Multilobular tumor of bone arising from the palatomaxillary suture line in the skull of a dog

Abstract

A 6-year-old neutered male bloodhound dog was presented for surgical evaluation of an intraoral hard palate mass noted during a routine dental cleaning performed by the primary veterinarian. Computed tomography (CT) of the skull revealed a well-defined, multilobular, mineralized mass with a coarse, granular appearance, centered along the palatomaxillary suture extending into both the nasal and oral cavities. Bilateral caudal maxillectomy was performed for curative-intent resection of the tumor. The histopathology of the mass was consistent with a completely excised palatomaxillary multilobular tumor of bone (MLTB). This is apparently the 1st successful report of surgical excision of an MLTB associated with the palatomaxillary suture line.

Key clinical message:

Our findings emphasized that MLTB should be considered as a differential diagnosis for masses arising in the location of cranial sutures, and a definitive diagnosis can be made postoperatively with histopathology of the mass.

Multilobular tumor of bone (MLTB) is a rare, slowgrowing, malignant neoplasm (1–5). Various terms have been used for this tumor, including, but not limited to, multilobular osteochondrosarcoma, multilobular osteoma, multilobular chondroma, and multilobular osteosarcoma, although MLTB is preferred (1,3,4). Most cases occur in middle-aged, medium-to-large-breed dogs, but a few cases have been described in cats, 1 horse, and 1 guinea pig (6–9). This tumor type is known to involve the flat bones of the skull more commonly, though cases are reported involving the cranium, maxilla, mandible, orbit, tympanic bulla, hard palate, and os penis (1,3,4,10–13). To our knowledge, this is the 1st report of successful surgical excision of an MLTB arising from the palatomaxillary suture line in the skull of a dog.

Case description

A 6-year-old, neutered male bloodhound dog weighing 65.3 kg was presented to The Ohio State University Veterinary Medical Center for surgical removal of an intraoral hard palate mass that was identified during a routine dental prophylaxis 3 wk earlier. Following the dental procedure, the dog was referred to a local specialty practice for further diagnostic evaluation. There, computed tomography (CT) and incisional surgical biopsy were pursued. The CT of the skull, performed under general anesthesia, revealed a well-defined, multilobular, mineralized mass with a coarse, granular appearance, centered along the palatomaxillary suture involving the caudal maxillary and palatine bones, that was predominately right-sided (Figure 1 A, B, C). The mass bulged dorsally into the ventral nasal cavity and ventrally into the oral cavity, causing ventral and leftward displacement of the tongue, and measuring approximately 5 × 3.8 × 4.1 cm. The CT findings were suggestive of an MLTB arising from the hard palate. Initial pathology assessment of the incisional biopsy was suspicious for a peripheral odontogenic fibroma due to the observed extensive regions of ossification. Given this discrepancy, a 2nd opinion was sought and, by combining information about the location, the symmetry of the multinodular mass on the suture line, and the compact nodular aggregates identified with histopathology, a diagnosis of MLTB was made.

Figure 1.

Transverse (A), dorsal reformat (B), and sagittal reformat (C) plane computed tomography (CT) images of the hard palate mass in a 6-year-old male bloodhound dog. The mass is predominantly mineral attenuating, is well-defined with multilobular margins, and has a centrally coarse granular appearance. The mass extends across the palatomaxillary suture, involving the caudal maxillary and palatine bones. Window width and window level were adjusted to 2500/250 (bone window), the slice thickness was 1.25 mm, and the image was acquired with 120 kVp.

The dog was referred to a tertiary hospital for surgical resection of the mass by a surgical oncologist. With the dog sedated, oral examination revealed a 5- × 4-centimeter, firm, pigmented and ulcerated mass arising from the right side of the hard palate and crossing midline. Complete blood cell count and serum biochemistry findings were unremarkable. There was no evidence of pulmonary metastatic disease on 3-view thoracic radiographs.

On the following day, the dog underwent surgery for removal of the suspected MLTB. The dog’s blood type, DEA 1.1 positive, was determined before surgery. The dog was placed under general anesthesia and positioned in dorsal recumbency, and a bilateral caudal maxillectomy was performed as described (14). During the bilateral caudal maxillectomy, the mucosal surface overlying the mass was noted to have numerous, well-demarcated, pale tan ulcerations (Figure 2 A, B). A minimum of 1.5 cm of grossly normal tissue was marked as the surgical margin around the mass for the planned resection. Bilateral buccal mucosal incisions were made rostral to the second premolars and extended dorsocaudally. Bilateral buccal mucosal flaps were elevated to form a bipedicle buccal flap to facilitate a tension-free closure over the defect.

Figure 2.

A — Gross specimen of the bloodhound dog’s tumor following bilateral caudal maxillectomy. B — Gross specimen of the dog’s tumor following bilateral caudal maxillectomy, highlighting the tumor’s local invasion into the dorsal nasal cavity. C — Photomicrograph of the multilobular tumor of bone (MLTB) arising from the palatomaxillary suture line. The mass consists of multiple osteochondral islands. Hematoxylin and eosin, 40× magnification. D — Higher-magnification view of the MLTB. The osteochondral islands are separated by fibrous septa. Hematoxylin and eosin, 100× magnification.

During surgery, blood loss resulted in hypotension that warranted transfusion of a single unit of packed red blood cells. Recovery was uneventful and, after inking the surgical margins, the entire caudal maxilla was submitted for histopathology. The dog was started on ampicillin-sulbactam, 30 mg/kg BW, IV, q8h intraoperatively and continued until the time of discharge. In hospital, the dog was maintained on fentanyl, 2 μg/kg per h BW, IV, CRI; dexmedetomidine, 0.25 mg/kg per h BW, IV, CRI; aminocaproic acid, 15 mg/kg per h BW, IV; and carprofen, 2.2 mg/kg BW, SC, q12h. Discharge from the hospital occurred 3 d after the procedure with amoxicillin-clavulanate, 14.4 mg/kg BW, PO, q12h, as an antibiotic; carprofen, 2.2 mg/kg BW, PO, q12h, as an anti-inflammatory and analgesic; capromorelin oral solution (Entyce; MWI, Boise, Idaho, USA), 3 mg/kg BW, PO, q24h, as an appetite stimulant; and trazodone, 300 mg, PO, q12h, as an anxiolytic.

Two weeks after the maxillectomy, the dog was re-examined at the local specialty practice for halitosis and mucopurulent nasal discharge. Following sedation, an oral examination was done, and 2 areas of dehiscence were identified at the rostral and caudal folds of the buccal flap. Oral antibiotic therapy was initiated, and the dog was transferred to The Ohio State University Veterinary Medical Center for a revision surgery. The area of dehiscence was revised by creating and elevating bilateral gingival flaps, rostrally and caudally to the defect, as described (15). Recovery was uneventful, and the dog was discharged the following morning with clindamycin, 5 mg/kg BW, PO, q12h, as an antibiotic; carprofen, 2.2 mg/kg BW, PO, q12h, as an anti-inflammatory and analgesic; and trazodone, 300 mg, PO, q12h, as an anxiolytic.

Histological examination of the mass revealed mature and remodeled osseous tissue with abundant, well-differentiated osteoblasts separated by fine, loose fibrous stroma and several bony nodules bordered by thin fibrous septa (Figure 2 C, D). The mass was compressing, but not invading, the adjacent soft tissue (respiratory epithelium dorsally and oral collagen and mucosa ventrally). Microscopically, no characteristics of aggressive behavior were identified. The palatomaxillary suture line tumor was suspected to have been completely removed based on histological analysis.

The patient is reportedly doing well 4 mo following the initial surgery. Recheck CT performed at the local specialty center 4 mo postoperatively revealed no evidence of tumor regrowth.

Discussion

This paper describes an MLTB arising from the palatomaxillary suture line in the skull of a dog. Palatomaxillary suture line tumors are relatively uncommon bone tumors in the dog; however, they are more common than those that arise from the palatoincisive suture line (1,16). Most bone tumors arising from the suture line of the palate do not form discrete multilobular patterns as MLTBs do and have fewer cartilaginous elements (1,16,17). To our knowledge, similar skull or palatal lesions have not been previously described in the human literature.

The dog presented herein was 6 y old at the time of diagnosis, which is between previously reported age ranges (3,4). The dog in this case was not exhibiting clinical signs of the tumor, and the tumor was identified during a routine dental prophylaxis. Typically, dogs with MLTBs are presented for examination following the identification of a palpable, firm mass arising from the surface of the skull (1). Alternatively, a dog may be presented following the loss of function of a structure that the mass is compressing with its growth (1). It is unknown when the dog in this case report would have become clinical for the mass because MLTB is characteristically a slow-growing tumor and dogs can remain asymptomatic for up to 1 y, even with metastatic pulmonary disease (1,18).

Advanced imaging such as CT can be extremely helpful, as it was in this case, for identifying the bone of origin and for surgical planning of the resection margins (3,4,10). The characteristic CT appearance of an MLTB is a coarsely granular, non-homogenous mass with mineral attenuation and well-defined margins, sometimes referred to as a “popcorn ball” appearance (10,12). When the original histopathological diagnosis of the dog’s tumor was odontogenic in origin, the tumor characteristics on CT, including its symmetry over the suture line and well-defined borders, helped encourage a 2nd histopathological assessment. Peripheral osteogenic fibroma, the diagnosis of the 1st incisional biopsy, has not been reported to occur in a suture line. A definitive diagnosis for MLTB can only be obtained via histopathology and the identification of compact nodular aggregates (1,12,19).

Other tumor types considered when evaluating a tumor originating from the palate are osteosarcoma and osteoma (17). Histologically, MLTBs exhibit the characteristic pattern of lobules bordered by thin septa of spindle cell mesenchyme and fibrous connective tissue (1,2,16). These septa are involuted, thin fibrovascular membranes proposed to arise from disturbed periosteal linings of adjacent intramembranous bone plates that form the sutures of the palate bones (1,16). Their lobules are characterized as cartilaginous, osseous, or osteocartilaginous islands (2). As was exhibited in the present case, the multinodular, compact aggregates seen on histopathology are diagnostic for an MLTB and not another tumor type (17). Microscopic indicators of malignant behavior in an MLTB include mitotic activity, loss of lobular architecture, necrosis, hemorrhage, and overgrowth of mesenchymal elements (1). Mitotic figures are uncommon in most cases, and when they are present, they undoubtedly signify metastatic potential (1). The tumor in this case exhibited none of these aggressive features, and none of the bone-forming cells demonstrated mitotic figures; therefore, other tumor types were excluded from consideration. Surgical resection could provide long-term local control or cure for this dog as no malignant progression was exhibited in the specimen (16). Ultimately, none of the differential diagnoses considered have been reported to occur in the suture lines of the palate or skull, and the tumor in this case was located in the palatomaxillary suture line (1).

Cranial sutures are fibrous joints formed from the union of 2 skull plates (16,20). Cranial suture lines are formed during embryonic development and function as intramembranous bone growth sites (21). To accomplish this intent, the mesenchymal-derived stem cells of the suture line produce new bone cells at the edges of overlapping bone fronts while remaining unossified and undifferentiated themselves (21). This cell production only occurs following an external stimulus, most commonly brain expansion (21). The histogenesis of MLTBs is unknown, but it has been proposed that they are derived from altered periosteal elements of membranous bones such as chondrocranium and viscerocranium (1,11,17). The multilobular pattern is attributable to the abnormal cellular activity arising from the periosteum of bones formed by intramembranous ossification (1,4). In the present case, the MLTB was diagnostically evaluated as straddling the palatomaxillary suture line. Based on general MLTB pathogenesis conjecture and the specific location of the tumor in this dog, we suspect that the tumor arose directly from a disturbance of the palatomaxillary suture line of the skull plate. It has been reported that non-brachycephalic breeds have delayed suture line closure rates compared to brachycephalic breeds, allowing for transformation of inactive suture line cells (20). When an external stimulus such as a trauma occurs, it is possible that the normally inactive mesenchymal-derived stomal cells become activated, but without a genetic program, allowing the uncontrollable growth of cells (21). While no history of a traumatic event was reported in the dog from this report, a fall or high-impact trauma cannot be ruled out since the dog was not always supervised. Additional case reports involving MLTBs at skull suture lines are necessary to establish a formal pathogenesis (1). CVJ