Annals of Otology, Rhinology & Laryngology http://aor.sagepub.com/
An Analysis of Vestibular Evoked Myogenic Potentials in Patients With Benign Paroxysmal Positional Vertigo Sertac Yetiser, Dilay Ince and Murat Gul Ann Otol Rhinol Laryngol published online 1 May 2014 DOI: 10.1177/0003489414532778 The online version of this article can be found at: http://aor.sagepub.com/content/early/2014/05/01/0003489414532778
Published by: http://www.sagepublications.com
Additional services and information for Annals of Otology, Rhinology & Laryngology can be found at: Email Alerts: http://aor.sagepub.com/cgi/alerts Subscriptions: http://aor.sagepub.com/subscriptions Reprints: http://www.sagepub.com/journalsReprints.nav Permissions: http://www.sagepub.com/journalsPermissions.nav
>> OnlineFirst Version of Record - May 1, 2014 What is This?
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
532778
research-article2014
AORXXX10.1177/0003489414532778Annals of Otology, Rhinology & LaryngologyYetiser et al
Article
An Analysis of Vestibular Evoked Myogenic Potentials in Patients With Benign Paroxysmal Positional Vertigo
Annals of Otology, Rhinology & Laryngology 1–10 © The Author(s) 2014 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/0003489414532778 aor.sagepub.com
Sertac Yetiser, MD1, Dilay Ince, MA1, and Murat Gul, MS2
Abstract Objective: Vestibular evoked myogenic potentials (VEMPs) selectively test the vestibular end-organ. The aim of this study was to analyze how the site of the diseased canal, type of particulate deposition, duration of symptoms, severity of nystagmus, recurrence, and age affect the VEMP in patients with benign paroxysmal positional vertigo (BPPV). Methods: One hundred two patients were enrolled in the study between 2009 and 2012. There were 36 men and 66 women with ages ranging from 16 to 71 years (mean age, 42.28 ± 11.29 years). Patients with BPPV were tested with rollon and head-hanging maneuvers under video-electronystagmography monitoring and with air conduction cervical VEMP testing. Patients were grouped for duration, severity, recurrence, age, site of canal involvement, and so on, and the results were compared in each subgroup. Kruskal–Wallis and Mann–Whitney U tests were used for the comparative analysis. Results: Twenty-four patients (23.5%) had a gross VEMP abnormality (absence of VEMP in 6 and greater than 25% depression of the amplitude in 18). Abnormality of VEMPs was not correlated with factors including age, severity of nystagmus, number of maneuvers applied, and the site of canal involvement (P < .05). However, persistence or recurrence of symptoms has an effect on VEMP results (P = .016). Conclusion: Vestibular evoked myogenic potential is a useful tool to study the otolithic function in patients with BPPV and should be included in the test battery. Keywords vestibular evoked myogenic potential, benign paroxysmal positional vertigo
Introduction Benign paroxysmal positional vertigo is one of the most common peripheral vestibular problems seen at outpatient clinics. Migrated otoconia either freely floating inside the canal or adhering to the cupula can provoke nystagmus and vestibular disturbance of sudden onset during head motion. The origin of these deposits is claimed to be the macular neuroepithelium. The site of the affected canal and the type of particulate deposition can be justified after roll-on and head-hanging maneuvers. The pathophysiological mechanism that induces the sense of vertigo in patients with benign paroxysmal positional vertigo (BPPV) is well documented.1 However, functional assessment of the saccule and the utricle has been the subject of clinical research for many years. Utricular or perhaps saccular degeneration is assumed to be the underlying cause and the source of so-called troublesome crystalloids. Selective testing of the vestibular end-organ was possible after introduction of vestibular evoked myogenic potential (VEMP) to the clinic by Colebatch and colleagues.2,3 Since then, VEMP testing has gradually become part of the vestibular test battery. It is
a short latency myogenic wave recorded from the sternocleidomastoid muscle (SCM) after intense acoustic stimulus and is used to assess the integrity and function of the sacculo-collic reflex.4 Neural bundles from the superior vestibular nerve mainly collect impulses from lateral and superior semicircular canals and the utricle. The inferior vestibular nerve is connected to the posterior semicircular canal and the saccule and is the main pathway of VEMPs. Patients with BPPV may show abnormal findings on VEMP.5 However, it is not known how this is related to the site of the affected canal (lateral or posterior), the type of particulate deposition (canalolithiasis or cupulolithiasis), the duration of symptoms, the severity of nystagmus on 1
Department of Otorhinolaryngology–Head and Neck Surgery, Anadolu Medical Center, Kocaeli, Turkey 2 Department of Statistics, University of Giresun, Giresun, Turkey Corresponding Author: Sertac Yetiser, MD, Department of Otorhinolaryngology–Head and Neck Surgery, Anadolu Medical Center, Cumhuriyet mah, 2255 sok, No:3, Gebze 41400, Kocaeli, Turkey. Email: [email protected]
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
2
Annals of Otology, Rhinology & Laryngology
video-electronystagmography (VNG), or age. Therefore, we aimed to analyze the different aspects of VEMP testing in patients with BPPV.
Materials and Methods One hundred two patients with VNG-confirmed BPPV problems who had been recruited between 2009 and 2012 were enrolled in the study. A verbal and a signed informed consent were obtained from each patient and control subject. The procedures were in accordance with the ethical standards of the Declaration of Helsinki and of the institutional review board. Those with hearing loss, tinnitus, spontaneous nystagmus, abnormal ear drum, or other vestibular or neurologic problems and those who used medication before testing that could affect the vestibular system and/or muscle tone were excluded. There were 36 men and 66 women with ages ranging from 16 to 71 years (mean age, 42.28 ± 11.29 years). All patients had normal otoscopic examination, normal hearing threshold, and no problems other than BPPV. The affected side for lateral canal BPPV (LC-BPPV) was determined according to the severity of nystagmus as seen on VNG recording (Micromed, Inc, Chatham, Illinois,USA). The type, duration, and direction of nystagmus were recorded with an infrared wireless video camera. Patients with posterior canal BPPV (PC-BPPV) were treated with Epley and patients with LC-BPPV were treated with either barbeque or Semont maneuvers. Patients who had recurrent symptoms after maneuvers were tested again by VNG within a week and were subjected to therapeutic maneuvers as dictated by VNG until resolution of symptoms. Air conduction cervical VEMP testing was used (Eclipse EP25; Interacoustics, Eden Prairie, Minnesota, USA) to test the patients. Patients with absence of bilateral VEMPs in the presence of unilateral BPPV were excluded. Fifteen healthy participants with no vestibular problems and intact eardrums (8 men, 7 women; mean age, 42.09 ± 9.28 years) were also tested with VEMP as the control group. Since the latency and amplitude difference between the ears was so small (± 1.00), the sum of data from both ears was set as 1 single control group (30 ears). Vestibular evoked myogenic potentials were recorded with disposable, self-adhesive, pregelled surface electrodes. Electrode impedances were below 5 kΩ. The active electrode was placed over the middle of the SCM and the reference electrode was placed over the upper sternum. The ground electrode was placed over the forehead. Tone-burst sound stimuli of 95 dB nHL with rarefaction polarity, 5 Hz stimulus repetition rate, 1 ms rise/fall time, and 2 ms plateau time were delivered at 500 Hz; 200 sweeps were averaged. Myogenic responses were amplified and band-pass filtered (800-10 Hz). The test was repeated with 85, 75, and 65 dB stimuli in search of the threshold. Stimulation was presented monaurally via an ipsilateral ear phone inserted in foam ear tips (Ear tone-ABR;
Interacoustics) while the participants turned their heads to the counter lateral side in the sitting position and the responses were recorded from the ipsilateral SCM. The test was reviewed twice on each occasion to ensure reproducibility. However, no more than 2 tests were done and the participants were allowed to have some rest between trials to prevent fatigue. The procedure was repeated on both sides. Results of VEMP were evaluated by the existence of the first successive p1-n1 biphasic wave. If this was not detected at 95 dB stimulation, the result was accepted as the absence of VEMP. Biphasic VEMP waves seen at 75 or 65 dB stimulation were accepted as VEMP with a lower threshold. Latency and amplitude measurements were made on potentials obtained at 95 dB stimulation. The latency and the amplitude of p1 and n1 waves and interpeak amplitude and latency differences were measured especially to determine the magnitude of the whole electrical activity and also to determine whether the myogenic potential is distorted or not. First, the response was observed during unrectified electromyograms (EMGs). The raw values were then converted into scaled scores. Since the VEMP amplitude is dependent on ongoing muscle EMG level and requires tonic contraction of the muscle, both corrected and raw EMG amplitudes were used in all comparative analyses.6,7 Results were given as mean and standard deviation. The corrected amplitudes were calculated by dividing the raw amplitudes by the prestimulus background EMG. Interaural p1-n1 amplitude symmetry was calculated as Lamp (1 with larger amplitude) – Samp (1 with smaller amplitude) / REamp (Right ear amplitude) + LEamp (Left ear amplitude) × 100. Greater than 25% asymmetry was accepted as abnormal. The percentage of vestibular asymmetry in the control group was measured as (REamp – LEamp / REamp + LE amp) × 100. Patients who required more than 2 repositioning maneuvers for the resolution of symptoms were considered to be recurrent or resistive cases. Patients who had severe nystagmus up to 50 to 60 seconds (or even more) during VNG testing were considered to be severe cases. Patients were grouped as those with PC-BPPV and LC-BPPV, those with cupulolithiasis and canalolithiasis, those younger than 30 years of age, those 31 to 50 years old, and those older than 51, those who had symptoms for less than 2 months and those with symptoms for more than 2 months, those with nystagmus lasting up to 1 minute or more and those with less severe nystagmus, and finally, those with recurrent and nonrecurrent symptoms (patients who had been cured after 1 single maneuver and those who needed to be treated with several maneuvers). Vestibular evoked myogenic potential results were compared between each subgroup. Patients with unilateral problems based on VNG were always grouped as affected and nonaffected (healthy) ears and groups were compared with each other and also with controls. However, since the sum of data from
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
3
Yetiser et al Table 1. Comparative Analysis of VEMP in the Affected and Healthy Ears of BPPV Patients Younger Than 30 Years (9 Patients), Between 31 and 50 Years Old (56 Patients), and Older Than 50 Years (18 Patients).a Age Group, y Ears Affected Healthy Affected Healthy Affected Healthy Affected Healthy Affected Healthy Affected Healthy
VEMP p1 lat (ms) p1 lat (ms) p1 amp (µV)b p1 amp (µV)c p1 amp (µV)b p1 amp (µV)c n1 lat (ms) n1 lat (ms) n1 amp (µV)b n1 amp (µV)c n1 amp (µV)b n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 lat (ms) p1-n1 lat (ms)
< 30
31-50
> 50
17.29 ± 3.89 17.29 ± 2.98 18.64 ± 8.77 0.39 ± 0.21 16.30 ± 8.23 0.36 ± 0.18 23.88 ± 4.49 24.70 ± 3.49 28.36 ± 15.19 0.63 ± 0.35 24.51 ± 16.09 0.52 ± 0.34 46.70 ± 22.79 0.98 ± 0.52 40.96 ± 23.72 0.86 ± 0.51 7.84 ± 1.41 9.04 ± 2.97
17.38 ± 2.95 17.44 ± 3.02 16.60 ± 9.72 0.37 ± 0.22 17.28 ± 8.95 0.36 ± 0.21 27.13 ± 3.13 26.25 ± 3.25 25.30 ± 15.67 0.54 ± 0.36 27.38 ± 14.64 0.62 ± 0.34 41.83 ± 24.91 0.90 ± 0.58 45.78 ± 23.29 0.99 ± 0.54 8.29 ± 1.78 8.56 ± 1.67
19.24 ± 3.89 18.15 ± 4.13 12.87 ± 8.35 0.30 ± 0.20 15.09 ± 10.11 0.36 ± 0.23 26.16 ± 4.25 26.51 ± 3.88 21.18 ± 12.70 0.43 ± 0.30 20.73 ± 14.08 0.49 ± 0.34 35.96 ± 19.25 0.78 ± 0.47 36.66 ± 23.73 0.88 ± 0.49 7.07 ± 1.63 8.34 ± 2.93
P Value .229 1.000, .823, .436 .247 .585, .699, .349 .940 .617, .729, .398 .233 .685, .752, .807 .461 .630, .468, .451 .595 .573, .221, .863 .499 .630, .472, .920 .760 .652, 1.000, .558 .037d .164, .680, .114
Abbreviations: BPPV, benign paroxysmal positional vertigo; VEMP, vestibular evoked myogenic potential. a Patients with bilateral problems or those with no unilateral VEMP response were excluded. No statistically significant difference was found when comparing each parameter between the affected and healthy ears. Apart from p1-n1 latency, comparative analysis of all parameters in the affected ears of the 3 age subgroups was not statistically significant. The first row of P values in each subgroup represents comparison of the affected ears of the 3 age subgroups. The second row shows the results of comparison of the affected and healthy ears of the 3 age subgroups: < 30, 31-50, and > 50 years, respectively. b Raw amplitudes. c Corrected mean amplitudes. d Statistically significant (P < .05).
both ears of the control subjects was set as 1 single agematched control group, the control group was not included in the age-group analysis (Table 1). Patients with no VEMP response were not included in group analysis. The Kruskal– Wallis test was used for multiple variance analysis of the groups in Table 1 and the Mann–Whitney U test was used for comparative analysis of the groups in Tables 2 to 5. Statistical significance was set at P < .05.
Results VEMP Results in General Vestibular evoked myogenic potential responses were elicited in all controls. In the study group (102 patients), VEMP responses were absent in 6 patients and amplitude was ipsilaterally depressed in 18 patients with unilateral BPPV, that is, the p1-n1 interaural amplitude difference was greater than 25%. Therefore, in total, 24 patients (23.5%) had a gross VEMP abnormality. Four patients also had lower VEMP thresholds. Excluding those patients with gross abnormality, the rest of the patients were classified into different subgroups.
Young Versus Older Patients Nine patients were younger than 30 years, 56 patients were between 31 and 50 years old, and 18 were older than 51 years. Apart from p1-n1 latency, comparative analysis of all VEMP parameters in the affected ears of the 3 age groups was not statistically significant (P > .05), although older patients had more depressed amplitude and prolonged latency. No statistically significant difference was found when comparing each parameter between the affected and healthy ears (Table 1).
Severity of Nystagmus Nineteen patients with BPPV had longer and intensive nystagmus lasting up to a minute regardless of canal involvement compared with 63 patients having less severe nystagmus. Comparative analysis of all VEMP parameters of the affected ears between the 2 groups and the controls was not statistically significant (P > .05). No statistically significant difference was found when comparing each parameter between the affected and healthy ears (Table 2).
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
4
Annals of Otology, Rhinology & Laryngology
Table 2. Comparative Analysis of VEMP in the Affected and Healthy Ears of Patients With BPPV Having Longer and Intensive (19 Patients) Nystagmus and Those With Less Severe Nystagmus (63 Patients).a Severity Groups Severe Nonsevere P value Severe Nonsevere P value Severe Nonsevere P value Severe Nonsevere P value Severe Nonsevere P value Severe Nonsevere P value
VEMP
Affected Ears
Healthy Ears
Controls
P Value
p1 lat (ms) p1 lat (ms)
17.10 ± 2.95 18.20 ± 3.44 .224 15.60 ± 9.33 0.32 ± 0.18 15.43 ± 9.20 0.32 ± 0.21 .792, .792 24.84 ± 2.87 25.87 ± 3.80 .139 27.27 ± 19.87 0.52 ± 0.36 26.27 ± 21.21 0.50 ± 0.34 .632, .841 40.82 ± 26.31 0.86 ± 0.51 40.69 ± 23.08 0.82 ± 0.54 .887, .778 7.68 ± 1.69 8.27 ± 1.92 .197
17.40 ± 2.04 17.51 ± 3.43
15.71 ± 1.06
16.11 ± 9.74 0.44 ± 0.21 15.66 ± 8.92 0.35 ± 0.20
23.80 ± 6.75 0.45 ± 0. 21
25.84 ± 1.82 25.49 ± 3.57
25.14 ± 1.41
29.20 ± 16.63 0.66 ± 0.32 25.95 ± 13.74 0.56 ± 0.32
35.54 ± 8.05 0.74 ± 0.34
49.30 ± 25.70 1.09 ± 0.52 40.20 ± 21.74 0.97 ± 0.48
58.69 ± 13.6 1.23 ± 0.53
8.42 ± 1.90 8.56 ± 2.07
9.42 ± 1.01
.319, .224 .316, .221 .224, .145 .105, .104 .764, .360 .425, .325 .225, .224 .625, .617 .312, .125 .205, .116 1.000, .354 .397, .272 .338, .188 .176, .164 1.000, .332 .388, .172 .214, .132 .314, .222
p1 amp (µV)b p1 amp (µV)c p1 amp (µV)b p1 amp (µV)c n1 lat (ms) n1 lat (ms) n1 amp (µV)b n1 amp (µV)c n1 amp (µV)b n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 lat (ms) p1-n1 lat (ms)
Abbreviations: BPPV, benign paroxysmal positional vertigo; VEMP, vestibular evoked myogenic potential. a Patients with bilateral problems or those with no unilateral VEMP response were excluded. No statistically significant difference was found when comparing each parameter between the affected ears, healthy ears, and those of the control subjects. Comparative analysis of all parameters in affected ears of the 2 subgroups was not statistically significant. P values as the result of comparison of the affected ears of the 2 subgroups are given below each parameter (for the amplitudes, first raw and then corrected amplitudes, respectively). P values as the result of comparison of the affected ears with healthy ears and the affected ears with the controls are given in the last column, respectively. b Raw amplitudes. c Corrected mean amplitudes.
Recurrent Versus Nonrecurrent Disease There were 54 patients who were cured after 1 single maneuver regardless of the site of the canal disease, whether lateral or posterior. Twenty-seven patients required 2 or more maneuvers. Comparative analysis of VEMP in the affected and healthy ears in BPPV patients who were cured with 1 single maneuver and those who needed 2 or more therapeutic maneuvers showed no statistically significant difference. Comparison of each parameter between affected ears of the 2 subgroups was not statistically significant (P > .05) (Table 3).
Lateral Versus Posterior Canal BPPV Forty-two patients with unilateral LC-BPPV and 35 patients with unilateral PC-BPPV were included. Fifteen patients had combined or bilateral BPPV. Of those, 9 had bilateral PC-BPPV and 1 patient had LC-BPPV on 1 side and PC-BPPV on the other side. Five patients were identified as
having multiple canals, PC- and LC-BPPV on the same side, as seen on roll-on and head-hanging maneuvers. Patients with bilateral problems or those with no unilateral VEMP response were excluded. Comparative analysis of all parameters in the affected ears of the 2 subgroups was not statistically significant (P > .05), although it is interesting that patients with lateral canal problems had more depressed p1 and n1 amplitudes (Table 4). Apart from p1 amplitude in patients with LC-BPPV, no statistically significant difference was found when comparing each parameter between the affected, healthy ears and those of the control subjects.
Canalolithiasis Versus Cupulolithiasis There were 18 patients with cupulolithiasis and 24 patients with canalolithiasis of the LC-BPPV. Comparative analysis of all parameters in the affected ears of the 2 subgroups was not statistically significant (P > .05), although it is
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
5
Yetiser et al Table 3. Comparative Analysis of VEMP in the Affected and Healthy Ears of BPPV Patients Who Were Cured With 1 Single Maneuver (54 Patients) and Those Who Needed 2 or More Therapeutic Maneuvers (27 Patients).a Recurrence Recurrent Single P value Recurrent Single P value Recurrent Single P value Recurrent Single P value Recurrent Single P value Recurrent Single P value
VEMP
Affected Ears
Healthy Ears
Controls
P Value
p1 lat (ms) p1 lat (ms)
18.12 ± 3.07 17.90 ± 3.56 .485 16.09 ± 8.27 0.34 ± 0.19 15.03 ± 9.44 0.31 ± 0.20 .920, .504 26.17 ± 3.02 25.87 ± 4.01 .729 24.72 ± 14.54 0.52 ± 0.32 24.20 ± 15.36 0.49 ± 0.34 .887, .672 41.31 ± 22.17 0.88 ± 0.50 39.79 ± 24.16 0.81 ± 1.05 .741, .555 7.93 ± 1.84 8.33 ± 1.95 .386
17.30 ± 3.44 17.52 ± 3.22
15.71 ± 1.06
18.22 ± 9.91 0.31 ± 0.23 17.29 ± 10.24 0.37 ± 0.20
23.80 ± 6.75 0.45 ± 0.20
26.32 ± 5.17 25.91 ± 3.46
25.14 ± 1.41
27.27 ± 17.18 0.57 ± 0.41 25.06 ± 13.78 0.58 ± 0.36
35.54 ± 8.05 0.74 ± 0.39
45.79 ± 27.27 1.01 ± 0.57 41.34 ± 22.09 0.91 ± 0.49
58.69 ± 13.6 1.23 ± 0.55
8.59 ± 2.29 8.72 ± 2.01
9.42 ± 1.01
.375, .124 .561, .432 .206, .112 .540, .236 .203, .193 .391, .172 .863, .504 1.000, .876 .568, .166 .505, .184 .791, .241 .175, .125 .519, .212 .378, .144 .672, .192 .275, .164 .250, .156 .275, .247
p1 amp (µV)b p1 amp (µV)c p1 amp (µV)b p1 amp (µV)c n1 lat (ms) n1 lat (ms) n1 amp (µV)b n1 amp (µV)c n1 amp (µV)b n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 lat (ms) p1-n1 lat (ms)
Abbreviations: BPPV, benign paroxysmal positional vertigo; VEMP, vestibular evoked myogenic potential. a Patients with bilateral problems or those with no unilateral VEMP response were excluded. No statistically significant difference was found in the comparison of each parameter between the affected ears, healthy ears, and those of the control subjects, and comparative analysis of the affected ears of the 2 subgroups was not statistically significant. P values as the result of comparison of the affected ears of the 2 subgroups are given below each parameter (for the amplitudes, first raw and then corrected amplitudes, respectively). P values as the result of comparison of the affected ears with healthy ears and the affected ears with the controls are given in the last column, respectively. b Raw amplitudes. c Corrected mean amplitudes.
interesting that patients with canalolithiasis had more depressed p1 and n1 amplitudes (Table 5). Apart from p1 amplitude in patients with canalolithiasis, no statistically significant difference was found when comparing each parameter between the affected ears, healthy ears, and those of the control subjects.
Short Versus Long Duration of Symptoms There were 36 patients who had symptoms lasting longer than 2 months and 43 patients with a shorter duration of symptoms. Comparative analysis of all parameters, apart from p1 latency, in the affected ears of the 2 subgroups was not statistically significant. Patients with a longer duration of symptoms had significantly longer p1 latency compared with those having a shorter duration of symptoms (P < .05). No statistically significant difference was found when comparing each parameter between the affected ears, healthy ears, and those of the control subjects (Table 6).
Discussion The pathophysiology of BPPV is primarily based on such a mechanical mechanism that the deposits that are freely floating or attached to the cupula trigger an additional cupular movement, disturbing the inertia during head motion, which makes the cupula more sensitive to gravitational forces. This generally explains the definite symptoms of the patients. However, degeneration of neural elements and their interaction with otolithic and canalicular receptors may also participate in some patients with BPPV. Gacek1 has found a significant decrease in superior and inferior ganglionary vestibular cells in BPPV. Some patients temporarily feel a loss of balance and postural instability after resolution of an acute episode of vertigo. Von Brevern et al8 have found an otolithic dysfunction most probably secondary to utricular degeneration. Di Girolano et al9 have pointed out the disturbed postural control in patients with BPPV. Residual dizziness even after a successful repositioning
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
6
Annals of Otology, Rhinology & Laryngology
Table 4. Comparative Analysis of VEMP in the Affected and Healthy Ears of BPPV Patients Who Had Posterior (35 Patients) or Lateral (42 Patients) Canal Disease.a PC- and LC-BPPV PC LC P value PC LC P value PC LC P value PC LC P value PC LC P value PC LC P value
VEMP
Affected Ears
Healthy Ears
Controls
P Value
p1 lat (ms) p1 lat (ms)
18.38 ± 3.76 17.34 ± 3.34 .208 17.72 ± 10.39 0.36 ± 0.221 13.75 ± 8.53 0.29 ± 0.18 .072, .136 25.90 ± 4.04 26.08 ± 3.46 .862 26.72 ± 18 0.57 ± 0.38 24.18 ± 14.63 0.48 ± 0.28 .495, .224 44.42 ± 27.70 0.94 ± 0.58 36.18 ± 21.36 0.77 ± 0.45 .144, .168 7.98 ± 1.86 8.43 ± 2.15 .263
17.90 ± 3.71 17.29 ± 3.17
15.71 ± 1.06
16.37 ± 9.96 0.37 ± 0.22 17.68 ± 8.40 0.38 ± 0.17
23.80 ± 6.75 0.45 ± 0.19
25.00 ± 4.03 26.04 ± 2.58
25.14 ± 1.41
24.63 ± 4.03 0.57 ± 0.33 26.63 ± 14.84 0.56 ± 0.32
35.54 ± 8.05 0.74 ± 0.42
41.02 ± 23.63 0.93 ± 0.51 44.05 ± 22.52 0.94 ± 0.48
58.69 ± 13.6 1.23 ± 0.49
8.12 ± 2.35 8.66 ± 1.57
9.42 ± 1.01
.618, .475 .672, .553 .585, .177 .792, .376 .039, .021d .024, .019d .920, .891 1.000, .798 .477, .218 1.000, .233 .185, .074 .174, .063 .585, .388 .765, .661 .088, .076 .295, .117 .499, .227 .573, .233
p1 amp (µV)b p1 amp (µV)c p1 amp (µV)b p1 amp (µV)c n1 lat (ms) n1 lat (ms) n1 amp (µV)b n1 amp (µV)c n1 amp (µV)b n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 lat (ms) p1-n1 lat (ms)
Abbreviations: BPPV, benign paroxysmal positional vertigo; LC, lateral canal; PC, posterior canal; VEMP, vestibular evoked myogenic potential. a Patients with bilateral problems or those with no unilateral VEMP response were excluded. Apart from p1 amplitude in patients with LC-BPPV, no statistically significant difference was found when comparing each parameter between the affected ears, healthy ears, and those of the control subjects. Comparative analysis of all parameters in the affected ears of the 2 subgroups was not statistically significant. P values as the result of comparison of the affected ears of the 2 subgroups are given below each parameter (for the amplitudes, first raw and then corrected amplitudes, respectively). However, P values as the result of comparison of the affected ears with healthy ears and the affected ears with the controls are given in the last column, respectively. b Raw amplitudes. c Corrected mean amplitudes. d Statistically significant (P < .05).
maneuver shows that BPPV is not only a disorder of the semicircular canals.10 It has been demonstrated that positive VEMP results are related not only to the integrity of the vestibular nerve but also to the normal functioning otolithic organ. Normative data analysis suggests that these potentials are very stable and reproducible.4,11 Test–retest consistency is reported to be high regardless of the time interval between the tests and the type of stimulus used.12-14 Diagnostic capacity is also as good as other modalities.15,16 However, patients with BPPV show less abnormal results on VEMP. We have found 23.5% abnormal VEMP results in this study. Hong et al17 found 25.8% VEMP abnormality in BPPV patients, which was less common compared to those patients with vestibular neurinitis and Ménière’s disease who had 36.6% and 69% abnormality, respectively. Akkuzu et al18 compared BPPV and patients with Ménière’s disease and found
a 30% abnormality in BPPV patients as compared to 50% abnormality in patients with Ménière’s disease. Children with BPV have been reported to have abnormal VEMP results.19,20 Yang et al21 reported abnormal VEMP results, especially in BPPV patients who are chronic and resistive, and proposed more extensive damage to the saccule as the disease recurs. We have observed a correlation between increasing age and prolongation of latency and a decrease in the amplitude of VEMPs in patients with BPPV. However, even though older patients had smaller amplitudes and longer latencies, comparative analysis of the 3 different age groups was not statistically significant. One possible influence on the VEMPs in older patients comes from less muscle tension. However, the authors state that this contribution is small and is not likely to account for the age-related changes. A decline in vestibular function with aging measured by
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
7
Yetiser et al
Table 5. Comparative Analysis of VEMP in the Affected and Healthy Ears in BPPV Patients Who Had Cupulolithiasis (18 Patients) or Canalolithiasis (24 Patients) of the Lateral Canal.a Canalolithiasis vs Cupulolithiasis Canalolithiasis Cupulolithiasis P value Canalolithiasis Cupulolithiasis P value Canalolithiasis Cupulolithiasis P value Canalolithiasis Cupulolithiasis P value Canalolithiasis Cupulolithiasis P value Canalolithiasis Cupulolithiasis P value
VEMP p1 lat (ms) p1 lat (ms) p1 amp (µV)b p1 amp (µV)c p1 amp (µV)b p1 amp (µV)c n1 lat (ms) n1 lat (ms) n1 amp (µV)b n1 amp (µV)c n1 amp (µV)b n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 lat (ms) p1-n1 lat (ms)
Affected Ears
Healthy Ears
Controls
P Value
17.51 ± 3.44 17.68 ± 3.15 .863 11.91 ± 5.93 0.25 ± 0.13 16.20 ± 10.92 0.34 ± 0.23 .110, .093 26.18 ± 3.81 25.96 ± 2.91 .100 20.11 ± 11.21 0.44 ± 0.24 25.26 ± 15.52 0.52 ± 0.35 .218, .343 32.16 ± 16.10 0.69 ± 0.35 41.53 ± 25.40 0.87 ± 0.57 .161, .166 8.58 ± 1.92 8.24 ± 2.42 .619
17.29 ± 2.37 17.29 ± 4.00
15.71 ± 1.06
16.00 ± 7.12 0.34 ± 0.15 19.93 ± 9.38 0.43 ± 0.22
23.80 ± 6.75 0.45 ± 0.17
26.04 ± 1.79 26.03 ± 3.35
25.14 ± 1.41
23.70 ± 13.97 0.50 ± 0.31 30.54 ± 14.97 0.64 ± 0.34
35.54 ± 8.05 0.74 ± 0.32
39.39 ± 20.57 0.83 ± 0.42 50.27 ± 25.50 1.08 ± 0.53
58.69 ± 13.6 1.23 ± 0.41
8.68 ± 1.73 8.62 ± 1.33
9.42 ± 1.01
.792, .584 .742, .572 .038, .020d .024, .018d .287, .301 .235, .455 .863, .856 .920, .862 .381, .246 .397, .118 .312, .407 .283, .377 .189, .090 .310, .283 .229, .435 .303, .552 .842, .207 .563, .132
Abbreviations: BPPV, benign paroxysmal positional vertigo; VEMP, vestibular evoked myogenic potential. a Patients with bilateral problems or those with no unilateral VEMP response were excluded. Apart from p1 amplitude in patients with canalolithiasis, no statistically significant difference was found when comparing each parameter between the affected ears, healthy ears, and those of the control subjects. Comparative analysis of all parameters in the affected ears of the 2 subgroups was not statistically significant. P values as the result of comparison of the affected ears of the 2 subgroups are given below each parameter (for the amplitudes, first raw and then corrected amplitudes, respectively). However, P values as the result of comparison of the affected ears with healthy ears and the affected ears with the controls are given in the last column, respectively. b Raw amplitudes. c Corrected mean amplitudes. d Statistically significant (P < .05).
VEMP in the elderly population, especially in those older than 60 years, is probably due to age-related degenerative changes in neural and sensory elements in structures lying along the pathway.22-26 Studies on neuroanatomy indicate a decrease in the number of otoconia, vestibular hair cell loss, and a decrease in the number of neurons in the vestibular nucleus with aging.27,28 On the other hand, latency seems to be more reliable than amplitude since amplitude has more variability and can be affected by basic muscle activity, the patient’s position, and other general conditions. Corrected amplitudes as well as raw amplitudes were also included in the comparative analysis of this study to overcome the problem of amplitude dependency on the intensity of tonic contraction of the muscle. However, the difference between the affected ears in the 3 age groups was not significant, anyway.
Recurrence of symptoms after therapeutic maneuvers could be indicative of a more severe problem of otoconial migration. Lee et al29 found that cervical and ocular VEMP abnormalities were higher in recurrent BPPV patients than in patients with nonrecurrent BPPV. Yang et al21 compared VEMP responses in the affected and nonaffected ears of 25 patients with PC-BPPV and 5 with LC-BPPV and no significant difference was found between the involved canals and the number of repositioning maneuvers. On the other hand, the number of repositioning maneuvers was higher in patients with no VEMP response, indicating more extensive damage. We could not find any difference in VEMP results between those who had been cured after 1 single maneuver and those who needed 2 or more therapeutic maneuvers regardless of the canal problem. Comparison of VEMP results between those with longer and intensive nystagmus
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
8
Annals of Otology, Rhinology & Laryngology
Table 6. Comparative Analysis of VEMP in the Affected and Healthy Ears of BPPV Patients Who Had Symptoms for Longer Than 2 Months (36 Patients) and Those (43 Patients) With Shorter Duration of Symptoms.a Duration of Symptoms Before Treatment Longer Shorter P value Longer Shorter P value Longer Shorter P value Longer Shorter P value Longer Shorter P value Longer Shorter P value
VEMP
Affected Ears
Healthy Ears
Controls
P Value
p1 lat (ms) p1 lat (ms)
18.74 ± 3.49 17.19 ± 3.31 .016d 15.14 ± 10.70 0.36 ± 0.22 16.18 ± 8.22 0.33 ± 0.19 .699, .460 26.91 ± 3.63 25.21 ± 3.99 .101 25.24 ± 17.17 0.54 ± 0.34 25.40 ± 14.92 0.54 ± 0.33 1.000, .920 41.18 ± 27.66 0.92 ± 0.54 39.68 ± 21.24 0.82 ± 0.51 .792, .419 8.05 ± 2.23 8.39 ± 1.58 .444
17.89 ± 3.77 17.01 ± 2.48
15.71 ± 1.06
16.63 ± 10.01 0.39 ± 0.21 17.78 ± 8.56 0.34 ± 0.18
23.80 ± 6.75 0.45 ± 0.23
26.68 ± 3.29 25.92 ± 2.60
25.14 ± 1.41
25.16 ± 16.30 0.61 ± 0.31 25.70 ± 13.58 0.50 ± 0.33
35.54 ± 8.05 0.74 ± 0.35
41.83 ± 25.27 0.98 ± 0.50 42.65 ± 21.94 0.88 ± 0.48
58.69 ± 13.6 1.23 ± 0.49
8.64 ± 2.33 8.30 ± 1.84
9.42 ± 1.01
.318, .218 .591, .367 .611, .177 .481, .219 .392, .193 .729, .228 .792, .677 .719, .632 1.000, .534 .504, .122 .920, .119 .625, .121 1.000, .449 .598, .228 .604, .195 .625, .209 .152, .098 .887, .233
p1 amp (µV)b p1 amp (µV)c P1 amp (µV)b p1 amp (µV)c n1 lat (ms) n1 lat (ms) n1 amp (µV)b n1 amp (µV)c n1 amp (µV)b n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 lat (ms) p1-n1 lat (ms)
Abbreviations: BPPV, benign paroxysmal positional vertigo; VEMP, vestibular evoked myogenic potential. a Patients with bilateral problems or those with no unilateral VEMP response were excluded. No statistically significant difference was found when comparing each parameter between the affected ears, healthy ears, and those of the control subjects. Apart from p1 latency, comparative analysis of all parameters in the affected ears of the 2 subgroups was not statistically significant. Patients with longer duration of symptoms had significantly longer p1 latency compared with those having short duration of symptoms. P values as the result of comparison of the affected ears of the 2 subgroups are given below each parameter (for the amplitudes, first raw and then corrected amplitudes, respectively). However, p values as the result of comparison of the affected ears with healthy ears and the affected ears with the controls are given in the last column, respectively. b Raw amplitudes. c Corrected mean amplitudes. d Statistically significant (P < .05).
at initial diagnosis and those with less severe symptoms was also inconclusive. However, patients with a longer duration of symptoms had significantly longer p1 latency compared with those having shorter duration of symptoms, which might be indicative of degeneration of neural elements and their interaction with otolithic and canalicular receptors as the BPPV recurs or persists in the long term. Longo et al5 studied patients with PC-BPPV alone and found higher abnormal VEMPs, but latency and thresholds were not different between patients and controls. Eryaman et al30 also studied patients with PC-BPPV alone and found 38.7% abnormality (absence of VEMP or latency delay) compared to controls but found no correlation between abnormal VEMP and the number of canalith reposition maneuvers required. Hong et al31 found VEMP abnormalities in patients with BPPV but without any difference
between involved semicircular canals. Comparative analysis of VEMP in BPPV patients who had posterior and lateral canal disease was not statistically significant, although amplitude depression was significant in patients with LC-BPPV as compared to healthy ears and those of control subjects in the present study. On the other hand, comparative analysis of VEMP in BPPV patients who had cupulolithiasis and canalolithiasis of the lateral canal was not statistically significant. However, decrease in p1 and n1 amplitude was statistically significant in patients with canalolithiasis as compared to healthy ears and those of control subjects. In conclusion, VEMP is a useful tool to study the otolithic function in patients with BPPV. Abnormality of VEMPs is not correlated with factors including age, severity of nystagmus at diagnosis, numbers of maneuvers
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
9
Yetiser et al applied, or site of canal involvement. However, the persistence or recurrence of symptoms has an effect on VEMP results since it has been detected that patients with a longer duration of symptoms or recurrences had significantly longer p1 latency compared with those having shorter duration of symptoms. Authors’ Note This article was presented at the 20th IFOS World Congress, June 1-5, 2013, Seoul, Korea, and has not been submitted for publication in another journal.
Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.
References 1. Gacek RR. Pathology of benign paroxysmal positional vertigo revisited. Ann Otol Rhinol Laryngol. 2003;112:574-582. 2. Colebatch JG, Halmagyi GM. Vestibular evoked potentials in human neck muscles before and after unilateral vestibular deafferentiation. Neurology. 1992;42:1635-1636. 3. Colebatch JG, Halmagyi GM, Skuse NF. Myogenic potentials generated by a click-evoked vestibulocollic response. J Neurol Neurosurg Psychiatr. 1994;57:190-197. 4. Basta D, Todt I, Ernst A. Normative data for P1/N1 latencies of vestibular evoked myogenic potentials induced by air- or bone-conducted tone bursts. Clin Neurophysiol. 2005;116(9):2216-2219. 5. Longo G, Onofri M, Pellicciari T, Quaranta N. Benign paroxysmal positional vertigo: is vestibular evoked myogenic potential testing useful? Acta Otolaryngol. 2012;132(1):39-43. 6. Welgampola MS, Colebatch JG. Characteristics and clinical applications of vestibular-evoked myogenic potentials. Neurology. 2005;64:1682-1688. 7. Colebatch JG. Properties of rectified averaging of an evokedtype signal: theory and application to the vestibular-evoked myogenic potential. Exp Brain Res. 2009;199(2):167-176. 8. Von Brevern M, Schmidt T, Schöfeld U, Lempert T, Clarke AH. Utricular dysfunction in patients with benign paroxysmal positional vertigo. Otol Neurotol. 2005;27:92-96. 9. Di Girolano S, Ottaviani F, Scarano E, Picciotti P, di Nardo W. Postural control in horizontal canal benign paroxysmal vertigo. Eur Arch Otorhinolaryngol. 2000;257:372-375. 10. Seok JI, Lee HM, Yoo JH, Lee DK. Residual dizziness after successful repositioning treatment in patients with benign paroxysmal positional vertigo. J Clin Neurol. 2008;4(3):107-110. 11. Maes L, Vinck BM, De Vel E, et al. The vestibular evoked myogenic potential: a test-retest reliability study. Clin Neurophysiol. 2009;120(3):594-600.
12. Bush ML, Jones RO, Shinn JB. The clinical reliability of vestibular evoked myogenic potentials. ENT J. 2010;89(4): 170-176. 13. Vanspauwen R, Wuts FL, Van de Heyning PH. Vestibular evoked myogenic potentials: test-retest reliability and normative values obtained with a feedback method for the sternocleidomastoid muscle contraction. J Vest Res. 2009;19:127-135. 14. Isaradisaikul S, Strong DA, Moushey JM, Gabbard SA, Ackley SR, Jenkins HA. Reliability of vestibular evoked myogenic potentials in healthy subjects. Otol Neurotol. 2008;29(4):542-544. 15. Maes L, Vinck BM, Wuyts F, et al. Clinical usefulness of the rotatory, caloric and vestibular evoked myogenic potential test in unilateral peripheral vestibular pathologies. Int J Audiol. 2011;50(8):566-576. 16. Murofushi T, Shimizu K, Takegoshi H, Cheng PW. Diagnostic value of prolonged latencies in the vestibular evoked myogenic potentials. Arch Otolaryngol Head Neck Surg. 2001;127(9):1069-1072. 17. Hong SM, Yeo SG, Kim SW, Cha CI. The results of vestibular evoked myogenic potential, with consideration of age-related changes, in vestibular neuritis, benign paroxysmal positional vertigo, and Meniere’s disease. Acta Otolaryngol. 2008;128(8):861-865. 18. Akkuzu G, Akkuzu B, Ozluoglu L. Vestibular evoked myogenic potentials in benign paroxysmal positional vertigo and Meniere’s disease. Eur Arch Otorhinolaryngol. 2006;263(6):510-517. 19. Zhang D, Fan Z, Han Y, et al. Benign paroxysmal vertigo of childhood: diagnostic value of vestibular test and high stimulus rate auditory brainstem response test. Int J Pediatr Otorhinolaryngol. 2012;76(1):107-110. 20. Chang CH, Young YH. Caloric and vestibular evoked myogenic potential tests in evaluating children with benign paroxysmal vertigo. Int J Pediatr Otorhinolaryngol. 2007;71(3):495-499. 21. Yang WS, Kim SH, Lee JD, Lee WS. Clinical significance of vestibular evoked myogenic potentials in benign paroxysmal positional vertigo. Otol Neurotol. 2008;29:1162-1166. 22. Agrawal Y, Zuniga MG, Davalos-Bichara M, et al. Decline in semicircular canal and otolith function with age. Otol Neurotol. 2012;33(5):832-839. 23. Basta D, Todt I, Ernst A. Characterization of age related changes in vestibular evoked myogenic potentials. J Vest Res. 2007;17(2-3):93-98. 24. Lee SK, Cha CI, Jung TS, Park DC, Yeo SG. Age-related differences in parameters of vestibular evoked myogenic potentials. Acta Otolaryngol. 2008;128(1):66-72. 25. Ochi K, Ohashi T. Age-related changes in the vestibularevoked myogenic potentials. Otolaryngol Head Neck Surg. 2003;129(6):655-659. 26. Su HC, Huang TW, Young YH. Cheng PW. Aging effect on vestibular evoked myogenic potential. Otol Neurotol. 2004;25(6):977-980. 27. Tang Y, Lopez I, Baloh R. Age-related change of the neuronal number in the human medial vestibular nucleus. A sterological investigation. J Vest Res. 2001-2002;11:357-363.
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
10
Annals of Otology, Rhinology & Laryngology
28. Ross MD, Peacor D, Johnsson LG, Allard LF. Observations on normal and degenerating human otoconia. Ann Otol Rhinol Laryngol. 1976;85:210-226. 29. Lee JD, Park MK, Lee BD, Lee TK, Sung KB, Park JK. Abnormality of cervical vestibular-evoked myogenic potentials and ocular vestibular evoked myogenic potentials in patients with recurrent benign paroxysmal positional vertigo. Acta Otolaryngol. 2013;133(2):150-153.
30. Eryaman E, Oz ID, Ozker BY, Erbek S, Erbek SS. Evaluation of vestibular evoked myogenic potentials during benign paroxysmal positional vertigo attacks; neuroepithelial degeneration? B-ENT. 2012;8(4):247-250. 31. Hong SM, Park DC, Yeo SG, Cha CI. Vestibular evoked myogenic potentials in patients with benign paroxysmal positional vertigo involving each semicircular canal. Am J Otolaryngol. 2008;29(3):184-187.
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
An Analysis of Vestibular Evoked Myogenic Potentials in Patients With Benign Paroxysmal Positional Vertigo Sertac Yetiser, Dilay Ince and Murat Gul Ann Otol Rhinol Laryngol published online 1 May 2014 DOI: 10.1177/0003489414532778 The online version of this article can be found at: http://aor.sagepub.com/content/early/2014/05/01/0003489414532778
Published by: http://www.sagepublications.com
Additional services and information for Annals of Otology, Rhinology & Laryngology can be found at: Email Alerts: http://aor.sagepub.com/cgi/alerts Subscriptions: http://aor.sagepub.com/subscriptions Reprints: http://www.sagepub.com/journalsReprints.nav Permissions: http://www.sagepub.com/journalsPermissions.nav
>> OnlineFirst Version of Record - May 1, 2014 What is This?
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
532778
research-article2014
AORXXX10.1177/0003489414532778Annals of Otology, Rhinology & LaryngologyYetiser et al
Article
An Analysis of Vestibular Evoked Myogenic Potentials in Patients With Benign Paroxysmal Positional Vertigo
Annals of Otology, Rhinology & Laryngology 1–10 © The Author(s) 2014 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/0003489414532778 aor.sagepub.com
Sertac Yetiser, MD1, Dilay Ince, MA1, and Murat Gul, MS2
Abstract Objective: Vestibular evoked myogenic potentials (VEMPs) selectively test the vestibular end-organ. The aim of this study was to analyze how the site of the diseased canal, type of particulate deposition, duration of symptoms, severity of nystagmus, recurrence, and age affect the VEMP in patients with benign paroxysmal positional vertigo (BPPV). Methods: One hundred two patients were enrolled in the study between 2009 and 2012. There were 36 men and 66 women with ages ranging from 16 to 71 years (mean age, 42.28 ± 11.29 years). Patients with BPPV were tested with rollon and head-hanging maneuvers under video-electronystagmography monitoring and with air conduction cervical VEMP testing. Patients were grouped for duration, severity, recurrence, age, site of canal involvement, and so on, and the results were compared in each subgroup. Kruskal–Wallis and Mann–Whitney U tests were used for the comparative analysis. Results: Twenty-four patients (23.5%) had a gross VEMP abnormality (absence of VEMP in 6 and greater than 25% depression of the amplitude in 18). Abnormality of VEMPs was not correlated with factors including age, severity of nystagmus, number of maneuvers applied, and the site of canal involvement (P < .05). However, persistence or recurrence of symptoms has an effect on VEMP results (P = .016). Conclusion: Vestibular evoked myogenic potential is a useful tool to study the otolithic function in patients with BPPV and should be included in the test battery. Keywords vestibular evoked myogenic potential, benign paroxysmal positional vertigo
Introduction Benign paroxysmal positional vertigo is one of the most common peripheral vestibular problems seen at outpatient clinics. Migrated otoconia either freely floating inside the canal or adhering to the cupula can provoke nystagmus and vestibular disturbance of sudden onset during head motion. The origin of these deposits is claimed to be the macular neuroepithelium. The site of the affected canal and the type of particulate deposition can be justified after roll-on and head-hanging maneuvers. The pathophysiological mechanism that induces the sense of vertigo in patients with benign paroxysmal positional vertigo (BPPV) is well documented.1 However, functional assessment of the saccule and the utricle has been the subject of clinical research for many years. Utricular or perhaps saccular degeneration is assumed to be the underlying cause and the source of so-called troublesome crystalloids. Selective testing of the vestibular end-organ was possible after introduction of vestibular evoked myogenic potential (VEMP) to the clinic by Colebatch and colleagues.2,3 Since then, VEMP testing has gradually become part of the vestibular test battery. It is
a short latency myogenic wave recorded from the sternocleidomastoid muscle (SCM) after intense acoustic stimulus and is used to assess the integrity and function of the sacculo-collic reflex.4 Neural bundles from the superior vestibular nerve mainly collect impulses from lateral and superior semicircular canals and the utricle. The inferior vestibular nerve is connected to the posterior semicircular canal and the saccule and is the main pathway of VEMPs. Patients with BPPV may show abnormal findings on VEMP.5 However, it is not known how this is related to the site of the affected canal (lateral or posterior), the type of particulate deposition (canalolithiasis or cupulolithiasis), the duration of symptoms, the severity of nystagmus on 1
Department of Otorhinolaryngology–Head and Neck Surgery, Anadolu Medical Center, Kocaeli, Turkey 2 Department of Statistics, University of Giresun, Giresun, Turkey Corresponding Author: Sertac Yetiser, MD, Department of Otorhinolaryngology–Head and Neck Surgery, Anadolu Medical Center, Cumhuriyet mah, 2255 sok, No:3, Gebze 41400, Kocaeli, Turkey. Email: [email protected]
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
2
Annals of Otology, Rhinology & Laryngology
video-electronystagmography (VNG), or age. Therefore, we aimed to analyze the different aspects of VEMP testing in patients with BPPV.
Materials and Methods One hundred two patients with VNG-confirmed BPPV problems who had been recruited between 2009 and 2012 were enrolled in the study. A verbal and a signed informed consent were obtained from each patient and control subject. The procedures were in accordance with the ethical standards of the Declaration of Helsinki and of the institutional review board. Those with hearing loss, tinnitus, spontaneous nystagmus, abnormal ear drum, or other vestibular or neurologic problems and those who used medication before testing that could affect the vestibular system and/or muscle tone were excluded. There were 36 men and 66 women with ages ranging from 16 to 71 years (mean age, 42.28 ± 11.29 years). All patients had normal otoscopic examination, normal hearing threshold, and no problems other than BPPV. The affected side for lateral canal BPPV (LC-BPPV) was determined according to the severity of nystagmus as seen on VNG recording (Micromed, Inc, Chatham, Illinois,USA). The type, duration, and direction of nystagmus were recorded with an infrared wireless video camera. Patients with posterior canal BPPV (PC-BPPV) were treated with Epley and patients with LC-BPPV were treated with either barbeque or Semont maneuvers. Patients who had recurrent symptoms after maneuvers were tested again by VNG within a week and were subjected to therapeutic maneuvers as dictated by VNG until resolution of symptoms. Air conduction cervical VEMP testing was used (Eclipse EP25; Interacoustics, Eden Prairie, Minnesota, USA) to test the patients. Patients with absence of bilateral VEMPs in the presence of unilateral BPPV were excluded. Fifteen healthy participants with no vestibular problems and intact eardrums (8 men, 7 women; mean age, 42.09 ± 9.28 years) were also tested with VEMP as the control group. Since the latency and amplitude difference between the ears was so small (± 1.00), the sum of data from both ears was set as 1 single control group (30 ears). Vestibular evoked myogenic potentials were recorded with disposable, self-adhesive, pregelled surface electrodes. Electrode impedances were below 5 kΩ. The active electrode was placed over the middle of the SCM and the reference electrode was placed over the upper sternum. The ground electrode was placed over the forehead. Tone-burst sound stimuli of 95 dB nHL with rarefaction polarity, 5 Hz stimulus repetition rate, 1 ms rise/fall time, and 2 ms plateau time were delivered at 500 Hz; 200 sweeps were averaged. Myogenic responses were amplified and band-pass filtered (800-10 Hz). The test was repeated with 85, 75, and 65 dB stimuli in search of the threshold. Stimulation was presented monaurally via an ipsilateral ear phone inserted in foam ear tips (Ear tone-ABR;
Interacoustics) while the participants turned their heads to the counter lateral side in the sitting position and the responses were recorded from the ipsilateral SCM. The test was reviewed twice on each occasion to ensure reproducibility. However, no more than 2 tests were done and the participants were allowed to have some rest between trials to prevent fatigue. The procedure was repeated on both sides. Results of VEMP were evaluated by the existence of the first successive p1-n1 biphasic wave. If this was not detected at 95 dB stimulation, the result was accepted as the absence of VEMP. Biphasic VEMP waves seen at 75 or 65 dB stimulation were accepted as VEMP with a lower threshold. Latency and amplitude measurements were made on potentials obtained at 95 dB stimulation. The latency and the amplitude of p1 and n1 waves and interpeak amplitude and latency differences were measured especially to determine the magnitude of the whole electrical activity and also to determine whether the myogenic potential is distorted or not. First, the response was observed during unrectified electromyograms (EMGs). The raw values were then converted into scaled scores. Since the VEMP amplitude is dependent on ongoing muscle EMG level and requires tonic contraction of the muscle, both corrected and raw EMG amplitudes were used in all comparative analyses.6,7 Results were given as mean and standard deviation. The corrected amplitudes were calculated by dividing the raw amplitudes by the prestimulus background EMG. Interaural p1-n1 amplitude symmetry was calculated as Lamp (1 with larger amplitude) – Samp (1 with smaller amplitude) / REamp (Right ear amplitude) + LEamp (Left ear amplitude) × 100. Greater than 25% asymmetry was accepted as abnormal. The percentage of vestibular asymmetry in the control group was measured as (REamp – LEamp / REamp + LE amp) × 100. Patients who required more than 2 repositioning maneuvers for the resolution of symptoms were considered to be recurrent or resistive cases. Patients who had severe nystagmus up to 50 to 60 seconds (or even more) during VNG testing were considered to be severe cases. Patients were grouped as those with PC-BPPV and LC-BPPV, those with cupulolithiasis and canalolithiasis, those younger than 30 years of age, those 31 to 50 years old, and those older than 51, those who had symptoms for less than 2 months and those with symptoms for more than 2 months, those with nystagmus lasting up to 1 minute or more and those with less severe nystagmus, and finally, those with recurrent and nonrecurrent symptoms (patients who had been cured after 1 single maneuver and those who needed to be treated with several maneuvers). Vestibular evoked myogenic potential results were compared between each subgroup. Patients with unilateral problems based on VNG were always grouped as affected and nonaffected (healthy) ears and groups were compared with each other and also with controls. However, since the sum of data from
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
3
Yetiser et al Table 1. Comparative Analysis of VEMP in the Affected and Healthy Ears of BPPV Patients Younger Than 30 Years (9 Patients), Between 31 and 50 Years Old (56 Patients), and Older Than 50 Years (18 Patients).a Age Group, y Ears Affected Healthy Affected Healthy Affected Healthy Affected Healthy Affected Healthy Affected Healthy
VEMP p1 lat (ms) p1 lat (ms) p1 amp (µV)b p1 amp (µV)c p1 amp (µV)b p1 amp (µV)c n1 lat (ms) n1 lat (ms) n1 amp (µV)b n1 amp (µV)c n1 amp (µV)b n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 lat (ms) p1-n1 lat (ms)
< 30
31-50
> 50
17.29 ± 3.89 17.29 ± 2.98 18.64 ± 8.77 0.39 ± 0.21 16.30 ± 8.23 0.36 ± 0.18 23.88 ± 4.49 24.70 ± 3.49 28.36 ± 15.19 0.63 ± 0.35 24.51 ± 16.09 0.52 ± 0.34 46.70 ± 22.79 0.98 ± 0.52 40.96 ± 23.72 0.86 ± 0.51 7.84 ± 1.41 9.04 ± 2.97
17.38 ± 2.95 17.44 ± 3.02 16.60 ± 9.72 0.37 ± 0.22 17.28 ± 8.95 0.36 ± 0.21 27.13 ± 3.13 26.25 ± 3.25 25.30 ± 15.67 0.54 ± 0.36 27.38 ± 14.64 0.62 ± 0.34 41.83 ± 24.91 0.90 ± 0.58 45.78 ± 23.29 0.99 ± 0.54 8.29 ± 1.78 8.56 ± 1.67
19.24 ± 3.89 18.15 ± 4.13 12.87 ± 8.35 0.30 ± 0.20 15.09 ± 10.11 0.36 ± 0.23 26.16 ± 4.25 26.51 ± 3.88 21.18 ± 12.70 0.43 ± 0.30 20.73 ± 14.08 0.49 ± 0.34 35.96 ± 19.25 0.78 ± 0.47 36.66 ± 23.73 0.88 ± 0.49 7.07 ± 1.63 8.34 ± 2.93
P Value .229 1.000, .823, .436 .247 .585, .699, .349 .940 .617, .729, .398 .233 .685, .752, .807 .461 .630, .468, .451 .595 .573, .221, .863 .499 .630, .472, .920 .760 .652, 1.000, .558 .037d .164, .680, .114
Abbreviations: BPPV, benign paroxysmal positional vertigo; VEMP, vestibular evoked myogenic potential. a Patients with bilateral problems or those with no unilateral VEMP response were excluded. No statistically significant difference was found when comparing each parameter between the affected and healthy ears. Apart from p1-n1 latency, comparative analysis of all parameters in the affected ears of the 3 age subgroups was not statistically significant. The first row of P values in each subgroup represents comparison of the affected ears of the 3 age subgroups. The second row shows the results of comparison of the affected and healthy ears of the 3 age subgroups: < 30, 31-50, and > 50 years, respectively. b Raw amplitudes. c Corrected mean amplitudes. d Statistically significant (P < .05).
both ears of the control subjects was set as 1 single agematched control group, the control group was not included in the age-group analysis (Table 1). Patients with no VEMP response were not included in group analysis. The Kruskal– Wallis test was used for multiple variance analysis of the groups in Table 1 and the Mann–Whitney U test was used for comparative analysis of the groups in Tables 2 to 5. Statistical significance was set at P < .05.
Results VEMP Results in General Vestibular evoked myogenic potential responses were elicited in all controls. In the study group (102 patients), VEMP responses were absent in 6 patients and amplitude was ipsilaterally depressed in 18 patients with unilateral BPPV, that is, the p1-n1 interaural amplitude difference was greater than 25%. Therefore, in total, 24 patients (23.5%) had a gross VEMP abnormality. Four patients also had lower VEMP thresholds. Excluding those patients with gross abnormality, the rest of the patients were classified into different subgroups.
Young Versus Older Patients Nine patients were younger than 30 years, 56 patients were between 31 and 50 years old, and 18 were older than 51 years. Apart from p1-n1 latency, comparative analysis of all VEMP parameters in the affected ears of the 3 age groups was not statistically significant (P > .05), although older patients had more depressed amplitude and prolonged latency. No statistically significant difference was found when comparing each parameter between the affected and healthy ears (Table 1).
Severity of Nystagmus Nineteen patients with BPPV had longer and intensive nystagmus lasting up to a minute regardless of canal involvement compared with 63 patients having less severe nystagmus. Comparative analysis of all VEMP parameters of the affected ears between the 2 groups and the controls was not statistically significant (P > .05). No statistically significant difference was found when comparing each parameter between the affected and healthy ears (Table 2).
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
4
Annals of Otology, Rhinology & Laryngology
Table 2. Comparative Analysis of VEMP in the Affected and Healthy Ears of Patients With BPPV Having Longer and Intensive (19 Patients) Nystagmus and Those With Less Severe Nystagmus (63 Patients).a Severity Groups Severe Nonsevere P value Severe Nonsevere P value Severe Nonsevere P value Severe Nonsevere P value Severe Nonsevere P value Severe Nonsevere P value
VEMP
Affected Ears
Healthy Ears
Controls
P Value
p1 lat (ms) p1 lat (ms)
17.10 ± 2.95 18.20 ± 3.44 .224 15.60 ± 9.33 0.32 ± 0.18 15.43 ± 9.20 0.32 ± 0.21 .792, .792 24.84 ± 2.87 25.87 ± 3.80 .139 27.27 ± 19.87 0.52 ± 0.36 26.27 ± 21.21 0.50 ± 0.34 .632, .841 40.82 ± 26.31 0.86 ± 0.51 40.69 ± 23.08 0.82 ± 0.54 .887, .778 7.68 ± 1.69 8.27 ± 1.92 .197
17.40 ± 2.04 17.51 ± 3.43
15.71 ± 1.06
16.11 ± 9.74 0.44 ± 0.21 15.66 ± 8.92 0.35 ± 0.20
23.80 ± 6.75 0.45 ± 0. 21
25.84 ± 1.82 25.49 ± 3.57
25.14 ± 1.41
29.20 ± 16.63 0.66 ± 0.32 25.95 ± 13.74 0.56 ± 0.32
35.54 ± 8.05 0.74 ± 0.34
49.30 ± 25.70 1.09 ± 0.52 40.20 ± 21.74 0.97 ± 0.48
58.69 ± 13.6 1.23 ± 0.53
8.42 ± 1.90 8.56 ± 2.07
9.42 ± 1.01
.319, .224 .316, .221 .224, .145 .105, .104 .764, .360 .425, .325 .225, .224 .625, .617 .312, .125 .205, .116 1.000, .354 .397, .272 .338, .188 .176, .164 1.000, .332 .388, .172 .214, .132 .314, .222
p1 amp (µV)b p1 amp (µV)c p1 amp (µV)b p1 amp (µV)c n1 lat (ms) n1 lat (ms) n1 amp (µV)b n1 amp (µV)c n1 amp (µV)b n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 lat (ms) p1-n1 lat (ms)
Abbreviations: BPPV, benign paroxysmal positional vertigo; VEMP, vestibular evoked myogenic potential. a Patients with bilateral problems or those with no unilateral VEMP response were excluded. No statistically significant difference was found when comparing each parameter between the affected ears, healthy ears, and those of the control subjects. Comparative analysis of all parameters in affected ears of the 2 subgroups was not statistically significant. P values as the result of comparison of the affected ears of the 2 subgroups are given below each parameter (for the amplitudes, first raw and then corrected amplitudes, respectively). P values as the result of comparison of the affected ears with healthy ears and the affected ears with the controls are given in the last column, respectively. b Raw amplitudes. c Corrected mean amplitudes.
Recurrent Versus Nonrecurrent Disease There were 54 patients who were cured after 1 single maneuver regardless of the site of the canal disease, whether lateral or posterior. Twenty-seven patients required 2 or more maneuvers. Comparative analysis of VEMP in the affected and healthy ears in BPPV patients who were cured with 1 single maneuver and those who needed 2 or more therapeutic maneuvers showed no statistically significant difference. Comparison of each parameter between affected ears of the 2 subgroups was not statistically significant (P > .05) (Table 3).
Lateral Versus Posterior Canal BPPV Forty-two patients with unilateral LC-BPPV and 35 patients with unilateral PC-BPPV were included. Fifteen patients had combined or bilateral BPPV. Of those, 9 had bilateral PC-BPPV and 1 patient had LC-BPPV on 1 side and PC-BPPV on the other side. Five patients were identified as
having multiple canals, PC- and LC-BPPV on the same side, as seen on roll-on and head-hanging maneuvers. Patients with bilateral problems or those with no unilateral VEMP response were excluded. Comparative analysis of all parameters in the affected ears of the 2 subgroups was not statistically significant (P > .05), although it is interesting that patients with lateral canal problems had more depressed p1 and n1 amplitudes (Table 4). Apart from p1 amplitude in patients with LC-BPPV, no statistically significant difference was found when comparing each parameter between the affected, healthy ears and those of the control subjects.
Canalolithiasis Versus Cupulolithiasis There were 18 patients with cupulolithiasis and 24 patients with canalolithiasis of the LC-BPPV. Comparative analysis of all parameters in the affected ears of the 2 subgroups was not statistically significant (P > .05), although it is
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
5
Yetiser et al Table 3. Comparative Analysis of VEMP in the Affected and Healthy Ears of BPPV Patients Who Were Cured With 1 Single Maneuver (54 Patients) and Those Who Needed 2 or More Therapeutic Maneuvers (27 Patients).a Recurrence Recurrent Single P value Recurrent Single P value Recurrent Single P value Recurrent Single P value Recurrent Single P value Recurrent Single P value
VEMP
Affected Ears
Healthy Ears
Controls
P Value
p1 lat (ms) p1 lat (ms)
18.12 ± 3.07 17.90 ± 3.56 .485 16.09 ± 8.27 0.34 ± 0.19 15.03 ± 9.44 0.31 ± 0.20 .920, .504 26.17 ± 3.02 25.87 ± 4.01 .729 24.72 ± 14.54 0.52 ± 0.32 24.20 ± 15.36 0.49 ± 0.34 .887, .672 41.31 ± 22.17 0.88 ± 0.50 39.79 ± 24.16 0.81 ± 1.05 .741, .555 7.93 ± 1.84 8.33 ± 1.95 .386
17.30 ± 3.44 17.52 ± 3.22
15.71 ± 1.06
18.22 ± 9.91 0.31 ± 0.23 17.29 ± 10.24 0.37 ± 0.20
23.80 ± 6.75 0.45 ± 0.20
26.32 ± 5.17 25.91 ± 3.46
25.14 ± 1.41
27.27 ± 17.18 0.57 ± 0.41 25.06 ± 13.78 0.58 ± 0.36
35.54 ± 8.05 0.74 ± 0.39
45.79 ± 27.27 1.01 ± 0.57 41.34 ± 22.09 0.91 ± 0.49
58.69 ± 13.6 1.23 ± 0.55
8.59 ± 2.29 8.72 ± 2.01
9.42 ± 1.01
.375, .124 .561, .432 .206, .112 .540, .236 .203, .193 .391, .172 .863, .504 1.000, .876 .568, .166 .505, .184 .791, .241 .175, .125 .519, .212 .378, .144 .672, .192 .275, .164 .250, .156 .275, .247
p1 amp (µV)b p1 amp (µV)c p1 amp (µV)b p1 amp (µV)c n1 lat (ms) n1 lat (ms) n1 amp (µV)b n1 amp (µV)c n1 amp (µV)b n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 lat (ms) p1-n1 lat (ms)
Abbreviations: BPPV, benign paroxysmal positional vertigo; VEMP, vestibular evoked myogenic potential. a Patients with bilateral problems or those with no unilateral VEMP response were excluded. No statistically significant difference was found in the comparison of each parameter between the affected ears, healthy ears, and those of the control subjects, and comparative analysis of the affected ears of the 2 subgroups was not statistically significant. P values as the result of comparison of the affected ears of the 2 subgroups are given below each parameter (for the amplitudes, first raw and then corrected amplitudes, respectively). P values as the result of comparison of the affected ears with healthy ears and the affected ears with the controls are given in the last column, respectively. b Raw amplitudes. c Corrected mean amplitudes.
interesting that patients with canalolithiasis had more depressed p1 and n1 amplitudes (Table 5). Apart from p1 amplitude in patients with canalolithiasis, no statistically significant difference was found when comparing each parameter between the affected ears, healthy ears, and those of the control subjects.
Short Versus Long Duration of Symptoms There were 36 patients who had symptoms lasting longer than 2 months and 43 patients with a shorter duration of symptoms. Comparative analysis of all parameters, apart from p1 latency, in the affected ears of the 2 subgroups was not statistically significant. Patients with a longer duration of symptoms had significantly longer p1 latency compared with those having a shorter duration of symptoms (P < .05). No statistically significant difference was found when comparing each parameter between the affected ears, healthy ears, and those of the control subjects (Table 6).
Discussion The pathophysiology of BPPV is primarily based on such a mechanical mechanism that the deposits that are freely floating or attached to the cupula trigger an additional cupular movement, disturbing the inertia during head motion, which makes the cupula more sensitive to gravitational forces. This generally explains the definite symptoms of the patients. However, degeneration of neural elements and their interaction with otolithic and canalicular receptors may also participate in some patients with BPPV. Gacek1 has found a significant decrease in superior and inferior ganglionary vestibular cells in BPPV. Some patients temporarily feel a loss of balance and postural instability after resolution of an acute episode of vertigo. Von Brevern et al8 have found an otolithic dysfunction most probably secondary to utricular degeneration. Di Girolano et al9 have pointed out the disturbed postural control in patients with BPPV. Residual dizziness even after a successful repositioning
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
6
Annals of Otology, Rhinology & Laryngology
Table 4. Comparative Analysis of VEMP in the Affected and Healthy Ears of BPPV Patients Who Had Posterior (35 Patients) or Lateral (42 Patients) Canal Disease.a PC- and LC-BPPV PC LC P value PC LC P value PC LC P value PC LC P value PC LC P value PC LC P value
VEMP
Affected Ears
Healthy Ears
Controls
P Value
p1 lat (ms) p1 lat (ms)
18.38 ± 3.76 17.34 ± 3.34 .208 17.72 ± 10.39 0.36 ± 0.221 13.75 ± 8.53 0.29 ± 0.18 .072, .136 25.90 ± 4.04 26.08 ± 3.46 .862 26.72 ± 18 0.57 ± 0.38 24.18 ± 14.63 0.48 ± 0.28 .495, .224 44.42 ± 27.70 0.94 ± 0.58 36.18 ± 21.36 0.77 ± 0.45 .144, .168 7.98 ± 1.86 8.43 ± 2.15 .263
17.90 ± 3.71 17.29 ± 3.17
15.71 ± 1.06
16.37 ± 9.96 0.37 ± 0.22 17.68 ± 8.40 0.38 ± 0.17
23.80 ± 6.75 0.45 ± 0.19
25.00 ± 4.03 26.04 ± 2.58
25.14 ± 1.41
24.63 ± 4.03 0.57 ± 0.33 26.63 ± 14.84 0.56 ± 0.32
35.54 ± 8.05 0.74 ± 0.42
41.02 ± 23.63 0.93 ± 0.51 44.05 ± 22.52 0.94 ± 0.48
58.69 ± 13.6 1.23 ± 0.49
8.12 ± 2.35 8.66 ± 1.57
9.42 ± 1.01
.618, .475 .672, .553 .585, .177 .792, .376 .039, .021d .024, .019d .920, .891 1.000, .798 .477, .218 1.000, .233 .185, .074 .174, .063 .585, .388 .765, .661 .088, .076 .295, .117 .499, .227 .573, .233
p1 amp (µV)b p1 amp (µV)c p1 amp (µV)b p1 amp (µV)c n1 lat (ms) n1 lat (ms) n1 amp (µV)b n1 amp (µV)c n1 amp (µV)b n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 lat (ms) p1-n1 lat (ms)
Abbreviations: BPPV, benign paroxysmal positional vertigo; LC, lateral canal; PC, posterior canal; VEMP, vestibular evoked myogenic potential. a Patients with bilateral problems or those with no unilateral VEMP response were excluded. Apart from p1 amplitude in patients with LC-BPPV, no statistically significant difference was found when comparing each parameter between the affected ears, healthy ears, and those of the control subjects. Comparative analysis of all parameters in the affected ears of the 2 subgroups was not statistically significant. P values as the result of comparison of the affected ears of the 2 subgroups are given below each parameter (for the amplitudes, first raw and then corrected amplitudes, respectively). However, P values as the result of comparison of the affected ears with healthy ears and the affected ears with the controls are given in the last column, respectively. b Raw amplitudes. c Corrected mean amplitudes. d Statistically significant (P < .05).
maneuver shows that BPPV is not only a disorder of the semicircular canals.10 It has been demonstrated that positive VEMP results are related not only to the integrity of the vestibular nerve but also to the normal functioning otolithic organ. Normative data analysis suggests that these potentials are very stable and reproducible.4,11 Test–retest consistency is reported to be high regardless of the time interval between the tests and the type of stimulus used.12-14 Diagnostic capacity is also as good as other modalities.15,16 However, patients with BPPV show less abnormal results on VEMP. We have found 23.5% abnormal VEMP results in this study. Hong et al17 found 25.8% VEMP abnormality in BPPV patients, which was less common compared to those patients with vestibular neurinitis and Ménière’s disease who had 36.6% and 69% abnormality, respectively. Akkuzu et al18 compared BPPV and patients with Ménière’s disease and found
a 30% abnormality in BPPV patients as compared to 50% abnormality in patients with Ménière’s disease. Children with BPV have been reported to have abnormal VEMP results.19,20 Yang et al21 reported abnormal VEMP results, especially in BPPV patients who are chronic and resistive, and proposed more extensive damage to the saccule as the disease recurs. We have observed a correlation between increasing age and prolongation of latency and a decrease in the amplitude of VEMPs in patients with BPPV. However, even though older patients had smaller amplitudes and longer latencies, comparative analysis of the 3 different age groups was not statistically significant. One possible influence on the VEMPs in older patients comes from less muscle tension. However, the authors state that this contribution is small and is not likely to account for the age-related changes. A decline in vestibular function with aging measured by
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
7
Yetiser et al
Table 5. Comparative Analysis of VEMP in the Affected and Healthy Ears in BPPV Patients Who Had Cupulolithiasis (18 Patients) or Canalolithiasis (24 Patients) of the Lateral Canal.a Canalolithiasis vs Cupulolithiasis Canalolithiasis Cupulolithiasis P value Canalolithiasis Cupulolithiasis P value Canalolithiasis Cupulolithiasis P value Canalolithiasis Cupulolithiasis P value Canalolithiasis Cupulolithiasis P value Canalolithiasis Cupulolithiasis P value
VEMP p1 lat (ms) p1 lat (ms) p1 amp (µV)b p1 amp (µV)c p1 amp (µV)b p1 amp (µV)c n1 lat (ms) n1 lat (ms) n1 amp (µV)b n1 amp (µV)c n1 amp (µV)b n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 lat (ms) p1-n1 lat (ms)
Affected Ears
Healthy Ears
Controls
P Value
17.51 ± 3.44 17.68 ± 3.15 .863 11.91 ± 5.93 0.25 ± 0.13 16.20 ± 10.92 0.34 ± 0.23 .110, .093 26.18 ± 3.81 25.96 ± 2.91 .100 20.11 ± 11.21 0.44 ± 0.24 25.26 ± 15.52 0.52 ± 0.35 .218, .343 32.16 ± 16.10 0.69 ± 0.35 41.53 ± 25.40 0.87 ± 0.57 .161, .166 8.58 ± 1.92 8.24 ± 2.42 .619
17.29 ± 2.37 17.29 ± 4.00
15.71 ± 1.06
16.00 ± 7.12 0.34 ± 0.15 19.93 ± 9.38 0.43 ± 0.22
23.80 ± 6.75 0.45 ± 0.17
26.04 ± 1.79 26.03 ± 3.35
25.14 ± 1.41
23.70 ± 13.97 0.50 ± 0.31 30.54 ± 14.97 0.64 ± 0.34
35.54 ± 8.05 0.74 ± 0.32
39.39 ± 20.57 0.83 ± 0.42 50.27 ± 25.50 1.08 ± 0.53
58.69 ± 13.6 1.23 ± 0.41
8.68 ± 1.73 8.62 ± 1.33
9.42 ± 1.01
.792, .584 .742, .572 .038, .020d .024, .018d .287, .301 .235, .455 .863, .856 .920, .862 .381, .246 .397, .118 .312, .407 .283, .377 .189, .090 .310, .283 .229, .435 .303, .552 .842, .207 .563, .132
Abbreviations: BPPV, benign paroxysmal positional vertigo; VEMP, vestibular evoked myogenic potential. a Patients with bilateral problems or those with no unilateral VEMP response were excluded. Apart from p1 amplitude in patients with canalolithiasis, no statistically significant difference was found when comparing each parameter between the affected ears, healthy ears, and those of the control subjects. Comparative analysis of all parameters in the affected ears of the 2 subgroups was not statistically significant. P values as the result of comparison of the affected ears of the 2 subgroups are given below each parameter (for the amplitudes, first raw and then corrected amplitudes, respectively). However, P values as the result of comparison of the affected ears with healthy ears and the affected ears with the controls are given in the last column, respectively. b Raw amplitudes. c Corrected mean amplitudes. d Statistically significant (P < .05).
VEMP in the elderly population, especially in those older than 60 years, is probably due to age-related degenerative changes in neural and sensory elements in structures lying along the pathway.22-26 Studies on neuroanatomy indicate a decrease in the number of otoconia, vestibular hair cell loss, and a decrease in the number of neurons in the vestibular nucleus with aging.27,28 On the other hand, latency seems to be more reliable than amplitude since amplitude has more variability and can be affected by basic muscle activity, the patient’s position, and other general conditions. Corrected amplitudes as well as raw amplitudes were also included in the comparative analysis of this study to overcome the problem of amplitude dependency on the intensity of tonic contraction of the muscle. However, the difference between the affected ears in the 3 age groups was not significant, anyway.
Recurrence of symptoms after therapeutic maneuvers could be indicative of a more severe problem of otoconial migration. Lee et al29 found that cervical and ocular VEMP abnormalities were higher in recurrent BPPV patients than in patients with nonrecurrent BPPV. Yang et al21 compared VEMP responses in the affected and nonaffected ears of 25 patients with PC-BPPV and 5 with LC-BPPV and no significant difference was found between the involved canals and the number of repositioning maneuvers. On the other hand, the number of repositioning maneuvers was higher in patients with no VEMP response, indicating more extensive damage. We could not find any difference in VEMP results between those who had been cured after 1 single maneuver and those who needed 2 or more therapeutic maneuvers regardless of the canal problem. Comparison of VEMP results between those with longer and intensive nystagmus
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
8
Annals of Otology, Rhinology & Laryngology
Table 6. Comparative Analysis of VEMP in the Affected and Healthy Ears of BPPV Patients Who Had Symptoms for Longer Than 2 Months (36 Patients) and Those (43 Patients) With Shorter Duration of Symptoms.a Duration of Symptoms Before Treatment Longer Shorter P value Longer Shorter P value Longer Shorter P value Longer Shorter P value Longer Shorter P value Longer Shorter P value
VEMP
Affected Ears
Healthy Ears
Controls
P Value
p1 lat (ms) p1 lat (ms)
18.74 ± 3.49 17.19 ± 3.31 .016d 15.14 ± 10.70 0.36 ± 0.22 16.18 ± 8.22 0.33 ± 0.19 .699, .460 26.91 ± 3.63 25.21 ± 3.99 .101 25.24 ± 17.17 0.54 ± 0.34 25.40 ± 14.92 0.54 ± 0.33 1.000, .920 41.18 ± 27.66 0.92 ± 0.54 39.68 ± 21.24 0.82 ± 0.51 .792, .419 8.05 ± 2.23 8.39 ± 1.58 .444
17.89 ± 3.77 17.01 ± 2.48
15.71 ± 1.06
16.63 ± 10.01 0.39 ± 0.21 17.78 ± 8.56 0.34 ± 0.18
23.80 ± 6.75 0.45 ± 0.23
26.68 ± 3.29 25.92 ± 2.60
25.14 ± 1.41
25.16 ± 16.30 0.61 ± 0.31 25.70 ± 13.58 0.50 ± 0.33
35.54 ± 8.05 0.74 ± 0.35
41.83 ± 25.27 0.98 ± 0.50 42.65 ± 21.94 0.88 ± 0.48
58.69 ± 13.6 1.23 ± 0.49
8.64 ± 2.33 8.30 ± 1.84
9.42 ± 1.01
.318, .218 .591, .367 .611, .177 .481, .219 .392, .193 .729, .228 .792, .677 .719, .632 1.000, .534 .504, .122 .920, .119 .625, .121 1.000, .449 .598, .228 .604, .195 .625, .209 .152, .098 .887, .233
p1 amp (µV)b p1 amp (µV)c P1 amp (µV)b p1 amp (µV)c n1 lat (ms) n1 lat (ms) n1 amp (µV)b n1 amp (µV)c n1 amp (µV)b n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 amp (µV)b p1-n1 amp (µV)c p1-n1 lat (ms) p1-n1 lat (ms)
Abbreviations: BPPV, benign paroxysmal positional vertigo; VEMP, vestibular evoked myogenic potential. a Patients with bilateral problems or those with no unilateral VEMP response were excluded. No statistically significant difference was found when comparing each parameter between the affected ears, healthy ears, and those of the control subjects. Apart from p1 latency, comparative analysis of all parameters in the affected ears of the 2 subgroups was not statistically significant. Patients with longer duration of symptoms had significantly longer p1 latency compared with those having short duration of symptoms. P values as the result of comparison of the affected ears of the 2 subgroups are given below each parameter (for the amplitudes, first raw and then corrected amplitudes, respectively). However, p values as the result of comparison of the affected ears with healthy ears and the affected ears with the controls are given in the last column, respectively. b Raw amplitudes. c Corrected mean amplitudes. d Statistically significant (P < .05).
at initial diagnosis and those with less severe symptoms was also inconclusive. However, patients with a longer duration of symptoms had significantly longer p1 latency compared with those having shorter duration of symptoms, which might be indicative of degeneration of neural elements and their interaction with otolithic and canalicular receptors as the BPPV recurs or persists in the long term. Longo et al5 studied patients with PC-BPPV alone and found higher abnormal VEMPs, but latency and thresholds were not different between patients and controls. Eryaman et al30 also studied patients with PC-BPPV alone and found 38.7% abnormality (absence of VEMP or latency delay) compared to controls but found no correlation between abnormal VEMP and the number of canalith reposition maneuvers required. Hong et al31 found VEMP abnormalities in patients with BPPV but without any difference
between involved semicircular canals. Comparative analysis of VEMP in BPPV patients who had posterior and lateral canal disease was not statistically significant, although amplitude depression was significant in patients with LC-BPPV as compared to healthy ears and those of control subjects in the present study. On the other hand, comparative analysis of VEMP in BPPV patients who had cupulolithiasis and canalolithiasis of the lateral canal was not statistically significant. However, decrease in p1 and n1 amplitude was statistically significant in patients with canalolithiasis as compared to healthy ears and those of control subjects. In conclusion, VEMP is a useful tool to study the otolithic function in patients with BPPV. Abnormality of VEMPs is not correlated with factors including age, severity of nystagmus at diagnosis, numbers of maneuvers
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
9
Yetiser et al applied, or site of canal involvement. However, the persistence or recurrence of symptoms has an effect on VEMP results since it has been detected that patients with a longer duration of symptoms or recurrences had significantly longer p1 latency compared with those having shorter duration of symptoms. Authors’ Note This article was presented at the 20th IFOS World Congress, June 1-5, 2013, Seoul, Korea, and has not been submitted for publication in another journal.
Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.
References 1. Gacek RR. Pathology of benign paroxysmal positional vertigo revisited. Ann Otol Rhinol Laryngol. 2003;112:574-582. 2. Colebatch JG, Halmagyi GM. Vestibular evoked potentials in human neck muscles before and after unilateral vestibular deafferentiation. Neurology. 1992;42:1635-1636. 3. Colebatch JG, Halmagyi GM, Skuse NF. Myogenic potentials generated by a click-evoked vestibulocollic response. J Neurol Neurosurg Psychiatr. 1994;57:190-197. 4. Basta D, Todt I, Ernst A. Normative data for P1/N1 latencies of vestibular evoked myogenic potentials induced by air- or bone-conducted tone bursts. Clin Neurophysiol. 2005;116(9):2216-2219. 5. Longo G, Onofri M, Pellicciari T, Quaranta N. Benign paroxysmal positional vertigo: is vestibular evoked myogenic potential testing useful? Acta Otolaryngol. 2012;132(1):39-43. 6. Welgampola MS, Colebatch JG. Characteristics and clinical applications of vestibular-evoked myogenic potentials. Neurology. 2005;64:1682-1688. 7. Colebatch JG. Properties of rectified averaging of an evokedtype signal: theory and application to the vestibular-evoked myogenic potential. Exp Brain Res. 2009;199(2):167-176. 8. Von Brevern M, Schmidt T, Schöfeld U, Lempert T, Clarke AH. Utricular dysfunction in patients with benign paroxysmal positional vertigo. Otol Neurotol. 2005;27:92-96. 9. Di Girolano S, Ottaviani F, Scarano E, Picciotti P, di Nardo W. Postural control in horizontal canal benign paroxysmal vertigo. Eur Arch Otorhinolaryngol. 2000;257:372-375. 10. Seok JI, Lee HM, Yoo JH, Lee DK. Residual dizziness after successful repositioning treatment in patients with benign paroxysmal positional vertigo. J Clin Neurol. 2008;4(3):107-110. 11. Maes L, Vinck BM, De Vel E, et al. The vestibular evoked myogenic potential: a test-retest reliability study. Clin Neurophysiol. 2009;120(3):594-600.
12. Bush ML, Jones RO, Shinn JB. The clinical reliability of vestibular evoked myogenic potentials. ENT J. 2010;89(4): 170-176. 13. Vanspauwen R, Wuts FL, Van de Heyning PH. Vestibular evoked myogenic potentials: test-retest reliability and normative values obtained with a feedback method for the sternocleidomastoid muscle contraction. J Vest Res. 2009;19:127-135. 14. Isaradisaikul S, Strong DA, Moushey JM, Gabbard SA, Ackley SR, Jenkins HA. Reliability of vestibular evoked myogenic potentials in healthy subjects. Otol Neurotol. 2008;29(4):542-544. 15. Maes L, Vinck BM, Wuyts F, et al. Clinical usefulness of the rotatory, caloric and vestibular evoked myogenic potential test in unilateral peripheral vestibular pathologies. Int J Audiol. 2011;50(8):566-576. 16. Murofushi T, Shimizu K, Takegoshi H, Cheng PW. Diagnostic value of prolonged latencies in the vestibular evoked myogenic potentials. Arch Otolaryngol Head Neck Surg. 2001;127(9):1069-1072. 17. Hong SM, Yeo SG, Kim SW, Cha CI. The results of vestibular evoked myogenic potential, with consideration of age-related changes, in vestibular neuritis, benign paroxysmal positional vertigo, and Meniere’s disease. Acta Otolaryngol. 2008;128(8):861-865. 18. Akkuzu G, Akkuzu B, Ozluoglu L. Vestibular evoked myogenic potentials in benign paroxysmal positional vertigo and Meniere’s disease. Eur Arch Otorhinolaryngol. 2006;263(6):510-517. 19. Zhang D, Fan Z, Han Y, et al. Benign paroxysmal vertigo of childhood: diagnostic value of vestibular test and high stimulus rate auditory brainstem response test. Int J Pediatr Otorhinolaryngol. 2012;76(1):107-110. 20. Chang CH, Young YH. Caloric and vestibular evoked myogenic potential tests in evaluating children with benign paroxysmal vertigo. Int J Pediatr Otorhinolaryngol. 2007;71(3):495-499. 21. Yang WS, Kim SH, Lee JD, Lee WS. Clinical significance of vestibular evoked myogenic potentials in benign paroxysmal positional vertigo. Otol Neurotol. 2008;29:1162-1166. 22. Agrawal Y, Zuniga MG, Davalos-Bichara M, et al. Decline in semicircular canal and otolith function with age. Otol Neurotol. 2012;33(5):832-839. 23. Basta D, Todt I, Ernst A. Characterization of age related changes in vestibular evoked myogenic potentials. J Vest Res. 2007;17(2-3):93-98. 24. Lee SK, Cha CI, Jung TS, Park DC, Yeo SG. Age-related differences in parameters of vestibular evoked myogenic potentials. Acta Otolaryngol. 2008;128(1):66-72. 25. Ochi K, Ohashi T. Age-related changes in the vestibularevoked myogenic potentials. Otolaryngol Head Neck Surg. 2003;129(6):655-659. 26. Su HC, Huang TW, Young YH. Cheng PW. Aging effect on vestibular evoked myogenic potential. Otol Neurotol. 2004;25(6):977-980. 27. Tang Y, Lopez I, Baloh R. Age-related change of the neuronal number in the human medial vestibular nucleus. A sterological investigation. J Vest Res. 2001-2002;11:357-363.
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
10
Annals of Otology, Rhinology & Laryngology
28. Ross MD, Peacor D, Johnsson LG, Allard LF. Observations on normal and degenerating human otoconia. Ann Otol Rhinol Laryngol. 1976;85:210-226. 29. Lee JD, Park MK, Lee BD, Lee TK, Sung KB, Park JK. Abnormality of cervical vestibular-evoked myogenic potentials and ocular vestibular evoked myogenic potentials in patients with recurrent benign paroxysmal positional vertigo. Acta Otolaryngol. 2013;133(2):150-153.
30. Eryaman E, Oz ID, Ozker BY, Erbek S, Erbek SS. Evaluation of vestibular evoked myogenic potentials during benign paroxysmal positional vertigo attacks; neuroepithelial degeneration? B-ENT. 2012;8(4):247-250. 31. Hong SM, Park DC, Yeo SG, Cha CI. Vestibular evoked myogenic potentials in patients with benign paroxysmal positional vertigo involving each semicircular canal. Am J Otolaryngol. 2008;29(3):184-187.
Downloaded from aor.sagepub.com at OhioLink on June 23, 2014
