Keywords
paraganglioma - carotid body tumor - bilateral neck mass - syncope - angiography
Introduction
Paragangliomas, including carotid body tumors (CBTs), are rare, predominantly benign
neuroendocrine neoplasms originating from paraganglia, clusters of cells associated
with the autonomic nervous system. Bilateral CBTs are especially uncommon, representing
less than 5% of cases.[1] These tumors can display diverse clinical manifestations, one of the most common
being neck masses.[2] This report documents a patient with bilateral carotid body paragangliomas, detailing
the clinical presentation, diagnostic evaluation, and therapeutic strategy that was
pursued.
Case Report
A 49-year-old woman presented with an initial complaint of bilateral neck masses persisting
for 1 year, accompanied by recurrent syncopal episodes. The patient denied pain, dysphagia,
or changes in voice. Physical examination revealed two pulsatile, painless masses
in the bilateral carotid regions. These masses were firm, fixed/nonmobile, and showed
bruits on auscultation. There were no signs of overlying skin changes or tenderness.
A supra-aortic trunk angiotomography and angiography were conducted, revealing two
heterogeneous nodular, hypervascular solid masses in each carotid space ([Fig. 1]). The clinical and imaging findings suggested bilateral carotid body paragangliomas.
Given the hypervascular nature of these tumors, a multidisciplinary approach was adopted.
Surgical resection was denominated as the primary treatment. An angiography was necessary
for surgical planning, providing a dynamic view of the tumor's vascular filling demonstrated
a hypervascularized mass occupying and deforming the right-sided carotid bifurcation
([Fig. 2A]), as well as a formation in the region of the left-sided carotid bifurcation ([Fig. 2B]). The left-sided lesion was classified as a Shamblim type III mass, being larger
than the right, which also fell under the category of Shamblim type III.
Fig. 1 (A) Three-dimensional CT angiography reformat image displaying bilateral carotid body
tumors (white arrows). (B) Axial view showing bilateral solid masses with intense and slightly inhomogeneous
enhancement at the level of the carotid bifurcation (white arrows). This lesion exhibits
bright and rapid enhancement, illustrating a carotid body tumor that splayed the bifurcation
of the internal carotid artery (ICA) and external carotid artery (ECA).
Fig. 2 Angiography of the right (A) and left (B) internal carotid arteries demonstrating abnormal enhancement associated with the
carotid body tumor. The cerebral blood flow study showed no alterations on either
side.
Preoperatively, optimizing blood pressure (BP) was crucial to mitigate the risks of
autonomic instability and intraoperative bleeding. While alpha-blockade was not routinely
required, antihypertensives were used as needed to maintain BP stability. In the absence
of embolization, priority was given to hemoglobin optimization, fluid resuscitation
planning, and blood crossmatching to manage the anticipated intraoperative blood loss.
Additionally, a thorough neurological assessment was performed to establish a baseline
for cranial nerve function and cerebral perfusion before carotid manipulation.
Postoperatively, BP fluctuations were carefully monitored, as bilateral CBT resection
can impair baroreceptor reflexes, leading to hypertension, orthostatic hypotension,
or labile BP responses. Short-acting IV antihypertensives were available for hypertensive
episodes, while fluid resuscitation, vasopressors, and fludrocortisone were considered
for persistent hypotension. Close neurological monitoring was essential for early
detection of stroke, cranial nerve dysfunction, or airway compromise due to postoperative
swelling or hematoma.
Surgical treatment was prioritized on the right side. An oblique incision was made
along the anterior border of the sternocleidomastoid muscle, extending proximally
toward the mastoid process. The hypoglossal nerve was carefully isolated, and the
vagus nerve, along with its pharyngeal and laryngeal branches, was identified. The
tumor segment involving the artery was dissected, coagulated, and removed, exposing
the arterial bifurcation. A subadventitial dissection technique was used to improve
the exposure of the tumor, exposing and permitting the identification of the common
carotid artery, internal carotid artery (ICA), and external carotid artery. Despite
the increased risk of bleeding, preoperative embolization of the tumor was not performed,
as it was believed that this would ease dissection and mobilization of the tumor.
The main blood supply to the tumor was located at the bifurcation of the internal
and external carotid arteries, as seen on dynamic angiographic analysis. Controlling
these flowing arteries helped manage bleeding. The right-sided surgery resulted in
a blood loss of 400 mL. Two months later, the tumor on the left side was resected,
with a blood loss of 600 mL. Fragments were sent off confirming the diagnosis through
histological analysis of the tissue fragments of both masses. There was no visible
evidence of neurological deficit after the surgery ([Figs. 3]
[4]
[5]).
Fig. 3 (A) Photograph of the patient showing the preoperative planning for right-sided carotid
body tumor surgery. A swelling in the upper lateral neck, corresponding to the tumor,
can be observed. Intraoperative images (B–D) demonstrate a large tumor encapsulating the internal carotid artery (ICA) and external
carotid artery (ECA), and adhering to and incorporating the hypoglossal nerve (HN).
The final image (D) shows the outcome of the surgery, with complete resection of the tumor and preservation
of the arteries.
Fig. 4 The images show preoperative angiography revealing a carotid body tumor that widens
the bifurcation of the internal carotid artery (ICA) and external carotid artery (ECA)
on the right side (A) and left side (C). Postoperative angiography of the right side (B) and left side (D) demonstrates complete resection of the tumor and preservation of the arteries.
Fig. 5 Shamblin classification.[5] Type I tumors are small lesions that do not splay the carotid bifurcation. Type
II tumors are larger, significantly splay the carotid bifurcation, but do not circumferentially
encase the carotid arteries. Type III tumors are large, encapsulate the internal or
external carotid arteries, and often adhere to or incorporate the adjacent cranial
nerves. CN, cranial nerve; ECA, external carotid artery; ICA, internal carotid artery;
SLN, superior laryngeal nerve. (Adapted with permission from Hoang et al.[12])
Discussion
Paragangliomas of the carotid body are scarce, accounting for less than 0.5% of head
and neck tumors.[3] Bilateral involvement is particularly unusual, presenting diagnostic and therapeutic
challenges. These tumors originate from chemoreceptor cells involved in the process
of blood oxygen level monitoring and are highly vascularized due to their paraganglial
origin.[4]
Clinical presentations of paragangliomas vary, with neck masses being one of the more
common findings. Symptoms such as syncope, seen in our patient, are less common and
may be related to baroreceptor dysfunction or compression of adjacent structures.
Advanced imaging modalities, including CT angiography and MRI, are critical for diagnosis,
allowing the detailed assessment of tumor size, vascularity, and anatomical relationships.[2] An angiography offers a dynamic view of the tumor's vascular supply and permits
detailed visualization of any potential invasion into the affected artery. In the
present case described, the arteries are displaced and dislocated by the tumor, but
they remain free from invasion.
Surgical resection continues to be the main route of treatment for paragangliomas,
though it poses challenges due to the proximity to critical vascular structures. Preoperative
embolization can be considered an option to minimize intraoperative bleeding.[1] In cases of bilateral tumors, carefully planned surgical procedures may be needed
to mitigate the risk of bilateral cranial nerve deficits.[4] In this case, although it was known that embolization could reduce blood loss, the
surgical team opted to proceed with tumor resection without preoperative embolization.
This decision was taken due to the fact that it would allow for better mobility of
the tumor and the surrounding arteries during dissection. Additionally, the team successfully
identified and coagulated the tumor's influx vessels, which provided improved control
over bleeding.
Paragangliomas are classified according to a histological grading system that determines
the tumor's aggressiveness, ranging from I to III. Grade III tumors are characterized
by high aggressiveness, including necrosis, a high mitotic index, and the potential
for local invasion and metastasis, making them challenging for surgical intervention.
These characteristics increase the complexity and risk of surgery, often requiring
a multifocal approach for appropriate management.[5]
In this specific case, both paragangliomas were classified as grade III, indicating
significant difficulty in surgery and a considerable risk of complications. Despite
these challenges, the entire medical team adopted a well-thought-out surgical approach,
resulting in successful resection and favorable recovery for the patient. This outcome
exceeded expectations associated with the complexity of the tumors, demonstrating
the success of the strategy employed and the effectiveness of the treatment. The clinical
analysis highlights the importance of detailed evaluation and planning in difficult
paraganglioma cases.
As mentioned previously for bilateral CBTs, the primary treatment is surgical resection,
which has a high cure rate following complete resection of benign tumors. However,
additionally, preoperative embolization is often used to reduce the tumor's vascularity
and size, easing safer resection by decreasing blood loss. Another approach is carotid
artery grafting and stenting to reduce blood supply to the tumor, which can also minimize
its size and vascularity prior to surgery. In cases where surgical resection is not
applicable or might result in significant neurological deficits, radiotherapy (RT)
is employed as an alternative. RT can also be used for recurrent tumors or malignant
CBTs. Additionally, chemotherapy is considered for malignant CBTs, although it is
less effective compared to surgery. In managing bilateral cases, the strategy is typically
to first operate on the smaller tumor to minimize the risk of baroreflex failure syndrome
and other postoperative complications. If the initial surgery preserves nerve function,
the contralateral tumor can be addressed; otherwise, RT may be recommended to avoid
further deficits. This approach aims to balance tumor management with the minimization
of surgical risks and complications.[6]
Despite approximately 30% of bilateral CBTs following a familial autosomal dominant
inheritance pattern, no other cases had been identified within the patient's family
at the time. These tumors are typically associated with mutations in genes encoding
subunits of the mitochondrial enzyme succinate dehydrogenase. Sporadic cases, such
as this one, often harbor somatic mutations in genes involved in metabolism and DNA
repair. However, a genetic workup had not been performed in this patient.[7]
A variety of surgical management strategies exist for bilateral carotid body paragangliomas,
each with distinct advantages and risks. Preoperative embolization, often used to
reduce intraoperative blood loss, was not performed in this case due to concerns about
ischemic complications such as embolic stroke, particularly given the tumor's proximity
to the ICA and the complex collateral circulation in the head and neck. Embolization
may also increase peritumoral inflammation and adhesions, potentially complicating
surgical dissection rather than easing it.[8]
[9] Simultaneous bilateral resection was another potential approach but was avoided
due to the high risk of baroreceptor failure and autonomic dysfunction, which could
lead to severe BP instability, orthostatic hypotension, and an increased risk of cerebrovascular
events.[10] Instead, a staged surgical approach was chosen, allowing the patient to adapt hemodynamically
between procedures. RT, while an option for patients with unresectable or high-risk
tumors, was not considered the optimal strategy in this case due to the patient's
relatively young age, progressive symptoms, and the tumor's high-risk Shamblin III
classification. Surgical resection offered definitive treatment, preventing further
compression-related complications and tumor progression, whereas RT primarily stabilizes
tumor growth and carries long-term risks such as vascular injury and cranial neuropathy.[11] Given these considerations, a staged surgical resection without embolization was
determined to be the safest and most effective approach, considering tumor removal,
hemodynamic stability, and neurological preservation.
Conclusion
This case illustrates the clinical presentation, diagnostic investigation, and management
of bilateral carotid body paragangliomas. Recognizing the characteristic features
and employing proper imaging techniques are crucial for accurate diagnosis and effective
treatment planning. The surgical techniques, as well as intimate knowledge of the
neuroanatomy of the region, are essential for managing the complexities associated
with bilateral paragangliomas to optimize patient outcomes.
