Quantitative Electromyographic Characteristics of Idiopathic Unilateral Vocal Fold Paralysis

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1 The Laryngoscope VC 2016 The American Laryngological, Rhinological and Otological Society, Inc. Quantitative Electromyographic Characteristics of Idiopathic Unilateral Vocal Fold Paralysis Wei-Han Chang, MD; Tuan-Jen Fang, MD; Hsueh-Yu Li, MD; Fu-Shan Jaw, PhD; Alice M. K. Wong, MD; Yu-Cheng Pei, MD, PhD Objectives/Hypothesis: Unilateral vocal fold paralysis with no preceding causes is diagnosed as idiopathic unilateral vocal fold paralysis. However, comprehensive guidelines for evaluating the defining characteristics of idiopathic unilateral vocal fold paralysis are still lacking. In the present study, we hypothesized that idiopathic unilateral vocal fold paralysis may have different clinical and neurologic characteristics from unilateral vocal fold paralysis caused by surgical trauma. Study Design: Retrospective, case series study. Methods: Patients with unilateral vocal fold paralysis were evaluated using quantitative laryngeal electromyography, videolaryngostroboscopy, voice acoustic analysis, the Voice Outcome Survey, and the Short Form-36 Health Survey quality-of-life questionnaire. Patients with idiopathic and iatrogenic vocal fold paralysis were compared. Results: A total of 124 patients were recruited. Of those, 17 with no definite identified causes after evaluation and follow-up were assigned to the idiopathic group. The remaining 107 patients with surgery-induced vocal fold paralysis were assigned to the iatrogenic group. Patients in the idiopathic group had higher recruitment of the thyroarytenoid lateral cricoarytenoid muscle complex and better quality of life compared with the iatrogenic group. Conclusion: Idiopathic unilateral vocal fold paralysis has a distinct clinical presentation, with relatively minor denervation changes in the involved laryngeal muscles, and less impact on quality of life compared with iatrogenic vocal fold paralysis. Key Words: Unilateral vocal fold paralysis, vocal cord palsy, videolaryngostroboscopy, laryngeal electromyography, quantitative electromyography. Level of Evidence: 4. Laryngoscope, 126:E362 E368, 2016 INTRODUCTION Idiopathic vocal fold paralysis (IVFP) had been reported as the most common cause of unilateral vocal fold paralysis. 1,2 Idiopathic vocal fold paralysis is diagnosed by excluding other etiologies, such as iatrogenic injury, neoplastic invasion, trauma, central nervous system lesions, and intubation. 1,3 With the advancement of diagnostic tools able to reveal the veridical diagnosis for a unilateral vocal fold paralysis, and the development of From the Institute of Biomedical Engineering, National Taiwan University (W-H.C., F-S.J.); the Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital at Taipei (W-H.C.), Taipei; the Department of Otolaryngology Head and Neck Surgery (T-J.F., H-Y.L.); the Department of Physical Medicine and Rehabilitation (Y-C.P.), Chang Gung Memorial Hospital at Linkou; the Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital at Taoyuan (A.M.K.W.); the School of Medicine (T-J.F., H-Y.L., A.M.K.W., Y-C.P.); and the Healthy Aging Research Center (Y-C.P.), Chang Gung University, Taoyuan, Taiwan. Editor s Note: This Manuscript was accepted for publication February 1, Supported by grants CMRPG 3D1412 from Chang Gung Medical Foundation in Taiwan and NMRPG B-182A-056-MY2 from National Science Council, Taiwan. The authors have no other funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Yu-Cheng Pei, MD, PhD, Chang Gung Memorial Hospital, No. 5 Fushing St., Taoyuan County 333, Taiwan. yspeii@gmail.com DOI: /lary E362 surgical techniques that could cause iatrogenic trauma, the incidence of unilateral IVFP has been decreasing over time while that of iatrogenic vocal fold paralysis has been increasing. 4 The precise pathophysiology of IVFP remains debatable 5 ; it has been suggested that virus infections 5 7 and underlying neurologic conditions 8 account for the development of IVFP. Although its clinical presentation 2,5,7 10 and longterm prognosis 2 have been the main themes of research into IVFP, the results remain inconsistent. In a case series of 39 patients, Ward and Berci 7 found that all cases of IVFP involved both the superior laryngeal nerve (SLN) and the recurrent laryngeal nerve (RLN), whereas Dray et al. 5 reported that bilateral IVFP only involved the RLN in a case series of four patients. The 1-year prognoses also varied, with Willatt and Stell 10 reporting that 50% of patients regained their vocal fold and voice functions, whereas Sulica et al. 2 found an incidence of motion recovery of 13% to 83%. Laryngeal electromyography (LEMG) is the gold standard for confirming the existence and extent of neuropathy in vocal fold paralysis, 9,11,12 with quantitative LEMG allowing analysis of the degree of nerve injury. Idiopathic vocal fold paralysis has not yet been comprehensively evaluated; it is necessary to apply objective evaluations to characterize its clinical characteristics. In this study, we hypothesized that unilateral IVFP may have different clinical and neurologic

2 characteristics than those caused by surgical trauma. We performed conventional LEMG in patients with unilateral vocal fold palsy to confirm the sites of neuropathies, and quantitative LEMG to assess the severity of injury of the thyroarytenoid lateral cricoarytenoid (TA LCA) muscle complex and cricothyroid (CT) muscle. The clinical presentations of unilateral IVFP were characterized based on comprehensive measurements including videolaryngostroboscopy, voice acoustic analysis, and voice- and health-related qualities of life. Finally, the clinical presentations of idiopathic and the more prevalent iatrogenic (surgery-induced) vocal fold palsy were compared. 1,16,17 MATERIALS AND METHODS Human Subjects We recruited patients from the otolaryngology outpatient clinic at a medical center from September 2011 to March Inclusion criteria were adults (> 18 years old) diagnosed with unilateral vocal fold paralysis and confirmed by laryngoscopy. Exclusion criteria were no evidence of neurogenic vocal fold palsy detected by LEMG; contraindications for or rejection of needle electromyography; or history of interventions to correct the paralyzed vocal fold position, such as intracordal injection, laryngoplasty, or laryngeal framework surgery. Patients with bilateral TA LCA impairment or CT muscle injuries in the healthy side according to LEMG studies were also excluded. All aspects of the study were specifically approved by the Human Studies Research Committee of Chang Gung Medical Foundation. Written informed consent was obtained from each participant prior to recruitment. Procedures Patients underwent assessments including videolaryngostroboscopy, voice acoustic analysis, LEMG with quantitative analysis, Voice Outcome Survey (VOS) questionnaire, and Short Form-36 Health Survey (SF-36) quality-of-life questionnaire. All of these assessments were performed within 2 weeks of the day of LEMG assessment. Videolaryngostroboscopy Patients were asked to project the vowel /e/ at their habitual pitch and intensity, and the voice and vocal fold vibration samples were recorded by videolaryngostroboscopy. The recorded movie was analyzed offline, frame by frame, using Image J software (Image J 1.44; National Institutes of Health, Bethesda, MD) to give the normalized glottal gap area (NGGA) following the method of Omori et al., 18 as described in the following equation: NGGA ¼ Glottal gap area = ðmembranous vocal fold lengthþ units Measurement of the NGGA has been described in detail previously. 14 Glottal gaps were measured in maximally closed phases during vocal fold vibration to give the closed-phase NGGAs (Fig. 1). Voice Acoustic Analysis A board-certified speech pathologist recorded voice samples while the patient read a standard passage and then sustained a vowel at conversational pitch and loudness. The Fig. 1. Measurement of normalized glottal gap area in the closed phase of phonation. The movie frame was captured from the video of videolaryngostroboscopy, and the glottal gap area was identified using a computer segmentation process. The membranous vocal fold length (L) was defined as the distance expressed in pixels from the anterior commissure to the tip of the membranous vocal process. maximal phonation time represented the duration for which a patient could sustain an /a/. A stable segment from the midportion of the vowel voice sample was used for the following acoustic analysis. Acoustic characteristics of the recorded voice were measured using a computerized speech laboratory system (CSL4300B 5.05; KayPENTAX, Montvale, NJ) to give the fundamental frequency (F0), jitter (frequency perturbation), shimmer (perturbation of amplitude), and harmonic-to-noise ratio. Finally, the patient produced each of a sustaining /s/ and /z/ as long as possible, from which the S/Z ratio (S/Z) was computed as the ratio of /s/ and /z/ durations. 19 Laryngeal Electromyography Examination The standard protocol for LEMG was performed by a board-certified otolaryngologist (T-J.F.) and physiatrists (Y-C.P. and W-H.C.). We examined the LEMG signals for bilateral TA LCA muscle complexes and CT muscles. The detailed procedure of LEMG has been described previously. 14 Quantitative Laryngeal Electromyography Analysis We developed a Matlab (The Mathworks, Natick, MA)- based program to analyze the raw LEMG data. The raw LEMG waveforms were first binned into nonoverlapping epochs, with epoch durations for the TA LCA and CT muscles of and 50 ms, respectively. A shorter bin width was chosen for the CT muscle to capture the dynamic control for the upward glissando /e/. The timing of each turn and its amplitude was localized using an automatic algorithm. Specifically, a turn was defined by the change in polarity, with an amplitude of at least 100 mv before and after the change, to exclude noise-related peaks. E363

3 Fig. 2. Flow diaphragm for subject enrollment, exclusion, allocation, and analysis. LEMG 5 laryngeal electromyography. Turn frequency was computed for each epoch as the number of turns divided by the epoch duration. Turn amplitude was computed as the mean of the absolute turn-amplitude values. For each muscle, we averaged the turn frequencies for the epochs with the turn frequencies that ranked among the top three epochs to yield the peak turn frequency. For the acoustic data recorded during LEMG, we adopted the MATLAB-based source codes composed by de Cheveigne and Kawahara, 20 which yielded parameters such as F0 and voice power. Voice Outcome Survey The VOS developed by Gliklich et al. 21 is a five-item survey that evaluates the physical and social problems induced by unilateral vocal fold paralysis using a Likert scaling technique. Survey items and total scores were normalized between 0 (worst) to 100 (best) based on published algorithms. The Mandarin version of VOS has undergone a standard surveyvalidation process. 22 Short Form-36 The SF-36 is a widely used tool to evaluate eight qualityof-life domains. The recall period for SF-36 is 4 weeks, and its scores are normalized according to published algorithms from 0 (worst) to 100 (best). We adopted the SF-36 Assessment Standard Taiwan version 1 with its Taiwanese norm. 23,24 Statistical Analysis Patients were divided into idiopathic and iatrogenic groups according to disease etiology. Differences between the two groups were compared using Student t tests for parametric data, Mann-Whitney U tests for nonparametric data (including results from SF-36), and v 2 tests for categorical data. The fundamental frequency obtained in acoustic analysis was analyzed by analysis of variance with group and age as the two main factors because age is known to affect fundamental frequency. The level of significance was defined as P <.05. RESULTS We initially recruited 177 patients with unilateral vocal fold paralysis diagnosed by laryngoscopy. Of those, 10 were excluded because of rejection or contraindication of LEMG and 18 because of incomplete LEMG data. A total of 149 patients thus had complete LEMG data. Of those, 17 were excluded: one because of lack of neurogenic vocal fold palsy, 10 because of bilateral laryngeal neuropathies, three because of superior laryngeal neuropathies in the healthy side according to LEMG study, and three because of a history of intracordal injection. Among the 132 patients who thus met the inclusion and exclusion criteria, eight were further excluded because of etiologies that were not idiopathic or surgically iatrogenic: five patients because of neoplasms, one because of surgery following radiotherapy, one because of radiotherapy, and one because of pulmonary tuberculosis. The remaining 124 patients were assigned to the idiopathic (n 5 17) group or the surgery-induced, iatrogenic (n 5 107) group, according to their etiologies (Fig. 2). Videolaryngostroboscopy data were missing for one patient in E364

4 TABLE I. Demographics, Glottal Area, Voice Acoustic Analysis, Laryngeal Muscle Recruitment, and Quality of Life in Patients With Idiopathic and Iatrogenic Vocal Fold Paralysis. Idiopathic Group Iatrogenic Group P Value Sex (male/female) 9/8 45/ Age (year) Etiology Idiopathic 17 Thyroid/parathyroid surgery 51 Esophageal surgery 21 Lung or mediastinal surgery 19 Heart surgery 7 Cervical spine surgery 5 Skull base surgery 2 Carotid body tumor resection (surgery) 1 Subclavical surgery 1 Paralysis side (right/left) 5/12 41/ CT (superior laryngeal nerve) involvement (yes/no) 9/8 24/83 < 0.001* Disease onset duration (month) (1 10) (1 10) Videolaryngostroboscopy NGGA Voice Acoustic Analysis Maximum phonation time (s) SZ ratio Fundamental frequency (Hz) Jitter (%) Shimmer (db) Harmonic-to-noise ratio Recruitment Analysis Lesion side of TA-LCA (turn/s) * Normal side of TA-LCA (turn/s) Turn ratio of TA-LCA Lesion side of CT (turn/s) Normal side of CT(turn/s) Turn ratio of CT Quality of Life VOS * SF-36 Vitality Physical functioning * Bodily pain * General health perceptions * Physical role functioning * Emotional role functioning * Social functioning * Mental health Data presented as mean 6 standard error of mean. *P < Idiopathic/iatrogenic group: n 5 16/101. Idiopathic/iatrogenic group: n 5 17/100. Idiopathic/iatrogenic group: n 5 17/103. CT 5 cricothyroid muscle; NGGA 5 normalized glottal gap area; SF-36 5 Short Form-36 Health Survey quality-of-life questionnaire; TA-LCA 5 thyroarytenoid lateral cricoarytenoid muscle complex; VOS: Voice Outcome Survey. the idiopathic group and six in the iatrogenic group; voice acoustic analysis data were missing for seven in the iatrogenic group; and quality-of-life data were missing for four in the iatrogenic group. Only complete data were used for statistical analysis of each parameter. E365

5 TABLE II. Glottal Area, Voice Acoustic Analysis, Laryngeal Muscle Recruitment, and Quality of Life in Patients With Idiopathic and Iatrogenic Vocal Fold Paralysis With or Without CT Paralysis. Recruitment Analysis Idiopathic Group (n 5 8) Isolated TA Paralysis Iatrogenic Group (n 5 83) P Value Idiopathic Group (n 5 9) Both TA and CT Paralysis Iatrogenic Group (n 5 24) P Value Videolaryngostroboscopy Closed-phase NGGA Voice Acoustic Analysis Maximum phonation time (s) SZ ratio Fundamental frequency (Hz) Jitter (%) Shimmer (db) Harmonic-to-noise ratio Recruitment Analysis Lesion side of TA-LCA (turn/s) * * Normal side of TA-LCA (turn/s) * Turn ratio of TA-LCA Lesion side of CT (turn/s) Normal side of CT (turn/s) Turn ratio of CT Quality of Life VOS * SF-36 Vitality Physical functioning * Bodily pain * * General health perceptions * Physical role functioning * Emotional role functioning * Social functioning * Mental health Data presented as mean 6 standard error of mean. *P < CT 5 cricothyroid muscle; NGGA 5 normalized glottal gap area; SF-36 5 Short Form-36 Health Survey quality-of-life questionnaire; TA-LCA 5 thyroarytenoid-lateral cricoarytenoid muscle complex; VOS: Voice Outcome Survey. Patient demographics, etiology of vocal fold paralysis, paralysis side, duration from disease onset to LEMG (disease-onset duration), clinical assessment, and quality of life are listed in Table I. There were no significant differences in age and sex between the two groups. Thyroid/parathyroid surgery, esophageal surgery, and lung/ mediastinal surgery were the major causes of iatrogenic vocal fold paralysis. Left-sided paralysis of the vocal fold was commonly seen in both the idiopathic and iatrogenic groups. There was no significant difference in the proportion of left-sided paralysis between the idiopathic and iatrogenic groups (P ). Videolaryngostroboscopy The NGGA did not differ between the two groups (Table I), indicating that glottal area was similar in idiopathic and iatrogenic vocal fold paralyses. Voice Acoustic Analysis Comparison of the parameters measured by voice acoustic analysis showed no differences between the groups in terms of maximal phonation time, SZ ratio, functional frequency, jitter, shimmer, or harmonic-tonoise level (Table I), indicating similar voice characteristics. Laryngeal Electromyography and Quantitative Analysis Laryngeal electromyography showed that 33 had combined TA LCA and CT muscle paralysis. The proportion of both superior and recurrent laryngeal neuropathies in the idiopathic group (9 of 17) was significantly higher than in the iatrogenic group (24 of 107) (P <.001), indicating a predominance of two-nerve injury in the idiopathic group. E366

6 We initially assigned patients to the idiopathic or iatrogenic group regardless of their CT muscle involvement. The turn frequency for the TA-LCA muscle complex in the lesioned side was significantly higher in the idiopathic group ( ) compared with the iatrogenic group ( ) (P 5.003), but there was no difference between the groups for the TA-LCA muscle complex in the normal side. The idiopathic group also had a higher turn ratio compared with the iatrogenic group, although the difference was not significant (P 5.084) (Table I), indicating that the level of denervation in the idiopathic group was relatively minor. There was no difference in turn frequency for the CT muscle in the lesioned or normal side, or in turn ratio between the two groups (all P >.05). Quality of Life: Voice Outcome Survey and Short Form-36 Compared with the iatrogenic group, the idiopathic group had higher scores in VOS and SF-36 domains of physical functioning, bodily pain, general health perceptions, physical-role functioning, emotional-role functioning, and social functioning than the iatrogenic group (all P <.05) (Table I), but no differences in the SF-36 domains of vitality and mental health (both P >.05). These results indicated that patients with unilateral IVFP had higher voice-related and general qualities of life than those with iatrogenic vocal fold paralysis. Subgroup Analysis We also performed subgroup analysis by further dividing the patients into those with isolated TA LCA muscle complex paralysis or combined TA LCA and CT muscle paralysis (Table II). Only the turn frequency of the lesioned-side TA differed between the idiopathic ( ) and iatrogenic ( ) groups (P 5.048) in the subgroup with isolated TA LCA muscle complex paralysis. In the subgroup with combined TA LCA and CT muscle paralysis, the turn frequency of lesion-sided TA between the idiopathic ( ) and iatrogenic ( ) groups was also different (P ). Similarly, the difference in turn frequency of the lesioned-side CT muscle between the idiopathic ( ) and iatrogenic ( ) groups was almost significant (P 5.055), and the turn frequency of the normal-sided TA differed significantly between the idiopathic ( ) and iatrogenic ( ) (P 5.043) groups. Subgroup analysis thus indicated that the level of denervation was relatively minor in the idiopathic group, regardless of involvement of the CT muscle. DISCUSSION Unilateral IVFP has a clinical presentation, with less impairment of laryngeal recruitment and also less impact on patients quality of life than iatrogenic vocal fold paralysis. To the best of our knowledge, only two studies have used LEMG to characterize IVFP to date, 9,25 and no study has applied quantitative LEMG to IVFP. Conventional LEMG visually identifies the electrodiagnostic signs of denervation (fibrillation, positive sharp wave), reinnervation (polyphasic or nascent motor unit potential), and motor-unit recruitment. 26,27 Recruitment is a reliable parameter for detecting neuropathy 27 and is significantly related to vocal fold motion, 28,29 but it is difficult to quantify objectively by conventional LEMG. It is therefore necessary to use quantitative LEMG to assess the level of denervation for investigational purposes. Idiopathic vocal fold paralysis accounts for approximately 12% to 42% of patients with vocal fold paralysis. 2 Most IVFP presents as unilateral paralysis. 8 Bilateral IVFP is relatively rare, 1,5 as supported by the present study. Left IVFP was also more common than right IVFP in this study, in accordance with the results of a previous study. 8 A more frequent involvement of the left vocal fold may be related to the longer, left RLN. 1,8 A small proportion (3% 12%) of patients with an initial diagnosis of IVFP are subsequently found to have malignances at long-term follow-up. 7,10,30 Ward and Berci 7 suggested that IVFP involving both the SLN and the RLN may be accounted for by lower motor nuclear lesions. Idiopathic vocal fold paralysis involving isolatedly the RLN while sparing the SLN should thus be carefully worked up in case of the presence of a tumor, with a suggested follow-up period of 2 to 5 years. 7,10,30 In our study, the proportion of patients with both SLN and RLN neuropathies in the idiopathic group was significantly higher than in the iatrogenic group, in accordance with Ward and Berci. 7 The positive predictive value of an initial working diagnosis of unilateral IVFP with isolated RLN neuropathy, as well as the existence of subclinical tumor, should also be determined in future studies. Laryngeal electromyography is helpful in locating the lesion and differentiating between lower motor neuron, peripheral neuropathy, and mechanical disorder. 31 It is also valuable in predicting outcome of vocal fold paralysis. 28,32,33 Furthermore, LEMG could show the activity of laryngeal muscles, further showing distinct patterns in unilateral vocal fold paralysis caused by difference etiologies. 19 Based on our results, most unilateral IVFP had concurrent SLN and RLN involvement and better turn frequencies of TA-LCA muscles. Quantitative LEMG had been used to differentiate between a paralytic and normal TA LCA muscle complex 13 and to predict the outcome of vocal fold paralysis. 11,12 The results of the present study showed higher quantitative recruitment in the lesioned-side TA LCA muscle complex in the idiopathic group compared with the iatrogenic group, which finding remained robust even after performing subgroup analysis to exclude confounding factors. This implies that unilateral IVFP occurs via a pathophysiological mechanism that leaves some innervations partially intact. However, in terms of outcome prediction, conventional LEMG offers qualitative data and is inadequate for classifying the severity of neuropathy in all cases of vocal fold paralysis. 17,28 Combining conventional and quantitative LEMG for outcome E367

7 prediction provided higher positive (100%) and negative predictive values (90%) and higher accuracy (91%). 12 The idiopathic group had better quality of life, which could be accounted for by its disease course. Patients with iatrogenic vocal fold palsy are more likely to have comorbidities such as tumors and to have undergone surgery that injured their laryngeal nerve, which complex situations may further affect their quality of life. Our study was limited by the fact that the patients had a wide variety of disease durations, which could affect disease symptoms and LEMG findings given that reinnervation occurred gradually over several months following nerve injury. 2,9,12 The sample size was too small to allow us to analyze the results of quantitative LEMG in differently timed sequences; further studies are needed to analyze the course of reinnervation in patients with unilateral IVFP. Additionally, some patients with IVFP may recover spontaneously before visiting an otolaryngologist 2,25 ; thus, the short-term prognosis of IVFP remains unclear. The complete-motion recovery of IVFP diagnosed in hospital is about 36%, and complete voice recovery is about 52%. 2 The present study recruited patients with unilateral IVFP lasting longer than 3 months; thus, some unilateral IVFP may have been excluded due to early recovery. We were therefore unable to determine the full recovery rate for vocal fold motion, and the follow-up period was too short to observe the long-term motion-recovery rate. CONCLUSION Unilateral IVFP, compared with iatrogenic vocal fold paralysis, has less denervation, better voice, and better quality of life. Quantitative LEMG can measure the severity of neuropathy and locate the extent of nerve involvement in patients with unilateral IVFP. 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