Magnetic resonance imaging of a solid, multilobular ameloblastoma in the mandible of a pony

Authors


Summary

This report describes a multilobular ameloblastoma that invaded the left mandible of a 31-year-old pony. The pony presented initially with a palpable mass that protruded from the left mandibular region. Ante mortem radiographs of the mass revealed an invasive, multilobular, bony mass with significant loss of dentition. One month following initial diagnostic work-up, the pony was subjected to euthanasia due to unrelated clinical signs of colic, secondary to a strangulating lipoma. Magnetic resonance imaging (MRI) of the head was performed post mortem to further characterise the mass and determine the extent of its invasion. The macroscopic and histopathological morphology and immunohistochemical properties of the neoplastic cells strongly supported a diagnosis of a multi-cystic ameloblastoma. To the authors' knowledge, this is the first report of an MRI of an ameloblastoma in the horse.

Introduction

Ameloblastomas are sporadic, odontogenic tumours of vertebrates which occur rarely in horses. Their behaviour is typically described as benign but locally invasive. These tumours are composed of epithelial neoplastic cells that do not induce production of enamel as they would in normal tooth formation (Gardner 1994). Ameloblastomas typically affect horses older than 10 years of age; however, they have been reported in a wide age range (Kutzler et al. 2007). No predisposing factors for growth of ameloblastomas have been identified (Gardner 1994). Clinical signs may include a slow growing mass protruding externally on the face or into the oral cavity, typically firm and nonpainful on palpation. Ameloblastomas have a predilection for the caudal aspect of the mandible and often involve the cheek teeth (Kutzler et al. 2007). Affected horses may exhibit weight loss, anorexia, halitosis and buccal ulceration as well as difficulty in prehension and mastication. Radiographic characteristics may be suggestive of an odontogenic tumour but are not considered to be pathognomonic for ameloblastomas. These radiographic features may include a cystic mass invading the mandible and, occasionally, radiographic evidence of dystrophic mineralisation may be present (Kutzler et al. 2007).

Histopathology is useful to rule out other types of odontogenic tumours such as complex or compound odontomas, ameloblastic odontomas, ameloblastic carcinomas and ameloblastic fibromas. There is increasing literature in human medicine on the use of MRI and computed tomography (CT) to help differentiate odontogenic tumours from each other and from other differential diagnoses such as osteosarcomas, dentigerous cysts, keratocysts and aneurysmal bone cysts (Leckie et al. 1993; Thompson et al. 1996; Cihangiroglu et al. 2002; Konouchi et al. 2006; Devenney-Cakir et al. 2010). Additionally, CT imaging of ameloblastomas in camelids have previously been described (Step et al. 2003; Britt et al. 2005) as well as CT and MRI images of an ameloblastoma in a dog (Kafka et al. 2004). Treatment and prognosis depend on the extent of invasiveness, as well as the ability to obtain complete surgical excision. This report describes the clinical presentation of a multilobular ameloblastoma and first reported use of MRI to evaluate the extent of the tumour and assist in diagnosis in the horse.

Case history

A 31-year-old, Pony of the Americas, gelding was presented to the University of Pennsylvania, New Bolton Center Field Service, for a solid mass, approximately 10 cm in diameter, on the left caudal mandibular region of undetermined duration. The owner had not observed the pony to have any masticatory problems, dysphagia or anorexia.

Clinical findings

The gelding was bright, alert and responsive but thin, with a body condition score of 4/9 on the Henneke scale. All vital parameters were within normal limits and no other abnormalities were noted on physical examination. A well demarcated, 10 cm in diameter, mass was firm on external palpation, mildly painful and closely adhered to underlying structures. The mass was lateral and caudal to adjacent mandibular molars 310 and 311. On examination of the oral cavity, a significant number of teeth were missing: right maxillary premolar 108, molars 109, 110 and 111 and right mandibular premolars 406 and 407. Premolar 206 was the only remaining tooth in the left maxillary arcade. The loss of the other teeth in this arcade was suspected to be due to normal senile attrition. All teeth in the left mandibular arcade, in close proximity to the mass, were present on examination of the oral cavity. Food had accumulated in the left side of the mouth where numerous maxillary cheek teeth were missing. No halitosis, oral ulceration or obvious submucosal protrusion of the mass into the oral cavity was noted. Complete blood count and chemistry panel were all within normal limits. The owner elected a trial period of conservative treatment. Oral phenylbutazone (Bute Boluses)1 (2.2 mg/kg bwt per os s.i.d.) was administered for one week.

Further diagnostics were pursued upon determination that there was no change to the mass with conservative treatment. Skull radiographs were performed which included the dorsoventral and oblique views of the mandible. These views demonstrated a multiloculated, expansile mass of the caudal body of the left mandible with a thin osseous rim and septa bordering a central radiolucent region (Fig  1). The mass was centred on molar 308 with periapical lysis surrounding all of the molars and moderate overlying ventrolateral soft tissue swelling. Differential diagnoses for the mass included odontogenic tumours (ameloblastoma, ameloblastic odontoma and ameloblastic carcinoma) odontogenic cyst, ossifying fibroma, aneurysmal bone cyst and malignant neoplasia (osteosarcoma, myxomatous tumours and invasive squamous cell carcinoma) (De Cock et al. 2003; Gibbs 2005; Knottenbelt and Kelly 2005). Biopsy tissue samples were obtained with a bone marrow biopsy needle (TrapLok)2 and submitted for histopathological examination. A tentative diagnosis of an odontogenic tumour was made due to the radiographic and histological appearances. Further classification was not possible due to the small tissue sample size.

Figure 1.

Oblique radiograph of the left mandible with a multiloculated expansile mass (white arrows), associated soft tissue swelling and apical lysis (white arrowhead) surrounding the molars.

Post mortem findings

Magnetic resonance imaging

One month later, the pony displayed signs of colic due to a strangulating lipoma diagnosed on post mortem examination. Colic signs had been unresponsive to treatment with analgesics and the pony was subjected to euthanasia with sodium pentobarbital (Euthasol)3 (90 mg/kg bwt i.v.). An MRI was performed post mortem on the head at the University of Pennsylvania, New Bolton Center, George D. Widener Hospital with the pony in right lateral recumbency using a 0.25 Tesla low-field magnet4. Dorsal, sagittal and transverse T1, T2 spin echo and STIR images were obtained with a 4 mm slice thickness and 0.4 mm slice gap. Magnetic resonance images demonstrated a multilobular, expansile mass erupting from the lateral, caudal body of the left mandible and extending rostrally within the medullary cavity to the level of the premolar 308 (Fig  2). There was thinning to complete destruction of the overlying cortical bone laterally and a focal area of cortical thinning medially. The mass was isointense to surrounding muscle on T1-weighted images (Fig  3) and heterogeneously hyperintense on T2-weighted and STIR images. A thin hypointense rim surrounded the mass in all sequences and contained multifocal small T2 hyperintense cystic regions (Fig  4). The overlying masseter muscle was compressed and displaced laterally with hyperintense regions on T2-weighted and STIR images. Magnetic resonance imaging findings were most consistent with a neoplastic process and suggestive of a tumour of odontogenic origin.

Figure 2.

Dorsal T2-weighted spin echo MR image through the body of the left and right mandibles: left is to the right and rostral to the bottom. There is a multilobular expansile mass (white arrowheads) extending to the level of premolar 308 with heterogeneous hyperintense signal intensity compared to the adjacent muscle. The mass is associated with the left mandibular molars. Note the cystic fluid region demarcated by the black arrow.

Figure 3.

Transverse T1-weighted MR image: left is on the right and ventral is on bottom, showing mass (white arrow) isointense to surrounding muscle.

Figure 4.

Transverse T2-weighted spin echo MR image: left is on the right and ventral is on the bottom. The mass is characterised by high signal intensity in the cystic regions of the mass (white arrows). Bony septa are present in the mass (black arrow).

Histopathology

Grossly, the mass was characterised by a 10 cm in diameter, smooth, ovoid tumour, lined by a variably thick osseous capsule of pre-existing bone (Fig  5). The mass protruded from the caudal left mandible compressing the surrounding skeletal muscle and was moderately firm with a reddish core (Fig  6). Histologically, the neoplasm was comprised of ribbons and cords of polygonal cells and bundles of spindle to stellate cells. Palisading along the basement membrane and apical polarisation of nuclei was particularly evident within slender dissecting cords of neoplasm. Within the centres of prominent cords there were polygonal to slightly elongate cells with intercellular bridges, typical of stellate reticulum. Mitotic figures were rare. The stroma was fibrovascular with dense multifocal areas of collagen accumulation (Figs  7-9). Immunohistochemical evaluation revealed intracytoplasmic cytokeratin AE1 and AE3 (epithelial markers) expression within neoplastic cells (Fig  10). Vimentin V9 (mesenchymal marker) expression was largely relegated to the mesenchymal stroma but also involved some fusiform and stellate neoplastic cells. The morphology and immunohistochemical distribution indicated the presence of an ameloblastoma. Evaluation of all other organs on post mortem examination revealed no evidence of metastasis.

Figure 5.

Gross examination of the lateral aspect of the mass which measured approximately 10 cm in diameter.

Figure 6.

Gross examination of the cut surface of the mass.

Figure 7.

Mandible. The pre-existing and reactive woven bone (B) is compressed, replaced and effaced by thick anastomosing cords of neoplastic cells (C) interpreted to be of neoplastic origin. H&E ×10.

Figure 8.

Ameloblastic thin epithelial cords separated by homogeneous matrix. H&E ×40.

Figure 9.

Dense aggregation of ameloblastic polygonal epithelial cells with mitotic figures (white arrows). H&E ×40.

Figure 10.

Ameloblastic epithelial cells expressing intracytoplasmic cytokeratins AE1 and AE3. Indirect immunohistochemistry and H&E×20.

Discussion

Ameloblastomas in the horse have rarely been reported in the veterinary literature. Mandibular swellings in horses are most commonly associated with dental disease or trauma. Only a small percentage are neoplastic and an even smaller number are due to ameloblastomas (Pirie and Dixon 1993). Review of the literature revealed 14 cases of mandibular ameloblastoma in equines (Kutzler et al. 2007; Snyder et al. 2008), while a concurrent review of odontogenic tumours in general revealed 22 cases (Hackett and Baxter 2008). In a review of hospital records at the George D. Widener Hospital at the University of Pennsylvania, New Bolton Center, from 1995 to 2009, only 3 out of 13 odontogenic tumour biopsy cases were reported as ameloblastomas, including this case.

In man, ameloblastomas comprise 1% of all cysts and tumours of the oral and maxillomandibular region and 10% of all odontogenic tumours of the mandible (Sham et al. 2009). As in horses, peak incidence has been noted in mature to older humans between 30 and 60 years old (Gardner et al. 2005; Sham et al. 2009). Ameloblastomas are often asymptomatic in both equine and human patients (Sham et al. 2009; Bisinelli et al. 2010). Untreated tumours can become quite large and cause facial deformity and impair function (Sham et al. 2009; Bisinelli et al. 2010). Ameloblastomas rarely exhibit metastatic properties, although the terms metastatic ameloblastoma (ameloblastoma with simultaneous metastatic growth) and ameloblastic carcinoma (evidence of malignancy within the primary tumour, regardless of whether or not there is metastasis) have been coined in associated case reports (Slootweg and Muller 1984; De Cock et al. 2003). An ameloblastic carcinoma has previously been identified in one horse (De Cock et al. 2003).

Histological examination is needed for diagnostic confirmation of ameloblastomas. Four forms of ameloblastomas in man have been described based on clinical behaviour, anatomic location, radiological and histological characteristics: solid/multicystic, unicystic, desmoplastic and extraosseous/peripheral. The solid/multicystic form is the most common and found to represent 85% of all ameloblastomas. This form has a propensity to be more aggressive with a high incidence of recurrence in comparison with the other 3 forms (Gardner et al. 2005). The unicystic form often is seen as a cystic, radiolucent region that surrounds the crown of a tooth that has not yet erupted and may be mistaken for a dentigerous cyst (Gardner et al. 2005). This variant comprises a single cystic cavity lined by nondescript epithelium and may also display luminal proliferation of epithelial cells or mural infiltration of the cyst wall. The desmoplastic form has a mottled, mixed radiolucent radiographic appearance with diffuse margins. Adjacent tooth roots often become involved and are resorbed. Extraosseous/peripheral ameloblastomas are soft tissue ameloblastomas of mucosal or gingival origin over tooth bearing parts of the jaw and histologically identical to intraosseous ameloblastomas (Gardner et al. 2005).

To the authors' knowledge, there is no report in the literature describing the MRI or CT appearance of an ameloblastoma in a horse. The MRI images of this case study are consistent with MRI findings of ameloblastomas in the human literature including intermediate signal intensity on T1-weighted images and high signal intensity on T2-weighted images. Magnetic resonance imaging can help aid in the diagnosis of ameloblastomas in man due to characteristic findings: 1) on T1-weighted images, ameloblastomas have a predilection for intermediate signal intensity, 2) signal intensity on T2 or STIR images is often high with enhancement in the solid portions and 3) ameloblastomas with multiple cystic portions show intermediate signal intensity in the T1-weighted images and high signal intensities on the T2-weighted images (Asaumi et al. 2002, 2005; Hisatomi et al. 2011). Magnetic resonance imaging has proven to be superior to CT when assessing soft tissue contrast and has the advantage of the ability to acquire multiplanar images (Asaumi et al. 2005). Magnetic resonance imaging can also provide additional information regarding the solidity, extension within the medullary cavity and aggressive nature of the tumour (Minami et al. 1992). Although i.v. contrast was not used in this case due to post mortem imaging, gadolinium-enhanced images have been used successfully in human medicine to further identify solid components of the tumour.

Surgical treatment was declined at the time of the original work-up of the tumour and would likely have been difficult given the extensive nature of the mass demonstrated on MRI (Figs 2-4). There are few reports of equine ameloblastoma treatments previously reported in the veterinary literature. Dixon et al. reported surgical removal of 2 ameloblastomas. One recurred in 2 months and the horse was subsequently subjected to euthanasia. The other showed no signs of recurrence in 4 years (Dixon et al. 2000). Treatment has remained a challenge in man to incorporate both adequate resection of the tumour as well as maintain acceptable facial aesthetic appearance and function. Without adequate resection, high rates of tumour recurrence have been found. Segmental mandibulectomy ± radiation therapy and facial reconstruction is the treatment of choice at this time for multicystic ameloblastomas (Bisinelli et al. 2010; Koukourakis et al. 2011).

Magnetic resonance imaging may be useful in the future to aid in diagnosing ameloblastomas and differentiating this type of tumour from other odontogenic tumours in the horse. Magnetic resonance imaging can determine the invasiveness of the lesion and extent of destruction prior to surgical excision to aid in prognosticating.

Manufacturers' addresses

  1. 1

    Vedco, St Joseph's, Missouri, USA.

  2. 2

    Medical Device Technologies, Inc., Gainesville, Florida, USA.

  3. 3

    Virbac AH, Fort Worth, Texas, USA.

  4. 4

    Siemens, Washington DC, USA.

Ancillary