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ORIGINAL RESEARCH
Sonography for Diagnosis of Benign
and Malignant Tumors of the Nose
and Paranasal Sinuses
Jun-jie Liu, MD, Yong Gao, MD, Ya-Fei Wu, MS, Shang-Yong Zhu, MD
Objectives—The purpose of this study was to demonstrate the reliability of sonography
for diagnosis of nose and paranasal sinus tumors.
Methods—Ninety-six consecutive patients with tumors underwent sonography and
computed tomography (CT) before surgical treatment. Tumor detectability and imaging
findings were evaluated independently and then compared with pathologic findings.
Results—Of 96 tumors, 75 were detected by sonography, for a detectability rate of 78.1%;
93 tumors were detected by CT, for a detectability rate of 96.9%. By comparison, sonography showed a trend toward higher detectability of nasal vestibular tumors than CT
(87.5% for sonography versus 50.0% for CT) and small lumps on the wing of the nose
(78.8% for sonography versus 33.3% for CT). Among the sonographic features,
boundary, shape, internal echo, calcification, bone invasion, vascular pattern, and
cervical lymph node metastasis all had significantly positive correlations with malignancy (P < .05), but size did not (P = .324). In addition, the vascular resistive index for
malignant tumors was significantly higher (mean ± SD, 0.66 ± 0.20) than the index
for benign lesions (0.24 ± 0.30; P < .001). Moreover, the detection rate for grade 1–3
(small–large) blood flow in benign lesions was only 43.8%, whereas the rate for malignant tumors was 97.7% (P < .001).
Conclusions—The vascular pattern may be a promising predictive indicator for distinguishing benign and malignant tumors of the nose and paranasal sinuses. Consequently,
sonography has high value for diagnosis of benign and malignant tumors of the nose
and paranasal sinuses, especially for nasal vestibular tumors and small lumps on the wing
of the nose.
Received November 11, 2013, from the Department
of Diagnostic Ultrasound, First Affiliated Hospital
of Guangxi Medical University, Nanning,
Guangxi, China. Revision requested January 3,
2014. Revised manuscript accepted for publication
January 29, 2014.
This study was supported by the Natural
Science Foundation of Guangxi Province, China
(grant 0832125).
Address correspondence to Shang-Yong
Zhu, MD, Department of Diagnostic Ultrasound,
First Affiliated Hospital of Guangxi Medical
University, 22 Shuang-Yong Rd, 530021
Nanning, Guangxi, China.
E-mail: [email protected]
Abbreviations
CT, computed tomography
Key Words—benign and malignant tumors; computed tomography; nose and paranasal
sinuses; sonography
T
umors of the nose and paranasal sinuses, which arise from
the head and neck, have complex anatomy and proximity
to the eye, brain, and cranial nerves. Nowadays, computed
tomography (CT), as one of the modern imaging techniques, has
been accepted as the reference standard for pathologic anatomic
evaluation and is considered an obligatory part of surgical planning
for the nose and paranasal sinuses.1,2 Some studies have demonstrated that sonography is a very useful method for differential diagnosis of head and neck tumors3–5 and the cervical lymph nodes6–8
and is even regarded as the preferred imaging method routinely used
to detect cervical lymph node metastasis of head and neck tumors.9
Moreover, previous studies have yielded promising results for
doi:10.7863/ultra.33.9.1627
©2014 by the American Institute of Ultrasound in Medicine | J Ultrasound Med 2014; 33:1627–1634 | 0278-4297 | www.aium.org
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Liu et al—Sonography for Diagnosis of Nose and Paranasal Sinus Tumors
sonography in the safe and noninvasive diagnosis of sinusitis and accurate evaluation of orbital and nasal fractures.10–14
However, it has rarely been used as an imaging technique
for investigation of nose and paranasal sinus tumors.
The purpose of our study was to evaluate the reliability of
sonography for diagnosis of benign and malignant tumors
of the nose and paranasal sinuses and to assess the concordance of sonography with CT, which is the current
clinical mainstay.
Materials and Methods
This study was performed with approval from the local
Institutional Review Board. Patients received verbal information about the study and gave informed consent to participate. From April 2011 to August 2012, consecutive
patients (58 male and 42 female; median age, 47.8 years;
range, 2–82 years) with tumors of the nose and paranasal
sinuses were enrolled randomly. Exclusion criteria were
patients who had clinically suspected tumors, had a surgical
history of nose and paranasal sinus tumors, or had undergone radiotherapy. Before surgery, all patients were investigated with sonography and CT within a time frame of 7 days.
The evaluators were blinded to the patients’ clinical information and the corresponding sonographic and CT findings,
and after comparison with postoperative histopathologic
results, the sonographic results were contrasted with CT results
to evaluate the possibility of sonography for diagnosis of
nose and paranasal sinus tumors.
Sonographic examinations were performed by 2 sonologists (J.L. and S.-Y.Z., with 11 and 24 years of experience
in head and neck sonography, respectively). Any discrepancies were resolved by consensus. Sonography was performed with a Technos MPX scanner (Esaote SpA, Genoa,
Italy) equipped with a 7.5–14.0-MHz linear transducer
(transducer body, 1.9 cm wide and 6.5 cm long; 1.2 cm wide
and 5.4 cm long where the surface of the transducer contacted the skin) and a 3.5–5.0-MHz convex array transducer
or an EUB-6500 scanner (Hitachi Medical Corporation,
Tokyo, Japan) equipped with a 7.5–14.0-MHz linear transducer (dimensions as above) and a 3.5–5.0-MHz convex
array transducer. All patients were in the supine position.
The scan region was from the middle to anterolateral aspects
of the face and from the upper frontal to alveolar margins,
including surrounding structures. The examination was
performed in transverse, oblique, and longitudinal planes
(Figure 1). The frontal sinus, lower orbital border, ethmoidal
sinus, nose, maxillary sinus, alveolar margin, and external
cheekbone were delineated.
The following sonographic features were assessed:
tumor detectability, site, size, shape, internal echo, calcification, bone invasion, vascular pattern, and cervical lymph
node metastasis. The size was defined as the maximum
length of the tumor in centimeters. A normal image was
defined as showing an acoustic shadow arising from the
bone wall (Figure 2A, left); a pathologic image was defined
as visualization of a hypoechoic nose and sinus cavity delineated by surrounding air (Figure 2A, right). Infiltration of
the surrounding structures indicated a hypoechoic tumor
spreading into the soft tissues of the face (Figure 2B). Bone
invasion was defined as interruption of the inner and outer
membranes, which normally appeared as hyperechoic lines
(Figure 2C). We classified the vascular patterns of the
tumors into 4 grades: grade 0, no blood flow signal inside
the tumor; grade 1, a small amount of blood flow, with 1 or
2 pointed or fine rodlike blood vessels visible inside the
tumor; grade 2, a moderate amount of blood flow, with 3
or 4 visible spotlike blood vessels or a long vessel across the
lesion with a length close to or longer than the tumor radius;
and grade 3, a larger amount of blood flow, with 5 or more
visible spotlike blood vessels or 2 long vessels across the
lesion (Figure 2D).
Figure 1. Probe locations in the transverse (left), oblique (center), and longitudinal (right) planes during the examination of the anterior paranasal
regions.
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Liu et al—Sonography for Diagnosis of Nose and Paranasal Sinus Tumors
For comparison, CT images were obtained with a
Somatom Sensation 16 CT system (Siemens AG,
Erlangen, Germany). The patients were imaged in the
supine position and were asked to breathe quietly and avoid
swallowing during scanning. The section thickness was 5
mm, with a 5-mm intersection gap. Axial, coronal, and sagittal planes were obtained. Contrast material was not used
routinely in this study because of the economic burden on
the patients. A pathologic image was defined as abnormal
increased density resembling soft tissues on low-density
images of the nasal cavity and paranasal sinuses (Figure 2E).
Infiltration of the surrounding structures indicated a highdensity tumor spreading into the adjacent soft tissues of the
face. Bone invasion was defined as intermediate soft tissue
density on normal bone images. These imaging interpretations were compared with postoperative histopathologic
results.
The SPSS version 13.0 statistical software package
(IBM Corporation, Armonk, NY) was used in this study.
The tumor detectability accuracy of sonography and CT
were calculated and compared by the Pearson χ2 test.
Differences in major clinical and sonographic features
between detectable benign and malignant tumors were
determined by an independent samples t test, Pearson χ2,
Fisher exact test, and Mann-Whitney U test. Statistical significance was set at P < .05.
Results
In this study, we investigated 100 patients with tumors of
the nose and paranasal sinuses. However, 4 patients left the
hospital or were transferred without pathologic results.
Therefore, the study included 96 tumors with pathologic
results. The pathologic diagnoses of the 96 complex tumors
Figure 2. Squamous cell carcinoma of the right ethmoid sinus in an 81-year-old woman. A, Oblique sonograms showing a normal acoustic shadow
(arrow) behind the bone wall in the left image and a hypoechoic tumor and many calcifications (arrow) in the right image. B, Longitudinal sonogram
of the right ethmoid sinus (E) at the eye level was showing the tumor (T; arrow) extending to the right eye. C, Transverse sonogram showing obvious bony invasion of the sinus wall (arrow). D, Sonogram clearly showing a rich vascular pattern (grade 3 blood flow) in the tumor (arrow). E, Computed tomogram showing the tumor arising from the right ethmoid sinus with intermediate to high density (long arrow) and extending to the right
eye (short arrows), corresponding to the sonographic findings.
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are shown in Table 1. Cysts (37.5% [18 of 48 patients])
and inflammatory polyps (35.4% [17 of 48 patients]) were
most common in the benign group; squamous cell carcinoma
(27.1% [13 of 48 patients]) was most common in the
malignant group.
Of the 96 tumors, 75 were detected by sonography,
for a detectability rate of 78.1%; 93 tumors were detected
by CT, for a detectability rate of 96.9% (including misdiagnosed cases). The accuracy of sonographic and CT detection compared with the pathologic results is summarized in
Table 2 (excluding misdiagnosed cases). There was no significant difference between the tumor detectability of
sonography and CT (P = .388).
For the 75 detectable tumors (21 benign and 43
malignant) on sonography, the major clinical and sonographic features are displayed in Table 3. In terms of the
major clinical features, age (P = .393) and sex (P = .665)
were not associated with benignity or malignancy. In terms
of the sonographic features, boundary (P < .001), shape
(P <.001), internal echo (P < .001), calcification (P = .003),
bone invasion (P < .001), vascular pattern (P < .001), and
cervical lymph node metastasis (P = .018) had significantly
positive correlations with malignancy, but size did not (P
Table 1. Pathologic Diagnoses of the 96 Tumors of the Nose and
Paranasal Sinuses
Diagnosis
n
Benign
Cyst
Inflammatory polyp
Aspergillosis
Papillary tumor
Angiofibroma
Sexually transmitted odontogenic myxoma
Fibroangioma
Hair vascular wall tumor
Ossifying fibroma
Malignant
Squamous cell carcinoma
Basal cell carcinoma
Natural killer/T-cell lymphoma
Sarcoma
Olfactory neuroblastoma
Malignant melanoma
Poorly differentiated adenocarcinoma
Diffuse large B-cell lymphoma
Adenoid cystic carcinoma
Vesicular nuclear cell carcinoma
Small cell malignant tumor
Neuroendocrine carcinoma
Mucinous chondrosarcoma
Lymphoepithelial carcinoma
Meningeal encephalocele
Metastatic thyroid papillary carcinoma
48
18
17
4
4
1
1
1
1
1
48
13
6
5
5
3
3
2
2
2
1
1
1
1
1
1
1
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= .324). In addition, the vascular resistive index for malignant tumors was significantly higher (mean ± SD, 0.66 ±
0.20) than the index for benign lesions (0.24 ± 0.30; P <
.001). Moreover, the detection rate for grade 1–3 blood
flow in benign lesions was only 43.8%, whereas the rate for
malignant tumors was 97.7% (P < .001).
Discussion
The bone and the air contained in the nasal cavity and
paranasal sinuses appear to be the main limitations of
sonography in these locations. However, previous evidence
has shown that sonography is capable of depicting normality, and its use has been proposed for first-line diagnosis of radiologic maxillary sinusitis.10,14,15 In our research,
we found during a training dissection that there were several cartilages on the wing of the nose (Figure 3), and the
bone thickness of the maxillary and frontal sinuses was
thin,16 which indicated that sonography may depict images
like those of other organs. Lichtenstein et al10 reported that
a 2.5- to 5-MHz range was adequate to pass through the
bone. Moreover, when a lesion was present, the surrounding air and bone in the nasal cavity and paranasal sinuses
improved the contrast of the hypoechoic tumor intensely.
These findings were helpful for clearly delineating the
boundaries of the tumors. In our study, the whole detectability rate of sonography was 78.1%.
The sonographic findings of the benign and malignant
tumors showed differences on grayscale images. From our
results, the boundary, shape, internal echo, calcification,
and bone invasion had all significantly positive correlations
with malignancy. In general, benign tumors displayed a
clear boundary, a round or oval shape, and homogeneity
(Figure 4A), whereas malignant tumors displayed an unclear
boundary, an irregular shape, heterogeneity, calcification,
and bone invasion (Figures 2A, right, and 5A, right).
Furthermore, sonography could also display the vascular
pattern clearly in color Doppler flow images. In our study,
malignant tumors had much richer blood flow (Figures 2D
and 5B) and a higher resistive index (Figure 5C) than
benign tumors (Figure 4B), and the detection rate for
grade 1–3 blood flow in benign tumors was only 43.8% (14
of 32), whereas the rate for malignant tumors was 97.7%
(42 of 43), which was highly significant. Some studies
found that tumor angiogenesis plays an important role in
the pathogenesis of tumor growth and metastases in many
organs.17–20 Therefore, the vascular pattern may be a promising predictive indicator for distinguishing benign and
malignant tumors of the nose and paranasal sinuses.
In addition, it is quite important for us to assess the vascu-
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Liu et al—Sonography for Diagnosis of Nose and Paranasal Sinus Tumors
lar pattern in tumors, which would affect possible blood
loss and the need for transfusions during future surgery.21–23
The results of our study also show that it is very important
to determine cervical lymph node metastasis, which existed
only in the malignant group. Many studies have indicated
that sonography shows high accuracy in differentiating
metastatic from benign nodes.6–8 Therefore, when tumors
of the nose and paranasal sinuses have cervical lymph node
metastasis, they have a much higher possibility of being
malignant.
When the accuracy of sonographic and CT detection
were compared with pathologic results, sonography
showed a trend toward higher detectability than CT in nasal
vestibular tumors (87.5% [7 of 8 patients] for sonography
versus 50.0% [3 of 6 patients] for CT) and small lumps on
the wing of the nose (78.8% [7 of 9 patients] for sonography versus 33.3% [3 of 9 patients] for CT). One case of a
nasal vestibular cyst and 1 case of a tumor on the wing of
the nose were not detected on CT; the tumor sizes were
0.4 and 0.8 cm, respectively. We assumed that these findings
might have been related to the CT scanning slices. It made
sense that sonography would be the better initial choice
than CT for nasal vestibular tumors and small lumps on
the wing of the nose.
Table 2. Accuracy of Sonography and CT for Detection of the 96 Tumors of the Nose and Paranasal Sinuses
Pathologic Examination
Subsite
Benign
Nasal cavity
14
Inflammatory polyp (9)
Papillary tumor (3)
Hair vascular wall tumor (1)
Fibroangioma (1)
Nasal vestibule
7
Cyst (6)
Inflammatory polyp (1)
2
Cyst (1)
Inflammatory polyp (1)
12
Cyst (5)
Inflammatory polyp (3)
Sexually transmitted
odontogenic myxoma (1)
Papillary tumor (1)
Aspergillosis (2)
Nose wing
Maxillary sinus
Ethmoidal sinus
6
Inflammatory polyp (3)
Cyst (2)
Angiofibroma (1)
Frontal sinus
2
Cyst (2)
Sphenoid sinus
Total
5
Cyst (2)
Aspergillosis (2)
Ossifying fibroma (1)
48
Malignant
Sonography
CT
Benign
Malignant
Benign Malignant
13
Squamous cell carcinoma (5)
Natural killer/T-cell lymphoma (4)
Malignant melanoma (2)
Sarcoma (1)
Meningeal encephalocele (1)
1
Small cell malignant tumor (1)
6 (42.9)
11 (84.6)
9 (64.3)
8 (61.5)
6 (85.7)
1 (100)
3 (42.9)
0
7
Basal cell carcinoma (6)
Squamous cell carcinoma (1)
18
Squamous cell carcinoma (4)
Adenoid cystic carcinoma (2)
1 (50.0)
6 (85.7)
1 (50.0)
2 (28.6)
8 (66.7)
16 (88.9)
9 (75.0)
17 (94.4)
5 (83.3)
5 (83.3)
4 (66.7)
0
1 (50.0)
1 (100)
0
2 (40.0)
1 (50.0)
39
30
33
Sarcoma (3)
Poorly differentiated adenocarcinoma (1)
Olfactory neuroblastoma (1)
Diffuse large B-cell lymphoma (2)
Natural killer/T-cell lymphoma (1)
Vesicular nuclear cell carcinoma (1)
Lymphoepithelial carcinoma (1)
Metastatic thyroid papillary carcinoma (1)
Mucinous chondrosarcoma (1)
6
4 (66.7)
Squamous cell carcinoma (2)
Neuroendocrine carcinoma (1)
Olfactory neuroblastoma (1)
Poorly differentiated adenocarcinoma (1)
Sarcoma (1)
1
2 (100)
Malignant melanoma (1)
2
0
Squamous cell carcinoma (1)
Olfactory neuroblastoma (1)
48
27
Values in parentheses are numbers of patients and percentages where applicable.
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To our knowledge, sonography has well recognized
advantages over CT, which include the obvious absence
of ionizing radiation, which makes it safe to use during
pregnancy and in children and to repeat examinations.
Moreover, radiologic examinations are time-consuming
procedures that include consultation with another
department, especially for patients in intensive care units.
Real-time sonography performed at the bedside can minimize the diagnostic time and referral of critically ill patients
for CT.10,24,25 Consequently, portable real-time sonography is easy to perform at the bedside and could be proposed as the first-line imaging modality in pregnancy and
children, follow-up examinations, and critically ill patients
for diagnosis of nose and paranasal lesions.
Excluding the 21 undetectable deep tumors, 10 of 75
detectable tumors were diagnosed incorrectly, including
1 nasal vestibular cyst, 1 squamous cell carcinoma and 1 papillary tumor in the nasal cavity, 1 basal cell carcinoma and 1
Table 3. Comparison of Major Clinical and Sonographic Features of the 75 Tumors of the Nose and Paranasal Sinuses Detected by Sonography
Final Pathologic Diagnosis
Feature
Clinical
Age, y
Sex
Sonographic
Size, cm
Boundary
Shape
Internal echo
Calcification
Bone invasion
Cervical lymph node metastasis
Vascularity
0
1
2
3
Resistive index
Benign
Malignant
P
45.3 ± 21.5
15 (female)
17 (male)
49.4 ± 19.3
18 (female)
25 (male)
.393a
.665b
2.8 ± 1.3
24 (clear)
18 (regular)
19 (homogeneous)
4 (existent)
5 (existent)
0 (existent)
3.1 ± 1.5
8 (clear)
4 (regular)
6 (homogeneous)
19 (existent)
38 (existent)
7 (existent)
8 (unclear)
14 (irregular)
13 (heterogeneous)
28 (nonexistent)
27 (nonexistent)
32 (nonexistent)
18
12
2
0
0.24 ± 0.30
35 (unclear)
39 (irregular)
37 (heterogeneous)
24 (nonexistent)
5 (nonexistent)
36 (nonexistent)
.324a
<.001b
<.001b
<.001b
.003b
<.001b
.018c
<.001d
1
15
15
12
0.66 ± 0.20
<.001a
Data are presented as mean ± SD where applicable.
aIndependent-samples t test.
bPearson χ2 test.
cFisher exact test.
dMann-Whitney U test.
Figure 3. Oblique image of the wing of the nose acquired during a training anatomic dissection showing several cartilages (arrows).
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Figure 4. Nasal vestibular cyst on the wing of the nose in a 45-year-old
woman. A, Oblique grayscale sonogram showing the cyst, which
resembles a cyst in other organs of the body. B, Color Doppler flow
image clearly showing no vascular pattern (grade 0 blood flow).
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inflammatory polyp on the wing of the nose, 1 olfactory neuroblastoma and 1 cyst in the maxillary sinus, 1 malignant
Figure 5. Basal cell carcinoma on the left wing of the nose in an 82-year-old
man. A, Oblique sonogram showing a normal acoustic shadow behind the
wing of the nose (arrow) in the left image and a hypoechoic tumor and bony
invasion (arrow) in the right image. M indicates mass. B, Sonogram clearly
showing a slightly rich vascular pattern (grade 2 blood flow) in the tumor
(arrow). C, Sonogram showing a high vascular resistive index (0.89).
melanoma in the frontal sinus, and 2 inflammatory polyps
in the ethmoidal sinus. We found that benign lesions could
also show features of malignant tumors, such as an unclear
boundary, an irregular shape, heterogeneity, calcification,
and bone invasion, as described above, which may involve
inflammatory heterogeneity or calcification and bone
interruption caused by long-time tumor absorption. Conversely, early-stage malignant lesions may show benign features as well.
There are limitations of the use of sonography for
imaging the nose and paranasal sinuses. The ultrasonic
acoustic barrier leads to nonvisualization of some deep
anatomic structures, and bony details, such as the sphenoid
sinus and posterior ethmoid sinus, cannot be distinguished.
However, the purpose of this study was only to evaluate the
reliability of sonography for diagnosis of benign and malignant tumors of the nose and paranasal sinuses. This study
provides initial data to support further studies. Additionally,
the imaging interpretations were performed by consensus
instead of by independent readings, which may have led to
a potential bias in the results.
In conclusion, sonography has high value for diagnosis
of benign and malignant tumors of the nose and paranasal
sinuses, especially for nasal vestibular tumors and small
lumps on the wing of the nose.
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