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CASE REPORT

Carotid Body Tumor as a Reversible Cause of Syncope

Paul Harlan Singh Janda, DO; Venkatachalam Veerappan, MD; Mark E. McKenzie, MD; and Neel V. Dhudshia, MD

The causes of syncope are diverse and extensive; carotid In the current report, we present the case of a patient body tumors are an extremely rare cause of syncope. These with syncope who, after other causes had been ruled out, was rare neoplasms represent less than 0.5% of all head and found to have a right-sided carotid body tumor as the cause tumors. The authors present a case of a woman with syncope of her condition. We also review the history, presentation, who was found to have a right-sided carotid body tumor. epidemiology, etiology, diagnosis, management, and prog - After surgical resection was performed, she did not have nosis of this condition. any additional syncopal or near-syncopal events. The authors provide a review of the literature on the natural history, pre - Report of Case sentation, and preferred management of carotid body tumors. Our patient was a 75-year-old white woman with a medical his - With modern diagnostic tools and treatment options, most tory that included hypertension, type 2 diabetes mellitus, and patients with this diagnosis can expect to recover fully. a prolapsed bladder. She was admitted to the hospital with a J Am Osteopath Assoc . 2011;111(11):638-644 chief complaint of syncope and left hip pain secondary to her fall. She reported having approximately 4 or 5 near-syncopal episodes before this admission. These earlier events consisted yncope is defined as the abrupt loss of consciousness of a sensation of dizziness but did not result in loss of con - Swith loss of postural tone. Approximately one-third of sciousness or postural tone. However, they were increasing in 1 individuals will have a syncopal episode during their lifetime. frequency. The patient reported that the events were occa - 2 According to Manolis et al, syncope is the reason for up to sionally linked to her position (ie, standing) and occurred at dif - 5% of all emergency department admissions. However, the ferent times throughout the day. She had no history of seizures causes of syncope are diverse and extensive; syncopes that or stroke. originate from vasodepressor, cardiogenic, and orthostatic Her syncopal episode occurred while she was standing at 3 causes are among the most common. the sink in her bathroom. She reported experiencing a pro - Carotid body tumors are rare neoplasms that are also drome of dizziness before falling to the floor. She stated that referred to as carotid body because they arise she had a rapid recovery, crawled to the toilet for positional 4 from paraganglionic cells. Carotid body tumors are an support, and then called out to her family members, asking 4-6 extremely rare cause of syncope, representing less than 0.5% them to phone for emergency medical services. The patient was 7 of all head and neck tumors. We reviewed the literature and neither disoriented nor weak after the episode and had no 8,9 found few reports of patients with these tumors. associated bowel or bladder incontinence or any oropharyn - geal trauma. Although she had type 2 diabetes mellitus, she was normoglycemic at her home when she was tended to by emergency medical services. During physical examination at admission, the patient appeared to be her stated age and was in no acute distress; she was awake, alert, and oriented. Her vital signs were stable. Her neck was not obese, enabling the physician (P.H.S.J.) to palpate a small, pulsatile right-sided mass with some mild tender - From the departments of neurology (Drs Janda and Veerappan), internal ness to light pressure. Except for this finding, the physical medicine (Dr McKenzie), and cardiothoracic surgery (Dr Dhudshia) at Valley examination findings were within normal limits for the patient’s Hospital Medical Center in Las Vegas, Nevada. Financial Disclosures: None reported. age. Address correspondence to Paul Harlan Singh Janda, DO, Valley Hospital On day 1, several diagnostic studies were performed. An Medical Center, 620 Shadow Ln, Las Vegas, NV 89106-4119. electrocardiogram exhibited normal sinus rhythm; an echocar - E-mail: [email protected] diogram showed an of 60% with mild, con - Submitted March 1, 2011; final revision received August 10, 2011; accepted centric left ventricular hypertrophy. Her orthostatic vital signs August 11, 2011. were unremarkable. Plasma metanephrine levels were mea -

638 • JAOA • Vol 111 • No 11 • November 2011 Janda et al • Case Report CASE REPORT sured and were within normal limits. A computed tomo - patient was informed of the risks and benefits of the procedure graphic (CT) scan of the brain without contrast material and agreed to proceed. The operation was uncomplicated. enhancement was unremarkable. The patient’s rate was At resection, the tumor appeared to be a highly vascu - monitored telemetrically and exhibited a sinus cardiac rhythm larized, solid mass resembling a tuft of capillaries. It was sent throughout her hospital stay. to the pathologist for histologic analysis. Histologic findings On day 2, results from magnetic resonance (MR) imaging were typical of a carotid body tumor and indicated no signs of of the brain, performed with and without gadolinium con - malignancy. Sections of the tumor appeared highly vascular, trast enhancement, demonstrated no acute changes or with cells palisaded by surrounding vessels. There were abnormal enhancement; only scant chronic white matter numerous cell clusters in zellballen formation, separated by a changes were noted. An MR angiogram of the brain was unre - prominent vascular stroma that is pathognomonic for carotid markable. An electroencephalogram was within normal limits body tumors. Hematoxylin-eosin staining revealed chief cells— and showed no areas of focal slowing and no spikes or sharp type I cells that are APUD (amine precursor uptake and decar - wave activities. Results from duplex Doppler carotid ultra - boxylation) cells with copious cytoplasm and large round sonography revealed normal carotid and vertebral ; it nuclei ( Figure 2 ), and S100 staining revealed the elongated also demonstrated a 1.5-cm nodule that was near the thyroid type II supporting cells ( Figure 3 ) that are also found in carotid gland but situated between the bifurcation of the right common body tumors. carotid into the right internal and external carotid The patient had no postoperative complications and exhib - arteries. ited no damage or deficits. She was closely followed On the third day, 3-dimensional CT angiography of the up for 15 months after hospital discharge and had no additional neck and CT of the neck with iopamidol contrast enhance - syncopal or near-syncopal episodes. ment (Isovue-370, 100 mL) was performed, and results from these tests demonstrated a 1.7-cm mass with an intense vascular Comment and Review of Literature blush at the bifurcation of the right Historical Background (Figure 1 ). The findings were deemed to be consistent with a A carotid body tumor is a rare neoplasm of the carotid body carotid body tumor. that was first described by Lushka in 1862. 10 In 1880, Riegner The vascular surgery department was consulted on day attempted the first surgical resection, which resulted in the 3 and recommended surgical resection of the tumor. The death of the patient. 11,12 Maydl’s resection attempt in 1886

A B

Figure 1. Three-dimensional computed tomographic (CT) angiogram (A) and transverse CT scan (B) of the neck of a 75-year-old woman presenting with complaint of sycope. The images revealed a 1.7-cm carotid body tumor (arrows) at the bifurcation of the right common carotid artery.

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Figure 2. Histologic analysis of a tumor in a 75-year-old woman revealed Figure 3. Histologic analysis of a tumor in a 75-year-old woman revealed numerous chief cells in the pathognomonic zellballen cluster formation elongated sustentacular cells that are pathognomonic for carotid body (arrow), separated by a vascular stroma (hematoxylin-eosin stain; orig - tumors (S100 stain; original magnification, ×40). inal magnification, ×40).

was reportedly successful, but the procedure caused sub - the lesion and is caused by the . 11 Rarely, stantial, irreversible residual complications of aphasia and carotid body tumors secrete catecholamines, which can result hemiplegia in his patient. The first published report of resec - in hypertension. 11,19 Our patient’s metanephrine levels were tion of a carotid body tumor with preservation of the carotid within normal limits, and she did not exhibit any hemody - arteries was by Scuddder in 1903. 11,12 In 1940, Gordon-Taylor namic instability. The majority of patients with carotid body illustrated an appropriate plane of dissection for the proce - tumors are asymptomatic until the tumor enlarges; carotid dure. 13 In 1953, Morfit et al 14 described arterial reconstruction body tumors expand slowly, with a growth rate of 0.5 cm per techniques, offered operative recommendations, and provided year. 4,7,9 Syncope, dizziness, and transient ischemic attacks the first documented report of a successful carotid body tumor are very rare presentations. 20 More frequent presentations are resection. A major publication by Shamblin et al 15 provided a neck discomfort, dysphagia, or dyspnea due to the size of the reliable template for categorizing carotid body tumors based mass, or hoarseness, dysphagia, or tongue weakness due to cra - on the degree of encirclement of the carotid arteries, a system nial nerve involvement. 11 Specifically, the 8th through 12th that is still used today. cranial may be involved. Involvement of the mandibular Although carotid body tumors have been reported in the branch of the seventh cranial nerve has been reported but is literature for many years, syncope has rarely been mentioned rare. 21,22 Williams et al 10 described 30 patients with carotid as a manifestation of these tumors. In 1947, McSwain and body tumors, none of whom presented with syncope. Singh Spencer described 2 patients in whom syncope was the pre - et al, 11 in their study of 10 patients with carotid body tumors, senting sign of carotid body tumor. 16 In 1967, Farr 17 described discovered similar findings. The lack of syncope as a pre - 37 patients with carotid body tumors, including only 1 who senting feature of carotid body tumor was also evident in the presented with syncope. On the basis of our literature review, study by Kraus et al 18 of 15 patients with carotid body tumors. instances of syncope as a presenting sign of a carotid body To our knowledge, it was McSwain and Spencer 16 who first tumor in more recent literature continue to be rare and excep - described syncope as the presenting manifestation of a carotid tional. body tumor. As previously mentioned, Farr, 17 in a study of 37 patients, reported only 1 patient in whom syncope was the Presentation presenting feature. Typically, patients with carotid body tumors Classically, patients with a carotid body tumor present with a are initially unaware of their diagnosis and are free of pain or slowly enlarging, painless neck mass, which is often anterior discomfort until the tumor is larger than 1 cm. 17,23 to the sternocleidomastoid muscle at the level of the hyoid. 18 These tumors are attached to the carotid sheath and have lim - Epidemiology ited vertical mobility and permissive lateral mobility. Occa - Syncope is a relatively common diagnosis. 24 In one of the sionally, pulsation can be palpated immediately anterior to largest studies that evaluated the incidence and prognosis of

640 • JAOA • Vol 111 • No 11 • November 2011 Janda et al • Case Report CASE REPORT syncope, in which 7814 men and women were followed up for more dated literature to classify carotid body tumors. 4,11,32,33 an average of 17 years as part of the Framingham Heart Study, However, carotid body tumors are more accurately termed 860 (11%) had syncopal episodes. 24 The incidence of syncope paragangliomas because they arise from paraganglionic cells, was similar in men and women; approximately one-third of which are epithelial cells of origin that migrate individuals were likely to have a syncopal episode in their life - closely with the autonomic nervous system’s ganglion cells. 4,11 time. 24 The , or carotid body tumor, encases the carotid As previously discussed, syncope due to a carotid body bulb and may subsequently compress the surrounding tumor is extremely rare, and very few patients with this pre - anatomic structures, including the cranial nerves and the sym - sentation have been described. Carotid body tumors may pathetic chain. 11 Typically, as evidenced by the rarity of syn - occur at any age but are most commonly diagnosed between cope as a manifestation of carotid body tumor, disruption of the third and sixth decades of life. 18,25 They seem to be slightly the carotid body by a tumor does not physiologically impair more common in women, and most patients are white. 26 In consciousness. The carotid sinus, located adjacent to the carotid Farr’s study 8 over a 40-year period, the tumors were more body, maintains and in response to pos - prevalent in neither men nor women, and the average age at tural changes; its compression by a mass can lead to both onset of symptoms was 46 years (range, 19-72 years). Williams orthostatic hypotension and failure of the to increase, et al, 10 in their study of 30 patients, noted similar epidemiologic and thus plausibly lead to syncope. 8 characteristics. Some reports have suggested an association Carotid body tumors are classified into 2 forms: sporadic between high altitudes and hyperplasia of the carotid body, and hereditary. The sporadic form is more common and tends usually occurring at or above a threshold level of 1500 m to occur slightly more often in women than in men. 24 The above sea level. 2,5,20,27-29 Our patient, however, lives in a city hereditary form accounts for roughly 30% of cases and is approximately 600 m above sea level. In addition, multiple equally common in both sexes. 20 Carotid body tumors are carotid body tumors and bilateral presentation have been bilateral in 5% of sporadic cases and in 33% of hereditary associated with a positive family history. 11 Carotid body cases. 5,34 Germ-line mutations in what have been identified as tumors are bilateral in 10% of cases, and 30% of patients with the paraganglioma susceptibility genes, notably PGL-1 and bilateral tumors have a positive family history. 30 PGL-2, have been attributed to heritable carotid body tumors, even in the absence of family history. 20,33 These genes encode Etiologic and Pathologic Characteristics for the succinyl dehydrogenase (SDH) enzymes, particularly The carotid body is a physiologically important paragan - the SDH-D and SDH-B subtypes. The SDH enzymes have glion. 9,20 It responds primarily to by detecting the been mapped to 4 chromosomal loci. Each of the subtypes hydrogen ion concentration and feeding back to the respira - has a dominant mode of inheritance with penetrance that may tory center in the medulla, which sends impulses to the be linked to both age and degree of hypoxia. The genes PGL- external intercostal muscles, diaphragm, vasculature, and 1 and PGL-2 display maternal imprinting (inactivation); hence, heart, thus reflexively increasing the rate and depth of venti - genes carrying a mutation that may manifest as carotid body lation, as well as slightly increasing blood pressure and heart tumor are inherited only from the father. 20,35,36 Although the rate. 4,9,11,22 Embryologically, the carotid body arises from a prevalence of these genes is low, patients who have them combination of the third branchial arch mesoderm and ecto - almost invariably present with multiple tumors. 33,37 dermal-derived neural crest cells. 11,20 Histologically, carotid body tumors are well vascularized and nonchromaffin in Diagnosis appearance. 7 The carotid body is multilobular and comprises Carotid body tumors may be diagnosed or suspected from a 3 types of cells, each of which is responsive to hypoxia. 20,25 patient’s history and physical examination findings, but the Type I cells, or chief cells, produce catecholamines and diagnosis is confirmed by imaging studies. 20 Approximately immunoreactive peptides and are arranged in a typical cluster 1 in 30,000 tumors of the head and neck is a paraganglioma, formation called zellbalen . Type II cells, also referred to as sus - and the most frequent site is the carotid body (45%). 25 A high tentacular cells , surround the type I cells and have characteristics index of suspicion is important in the diagnosis of carotid similar to those of Schwann cells. Type III cells are sensory body tumor. 17 The differential diagnosis is manifold and nerve endings that function as the afferent limb for chemore - includes branchiogenic cyst, aberrant thyroid gland, neurofi - ceptor reflexes by means of the carotid sinus nerve to the res - broma, cervical node hyperplasia, lymphoma, metastatic car - piratory control center. 20,25 cinoma, aneurysm, deep-lobe parotid enlargement, and arte - Before 1988, neoplasia was the only documented patho - riovenous malformation. 7,11,19,30 In most cases, such diagnoses logic state affecting the carotid body. In more recent literature, can be excluded with ultrasonography. 7 Moreover, the initial chronic hypoxemia has been described as a stimulus for hyper - use of such noninvasive modalities provides excellent infor - trophy and hyperplasia of the carotid body. 22,31 The descrip - mation in the workup of a neck mass, specifically in depicting tive term chemodectoma (meaning “of origin”), the distortion of the internal and external carotid arteries sec - originally coined by Mulligan in 1951, is sometimes used in ondary to the mass effect of a carotid body tumor. 4,19,20,22,38

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Widening of the carotid bifurcation with a well-defined tumor ◾ There is no reliable screening mechanism to follow the his - blush is virtually pathognomonic from a radiologic perspec - tologic progression of these tumor. tive. 9,11,19 Bilateral studies enable the detection of multicentric ◾ The surgical risk in Shamblin group I tumors is minimal; disease 17,39 ; this approach was used in our case. Computed some tumors are malignant at presentation. tomographic angiography is consistently described as the ◾ To our knowledge, spontaneous regression has never been most valuable study in the diagnosis of a carotid body tumor, 19 reported. and our experience supports this judgment. It is the most ◾ All carotid body tumors will eventually become symp - accurate modality and is the reference standard in the diagnosis tomatic. of carotid body tumors. 4,9,19,25,40 This diagnostic study dis - closes important details, including unsuspected contralateral The surgical technique is well documented. Early proximal tumors, the need for preoperative embolization, and the degree and distal control of the common, internal, and external carotid of atherosclerosis in the carotid artery. 11,20 arteries is imperative. Identification of a relatively avascular Fine-needle aspiration is not useful in the evaluation of plane between the tumor and artery is equally important for carotid body tumors. 9,17,20,41 Open biopsy should also be an uncomplicated course. The most widely recommended avoided because it may result in substantial hemorrhage from approach is subadventitial resection through the avascular these highly vascular tumors. 9,11 Urinary or serum screening space between the carotid vessels, 11,17,25,47 as initially described for metanephrines is not necessary but is occasionally per - by Gordon-Taylor. 13 formed if the patient is exhibiting vasomotor instability or Carotid body tumors are radiosensitive and may be man - hypertension. 4,11,30 aged with radiation therapy if necessary. 4,11,45 -50 The choice In 1971, Shamblin 15 developed a classification system between surgery and radiation therapy is based on the risk of based on the relationship between the carotid body tumor treatment complications and the anatomic presentation of the and its adjacent vessel walls that helps predict surgical outcome tumor. 7,11,17,20,22 Radiation therapy does not completely remove on the basis of angiographic findings. This system yields the tumor. Instead, it provides a mechanism to halt further 3 groups of tumors, as follows: tumor growth. 33,42 Tumors categorized as Shamblin group II or III are often associated with a higher rate of operative com - ◾ Group I —These tumors do not involve the vessel walls and plications, especially for group II. 11,51,52 Moreover, for patients are consequently easier to resect surgically. They are usually with Shamblin group III tumors that present as technically less than 5 cm in diameter and infrequently widen the carotid difficult to resect or as unresectable, radiation therapy should bifurcation. The tumor in the patient described in the present be strongly considered. 7,11,17,20,22,25 Despite the documented report was classified as group I. degree of surgical difficulty, successful resection of Shamblin ◾ Group II —These tumors more intimately involve the adja - group III tumors has been reported, although these proce - cent vessel walls but do not encase them. They are often dures involved vascular reconstruction with synthetic grafts or larger than 5 cm in diameter. autologous vein grafts. 17,25 Recommendations in the literature ◾ Group III —These tumors are intramural and encase both the advocate radiation therapy for patients with carotid body internal and external carotid arteries in addition to regional tumors stratified as Shamblin group III and for the manage - nerves. They are often larger than 5 cm in diameter. ment of residual tumor when resection is incomplete owing to the anatomic location of the tumor. 4,20 Given that carotid body Because group II and III tumors are often larger than tumors are small, asymptomatic, slow-growing tumors that 5 cm, these tumors often widen the bifurcation of the carotid typically present in elderly patients, who are likely to have arteries. A progression in the Shamblin group classification significant risk factors for surgical intervention or adverse of a tumor correlates with an increased likelihood of regional reactions to radiation therapy, the tumors may be managed by nerve involvement as well as intraoperative and postopera - observation alone. 9,11,17,33,45,46,53 tive complications. 14 This classification system is still used in the assessment and management of carotid body Prognosis tumors. 9,11,14,17,20,25,33 Carotid body tumors grow slowly and have a doubling time of approximately 4 years. 54 Accurate preoperative diagnosis in Treatment combination with modern surgical techniques yield excellent Since carotid body tumors were first discovered, there has results with minimal complications in most patients. 11,33 Fur - been no consensus on the best treatment options. 5 Currently, thermore, survival after resection is equivalent to that in age- surgical resection is the mainstay of management if the patient’s and sex-matched control subjects. 11,21 Without treatment, surgical risk is acceptable, and resection should be performed carotid body tumors may become life threatening because of early so that tumor size does not increase the risk. 9,14,17,20,30,33,42- their increasing size and associated effects. 11 46 The rationales for resection include the following 11,20 : Bilateral tumors occur in approximately 10% of patients with tumors, and 30% of patients with bilateral tumors have

642 • JAOA • Vol 111 • No 11 • November 2011 Janda et al • Case Report CASE REPORT a family history of bilateral tumors. 11,21,29 Bilateral carotid 9. Maxwell JG, Jones SW, Wilson E, et al. Carotid body tumor excisions: adverse outcomes of adding carotid endarterectomy. J Am Coll Surg . 2004;198 body tumors, which have a genetic component, are known to (1):36-41. occur. Patients with multiple paragangliomas should have 10. Williams MD, Phillips MJ, Nelson WR, Rainer WG. Carotid body tumor. Arch extended follow-up, and their family members should be Surg . 1992;127(8):963-968. investigated as well, given the increased risk of complications 11. Singh D, Pinjala RK, Reddy RC, Satya Vani PV. Management of carotid body and potential for metastatic disease. 11,33 paragangliomas. Interact Cardiovasc Thorac Surg . 2006;5(6):692-695. Carotid body tumors often exhibit a locally aggressive 12. Lahey FH, Warren KW. A long-term appraisal of carotid body tumors and infiltrative growth pattern. 11,33 Malignancy occurs in 6% with remarks on their removal. Surg Gynecol Obstet . 1951;92(4):481-491. to 12% of cases, ranking carotid body tumors as the most fre - 13. Gordon-Taylor G. On carotid tumours. Br J Surg . 1940;28(110):163-172. quently malignant head and neck paraganglioma. 7,8,11,20,33,49 14. Morfit HM, Swan H, Taylor ER. Carotid body tumors, report of 12 cases, Metastasis most frequently involves the liver, bones, and including one case with proved visceral dissemination. Arch Surg . 1953;67(2): lungs. 20,55 Surgical excision of metastatic disease is often pal - 194-214. liative and is considered the first-line treatment modality for 15. Shamblin WR, ReMine WH, Sheps SG, Harrison EG Jr. Carotid body tumor patients who are cleared for surgery; minor postoperative (chemodectoma); clinicopathologic analysis of ninety cases. Am J Surg . 1971; neuropathies, if present, are transient. 17,20,33 122(6):732-739. 16. McSwain B, Spencer FC. Carotid body tumor in association with carotid sinus Conclusion syndrome: report of two cases. Surgery . 1947;22(2):222-229. Carotid body tumors are rare and often present challenges to 17. Farr HW. Carotid body tumors: a thirty year experience at Memorial Hos - pital. Am J Surg . 1967;114(4):614-619. physicians in diagnosis and management. Although they are 18. Kraus DH, Sternman BM, Hakaim AG, et al. Carotid body tumors. Arch Oto - a rare cause of syncope, spontaneous syncope with no other laryngol Head Neck Surg . 1990;116(12):1384-1387. apparent cause should prompt evaluation for a neck mass. If 19. Crowell WT, Grizzle WE, Siegel AL. Functional carotid paragangliomas: bio - no mass is palpable, ultrasonography of the neck, followed by chemical, ultrastructural, and histochemical correlation with clinical symptoms. CT angiography when indicated, may reveal a carotid body Arch Pathol Lab Med . 1982;106(12):599-603. tumor. Surgical resection is the treatment of choice, but radi - 20. Bafitis H, Posevitz L, Stahl HD. Paragangliomas of the carotid body: report ation therapy should be considered in patients with compli - of a case. J Am Osteopath Assoc . 1986;86(9);577-583. cated tumors or contraindications to surgery. Treatment 21. Knight TT Jr, Gonzales JA, Rary JM, Rush DS. Current concepts for the sur - should be individualized, addressing the size and anatomic gical management of carotid body tumor. Am J Surg . 2006;191(1):104-110. presentation of the tumor, patient demographics, and asso - 22. Nora JD, Hallet JW Jr, O’Brien PC, Naessens JM, Cherry KJ Jr, Pairolero PC. ciated deficits secondary to the tumor. With the use of modern Surgical resection of carotid body tumors: long-term survival, recurrence, and metastasis. 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644 • JAOA • Vol 111 • No 11 • November 2011 Janda et al • Case Report