Denervation of the Tensor Veli Palatini Muscle and Effusion in the Tympanic Cavity

Introduction

In dogs, common disorders that affect the trigeminal nerve (cranial nerve V) include nerve sheath neoplasms, hematopoietic neoplasms, and trigeminal neuropathy/neuritis.^1–3 In addition, lesions involving the pons may also affect the function of the trigeminal nerve.⁴ Typically, dogs with a nerve sheath neoplasm involving the trigeminal nerve are older adult dogs with a chronic history of unilateral atrophy of the muscles of mastication.¹ Although definitive diagnosis requires microscopic evaluation of the affected nerve, MRI can provide a presumptive diagnosis.⁵ The trigeminal nerve provides sensory innervation to the skin of the face and the eye via its maxillary, mandibular, and ophthalmic branches. Additionally, the mandibular branch provides innervation to the muscle of mastication. Consequently, disorders involving the trigeminal nerve or its neuronal cell bodies in the pons result in varying degrees of atrophy of the muscles of mastication alone or in conjunction with sensory loss to the skin of the face and cornea. Less commonly known is that the mandibular branch of the trigeminal nerve gives rise to the nerve of the tensor veli palatini muscle (TVPM) that innervates the TVPM. In fact, the TVPM is the only muscle of the pharynx that is not innervated by the glossopharyngeal nerve. The action of the TVPM is to open the pharyngeal orifice of the auditory tube and thereby allow pressure equilibration between the tympanic cavity and the atmosphere as well as allow drainage of fluid.⁶ In addition, the TVPM also tenses and elevates the palate along with the levator veli palatini and palatinus muscles, which helps to protect the nasopharynx during swallowing. Effusion is observed in the tympanic cavity ipsilateral to a disorder of the trigeminal nerve in 30% of dogs.⁷ The purpose of the present case report is to provide definitive evidence of denervation of the TVPM in a dog with a trigeminal nerve sheath neoplasm and concurrent effusion in the ipsilateral tympanic cavity.

Case Report

A 10 yr old female spayed English springer spaniel was presented for right-sided atrophy of the muscles of mastication, facial analgesia, facial nerve paralysis, and vestibular dysfunction. Two mo prior to presentation, the dog was evaluated by the referring veterinarian for right-sided facial paralysis that was presumed secondary to otitis media. After 3 wk of antibiotics therapy, no improvement was seen. Two wk prior to presentation, the dog developed right-sided vestibular ataxia and the owner noted atrophy of the temporalis and masseter muscles. Based on the progression of the neurological deficits, the dog was referred to the Neurology Service at the Veterinary Specialists & Emergency Center, VCA SouthPaws.

At referral, the physical examination was normal with the exception of tear staining of the hair along the medial canthus and enophthalmos as well as conjunctivitis in the right eye. Otoscopic examination revealed no evidence of otitis externa. The tympanum was intact bilaterally.

On neurological exam, the gait was consistent with right-sided vestibular ataxia. Postural reactions were abnormal in the right thoracic and pelvic limbs. Spinal reflexes were normal in all limbs. There was a menace response deficit and an absent palpebral reflex in the right eye. However, the dog appeared visual. The pupillary light reflex was normal bilaterally and the pupils were symmetric and appropriate in size. There was right-sided facial analgesia noted when a noxious stimuli (pressure with a closed forceps) was applied to the nasal septum mucosa, or when the superior lip and skin over the mandible were pinched. The right temporalis and masseter muscles were severely atrophied. There was a right-sided head tilt with spontaneous, rotatory nystagmus with the fast phase directed towards the left. Based on the neurologic deficits, the anatomic diagnosis was consistent with a right-sided lesion involving the pons and rostral medulla resulting in deficits involving the functions of the trigeminal, facial, and vestibular nerves (cranial nerves V, VII, and VIII, respectively). Given the chronic and progressive course, the differential diagnosis included neoplasia, such as a nerve sheath neoplasm of a cranial nerve, meningioma, choroid plexus neoplasm, or lymphoma; an infectious disease; or a noninfectious inflammatory disease.

Complete blood count, chemistry profile, urinalysis, and three view thoracic radiographs were normal. MRI of the head was performed using 1.5 telsa unit^a and a head coil. The MRI disclosed a right-sided, well-delineated, ovoid, extraparenchymal mass compressing and invading the pons and rostral medulla. The lesion continued as an enlargement of the trigeminal nerve within the trigeminal canal and extended rostrally as an enlargement of the mandibular, maxillary, and ophthalmic nerves. The three foraminae that served for these nerves to leave the cranial cavity were visibly enlarged, which included the oval and round foraminae and the orbital fissure, respectively. The lesion was hyperintense on T2-weighted images, isointense-to-hypointense on T1-weighted images, and displayed strong and homogenous enhancement on T1-weighted images obtained after intravenous contrast medium administration^b. Additionally, there was atrophy of the right temporalis, masseter, digastricus, and pterygoid muscles. These muscles also displayed abnormal contrast enhancement. The MRI findings were consistent with a nerve sheath neoplasm involving the trigeminal nerve and its branches and denervation atrophy of the muscles innervated by the mandibular nerve.⁵

Finally, there was material within the right tympanic cavity (Figure 1). The material was hyperintense on T2-weighted images and T2-weighted fluid attenuated inversion recovery images, hyperintense on T1-weighted images, and did not display contrast enhancement. The material within the right tympanic cavity was likely effusion based on the MRI characteristics.⁸

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The dog was treated with prednisone^c (0.5 mg/kg per os q 12 hr) for 2 mo. Despite corticosteroid therapy, the dog's vestibular dysfunction worsened and the owners elected to euthanize the dog based on neurological deterioration. Postmortem, gross, and microscopic examination of the lesion, brain, and soft tissues of the head was performed. The right and left TVPM were identified grossly, resected, and submitted for microscopic evaluation.

The gross lesion of the trigeminal nerve appeared as a reddish, extraparenchymal mass compressing and, likely, invading the brainstem at the level of the pons and rostral medulla (Figure 2). It extended as an enlarged trigeminal nerve along the ventral aspect of the cranial cavity. On the floor of the cranial cavity and ventral aspect of the skull, the enlarged main branches of the trigeminal nerve (the mandibular, maxillary, and ophthalmic nerves) were easily visible as they exited the oval, rostral alar foramina, and orbital fissure, respectively.

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Microscopically, the mass was a densely cellular neoplasm composed of spindle cells arranged into interlacing streams and bundles. The neoplastic cells infiltrated and surrounded individual and groups of axons as well as neuronal cell bodies within the ganglion. Neoplastic cells had indistinct borders with pale eosinophilic cytoplasm. The nuclei were oval to elongate with stippled chromatin. Mitotic figures were rare. Areas of lymphocytic infiltration were also observed. The gross and microscopic findings were consistent with a nerve sheath neoplasms of the trigeminal nerve and its branches.^9,10

Grossly, all the muscles of mastication were pale and atrophied. Likewise, the TVPM on the right side was atrophied (Figure 3). Subjectively, the external appearance of the pharyngeal opening of the right auditory tube was more concave on the lateral side. Microscopically, varying degrees of myofiber atrophy were present throughout the right TVPM (Figure 4). While many atrophied myofibers were angular in shape, most were so atrophied that their shape was severely collapsed and distorted. In comparison to the left TVPM, the cytoplasm was more basophilic. Vesicular nuclei were abundant. There also were thick bands of collagen dissecting through the muscle fascicles of the TVPM on the right side. The gross and microscopic findings of the right TVPM were consistent with neurogenic atrophy. Grossly, the effusion in the tympanic cavity was a yellow-to-tan, discolored clear fluid. Cytologically, the fluid was devoid of cells.

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Discussion

Clinically, the neurologic deficits, atrophy of the muscles of mastication and facial analgesia, were consistent with dysfunction of the trigeminal nerve or its neuronal cell bodies in the trigeminal ganglion and pons. The MRI, gross, and microscopic findings were consistent with a nerve sheath neoplasm of the trigeminal nerve, which resulted in compression and invasion of the pons and rostral medulla. In addition, signs related to the facial and vestibular nerve dysfunction, respectively, were also observed on the neurological examination. Interestingly, the dog initially was evaluated for facial paralysis. It is possible that subtle atrophy of the muscles of mastication was not appreciated by the owner or at the time of the first examination. The facial and vestibular nerve dysfunctions were likely secondary to compression of the facial nerve, vestibular nerve, or their neuronal cell bodies (VII) or connections (VIII) in the rostral medulla.

The MRI also disclosed effusion in the tympanic cavity. This is likely related to the dysfunction of the trigeminal nerve or its motor neuronal cell bodies, specifically related to denervation of the TVPM that enables normal function of the auditory tube.¹¹ The auditory tube is a musculotubal conduit between the tympanic cavity and the nasopharynx. It allows for pressure between the tympanic cavity and the atmosphere to be equalized across the tympanic membrane.⁶ In addition, it allows for drainage of fluid from the tympanic cavity.⁶ The auditory tube extends from the rostral aspect of the tympanic cavity to the nasopharnyx. Normally closed, the pharyngeal orifice is opened by the action of the TVPM.¹² The innervation of the TVPM is provided by the nerve of the TVPM, a small branch of the mandibular nerve.^13–15 The nerve of the TVPM has a short course and, given the small size of the TVPM, it is difficult to appreciate these structures on MRI or grossly at necropsy. In the case presented here, the gross and microscopic changes involving the TVPM were consistent with neurogenic atrophy. As a consequence, the TVPM likely was unable to open the pharyngeal orifice of the auditory tube creating a functional obstruction.

Experimentally, selective paralysis or surgical alteration of the TVPM results in effusion in the tympanic cavity.^11,16 The pathophysiological mechanism that explains development of effusion in the tympanic cavity is known as the hydrops ex vacuo theory.¹⁷ Briefly, if the pharyngeal orifice is unable to open, gases within the tympanic cavity and auditory tube are absorbed across the mucosa, which creates negative pressure within the tympanic cavity.^16,17 This negative pressure results in fluid transudation.^11,16,17 Ultimately, it is a functional obstruction of the auditory tube caused by TVPM paralysis that results in fluid transudation and development of effusion in the tympanic cavity.¹⁷ The same pathophysiological mechanism, hydrops ex vacuo, likely underlies the development of effusion in the tympanic cavity in the present case. The prevalence of effusion in the ipsilateral tympanic cavity of dogs with trigeminal nerve dysfunction is 30%.⁷ In addition, the presence of effusion in the tympanic cavity has been correlated with the severity of the atrophy of the muscles of mastication, the size of the neoplasm, and severity of the atrophy of the TVPM in dogs with trigeminal nerve sheath neoplasms.¹⁸ While that study purports a causal association, to the authors' knowledge, this is the first report that demonstrates neurogenic atrophy of the TVPM and effusion in the tympanic cavity secondary to a nerve sheath neoplasm. Although this does not provide definitive causative evidence, it does establish the first step in defining the pathophysiological basis, dysfunction of the TVPM, for the presence of effusion in the tympanic cavity in animals with trigeminal nerve disorders.

Conclusion

Benign and malignant disorders involving the trigeminal nerve are commonly encountered in small animal practice. Ascertaining a definitive diagnosis is paramount to defining appropriate therapy and an accurate prognosis. Often, MRI is the foundation to establishing a presumptive diagnosis. Clinicians need to recognize the imaging features associated with various etiologies that affect the trigeminal nerve. Similarly, knowledge of the secondary consequences of dysfunction of the trigeminal nerve, namely effusion in the tympanic cavity, will enable clinicians to focus on the primary disease process and not pursue an incorrect diagnosis. In the future, further investigation establishing the presence of negative pressure within the tympanic cavity is necessary to further support the hydrops ex vacuo theory. Moreover, analysis of the effusion may reveal properties consistent with a transudate, rather than an exudate; this is similar to what occurs with an infectious otitis media. Finally, similar to the experimental observations, this case report supports the development of effusion in the tympanic cavity with spontaneous disorders involving the trigeminal nerve as a result of paralysis of the TVPM.