20.1 Goals

1. 
   

   Review and understand the literature that describes the symptomatology and natural history of head-and-neck paragangliomas, specifically carotid body tumors (CBTs).

   
   
2. 
   

   Review the classification scheme of CBTs and how it applies to the treatment decision for these tumors.

   
   
3. 
   

   Critically analyze the literature that evaluates the utility of preoperative embolization of these tumors.

20.2 Case Example

20.2.3 Follow-up

The patient did very well after definitive treatment of her right CBT, including preoperative embolization followed by surgical resection by an interdisciplinary team involving a neurointerventionalist, vascular neurosurgeon, and otorhinolaryngologist. Total operative time for surgical resection was 189 minutes with an estimated blood loss of 100 raL The patient was discharged home on postoperative day 2, with 1 additional day of hospital stay preceding surgical resection for her embolization. The patient remained at her neurologic baseline following surgery, with slight hoarseness. At her 6-month follow-up appointment, she had persistent mild hoarseness of voice, but otherwise had no complaints.

20.3 Case Summary

1. 
   

   What are the general characteristics, symptomatology, and natural history of carotid body paragangliomas? Paragangliomas are highly vascular, slow growing, and relatively rare tumors of neural crest cell origin with an incidence of approximately 1:30,000. ²³ CBTs are the most common paraganglioma of the head and neck and account for roughly 70% of head-and-neck paragangliomas. ³ They originate from the carotid body, as their namesake implies, and they are generally nonsecretory, although 10% can be. ⁴ Historically they have been called by many names including chemodectoma, glomus caroticum, in addition to carotid body paraganglioma. They derive their blood supply from branches of the external carotid artery, with the most common arterial supply coming from branches of the ascending pharyngeal artery. ⁵

   
   

   A majority of CBTs are diagnosed due to an insidious neck swelling, typically at the anterior border of the sternocleidomastoid muscle. ⁶ The mass tends to be firm and painless and can be pulsatile due to their high degree of vascularity. These tumors are usually highly mobile in the medial-lateral direction but resist manipulation in the rostral-caudal dimension due to the tumor’s attachment to the carotid body and carotid bifurcation (Fontaine’s sign). ¹ CBTs also may be found due to progressive cranial nerve dysfunction, including hoarse voice or difficulty swallowing. ^{7 , 8} A minority of these masses are found incidentally.

   
   

   These lesions are typically slow growing and their symptomatology is explained by direct compression of nearby neurovascular structures, with an average rate of growth of 0.5 cm per year. ⁹ While mostly benign, there is a small but definite risk of malignancy that is approximately 2 to 5%. ^{10 , 11 , 12} The treatment modality of choice for these lesions is surgical resection with or without preoperative embolization, given their predictable growth and small, but definite, risk of malignancy.

   
   
2. 
   

   What patient factors would you consider when deciding on your re commendation for treatment versus observation?

   
   

   As with all candidates for surgery, the age and medical comorbidities of the patient need to be carefully considered in the context of the patient’s symptoms. A young, relatively healthy patient should have definitive treatment of their paraganglioma regardless of symptomatology as the natural history dictates that the tumor will invariably enlarge and eventually become symptomatic. ^{7 , 8 , 9 , 10 , 11 , 12} However, an elderly patient with multiple medical comorbidities and an asymptomatic or mildly symptomatic CBT may be better served by either close observation or radiation therapy, as opposed to undergoing a relatively higher risk surgery.

   
   
3. 
   

   What tumor factors would you consider when deciding on your recommendations for observation or treatment of carotid body paragangliomas?

   
   

   Classification of carotid body paragangliomas based on operative risk was first proposed by Shamblin in 1970 based on retrospective review of 90 patients who underwent CBT resection. ⁵ He identified three groups in his classification scheme, with group 1 including CBTs that were not associated with the carotid vessels and were easily dissected from the vessel adventitia. Group 2 includes those tumors that partially encase the carotid vessels, while group 3 includes tumors that completely encase the carotid artery. Group 1 tumors are the easiest to surgically resect, while the group 3 tumors are much more difficult, sometimes requiring external carotid artery sacrifice or internal carotid artery repair.

   
   

   The Shamblin grade alone does not inform a decision regarding the need for surgical resection as these lesions should be surgically resected if the patient is medically able to tolerate surgery. It does, however, inform the surgeon of the potential difficulty of surgical resection and potential benefit of adjuvant treatments, such as preoperative embolization. Group 2 and 3 patients’ tumors are more difficult to dissect and resect due to their proximity to and involvement of the carotid vasculature, making vessel injury requiring repair or bypass more likely. This potentially could increase intraoperative blood loss, operative time, and potential for ischemic events or strokes. ^{13 , 14 , 15} Given that these tumors will continue to grow without definitive treatment, these tumors should be resected despite their Shamblin classification. However, the Shamblin classification does provide important information for the physician in managing the patient’s expectations and informing them about the potential risks of the surgical resection. It also provides information regarding the utility of preoperative angiography, including balloon-test occlusion and preoperative tumor embolization.

   
   
4. 
   

   What preoperative imaging should be performed for adequate work-up of a CBT?

   
   

   Appropriate preoperative imaging is essential for proper diagnosis and treatment planning for CBTs. All patients should have either a CT neck with contrast or an MRI with contrast, and a preoperative angiogram. The preoperative angiogram helps elucidate the vascular anatomy of the tumor, which may aid in appropriate diagnosis (differentiating between a schwannoma vs. a paraganglioma) and also gives information that is useful for surgical resection, regardless of the decision to embolize. ¹⁴ It allows the surgeon to have a working map of important vascular feeders and helps identify possible tumor invasion of the carotid vasculature, thereby alerting the surgeon to the possibility of having to perform a vessel sacrifice, repair, or bypass during resection. In addition, the angiogram provides critical information about the intracranial circulation, such as whether there is a patent anterior or posterior communicating artery with adequate collateral flow. These details are essential to know if there is a possibility of temporary or permanent occlusion of the internal carotid artery during surgery. In patients where carotid injury, repair, or bypass may be unavoidable, the patient should undergo provocative testing at the time of angiogram to determine whether the patient would be able to tolerate vessel sacrifice or temporary occlusion without ischemic consequences.

   
   
5. 
   

   When is preoperative embolization appropriate?

   
   

   Surgical resection is the definitive treatment of carotid body paragangliomas. Given their highly vascular nature, preoperative embolization can provide a significant benefit by decreasing operative time and blood loss and making surgical resection of the tumor easier and safer, especially for Shamblin 2 and 3 tumors. ^{12 , 13 , 15 , 16 , 17 , 18 , 19 , 20 , 21 , 22 , 23} However, the exact role of preoperative embolization in CBTs remains controversial owing to several contradicting case series. The relative rarity of these tumors makes them difficult to study in a more rigorous way. Several groups have proposed that there is no benefit of preoperative embolization when compared to surgical resection alone without emboliza-tion. ^{24 , 25 , 26 , 27 , 28}

   
   

   When analyzing the series that shows no difference, the number of patients included is small and the complication rate from embolization is higher than expected for the majority of these cases. Many of these studies have cited the stroke rate associated with embolization to be as high as 10%, an unacceptably high rate for an appropriately trained interventionalist, especially with the safe technology now available for embolization. ^{12 , 19 , 26} Not surprisingly, studies citing such a high rate of stroke from embolization were published more than 15 years ago. Most ofthe studies showing no benefit from preoperative embolization are not stratified based on Shamblin classification of these tumors. Sham-blin group 1 tumors are typically small and can be easily dissected off the carotid vasculature, so preoperative embolization should not affect overall operative time, estimated blood loss, or neurologic outcomes. Shamblin group 2 and 3 tumors are larger, more complex, and more intimately related with the carotid vasculature, allowing for greater potential for benefit from preoperative embolization.

   
   

   Transarterial embolization is the standard method for tumor embolization, consisting of superselective catheterization and embolization using a combination of PVA particles, N-butyl cyanoacrylate (NBCA) glue, and Onyx. As with all head-and-neck tumor embolization, it is imperative to understand potential external to internal carotid artery anastomoses to ensure that embolization is performed safely. The proximity of tumor supplying arterial branches to the internal carotid artery is also important, as reflux of embolic material can lead to ischemic events. Percutaneous embolization using Onyx has more recently been described and has been shown to be effective in significantly reducing tumor blush. ^{29 , 30} However, some interventionalists remain wary of percutaneous embolization with tumors intimately related to the internal carotid artery, as reflux could result in embolic stroke.

   
   
6. 
   

   What treatment would you recommend for this patient’s CBT? The patient was recommended preoperative embolization followed by surgical resection of her paraganglioma. The patient is young and healthy with a symptomatic Shamblin 2 right CBT paraganglioma. The natural history of the tumor dictates that it will continue to enlarge, albeit slowly. The patient already has developed hoarseness, but is otherwise asymptomatic. As the tumor continues to grow the patient’s hoarseness will undoubtedly worsen and she will likely develop additional symptoms from local compression of vital structures in the region ofthe carotid body. As the tumor continues to enlarge, it may eventually fully encase the external and internal carotid arteries (Shamblin group 3), which has been shown to carry a significantly higher operative risk than Shamblin grade 1 and 2 tumors. The Shamblin grade 3 tumors have more morbidity associated with resection, including a greater risk of cranial nerve injury, vessel injury, and stroke. ³¹ All of these factors favor early surgical resection for this patient.

   
   

   A CTor MRI neck with contrast is necessary to characterize the location of the tumor and delineate its anatomic relation with other important neurovascular structures. Catheter angiogram is an exceptionally useful modality to characterize the vascularity ofthe tumor, delineate the vascular supply to the tumor for intraoperative planning, and to ensure the appropriate preoperative diagnosis. The angiogram also allows for better characterization ofthe intracranial circulation, including the presence of patent anterior or posterior communicating arteries. It can also identify invasion of the external or internal carotid arteries and allow for further provocative testing, such as balloon-test occlusion, in case vessel sacrifice or temporary occlusion is needed intraoperatively. Lastly, preoperative embolization of Shamblin group 2 and 3 CBTs has been shown to decrease operative time and estimated blood loss, and allows for less burdensome tumor resection.

   
   

   A multidisciplinary team, including a head-and-neck surgeon, vascular surgeon or vascular neurosurgeon, and experienced neurointerventionalist, is recommended when treating paragangliomas. This patient underwent preoperative CT neck with contrast indicating a highly vascular tumor partially encasing the internal and external carotid arteries, consistent with a Shamblin group 2 CBT. A preoperative angiogram was performed which redemonstrated the tumor’s size and hypervas-cularity with multiple direct arterial feeders arising from the right superior thyroid artery, right occipital, and right ascending pharyngeal arteries. Each of these feeding arteries was successfully selectively catheterized and embolized utilizing a combination of PVA particles and Onyx to reduce tumor blush by 95% (Fig. 20.1 and Fig. 20.2).