Cricothyroid Muscle Dysfunction Impairs Vocal Fold Vibration in Unilateral Vocal Fold Paralysis

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1 The Laryngoscope VC 2013 The American Laryngological, Rhinological and Otological Society, Inc. Cricothyroid Muscle Dysfunction Impairs Vocal Fold Vibration in Unilateral Vocal Fold Paralysis Yu-Cheng Pei, MD, PhD; Tuan-Jen Fang, MD; Hsueh-Yu Li, MD; Alice M. K. Wong, MD Objectives/Hypothesis: The relevance of the cricothyroid (CT) muscle in patients with unilateral vocal fold paralysis (UVFP) remains controversial. To clarify the functional significance of the CT muscle in patients with UVFP, the confounding effect of the severity of recurrent laryngeal nerve injury should be taken into consideration. In the present study, quantitative laryngeal electromyography (LEMG) was used to measure the severity of paralysis of the thyroarytenoid-lateral cricoarytenoid (TA-LCA) muscle complex to allow the functional contribution of the CT muscle to be determined. Study Design: Cross-sectional study performed in an otolaryngology outpatient clinic. Methods: Thirty-one patients with a main diagnosis of UVFP were recruited. The main outcome measures included LEMG examination, quantitative LEMG analysis of the TA-LCA muscle complex, UVFP-related quality-of-life questionnaire (Voice Outcome Survey [VOS]), voice acoustics analysis, videolaryngostroboscopy, and general quality-of-life questionnaire (Short Form-36 Health Survey [SF-36]) assessments. Results: The vocal cord position did not differ between patients with and without CT muscle impairment. Patients with both TA-LCA and CT paralysis showed poorer vocal fold vibration (P 5.048) and higher fundamental frequency (P 5.02), and the VOS and SF-36 were both poorer compared with patients with only TA-LCA paralysis. Conclusions: Although the vocal cord position was not influenced by CT muscle function, coexisting CT muscle paralysis may damage the voice by impairing vocal fold vibration in UVFP patients. Key Words: Laryngeal electromyography, unilateral vocal fold paralysis, superior laryngeal nerve, voice, quality of life.. Level of Evidence: 4. Laryngoscope, 124: , 2014 INTRODUCTION The thyroarytenoid-lateral cricoarytenoid (TA-LCA) muscle complex is innervated by the recurrent laryngeal nerve (RLN) and adducts the vocal folds during phonation. Accordingly, neuropathy of the RLN causes weakness of the TA-LCA muscle complex and thus impairs functional vocal fold adduction. The cricothyroid (CT) muscle is controlled by the external branch of the superior laryngeal nerve (esln), and increases the tension of the vocal folds during phonation. Injury of the esln would thus impair control of voice frequency by limiting the ability of the CT muscle to tighten the vocal folds. From the Department of Physical Medicine and Rehabilitation (Y.-C.P., A.M.K.W.), School of Medicine (Y.-C.P., T.-J.F, H.-Y.L.), and Department of Otolaryngology Head and Neck Surgery (T.-J.F, H.-Y.L.), Chang Gung Memorial Hospital, Taipei, Taiwan, R.O.C. Editor s Note: This Manuscript was accepted for publication May 9, Presented at the 8th East Asia Conference on Phonosurgery, Jeju Island, Korea, November 30 December 1, This work was supported by a National Science Council grant (NSC B ). The funder had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors have no other funding, financial relationships, or conflicts of interest to disclose. Y.-C.P. and T.-J.F. conceived and designed the experiments, performed the experiments, and wrote the manuscript. All of the authors contributed materials and analysis tools. Send correspondence to Tuan-Jen Fang, MD, No. 5 Fushing St., Taoyuan 333, Taiwan. fang3109@cgmh.org.tw DOI: /lary The observation that patients with neuropathy involving both the RLN and esln tended to have a wider glottal gap was thought to indicate that lesions of the CT muscle may affect the vocal fold position in patients with unilateral vocal fold paralysis (UVFP). 1 3 After the introduction of laryngeal electromyography (LEMG), Koufman et al. 4 compared the vocal fold positions in patients with UVFP by categorizing the arytenoid position as paramedian, intermediate, or lateralized and showed that involvement of the esln did not alter vocal fold position. 4 However, the exact functional role of the esln in patients with UVFP remains unclear. The relevance of CT muscle function in UVFP might depend on the influence of the TA-LCA complex. However, because the severity of TA-LCA damage may differ among patients, the real impact of the CT muscle is unknown. LEMG 3,5 8 can provide valuable information about the spatial extent and cause in patients with impaired unilateral vocal fold movement. LEMG is mainly used for diagnostic confirmation and for predicting prognosis (e.g., patients showing minimal or no motor unit recruitment tend to have a poor prognosis) Conventional LEMG has been used qualitatively to assess if motor unit recruitment is normal. However, quantitative LEMG was used to evaluate the function of the adductor complex in patients with UVFP by Statham et al. 13 Quantitative LEMG can thus be utilized to give objective measurements of the interference pattern and the severity of neuromuscular impairment of the TA-LCA muscle complex. 201

2 In the present study, we investigated if the involvement of the esln in patients with UVFP further impaired neuromuscular control of their vocal folds, thus affecting the dynamic motion of the vocal folds during phonation, voice acoustics, and quality of life. We also used quantitative LEMG analysis to determine the degree to which muscles were denervated by analyzing the maximal turn frequency of the TA-LCA muscle complex. 11,13,14 These comprehensive assessments will help to demonstrate the differences in disease presentation and functional impairment between UVFP patients with and without concurrent involvement of the esln. MATERIALS AND METHODS Human Subjects We recruited patients from the otolaryngology outpatient clinic at a medical center from September 2011 to June Inclusion criteria were adult (>18 years old) patients diagnosed with UVFP and confirmed by laryngoscopy. Exclusion criteria were bilateral vocal fold paralysis confirmed by denervation changes at the bilateral TA-LCA complex observed by LEMG; contraindications for needle electromyography (EMG); or history of interventions to correct the paralyzed vocal fold position, such as intracordal injection, laryngoplasty, or laryngeal framework surgery. 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 LEMG with quantitative analysis, videolaryngostroboscopy, Voice Outcome Survey (VOS) questionnaire, voice acoustic analysis, and Short Form-36 Health Survey (SF-36) quality-of-life questionnaire. These assessments were performed within 2 weeks of the day of LEMG assessment. LEMG Examination The standard protocol for LEMG was performed by a board-certified otolaryngologist (T.-J.F.) and physiatrist (Y.-C.P.). The patients were seated on an examination chair specifically designed for LEMG examination, with their neck extended and head supported by an adjustable neck-head rest. To avoid discomfort, 1 to 2 ml of 2% lidocaine hydrochloride was injected into the subcutaneous tissue at the LEMG needle-insertion sites. LEMG signals were obtained using a concentric needle electrode with the surface-ground electrode adhered to the forehead. We examined the EMG signals on bilateral TA-LCA muscle complexes and CT muscles. With the concentric needle electrode in the TA-LCA muscle complex, the patient was asked to produce three series of /e/ sounds at three different intensities (low, moderate, and highest possible), with each /e/ lasting at least 400 ms and each inter-/e/ interval lasting about 200 ms. To evaluate CT function, the patients were asked to produce a glissando upward /e/ at normal loudness. For each test, we initially observed insertional activity and spontaneous activity. We then performed semiquantitative motor unit analysis and recruitment analysis, specifically when the rise time of a motor unit action potential was <0.6 ms, indicating a close proximity to the recorded motor unit. A Nicolet Viking Select (Cardinal Health, Dublin, OH) was used with its band-pass filter set between 20 Hz and 10 khz. Abnormal LEMG was defined as the existence of spontaneous activities (such as fibrillation, positive sharp wave, and complex repetitive discharge), >30% polyphagia, or decreased interference pattern (reduced, discrete, or no interference pattern). Motor unit recruitment tracings were recorded with sweep speeds of 10 ms per division and a gain of 200 lv per division. Quantitative LEMG Analysis We developed a Matlab-based program to analyze raw EMG data. We first binned the raw EMG data in each 200-ms epoch. An automatic algorithm was used to localize the timing of each turn and its amplitude. 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 peaks inherent to noise. Turn frequency was computed for each epoch as the number of turns divided by epoch duration, and mean turn amplitude was computed as the mean of the absolute turn-amplitude values. For the TA-LCA muscle complex, we averaged the turn frequencies for the epochs whose turn frequency ranked among the top three epochs to yield a peak frequency turn index.. 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) and yielded the normalized glottal gap area (NGGA) following Omori et al. s method, 15 as described in Equation (1): Glottal gap area NGGA 5 Membranous vocal fold length units (1) Glottal gap area represents the image area in square pixels within the glottal area identified using the segmentation process, and membranous vocal fold length represents the distance expressed in pixel length from the anterior commissure to the tip of the membranous vocal process. The glottal gaps were measured in both maximally open and closed phases during vocal fold vibration to yield open-phase and closed-phase NGGAs, respectively (Fig. 1A,B). The dynamic NGGA was then computed using Equation (2): Dynamic NGGA 5 ðopen-phase NGGAÞ2 ðclosed-phase NGGAÞ (2) Voice Acoustic Analysis A certified speech pathologist recorded voice samples while the patient read a standard passage and then sustained a vowel in conversational pitch and loudness. The maximal phonation time (MPT) represented the duration a patient could sustain an /a/. A stable segment from the mid portion 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; Kay- PENTAX, Montvale, NJ) that yielded the fundamental frequency (F0), jitter (frequency perturbation), shimmer (perturbation of amplitude), and harmonic-to-noise (H/N) ratio. Finally, the patient produced each of a sustaining /s/ and /z/ as 202

3 Fig. 1. The measurement of normalized glottal gap area in the open phase (A) and closed phase (B) of phonation. In each subplot, the left inset illustrates the movie frame captured from the videolaryngostroboscopy and the right inset the pixels within the glottal gap area identified using a computer segmentation process. The membranous vocal fold length (L) is defined by the distance expressed in pixels from the anterior commissure to the tip of the membranous vocal process. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] long as possible, from which the S/Z ratio (S/Z) was computed as the ratio of /s/ and /z/ durations. 16 UVFP-Related Health: VOS The VOS developed by Gliklich et al. 17 is a 5-item survey that evaluates the physical and social problems induced by UVFP, 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 survey-validation process. 18 General Health: SF-36 The SF-36 is a widely used quality-of-life assessment tool that evaluates eight quality-of-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. 19,20 Statistical Analysis The patients were divided into two groups: the RLN and groups. 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 VOS), and v 2 tests for categorical data. Analysis of variance (ANOVA) was used to analyze the fundamental frequency obtained in acoustic analysis in a model using group and age as the two main factors, because age is known to affect fundamental frequency. Quantitative LEMG data were compared between lesioned and normal TA muscles using paired t tests. The level of significance was defined as P <.05. RESULTS We retrospectively reviewed 35 patients diagnosed with UVFP during the study period. Four patients were excluded: one because of no TA-LCA involvement (finally diagnosed as thyroarytenoid dislocation) and three because of bilateral TA-LCA involvement. A final list of 31 (15 male, 16 female) patients remained for data analysis. Among these 31 patients, 20 (65%) had unilateral TA-LCA involvement, 10 (32%) had unilateral TA-LCA muscle complex and CT muscle involvement with TA- LCA and CT involvement on the same side, and one (3%) had unilateral TA-LCA and bilateral CT involvement. Accordingly, these patients were categorized into two groups: the RLN group (20 patients) and the group (11 patients), according to the spatial extent of muscle involvement. The demographics of the two groups are shown in Table I. There were no significant differences in any characteristics between the two groups. The etiologies of UVFP included: esophageal surgery (26%), idiopathic origin (22%), thyroid surgery (19%), skull base surgery (13%), lung surgery (6%), and other (virus infection, subclavian surgery, and heart surgery) (13%) (Table II). Quantitative LEMG The raw EMG signals for a normal TA-LCA muscle complex when a sample patient produced a series of /e/ sounds at three different intensities are shown in Figure 2A. The mean turn amplitude of the lesioned and normal TA-LCA muscle complexes as a function of the turn frequency in multiple 200-ms epochs in this sample patient is shown in Figure 2B. Mean turn amplitude was positively correlated with turn frequency, and the peak frequency in the lesioned side was substantially lower than that in the normal side. 13 We then analyzed the peak frequencies and found that the peak frequency of the TA-LCA muscle complex in the lesioned side did not differ between the two groups (P 5.85) (Table III). Similarly, the peak frequency in the normal side did not differ between the two groups Parameter TABLE I. Demographic Data. RLN P Value Number Gender, M/F 10/10 5/6.81 Age, yr Disease duration, 10/10 8/3.28 <6 / >6, mo Paralysis side, R/L 7/13 2/9.43 Data are presented as mean 6 standard deviation or number. esln 5 external branch of the superior laryngeal nerve; F 5 female; L 5 left; M 5 male; R 5 right; RLN 5 recurrent laryngeal nerve. 203

4 Etiology TABLE II. Etiology of Unilateral Vocal Fold Paralysis. RLN Subtotal Esophageal surgery 4 (20%) 4 (36%) 8 (26%) Idiopathic 6 (30%) 1 (9%) 7 (22%) Thyroidectomy 4 (20%) 2 (18%) 6 (19%) Skull base surgery 1 (5%) 3 (27%) 4 (13%) Lung surgery 2 (10%) 0 (0%) 2 (6%) Other 3 (45%) 1 (9%) 4 (13%) Subtotal Data are presented as number (%). esln 5 external branch of superior laryngeal nerve; RLN 5 recurrent laryngeal nerve. Videolaryngostroboscopy Analysis of the glottal gap showed that closed-phase NGGA was smaller in the RLN ( ) than in the group ( ), though the difference was not significant (P 5.20). In contrast, the open-phase NGGA was larger in the RLN ( ) than in the group ( ), though again, the difference was not significant (P 5.21). However, dynamic NGGA, the difference between open- and closed-phase NGGAs, was significantly larger in the RLN ( ) than in the group ( ) (P 5.048) (Table III). These findings indicate that the RLN group had better neuromuscular control during phonation than the group, manifested by better vibration dynamics, a relatively narrower closed glottal gap, and a relatively wider open glottal gap. (P 5.49). These findings support the basic assumption that the severity was comparable between the two groups, and differences in other measurements were therefore not caused by different degrees of RLN damage in the two groups. UVFP-Related Health and Voice Acoustic Analysis The mean VOS score was higher in the RLN ( ) group compared with the group ( ) (P <.01) (Table III), indicating that the involvement of the esln in patients with UVFP further impaired their voice quality. We then performed voice acoustic analysis and found that the group ( Hz) had a higher fundamental frequency compared with the RLN group ( Hz), even after accounting for gender in an ANOVA model (P 5.02). This finding is reminiscent of the observation made by Roy et al., who showed that fundamental frequency increased after acute esln block using lidocaine. 21 Other voice parameters, including MPT (P 5.96), S/Z ratio (P 5.37), jitter (P 5.52), shimmer (P 5.48), and H/N ratio (P 5.54), did not differ between the two groups (Table III). General Health: SF-36 We compared quality-of-life domains measured by SF-36 between the two groups (Table IV). The group had relatively lower scores in role limitations due to physical health (P 5.03) and role limitations due to emotional problems (P 5.01) compared with the RLN group, and nonsignificantly lower scores in physical functioning (P 5.06), general health (P 5.13), and social functioning (P 5.06). Only the domains of bodily pain (score of 0 in both groups), vitality (P 5.52), and mental health (P 5.82) did not differ between the two groups. These results indicate that quality of life was more severely affected in patients in the group than in their RLN counterparts. Fig. 2. (A) The raw laryngeal electromyography (EMG) signals at the normal thyroarytenoid-lateral cricoarytenoid (TA-LCA) muscle complex during a task in which a sample patient with unilateral vocal fold paralysis produced a sustained /e/ at three different intensities. (B) The mean turn amplitude of the lesioned and normal TA-LCA muscle complexes as a function of the turn frequency in this sample patient. Each point on the scatter plot indicates the data computed from one 200-ms epoch. Mean turn amplitude was positively correlated with turn frequency, and the peak turn frequency in the lesioned side was substantially lower than that in the normal side. DISCUSSION The esln originates from the vagus nerve that arises from the nucleus ambiguus and leaves the skull base through the jugular foramen. 22 It splits into internal and external branches at the level of the thyrohyoid junction. Its external branch controls the motion of the CT muscle, whereas its internal branch penetrates into the thyrohyoid membrane to receive sensory inputs from 204

5 TABLE III. Comparison of Qualitative Laryngeal Electromyography, Anatomical, and Functional Outcomes Between s. N * All RLN P Value Peak frequency at lesion TA-LCA, turn/s 20/ Peak frequency at normal TA-LCA, turn/s 20/ Closed phase NGGA 20/ Open phase NGGA 20/ Dynamic NGGA 20/ VOS score 20/ Maximal phonation time, s 19/ S/Z ratio 18/ Fundamental frequency, Hz 19/ Jitter 18/ Shimmer 19/ H/N ratio 18/ Data are presented as mean 6 standard deviation or as the number of patients. *Number of patients in RLN group/ group. P <.05. Using gender as an independent variable in an analysis of variance model. esln 5 external branch of superior laryngeal nerve; H/N ratio 5 harmonic-to-noise ratio; NGGA 5 normalized glottal gap area; RLN 5 recurrent laryngeal nerve; S/Z ratio 5 ratio of /s/ and /z/ durations; TA-LCA 5 thyroarytenoid-lateral cricoarytenoid; VOS 5 Voice Outcome Survey. the upper larynx. UVFP can be caused by lower or higher laryngeal nerve lesions. The existence of different laryngeal and phonatory presentations between patients with RLN and those with both RLN and esln involvements highlights a longstanding controversy. In 1881, Semon proposed that the nerve fibers innervating vocal fold abductors were more sensitive to injury than those innervating adductors. Accordingly, in a progressive neuropathy, the vocal fold will first present in a median position and later in a lateralized position. 23 However, the Semon hypothesis was not compatible with most clinical observations that the vocal fold tends to move from lateral to median over time. To explain this discrepancy, the Wagner-Grossman hypothesis proposed that the intact CT muscle can maintain the vocal fold in the paramedian position in patients with RLN paralysis. 24 The hypothesis was supported by several observations. First, the paralysis or removal of the CT muscle could relieve the airway obstruction caused by bilateral RLN paralysis. 1,25,26 Second, Dedo s study in 1970 found that the site of laryngeal nerve injury related to CT function influenced the position of the vocal folds in patients with UVFP. 3 However, the Wagner-Grossman hypothesis was not supported by a majority of recent studies. In a case series with careful localization of the sites of nerve lesion, Woodson found that esln involvement in patients with UVFP did not induce statistically significant lateralization of the vocal fold. 27 Furthermore, several animal studies indicated that esln involvement does not affect the vocal fold position in acute 28 and chronic 29 settings. Based on an LEMG study, Koufman et al. 4 reported that vocal fold position would not be influenced by CT function in laryngeal paralysis. However, neither of these studies eliminated the influences of the RLN in patients with partial denervation or reinnervation. It is possible that the severity of RLN damage may differ among different groups or TABLE IV. Comparison of Quality-of-Life Domains Measured by the Short Form-36 Health Survey Between s. All RLN group P Value Physical functioning Role limitations due to physical health * Bodily pain NA General health Vitality Social functioning Role limitations due to emotional problems * Mental health Data are presented as mean 6 standard deviation. *P <.05. esln 5 external branch of superior laryngeal nerve; NA 5 not applicable; RLN 5 recurrent laryngeal nerve. 205

6 study cohorts. Thus, to identify the role of the CT muscle in UVFP, it is necessary to control the influences of these confounders. Quantitative EMG is an established method that provides parametric measurement of muscle recruitment. It has recently been adopted for studying the TA- LCA muscle complex by Statham et al. 13 They found that turn frequency could be used to differentiate between healthy and paralyzed TA-LCA muscle complexes. The use of quantitative LEMG has two advantages. First, it is objective and can be executed automatically by computer software to avoid inter-rater variance. Second, it offers a continuous value for LEMG recruitment, so it lacks the problems associated with ceiling or floor values and could thus detect minute changes in recruitment that could not be detected using traditional discrete scores. The present study used quantitative LEMG analysis to quantify the severity of neuropathy involving the TA-LCA muscle complex. The turn frequencies of the TA-LCA muscle complex measured by quantitative LEMG were similar in both groups, suggesting that the residual innervation from the paralyzed RLN was similar. After controlling for the confounding effect associated with different severities of RLN injury, the influence of CT dysfunction in patients with UVFP can be elucidated. The results of the present study were in accord with those of Woodson 27,29 and Koufman 4 in that the vocal cord position was not influenced by the CT muscle in UVFP. Quantitative measurements of the glottal gap during phonation (i.e., comparison of open-phase NGGA and closed-phase NGGA between groups) showed no significant difference between those with and without CT muscle paralysis. The phonatory vocal fold position might be determined by multiple factors such as residual or regenerated innervation, compensation from the healthy side, or simultaneous contraction of antagonistic muscles. 24 However, as observed in the present study, paralysis of the CT muscle can affect the dynamic glottal gap areas between phonatory phases, indicating relatively poor vibration dynamics during phonation. Laryngopharyngeal sensation was reported to be decreased in 83% of patients with UVFP and in 35% of patients demonstrating absence of the laryngeal adductor reflex. 30 One limitation of the present study was the lack of assessments of sensory function and extralaryngeal motor function governed by the upper vagus branches. Indeed, sensation effects (such as laryngeal hypoesthesia) and extralaryngeal motor effects (such as palate and pharynx weakness) could contribute to the impairments observed in the patient-completed instruments, including the VOS and SF-36. Further studies should focus on the functional impact of sensory impairment in patients with UVFP. CONCLUSION Among patients with UVFP, patients with combined CT muscle dysfunction demonstrated relatively profound speech impairment evidenced by reduced vocal fold vibration and higher modal fundamental frequency. These impairments may further limit the patient s quality of life. Acknowledgments The authors thank Chia-Fen Chang for collecting the data. BIBLIOGRAPHY 1. Grossman M. Contribution to the mutual functional relationships of the muscles of the larynx. Arch Laryngol Rhinol 1906;18: Faaborg-Andersen K. The position of paretic vocal cords. Acta Otolaryngol 1964;57: Dedo HH. The paralyzed larynx: an electromyographic study in dogs and humans. Laryngoscope 1970;80: Koufman JA, Walker FO, Joharji GM. The cricothyroid muscle does not influence vocal fold position in laryngeal paralysis. Laryngoscope 1995;105: Faaborg-Andersen K, Buchthal F. 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