Journal of the Egyptian Nat. Cancer Inst., Vol. 20, No.

3, September: 230-236, 2008

Nasopharyngeal Carcinomas:
Prognostic Factors and Treatment Features
M.D.**; ZAFER ZDO GAN,

BILGIN KADRI ARIBAS,

M.D.*; FAIK ETINDAG,
M.D.**;
AYSEN DIZMAN, M.D.**; PELIN DEMIR, M.D.*; DILEK NIL NL, M.D.* and

ZEYNEL YOLOGLU,
M.D.*
The Departments of Radiology* and Radiation Oncology**, Ankara Oncology Education and Research Hospital,
Ankara, Turkey.

Key Words: Nasopharyngeal carcinoma Prognostic

factor MRI CT Radiotherapy Chemotherapy.

ABSTRACT
Purpose: We retrospectively evaluated the clinical,
radiological and pathological features determining the
prognosis of patients with nasopharyngeal carcinoma in
Ankara Oncology Hospital, Turkey.

INTRODUCTION
The nasopharynx is a cuboidal cavity formed
by muscle and fascia with an epithelial mucosal
covering. Nasopharyngeal carcinoma is a rare
tumor that arises in this epithelium [1] . It is
more common in males by a margin of about 2
to 1 and its incidence peaks at 50 to 60 years
of age; a small peak also occurs during late
childhood [1].

Material and Methods: Two hundred and fifty-nine

patients, 74 women and 185 males with nasopharyngeal
carcinoma were treated between 1993 and 2008. All
imaging data including CT and MRI were reevaluated
according to the criteria which determine parapharyngeal,
oropharyngeal, nasal, skull-base (bone)/sinus, infratemporal fossa, orbit, intracranial involvements and lymph
node metastasis by our radiologists. The patients were
restaged using the AJCC 2002 classification with these
new radiological findings and clinical data base. We
evaluated prognostic factors using univariate KaplanMeier and multivariate Cox regression analyses. Gender,
age (40-year cut-off), histology, T- and N-stage, tumor
size, regional involvement, radiotherapy and/or chemotherapy and response to therapy were studied as variables.

Nasopharyngeal carcinoma is highly radiosensitive and radical external beam radiotherapy is the mainstay of treatment for this neoplasm and its regional lymph node metastasis
[2]. There have been studies on prognostic factors of nasopharyngeal carcinoma; however,
their outcomes are still controversial [1-9]. So,
radiology and radiation oncology clinics collectively reevaluated prognostic factors which
influence survival of the patients treated with
nasopharyngeal carcinoma.

Results: Five-year disease-free and overall survival

rates were 454% and 723%, respectively. We found
that age, gender, WHO type, radiotherapy and/or chemotherapy, N-stage and response to therapy were significant
prognostic factors on disease-free survival and overall
survival. In the chemo-radiotherapy group, we did not
detect any survival difference between patients given four
or fewer chemotherapy courses.

MATERIAL AND METHODS

Conclusions: Radiotherapy improved survival but

chemotherapy, in the neoadjuvant and adjuvant setting,
had no added effect to radiotherapy. N-stage and response
to treatment were the most important independent predictors on survival. Age, gender, type, therapy and bone/sinus
involvement were among the predictive factors on multivariate analysis, as well.

In this study, we retrospectively reviewed

the clinical, radiological, laboratory and pathological data of 259 patients treated for nasopharyngeal carcinoma between 1993 and 2008. Of
them, 74 (28.5%) were women and 185 (71.2%)
were males. The mean and median ages were
43.617.6 and 46 years (range, 9-89 years),
respectively. There was a second peak in the
second decade in 38 patients (14.7%).

Correspondence: Dr Bilgin Kadri Aribas

bilginaribas@hotmail.com

230

Nasopharyngeal Carcinomas

All patients had nasopharynx biopsies which

diagnose a nasopharyngeal carcinoma. They
had as well hospital records including history,
complete blood count, physical examination,
direct nasopharyngoscopy, chest X-ray, head/
neck computed tomography (CT) and sometimes
(69 patients) magnetic resonance imaging
(MRI). In clinical necessity, abdomen ultrasonography (US) and bone scintigraphy were
done as well. Image interpretation was made
by a group of radiologists (B.K.A., P.D., D.N..
and Z.Y.) with consensus. The aim of this interpretation was to reevaluate parapharyngeal,
oropharyngeal, nasal, skull-base (bone/sinus),
orbit and infra temporal fossa involvements,
intracranial invasion, also to assess lymph node
metastasis on CT and/or MRI images. Prevertebrally muscle invasion was interpreted only
on MRI (69 patients). In the light of clinical
and new radiological data, we restaged all patients according to the 2002 TNM classification
of the American Joint Committee on Cancer
(AJCC). In this way, all patient data coming
from different hospitals were uniformly grouped
to 2002 TNM classification On CT, parapharyngeal invasion (T2b) was accepted positive if
there was distortion of the parapharyngeal fat
plane or extension beyond a line drawn from
the medial pterygoid plate to the lateral aspect
of the carotid artery as described by King et al.
[4]. CT findings were well correlated with those
of MRI if it was performed. To assess skullbase and sinus invasions on axial and coronal
CT images, we used the criteria of appearance
of bone destruction, besides, disappearance of
fatty plane on contiguous soft-tissue extension.
Gender, age, histology, T- and N-stage, tumor
size, regional involvement, radiotherapy and/or
chemotherapy and response to therapy were
recorded. Age was defined as two groups; 40year and >40-year. Three groups were determined for nasopharyngeal tumor size: <1cm,
1-3cm and >3cm. We classified histological
types of nasopharyngeal carcinoma using criteria
of the World Health Organization (WHO) such
as type 1 (squamous), type 2 (non-keratinizing
squamous) and type 3 (undifferentiated).
For all cases, two dimensional conventional
radiotherapy planning technique and customized
cerrobend blocks were used. A total dose of 6074Gy with daily fraction of 1.8-2Gy, 5 fractions
weekly was given by using linear accelerators

231

(Saturn 41, Saturn 43) in two or three phases.

Two lateral parallel opposed fields were used
for tumor and upper cervical lymph nodes,
whereas anterior field for low cervical nodes.
In our asymmetric collimator technique, we
generally separate two overlapping fields over
the thyroidal cartilage and sparing larynx by
casting an anterior block. The first phase was
completed according to the spinal cord dose up
to 46-50Gy. In the second phase, 9-12 MeV
electron beams were used for posterior neck
region. The posterior neck dose was between
50-70Gy according to the degree of involvement. Custom-made fields covering tumor extension plus one cm margin were performed for
every patient.
Before 2008, we administered 2-3 courses
of neoadjuvant chemotherapy for patients with
stage 2 due to shortage of radiotherapy equipment. The chemotherapy regimen contained
cisplatin 80m/m2 on day 1 and 5-fluorouracil
750mg/m 2 on days 1-5. After radiotherapy,
patients with stage 2 were given two more
chemotherapy courses as adjuvant. The patients
were classified according to the therapentic
modalities received (Table 1). Chemoradiotherapy administered group was further divided
into two: Those who were given less than or
equal to three or more than three of total chemotherapy courses. Various chemotherapy regimens were administered in case of metastasis.
Follow-up was performed every three
months for the first two years and every four
months thereafter. Every patient was routinely
assessed by using fiber-optic nasopharyngoscopy and contrasted nasopharynx and neck CT in
the end of the third month. MRI was performed
in clinical necessity. Endoscopic biopsy was
taken in suspected recurrent or residual lesions.
Radiotherapy and/or chemotherapy and clinical features were reviewed from the records
by the radiation oncologists (F.., Z. and
A.D.). Overall survival was identified as the
time from diagnosis to death or last follow-up,
while disease-specific survival was defined as
the time from diagnosis to death which was
caused by nasopharynx carcinoma. As a diseasefree survival, we accepted the length of time
with no signs of recurrence or metastasis. The
Kaplan-Meier method and the log-rank test for
linear trend were used for these assessments.
Multivariate analysis was performed using the

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Bilgin K. Aribas, et al.

Cox regression analysis. We entered type, diameter, therapy, T-stage and N-stage as categorical variables in Cox regression analysis. A pvalue of 0.05 or less at 95% confidence interval
was considered to be statistically significant.
Primary endpoints of this study were diseasefree and overall survivals.
RESULTS
Table (1) demonstrates the demographic data
of patients with nasopharyngeal carcinoma. The
mean and median follow-up periods were 24.9
27.7 and 14 months (range, 1-170 months),
respectively.
In our series, eight of 259 patients had concomitant second malignancies: Seven carcinomas (lung, larynx, breast, testis, thyroid, renal
and prostate) and one gluteal alveolar rabdomyosarcoma. Our clinical signs and symptoms
were 179 neck masses (69.1%), 35 nasal obstructions (13.5%), 21 hearing losses and ear
fellnesses (8.1%) and 16 epistaxes (6.2%), five
diplopia (2.0%), seven tinnitus (2.7%) and seven
dysphasia (2.7%).
As a treatment modality, a total of 65 patients
received only radiotherapy. Among them, sixtyone patients (24.7%) had 60Gy, while four
patients (1.6%) had <60Gy.
There were eight patients with distant metastasis on diagnosis; in addition 56 patients
with metastasis were detected after diagnosis.
These eight patients were excluded from metastasis and progression evaluation for systemic
failure. Of these 56 patients, there were 41
skeletal, 23 lung, 13 hepatic and 10 other organ
metastases. The most frequently involved sites
of skeletal metastasis were the vertebrae, cranium and pelvis, in order. There were 38 locoregional recurrences and the median time for this
was thirteen months.
Prognostic factors for overall survival by
univariate and multivariate analysis are shown
in tables (2,3). Five-year disease-free, diseasespecific, overall, locoregional recurrence-free
and metastasis-free survivals were 454%,
763%, 723%, 763% and 664%, respectively.
The prognostic factors for the disease-free
survival were gender, diameter, oropharynx,
bone/sinus, intracranial, parapharyngeal, T-

stage, N-stage, therapy and response on univariate analysis. Nevertheless, these were age (p=
0.018), gender (p=0.032), type (p=0.044), therapy (p=0.019), N-stage (p=0.005) and response
(p<0.001) on multivariate analysis. The fiveyear disease-free survival rates were as follows:
40 year (466%), >40 year (445%); female
(597%) and male (404%); type 1 (289%),
type 2 (497%) and type 3 (475%); radiotherapy (578%), combined chemo-radiotherapy
(444%). N0 stage (849%), N1 (466%), N2
(416%), N3a (0%) and N3b (0%); response
(514%) and no response (0%).

Table (1): Analysis of patients with nasopharyngeal carcinoma.

Features

Patients (%)

Total
Female/Male
Age (median; range)
Follow-up (median; range)

259 (100)a
74 (28.5)/185 (71.2)
46; 9-89 years
14; 1-170 months

WHO type:
1
2
3

29 (11.2)
67 (25.8)
163 (62.7)

Diameter:
<1cm
1-3cm
>3cm

31 (12.0)
62 (23.9)
166 (64.1)

T-stage:
1
2a/2b
3
4

46 (17.8)
43 (16.6)/93 (35.9)
41 (15.8)
36 (13.9)

N-stage:
0
1
2
3a/3b

30 (11.6)
111 (42.9)
102 (39.4)
8 (3.1)/8 (3.1)

Therapy:
Radiotherapy
Chemotherapy
Combinedb
<60Gy radiotherapy
No therapy

65 (25.9)
7 (2.8)
175 (69.7)
4 (1.6)
8 (3.1)

Response to treatmentc:
No
Yes

27 (11.1)
217 (88.9)

a Numbers in parenthesis are percentages.

b Chemo-radiotherapy.
c Response was not evaluated in the other 15 of 259 patients.
(8 with no therapy and 7 patients not being evaluated).

Nasopharyngeal Carcinomas

233

Table (2): Prognostic factors on disease-free, disease-specific and overall survivals.

Features
Agea
Gender
WHO type
Diameter
Oropharynx
Prevertebrald
Bone/sinus
Intracranial
Parapharyngeal
Nasal
T-stage
N-stage
Therapy
Response

Disease-free survival

Disease-specific

Overall survival

0.221b; 0.018c
0.017; 0.032
0.057; 0.044
<0.001; 0.112
0.014; 0.089
0.980
0.005; 0.565
0.004; 0.828
<0.001; 0.471
0.891; 0.852
<0.001; 0.923
<0.001; 0.005
<0.001; 0.019
<0.001; <0.001

0.296; 0.178
0.066; 0.240
0.616; 0.880
<0.001; 0.259
0.768; 0.811
0.754
0.142; 0.401
0.060; 0.464
<0.001; 0.925
0.924; 0.849
<0.001; 0.670
<0.001; 0.001
<0.001; 0.144
<0.001; 0.009

0.364; 0.476
0.327; 0.914
0.553; 0.884
<0.001; 0.327
0.588; 0.522
0.587
0.280; 0.522
0.071; 0.448
<0.001; 0.940
0.724; 0.743
<0.001; 0.632
<0.001; <0.001
<0.001; 0.465
<0.001; 0.001

a 40-year and >40-year.

b The first, p value in univariate analysis and c the second, p value in multivariate analysis.
d Only univariate analysis was made in prevertebral involvement. 26 of 69 patients had this
invasion in MRI.
Five-year disease-free survival rates were 935% in stage 1, 877% in stage 2a, 686% in stage
2b, 699% in stage 3 and 739% in stage 4.

Table (3): Prognostic factors on recurrence-free and metastasis-free survivals.

Features
Agea
Gender
WHO type
Diameter
Oropharynx
Prevertebrald
Bone/sinus
Intracranial
Parapharyngeal
Nasal
T-stage
N-stage
Therapy
Response

Recurrence-free survival

Metastasis-free survival

0.239b; 0.016c
0.870; 0.873
0.026; 0.012
0.002; 0.129
0.051; 0.124
0.968
0.065; 0.048
0.522; 0.592
<0.001; 0.145
0.350; 0.738
0.021; 0.141
0.157; 0.366
<0.001; 0.455
<0.001; 0.179

0.476; 0.930
0.113; 0.036
0.050; 0.053
<0.001; 0.741
0.026; 0.101
0.737
0.054; 0.940
0.116; 0.677
<0.001; 0.643
0.560; 0.729
<0.001; 0.779
0.011; 0.683
0.167; 0.421
<0.001; <0.001

a 40-year and >40-year.

b The first, p value in univariate analysis and c the second, p value in multivariate analysis.
d Only univariate analysis was made in prevertebral involvement.

The prognostic factors that affected diseasespecific survival were diameter, parapharyngeal,
T-stage, N-stage, therapy and response, whereas
they were N-stage (p=0.001) and response
(p=0.009) on multivariate analysis. Five-year
disease-specific survival rates were; N0 stage
(946%), N1 (825%), N2 (736%), N3a (0%)
and N3b (0%); response (813%) and no response (4411%).

Similarly, prognostic factors affecting the

overall survival were diameter, parapharyngeal,
T-stage, N-stage, therapy and response, whereas
these were N-stage (p<0.001) and response
(p=0.001) on multivariate analysis. Five-year
overall survival rates of them were such as: N0
stage (897%), N1 (805%), N2 (696), N3a
(0%) and N3b (0%); response (794%) and no
response (3310%).

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Bilgin K. Aribas, et al.

However, the prognostic factors for locoregional recurrence were type, diameter, parapharyngeal, T-stage, therapy and response on
univariate analysis. These were age (p=0.016),
type (0.012) and bone/sinus (p=0.048) on multivariate analysis. Five-year recurrence-free
survival rates of them were as follows: 40year (785%) and >40-year (755%); type 1
(6012%), type 2 (895%), type 3 (744%)
and no bone/sinus (804%) and bone/sinus
(687%).
Prognostic factors affecting distant metastasis were type, diameter, oropharynx, parapharyngeal, T-stage, N-stage and response on
univariate analysis, while they were gender
(p=0.036) and response (p<0.001) on multivariate analysis. Five-year metastasis-free survival
rates of them were as follows: Female (747%)
and male (625%); response (684%) and no
response (0%).

As a treatment modality, seven patients

received chemotherapy-only treatment (cisplatin
based). Details are given in Table (4). Among
175 patients with chemo-radiotherapy group,
142 had a total of four courses as neoadjuvant
and adjuvant, whereas 33 had less than four
courses (due to intolerance or rejecting the
recommended therapy). The survival rates did
not statistically differ according to the numbers
of chemotherapy courses (p>0.05) (Table 5).
Various complications were documented in
the series. Poor quality life and anxiety depression were usually seen after chemotherapy
and/or radiotherapy. The complication leading
to poor quality of life was mostly xerostomia.
Serious and/or fatal complications are summarized in Table (6). Serious complications were
seen in 3.1% (8/259), 1.5% (4/259) was fatal
(two due to chemotherapy and two to radiotherapy).

Table (4): Characteristics of patients in the chemotherapy-only group.

T-stage/N-stage

WHO type

Cures

Complication due
to therapy

Follow-up/
fatality

34/F

T2b/N3b

Hemorrhage

1/year

58/F

T2b/n1

No

5/no

62/M

T4/N1

No

2a/no

33/F

T2a/N0

No

2a/no

33/M

T2b/N1

No

2b/yes

46/M

T2b/N2

10

No

27c/no

14/M

T2b/N1

Pancytopenia

3b/yes

Age/gender

Gender; F: Female, M: Male. Follow-up: Months.

a They abandoned therapy after two months.
b Local response to chemotherapy was not found in these patients.
c Bone and liver metastasis was seen in the second month and local progression was in the 8th month.

Table (5): Prognostic findings of cure-number in the chemo-radiotherapy group.

Survivalsa

p valuea

Four cures (%)b

1-3 cures (%)b

Disease-free survival

0.191

445

4510

Disease-specific survival

0.502

784

848

Overall survival

0.634

745

848

Recurrence-free survival

0.554

755

6910

Metastasis-free survival

0.190

585

7710

a Univariate Kaplan-Meier survival analysis were performed with log-rank test.

b Five-year survival rates in two groups. Four cures in 142 and 1-3 cures in 33 patients.
Five patients had one cure, eleven patients two cures and seventeen patients three cures.

Nasopharyngeal Carcinomas

235

Table (6): Serious and/or fatal complications.

Age/gender

Etiology

34/F

Chemotherapy

Cures/total dose

Complication due to therapy

Fatal complication

Massive hemorrhage

Yes
Yes

14/M

Chemotherapy

Pancytopeniaa

80/M

Radiotherapy

70 Gy

Nutrient deficiency

Yes

48/F

Radiotherapy

42 Gy

Nutrient deficiency

Yes

37/M

Radiotherapy

70 Gy

Carotid artery ruptureb

No
No

47/M

Radiotherapy

70 Gy

Radio-necrosisc

47/M

Radiotherapy

72 Gy

Radio-necrosisd

No

14/M

Radiotherapy

68 Gy

Severe larynx edema

No

Gender; F: Female, M: Male.

a Pancytopenia, erythema gangrenosum and fungal infections of lung led to death.
b Patient with a tumor invading the right cavernous sinus, treated with embolization.
c Bilateral temporal and right parietal lobe radio-necrosis seen 43 months after radiotherapy.
d Right temporal lobe necrosis seen 35 months after radiotherapy.

DISCUSSION
The incidence of nasopharyngeal carcinoma
is 0.35 per 100,000 populations in Turkey [5].
The prognostic value of the tumor type is not
definitive; some series reported that type 2 and
3 diseases had better prognosis than type 1 [1],
but the others reported that histopathology did
not have for response and survival in their series
[5]. In our series, tumor type was found predictive in progression and locoregional recurrence
at which type 1 had the worst prognosis.
Patients under 40 years of age had a better
prognosis for overall survival in some series
[2]; we observed the same finding for diseasefree and recurrence-free survivals. Female patients had better prognosis on disease-free survival in Erkal et al.s report [5]; likewise, this
was the case for disease-free and metastasisfree survivals in our series.
The nasopharynx has a rich lymphatic network and approximately 90% of patients develop lymphadenopathy in their life-span. We
detected 88.4% of patients with cervical lymph
node involvement, of which 42.9% was unilateral. High-grade tumors with large and/or multiple bilateral and/or lower neck lymphadenopathy are associated with high incidence (5070%) of distant metastases [3]. T-stage and Nstage usually determine the natural history for
nasopharyngeal carcinomas [5]. The multifarious
extensions of nasopharyngeal carcinoma and
the proximity to organs whose functions must
be preserved render the radiotherapy technique

quite cumbersome, demanding an absolute individualization to achieve high local control

rates and to avoid severe late sequelae [3].
CT and MRI are the methods that can give
a reliable image of the nasopharyngeal cancer
extensions and thus guide correctly the radiotherapy planning [3]. Our local tumor response
rate was found to be 88.9%, although all nasopharyngeal carcinomas were treated with 2D radiotherapy technique in this period. It is
well-known that node positive nasopharyngeal
carcinomas are prone to develop distant metastasis [7]. N-stage was predictive in overall,
disease-specific and disease-free survivals in
the current series.
T-stage predicts local response and survival
Local recurrence for patients with skullbase invasion ranges from 45% to 88% [6]. In
our series, nasopharyngeal carcinomas with
bone/sinus involvement were 41 cases, of which
a significant number (10 patients) had recurrences.
[5] .

In our series, prevertebral involvement had

no predictive value on survival, although it was
an independent predictor in Feng et al.s series
[9]. Prevertebral involvement was evaluated in
only 69 patients with nasopharynx MRI. The
result might have been changed as a predictor
factor for survival if MRI had been performed
in all the patients.
Tumor control in nasopharyngeal carcinoma
has been directly correlated with the dose of

236

radiation delivered to the tumor [1]. If we could

deliver more than 70Gy without giving doses
to the critical structures, we would get better
tumor control rates and survival. With modern
radiotherapy e.g. IMRT, high radiotherapy dose
to the target volume can be given with minimal
doses to the organs at risk.
Although primary therapy for nasopharyngeal carcinoma is radiation, over the past several
decades the role of systemic therapy has been
investigated. Currently, concurrent chemoradiotherapy has been accepted as a standard
treatment. The most important data come from
Intergroup study 0099 [1,2,5]. We administered
chemotherapy as a neoadjuvant and adjuvant
setting instead of concurrent chemoradiotherapy. There was no survival difference between
the radiotherapy group and the chemoradiotherapy group in our multivariate analysis.
Also, the number of chemotherapy courses
in the chemo-radiotherapy group was not a
prognostic factor on survival in our series.
Recently, we have administered 25mg cisplatin/
m 2 /week, with a total of seven times during
radiotherapy.
Serious complications were 3.1% with 1.5%
fatality in the series. Temporal lobe necrosis is
a well-recognized complication of radiation
therapy for nasopharyngeal carcinoma [8]. The
cumulative incidence is 3% and the latent interval ranges from 1.5 to 13 years (median, 5
years) [8]. We encountered this complication in
two patients (0.8%) 43 and 35 months after
radiotherapy (70Gy), respectively.
In conclusion, radiotherapy improved survival but chemotherapy as neoadjuvant and
adjuvant setting had no further effect to the
radiotherapy. Concurrent chemo-radiotherapy

Bilgin K. Aribas, et al.

could increase survival rates. In our series, Nstage and response were found the most important independent predictors on survival. Age,
gender, type, therapy and bone/sinus involvement were predictive parameters, as well.
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