Diagnostic Value of Magnetic Resonance Imaging and Computed Tomography for Oral Masses in Dogs

INTRODUCTION Oral tumours are the 4th most common neoplasm in the dog, representing approximately 5–7 % of all tumours 5,7,22,24. The incidence of oral tumours is known to vary among breeds. Squamous cell carcinoma (SCC) and fibrosarcoma (FS) tend to occur in large breeds, whereas malignant melanoma occurs more commonly in heavily pigmented small breeds 22. The most common sites for neoplasia within the oropharynx in order of decreasing frequency are the gingival and dental alveoli, the tonsils, the lips and the buccal mucosa, the palate and the tongue 22. The term 'epulis' refers to any tumour or tumour-like lesion on the gingiva 20,21. Epulis is not a diagnosis in itself and its true nature must be determined histologically. A number of hisopathological entities can clinically present as an 'epulis', including all the malignant tumour types 20. Survey radiographs of oral masses in


INTRODUCTION
Oral tumours are the 4th most common neoplasm in the dog, representing approximately 5-7 % of all tumours 5,7,22,24 .The incidence of oral tumours is known to vary among breeds.Squamous cell carcinoma (SCC) and fibrosarcoma (FS) tend to occur in large breeds, whereas malignant melanoma occurs more commonly in heavily pigmented small breeds 22 .The most common sites for neoplasia within the oropharynx in order of decreasing frequency are the gingival and dental alveoli, the tonsils, the lips and the buccal mucosa, the palate and the tongue 22 .The term 'epulis' refers to any tumour or tumour-like lesion on the gingiva 20,21 .Epulis is not a diagnosis in itself and its true nature must be determined histologically.A number of hisopathological entities can clinically present as an 'epulis', including all the malignant tumour types 20 .
Survey radiographs of oral masses in dogs give limited information in that at least 40 % of the bone has to be eroded before radiographic changes are seen 24 .In addition, soft tissue swelling and margins cannot be clearly defined.Computed tomography (CT) has been generally used by the Dentistry Section of the Onderstepoort Veterinary Academic Hospital as an advanced imaging modality to further evaluate oral masses (90 % of which are tumours) in dogs.The soft-tissue margins of these masses were indistinct on CT images.Human literature 1,4,9,[10][11][12]15,16,18,19,25 suggests that magnetic resonance imaging (MRI) may be superior in assessing the extent and invasion of oral masses, in particular, oral tumours. The purpose ofthis study was to ascertain which of the 2 advanced imaging modalities, CT or MRI, would provide the most accurate information regarding margins and possible invasion of oral masses in dogs.This information is vital for the longterm prognosis, radiation and/or surgical planning and subsequent removal of oral masses.

MATERIALS AND METHODS
Nineteen dogs with oral masses were included in this study.The preliminary work-up consisted of a full clinical evaluation, macroscopic assessment of oral masses (describing size, shape and margination), palpation of regional and peripheral lymph nodes, left and right lateral recumbent thoracic radiographs 3 as a preliminary screening method for thoracic metastases, and blood urea nitrogen strip testing.The patients were then taken to a private human hospital for the MRI and CT examinations.General anaesthetic was given according to a previously described protocol 8 .Patients underwent MR examinations before the CT scans because MR artefacts were anticipated from the use of iodinated CT contrast media.The MR scanner was a 1.5Tesla Visart Toshiba unit.A head coil was used for the large dogs, an extremity coil for the smaller dogs.T2-weighted and pre-and post-contrast T1-weighted sequences were most commonly used and sequences were performed in sagittal, dorsal and transverse planes.The selected slice thickness was determined by the size of the mass in the particular patient, but the minimum slice thickness was 3 mm.For the post-contrast MR examinations, a gadolinium compound (Magnevist, Schering Plough), was injected intravenously by hand in a bolus at a dose of 1 m /5 kg and the post-contrast T1weighted sequence was acquired immediately.The entire MR-procedure lasted approximately 40-50 minutes.
Soft tissue and bone windows were obtained for the CT studies utilizing a helical 3rd generation Express-SX Toshiba CT unit.For the contrast studies, a nonionic, water-soluble contrast medium, iohexol (Omnipaque 300, Nycomed) was injected intravenously by hand in a bolus at a dose rate of 2 m /kg.Postcontrast images of the oral masses and of the thorax were obtained immediately following contrast injection.Soft tissue and bone windows were obtained.The entire CT procedure lasted approximately 10 minutes.Size, shape, margination, location of the oral masses and invasion of adjacent structures were assessed on pre-and post-contrast MR and CT images.The thorax was evaluated on CT images to exclude pulmonary metastases.All masses were biopsied and the tissue submitted for histopathological evaluation.

RESULTS
A summary of the findings of all the clinical cases is provided in Table 1.The female to male ratio was 10:9.The age varied from 1.5 to 13 years with a mean age of 8 years.The large breeds outnumbered the small breeds by 16 to 3. Eleven malignant and 10 non-malignant masses were diagnosed histopathologically.One patient (case no. 5) had 2 different histopathological types (focal fibrous hyperplasia and peripheral odontogenic fibroma) and another (case no.9) was initially diagnosed with focal fibrous hyperplasia which transformed into a leiomyosarcoma within 2 months.The most commonly occurring malignant tumour in this study was the osteosarcoma (5 cases) and the most common non-malignant mass was focal fibrous hyperplasia (5 cases).Five of the patients had malignant tumours that were so extensive and invasive that they were inoperable, but surgery was performed in 14 cases.Table 2 shows the comparison between of macroscopically-assessed size, shape and margination of the oral masses, and those on MR and CT examinations.MRI provided more accurate information regarding the size of the masses and invasion of adjacent structures, especially that of soft tissue (Fig. 1).Extension of the tumour within bone was also better seen on MR images (Fig. 2).Visualisation of the masses in 3 different planes on MR images facilitated tumour definition and delineation.Transverseonly CT images were reconstructed on 2 patients in an attempt to obtain a similar 3-dimensional view of the mass.The small size and sample volume of the respective masses resulted in poor 3D reconstruction in these cases.
An advantage CT had over MRI was that slice thickness could be reduced to 1 mm if tumours were very small, that is    5 mm or less.MR images obtained using slice thicknesses of less than 3 mm were grainy and of poor quality, even when, to compensate, acquisition time was lengthened.
Oral masses of the caudal mandible and maxilla that extended into the nasopharynx, nasal passages, or even brain, were better evaluated with MRI (Fig. 3a-d).Cortical bone erosion, a feature of infiltrative benign and some malignant oral masses and calcification within the mass were better seen on CT images (Fig. 1a).Peri-lesional oedema (often seen around aggressive lesions in the brain) was not a prominent feature of malignant oral tumours.
A single case of post-treatment osteosarcoma proved difficult to evaluate on MR images (Fig. 4a,b).Margins could not be accurately assessed due to the fact that adjacent granulation tissue and inflammation had the same signal intensity as the tumour.Disrupted bone was the main criterion used to distinguish tumour margins and therefore CT proved to be more helpful than MRI.The typical appearance of an osteosarcoma was of a very mottled, multiloculated type of mass, with intensely hyperintense, 'popcorn-like' pockets of fluid accumulation apparent on T2-weighted images.These pockets of fluid were thought to be due to haemorrhagic cysts that form as a result of the severe and aggressive bone destruction that takes place in this tumour type.
Contrast-MRI provided useful additional information in that margins were better defined and the pattern of enhancement could be used to further classify a lesion.No enhancement of the masses, however, could be detected on post-contrast CT images.

DISCUSSION
It appears that the most important diagnostic tool when evaluating oral masses is establishing the histopathological type.Once this information has been acquired, location of the oral mass is the 2nd most  relevant criterion.The advent of radical surgical techniques coupled with the use of radiation and/or chemotherapy has dramatically improved survival rate for dogs with oral tumours 6,13,17,23 .Masses of the rostral mandible do not require further diagnostic imaging techniques as far as surgical planning is concerned.Surgical margins are determined by the histopathological type and radical surgery should be performed on all malignant types.Should inoperable masses require radiation treatment, pre-and post-treatment CT images are advised.Magnetic resonance imaging appears to be too sensitive to inflammation and granulation tissue once treatment or surgery is performed and tumour margins cannot therefore be accurately assessed after treatment.The single case of post-treatment osteosarcoma (Fig. 4a) confirmed the difficulty in differentiating between original mass and granulation tissue on MR images due to the previously performed surgery.In this case, CT provided the necessary clarity (Fig. 4b).
Furthermore, the use of CT has a distinct advantage in anaesthetic risk patients.The entire CT examination is considerably shorter than the MR examination.
All masses were seen with both imaging modalities.However, as expected, the soft tissue margins were only clearly visible on MR images (Fig. 1a,b).Bone invasion could be seen with both imaging modalities, but the margination of the tumour within the bone was better seen on MR images, mainly because of the superior post-contrast studies and the fact that the tumour can be imaged using several primary acquisition planes.(Fig. 2a-c).
The reason why contrast CT was of such poor value was likely to be as a result of hand-administered intravenous injection as opposed to using a pressure-injector.Using the latter would have provided arterial, venous and parenchymatous phases of contrast uptake, but the method is rather costly and it was felt that such a study would go beyond the scope of trying to find the easiest and most effective imaging modality to assess oral masses.A separate study is needed to accurately assess post-contrast CT with pressure-injectors.Technical difficulties and cost may prove to be a major disadvantage compared with the ease of hand-administered intravenous bolus injection of MRI.Contrast MRI generally improved the definition of all the masses (Fig. 4) and the pattern of enhancement can assist in making a diagnosis (Fig. 5).However, contrast uptake in the nasal passages posed a slight problem when the tumour was situated adjacent to nasal turbinates, which normally show moderate enhancement 14 .It then became difficult to assess tumour margins accurately on post-contrast T 1 -weighted images.In these instances, T2-weighted images assisted in delineating these tumours (Fig. 6).
The appearance of the osteosarcoma on MR images was characteristic on T2-weighted images in the 5 cases in this series that these were diagnosed tentatively as such on MR alone (Figs 2 , 7).

CONCLUSION
In general, oral masses are better evaluated using MRI, once the histological type has been verified and if the mass is located in the caudal mandible, oropharynx and maxilla.Contrast administration is advised when using MRI.Owing to the short imaging time and the fact that general anaesthesia is not necessarily required, CT may be used in anaesthetic risk patients.When the tumour is of a very small size, CT may also be advantageous in producing thinner slice images.

Fig. 1 :
Fig. 1: a: A computed tomographic bone window image of patient 11.Although bone destruction and extension of the tumour into the R nasal passages is clearly seen, the soft tissue margins on the buccal aspect are not well defined.Note the intra-lesional calcification (arrow) not seen on MR image (1b).Diagnosis: squamous cell carcinoma.b: T2-weighted MR image of patient 11.Similar bone destruction and extension into the nasal cavity is seen but soft tissue margins are now clearly defined on the buccal aspect (short arrows).A 2nd tumour focus (long arrow) as well as hypostatic oedema (block arrow) of the opposite nasal passage could not be seen on CT images.

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Fig. 2: a: Computed tomographic soft tissue window image of patient 19.An expansile mass can be seen in the region of the caudal right mandible (arrows).Soft tissue margins are indistinct.Diagnosis: osteosarcoma.b: Patient 19.T2-weighted MR image of the same tumour slightly more caudally shows distinct soft tissue and bone margins.Compare with (c).c: T2-weighted image of the same tumour in the dorsal plane.Note how distinctive the margins of the rostral and caudal aspect of the mass are within the bone (arrows).

Fig. 3 :
Fig. 3: a: Computed tomographic bone window image of patient 15.An extensive soft tissue mass is evident on the dorsal and lateral aspect of the left maxilla, fairly caudally at the level of the nasopharyngeal opening (1) and the maxillary recess (arrow).Note that the soft tissue margins are poorly defined although grossly visible.Diagnosis: fibrosarcoma.b: Patient 15.T2-weighted image of the same tumour.The soft tissue margins are well defined and can be seen extending dorsally to the nasal bone and axially towards the midline of the hard palate (arrows).c: Patient 15.T1-weighted pre-contrast image in dorsal plane.Note that the caudal margin of the mass is poorly defined (arrow).Note, too, that the appearance of this tumour type differs greatly from the osteosarcoma (Figs 2, 4, 7); it is more hypointense, a feature of fibrous tissue on T1 and T2-weighted MR images.d: Patient 15.Compare the post-contrast image of the same slice as in (3c).The caudal margin of the tumour is better defined.Note the homogenous uptake of contrast by this tumour type.

0038- 2809 Fig. 4 :
Fig. 4: a.A transverse T2-weighted MR image of patient 2. The entire hyperintense region is abnormal.Previously performed surgery of the left maxillary region (arrow) made delineation of the tumour from granulation tissue impossible.Diagnosis: osteosarcoma.b: Patient 2. Computed tomographic image of the same tumour showed that the entire cranium is affected.Extensive bone destruction is evident.The surgical site can clearly be seen (arrow).

Fig. 5 :
Fig. 5: A post-contrast T1-weighted image of patient 18.A 'ring'-enhancement pattern (arrow) is seen in those conditions in which any form of capsule is present, as is the case with a pharyngeal mucocoele.This type of enhancement usually indicates a slow-growing, benign process.Diagnosis: pharyngeal mucocoele.

Fig. 6 :
Fig. 6: a: A pre-contrast T1-weighted image of patient 11 in the sagittal plane.The triangular mass is visible just caudal to the upper canine (small arrows).The dorsal and caudal margins of the mass are indistinct (block arrow).Diagnosis: squamous cell carcinoma.b: Patient 11.Post-contrast T1-weighted image of the same slice does not improve dorsal and caudal delineation of the mass.Notice the normal, moderate homogenous contrast uptake by the nasal turbinates.c: Patient 11.A transverse T2-weighted image of the same tumour clearly shows that there is no extension of the mass into the nasal turbinates (arrows).The mass is hypointense to the nasal turbinates on T2-weighted images.

Table 2 : Comparison of macroscopic assessment, CT and MRI with regards to size and margination of oral masses in dogs.
CASE NO.1915 × 20 mm hard ulcerative and sunken mass is seen on the buccal aspect of the R caudal mandible.Seems to involve bone, PM4, M1 and 2 absent.Expansile bone mass of 30 × 35 × 39 mm with poorly defined soft tissue margins.Cortical bone destruction visible dorsally on the lingual aspect of the mandible.32× 35 × 42 mm bone and soft tissue mass, heterogenous contrast uptake clearly defines the tumour borders within the bone, loss of teeth evident.Typical 'popcorn'-like appearance on T2-weighted images.