Carotid chemodectomas: questions to ensuring radicality, efficacy, and safety of surgical treatment

• Alexey A. Fokin
• Sergey P. Zotov
• Roman V. Skorobogachev
• Alexey V. Sazanov
• Vladimir V. Vladimirskij
• Sergey S. Zaytsev
• Oleg S. Tereshin

Abstract

Background. In Russia and the world, there is an increase in the number of cancer patients with localization on the head and neck. According to the Global Cancer Observatory (GLOBOCAN), 890.000 new cases of head and neck cancer and 450.000 deaths were registered in 2018, with a forecast of a 30% increase in the incidence by 2030. Carotid chemodectomas (CC) account for 0.5% of all head and neck tumors. The frequency of occurrence is estimated as 1 per 30000–100000 people. CCS in most patients are benign, but 10% may be malignant.

The aim to determine the rational surgical tactics in patients with carotid hemodectomas, from the standpoint of the radicality, effectiveness and safety of the operation.

Study design: a retrospective, multicenter study.

Material and methods. An analysis was conducted of the medical records of 80 patients with CBTs who underwent treatment in the vascular surgery departments of Regional Clinical Hospital No. 3, City Clinical Hospital No. 8, Chelyabinsk Regional Clinical Hospital and Chelyabinsk Regional Clinical Center of Oncology and Nuclear Medicine in Chelyabinsk from 1985 to 2025. In particular, the results of instrumental research methods were assessed and a histological analysis of the obtained biopsy materials was performed. The literature search, as well as the systematization and analysis of information, was conducted from scientific literature sources located in the PubMed, Web of Science, and Elibrary databases.

Results. When writing the work, a literature search was conducted, as well as an analysis of the most significant clinical observations of patients with CС, including those with signs of malignancy, bilateral lesion, hereditary history, as well as a combination of tumors with atherosclerotic lesions of the internal carotid artery and the development of critical stenosis.

Conclusion. To ensure the radicality, efficacy, and safety of carotid body tumor removal, the following principles should be considered: for type III tumors according to the Shamblin classification, as well as for tumors with malignant properties, en bloc resection followed by internal carotid artery reconstruction is advisable. The sequence of tumor removal in bilateral cases is determined by their size, Shamblin classification, and the presence of symptoms. Simultaneous bilateral tumor removal should not be performed due to the risk of fatal complications. Lymph node dissection should be performed in cases of enlarged lymph nodes in the surgical area, tumor recurrence, and aggressive or malignant tumor forms. Preoperative embolization of branches of the external carotid artery prior to surgical tumor removal has not proven its effectiveness. Patients with carotid body tumors, especially those with a family history or multiple tumors, are recommended to undergo genetic testing.

Keywords:  carotid chemodectoma; Shamblin classification; internal carotid artery repair

Introduction

Carotid chemodectomas (CCs), hereinafter synonymously also referred to as carotid body tumor/s (CBTs) or carotid paraganglioma/s, are rare tumors developing from chemoreceptor cells in the area of the carotid sinus. An important peculiarity of CC is intimal adherence to carotid arteries (CA) and pronounced vascularization. The innervation of the carotid glomus is provided by a branch of the glossopharyngeal nerve. The tumor is supplied with blood from CAs – mainly from the external carotid artery (ECA), thyrocervical trunk and vertebral artery [1–3]. CC accounts for 0.5% of all head and neck tumors. CCs are the most common type accounting for approxi­mately 60–70% of all chemodectomas. The incidence is estimated as 1 per 30 000–10 0000 people. This type of tumors is observed more often in women, with a 2:1 female-to-male ratio. The average age at diagnosis is 40–50 years [4–6]. 30–40% of patients have family forms associated with mutations in genes SDHB, SDHC, SDHD (succinate dehydrogenase complex). The majority of CCs are benign, however about 10% may be malignant. The latest consensus conclusion of the World Health Organization (WHO) stated that all chemodectomas should be assigned to malignant tumors [7–9]. Formation of the program of treating any tumors, including CC, requires a multidisciplinary approach with an obligatory examination by an oncologist.

In most patients, CCs are asymptomatic. Usually, this is a slow-growing painless neoplasm. The appearing symptomatology is commonly characteristic of an extensively growing tumor: discomfort or local painfulness, dysphagia, dizziness, tinnitus, impairments from the part of cerebral nerves (dysphonia in involvement of the vagus nerve or branches of the glossopharyngeal nerve, Horner syndrome – ingrowth or compression of the sympathetic cervical plexus), as well as transient ischemic cerebral attacks. A systolic murmur may be heard in the projection of the tumor. In the overwhelming majority of patients, CCs are unilateral, however 10–30% have bilateral location, more often in hereditary forms [5, 10].

A screening diagnostic method is an ultrasonographic examination of the brachiocephalic arteries with Doppler sonography, making it possible to visualize the tumor, assess its blood supply, and connection with the CA. The “gold standard” is multislice computed tomography (MSCT)-angiography during which it is possible to determine the exact size of the neoplasms, localization and interrelations with the surrounding structures. Contrast enhancement makes it possible to assess blood supply of the tumor, as well as the presence of an atherosclerotic lesion of the carotid basin. Puncture angiography also provides optimal information about tumor blood supply and the state of the carotid basin, however not allowing for the full assessment of the interrelationship with the surrounding tissues. Besides, angiography is an invasive method of examination thus also limiting its application. Tumor biopsy prior to operation is not recommended due to the risk of bleeding, formation of false aneurysms and tumor dissemination, as well as low informative value. Surgical removal of the tumor is the main method of treatment of this pathology [2, 11].

While writing the work, we carried out search of literature on the subject of CC, supplemented by analyzing clinical cases from own practice, evaluating the signs of malignancy, bilateral character of the lesion, hereditary history, as well as a combination of CC with atherosclerotic lesions of the internal carotid artery (ICA) and the development of critical stenosis.

Objective. To determine the rational surgical tactics in patients with CCs from the standpoint of radicality, efficacy and safety of the operation.

Patients and methods

We performed a retrospective analysis of case histories of patients who underwent treatment in the vascular surgery departments of the Regional Clinical Hospital № 3, City Clinical Hospital № 8, Chelyabinsk Regional Clinical Hospital and Chelyabinsk Reginal Clinical Center of Oncology and Nuclear Medicine from 1985 to 2025, with a total of 80 patients operated on over that period. There were 46 (57.5%) women and 34 (42.5%) men, with the mean age amounting to 52.5 years. During the past15 years, we used ultrasound examination (USE) as screening diagnosis. Besides, MSCT was performed. At an earlier stage of the development of diagnosis, it was possible to identify the disease by means of subtraction digital angiography. According to the classification of W.R. Shamblin (1971), carotid body tumors of type I, type II and type III were diagnosed in 7, 54 and 19 patients, respectively.

All gross specimens of the removed tumors were examined histologically, with hematoxylin and eosin stain.

Literature search, as well as systematization and analysis of the information were carried out from the sources of scientific literature in the bases PubMed, Web of Science, eLibrary.

Results

During the reporting period, a total of 80 patients were operated on for CC, including those with signs of malignancy, bilateral lesions, hereditary history, as well as a combination of the tumor with atherosclerotic lesions of the ICA and the development of critical stenosis.

Of the 80 patients, five (6.25%) patients were found to have bilateral CC, with this pathology diagnosed in close relatives: a father and son.

Case report 1

69-year-old patient C. during one year complained of a painless, dense formation on the neck on both sides. The MSCT findings revealed signs of a bilateral CBT measuring 28 mm on the right and 25 mm on the left, classified as Shamblin II (Fig. 1).

The first stage consisted in removal of the smaller CC (on the left) with preservation of precerebral arteries. A month later, the second stage was to remove the CC on the right: en bloc resection of the tumor with the involved vessels and autovenous prosthetic repair of the right ICA with a fragment of the great saphenous vein. The scope and character of the operation was dictated by tightness of the tumor to the CA. After the first operation there were no signs of neuropathy, the second one was followed by hoarseness of voice, difficulty swallowing due to neuropathy of the glossopharyngeal and hypoglossal nerves. After the rehabilitation measures, the signs of neuropathy regressed completely. Later on, a CBT was diagnosed in the patient’s son.

The tumors in seven (8.75%) patients turned out to be malignant: tumor size exceeding 5 cm, ingrowth of the tumor into the surrounding tissues, with the tumors classified as Shamblin III in all seven patients. Three patients were found to have metastases to the regional lymph nodes.

Case report 2

76-year-old patient M. complained during a year of the presence of a painless, dense formation on the right side of the neck. The findings of MSCT-angiography revealed a right-sided CC measuring 50 mm and classified as Shamblin III (Fig. 2).

Intraoperatively: a 5×4 cm neoplasm, significantly vascularized, of dense consistency, circularly encasing the ICA and ECA. The hypoglossal nerve grew into the tumor, thus requiring resection of the nerve followed by its suturing perineurally. Taking into account the peculiarities of tumor growth, a decision was made upon en bloc resection of the tumor with the involved vessels. Common carotid to internal carotid artery autovenous prosthetic repair with a fragment of the great saphenous vein was performed, followed by cervical lymphadenectomy.

Histological examination: the tumor is represented by oval-shape islets of cells with eosinophilic cytoplasm, surrounded by thin interlayers of connective tissue. In places, cells with moderate atypia. No mitoses revealed, with the cells growing into the outer layer of the artery. A malignant nature of the tumor with metastases to the cervical lymph nodes was confirmed. The patient was postoperatively diagnosed as having neuropathy of the glossopharyngeal and hypoglossal nerves on the right, manifesting itself as hoarseness of voice, difficulty swallowing. After rehabilitation measures the signs of neuropathy significantly decreased.

In 2 (2.5%) patients, CCs were combined with atherosclerotic critical stenosis of the ICA.

Case report 3

62-year-old patient F. complained for 3 years of the presence of a painless, dense formation on the left side of the neck, headache, with a history of cerebral infarction in the left carotid basin 3 months before admission to hospital. The findings of ultrasonographic Doppler scanning of the brachiocephalic arteries revealed a 90% stenosis of the left ICA, as well as a formation in the left carotid sinus. It was followed by cerebral angiography and MSCT-angiography (Fig. 3), confirming the diagnosis.

CC on the left was removed, followed by eversion endarterectomy from the left internal, external and common carotid arteries. Intraoperatively: a volumetric CA-separating solid formation measuring 27×34 mm with own vascular network, a 90% stenosis of the left ICA (Fig. 4).

Histology: mature paraganglioma with a distinct capsule without tumorous infiltration. In the lymph nodes the picture of follicular hyperplasia, with no tumor growth.

There were no events of neuropathy in the postoperative period.

While performing operations, we managed to spare the native arteries in 53 (66.25%) patients. A further 6 (7.5%) patients were subjected to resection of the ECA and 19 (23.75%) patients underwent en bloc resection. 2 (2.5%) patients required surgery for tumor recurrence. Intraluminal shunt was not used. There were no lethal outcomes. The signs of neuropathy due to lesions of cranial nerves (vagus nerve, hypoglossal nerve, glossopharyngeal nerve, branches of the facial nerve) were observed in 18 (23%) patients.

Discussion

The carotid body is a highly specialized organ performing functions of a chemoreceptor sensitive to fluctuations of arterial blood pO₂, pCO₂ and pH levels. Stimulation of the carotid body induces reflex changes in the vasomotor and respiratory activity for rapid adaptation to hypoxia and protection of organs from hypoxic damage. The development of CC is associated with genetic and molecular impairments, as well as response to chronic hypoxia [2, 5, 12]. Approximately 30–40% of CCs have a hereditary nature [7]. During practical work, we encountered a diagnosis of CC in a father and son, with the father’s tumor having bilateral localization. Most often, hereditary CCs are associated with mutations in the SDHB, SDHC and SDHD genes. These mutations lead to impairment of cellular metabolism and contribute to the development of tumors of the paraganglionar system. Inheritance occurs in an autosomal dominant manner with imprinting (SDHD mutation manifests itself only in transmission from a father). The most common mutation in family forms is encountered in the SDHD gene (11q23). The SDHB gene (1q36) is associated with a high risk of malignancy and metastases. Mutations in SDH genes result in a defect of the mitochondrial respiratory chain, thus leading to accumulation of succinate. The latter inhibits the enzymes dependent on alpha-ketoglutaric acid (e. g., prolyl hydrogenase), thus inducing stabilization of HIF-1α (hypoxia-inducing factor), which, in turn, leads to activation of angiogenesis. There appears a pseudohypoxic condition, i. e., the cells behave as in conditions of hypoxia, even with the normal level of O₂. Chronic hypoxia (or pseudohypoxia in SDH mutations) leads to activation of chemoreceptors of the carotid body, thus resulting in proliferation of glomus (chromaffin) cells and, consequently, formation of a tumor. A peritumoral vascular network is formed around the tumor, due to which the latter is richly vascularized [7, 9].

The main classification of CBTs is that of W.R. Shamblin, 1971 (Fig. 5), according to which surgical tactics is built and the risk of possible complication is predicted. Three main types of CC are distinguished:

Type I – the tumor is up to 2.5 cm in size, is easily separated from the vessels, because it loosely touches their adventitia and does not encapsulate them;

Type II – the tumor is from 2.5 to 5 cm in size, partially encapsulating the CA;

Type III – the tumor is >5 cm in size, completely encapsulates the CA, thus hampering surgical removal [4, 8].

Currently, surgery is the main and generally accepted method of treatment of CCs. The presence of clinical symptomatology or patent’s young age belong to the absolute indications for a surgical intervention [4, 8, 13, 14]. In comorbid patients over 60 years of age with benign, asymptomatic tumors of small sizes, watchful waiting is possible, since the average growth of CC amounts to 10.4% a year, however this approach increases the risk of complications due to proximity of the tumor to critical structures – the CA, craniocerebral nerves and sympathetic trunk. The complication rate varies depending on the tumor size (Shamblin classification), surgeon’s experience and chosen surgical technique. The mortality rate is approximately 1–2%, with an overall complication rate of 20–40% (in Shamblin II–III tumors reaching 60%) [6, 7, 15]. In the group of neurological complications, prevailing are lesions of craniocerebral nerves: vagus nerve (X): 10–25% of cases, manifesting themselves as hoarseness of voice, dysphagia; hypoglossal nerve (XII); 5–15% – deviation of the tongue to the side of the lesion; less frequently damaged is the glossopharyngeal nerve (IX), manifesting as difficulty swallowing; damages of the sympathetic nerve account for 3–10%, leading to Horner’s syndrome (ptosis, miosis, anhidrosis); damage of the facial nerve (VII) is also possible in high location of the tumor. Persistent nerve paresis remains in 5–10% of patients, thus requiring logopedic, rehabilitation care. Cerebral infarction occurs in 1–5%, according to other data – from 23 to 50% [12, 16, 17]. Vascular complications include bleeding (2–7%) – more often in incomplete resection or invasion of the artery, thrombosis of the CA (1–3%); a false aneurysm (<1%) occurring in partial resection of the arterial wall [16–18].

Although CCs in most patients are benign tumors, approximately in 10% of cases they can exhibit malignant properties. However, the latest WHO consensus suggests that all chemodectomas should be assigned to malignant tumors [12]. To date, there are no definite and reliable criteria for malignancy, therefore the latter is determined not by histological features but rather by its clinical behavior. Malignancy of CCs is characterized by the tumor’s ability to invasive growth – infiltration of the tumor into the surrounding structures (vessels, nerves, soft tissues), to recurrence, and metastatic spreading [5, 7, 8]. Mention should be made that the main routes of metastatic spreading of CCs are lymph nodes, lungs, bones, liver, and thyroid. Tumor recurrence occurs in 10% of patients, especially in incomplete removal of the tumor. The risk of malignancy is higher in patients with hereditary forms, especially in mutations in the SDHB gene. The main risk factors of malignancy are hereditary forms, especially mutations in the SDHB gene, tumor size (>5 cm), young age, as well as multiple tumors [7, 9].

In treatment of malignant CC, it is particularly important to comply with the principle of radicality. It has been proven that the incidence of CA damage in patients with malignant forms of the tumor is 4 times higher than that in a benign course of the process, since the tumor is much more difficultly separated from the vascular wall. In similar clinical situations, the most appropriate is en bloc excision of the tumor conglomerate with vessels without an attempt of their exposure to be followed by plasty in one way or another [19, 20].

An important factor of efficacy of the operation is radical removal of the tumor in order to prevent its recurrence. While in type I and II CC, removal of the tumor presents no surgical difficulties, in Shamblin III it is hard to achieve radical removal. Besides, preserving native arteries in this situation is also practically impossible, because denudation of the tumor increases the risk of developing complications, formation of an aneurysm of the ICA due to thinning of its wall [14, 18, 19]. Thus, B. Babu, D. Jayant et al. (2024) published a clinical case of a pseudoaneurysm of the ICA and its rupture after excision of a tumor of the carotid body [18]. A 47-year-old male patient presented with a right-sided Shamblin type III carotid body tumor. The latter was routinely removed by means of sub adventitial resection with no complications. Ten days after surgery the patient developed a rapidly increasing swelling at the surgical site, accompanied by dyspnea, dysphagia, tachycardia and tachypnea. He presented with a right-sided cervical pulsating formation measuring 10×8 cm with deviation of the trachea to the left. MSCT-angiography revealed a pseudoaneurysm measuring 2.6×1.6 cm originating from the distal portion of the common carotid artery to its bifurcation with active bleeding and a hematoma measuring 7.7×5.5×10 cm. Intraoperatively they revealed 200 ml of blood clots and active bleeding from the CCA bifurcation. After clamping of arteries, the ECA was ligated, the pseudoaneurysm excised and a common carotid to internal carotid artery bypass was done with a reversed saphenous vein graft. In the postoperative period, there were signs of paresis of the mandibular nerve, which subsequently regressed [18]. This case report demonstrates that in Shamblin type III tumor, it is appropriate to perform radical en bloc removal followed by ICA repair, thus making it possible to minimize the risk of postoperative complications.

It remains an important and debatable question whether lymph node dissection is necessary in removal of CC. There is an opinion about the need for routine lymph node dissection because tumor’s malignancy is determined predominantly by metastatic spreading rather than by histological characteristics of a primary neoplasm, however this procedure increases the risk of developing such complications as lymphorrhea or seroma (up to 15%), lesions of cranial nerves. According to the NCCN guidelines (2024) on the subject “neuroendocrine tumors”, there is no data that prophylactic lymph node dissection decreases the risk of tumor recurrence. At the same time, lymphadenectomy should be carried out in enlarged lymph nodes, tumor recurrence, aggressive and malignant forms of tumor (rapid growth, presence of the SDHB gene, large tumor size, and invasive tumor growth) [2, 6, 21].

A bilateral location of CC is a rare condition. Bilateral CBTs are encountered in 10–20% of cases, more often in hereditary forms. Because of a limited number of clinical cases, a common standard of surgical tactics has not yet been developed, However, we can definitely say that simultaneous bilateral removal of tumors should not be performed due to the risk of life-threatening complications: lesions of vagus nerves on both sides, which may lead to respiratory arrest. Besides, degeneration of the carotid sinuses leads to uncontrolled hypertension. .It is still a debatable question about the sequence of removal of bilateral CBTs: primary resection of a larger or smaller neoplasm. Y. Ding et al. (2024) recommended to begin treatment from the side of a larger tumor and more pronounced symptoms with Shamblin I–II type bilateral chemodectomas and to monitor the contralateral tumor. Vice versa, in patients with type II–III it is recommended to remove a smaller tumor as the first stage, thus minimizing the risk of complications, with no decrease in quality of life of the patient. We can say that the so-called “strategical reserve” is maintained – if the first operation is followed by complications, including cerebral infarction, the second side remains compensated. The interval between the operations should take into account the patient’s general condition and neurological deficit after the first operation performed. If necessary, the interval may amount to 6 months [10, 12]. Hence, the sequence of removing neoplasms in bilateral CBTs is determined not by their size but rather by the Shamblin classification and the presence of symptomatology.

A rarer situation is a combination of the tumorous process with an atherosclerotic lesion of the CA bifurcation. World literature described both simultaneous and staged removal of a tumor, as well as reconstruction of the carotid basin for ICA critical stenosis. An appropriate approach to treating thus condition requires a balance between oncological radicality and prevention of ischemic stroke. Performing carotid endarterectomy in combination with CBT removal entails additional risks of the operation, with the mortality rate increasing up to 8.8% [22–27]. Taking into account a small number of cases, there is no unequivocal choice of treatment tactics as yet. Relying mainly on sporadic cases described in foreign and national literature, as well as on own experience, we came to a conclusion that one should strive for simultaneous removal of the tumor and performing carotid reconstruction. It is advisable to remove the tumor and atherosclerotically altered arteries in an en bloc manner with prosthetic repair of the ICA, which decreases the time of the operation and consequently that of anesthesiological support, thus reducing complications. An advantage of this method is radicality and exclusion of a secondary intervention, as in staged removal. A severe accompanying pathology and bilateral lesion can be managed by a staged approach, making it possible to stent the ICA. However, in a staged approach there are no guarantees of radical removal of the tumor, with a potential risk of in-stent thrombosis, especially in patient non-compliance with the dual antiplatelet therapy regimen. Thus, in such clinical situations, the decision should be made by a multidisciplinary team, including a vascular surgeon with sufficient experience, oncologist, neuropathologist, and surgical treatment should be performed in a specialized center.

Embolization of ICA branches before surgical removal of CC also remains a debatable question. Mention should herein be made of a large meta-analysis published in the Journal of Vascular Surgery (2023) where the authors assessed efficacy of embolization in 553 patients [28] and showed that embolization did not decrease intraoperative blood loss in Shamblin I–II tumors, whereas in Shamblin III, the difference amounted to 50–100 ml which is not a clinically meaningful parameter, Besides, embolization of ICA branches results in increased risk of ischemic stroke, thus embolization of the pharyngeal artery can lead to retrograde thrombosis of the ICA. It was also noted that partial embolization provoked inflammation, thus hampering exposure of the tumor during its removal. Embolization of the ICA branches can be considered in tumor relapse with cicatricial alterations. Such being the case, this procedure should be performed 24–48 hours before surgery in order to avoid postembolization inflammatory reaction in the surrounding tissues [12, 21, 28, 29].

CBTs are poorly sensitive to radio- and chemotherapy. However, it should be mentioned that radiotherapy plays an important role in treatment of CC in inoperable tumors or as adjuvant therapy after surgery, especially in malignant forms. Currently, stereotaxic radiotherapy is used, being suitable for precise irradiation of the tumor with minimal effect on the surrounding tissues. Fractionated radiation therapy is used in large tumors or proximity to critical structures (e. g., CA). Proton therapy making it possible to minimize damage of healthy tissues owing to accurate distribution of the radiation dose. Chemotherapy is rarely used, mainly in malignant forms of CC with metastases or in inefficiency of other methods of treatment. In some cases radiation and chemotherapy can be used in combination in order to improve efficiency of treatment, especially in aggressive forms of the tumor [2, 5, 21].

Conclusion

Thus, to ensure radicality, efficiency and safety of CBT removal, the following principles should be considered:

1. Surgical treatment for CC remains the “gold standard”. In our opinion, in Shamblin type III tumor, it is more advisable to remove it en bloc followed by ICA repair, thus minimizing complications in the postoperative period and decreasing the probability of tumor recurrence. The same principle applies to malignant CBTs, primarily to ensure radicality of treatment.
2. The sequence of removing neoplasms in bilateral location of CC is determined by their size, Shamblin classification, and the presence of symptomatology. It can definitely be said that simultaneous bilateral removal of tumors should not be performed because of the risk of life-threatening complications.
3. Lymphadenectomy should be carried out in enlarged lymph nodes in the zone of operation, tumor relapse, aggressive and malignant forms of the tumor, however routine performance of this procedure has not proven its efficacy.
4. Embolization of ICA branches prior to CBT removal failed to prove effectiveness, but rather, on the contrary, increasing the risks of complications, with the same applying to needle biopsy.
5. Patients with CBT, especially with a family history or multiple tumors are recommended to undergo genetic testing. Once a mutation revealed, first-degree relatives should be examined.

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