Introduction
Teeth chattering or jaw tremors, usually accompanied by other clinical or neurological signs, have been reported in multiple conditions such as focal epileptic seizures in epilepsy,1,2 infectious meningoencephalitis3 or meningoencephalitis of unknown origin,4 dystonia in paroxysmal dyskinesia,5 compulsive behavior, tremor or focal seizures in degenerative encephalopathies,6–9 sleep REM behavioral disorder10 or narcolepsy,11 corticosteroid-responsive tremor syndrome,12 generalized fasciculations or focal seizures in metabolic or toxic diseases13–20 or untreated dental21 or oral22 pain. Nevertheless, teeth chattering has been previously observed as the sole sign in otherwise healthy middle- to older-age dogs.23
We have observed an episodic mandibular tremor (EMT), which is a rapid short-lasting tremor of the mandible, manifested as teeth chattering in dogs with no underlying neurological disease. The aim of this study was to describe the clinical course and clinical signs of EMT in dogs in an attempt to understand the underlying etiology.
Methods
The present report is of a retrospective, observational, multicenter case-series study with a prospective public, online questionnaire conducted by 5 veterinary hospitals between January 2018 and December 2023. Ethical approval was granted by the Royal Veterinary College Social Sciences Research Ethical Review Board (URN: SR2023 - 0109).
Search terms included the following: jaw tremor, jaw chomping, jaw chatter, mandibular tremor, and teeth chattering. Inclusion criteria consisted of (1) complete medical records, (2) clinical features consistent with episodic tremor of the mandible, and (3) video footage availability. Exclusion criteria included tremors with an unclear description, tremors affecting other parts of the body, and evidence of features consistent with epileptic seizures (eg, unconsciousness, autonomic signs, and postictal signs).
Complete medical records consisted of signalment; presenting complaints; clinical, neurological, and clinicopathological findings; and video footage. Tremor assessment was performed based on history and evaluation of video footage. Magnetic resonance imaging, CT, and CSF analysis findings and other diagnostic test results were obtained when available. All neurological examinations were performed by a board-certified neurologist or a neurology resident under the direct supervision of a board-certified neurologist. Magnetic resonance imaging devices used included high-field or low-field magnets (Intera 1.5-T Pulsar System; Philips Medical Systems; 1.5T Magnetom; Siemens; Intera 1.5T; Philips Healthcare; Aperto Lucent 0.4T, Hitachi; Vet-MR Grande 0.24T; Esaote). Magnetic resonance imaging sequences performed varied between institutions but always included transverse and sagittal T2-weighted, transverse FLAIR, and transverse and sagittal T1-weighted pre- and postcontrast (gadopentetate dimeglumine, 0.1 mmol/kg, IV bolus) images. Follow-up was achieved at 2 stages (short term [on discharge] and long term [clinical or phone call reexaminations]) when available.
To investigate the presence of these findings in the wider population, owners of dogs with this clinical sign were invited internationally to participate in an online public questionnaire (Supplementary Material S1). The request was made between July 2023 and November 2023 through social media of the participating hospitals, kennel clubs, and canine societies. A description of typical features of EMT was provided through available video recordings (Supplementary Video S1). Following a consent form, owners were then asked if their dog had exhibited episodes consistent with those described. Only those that answered “yes” to this question were given further access to answering the complete questionnaire. In the first section of the questionnaire, owners were asked to provide the species, breed, sex, age, and country of residence of the pet. In the second section of the questionnaire, a combination of open and closed questions was used to establish the phenomenology of episodes and clinical course and concurrent diseases. In the third section of the questionnaire, owners evaluated the quality of life (QoL) of their dogs, taking into consideration the episode occurrence. The aims of the questionnaire were to gain further insight into the incidence of the episodes within the dog population, characterize the phenomenology of the episodes, and investigate long-term outcome, QoL, and treatment efficacy and natural history of the disease from the owners’ perspective.
Descriptive statistical analysis was performed using a standard statistical software (SPSS Statistics 26; IBM Corp). Data were assessed for normal distribution using the Shapiro-Wilk test for normality. Numerical variables abnormally distributed were presented as median, IQR, and range. Categorical variables were summarized as counts and percentages.
Results
Retrospective hospital cases
Seventeen dogs were identified with reported EMT. Eleven of these dogs had video recordings available and met the inclusion criteria.
Of all dogs presented with EMT, 1 also showed night restlessness and 1 spontaneous episodic vocalization. Breeds included Cavalier King Charles Spaniel (CKCS; 4/11 [36.4%]), CKCS-Bichon Frise cross (Cavachon; 2/11 [18.2%]) and 1 (9.1%) of each of the following: Northern Inuit, Löwchen, Springer Spaniel, Labrador Retriever, and West Highland White Terrier. Seven dogs were male (4 neutered) and 4 dogs were female (all neutered). Median age at presentation was 3 years (range, 2.0 to 9.3 years; IQR, 3.6 years). Median body weight at presentation was 9.2 kg (range, 6 to 16 kg; IQR, 5.33 kg). Median duration from initial manifestation of EMT to presentation was 3 months (range, 22.5 days to 2.5 years; IQR, 3.75 months).
Clinical examination revealed periodontal disease (3/11 [27.3%]) with buccal ulcers (1/11 [9%]), pododermatitis (2/11 [18.2%]), and 1 (9%) of each of the following: historically fractured tooth and chronic oral eosinophilic granulomas (in remission). Palpation of the temporomandibular joints and external ear canals was unremarkable in all dogs. Neurological examination was normal in all dogs, with 1 dog (with reported spontaneous vocalization) having mild cervical hyperaesthesia.
Tremor assessment disclosed EMT characterized by rapid and short-lasting episodes of teeth chattering in all dogs (Supplementary Video S1). In 4 of 11 (36.4%) dogs, the tremor could be terminated by distraction; in 2 of 11 (18.2%), the tremor was nondistractible. In 5 dogs, this information was not available. All dogs were awake and conscious during the episode, whereas in 3 of 11 (27.3%) dogs, episodes also occurred during sleep. Lip smacking (5/11 [45.5%]) was sometimes present during an episode, whereas blinking was rarer (1/11 [9%]). Episodes were more intense when yawning (4/11 [36.4%]), when eating (1/11 [9%]), or when opening the mouth (1/11 [9%]). In none of the dogs were there autonomic, interepisode, or postepisode signs. Duration of an episode was variable, usually < 1 minute, whereas frequency varied from multiple episodes a day to a few per month.
Hematology and serum biochemistry were unremarkable in 8 of 9 dogs, whereas 1 of 9 dogs had stress lymphopenia, hypoproteinemia, and hypoalbuminemia. In 1 dog tested, serology for anti-canine transglutaminase-2 IgA was normal, whereas serology for anti-gliadin antibodies was increased (0.23; reference interval, < 0.12). Serology for anti-2M antibodies was unremarkable in 1 dog in which it was assessed. Serology (indirect immunofluorescence) for Toxoplasma gondii IgG and IgM was negative in 2 dogs in which it was assessed.
Advanced imaging included MRI of the head and neck in 1 dog, CT of the head and neck in 1 dog, and MRI and CT of the head and neck in 2 dogs. Brain parenchyma was normal in all dogs. Concurrent findings included Chiari-like malformation with syringomyelia (n = 3), primary secretory otitis media (PSOM; 3), intervertebral disk protrusions (2), dorsal atlantoaxial band (1), and atlanto-occipital overlap (1). Cerebellomedullary cisternal CSF analysis was normal in 2 dogs that also had MRI. Electroencephalography did not reveal any epileptogenic activity in 1 dog; however, no episode occurred during the test.
All dogs were diagnosed with idiopathic EMT. Concurrent diseases were present in 8 of 11 (72.7%) dogs, including Chiari-like malformation with syringomyelia (n = 3), PSOM (3), periodontal disease (3) with buccal ulcers (1), inflammatory bowel disease (2), pododermatitis (2), intervertebral disk protrusions (2), atlantoaxial dorsal band (1), atlanto-occipital overlap (1), eosinophilic oral granuloma complex (1), eosinophilic bronchopneumopathy (1), fractured tooth (1), meningomyelitis of unknown origin (1; Table 1).
Concurrent diseases in dogs with episodic mandibular tremor.
| Case No. | Breed | Concurrent disease (status) | ||||
|---|---|---|---|---|---|---|
| 1 | CKCS | CLM+SM (clinical) | PSOM (subclinical) | |||
| 2 | CKCS | CLM+SM (clinical) | PSOM (clinical) | Eosinophilic oral granuloma complex (remission) | Periodontal disease (clinical) | IVDP (subclinical) |
| 3 | CKCS | IBD (remission) | Periodontal disease (clinical) | Buccal ulcers (clinical) | ||
| 4 | Cavachon | IBD (remission) | Periodontal disease (clinical) | |||
| 5 | Northern Inuit | |||||
| 6 | CKCS | CLM+SM (subclinical) | PSOM (clinical) | Atlantoaxial | Atlanto-occipital | IVDP (subclinical) |
| 7 | Löwchen | Pododermatitis (clinical) | band (subclinical) | overlap (subclinical) | ||
| 8 | Springer Spaniel | Meningomyelitis of unknown origin (in remission) | ||||
| 9 | Cavachon | |||||
| 10 | Labrador | Eosinophilic bronchopneumopathy (in remission) | Fractured tooth (historical) | Pododermatitis (clinical) | ||
| 11 | West Highland | |||||
| White Terrier | ||||||
CKCS = Cavalier King Charles Spaniel. CLM+SM = Chiari-like malformation with syringomyelia. IBD = Inflammatory bowel disease. IVDP = Intervertebral disk protrusion. PSOM = Primary secretory otitis media.
Treatment for the teeth-chattering episodes per se was initiated in 7 of 11 (63.6%) dogs and included gabapentin (n = 5), methocarbamol (1) or paracetamol (1), and gluten-free diet (1). In 3 of 11 (27.3%) dogs, treatment for underlying disease was attempted. In 2 dogs with PSOM, myringotomy and middle ear flush were performed, and prednisolone was administered. One of them had previously severe periodontal disease, and 8 teeth extractions had been performed. In 1 dog with periodontal disease and buccal ulcers, amoxycilline-clavulate was administered. Two dogs with a disease in remission were already in treatment (one dog with prednisolone and cytarabine for meningomyelitis of unknown origin, the other dog with prednisolone and inhaled fluticasone for eosinophilic bronchopneumopathy) when EMT occurred.
All dogs were alive on discharge. Long-term follow-up was available for 8 of 11 (72.7%) dogs, and median follow-up time was 44 days (range, 30 to 1,544 days; IQR, 654 days). Frequency and intensity of EMT remained unchanged in dogs treated with gabapentin (n = 4), methocarbamol (1), or paracetamol (1). Partial response (ie, reduction of EMT frequency) was noticed in 1 dog treated with gabapentin; however, within 2 to 3 months from onset, episodes returned to initial frequency. Additionally, initial response was noticed for the first 2 weeks in 1 dog treated with a gluten-free diet, but soon the episodes returned.
In 2 CKCSs, PSOM was considered to have caused the EMT. In the first PSOM case, which also had eosinophilic oral granuloma complex in remission and periodontal disease, several treatments had taken place. Previous teeth extraction did not alter the EMT frequency. Episodic mandibular tremor ceased shortly after myringotomy and middle ear flush. However, 2 weeks after treatment, EMT recurred with the repeat CT revealing normal middle ears. When EMT frequency increased and some mild pharyngeal lesions appeared, prednisolone ceased the episodes, and a suspicion of eosinophilic oral granuloma complex relapse was raised. In the second PSOM case, EMT along with head shaking ceased shortly after myringotomy, middle ear flush, and administration of anti-inflammatory prednisolone. In 1 instance, EMT recurred 10 days after discontinuation of steroids. This cycle of treatment and subsequent cessation of EMT was repeated multiple times through a 2-year follow-up period. However, there were multiple occasions when the dog was treated with prednisolone only and the EMT was still present. In 1 dog with periodontal disease and buccal ulcers, amoxycilline-clavulate did not result in EMT frequency change.
Questionnaire results
Study population—The questionnaire was completed for 31 dogs. Breeds included CKCS (13/31 [41.9%]), crossbreeds (7/31 [22.6%]), English Springer Spaniel (2/31 [6.5%]), Dachshund (2/31 [6.5%]), Labrador Retriever (2/31 [6.5%]), and 1 each (1/29 [3.2%]) of the following: Cocker Spaniel, Lakeland Terrier, French Bulldog, Golden Retriever, and Hokkaido. Of the crossbreeds, 2 were Cavachon, 1 Lurcher, 1 Jack Russell Terrier cross, 1 Labradoodle, and 2 unspecified. Sex included females (18/31 [58%]; 5 neutered) and males (13/31 [41.9%]; 8 neutered). Countries of residence included the UK (21/31 [67.7%]), Greece (4/31 [12.9%]), Belgium (3/31 [9.7%]), the US (2/31 [6.5%]), and Romania (1/31 [3.2%]). Median age at onset of EMT was 3 years (range, 3 months to 14.5 years; IQR, 7 years).
Episode analysis—All episodes had 1 clinical feature, that of EMT, described as “jaw tremor,” “teeth chattering,” “bottom jaw movements,” “vibrating jaw,” “jaw shuddering,” or “episodic opening and closing of the jaw.” Dogs were maintaining a sitting (16/31 [51.6%]), standing (10/31 [32.3%]), or lying (9/31 [29%]) posture. In 1 dog, the episode could continue through the transition from sitting to standing. No accompanying gastrointestinal signs were observed during or around the episode in most dogs (27/31 [87%]), whereas the remaining owners were unsure. Lip smacking was reported in 1 dog (1/31 [3.2%]). In all dogs, the episodes occurred when awake, and in 5 of 31 (16.1%), the episodes occurred during sleep. Most dogs (26/31 [83.8%]) were reported to have normal mentation during an episode, and 3 of 31 (9.7%) were fixated on an object (eg, treat or toy), whereas 2 of 31 (6.5%) owners were unsure. Four dogs (12.9%) were reported to have a “worried” face during an episode; however, the majority of owners considered their dog to not be in pain during the episodes (29/31 [93.5%]). Most dogs did not have any difficulty with chewing or swallowing food (29/31 [93.5%]). Most owners were unsure whether they could distract the dog out of the teeth chattering (13/31 [41.9%]), whereas 10 of 31 (32.2%) could distract the dog, and 8 of 31 (25.8%) could not. One owner mentioned that although they could distract the dog, the tremor episode would continue. No autonomic signs were reported in most dogs (28/31 [90.3%]), 1 owner reported mild ptyalism, and 2 were unsure. No postepisode signs were reported in any of the dogs, while all dogs could snap out of an episode. Median episode duration was 13.5 seconds (range, 2 to 90 seconds; IQR, 58 seconds), and episode frequency could range from multiple a day to a few per year, with a median frequency of 4 episodes/mo.
Precipitating factors—In half of the dogs (16/31 [51.6%]), a possible precipitating factor was noticed, whereas in the other half (15/31 [48.4%]) an episode would happen randomly. Excitement (9/31 [29%]) was the most common trigger, followed by anxiety (4/31 [12.9%]), yawning (4/31 [12.9%]), and anticipation for a toy or a treat or playing with a toy (4/31 [12.9%]). In 2 dogs, an episode would be elicited while eating, and in another 2 dogs an episode would be elicited while self-grooming. In 3 dogs, the period around sleep or sleepiness was reported to trigger an episode. The following triggers were reported in a single case each: being told off, being stroked and patted on the head and ears, drinking, tiredness, looking for attention, fireworks, and loud noise. None of the owners had made any recent change to the diet prior to the onset of the tremors.
Concurrent medical conditions—Owners reported that most of the dogs had a concurrent medical condition (20/29 [64.5%]; Supplementary Material S2). Seven (22.6%) and 10 (32.2%) dogs were reported to have dental disease (eg, plaque or gingivitis, teeth removal) or ear disease (eg, otitis), respectively. No dog was reported to have temporomandibular joint disease. Most dogs did not undergo an MRI or CT scan (20/31 [64.5%]). Chari-like malformation, syringomyelia, and PSOM were reported in 1 dog that had an MRI scan, and 10 of 27 (37%) owners reported that none of the above were found in the MRI or CT.
Treatment—Only 3 of 31 (9.7%) dogs were in treatment for EMT. Two dogs were treated with gabapentin (10 mg/kg, PO, q 8 h) for EMT, and 1 dog was treated with prednisolone (0.5 mg/kg, PO, q 24 h) to treat otitis externa as a possible underlying cause for EMT. All owners considered the episodes to temporarily decrease or cease.
Clinical progression and QoL—Episode frequency was reported to be static over time in 16 of 31 dogs (51.6%), decreasing in frequency in 7 of 31 (22.6%), or increasing in frequency in 5 of 29 (17.2%) without treatment, whereas for 3 of 31 (9.7%) dogs, the owners were unsure. Most (26/31 [83.9%]) of the owners considered that EMT did not affect the QoL of their dogs, with 25 of 31 (80.6%) scoring their dog’s QoL as excellent (7 to 10 on a scale of 1 to 10).
Discussion
This study describes for the first time the clinical features of EMT in dogs without an underlying neurological disease. Episodic mandibular tremor is characterized by episodes of rapid and short-lasting (< 1 minute) teeth chattering in the absence of other neurological signs. Occasionally, lip smacking could accompany the tremor. The dogs retain consciousness, they do not exhibit autonomic signs during episodes, and the episodes tend to stop abruptly. Cavalier King Charles Spaniel was the overrepresented breed. The age of onset was usually 3 years old. Excitement was the most commonly reported trigger in half of the dogs, followed by anxiety, yawning, and playing with a toy or treat. The animals were typically normal between the episodes, and in dogs where diagnostic investigations were performed, no underlying causative disease was identified.
An idiopathic cause was considered in the cases of this study, raising a question as to whether EMT could represent a novel movement disorder. In our hospital cases, there was no clinical manifestation of pain or any evident source of pain (eg, temporomandibular joints, dental pain) at the time of examination or in the diagnostic imaging findings. Additionally, although teeth chattering as a result of shivering thermogenesis behavior due to cold weather is known in humans24 and anecdotally seen in dogs, it was considered unlikely, as history was not suggestive of it. Most dogs had concurrent diseases, not all of which were painful. Moreover, the variable nature of those diseases could not explain a consistent etiological causative relationship between them and EMT. As excitement and anxiety were reported as triggers for EMT in dogs, it is possible that EMT could resemble a movement disorder exhibited because of stress (eg, stress of disease), similarly to what has been reported in dogs with idiopathic episodic head tremor25 or as a result of excitement (eg, EMT occurring while looking at a toy or treat). Moreover, the overrepresentation of CKCS and their crossbreeds might indicate a genetic underlying etiology that would be worthy of future investigation. An epileptic nature was considered unlikely, as the tremor could be terminated by distraction in some dogs, and in 1 dog that had undergone electroencephalography, no epileptogenic activity was found, although no episode occurred during the examination. De Lahunta et al23 report teeth chattering in otherwise normal middle-aged to elderly dogs; however, no further information is provided other than an observation. Moreover, a human pediatrician observed a rapid EMT in his own dog.26 This was a Shetland Sheepdog crossbreed that manifested EMT when playing with a toy or when stroked on the head.26 The pediatrician considered this phenomenon similar to “binkie flutter” (ie, a rapid vibratory movement of the pacifier in an infant’s mouth) and speculated a possible common neuromuscular mechanism acting as a rapid control of the jaws in response to high-frequency feedback signals.26
On the other hand, almost three-fourths of the population of dogs in this study did have a concurrent medical disease, including PSOM or periodontal disease. Episodic mandibular tremor could be therefore associated with a pain response (oral, dental, otogenic or other) or, as discussed previously, be a movement disorder secondary to stress of the disease. Primary secretory otitis media,27 Chiari-like malformation,28 periodontal disease,29 and eosinophilic granuloma complex22 are highly prevalent diseases in CKCS, and therefore their concurrence with EMT might be a result of (1) the overrepresentation of this breed for each of those diseases, (2) a potential underlying genetic predisposition for each of the diseases, (3) a complex association between those diseases, or (4) the manifestation of EMT as a pain response secondary to 1 or more of those diseases. The fact that EMT temporarily ceased in 2 cases that were treated with steroids, myringotomy, and ear flush suggested that EMT could be associated with PSOM as a manifestation of otogenic pain or as a stress-associated movement disorder. In some dogs, PSOM was however not relapsing, while recurrence of EMT was observed. In 1 dog, a suspicion of eosinophilic oral granuloma complex relapse was possibly associated with an increase in EMT frequency. An association between teeth chattering and eosinophilic oral granuloma complex has been previously described.22
Mandibular tremor in humans is a neurological sign that has been reported in the 2 most common tremor syndromes, Parkinson disease and essential tremor.30 Other less common causes of mandibular tremors can be orthostatic jaw tremor, dystonic jaw tremor, neuroleptic treatment, or physiological shivering.31 Mandibular tremor was observed in 26.5% of patients with parkinsonism and 37.7% of patients with essential tremor in a recent retrospective study.30 That study concluded that most of the isolated mandibular tremors remained isolated and did not progress to other parts of the body. Orthostatic jaw tremor is rare, with pathognomonic masticatory muscle discharges exceeding 12 Hz on conscious electromyography.32,33 Dystonic jaw tremor has been less commonly reported in humans with jaw dystonia and is usually accompanied by dystonia elsewhere in the body.31,34 Task-specific tremor, or dystonia, is a less common type of action tremor or dystonia that emerges while the patient is performing or attempting to perform specific motor tasks such as eating, drinking, or tooth brushing.35–37
In dogs, parkinsonian tremor has not been reported.38 In fact, the most common nonparkinsonian jaw tremor in humans is essential jaw tremor, and there has been evidence to support that it may be a result of the interaction between central neurogenic oscillators and the periodontal reflex loop (ie, the reflex feedback from the periodontium to the masticatory muscles under isometric conditions).39,40 De Lahunta et al23 suggest that teeth chattering might be a result of a trigemino-trigeminal reflex, originating from stretch of the intrafusal fibers in the muscles of mastication and ending when the dog yawns or widely opens its mouth. Indeed, previous experimental studies in decerebrate cats showed that jaw-jerk is a true stretch reflex, which therefore can be initiated by proprioceptive stimuli; it involves 1 synapse and originates from the roots of the mesencephalic nucleus of the trigeminal nerve.41 In contrast, in experimental studies in rats, teeth chattering was entirely localized in the medial hypothalamus.42 In another study43 with rats, striatal cholinergic and dopaminergic mechanisms, including the substantia nigra, were suggested to be involved in the generation of tremulous jaw movements. In cases where pain is ruled out, we propose that EMT in dogs might represent an idiopathic movement disorder, originating from the peripheral nervous system (eg, trigeminal nerve) or CNS (ie, hypothalamus or basal nuclei), that might resemble a focal essential tremor. Essential tremor, one of the most common movement disorders in humans, is characterized by action tremor usually of the upper extremities, although there is high clinical heterogeneity and it can be minimally focal (ie, a small part of the body).44 Essential tremor has been associated with cerebello-thalamo-cortical circuits in humans, with recent studies showing that the cerebellum might be the central hub of the network.45 Essential tremor has previously been speculated in dogs. Terriers with hereditary ataxia manifested mandibular tremors that were speculated to be essential.6,8 The most classic example of suspected essential tremor in dogs is the benign idiopathic rapid postural tremor (ie, the so-called senile tremor).46 This tremor is a progressive postural tremor of older dogs38 that can be exacerbated on activity or excitement and has been particularly observed in aging terrier breeds.47 In Fox Terriers with hereditary ataxia, EMT has been speculated to potentially represent essential tremor.8
The limitations of this study included (for the clinical cases) its retrospective nature and (in some of the clinical cases) its lack of complete investigations as well as its lack of electroencephalography or conscious electromyography. Limitations also originated from the questionnaire part of the study, as most of these cases did not have investigations; the results of the survey were derived from owners and were therefore dependent on the accuracy of their descriptions, and video footage was not a requirement for inclusion in the questionnaire.
In conclusion, EMT manifested as teeth chattering might be a stress- or excitement-associated idiopathic movement disorder of dogs, although a manifestation of pain due to an underlying systemic disease should be first ruled out. It is usually manifested in young dogs. Cavalier King Charles Spaniels might be overrepresented, which raises the possibility of a genetic background. Although EMT does not seem to negatively affect QoL in affected dogs, further studies are necessary to evaluate the response to treatment. Episodic mandibular tremor might represent essential tremor, but further electromyographic studies need to be done.
Supplementary Materials
Supplementary materials are posted online at the journal website: avmajournals.avma.org.
Acknowledgments
None reported.
Disclosures
The authors have nothing to disclose. No AI-assisted technologies were used in the generation of this manuscript.
Funding
The authors have nothing to disclose.
ORCID
T. Liatis https://orcid.org/0000-0003-2815-2527
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