Successful patient outcome following surgery of carotid body tumor and temporary hypoglossal nerve dysfunction

Abstract

Carotid body tumors, also known as paragangliomas or chemodectomas, are rare tumors. They are mostly benign slow-growing tumors arising from neural crest cells, but can give rise to complications because of their location and close relation to carotid vessels and cranial nerves. A 40-year male patient diagnosed with a carotid body tumor is discussed along with a review of cranial nerve complications associated with the management of carotid body tumors. This case highlights the complete recovery after a temporary hypoglossal nerve deficit following surgery. Another important aspect is that syncopal attacks might occur in carotid body tumors and early surgery is required to prevent complications.

Introduction

Carotid body tumors (CBTs) are rare tumors [1] with an estimated incidence of 1:30,000 [2]. They arise most commonly at the site of bifurcation of the common carotid artery into the internal and external carotid arteries. They are also known as paragangliomas or chemodectomas. CBTs rarely secrete catecholamines, and in this aspect, they differ from paragangliomas at other sites that secrete catecholamines most of the time. These are slow-growing, generally benign tumors but rarely they turn malignant and metastasize. However, they can give rise to complications due to the involvement of the carotid vessels and cranial nerves. Although there are numerous case series and reports on CBTs in literature, they continue to generate interest because of their rarity, complications, difficult surgery, and high chance of complications. We hereby discuss a case of a Shamblin Class 3 CBT, along with various complications associated with its surgery, as reported in the literature [1, 2]. Informed consent was taken from the patient in the study.

Case report

A 40-year-old male patient presented with the complaints of gradually increasing swelling in the right side of the neck near the angle of the mandible for 6 months. On examination, the mass was rubbery in consistency, was pulsatile, and was mobile horizontally, but not vertically. Ultrasonography (USG) and Doppler study were done and they were consistent with the diagnosis of CBT. A computed tomographic (CT) angiogram was also done, and it confirmed the findings of CBT, its vascularity, and its relation to carotid vessels (Fig. 1a, b). The patient was planned for surgery, but in the meantime, the patient sustained a fall, post syncope, which led to a depressed skull fracture. The patient was conservatively managed for head injury and underwent surgery for CBT after 1 month. Under general anesthesia, an oblique incision was made along the anterior border of the sternocleidomastoid muscle on the right side. After incising the platysma and subcutaneous tissue, the sternocleidomastoid was retracted posteriorly. The tumor was very vascular and densely adherent to the carotid bifurcation and proximal parts of the internal carotid artery (ICA) and external carotid artery (ECA). It was carefully mobilized from the carotid vessels along the subadventitial plane, utilizing a combination of blunt and sharp dissection using bipolar electrocautery. The excised mass was (Fig. 2a) sent for histopathology examination (HPE) and immunohistochemistry (IHC). The wound was closed after inserting a mini suction drain. The patient recovered well and was discharged on the fifth postoperative day. There was a mild deviation of the tongue postoperatively, probably due to hypoglossal nerve injury, which recovered within a month with conservative treatment. HPE showed the zellballen pattern characteristic of a paraganglioma (Fig. 2b); IHC showed chief cells and sustentacular cells (Fig. 2c, d). The patient has been followed up for 9 months without any evidence of recurrence or metastatic disease.

Fig. 1.

a CT angiogram of the neck vessels showing highly vascular tumor at right carotid bifurcation. b CT neck in axial section showing the relation of the tumor with carotid vessels and surrounding tissues

Fig. 2.

a Gross appearance of the excised tumor. b HPE image of the excised specimen showing the characteristic zellballen pattern. c IHC image showing chief cells. d IHC image showing chief cells and sustentacular cells

Discussion

Paragangliomas originate from the neural crest and they usually occur in the head and neck, adrenals, thorax, and abdomen. Mutations in succinate dehydrogenase (SDH) gene subunits D, B, and C have shown co-relation with paragangliomas. CBTs are usually classified according to the Shamblin classification depending upon the degree of the carotid vessel encasement.

Most of the patients present with a painless slow-growing neck mass. Other common symptoms are headache, tinnitus, hearing loss, hoarseness of voice, pain in the neck, and dizziness. In our case, the patient had an episode of syncope probably due to pressure on the baroreceptors by the CBT during neck movement. This case also highlights that syncopal attacks might occur in CBTs and early surgery is required to prevent complications. CBTs are an extremely rare cause of reversible syncope. Convulsive syncope has also been reported with CBTs, though very rarely [3]. Most patients recover completely with timely surgical intervention. On examination, CBTs are usually pulsatile, mobile horizontally, but not vertically. USG and Doppler studies generally show the increased vascularity of the mass and its close relation to the carotid vessels. CT angiogram or magnetic resonance (MR) angiogram helps in delineating the extent of the tumor, its vascularity, condition of the carotid vessels, and presence of other swellings or enlarged nodes. Biopsy or fine-needle aspiration cytology (FNAC) is avoided due to high vascularity, and a high index of suspicion for paraganglioma should be there in case of pulsatile neck swelling in close relation to the carotid vessels.

Anesthetic management has important implications in the prevention of complications during surgery for paragangliomas [4]. Although rarely seen in neck paragangliomas, catecholamine secretion can lead to a hypertensive crisis. Alpha-adrenergic blockers are used for the treatment of hypertensive crisis. Some patients may also develop bradycardia and hypotension during tumor manipulation, which may require inotropic support. During carotid clamping in difficult cases, it is imperative to prevent hypotension and maintain mean blood pressure to prevent ischemia to the brain and stroke. Hypocapnia and hypercapnia can both be detrimental and normocapnia should be maintained and hypoxia has to be avoided. Significant blood loss can occur in Shamblin 3 class tumors and tumors of large volume. Surgery for CBT can involve excision of the tumor or with repair or reconstruction of carotid arteries. A carotid shunt may be required in cases where ICA reconstruction is required and where the retrograde pressure in the ICA is less than 50 mmHg after carotid clamping. As the tumor is very vascular, subadventitial resection of the tumor is the standard treatment. Koskas et al. recommended subadventitial resection of the tumor with deliberate resection of the ECA [5]. Although ECA can usually be ligated on one side without adverse effects if the contralateral vessels are normal, the resection of ECA may not be required in Shamblin class 1 and class 2 patients. In Shamblin class 3, and some difficult cases of Shamblin class 2, ECA resection may be helpful. Pre-operative embolization has also been used with success in CBT excision.

The most common early complication of carotid body surgery is cranial nerve injury (CNI) with a reported incidence of 15–30% [2]. The other complications are neck hematoma, stroke, internal carotid artery injury, vocal cord palsy, baroreflex failure syndrome [6], and mortality. Late complications are local recurrence and distant metastasis. Baroreflex failure syndrome is an important complication of bilateral carotid surgery due to denervation of the baroreceptors of both sides [6]. Patients may develop tachycardia, hypertension, anxiety, and headache. They require aggressive medical management to prevent cardiovascular and neurological complications due to severe hypertension. Nerve injuries commonly seen in CBT surgery are the vagus, hypoglossal, glossopharyngeal, facial, and superior laryngeal nerves [7]. The effects of nerve palsies include vocal cord palsy, palatal palsy, tongue palsy, facial palsy, and Horner’s syndrome. In our case, the patient had hypoglossal nerve injury which recovered spontaneously after 1 month with conservative treatment. The vagus is the most commonly injured nerve, followed by hypoglossal and superior laryngeal nerves [7]. Control of the inferior pharyngeal vein is important in preventing vagus and hypoglossal nerve injuries. Robertson et al. in their meta-analysis of 104 observational studies have reported mean 30-day CNI as high as 25.4% with 11.15% persisting after 30 days [7]. Amato et al. conducted a review of 19 studies over 10 years covering 625 procedures [8]. The incidence of cranial nerve injury was 48.32%, of which 31.04% were temporary and 17.28% were permanent.

Hypoglossal nerve dysfunction during carotid surgery can be due to excessive traction, use of unipolar cautery, nerve handling, separation of the tumor from surrounding structures, and rarely nerve transaction. In majority of cases, the nerve dysfunction is temporary (neuropraxia) and resolves within 1–2 months. Symptoms like dysphagia, dysarthria, and tongue deviation to the same side can occur. Short courses of steroids are helpful in some cases by reducing the inflammation and edema. Methylcobalamin supplements may help in patients with neuropraxia. Unilateral hypoglossal or vagus nerve injury is usually well tolerated. Pre-operative assessment of cranial nerve function is important in cases of CBT. Indirect laryngoscopy to pre-operatively diagnose vocal cord palsy is of significant value. The patient needs to be adequately counseled for the possibility of prolonged intubation or tracheostomy, if there is pre-operative vocal cord palsy due to carotid surgery on the contralateral side. Bilateral carotid surgery therefore should be avoided in a single sitting. Radiotherapy or observational treatment or peptide receptor radionuclide therapy (PRRT) may be required in such cases.

In cases where the nerve transaction occurs intra-operatively, primary repair should be done either by an end-to-end repair or by using an interposition nerve graft. The commonly used nerve grafts are sural nerve, antebrachial cutaneous nerves, lateral femoral cutaneous nerve, and the superficial sensory branch of the radial nerve [9]. If the tumor is large and extends up to the skull base, chances of injury to the hypoglossal and glossopharyngeal nerves increase, whereas vagus nerve injury can occur at any site along the length of the carotid artery. Injury to the vagus nerve can lead to vocal cord palsy and hoarseness of voice. Cases with a permanent injury of the vagus nerve will need speech therapy.

Radiotherapy as a treatment for CBT is generally not the first option as it is a benign lesion in the majority of cases. However, external beam radiotherapy or stereotactic radiosurgery may be used as an option in cases of recurrent disease or in patients with co-morbidities [10]. PRRT is emerging as a suitable alternative for the treatment of neuroendocrine tumors in cases with advanced disease or cases with metastasis. As paragangliomas are slow-growing tumors, observation as a treatment and repeated scan is also advocated in cases with comorbidities, for recurrent tumors after radiotherapy, advanced age, and multiple lesions.

Conclusion

Shamblin class 3 tumors have higher chances of hypoglossal and other cranial nerve injuries. Syncopal attacks can occur in patients having CBT and early surgery prevents associated complications. Unilateral hypoglossal nerve injury is usually well tolerated and when due to neuropraxia, it resolves within a few weeks.

Funding

None.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Not required as no new procedure was done.

Informed consent

Obtained.