Corresponding author: Monica Aleman, MVZ, PhD, Dipl. ACVIM, Department of Medicine and Epidemiology, Tupper Hall 2108, One Shields Avenue, University of California, Davis, CA 95616; e-mail: firstname.lastname@example.org.
Background: Facial and vestibulocochlear nerve dysfunction occurs commonly in horses with temporohyoid osteoarthropathy (THO); however, auditory dysfunction has not been thoroughly assessed.
Objective: To determine if auditory abnormalities occur in horses with THO.
Animals: Eleven diseased and 8 control horses.
Methods: This is a prospective study in which brainstem auditory-evoked responses (BAER) were recorded in 11 horses diagnosed with THO through neurologic, endoscopic, radiographic, or computed tomographic examinations. BAER findings were compared with those recorded from 8 adult control horses.
Results: All horses with THO were found to have BAER abnormalities that included complete unilateral BAER loss (82%, n = 9/11), partial unilateral BAER loss (18%, n = 2/11) on the most affected side, and contralateral partial BAER loss (46%, n = 5/11). Nine horses had bilateral THO based on diagnostic imaging findings; of these, 5 (56%) horses also had bilateral BAER abnormalities. The complete absence of BAER in affected horses was most consistent with peripheral sensorineural hearing loss. There was a significant association between complete BAER loss and neurologic and diagnostic abnormalities.
Conclusions and Clinical Importance: Auditory abnormalities such as complete or partial BAER loss are common in horses with THO. The BAER test is an objective diagnostic tool that can aid along with other diagnostic modalities in the assessment, management, and follow-up of horses with THO. Furthermore, BAER studies may help to elucidate the pathophysiology of THO in horses.
Temporohyoid osteoarthropathy (THO) in horses is a disorder of the petrous temporal and stylohyoid bones that form the temporohyoid joint.1,2 The proposed etiologies include inflammation, infection of the middle/inner ear (otitis media/interna) secondary to a hematogenous or ascending infection from the upper respiratory tract or guttural pouches or both, extension of otitis externa, and a nonseptic primary degenerative process that results in arthrosis of the temporohyoid joint.1,3–5 However, the exact cause of THO remains unknown. In addition, infections of the middle ear appear to be uncommon in horses.1 Regardless of the etiology, the disorder results in bony proliferation of the tympanic bulla, proximal stylohyoid, and petrous temporal bones; fusion of the temporohyoid joint; and subsequent fractures of the stylohyoid and petrous temporal bones.1 Fractures of the basisphenoid and occipital bones have also been reported in horses with THO and can cause seizures.1 Depending on duration and severity, 2 clinical presentations may be observed in horses with THO.1 Non neurological clinical signs include head shaking, ear rubbing, resentment of manipulation of the head or ears, resistance to the bit, and pain on palpation at the base of the ear.1 Dropping feed and weight loss have also been documented.1 The neurologic signs involve acute onset of facial (CN VII), vestibulocochlear (CN VIII), and rarely glossopharyngeal (CN IX) and vagus (CN X) nerve dysfunction.1,3,6
Brainstem auditory-evoked response (BAER) testing evaluates the integrity of the auditory pathway.7 It is useful in the detection of unilateral and bilateral deafness.8,9 Reference values for BAERs in adult horses and ponies10–14 and neonatal foals are available in the literature.15 BAER as a diagnostic modality in horses has been limited to a few reports that include congenital sensorineural deafness in American Paint horses,16,17 presumed gentamicin vestibulotoxicity,18 foals exposed to endophyte-infected fescue in utero,15 head trauma, vestibular signs because of THO in a single horse8 and secondary to lightning strikes in 2 horses,19 and central (brainstem) lesions.9 Vestibulocochlear dysfunction has been reported in horses with THO; however, only vestibular signs have been thoroughly described.1,2,5,20 Information relating hearing status to a diagnosis of THO in this species is limited.8,9 Therefore, the purpose of this study was to determine if auditory abnormalities were present in horses with THO. In addition, the association between BAER loss, neurologic signs, and abnormalities of the hyoid apparatus, petrous temporal bone, temporohyoid joint, and tympanic bulla as identified by endoscopic, radiographic, or computed tomographic (CT) evaluation was evaluated.
Materials and Methods
This prospective study included horses diagnosed with THO through a neurologic examination and one or more of the following diagnostic modalities: endoscopy, radiography, or CT. Horses with a definitive diagnosis of THO were evaluated through a BAER exam from January 2005 to December 2007 at the William R. Pritchard Veterinary Medical Teaching Hospital. A neurologic examination was performed by one of the authors (MA) to determine if neurologic deficits were present.21 This examination included blindfolding. Ataxia, when present, was graded according to a standard scheme described by Mayhew.22 Otoscopic evaluation and a Schirmer's test were part of the physical examination in all horses with THO. Clinical pathology and serology data such as complete cell blood count, serum biochemistry, cerebrospinal fluid cytology, and serology for EPM and West Nile Virus were collected.
Endoscopic, radiographic, and CT examinations were evaluated by one of the authors (SMP) blinded to the results of the BAER. Endoscopic abnormalities were graded as mild, moderate, or severe and defined by thickening of the stylohyoid bone at any point along its length. Fracture of the stylohyoid bone was considered severe. For radiographic and CT abnormalities, the lesions were described as follows. Mild remodeling of the stylohyoid or petrous temporal bone or both; moderate remodeling of the ceratohyoid, stylohyoid, and petrous temporal bones with fusion of the temporohyoid joint; and severe remodeling of the ceratohyoid, stylohyoid petrous temporal bones, fusion of the temporohyoid joint, sclerosis of the tympanic bullae, or fracture of any of the bones mentioned. Additionally, findings such as soft tissue swelling and presence of fluid suggestive of otitis externa, media, or interna were evaluated through CT examination.
Brainstem Auditory-Evoked Potentials
A Nicolet Viking IV-evoked potential systema was used for recording BAERs. Depending on patient cooperation, horses were placed in a quiet recovery stall or in examination room stocks and sedated with xylazine hydrochloride at a dosage of 0.3–0.4 mg/kg IV. Insert earphonesb fitted with large disposable eartipsc were placed in each horizontal auditory canal. Platinum needle electrodesd were inserted subcutaneously as follows. One electrode was placed at the vertex (V) on the midline at the center point between the intercanthus and the occipital protuberance. Left and right mastoid electrodes (LM and RM, respectively) were positioned ventral to the most caudal area of the zygomatic arch on each side (Fig 1). An additional recording electrode was placed on the dorsal midline at the level of the second cervical vertebra (C2, Fig 1); this is a modification of the 1st thoracic (T1) electrode placement used in small animals.23,24 In keeping with the convention of upward deflections being positive, the mastoid and C2 electrodes were designated as active inputs, whereas the vertex was referential. A ground electrode (Z) was positioned between the occipital protuberance and C2.
Each BAER recording was the average of a minimum of 400 responses over a 10 ms epoch. Single replications were performed for all recordings and superimposed on the original tracings. An alternating (rarefaction plus condensation) broadband click stimulus at 90 dB hearing level (nHL) was applied at a rate of 10.1 Hz. To avoid bone conduction stimulation of the contralateral ear, a white noise-masking sound at 60 dB nHL was applied to the opposite ear. Simultaneous recordings were conducted using 2 derivations per ear tested: (1) vertex to ipsilateral mastoid (V-M), and (2) vertex to C2 (V-C2). Disposable eartips were examined immediately after use to ensure that they were patent (not occluded by debris from the ear canal). Positive peaks, when present, were identified to the best of our ability using superimposed replicate tracings to aid in labeling; and their latencies were consistent with the system described earlier (Fig 2).23 Negative peaks (troughs) following waves I and V were also labeled (I′ and V′, respectively) to facilitate amplitude calculations of these peaks. Interpeak intervals between waves I–III, III–V, and I–V were also measured. Amplitude ratios were calculated by dividing wave V amplitude by the amplitude of wave I on the vertex to C2 derivation. A grading system was also used for statistical analysis as grade 0 = presence of identifiable BAER peaks, and 1 = absence of identifiable BAER peaks. Those horses in the latter group were excluded from further analysis, as latencies and amplitudes could not be determined. Absence of identifiable BAER peaks was most compatible with complete hearing loss (Fig 3, upper tracings); and increased peak latencies or difficulty identifying peaks or both were suggestive of partial hearing loss (Figs 4 and 5). Eight client-owned adult horses (5–20 years of age) with no clinical, radiographic, and endoscopic evidence of THO of both sexes and of Quarter Horse, Thoroughbred, and Warmblood breeds were used as controls for statistical comparison (Fig 2).
Data were entered for analysis into a statistics software.e A Wilcoxon's signed-rank test was used to compare clinical signs and abnormalities observed during endoscopic, radiographic, and tomographic evaluation in the affected versus nonaffected ears of horses with complete unilateral hearing loss. To confirm that there were no differences between right and left ears in control horses, a Wilcoxon's signed-rank test was also used to compare peak latencies, intervals, and amplitudes in both derivations. These data were then compared with values obtained from the nonaffected ears of THO horses, conditional on side, by Mann-Whitney tests. Statistical significance was defined as P < .05.
Twenty-five horses were diagnosed with THO during the study period. Client compliance and safety concerns resulted in BAER testing of 11 horses. Horses were Quarter Horse (n=6), Thoroughbred (n=2), Warmblood (n=2), and Paint (n=1) breeds. Six females, 4 geldings, and 1 stallion were included. The mean and median ages at presentation were 11.2 and 11 years, respectively, with a range from 7 to 16 years of age. According to the owner or referring veterinarian, the onset of clinical signs ranged from a few hours to 4 years before presentation. More than half of the horses (n = 7/11) developed signs within 3 weeks before admission. Age at onset of clinical signs was estimated and the mean and median ages were 10.7 and 10 years, respectively.
The most common nonneurologic clinical sign was secondary unilateral exposure ulcerative keratitis (n = 7/11). These horses presented with a deep, large, horizontal corneal ulcer, corneal edema, and anisocoria (n =7/7), and 2 horses had corneal fibrosis. A Schirmer's tear test performed in all 11 horses revealed tear production ranging from 5 to 19 and from 20 to 35 mm/min in the ipsilateral and contralateral eye, respectively (reference >20 mm/min). Three horses also had a history of difficulty eating and drinking that in 1 horse resulted in weight loss. Other signs included violent head toss on ear palpation, head shaking, chewing movements, and lethargy. Otoscopic examination was unremarkable in 10 horses, and 1 horse had unilateral erythema and narrowing of the external ear canal. None of the horses had evidence of ear tick infestation.
Neurologic abnormalities were identified in all 11 horses. In 8 horses, neurologic deficits were unilateral (right side n = 5; left side n = 3) and in 3 horses bilateral. Signs included a combination of facial nerve paralysis and vestibular dysfunction in 8 of 11 horses (two or more of the following: head tilt [n = 8/8], nystagmus [5/8], circling [4/8], leaning [2/8], or ataxia [8/8]); and exclusive facial nerve dysfunction in 3 horses. Mild and severe ataxia was observed in 2 and 6 horses, respectively. Blindfolding increased the severity of vestibular signs in 8 horses and revealed vestibular deficits in 1 horse with apparently exclusive facial nerve dysfunction. Bilateral facial nerve paralysis resulted in failure to prehend food in 3 horses. One horse had a seizure-like episode before referral.
The significant laboratory abnormalities included anemia, neutrophilia, and lymphopenia (n = 1/11); hyperglycemia (n = 4/11); and increases in serum indirect and total bilirubin (n = 5/11), serum creatine kinase, and aspartate aminotransferase (n = 1/11). Serum immunofluorescent antibody test for Sarcocystis neurona and Neospora hughesi, serum IgM-capture ELISA for West Nile virus, and nasal swab and whole blood EDTA polymerase chain reaction testing for Herpes virus 1 were negative in all horses tested (n = 8/8). Cerebrospinal fluid analysis was performed in only 1 horse (the one with the history of a seizure-like episode) and revealed marked histiocytic inflammation and previous hemorrhage (TNC = 130/μL, RBC = 15,800/μL, TP 181 mg/dL).
Six horses had all 3 diagnostic modalities, 4 had 2 (radiography and endoscopy, n = 3/4; radiography and CT, n=1/4), and 1 had radiography only. Endoscopic examination was performed and found abnormal in 9 of 9 horses. Abnormalities included stylohyoid thickening (body and articular head, n = 9/9) and abnormal shape (suspected healed fracture based on profound angulation and thickening at the angulated point of the stylohyoid bone, n=1/9), and erythema of the guttural pouch (n=1/9). The abnormalities ranged in severity from mild (n=2/9) to moderate (n=5/9) to severe (n=2/9). Six horses had unilateral and 3 horses had bilateral abnormalities with 1 side more affected. Other findings included left laryngeal hemiplegia (n = 2/9) and retropharyngeal polyp (n = 1/9). There was no evidence of guttural pouch infection (n = 9/9).
Radiographic abnormalities were found in all 11 horses. They included stylohyoid bone thickening (n = 11), temporohyoid joint remodeling (n = 7/11), and chronic fracture of the proximal stylohyoid bone with excessive callous formation (n = 3/11). Horses with bilateral abnormalities (n = 8/11) had more severe alterations than horses with unilateral abnormalities except for 1 horse.
CT was performed and found abnormal (bilateral lesions) in 7 of 7 horses. Moderate to severe abnormalities were observed on 1 side in combination with mild to moderate on the contralateral side. The abnormalities included osseous proliferation (thickening and sclerosis) of the stylohyoid and temporal bones (n=7/7), temporohyoid joint remodeling (n=7/7), narrowing of the external acoustic meatus (n=6/7), thickening of the tympanic bulla (n=6/7), presence of fluid in the tympanic bulla (n=3/7), and fracture of the proximal stylohyoid bone with remodeling (n=3/7).
Brainstem Auditory-Evoked Potentials
On BAER examination, 9 horses were diagnosed with complete BAER loss on the side that was most affected clinically (Fig 3). The remaining 2 horses had partial BAER loss on the most affected side (Fig 4: subtle delay in peak latencies associated with stimulation of the right ear; Fig 5: decrease in peak amplitudes with prolonged latencies upon stimulation of the left ear). Three horses with apparent exclusive unilateral neurologic deficits (facial paralysis, n=1/3; and facial and vestibular dysfunction, n=2/3) had complete BAER loss on the ipsilateral side and partial BAER loss on the contralateral side. There was no statistical difference between gender and auditory abnormalities. There was a significant association between absence of BAERs and both facial and vestibular nerve dysfunction (P= .0001 and .0026, respectively) and the presence of endoscopic, radiographic, and CT abnormalities (P= .0031, .002, and <.001, respectively). Based on diagnostic findings (endoscopy, radiography, and CT), 9 horses had bilateral THO. Their BAERs were as follows: 5 of 9 horses had complete unilateral BAER loss and contralateral partial BAER loss; 2 of 9 had complete unilateral BAER loss and no contralateral auditory abnormalities; and 2 of 9 had partial unilateral BAER loss of the more affected side and no contralateral auditory abnormalities. The remaining 2 of 11 horses with THO had mild and severe unilateral THO as identified on endoscopic and radiographic evaluation. In those 2 horses, complete unilateral BAER loss and no contralateral auditory abnormalities were identified.
Peak latencies, interpeak intervals, amplitudes, and amplitude ratios for both groups of horses are shown in Table 1. These parameters were determined in horses with identifiable peaks (controls, n=8/8; and THO horses' hearing ear: left n=7, and right n=6). Horses with absent BAERs were not further used in constructing peak latencies or amplitudes. There were statistical differences between controls and horses with THO in peak latencies, interpeak intervals, and peak amplitudes but no difference in amplitude ratios (Table 1). BAER follow-up performed several months after bilateral ceratohyoidectomy was available in 2 horses but remained unchanged (complete unilateral BAER loss). These horses had chronic THO with signs present for 2.5 months and 4 years before admission.
Table 1A. BAER peak latencies and interpeak intervals.
Latencies for peaks I, III, IV, and V and peak intervals (I–III, III–V, I–V) were determined only in horses with identifiable peaks on BAER, and shown in ms for control (left = 8/8, right = 8/8 ears) and THO (hearing ear: left = 7/11, right = 6/11) horses using 2 derivations: V-M and V-C2. Median and ranges are shown. *P≤ .05 and**P≤ .001 denote differences between control and THO horses. BAER, brainstem auditory-evoked responses; THO, temporohyoid osteoarthropathy.
Table 1B. BAER peak amplitudes and amplitude ratios.
Amplitudes for peaks I and V and amplitude ratios for V/I were calculated only in horses with identifiable peaks on BAER and shown in μV for control (left = 8/8, right = 8/8 ears) and THO (hearing ear: left 7/11, right = 6/11) horses using 2 derivations: V-M and V-C2. Median and ranges are shown.
P≤ .05 denotes differences between control and THO horses.
This study demonstrated that auditory system abnormalities as identified by BAER occur in horses with THO. The findings included complete unilateral BAER loss in 82% (n=9/11) and partial unilateral BAER loss in 18% (n=2/11) of the horses. Partial auditory abnormalities were also observed on the contralateral side in 56% (n=5/9) of the horses with complete unilateral BAER loss. These 5 horses represented 46% (n=5/11) of all horses with THO in this study. Absence of identifiable BAER peaks was most compatible with complete hearing loss; and increased peak latencies or difficulty identifying peaks or both were suggestive of partial hearing loss. The majority of horses with THO in this study had a complete absence of BAERs, which is most consistent with peripheral sensorineural hearing loss; however, severe conduction disturbances could not be ruled out.25 Bone conduction brainstem auditory-evoked potentials are routinely done in other species to help differentiate between the 2 types of hearing loss, but previous attempts to establish normal values in the horse were unsuccessful in 1 study.17 Pathology involving or compressing the vestibulocochlear nerve would likely result in peripheral sensorineural hearing loss. Remodeling of the stylohyoid bone, temporohyoid joint, and tympanic bulla, and narrowing of the acoustic meatus as identified on diagnostic imaging in all horses and at necropsy in 3 horses, resulting in cranial nerve compression, was compatible with our BAER findings. The delay in peak latencies noted in 2 horses (Figs 4, 5), though suggestive of a conductive abnormality, would also be consistent with insults to the distal portion of the vestibulocochlear nerve.9 This finding is worthy of further investigation because infection or inflammation of the external ear canal can result in conduction abnormalities and has been proposed as a possible cause of THO in horses.1 Furthermore, fluid was identified in the tympanic bulla in 3 horses, a finding that may be compatible with infection or inflammation. It was unclear if this abnormality was primary or secondary. Future histopathologic studies are indicated to determine whether increases in peak latencies and interpeak intervals and decreases in amplitudes (complete or partial) are related to demyelination, axonal dropout, or a combination of the two. Although there were statistical differences in peak amplitudes between control and THO horses, amplitude ratios were not significantly different. Amplitude ratios of evoked potentials are considered better indicators of abnormality than absolute peak amplitudes because amplitude ratios are less variable and less likely to be affected by technical problems.26
BAERs vary with age, sex, breed, head size, and temperature in other species.27,28 Differences in BAERs in our study by gender were not observed in controls or horses with THO. Breed differences were not established because of the low number of horses. Differences in BAERs by weight, height, and interaural distance were not investigated.11 Based on diagnostic findings, all but 2 horses had bilateral THO. However, only 3 horses had bilateral neurologic deficits. Both presence of clinical signs and abnormalities of the temporohyoid bones were strongly associated with auditory abnormalities, including absence of BAERs. The most common clinical signs included facial nerve paralysis and decreased tear production (n=11/11), vestibular nerve dysfunction (n = 8/11), and exposure ulcerative keratitis (n=7/11). Decreased tear production and exposure ulcerative keratitis were compatible with facial nerve dysfunction. Absence of BAERs was identified in 9 of 11 horses with facial paralysis and in 7 of 8 horses with vestibular dysfunction. Bilateral BAER abnormalities were observed in 3 horses with apparent exclusive unilateral neurologic deficits. Duration of clinical signs was not associated with BAER loss because abnormalities were found on BAER within hours of the earliest clinical signs.
There were methodological differences between our BAER study and previous studies performed in horses.8,10–15 Differences included type of stimulus transducer and derivations used. In addition, some studies were done under general anesthesia.10,15 The use of insert earphones, whereby the sound source is separated from the site of stimulus delivery by tubing 25 cm in length, adds an additional 0.9 ms to the recorded latencies for each peak when compared with those reported in other equine studies.bTables 1A and B contain the data obtained from these BAER recordings. Another difference was the derivations used: V-M and V-C2. The former (V-M) was consistent with that used in previous studies. Based on Holliday and Te Selle's canine BAER study regarding the effects of electrode position on wave form appearance, an additional derivation was adapted for use in the present study.23 They established that a noncephalic (caudal cervical or cranial thoracic) site was the ideal choice for inactive electrode placement, whereas in V-M recordings both electrodes were active.23 Because interelectrode distances were comparable, C2 was selected for use in horses. Both V-C2 and V-M derivations are routinely used at our institution for recording BAERs in horses. Peaks can be compared between the 2 derivations, often aiding in the labeling process. On the V-C2 recording, peak I comes in slightly earlier and the 2nd peak can usually be readily identified. Peak II may not be obvious on V-M, occasionally appearing only as a small deflection within IN (Fig 2). Peak V is frequently more distinct in V-C2 tracings. Most veterinary publications are in agreement on the designation of peaks I, V, and VN, in addition to VI and VII, when present. However, there is discrepancy in the labeling of the remaining peaks.28,29
BAER thresholds were not sought in this study because the main purpose of the study was to screen for BAER abnormality and assess its association with clinical signs and diagnostic findings. Maximal stimulus intensity was selected to compensate for conditions (eg, debris in the canal, thickened tympanic membrane) that could induce conductive hearing loss. Typically, peak latencies decrease as the stimulus intensity increases.27 These data are often displayed in a latency-intensity curve by plotting the latency to peak V over multiple stimulus intensities (usually in 10 dB increments). Further studies in both affected and normal horses are indicated to determine whether hearing thresholds vary between these groups.
BAER is a noninvasive, safe, inexpensive, and easy to perform diagnostic procedure that requires minimal restraint and provides objective information regarding the functional status of the auditory system. This study confirmed the diagnostic value of BAER testing for assessing the vestibulocochlear nerve in horses with THO. Presence of neurologic deficits (facial paralysis followed by vestibular nerve dysfunction) and abnormalities in the temporohyoid apparatus were strongly associated with BAER abnormalities. Furthermore, horses with apparent exclusive facial nerve dysfunction were shown to have BAER abnormalities. Few horses with exclusive unilateral neurologic deficits had bilateral auditory alterations. In conclusion, auditory abnormalities are common in horses with THO. Diseased horses appear to have peripheral sensorineural hearing loss that may be complete or partial; and in some cases of bilateral THO also have contralateral partial hearing loss.
aNicolet Biomedical Inc, Madison, WI
bTIP 300, Nicolet Biomedical Inc
cER3-14C, Etymotic Research Inc, Elk Grove Village, IL
dFE-2, Grass/Astro-Med Inc, West Warwick, RI
eStatXact8, Cytel Inc, Cambridge, MA
The authors thank Mr John Doval from the Media Lab for technical assistance.