Cholesteatoma After Lateral Bulla Osteotomy in Two Brachycephalic Dogs
This report describes a French bulldog and a pug that presented to the authors’ hospital following total ear canal ablation (TECA) and lateral bulla osteotomy (LBO), with signs of recurring otitis media and difficulty opening their mouths. The bulldog also had unilateral facial paralysis and sensory deficits of the trigeminal nerve on the ipsilateral side. Computed tomography and MRI scans suggested cholesteatoma in the bulldog, but showed only slight enlargement of the bulla in the pug. Histopathologic examination of samples yielded cholesteatoma in both cases. The authors suspect that development of the cholesteatomas was linked to the TECA/LBO surgery in both cases. Cholesteatomas may occur more frequently than currently thought. Even if only slight changes of the bulla wall are detected on CT, early-stage cholesteatoma should be considered. The narrow anatomic conditions in brachycephalic dogs possibly predispose such breeds to develop cholesteatoma after middle ear surgery because complete removal of all inflammatory and epithelial tissue can be more difficult than in other breeds. To the authors’ knowledge, this is the first report of an aural cholesteatoma causing sensory deficits of the trigeminal nerve.
Introduction
Cholesteatoma is an epidermoid cyst containing keratotic material. The cyst is surrounded by keratinizing squamous epithelium, which is constantly shedding keratin debris, resulting in progressive expansion of the cyst and eventual destruction of the adjacent tissue by increasing pressure and osteoclastic bone resorption activated by inflammatory chemokines.1,2 In humans, cholesteatoma is a well described, yet not fully understood, complication of otitis media.3,4 Most cholesteatomas in adults are acquired.5
There are two main forms of cholesteatomas: primary and secondary. The primary form is believed to develop due to chronic misventilation of the tuba auditiva, resulting in retraction of the tympanic membrane into the tympanic cavity. In turn, adhesions form in the middle ear, followed by cholesteatoma formation.6,7 In contrast, secondary cholesteatomas form as a complication of either otitis media or trauma. Secondary cholesteatomas are thought to be caused by metaplasia of the epithelium lining the tympanic cavity to stratified squamous epithelium due to chronic inflammation.8 More recent studies support the theory that squamous epithelium of the external ear canal or the tympanic membrane migrates into the tympanic cavity, which requires a trigger, such as an inflammatory process, and a bridge, such as granulation tissue, for the cells to migrate.9 According to the literature, those migrations do not necessarily require a defect in the tympanic membrane, but even perforations (especially if they are due to chronic inflammation) can permit migration.10,6 Cholesteatoma formation after surgical procedures has also been reported in humans.4,7
A third form, congenital cholesteatoma, is rare in humans and develops from dispersed cells during embryogenesis. In contrast to the other forms, congenital cholesteatomas form behind an intact tympanic membrane. Congenital cholesteatomas can also develop in other locations (e.g., intracranial) where they are usually referred to as epidermoid cysts.1
The only animal that has been shown to develop spontaneous cholesteatomas is the Mongolian gerbil, which develop these with aging due to epithelial migration on the tympanic membrane.11,12 Such gerbils are used as a study model for human cholesteatomas because cholesteatoma formation can be induced by ligation of the ear canal or the eustachian tube, after which keratin accumulates in the external ear canal, displacing the tympanic membrane into the middle ear.13,14 Similar mechanisms in dogs with cholesteatomas as a complication of otitis media were shown by Little et al. (1991).15
Most cholesteatomas in dogs develop secondary to otitis media, but congenital middle ear cholesteatomas may occur as well. A recent publication mentioned auditory tube dysfunction as a cause for otitis media with effusion, specifically in brachycephalic dogs, so primary cholesteatomas may appear in those dogs.16 Development of a cholesteatoma after lateral bulla osteotomy (LBO) has been previously mentioned by Hardie et al (2008).17 The purpose of this case report is to describe an end-stage cholesteatoma causing sensory deficits of the trigeminal nerve and to describe the clinical and diagnostic findings of an early stage cholesteatoma, both of which occurred after an LBO.
Case Report
A 7 yr old male French bulldog and a 6 yr old male pug presented to the ENT department of the Department of Small Animal Clinical Sciences with head tilts, circling, and ataxia. The bulldog had also had episodes of loss of consciousness three times within the 3 mo period prior to presentation. The owners ascribed those episodes to breathing difficulties due to brachycephalic syndrome. The pug exhibited pain on opening the mouth, which resulted in rejection of both food and water. Both dogs had a history of total ear canal ablation (TECA) and LBO. Those procedures were performed bilaterally in the bulldog 41 mo and 37 mo prior to presentation and on the right ear in the pug 11 mo previously. Both dogs had a right-sided facial paralysis postsurgically, which resolved over the following weeks. The pug also had a slight head tilt to the right since the surgery was performed.
On examination, the bulldog exhibited difficulties breathing, chewing, and swallowing and had to be hand-fed. Excessive salivation was also present. Based on the owners’ description of the loss of consciousness (together with convulsions and urination), a neurologic rather than respiratory problem was suspected. It was known from previous CT scans obtained at initial presentation 41 months earlier, that the dog had bilaterally enlarged ventricles.
On physical examination, the bulldog only had a mild nasal stridor. All other vital parameters were within normal limits. A moderate epiphora was noted in the right eye, and the dog had a bilateral mucous nasal discharge. The right lower lip appeared lower than the left side, and the tongue hung outside the mouth on the right side. On inquiry, the owners reported that the hanging tongue had been present since the dog was a puppy.
There was no menace response and no sensitivity in the nostril, eyelid, cornea, lip, or the inside of the ear on the right side. There was a head tilt to the right, slight circling to the right, and a right-sided ventral strabismus, and the postural reflex of the right forelimb was reduced. Right-side vestibular syndrome, facial paralysis, and trigeminal sensory loss were diagnosed.
Physical examination of the pug revealed that opening of the mouth was impossible and palpation of the left ear led to vocal pain expression. Otherwise, the dog had normal vital parameters. Complete blood count showed mild leukocytosis only. The following day, the dog had a head tilt to the right side, but no pain on palpation of the ear or mucous secretion from the left ear.
Both dogs underwent diagnostic imaging under general anesthesia. A computed tomographya of the bulldog showed a left tympanic bulla with increased wall thickness containing soft tissue–attenuating material, which was interpreted as granulation tissue. No other remarkable changes were present compared with what the authors detected on previous scans. There was osteolysis of the ventral right tympanic bulla caused by a soft-tissue attentuating mass of approximately 2.5cm diameter. The mass extended medial and rostral to the temporomandibular joint and compressed the left lateral aspect of the nasopharynx. There was no enhancement following contrast mediumb injection. Lysis of the petrous temporal bone was identified along the medial margin of the bulla. The lateral ventricles had marked enlargement, which was present on previous scans (Figure 1).
Citation: Journal of the American Animal Hospital Association 48, 4; 10.5326/JAAHA-MS-5760
MRIc of the bulldog showed an enlarged central canal and herniation of the cerebellum into the foramen magnum. The mass emanating from the bulla had relatively sharp boundaries and was hyperintense in T2-weighted images and isointense to musculature in T1-weighted images without enhancement after gadoliniumd administration. MRI also revealed involvement of the pars petrosa of the temporal bone and a loss of borderlines with the meninges (Figure 2).
Citation: Journal of the American Animal Hospital Association 48, 4; 10.5326/JAAHA-MS-5760
In the pug, the CT scans showed debris in the external ear canal with an air-filled tympanic bulla on the left, which, in conjunction with the clinical symptoms, was interpreted as otitis externa. The scans showed a soft-tissue-filled tympanic bulla on the right side, with a very mild expansion and thinning of the bulla wall compared with the left side. The left side had a thickened bulla wall, as often detectable in brachycephalic dogs. The right bulla wall was not contiguous over its entire surface, but showed interruptions on the medial and lateral parts. There was a fracture of the styloid bone on the right (Figure 3). MRI showed a mass with relatively sharp boundaries filling the tympanic cavity that was hyperintense in T2-weighted images and isointense to musculature in T1-weighted images. No enhancement after gadoliniumd administration was noted (Figure 4).
Citation: Journal of the American Animal Hospital Association 48, 4; 10.5326/JAAHA-MS-5760
Citation: Journal of the American Animal Hospital Association 48, 4; 10.5326/JAAHA-MS-5760
Differential diagnoses for the bulldog were cholesteatoma and neoplasia, but the way the lesion presented in CT and MRI was highly indicative of cholesteatoma. Subsequently, a retrograde nasopharyngeal endoscopye was performed. Compression of the lumen on the right side caudal to the hamulus of the pterygoid bone was noted (Figure 5). Tru-cut biopsies from the area of the mass were obtained.
Citation: Journal of the American Animal Hospital Association 48, 4; 10.5326/JAAHA-MS-5760
In the pug, a tentative diagnosis of recurrent otitis media in the formerly operated ear was made, and the dog underwent ventral bulla osteotomy (VBO). Intraoperatively, caseous material was removed from the bulla. The dog recovered well from surgery and exhibited a slight Horner’s syndrome on the right side postoperatively, which resolved after 7 days.
Histopathologic examination of the biopsy specimens from the bulldog showed fibrotic tissue that was lined by squamous epithelium and areas with abundant keratotic material. No signs of florid inflammation were evident. Histopathology of the tissue removed from the pug revealed cystic cavities filled with keratin debris, surrounded by a thin margin of squamous epithelium with fully differentiated keratinocytes. Granulation tissue, fibrosis, and some granulocytes and macrophages were also noted. The histopathologic findings were consistent with cholesteatoma in both cases.
Bacteriological examination performed after the VBO in the pug revealed massive infection with Staphylococcus pseudintermedius that was resistant to every tested antibiotic except cephalosporins. The pug was therefore prescribed, which was administered for the following 21 days.
Because of the severity of symptoms, wide extension of the cholesteatoma, and guarded prognosis, surgery was not a viable option for the owner of the bulldog. The bulldog was therefore discharged and euthanized 4 wk after presentation.
The pug continued to do well for 5 mo postsurgically. At the time this manuscript was written, the pug had no clinical signs except for the slight right-sided head tilt, which had already been present since the first surgery. A follow-up CT scan performed 5 mo after surgery showed no signs of recurrence. The pug will continue to be monitored.
Discussion
There are only a few reports regarding middle ear cholesteatoma in dogs.15,17–20 Reported symptoms in dogs include head tilt, ataxia, and circling (due to involvement of the vestibular system), unilateral facial palsy, pain, deafness, and problems associated with opening the mouth.15,17,18 The bulldog showed clear involvement of the facial nerve in the lesion, and both dogs had signs of a vestibular syndrome, pain, and problems associated with opening the mouth. Hardie et al. (2008) reported one dog with temporalis and masseter muscle atrophy.17 Those muscles are innervated by the mandibular nerve, which is the motor branch of the trigeminal nerve. The authors of this report could not find any reports on dogs with cholesteatoma that also showed loss of sensory function of the trigeminal nerve as described in the bulldog. Trigeminal neuralgia is even a rare entity in humans with cholesteatoma.21
The ophthalmic and maxillary nerves are merely sensory. The ophthalmic and maxillary nerves leave the skull cavity through the fissura orbitalis in the orbita, whereas the mandibular nerve exits via the oval foramen. The oval foramen is rostral to the tympanic bulla and the close proximity of the oval foramen and tympanic bulla may explain involvement of the mandibular nerve in an extensively growing cholesteatoma. The fissura orbitalis, on the other hand, is rostrodorsal to the tympanic bulla in the orbita, and although the anatomic structures are “squeezed” together in brachycephalic dogs, the MRI findings in the bulldog in this report do not suggest an extension of the cholesteatoma into the area of the fissura orbitalis. In contrast, the authors suspect that involvement of the petrosal bone of the os temporale may have affected the canalis nervi trigemini, which runs inside the petrosal bone. A recent study showed involvement of the canalis nervi trigemini canal in one dog with cholesteatoma, but the only described symptom related to this condition was atrophy of the temporal and masseter muscles.18 The authors suggest that involvement of the trigeminal canal in the petrosal bone is responsible for the sensory trigeminal deficits in the bulldog described herein.
The clinical presentation of lesions gives an initial indication of a central vestibular problem in the brainstem, which can be associated not only with facial paralysis, but also with trigeminal sensory loss, dysphagia, and tongue paresis associated with cranial nerve IX–XII involvement.22 However, after diagnostic imaging, the cholesteatoma was thought to be causing these problems on the periphery by involvement of the vestibular apparatus in the lesion, while mimicking a central problem because of the multiple cranial nerves involved. Nevertheless, the authors cannot rule out that some of the neurologic problems were perhaps associated with hydrocephalus and cerebellar herniation instead.
The convulsions the bulldog was exhibiting prior to presentation could be sequelae of the extensive hydrocephalus, with the onset only coinciding with the other symptoms. However, it is also possible that the dog developed meningoencephalitis after expansion of the cholesteatoma and destruction of the temporal bone. In the study conducted by Hardie et al. (2008), some dogs with late-stage cholesteatoma developed seizures as well.17 MRI scans in this bulldog were not indicative of meningoencephalitis. The authors did not perform cerebrospinal fluid analysis because a cerebrospinal fluid puncture in a dog with cerebellar herniation and extensive hydrocephalus carries too many risks, including possible death.23
The breathing difficulties can easily be explained by compression of the nasopharynx. Discomfort and problems in mouth opening have previously been explained by either periosteal reactions or sclerosis of the temporomandibular joint.18 They could also be caused by involvement of the motor aspects of the trigeminal nerve. Travetti et al. (2010) described a dog with temporal muscle atrophy.18 However, in the cases included in this report, no temporal muscle atrophy was noted. The difficulties associated with swallowing in the bulldog could have been caused by involvement of the glossopharyngeal nerve in the cholesteatoma, which exits the skull cavity through the foramen jugulare, just caudal to the bulla tympanica.
The excessive salivation in the bulldog was likely to secondary to difficulties associated with swallowing, whereas the epiphora was probably secondary to the loss of blinking ability due to facial nerve involvement.
Potential complications following LBO (as a treatment of otitis media) include nerve damage and recurrence of both infection and clinical signs.24 Development of cholesteatoma following LBO was previously reported by Hardie et al. (2008).17 In that study, the authors discussed the presence of cholesteatoma concomitant with otitis media prior to the first surgery versus the transfer of squamous epithelium remnants into the middle ear during surgery and onset of transformation in the presence of ongoing infection and inflammation. The authors of the current report assume that surgery may be a direct cause for cholesteatoma development in the dogs described in this report. Humans with prior ear surgery (of any sort) have a higher incidence of cholesteatoma.7 In LBO and TECA, the barrier between the squamous epithelium of the ear canal and the respiratory epithelium of the middle ear is eliminated. In cases where complete removal of these tissues cannot be achieved, the preconditions for cholesteatoma formation are created. After ablation of the ear canal, there is no possibility for any keratotic material that is shed from squamous epithelium remnants to be emitted. All keratotic material accumulates inside the middle ear remnant and begins to form a cyst.
Nonetheless, it is possible that cholesteatomas were already present prior to the initial surgeries in both dogs described herein. Chronic otitis media may have led to secondary cholesteatoma, which was not removed completely and recurred. Primary cholesteatoma is associated with auditory tube dysfunction.6,7,19 Owen et al. (2004), and recently Hayes et al. (2010), discussed the possibility of tube dysfunction in brachycephalic dogs, which would predispose them to developing primary cholesteatomas.16,25 Humans with a larger nasopharynx show better ear aeration and have a lower incidence of cholesteatoma, so the small nasopharynx in brachycephalic dogs could be another predisposing factor for developing primary cholesteatomas.6
In the bulldog, CT scans performed at the time of the initial surgery did not reveal any bulla enlargement, so it is unlikely that a primary cholesteatoma grew back after incomplete removal. The surgery reports of that dog, which had been operated at the authors’ clinic, described removal of granulation tissue. However, at the time of LBO, no samples for histopathology were taken, so there is no definite proof that there was not any keratotic material present in the tympanic cavity at that time. As Hardie et al. (2008) suggested, histopathologic examination of material removed during a TECA, LBO, or VBO should always be performed, and tissues should be taken (separately) from both the external ear and the middle ear.17
For the pug, histopathology from the clinic that had performed the LBO 11 mo prior to presentation to the authors reported an external ear canal polyp with a thick, keratinizing epithelium. Davidson et al. (1997) discussed a German shepherd with a cholesteatoma, which had a history of a polypoid lesion in the horizontal ear canal and a histopathologic diagnosis of an apocrine cyst. It is possible that either removal or even just the presence of this structure led to disintegration of the squamous-respiratory epithelium barrier and development of a cholesteatoma. It is also possible that the polypoid mass was already part of the cholesteatoma itself.20 Both scenarios are possible for the pug in this report as well. Chang and Kim (2008) suggested that, in humans, a granular polyp within an ear canal represents a cholesteatoma until proven otherwise.5
Chole (1993) and Moriyama et al. (1984) concluded from their research that the inflammatory process is responsible for bone resorption in cholesteatomas.2,26 This inflammation may be present either with or without infection. At present, it is not known whether there was infection in the bulldog, as biopsies could not be obtained under aseptic conditions, making a bacteriologic examination of samples not useful. In the pug, the concomitant infection may be the reason why this dog showed clinical signs early on in the disease and therefore could be diagnosed and treated. The bulldog only showed clinical signs when the disease had progressed to an incurable stage. In humans, it is known that some cholesteatomas are asymptomatic and can be present for years until they result in clinical signs.2,17,26
The bulldog showed no signs of recurrence of otitis media postsurgically and remained asymptomatic for almost 3 yr until it was presented to the authors’ clinic with neurologic symptoms. It was assumed that the otitis media was resolved by the surgery and that the cholesteatoma developed independent of the former disease. Histopathologic examination of the biopsies showed no signs of florid inflammation. The authors presume that remnants of external ear canal squamous epithelium led to formation of cholesteatoma years after successful treatment of otitis media in the bulldog. Similar mechanisms have been described in humans.5
In the pug, the head tilt never completely resolved after the initial surgery. Nerve damage during the first surgery is possible, but it is also possible that the infection and inflammation were never completely cured. During the initial surgery, squamous epithelium from the external ear canal may have been transferred into the middle ear, which led to the development of cholesteatoma. Bacteria have been seen invariably within the keratin of cholesteatoma in gerbils and are reported to be associated with human cholesteatomas as well.2,27
A re-evaluation of the CT scans of the pug led to a radiologic diagnosis of early-stage cholesteatoma. The authors conclude that cholesteatoma should be considered if any radiographic changes exhibiting even the slightest enlargement of the tympanic cavity or thinning of the bulla wall are noted.
In human medicine, diffusion-weighted MRI sequences are now used to detect cholesteatoma prior to histopathology.28 This technique might be applicable to veterinary medicine, as well.
In the study by Little et al. (1991), cholesteatoma was present in 11% of dogs with otitis media.15 Cholesteatomas as the underlying cause of recurrence of clinical signs in dogs that were treated for otitis media may appear more frequently than are currently diagnosed. In a study performed by Smeak et al. (1996) on recurrent otitis media in dogs that underwent TECA/LBO reported the presence of epithelial remnants and keratin in histopathology after a second surgical intervention in some of the dogs.24 Those findings are consistent with cholesteatoma. The authors of that report state the necessity of good exposure of the tympanic cavity to remove all epithelial remnants to avoid recurrent infection.
Review of the TECA and LBO surgery reports performed 3 yr earlier on the bulldog revealed that the anatomic circumstances made it very difficult to achieve good exposure of the bulla. Consequently, complete removal of all modified tissue was difficult and could not be achieved. Because of the hypertrophic bulla wall, the cavity was extremely narrow and access from the lateral aspect was therefore limited. Such difficulties may be prevalent in brachycephalic dogs with stenotic external ear canals and frequently hypertrophic bulla walls. In cases where anatomic malformation is already present on CT scans preoperatively, aggressive surgery should be conducted on first intervention. If extraction of the bulla lining is difficult during an LBO, it may be indicated to perform a VBO early on in a subsequent procedure, even if the dog shows no recurrent signs of otitis media after LBO. This is because development of a cholesteatoma years later is possible if any squamous epithelium remains. Alternatively, a VBO may be considered as first intervention because it can offer better exposure of the tympanic cavity, has the benefit of maintaining the external ear canal, and facilitates removal of debris from the middle ear if performed without TECA.24 However, an LBO provides better exposure for removal of epithelium from the osseous ear canal, so surgical approach should be elected based on involvement of the external ear canal and other parameters.24 To the authors’ knowledge, there are no prospective studies published that analyze the influence of surgery on cholesteatoma induction. There also do not appear to be any reports that compare LBO versus VBO with regard to cholesteatoma formation. According to Hardie et al. (2008), no one surgical approach is superior to another in terms of outcome.17 Regardless of the approach, complete removal of tissue is critical, and if this cannot be achieved, it may be necessary to perform both procedures to avoid any conditions predisposing to cholesteatoma formation. A second procedure or a “second-look” surgery are well-accepted policies in humans after canal wall up mastoidectomy for otitis media or cholesteatoma treatment because recurrence of cholesteatoma is high.29 Diagnostic imaging is not yet sensitive enough to detect every recurrent cholesteatoma and cannot replace second-look interventions in humans.29 It is questionable whether to adopt this practice of second-look surgery in veterinary surgery as well.
Conclusion
Cholesteatomas may be present more often than currently suspected in veterinary medicine. Any enlargement of the tympanic cavity or thinning of a formerly thick bulla wall is highly indicative of early-stage cholesteatoma. The authors of this report conclude that cholesteatomas that grow extensively and destroy parts of the petrosal bone may involve the trigeminal nerve canal and therefore can cause trigeminal deficits. Incomplete removal of tissue in dogs undergoing either TECA or LBO with anatomic structural malformations may lead to development of a cholesteatoma. This may happen with or without concomitant bacterial infection. It is crucial for all tissue to be removed to prevent such a development. In dogs where this cannot be achieved, a second intervention should be considered and it should not be postponed until (or if) the dog presents with symptoms of recurrence, as these might occur late. The removed material should be histopathologically examined, and tissues removed from the external ear canal should be kept separate from those removed from the middle ear. The narrowed anatomic conditions in brachycephalic dogs with their stenotic bony ear canals and thick bulla walls could predispose brachycephalic breeds to cholesteatoma development after middle ear surgery. This is because complete removal of all inflammatory and epithelial tissue can be more difficult than in other breeds. Nonetheless, the incidence of primary cholesteatomas due to auditory tube dysfunction cannot be ruled out in brachycephalic dogs. The authors are currently conducting a prospective study to analyze the incidence of primary cholesteatomas in dogs.
Computed tomography of the bulldog. Note disintegration of the petrous bone (*) and the compression of the nasopharynx (arrows). R, right; L, left.
T2-weighted (A) and T1-weighted (B) MRI scans of the bulldog. Note the T2 hyperintense and T1 isointense mass in the right middle ear and the enlarged ventricles (V). L, left; R, right.
Computed tomography of the pug. Note disintegration of the petrous bone (*) and the slight bulla enlargement in the pug, which may have led to fracture of the styloid bone (#). L, left; R, right.
T2-weighted (A) and T1 weighted (B) MRI scans of the pug. Note the T2 hyperintense and T1 isointense mass in the right middle ear. L, left; R, right.
Retrograde view of the nasopharynx of the bulldog with a 120° endoscope. Note that the right choana (CH) is not visible due to external compression of the nasopharynx by the cholesteatoma (arrows). D, dorsal; L, left; MNP, meatus nasopharyngeus (dashed circle); R, right; V, ventral.
Contributor Notes
