Laryngeal Electromyography: Are the Results Reproducible? Machado Ju nior, and Aline E. Wolf, Campinas, S~ao Paulo, Brazil Agrı´cio N. Crespo, Paulo A. T. Kimaid, Almiro Jose Summary: Laryngeal electromyography (LEMG) is an auxiliary diagnostic technique that is used to study neurologic diseases that affect the larynx. This study aimed to verify the reproducibility and accordance of LEMG findings obtained by different approaches applied to the same intrinsic laryngeal muscle in patients with neurologic disorders of the larynx. Study Design. This study is prospective, blind, randomized, and controlled. Methods. Forty subjects (20 males and 20 females) aged between 21 and 78 years underwent LEMG of the thyroarytenoid muscles by different techniques, with a total of 120 insertion sites for analysis. The electrophysiological findings were grouped as follows: (1) equal LEMG findings; (2) different LEMG findings but in agreement on the same electromyographic pattern; and (3) different LEMG findings and in discord on the same electromyographic pattern. Results. We found 5% discordance in the LEMG findings between the sites analyzed. Conclusions. LEMG is an important and useful technique, but caution must be taken to avoid misinterpretation and the wrong muscle approach. Key Words: Laryngeal–Electromyography–Neurological diseases. INTRODUCTION Laryngeal electromyography (LEMG) is an auxiliary technique that is used to study neurologic diseases that affect the function of the larynx. LEMG is performed by inserting needle electrodes into the intrinsic laryngeal muscles. The clinical utility of LEMG has expanded greatly in the last three decades, but no clear consensus exists on its role in diagnosis and prognosis.1,2 The different techniques developed, the types of electrodes used, the variability of study designs, and the different ways of analyzing the results make it difficult to compare results among authors. In 2012, it was published the first metaanalysis showing that LEMG is a good predictor of poor recovery in patients with vocal fold paralysis and is clinically useful in identifying candidates for early definitive intervention.3 In addition, anecdotal remarks indicate that obtaining reproducible results is difficult even when LEMG is performed repeatedly in the same patient. Are the results reproducible? Do examiners subjectively misinterpret the results? Are the muscles correctly approached? Recently, an American Association of Electrodiagnostic Medicine (AAEM) Task Force identified the absence of prospective blinded LEMG studies.4 The aims of this study were to evaluate the reproducibility and accordance of the LEMG findings obtained with different randomized and controlled approach techniques5 of the same laryngeal muscles in patients with neurologic diseases that affect the larynx. This prospective blind study uses controlled techniques. SUBJECTS AND METHODS Subjects This study prospectively examined 40 patients who complained of dysphonia and were referred by the neurolaryngology ambuAccepted for publication September 8, 2014. From the Department of Othorynolaryngology, Medicine School, UNICAMP, Campinas, S~ao Paulo, Brazil. Address correspondence and reprint requests to Almiro Jose Machado Junior, Department of Othorynolaryngology, Medicine School, UNICAMP, Rua Maria Monteiro, 841 ap 11 Cambuı´, Campinas, SP 13025-151, Brazil. E-mail: [email protected] Journal of Voice, Vol. 29, No. 4, pp. 498-500 0892-1997/$36.00 Ó 2015 The Voice Foundation http://dx.doi.org/10.1016/j.jvoice.2014.09.009
latory clinic of the UNICAMP School of Medicine after undergoing laryngological, phoniatric, and laryngeal endoscopic evaluation. With consent from the ethical committee for human research, all patients underwent LEMG. Technique All patients were examined in the dorsal decubitus, after skin asepsis with alcohol and insertion of electrodes guided by surface laryngeal references. Anesthesia was not necessary. The same experienced and board-certified laryngologist performed all approaches of the intrinsic laryngeal muscles. We used two approach techniques to the thyroarytenoid (TA), as described previously5: (1) across the cricothyroid (CT) membrane in the midline or 0.5 cm from the midline and (2) across the thyroid cartilage. These two approach techniques gave us two different sites for analysis. The clinical diagnostic evaluation, side affected, and approach technique to the muscles were known by the laryngologist but not by the neurophysiologist. Every patient was intended to be evaluated bilaterally to make a final LEMG report. This decision changes in half of the cases when there was no advantage to the diagnostic to lessen discomfort to the patient during the examination. We considered for the research only the cases where there were two electrodes insertions in the same muscle to compare: if only one side was evaluated with two punctures, it was considered unilateral evaluation, and if both sides were evaluated with two punctures, it was considered bilateral. The LEMG results were interpreted by the same neurophysiologist, who was an experienced neurologist and board certified in electromyography. The examination was performed with a bipolar concentric needle electrode inserted percutaneously by the laryngologist, guided by surface references until the sound of muscle activity, and the sharp motor unit potential (MUP) were achieved and considered by the neurophysiologist for analysis. Owing to the differences in the amplitudes and durations of the motor unit action potentials (MUAPs) between the laryngeal muscles (including the TA, CT, posterior cricoarytenoid [CAP], and lateral cricoarytenoid [CAL]), only the TA muscle findings were included in the study analysis. Only the
Agrı´cio N. Crespo, et al
Laryngeal Electromyography
registers that the neurophysiologist approved as optimal were included in the study.6 The LEMG findings were known by the neurophysiologist but not by the laryngologist. The LEMG findings adopted in this study were the same as for any other electromyography analysis1: (1) at rest: electric silence, positive sharp waves, fibrillation potentials, fasciculation potentials, and repetitive discharges; (2) MUAP analysis: the patients were asked to phonate /e/, /i/, or deep inspiration to activate the muscles. Amplitude, duration, phase numbers, and frequency of recruitment were analyzed according to author’s previously published data6; and (3) increased effort: interferential, reduced, 2–3 MUAP only, or no action. A third researcher (a speech pathologist) took note of the difficulties reported by the laryngologist in identifying the laryngeal surface anatomic references, the order of the punctures, the side, and the approach used. The LEMG findings were numbered in the same order as the techniques were numbered the speech pathologist at the end of the study. The CT, CAP, and CAL findings were not included in the study analysis but were used for writing the LEMG reports. The electrophysiological findings can define three patterns, normal, neurogenic, or myogenic reported previously.1,6,7 The LEMG findings at each point of analysis were grouped as (1) equal when the same LEMG findings were encountered in the two different sites approached (eg, normal at one point and the other; fibrillation at one point and the other); (2) different LEMG findings but in accordance with the same electromyographic pattern (eg, neurogenic with repetitive discharge at one point and neurogenic with only fibrillation at the other point); and (3) different LEMG findings and discordant when they could not be correlated with the same electromyographic pattern (eg, normal at one point and neurogenic in the other). Equipment The readings were obtained using a four-channel Nihon Kohden Neuropack M1 (MEB9200) apparatus (Nihon Kohden, Tokyo, Japan), with a common mode rejection ratio of less than 112 dB and 0.6 mVrms noise level. The amplifiers input impedance was 1000 MU. The band-pass filter was set to 10– 10 000 Hz, the sensitivity was 20–50 mV/cm for rest analysis, 100–200 mV/cm for MUP analysis, and 500–1000 mV/cm for interference pattern analysis. The sweep speed was 5–10 ms/ cm for rest and MUP analysis and 30–50 ms/cm for interference pattern analysis. A concentric needle electrode of 37 mm length and 0.07 mm2 contact area was used. RESULTS We studied 40 patients (20 males and 20 females) aged 21– 78 years (mean 48.2 years). Twenty patients were examined bilaterally (40 TA), and 20 patients were examined unilaterally (20 TA). Each TA muscle was examined twice with different approaches at the 60 pairs of sites of insertions (30 on the left). Ninety-five percent of the LEMG findings were equal or in accordance when comparing the analyzed sites, and 5% were discordant. The frequency of equal LEMG findings obtained
499 at different electrode placement sites in the same TA muscle was 76.7% (group 1). There was no predominance for sex, difficulty in recognizing the surface anatomic references, or the pathologies. A total of 11 analyzed pairs of LEMG findings were in group 2. These pairs were obtained in patients with vocal fold immobility who showed characteristics of peripheral nerve compromise, but the patients had a variety of neurogenic findings. Two cases of group 3 LEMG findings were obtained with right-hand side approaches in patients with easily recognizable laryngeal surface references. One group 3 pair was obtained from a patient with right vocal fold immobility, another was obtained from a patient with right vocal fold paresis, and the last was obtained from a patient with left vocal fold hypomobility. The analysis of these three pairs showed the same pattern of discordance, which was normal morphology at one site and discretely longer than normal MUAP durations at the other time.
DISCUSSION Many reports describe the importance of LEMG in neurologic and laryngological diagnosis and prognosis for vocal fold immobility,1,2,7–10 but there is no clear consensus among them.4 There are anecdotal descriptions of difficulty in obtaining reproducible results when LEMG is performed repeatedly in the same patient. We found a high frequency (95%) of equal or concordant LEMG findings between the sites analyzed. We thought that LEMG analysis was dynamic and would need to be performed at the moment of the examination (in real time) by an experienced neurophysiologist. A total of 76.7% of the analyzed site pair LEMG findings were exactly the same, showing that the variability of the LEMG findings was less common than expected. All 11 pairs of LEMG findings from group 2 were obtained in patients with vocal fold immobility and characteristics of peripheral nerve compromise. The pairs of LEMG findings were different for the group 2 patients but were not discordant for the underlying neurologic process. These findings could be explained by fascicular compromise or the evolution of nerve compromise or regeneration. Both hypotheses could explain different time-related LEMG findings in the same muscle. Two pairs of group 3 findings were obtained with a right-hand side approach in patients with easily recognizable laryngeal surface references. Thus, difficulty in recognizing surface references in the muscle approach was not correlated with discordance. In fact, there is no difficulty in inserting the needle electrodes in the TA muscle if the techniques are correctly used.5 One group 3 pair was obtained from a patient with right vocal fold immobility, one from a patient with right vocal fold hypomobility, and the other pair was obtained from a patient with left vocal fold hypomobility. The analysis of these three pairs showed the same pattern of discordance, which was normal MUAP morphology at one time and discretely longer than normal MUAP durations at the other time. In our opinion, two possibilities must be considered: neurophysiologist misinterpretation because the neurogenic findings were close to limits between the normal and discretely increased MUAP duration. In these cases, it would be necessary to quantitatively analyze the MUAP duration or to use information obtained from other
500 muscles related to the same nerve (eg, CAP or CAL). One report showed age-induced remodeling of MUAP, with increasing duration, especially in the left-hand side11; however, in two of our patients, the findings were obtained from the right-hand side, and only one patient was older than 60 years of age. The crosstalking phenomenon was avoided with the use of concentric needle electrodes, which explore a more restricted area and show stable baselines compared with other electrodes.11 We also must consider the possibility of electrode misplacement by the laryngologist. To avoid it, the laryngologist should be trained to approach laryngeal muscles on both sides precisely. The small dimension of the intrinsic laryngeal muscles and their anatomic location behind the thyroid cartilage obviously increase the possibility of electrode misplacement. The accuracy of needle placement in muscles of lower limbs guided only by anatomic landmarks or by ultrasound showed a high rate of misplacement, especially in deep muscles.12,13 Currently, LEMG is being widely used to identify presbylarynx of paresis14 and to study the severity of dysphagia,15 but it needs to be compared across studies before being incorporated into standard procedures as proposed by the Working Group on Neurolaryngology of the European Laryngological Society.16,17 CONCLUSIONS In our opinion, LEMG is an important and useful technique, but caution should be taken to avoid misinterpretation and incorrect muscle approaches. REFERENCES 1. Dumitru D. Electrodiagnostic Medicine. Philadelphia, PA: Hanley-Belfus Mosby; 2012. 2. Hydman J, Gunnar B, Person JKE, Zedenius J, Mattsson P. Diagnosis and prognosis of iatrogenic injury of the recurrent laryngeal nerve. Ann Otol Rhinol Laryngol. 2009;118:506–511. 3. Rickert SM, Childs LF, Carey BT, Murry T, Sulica L. Laryngeal electromyography for prognosis of vocal fold palsy: a meta-analysis. Laryngoscope. 2012;122:158–161.
Journal of Voice, Vol. 29, No. 4, 2015 4. Sataloff RT, Praneetvatakul P, Heuer RJ, Hawkshaw MJ, HemanAckah YD, Schneider SM, Mandel S. Laryngeal electromyography: clinical application. J Voice. 2010;24:228–234. 5. Crespo AN, Kimaid PAT, Quagliato EMAB, Vianna MA, Resende LAL, Wolf AE. Laryngeal electromyography: technical features. Electromyogr Clin Neurophysiol. 2004;44:237–241. 6. Kimaid PAT, Crespo AN, Quagliato EMAB, Vianna MA, Resende LAL, Wolf AE. Laryngeal electromyography in normal Brazilian population. Electromyogr Clin Neurophysiol. 2004;44:243–245. 7. Kimaid PAT, Crespo AN, Quagliato EMAB, Vianna MA, Resende LAL, Wolf AE. Laryngeal electromyography: contribution to vocal fold immobility diagnosis. Electromyogr Clin Neurophysiol. 2004;44:371–374. 8. Munin MC, Murry T, Rosen CA. Laryngeal electromyography. Diagnosis and prognostic applications. Otolaryngol Clin North Am. 2000;33: 759–770. 9. Parnes SM, Satya-Murti S. Predictive value of laryngeal electromyography in patients with vocal cord paralysis of neurogenic origin. Laryngoscope. 1985;95:1323–1326. 10. Sittel C, Stennert E, Thumfart WT, Dapunt U, Ecke HE. Prognostic value of laryngeal electromyography in vocal fold paralysis. Arch Otolaryngol Head Neck Surg. 2001;127:155–160. 11. Takeda N, Thomas GR, Ludlow CL. Aging effects on motor units in the human thyroarytenoid muscle. Laryngoscope. 2000;110:1018–1025. 12. Haig AJ, Goodmurphy CW, Harris BS, Ruiz AP, Etemad J. The accuracy of needle placement in lower-limb muscles: a blinded study. Arch Phys Med Rehabil. 2003;84:877–882. 13. Boon AJ, Oney-Marlow TM, Murthy NS, Harper CM, McNamara TR, Smith J. Accuracy or electromyography needle placement in cadavers: non-guided vs. ultrasound guided. Muscle Nerve. 2011;44:45–49. 14. Stager SV, Bielamowicz SA. Using laryngeal electromyography to differentiate presbylarynges from paresis. J Speech Lang Hear Res. 2010;53: 100–113. 15. Ryu JS, Lee JH, Kang JY, Kim MY, Shin DE, Shin AS. Evaluation of dysphagia after cervical surgery using laryngeal EMG. Dysphagia. 2012; 27:318–324. 16. Volk GF, Hagen R, Pototschnig C, et al. Laryngeal electromyography: a proposal for guidelines of the European Laryngological Society. Eur Arch Otorhinolaryngol. 2012;269:2227–2245. 17. Wang C, Chang M. A proposal to extend application of laryngeal electromyography (LEMG)-guided vocal fold injection to treatment of unilateral vocal fold paralysis to enhance clinical popularity of LEMG: response to the paper by G.F. Volk et al. Eur Arch Otorhinolaryngol. 2013;270: 1563–1565.
latory clinic of the UNICAMP School of Medicine after undergoing laryngological, phoniatric, and laryngeal endoscopic evaluation. With consent from the ethical committee for human research, all patients underwent LEMG. Technique All patients were examined in the dorsal decubitus, after skin asepsis with alcohol and insertion of electrodes guided by surface laryngeal references. Anesthesia was not necessary. The same experienced and board-certified laryngologist performed all approaches of the intrinsic laryngeal muscles. We used two approach techniques to the thyroarytenoid (TA), as described previously5: (1) across the cricothyroid (CT) membrane in the midline or 0.5 cm from the midline and (2) across the thyroid cartilage. These two approach techniques gave us two different sites for analysis. The clinical diagnostic evaluation, side affected, and approach technique to the muscles were known by the laryngologist but not by the neurophysiologist. Every patient was intended to be evaluated bilaterally to make a final LEMG report. This decision changes in half of the cases when there was no advantage to the diagnostic to lessen discomfort to the patient during the examination. We considered for the research only the cases where there were two electrodes insertions in the same muscle to compare: if only one side was evaluated with two punctures, it was considered unilateral evaluation, and if both sides were evaluated with two punctures, it was considered bilateral. The LEMG results were interpreted by the same neurophysiologist, who was an experienced neurologist and board certified in electromyography. The examination was performed with a bipolar concentric needle electrode inserted percutaneously by the laryngologist, guided by surface references until the sound of muscle activity, and the sharp motor unit potential (MUP) were achieved and considered by the neurophysiologist for analysis. Owing to the differences in the amplitudes and durations of the motor unit action potentials (MUAPs) between the laryngeal muscles (including the TA, CT, posterior cricoarytenoid [CAP], and lateral cricoarytenoid [CAL]), only the TA muscle findings were included in the study analysis. Only the
Agrı´cio N. Crespo, et al
Laryngeal Electromyography
registers that the neurophysiologist approved as optimal were included in the study.6 The LEMG findings were known by the neurophysiologist but not by the laryngologist. The LEMG findings adopted in this study were the same as for any other electromyography analysis1: (1) at rest: electric silence, positive sharp waves, fibrillation potentials, fasciculation potentials, and repetitive discharges; (2) MUAP analysis: the patients were asked to phonate /e/, /i/, or deep inspiration to activate the muscles. Amplitude, duration, phase numbers, and frequency of recruitment were analyzed according to author’s previously published data6; and (3) increased effort: interferential, reduced, 2–3 MUAP only, or no action. A third researcher (a speech pathologist) took note of the difficulties reported by the laryngologist in identifying the laryngeal surface anatomic references, the order of the punctures, the side, and the approach used. The LEMG findings were numbered in the same order as the techniques were numbered the speech pathologist at the end of the study. The CT, CAP, and CAL findings were not included in the study analysis but were used for writing the LEMG reports. The electrophysiological findings can define three patterns, normal, neurogenic, or myogenic reported previously.1,6,7 The LEMG findings at each point of analysis were grouped as (1) equal when the same LEMG findings were encountered in the two different sites approached (eg, normal at one point and the other; fibrillation at one point and the other); (2) different LEMG findings but in accordance with the same electromyographic pattern (eg, neurogenic with repetitive discharge at one point and neurogenic with only fibrillation at the other point); and (3) different LEMG findings and discordant when they could not be correlated with the same electromyographic pattern (eg, normal at one point and neurogenic in the other). Equipment The readings were obtained using a four-channel Nihon Kohden Neuropack M1 (MEB9200) apparatus (Nihon Kohden, Tokyo, Japan), with a common mode rejection ratio of less than 112 dB and 0.6 mVrms noise level. The amplifiers input impedance was 1000 MU. The band-pass filter was set to 10– 10 000 Hz, the sensitivity was 20–50 mV/cm for rest analysis, 100–200 mV/cm for MUP analysis, and 500–1000 mV/cm for interference pattern analysis. The sweep speed was 5–10 ms/ cm for rest and MUP analysis and 30–50 ms/cm for interference pattern analysis. A concentric needle electrode of 37 mm length and 0.07 mm2 contact area was used. RESULTS We studied 40 patients (20 males and 20 females) aged 21– 78 years (mean 48.2 years). Twenty patients were examined bilaterally (40 TA), and 20 patients were examined unilaterally (20 TA). Each TA muscle was examined twice with different approaches at the 60 pairs of sites of insertions (30 on the left). Ninety-five percent of the LEMG findings were equal or in accordance when comparing the analyzed sites, and 5% were discordant. The frequency of equal LEMG findings obtained
499 at different electrode placement sites in the same TA muscle was 76.7% (group 1). There was no predominance for sex, difficulty in recognizing the surface anatomic references, or the pathologies. A total of 11 analyzed pairs of LEMG findings were in group 2. These pairs were obtained in patients with vocal fold immobility who showed characteristics of peripheral nerve compromise, but the patients had a variety of neurogenic findings. Two cases of group 3 LEMG findings were obtained with right-hand side approaches in patients with easily recognizable laryngeal surface references. One group 3 pair was obtained from a patient with right vocal fold immobility, another was obtained from a patient with right vocal fold paresis, and the last was obtained from a patient with left vocal fold hypomobility. The analysis of these three pairs showed the same pattern of discordance, which was normal morphology at one site and discretely longer than normal MUAP durations at the other time.
DISCUSSION Many reports describe the importance of LEMG in neurologic and laryngological diagnosis and prognosis for vocal fold immobility,1,2,7–10 but there is no clear consensus among them.4 There are anecdotal descriptions of difficulty in obtaining reproducible results when LEMG is performed repeatedly in the same patient. We found a high frequency (95%) of equal or concordant LEMG findings between the sites analyzed. We thought that LEMG analysis was dynamic and would need to be performed at the moment of the examination (in real time) by an experienced neurophysiologist. A total of 76.7% of the analyzed site pair LEMG findings were exactly the same, showing that the variability of the LEMG findings was less common than expected. All 11 pairs of LEMG findings from group 2 were obtained in patients with vocal fold immobility and characteristics of peripheral nerve compromise. The pairs of LEMG findings were different for the group 2 patients but were not discordant for the underlying neurologic process. These findings could be explained by fascicular compromise or the evolution of nerve compromise or regeneration. Both hypotheses could explain different time-related LEMG findings in the same muscle. Two pairs of group 3 findings were obtained with a right-hand side approach in patients with easily recognizable laryngeal surface references. Thus, difficulty in recognizing surface references in the muscle approach was not correlated with discordance. In fact, there is no difficulty in inserting the needle electrodes in the TA muscle if the techniques are correctly used.5 One group 3 pair was obtained from a patient with right vocal fold immobility, one from a patient with right vocal fold hypomobility, and the other pair was obtained from a patient with left vocal fold hypomobility. The analysis of these three pairs showed the same pattern of discordance, which was normal MUAP morphology at one time and discretely longer than normal MUAP durations at the other time. In our opinion, two possibilities must be considered: neurophysiologist misinterpretation because the neurogenic findings were close to limits between the normal and discretely increased MUAP duration. In these cases, it would be necessary to quantitatively analyze the MUAP duration or to use information obtained from other
500 muscles related to the same nerve (eg, CAP or CAL). One report showed age-induced remodeling of MUAP, with increasing duration, especially in the left-hand side11; however, in two of our patients, the findings were obtained from the right-hand side, and only one patient was older than 60 years of age. The crosstalking phenomenon was avoided with the use of concentric needle electrodes, which explore a more restricted area and show stable baselines compared with other electrodes.11 We also must consider the possibility of electrode misplacement by the laryngologist. To avoid it, the laryngologist should be trained to approach laryngeal muscles on both sides precisely. The small dimension of the intrinsic laryngeal muscles and their anatomic location behind the thyroid cartilage obviously increase the possibility of electrode misplacement. The accuracy of needle placement in muscles of lower limbs guided only by anatomic landmarks or by ultrasound showed a high rate of misplacement, especially in deep muscles.12,13 Currently, LEMG is being widely used to identify presbylarynx of paresis14 and to study the severity of dysphagia,15 but it needs to be compared across studies before being incorporated into standard procedures as proposed by the Working Group on Neurolaryngology of the European Laryngological Society.16,17 CONCLUSIONS In our opinion, LEMG is an important and useful technique, but caution should be taken to avoid misinterpretation and incorrect muscle approaches. REFERENCES 1. Dumitru D. Electrodiagnostic Medicine. Philadelphia, PA: Hanley-Belfus Mosby; 2012. 2. Hydman J, Gunnar B, Person JKE, Zedenius J, Mattsson P. Diagnosis and prognosis of iatrogenic injury of the recurrent laryngeal nerve. Ann Otol Rhinol Laryngol. 2009;118:506–511. 3. Rickert SM, Childs LF, Carey BT, Murry T, Sulica L. Laryngeal electromyography for prognosis of vocal fold palsy: a meta-analysis. Laryngoscope. 2012;122:158–161.
Journal of Voice, Vol. 29, No. 4, 2015 4. Sataloff RT, Praneetvatakul P, Heuer RJ, Hawkshaw MJ, HemanAckah YD, Schneider SM, Mandel S. Laryngeal electromyography: clinical application. J Voice. 2010;24:228–234. 5. Crespo AN, Kimaid PAT, Quagliato EMAB, Vianna MA, Resende LAL, Wolf AE. Laryngeal electromyography: technical features. Electromyogr Clin Neurophysiol. 2004;44:237–241. 6. Kimaid PAT, Crespo AN, Quagliato EMAB, Vianna MA, Resende LAL, Wolf AE. Laryngeal electromyography in normal Brazilian population. Electromyogr Clin Neurophysiol. 2004;44:243–245. 7. Kimaid PAT, Crespo AN, Quagliato EMAB, Vianna MA, Resende LAL, Wolf AE. Laryngeal electromyography: contribution to vocal fold immobility diagnosis. Electromyogr Clin Neurophysiol. 2004;44:371–374. 8. Munin MC, Murry T, Rosen CA. Laryngeal electromyography. Diagnosis and prognostic applications. Otolaryngol Clin North Am. 2000;33: 759–770. 9. Parnes SM, Satya-Murti S. Predictive value of laryngeal electromyography in patients with vocal cord paralysis of neurogenic origin. Laryngoscope. 1985;95:1323–1326. 10. Sittel C, Stennert E, Thumfart WT, Dapunt U, Ecke HE. Prognostic value of laryngeal electromyography in vocal fold paralysis. Arch Otolaryngol Head Neck Surg. 2001;127:155–160. 11. Takeda N, Thomas GR, Ludlow CL. Aging effects on motor units in the human thyroarytenoid muscle. Laryngoscope. 2000;110:1018–1025. 12. Haig AJ, Goodmurphy CW, Harris BS, Ruiz AP, Etemad J. The accuracy of needle placement in lower-limb muscles: a blinded study. Arch Phys Med Rehabil. 2003;84:877–882. 13. Boon AJ, Oney-Marlow TM, Murthy NS, Harper CM, McNamara TR, Smith J. Accuracy or electromyography needle placement in cadavers: non-guided vs. ultrasound guided. Muscle Nerve. 2011;44:45–49. 14. Stager SV, Bielamowicz SA. Using laryngeal electromyography to differentiate presbylarynges from paresis. J Speech Lang Hear Res. 2010;53: 100–113. 15. Ryu JS, Lee JH, Kang JY, Kim MY, Shin DE, Shin AS. Evaluation of dysphagia after cervical surgery using laryngeal EMG. Dysphagia. 2012; 27:318–324. 16. Volk GF, Hagen R, Pototschnig C, et al. Laryngeal electromyography: a proposal for guidelines of the European Laryngological Society. Eur Arch Otorhinolaryngol. 2012;269:2227–2245. 17. Wang C, Chang M. A proposal to extend application of laryngeal electromyography (LEMG)-guided vocal fold injection to treatment of unilateral vocal fold paralysis to enhance clinical popularity of LEMG: response to the paper by G.F. Volk et al. Eur Arch Otorhinolaryngol. 2013;270: 1563–1565.
