Abstract
This study reviews rim excision as a treatment for canine acanthomatous ameloblastomas (CAA) in dogs with <3 mm of bone involvement. Removal of a canine tooth was involved in 47% of the cases; 33% cases involved the caudal dentition. Follow-up ranged from 3 months to 5 years. No evidence of recurrence was seen. Client satisfaction with cosmesis and the animal’s ability to masticate was judged to be good. With appropriate case selection, rim excision appears to be a viable option for CAA and results in improved dental occlusion, cosmesis, and no evidence of epulis recurrence.
Introduction
Canine acanthomatous ameloblastoma (CAA) is characterized as a benign odontogenic tumor or epulis. The prevalence of epulides, including CAA, is not known. Routine histopathology of excised gingival masses is not always performed, which may skew the reported prevalence of CAA.1 In one clinicopathological study of canine epulides, acanthomatous epulides were reported to make up 18% of benign oral tumors. Yoshida et al found that on histopathological analysis, acanthomatous epulides had a marked invasion of the epithelium and recurrence after marginal excision. Moderate local invasion of the bone and induction of the periodontal ligament were seen, which differed from other epulides.2
Canine acanthomatous ameloblastoma has undergone numerous terminology changes as the histopathological studies of oral tumors have redefined and reclassified epulides. In 1993, Gardner and Baker suggested that acanthomatous epulides were a type of ameloblastoma that developed from the gingival epithelium (peripheral) or from the alveolar bone (intraosseous).3 Further study comparing these canine epulides to those seen in humans found numerous similarities between the canine acanthomatous epulis and the human interosseous ameloblastoma.
Treatment of CAAs has evolved as more information regarding the nature of these oral tumors has been amassed. The difference in this benign soft tissue tumor compared to other odontogenic tumors is that it is locally invasive and has a high rate of recurrence following marginal resection.4 In the dog, CAAs have never been reported to metastasize.5 Besides surgical intervention, irradiation and intralesional bleomycin have been used with varying success.6
Currently the recommended treatment for CAA is radical surgical resection based on the site of the tumor (i.e., mandibulectomy or maxillectomy in the region of the tumor).1,4,7 No incidence has been reported of recurrence of CAA after radical surgical resection of the affected area. Nonetheless, veterinary textbooks do mention another possible surgical procedure for benign masses: the rim excision or alveolar ridge resection. With rim excision, the ventral cortical bone of the mandible or the most dorsal portion of the maxillary or incisor bone remains intact1,8 while the tumor, surrounding teeth, and periodontal structures are removed. The advantages of rim excision over complete resection of the mandible include continuity of the jaw, decreased to absent mandibular drift, and improved dental occlusion.8 To our knowledge, the use of rim excision for CAA has not been reported in the veterinary literature. The goal of this study was to review the use of rim excision for the treatment of CAAs. It was hypothesized that with appropriate case selection, rim excision will prove curative, will bring an excellent return to function, and provide satisfactory cosmesis in the opinion of the clients.
Materials and Methods
Medical Records Review
The computerized records system was searched for maxillectomies and mandibulectomies performed at Veterinary Surgical Associates (VSA) from 2000 through 2007. Cases were included if the dog was diagnosed with an acanthomatous epulis or acanthomatous ameloblastoma. The remaining cases in which surgery was performed for neoplasia or fractures were excluded. The surgical reports were reviewed, and only dogs that underwent rim excision were included.
Criteria for rim excision included a gingival mass <2 cm in the largest dimension and <3 mm (approximately) of bone involvement adjacent to the tooth root (based on available dental radiographs). If the mass had been previously removed by the referring veterinarian, the gingival scar was used to determine the extent of previous excision and the width of margins of the rim excision.
Medical records of VSA were reviewed for signalment, location of the mass, surgical procedure, complications, and biopsy results. In addition to VSA records, follow-up after surgery was obtained from the referring veterinarians’ records. These records were reviewed for postoperative complications, recurrence of the mass, additional oral masses, or oral disease. When possible, clients were contacted during manuscript preparation, to determine if postoperative tumor development reoccurred. Clients were also questioned about their satisfaction with the procedure, their perception of cosmesis, and their dog’s prehension and mastication abilities.
Surgical Techniques
General anesthesia and perioperative pain medication were utilized in all cases, but protocol varied by surgeon preference. For mandibular CAAs, an incision was made through the gingiva encircling the mass and grossly involved dentition. A sagittal saw was used to cut the alveolar bone rostral, caudal, and ventral to the tooth roots, leaving the ventral mandible intact. A high-speed burr was used to remove any remaining tooth roots and periodontal ligament. Care was taken to remain dorsal to the mandibular artery and vein. Deep tissues and gingiva were closed using absorbable suture in a combination of suture patterns according to surgeon preference. In general, deep tissues were closed in a simple continuous pattern, and the mucosa was closed with a cruciate or simple interrupted suture pattern.
An osteotome was used to perform the rim excisions in the maxilla. When mild hemorrhage was encountered during maxillary rim excision, hemoclips were used for hemostasis. A high-speed burr smoothed bone edges and removed any remaining periodontal ligament. A buccal mucosal flap was elevated from the maxillary lip to close the defect.
Results
Case Selection
A total of 13 dogs were identified that had histopathological diagnosis of acanthomatous epulis/ameloblastoma and rim excision as the method of surgical removal. One additional dog (case no. 6) was reported as a “well-differentiated collagenous stromal proliferation” and was included in this study. One dog (case no. 8) had rim excision performed at two separate locations. At 9 years of age, the dog originally had a rim excision centered on the mandibular right third premolar for an acanthomatous ameloblastoma. This dog was presented the following year for evaluation of an acanthomatous ameloblastoma at the base of the first right mandibular premolar. Mandibular computed tomography (CT) identified the mass involving the tooth root of the right first mandibular premolar with close association to the second premolar and canine tooth root. No evidence of involvement with the previous resection was noted. Both tumors and results were included in the study as individual cases (case nos. 8, 9). Therefore, in total, this retrospective study included 14 dogs and 15 surgical procedures (cases) [see Table⇓].
Clinical Data on 15 Cases of Rim Excision for Canine Acanthomatous Ameloblastoma
Due to the nature of this technique (i.e., the use of a burr), the surgical margins could not be accurately determined and were not available for histopathological review. Therefore, while histopathology was used to confirm the diagnosis of CAA, margins cannot be adequately evaluated to confirm removal of all microscopic disease.
Mean age for dogs at the time of surgery was 8.6 years (range 3 to 11 years). Thirteen (86.7%) of the 15 cases were ≥6 years of age at time of surgery. The remaining two cases were 3 and 5 years of age, respectively. Seven (50%) dogs were neutered males. One (7%) dog was an intact male, and six (42.8%) dogs were spayed females. The male to female ratio was 1.3.
Location of the Mass
Twelve cases involved mandibular rim excision. Distributions of right- and left-sided masses involving the mandible were 50% right-sided (six of 12) and 42% left-sided (five of 12); one (6%) mass was centralized at the left and right first and second incisors. Forty-seven percent (seven out of 15) of the cases involved the removal of a canine tooth. Thirty-three percent (five out of 15) involved the caudal premolars or molars. Incisor teeth were removed without removal of a canine tooth in 20% (three out of 15) of the cases. Three cases involved maxillary rim excision. One was centered on the right maxillary incisors, one was on the left incisors, and the third involved the left maxillary canine to the third premolar.
Previous Medical History
Seven cases had previous marginal excision at the referring veterinary hospital, and either the mass had recurred or incomplete excision was noted by histopathology. These dogs were then referred for more aggressive surgery. For the remaining cases, the referring veterinarians had a suspicion of CAA based on oral examination and, in some cases, dental radiography.
Complications of the Procedure
No intraoperative or perioperative complications were noted in the medical records of any of the 15 cases. Approximately 3 months after rim excision, one client noted a mass on the ventral aspect of the mandible in the area of the surgery (case no. 11). Oral examination revealed no further abnormalities. Mandibular radiographs were obtained that showed ventral callus formation at the junction of the caudal surgical site and normal jaw. A small fracture was noted as well [see Figure⇓]. We suspect that the fracture was secondary to stress riser formation between jaw and surgical site because of the dramatic change in mandibular height at that location. The mandible was palpably stable and non-painful, and the client reported no difficulty during the dog’s mastication. No treatment was instituted. The radiographs also did not show any changes to the bone rostral or caudal to the surgical site that would indicate continued disease process.
Lateral skull radiograph of case no. 11. Note the ventral mandibular cortical thickening at the site of and caudal to the rim excision.
Postoperative Follow-up
As indicated in the Table⇑, owners from nine of the 15 cases were available for a follow-up telephone consultation during the preparation of this manuscript. Four dogs had been euthanized for diseases unrelated to this study. The follow-up period for these phone conversations ranged from 7 months to 3.5 years. All nine of the clients available reported no regrowth of the mass. All nine clients were satisfied with the surgical outcome and their dog’s ability to masticate and prehend food and toys. Three clients reported that their dogs chewed hard toys, balls, and bones on the contralateral side or didn’t chew as vigorously as previous to surgery. No client noted any problems with chewing kibble on the surgical side. No client expressed dissatisfaction with the cosmesis. Many clients reported that without an oral examination, they could not tell where surgery was performed. The follow-up examinations at VSA or the referring veterinarian’s ranged from 3 months to 5 years. No evidence of regrowth was seen on physical examinations.
Discussion
Classifications of ameloblastomas have been debated in both the human and veterinary literature. These tumors have been defined as benign, locally invasive, clinically malignant, and malignant.9 Metastasis has never been documented in dogs; however, in humans, malignant ameloblastomas and ameloblastic carcinomas have been noted to metastasize to the lungs, pleura, orbit, skull, and brain.10 In human ameloblastomas, histopathological categories include plexiform, unicystic, acanthomatous, granular, and follicular. A highly significant association has been seen between category of human ameloblastomas and recurrence. Follicular, granular cell, and acanthomatous types have a higher risk of recurrence and higher infiltrative tendency than other types.11 Veterinary studies do not describe cytological evidence of malignancy or cellular atypia, which makes it difficult to differentiate between the benign tumor reported in dogs and the potentially more aggressive variation seen in human ameloblastomas.3,10 Canine acanthomatous ameloblastomas are characterized by infiltration of the epithelial cell, few mitotic figures, cords or clusters of cells invading the submucosa, and local invasion of the surrounding bone.2 The variation in behavior of both the human and canine forms makes classification difficult and, correspondingly, the treatment decisions are debated. Local control and recurrence continue to be frustrating for clinicians.12 Histopathological studies have reported that 68% of CAA tumors recur after simple marginal removal. Therefore, more aggressive therapies such as radical wide excision, radiation, or intralesional bleomycin therapy have been recommended.5,7,8,13,14
This paper reviews rim excision as an alternative surgical technique for management of CAA. With this technique, the mass, gingiva, involved teeth, and periodontal ligament are excised. The ventral cortex of the mandible or the dorsal aspects of the incisor or maxillary bones (depending on the tumor location) remain intact. Therefore, the risk for malocclusion is decreased, and cosmesis postoperatively is improved compared to the alternate surgical approaches. Our hypothesis was that with appropriate case selection, recurrence or recrudescence would not occur with rim excision. To our knowledge, this is the first case series of rim excision for the treatment of CAA.
Within this small number of cases, no evidence of tumor recurrence was seen. Due to the nature of this surgical technique, case selection was biased toward masses <2 cm in diameter with limited bone loss of <3 mm. The selection of a small tumor size may have influenced the results and the lack of recurrence. We also cannot verify that adequate margins were achieved by histopathology, as the true surgical margin was removed with the burr drill and could not be submitted. Instead, follow-up data were reliant upon the clients’ reports of good function and lack of recurrence, as well as oral examinations noted within the medical records.
Marginal mandibulectomy techniques were first reported in the 1970s for human patients having a variety of oral carcinomas. Such techniques continue to be used today for humans with neoplasias such as squamous cell carcinoma and ameloblastomas. In human medicine, numerous imaging studies are undertaken to evaluate the extent of bony invasion before a surgical technique is recommended; these imaging studies include CT, bone scintigraphy, and magnetic resonance imaging (MRI).15 Resection of the jaw includes a 1.5- to 2-cm margin of normal bone from the radiological limit of the tumor.11 When possible, rim excision affords improved quality of life scores when compared to segmental resection.12 Similar to human patients, each client contacted in this study reported a high level of satisfaction with both the function and cosmesis of their dog’s mandible after rim resection for CAA. Reports state that in human ameloblastomas, the cancellous bone is invaded, but the Haversian systems of the cortical bone are not. Therefore, rim excision to maintain the ventral border is a suitable alternative to segmental resection.11
In the study reported here, two findings were unexpected. The first was the dog that underwent rim excision for two separate CAA lesions. While both masses were in the right mandibular quadrant, CT analysis did not reveal continuation of the second mass from the more caudal location of the first rim excision. Since full mandibulectomy and histopathology were not performed, local invasion of the adjacent bone cannot be ruled out as a cause for the second CAA. To our knowledge, multiple CAAs in the same animal have not been previously reported in the veterinary literature.
The second surprising finding was the ventral cortical bony callus that developed on a dog that underwent rim excision centered on the right mandibular first premolar and right mandibular canine tooth. We suspect that the fracture was secondary to stress riser formation between the jaw and the surgical site; however, histopathology was not employed to verify the fractures or confirm the subsequent callus formation. At the time of writing, no further treatments had been instituted, and the dog was doing well without evidence of tumor regrowth.
Limitations of this study are its retrospective nature and the inherent inability of the surgical technique to allow margin evaluation by histopathology. Initial radiographs, if obtained by the referring veterinarians, were not available for review at the time of this study. Radiographs were evaluated by the primary surgeon preoperatively to confirm appropriate case selection for rim excision. Additionally, although clients were contacted, follow-up oral examinations and dental radiographs were not performed. These follow-up procedures would have been ideal to verify the clients’ reports of functionality and lack of recurrence following rim excision.
Due to the low incidence of CAA, a large prospective multicenter study of rim excision might be undertaken to better evaluate jaw function and long-term monitoring for recurrence. Ideally, a scoring system would be created based on a large number of dogs with a variety of tumor sizes, and any local or systemic recurrence would be noted. This scoring system could guide clinicians on the use of rim excision versus mandibulectomy or maxillectomy.
Conclusion
Overall, client satisfaction with cosmesis and perception of the dog’s ability to masticate was good to excellent. No clients were dissatisfied with the appearance of their pet, and most could not tell where the surgery had been performed. Complications associated with rim excision were limited to one case in which a ventral callus was palpated at the site of surgery. No recurrence of CAA was reported. Overall, based on this small number of cases, rim excision appears to be a viable treatment option for CAAs that are <2 cm and have <3 mm of bone destruction evident on radiographs. Rim excision results in improved dental occlusion and cosmesis compared to more radical excision.
Footnotes
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Doctor Murray’s current address is MedVet Medical and Cancer Center for Pets, 300 East Wilson Bridge Road, Worthington, Ohio 43085.
