Its clinical presentation is of an asymptomatic, slow-growing tumor on the lateral neck and generally is diagnosed incidentally. When it has a large size it can cause symptoms due to the effect of compression (dysphagia, asphyxia, dysphonia, stridor, etc.). Growth of a paraganglioma in the carotid body is slow (5 mm/year).1,2,14 In terms of the diagnostic approach, Doppler ultrasound provides information about its concomitance with carotid atherosclerosis and the hemodynamics of these lesions. The procedure that confirms the disease is an arteriogram because one can observe the separation and widening of the internal and external carotid arteries as a result of a highly vascular tumor (Lyre sign) as well as providing detailed information about the anatomic relationships of the tumor and the carotid system with the adjacent structures.1,14-16 The treatment of choice of a carotid paraganglioma is surgical resection and its complexity is due to the size of the tumor, vascularization, adherence to the arterial wall and compromise
of the structures of the parapharyngeal space as well as the cranial nerves. According to Shamblin et al., paragangliomas of the carotids are classified according to their topography into three types: group I are tumors that are minimally adhered to the carotid body and therefore are thought to be of easy extraction. Group II tumors are larger in size with moderate adherence to the arterial plane for which careful resection of the subadventitia is required. Group III are large tumors that completely surround the arterial wall, are intimately adhered to the carotid bifurcation, are difficult to dissect from the arterial wall and occasionally require interposition of a vascular graft.17-19 In this case, the patient had a tumor that was classified as Shamblin type III that surrounded the common, external and internal carotid arteries. The operative mortality varied between 0 and 3%, with reports of postoperative transitory neurological deficit in 27 to 46% of patients, including paresthesia and cranial nerve paralysis.15,16 In conclusion, paraganglioma of the carotid body is a rare disease. Due to the lack of symptoms in its initial stage and its slow evolution, a clinical suspicion for its diagnosis is required. Early excision of the tumor is the indicated treatment and the morbidity and mortality they cause vary according to the size of the tumor. In the case described here, complete resection of the tumor was achieved with expected intraoperative events according to its classification (Shamblin III) as was dissection of the vagus and glossopharyngeal nerve branches. The patient is in rehabilitation and is progressing favorably with minimal functional sequelae.
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16. Dickinson PH, Griffin SM, Guy AJ, McNeill IF. Carotid body tumor: 30 years experience. Br J Surg 1986;73(1):14-16. 17. García Rojo M, Martínez García C, Gamallo Amat C, Patrón Romero M. New histopathologic data of prognostic value in extra-adrenal paragangliomas. Study of 9 cases. Med Clin (Barc) 1993;101(9):327-332. 18. Rutherford RB, Baker JD, Emst C, Johnston KW, Porter JM, Ahn SS. Cirugía Vascular. 6ta ed. Madrid, España: Elsevier, 2006. p. 2064-2093. 19. Shamblin WR, ReMine WH, Sheps SG, Harrison EG Jr. Carotid body tumor (chemodectoma). Clinicopathologic analysis of ninety cases. Am J Surg 1971;122(6):732739.
