Carotid body tumor: Surgical management and complications

Ishwar Singh; Ravi Meher; Padam Singh Bhandari; Karandeep Singh

doi:10.4103/jhnps.jhnps_62_21

ORIGINAL ARTICLE

Year : 2021 | Volume : 9 | Issue : 2 | Page : 153-158

Carotid body tumor: Surgical management and complications

Ishwar Singh¹, Ravi Meher¹, Padam Singh Bhandari², Karandeep Singh¹
¹ Department of ENT, Maulana Azad Medical College and Associated Lok Nayak Hospital, New Delhi, India
² Department of Burns and Plastic Surgery, Maulana Azad Medical College and Associated Lok Nayak Hospital, New Delhi, India

Date of Submission	18-Oct-2021
Date of Acceptance	24-Oct-2021
Date of Web Publication	17-Dec-2021

Correspondence Address:
Dr. Ravi Meher
Department of ENT, Maulana Azad Medical College, New Delhi
India

Source of Support: None, Conflict of Interest: None

Check

DOI: 10.4103/jhnps.jhnps_62_21

Abstract

Introduction: Carotid body tumors (CBT) or paragangliomas account for approximately 3% of all paragangliomas occurring in the head-and-neck region. Delay in the surgical resection of tumors may be associated with high morbidity or mortality and risk of malignant transformation. Methodology: Three cases of CBTs were included in the study, out of which one case presented as bilateral neck swelling. All the patients were clinically and radiologically evaluated and taken up for surgical excision of the tumor. In case with bilateral tumor, a staged removal was planned. Results: Out of three patients, a female patient developed stroke postoperatively, she was managed and discharged in stable condition, and another male patient developed left vagal palsy. Conclusion: Excision of shambling Type III CBTs is difficult and one should know the collateral circulation of the tumor preoperatively. Bilateral CBT resection requires staging procedures to reduce the risk of cardiovascular and neurological issues.

Keywords: Bilateral, carotid body tumor, paraganglioma, resection

How to cite this article:
Singh I, Meher R, Bhandari PS, Singh K. Carotid body tumor: Surgical management and complications. J Head Neck Physicians Surg 2021;9:153-8

How to cite this URL:
Singh I, Meher R, Bhandari PS, Singh K. Carotid body tumor: Surgical management and complications. J Head Neck Physicians Surg [serial online] 2021 [cited 2023 Jun 4];9:153-8. Available from: https://www.jhnps.org/text.asp?2021/9/2/153/332726

Introduction

Carotid body tumors (CBTs) or paragangliomas or chemodectomas are rare tumors originate from paraganglionic tissue derived from the neural crest present though out the body. CBTs are the most common head-and-neck paragangliomas. The reported incidence of CBTs is 1–2 per 100,000.^[1],[2] They are generally benign, usually unilateral; and there is no report of spontaneous regression.^[3] CBTs grow slowly and rarely metastasize.^[4] CBTs arise from the carotid bodies present at the bifurcation of common carotid artery (CCA). B/L CBT in females is a rare entity. The association between CBTs and stroke has not been clearly demonstrated in the literature; however, cerebrovascular accidents are serious postoperative complications.^[5] Complete surgical resection is the primary modality of management for the CBT. In this paper, we reported three cases of CBT, one bilateral and two unilateral which were successfully treated with complete surgical excision via cervical approach and reviewed the current literature, mainly highlighting the case with the bilateral tumor. Surgical excision in case of bilateral tumor is challenging in terms of the decision of which side to operate, preembolization needed or not, whether both sides to be operated in a single setting or not and the complication associated.

Clinical Presentation

Case 1

A 45-year-old female presented with bilateral neck swelling [Figure 1], left side greater than of right side for 1 year and 6 months, respectively, with no pressure symptoms or neurological symptoms. On palpation, swellings were nontender with smooth surface, well-defined margins, and firm in consistency with positive Fontaine sign. Further imaging studies were ordered, contrast-enhanced computed tomography (CECT) angiography [Figure 2] showed two well-defined intensely enhancing soft tissue mass lesions in bilateral carotid space with splaying of external carotid artery (ECA) and internal carotid artery (ICA). Magnetic resonance imaging (MRI) [Figure 2] showed well-defined soft tissue mass lesions in bilateral carotid space which were iso-intense on T1, hyperintense on T2 with multiple tubular and curvilinear T2 flow voids within. Abdominal ultrasonography and noncontrast computed tomography (NCCT) of the head were done, showing no abnormal findings. We planned to surgically resect the larger tumor first based on the reviewed literature. Therefore, the patient underwent surgical resection of the left-side tumor first [Figure 3]. A left transverse cervical incision was made, subplatysmal flaps raised; sternocleidomastoid muscle retracted laterally and carotid sheath exposed; internal jugular vein dissected from carotid sheath and retracted laterally; tumor found engulfing the CCA which was protected using tapes; ICA separated from the tumor; and ECA could not be freed from tumor, feeders ligated from inferior pole. It was only after ECA ligation that the tumor was completely removed. Postoperative histopathology report showed a typical Zellballen pattern of arrangement of nest cells [Figure 4] separated by sustentacular cells. The tumor was positive for synaptophysin, chromogranin, and neuron-specific enolase suggestive of paraganglioma. In postoperative period, the patient developed right hemiparesis. NCCT of the head showed left frontotemporoparietal region infarct with midline shift of 8 mm [Figure 2] and MRI of the brain revealed subacute infarct with hemorrhagic transformation in middle cerebral artery territory. The patient was started on mannitol, atorvastatin, and ecosprin after neurology consultation. With extensive physiotherapy and medical management, she was able to walk and was discharged in stable condition with minimal weakness of limbs.

Figure 1: Showing the clinical image of case 1 with bilateral carotid body tumor

Click here to view

Figure 2: Radiological images of the patient suggestive of carotid body tumor and postoperative image of subacute infarct. (a) Contrast enhanced computed tomography angiography showing CBT with Lyre's sign, (b) Angiographic image similar to Figure 2, Image a, with reverse contrast characteristics compared to a, (c) Magnetic resonance imaging scan showing CBT, and (d) Non-contrast computed tomography scan done in postoperative period showing left frontotemporoparietal infarct

Click here to view

Figure 3: Intraoperative images of case 1

Click here to view

Figure 4: Postoperative HPE slide (H and E, ×400) of carotid body tumor showing typical nest cells in Zellballen pattern

Click here to view

Case 2

A 35-year-old female patient was presented with swelling on the left cervical region [Figure 5]. Physical examination and computed tomography (CT) angiography revealed a well-defined intensely enhancing soft tissue mass lesion in carotid space with splaying of ECA and ICA mass on right carotid bifurcation that was considered as CBT. Her lesion was found to be Shamblin Type III intraoperatively. The patient underwent complete surgical resection of the tumor and postoperative histopathology revealed features suggesting paraganglioma. Postoperatively, the patient developed left vagal paresis as a complication of surgery. The patient was given a course of steroids, and speech therapy was also given concurrently; after a month, the patient improved, as confirmed with the endoscopic examination.

Figure 5: Showing images of case 2 clinical picture, computed tomography angiography image, and intraoperative shambling Type III carotid body tumor

Click here to view

Case 3

A 20-year-old male patient presented to the outpatient department with gradually increasing swelling in the left side of the neck [Figure 6]. Physical examination and CT angiography (CTA) revealed a mass on left carotid bifurcation that was considered as CBT. Intraoperatively, the lesion was classified as Shamblin Type II. Complete surgical excision of the tumor was done with no intraoperative or postoperative complication.

Figure 6: Showing case 3 clinical picture and computed tomography angiography image of the carotid body tumor

Click here to view

Discussion

CBTs are very rare; however, they are the most common form of paraganglioma of the head-and-neck region, with a female predominance in the fifth and sixth decades of life.^[6],[7] CBTs are commonly seen in females, probably due to the chronic hypoxic stimulation that women may have because of the monthly erythrocyte loss caused by menstruation. Women living at high altitudes (more than 2200 m above sea) seem to be more sensitive to this pathology because the hypoxic stress is higher,^[8] also there is a genetic role in the development of CBTs.^[9] Patients usually present between the fifth and seventh decades of life with an asymptomatic lateral neck mass in the anterior triangle of the neck. Bilateral CBTs have an incidence of approximately 10%.^[10] CBTs are slow-growing neoplasms that can remain asymptomatic for many years. The median growth rate is 1.0 mm/year and the median tumor doubling time is 4.2 years; therefore, a “wait and scan” policy might be justified in some cases.^[11] Despite being a benign and slow-growing tumor, surgical resection of CBTs is the treatment of choice.^[12] CBTs have a small risk of malignancy (around 5%); however, all CBTs should be viewed as having malignant potential. According to the tumor size, CBTs are divided into three groups according to the Shambling classification system:^[13] Class 1: without encasement of the vessel wall, tumor size <5 cm, and no widened carotid bifurcation; Class 2: tumor attached to the blood wall but without encasement; and Class 3: tumor attached to blood vessel with encasement of the blood wall and tumor size larger than 5 cm with widened carotid bifurcation. Preoperative imaging provides information about the size and vascularity of the tumor, level of bifurcation, the shambling type, and nature of the vessel wall. Earlier digital subtraction angiography (DSA) was regarded as the gold standard for the final diagnosis;^[7] however, due to unavailability and high cost of this facility, it is not used commonly as a diagnostic modality. Currently, CTA and MRI are used for the diagnosis of CBT as these techniques are able to define the size and margins of the tumor mass, and the adherence of the tumor mass to the peripheral tissues.^[15],[16] We did not get any preoperative embolization in any of our patients. According to the study by Hua et al.,^[17] preoperative DSA and transarterial embolization are not recommended for patients with CBT because of its invasive nature. Moreover, these studies have limitations like, poor delineation of the adherence of the tumor mass to the peripheral tissues prior to surgery, ectopic embolism and vascular rupture. In addition, a high risk of cardiac arrest was observed in patients with carotid body hypersensitivity. DSA is now being replaced by the emerging CTA, which provides an accurate angiogram and adds the advantage of detecting the extent and the relation to the skull base and surrounding structures in case of large CBTs.^[18]

In a retrospective study of 58 patients of CBT by Hua et al.,^[17] tumor resection, without reconstruction and ligation of the CCA, may be done for patients with Shamblin Grade III tumors. Reconstruction or ligation causes potential damage to the nervous system and is only required in patients with tumor cells invading the middle layer and tunica intima of the carotid artery. In some cases, endovascular embolization may be performed prior to surgery, using liquid agents or coils to reduce the tumor size or intraoperative complications, such as bleeding.^[19] In selected cases, conventional radiotherapy or stereotactic radiosurgery may be treatment options.^[20] There has been controversy concerning the usefulness of preoperative embolization. Some authors prefer routine preoperative embolization because it can lower blood flow and decrease tumor size and decrease the length of hospital stay.^[21],[22] Others have similar findings that selective preoperative embolization can facilitate tumor excision with less blood loss, particularly in larger tumors (Shamblin Type II and III).^[23],[24] There are some groups who disagree on preoperative routine embolization due to postembolization morbidity, such as the potential risk of stroke by embolic particles.^[23],[25]

CBT surgery can be challenging because of neurovascular structures that are adjacent to or involved in the tumor. This is particularly true for larger CBTs that encompass the carotid arteries, as evidenced by the fact that strokes were encountered after resection of a Shamblin III. It has been suggested that the decrease in blood loss might reduce perioperative morbidity which can be achieved effectively by creating a craniocaudal dissection route whereby the tumor feeder vessels are ligated before the tumor and ICA are manipulated.

Bilateral CBTs are difficult to treat, they require an accurate preoperative imaging study, and they bring a higher rate of complications intraoperative and postopertively.^[14] Moreover, there is a risk of damage to the Hering nerve (a branch of ninth nerve innervates carotid sinus and carotid body) during surgical excision of tumor. In a retrospective study of 49 patients by Lamblin et al.,^[26] 12 patients of CBT were operated, of which 9 were bilateral. Six patients with bilateral CBP underwent bilateral resection, with the smaller tumor generally treated in the first step. In some cases, other treatments were proposed for the contralateral CBT like radiation therapy (due to ipsilateral vagus nerve lesion during the first procedure), or medical surveillance. Bilateral resection of the Hering nerve provokes labile blood pressure, headache, diaphoresis, and emotional instability.^[27] According to some authors for bilateral CBTs, it is better to resect the smaller tumor first, in order to increase the probability of preserving at least one functional branch of adjacent neurovascular structures. In our patient, we planned to resect the tumor of the left side first because of its rapid progression and risk of malignant change. Both sides were not planned to be resected in the same setting due to the risk of injury to the bilateral Hering nerves and their consequences and risk of injury to major neurovascular of both the sides. Regarding postoperative complications, the incidence of stroke with CBT is reported to be as high as 11%.^[5] The other reported postoperative neurological complications are typically nerve palsies.^[28] In our case, the complication could be due to dislodgement of thrombus due to prolong handling of carotid vessels, as the tumor was Grade 3 and completely encircling the vessel. Hence, gentle handling of the vessel should be done during the surgery. Radiotherapy is indicated for very large size and recurrent tumors. It is also indicated for malignant transformation with metastasis to the regional lymph node.^[29] Vascular repair in case of intraoperative vascular injury has become safer with improved surgical techniques: early control of proximal and distal carotid vessels, subadventitial tumor dissection, effective heparin therapy, precise hemodynamic control, and reduced clamping time have all reduced postoperative risk. Higher Shamblin grade and larger tumor size correlate with higher risk of intraoperative vascular lesion, thus both allowed prediction of risk.^[30] This case is reported because of its rarity, highlighting difficulty in surgical management and the cause of stroke in postoperative period and recovery. However, despite the difficulties faced, the patient had a good outcome and was currently doing well.

There is a role of genetic testing also in CBT as it can of familial variety. Succinate dehydrogenase (SDH) is an enzyme in mitochondria responsible for oxidative phosphorylation, intracellular oxygen sensing, and signaling. SDH is a part of the mitochondrial electron transport chain and catalyzes the oxidation of succinate into fumarate in the Krebs cycle. SDH mutations cause dysregulation of hypoxia leading to paraganglia hypertrophy and also cause inactivation of factors that causes apoptosis in paraganglionic cells. All these lead to uncontrolled growth of paraganglionic cells.

Approximately 30% of all paragangliomas are caused by mutation of genes associated with the mitochondrial SDH complex and follow autosomal dominant inheritance. The three genes of SDH complex which can be affected by mutation are Succinate dehydrogenase-D (SDHD), Succinate dehydrogenase-B (SDHB), Succinate dehydrogenase-C (SDHC). SDHD is the most common mutation, followed by SDHB and then SDHC.^[31]

SDHB mutation is associated with malignant change in sympathetic paraganglioma
SDHC mutations are associated with CBT paragangliomas
SDHD mutations are related to multifocal head-and-neck paragangliomas, such as bilateral CBTs, adrenal pheochromocytoma, extra-adrenal pheochromocytoma, and multifocal benign tumors.

Since the mutation of SDHD gene is associated with multifocal PGLs, all patients with this mutation should undergo yearly MRI or CECT and indium-111 octreotide body scan to look for other possible PGL.^[32]

Conclusion

Bilateral CBTs are rare tumors, meticulous surgical techniques, as well as knowledge of the anatomy of the region, are of paramount importance for decreasing cranial nerves lesions during surgical resection of these tumors. Excision of Shamblin Type III CBTs is difficult, and therefore, one should know the collateral circulation of the tumor and preoperative balloon occlusion test can be useful in such cases. Bilateral CBT resection requires staging procedures to reduce the risk of cardiovascular and neurological issues. As the tumor enlarges, over the course of several years, it may cause neurological or pressure symptoms or rarely undergo metastatic change, more frequently than it was thought previously, CBT may secrete catecholamines, leading to the complications associated with them. For these reasons, surgical resection remains the treatment of choice for these diseases. Careful attention should be made only for those cases in which the tumor is very large or the patient is elderly. There is also a role of genetic analysis of SDH in the management of CBT and must be performed where ever it is available and feasible.

Summary

CBTs are rare tumors of head-and-neck region
Complete surgical resection is the main modality of treatment
Bilateral carotid tumor surgery needs proper planning as to which side to be operated on firs and why
Shamblin Type III CBTs are difficult to resect and commonly associated with the complications intraoperative or postoperative
Collateral circulation of the CBT should be known before planning for resection of Type III tumors
Handling of the major vessels during resection of tumor is of paramount importance.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

Disclosure

This material has never been published and is not currently under evaluation in any other peer reviewed publication.

Ethical approval

The permission was taken from Institutional Ethics Committee prior to starting the project. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

1.	Sevilla García MA, Llorente Pendás JL, Rodrigo Tapia JP, García Rostán G, Suárez Fente V, Coca Pelaz A, . Head and neck paragangliomas: Revision of 89 cases in 73 patients. Acta Otorrinolaringol Esp 2007;58:94-100.
2.	Jena A, Reddy GV, Kadiyala V, Brinda K, Patnayak R, Chowhan AK. A case of large carotid body tumor: Surgical challenge. Indian J Vasc Endovasc Surg 2016;3:96-8. [Full text]
3.	Wang SJ, Wang MB, Barauskas TM, Calcaterra TC. Surgical management of carotid body tumors. Otolaryngol Head Neck Surg 2000;123:202-6.
4.	Mathew BK, Bandgar T, Menon PS, Shah NS. Carotid body tumours: Three case reports. Singapore Med J 2009;50:e58-60.
5.	Sajid MS, Hamilton G, Baker DM, Joint Vascular Research Group. A multicenter review of carotid body tumour management. Eur J Vasc Endovasc Surg 2007;34:127-30.
6.	Patlola R, Ingraldi A, Walker C, Allie D, Khan IA. Carotid body tumor. Int J Cardiol 2010;143:e7-10.
7.	Ma D, Liu M, Yang H, Ma X, Zhang C. Diagnosis and surgical treatment of carotid body tumor: A report of 18 cases. J Cardiovasc Dis Res 2010;1:122-4. [PUBMED] [Full text]
8.	Luna-Ortiz K, Rascon-Ortiz M, Villavicencio-Valencia V, Granados-Garcia M, Herrera-Gomez A. Carotid body tumors: Review of a 20-year experience. Oral Oncol 2005;41:56-61.
9.	Rodríguez-Cuevas S, López-Garza J, Labastida-Almendaro S. Carotid body tumors in inhabitants of altitudes higher than 2000 meters above sea level. Head Neck 1998;20:374-8.
10.	Amato B, Serra R, Fappiano F, Rossi R, Danzi M, Milone M, . Surgical complications of carotid body tumors surgery: A review. Int Angiol 2015;34:15-22.
11.	Jansen JC, van den Berg R, Kuiper A, van der Mey AG, Zwinderman AH, Cornelisse CJ. Estimation of growth rate in patients with head and neck paragangliomas influences the treatment proposal. Cancer 2000;88:2811-6.
12.	Wieneke JA, Smith A. Paraganglioma: Carotid body tumor. Head Neck Pathol 2009;3:303-6.
13.	Shamblin WR, ReMine WH, Sheps SG, Harrison EG Jr. Carotid body tumor (chemodectoma). Clinicopathologic analysis of ninety cases. Am J Surg 1971;122:732-9.
14.	Makeieff M, Raingeard I, Alric P, Bonafe A, Guerrier B, Marty-Ane C. Surgical management of carotid body tumors. Ann Surg Oncol 2008;15:2180-6.
15.	Tang F, Han D, Qu S, Liang J, Liu B, Huang Y. Diagnosis and management of jugulare glomus tumor and carotid body tumor. Lin Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 2014;28:612-7.
16.	Derchi LE, Serafini G, Rabbia C, De Albertis P, Solbiati L, Candiani F, Carotid body tumors: US evaluation. Radiology 1992;182:457-9.
17.	Hua Q, Xu Z, Jiang Y. Diagnosis and surgical treatment of carotid body tumor: A retrospective analysis of 58 patients. Oncol Lett 2017;14:3628-32.
18.	Sanlı A, Oz K, Ayduran E, Aydın S, Altın G, Eken M. Carotid body tumors and our surgical approaches. Indian J Otolaryngol Head Neck Surg 2012;64:158-61.
19.	Cvjetko I, Erdelez L, Podvez Z, Buhin M, Vidjak V, Borovecki A, Coil embolization and surgical removal of carotid body paraganglioma. J Craniofac Surg 2013;24:e242-5.
20.	Erdogan BA, Bora F, Altin G, Paksoy M. Our experience with carotid body paragangliomas. Prague Med Rep 2012;113:262-70.
21.	DuBois J, Kelly W, McMenamin P, Macbeth GA. Bilateral carotid body tumors managed with preoperative embolization: A case report and review. J Vasc Surg 1987;5:648-50.
22.	Schick PM, Hieshima GB, White RA, Fiaschetti FL, Mehringer CM, Grinnell VS, . Arterial catheter embolization followed by surgery for large chemodectoma. Surgery 1980;87:459-64.
23.	van der Bogt KE, Vrancken Peeters MP, van Baalen JM, Hamming JF. Resection of carotid body tumors: Results of an evolving surgical technique. Ann Surg 2008;247:877-84.
24.	Kasper GC, Welling RE, Wladis AR, CaJacob DE, Grisham AD, Tomsick TA, A multidisciplinary approach to carotid paragangliomas. Vasc Endovascular Surg 2006;40:467-74.
25.	Litle VR, Reilly LM, Ramos TK. Preoperative embolization of carotid body tumors: When is it appropriate? Ann Vasc Surg 1996;10:464-8.
26.	Lamblin E, Atallah I, Reyt E, Schmerber S, Magne JL, Righini CA. Neurovascular complications following carotid body paraganglioma resection. Eur Ann Otorhinolaryngol Head Neck Dis 2016;133:319-24.
27.	Robertson D, Hollister AS, Biaggioni I, Netterville JL, Mosqueda-Garcia R, Robertson RM. The diagnosis and treatment of baroreflex failure. N Engl J Med 1993;329:1449-55.
28.	Sen I, Stephen E, Malepathi K, Agarwal S, Shyamkumar NK, Mammen S. Neurological complications in carotid body tumors: A 6-year single-center experience. J Vasc Surg 2013;57:64S-8S.
29.	Naik SM, Shenoy AM, Nanjundappa, Halkud R, Chavan P, Sidappa K, . Paragangliomas of the carotid body: Current management protocols and review of literature. Indian J Surg Oncol 2013;4:305-12.
30.	Lim JY, Kim J, Kim SH, Lee S, Lim YC, Kim JW, . Surgical treatment of carotid body paragangliomas: Outcomes and complications according to the shamblin classification. Clin Exp Otorhinolaryngol 2010;3:91-5.
31.	Berger G, Łukasiewicz A, Grinevych V, Tarasów E. Carotid body tumor – Radiological imaging and genetic assessment. Pol Przegl Chir 2020;92:39-44.
32.	Antonello M, Piazza M, Menegolo M, Opocher G, Deriu GP, Grego F. Role of the genetic study in the management of carotid body tumor in paraganglioma syndrome. Eur J Vasc Endovasc Surg 2008;36:517-9.