AJR 2000; 175:1357-1360
© American Roentgen Ray Society
Identification of Feeding Arteries to Establish the Intra- or Extraparotid Location of Jugulodigastric Nodules
Value of Color Doppler Sonography
Carlo Martinoli1,
Francesco Giovagnorio2,
Fabio Pretolesi1 and
Lorenzo E. Derchi1
1
Cattedra "R" di Radiologia, DICMI,
Università di Genova, Largo Rosanna Benzi 8,
1-16132 Genova, Italy.
2
Cattedra di Radiologia, Università "La
Sapienza," Policlinico Umberto I. Viale Regina Elena 324, 1-00161 Roma,
Italy.
Received January 5, 2000;
accepted after revision May 2, 2000.
Address correspondence to C. Martinoli.
Abstract
OBJECTIVE. The objective of our study was to determine the value of
color Doppler imaging as an adjunct to gray-scale sonography to reveal the
intra- or extraparotid origin of jugulodigastric nodules of uncertain
location.
SUBJECTS AND METHODS. Forty nodules in the jugulodigastric area from
38 patients were imaged with gray-scale, color, and power Doppler sonography.
Nodules receiving vessels from salivary glands were assumed to be
intraglandular; those accepting vessels from paraparotid spaces were
considered to arise from outside the gland. Imaging results were correlated
with biopsy and surgical findings.
RESULTS. In 38 of 40 cases, color and power Doppler sonography
displayed discrete feeding arteries leading to the nodules: 25 nodules had one
supplying artery, nine received two arteries, and four had three or more
arteries. Intraparotid nodules received vessels from the gland in 20 cases. In
two cases, the source of vessels was indeterminate. In two malignant tumors,
multiple arteries derived from both the parotid and the neck spaces. All 14
extraparotid nodules received the arterial supply from paraparotid spaces.
Color Doppler sonography enabled prediction of the intraglandular location of
the nodules in 91% of cases and the extraglandular location in 87.5% of cases.
The correct diagnosis was achieved in 34 of 40 nodules, with a global accuracy
of 85%.
CONCLUSION. Color Doppler sonography can help to assess the intra-
or extraparotid location of jugulodigastric nodules. In practice, this
technique can support the diagnosis when gray-scale sonography raises doubts
about the origin of a jugulodigastric nodule.
Introduction
Sonography has an established role in the diagnostic assessment of neck
masses, and color and power Doppler techniques are currently used to better
reveal the vascular invasion and to categorize the tumors according to
histopathology on the basis of grade and pattern distribution of the
intratumor neovasculature
[1,2,3,4].
One of the problems with diagnostic sonography remains the assessment of
nodules located in the jugulodigastric area, close to the parotid and the
submandibular glands. Most have a similar hypoechoic appearance, and, in some
cases, it can be difficult to predict confidently whether they originate from
the salivary glands or derive from the immediate lateral neck spaces
[5]. Although CT and MR imaging
of the neck are valuable for the assessment of the tumor extent and the
relationship with adjacent structures, the contribution of these techniques is
often inadequate for this purpose
[6].
We theorized that the feeding arteries might prove helpful for establishing
the intra- or extraglandular origin of the nodules located at the boundaries
of the parotid and submandibular glands. Accordingly, an attempt has been made
in this study to determine the value of color Doppler sonography in revealing
the intra- or extraparotid nature of jugulodigastric nodules of uncertain
origin, on the basis of the source of their feeding arteries.
Subjects and Methods
From December 1997 through October 1999, we prospectively examined 38
consecutive patients (20 men and 18 women; age range, 26-86; mean, 61.4
± 16 years) with a total of 40 neck nodules located in the
jugulodigastric area. Patients were referred to our departments for imaging
evaluation of a palpable mass. The criterion for inclusion in the study group
was detection of a discrete nodule located at the boundaries of the parotid
and submandibular glands that was difficult to categorize as an intra- or
extraparotid tumor on gray-scale sonography. With the exception of para- and
intraparotid lymph nodes presenting with typical echotexture (central
echogenic hilum and peripheral hypoechoic cortex)
[7], all neck masses, from
purely cystic to solid, were included in the study regardless of appearance on
gray-scale sonography. In all cases, sonography was the first imaging
procedure for evaluation of the palpable nodule.
Sonographic and Doppler studies were conducted with two different scanners
(HDI-3000, Advanced Technology Laboratories, Bothwell, WA; or Au5, EsaOte
Biomedica, Genoa, Italy) equipped with broadband (10-5, 7.5-10, and 10-13 MHz)
linear array transducers, operating at 5-6 MHz for Doppler imaging. Color
Doppler settings were chosen to maximize low-volume flow sensitivity: the
pulse repetition frequency used was 1 kHz, and the band-pass filter was set at
50 Hz. To increase depiction of vessel continuity, the power mode was also
used, with the same pulse repetition frequency of 1 kHz as used in color
Doppler sonography. No attempt was made to compare the efficacy of power
Doppler sonography with that of color Doppler sonography. Examinations were
performed with the patient supine, keeping the neck hyperextended. The region
of interest was scanned from the retromandibular approach, dorsal to the ramus
of mandible, with minimum probe pressure because even slight compression with
the transducer could obliterate color signals in the thin vessels leading to
the nodule (presumably because of a low blood perfusion pressure). When a
supplying vessel was identified, scanning was oriented along the best plane to
elongate and optimally display it.
Doppler imaging evaluation was essentially based on the assessment of the
source of the arteries directed to the nodule. Specifically, if a nodule close
to the border of the parotid or submandibular glands received the arterial
supply from inside the gland, we assumed that it had an intraglandular
location (Fig. 1). If the
nodule accepted vessels from the extraparotid neck spaces, it was considered
extraglandular (Fig. 2). When a
nodule showed more than one feeding artery, the overall number and source of
them was recorded. Spectral Doppler analysis was used to confirm the presence
of arterial flow in the vessels leading to the nodule. No attempt was made in
this study either to evaluate the grade and pattern distribution of intratumor
vasculature or to correlate it with the respective histopathologic findings.
In all cases, notation was made of the largest diameter, echotexture (solid
versus cystic versus mixed), and border (sharp versus unsharp) of the
nodule.
Sonographic studies were performed by two radiologists who worked
independently and collected and analyzed the data for the purpose of this
study before reviewing the clinical histories of the patients. The same
radiologists reviewed the patients' files and dictated the official report of
the study. The histopathologic diagnosis was made by means of examination of
biopsy specimens obtained with either operative excision (29/40 cases) or
fine-needle aspiration biopsy (11/40 cases) under sonographic guidance. The
decision to perform a biopsy or to excise a nodule was made by the referring
physician on the basis of all clinical and imaging data. At the time of
excision, the surgeon was always asked to grossly determine the intra- or
extraparotid location of the lesion. In each case, the initial sonographic
interpretation was compared with the final histopathologic interpretation with
regard to location of the nodule.
Results
Of the 40 jugulodigastric nodules, histopathologic examination yielded 15
benign (8 pleomorphic adenomas, 6 Warthin's tumors, and 1 benign
lymphoepithelial cyst) and seven malignant (1 mucoepidermoid carcinoma, 2
acinic cell carcinoma, 2 undifferentiated carcinoma, and 2 adenocarcinoma)
salivary gland tumors, fifteen lymphadenopathies (7 reactive, 3 non-Hodgkin's
lymphomas, 5 metastatic from 3 squamous cell carcinoma, 1 papillary carcinoma
of the thyroid, and 1 nasopharyngeal carcinoma), one branchial cyst, and two
lipomas. The maximum size of the nodules on sonography ranged from 5 to 51 mm
(mean, 24.3 ± 11.7 mm). On gray-scale sonography, the nodules presented
as hypoechoic masses of various shape and echogenicity, including solid (85%),
mixed (10%), and cystic (5%) appearance. Most were well-circumscribed nodules
with sharp margins; in six cases, all nodules were malignant tumors of the
parotid with irregular or ill-defined borders. The more common location of the
nodules was adjacent to the dorsal aspect of the parotid or just caudal to its
lower pole. Eight of the lymph nodes were associated with other nodal masses
located along the ipsilateral cervical space.
With the exception of two lipomas accounting for 5% of all lesions,
discrete feeding arteries could be detected in the other 38 cases on color and
power Doppler sonography. Of these nodules, 25 (62.5%) displayed one supplying
artery, nine (22.5%) received two arteries, and four (10%) had three or more
arteries. No correlation was found between tumor size and detectable
vascularity, but all nodules that received three or more feeding arteries were
malignant. Overall, an exclusive arterial supply was observed from the parotid
gland in 19 cases (47.5%), from the submandibular gland in one case (2.5%),
and from the extraparotid spaces in the other 14 cases (35%) (Figs.
3 and
4). In two advanced cases (5%)
of undifferentiated carcinoma and adenocarcinoma with signs of extraparotid
invasion, the neoplasm received distinct arterial supply from the gland and
the paraparotid spaces, so we could not categorize it as intra- or
extraparotid. Also, color Doppler sonography findings were not convincing in
two nodes (5%) because the feeding artery twisted and turned for a long tract
close to the borders of the gland before reaching the nodule. A careful
scanning technique was generally required to appreciate these vessels,
especially with regard to their frequent tortuosity and tendency to redirect
their course while approaching the nodule.
View larger version (134K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 3. —69-year-old man with solid hypoechoic nodule (N) close to
lower pole of left parotid gland (P). Color Doppler sonogram shows single
arterial supply (arrow) leading to nodule from inside gland. Cytology
(not shown) revealed pleomorphic adenoma.
|
|
View larger version (106K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 4. —45-year-old woman with solid hypoechoic nodule (N) close to
left parotid gland, somewhat similar to nodule described in
Figure 3. Color Doppler
sonogram shows nodule receiving vessels (arrow) from extraparotid
spaces. Diagnosis was reactive lymph node. Asterisk = external carotid artery,
P = parotid gland.
|
|
Most of the extraparotid feeding arteries were enveloped by fat and reached
the nodule from depth to surface following different paths; in three cases, a
direct origin of these vessels from the external carotid artery was
documented. On the contrary, the intraparotid branches tended to reach the
nodule crossing the superficial lobe of the gland in a cranial caudal
direction and from an anterior to a posterior direction. Each artery could
variably be associated with one or more efferent veins; in some extraparotid
tumors, the venous routes had an independent course with respect to the
arteries and were seen to drain directly into the retromandibular vein or into
the external jugular vein. The neoplastic thrombosis of a small efferent vein
was observed in one mucoepidermoid carcinoma.
All jugulodigastric nodules that accepted exclusive blood supply from the
parotid or the submandibular gland were salivary gland tumors, including 15
benign and five malignant histotypes (Fig.
5A,5B,5C).
On the contrary, cases showing selective blood supply from the lateral neck
spaces were extraparotid masses, including 13 enlarged cervical nodes and one
branchial cyst. By relying solely on this method, we predicted the
intraglandular location of the nodules in 20 (91%) of 22 cases and the
extraglandular location in 14 (87.5%) of 16 cases
(Table 1). Overall, the correct
diagnosis was achieved in 34 of 40 nodules, with a global accuracy of 85%.
View larger version (135K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 5B. —43-year-old woman with 5-mm cystic nodule in jugulodigastric
area. Color Doppler (B) and power Doppler (C) sonograms show
discrete feeding artery (arrow) proceeding toward nodule from inside
submandibular gland. Needle aspirate (not shown) revealed Warthin's tumor.
|
|
View larger version (124K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 5C. —43-year-old woman with 5-mm cystic nodule in jugulodigastric
area. Color Doppler (B) and power Doppler (C) sonograms show
discrete feeding artery (arrow) proceeding toward nodule from inside
submandibular gland. Needle aspirate (not shown) revealed Warthin's tumor.
|
|
Discussion
Anatomic spaces located between the parotid and submandibular glands,
commonly referred to as jugulodigastric spaces, can be involved by neoplasms
of different origin; apart from salivary tumors, abnormally enlarged lymph
nodes are the most frequent ones
[8]. Soft-tissue tumors that
arise adjacent to the gland, such as lipomas, neurogenic tumors, or branchial
cysts, are rare. At times, these masses can displace the gland or invade it in
such a way that they mimic a salivary tumor. Similarly, an exophytic tumor
arising from the salivary glands can mimic an extraglandular mass or lymph
node on imaging studies.
Even with imaging studies, it has not always been possible to determine the
origin of a jugulodigastric mass. Diagnostic sonography is an effective
modality to define the size and structure of these masses. However, no
accurate criteria have been advocated for distinguishing a parotid tumor
bulging out of the parotid boundaries from an extrinsic lesion large enough to
seem continuous with the gland. Even using high-frequency transducers, this
differentiation may not be straightforward because the parotid has undefined
margins and the capsular level is not displayed on gray-scale sonography
[5]. On CT and MR imaging, an
intact fat plane between the mass and the gland has been described as strong
evidence that the mass arises outside the gland. However, if this plane is not
observed on every scan plane, it is not possible to determine the true
location of the mass [6]. The
relationship of the mass to the anterior facial vein has recently been
advocated as an additional landmark in predicting whether the mass arises from
or is adjacent to the submandibular gland on CT and MR imaging. Primary
disease of the gland is not separated from the gland by the vein; the facial
vein separates lymphadenopathy from the gland and, theoretically, separates
the gland from soft-tissue tumors lateral to the gland
[6]. This vein can readily be
identified on sonography, too. However, this landmark would be useful to
separate the mass solely from the submandibular gland, and not from the
parotid. In addition, the facial vein sweeps around the lateral aspect of the
submandibular gland, and a tumor medial to this gland will therefore not be
separated from the gland itself by the vein.
In the current study, we investigated the tumor vascularity with color
Doppler imaging in an attempt to predict more accurately the intraor
extraglandular origin of a jugulodigastric nodule according to the recognition
of the arteries from which it receives the blood supply. A similar approach
was described in another setting to localize abnormal parathyroid glands
before neck exploration by revealing their feeding arteries using color and
power Doppler sonography [9].
The method we used in this study was easy to apply. Color and power Doppler
imaging performance was excellent in giving significant information regarding
the position of origin of jugulodigastric lesions with respect to the salivary
glands. Findings were handy and reliable: all benign and most malignant
salivary tumors showed one or more feeding arteries derived from inside the
gland, as an expression of the primary vasculature that accompanies the tumor
during its growth, whereas all extraparotid masses received vessels
exclusively from extraparotid spaces.
In this latter location, the predominant type was enlarged lymph nodes that
simulated a solid tumor on gray-scale sonography because of an abnormal
appearance with absence of a central zone of hyperechogenicity. Lymph nodes
are not only resident elements of the paraparotid fat spaces but also elements
within the parotid as a result of the encapsulation of the lymphatic system in
the parotid anlagen during development
[10]. In our series, the
extraparotid site of the nodes was proven by surgical exploration in eight of
12 cases. The remaining four were reactive nodes on biopsy, and we could make
only a presumptive diagnosis of their extraparotid location. This is a
limitation of our study because the recognition of a node cannot be taken as
proof of its site. However, we considered unlikely that these nodes originated
from the parotid. Reactive enlargement of intraparotid nodes usually occurs as
part of an inflammatory disease affecting either the gland, such as acute
viral and bacterial sialadenitis and infectious granulomatous disease, or the
external ear and scalp [8].
These specific clinical contexts were not encountered in our cases. In fact,
lymphadenopathies were caused by acute odontogenic and upper respiratory tract
infections and occurred in the absence of any other focal or diffuse parotid
abnormality. In addition, other ipsilateral, cervical, and submandibular
lymphadenopathies coexisted in three of these cases.
The main drawbacks of this method include evaluation of avascular masses
and of nodules supplied by tortuous vessels that run close to the margin of
the gland. In these cases, a definitive diagnosis based on color Doppler
sonography can become difficult and time-consuming. Another intrinsic
limitation emerged, in our experience, from the examination of two locally
invasive parotid malignancies that parasitized blood vessels from the
paraparotid spaces. In advanced neoplasms that continuously incorporate into
themselves the vasculature of the host, irrespective of its source, it is
conceivable that additional routes from extraparotid spaces may participate in
the arterial supply to the mass. Conversely, it is also possible that
paraparotid malignancies invading the gland may accept blood supply from the
parotid vasculature; however, we did not encounter cases of this latter type.
Although the usefulness of this method is intrinsically limited here, we
believe that these equivocal cases have a low significance because evaluation
of advanced neoplasms with sonography is relatively uncommon in the
jugulodigastric region; CT and MR imaging are the preferred diagnostic
modalities for large lesions in this area
[8].
In this study, the efficacy of Doppler imaging was not compared with that
of CT and MR imaging with regard to location of the nodule. Although CT and MR
imaging can contribute substantially to the diagnosis of jugulodigastric
nodules, these modalities have been performed in only a limited number of
cases in our series (especially for evaluating the spread of neoplasms to deep
structures that sonography could not image effectively and for staging
purposes). Actually, most nodules in our series presented as relatively small
superficial masses that turned out to be lymph nodes or benign parotid tumors.
At our institution, sonography is used as the first imaging procedure for the
visualization of neck masses, and, at least in our experience, the diagnostic
assessment of superficial nodules was effectively carried out with this
modality only, without requiring further high-cost imaging studies. Color
Doppler imaging is then used as an adjunct to conventional gray-scale
sonography.
We believe that the main advantage of analysis of the feeding vessels to
the nodule is a reinforcement of the diagnostic impression in cases in which
some doubt of its origin may exist from the initial observation on gray-scale
sonography. The position of a nodule is an important component of the imaging
report because the list of possible lesions arising in the parotid is
different from the list for a lesion located in the paraparotid spaces.
Although the use of imaging-guided biopsies of parotid masses depends on the
surgical concepts of the referring head and neck surgeons, many surgeons
believe that any salivary gland mass should be removed, and thus the needle
diagnosis is immaterial to the surgical options
[8]. Therefore, more important
than giving a specific diagnosis, imaging has to provide accurate tumor
mapping. An earlier and more confident determination of the origin of the
nodule can benefit the clinician for surgical planning and preoperative
patient counseling. In fact, a false diagnosis of parotid mass (i.e., for a
reactive cervical node) may lead to an unnecessary operation. On the other
hand, the ministerpretation of a parotid tumor for a cervical node may cause
exposure of the patient to unnecessary risk because parotid tumor surgery
requires a surgeon skilled in facial nerve surgery.
In conclusion, the presented data suggest that color Doppler imaging should
be part of the sonographic examination of the jugulodigastric area when a
nodule of uncertain parotid origin is encountered on gray-scale sonography.
The assessment of the origin of the nodule may be most important when deciding
to perform percutaneous biopsies or in deciding to proceed with surgery.
References
-
Martinoli C, Derchi LE, Solbiati L, Rizzatto G, Silvestri E,
Giannoni M. Color Doppler sonography of salivary glands.
AJR
1994;163:933
-941[Abstract/Free Full Text]
-
Giovagnorio F, Caiazzo R, Avitto A. Evaluation of vascular patterns
of cervical lymph nodes with power Doppler sonography. J Clin
Ultrasound 1997;25:71
-76[Medline]
-
Tschammler A, Ott G, Schang T, Seelbach-Goebel B, Schwager K, Hahn
D. Lymphadenopathy: differentiation of benign from malignant disease: color
Doppler US assessment of intranodal angio-architecture.
Radiology
1998;208:117
-123[Abstract/Free Full Text]
-
Schick S, Steiner E, Gahleitner A, et al. Differentiation of benign
and malignant tumors of the parotid gland: value of pulsed Doppler and color
Doppler sonography. Eur Radiol
1998;8:1462
-1467[Medline]
-
Gritzmann N. Sonography of the salivary glands.
AJR
1989;153:161
-166[Abstract/Free Full Text]
-
Weissman JL, Carrau RL. Anterior facial vein and submandibular
gland together: predicting the histology of submandibular masses with CT or MR
imaging. Radiology
1998;208:441
-446[Abstract/Free Full Text]
-
Vassallo P, Wernecke K, Roos N, Peters PE. Differentiation of
benign from malignant superficial lymphadenopathy: the role of high-resolution
US. Radiology
1992;183:215
-220[Abstract/Free Full Text]
-
Silvers AR, Som PM. Salivary glands. Radiol Clin North
Am 1998;36:941
-966[Medline]
-
Lane MJ, Desser TS, Weigel RJ, Jeffrey RB Jr. Use of color and
power Doppler sonography to identify feeding arteries associated with
parathyroid adenomas. AJR
1998;171:819
-823[Abstract/Free Full Text]
-
Johns ME. The salivary glands: anatomy and embryology.
Otolaryngol Clin North Am
1977;10:261
-271[Medline]
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati What's this?
Top
Abstract
Introduction
