Elsevier

World Neurosurgery

Volume 101, May 2017, Pages 559-567
World Neurosurgery

Literature Review
Overt and Subclinical Baroreflex Dysfunction After Bilateral Carotid Body Tumor Resection: Pathophysiology, Diagnosis, and Implications for Management

https://doi.org/10.1016/j.wneu.2017.02.073Get rights and content

Background

Carotid body paragangliomas are rare, usually benign, tumors arising from glomus cells of the carotid body. Bilateral involvement is present in ∼5% of sporadic cases and up to one third of familial cases. In most patients undergoing bilateral resection of carotid body tumors, a condition known as baroreflex failure syndrome (BFS) develops after resection of the second tumor characterized by headache, anxiety, emotional lability, orthostatic lightheadedness, hypertension, and tachycardia. This condition is believed to result from damage to the carotid baroreceptor apparatus. Patients without overt cardiovascular abnormalities may have subclinical baroreceptor dysfunction evident only on specific testing, measuring heart rate and sympathetic nerve responses to baroloading (e.g., phenylephrine) and barounloading (e.g., Valsalva maneuver). Given the high incidence of BFS in patients undergoing bilateral resection of carotid body tumors, it is suggested that operation is limited to unilateral resection of the dominant/symptomatic lesion and nonsurgical intervention (i.e., embolization, radiotherapy) on the contralateral side. Alternatively, refinement of surgical technique to prevent injury to elements of the baroreceptor apparatus may prevent this complication of bilateral tumor resection.

Methods and Results

We present a case of a 16-year-old girl with bilateral jugular vagale and carotid body tumors who developed hypertension after surgical resection of her left jugular vagale tumor and worsening of hypertension concurrent with progression, requiring intensity-modulated radiation therapy and a resection for significant progression of her left jugular vagale tumor. Additional case studies and series of bilateral carotid body tumors and BFS were identified through a comprehensive literature search in the PubMed database.

Conclusions

Our case shows the generalizability of BFS to patients with tumors involving the vagal baroafferent fibers.

Introduction

Carotid body tumors (CBTs) are (typically) benign, slow-growing tumors arising from glomus cells, with an annual incidence of 1.6 per 10,000.1 Most synthesize (and some secrete) catecholamines. Some show nodal or distant metastasis.2, 3 Proto-oncogene mutations involving c-myc, bcl-2, and c-jun,4 among others, have been described, as well as germline mutations in succinate dehydrogenase.5 CBTs represent the most common type of paraganglioma and 5% present bilaterally.6 In familial cases (typically autosomal dominant), bilaterality affects 26%–33% of patients.7, 8 Bilateral resection may cause the baroreflex failure syndrome (BFS), with reported prevalence of ∼66%.9

Section snippets

Methods

Case studies and series of bilateral CBTs and BFS were identified through a comprehensive literature search in the PubMed database.

Case Description

A 16-year-old girl presented with postural dizziness/lightheadedness, hoarseness, chronic cough, and dysphagia. On examination, she had a blood pressure (BP) of 120/80 mm Hg (right arm, sitting), a heart rate (HR) of 64 bpm, and evidence of neuropathies of the left vagus, accessory, and hypoglossal nerves with vocal cord paresis, atrophy of the sternocleidomastoid and trapezius muscles, and atrophy and fasciculations of the left side of the tongue. Arteriography identified bilateral glomus

Baroreflex Dysfunction

BFS has been reported by several investigators after bilateral CBT resection or carotid endarterectomy, neck trauma/irradiation, and brainstem stroke. In cases of bilateral CBTs, this typically follows resection of the second tumor, but not in all patients.10

Baroreceptors are stretch receptors concentrated in the carotid sinus and aortic arch and also located in the great vessels from heart to skull base.11, 12 Carotid and aortic arch baroreceptors relay via the carotid sinus (branch of cranial

Conclusions

Bilateral resection of CBTs frequently causes overt or subclinical baroreflex dysfunction, as a result of injury to the carotid baroreceptor apparatus. These patients show headache, anxiety, or emotional lability, as well as abnormalities of resting ABP, increased ABP variability, tachycardia, orthostasis, and episodes of hypotension. In some cases, baroreflex dysfunction improves, perhaps through compensation by aortic or other extracarotid baroreceptors. However, in many patients, BFS

References (85)

  • I. Gur et al.

    Baroreceptor failure syndrome after bilateral carotid body tumor surgery

    Ann Vasc Surg

    (2010)
  • L. Díez Porres et al.

    Multiple paraganglioma: careful with surgery!

    Rev Clin Esp

    (2003)
  • S. Demattè et al.

    Role of ultrasound and color Doppler imaging in the detection of carotid paragangliomas

    J Ultrasound

    (2012)
  • I.B. Rosen et al.

    Vascular problems associated with carotid body tumors

    Am J Surg

    (1981)
  • J. DuBois et al.

    Bilateral carotid body tumors managed with preoperative embolization: a case report and review

    J Vasc Surg

    (1987)
  • A.H. Power et al.

    Impact of preoperative embolization on outcomes of carotid body tumor resections

    J Vasc Surg

    (2012)
  • H.S. Ong et al.

    Radical resection of a Shamblin type III carotid body tumour without cerebro-neurological deficit: improved technique with preoperative embolization and carotid stenting

    Int J Oral Maxillofac Surg

    (2014)
  • W.M. Mendenhall et al.

    Chemodectoma of the carotid body and ganglion nodosum treated with radiation therapy

    Int J Radiat Oncol Biol Phys

    (1986)
  • R.A. Cooper et al.

    An unusual case of carotid body tumour

    Clin Oncol (R Coll Radiol)

    (1998)
  • J.R. Hamilton et al.

    Radionuclide angiography and surgery for familial bilateral chemodectomas

    Eur J Vasc Surg

    (1987)
  • J.C. Oosterwijk et al.

    First experiences with genetic counselling based on predictive DNA diagnosis in hereditary glomus tumours (paragangliomas)

    J Med Genet

    (1996)
  • J.O. Defraigne et al.

    Lymphatic, hepatic and osseous metastasis of a carotid chemodectoma. Apropos of a case

    J Chir (Paris)

    (1997)
  • D.G. Wang et al.

    Oncogene expression in carotid body tumors

    Cancer

    (1996)
  • C. Neumayer et al.

    Novel SDHD germ-line mutations in pheochromocytoma patients

    Eur J Clin Invest

    (2007)
  • P.H. Dickinson et al.

    Carotid body tumour: 30 years experience

    Br Surg

    (1986)
  • S. Grufferman et al.

    Familial carotid body tumors: case report and epidemiologic review

    Cancer

    (1980)
  • J.L. Netterville et al.

    Carotid body tumors: a review of 30 patients with 46 tumors

    Laryngoscope

    (1995)
  • R.F. Rogers et al.

    NTS neuronal responses to arterial pressure and pressure changes in the rat

    Am J Physiol

    (1993)
  • D. Robertson et al.

    The diagnosis and treatment of baroreflex failure

    N Engl J Med

    (1993)
  • A.A. Smit et al.

    Long-term effects of carotid sinus denervation on arterial blood pressure in humans

    Circulation

    (2002)
  • I. Jeske et al.

    Quantitative analysis of bulbospinal projections from the rostral ventrolateral medulla: contribution of C1-adrenergic and nonadrenergic neurons

    J Comp Neurol

    (1992)
  • P.G. Guyenet et al.

    Regulation of sympathetic tone and arterial pressure by the rostral ventrolateral medulla after depletion of C1 cells in rats

    Ann N Y Acad Sci

    (2001)
  • J.H. Coote et al.

    Effect of renal nerve stimulation, renal blood flow and adrenergic blockade on plasma renin activity in the cat

    J Physiol

    (1972)
  • N.C. Hughes-Jones et al.

    The nature of the action of renin and hypertensin on renal function in the rabbit

    J Physiol

    (1949)
  • A. Dendorfer et al.

    Angiotensin II induces catecholamine release by direct ganglionic excitation

    Hypertension

    (2002)
  • V.S. Bishop et al.

    Angiotensin II modulation of the arterial baroreflex: role of the area postrema

    Clin Exp Pharmacol Physiol

    (2000)
  • J.H. Birrell

    Carotid body tumours; a study of three cases including a bilateral example

    Aust N Z J Surg

    (1952)
  • J.B. Wood et al.

    Bilateral removal of carotid bodies for asthma

    Thorax

    (1965)
  • A. Dahan et al.

    Plasticity of central chemoreceptors: effect of bilateral carotid body resection on central CO2 sensitivity

    PLoS Med

    (2007)
  • D. Zikk et al.

    Sleep apnea following bilateral excision of carotid body tumors

    Laryngoscope

    (1983)
  • A.J. Roncoroni et al.

    Bilateral carotid body paraganglioma and central alveolar hypoventilation

    Respiration

    (1993)
  • A. Baraka

    Postoperative respiratory depression following excision of carotid body tumours

    Can J Anaesth

    (1994)
  • Cited by (15)

    • Operative management of symptomatic, metachronous carotid body tumors involving the skull base and its neurological sequelae

      2021, Journal of Vascular Surgery Cases and Innovative Techniques
      Citation Excerpt :

      Furthermore, unilateral hypoglossal nerve paralysis has minimal effect on speech and swallowing as the contralateral nerve is enough for this function, despite the expected hemitongue atrophy. BFS is a well-documented sequela of bilateral CBT resection due to unopposed sympathetic brainstem signals from bilateral baroreceptor denervation.10,11 Headache, anxiety, hypertension, and tachycardia classically characterize this morbidity,2,8,10-12 and its spectrum ranges from hypertensive crisis to volatile hypertension and orthostatic tachycardia.3

    • Blood Pressure Management in Afferent Baroreflex Failure: JACC Review Topic of the Week

      2019, Journal of the American College of Cardiology
      Citation Excerpt :

      In some cases, radiation injury also produces carotid artery stenosis that contributes to the symptomatology. Afferent baroreflex failure can also result from bilateral resection of neck tumors, most commonly carotid body paragangliomas, with damage to the carotid sinus nerve (17–19). It can also be caused by familial dysautonomia (hereditary sensory and autonomic neuropathy type 3), a rare congenital disease characterized by developmental failure of afferent neurons, affecting individuals of Ashkenazi Jewish ancestry (20).

    • Surgical Management of Bilateral Carotid Body Tumors

      2019, Annals of Vascular Surgery
      Citation Excerpt :

      Its main function is to monitor blood arterial oxygen partial pressure (PaO2) and arterial carbon dioxide partial pressure (PaCO2) as well as pH changes in the arterial blood. On the other side, carotid baroreceptors are located in the carotid sinus, and they regulate arterial blood pressure (ABP).8,10 CBTs are rare and are considered to have an incidence of 1-2 per 100,000 patients, accounting for 0.012% of all body tumors.

    View all citing articles on Scopus

    Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

    View full text