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Howlett et al. Sonographically Guided Biopsy of Parotid Mass

Head and Neck Imaging • Original Research

Sonographically Guided Core Biopsy of A Parotid Mass


David C. Howlett1 Leon J. Menezes2 Khari Lewis1 Andrew B. Moody2 Nick Violaris3
Michael D. Williams2
Howlett DC, Menezes LJ, Lewis K, Moody AB, Violaris N, Williams MD OBJECTIVE. The
purpose of this study was to evaluate the accuracy of sonographically guided core
biopsy in the evaluation of parotid masses. SUBJECTS AND METHODS. Between 1998 and
2004, 135 patients consecutively presenting with a parotid mass were prospectively
enrolled into this study. A single operator performed initial diagnostic
sonography and then sonographically guided core biopsy using local anesthesia.
Biopsy was performed with an 18- or 20-gauge needle and a spring-loaded biopsy gun
with a mean of two passes per patient. Outcome measures were accuracy,
sensitivity, specificity, and predictive values of sonographically guided core
biopsy compared with the final pathologic diagnosis in the surgical group. In the
nonsurgical group, final diagnosis was established on the basis of histologic
findings after adequate core biopsy and clinical follow-up. RESULTS. All
sonographically guided core biopsy specimens were considered satisfactory for
histologic evaluation. Overall there were 71 benign tumors, 35 malignant tumors,
and 29 miscellaneous, nonneoplastic lesions. In 76 (56%) of the 135 patients who
underwent surgery, sonographically guided core biopsy and surgical histologic
findings were correlated for 74 patients. In two cases sonographically guided core
biopsy and surgical histologic findings did not correlate. In one case, the
sonographically guided core biopsy finding was mucoepidermoid carcinoma, but the
final diagnosis was squamous cell carcinoma. In the other case, the finding at
sonographically guided core biopsy was squamous cell carcinoma, but the final
diagnosis was mucoepidermoid carcinoma. The treatment of these patients was not
affected. Fifty-nine (44%) of the 135 patients avoided surgery. In differentiation
of benign from malignant disease, sonographically guided core biopsy had a
sensitivity, specificity, and diagnostic accuracy of 100%. Sonographically guided
core biopsy also had positive and negative predictive values of 100% in the
diagnosis of malignancy. There were no significant complications of
sonographically guided core biopsy. CONCLUSION. Sonographically guided core biopsy
is a highly accurate technique for evaluation of parotid lesions and can be safely
performed as an outpatient procedure. Sonographically guided core biopsy has
potential advantages over fine-needle aspiration cytologic examination,
particularly in the typing and grading of lymphoma and carcinoma and in improved
differentiation of reactive nodal hyperplasia from lymphoma. The use of
sonographically guided core biopsy may help reduce the need for surgical biopsy
and facilitates prompt referral to the appropriate clinical team. umerous
pathologic processes present with parotid swelling, and it is frequently difficult
on clinical grounds alone to determine with confidence the nature of a parotid
mass. Reaching an accurate diagnosis when contemplating surgery is important,
because many nonneoplastic and some neoplastic lesions may not require surgical
intervention, particularly in patients at poor anesthetic risk. It also may be
possible to manage certain benign neoplasms, such as Warthin’s tumor, with
minimally invasive surgical techniques such as extracapsular dissection. Accurate
diagnosis is essential for

Keywords: head and neck imaging, head and neck radiology, parotid gland,
sonography DOI:10.2214/AJR.05.1549 Received September 1, 2005; accepted after
revision December 7, 2005.
1Department
of Radiology, Eastbourne District General Hospital, East Sussex BN21 2UD, United
Kingdom. of Maxillofacial Surgery, Eastbourne District General Hospital, King’s
Dr., Eastbourne, East Sussex BN21 2UD, United Kingdom. Address correspondence to
D. C. Howlett (David.Howlett@ESHT.NHS.UK).

2Department

3Department of Ear, Nose and Throat Surgery, Eastbourne

District General Hospital, Eastbourne, East Sussex, BN21 2UD, United Kingdom. AJR
2007; 188:223–227 0361–803X/07/1881–223 © American Roentgen Ray Society

selection of the appropriate operative procedure and to allow informed patient


consent. After the fall from favor of open biopsy as the result of a high level of
tumor seeding [1], fine-needle aspiration cytology (FNAC) has been widely adopted
for assessment of parotid masses. High diagnostic accuracy has been found in some
studies [2–6]. FNAC has welldocumented limitations, however, and is frequently
associated with high levels of inadequate or false-negative diagnoses [7, 8]. It
is against this background that sonographically guided core biopsy of the parotid
gland has been investigated [9–11]. Previous studies in-

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Howlett et al.
patient, the benefits and potential hazards of the procedure having been
explained. Contraindications to biopsy included inability to provide written
consent or to cooperate and concurrent use of anticoagulant medication or presence
of known bleeding diathesis. Preprocedural assessment of platelet count and
clotting parameters was not undertaken routinely. All diagnostic sonographic
examinations and biopsies were performed by a single operator using a freehand
biopsy technique. With an aseptic technique and after administration of 1%
lidocaine local anesthetic, a small skin incision was made and a biopsy needle
introduced under sonographic guidance. Biopsy specimens were obtained with a
spring-loaded device. For the first 16 patients a 22-mm fixed-throw mechanism
(Biopty Gun, Bard) was used, and thereafter, a 15- to 22-mm variable throw device
(Magnum gun, Bard). An average of two passes were made per patient. Biopsy samples
were fixed in a jar containing 10% formalin and were sent for histologic analysis.
All parotid lesions were demarcated sonographically as lying in the superficial
lobe of the gland and had a size range of 6–58 mm. In most (n = 122) of the
patients, 18-gauge needles were used. Because of the hazards of facial nerve and
vascular injury, 20-gauge needles were used in patients (n = 13) with smaller
lesions situated close to the main intraparotid vessels. Under sonographic
guidance, lesions were approached along the longitudinal, oblique, or transverse
plane, depending on the position of the lesion and to avoid adjacent structures
(Fig. 1). Biopsy specimens of cystic lesions were obtained from the cyst wall,
samples being directed at the more solid components of lesions of mixed cystic and
solid appearance. The needle throw of the variable-throw biopsy device was
selected according to the size and situation of the lesion to allow adequate
lesion sampling but to ensure the needle did not exit deep in relation to the
lesion (Fig. 2). Most of the biopsy procedures took less than 15 minutes. After
biopsy, patients were asked to compress the puncture site and were observed for 30
minutes before discharge. Final diagnosis was established on the basis of adequate
histologic findings in the core biopsy specimen and surgical histologic findings
for the surgical group or clinical follow-up findings for patients who did not
undergo surgery. The follow-up period ranged from a few months to 7 years.

Fig. 1—32-year-old woman with normal parotid gland. Longitudinal sonogram shows
main intraparotid vessels. Retromandibular vein (large arrow) is superficial to
external carotid artery (small arrow). Facial nerve is not shown but passes just
superficial to retromandibular vein. Deep parotid lobe (D) is deep in relation to
plane passing through path of nerve, and superficial lobe (S) is superficial to
this plane.

volved 16 [9], 54 [10], and 53 [11] patients with parotid swelling and showed a
diagnostic accuracy of 97% [10, 11] to 100% [9] for sonographically guided core
biopsy findings compared with surgical histologic findings, and there were no
significant complications. In two of the studies [9, 10], 18-gauge or smaller
needles were used with a mean of two passes per patient. In the third study [11],
small- and largebore needles (up to 14-gauge) and a range of needle passes were
used. The purpose of our study was to evaluate the accuracy and safety of
sonographically guided core biopsy performed only with small-bore needles in a
series of 135 patients presenting with a parotid mass. Subjects and Methods
Over the 7-year period from 1998 to 2004, 135 patients consecutively referred for
evaluation of a parotid mass were incorporated into this prospective study. Sixty-
three patients were men, and 72 were women. The age range was 18–93 years (mean,
60 years). After initial diagnostic sonographic examination (ATL HDI 5000 system,
Philips Medical Systems) with a high-resolution linear array transducer (12–5 MHz;
7–4 MHz in larger patients or for deeper lesions), the operator proceeded to core
biopsy. Before biopsy, written consent was obtained from the
Results Of the 135 patients in the study, 76 underwent surgery and 59 avoided
surgery. Initial sonograms showed a focal lesion suitable for biopsy in 124
patients; 11 patients in the nonsurgical group had diffuse sonographic
abnormalities with no discrete focal lesion. All sonographically guided core
biopsy specimens were considered satisfactory for evaluation by the
histopathologist. In the surgical group, 55 patients had a diagnosis of benign
neoplasm (37, pleomorphic adenoma [Fig. 3]; 16, Warthin’s tumor [Fig. 4]; two,
oncocytoma). Eighteen patients had a diagnosis of malignancy (three,
mucoepidermoid carcinoma [Fig. 5]; one, adenoid cystic carci-

Fig. 2—68-year-old woman with painless, progressive parotid gland enlargement and
Sjögren’s syndrome. Biopsy findings confirmed diagnosis of non-Hodgkin’s lymphoma
complicating Sjögren’s syndrome. A and B, Sonograms show 16-mm pseudocystic mass
in tail of right parotid gland. Tip of biopsy needle (arrow, A) is positioned so
that on needle discharge with 15-mm setting of biopsy device, needle traverses but
does not exit lesion. Confirmation of needle placement is seen in B.

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Sonographically Guided Biopsy of Parotid Mass and no focal lesion found at


sonography (six, fatty infiltration; one, Sjögren’s syndrome [Fig. 6]; one
sarcoidosis, two chronic sialadenitis, one, normal parotid gland). The patient
with a core biopsy diagnosis of normal parotid tissue presented with bilateral
parotid swelling. At sonography the glands appeared hyperechoic and enlarged,
suggestive of fatty infiltration. Biopsy specimens were obtained from the
superficial lobe of the right parotid gland. After a normal histology report, no
further investigations were undertaken. There was complete agreement between the
results of sonographically guided core biopsy and surgical histologic findings in
74 of 76 patients. The two cases that did not correlate were malignant tumors. One
of these tumors was diagnosed as squamous cell carcinoma at sonographically guided
core biopsy, but the final histologic result was mucoepidermoid carcinoma. In the
other case, the core biopsy diagnosis was mucoepidermoid carcinoma, but the final
histologic result was squamous cell carcinoma. The treatment of these two patients
was not affected by these findings; both underwent surgical excision. Only six of
17 patients with a core biopsy diagnosis of non-Hodgkin’s lymphoma needed surgical
biopsy for further treatment information. The eight patients with reactive nodal
hyperplasia diagnosed at sonographically guided core biopsy were well during
clinical followup. Sixteen patients with benign neoplasms did not undergo surgical
treatment. They either declined or were unfit for surgery and continued to undergo
observation. Three nonneoplastic lesions were managed surgically either for
symptom control or at patient request. Sonographically guided core biopsy was well
tolerated by all patients with no immediate complications. A small subclinical
hematoma was present at surgery in one patient who had undergone biopsy of a
Warthin’s tumor. The hematoma was in the soft tissue overlying the gland at the
biopsy site and was impalpable. The patient had no predisposing risk factors for
bleeding, and surgery was unaffected. No evidence of tumor seeding was detected
during follow-up. To assess the utility of sonographically guided core biopsy in
the diagnose of malignancy and to differentiate benign from malignant disease, we
compared histologic results and sonographically guided core biopsy findings for
the 76 patients who underwent both biopsy and surgery. There were 18 true-positive
findings (malignant diagnosis) and 58 truenegative findings (benign diagnoses) and
no

Fig. 3—48-year-old man with painless parotid mass. Sonogram of pleomorphic adenoma
shows rounded and circumscribed hypoechoic solid mass in superficial lobe of
parotid. Distal acoustic enhancement is evident.

Fig. 4—55-year-old man with painless slow-growing parotid mass. Sonogram of


Warthin’s tumor shows circumscribed hypoechoic mass with inhomogeneous internal
architecture containing solid and prominent cystic components.

Fig. 5—67-year-old woman with painless, rapidly enlarging parotid mass. Sonogram
of mucoepidermoid carcinoma shows ill-defined, hypoechoic mass in superficial lobe
of parotid gland. Lesion is of heterogeneous echotexture, and distal acoustic
shadowing is present. Sonographic features are those of primary malignant tumor of
parotid, although histologic subtypes cannot be differentiated with sonography.

Fig. 6—70-year-old man with painless parotid gland enlargement. Longitudinal


sonogram shows diffuse involvement of parotid gland in Sjögren’s syndrome. Gland
appears coarse and hypoechoic and contains multiple small hypoechoic foci that are
in keeping with sialectatic changes of Sjögren’s syndrome.

noma; two, adenocarcinoma; one, oncocytic carcinoma; two, squamous cell carcinoma;
two, poorly differentiated carcinoma; one, melanoma; six, non-Hodgkin’s lymphoma).
Three patients had miscellaneous, nonneoplastic diagnoses (one, lymphadenitis; one
lymphoepithelial cyst; one, actinomycosis). In the nonsurgical group, 16 patients
had a diagnosis of benign neoplasm (eight, pleomorphic adenoma; eight, Warthin’s
tumor), and 17

had a diagnosis of malignant neoplasm (one, adenocarcinoma; one, small cell lung
carcinoma; one, nasopharyngeal carcinoma; three, squamous cell carcinoma; 11, non-
Hodgkin’s lymphoma). Fifteen patients had a nonneoplastic diagnosis and a focal
lesion present at sonography (eight, reactive nodal hyperplasia; three,
tuberculosis; one, sarcoidosis; one, retention cyst; two, sclerosing
sialadenitis). Eleven patients had a nonneoplastic diagnosis

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Howlett et al. false-positive or false-negative findings, giving sonographically


guided core biopsy a sensitivity, specificity, and diagnostic accuracy of 100% and
100% positive and negative predictive values in the diagnosis of malignancy.
Discussion FNAC as a technique has a number of advantages in assessment of parotid
masses. It is fast, safe, well tolerated, and accurate when performed by skilled
practitioners. The accuracy of FNAC can be enhanced within a specialist clinic,
which may be led by a cytologist [3] or a radiologist [12]. Outside the specialist
clinic, however, the accuracy of FNAC decreases significantly with acquisition of
large numbers of aspirate samples that do not give enough information for
diagnosis [7, 8]. Even when the procedure is performed by an experienced
practitioner, there are well-recognized pitfalls in the cytologic diagnosis of
pleomorphic adenoma [13, 14] and Warthin’s tumor [15]. Despite the use of
ancillary cytologic techniques (flow cytometry and in situ hybridization) with
FNAC in the diagnosis of lymphoid proliferation, it is often difficult to
differentiate low-grade lymphoma from reactive nodal hyperplasia [16], and FNAC
diagnosis of lymphoma is not generally considered definitive [17]. In these cases
FNAC often acts as an indicator of the need for surgical biopsy. Differentiation
of reactive atypia in benign squamous epithelium from well-differentiated squamous
cell carcinoma may not be possible with FNAC [18]. In addition, it often is not
possible to diagnose parotid involvement by systemic disease such as Sjögren’s
syndrome and sarcoidosis with FNAC or to accurately grade and type carcinomas and
lymphomas or to differentiate in situ from invasive disease [10, 16]. FNAC has a
low predictive value for benign nonneoplastic lesions [6], and a negative FNAC
result has a low negative predictive value [5]. FNAC is more likely not to give
enough information for diagnosis of small lesions, those of low cellularity, and
those with uncommon histologic features. The pitfalls of FNAC have led some
authors to study the use of sonographically guided core biopsy in assessment of
parotid masses [9–11]. The combination of initial diagnostic sonography with
biopsy is useful because the parotid glands are superficial structures, readily
amenable to assessment with high-resolution sonography. Sonography is the initial
imaging technique of choice for the characterization and delineation of parotid
masses, and the findings can be used as a guide for additional imaging (usually
MRI) of possibly malignant lesions and of lesions the full extent of which is
difficult to assess, particularly if there is deep lobe involvement, an area of
sonographic weakness due to mandibular obscuration [19, 20]. The use of
sonographic guidance for biopsy is important because it allows accurate needle
placement, such that the needle traverses but does not exit deep in relation to
the lesion and avoids adjacent structures. A variable throw ability of the biopsy
device is useful when space is confined. Some needle devices allow initial passage
of the inner stylet for exact positioning of the needle tip, with subsequent
discharge of the outer sheath over the fixed inner stylet to obtain a core of
tissue. This technique may help reduce damage to deeper structures. Sonographic
guidance also allows central sampling of a lesion with improved diagnostic yield
[21], and necrotic areas can be bypassed. Sonography may also depict clinically
impalpable disease. In our study, sonographically guided core biopsy had a
diagnostic accuracy of 100% in the surgical group, comparable with previous
findings. Sonographically guided core biopsy also had 100% sensitivity and
specificity in the differentiation of benign from malignant disease and 100%
positive and negative predictive values in the diagnosis of malignancy. There was
no correlation between sonographically guided core biopsy findings and surgical
histologic findings in only two cases, of mucoepidermoid and squamous cell
carcinoma, but management was unaffected. In all cases, biopsy specimens with
which a diagnosis could be determined were obtained with small-bore needles (18-
or 20-gauge) with an average of two passes per patient. Sonographically guided
core biopsy was well tolerated with no significant complications. Unlike FNAC,
sonographically guided core biopsy requires formal histologic reporting, which is
time-consuming, and it is more invasive than FNAC, requiring local anesthesia and
a skin incision. The main advantage of core biopsy over FNAC is that a core of
tissue is obtained that can be used for formal histologic and immunohistochemical
analysis. This advantage improves differentiation of low-grade lymphoma from
reactive nodal hyperplasia, allows grading and typing of lymphoma and poorly
differentiated carcinoma, and helps determine the likely origin of metastatic
carcinoma. In our study only six (35%) of 17 patients with nonHodgkin’s lymphoma
needed surgical biopsy for additional treatment information, and no patient with a
core biopsy diagnosis of reactive nodal hyperplasia underwent surgical excision,
clinical follow-up sufficing. Eleven patients in whom no focal lesion was detected
with sonography underwent sonographically guided core biopsy for evaluation of
possible parotid involvement by systemic disease. Although there were no major
complications of sonographically guided core biopsy in our study, there are
hazards of core biopsy that need to be considered, including hemorrhage, facial
nerve injury, and tumor seeding. The retromandibular vein and external carotid
artery are the major intraparotid vessels; they are well visualized with
sonography (Fig. 1) and can be avoided [20]. The facial nerve is not readily
identified with sonography, although its position can be inferred because the
nerve passes in a plane superficial to the retromandibular vein and can be avoided
[14, 20]. Tumor seeding along the needle track is a hazard of both FNAC and core
biopsy. The risk of tumor seeding varies according to the organ involved and the
size of the needle used. Tumor seeding is described in as many as 12% of cases of
FNAC of thoracic mesothelioma [22], with an incidence of only 0. 02% for abdominal
tumors [23]. Evidence suggests that tumor seeding tends to occur with larger-bore
needles, probably because these needles allow aspiration of sizable stromal
fragments and allow survival of malignant cells [22]. Tumor seeding in the parotid
gland is extremely rare after needle biopsy and has been described only in
association with the use of large-bore needles [24]. Some surgeons excise the
biopsy track, although this approach has not been adopted at our institution.
Although there was no evidence of tumor seeding in our study population, patient
follow-up was limited to only a few months in some cases, and continued
surveillance is needed. In conclusion, sonographically guided core biopsy is a
highly accurate, safe, and well-tolerated technique for the diagnosis of parotid
mass. The procedure can be performed with small-bore needles on an outpatient
basis. Sonographically guided core biopsy has advantages over FNAC, particularly
in differentiation of lymphoma from reactive nodal hyperplasia, in typing and
grading of carcinoma and lymphoma, and in the assessment of parotid involvement by
systemic disease. The use of sonographically guided core biopsy may reduce the
high rate of surgical biopsy associated with FNAC that does not provide enough
information for diagnosis and may facilitate both prompt referral to the relevant

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Sonographically Guided Biopsy of Parotid Mass clinical team and selection of an


appropriate operative procedure if needed. Acknowledgments We thank Carrie Favell
for typing the manuscript, Nick Taylor for preparing the illustrations, and David
Sallomi for assistance with the statistics.
7. McGurk M, Hussain K, Role of fine needle aspiration cytology in the management
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