ORIGINAL ARTICLE
Extracranial schwannoma in the carotid space: A retrospective review of 91 cases
Xiaoke Zheng, MD,1 Kai Guo, MD,1,2 Hongshi Wang, MD,1 Duanshu Li, MD,1 Yi Wu, MD,1,2 Qinghai Ji, MD,1 Qiang Shen, MD,1 Tuanqi Sun, MD, PhD,1,2
Jun Xiang, MD, PhD,1 Wei Zeng, MD,1 Yaling Chen, MD,1 Zhuoying Wang, MD, PhD1*
1
Department of Head and Neck Surgery, Shanghai Cancer Center, Fudan University, Shanghai, China, 2Department of Oncology, Shanghai Medical College, Fudan University,
Shanghai, China.
Accepted 6 May 2016
Published online 21 July 2016 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/hed.24523
ABSTRACT: Background. Schwannomas of the vagus nerve and cervical sympathetic nerve are rare; hence, only limited information exists
regarding their diagnosis and clinical management.
Methods. We conducted a retrospective review of the clinical features,
imaging studies, and treatment results of patients with schwannoma of
the vagus nerve and schwannoma of the sympathetic nerve.
Results. Of 91 patients, 91% (n 5 83) were preoperatively diagnosed
with schwannoma tumors. Using the hyoid bone as an anatomic landmark, the location of the schwannoma of the vagus nerve in the
carotid space was significantly different to the location of schwannoma of the sympathetic nerve (p 5 .003). Although 52 of the 76
patients followed up (68%) had postoperative nerve weaknesses, 13
patients (50%) and 14 patients (53.8%), respectively, fully recovered
from schwannoma of the vagus nerve and schwannoma of the
sympathetic nerve.
Conclusion. In the carotid space, schwannomas of the vagus nerve are
usually located below the hyoid bone, whereas schwannomas of the
sympathetic nerve more commonly arise from the suprahyoid compartment. Accurate preoperative diagnosis and the intracapsular enucleation
surgical approach decreased the incidence of postoperative morbidity.
C 2016 Wiley Periodicals, Head Neck 39: 42–47, 2017
V
INTRODUCTION
(1) schwannoma confirmed by postoperative pathology;
(2) schwannoma located in the carotid space; or (3) nerve
of origin accurately identified as the vagus or the cervical
sympathetic nerve.
Diagnosis of schwannoma in the carotid space was
made on radiologic imaging of the probable nerve of origin, as previously described.4,5 The nerve of origin was
then verified intraoperatively. Carotid space schwannomas
were subdivided according to whether the position of the
maximum diameter of the tumor was in the suprahyoid
compartment or the infrahyoid compartment, which can
also be further separated by the styloid process.
All patients underwent intracapsular enucleation of schwannomas via the transcervical approach to preserve continuity of
the nerve. One patient with a case of schwannoma of the vagus
nerve underwent intraoperative nerve monitoring.
Continuous variables were described using the mean or
the median. Differences between categorical variables were
analyzed using the chi-square or Fisher exact test, with significance defined a priori as p < .05. Univariate logistic
regression was performed to identify which variables were
associated with postoperative complications of schwannoma of the vagus nerve and schwannoma of the cervical
sympathetic nerve, respectively. All analyses were performed with Stata software version 12 (Stata Corp, College
Station, TX) with a bilateral A-type one error of 5%.
1
1
Schwannoma was first described by Verocay in . Most
schwannomas are benign, slow growing, solitary encapsulated nerve sheath tumors comprised of schwann cells.
They can arise from any cranial, peripheral, or autonomic
nerve in the body except the olfactory and optic nerves.2
Approximately 25% to 45% of extracranial schwannomas
are located in the head and neck.3
The carotid space is a roughly cylindrical space that
extends from the skull base through to the aortic arch.
Schwannomas in the carotid space most commonly arise
from the vagus nerve and the cervical sympathetic chain,
and are extremely difficult to distinguish when their symptoms and masses are not specific. Therefore, accurate preoperative identification of the nerve of origin is crucial for
nerve preservation during surgery and to manage postoperative complications. This study was a retrospective review of
a series of carotid space schwannomas, with special attention paid to preoperative diagnosis and complications.
MATERIALS AND METHODS
We retrospectively reviewed patients with schwannomas diagnosed and treated at the Department of Head
and Neck Surgery, Fudan University Cancer Center from
January 2008 to December 2014. Inclusion criteria were:
KEY WORDS: extracranial, schwannomas, carotid space, vagus
nerve, cervical sympathetic nerve
RESULTS
*Corresponding author: Z. Wang, Department of Head and Neck Surgery, and the
Department of Oncology, Shanghai Medical College, Fudan University, No. 270
Dong-An Road, Shanghai 200032, China. E-mail: [email protected]
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JANUARY 2017
From 2008 to 2014, there were 275 patients with schwannoma treated at our institution. However, only 91 patients
EXTRACRANIAL
SCHWANNOMA IN THE CAROTID SPACE
FIGURE 1. The selection process of
patients with eligible criteria. SVN,
schwannomas of vagus nerve; SSN,
schwannomas of the cervical sympathetic
nerve; NOO, nerve of origin.
met the study criteria and were included in this analysis.
Details of case inclusions and exclusions are shown in Figure 1.
The median patient age was 42 years (range, 15–73
years), and the average maximum tumor diameter was
4.28 cm (range, 1.8–11.5 cm). The clinical presentations
are depicted in Table 1. Most of the tumors presented as
a palpable mass (n 5 72; 79%). Most patients (n 5 85;
93%) were asymptomatic and without neurologic deficits
TABLE 1. Summary of demographic characteristics, clinical profiles, and
preoperative examinations of schwannoma.
Variables
Sex
Male
Female
Syndromes
Neck mass
No symptoms
Dysphagia
Hoarseness
Horner’s syndrome-related sequel
Local numbness
Location
Suprahyoid
Infrahyoid
Preoperative examination
CT
MRI
FNAB
Ultrasound
Abbreviation: FNAB, fine-needle aspiration biopsy.
No. of patients (%)
48 (53)
43 (47)
72 (79)
13 (14)
3 (3)
1 (1)
2 (2)
1 (1)
47 (51.6)
44 (48.4)
43 (47)
50 (55)
56 (61)
73 (80)
at presentation. In some schwannoma of the vagus nerve
cases, a paroxysmal cough may be produced on palpation
of the mass.6,7 However, preoperative Horner syndrome is
rarely seen in schwannoma of the sympathetic nerve.
Ultrasound was the most common form of preoperative
imaging (n 5 73; 80%; Table 1). The tumor was preoperatively diagnosed as a schwannoma in 91% of the patients
(n 5 83). The nerve of origin had been correctly diagnosed preoperatively according to specific radiographic
characteristics in approximately 1 in 3 patients (n 5 30),
including 15 patients correctly diagnosed through ultrasound. On CT scans, schwannomas showed relatively
homogeneous contrast enhancement, with internal cystic
change becoming more prominent as the tumors enlarged
(see Figure 2). The MRI showed the tumors as hypointense on T1-weighted images and heterogeneously hyperintense on T2-weighted images (see Figure 3).
Preoperative fine-needle aspiration biopsy (FNAB) as a
diagnostic approach was carried out in 56 of 91 patients
(Table 2); the accuracy of FNAB was only 33.9%, including 2 malignant peripheral nerve sheath tumors.
Of the 91 cases reviewed, 45.7% were schwannoma of
the sympathetic nerves (n 5 42). The locations of schwannoma of the vagus nerve and schwannoma of the sympathetic nerve in the carotid space using the hyoid bone as an
anatomic landmark were significantly different (p 5 .003;
Table 3). Of the 4 patients with multiple schwannomas in
the carotid space, 3 cases were schwannoma of the vagus
nerves and 1 patient had both schwannoma of the vagus
nerve and schwannoma of the sympathetic nerve.
In total, 76 of 91 patients were followed up, with an average
follow-up period of 39 months (range, 3–224 months). No
recurrence was observed in the follow-up period. Fifty-two of
the 76 patients (68%) had postoperative nerve weakness
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ZHENG ET AL.
FIGURE
2. Axial
contrastenhanced CT of extracranial
schwannomas in the carotid
space. (A) Axial contrastenhanced CT scan shows the
tumor (M) that separated the
internal jugular vein (IJV) from
the internal carotid artery (ICA) or
common carotid artery (CCA) was
schwannoma of the vagus nerve
(SVN) in the carotid space. (B)
Axial contrast-enhanced CT scan
shows the tumor (M) that displaced the IJV (arrow) and the
external carotid artery (ECA) and
the internal carotid artery (ICA) in
a posterior direction was the cervical sympathetic nerve (SSN) in
the carotid space.
(Table 4); these nerve deficits were only transient in 13
patients (50%) and 14 patients (53.8%) with schwannoma of
the vagus nerve and schwannoma of the sympathetic nerve,
respectively. Collectively, the mean time to recovery was 6
months (95% confidence interval [CI] 5 3.6–9.0). Vocal cord
paralysis and Horner’s syndrome were the predominant postoperative complications, with 26.2% and 33.3% with permanent injury, respectively. The mean time to recovery for vocal
cord paralysis or hoarseness was 8 months (95% CI 5 2.2–
13.5) and the mean time to recovery for Horner’s syndrome
was 5 months (95% CI 5 3.3–6.5).
Univariate analysis revealed that tumor position (p 5
.857 for schwannomas of the vagus nerve; p 5 .352 for
schwannomas of the sympathetic nerve), tumor size
(p 5 .062 for schwannomas of the vagus nerve; p 5 .828 for
schwannomas of the sympathetic nerve), and patient sex
(p 5 .796 for schwannomas of the vagus nerve; p 5 0.074
for schwannomas of the sympathetic nerve) were not significant predictors for the development of postoperative complications related to schwannoma of the vagus nerve or
schwannoma of the sympathetic nerve. Three patients
(7.1%) developed first bite syndrome, including 1 patient
with Frey’s syndrome. First bite syndrome was significantly
associated with Horner’s syndrome (p 5 .042), tumor presence in the parapharyngeal space (PPS; p 5 .005), and
schwannoma of the sympathetic nerve (p 5 .04).
FIGURE 3. Axial T1-weighted
MRI of extracranial schwannomas in the carotid space. (A)
Axial T1-weighted MRI of the
right cervical vagus nerve
shows the heterogeneous mass
(M) that separated the internal
jugular vein (IJV) from the internal carotid artery (ICA) and the
external carotid artery (ECA). (B)
Axial T1-weighted MRI of the
left cervical sympathetic nerve
shows a heterogeneous mass
(M). Fat seen around the tumor
represents the “split fat” sign.
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EXTRACRANIAL
TABLE 2. Preoperative biopsy results.
TABLE 4. Surgical adverse events of schwannoma of the vagus nerve
and schwannoma of the sympathetic nerve.
Biopsy results
No. of patients (%)
Total
Schwannoma
Spindle cell neoplasm
Benign soft tissue neoplasm
Lymph node
Salivary glands
Inadequate material
Malignant mesenchymal neoplasm
56 (100)
17 (30.3)
20 (35.7)
10 (18.0)
3 (5.3)
1 (1.8)
3 (5.3)
2 (3.6)
DISCUSSION
Schwannoma is a benign nerve sheath tumor arising
from the schwann cells. Schwannoma of the vagus nerve
and schwannoma of the sympathetic nerve are the most
common schwannomas in the carotid space. In our retrospective review, nearly half of all tumors were schwannomas of the sympathetic nerve; this is in contrast to a
previous study that described schwannoma of the sympathetic nerve as a very rare disease.8 Because most patients
were without neurologic deficits at presentation, preoperative diagnosis of schwannoma was still a substantial challenge for surgeons. Knowledge of FNAB and imaging
characteristics obtained through CT and MRI with contrast is crucial in diagnosing carotid space schwannomas
and the nerve of origin.4,5,9
FNAB was performed on 56 patients. A definitive cytological diagnosis of schwannoma based on the presence
of characteristic Verocacy bodies was only made in 17
patients (30.3%); this was similar to previously reported
rates of 21% and 25%.10,11 In another 20 (35.7%) and 10
patients (18.0%), the diagnosis of schwannoma was suggested by the presence of spindle cells and benign soft
tissue, respectively. Tumors containing Verocacy bodies,
spindle cells, or benign soft tissue on histopathology tend
to be diagnosed as schwannomas. Moreover, FNAB has a
high rate of accuracy for excluding malignancy.11–13
The cervical vagus nerve runs within the carotid sheath
between the internal carotid artery (ICA) or common
carotid artery (CCA) and the internal jugular vein (IJV)
as a neurovascular bundle. The cervical sympathetic trunk
is located deep to the prevertebral fascia, posteromedial
to the carotid vessels, as it runs longitudinally over the
longus capitis and longus colli muscles.4 Radiographic
characteristics of schwannomas of the vagus nerve are
displacement of the IJV and CCA with separation,
whereas the radiographic characteristics of schwannomas
TABLE 3. Location of schwannoma of the vagus nerve and schwannoma
of the sympathetic nerve in suprahyoid and infrahyoid.
Location
Suprahyoid
Infrahyoid
SCHWANNOMA IN THE CAROTID SPACE
Schwannoma of
the vagus nerve
Schwannoma of the
sympathetic nerve
19*
31
29*
13
p value
.003
* One patient had both schwannoma of the vagus nerve and schwannoma of the sympathetic
nerve in suprahyoid neck region, therefore, the total cases of schwannoma of the vagus
nerve and schwannoma of the sympathetic nerve were 92.
Schwannoma of
the vagus nerve
No. of
Schwannoma of the
No. of
patients 5 41* sympathetic nerve patients 5 36*
Hoarseness
24 (58.3%) Horner syndrome
26 (72.2%)
Cough
8 (19.5%) First-bite syndrome 3 (8.3%)
Horner syndrome 2 (4.8%) Frey’s syndrome
1 (2.7%)
* Among the 91 patients, only 76 patients followed up. One patient had both schwannoma of
the vagus nerve and schwannoma of the sympathetic nerve in the suprahyoid neck region,
therefore, the total cases of schwannoma of the vagus nerve and schwannoma of the sympathetic nerve were 77.
of the sympathetic nerve are displacement of the IJV and
CCA together.4,5,14 On CT scans, schwannomas were relatively homogeneous, with internal cystic change becoming more prominent as the tumors enlarged.15 This cystic
change may be related to mucinous degeneration, hemorrhage, necrosis, and microcyst formation.16 The tumors
were hypointense on T1-weighted MRI images and heterogeneously hyperintense on T2-weighted images. MRI is
reportedly superior to CT because of better soft tissue
delineation, particularly regarding fat signs, which determined the spatial relationship between the tumor and the
great vessels of the carotid space.11,17 Ultrasound was
performed on 76 patients, and was the most commonly
used approach (see Figure 4). Ultrasound imaging of
schwannomas revealed a round or elliptical cross-section
with a clear border with the internal echo reflective of the
histology. Ultrasound has greater diagnostic utility if the
diameter of the nerve of origin is large and the tumor is
connected to a well-delineated nerve.18,19 In our study,
the nerve of origin was correctly diagnosed via ultrasound
in 15 patients, proving that ultrasound was a valuable preoperative diagnostic method. The tumor had separated the
IJV from the ICA or CCA in 86% (43 of 50) of schwannoma of the vagus nerve cases in our study, similar to
Anil and Tan20 study. However, in contrast to the Saito
et al5 study, these 7 schwannomas of the vagus nerve
were independent of location and tumor size, which might
be sporadic incidence.
The surgical approach we used was intracapsular enucleation, which reportedly results in less morbidity
because of better nerve preservation21,22 compared with
the postauricular23 or transaxillary24 approaches. Monitoring for postoperative nerve palsy should be part of the
management of schwannomas. In our series, the incidence
of complications (26.2% for vocal cord paralysis and
33.3% for Horner’s syndrome) was relatively low compared to a previous meta-analysis in which 87.5% of the
patients with schwannomas of the vagus nerve developed
hoarseness,25 and another study in which 80% of the
patients developed varying degrees of Horner’s syndrome.26 The lower incidence of adverse outcomes in our
study is potentially because of our accurate preoperative
diagnosis, especially in diagnosing the nerve of origin,
and the intracapsular enucleation surgical approach. For
patients with schwannoma of the vagus nerve requiring
reoperation, intraoperative nerve monitoring can successfully preserve the vagus nerve and decrease postoperative
morbidity.27
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ZHENG ET AL.
FIGURE 4. Axial sonogram of
extracranial schwannomas in
the carotid space. (A) Axial
sonogram of the right cervical
vagus nerve shows the tumor
(M) that separated the internal
jugular vein (IJV) from the common carotid artery (CCA). (B)
Axial sonogram of the right cervical sympathetic nerve shows
the tumor (M) that displaced the
IJV (arrow) and the external
carotid artery (ECA) and the
internal carotid artery (ICA) in a
posterior direction. [Color figure
can be viewed at wileyonlinelibrary.com]
Navaie et al26 reported that approximately 20% of cases
developed first bite syndrome. In contrast, first bite syndrome occurred in only 7.1% of schwannoma of the sympathetic nerve cases in our study. Ignorance and lack of
recognition of first bite syndrome are potential reasons
for such a low incidence of first bite syndrome compared
with previous reports. First bite syndrome manifests as
pain in the parotid gland or temporomandibular joint on
the operated side upon the first bite of each meal that
diminishes over the next several bites, developing almost
3 months after surgery.28 It has been hypothesized that
the pain is due to parasympathetic hyperactivation that
stimulates an exaggerated myoepithelial cell contraction
throughout the parotid gland.28 Management of first bite
syndrome includes relaxation, limiting the first bite to
bland foods,29 intraparotid botulinum toxin type A injections,30 and medications, such as gabapentin; 1 study
found that 68% of first bite syndrome patients recovered.31 Although only 3 patients reported first bite syndrome in our study, the significant commonalities of
these cases were schwannoma of the sympathetic nerve in
the PPS with concurrent Horner’s syndrome. Identification of these characteristics is essential for predicting
morbidity and allowing high-risk patients to be informed
and well-prepared.
We found that the complications of both schwannoma
of the vagus nerve and schwannoma of the sympathetic
nerve were not related to sex, tumor size, or position; this
was different from a report of Siqueira et al.32 The surgeons’ experience seems to be more important than tumor
size and position in reducing postoperative adverse
events. There were 2 cases diagnosed as malignant
peripheral nerve sheath tumor; a previous report suggested that the only significant negative prognostic factor
of malignant tumor was occurrence of metastases.33 The
small number of clinical cases impacts the credibility of
the inference. For the therapy of malignant peripheral
nerve sheath tumors, although operation is the preferred
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HEAD & NECK—DOI 10.1002/HED
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method for malignant schwannomas, Yafit et al34 concluded that for other patients who had operation contraindication disease, it is not an ideal option. Moreover,
radiotherapy had been proved that had abundant evidence
in promoting local control and quality of life of acoustic
schwannoma in serial studies.35–40 Besides, Liu et al41
reported that using recombinant adenovirus-p53 combined
with radiotherapy had a significant effect for the patient
with a large intrathoracic malignant schwannoma. To sum
up, radiotherapy as an adjuvant therapy has a certain
function on schwannomas.
CONCLUSION
In conclusion, nearly one-third of extracranial schwannomas were located in the carotid space. Of the schwannomas in the carotid space, schwannomas of the vagus
nerve tended to be located below the hyoid bone, whereas
schwannomas of the sympathetic nerve more commonly
arose from the suprahyoid. Postoperative complications of
schwannoma of the vagus nerve and schwannoma of the
sympathetic nerve were unrelated to sex, tumor size, and
position; however, the patients who had a schwannoma of
the sympathetic nerve lesion located in the PPS and had
Horner’s syndrome were more likely to develop first bite
syndrome. The incidence of postoperative morbidity was
decreased by accurate preoperative diagnosis, particularly
in diagnosing the nerve of origin and use of the intracapsular enucleation surgical approach.
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