Laryngeal Electromyography and Prognosis of Unilateral Vocal Fold Paralysis A Long-term Prospective Study

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1 The Laryngoscope VC 2014 The American Laryngological, Rhinological and Otological Society, Inc. Laryngeal Electromyography and Prognosis of Unilateral Vocal Fold Paralysis A Long-term Prospective Study Chen-Chi Wang, MD; Ming-Hong Chang, MD; Armando De Virgilio, MD; Rong-San Jiang, MD, PhD; Hsiu-Chin Lai, SLP; Ching-Ping Wang, MD; Shang-Heng Wu, MD; Shih-An Liu, MD, PhD Objectives/Hypothesis: To confirm the value of using laryngeal electromyography (LEMG) to predict the long-term prognosis of unilateral vocal fold paralysis (UVFP), and elucidate the adequate timing of LEMG. Study Design: Prospective cohort prognosis study. Methods: The LEMG data of 84 patients with UVFP were prospectively collected, and 81 patients received follow-up at least 6 months after symptom onset. If the paralyzed vocal fold had <20% recruitment reduction during phonation compared to the normal vocal fold signals, and absence of fibrillation when the patient was silent, the prognosis was considered to be good (negative finding). Otherwise, the prognosis was considered to be poor (positive finding). The association between UVFP outcome and LEMG prognostic rules and the accuracy, sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) of LEMG were calculated. Results: The mean duration of LEMG after symptom onset was 3.7 months, and follow-up after symptoms onset was 18.4 months. Sixty-six of 71 patients with a positive finding had persistent UVFP; four of 10 patients with a negative finding recovered vocal fold motion. LEMG results were significantly associated with the outcome of UVFP (P 5.007). The overall accuracy, sensitivity, specificity, PPV, and NPV of LEMG were 86.4%, 91.7%, 44.4%, 93.0%, and 40.0%, respectively. When LEMG was done more than 2 months after symptom onset, the PPV was 97.9%. Conclusions: LEMG has a high PPV in predicting the long-term outcome of UVFP patients with poor prognosis. Permanent laryngeal framework surgery is feasible if patients have positive findings at least 2 months after symptom onset. Key Words: Fibrillation, laryngeal electromyography, prognosis, recruitment reduction, vocal fold paralysis. Level of Evidence: 1b Laryngoscope, 125: , 2015 INTRODUCTION Unilateral vocal fold paralysis (UVFP) is considered a common disorder in the practice of otolaryngology. Incomplete vocal fold adduction in UVFP may cause formation of a constant glottal gap, which is usually associated with hoarseness of voice and aspiration during Additional Supporting Information may be found in the online version of this article. From the School of Medicine (C.-C.W., S.-A.L.), National Yang-Ming University, Taipei, Taiwan; School of Speech Language Pathology & Audiology (C.-C.W., C.-P.W.), Chung-Shan Medical University, Taichung, Taiwan; Department of Otolaryngology Head & Neck Surgery (C.-C.W., R.-S.J., H.-C.L., C.-P.W., S.-H.W., S.-A.L.), Taichung Veterans General Hospital, Taichung, Taiwan; Department of Neurology (M.-H.C.), Taichung Veterans General Hospital, Taichung, Taiwan; Department of Sensory Organs (A.D.), ENT Section, Sapienza University of Rome, Rome, Italy; School of Medicine (R.-S.J.), Chung-Shan Medical University, Taichung, Taiwan. Editor s Note: This Manuscript was accepted for publication September 29, This work was supported by research grants from Taichung Veterans General Hospital (No. TCVGH B and No. TCVGH C). This study was approved by the institutional review board of Taichung Veterans General Hospital (IRB TCVGH No. C07083 and No. C08208). The authors have no other funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Chen-Chi Wang, MD, Department of Otolaryngology Head & Neck Surgery, Taichung Veterans General Hospital, No. 1650, Sec. 4, Taiwan Boulevard, Taichung 40705, Taiwan. entccwang@msn.com DOI: /lary swallowing. The impairment of laryngeal nerve function can have various causes, but two types of paralysis, idiopathic and iatrogenic, are the most frequent conditions. 1,2 In UVFP, accurate prediction of poor prognosis is very important to ensure that suitable candidates are selected for permanent laryngeal framework surgery such as thyroplasty type I or arytenoid adduction. 3 Since laryngeal electromyography (LEMG) was introduced in 1944 by Weddel and Pattle, 4 it has become a valuable tool for supporting laryngological assessment. It is commonly used for predicting prognosis of UVFP, and several retrospective studies have shown that LEMG has a high positive predictive value (PPV) for screening patients with poor recovery. Our previous study found that the PPV was high especially when LEMG was done more than 2 months after the symptom onset. 5,6 In 2009, the Neurolaryngology Study Group of the American Academy of Otolaryngology/Head and Neck Surgery (AAO-HNS) (an unaffiliated group of interested professionals but not a formal part of the AAO-HNS) concluded that LEMG was primarily a qualitative, not a quantitative, examination. 7 By qualitative analysis, we found more than 90% of patients with abnormal findings, such as fibrillations and absent or reduced voluntary motor unit potentials, did not recover vocal fold mobility. 5,6 However, the amount of evidence in some studies was inadequate due to retrospective data review, short-term follow-up duration, or small case

2 numbers. 6,8 The optimal timing of LEMG in relation to symptom onset also remains unclear. The Neurolaryngology Study Group of the AAO-HNS as well as the European Laryngological Society recommended that further prospective studies be conducted and methods and interpretations of LEMG be standardized. 7,9 In this study, we prospectively collected data during a long-term follow-up to investigate the usefulness of LEMG in predicting the prognosis of UVFP. MATERIALS AND METHODS From May 2007 to February 2013, after institutional review board approval (IRB TCVGH No. C07083 and No. C08208), we prospectively followed up 84 patients with idiopathic or iatrogenic UVFP who received LEMG 3 or more weeks after the symptom onset. The outcome measurement was done with regular follow-up for all of the 84 patients with flexible videolaryngoscopy or videostroboscopy after LEMG to check for vocal fold motion recovery. Compared to the healthy side, if the paralyzed vocal fold recovered >75% motion with obvious abduction during inspiration, we defined the patient has having had motion recovery. Except for patients who recovered vocal motion <6 months after symptoms onset, only patients who received follow-up 3 or more months after LEMG and 6 or more moths after symptom onset are included for statistical analysis. Eighty-one patients fulfilled the criteria, and the association of the LEMG result and UVFP outcome were then analyzed. To elucidate the optimal timing of LEMG after symptoms onset, we also dichotomized the patients into two groups: 1) LEMG was performed <2 months after symptom onset and 2) LEMG was performed >2 months after symptoms onset. The dichotomization is based on the finding that LEMG done <2 months after symptoms onset had a higher false-positive rate in our previous retrospective study with short-term follow-up. 5 The predictive values of LEMG in different timing after symptom onset were compared again in this research with prospective long-term follow-up. The office-based LEMG was performed by a laryngologist familiar with the anatomy of intrinsic laryngeal muscles (C.- C.W.). The LEMG findings were interpreted by a neurologist with 20 years experience in electrodiagnostic medicine (M.-H.C.). All LEMG examinations were performed by the same apparatus (Cadwell Sierra 6200A; Cadwell Laboratories, Inc., Kennewick, WA) using a computer-based electrodiagnostic system. LEMG signals were monitored on a computer screen and by means of a speaker simultaneously. Low-frequency filter settings were set at 10 Hz, and high-frequency filter settings were set at 10,000 Hz. Motor unit recruitment tracings were recorded with sweep speeds at 10 ms per division using a gain of 50 to 200 lv per division. A 26-gauge monopolar injectable needle electrode (Boject Disposable Needle Electrode; Alpine Biomed ApS, Skovlunde, Denmark) was used in conjunction with both a surface disk reference electrode and a ground electrode, which were affixed to superior cervical and clavicle levels, respectively. The procedure and prognostic analysis has been described in detail in our previous studies. 5 Briefly, the thyroarytenoid (TA) muscle was approached by inserting a needle through the cricothyroid ligament approximately 0.5 cm from the midline, and the signals obtained from the TA muscle represented the recurrent laryngeal nerve function. The position of the needle was validated by asking the patient to repeat a sustained vowel /i/. The neurologist compared the recruitment pattern of the paralyzed vocal fold to that of the normal vocal fold and estimated the percentage of recruitment reduction (RR) in the paralyzed vocal fold. According to our previous study, 5 we defined the recruitment pattern of the paralyzed vocal fold TA muscle with <20% RR as normal to nearly normal. If the paralyzed vocal fold TA muscle had >20% RR, there was obvious recruitment reduction (Fig. 1). Finally, we asked the patient to keep silent to see if there was any spontaneous activity such as fibrillation potentials (FIBs) in paralyzed vocal folds with ongoing axonal degeneration (Fig. 2). Because positive sharp wave was rarely detected and always occurred with FIBs in this study, it was not a parameter for analysis. The preset rules described in our previous study 5 were then used to predict the prognosis of unilateral vocal fold paralysis. If the paralyzed vocal fold had normal to nearly normal recruitment (<20% RR) during phonation compared to the normal vocal fold LEMG, and absence of fibrillation when the patient kept silent, the prognosis was defined to be good (LEMG-negative finding). Otherwise, the prognosis was defined to be poor (LEMG-positive finding). We made a prognostic prediction promptly after the LEMG and blindly before knowing the outcome of paralyzed vocal fold mobility. Moreover, to treat the patients simultaneously, we used LEMG-guided hyaluronic acid (HA) vocal fold injection to correct the glottal gap of UVFP. 10,11 After completion of LEMG signal recording, 1.0 ml of HA Restylane Perlane (Q-Med, Uppsala, Sweden) was injected via a 26-gauge injectable needle into the TA muscle to augment the paralyzed vocal fold (see Supporting Video 1 in the online version of this article). In our recent published long-term follow-up data of HA injection, 10 about 81% of our patients did not need open laryngeal framework surgery after one (60%) or two and three injections (21%) of HA, with a mean follow-up of 17.4 months. That simultaneous injection gave our patients an opportunity to have serviceable voice for a long follow-up duration of immobile vocal fold without permanently fixing the paralyzed vocal fold in the midline with laryngeal framework surgery. The motions of paralyzed vocal folds were checked regularly by laryngoscopy after LEMG. The association of UVFP outcome and LEMG prognostic rules was analyzed with the Fisher exact test. P <.5 was considered significant. The accuracy, sensitivity, specificity, PPV, and negative predictive value (NPV) of LEMG were calculated for all 81 patients. Furthermore, we dichotomized those patients according to timing of LEMG (2 months and >2 months) after symptom onset. Therefore, we could observe the influence of timing of LEMG on the aforementioned accuracy, sensitivity, specificity, PPV, and NPV measurement. RESULTS From May 2007 to February 2013, the LEMG data of 84 patients were collected. Three patients were excluded for statistical analysis because they did not fulfill the criteria of follow-up 3 or more months after LEMG and 6 or more moths after symptom onset. In 81 patients with idiopathic (n 5 14) or iatrogenic (n 5 67) UVFP, there were 35 men and 46 women. Their ages ranged from 21 to 82 years, with a mean of years. The timing of LEMG after symptom onset ranged from 1 to 11 months, with a mean of months (median months). Twenty eight patients received LEMG within 2 months after symptom onset, and 53 patients received LEMG more than 2 months after symptom onset. The outcome measurement time after LEMG ranged from 3 to 66 months with a mean of months (median months). The outcome measurement time after symptom onset ranged from 4 to 68 months, with a mean of months (median 5 15 months). For 72 patients without vocal fold 899

3 Fig. 1. The nearly normal and obvious recruitment reduction (RR) patterns of paralyzed vocal fold in laryngeal electromyography (EMG). TA 5 thyroarytenoid muscle. motion recovery, the outcome measurement time after symptom onset ranged from 6 to 68 months, with a mean of months (median months) Of the 81 included patients, 71 patients had positive LEMG findings and 66 had UVFP that persisted in Fig. 2. Fibrillation potentials (fibs) that were found in paralyzed vocal folds with ongoing axonal degeneration. EMG 5 electromyography; TA 5 thyroarytenoid muscle. 900 the follow-up. Ten patients had negative LEMG findings, and four patients recovered vocal fold motion (Table I). In 71 patients of positive LEMG findings, the mean of recruitment reduction was 72% 6 20% (median 5 80% as shown in Fig. 1A). In 10 patients with negative LEMG findings, the mean of recruitment reduction was % (median 5 10 as shown in Fig. 1B). The box plot of recruitment reduction in two groups of different LEMG findings is shown in Figure 3. LEMG findings were significantly associated with the outcome of UVFP (P 5.007, Fisher exact test). The accuracy, sensitivity, specificity, PPV, and NPV of LEMG were 86.4%, 91.7%, 44.4%, 93.0%, and 40.0%, respectively. Analysis of the 28 patients who received LEMG within 2 months after symptom onset revealed that 24 patients had positive LEMG findings, and 20 of them had UVFP that persisted in the follow-up. Four patients had negative LEMG findings, and two patients recovered vocal fold motion. LEMG findings were not significantly associated with the outcome of UVFP (P 5.191, Fisher exact test). Analysis of the 53 patients who received LEMG more than 2 months after symptom onset showed that 47 patients had positive LEMG findings, and 46 of them had UVFP that persisted in the follow-up. Six patients had negative LEMG findings, and two patients recovered vocal fold motion. LEMG findings were significantly associated with the outcome of UVFP (P 5.031, Fisher exact test) (Table I). The accuracy, sensitivity, specificity, PPV, and NPV of the

4 TABLE I. Outcome Prediction and Timing of LEMG. Persistent Paralysis, n (%) UVFP Outcome Recovered Motion, n (%) P Value LEMG >3 weeks, n 5 81 LEMG positive 66 (82.5) 5 (5.0).007* LEMG negative 6 (7.5) 4 (5.0) LEMG >2 months, n 5 53 LEMG positive 46 (86.8) 1 (1.9).031* LEMG negative 4 (7.5) 2 (3.8) *P <.05 indicates statistical significance in the Fisher exact test. LEMG 5 laryngeal electromyography; UVFP 5 unilateral vocal fold paralysis. different LEMG timings (2 months vs. >2 months after symptom onset) are listed and compared to the overall patient data in Table II. Of the 81 patients, nine (11.1%) patients (four idiopathic and five iatrogenic) recovered vocal fold motion. The timing of recovery after LEMG for the nine patients was 6, 5, 5, 15, 5, 3, 6, 18, and 4 months, respectively, with a mean of months (median 5 5 months). The timing of recovery after symptom onset for the nine patients was 7, 9, 6, 20, 9, 4, 7, 19, and 5 months, respectively, with a mean of months (median 5 7 months) (see Supporting Video 2 in the online version of this article). DISCUSSION Since Weddel and Pattle 4 first suggested that LEMG may have prognostic value for vocal fold paralysis, the results of many studies have supported their suggestion. However, according to the meta-analysis by Rickert et al. 6 and the review by Sataloff et al., 8 all of these studies were retrospective, and not enough evidence was provided to support the utility of LEMG in predicting the prognosis of vocal fold paralysis. In the article published by Volk et al. in 2012, 9 the authors noted that although LEMG has been considered as a valuable diagnostic tool for more than 60 years, many laryngologists do not routinely use it. This may be due to a persisting lack of agreement on methodology, interpretation, validity, and clinical application of LEMG. Therefore, on the issue of vocal fold paralysis, we need to devise simple diagnostic rules with acceptable accuracy to increase the popularity of LEMG in clinical practice. In this prospective study with long-term follow-up, we tried to offer sufficient evidence to prove the usefulness of LEMG in predicting the outcome of UVFP. In the literature, the prognostic criteria vary from study to study, but many criteria fundamentally mirror the Seddon classification of nerve injury. In Seddon s classification, absent voluntary motor units and spontaneous activities such as fibrillation potentials reflect axonotemesis, or neurotemesis, which indicates poor prognosis. 12 In contrast, near-normal voluntary motor unit potentials and recruitment without spontaneous activities reflect neuropraxy, which might have better prognosis. 12 According to the meta-analysis by Rickert et al., 6 most studies do not define near-normal status quantitatively. In our previous retrospective study, 5 we defined it as <20% RR (80% 100% of normal motor unit recruitment). In the present study, this preset rule was used again prospectively to predict the prognosis of UVFP. In our 81 studied subjects, the accuracy (86.4%), sensitivity (91.7%), and PPV (93.0%) were as high as in our previous retrospective report (87.1%, 92.3%, and 92.3%, respectively) with shorter follow-up duration (3 5 months after LEMG). 5 Obviously, a shorter follow-up period than optimal would lead to overstating the number of patients who will not recover, and may influence the results of LEMG study, especially the PPV. In this prospective study, the median follow-up times after LEMG and symptom onset were 11.0 months and 15.0 months, respectively, indicating that LEMG could predict absence of recovery even in the long run in patients with UVFP. In contrast, the NPV, indicating presence of recovery, was lower (40%) in this study. The result was in line with that of our previous retrospective study (60%). 5 It is not surprising that the NPV was lower because laryngeal reinnervation is a complex and indefinite process. The principal problem is the admixture of adductor and abductor fibers within the recurrent laryngeal nerve. This anatomical structure raises the possibility of inappropriate and even counterproductive aberrant reinnervation when repair does occur. 6 Crumley and others have examined this synkinesis phenomenon extensively. 13 However, an accurate prediction of no recovery is more important than a prediction of recovery. LEMG with high PPV can spare a vocally disabled person a wait of several months for recovery, or the need for more vocal fold injection procedures with absorbable materials. In our proposed initial management strategy of UVFP by LEMG-guided HA vocal fold injection, 11 we Fig. 3. Box plot of recruitment reduction (RR) in different LEMG findings. The median RR was 80% in the laryngeal electromyography (LEMG)-positive group and 10% in LEMG-negative group. 901

5 TABLE II. Predictive Values of Laryngeal Electromyography Preset Rules in Unilateral Vocal Fold Paralysis at Different Timings. Timing No. Accuracy Sensitivity Specificity PPV NPV Overall % (2) 91.7% (2) 44.4% (2) 93.0% (2) 40.0% (2) 2 months % (3) 90.9% (3) 33.3% (3) 83.3% (3) 50.0% (1) >2 months % (1) 92.0% (1) 66.7% (1) 97.9% (1) 33.3% (3) All data are reported as percentages (ranking). The ranking indicates the relative performance (1 being the best, 3 the worst) of each characteristic in the given category. NPV 5 negative predictive value; PPV 5 positive predictive value. encouraged patients with a positive result (poor prognosis) to have permanent laryngeal framework surgery, such as thyroplasty type I or arytenoid adduction, once the injected HA was absorbed during deteriorated vocal function. For patients with a negative result (good prognosis), the injected HA might ameliorate the symptoms before possible spontaneous recovery. Another important undetermined issue in regard to LEMG for UVFP is the appropriate timing of LEMG to achieve better accuracy. Clearly, the longer the time it takes after symptom onset to identify poor prognosis, the more reliable the prognosis is likely to be. However, the clinical utility of LEMG lies in early accuracy. In our previous retrospective study with 45 patients, 5 we found the false-positive rate was higher when LEMG was performed within 2 months after symptom onset. In this prospective study, we had a similar finding. As shown in Table II, LEMG performed >2 months after symptom onset achieved the highest accuracy (90.6%), sensitivity (92.0%), specificity (66.7%), and PPV (97.9%). The natural history of UVFP has not been clearly established, and the potential timing for spontaneous recovery varies from one clinical scenario to another. However, Hirano et al. 14 suggested excluding patients from LEMG testing 6 months after symptom onset based on their impression that few patients recovered after that interval. Therefore, permanent laryngeal framework surgery is usually indicated clinically for patients with UVFP 6 months after symptom onset. However, in our present study, only 33% (3/9) of patients with recovery were within 6 months from symptom onset. It seems that the 6-month criterion is arbitrary and unreliable. Therefore, more objective adjuvant guidance is needed when LEMG is used for management of UVFP. LEMG has often been dismissed as being a subjective test, particularly as to judgments regarding the degree of recruitment. According to our result, the median recruitment reduction was 80% in the LEMG-positive group and 10% in the LEMG-negative group. It seems that it is usually not hard to dichotomize patients to poor prognosis or good prognosis based on recruitment reduction. Furthermore, when LEMG is performed by an experienced neurologist familiar with electrodiagnostic medicine and following unambiguous preset rules, as in our previous study and the present study, the level of accuracy remained high. Because clinical electrophysiology is a fundamental part of resident training in neurology but not in otorhinolaryngology, we suggest laryngologists and neurol- 902 ogists should work as a team. The European Laryngological Society also proposed this type of cooperation as a guideline for LEMG. 9 However, further investigation by other cooperative teams is needed to confirm the reliability of our preset rules and findings. In addition, Statham et al. 15 and Smith et al. 16 have proposed quantitative LEMG criteria, such as turns and amplitudes, to improve the prediction of motion recovery in paralyzed vocal folds in their retrospective studies with a short-term mean follow-up of 3 months. However, the automatic algorithms have not been widely established yet. 9 In Smith s pioneer quantitative LEMG study, 16 they integrated both qualitative and quantitative LEMG data and retrospectively categorized their patients to poor, fair, poor/fair, and excellent prognosis groups. The value of quantitative LEMG needs to be confirmed with a prospective study using purely quantitative LEMG data with a long-term follow-up in the future. By applying our simple semiquantitative rules, we found that the PPV (93.0%) was similar to that (89.5%) reported by Smith et al. 16 and acceptable in guiding the management of UVFP. The reality is that the chance of spontaneous recovery was very low in this study, and 88.9% (72/81) of our study subjects did not recover vocal fold function. A positive result from a simple semiquantitative rule could therefore confirm this poor result. Reviewing another retrospective study cited in Rickertetal. smeta-analysis, 6 the recovery rate is variable from Sittel et al. s 8.1% (9/111) 17 to Gupta and Bastian s 50% (9/18). 18 In our previous study cited by Richert et al. s meta-analysis, the recovery rate was 29% (13/45). Obviously, we could not predict what kind of patient we would encounter during the period of study. That is why we need LEMG to help us differentiate prognosis and guide further treatment. Although the percentage of patients with recovery varies in different studies, the association of LEMG result and prognosis still remains significant. Another limitation of this study is the outcome measurement. We used vocal fold motion recovery as an end point, which was also used in other studies in Rickert et al. s meta-analysis. 6 However, according to the observation of Crumley, 19 some UVFP patients may have favorable synkinesis (aberrant reinnervation) with little or no phonatory deficit, although there is no recovery of vocal fold motion. Because we could not only observe patients without any treatment, and HA injection changed the patients phonatory function, we were unable to use spontaneous function recovery as a second

6 end point in this study. In addition, the role of diagnosing synkinesis in UVFP remains undetermined. Crumley commented that LEMG may eventually assist the laryngologist in establishing synkinesis diagnosis, but currently not enough normative data exist for confirming laryngeal synkinesis unequivocally in every case. 20 Furthermore, our study protocol did not contain performing LEMG data at last follow-up. Therefore, electrical recovery could not be used as another end point in our article. Recently, Statham et al. proposed that detecting synkinesis might improve the accuracy of LEMG to predict prognosis of UVFP in their retrospective study. 21 The synkinesis testing was positive in 9.7% of their cohort. It seems that the synkinesis test is a potential adjunct procedure to improve the NPV and sensitivity of LEMG, and they concluded that the issue needs further investigation and validation. CONCLUSION With a long-term prospective follow-up, this study confirmed that our LEMG rules can provide reliable prognostic information for UVFP. For patients with positive LEMG findings, the chance of recovery of vocal fold motion will be very low. If LEMG is performed more than 2 months after the symptom onset, the PPV could be improved from 93.0% to 97.9%. Surgeries (such as thyroplasty type I or arytenoid adduction) could be performed as soon as possible after a positive LEMG finding. Acknowledgments The authors thank Ms. Anting Yu for her help in collecting the data. BIBLIOGRAPHY 1. Yamada M, Hirano M, Ohkubo H. Recurrent laryngeal nerve paralysis: a 10-year review of 564 patients. Auris Nasus Larynx 1983;10(Suppl): S1 S Havas T, Lowinger D, Priestley J. Unilateral vocal fold paralysis: causes, options and outcomes. Aust N Z J Surg 1999;69: Misono S, Merati AL. Evidence-based practice: evaluation and management of unilateral vocal fold paralysis. Otolaryngol Clin North Am 2012; 45: Weddel GB, Pattle RE. The electrical activity of voluntary muscle in man under normal and pathological conditions. Brain 1944;67: Wang CC, Chang MH, Wang CP, Liu SA. Prognostic indicators of unilateral vocal fold paralysis. Arch Otolaryngol Head Neck Surg 2008;134: Rickert SM, Childs LF, Carey BT, Murry T, Sulica L. Laryngeal electromyography for prognosis of vocal fold palsy: a meta-analysis. Laryngoscope 2012;122: Blitzer A, Crumley RL, Dailey SH, et al. Recommendations of the Neurolaryngology Study Group on laryngeal electromyography. Otolaryngol Head Neck Surg 2009;140: Sataloff RT, Mandel S, Mann EA, Ludlow CL. Practice parameter: laryngeal electromyography (an evidence-based review). Otolaryngol Head Neck Surg 2004;130: Volk GF, Hagen R, Pototschnig C, et al. Laryngeal electromyography: a proposal for guidelines of the European Laryngological Society. Eur Arch Otorhinolaryngol 2012;269: Wang CC, Chang MH, Jiang RS, et al. Laryngeal electromyographyguided hyaluronic acid vocal fold injection for unilateral vocal fold paralysis a prospective long term follow up outcome report. JAMA Otolaryngol Head Neck Surg. In press. 11. Wang CC, Chang MH. 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: Seddon H. Three types of nerve injury. Brain 1943;66: Crumley RL. Laryngeal synkinesis: its significance to the otolaryngologist. Ann Otol Rhinol Laryngol 1989;98: Hirano M, Nosoe I, Shin T, Maeyama T. Electromyography for laryngeal paralysis. In: Hirano M, Kirchner J, Bless D, eds. Neurolaryngology: Recent Advances. 1st ed. Boston, MA: College Hill; 1987: Statham MM, Rosen CA, Nandedkar SD, Munin MC. Quantitative laryngeal electromyography: turns and amplitude analysis. Laryngoscope 2010;120: Smith LJ, Rosen CA, Niyonkuru C, Munin MC. Quantitative electromyography improves prediction in vocal fold paralysis. Laryngoscope 2012; 122: Sittel C, Stennert E, Thumfart WF, Dapunt U, Eckel HE. Prognostic value of laryngeal electromyography in vocal fold paralysis. Arch Otolaryngol Head Neck Surg 2001;127: Gupta SR, Bastian RW. Use of laryngeal electromyography in prediction of recovery after vocal cord paralysis. Muscle Nerve 1993;16: Crumley RL. Laryngeal synkinesis revisited. Ann Otol Rhinol Laryngol 2000;109: Crumley RL. Unilateral recurrent laryngeal nerve paralysis. J Voice 1994; 8: Statham MM, Rosen CA, Smith LJ, Munin MC. Electromyographic laryngeal synkinesis alters prognosis in vocal fold paralysis. Laryngoscope 2010;120: