Bilateral Extracapsular Soft-Tissue Ossification Affecting Range of TMJ Motion in an Airedale Terrier

Introduction

In dogs, the temporomandibular joint (TMJ) is formed by the articulation between the condyle of the mandible, the mandibular fossa of the temporal bone, and the anterior portion of the retroarticular process of the temporal bone.^1,2 The TMJ is classified as diarthrodial because of its division into a dorsal and ventral compartment by an intra-articular disc because it is surrounded by a thin, fibrous capsule with a lateral ligament. The TMJ is situated in close relationship to the external acoustic meatus. Movements of the mandible are mostly synchronous; however, the mandibular symphysis in canines allows for slight independent movement. The coronoid processes are broad, and their thicker superior edges extend beyond the dorsal aspect of the zygomatic arches when the mouth is closed.² Failure of joint mobility can result in decreased range of motion, difficulty prehending food, difficulty grooming, and possible pain.

Ankylosis is defined as an abnormal immobility and consolidation of a joint.³ Decreased motility of the mandible is related to either disorders of the bony structures (e.g., TMJ, zygoma, coronoid process) or to masticatory muscle abnormalities. Ankylosis of the TMJ can be classified as either true or false ankylosis. True ankylosis involves structures within the joint capsule, and false ankylosis is caused by bony and soft tissue structures outside the joint causing limitations to normal movement. Cases of true (intracapsular) and false (extracapsular) ankylosis have been identified in cats and dogs previously, however, this report documents an unusual case of false ankylosis due to spontaneous bilateral soft-tissue ossification.

Case Report

A 3 mo old female Airedale terrier presented to the Dentistry and Oral Surgery Service at the University of Wisconsin School of Veterinary Medicine with a history of inability to open her mouth, a shortened mandible with lateral and ventral deviation to the left, and crowding of her left mandibular premolars. Signs included the ability to eat only softened food by use of her tongue. She was referred to the Dentistry and Oral Surgery Service for evaluation of the restricted range of motion involving her lower jaw.

The puppy was born in a litter from which both parents were known to be heartworm positive. The dam had been treated with melarsomine 10 days before whelping. She had a litter of two pups, but the male died acutely (cause unknown). It is unknown if the dam had evidence of other systemic disease. At the time of transition from nursing to hard food, functional abnormalities associated with the female pup were recognized. The dog avoided hard food and would eat only soft food through the left side of her mouth. As early as the patient’s first veterinary appointment, the owners requested evaluation of her ears. During the patient’s referral evaluation, otoscopic examination was normal.

Differential diagnoses based on history included masticatory myositis (MM), craniomandibular osteopathy (CMO), intra-articular TMJ dysplasia, lateralization of the coronoid process, and fracture. The patient underwent a thorough evaluation to determine the cause of decreased range of motion of the TMJ.

On presentation, the dog’s general physical examination was grossly normal. Oral examination revealed that the mandible was shortened, deviated to the left side, and exhibited limited TMJ range of motion. The suspected diagnoses were mandibular distoclusion with left-sided deviation of the mandible and bilateral TMJ ankylosis resulting in decreased range of motion. There was no pain on palpation of either the masticatory muscles or TMJ. A complete blood cell count revealed a slightly lowered red blood cell count (5.43 × 10⁶/µL; reference range, 5.5–8.5 × 10⁶/µL) and a high lymphocyte count (5.58 × 10³/µL; reference range, 1–4.8 × 10³/µL). Serum biochemical analysis showed a slightly elevated Ca (11.3 mg/dL; reference range, 8.7–11.2 mg/dL), elevated phosphorus (9.5 mg/dL; reference range, 2.5–7.9 mg/dL), and low creatinine (0.4 mg/dL; reference range, 0.5–2 mg/dL). Two lateral skull radiographs were taken by the referring veterinarian. Those radiographs demonstrated bilateral hypoplastic coronoid processes of the mandible and thickened tympanic bullae walls.

Computed tomography (CT) was recommended to further evaluate the mandible and TMJ and to investigate the decreased range of motion. The patient was premedicated with intramuscular acepromazine^a (0.02 mg/kg) and butorphanol^b (0.05 mg/kg). General anesthesia was induced with propofol^c (4.4 mg/kg IV) and maintained with isoflurane^d in O₂. CT imaging of the skull was performed with a slice thickness of 1.5 mm^e. CT revealed deformity of the mandibles with complete right-sided TMJ extracapsular ankylosis due to ossification of the soft tissue resulting in malocclusion. Bilateral otitis media was present, with thickening of the tympanic bulla either due to reactive osteitis or hyperostosis. There was deformation and abnormal thickening of multiple bones of the cranium. (Table 1, Figure 1). Monitoring for worsening of the craniofacial abnormalities and restricted TMJ motion was recommended.

Table 1 Summary of the CT Findings in an Airedale Terrier at 3 mo and 3 yr of Age

CT, computed tomography; TMJ, temporomandibular joint.

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At 5 mo of age, the client elected to pursue therapy in hopes of improving the patient’s range of motion of the TMJ. General anesthesia was induced as described previously. Tongue depressors were stacked and placed between the mandibular and maxillary incisors, gradually inserting additional tongue depressors in an attempt to increase range of motion. That procedure was previously described for the treatment of dogs with MM.⁴ In total, 34 tongue depressors were placed and left in the mouth for 10 min in attempt to stretch the soft tissues and break down the ossification. The distance between the mandibular incisors and the hard palate was 2.5 cm (but it was unclear from the dog’s medical record if that measurement was pre- or post-treatment). The patient was discharged with carprofen^f (2.2 mg/kg per os q 12 hr for 10 days), and a fentanyl patch^g (25 µg/hr) was also placed and left on for 4 days. The owners were instructed to encourage chewing behavior by placing rubber toys between the patient’s jaws for 15 min intervals 4–5 times/day.

Seven weeks later, the dog was re-examined. A conscious oral evaluation revealed an incisor distance of 2.5cm. There were no detectable change in the jaw’s range of motion.

At 11 mo of age, a dental cleaning with pre-emptive extractions was performed to reduce periodontal disease associated with tooth crowding. At that time, the patient had stage I periodontal disease (gingivitis). Otitis externa was diagnosed with marked ceruminous exudate and excessive yeast (4+) was present on cytology. Intubation for anesthesia was difficult and was performed endoscopically. Oral examination revealed that the teeth extending from the left mandibular canine tooth to the left mandibular first molars were tipped buccally, the second, third, and fourth left mandibular premolars were crowded and rotated. The fourth left mandibular premolar was extracted. The right mandibular canine tooth was oriented palatally to the right maxillary canine tooth, and there was no evidence of either palatal trauma or occlusal wear from the malpositioned teeth.

At 2 yr of age, the patient presented for dental cleaning. At that time, the patient had stage I periodontal disease and was not taking any medications. Serum biochemical analysis showed a moderate increase in alanine transaminase activity (378 U/L; reference range, 14–151 U/L). Endoscopic intubation was necessary. The owners reported the referring veterinarian had been treating the patient for otitis externa. Another otoscopic evaluation was requested, and otoscopic examination under sedation showed no abnormalities. A sedated oral examination revealed abnormalities consistent with what was previously described. The incisal distance (from the cusp of the right maxillary first incisor to the cusp of the right mandibular first incisor) was 2.9 cm on opening and 2.4 cm when the jaw was fully closed. Marked atrophy of the temporal and masseter muscles was present, with sinking of the eyes and protrusion of the third eyelids.

At 3 yr of age, the patient was diagnosed with stage Vb lymphoma involving the lung, jejunum, spleen, and liver.⁵ Chemotherapy was not pursued, and the patient was prescribed a tapering dose of prednisone^h for palliation. The patient was euthanized 7 wk after diagnosis, and necropsy confirmed the diagnosis of multicentric lymphoma.

A postmortem oral examination demonstrated restricted TMJ range of motion, documenting closed and open measurements of the incisal distances of 2.4 cm and 2.9 cm, respectively, which were the same as the measurements recorded when the dog was 2 yr of age. There were no changes in the dental orientation, no signs of soft-tissue trauma from maloccluded teeth, or signs of occlusal wear involving maloccluded teeth.

There was severe atrophy of the temporalis muscles bilaterally such that the muscle could not be identified grossly. The masseter muscles were present bilaterally in the massenteric fossa of each mandible, but they were markedly atrophied. A biopsy was submitted of the masseter muscle, which showed skeletal muscle bundles that were reduced in size, separated, and infiltrated by numerous adipocytes and thin to thick bands of dense collagenous fibrous connective tissue. No active inflammation or degeneration was noted. Those findings were consistent with severe diffuse atrophy, steatosis, and multifocal fibrosis of the masseter muscle as a result of disuse.⁶

A postmortem CT scan was performed on the head and mandible to evaluate additional changes (Table 1). Interpretations made from the CT were bilateral skull and TMJ dysplasia with cranial hyperostosis and temporal muscle hypoplasia. There was anomalous bony bridging between the skull and angles of the mandibles creating ankylosis (Figures 2A, B), and a persistent right-sided otitis media and resolved left-sided otitis media.

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Examination of the skull after fixation demonstrated new bone formation (bilaterally) extending approximately 1.3 cm from the temporal bone to the dorsomedial aspect of the mandibular angular process. The lesion began ventral to the retroarticular process of the temporal bone at the dorsolateral aspect of the tympanic bulla cranial to the external acoustic meatus. It extended with rough ossification to the medial mandible directly ventral to the course of the mandibular branch of the trigeminal nerve as it entered the mandibular foramen from the foramen ovale.

Discussion

The patient in this report was suspected to have developed decreased range of motion of the TMJ around the time of weaning due to the bilateral extracapsular ossification and ankylosis that were evident on CT imaging performed at 3 mo of age. Congenital causes of abnormal bone formation secondary to abnormalities involving the TMJs bilaterally in attempt to gain stabilization are possible. The dam was positive for heartworm, and it is unknown if she had other systemic diseases that may have led to abnormalities in the formation of the TMJ. There has been no research on the negative effects with the use of melarsomine in pregnant bitches. Therefore, melarsomine treatment cannot be ruled out as a potential cause of the changes seen in this case. There is evidence that the patient had some form of hyperostotic disease based on the increased thickening of the calvarium between 3 mo and 3 yr of age, and progressive bone formation in the region of the lateral pterygoid muscle, within the calvarium, and at the area of the dens.

Blood work performed at 3 mo of age showed significant elevations in the lymphocyte count and phosphorus levels that were not considered to be attributed to the patient’s condition. Age-related elevations in lymphocyte count and phosphorus levels have been established.⁷

In a recent article, 37 cases of locked jaw (defined as the inability to open and close the mouth) in dogs and cats that presented over several years to two schools of veterinary medicine were compared.⁸ More cases were seen in dogs than cats, and no breed or sex predilection was noted, but the condition occurred most commonly in middle-aged dogs (mean age, 5 yr).⁸ The causes of locked jaw in order of occurrence were as follows: fractures of bones of the head (32%), MM (23%), and osteosarcoma (13%). Central nervous system lesions were less commonly reported.⁸ Other potential causes of locked jaw include TMJ dysplasia with displacement of the coronoid process, CMO, other hard-tissue neoplasias, osteoarthritis, retrobulbar abscess or other infection, tetanus, and severe ear disease.^8,9

Effects of ankylosis have included slow prehension of food and exercise intolerance (inability to pant/move air) when the ability to open the mouth is reduced.³ Other signs of TMJ disorders that should be assessed are pain on mastication, difficulty prehending, inability to open or close the jaw, swelling of the jaw or masticatory muscles, and atrophy of the masticatory muscles that may result in enophthalmos.⁹

Dysplasia of the TMJ has been described in canines and can lead to subluxation of the condyles, resulting in locking of the coronoid process lateral to the ipsilateral zygomatic arch. Locking of the coronoid process occurs after wide-mouth opening makes the coronoid process palpable ventral or lateral to the zygomatic arch.^10–16 TMJ dysplasia resulting in open-mouth jaw locking has been reported in the basset hound, Irish setter, Weimaraner, and Akita Inu.^9,11–15 Open-mouth jaw locking has also been described in the Gordon setter, bloodhound, Dalmation, golden retriever, boxer and Bernese mountain dog.^12,15–16

CMO is a disorder with predisposition to terriers and is most common in West Highland white terriers, although other breeds have been affected.^9,17–20 This disease involves nonneoplastic bone proliferation around the tympanic bullae and ventral borders of the mandibular rami (usually between 3 mo and 8 mo of age), but has been seen as early as 2 wk of age.¹⁷ Thickening of the calvaria without changes to the outer surface of the bone has been found together with thickening of the tentorium cerebella.¹⁷ There have been reports of exuberant bone formation resulting in bony ankylosis involving bones associated with the TMJ (true ankylosis) or ankylosis resulting from periostitis involving the tympanic bullae, with the angular process of the mandible resulting in inability to move the mandible (false ankylosis).^17,21 The cause of CMO is unknown, but the condition results in pain, swelling of either the mandible or tympanic bullae, intermittent fever, and restriction/inability to open the jaw.⁹

Although the patient in this case study was a terrier, there have been no specific reports of CMO in Airedale terriers. This patient presented with symptoms earlier than the typical age of most patients that developed CMO. Due to the lack of presenting clinical signs (pain on palpation, swelling along the mandible) and the primary complaint of inability to move the mandible, CMO was not initially suspected. The thickening of the calvaria over time with rough ossification near the tympanic bulla on CT makes this condition suspicious; however, there was no evidence of resorption of normal bone or periosteal proliferation. Instead, the calvarium had the appearance of normal misshapen bone. Histopathology of the ossified area may have helped establish a definitive diagnosis.

Calvarial hyperostosis is a condition that has been reported to occur mostly in bullmastiffs and is hypothesized to be an inherited condition.^22–24 A similar condition has also been reported in a Pit bull terrier.²⁵ This condition is rare and has not been reported in Airedale terriers. Calvarial hyperostosis involves periosteal proliferation of the frontal and parietal bones.²⁵ The condition manifests between 5 mo and 10 mo of age, and clinical signs include pain with palpable swellings of the calvarium.²² Affected dogs may be febrile, and the appendicular skeleton may be affected. Partial to complete resolution of the condition can occur with skeletal maturity.²²

In contrast to cases of calvarial hyperostosis, the patient described herein presented with a nonpainful condition that was present since weaning. On external palpation, no masses or thickening of either the calvarium or mandible was evident. The condition did not resolve with maturity. Instead, between 3 mo and 3 yr of age, the condition progressed to complete ossification of soft-tissue structures in the location of the lateral pterygoid muscles with bridging ankylosis of the extracapsular soft tissues neighboring the TMJ and increased thickening of the parietal bones. Due to the involvement of the calvarium, this patient may have had a condition similar to, but different from, calvarial hyperostosis or CMO. The two conditions have recently been described as sharing a similar disease process, but having different clinical presentations. The term idiopathic canine juvenile cranial hyperostosis has been used as a term to describe both conditions.²⁵ This patient’s age of onset, breed, clinical presentation, and CT findings suggest a unique disease process that, if associated with either CMO or calvarial hyperostosis, would be an atypical pattern of abnormalities. This patient’s condition does not lead to a diagnosis consistent with any of the previously reported diseases.

Diseases that affect the muscles of mastication, such as MM, can cause false ankylosis of the TMJ. MM is an immune-mediated response to myosin isoforms that are unique to the muscles of mastication called 2M muscle fibers.²⁶ A previous study has shown that dogs placed on immunosuppressive therapies can improve clinically but demonstrate a positive 2M antibody response.²⁶ Signs of MM include acute swelling, pain on muscle palpation, trismus, and late-onset muscle atrophy. Histopathology of the affected muscles shows fiber necrosis, phagocytosis, and cellular infiltration.²⁶ The ultimate result of diseases that affect the muscles of mastication, when left untreated, is fibrosis and reduced range of motion.

Antibody titers against 2M muscle fibers were not recommended in the current case because the patient did not have sufficient data on CT and physical examination supportive of MM. The current patient had soft-tissue ossification evident on early CT imaging, which had not been reported in patients with MM.²⁷ Additionally, there was no pain or swelling on palpation of the muscles of mastication, and no evidence of either necrosis or inflammatory cells on histopathology of the masseter muscle.

Osteoarthritis has been a reported cause of jaw locking from proliferation of active osteomyelitis of the tympanic bulla that can extend to involve the TMJ.⁹ Osteophytes can surround the articular surfaces of the temporal bone and mandible. Irregular, dense new bone formation can be seen on radiographs of the tympanic bulla and TMJ. Further, arthritis of the TMJ secondary to septic processes has been described in horses.²⁸ Osteoarthritis of the TMJ can occur secondary to otitis media, and there is usually poor resolution following medical and surgical means, except in cases in which a bulla osteotomy is used early to establish drainage of the ear.⁹

In addition to the functional impact resulting from a restricted range of motion, there can also be developmental consequences. Previous research on the mandible in canines has shown that the force exerted by muscle has a significant impact on development. In addition, the occlusion of the cheek teeth prevents lateral growth of the mandible, and interdigitation of the canine teeth aids in maintaining alignment between the mandible and maxilla.²⁹ Previous cases have shown that deviation of the jaw to one side is indicative of either ankylosis or pseudoankylosis of the TMJ on that side.

One study demonstrated that the occlusal surfaces of the mandibles of various species, including the dog, were interfered with by the extraction of deciduous teeth of the maxilla of one side of the head.³⁰ Skulls were examined 4 months after deciduous tooth extraction and there was a shorter height and length of the ramus of the mandible, and the condyle of the extraction side was less developed than the condyle on the working side of the mouth. Also, due to disuse of the mandibular teeth, the alveolar bone surrounding the teeth was thinner than the bone surrounding the teeth on the used side. In studies performed over a longer period of time, complete twisting of the skull with shortening of the side that was not being used was evident. Those findings were consistent with Wolff’s Law with respect to bone’s ability to adapt and remodel, depending on the load that is placed on it. The muscles of mastication exert tremendous force, and without continual use of those muscles, it is apparent how malformations of the skull can develop in a similar way to the changes seen in this case.

In cases of false ankylosis in humans, surgical removal of the affected tissue is the recommended treatment and has been used with success.³¹ When the TMJ was involved, surgical excision of the condyle, combined with gap arthroplasty, has been effective.³¹ In veterinary medicine, unilateral and bilateral condylectomy procedures have been successfully used in patients with TMJ ankylosis.^3,8,10,32 In a reported case where there was bony ankylosis between the mandible and skull, repeated surgical procedures were needed due to recurrence of ankylosis.³² It has been reported that surgical correction of ankylosis in young dogs should be performed as early as possible before deformation of the mandible occurs, which will have serious repercussions on occlusion.³²

In the current case, surgical correction was discussed, but not elected, because the patient’s abnormalities were chronic, the patient was not painful, and the quality of life and adaptation to the condition was manageable. In addition to resection of the ossified tissues, addressing the misshapen mandibular condyles would have been necessary to restore any sort of range of motion. Postsurgical range of motion and lower jaw function would have been difficult to predict, especially because the procedure would have needed to be performed bilaterally. Conservative, nonsurgical therapies were chosen in the hope that the incomplete ankylosis offered the potential for slight improvement in the range of motion. The patient maintained a good quality of life and was able to maintain normal body weight by eating a softened diet. In cases of TMJ ankylosis, the authors recommend early surgical intervention.

When managing a patient with either severe malocclusion or permanently reduced range of jaw motion, consideration should be made for the loss of dental self-cleaning mechanisms. Stressing the importance of daily home care as well as cleanings q 6–12 mo could be necessary. In addition, selective pre-emptive extraction of crowded teeth to preserve the functionality of strategic teeth could be required. Daily home care and professional dental cleanings successfully managed oral disease in this patient with severe malocclusion and restricted range of motion.

Conclusion

Although the underlying cause of the condition remains unknown, extra-articular TMJ ankylosis secondary to new bone formation should be a differential diagnosis in patients with decreased range of motion of the jaw and an inability to fully close the mouth. CT imaging provides the most definitive method for evaluating patients with this condition.