International Journal of

Radiation Oncology
biology physics

www.redjournal.org

Clinical Investigation: Central Nervous System Tumor

Treatment of Head and Neck Paragangliomas With External

Beam Radiation Therapy
Charles Dupin, MD,* Philippe Lang, MD,y Bernadette Dessard-Diana, MD,z
Jean-Marc Simon, MD,y Xavier Cuenca, MD,y Jean-Jacques Mazeron, MD, PhD,y
and Loı̈c Feuvret, MDy
*Department of Radiotherapy, Comprehensive Cancer Center, Institut Bergonié, Bordeaux, France; yDepartment of
Radiotherapy, Pitié Salpétrière, Paris, France; and zDepartment of Radiotherapy, Hopital Européen Georges Pompidou,
Paris, France

Received Nov 23, 2013, and in revised form Feb 5, 2014. Accepted for publication Feb 6, 2014.

Summary
Today first-line surgery and/
or external beam radiation
therapy are the main options
for the management of head
and neck paraganglioma, and
recently radiosurgery has
been presented as an alter-
native. We retrospectively
evaluated 81 head and neck
paragangliomas treated with
external beam radiation
therapy with conventional
fractionation. Only 1 recur-
rence was observed, but 2
toxic deaths occurred in pa-
tients with bulky disease.
External beam radiation
therapy is an excellent option
in head and neck
paragangliomas.
Purpose: To retrospectively assess the outcomes of radiation therapy in patients with
head and neck paragangliomas.
Methods and Materials: From 1990 to 2009, 66 patients with 81 head and neck paragan-
gliomas were treated by conventional external beam radiation therapy in 25 fractions at a
median dose of 45 Gy (range, 41.4-68 Gy). One case was malignant. The median gross target
volume and planning target volume were 30 cm3 (range, 0.9-243 cm3) and 116 cm3 (range,
24-731 cm3), respectively. Median age was 57.4 years (range, 15-84 years). Eleven patients
had multicentric lesions, and 8 had family histories of paraganglioma. Paragangliomas were
located in the temporal bone, the carotid body, and the glomus vagal in 51, 18, and 10 pa-
tients, respectively. Forty-six patients had exclusive radiation therapy, and 20 had salvage
radiation therapy. The median follow-up was 4.1 years (range, 0.1-21.2 years).
Results: One patient had a recurrence of temporal bone paraganglioma 8 years after treat-
ment. The actuarial local control rates were 100% at 5 years and 98.7% at 10 years. Patients
with multifocal tumors and family histories were significantly younger (42 years vs 58 years
[PZ.002] and 37 years vs 58 years [PZ.0003], respectively). The association between fam-
ily predisposition and multifocality was significant (P<.001). Two patients had cause-
specific death within the 6 months after irradiation. During radiation therapy, 9 patients
required hospitalization for weight loss, nausea, mucositis, or ophthalmic zoster. Two late
vascular complications occurred (middle cerebral artery and carotid stenosis), and 2 late
radiation-related meningiomas appeared 15 and 18 years after treatment.
Conclusion: Conventional external beam radiation therapy is an effective and safe treatment
option that achieves excellent local control; it should be considered as a first-line treatment
of choice for head and neck paragangliomas. Ó 2014 Elsevier Inc.

Reprint requests to: Charles Dupin, MD, Institut Bergonié, Compre- Conflict of interest: none.
hensive Cancer Center, Department of Medical Oncology, 229 cours de Supplementary material for this article can be found at
l’Argonne, 33000 Bordeaux, France. Tel: (þ33) 5-56-33-33-20; E-mail: www.redjournal.org.
c.dupin@bordeaux.unicancer.fr

Int J Radiation Oncol Biol Phys, Vol. 89, No. 2, pp. 353e359, 2014
0360-3016/$ - see front matter Ó 2014 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.ijrobp.2014.02.010
354 Dupin et al. International Journal of Radiation Oncology  Biology  Physics

Introduction summarized in Table 1. Characteristics of the para-

Head and neck paragangliomas are rare tumors whose
incidence is estimated at 1-10 cases per million people per
year (1). The tumors originate in the head and neck para-
ganglia, and they are benign in 90%-95% of cases (2).
Genetic susceptibility has been found in 15% of cases with
mutations in the SDHB, SDHC, and SDHD genes (succinate
dehydrogenase complex, subunit B, C, and D, respectively)
(2). The medical challenge for these slow-growing tumors
with a good prognosis is to achieve the best local control
with the least toxicity. The 2 main treatment options are
surgery and radiation therapy.
Conventional fractionated external beam radiation
therapy (EBRT) has been performed since 1950, with
local control rates of 95% (3), and it is usually proposed as
an alternative to surgery. Radiation therapy does not
usually eliminate the radiologic tumor, and thus the aim is
to stop the progression of symptomatic disease (4). No
randomized trials have compared these 2 treatments,
which have different toxicities, owing to the rarity of the
disease and the different characteristics of these 2 pop-
ulations (5).
The main objective of this retrospective, single-center
study was to report the results of EBRT for head and neck
paragangliomas.
Methods and Materials
All patients irradiated at Pitié Salpétrière Hospital (Paris,
France) for head and neck paragangliomas from January
1990 to December 2009 were included. The diagnosis was
defined radiologically by angiography or magnetic reso-
nance (MR) angiography (46 patients) or histologically (20
patients). No patient was excluded from the study.
Patient and disease characteristics
Sixty-six patients were included for the treatment of 81
paragangliomas. Patient and treatment characteristics are
gangliomas are summarized in Table 2. The median and
mean follow-up durations were 4.1 years and 5.9 years
(range, 0.1-21.2 years), respectively.
Neurologic involvement before EBRT was the same for
exclusive and postoperative radiation therapy. Only facial
palsy was more common before postoperative radiation
therapy (50%) than before exclusive radiation therapy (9%)
(Fig. 1).
Radiation therapy indications
Forty-six patients had radiation therapy alone because of
advanced age, risk of postoperative sequelae, and an
elective indication for tympanic paragangliomas. Three
patients had postoperative radiation therapy because of
incomplete resection and 17 patients for recurrence after
surgery.
Radiation therapy
All patients were immobilized with a thermoplastic head
mask. Helical CT simulation was performed in all pa-
tients and merged with the previously generated thin-
slice MR images from 2001. Target volumes were defined
according to International Commission for Radiation
Units and Measurements report 50 definitions (6); gross
target volume was defined according to the area of
contrast enhancement on CT and MRI T2 fat sat or
contrast enhancement on MRI T1. Clinical target volume
was defined by adding a 7-mm margin to the gross target
volume along the main vessels. Clinical target volumes
were expanded by a 3-mm margin to form the planning
target volumes (PTVs). The median prescribed dose was
45 Gy (range, 45-46 Gy) to the PTV except for 2 patients.
The first had a sellar localization (67 Gy) and the second
a malignant paraganglioma (68 Gy). The median dose per
fraction was 1.8 Gy (range, 1.8-2.0 Gy). The median
treatment duration was 36 days (range, 32-52 days).
Irradiation was performed with either a 60Co machine or

Table 1 Patient characteristics

Characteristic All patients (nZ66) Exclusive RT (nZ46) Postoperative RT (nZ20)
Follow-up (y), median (range) 4.1 (0.1-21.2) 4.0 (0.1-21.0) 4.1 (0.4-21.2)
Age (y), median (range) 57.4 (15.1-83.7) 60.8 (24.4-83.7) 52.1 (15.1-78.1)
Sex ratio (no. female/no. male) 3.7 (52/14) 2.8 (34/12) 9 (18/2)
Cases with family histories, n (%) 8 (12) 4 (9) 4 (20)
Malignant cases, n 1 0 1
Multifocal paragangliomas, n (%) 11 (17) 7 (15) 4 (20)
GTV (cm3), median (range)* 30 (0.9-243) 17 (1.4-243) 19 (0.9-34)
PTV (cm3), median (range)* 116 (24-731) 113 (29.4-731) 119 (24-224)
Dose (Gy), median (range) 45.0 (41.4-68.0) 45.0 (41.4-67.0) 45.0 (43.2-68.0)
Abbreviations: GTV Z gross target volume; PTV Z planning target volume; RT Z radiation therapy.
* Data available for 39 patients.
Volume 89  Number 2  2014 RT in head and neck paragangliomas 355

Table 2 Tumor characteristics

All paragangliomas Tympano-jugular Vagal paragangliomas Carotid paragangliomas
Characteristic (nZ81)* paragangliomas (nZ51)y (nZ18)z (nZ10)
Follow-up (y), mean (range) 5.9 (0.1-21.2) 5.9 (0.1-21.2) 4.2 (0.5-13.2) 8.5 (1.1-21.2)
Age (y), median (range) 57.4 (15,1-83.7) 57,4(15.1-80.5) 48.8 (23.1-75.6) 33.5 (24.4-83.7)
Sex ratio (no. female/no. male) 3.7 (52/14) 3.9 (39/10) 2,4 (12/5) 2 (4/2)
Multifocal paragangliomas, n (%) 26 (32) 9 9 8
Exclusive RT, n (%) 60 (74)* 35 14 9
Postoperative RT, n (%) 21 (26) 16 4 1
Abbreviation as in Table 1.
* Two histologically proven paragangliomas (sella tursica and cerebellum) do not appear in the other columns.
y
Fisch classification (7) of jugular paragangliomas was A: 4%; B: 10%; C: 45%; D: 41%.
z
One vagal paraganglioma with metastatic cervical node is included in this column.

a 4- to 18-MV photon beam from a linear accelerator. Results

The median number of fields was 3 (range, 2-6).
Follow-up and statistical analysis
Patients were followed annually with MRI. Follow-up was
begun as of the first date of treatment. Telephonic follow-up
was done if patients were not able to visit the hospital.
Twenty-two patients were lost to follow-up at the time of
analysis. Local control was defined as stability or regres-
sion of clinical signs and the absence of radiologic
progression.
Absence of specific treatment failure was defined as
including both local control and no early cause-specific
death. Relevant side effects were noted according to
Common Terminology Criteria for Adverse Events (version
4.03). Statistical tests for mean age comparisons were
bilateral Student t test with an a risk of 5% and the Fisher-
Snedecor test for validation of the homogeneity of vari-
ances. The c2 test was used to analyze the association
between family predisposition and multifocality. Analyses
of patient follow-up for local control and absence of spe-
cific treatment failure were performed using the Kaplan-
Meier method.
Population
Patients with multifocal tumors were significantly younger
(42 years vs 58 years; PZ.002). Patients with family his-
tories were significantly younger (37 years vs 58 years;
PZ.0003) (Fig. e1, available online). Of the 8 patients with
family histories of paraganglioma, 5 had multifocal lesions.
The association between family predisposition and multi-
focality was significant (P<.001).
Local control and absence of specific treatment
failure
For head and neck paragangliomas, local control was
100% at 5 years and 98.7% (95% confidence interval [CI]
96%-100%) at 10 years. Absence of specific treatment
failure was 97% (95% CI 94%-100%) at 1 year and 5 years
and 94% (95% CI 87%-100%) at 10 years (Fig. 2). For
jugular and tympanicum paragangliomas, local control was
100% at 5 years and 98% (95% CI 94%-100%) at 10 years.
Absence of specific treatment failure was 95% (95% CI
90%-100%) at 1 year and 5 years and 91% (95% CI
81%-100%) at 10 years.
No local recurrence or death due to disease occurred for
vagal paragangliomas, carotid paragangliomas, the cere-
bellar paraganglioma, the paraganglioma in the sella tur-
cica, or metastatic paraganglioma.

Analysis of local failure

A 57-year-old woman was irradiated at 46.8 Gy for Fisch B

Fig. 1. Initial neurologic impairment before exclusive
radiation therapy or before postoperative radiation therapy.
)P<.001, c2 test.
(7) tympanic paraganglioma with a PTV of 51 cm3. The
tumor had been treated by embolization 19 years before.
Sixty-five months after irradiation, pain recurred, and
7 years later the patient underwent surgery resection of
local recurrence in the mastoid. She is currently being
monitored clinically and radiologically; 5 years after sur-
gery she presents with occasional bleeding from the ear.
356 Dupin et al. International Journal of Radiation Oncology  Biology  Physics

Fig. 2. (A, B) Kaplan-Meier estimate of the absence of treatment failure (A) and local control (B) of 81 head and neck
paragangliomas treated by external beam radiation therapy between 1990 and 2009. (C, D) Kaplan-Meier estimate of the
absence of treatment failure (C) and local control (D) of 51 jugular paragangliomas treated between 1990 and 2009.
NZnumbers of paragangliomas at risk.

Analysis of the 2 cases of early death Acute toxicity

Two patients died of disease symptoms in the 6 months
after radiation therapy. Both patients initially presented a
Fisch D2 significant intracranial invasion with palsy of
cranial nerves 8, 9, 10, 11, and 12 associated with choking.
The first patient was a 68-year-old woman irradiated at
45 Gy by 2 fields of 65  85 mm. Corticosteroid therapy
was administered for 30 days to treat nausea. Weight loss
was 14%. After radiation therapy her trouble swallowing
worsened, causing aspiration pneumonia requiring hospi-
talization. She died of pulmonary embolism 4 months after
the end of treatment. No radiologic investigation was per-
formed. The second patient was a 77-year-old man irradi-
ated at 45 Gy in a volume of 731 cm3 (major axis, 8 cm),
with a short hospitalization of 6 days for dehydration.
Initially he presented oculomotor and facial nerve palsy.
Five months after radiation therapy, the patient died of
cachexia and secondary symptoms of the disease. No
radiologic investigation was performed.
Details regarding toxicity are presented in Table 3. Forty-
five patients had grade 1-2 nausea, and 34 of them were
treated with corticosteroids. Fifteen patients had a weight
loss of more than 10% of their initial weight. Nine patients
were hospitalized (grade 3-4) for a mean of 13 days (range,
5-30 days) for weight loss, nausea, mucositis grade 3, or
ophthalmic zoster.
Late toxicity
Twenty patients had grade 1-2 xerostomia at 2 years. Five
years after radiation therapy, 1 patient had a stroke asso-
ciated with 75% stenosis of the ipsilateral middle cerebral
artery. Five years after radiation therapy, another patient
had symptomatic carotid stenosis at the original tumor site.
Evolution was favorable after treatment in both cases. One
patient had symptomatic paresis of the spinal accessory and
Volume 89  Number 2  2014 RT in head and neck paragangliomas 357

Table 3 Acute and late toxicities classified according to CTCAE, version 4.03
Toxicity Grade 1-2 Grade 3-4*
y
Acute toxicity Nausea (45) Hospitalization (9): weight loss, nausea,
Weight loss (15) mucositis, or ophthalmic zoster
Late toxicity Xerostomia (20) Middle cerebral artery stenosis 75% (1)
Aphthous ulcer (1) Carotid stenosis (1)
Accessory and hypoglossal nerve paresis Temporal necrosis (reirradiation) (1)
and swallowing disorders (1)
Transient worsening of swallowing disorders (1)
Secondary neoplasm Cavernous sinus meningioma (1)
Parietal meningioma treated by surgery
without sequelae (1)
Abbreviation: CTCAE Z Common Terminology Criteria for Adverse Events.
Values in parentheses are number of patients.
* No grade 4 late toxicity was found.
y
Thirty-four patients required corticosteroids.

hypoglossal nerves, classified as grade 2 radiation toxicity, Radiation therapy is therefore an alternative treatment of
due to a reduction of the paraganglioma on MRI. One pa- choice for these localizations.
tient had a transient worsening of choking 6 months after For jugular paragangliomas, our results are similar to
the end of radiation therapy, which resolved spontaneously. those of a recent review of the literature (1989-2010), in
One patient presented temporal radionecrosis 6 months which the local control rate was 93% (Table 4) (3, 4, 8-12,
after radiation therapy. She had been irradiated with 14-19). Previously, Pryzant et al (15) estimated local con-
2  5 Gy 2 years earlier for head and neck lymphoma. She trol at 89% with radiation therapy for 373 patients in a
died 1 year later of acute myeloid leukemia type 6. series lasting from 1964 to 1989. This improvement in local
Two patients had secondary meningiomas. One patient control is probably related to the improvement in target
treated at age 50 years presented a cavernous sinus me- volume identification and homogeneity of dose delivery.
ningioma with grade 2 oculomotor disorders 18 years after Surgical management of jugular paragangliomas has
irradiation; she has been monitored for 2 years at time of yielded variable local control rates according to literature
writing. One patient treated at age 30 years for 3 para- reviews. Gottfried et al (20) reported local control at 92%
gangliomas (1 carotid and 2 Fisch type D2 skull base) with a mean follow-up of 4.1 years. Ivan et al (21) reported
presented a parietal meningioma 15 years after irradiation. local control of 69% in cases of incomplete resection and
It was treated by surgery and has been in complete remis- 86% after complete resection with a mean follow-up of 6
sion for 5 years at time of writing. years and 7.3 years, respectively. These studies were het-
erogeneous, but the more recent studies seem to show an
Discussion
Table 4 Review of the literature on local control of jugular
We present here the largest series, to our knowledge, of paragangliomas treated by EBRT
paragangliomas treated by homogeneous EBRT, with Year of First author Treatment Local
excellent local control results. Of 81 cases there was only publication (reference) dates control/total
1 that relapsed 8 years after treatment, and 2 patients of 66
1989 Pryzant (15) 1965-1984 18/19
died of their disease within 6 months after radiation 1990 Boyle (14) 1971-1988 9/9
therapy. Rates of local control and disease-specific sur- 1992 Powell (16) 1949-1985 52/59
vival at 10 years were 98.7% and 94%, respectively. 1992 Schild (17) 1974-1988 8/8
Tolerance of the treatment was acceptable. Interpretation 1992 Verniers (18) 1970-1990 17/19
of these results must take into account the limitations of a 1992 Larner (4) 1932-1985 25/29
retrospective study with a follow-up period that can be 1995 de Jong (19) 1956-1991 34/38
considered short for this type of pathology. For the 2002 Saringer (11) 1978-2001 3/18
recurrence after 8 years, no risk factor for long-term 2002 Elshaikh (12) 1969-1999 5/5
relapse was found as compared with other studies (3, 8). 2005 Pemberton (10) 1965-1987 47/49
Here our study shows its main limitation, because the 2006 Krych (9) 1967-1994 19/19
2008 Hinerman (3) 1968-2004 75/80
mean follow-up of 5.9 years is shorter than the latency of
2010 Lightowlers (8) 1998-2008 20/21
the first recurrence detected. However, 25 paragangliomas 2014 Dupin 1990-2009 50/51
were followed for 8 years, 16 for 10 years, and 7 for 15 Total 394/424 (93%)
years. For vagal and carotid paragangliomas, local control
Abbreviation: EBRT Z external beam radiation therapy.
was 100% in our study and in the literature (3, 9-14).
358 Dupin et al.
improvement in local control. Thus, radiation therapy and
surgery have, at this time, equivalent local control rates.
In terms of early toxicity, our methodology, from which
we did not exclude any patients, shows 2 deaths related to
the disease within 6 months after irradiation. To our
knowledge this has never been reported. In fact, Hinerman
et al (3) and Larner et al (4) reported excellent median
follow-ups of 8.5 and 16.2 years, respectively. However, no
patient followed during a period of less than 2 or 5 years,
respectively, was reported. By not reporting patients with
short follow-ups, results can potentially be biased. Risk
factors for early death that we observed were advanced age,
bulky disease with significant local invasion (Fisch D2),
and cranial nerve involvement. In any case, this underlines
the importance of the implementation of supportive care for
patients with benign disease; and even when a disease is
benign, physicians should not underestimate the functional
consequences it, and its treatment, can have on their
patients.
In our study, 5 patients showed grade 3 late toxicity. We
describe 2 cases of radiation-induced meningioma after 15
and 18 years of follow-up. These 2 cases may justify fears
related to radiation therapy, but with regular and extended
monitoring these meningiomas are potentially manageable
without sequelae. Moreover, in a recent review, Krych et al
(9, 14) report only 3 cases of secondary malignancies
(fibrosarcoma, astrocytoma). Similarly, Springate et al (22)
calculated a risk of 0.28% for secondary tumors. Usually,
secondary neoplasms occur very late after radiation therapy
and have to be counterbalanced with the immediate and
deterministic side effects of the surgery. Huy et al (5)
compared radiation therapy and surgery for jugular para-
gangliomas. Of the 47 patients treated by surgery, 7 experi-
enced cerebrospinal fluid leakage through the skin incision,
and 11 patients experienced severe aspiration pneumonia
and/or marked dysphonia or swallowing problems. At 1 year
after operation, there was a 33% incidence of facial weak-
ness. In this study, toxicity in the radiation therapy group was
unquestionably considered more acceptable.
Stereotactic radiation therapy may be evoked as an
alternative for the treatment of small jugular para-
gangliomas. Guss et al (23) have reported an interesting
local control rate of 97% with a mean follow-up of more
than 36 months. The mean volumes treated by each tech-
nique are different: stereotactic radiation therapy, from
5.2 cm3 (24) to 13.2 cm3 (25); conventional radiation
therapy, 23 cm3 in the study by Lightowlers et al (8) and
30 cm3 in our study. Moreover, in a meta-analysis, Gott-
fried et al (20) reported neurologic toxicity in 8.5% of
patients. Stereotactic radiation therapy could be preferred
for small jugular paragangliomas.
For the first time, to our knowledge, our clinical study of
radiation therapy shows the link between early disease,
multifocality, and family history. Even if this link is only
statistical, it is in agreement with epidemiologic studies (2,
26). Burnichon et al (2) showed that SDH mutation carriers
were 14 years younger at the age of diagnosis than
International Journal of Radiation Oncology  Biology  Physics
nonemutation carriers and that SDH mutation carriers were
92% in patients with multiple paragangliomas and 99% in
patients with family history of paragangliomas. Extrapo-
lating these results to our study, 13 patients (20%) would
have had a genetic predisposition because of their family
history and/or their multifocal involvement, which is
similar to some clinical studies (26). Genetic testing should
be routinely offered to all patients with head and neck
paragangliomas (2).
In conclusion, irradiation of 45 Gy in 25 fractions is an
excellent treatment for head and neck paragangliomas, with
local control that is at least equivalent to that of surgery and
with a toxicity that seems to us less harmful. A more
important place should be given to radiation therapy in
first-line treatment.
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