Carotid body tumor: retrospective analysis on 22 patients

CONTEXT AND OBJECTIVE: Carotid body tumors, or chemodectomas, are the most common head and neck paragangliomas, accounting for 80% of the cases. They may present minor symptoms; however, they deserve special attention in order to achieve accurate diagnosis and adequate treatment. The objectives of this study were to show the approach towards chemodectomas and evaluate the complications of the patients treated surgically without previous embolization. DESIGN AND SETTING: Retrospective study on chemodectomas followed up at the Head and Neck Surgery Service, Department of Surgery, Unicamp. METHODS: Twenty-two patients were evaluated between 1983 and 2009. The diagnosis was based on clinical findings and imaging methods. The epidemiological characteristics, lesion characteristics, diagnostic methods, treatment and complications were analyzed. RESULTS: The paragangliomas were classified as Shamblin I (9%), II (68.1%) and III (22.7%). Angiography, magnetic resonance imaging and computed tomography confirmed the diagnosis in 20 patients (90.9%). Five (22.7%) had significant bleeding during the surgery, while four (18.1%) had minor bleeding. Four patients (18.1%) developed neurological sequelae. Seven (31.8%) needed ligatures of the external carotid artery. Three patients (13.6%) underwent carotid bulb resection. The postoperative follow-up ranged from 3 months to 14 years without recurrences or mortality. CONCLUSIONS: In our experience and in accordance with the literature, significant bleeding and neurological sequelae may occur in chemodectoma cases, particularly in Shamblin III patients. The complications from treatment without previous embolization were similar to data in the literature data, from cases in which this procedure was applied prior to surgery.


INTRODUCTION
Paragangliomas are tumors located along the human body's sympathetic and parasympathetic chains. They may grow along these fibers, and may be located in various parts of the body, such as the abdomen, chest, mediastinum, retroperitoneum and head and neck regions, but mostly associated with adrenal gland. The head and neck region is the most common site of extra-adrenal paragangliomas, accounting for approximately 70% of the cases, and the carotid body is responsible for the majority of these cases. Because of their location and vascularization, they can pose a great technical challenge for surgeons. 1 These tumors are often benign, presenting slow growth, 2 and are located in the upper cervical region. There is no evidence of gender predominance. They may only present minor symptoms, commonly only a pulsatile mass in the neck. However, they can cause local discomfort, dysphagia, hoarseness, stridor, vertigo and paralysis of the cranial nerves, and sometimes attain large volumes (some authors have described tumors as large as 10 cm). 1 They can be divided into tumors with either sporadic or familial traits. In the sporadic type, bilaterality has been reported in 5 to 10% of the cases. 3 The familial form is manifested through a dominant autosomal gene, and in these cases, bilaterality may reach up to 30%. 4 Recent studies have described a mutation along germinative lines, which may explain the etiology, through identification of six specific genes (RET, VHL, NF1 and subunits of SDH). 4 The hereditary form is mostly correlated with mutations in the SDHD gene. 5,6 The incidence in the general population is difficult to estimate. However, according to Rodriguez-Cuevas, 7 the incidence in the general population is about 0.01%. Since 1969, when Árias-Stella demonstrated carotid body enlargement in highaltitude Peruvian populations (due to the low oxygen pressure), it has been known that chronic hypoxia is an important factor in the etiology of this neoplasm. 8 The malignant potential is about 6% and the criteria are based on cell atypia, mitosis, local invasions and, especially, by the presence of metastasis. [9][10][11] The diagnosis is based on clinical history, physical examination, imaging methods (such as ultrasound, computed tomography and magnetic resonance) and vascular evaluations (including angiography, tomographic angiography and magnetic resonance angiography). 12,13 In this context, based on the Shamblin classification, Arya et al. used magnetic resonance imaging to pre-classify carotid body tumors before surgical treatment. 14 This could improve preoperative management and reduce the complication rate. 9 The best treatment for carotid body paragangliomas is a surgical approach. The literature shows that patients may or may not undergo prior embolization. Some authors have justified using embolization because it reduces complications such as bleeding or neurological sequelae, 15 although this procedure is not without its own inherent complications. 16

OBJECTIVES
The objectives of this study were to present an academic institution's experience of dealing with carotid body paragangliomas, such as the diagnostic methods, complementary examinations and treatment, and to show the possible complications that may occur over the natural evolution of the disease or in relation to surgery without previous embolization. Bleeding was measured in our study and was classified as minimal (less than 200 ml), moderate (ranging from 200 to less than 1000 ml) and significant (over 1000 ml), according to the need for blood transfusion. Thus, when the bleeding was minimal, blood transfusion was not needed. In cases of moderate bleeding, one or two red blood cell units were infused. Finally, when the bleeding was significant, more than two red blood cell units were infused.

This
The tumors were divided by means of the Shamblin classification, 8 according to the involvement of the carotid wall and difficulty of surgical resection. Shamblin I was reserved for tumors that were relatively small and easy to resect, with minimal or no adherence to the carotid wall. Shamblin II consisted of tumors with partial involvement of the carotid wall, and Shamblin III completely involved the carotid bifurcation.
All the patients underwent surgical treatment, without embolization or prior radiotherapy. The resection was complete in all patients, with a sub-adventitial avascular approach (Figure 1).

DISCUSSION
The carotid body is a structure that measures around 2 x 3 x 5 millimeters, located at the common carotid artery bifurcation, in the adventitia between the external and internal carotids. It contains chemoreceptors that are sensitive to hypoxia, hypercapnia and acidosis, and aims to maintain the body's homeostasis and blood pressure. As reported by Kapoor et al., this structure was first described by Von Haller in 1743. 6 The incidence of this tumor is greater at higher altitudes, due to the chronic hypoxia. 7  seems to be preferable nowadays. 14 In the literature, the best treatment is considered to be surgical, with dissection of the tumor in the sub-adventitial avascular plane of the artery. 12 Large tumors (Shamblin II and III) may require vascular procedures, including repairs, sutures and resections of the arterial segments. 19 At times, it may be necessary to sacrifice the external carotid artery, perform anastomosis between the internal and common carotid arteries or undertake vascular reconstruction with grafts. [11][12][13]20,21 Some authors have described use of a stent inserted into the internal carotid artery before the surgery, in cases presenting as Shamblin III with complete involvement of this artery. 22 Occurrences of technical complications in anastomoses between the common and internal carotid arteries after resection of the carotid body have also been reported in the literature. These cases evolved with several hematomas and, in some cases, with stroke caused by deficits of cerebral irrigation. 8,13,23 This complication did not occur in our series.
In patients with bilateral tumors, obviously, the procedures should not be done at the same time, but spaced out one from another, especially because of possible vascular or cranial nerve lesions. 8  bleeding, but the patients that they followed up did not present any differences in definitive neurological sequelae. 16 Although our series did not have any cases of malignant chemodectoma, it is important to mention that the malignant potential has been reported to be around 2-6 % in the literature, most frequently with metastasis to regional lymph nodes. 8,23 Some authors have prescribed chemotherapy for metastasized cases. 31 Finally, although we did not have any cases of mortality, the literature mentions a mortality rate of less than 2%. 1

CONCLUSIONS
Complementary imaging study methods such as ultrasonography, computed tomography, magnetic resonance or, especially, arteriography need to be included in evaluations today, in order to analyze the involvement of the carotid artery and to program the surgical treatment for carotid body tumors.
This study, in agreement with the literature, demonstrated that significant bleeding and neurological sequelae may occur, and that this risk increases according to the Shamblin classification, particularly in Shamblin III patients. Even though preoperative embolization may be an important alternative, the complications observed in treatment without previous embolization were similar.