Hearing in animals can be evaluated using electrodiagnostic procedures that assess the integrity of the peripheral and central auditory components. One such electrodiagnostic procedure is the brainstem auditory-evoked response (BAER) test.1 The BAER is unaffected by the level of arousal or a wide range of pharmacologic agents, including general anesthesia.1,2
Brainstem auditory-evoked response data in the dog suggest that the BAER test is far from standardized, resulting in large discrepancies between studies.3 A previous study4 has shown that absolute latencies, as well as interpeak latency intervals, are breed dependent, suggesting that BAER data should be developed by breed.
The Cavalier King Charles Spaniel (CKCS) is a breed that is prone to the disease primary secretory otitis media (PSOM) or otitis media with effusion (OME)5,6 As such, CKCS may experience conductive hearing loss due to PSOM.7 In a recent study5 of PSOM in CKCS, of the 39 CKCSs that presented for hearing loss, 31 (79%) had PSOM and 8 (21%) did not have PSOM. These results suggest that, in addition to conductive hearing loss due to PSOM, CKCS may also have a congenital hereditary or acquired sensorineural hearing loss.5
Another common disease in the CKCS is Chiari-like malformation (CM). Chiari malformation in humans is divided into CM type 1, CM type 2, CM type 3, and CM type 4. CM type 1 is defined by herniation of cerebellar tonsils and medulla oblongata through the foramen magnum and is most similar to the CM grade 2 in the dog.8 Auditory brainstem response (ABR) abnormalities, at the peripheral level as well as retrocochlear,8,9 have been identified in humans with CM type 1 and have been speculated to be due to compression of the vestibular and cochlear nucleus by the herniated tonsils, stretching of the cochleovestibular nerve over the porus acousticus, or distortion of the posterior inferior cerebellar artery resulting in ischemia.10
To evaluate hearing loss in the CKCS, based on ABR abnormalities reported in humans with CM, BAER data for the CKCS need to be established with respect to the degree of CM. Therefore, the purpose of this study was to establish breed-specific BAER data and to determine if BAER indexes differed based on CM grade in CKCS with owner-reported normal hearing. We hypothesized that there would be latency differences based on CM grade.
Materials and Methods
Inclusion criteria
Client-owned CKCS between the ages of 1 to 2 years were presented for entry into the study. To qualify for the study, dogs had to be in good general health, have no apparent hearing abnormalities as assessed by the owner, be fasted overnight for 12 hours, and be able to undergo general anesthesia. A general physical examination (including otoscopic examination) and neurological examination were performed, along with fluoroscopic screening before the magnetic resonance imaging (MRI).
Exclusion criteria
If on otoscopy, excessive exudates were found in the ear canal, hyperplasia/stenosis of the ear canal and/or bilateral bulging tympanic membranes, specifically the pars flaccida (which would be indicative of bilateral PSOM), all of which may cause conductive hearing loss, the CKCS was excluded from the study.
Study protocol
If the CKCS met all inclusion criteria, then it was enrolled in the study. All owners signed a consent form upon enrollment of their CKCS. Owners completed a questionnaire to assess any perceived neurological or otic abnormalities, which included scratching the neck, pruritic ears, past ear infections, neck pain, abnormal gait, droopy face/lip, head tilt, circling, shaking the head, difficulty yawning, yelping, and licking/chewing the paws. A standard neurological examination was performed by a board-certified neurologist consisting of evaluation of mental status (level and content of consciousness), gait and body posture, postural reactions (conscious proprioceptive positioning or hopping), cranial nerve function, and segmental spinal reflexes (extensor tone, patellar, flexor, and perineal and cutaneous trunci reflexes). In addition, the presence of signs of paraspinal hyperesthesia was evaluated by spinal palpation. The CKCS was then premedicated, intubated, and placed under general anesthesia; the following diagnostic tests were performed in the listed order.
CT scan
A CT scan was performed to evaluate the middle ear for soft tissue density, suggestive of PSOM. If a soft tissue density was identified in both middle ears, the CKCS was excluded from the study, as the material in the middle ear could lead to an abnormal BAER test. If a soft tissue density was identified in only 1 ear, the dog remained in the study and the opposite ear was used for the BAER testing.
CKCS were positioned in sternal recumbency with their heads placed in a positioning trough. Transverse images were acquired in a plane perpendicular to the hard palate, from the nose to mid cervical vertebrae 1. Computed tomography scans were performed using either an 8-slice helical CT scanner (LightSpeed Ultra; GE Healthcare) or a 128-slice CT scanner (GE Revolution EVO; GE Healthcare). For the 8-slice helical CT scanner, the slice thickness and index were 1.25 mm. The kilovoltage peak was 140, and the milliampere was 250. The display field of view was 12 to 15 cm. The scan time varied from 14 to 18 seconds. For the 128-slice CT scanner, the slice thickness was 1.25 mm. The kilovoltage peak was 120, and the milliampere was 220 to 500 with a display field of view of 25 cm. The scan time varied from 8 to 14 seconds. For both CT scanners, the images were reconstructed with both a standard (soft tissue) algorithm and a bone algorithm, Display settings were consistent with soft tissue display of 400 window width (WW) and 40 window level (WL) and bone display of 2,500 WW and 250 WL. Image interpretation was performed by a board-certified veterinary radiologist.
Brainstem auditory-evoked response test
One ear was randomly selected for BAER testing by a coin flip unless a soft tissue density was identified in 1 middle ear. In that case, the opposite ear was automatically chosen as the test ear. CKCS were placed in sternal recumbency for BAER testing, and a 3A insert earphone was positioned in the ear canal. Subdermal needle electrodes were placed at the vertex of the head (noninverting electrode) and just rostral to the base of each ear (tragus) with the inverting electrode inserted at the base of the test ear, and the ground electrode was inserted at the base of the contralateral ear (Supplementary Video S1).2,3 BAER testing was performed (SmartEP; Intelligent Hearing Systems) in the test ear using a 100-microsecond broadband click. The bandpass filter settings were 100 to 1,500 Hz. The rate was set to 20 clicks per second. The impedance used in all cases was 0 ohms. Recordings were performed by a board-certified dermatologist and made during the first 10 milliseconds after the stimulus. An alternating polarity was chosen to reduce stimulus artifact and mitigate wave distortion; 1,024 sweeps were performed. Two repeated averages were made from the ear. BAER measurements were initiated with 116 decibels peak equivalent sound pressure level (dB peSPL) click. The stimulus level was reduced by increments (eg, 102, 96, 93, 90, 87, 84, 81, 77, 75, 74, 71, 67, 63, 59, 56, 54, 50, 46, 39, 33, 24, and 19 dB), and the lowest intensity in decibels in which wave V was still present was designated as threshold.3
Magnetic resonance imaging
Magnetic resonance imaging was performed for evaluation of CM and SM. Dogs were imaged in dorsal recumbency using a 3.0 Tesla magnet (Achieva magnet; Phillips Healthcare) or 3.0 Tesla magnet (Ingenia magnet; Philips Healthcare). At minimum, T1-weighted (repitition time [TR] = 450 to 700 milliseconds; echo time [TE] = 8 milliseconds) and T2-weighted (TR = 3,500 to 5,000 milliseconds; TE = 110 milliseconds) images were obtained in the sagittal plane for review and included the head down to C7, with additional sequences and transverse images obtained on a case-by-case basis as medically indicated and dependent on presence and location of syringes.
Image interpretation was performed by a board-certified veterinary radiologist. A commercially available Digital Imaging and Communications in Medicine (DICOM) viewing software program (Horos2k v. 2.0.2; https://www.horosproject.org) was used to measure syrinx height (in mm), at the location of maximum apparent height, and grade the CM in the sagittal plane. CM and SM grades were assigned using the British Veterinary Association grading scheme. Using MRI findings, the classification scheme grades CM and SM into grades 0, 1, and 2. The CM grades range from no malformation (CM grade 0) to an indented cerebellum (CM grade 1) to CM grade 2 where the cerebellum is impacted or herniated through the foramen magnum. For grading SM, a grade 0 would indicate no central canal dilation (normal), SM grade 1 is where the central canal is dilated but less than 2 mm in diameter, and for SM grade 2, the central canal dilation is 2 mm or greater.11
BAER analysis
The morphology of the BAER waveform (pattern, overall shape, and presence or absence of waves) was assessed by a board-certified neurologist at all intensities for the presence of positive peaks as well as the presence of a large trough after wave V. The wave V threshold was the lowest stimulus intensity at which wave V was identified and was estimated based on all tested intensities.
The latency of each wave was defined as the time from the stimulus onset to the positive peak of each of the waves. The latencies were marked by a board-certified neurologist and dermatologist. The wave I-III, III-V, and I-V interpeak latencies were calculated as the latency between the 2 waves, respectively. Latencies were evaluated at 10 stimulus intensities.
Statistical analysis
Descriptive statistics were performed on latencies of peaks for all reported waves and interpeak latencies for all CKCS and between CM grades. Wave V mean (± SD) latencies were plotted against intensities and compared between CM grades (latency intensity function). The latencies were tested for normality with the assessment of skewness and kurtosis and a Shapiro-Wilk test. Median, interquartile range, and minimum and maximum values were used for latencies in which the distribution was not normal. For comparisons of latencies between dogs with respect to CM grades, Kruskal-Wallis tests were used. Analysis was performed using a commercially available statistical software package (SAS 9.4; SAS Institute), and statistical significance was set at P < .05.
Results
Demographics
Between April 2012 and June 2018, 29 CKCS were evaluated for entry into the study. Nine were disqualified: 4 due to inability to assess the tympanic membrane due to hyperplasia, stenosis, and/or wax accumulation and 5 due to bilateral PSOM. Therefore, 20 CKCS were enrolled and completed the study. Of these 20 CKCSs, 13 were Blenheim, 3 were tricolor, 3 were black and tan, and 1 was ruby in color; 12 (60%) were females (3 spayed) and 8 (40%) were males (5 castrated); and the mean age ± SD at presentation was 16.7 ± 3 months (range, 12 to 23 months).
Questionnaire
From the questionnaire, 7 (35%) CKCS had at least 1 abnormality (2 had 1, 1 had 2, 3 had 3, and 1 had 4) identified. Five CKCS were scratching their neck (mild; 2 only with their collar on, 1 resolved with oclacitinib), 3 had previous ear infections, 3 were licking/chewing their paws (2 resolved with either oclacitinib or diphenhydramine), 2 had pruritic ears (mild, 1 resolved with oclacitinib), 2 were shaking their head (mild), 1 had an abnormal gait (scoliosis), and 1 had vocalized (yelped) the week before enrollment.
Neurological examination
All dogs had at least 1 neurological abnormality identified (range, 1 to 5). Pain was identified in 15 CKCS (5 cervical, 3 cervical, lumbar, and lumbo-sacral; 2 cervical and lumbar, 2 cervical and lumbo-sacral, 2 lumbo-sacral, and 1 tail), decreased proprioceptive positioning in 11 CKCS (pelvic limb [3 unilateral, 5 bilateral], 1 pelvic and 1 thoracic limb [2], both pelvic and thoracic limbs [1]), and incomplete palpebral closure in 10 CKCS (3 unilateral, 7 bilateral), and menace was decreased unilaterally in 1 eye and absent in the other in 1 CKCS.
Advanced imaging
On CT scan, 6 (30%) CKCS had soft-tissue density identified unilaterally in the tympanic bulla (right bulla of 3 and left bulla of 3). CM and SM grades were assigned based on the results of the MRI. There were no CKCS with CM0; therefore, subsequent comparisons were made for CKCS with CM1 or CM2. There were 9 (45%) CKCS with CM1 and 11 (55%) with CM2. On the other hand, 55% of the CKCS were SM0, 3 (15%) were SM1, and 6 (30%) were SM2. The median syrinx height was 1.32 mm (range, 1 to 1.61 mm) and 2.83 mm (range, 2.02 to 4.22 mm) for CKCS with SM1 and SM2, respectively.
CM/SM grading was combined for each individual CKCS. Of the 9 CKCS with CM1, 8 (89%) were SM0 and 1 (11%) was SM1. Of the 11 CKCS with CM2, 3 (27%) were SM0 while 2 (18%) were SM1 and 6 (55%) were SM2.
BAER results
Wave morphology and threshold—Variations in BAER waveform morphology were identified (Table 1). Wave IV was not present at any intensity for any of the 20 CKCS. In addition to lacking wave IV, all CKCS with CM1 had at least 1 BAER morphologic variation: 4 had 1, 4 had 2, and 1 had 3 of these variations. For example, 1 CKCS had wave III disappear at 96 dB and reappear at 77 dB, wave II and III merge to form a complex (63 dB), and a bifid wave III (56, 54, 50, 46, 39 dB; Figure 1). Furthermore, for these 9 CKCS, 1 (11%) had no wave III, 4 (44%) had a bifid II or III wave, 5 (56%) had wave II-III or III-V merge to form a complex, and 5 (56%) had a wave I or wave III disappear and reappear (Table 1).
BAER waveform morphology variations for 20 Cavalier King Charles Spaniels
| Wave morphology variations | All CKCS, n = 20 (%) | CM1 CKCS, n = 9 (%) | CM2 CKCS, n = 11 (%) |
|---|---|---|---|
| No wave III | 2 (10%) | 1 (11%) | 1 (9%) |
| No wave IV | 20 (100%) | 9 (100%) | 11 (100%) |
| Bifid wave II | 10 (50%) | 3 (33%) | 6 (50%) |
| Bifid wave III | 2 (10%) | 1 (11%) | 1 (9%) |
| Wave II-III merge | 10 (50%) | 4 (44%) | 6 (55%) |
| Wave III-V merge | 5 (25%) | 1 (11%) | 4 (36%) |
| Wave I disappear/reappear | 6 (30%) | 2 (22%) | 4 (36%) |
| Wave III disappear/reappear | 5 (25%) | 3 (33%) | 2 (18%) |
| Wave V disappear/reappear | 1 (5%) | 0 | 1 (9%) |
BAER = Brainstem auditory-evoked response. CKCS = Cavalier King Charles Spaniels. CM = Chiari-like malformation.
Morphologic variations in brainstem auditory-evoked response testing of an individual Cavalier King Charles Spaniels. A—Wave III present at 116 and 102 dB and then disappearing at 96 dB and reappearing at 77 dB (highlighted in yellow). B—Wave II and III merging to form a complex at 63 dB (highlighted in yellow) and a bifid wave III at 56, 54, 50, 46, and 39 dB (highlighted in blue).
Citation: American Journal of Veterinary Research 84, 7; 10.2460/ajvr.23.03.0064
For the CM2 CKCS, in addition to lacking wave IV, all CKCS with CM2 had some type of BAER morphologic variation: 3 had 1, 4 had 2, 2 had 3, and 2 had 4 of these variations. For these 11 CKCS, 1 had no wave III (9%), 7 (64%) had a bifid II or III wave, 10 (91%) had wave II-III and/or III-V merge for form a complex and 7 (64%) had a wave I and/or wave III or wave V disappear and reappear (Table 1).
Threshold was defined as the lowest stimulus intensity at which wave V was identified and was estimated based on all tested intensities. The median threshold for all CKCS was 43 dB (range, 33 to 59). When the CKCS were grouped by CM grade, the median threshold for those CKCS with CM1 was 39 (range, 33 to 56) and for those with CM2 was 46 (range, 33 to 59). There were no significant differences in the threshold for CKCS with CM1 compared to those with CM2.
Wave latencies and latency intensity curve—Absolute latencies for waves I, II, III, and V and for interpeak latencies for I-III, I-V, and III-V were reported for all CKCS (Table 2) and between CM grades (Table 3). The absolute latencies for CKCS with CM2 were consistently longer than those for CKCS with CM1 at all tested intensities with the exception of wave II and V at 33dB with a significant difference (CM2 latency longer than CM1) for wave V at 102 dB (P = .04) and wave II at 74 dB (P = .008). The interpeak latency comparisons were inconsistent between CM1 and CM2. For interpeak I-III, the latencies were longer for those CKCS with CM2 except at 90 dB. Interpeak III-V latencies were longer for those CKCS with CM2 at 116, 90, and 81 dB but longer for CKCS with CM1 at 102 and 74 dB. Finally, for interpeak I-V, the latencies for CKCS with CM2 were longer from 116 down to 74 dB but were longer for CKCS with CM1 for the remaining intensities, 63 to 50 dB, with a significantly longer interpeak latency at 59 dB (P = .03). The wave V latency intensity function was plotted by CM grade (Figure 2).
Median (interquartile range) latencies for all dB for all CKCS
| Absolute latencies | Interpeak latencies | ||||||
|---|---|---|---|---|---|---|---|
| Intensity | Wave I | Wave II | Wave III | Wave V | I-III | I-V | III-V |
| 116 dB | 1.43 (0.13) | 2.30 (0.20) | 3.18 (0.28) | 4.10 (0.24) | 1.85 (0.20) | 2.74 (0.23) | 0.92 (0.15) |
| 102 dB | 1.47 (0.16) | 2.41 (0.18) | 3.33 (0.37) | 4.19 (0.20) | 1.95 (0.30) | 2.72 (0.20) | 0.80 (0.27) |
| 90 dB | 1.55 (0.15) | 2.53 (0.19) | 3.30 (0.50) | 4.32 (0.24) | 1.75 (0.43) | 2.71 (0.25) | 0.89 (0.25) |
| 81 dB | 1.68 (0.22) | 2.67 (0.30) | 3.22 (0.22) | 4.38 (0.25) | 1.60 (0.25) | 2.65 (0.25) | 1.18 (0.10) |
| 74 dB | 1.74 (0.18) | 2.83 (0.38) | 3.18 (0.07) | 4.40 (0.23) | 1.50 (0.03) | 2.70 (0.31) | 1.17 (0.07) |
| 63 dB | 2.09 (0.26) | 3.20 (0.32) | 4.78 (0.30) | 1.29 (0.68) | 2.56 (0.17) | 1.23 (0.60) | |
| 59 dB | 2.25 (0.29) | 3.29 (0.44) | 4.95 (0.27) | 0.92* | 2.67 (0.17) | 1.4 (0.70) | |
| 50 dB | 2.45 (0.20) | 3.45 (0.50) | 5.15 (0.42) | 1.13* | 2.65 (0.10) | 1.50 (0.14) | |
| 33 dB | 2.85 (0.20) | 3.95 (0.23) | 5.68 (0.20) | 2.93* | 1.58* | ||
Median (interquartile range) latencies for all dB for all CKCS separated by CM grade
| Absolute latencies | Interpeak latencies | |||||||
|---|---|---|---|---|---|---|---|---|
| Intensity | CM grade | Wave 1 | Wave II | Wave III | Wave V | I-III | I-V | III-V |
| 116 dB | 1 | 1.38 (0.10) | 2.23 (0.20) | 3.18 (0.20) | 4.10 (0.20) | 1.83 (0.23) | 2.73 (0.22) | 0.89 (0.15) |
| 2 | 1.43 (0.13) | 2.35 (0.20) | 3.38 (0.35) | 4.15 (0.23) | 1.88 (0.25) | 2.75 (0.16) | 0.95 (0.18) | |
| 102 dB | 1 | 1.45 (0.18) | 2.33 (0.23) | 3.30 (0.20) | 4.08 (0.12)% | 1.93 (0.22) | 2.68 (0.12) | 0.95 (0.23) |
| 2 | 1.50 (0.10) | 2.43 (0.15) | 3.41 (0.48) | 4.25 (0.27) | 1.98 (0.45) | 2.75 (0.21) | 0.79 (0.43) | |
| 90 dB | 1 | 1.50 (0.10) | 2.50 (0.25) | 3.30 (0.50) | 4.3 (0.20) | 1.80 (0.45) | 2.67 (0.23) | 0.83 (0.37) |
| 2 | 1.60 (0.12) | 2.53 (0.15) | 3.30 (0.58) | 4.35 (0.47) | 1.70 (0.50) | 2.78 (0.30) | 0.95 (0.45) | |
| 81 dB | 1 | 1.55 (0.10) | 2.53 (0.33) | 3.13 (0.25) | 4.35 (0.25) | 1.55 (0.25) | 2.65 (0.23) | 1.10 (0.50) |
| 2 | 1.73 (0.10) | 2.68 (0.23) | 3.23 (1.03) | 4.39 (0.15) | 1.65 (1.0) | 2.67 (0.20) | 1.19 (0.02) | |
| 74 dB | 1 | 1.64 (0.20) | 2.62(0.34)$ | 3.13 (0.15) | 4.36 (0.14) | 1.50 (0.02) | 2.65 (0.28) | 1.20 (0.12) |
| 2 | 1.78 (0.10) | 2.93 (0.27) | 3.66 (0.95) | 4.50 (0.23) | 1.96 (0.85) | 2.70 (0.47) | 0.86 (0.62) | |
| 63 dB | 1 | 2.05 (0.40) | 3.2 (0.45) | 4.75 (0.37) | 1.29 (0.68) | 2.63 (0.23) | 1.23 (0.60) | |
| 2 | 2.25 (0.17) | 3.2 (0.15) | 4.78 (0.27) | 2.55 (0.05) | ||||
| 59 dB | 1 | 2.15 (0.12) | 3.20 (0.35) | 4.93 (0.17) | 0.92* | 2.70(0.11)& | 1.4 (0.70) | |
| 2 | 2.29 (0.29) | 3.38 (0.25) | 4.95 (0.30) | 2.59 (0.14) | ||||
| 50 dB | 1 | 2.37 (0.21) | 3.4 (0.30) | 5.13 (0.25) | 1.13* | 2.68 (0.22) | 1.50 (0.14) | |
| 2 | 2.48 (0.23) | 3.63 (0.60) | 5.25 (0.49) | 2.62 (0.07) | ||||
| 33 dB | 1 | 4.04 (0.12) | 5.78 (0.22) | 1.58* | ||||
| 2 | 2.85 (0.20) | 3.75 (0.22) | 5.58 (0.21) | 2.93* | ||||
Relationship (mean ± SD) between wave V latency and click intensity (dB peSPL) in Cavalier King Charles Spaniels with Chiari-like malformation 1 (CM1) and CM2.
Citation: American Journal of Veterinary Research 84, 7; 10.2460/ajvr.23.03.0064
Discussion
Our study established breed-specific data of BAER measures for CKCS with CM1 and CM2. Specifically, we now have BAER data of absolute and interpeak latencies, as well as the threshold in CKCS based on CM grade. In addition, wave V latency intensity function was constructed with respect to CM grade that can be utilized to assess the presence and type of hearing loss in the CKCS. We hypothesized that the recorded BAER latencies would be longer in CKCS with CM2 versus the latencies in CKCS with CM0 or CM1. Unfortunately, and consistent with other recent publications in this breed, none of the CKCS in our study had CM0, and as such all comparisons were performed between those CKCS with CM1 versus those with CM2. This was not unexpected, as previous studies were unable to identify CKCS without the malformation.12,13
All CKCS regardless of CM grade had some type of morphologic change identified on the BAER testing. These changes may be normal for the CKCS, and as such, when morphologic changes are noted during BAER testing, a diagnosis of a pathologic condition should be made with caution. For example, in our study, wave IV was not identified in any CKCS, which is in agreement with previous BAER studies in canines4,14 as well as ferrets,15 where wave IV is often absent. On the other hand, the disappearance and reappearance of waves I, III, and V in some CKCS were unexpected. This morphologic change occurred in both CKCS with CM1 and CM2. The BAER is a measure of neural synchrony along the auditory pathway to the brainstem, and as one decreases intensity, there is an increase in latency and also a common finding of depletion of overall waveform morphology due to a reduced neural firing. It may be that the anatomy of the CKCS skull leads to changes in or damage to this pathway, causing variability in neural firing and conduction and resulting in poorer quality of certain waveforms at certain intensities.
In conclusion, BAER data in CKCS with respect to CM grade have been established. BAER indexes differed based on CM grade in CKCS, but the influence of the grade of the malformation, be it CM1 or CM2, is not always statistically significant or predictable.
Supplementary Materials
Supplementary materials are posted online at the journal website: avmajournals.avma.org.
Acknowledgments
This study was supported by the American Cavalier King Charles Spaniel Club Charitable Trust (ACKCSCCT) and The Ohio State University-College of Veterinary Medicine (OSU-CVM) Canine Intramural Grant (Paladin Fund).
The authors have nothing to declare.
The authors thank Tim Vojt for his assistance in creating Figures 1 and 2.
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