Surgical treatment of feline inductive odontogenic tumor by marginal resection in a cat

Abstract

A 1-year-old mixed-breed cat was referred for an approximately 2-cm mass centered on the upper right canine tooth. Computed tomography (CT) revealed the lesion extended to the nasal cavity and orbit, causing thinning and expansion of the adjacent cortical bone. Excisional biopsy confirmed the diagnosis of a feline inductive odontogenic tumor. Based on the findings of CT imaging, the primary alveolar bone lesion was removed with the tumor, while the adjacent bones, which had been expanded and thinned, were preserved by marginal resection including the surrounding periosteum-like membrane. No local recurrence was observed for seven years. To validate the therapeutic outcome of this case, further research in diagnostic imaging and pathology will be crucial.

Odontogenic tumors are categorized based on their differentiated cell types and inductive properties; specifically, the capacity of the neoplastic epithelial elements to induce differentiation in mesenchymal elements to form odontogenic components [1, 11, 16]. The incidence of odontogenic tumors in cats is rare. A feline inductive odontogenic tumor (FIOT) arises from the odontogenic epithelium and induces mesenchymal cellular elements to form aggregated dental papillae [1, 3, 12]. Feline inductive odontogenic tumors typically manifest between 8 and 18 months of age, with no significant difference in incidence between males and females. While FIOTs generally occur on the rostral aspect of the maxilla, the tumors rarely occur in the mandible [1, 6, 13]. Despite being benign tumors, FIOTs are thought to be locally invasive and are usually treated with surgical excision, including maxillary or mandibular resection [2, 4, 6, 12]. These tumors have a favorable prognosis when surgical excision achieves clean margins [1, 8, 12]. Previous reports have shown positive prognoses following extensive excision of FIOTs including adjacent bone resection [1, 8]. The present report describes the details and surgical management of a specific case that was successfully performed without resorting to radical maxillectomy.

A 1-year-old neutered male mixed-breed cat weighing 5.4 kg presented to a referral veterinarian with swelling on the right side of the face. The upper right canine tooth (104) had fallen out, and six months later, this lesion began to swell. Following the excision, histopathological assessment of the lesion indicated the possibility of an odontogenic cyst. The lesion recurred after two months and was re-excised, revealing a histopathological diagnosis of an ameloblastoma. Thereafter, the cat was referred to Rakuno Gakuen University Animal Hospital. Upon a general physical examination involving palpation, it was revealed that the swelling extended from the bridge of the nose to the caudal maxillary bone. Additionally, the patient also had a red, smooth, oral lesion, measuring approximately 2 cm. This lesion extended from the inside to the outside the dentition, and was centered on the missing right maxillary canine tooth (104).

Radiographic examination revealed that the right maxillary bone was compressed medially and laterally from the third incisor (103) to the second premolar (106) of the right maxilla (Fig. 1).

Fig. 1.

A head radiographic examination showed that the right maxillary bone had expanded and thinned (arrows) laterally from the third incisor to the second premolar levels.

To assess the extent of the lesion and changes in surrounding tissues, a head computed tomography (CT) was performed with 2.5 mm slice thickness using pre- and postcontrast imaging sequences in the prone position. The lesion had a soft tissue density characterized with a mixed contrast pattern. It extended towards the right nasal cavity, centered at the scar on the upper maxillary canine tooth (104), causing the displacement of the nasal septum (Fig. 2A and 2D). Additionally, a non-enhancing cystic lesion with a low CT value was identified, extruding and extending into the maxilla and orbit. This lesion existed the root of the right second premolar (106) to the first molar (108) (Fig. 2B and 2C). This lesion caused thinning and expansion of the adjacent cortical bone and extended further into the orbit (Fig. 2E and 2F). Consequently, an excisional biopsy of the oral prominent lesion was conducted using a scalpel, and the sample was submitted for histopathological examination. Following this examination, the lesion was identified as FIOT. Two weeks after the biopsy, the tumor relapsed into its pre-biopsy size. The owner was presented with and consented to an informed document outlining the proposed surgical plan, which involved removing the affected alveolar bones at the odontogenic tumor site while preserving the bones exhibiting benign changes characterized by thinning and expansion, similar to odontogenic cysts and bone cysts.

Fig. 2.

Location of the lesion and relationship to the bone identified from the computed tomography (CT) images. (A–F) Images before surgery. (G–I) Images 37 days after surgery. (J–L) Images one year after surgery. (A, D, G, J) Images at the maxillary canine level. (B, E, H, K) Images at the maxillary second premolar level. (C, F, I, L) Images at the orbit level. (A–C) Images obtained under soft tissue conditions immediately after angiography. (D–L) Images obtained under bone conditions. A) The lesion had a soft tissue density with or without contrast enhancement and had extended into the right nasal cavity. B) Right nostril occupancy decreases as it progresses caudally. C) Cystoid lesions with low CT values extend through into the orbit. The first and second premolar roots were in this cystic lesion. D) The tumor had extended into the right nasal cavity and compressed the nasal septum. E) Right nostril occupancy had compressed the maxillary bone and infraorbital foramen. F) The lesion extended and thinned the adjacent maxilla and cheekbones. G) A nasal cavity was remodeled; however, a part of the ethmoid bone might be missing. H) A large part of the maxillary bone was preserved; however, an alveolar bone and this tooth were missing. I) A third premolar tooth was missing, and the maxillary bone had been slightly remodeled. J) The maxillary and ethmoid bones were remodeled; however, the nasal septum remains slightly curved. K) Only part of the maxillary bone had not yet been remodeled. L) The maxillary bone had been remodeled.

The cat was premedicated with midazolam (0.1 mg/kg intravenous injection [IV]) (Sandoz K.K., Tokyo, Japan), ketamine hydrochloride (0.5 mg/kg IV) (Fujita Pharma, Tokyo, Japan), fentanyl (1 μg/kg IV) (Daiichi Sankyo Propharma, Tokyo, Japan), and atropine sulfate (0.05 mg/kg intramuscular injection) (Fuso Pharmaceutical, Osaka, Japan). Anesthesia was induced with propofol (6 mg/kg IV) (Mylan Inc., Canonsburg, PA, USA) and maintained with sevoflurane (SEVOFLO^®, Zoetis JP, Tokyo, Japan) in oxygen delivered via an endotracheal tube. Fentanyl (2 μg/kg/hr continuous rate infusion [CRI]), remifentanil hydrochloride (20 μg/kg/hr CRI) (Daiichi Sankyo Propharma), ketamine hydrochloride (0.6 mg/kg/hr CRI), and robenacoxib (2 mg/kg subcutaneous injection [SC]) (Onsiol^®, Elanco, Tokyo, Japan) were administered for pain control. Cefazolin sodium hydrate (25 mg/kg IV) (Cefamezin α^®, LTL Pharma, Tokyo, Japan) was administered at induction of anesthesia. The cat was fixed in the supine position, and the oral cavity was disinfected with Lugol’s solution, draped, and surgery initiated. In this particular case, the tumor had extended into the nasal cavity and orbit. Therefore, opting for a wide resection, which includes the maxilla, lacrimal, palatine, and zygomatic bone, might result in significant change in the cat’s facial features and temporary functional deficits in eating and drinking [10, 15, 17]. Consequently, a course of marginal resection was chosen. To begin with, teeth 106, 107, and 108 were extracted (Fig. 3A). Then, the hard palate and gingiva were incised outside of the tumor using an electric scalpel. After the bones outside the tumor were exposed, the tumor mass was scraped from the bones using a periosteal elevator, revealing a periosteal-like membrane between them (Fig. 3B). While preserving the expanded maxillary bone in the nasal cavity, the alveolar bone was kept attached to the tumor. The lesion that had expanded into the orbit was exposed, and the protruding bone was broken off by a rongeur and scraped while the periosteal-like membrane was kept intact (Fig. 3C–E). During these surgical procedures, the expanded bones were nearly fully preserved (Fig. 3F). The incision lines made by an electric scalpel were trimmed to debride the burned tissue, and the lip mucosa and hard palate were sutured with 4–0 polydioxanone suture (PDS II; Ethicon Inc., Somerville, NJ, USA) (Fig. 3G and 3H). Postoperative pain management included ketamine 0.12 mg/kg/hr and fentanyl 1 μg/kg/hr. Further, cefazolin 25 mg/kg IV twice daily (BID), enrofloxacin 5 mg/kg SC onec daily (SID), and lobenacoxib 2 mg/kg SC SID were administered postoperatively during hospitalization.

Fig. 3.

A) Appearance after extracting the second premolar from the first molar in the right maxilla. B) The incision was advanced caudally. C) Exposure of the maxilla (arrow) was confirmed in the caudal region of the tumor. D) The maxillary bone was shaved off to expose the dorsal lesion (arrowhead). E) The lesion was scraped using a periosteal elevator. At the site in contact with the bone, the lesion was removed together with the periosteum or endosteum using a periosteal elevator. F) Appearance after tumor removal. G) The hard palate and labial mucosa were sutured using 4-0 PDS. H) Resected tumor, rostral on the left and dorsal on the bottom. Lesioned regions that extended into the nasal cavity (arrow) and extended into the orbit (arrowhead). A cystic lesion that has expanded to the orbit cannot be directly seen in this figure. PDS, polydioxanone suture.

The cat began eating wet food 24 hr after the surgery. The cat recovered well and was discharged from the hospital on the 4th postoperative day.

Histopathological examination confirmed the diagnosis of a FIOT. The gingival incision site and the dorsal and medial margins were complete and the resected surfaces may have included periosteal tissue (Fig. 4A). However, the assessment of the lateral margin on the labial mucosa side yielded inconclusive result. The visible membrane contained degenerated collagen fibers and inflammatory cells. Partial membrane damage was observed, exposing the tumor (Fig. 4B). Multiple cysts were formed within the tumor, which compressed the tumor cells. The cyst-like lesion extending into the orbit showed tumor cell infiltration into the cyst wall on the rostral side, and the cyst wall was composed of granulation tissue on the caudal side.

Fig. 4.

A) Histology of the dorsal margin of the tumor: Tumor cells showed a square arrangement, an alveolar structure, and a high degree of infiltration into the surrounding connective tissue. The extensive focal proliferation of immature odontogenic mesenchymal cells was also observed, mimicking the appearance of the dental papilla. The margin was complete at the dorsal stump. B) Histological findings on the labial mucosal side of the tumor: Degenerated collagen fibers and inflammatory cell structures clinically visible as a membrane have partially disappeared, and the tumor remains exposed at the stump (red dotted line).

Computed tomography scans were conducted on the 37th day, 6th months, and one year after the surgery. None of the examinations showed any evidence of recurrence or metastasis. The postoperative CT images on the 37th day revealed the preservation of a large part of the maxillary bone (Fig. 2G–I).

The images at the 6th month or one year follow-up revealed, gradual reing of a large part of the maxillary bone structure was observed (Fig. 2J–L). During a follow-up via telephone, no signs of recurrence, metastasis, and eating difficulties were reported. However, at eight years of age, the cat died suddenly due to unknown reasons. Remarkably, no recurrence was detected for approximately seven years after the surgery until its sudden demise.

Accurate pathological diagnosis of FIOT may be difficult based on the small size of the lesion sample. After a tissue biopsy at the first and second operations, the cat was not diagnosed with a FIOT. The first biopsy was obtained by curettage and the second by resection. At the last biopsy performed at our animal hospital, a lesion with a visible area was largely resected. The cat was then diagnosed with a FIOT. The two biopsies performed by the referral veterinarian did not lead to a definitive diagnosis, likely due to the small tissue sample. In cases in which the biopsy tissue only displays epithelial odontogenic tumor without any evidence of inducibility, it might be diagnosed as an ameloblastoma [5].

Several studies have reported that FIOTs in cats grow over a short period and repeatedly recur in cases when treatment is inadequate [1, 8, 19]. In this case, the recurrence occurred after removal by a referral veterinarian, and a significant increase in tumor size was apparent two weeks after the biopsy obtained at our animal hospital. Feline inductive odontogenic tumors are expected to grow rapidly if macroscopic lesions remain. Because marginal resection of FIOT might have a risk of recurrence, a CT scan was conducted at an early time, on the 37th day after surgery in this study.

A feline inductive odontogenic tumor is a benign odontogenic tumor derived from odontogenic cells of the tooth plate epithelium [5, 18, 19]. Several reports with radiographic images of FIOT have shown infiltration into the surrounding cortical bone [3, 8, 14]. In contrast, there are pathologists who disagree that an FIOT is invariably an infiltrative lesion [12]. Interestingly, there is also a debate in human medicine about how to remove ameloblastoma, which is a benign odontogenic tumor. The choice between radical treatment with jawbone resection or conservative treatment without jawbone resection remains controversial [7]. In the latter, some surgeons have removed the lesions with marginal resection alone [9]. Similar to the conservative treatment with ameloblastoma in humans, it is preferable to debate the resection method of FIOT.

Recently, CT scans were generally, enabling clearer identification of tumor boundaries that were previously difficult to discern. In this case, CT images revealed benign changes characterized by thinning and expansion of the cortical bone, resembling features observed in odontogenic cysts and bone cysts. This observation led to the decision to preserve the surrounding bones. Histopathological examination revealed that there were periosteum-like tissues between the tumors and the surrounding expanded bones. Further investigations should be recommended to determine whether such membranes on the expanded bones constantly exist using the FIOT specimens removed with marginal or wide margin.

In conclusion, unlike previous reports, this case involved the removal of the tumor along with the alveolar bone at the primary tumor site, preserving as much of the surrounding bone as possible. No recurrence was observed for seven years. However, considering that the infiltrative nature of FIOT has not been elucidated, it must be acknowledged that marginal resection may have a risk of increasing the recurrence rate. Further research in diagnostic imaging and pathology will be crucial.

CONFLICTS OF INTEREST

The authors declare no conflicts of interest.