Eur Arch Otorhinolaryngol DOI 10.1007/s00405-013-2724-5
OTOLOGY
Comparison of chirp versus click and tone pip stimulation for cervical vestibular evoked myogenic potentials Bo-Chen Wang • Yong Liang • Xiao-Long Liu Jing Zhao • You-Li Liu • Yan-Fei Li • Wei Zhang • Qi Li
•
Received: 9 April 2013 / Accepted: 19 September 2013 Ó Springer-Verlag Berlin Heidelberg 2013
Abstract The current study explored differences among cervical vestibular evoked myogenic potentials (cVEMP) that were evoked by CE-chirp and click and tone pip in healthy controls, and tried to explain the differences of cVEMP between the three of them. Thirty normal volunteers were used as subjects for CE-chirp and click and tonepip (Blackman pip) stimuli. The latency of P1, N1, peakto-peak P1–N1 amplitude, and cVEMP interaural difference were obtained and analyzed. The response rates of cVEMP were 93 % for click and 100 % for both Blackman pip and CE-chirp, respectively. The P1 and N1 latencies of cVEMP evoked by CE-chirp were the shortest, followed by click, with Blackman pip the longest (F = 6,686.852, P \ 0.001). All indices of cVEMP evoked by the three stimuli showed no significant difference between the left and right ears or between genders. cVEMP responses were significantly different between the three stimuli. Compared with the currently used stimulus, CE-chirp can evoke cVEMP with shorter latencies and demonstrates increased speed and reliability. Keywords
Chirp Click Blackman pip cVEMP
B.-C. Wang and Y. Liang contributed equally to this work. B.-C. Wang Y. Liang (&) X.-L. Liu J. Zhao Y.-L. Liu Y.-F. Li W. Zhang Q. Li Department of Otolaryngology-Head and Neck Surgery, Nanfang Hospital, Southern Medical University, Guangzhou 510515, Guangdong, China e-mail: [email protected] B.-C. Wang Department of Otolaryngology-Head and Neck Surgery, The First People’s Hospital of Foshan City, Foshan, Guangdong, China
Introduction cVEMP Cervical vestibular evoked myogenic potentials (cVEMP) are the inhibitory electrical potentials generated after a sound stimulus. They originate in the saccule and are conducted by the lower portion of the vestibular nerve to the central nervous system (CNS), generating inhibitory electrical responses that can be picked up by electrodes placed on the sternocleidomastoid (SCM) muscle [1, 2]. Currently, cVEMP is considered to be a non-invasive electrophysiological examination that shows the integrity of the sacculocollic pathway, and a clinical test that objectively evaluates the function of the saccule and inferior vestibular nerve region [3]. Normal cVEMP responses are characterized by biphasic (positive–negative) waves. The first biphasic complex is usually tagged as p13–n23 or P1–N1, and the second one is tagged as p33–n34 or P2–N2. However, the P2–N2 complex is of non-vestibular origin, which cannot be presented in all normal subjects. Different acoustic stimuli induce different cVEMP, and click, tone burst, and tone pip are acoustic stimuli in common use [4–8]. The chirp stimulus According to Be´ke´sy’s [9] ‘‘traveling wave theory’’, the cochlear traveling wave takes some time to travel from the base of the cochlea to its apical end, and there are specific frequency areas positioned longitudinally along the basilar membrane; the high frequency acoustic vibration peak is located in the cochlear base, whereas the low frequency acoustic vibration peak is located close to the top of the cochlear. Thus, the different neural units along the cochlear partition will not be stimulated at the same time when
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using traditional acoustic stimulation, such as click, tone burst, and tone pip, the delay of the traveling wave near the top of the cochlear leads to unfavorable synchronization and neural activity across all nerve fibers is disorganized relative to that of the entire basement membrane with synchronization, which causes the weak of nerve fiber impulse conduction. Shore and Nutall [10] first applied chirp to auditory electrophysiology in 1985. Chirp stimuli are designed to compensate for the time delay in the auditory periphery in an attempt to increase the temporal synchrony between the neural elements. This lack of temporal synchrony can be partly neutralized by an upward chirp stimulus, in which higher frequency components are delayed relative to lower frequency components. This was verified in the reports of Lutkenhoner et al. [11] and Kristensen et al. [12] who reported that the amplitude of the reaction of ABR induced by increasing chirp was higher compared with standard click, and many other scholars have studied the use of chirp within the auditory field and applied chirp to acoustic brainstem reaction (ABR) [13–16] and the auditory stable state response (ASSR) test [16–18]. Based on the traditional chirp acoustic stimulator, the broad-band CE-chirp was designed as described by Elberling et al. [17] using a delay model based on derivedband ABR latencies, which are more appropriate for clinical auditory electrophysiology tests. The main feature of the CE-chirp is that the frequency of the stimulus signal increases as time goes on. By adjusting the phase of the harmonics the final stimulus can be designed to produce a specific phase spectrum; for instance to compensate for cochlea traveling wave delay or the phase response of the earphone. The current study showed that frequency spectrums of CE-chirp and click were identical, but the time domains were different. Both tone burst and tone pip are short pure tones with an envelope shape comprising rise, plateau, and fall time. Specifically, after several cycles, tone burst and tone pip reach their maximum amplitude (intensity) that will continue over several cycles, and after a few more cycles they become silent. Aims of the present study The CE-chirp can compensate for temporal dispersion in the cochlea related to traveling wave delay [15], and has a different time domain from click, but the same frequency spectrum range from 200–8,000 Hz. It has been applied to tests of ABR and ASSR with favorable outcomes, for example, with shorter latency and larger amplitude in ABR. However, the application of CE-chirp to cVEMP has not yet been reported. As acoustic stimulators such as click, tone burst, and tone pip can stimulate and induce cVEMP, the CE-chirp, theoretically, can also be applied to the
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cVEMP test. In this study, we investigated the mechanisms of generation of cVEMP using CE-chirp, and explored the feasibility and advantages of using CE-chirp to induce cVEMP in comparison with other stimuli.
Methods Subjects A total of 30 healthy medical college students were introduced as subjects (60 ears, 9 males, and 21 females; age range 20–30 years with a mean of 24), and they were without history of acute and chronic ear illnesses including ear trauma, otitis media, and dizziness. Before the test, all subjects received examination by otoscopy, acoustic impedance, ear drum intactness, pure tone audiometry DPOAE and cVEMP. The pretest results were within the normal range, and subjects showed favorable differentiation of cVEMP waves induced by Blackman pip. Procedures Subjects were required to maintain a sitting posture. After cleaning the subject’s skin with 75 % ethyl alcohol and a facial scrub, surface electromyographic (EMG) electrodes were placed on the upper half of each SCM muscle, the reference electrodes were placed on the sternal notch, and the ground electrodes were placed on the forehead. Then, insertion type earphones were fixed approximately 0.5-cm deep into the external auditory canal to record cVEMP of the bilateral SCM. During the period of recording, subjects were required to turn their heads to the contralateral side until the lateral margin of the SCM could be observed with the naked eye, and the recorded SCM was maintained at tetanic contraction and as steady as possible. EMG activity was recorded using a commercial system (AEP module, Audera V2.7, Grason-Stadler, MN, USA) and was monitored at 50 lV. The EMG signal was amplified and bandpass filtered (10–1,500 Hz). Electrode resistance was \2 KX. The sound stimulus of tone pip (Blackman pip) was set to 100 dB nHL, rarefaction 500 Hz, 2-ms rise/fall time, and 1-ms plateau. The stimulus was transmitted through inserted earphones, and the repetition rate was 9.0 Hz. The analysis time was 54 ms, and 500 consecutive runs were averaged for each trial. Two consecutive trials were collected for averaging and further analysis. The CEchirp octave band (CE-chirp, Audera V2.7) and click stimuli of 0.1 ms duration were used to elicit cVEMP responses. The hardware settings and procedures were the same as for Blackman pip stimuli. The only difference was the intensity of click, which was set at 94.5 dB nHL. In order to eliminate the effect of muscle fatigue, all subjects
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were given CE-chirp octave band and Blackman pip in random order, and click was finally gave. Similarly, data from two consecutive trials were collected for averaging to increase the reproducibility of data. cVEMP responses The latency P1 was defined as the positive polarity of the biphasic wave that appeared at approximately 13 ms, and the latency N1 was defined as the negative polarity of the biphasic wave that appeared at approximately 23 ms. The initial positive–negative polarity of the waveform with peaks was determined for the presence or absence of cVEMP responses. The following recorded double phase was nominated as P2 (positive wave) and N2 (negative wave). The amplitude was defined as the peak-to-peak P1–N1 maximum energy in lV. cVEMP induced by different acoustic stimuli were recorded, and the latencies of each peak (P1, N1, P2, and N2), peak-to-peak duration (P1–N1 interval), and peakto-peak amplitude (P1–N1 amplitude) were measured and compared between the three different procedures.
Statistical analysis All statistical analyses were performed using SPSS 19.0 for Windows. A paired t tests, and two-way analysis of variance (ANOVA) was used to compare differences between stimuli. A value of P \ 0.05 was accepted as statistically significant. Descriptive analyses were performed for the following variables: P1 latency, N1 latency, P1–N1 amplitude, and P1–N1 interval. Data are presented as mean ± standard deviation (SD).
Results cVEMP response by the three stimuli The typical responses of click, CE-chirp octave band, and Blackman pip were shown in Fig. 1. cVEMP could be evoked by click in only 56 ears (93 %), while it could be induced by Blackman pip and CE-chirp in all subjects, and there were differences between P1 and N1 latencies among
Fig. 1 cVEMP evoked by click, CE-chirp octave band, and Blackman pip in a healthy female aged 25 years
Table 1 Comparison of cVEMP evoked by click, CE-chirp octave band, and Blackman pip stimulation
Click
n
P1 (ms) Mean ± SD
N1 (ms) Mean ± SD
Amplitude (lV) Mean ± SD
P1–N1 (ms) Mean ± SD
56
9.527 ± 2.464
15.451 ± 3.025
5.121 ± 2.787
5.957 ± 1.619
CE-chirp
60
4.905 ± 2.113
11.877 ± 2.775
14.422 ± 5.505
6.973 ± 1.564
Blackman pip
60
11.812 ± 2.141
19.100 ± 2.926
13.334 ± 5.849
7.240 ± 1.649
F
6,686.852
12,731.526
1,284.372
4,524.058
P
\0.001
\0.001
\0.001
\0.001
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N1 t = 147.149, P \ 0.001). The latency of cVEMP evoked by the CE-chirp octave band was approximately 7 ms shorter compared with the cVEMP evoked by Blackman pip 2-1-2 cycles. The amplitude of P1–N1 was also significantly different (P \ 0.05), but interspike interval was not significantly different (P = 0.195, Table 2). The data of Table 3 showed that no statistically significant differences were found between genders or between the two ears (P [ 0.05). Stimuli differences between the left and right ears
Fig. 2 cVEMP evoked by click (n = 56), CE-chirp octave band (n = 60), and Blackman pip (n = 60)
the three stimuli. Similar to P1 latency, N1 latency of CEchirp was the shortest, followed by click, and Blackman pip had the longest latency. The P1 latency of click, CEchirp, and Blackman pip was 9.527 ± 2.464, 4.905 ± 2.113, and 11.812 ± 2.141 ms, respectively (F = 6,686.852, P \ 0.001, two-way ANOVA). The N1 latency of click, CE-chirp, and Blackman pip was 15.451 ± 3.025, 11.877 ± 2.775, and 19.100 ± 2.926 ms, respectively (F = 12,731.526, P \ 0.001, two-way ANOVA). The P1–N1 latency of click, CE-chirp, and Blackman pip was 5.957 ± 1.619, 6.973 ± 1.564, and 7.240 ± 1.649 ms, respectively (F = 4524.058, P \ 0.001, two-way ANOVA, Table 1, Fig. 2). CE-chirp- and Blackman pip -stimuli compared A paired t test was used to compare cVEMP evoked by the CE-chirp octave band with those evoked by Blackman pip 2-1-2 cycles. The latencies of P1 and N1 were significantly different between the stimuli (P1 t = 41.921, P \ 0.001; Table 2 Comparison of cVEMP evoked by click, CEchirp octave band, and Blackman pip stimulation
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There were 27 subjects of both left and right ears that were able to evoke cVEMP by click, 30 subjects by CE-chirp and 30 subjects by Blackman pip. The differentials between the left and right ears were signed by DP1, DN1, DAM, and DP1–N1. The differentials of cVEMP evoked by the three stimuli were not statistically significant by two-way ANOVA. The computational parameters were listed in Table 4. The DP1 of click, CE-chirp, and Blackman pip was 0.270 ± 2.419, 0.087 ± 2.043, and 0.215 ± 2.361 ms, respectively (F = 0.265, P = 0.609). The DN1 was 0.606 ± 2.715, 0.420 ± 2.987, and 0.103 ± 3.383 ms, respectively (F = 2.534, P = 0.117). The DAM was 0.041 ± 2.826, 0.086 ± 7.100, and 0.864 ± 7.773 lV, respectively (F = 0.799, P = 0.375). Finally, the D(P1–N1) was 0.264 ± 1.682, 0.507 ± 2.025, and 0.414 ± 2.102 ms, respectively (F = 4.330, P = 0.042) (Table 4).
Discussion cVEMP are considered to be a non-invasive electrophysiological measure that shows the integrity of the sacculocollic pathway. Currently, it is the only available method to objectively assess the function of the saccule and the inferior portion of the vestibular nerve (IVN). Moreover, cVEMP has important clinical use for the diagnosis of vestibular system diseases and related diseases such as Meniere’s disease, endolymphatic hydrops, vestibular schwannoma, superior semicircular canal dehiscence syndrome, large vestibular aqueduct syndrome, and vestibular neuritis, and others [7, 19]. Click, tone burst, and tone pip
Indices (mean ± SD, n = 60) P1 (ms)
N1 (ms)
Amplitude (lV)
P1–N1 (ms)
CE-chirp
4.904 ± 2.113
11.877 ± 2.775
14.422 ± 5.505
6.973 ± 1.564
Blackman pip
11.812 ± 2.140
19.100 ± 2.926
13.334 ± 5.849
7.240 ± 1.649
t
41.921
47.149
2.313
1.312
P
\0.001
\0.001
0.024
0.195
0.684 0.532 0.656
6.668 ? 1.667
6.842 ? 1.364
6.997 ? 1.425
7.762 ? 1.783
14.553 ? 5.967
14.260 ? 4.749
0.744 0.350 0.572
7.348 ? 1.898 7.364 ? 1.538
7.643 ? 1.114
13.927 ? 7.134
13.392 ? 5.706
0.086 0.458
In this study, cVEMP were recorded by click, CE-chirp, and Blackman pip, with response rates of 93, 100, and 100 %, respectively. Thus, click response rate was relatively low compared with the other stimuli. As the stimulus intensity of click was relatively weak (94.5 dB nHL), the influence of stimulus intensity could not be excluded. Moreover, the results demonstrated that the CE-chirp octave band can be used as a new cVEMP acoustic stimulator, which can more stably induce cVEMP responses compared with other stimuli.
0.254
0.600
0.869
The effect of the three acoustic stimuli on cVEMP latency
P
14.032 ? 4.620
15.190 ? 7.580
11.921 ? 3.044
11.074 ? 2.329
12.046 ? 2.737
12.181 ? 2.927
5.255 ? 2.004
9
5.051 ? 2.272 21 Female
Male
4.418 ? 1.857
4.233 ? 2.319
0.612 0.530 0.528 0.633 P
CE-Chirp
0.857
11.837 ? 4.765
19.291 ? 3.244
18.484 ? 2.295
19.279 ? 2.918 12.039 ? 2.133
9
11.641 ? 2.305
21 Female
Blackman pip
Male
11.917 ? 2.093
RE
11.210 ? 2.356
18.856 ? 3.098
13.359 ? 5.151
RE LE LE RE LE LE
RE
P1–N1 (ms) N1 (ms)
Amplitude (lV)
are acoustic stimuli commonly used in tests of cVEMP. As a result of the distinctive properties of the acoustic stimuli, the cVEMP indices, induced by different acoustic stimulators, were different [4, 8, 20]. The current study mainly focused on the function and value of CE-chirp to cVEMP responses. The current study showed that frequency spectrums of CE-chirp and click were identical, but the time domains were different. Chirp includes the broadband CEchirp and four kinds of octave-band chirps (frequency 500, 1,000, 2,000, and 4,000 Hz). The frequency of broadband CE-chirp is in the range of 500–8,000 Hz [21]. A study by Akin et al. [22] suggested that the optimal and lowest thresholds of cVEMP responses could be obtained at the frequencies of 500 and 750 Hz. Thus, in this study we used the CE-chirp octave band at a frequency of 500 Hz. The effect of the three acoustic stimuli on the response rate of cVEMP
P1 (ms) n
Table 3 Mean ± SD obtained for P1, N1, amplitude, and P1–N1 for gender and interaural elicited by Blackman pip- and CE-chirp-evoked cVEMP in healthy subjects
6.300 ? 1.628
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By comparing the latencies of cVEMP indices, this study showed two important results. First, the latency of P1 response by click was approximately 2 ms shorter compared with Blackman pip, in agreement with similar conclusions shown in many other studies. Cheng et al. [4] and Viciana et al. [21] suggested that the latencies of cVEMP responses induced by click were 1 ms shorter compared with short tone burst (STB), and theorized that it maybe because of the delay of the STB stimulus in reaching maximum intensity in a 1-ms rise/fall time. Meanwhile, a previous study [23] also depicted that primary vestibular neurons might have double or triple firings to one tone burst. Both tone burst and tone pip are short pure tones with an envelope shape comprising rise, plateau, and fall time. Specifically, after several cycles, tone burst and tone pip reach their maximum amplitude (intensity) that will continue over several cycles, and after a few more cycles they become silent. Therefore, changes in the three parts of the cycle, especially in the rise time, will affect the frequency spectrum of tone burst and tone pip. In addition, side-lobe
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Eur Arch Otorhinolaryngol Table 4 Differentials of P1, N1, amplitude, and P1–N1 of cVEMP between the left and right ear
Click
n
DP1 (L–R) (ms) Mean ± SD
DN1 (L–R) (ms) Mean ± SD
DAmplitude (L–R) (lV) Mean ± SD
DP1–N1 (L–R) (ms) Mean ± SD
27
0.270 ± 2.419
0.606 ± 2.715
0.041 ± 2.826
0.264 ± 1.682
CE-chirp
30
0.087 ± 2.043
0.420 ± 2.987
0.086 ± 7.100
0.507 ± 2.025
Blackman pip
30
0.215 ± 2.361
0.103 ± 3.383
0.864 ± 7.773
0.414 ± 2.102
F
0.265
2.534
0.799
4.330
P
0.609
0.117
0.375
0.042
energy is higher if the duration is shorter, or lower if the duration is longer. This may explain why the P1 latencies by click and Blackman pip in this study were 9.527 ± 2.464 and 11.812 ± 2.141 ms with approximately 2 ms difference between them. However, the main reason is likely that this study used Blackman Pip 2-1-2 cycles (rise/fall time, 2 ms). For the effect of stimulus intensity on latency, Akin et al. [19] argued that the stimulus intensity of cVEMP should be 95–100 dB nHL, within which the latency of cVEMP was the most invariable. However, previous studies all chose click with high stimulus intensity (120 dB SPL). A decline in the stimulus intensity of click results in a decrease in amplitude of the cVEMP response, such that the cVEMP response cannot be generated when the stimulus intensity decreases to 90–100 dB SPL. Conversely, the amplitude of the cVEMP response increases with an increase in stimulus intensity. The functional relationship is denoted by Y = 8.3X - 650 (where X is dB HL, and Y is lV) [24], which shows that the amplitude of cVEMP response is positively correlated with both stimulus intensity and muscle tone [25]. McNerney et al. [26] also argued that the latencies of cVEMP’ indices become invariable when the acoustic stimulus is over 110 dB pSPL. The effect of the three acoustic stimuli on cVEMP amplitude and the difference between the two ears Neck muscle strength is one of the main external factors that affects the amplitude of the cVEMP, in addition to the intensity of the stimuli and absolute sound energy. In order to eliminate the effect of muscle fatigue, all subjects were given CE-chirp and Blackman pip in random order, and EMG activity was recorded and monitored at [50 lV. Under the same stimulus intensity, the amplitude of cVEMP induced by Blackman pip and CE-chirp was 13.334 ± 5.849 lV and 14.422 ± 5.505 lV, respectively. Although the difference was significant (P \ 0.05), it is not clear whether such a small difference could be affected by muscle strength. By analyzing the interaural difference in cVEMP (in both the right and left ears) elicited by the three stimuli, we found that there was no obvious interaural
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difference among the three stimuli or among different subjects. However, the SD of all the parameters in the CEchirp group was the smallest, which suggests that the interaural difference in cVEMP induced by CE-chirp was more stable. The effect of the CE-chirp stimuli on cVEMP latency P1 and N1 induced by CE-chirp had latencies of 4.905 ± 2.113 and 11.877 ± 2.775 ms, respectively, compared with latencies induced by other stimuli (click 9.527 ± 2.4647, 15.451 ± 3.025 ms; Blackman pip 11.812 ± 2.141, 19.100 ± 2.926 ms). CE-chirp latency was significantly shorter, and the SD of the latency was smaller with less fluctuation and was more stable. In addition, the statistical result of P1–N1 also showed that SD latency of CE-chirp was the smallest and most steady (CE-chirp 1.564 ms, click 1.619 ms, Blackman pip 1.649 ms). Reasons why the cVEMP latency was significantly shorter may be as follows: Previous studies [27–29] showed that components of the cochlea were not related to cVEMP, however, whether the physiological structure of the cochlea affects cVEMP or not has not yet been elucidated. CE-chirp overcomes the afferent nerve energy dispersion induced by cochlear traveling wave delay, and obtains a more favorable synchronization of basilar membrane impulses, which causes an increase in energy and amplitude of basilar membrane vibration. Furthermore, due to the unity of the membranous labyrinth in the cochlea and vestibular, there will be strenuous movement of endolymph fluid. Kondrachuk’s experiment [30] showed that a weak change in endolymph pressure could cause significant displacement of the basement membrane, which indicated that CE-chirp could activate the sacculus more effectively and with greater sensitivity. These can be indirectly reflected by the ‘‘third window effect’’, and Arts’s [31], Modugno’s [32], Gopen’s [33] and Zhou’s [34] experiment found, cVEMP responses were present with abnormally low thresholds, in patients with superior semicircular canal dehiscence(SSCD), Bilateral Dehiscence of the Bony Cochlear Basal Turn, posterior semicircular canal
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dehiscence and enlarged vestibular aqueduct (EVA), or many studies have shown that cVEMP derived from the sacculus is related to the inferior vestibular nerve activity. The upper terminal branches of the vestibular nerve mainly distribute in the superior semicircular canal, horizontal semicircular canal, utricle, and a small part of the sacculus. The function of the upper terminal branches can be evaluated using the variable temperature test. IVN branches distribute in the posterior semicircular canal and most parts of the sacculus, and IVN function can be evaluated using cVEMP. The vestibule itself has certain frequency characteristics, as Kerr et al. [35] and Perez et al. [36] have shown there was a correlation between vestibular organ frequency distribution, anatomical position, and basement membrane width. The CE-chirp’s frequency distribution spectrum from low to high frequency may synchronously better activate the entire inferior portion of the vestibular nerve pathway receptors (posterior semicircular canal and the sacculus).
Summary and conclusion The results obtained from the current study demonstrate that CE-chirp is a novel, sensitive, efficient, and reliable stimulus of cVEMP. Compared with conventional stimuli, CE-chirp can evoke cVEMP with shorter latencies and produce a more stable reaction. Further studies will be performed to explain the reason for this phenomenon in future.
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Eur Arch Otorhinolaryngol 29. Takegoshi H, Murofushi T (2003) Effect of white noise on vestibular evoked myogenic potentials. Hear Res 176:59–64 30. Kondrachuk AV (2000) Computer simulation of the mechanical stimulation of the saccular membrane of bullfrog. Hear Res 143:130–138 31. ArtsHA, Adams ME, Telian SA, El-Kashlan H, Kileny PR (2009)Reversible electrocochleographic abnormalities in superior canaldehiscence. Otol Neurotol 30:79–86 32. Modugno GC, Brandolini C, Cappello I, Pirodda A (2004) Bilateral dehiscence of the bony cochlear basal turn. Arch Otol Head Neck Surg 130:1427–1429
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33. Gopen Q, Zhou G, Poe D, Kenna M, Jones D (2010) Posterior semicircular canal dehiscence: first reported case series. Otol Neurotol 31:339–344 34. Zhou G, Gopen Q, Kenna MA (2008) Delineating the hearing loss in children with enlarged vestibular aqueduct. Laryngoscope 118:2062–2066 35. Kerr AG (2005) Assessment of vertigo. Ann Acad Med Singapore 34:285–288 36. Perez N, Rama-Lopez J (2003) Head-impulse and caloric tests in patients with dizziness. Otol Neurotol 24:913–917
OTOLOGY
Comparison of chirp versus click and tone pip stimulation for cervical vestibular evoked myogenic potentials Bo-Chen Wang • Yong Liang • Xiao-Long Liu Jing Zhao • You-Li Liu • Yan-Fei Li • Wei Zhang • Qi Li
•
Received: 9 April 2013 / Accepted: 19 September 2013 Ó Springer-Verlag Berlin Heidelberg 2013
Abstract The current study explored differences among cervical vestibular evoked myogenic potentials (cVEMP) that were evoked by CE-chirp and click and tone pip in healthy controls, and tried to explain the differences of cVEMP between the three of them. Thirty normal volunteers were used as subjects for CE-chirp and click and tonepip (Blackman pip) stimuli. The latency of P1, N1, peakto-peak P1–N1 amplitude, and cVEMP interaural difference were obtained and analyzed. The response rates of cVEMP were 93 % for click and 100 % for both Blackman pip and CE-chirp, respectively. The P1 and N1 latencies of cVEMP evoked by CE-chirp were the shortest, followed by click, with Blackman pip the longest (F = 6,686.852, P \ 0.001). All indices of cVEMP evoked by the three stimuli showed no significant difference between the left and right ears or between genders. cVEMP responses were significantly different between the three stimuli. Compared with the currently used stimulus, CE-chirp can evoke cVEMP with shorter latencies and demonstrates increased speed and reliability. Keywords
Chirp Click Blackman pip cVEMP
B.-C. Wang and Y. Liang contributed equally to this work. B.-C. Wang Y. Liang (&) X.-L. Liu J. Zhao Y.-L. Liu Y.-F. Li W. Zhang Q. Li Department of Otolaryngology-Head and Neck Surgery, Nanfang Hospital, Southern Medical University, Guangzhou 510515, Guangdong, China e-mail: [email protected] B.-C. Wang Department of Otolaryngology-Head and Neck Surgery, The First People’s Hospital of Foshan City, Foshan, Guangdong, China
Introduction cVEMP Cervical vestibular evoked myogenic potentials (cVEMP) are the inhibitory electrical potentials generated after a sound stimulus. They originate in the saccule and are conducted by the lower portion of the vestibular nerve to the central nervous system (CNS), generating inhibitory electrical responses that can be picked up by electrodes placed on the sternocleidomastoid (SCM) muscle [1, 2]. Currently, cVEMP is considered to be a non-invasive electrophysiological examination that shows the integrity of the sacculocollic pathway, and a clinical test that objectively evaluates the function of the saccule and inferior vestibular nerve region [3]. Normal cVEMP responses are characterized by biphasic (positive–negative) waves. The first biphasic complex is usually tagged as p13–n23 or P1–N1, and the second one is tagged as p33–n34 or P2–N2. However, the P2–N2 complex is of non-vestibular origin, which cannot be presented in all normal subjects. Different acoustic stimuli induce different cVEMP, and click, tone burst, and tone pip are acoustic stimuli in common use [4–8]. The chirp stimulus According to Be´ke´sy’s [9] ‘‘traveling wave theory’’, the cochlear traveling wave takes some time to travel from the base of the cochlea to its apical end, and there are specific frequency areas positioned longitudinally along the basilar membrane; the high frequency acoustic vibration peak is located in the cochlear base, whereas the low frequency acoustic vibration peak is located close to the top of the cochlear. Thus, the different neural units along the cochlear partition will not be stimulated at the same time when
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using traditional acoustic stimulation, such as click, tone burst, and tone pip, the delay of the traveling wave near the top of the cochlear leads to unfavorable synchronization and neural activity across all nerve fibers is disorganized relative to that of the entire basement membrane with synchronization, which causes the weak of nerve fiber impulse conduction. Shore and Nutall [10] first applied chirp to auditory electrophysiology in 1985. Chirp stimuli are designed to compensate for the time delay in the auditory periphery in an attempt to increase the temporal synchrony between the neural elements. This lack of temporal synchrony can be partly neutralized by an upward chirp stimulus, in which higher frequency components are delayed relative to lower frequency components. This was verified in the reports of Lutkenhoner et al. [11] and Kristensen et al. [12] who reported that the amplitude of the reaction of ABR induced by increasing chirp was higher compared with standard click, and many other scholars have studied the use of chirp within the auditory field and applied chirp to acoustic brainstem reaction (ABR) [13–16] and the auditory stable state response (ASSR) test [16–18]. Based on the traditional chirp acoustic stimulator, the broad-band CE-chirp was designed as described by Elberling et al. [17] using a delay model based on derivedband ABR latencies, which are more appropriate for clinical auditory electrophysiology tests. The main feature of the CE-chirp is that the frequency of the stimulus signal increases as time goes on. By adjusting the phase of the harmonics the final stimulus can be designed to produce a specific phase spectrum; for instance to compensate for cochlea traveling wave delay or the phase response of the earphone. The current study showed that frequency spectrums of CE-chirp and click were identical, but the time domains were different. Both tone burst and tone pip are short pure tones with an envelope shape comprising rise, plateau, and fall time. Specifically, after several cycles, tone burst and tone pip reach their maximum amplitude (intensity) that will continue over several cycles, and after a few more cycles they become silent. Aims of the present study The CE-chirp can compensate for temporal dispersion in the cochlea related to traveling wave delay [15], and has a different time domain from click, but the same frequency spectrum range from 200–8,000 Hz. It has been applied to tests of ABR and ASSR with favorable outcomes, for example, with shorter latency and larger amplitude in ABR. However, the application of CE-chirp to cVEMP has not yet been reported. As acoustic stimulators such as click, tone burst, and tone pip can stimulate and induce cVEMP, the CE-chirp, theoretically, can also be applied to the
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cVEMP test. In this study, we investigated the mechanisms of generation of cVEMP using CE-chirp, and explored the feasibility and advantages of using CE-chirp to induce cVEMP in comparison with other stimuli.
Methods Subjects A total of 30 healthy medical college students were introduced as subjects (60 ears, 9 males, and 21 females; age range 20–30 years with a mean of 24), and they were without history of acute and chronic ear illnesses including ear trauma, otitis media, and dizziness. Before the test, all subjects received examination by otoscopy, acoustic impedance, ear drum intactness, pure tone audiometry DPOAE and cVEMP. The pretest results were within the normal range, and subjects showed favorable differentiation of cVEMP waves induced by Blackman pip. Procedures Subjects were required to maintain a sitting posture. After cleaning the subject’s skin with 75 % ethyl alcohol and a facial scrub, surface electromyographic (EMG) electrodes were placed on the upper half of each SCM muscle, the reference electrodes were placed on the sternal notch, and the ground electrodes were placed on the forehead. Then, insertion type earphones were fixed approximately 0.5-cm deep into the external auditory canal to record cVEMP of the bilateral SCM. During the period of recording, subjects were required to turn their heads to the contralateral side until the lateral margin of the SCM could be observed with the naked eye, and the recorded SCM was maintained at tetanic contraction and as steady as possible. EMG activity was recorded using a commercial system (AEP module, Audera V2.7, Grason-Stadler, MN, USA) and was monitored at 50 lV. The EMG signal was amplified and bandpass filtered (10–1,500 Hz). Electrode resistance was \2 KX. The sound stimulus of tone pip (Blackman pip) was set to 100 dB nHL, rarefaction 500 Hz, 2-ms rise/fall time, and 1-ms plateau. The stimulus was transmitted through inserted earphones, and the repetition rate was 9.0 Hz. The analysis time was 54 ms, and 500 consecutive runs were averaged for each trial. Two consecutive trials were collected for averaging and further analysis. The CEchirp octave band (CE-chirp, Audera V2.7) and click stimuli of 0.1 ms duration were used to elicit cVEMP responses. The hardware settings and procedures were the same as for Blackman pip stimuli. The only difference was the intensity of click, which was set at 94.5 dB nHL. In order to eliminate the effect of muscle fatigue, all subjects
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were given CE-chirp octave band and Blackman pip in random order, and click was finally gave. Similarly, data from two consecutive trials were collected for averaging to increase the reproducibility of data. cVEMP responses The latency P1 was defined as the positive polarity of the biphasic wave that appeared at approximately 13 ms, and the latency N1 was defined as the negative polarity of the biphasic wave that appeared at approximately 23 ms. The initial positive–negative polarity of the waveform with peaks was determined for the presence or absence of cVEMP responses. The following recorded double phase was nominated as P2 (positive wave) and N2 (negative wave). The amplitude was defined as the peak-to-peak P1–N1 maximum energy in lV. cVEMP induced by different acoustic stimuli were recorded, and the latencies of each peak (P1, N1, P2, and N2), peak-to-peak duration (P1–N1 interval), and peakto-peak amplitude (P1–N1 amplitude) were measured and compared between the three different procedures.
Statistical analysis All statistical analyses were performed using SPSS 19.0 for Windows. A paired t tests, and two-way analysis of variance (ANOVA) was used to compare differences between stimuli. A value of P \ 0.05 was accepted as statistically significant. Descriptive analyses were performed for the following variables: P1 latency, N1 latency, P1–N1 amplitude, and P1–N1 interval. Data are presented as mean ± standard deviation (SD).
Results cVEMP response by the three stimuli The typical responses of click, CE-chirp octave band, and Blackman pip were shown in Fig. 1. cVEMP could be evoked by click in only 56 ears (93 %), while it could be induced by Blackman pip and CE-chirp in all subjects, and there were differences between P1 and N1 latencies among
Fig. 1 cVEMP evoked by click, CE-chirp octave band, and Blackman pip in a healthy female aged 25 years
Table 1 Comparison of cVEMP evoked by click, CE-chirp octave band, and Blackman pip stimulation
Click
n
P1 (ms) Mean ± SD
N1 (ms) Mean ± SD
Amplitude (lV) Mean ± SD
P1–N1 (ms) Mean ± SD
56
9.527 ± 2.464
15.451 ± 3.025
5.121 ± 2.787
5.957 ± 1.619
CE-chirp
60
4.905 ± 2.113
11.877 ± 2.775
14.422 ± 5.505
6.973 ± 1.564
Blackman pip
60
11.812 ± 2.141
19.100 ± 2.926
13.334 ± 5.849
7.240 ± 1.649
F
6,686.852
12,731.526
1,284.372
4,524.058
P
\0.001
\0.001
\0.001
\0.001
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N1 t = 147.149, P \ 0.001). The latency of cVEMP evoked by the CE-chirp octave band was approximately 7 ms shorter compared with the cVEMP evoked by Blackman pip 2-1-2 cycles. The amplitude of P1–N1 was also significantly different (P \ 0.05), but interspike interval was not significantly different (P = 0.195, Table 2). The data of Table 3 showed that no statistically significant differences were found between genders or between the two ears (P [ 0.05). Stimuli differences between the left and right ears
Fig. 2 cVEMP evoked by click (n = 56), CE-chirp octave band (n = 60), and Blackman pip (n = 60)
the three stimuli. Similar to P1 latency, N1 latency of CEchirp was the shortest, followed by click, and Blackman pip had the longest latency. The P1 latency of click, CEchirp, and Blackman pip was 9.527 ± 2.464, 4.905 ± 2.113, and 11.812 ± 2.141 ms, respectively (F = 6,686.852, P \ 0.001, two-way ANOVA). The N1 latency of click, CE-chirp, and Blackman pip was 15.451 ± 3.025, 11.877 ± 2.775, and 19.100 ± 2.926 ms, respectively (F = 12,731.526, P \ 0.001, two-way ANOVA). The P1–N1 latency of click, CE-chirp, and Blackman pip was 5.957 ± 1.619, 6.973 ± 1.564, and 7.240 ± 1.649 ms, respectively (F = 4524.058, P \ 0.001, two-way ANOVA, Table 1, Fig. 2). CE-chirp- and Blackman pip -stimuli compared A paired t test was used to compare cVEMP evoked by the CE-chirp octave band with those evoked by Blackman pip 2-1-2 cycles. The latencies of P1 and N1 were significantly different between the stimuli (P1 t = 41.921, P \ 0.001; Table 2 Comparison of cVEMP evoked by click, CEchirp octave band, and Blackman pip stimulation
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There were 27 subjects of both left and right ears that were able to evoke cVEMP by click, 30 subjects by CE-chirp and 30 subjects by Blackman pip. The differentials between the left and right ears were signed by DP1, DN1, DAM, and DP1–N1. The differentials of cVEMP evoked by the three stimuli were not statistically significant by two-way ANOVA. The computational parameters were listed in Table 4. The DP1 of click, CE-chirp, and Blackman pip was 0.270 ± 2.419, 0.087 ± 2.043, and 0.215 ± 2.361 ms, respectively (F = 0.265, P = 0.609). The DN1 was 0.606 ± 2.715, 0.420 ± 2.987, and 0.103 ± 3.383 ms, respectively (F = 2.534, P = 0.117). The DAM was 0.041 ± 2.826, 0.086 ± 7.100, and 0.864 ± 7.773 lV, respectively (F = 0.799, P = 0.375). Finally, the D(P1–N1) was 0.264 ± 1.682, 0.507 ± 2.025, and 0.414 ± 2.102 ms, respectively (F = 4.330, P = 0.042) (Table 4).
Discussion cVEMP are considered to be a non-invasive electrophysiological measure that shows the integrity of the sacculocollic pathway. Currently, it is the only available method to objectively assess the function of the saccule and the inferior portion of the vestibular nerve (IVN). Moreover, cVEMP has important clinical use for the diagnosis of vestibular system diseases and related diseases such as Meniere’s disease, endolymphatic hydrops, vestibular schwannoma, superior semicircular canal dehiscence syndrome, large vestibular aqueduct syndrome, and vestibular neuritis, and others [7, 19]. Click, tone burst, and tone pip
Indices (mean ± SD, n = 60) P1 (ms)
N1 (ms)
Amplitude (lV)
P1–N1 (ms)
CE-chirp
4.904 ± 2.113
11.877 ± 2.775
14.422 ± 5.505
6.973 ± 1.564
Blackman pip
11.812 ± 2.140
19.100 ± 2.926
13.334 ± 5.849
7.240 ± 1.649
t
41.921
47.149
2.313
1.312
P
\0.001
\0.001
0.024
0.195
0.684 0.532 0.656
6.668 ? 1.667
6.842 ? 1.364
6.997 ? 1.425
7.762 ? 1.783
14.553 ? 5.967
14.260 ? 4.749
0.744 0.350 0.572
7.348 ? 1.898 7.364 ? 1.538
7.643 ? 1.114
13.927 ? 7.134
13.392 ? 5.706
0.086 0.458
In this study, cVEMP were recorded by click, CE-chirp, and Blackman pip, with response rates of 93, 100, and 100 %, respectively. Thus, click response rate was relatively low compared with the other stimuli. As the stimulus intensity of click was relatively weak (94.5 dB nHL), the influence of stimulus intensity could not be excluded. Moreover, the results demonstrated that the CE-chirp octave band can be used as a new cVEMP acoustic stimulator, which can more stably induce cVEMP responses compared with other stimuli.
0.254
0.600
0.869
The effect of the three acoustic stimuli on cVEMP latency
P
14.032 ? 4.620
15.190 ? 7.580
11.921 ? 3.044
11.074 ? 2.329
12.046 ? 2.737
12.181 ? 2.927
5.255 ? 2.004
9
5.051 ? 2.272 21 Female
Male
4.418 ? 1.857
4.233 ? 2.319
0.612 0.530 0.528 0.633 P
CE-Chirp
0.857
11.837 ? 4.765
19.291 ? 3.244
18.484 ? 2.295
19.279 ? 2.918 12.039 ? 2.133
9
11.641 ? 2.305
21 Female
Blackman pip
Male
11.917 ? 2.093
RE
11.210 ? 2.356
18.856 ? 3.098
13.359 ? 5.151
RE LE LE RE LE LE
RE
P1–N1 (ms) N1 (ms)
Amplitude (lV)
are acoustic stimuli commonly used in tests of cVEMP. As a result of the distinctive properties of the acoustic stimuli, the cVEMP indices, induced by different acoustic stimulators, were different [4, 8, 20]. The current study mainly focused on the function and value of CE-chirp to cVEMP responses. The current study showed that frequency spectrums of CE-chirp and click were identical, but the time domains were different. Chirp includes the broadband CEchirp and four kinds of octave-band chirps (frequency 500, 1,000, 2,000, and 4,000 Hz). The frequency of broadband CE-chirp is in the range of 500–8,000 Hz [21]. A study by Akin et al. [22] suggested that the optimal and lowest thresholds of cVEMP responses could be obtained at the frequencies of 500 and 750 Hz. Thus, in this study we used the CE-chirp octave band at a frequency of 500 Hz. The effect of the three acoustic stimuli on the response rate of cVEMP
P1 (ms) n
Table 3 Mean ± SD obtained for P1, N1, amplitude, and P1–N1 for gender and interaural elicited by Blackman pip- and CE-chirp-evoked cVEMP in healthy subjects
6.300 ? 1.628
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By comparing the latencies of cVEMP indices, this study showed two important results. First, the latency of P1 response by click was approximately 2 ms shorter compared with Blackman pip, in agreement with similar conclusions shown in many other studies. Cheng et al. [4] and Viciana et al. [21] suggested that the latencies of cVEMP responses induced by click were 1 ms shorter compared with short tone burst (STB), and theorized that it maybe because of the delay of the STB stimulus in reaching maximum intensity in a 1-ms rise/fall time. Meanwhile, a previous study [23] also depicted that primary vestibular neurons might have double or triple firings to one tone burst. Both tone burst and tone pip are short pure tones with an envelope shape comprising rise, plateau, and fall time. Specifically, after several cycles, tone burst and tone pip reach their maximum amplitude (intensity) that will continue over several cycles, and after a few more cycles they become silent. Therefore, changes in the three parts of the cycle, especially in the rise time, will affect the frequency spectrum of tone burst and tone pip. In addition, side-lobe
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Click
n
DP1 (L–R) (ms) Mean ± SD
DN1 (L–R) (ms) Mean ± SD
DAmplitude (L–R) (lV) Mean ± SD
DP1–N1 (L–R) (ms) Mean ± SD
27
0.270 ± 2.419
0.606 ± 2.715
0.041 ± 2.826
0.264 ± 1.682
CE-chirp
30
0.087 ± 2.043
0.420 ± 2.987
0.086 ± 7.100
0.507 ± 2.025
Blackman pip
30
0.215 ± 2.361
0.103 ± 3.383
0.864 ± 7.773
0.414 ± 2.102
F
0.265
2.534
0.799
4.330
P
0.609
0.117
0.375
0.042
energy is higher if the duration is shorter, or lower if the duration is longer. This may explain why the P1 latencies by click and Blackman pip in this study were 9.527 ± 2.464 and 11.812 ± 2.141 ms with approximately 2 ms difference between them. However, the main reason is likely that this study used Blackman Pip 2-1-2 cycles (rise/fall time, 2 ms). For the effect of stimulus intensity on latency, Akin et al. [19] argued that the stimulus intensity of cVEMP should be 95–100 dB nHL, within which the latency of cVEMP was the most invariable. However, previous studies all chose click with high stimulus intensity (120 dB SPL). A decline in the stimulus intensity of click results in a decrease in amplitude of the cVEMP response, such that the cVEMP response cannot be generated when the stimulus intensity decreases to 90–100 dB SPL. Conversely, the amplitude of the cVEMP response increases with an increase in stimulus intensity. The functional relationship is denoted by Y = 8.3X - 650 (where X is dB HL, and Y is lV) [24], which shows that the amplitude of cVEMP response is positively correlated with both stimulus intensity and muscle tone [25]. McNerney et al. [26] also argued that the latencies of cVEMP’ indices become invariable when the acoustic stimulus is over 110 dB pSPL. The effect of the three acoustic stimuli on cVEMP amplitude and the difference between the two ears Neck muscle strength is one of the main external factors that affects the amplitude of the cVEMP, in addition to the intensity of the stimuli and absolute sound energy. In order to eliminate the effect of muscle fatigue, all subjects were given CE-chirp and Blackman pip in random order, and EMG activity was recorded and monitored at [50 lV. Under the same stimulus intensity, the amplitude of cVEMP induced by Blackman pip and CE-chirp was 13.334 ± 5.849 lV and 14.422 ± 5.505 lV, respectively. Although the difference was significant (P \ 0.05), it is not clear whether such a small difference could be affected by muscle strength. By analyzing the interaural difference in cVEMP (in both the right and left ears) elicited by the three stimuli, we found that there was no obvious interaural
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difference among the three stimuli or among different subjects. However, the SD of all the parameters in the CEchirp group was the smallest, which suggests that the interaural difference in cVEMP induced by CE-chirp was more stable. The effect of the CE-chirp stimuli on cVEMP latency P1 and N1 induced by CE-chirp had latencies of 4.905 ± 2.113 and 11.877 ± 2.775 ms, respectively, compared with latencies induced by other stimuli (click 9.527 ± 2.4647, 15.451 ± 3.025 ms; Blackman pip 11.812 ± 2.141, 19.100 ± 2.926 ms). CE-chirp latency was significantly shorter, and the SD of the latency was smaller with less fluctuation and was more stable. In addition, the statistical result of P1–N1 also showed that SD latency of CE-chirp was the smallest and most steady (CE-chirp 1.564 ms, click 1.619 ms, Blackman pip 1.649 ms). Reasons why the cVEMP latency was significantly shorter may be as follows: Previous studies [27–29] showed that components of the cochlea were not related to cVEMP, however, whether the physiological structure of the cochlea affects cVEMP or not has not yet been elucidated. CE-chirp overcomes the afferent nerve energy dispersion induced by cochlear traveling wave delay, and obtains a more favorable synchronization of basilar membrane impulses, which causes an increase in energy and amplitude of basilar membrane vibration. Furthermore, due to the unity of the membranous labyrinth in the cochlea and vestibular, there will be strenuous movement of endolymph fluid. Kondrachuk’s experiment [30] showed that a weak change in endolymph pressure could cause significant displacement of the basement membrane, which indicated that CE-chirp could activate the sacculus more effectively and with greater sensitivity. These can be indirectly reflected by the ‘‘third window effect’’, and Arts’s [31], Modugno’s [32], Gopen’s [33] and Zhou’s [34] experiment found, cVEMP responses were present with abnormally low thresholds, in patients with superior semicircular canal dehiscence(SSCD), Bilateral Dehiscence of the Bony Cochlear Basal Turn, posterior semicircular canal
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dehiscence and enlarged vestibular aqueduct (EVA), or many studies have shown that cVEMP derived from the sacculus is related to the inferior vestibular nerve activity. The upper terminal branches of the vestibular nerve mainly distribute in the superior semicircular canal, horizontal semicircular canal, utricle, and a small part of the sacculus. The function of the upper terminal branches can be evaluated using the variable temperature test. IVN branches distribute in the posterior semicircular canal and most parts of the sacculus, and IVN function can be evaluated using cVEMP. The vestibule itself has certain frequency characteristics, as Kerr et al. [35] and Perez et al. [36] have shown there was a correlation between vestibular organ frequency distribution, anatomical position, and basement membrane width. The CE-chirp’s frequency distribution spectrum from low to high frequency may synchronously better activate the entire inferior portion of the vestibular nerve pathway receptors (posterior semicircular canal and the sacculus).
Summary and conclusion The results obtained from the current study demonstrate that CE-chirp is a novel, sensitive, efficient, and reliable stimulus of cVEMP. Compared with conventional stimuli, CE-chirp can evoke cVEMP with shorter latencies and produce a more stable reaction. Further studies will be performed to explain the reason for this phenomenon in future.
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