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The impact of stimulation rates in vestibular evoked myogenic potential testing

Abstracts

Vestibular evoked myogenic potentials (VEMP) have been used in complementary otoneurological assessment, but the use of VEMP in clinical settings is limited. VEMPs can be used to assess vestibular function, particularly of the saccule, the inferior vestibular nerve, and/or the vestibular nucleus.

OBJECTIVE:

To verify the highest possible - and reliable - stimulation rate to obtain VEMPs.

METHOD:

The VEMPs of 18 subjects were acquired using stimulation rates ranging between 5.1 and 40.8 stimuli per second. Study design: cross-sectional contemporary cohort study.

RESULTS:

Latencies were kept unaltered and amplitudes were progressively reduced as stimulation rates were increased. However, ANOVA and the Kruskal-Wallis test failed to find statistically significant differences between the tested parameters. The study further indicated that when stimulation rates of 5.1 and 10.2 stimuli per second were compared, no statistically significant differences were observed in latency.

CONCLUSION:

The highest reliable stimulation rate observed in the group of young adults with normal hearing included in this study was 10.2 stimuli per second.

acoustic stimulation; vestibular evoked myogenic potential; vestibular function tests


Os potenciais miogênicos evocados vestibulares (VEMP) vêm sendo empregados como exame complementar para estudos otoneurológicos, ainda pouco explorados clinicamente. Esse potencial avalia a função vestibular, especificamente do sáculo, nervo vestibular inferior e/ou núcleo vestibular.

OBJETIVO:

Verificar a maior taxa de estímulos possível (e confiável) na obtenção do VEMP.

MÉTODO:

Foi registrado o potencial em 18 sujeitos, variando-se a taxa de estímulos entre 5,1 e 40,8 estímulos/s. Forma de estudo: Estudo de coorte contemporânea com corte transversal.

RESULTADOS:

As latências se mantiveram constantes e as amplitudes foram progressivamente reduzidas com o aumento da taxa de estimulação. Contudo, não houve diferença estatisticamente significativa entre os parâmetros simultaneamente, quando aplicados os testes ANOVA e Kruskal-Wallis. Os dados obtidos nesta pesquisa demonstraram que, quando comparadas as taxas de estimulação de 5,1 e 10,2 estímulos/s, houve ausência de diferença estatisticamente significativas para o parâmetro latência.

CONCLUSÃO:

Conclui-se que a maior taxa de estimulação confiável é a de 10,2 estímulos/s, para a amostra estudada de adultos jovens ouvintes normais.

estimulação acústica; potencial evocado motor; testes de função vestibular


INTRODUCTION

Vestibular evoked myogenic potentials (VEMP) have been used in the complementary assessment of vestibular function, particularly of the saccule, the inferior vestibular nerve, and/or the vestibular nucleus11. Damen MMJ. Vestibular evoked myogenic potential (VEMP). Clinical application of the threshold. Medical Engineering. Eindhoven: Technische Universiteit Eindhoven; 2007.

2. Pollak L, Kushnir M, Stryjer R. Diagnostic value of vestibular evoked myogenic potentials in cerebellar and lower-brainstem strokes. Neurophysiol Clin. 2006;36(4):227-33. DOI: http://dx.doi.org/10.1016/j.neucli.2006.08.014
http://dx.doi.org/10.1016/j.neucli.2006....

3. Rauch SD. Vestibular evoked myogenic potentials. Curr Opin Otolaryngol Head Neck Surg. 2006;14(5):299-304. DOI: http://dx.doi.org/10.1097/01.moo.0000244185.65022.01
http://dx.doi.org/10.1097/01.moo.0000244...

4. Sazgar AA, Dortaj V, Akrami K, Akrami S, Karimi Yazdi AR. Saccular damage in patients with high-frequency sensorineural hearing loss. Eur Arch Otorhinolaryngol. 2006;263(7):608-13. PMID: 16625399 DOI: http://dx.doi.org/10.1007/s00405-006-0038-6
http://dx.doi.org/10.1007/s00405-006-003...

5. Lütkenhöner B, Stoll W, Basel T Modeling the vestibular evoked myogenic potential. J Theor Biol. 2010;263(1):70-8. PMID: 19896953 DOI: http://dx.doi.org/10.1016/j.jtbi.2009.10.036
http://dx.doi.org/10.1016/j.jtbi.2009.10...
- 66. Akin FW, Murnane OD, Panus PC, Caruthers SK, Wilkinson AE, Proffitt TM. The influence of voluntary tonic EMG level on the vestibular-evoked myogenic potential. J Rehabil Res Dev. 2004;41(3B):473-80. PMID: 15543465.

Responses are captured from neck muscles through surface electrodes. The tracings derived from acoustic stimulation are made up of two complexes of two-phase waves: p13 and n2311. Damen MMJ. Vestibular evoked myogenic potential (VEMP). Clinical application of the threshold. Medical Engineering. Eindhoven: Technische Universiteit Eindhoven; 2007. , 77. Halmagyi GM, Colebatch JG, Curthoys IS. New tests of vestibular function. Baillieres Clin Neurol. 1994;3(3):485-500.

8. 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):184-7. DOI: http://dx.doi.org/10.1016/j.amjoto.2007.07.004
http://dx.doi.org/10.1016/j.amjoto.2007....

9. Pérez Guillén V, González García E, García Piñero A, Piqueras Del Rey A, Morera Pérez C, Pérez Garrigues H. Vestibular evoked myogenic potential: a contribution to the vestibular physiology and pathology knowledge. Quantitative patterns in healthy subjects. Acta Otorrinolaringol Esp. 2005;56(8):349-53. PMID: 16285433

10. Shimizu K, Murofushi T, Sakurai M, Halmagyi M. Vestibular evoked myogenic potentials in multiple sclerosis. J Neurol Neurosurg Psychiatry. 2000;69(2):276-7. PMID: 10960289 DOI: http://dx.doi.org/10.1136/ jnnp.69.2.276
http://dx.doi.org/10.1136/jnnp.69.2.276...
- 1111. Colebatch JG, Halmagyi GM. Vestibular evoked potentials in human neck muscles before and after unilateral vestibular deafferentation. Neurology. 1992;42(8):1635-6. DOI: http://dx.doi.org/10.1212/WNL.42.8.1635
http://dx.doi.org/10.1212/WNL.42.8.1635...
. VEMPs can be obtained from air, bone, and galvanic acoustic stimulation44. Sazgar AA, Dortaj V, Akrami K, Akrami S, Karimi Yazdi AR. Saccular damage in patients with high-frequency sensorineural hearing loss. Eur Arch Otorhinolaryngol. 2006;263(7):608-13. PMID: 16625399 DOI: http://dx.doi.org/10.1007/s00405-006-0038-6
http://dx.doi.org/10.1007/s00405-006-003...
.

Response characteristics are correlated to the type of stimulation and frequencies used. Tone bursts1111. Colebatch JG, Halmagyi GM. Vestibular evoked potentials in human neck muscles before and after unilateral vestibular deafferentation. Neurology. 1992;42(8):1635-6. DOI: http://dx.doi.org/10.1212/WNL.42.8.1635
http://dx.doi.org/10.1212/WNL.42.8.1635...

12. Burkard RF, Eggermont JJ, Don M, eds. Auditory evoked potentials: Basic principles and Clinical Application. Philadelphia: Lippincott Williams & Wilkins; 2007.

13. Timmer FC, Zhou G, Guinan JJ, Kujawa SG, Herrmann BS, Rauch SD. Vestibular evoked myogenic potential (VEMP) in patients with Ménière's disease with drop attacks. Laryngoscope. 2006;116(5):776-9. PMID: 16652086 DOI: http://dx.doi.org/10.1097/01.mlg.0000205129.78600.27
http://dx.doi.org/10.1097/01.mlg.0000205...

14. 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):2216-9. PMID: 16043396 DOI: http://dx.doi.org/10.1016/j.clinph.2005.06.010
http://dx.doi.org/10.1016/j.clinph.2005....
- 1515. Sheykholeslami K, Habiby Kermany M, Kaga K. Frequency sensitivity range of the saccule to bone-conducted stimuli measured by vestibular evoked myogenic potentials. Hear Res. 2001;160(1-2):58-62. PMID: 11591491 or clicks1616. Kelsch TA, Schaefer LA, Esquivel CR. Vestibular evoked myogenic potentials in young children: test parameters and normative data. Laryngoscope. 2006;116(6):895-900. PMID: 16735887 DOI: http://dx.doi.org/10.1097/01.mlg.0000214664.97049.3e
http://dx.doi.org/10.1097/01.mlg.0000214...
, 1717. Huang TW, Su HC, Cheng PW. Effect of click duration on vestibular-evoked myogenic potentials. Acta Otolaryngol. 2005;125(2):141-4. PMID: 15880943 DOI: http://dx.doi.org/10.1080/00016480410016900
http://dx.doi.org/10.1080/00016480410016...
can be used in acoustic stimulation. Lower frequencies produce more homogeneous responses, with 500 Hz66. Akin FW, Murnane OD, Panus PC, Caruthers SK, Wilkinson AE, Proffitt TM. The influence of voluntary tonic EMG level on the vestibular-evoked myogenic potential. J Rehabil Res Dev. 2004;41(3B):473-80. PMID: 15543465 , 1212. Burkard RF, Eggermont JJ, Don M, eds. Auditory evoked potentials: Basic principles and Clinical Application. Philadelphia: Lippincott Williams & Wilkins; 2007. , 1818. Cheng PW, Murofushi T. The effects of plateau time on vestibular-evoked myogenic potentials triggered by tone bursts. Acta Otolaryngol. 2001;121(8):935-8. PMID: 11813898 DOI: http://dx.doi.org/10.1080/00016480127377
http://dx.doi.org/10.1080/00016480127377...

19. Cheng PW, Murofushi T. The effect of rise/fall time on vestibular-evoked myogenic potential triggered by short tone bursts. Acta Otolaryngol. 2001;121(6):696-9. PMID: 11678168 DOI: http://dx.doi.org/10.1080/00016480152583638
http://dx.doi.org/10.1080/00016480152583...
- 2020. Murofushi T, Matsuzaki M, Wu CH. Short tone burst-evoked myogenic potentials on the sternocleidomastoid muscle: are these potentials also of vestibular origin? Arch Otolaryngol Head Neck Surg. 1999;125(6):660-4. PMID: 10367923 DOI: http://dx.doi.org/10.1001/archotol.125.6.660
http://dx.doi.org/10.1001/archotol.125.6...
as the most effective frequency. Response is analyzed by the selection of peaks and assessment of amplitudes and latencies2121. Stapells DR. Current status of the auditory steady-state responser for estimating an infant's audiogram. In: Seewald RC, Bamford J. A sound foundation through early amplification. Chicago: Ponak; 2005. p.43-59. , 2222. Picton TW, John MS, Dimitrijevic A, Purcell D. Human auditory steady-state responses. Int J Audiol. 2003;42(4):177-219. PMID: 12790346 DOI: http://dx.doi.org/10.3109/14992020309101316
http://dx.doi.org/10.3109/14992020309101...
.

In the clinical setting, VEMP testing presents a series of favorable traits, as it is an objective, non-invasive, easy-to-perform test that does not bring discomfort to patients33. Rauch SD. Vestibular evoked myogenic potentials. Curr Opin Otolaryngol Head Neck Surg. 2006;14(5):299-304. DOI: http://dx.doi.org/10.1097/01.moo.0000244185.65022.01
http://dx.doi.org/10.1097/01.moo.0000244...
, 1414. 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):2216-9. PMID: 16043396 DOI: http://dx.doi.org/10.1016/j.clinph.2005.06.010
http://dx.doi.org/10.1016/j.clinph.2005....
. However, there is no agreed standard to obtain VEMPs, and a wide array of methods and protocols have been used2323. Felipe L, Kigman H, Gonçalves DH. Potencial evocado miogênico vestibular. Arq Int Otorrinolaringol. 2012;16(1):103-7. DOI: http://dx.doi.org/10.7162/S1809-48722012000100015
http://dx.doi.org/10.7162/S1809-48722012...
. The most frequently described stimulation rate is 5 Hz. Nonetheless, higher rates, if reliable, would expedite the testing protocol.

This study aims to find the highest reliable stimulation rate to obtain VEMPs.

METHOD

This study was approved by the institution's Research Ethics Committee and given permit 990/09. All participants signed informed consent terms before joining the study.

Eighteen individuals (36 ears) were enrolled in the study as per the following criteria: ages between 18 and 35 years and auditory thresholds equal to or lower than 20 dBNA with differences between ears per frequency of 10 dB or under. The number of participants was calculated based on the sample size for an infinite population with an alpha of 0.05, a standard deviation of 9 µV and tolerable error of 3 µV.

Individuals exposed to occupational or leisure noise, previously submitted to middle or inner ear surgery, with more than three cases of outer or middle ear infection in the current year, prior use of ototoxic medication, presence of systemic alterations conducive to vestibulocochlear involvement such as diabetes, high blood pressure, hormonal disorders, and presence of tinnitus, vertigo, dizziness or other vestibulocochlear alterations were excluded.

Participants were asked to answer a questionnaire for screening purposes. The following procedures were then carried out: otoscopic examination, pure-tone audiometry, and VEMP testing.

Surface electrodes positioned on the subjects' skin were used to record VEMPs. The positive electrode was placed on the middle third of the sternocleidomastoid (SCM) muscle on the side where stimulation was applied; the negative electrode was positioned at the level of the tendon of the SCM, just above the clavicle; and the ground electrode was placed on the frontal middle line. Patients were seated during the acquisition of SCM records, with their heads in maximum lateral rotation turned to the opposite side of stimuli application.

In VEMP examination, the mean value for 200 tone burst stimuli at 500 Hz was calculated, with stimulation rates set at 5.1, 10.2, 20.4, and 40.8 stimuli per second at an intensity of 95 dBNAn with subjects wearing ER-A3 ear buds. A pass-band filter (5-1000 Hz) with exhibition of 10 to 25 µV per division was used. Stimulation rates were not set as integer numbers in order to prevent potentials from being acquired in phase with the frequency of the Brazilian grid, set at 60 Hz2424. Lins OG. Audiometria fisiológica tonal utilizando respostas de estado estável auditivas do tronco cerebral [Tese de Doutorado]. São Paulo: Universidade Federal de São Paulo, Escola Paulista de Medicina; 2002. , 2525. Pauli-Magnus D, Hoch G, Strenzke N, Anderson S, Jentsch TJ, Moser T. Detection and differentiation of sensorineural hearing loss in mice using auditory steady-state responses and transient auditory brainstem responses. Neuroscience. 2007;149(3):673-84. PMID: 17869440 DOI: http://dx.doi.org/10.1016/j.neuroscience.2007.08.010
http://dx.doi.org/10.1016/j.neuroscience...
. Records were captured in 40 ms windows to encompass all responses1414. 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):2216-9. PMID: 16043396 DOI: http://dx.doi.org/10.1016/j.clinph.2005.06.010
http://dx.doi.org/10.1016/j.clinph.2005....
, 1515. Sheykholeslami K, Habiby Kermany M, Kaga K. Frequency sensitivity range of the saccule to bone-conducted stimuli measured by vestibular evoked myogenic potentials. Hear Res. 2001;160(1-2):58-62. PMID: 11591491.

Wave morphology was used in the interpretation of test findings. Waves p13 and n23 were delimited by the latencies of the first positive and negative peaks by two authors/examiners. Discrepancies between authors/examiners were resolved by a third author/ examiner.

Statistical method

The data sets were treated and processed using application Predictive Analytics SoftWare (PASW® Statistic) release 17.0. Mean values were presented in tables and graphs, along with standard deviations and percentile distributions.

Latency and amplitude normality for waves p13 and n23 was analyzed through the Kolmogorov-Smirnov test. ANOVA was used to compare latencies and amplitudes at different stimulation rates (5.1, 10.2, 20.4, and 40.8 stimuli per second) obtained in VEMP testing, and pairs were compared using the Tukey or the Kruskal-Wallis test depending on whether the samples followed a normal distribution or not, respectively. The Mann-Whitney test was used to further analyze amplitudes, with the purpose of comparing stimulation rates and check for statistically significant differences. Statistical significance was attributed to events with p ≤ 0.05; a beta error of 0.1 was admitted.

RESULTS

The sample included 18 subjects (36 ears), 12 females (24 ears) and six males (12 ears). The individuals were aged between 21 and 27 years, and had a mean age of 23.03 ± 1.33 years.

VEMPs were recorded through stimulation and unilateral data acquisition. Proper morphology was attained in 100% of the ears using a stimulation rate of 5.1 stimuli per second; in 96.87% at 10.2 stimuli per second; in 86.11% at 20.4 stimuli per second; and in 72.22% at 40.8 stimuli per second. Tone bursts at 500 Hz were used in acoustic stimulation.

The Kolmogorov-Smirnov revealed latencies and amplitudes followed a normal distribution pattern, except for the latencies seen in wave p13 for stimulation rates of 10.2 and 40.8 stimuli per second. Non-parametric tests were thus used.

The waves were delimited in the test tracings and absolute latencies and amplitudes were determined for waves p13 and n23. Table 1 shows the data related to these parameters for each stimulation rate irrespective of ear.

Table 1
VEMP latencies and amplitudes for each stimulation rate.

Table 1 shows that the p13 and n23 wave latencies were kept constant and amplitudes decreased gradually as stimulation rates were increased. However, ANOVA and the Kruskal-Wallis test failed to reveal statistically significant differences between parameters.

Amplitudes were further analyzed by comparing stimulation rates. The Mann-Whitney test revealed statistically significant differences for wave p13 between stimulation rates of 5.1 and 20.4 stimuli per second (p = 0.03), and 5.1 and 40.8 stimuli per second (p = 0.01). For wave n23, amplitudes were statistically different only when stimulation rates of 5.1 and 40.8 stimuli per second were compared (p = 0.02), with no significant differences seen between stimulation rates of 5.1 and 20.4 stimuli per second (p = 0.06).

Graph 1 shows a comparison between amplitudes at different stimulation rates.

Graph 1
Comparison between amplitudes according to stimulation rate.

DISCUSSION

The results seen in the studied population showed that it is possible to consistently acquire records for waves p13 and n23 in the time domain on all analyzed stimulation rates, as similarly reported by other authors1515. Sheykholeslami K, Habiby Kermany M, Kaga K. Frequency sensitivity range of the saccule to bone-conducted stimuli measured by vestibular evoked myogenic potentials. Hear Res. 2001;160(1-2):58-62. PMID: 11591491 , 2626. Wu CH, Murofushi T. The effect of click repetition rate on vestibular evoked myogenic potential. Acta Otolaryngol. 1999;119(1):29-32. DOI: http://dx.doi.org/10.1080/00016489950181891
http://dx.doi.org/10.1080/00016489950181...
.

The VEMP latency and amplitude results at a stimulation rate of 5.1 stimuli per second seen in this study were similar to the values reported in the literature66. Akin FW, Murnane OD, Panus PC, Caruthers SK, Wilkinson AE, Proffitt TM. The influence of voluntary tonic EMG level on the vestibular-evoked myogenic potential. J Rehabil Res Dev. 2004;41(3B):473-80. PMID: 15543465 , 2727. Oliveira AC. Estudo dos potenciais evocados miogênicos vestibulares de estado estável [Tese de doutorado]. Ribeirão Preto: Universidade de São Paulo: Faculdade de Medicina de Ribeirão Preto; 2010.. As for other stimulation rates, reports in the literature indicate that latency and amplitude tend to decrease as the stimulation rate is increased - a finding in disagreement with this study when latency is considered1515. Sheykholeslami K, Habiby Kermany M, Kaga K. Frequency sensitivity range of the saccule to bone-conducted stimuli measured by vestibular evoked myogenic potentials. Hear Res. 2001;160(1-2):58-62. PMID: 11591491 , 2626. Wu CH, Murofushi T. The effect of click repetition rate on vestibular evoked myogenic potential. Acta Otolaryngol. 1999;119(1):29-32. DOI: http://dx.doi.org/10.1080/00016489950181891
http://dx.doi.org/10.1080/00016489950181...
.

Some authors have related the decrease in amplitude consequent to stimulation rate increases to possible SCM muscle fatigue during testing, as subjects are required to produce effective muscle contraction in order to allow for proper recording of potentials. Thus, the longer the tests, the lower the amplitude2727. Oliveira AC. Estudo dos potenciais evocados miogênicos vestibulares de estado estável [Tese de doutorado]. Ribeirão Preto: Universidade de São Paulo: Faculdade de Medicina de Ribeirão Preto; 2010.. Others have described the reduction in amplitude as a consequence of reflex habituation, as the high rate of stimulation exhausts sensory cells and delays the activation of the first neuron2828. Murofushi T, Curthoys IS. Physiological and anatomical study of click-sensitive primary vestibular afferents in the guinea pig. Acta Otolaryngol. 1997;117(1):66-72. PMID: 9039484 DOI: http://dx.doi.org/10.3109/00016489709117994
http://dx.doi.org/10.3109/00016489709117...

29. Murofushi T, Curthoys IS, Topple AN, Colebatch JG, Halmagyi GM. Responses of guinea pig primary vestibular neurons to clicks. Exp Brain Res. 1995;103(1):174-8. PMID: 7615033 DOI: http://dx.doi. org/10.1007/BF00241975
http://dx.doi.org/10.1007/BF00241975...
- 3030. Murofushi T, Curthoys IS, Gilchrist DP. Response of guinea pig vestibular nucleus neurons to clicks. Exp Brain Res. 1996;111(1):149-52. PMID: 8891646 DOI: http://dx.doi.org/10.1007/BF00229565
http://dx.doi.org/10.1007/BF00229565...
. However, in order to prevent tested individuals from getting tired and to avoid SCM muscle fatigue, the subjects included in this study were asked to rest for one minute between each data acquisition cycle, i.e., when stimulation rates were changed, to prevent muscle fatigue and habituation from occurring.

No statistically significant differences were seen in latency when stimulation rates of 5.1 and 10.2 stimuli per second were compared, as also reported by other authors1515. Sheykholeslami K, Habiby Kermany M, Kaga K. Frequency sensitivity range of the saccule to bone-conducted stimuli measured by vestibular evoked myogenic potentials. Hear Res. 2001;160(1-2):58-62. PMID: 11591491 , 2626. Wu CH, Murofushi T. The effect of click repetition rate on vestibular evoked myogenic potential. Acta Otolaryngol. 1999;119(1):29-32. DOI: http://dx.doi.org/10.1080/00016489950181891
http://dx.doi.org/10.1080/00016489950181...
. However, most choose a rate of five stimuli per second, as it allows for more consistent data acquisition and easier identification of tracings2626. Wu CH, Murofushi T. The effect of click repetition rate on vestibular evoked myogenic potential. Acta Otolaryngol. 1999;119(1):29-32. DOI: http://dx.doi.org/10.1080/00016489950181891
http://dx.doi.org/10.1080/00016489950181...
.

Lastly, the rate of 10.2 stimuli per second appears to be more adequate in clinical applications as it produces waves with more adequate morphology, with equal tracing identification and amplitudes which are not statistically different when compared to the rate of five stimuli per second, in addition to being visible to the naked eye. Additionally, tests performed at a rate of 10.2 stimuli per second reduce patient discomfort and data acquisition times1515. Sheykholeslami K, Habiby Kermany M, Kaga K. Frequency sensitivity range of the saccule to bone-conducted stimuli measured by vestibular evoked myogenic potentials. Hear Res. 2001;160(1-2):58-62. PMID: 11591491. Further studies with larger populations are yet required to confirm the adjustments recommended for the testing protocol.

CONCLUSION

The highest reliable stimulation rate observed for the population included in this study was 10.2 stimuli per second.

REFERÊNCIAS

  • 1
    Damen MMJ. Vestibular evoked myogenic potential (VEMP). Clinical application of the threshold. Medical Engineering. Eindhoven: Technische Universiteit Eindhoven; 2007.
  • 2
    Pollak L, Kushnir M, Stryjer R. Diagnostic value of vestibular evoked myogenic potentials in cerebellar and lower-brainstem strokes. Neurophysiol Clin. 2006;36(4):227-33. DOI: http://dx.doi.org/10.1016/j.neucli.2006.08.014
    » http://dx.doi.org/10.1016/j.neucli.2006.08.014
  • 3
    Rauch SD. Vestibular evoked myogenic potentials. Curr Opin Otolaryngol Head Neck Surg. 2006;14(5):299-304. DOI: http://dx.doi.org/10.1097/01.moo.0000244185.65022.01
    » http://dx.doi.org/10.1097/01.moo.0000244185.65022.01
  • 4
    Sazgar AA, Dortaj V, Akrami K, Akrami S, Karimi Yazdi AR. Saccular damage in patients with high-frequency sensorineural hearing loss. Eur Arch Otorhinolaryngol. 2006;263(7):608-13. PMID: 16625399 DOI: http://dx.doi.org/10.1007/s00405-006-0038-6
    » http://dx.doi.org/10.1007/s00405-006-0038-6
  • 5
    Lütkenhöner B, Stoll W, Basel T Modeling the vestibular evoked myogenic potential. J Theor Biol. 2010;263(1):70-8. PMID: 19896953 DOI: http://dx.doi.org/10.1016/j.jtbi.2009.10.036
    » http://dx.doi.org/10.1016/j.jtbi.2009.10.036
  • 6
    Akin FW, Murnane OD, Panus PC, Caruthers SK, Wilkinson AE, Proffitt TM. The influence of voluntary tonic EMG level on the vestibular-evoked myogenic potential. J Rehabil Res Dev. 2004;41(3B):473-80. PMID: 15543465
  • 7
    Halmagyi GM, Colebatch JG, Curthoys IS. New tests of vestibular function. Baillieres Clin Neurol. 1994;3(3):485-500.
  • 8
    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):184-7. DOI: http://dx.doi.org/10.1016/j.amjoto.2007.07.004
    » http://dx.doi.org/10.1016/j.amjoto.2007.07.004
  • 9
    Pérez Guillén V, González García E, García Piñero A, Piqueras Del Rey A, Morera Pérez C, Pérez Garrigues H. Vestibular evoked myogenic potential: a contribution to the vestibular physiology and pathology knowledge. Quantitative patterns in healthy subjects. Acta Otorrinolaringol Esp. 2005;56(8):349-53. PMID: 16285433
  • 10
    Shimizu K, Murofushi T, Sakurai M, Halmagyi M. Vestibular evoked myogenic potentials in multiple sclerosis. J Neurol Neurosurg Psychiatry. 2000;69(2):276-7. PMID: 10960289 DOI: http://dx.doi.org/10.1136/ jnnp.69.2.276
    » http://dx.doi.org/10.1136/jnnp.69.2.276
  • 11
    Colebatch JG, Halmagyi GM. Vestibular evoked potentials in human neck muscles before and after unilateral vestibular deafferentation. Neurology. 1992;42(8):1635-6. DOI: http://dx.doi.org/10.1212/WNL.42.8.1635
    » http://dx.doi.org/10.1212/WNL.42.8.1635
  • 12
    Burkard RF, Eggermont JJ, Don M, eds. Auditory evoked potentials: Basic principles and Clinical Application. Philadelphia: Lippincott Williams & Wilkins; 2007.
  • 13
    Timmer FC, Zhou G, Guinan JJ, Kujawa SG, Herrmann BS, Rauch SD. Vestibular evoked myogenic potential (VEMP) in patients with Ménière's disease with drop attacks. Laryngoscope. 2006;116(5):776-9. PMID: 16652086 DOI: http://dx.doi.org/10.1097/01.mlg.0000205129.78600.27
    » http://dx.doi.org/10.1097/01.mlg.0000205129.78600.27
  • 14
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    » http://dx.doi.org/10.1016/j.clinph.2005.06.010
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  • Federal University of Pernambuco.

Publication Dates

  • Publication in this collection
    Sep-Oct 2013

History

  • Received
    31 Aug 2012
  • Accepted
    29 May 2013
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