Ultrasound and multidetector computed tomography of mandibular salivary gland adenocarcinoma in two dogs


D. Lenoci and M. Ricciardi

"Ultrasound and multidetector computed tomography of mandibular salivary gland adenocarcinoma in two dogs"

Open Veterinary Journal, (2015), Vol. 5(2): 173-178


Abstract
Malignant tumors of the salivary glands are rare in dogs, with adenocarcinoma being the most represented. Parotid
and mandibular glands are most commonly affected in dogs. Because of local invasivity and high metastatic potential,
preoperative imaging evaluation of mandibular region and tumoral staging is essential along with biopsy sampling.
The present manuscript describes the ultrasound and computed tomographic imaging findings of mandibular gland
adenocarcinoma in two dogs and discusses their clinical utility.
Keywords: Computed tomography, Dog, Salivary gland tumor, Ultrasound.

 

Introduction
The major causes of localized bulging in the upper neck region in dogs include salivary mucoceles, sialoadenitis,
sialolithiasis, lymph nodes abscesses, salivary gland infarction and foreign bodies, lymph node and salivary
gland tumours (Militerno et al., 2005; Torad and Hassan, 2013). Salivary gland neoplasms are described
as rare accounting for 0.17% of all small animal tumors (Carberry et al., 1988). In dogs mandibular and parotid
glands seem to be most commonly involved without breed and sex predisposition (Spangler and Culbertson,
1991; Hammer et al., 2001; Marconato and Amadori 2012). Among malignant salivary gland tumors several
histotypes have been reported with adenocarcinoma being the most represented (Head and Else, 2002; Head
et al., 2003; Sozmen et al., 2003).
These neoplasms are considered extremely aggressive, usually locally invasive, so they may extend through
the capsule of the gland to infiltrate adjacent tissues; rapid metastatization to regional lymph nodes and to
other organs, such as lungs and bones, is also described in the progression of the disease (Burek et al., 1994;
Habin and Else, 1995; Morris and Dobson, 2001). As for all localized tumors the treatment of choice is the
surgical removal with a surgical success rate depending on the local invasivity and involvement of surrounding
vital structures. Adjunctive radiation therapy or chemotherapy may be considered following surgery
(Evans and Thrall, 1983). Median survival times in most aggressively treated cases is 1 - 2 years (Hammer
et al., 2001). Furthermore, literature indicates that early diagnosis significantly improves the survival times in
dogs (Hammer et al., 2001; Sidaway et al., 2004).To date different reports have described the clinical
approach for mandibular gland malignancies in dogs, underlying the importance of cytopathological and
histopathological evaluation before and after surgical treatment (Militerno et al., 2005; Smrkovski et al.,
2006; Almeida et al., 2010). In this scenario specific veterinary literature regarding the imaging appearance
of these neoplasms on ultrasound and CT examinations is scarce with only sporadic descriptions and images
available for review (Smrkovski et al., 2006; Marconato and Amadori, 2012;). This paper describes
and compares the ultrasonographic and computed tomography imaging findings in two cases of canine
mandibular gland adenocarcinoma and discusses the role of these two techniques in the diagnostic utility
of this disease.


Case Details
Dog 1
An 11-year-old intact male dalmatian dog was evaluated for a 2-months history of progressive left
submandibular swelling. On physical examination the patient did not show any abnormality except for a fixed,
firm non-painful subcutaneous mass located ventro-caudal to the left mandibular angle. No mandibular
lymph nodes enlargement was evident on palpation. Hematobiochemical and urinalysis were normal.
Dog 2
A 13-year-old intact female dalmatian dog was evaluated for a bulky swelling in the right mandibular
region first noted by the owner 30 days before. At palpation the mass appeared soft, non-painful and
slightly mobile with respect to surrounding tissue. Because of the considerable dimensions of the mass the
evaluation of mandibular lymph nodes was difficult. General physical examination, hematobiochemical and
urinalysis were normal.

 

Imaging
Dog 1
In order to clarify the anatomical origin of the neoformation, a B-mode ultrasound examination of
the upper neck was performed with the dog in dorsal recumbency, using a portable ultrasound machine
(MyLab 30 Gold Vet®, Esaote, Genoa, Italy), with a linear, high frequency, transducer 10–18 MHz.
Ultrasound videotapes and static images were reviewed. Presence of the following ultrasonographic
abnormalities were recorded: Left submandibular gland enlargement with increased sphericity index,
well-circumscribed, hypoechoic, inhomogeneous parenchymal echogenicity with several small mineral
foci and tortuous vessels (Fig. 1). These findings were suggestive of primary mandibular gland neoplasia.
Differential diagnoses included sialoadenitis, but it was considered less likely due to the presence of
parenchymal mineralizations.
Based on the suspicious of primary neoplasm, multidetector computed tomography of the whole
body was performed immediately after the ultrasound examination for regional anatomical characterization
and complete staging. A 16-slice MDCT scanner (Somatom Emotion, Siemens, Forchheim, Germany)
was used with the patient in sternal recumbency on the CT table under general anesthesia. Computed
tomography images were acquired before and after the intravenous injection of iodinate contrast medium
(640 mg I/kg; Iopamigita® Insight Agents GmbHR, Heildeberg, Germany) using the following technical
parameters: Standard acquisition algorithm, 110 kVp, 200 mAs, 1.5-mm slice thickness, pitch of 0.8, and
0.6 s/rotation. Three-dimensional (3D) multiplanar reformatted images were obtained using a dedicated
3D software (Pixmeo, OsiriX; OsiriX DICOM-viewer; Pixmeo, Geneva, Switzerland). Computed tomography
scans showed enlargement of the left mandibular salivary gland. The abnormal parenchima appeared
homogeneous, isoattenuating to the soft tissue, with multiple irregular areas hypoattenuating to the soft
tissue mixed to small foci hyperattenuating to the soft tissue suggestive of mineralizations. No enlargment of
ipsilateral mandibular lymph nodes were seen while the left medial retropharingeal lymph node was enlarged
compared to the controlateral one. No vascular or parotid compressions were evident. No muscular

infiltrations were seen (Fig. 2).


Dog 2
Diagnostic work-up continued with regional ultrasound and total-body computed tomography as described for
dog 1.
Ultrasound evaluation revealed a large heterogeneous cavitated mass in the soft tissues of the neck, on the
right side. The marginal parenchyma was hypoecoic with mineral foci while the central component

appeared anechoic with irregular contours and far enhancement, suggestive of free fluid. The mass was
suspected to originate from thyroid gland, but after ultrasound-guided drainage of the fluid component, the
empty mass appeared caudal to the more hypoecocic digastricus muscle, landmark of mandibular salivary
glands (Fig. 3). The medial retropharingeal lymph node was hypoecoic and enlarged.

 

 

CT showed significant enlargement of the right mandibular salivary gland. This structure appeared
on native images as a large fluid-filled cavity hypoattenuating to the soft tissue (mean attenuation

value: 25 HU) surrounded by irregular peripheral tissue and crossed by multiple septa isoattenuating to the soft
tissue. Multiple small irregular foci hyperattenuating to the soft tissue (mean attenuation value: 278 HU)

suggestive of mineralizations were seen within the parenchymatous component of the mass. No significant
enhancement of the neoformation was noted after intravenous contrast medium administration (Fig. 4).
Right mandibular and medial retropharingeal lymph nodes enlargement was associated. The linguofacial
and maxillary veins were not visible immediately cranial to the bifurcation of the external jugular vein
where they came in close connection to the mass. These findings were suggestive of vascular compression. The
right parotid gland appeared also compressed between the mass and the ear canal. No muscular infiltrations
were seen. Within the left lung multiple homogeneous nodular lesions isoattenuating to the soft tissue were
seen diffuse in the cranial and caudal lobes (Fig. 5).Based on ultrasound and CT findings a presumptive
diagnosis of primary neoplasia of the left (dog 1) and right (dog 2) mandibular glands was made in both
patients. Sialoadenitis in dog one was considered less likely. In both dogs regional lymph nodes appeared
involved and in dog 2 the nodular lesions within the left lung appeared compatible with pulmonary metastasis.


Outcome
Dog 1 underwent surgical excision of the pathologic mandibular glands and retropharyngeal lymph node. In
dog 2 a bioptic sample of the neoformation was taken but complete surgical excision was refused by the
owner. All the removed tissues were then submitted for histopathology.
In both dogs the histopathologic examination revealed glandular tissue infiltrated by a non-encapsulated

neoplastic proliferation. Neoplastic tissue consisted of tubules and clusters of pleomorphic epithelial cells
with moderate-high nuclear-cytoplasmic ratio, round or oval central nucleus, vesicular chromatin and one
or more nucleoli. A thick, dense fibrous stroma with centers of cartilaginous metaplasia sustained the
neoplastic tissue. In different points the cells were arranged around necrotic centers. Mitotic rate ranged
from one to four mitosis per high-power field. In dog 2 the immunohistochemical staining of neoplastic cells
demonstrated intense cytoplasmatic expression of cytokeratin. These findings were suggestive of salivary
gland adenocarcinoma. In dog 1 histopathologic evaluation of the medial retropharyngeal lymph
node revealed a reactive hyperplasia without signs of neoplastic infiltration.

 

 

In dog 1 no local complications were observed soon after tumor removal. After surgery, the dog was treated
with enrofloxacin (5 mg/kg daily per os) for a week. Two days after surgery the dog started to eat autonomously
and 90 days later no recurrence of the disease was noted. Monitoring of the mandibular region and lungs
was recommended to the owner.
Surgery and chemotherapy were both refused by the owner of dog 2.

 

Discussion
In human medical literature imaging is always included in the diagnostic setting of patients with salivary gland
tumor before cytopatologic sampling or in conditions where there are some limitations in performing fine
needle aspiration (FNA), such as unusual location or patients’ unwillingness (Liu et al., 2015). Besides
identifying the masses of salivary glands, imaging is also useful in differentiating them from the masses/
pathologies of adjacent cervical spaces. Nodal masses, peripheral nerve schwannomas, and masseteric
hypertrophy may mimic tumors of salivary glands clinically. In proven cases of salivary gland tumors,
imaging helps in delineating the extent of the lesion and invasion of adjacent cervical spaces, skull base,
mandible, and nerves/meninges (Welkoborsky, 2011; Rastogi et al., 2012; Carotti et al., 2014;).
Because of their superficial anatomic location, distinct borders and homogenous echotexture, the
salivary glands are ideally positioned for sonographic assessment. The advantages of this technique include
high diagnostic accuracy, non-invasiveness, lack of radiation exposure, high reproducibility, low costs and
possibility of ultrasound-guided fine-needle biopsy (Welkoborsky, 2011). When combined with color
Doppler imaging, ultrasound (US) helps in assessing the vascularity and nature of the lesion (malignant vs
benign lesions) (Rastogi et al., 2012). In a previous study US achieved a sensitivity of 88%, a specificity
of 54% in assessing a tumor entity-maligne or benigne (Rudack et al., 2007).

Ultrasound and CT have been already reported as useful diagnostic tools for the evaluation of different
salivary gland pathologies in dogs such as sialolithiasis (Lee et al., 2014) mucocele (Torad and Hassan, 2013)
and sialoadenitis (Cannon et al., 2011). In these reports ultrasound and computed tomography (CT) allowed
a precise identification of the affected glands and a detailed morphologic evaluation of the type of disease.
However, descriptions of imaging findings of salivary gland tumor in dogs are limited to a single reported
case of pleomorphic adenoma of the mandibular gland in a Basset Hound in which computed tomography was
performed (Smrkovski et al., 2006). To the authors’ knowledge this is the first report describing and
comparing the US and CT characteristics of salivary gland adenocarcinomas in dogs, evaluating the clinical
utility of these imaging techniques for the diagnosis of this disease.
In our cases ultrasound examination alone was sufficient to identify the tumors, appearing as a first-line tool for
the imaging diagnosis of salivary neoplastic pathology. However, in cases of very large masses, as seen in
dog 2, ultrasound could not accurately identify their anatomical location and define possible infiltrations of
surrounding soft tissue.

In human medicine, CT and MRI are commonly used as adjunctive imaging diagnostic methods for salivary
gland tumors, usually following US examination. CT, with its good anatomic resolution, soft tissue contrast,
and morphologic detail, can provide meaningful information regarding deep located masses, bone
invasion and may help the surgeons during the procedure (Liu et al., 2015).
Analysis of different enhancement patterns by using dynamic multidetector computed tomography (MDCT)
demonstrated to be helpful in the differential diagnosis of salivary gland tumors and for distinction between
adenomas and malignant tumors (Choi et al., 2000; Yerli et al., 2007).
In our cases CT scan confirmed the ultrasonographic findings related to the neoplastic salivary glands
and provided useful adjunctive information on the relationships between the masses and adjacent
musculature (evaluation of muscular infiltration or compression), jugular vein tributaries, especially in
dog 2, regional lymph nodes involvement, particularly the deep medial retropharyngeal. Furthermore CT
allowed complete whole body scan in few seconds for oncologic staging, according to the Tumor-Node-

Metastasis (TNM) classification reported for salivary gland tumor in animals (Thackray and Sobin, 1972).
Accordingly to the report in human medical literature (Rudack et al., 2007), we did not find significant
differences between US and CT for regional anatomic evaluation. Both US and CT appeared specific for
identification of the affected glands with respect to the surrounding parotid gland, mandibular and
retropharyngeal lymph nodes and adjacent musculature. However, assessment of vascular displacement
(maxillary and linguofacial veins) and pulmonary distant metastasis in dog 2 was clarified on CT images.
Furthermore no difference in the appearance of tumoral parenchyma was evident comparing the US
and CT findings. The pathologic gland tissue varied in these two dogs from hynomogeneous solid mass
with focal mineralization and fluid areas (suggestive of necrotic foci as then confirmed by histopathology)
to large cystic-like mass with sporadic parenchymal mineralizations.
Calcifications and necrotic foci have been reported as imaging findings in carcinomatous changes of
salivary glands both in humans and dogs (Marconato and Amadori, 2012; Li et al., 2014) and were clearly
identified both on US and CT scans in the two cases we described.
Different from what is commonly described for salivary gland tumors (Habin and Else, 1995; Morris and
Dobson, 2001; Militerno et al., 2005;) in this two dogs the growth pattern appeared purely expansive without
infiltrations of surrounding structures even taking into account the big dimensions reached by neoplastic gland
in dog 2.

Lymphatic drainage of the mandibular gland is pertaining to the medial retropharyngeal lymph node
(Evans and de Lahunta, 2013). Ipsilateral mandibular lymph nodes were enlarged in dog 2 while in
both dogs an ipsilateral medial retropharingeal lymphadenopathy was evident in both US and
CT images. Differently from mandibular lymph nodes that are superficial and palpable, medial
retropharingeal lymph nodes are deeply located in the neck, medially to the mandibular gland and just
caudal to the proximal insertion of digastricus muscle (Evans and de Lahunta, 2013). This lymph nodes
appeared easily evaluable on first US examination as previously described in dogs (Burns et al.,
2008). In dog 1 the imaging finding of lymph node involvement was confirmed on histopathology
as reactive lymphoadenopathy without signs of neoplastic involvement. Total-body CT staging in
dog 2 revealed multiple nodular lesions within the left lung suggestive of distant metastasis. In a study
on twenty-four dogs with salivary tumors 17% and 8% of patients had lymph node and distant metastasis,
respectively (Hammer et al., 2001). In the authors’ opinion, giving the high metastatic potential of the
salivary gland adenocarcinoma towards regional lymph nodes and distant organs, regional evaluation,
lymph nodes mapping and extensive whole-body scan are essential for tumoral staging, accordingly to
the TNM classification (Thackray and Sobin, 1972),and can be helpful for an accurate surgical planning.

In conclusion, US and CT are reliable methods in diagnosing salivary gland tumors clinically in people
(Rastogi et al., 2012), and findings from the present study supported the use of ultrasonography as a useful
diagnostic tool for characterizing these disease in dogs before FNA or biopsy sampling and surgery. In both
patients the overall imaging findings oriented toward a presumptive diagnosis of mandibular gland neoplasia.
Salivary gland tissue could be differentiated from lymph node tissue and other neighboring structures
based on sonographic characteristics. These findings support the use of US as first regional imaging for
mandibular gland tumors characterization.
Even if significant differences between US and CT findings on mandibular gland were not detected in our
patients, computed tomography revealed its clinical utility for peritumoral vascular assessment, medial
retropharyngeal lymph nodes evaluation and total-body staging for detection of distant metastasis. Contrary
to what was reported in human medical literature, preoperative assessment of salivary gland tumor is
not routinely adopted in small animal practice based on the few veterinary reports on these disorders. To
the author opinion regional and total-body imaging evaluation, with on US and CT respectively, are useful
for the diagnostic, clinical and surgical management of mandibular gland adenocarcinoma in dogs.

 

Acknowledgments
The authors wish to thank all the staff of the Pingry Veterinary Hospital of Bari, Italy for their assistance
with data collection.
Conflict of interest
The authors declare that there is no conflict of interest.

 

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