ultrasonography of the canine, feline and equine tongue: normal findings and case history reports

ULTRASONOGRAPHY OF THE CANINE, FELINE AND EQUINE TONGUE: NORMAL FINDINGS AND CASE HISTORY REPORTS

MAURICIO SOLANO, MED. VET., DOMINIQUE G. PENNINCK, DVM

A submental approach using a 5,7.5 and 10 MHz mechanical sectorial transducers was used to evaluate the ultrasonographic appearance of the normal and abnormal canine, feline and equine tongue. Seven normal animals were used to characterize the in vivo normal ultrasonographic appearance of the oropharynx. Consistently seen anatomical landmarks included the lingual parenchyma, lingual artery, soft and hard palate interfaces, mandible, basihyoid bone and sublingual musculature. Seven fresh canine, feline and equine cadavers were dissected to confirm the ultrasonographic findings. Seven animals with signs of ptyalism, dysphagia, halitosis and visible lingual lesions were also studied. A foreign body and abscesses secondary to a penetrating wound were detected in a horse. Ultrasound guidance aided surgical dissection, removal of the foreign body and intraoperative drainage of the abscesses. Ultrasound provided valuable non-invasive documentation of the architecture, size and margins of six lingual neoplasms. Ultrasonographic monitoring of the response to the treatment of lingual lesions may be beneficial in the management of patients. Veterinary Radiology & Ultrasound, Vol. 37, No. 3, 1996, p p 206-213.

Key words: tongue ultrasound studies, canine tongue, feline tongue, equine tongue, tongue neoplasms, tongue foreign body, tongue radiotherapy, lingual ultrasound studies.

Introduction common foreign bodies have been described'." and a pro-

IAGNOSIS OF LINGUAL abnormalities in domestic ani- D mals relies primarily on visual examination, palpation, biopsy and exploratory surgery. Even in cooperative or chemically restrained animals, the tongue is only partially accessible to inspection and palpation.

Foreign body penetration and laceration of the tongue are common.'-3 A foreign body in soft tissue may produced a sinus tract which can make the object difficult to locate without producing additional soft tissue t r a ~ m a . ~ Radiogra- phy is often used to characterize and locate foreign bodies , 2 3 3 , 5 but usually is limited to the detection of radiopaque materials. Draining tracts due to a radiolucent foreign body may examined with sinography (fistul~graphy)~.~ however, artifacts from leaking contrast medium, and the need for anesthesia complicate this procedure.6

Ultrasound has proven valuable for identifying foreign bodies in soft t i s s~e .~ , ' - ' ~ The acoustic characteristics of

~- -

From the Department of Surgery, Section of Radiology, Tufts Univer- sity School of Veterinary Medicine, 200 Westboro Road, Noith Grafton, MA 01536.

Address correspondence and reprint requests to Dr. Penninck, at the above address. Dr. Solano's present address is: Department of Companion Animals, Atlantic Veterinary College, University of Prince Edward Island, 550 University Ave. Charlottetown, Prince Edward Island C1A 4P3 Can- ada.

Received December 12, 1994, accepted for publication May 31, 1995.

tocol for examination of intramuscular foreign bodies has been proposed.' Ultrasound is superior to survey radiogra- phy in determining the precise location of the foreign body' and has been used intraoperatively to guide surgical dissection, thus minimizing trauma to adjacent normal structures .53'0

Tumors of the tongue are uncommon in animals.'"'4 In a retrospective study of 361 patients with oral and pharyngeal neoplasia in the dog,14 only 12 were primary lingual tumors. Squamous cell carcinoma (SCC) accounted for 37% to 58% of all lingual tumors.13214 Other cell types have been reported less commonly. 132'5,16 Lingual neoplasia in horses is uncommon. 17,'' When suspected, lymphoma and SCC should be considered. l 7

In a recent study of canine tongue tumors,'' inability to fully evaluate tumor size using conventional methods was evident as judged by incomplete surgical resection of tumor in 50% of the patients. Given the suitability of ultrasound for soft tissue evaluation, the value of this modality war- rants further investigation for lingual neoplasia.

The objectives of this study were therefore: 1) to describe the normal ultrasonographic anatomy of the tongue and associated oropharyngeal structures in dogs, cats and horses; 2) to determine the efficacy of ultrasound in detecting pathologic changes in patients with lingual neoplasia and foreign bodies; and 3) to assess ultrasound as a tool for measuring the response to therapy.

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FIG. 1. (A) Approach for submental sonographic examination of the oropharynx. Examination of this area was easier to perform with the animal sitting or standing and their mouth closed (see materials and methods for a more detailed explanation). (B) Schematic representation of sagittal and transverse examination techniques. On the sagittal sonogram the rostral end of the animal is towards the reader’s left. On the transverse image the right aspect of the animal is towards the reader’s left. Note the near field is always ventral. All images are from live animals.

Materials and Methods

This report is based on 21 animals separated in three study groups. Group A (7 healthy animals) included 3 adult medium size dogs, 3 cats and 1 horse. These animals were used to describe the in vivo ultrasonographic anatomy of the tongue and adjacent oropharynx. Group B (7 fresh cadavers) included 3 dogs, 3 cats and 1 horse: Immediately following ultrasound examination of these additional animals, water-soluble dyes of various colors” were injected under ultrasound guidance into the structures of interest, to facil- itate identification of landmarks during subsequent dissection.*’ Group C (7 patients) 3 dogs, 3 cats and 1 horse all suspected of having a lingual mass or foreign body were also included in the study. Ptyalism, dysphagia, halitosis, hemorrhage, pain, anorexia and swelling of the tongue were the most common clinical signs.

All animals (including cadavers) were examined standing or sitting with the head in a neutral or extended position. Real time sector images were obtained, using 7.5 and 10 MHz mechanical transducers? from a submental approach, after routine skin preparation and application of transmis- sion gel.$ Examinations in horses were performed with a 5 MHz transducer. Sagittal and transverse images were produced by slightly moving the transducer from the left to right horizontal ramus of the mandible and by scanning caudally from the mandibular symphysis to the thyroid car- tilage respectively (Fig. 1A and 1B).

Ultrasonographic features of the lesions identified were described by location, extent, size and echogenicity relative

*Food Colorant. G.E. Barbour Inc. Sussex NB EOE-lPO. tUltramark 8’”, Advanced Technology Laboratories Inc. Bothell WA

$Echotrack, Echo Ultrasound Reedsville. PA 170849772, 9804 1.

to the appearance of the normal tongue. The confirming diagnosis was obtained by surgery or biopsy.

Results

Canine Ultrasonographic Anatomy

The normal canine tongue of healthy animals (group A) and cadavers (group B) was found to be homogeneously and finely echogenic (Fig. 2a). Due to the mandibular symphysis and narrow submental space in the rostral third of the oropharynx, the most rostral portion of the tongue could not be visualized by the submental approach. Consistent ultrasonographic landmarks identified in experimental groups A and B included an acoustic interface between the hard palate, lingual parenchyma and air in the oropharynx. This interface was visualized as a linear, highly echogenic area dorsal to the body of the tongue (Fig. 2a). The caudal third of this interface (dorsal to the root of the tongue) was less well defined. The most caudal landmark was the acoustic shadow generated by the basihyoid bone caudal to the root of the tongue (Fig. 2b). Caudal to the basihyoid bone, acoustic shadows generated by air in the pharynx obscured the tonsils and dorsal wall of the laryngopharynx (Fig. 2b). The mylohyoid and the geniohyoid mm. were identified as a poorly echogenic structures ventral to the tongue (Fig. 2a). It was impossible to differentiate between these two muscles, even with the 10 MHz transducer. On transverse images, the acoustic shadows of the left and right horizontal rami of the mandible provided the most prominent landmarks. In some medium to large dogs, the shape of the tongue on transverse images changed from ovoid (over the caudal third) to bilobed (rostral two thirds) (Fig. 2c). In healthy dogs (group A), the lingual arteries could be seen by

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SOLANO AND PENNINCK 1996

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FIG. 2. (A) Sagittal sonogram of the body of the tongue (T) of a normal dog. Note the linear interface between the hard palate, lingual parenchyma and air in the oropharynx (arrows). The sublingual muscles (m) are poorly echogenic and somewhat obscured by the near field artifacts. (B) Sagittal sonogram of the root of the tongue (T) of a normal dog. Note the acoustic interface between the soft palate, lingual parenchyma and air in the oropharynx (arrows). Shown are the acoustic shadow generated by the basihyoid bone (b), the acoustic shadow generated by air in the pharynx obscuring pharyngeal structures (ph) and the area of thc sublingual muscles (m). (C) Transverse sonogram of the rostral third of the tongue (T) of a normal dog. The (m) designates the acoustic shadows generated by the horizontal rami of thc mandible. Shown are the acoustic interface between the hard palate, lingual parenchyma and air in the oropharynx (arrow) and the area of the sublingual muscles (sb). Note the bilobed appearance of the tongue. (D) Parasagittal sonogram of the body of the tongue (T) of a normal dog. Notc the lingual artery with strong echogenic walls (black anow) and the acoustic interface between tongue, palate and air in the oropharynx (white arrows)

parasagittal scanning the tongue as two anaechoic to hypoechoic tubular structures in the ventral third of the tongue with highly echogenic walls (Fig. 2d). The lingual arteries were difficult to detect in cadavers.

Feline

The appearance of the tongue and oropharynx in cats (groups A and B) was similar to that of dogs. The 10 MHz transducer provided the best visualization of the anatomic landmarks. The lingual parenchyma was homogeneously echogenic. The mylohyoid and geniohyoid muscles were difficult to differentiate even with the 10 MHz transducer. Other landmarks, such as basihyoid bone, lingual artery, hard palate-soft tissue interface, and acoustic shadows of the mandible were as described for dogs.

Equine The sublingual musculature in the near field, was not

identified. In addition to the previously described landmarks for dogs and cats, the genioglossus muscle was readily identified in horses in groups A and B as several parallel echogenic lines overlying the root of the tongue (Fig. 3a). The rostral narrowing of the submental space in horses and the strong, wide acoustic shadows generated by the mandible precluded assessment of the rostral portion of the tongue. Transverse images were characterized by similar limitations (Fig. 3b).

Case History Reports No I

A 12 year old Percheron gelding was presented with dysphagia, profuse salivation and a lacerated tongue. Right

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FIG. 3 . (A) Sagittal sonogram of the root of the tongue (T) of a normal horse. Note the parallel fibers of the genioglossus muscle (arrow heads) and the acoustic interface between tongue, palate and air in the oropharynx (arrows). (B) Transverse sonogram of the body of the tongue (T) of a normal horse. The (M) designates the acoustic shadows generated by the horizontal rami of the mandible. The arrows demarcate the lingual surface of the horizontal rami of the mandible. Note the attenuation of the sound beam along the deep-located areas of the lingual parenchyma (a).

lateral and dorsoventral radiographs of the head revealed a 17 cm length of wire that was either within the tongue or sublingual soft tissues. Ultrasound examination confirmed that the foreign body was imbedded in the lingual parenchyma. Several rounded, well defined anechoic areas were also identified in the tongue and were compatible with fluid pockets (Fig. 4). The parenchyma of the ventral two thirds of the tongue was hypoechoic compared to the normal dorsal third. Ultrasound was used intraoperatively to guide placement of a Wescott needle to guide the surgeon. A second I8 gauge Wescott needle was used to drain serosan- guinous fluid from the pockets. Streptococcus sp. were iso- lated from the fluid. Four days after surgery, the clinical signs had resolved and the abscesses were no longer identified on ultrasound examination.

No 2

A 7 year old, castrated male, Himalayan cat was presented with 2 weeks of anorexia, occasional vomiting, weight loss and severe generalized icterus.

A diffusely hyperechoic liver was seen during abdominal ultrasonography. In preparation for an ultrasound guided liver biopsy under general anesthesia, a large sublingual mass was detected during intubation. Ultrasonographically the sublingual mass was diffusely hypoechoic and ill defined and involved the lingual frenulum and the root of the tongue. The lingual portion of the mass was closely associated with a vessel and measured 1.2 cm. in depth (Fig. 5). The lingual mass was resected. The decreased cardiovascu- lar function of the patient after surgery lead to cardiopul-

FIG. 4. Sagittal sonogram of the body of the tongue (black T) of a horse. The white (T) indicates the hypoechoic and possibly edematous lingual parenchyma. The (a) represents abscesses. There is a linear foreign body (arrow heads) generating reverberation artifacts (small arrows). The white arrows denote the tongue/palate interface.

FIG. 5 . Sagittal sonogram of the caudal third of the tongue (T) of a cat with a lingual squamous cell carcinoma (patient 2). The 1.2 cm long hypoechoic tongue tumor is between the calipers. Note the poorly defined caudal tumor border. A vessel can be seen entering the tumor (arrow).

210 SOLANO AND PENNINCK 1996

FIG. 6 . Sagittal sonogram of the body of a canine tongue with a lingual rhabdomyoma (patient 3). The entire tongue (T) is diffusely hypoechoic and intermixed with linear echogenic areas (arrows). Compare the echogenicity with that of a normal tongue in figure 2A.

monary arrest and death. A squamous cell carcinoma and severe diffuse hepatic lipidosis were identified on histology of the partially resected lingual mass and liver tissue.

No 3

A 21 month old, neutered female Fox Terrier, was presented with a history of gagging and protrusion of the tongue. A tongue biopsy had been performed by the referring veterinarian and the diagnosis was a rhabdomyoma. Ultrasonographically, the entire tongue was diffusely hypoechoic and intermixed with well defined linear echogenic areas extending to and surrounding the lingual vessels (Fig. 6).

Orthovoltage radiotherapy5 of the tongue was combined with oral prednisone ( 5 mgs orally every other day for 5 weeks) and oral metronidazole (125 mg daily for 15 days). A total tumor dose of 40 Gy was delivered, at 4 Gy per fraction, on a Monday-Wednesday-Friday schedule. The owner reported some resolution of clinical signs and reduction in the size of the tongue. However, ultrasonographically there were no significant changes in the appearance of the lesions 30 days after initiation of radiotherapy. The animal remained asymptomatic at 11 months after initial diagnosis.

No 4

A 12 yr-old neutered female, domestic short haired, cat was presented with a history of halitosis and thick mucoid salivation. A mass in the root of the tongue, to the right, was detected on physical examination. Sonographically there was a 1 .O cm thick x 1.3 cm long ovoid ill-defined hyperechoic mass located in the caudal third of the tongue

??Siemens Stabilipan 11'" Quality Radiology Inc. Hanover MA 02339.

parenchyma (Fig. 7). Only a small portion of the mass protruded from the lingual surface. The histologic diagnosis was squamous-cell carcinoma. The owner elected euthanasia.

No 5

A 12 yr-old neutered female Brittany spaniel was referred with progressive dyspnea of 8 months duration. A biopsy and resection of a sublingual mass had been performed by the referring veterinarian and the diagnosis was amelanotic melanoma. A white, lobulated, sublingual mass was detected during examination at the site of the previous surgery. Ultrasonographically there was a hypoechoic, ovoid, well-defined mass, measuring 2.0 cm in diameter located ventral to the middle third of the tongue. There was no apparent involvement of the lingual parenchyma (Fig. 8). A second biopsy, involving removal of the sublingual mass, was interpreted as ulcerated granulation tissue and a sub- mucosal cyst. There was no evidence of recurrence of the amelanotic melanoma.

No 6

A 9 yr-old female Akita was presented with a one week history of malodorous breath and an ulcerated polypoid lingual mass. Ultrasonographically there was an amorphous hypoechoic, 3.8 cm long mass, centered caudal to the root of the tongue, extending rostrally and dorsally over the caudal third (Fig. 9). Acoustic shadows generated from air in the pharynx obscured the caudal extent of the mass. Evaluation of sagittal images of the tongue confirmed involvement of the left aspect of the root of the tongue by the mass. This was indicated by the hypoechoic nature of the lingual parenchyma. The mass also exhibited strongly echogenic irregular borders. The polypoid mass was re-

FIG. 7. Sagittal sonogram of the caudal two thirds of a feline tongue with a lingual squamous cell carcinoma (patient 4). The 1.3 cm long hyperechoic lingual tumor is between calipers. The normal parenchyma of the tongue (T) and the tongue/palate interface (arrows) are shown.

VOL. 37, No. 3 ULTRASONOGRAPHY OF THE TONGUE 21 1

FIG. 8. Transverse sonogram of the mid-body of a canine tongue (patient 5). The 2.0 cm diameter echogenic sublingual amelanotic melanoma is between the calipers. Note the bilobulated appearance of the normal lingual parenchyma (T), tongueipalate interface (arrows) and the acoustic shadow generated by the mandible (M).

sected. The histologic diagnosis was an intraductal cystic papillary and tubular adenocarcinoma most likely of salivary gland/duct origin. The owner declined further treatment. Four months after initial presentation a new tumor in the mouth was reported by the referring veterinarian.

No 7

A 6 yr-old, neutered female, domestic short haired cat was presented with a 3 week history of ptyalism, anorexia and extreme weakness. The referring veterinarian noticed a large oral mass, which was diagnosed by biopsy as a squamous cell carcinoma. Under general anesthesia, the bulk of the mass appeared sublingual and was displacing the rostra1 third of the tongue dorsally. Ultrasonographically, a large

1.8 cm long, well defined sublingual mass with complex echotexture extended into the caudal two thirds of the tongue (Fig. 10). Normal tongue parenchyma was replaced by a mostly hyperechoic and heterogenous, diffuse lesion.

Following orthovoltage radiotherapy of the tongue (total tumor dose of 40 Gy, at 4 Gy per fraction, delivered on a Monday-Wednesday-Friday schedule) the sublingual portion of the mass reduced from 1.8 cm to 1.4 cm, however, partial necrosis of the lingual parenchyma was also noted. Follow-up ultrasonography after removal of necrotic tissue at the eighth treatment disclosed no changes in the appearance of the remaining smaller sublingual mass. Initial signs did not resolved. The animal died 3 months after initial diagnosis.

Discussion

Ultrasonographic Anatomy

The ultrasonographic appearance of the tongue in the dog, cat and horse is similar to that of humans. The acoustic interface between the hard palate and air in the oropharynx is visualized as a highly echogenic line dorsal to the body of the tongue. However, the caudal third of this interface (dorsal to the root of the tongue) is not as well defined, which is likely due to the presence of the soft palate, instead of the hard palate. The soft palate presumably has an acoustic impedance similar to that of the lingual parenchyma (Fig. 2b). Contrary to the findings in humans, the geniohyoid and mylohyoid mm. of the dog, cat and horse are difficult to distinguish from one another, even with high frequency transducers. In horses and mid-size to large dogs, the fibers of the genioglossus are clearly visualized (Fig. 3a). As in humans the submental approach was the most informative

FIG. 10. Transverse sonogram of the body of a feline tongue with a lingual squamous cell carcinoma (patient 7). The bulk of the large mass of complex echotexture is between arrow heads. The dorsally displaced lateral aspects of the lingual parenchyma (T) and the acoustic shadows of the mandible (M) are shown.

FIG. 9. Sagittal sonogram of the root of a canine tongue with a lingual adenocarcinoma (patient 6). Shown are the large hypoechoic mass (m) and the normal lingual parenchyma (T). The strongly echogenic and irregular borders (arrow) were confirmed as ulcerated surfaces of the tumor.

212 SOLANO AND PENNINCK 1996

and easiest to use, even with animals under general anesthesia. However, the most rostra1 end of the tongue cannot be visualized using this approach, especially in horses, due to the narrow submental space just caudal to the mandibular symphysis, and the strong shadows generated by the mandibular body. Therefore, only the caudal half of the tongue can be evaluated ultrasonographically in horses.

Case History Reports

Foreign Body

The foreign body was diagnosed by the presence of a strong linear acoustic interface and the reverberation arti-

Precise and rapid localization of the metallic foreign body in the lingual parenchyma and identification of associated abscess formation was achieved by ultrasound examination. Furthermore we were able to guide the surgical dissection ultrasonographically, thereby reducing soft tissue trauma and surgery time. Interventional ultrasound played a pivotal role in the drainage of the abscesses, and was the method of choice for measuring the response to treatment after surgery.

Neoplasms

Ultrasonographic anatomy of the human tongue has been described21 and the technique has been validated as effective in detecting and staging neoplasm^.^^-^^ Ultrasono- graphic examination of the tongue may characterize tumors by revealing architecture, size and extension of a lesion.24 Even though the ultrasonographic characteristics of lingual tumors are not specific for tumor cell type, malignant and inflammatory lesions usually are hypoechoic and occasion- ally cystic. Hyperechoic lesions are most likely scar tissue.22 Descriptions of hyperechoic neoplasms were not found in the In the present series, one hyperechoic lesion was detected (patient 4), which was diagnosed as a squamous cell carcinoma; therefore definite diagnosis of lingual cancer should be obtained from biopsy.

Ultrasonographically the true extent of the lingual mass was apparent in each patient. In patients 2, 3 and 4, ultrasonography was useful in confirming that previously unde- tected portions of the tumors extended deep into the root of the tongue and in patient 5, lingual involvement by a sublingual mass was ruled-out.

These patients also illustrate the role of ultrasound de- ciding upon the most appropriate treatment. In patient 3, radiotherapy was the treatment of choice due to the diffuse

character of the lingual tumor. This form of examination may aid in choosing between euthanasia (patient 4) and surgical resection (patient 5).

The role of ultrasound in examination of the tongue is limited by protrusion of the lingual mass into the pharynx (patient 6). When this occurs the acoustic shadows generated by air in the pharynx may obscure portions of the mass.

Assessment of regional lymphadenopathy in animals with tongue tumors is routinely based on palpation which may explain the lower incidence of canine patients with detectable nodal metastasis at clinical presentation (1 2%) in com- parison with humans (60%). l 3 Ultrasonographic descriptions of the retropharyngeal and mandibular lymph nodes were considered beyond the scope of this paper due to their location outside the oropharyngeal cavity.2* However, due to the suitability of ultrasound for lymph node evaluation26 ultrasonographic assessment of regional lymphadenopathy should be performed to fully stage the lingual neoplasms.

In humans, lesions such as ulcers, located at the tip of the tongue or those involving the superficial layers often cannot be detected.21 In animals some lesions also may not be detectable due to their small size and proximity to the palate/air interfaces.

Another aspect of these lingual lesions not detectable on physical examination were the blood supply and interfaces with normal tissue. In patient 2, the risk of serious hemorrhage during surgical resection was predicted, based on vas- cularity of the lesion. The information obtained ultrasonographically also suggested that complete tumor resection would be difficult based on the ill-defined tumor borders. However, the extent and correlation between tumor borders as seen ultrasonographically and the actual tumor border seen histopathologically requires further study.

Ultrasonographic assessment of the response to treatment was possible by acquiring baseline information prior to ra- diation therapy in patients 3 and 7. Special attention was given to the echotexture size and extension of the lesions. In patient 3, no change in tumor size was measurable over 30 days of radiotherapy. In patient 7, a reduction in size of the mass was measured at the end of the eighth treatment. Therefore the potential to objectively assess response to therapy exists, if follow-up examinations are scheduled.

In summary, we have described the ultrasonographic anatomy of the oropharynx and provided preliminary information to assess the efficacy of ultrasonography in patents with lingual neoplasia and foreign bodies. Ultrasonography of the oropharynx accurately characterized lingual neoplasia and detected a foreign body with secondary abscess formation. Ultrasonography was effective in guiding surgical dissection to remove the foreign body and in intraoperative drainage of the abscesses. Ultrasonographic monitoring of the response to the treatment of lingual lesions may be beneficial in managing patients.

VOL. 37, No. 3 ULTRASONOGRAPHY OF THE TONGUE 21 3

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ultrasonography of the canine, feline and equine tongue: normal findings and case history reports

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