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Nonselective Laryngeal Reinnervation versus Type 1 Thyroplasty in Patients with Unilateral Vocal Fold Paralysis: A Single Tertiary Centre Experience
ARTICLE IN PRESS
Nonselective Laryngeal Reinnervation versus Type 1 Thyroplasty in Patients with Unilateral Vocal Fold Paralysis: A Single Tertiary Centre Experience Azlina Ab Rani, Mawaddah Azman, Muhammad Azhan Ubaidah, Mohd Razif Mohamad Yunus, Abdullah Sani, and Marina Mat Baki, Cheras, Malaysia Summary: Objective. This study compared the voice outcomes of selected patients with unilateral vocal fold palsy (UVFP) who underwent either nonselective laryngeal reinnervation (LR) or Type 1 thyroplasty (thyroplasty) in a Malaysian tertiary centre using multidimensional voice assessments. Participants. The study included 16 patients with UVFP who underwent either LR (9 patients) or thyroplasty (7 patients) between 2015 and 2018 who fulfilled the inclusion criteria. Main Outcome Measures. The outcomes were measured subjectively and objectively with: (1) voice handicap index-10 (VHI-10- Malay version); (2) auditory perceptual evaluation using the breathiness component of Grade, Roughness, Breathiness, Asthenia, Strain scale; (3) maximum phonation time (MPT); and (4) acoustic analysis (jitter%, shimmer%, and NHR) using OperaVOXTM. The outcomes were measured at baseline, 6 and 12-months postoperative. The comparison of outcomes between pre and postoperative of each group was evaluated using one-way ANOVA test. Mann-Whitney test was used to compare the outcomes between the two groups. Results. Comparison of each group at different time points showed significant improvement of VHI-10 and MPT of LR group between baseline and 12 months (P ≤ 0.05) whereas, the improvement in thyroplasty group was observed at all time points (P ≤ 0.05). When comparing between the two groups at 12 months, the VHI-10 and MPT was significantly better in the LR group than thyroplasty group with P = 0.004 and P = 0.001 respectively. Other outcome measures did not reveal significant difference between the two groups. Conclusion. This observational study showed that LR may be better than thyroplasty in improving VHI-10 and MPT in selected patients with UVFP. Key Words: Vocal fold−Paralysis−Thyroplasty−Laryngeal reinnervation.
INTRODUCTION Unilateral vocal fold palsy (UVFP) occurs as a result of insults or injuries to the recurrent laryngeal nerve (RLN). One of the common causes of UVFP is surgical complications (iatrogenic) which can be further divided into occurrence during the head, neck and thoracic procedures.1 Patients with UVFP frequently complain of hoarseness with or without aspiration symptoms. The severity of the hoarseness would usually depend on the phonatory gap contributed by the position of the paralysed vocal fold, presence of atrophy as well as the arytenoid position.2 A big phonatory gap causes breathy and an easily fatigued voice due to glottis insufficiency.3 This voice abnormality affects the quality of life especially in those with a high voice demand, making voice rehabilitation pertinent.4 Conventionally, voice therapy is the first line of treatment while waiting for the RLN function to recover within 6 months.5 However, there is a recommendation for early temporary medialisation that may give a rapid and improved voice outcome.6 Patients who persist to have voice issues Accepted for publication September 26, 2019. From the Faculty of Medicine, Universiti Kebangsaan Malaysia Medical Centre, Cheras, Kuala Lumpur, Malaysia. Address correspondence and reprint requests to Marina Mat Baki, Department of Otorhinolaryngology, Universiti Kebangsaan Malaysia Medical Centre, Jalan Yaacob Latiff, Bandar Tun Razak, 56000 Cheras, Kuala Lumpur, Malaysia. E-mail: [email protected] Journal of Voice, Vol. &&, No. &&, pp. &&−&& 0892-1997 © 2019 The Voice Foundation. Published by Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jvoice.2019.09.017
even after 6 months of the RLN nerve insult may be offered other surgical interventions such as Type 1 thyroplasty, with or without arytenoid adduction, as well as nonselective laryngeal reinnervation.7 To the best of our knowledge, there is a still ongoing research on the best surgical options to improve the glottal function in chronic UVFP.8 Nonselective laryngeal reinnervation is a relatively new surgical procedure in South East Asia. The present study was aimed to compare the voice outcomes of selected patients with UVFP who underwent either nonselective laryngeal reinnervation (LR) or Type 1 thyroplasty (thyroplasty) in a Malaysian tertiary centre using multidimensional voice assessments.
MATERIALS AND METHODS This investigation was an observational study among patients with UVFP who had undergone either nonselective LR or a type 1 thyroplasty at Universiti Kebangsaan Malaysia Medical Centre from 2015 to 2018, performed by multiple surgeons (three surgeons). The nonselective laryngeal reinnervation was mainly performed by MMB, while the type 1 thyroplasty was performed by either MMB, MA or AS. A retrospective analysis of longitudinal data was done to evaluate the voice outcomes at baseline, 6 and 12 month postsurgical intervention.
ARTICLE IN PRESS 2 Patients between the ages of 18 to 60 years old with a duration of UVFP within 36 months upon surgical intervention as well as have completed a minimum of 12 months postoperative assessment was included in this study. The exclusion criteria were patients with concomitant other lower cranial nerve palsies, severe cardiopulmonary diseases, high vagal paralysis or duration of UVFP of more than 3 years. SURGICAL TECHNIQUE Type 1 thyroplasty (thyroplasty) The patient was positioned in the supine position and local anaesthesia was infiltrated. A transverse skin incision was made over the thyroid cartilage followed by an elevation of the platysma. The strap muscles attached to the ipsilateral thyroid cartilage lamina were then released and the outer perichondrium was elevated. A window was then created using a cutting burr size 4.0 at the estimated level of the vocal cord, which is halfway between the thyroid notch and lower border of the thyroid cartilage (imaginary line). This thyroid window was routinely performed superior to the thyroid tubercle in an ovoid shape and below the imaginary line, whereby the largest axis measured 6 to 7mm and the distance from the middle ranges from 13 to 17mm.9 The intact inner perichondrium was then elevated anteriorly, inferiorly, and posteriorly to create pockets in the paraglottic space where the polytetrafluoroethylene ribbon implant was inserted. The adequacy of the medialisation was determined endoscopically as well as through the patient’s ability in counting 1 to 10 in a single breath. Haemostasis was then secured and the wound was closed in layers.
Nonselective laryngeal reinnervation (LR) This surgical technique used in this study was described by Crumley,10 with slight modification from Wang et al.5 A horizontally oblique incision was made at the mid-thyroid cartilage level. The fascia between the strap muscles and the sternocleidomastoid muscles was opened to identify the ansa cervalis nerve superficial to the internal jugular vein. The main, sternohyoid or sternothyroid branch of the ansa cervicalis was identified and dissected to its termination in the muscle. The RLN was then identified at the tracheo-oesophageal groove. In post-thyroidectomy cases, the RLN was identified by doing an intralaryngeal dissection, whereby the nerve was found a few millimetres medial to the cricothyroid joint, overlying the posterior cricoarytenoid muscle. In intraoperative thyroidectomy cases where the RLN was accidentally transected, the distal stump of RLN was repaired to the ansa cervicalis. If the proximal part of the RLN was identified and tension free repair was possible, end-to-end neurorrhaphy was performed instead. The ansa cervicalis (proximally) and RLN (distally) were transected, retaining sufficient length for a tension free neurorrhaphy which was then performed using an operating microscope and 9/0 ethilon sutures, reinforced by fibrin glue. Temporary augmentation of the paralysed
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vocal fold was done by injecting hyaluorinic acid endoscopically in the same setting. VOICE ASSESSMENT Subjective evaluation Patients’ voice-related, self-reported outcomes were evaluated using the local language of voice handicap index-10 (malayVHI-10: mVHI-10).11,12 These questionnaires were filled in by the patients to determine how badly the voice disorder caused by UVFP has affected their lives. Perceptual evaluation by a laryngologist was done using the Grade, Roughness, Breathiness, Asthenia, Strain (GRBAS) scale as proposed by Hirano et al.13 In the current study, breathiness component of the GRBAS scale was documented as proposed by Mattei et al.14 Objective evaluation Objective evaluation of voices was done by performing acoustic analysis and measuring maximum phonation time (MPT). Acoustic analysis is noninvasive computer software that measures the quality of recorded voices. It was performed using OperaVOXTM (On Person RApid VOice eXaminer), portable voice analysis software running on iPod touch 6th generation (Apple, USA) to measure the fundamental frequency (F0), jitter % (cycle-to-cycle variation in pitch), shimmer % (cycleto-cycle variation in amplitude), and noise-to-harmonic ratio (NHR).15 MPT was used to assess the glottis efficiency by measuring the longest duration (seconds) of the patients’ ability to sustain a phonation /a/. STATISTICAL ANALYSIS The comparison of outcomes between pre- and postoperative of each group was evaluated using the one-way ANOVA test. For comparison of outcomes between both groups at 12 months postoperative, the Mann-Whitney test was used. P value ≤ 0.05 was considered to be statistically significant. RESULTS Demography A total of 31 patients with UVFP were identified for this study, whereby 10 patients underwent LR and 21 patients underwent thyroplasty. Among the 31 patients, 16 patients were included in the present study according to the inclusion and exclusion criteria. For the LR group, the mean age was of 41.4, ranging from 28 to 59 years old (8 females and 1 male). The aetiologies were iatrogenic (thyroidectomy) except one patient (old left upper lobe pulmonary tuberculosis). Three patients had the LR in the same setting as a thyroidectomy. Therefore, these three patients had normal voice parameters at baseline (preoperative). Out of 14 patients who were excluded in the thyroplasty group, four patients had the duration of palsy for more than 3 years, two had concurrent lower cranial nerve palsies,
ARTICLE IN PRESS Azlina Ab Rani, et al
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Nonselective LR vs Type 1 Thyroplasty in Patients with UVFP
TABLE 1. Summary of the Demography of the Patients Included for Review Nonselective Laryngeal Reinnervation (n = 9) Age Gender
Mean (SD) 44.29 (13.70)
Min, Max 28, 59
Mean (SD) 44.43 (10.05)
Min, Max 33, 60
Male
Female
Male
Female
1
Duration of palsy (Mean), months Aetiology
Type I Thyroplasty (n = 7)
8 0.4 Iatrogenic: 88.9%% (n = 8), Lobar tuberculosis: 0.11%% (n = 1)
three had a severe cardiopulmonary disease, three were exceeding the age limit and two had incomplete data. One patient was excluded from the LR group as the LR was performed in the same setting as vagal paraganglioma excision that resulted in a high vagal paralysis and multiple lower cranial nerve paralysis. For the thyroplasty group, the mean age was of 44.4, ranging from 33 to 60 years old. Six patients were female and one patient was male. The aetiologies were iatrogenic 71.4% (n = 5), neck trauma 0.14% (n = 1) and thyroid carcinoma 0.14% (n = 1). Simple t test was performed and noted that the age distribution for both groups was not statistically significant (P = 0.982). The patients’ demographic data are summarized in Table 1. Subjective evaluation (VHI-10 and breathiness component of the GRBAS scale) For the LR group, the mean (standard deviation [SD]) of VHI-10 at baseline was 18.57 (18.08). At 6 and 12 months postoperatively, the VHI-10 was of 8.43 (7.25) and 1.57 (2.572), respectively. The breathiness of the GRBAS scale percentage for a score of two or more (moderate to severe) at baseline was 71.4% while at 6 and 12 months were both 0%. However, when comparing the breathiness percentage value in both groups, it was not statistically significant, indicating both groups have near-normal voice perception. For the thyroplasty group, the mean (SD) of VHI-10 at baseline was 31.29 (3.35). At 6 and 12 months postoperatively, they were of 16.86 (11.64) and 10.29 (5.88), respectively. The breathiness of the GRBAS scale percentage for a score of two or more at baseline was 85.71% and at 6 and 12 months were 0% and 14.29%, respectively. Objective evaluation (MPT and acoustic analysis) For the LR group, the mean (SD) of MPT and acoustic analysis which comprises jitter, shimmer, and NHR were of 11.58 (4.88), 2.24 (2.06), 8.11 (5.01), and 0.32 (0.53), respectively. At 6 and 12 months, the values were of 15.21 (7.77) and 15.29 (5.82) for MPT; 1.77 (1.76) and 1.20 (0.76) for
1
6 9.1 Iatrogenic: 71.4% (n = 5), Neck trauma: 0.14% (n = 1), Thyroid carcinoma: 0.14% (n = 1)
jitter; 6.28 (3.77) and 5.97 (1.92) for shimmer; and 0.16 (0.25) and 0.06 (0.11) for NHR, respectively. For the thyroplasty group, the mean (SD) of MPT and acoustic analysis were of 4.79 (1.95), 6.08 (2.57), 9.27 (6.66) and 0.81 (0.86), respectively. At 6 and 12 months, the values were of 7.37 (1.59) and 8.70 (0.87) for MPT; 3.70 (1.56) and 3.18 (2.10) for jitter; 8.05 (4.25) and 8.23 (4.73) for shimmer; and 0.21 (0.38) and 0.29 (0.46) for NHR, respectively. Comparison between pre- and postoperative outcomes of each group The multidimensional voice outcomes were compared between preoperative and postoperative at different time points. For the LR group, comparison of VHI-10 showed a significant improvement between the baseline and 12 months postoperative (P = 0.038). (Figure 1). As for the thyroplasty group, the VHI-10 was significantly improved at 6 months (P = 0.036) and 12 months (P = 0.001) when compared to the baseline. (Figure 2). There were no significant changes of MPT between the baseline when compared with 6 months
FIGURE 1. One-way ANOVA test for Voice Handicap Index-10 (VHI-10) score of the nonselective laryngeal innervation group over 12 months from the baseline which showed significant improvement. **P ≤ 0.05.
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Thyroplasty
VHI-10 Score
40 30 20 10
6
B
as
el
in e M on 12 th s M on th s
0
Time FIGURE 2. One-way ANOVA test for Voice Handicap Index-10 (VHI-10) score of the thyroplasty group over 12 months from the baseline which showed significant improvement. **P ≤ 0.05. (P = 0.219) and 12 months (P = 0.078) postoperative in the LR group. (Figure 3). For the thyroplasty group, the MPT was significantly increased when comparing the baseline to 6 months (P = 0.04) and 12 months (P = 0.001) postoperative (Figure 4). Comparison at 12 months between 2 groups Comparison of voice parameters between the LR and the thyroplasty group showed that both VHI-10 was better and MPT was longer in the LR (P = 0.001) than the thyroplasty group (P = 0.004 and P = 0.001 respectively). There was no significant difference between both groups with regards
FIGURE 3. One-way ANOVA test for assessing maximum phonation time (MPT) of the nonselective laryngeal innervation group over 12 months which showed no significant difference. **P > 0.05.
FIGURE 4. One-way ANOVA test for assessing maximum phonation time (MPT) of the thyroplasty group over 12 months from the baseline which showed significant improvement. **P ≤ 0.05.
to breathiness component of the GRBAS scale and acoustic analysis (jitter, shimmer and NHR). The summary is tabulated in Table 2. DISCUSSION Overview The need to restore normal or near-normal voice in patients with unilateral vocal fold paralysis is a challenge. Surgical procedures proposed to enable this have their own set of advantages and disadvantages. As to which of the surgical option has a better chance of improving UVFP patients’ voice is still a matter under consideration in a number of researches.16 Here, results from a series of cases that fit the inclusion criteria comparing the voice outcomes of 2 promising surgical techniques, nonselective laryngeal reinnervation or Type 1 thyroplasty, were reported.
Synopsis of key findings There was a significant improvement in the mean of VHI-10 in each group as well as the mean of MPT in the thyroplasty group when comparing pre- and postoperative outcomes. Significantly better VHI-10 and MPT scores were present in the LR group as compared to the thyroplasty group at 12 months postoperative. In the LR group, three patients
ARTICLE IN PRESS Azlina Ab Rani, et al
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Nonselective LR vs Type 1 Thyroplasty in Patients with UVFP
TABLE 2. The Mann Whitney U Test to Compare the Outcomes of Both Objective and Subjective Assessments in Both Groups at 12 Months Post-op Nonselective Laryngeal Reinnervation
Type 1 Thyroplasty
Outcome Measure
Mean (SD)
Median (IQR)
Mean (SD)
Median (IQR)
p Value
VHI-10 MPT Jitter Shimmer Noise-Harmonic Ratio
1.57 (2.57) 15.29 (5.87) 1.20 (0.76) 7.35 (2.23) 0.06 (0.11)
0.00 (0.00, 2.00) 14.30 (10.50, 16.50) 0.79 (0.70, 2.11) 7.07 (6.24, 9.98) 0.02 (0.01, 0.05)
10.29 (5.88) 8.70 (0.86) 3.18 (2.10) 8.22 (4.73) 39.34 (103.90)
10.00 (5.00, 13.00) 8.90 (7.60, 9.30) 2.16 (2.06, 5.77) 7.41 (5.14, 8.49) 0.06 (0.06, 0.14)
0.004* 0.001* 0.128 0.383 0.071
* p ≤ 0.05.
had nonselective reinnervation performed in the same setting as the iatrogenic transection of the RLN, thus the preoperative assessment of these patients’ voice was considered to be the baseline, revealing a completely normal voice. This may explain why the mean of VHI-10 and MPT at baseline was better in the LR than the thyroplasty group as well as the absence of a statistically significant improvement in MPT between baseline and 12 months postoperative. The breathiness component on the GRBAS scale percentage for a score of two or more (moderate to severe) in the LR group at baseline was 71.4% and improved to 0% after 12 months. This showed that at the beginning there were patients with a near-normal or normal voice in this group; the voice of all of the patients in this group improved to near normal or normal after 12 months. The breathiness component of the GRBAS scale percentage for a score of two or more for the thyroplasty group at baseline was 85.71%. This value showed an improvement of up to 6 months where the percentage was from 85.71% to 0%. However, for the subsequent 6 months, the percentage of patients with breathiness increased to 14.29%. The acoustic analysis parameters (jitter, shimmer and NHR) of both groups showed improvement between pre- and postoperative and were comparable between both groups at 12 months.
Comparison with previous studies Studies comparing LR with other recommended surgical intervention for UVFP was limited. In a large observational study, Wang et al5 compared the voice outcomes of 237 patients with UVFP who underwent LR with voices of 237 normal members of a similar population. The study demonstrated that the voices of UVFP patients who had undergone LR were similar to voices of healthy people. Although the comparison between both groups was made, the study did not evaluate the effectiveness of the two different surgical techniques to treat UVFP. A randomised controlled trial (RCT) was performed in the US by Paniello et al8 comparing LR and type I thyroplasty. The results documented that there was no significant difference of voice outcomes between the two groups. This may suggest that LR is as effective as thyroplasty in rehabilitating UVFP patients’ voices. However, it was suspended
prematurely with only 20% of subjects enrolled. Another similar study was planned by a UK group of researchers aiming to replicate and complete the RCT study accordingly. Predicaments in recruiting and randomizing were inherent in surgical trials due to the strong surgical preference of patients as well as surgeons. Therefore, a feasibility study was carried out first to predict the success of the main trial and explore steps that need to be taken to minimise issues of recruitment and randomization of patients.16 At the time of writing, the report on the findings from this study has yet to be published. Meng Li et al studied the effect of denervation duration on the outcomes of LR.17 This study investigated paralysed intrinsic laryngeal muscles specimen from UVFP patients undergoing LR with median denervation period of 16.1 months and maximum denervation period of 45 months. The study demonstrated that the number of acetylcholine receptors negatively correlated with duration of palsy. Hence, better voice outcomes may be achieved if the LR procedure was performed within 2 years.17 In another study, Meng Li et al. also investigated the effect of age on the success of LR.18 The mean age of patients’ was 44.0, ranging from 17−69 years. The results demonstrated that age may play an important factor in the voice outcomes of patients with UVFP following LR in which it is maybe less effective in patients older than 60 years of age.18 The present study was observational with longitudinal data which excluded patients older than 60 years old or duration of palsy of more than 3 years when the surgical intervention, either LR or thyroplasty, was performed. Multidimensional voice outcome measures were employed (VHI-10, MPT and perceptual evaluation- breathiness component of GRBAS scale) to demonstrate that near normal to normal voice was achievable in the LR group; significantly better than the thyroplasty group. STUDY LIMITATION The main limitation of the present study was the retrospective nature and the small number of patients recruited. The LR surgery was relatively new in the South East Asian region and to the authors’ knowledge, the study centre was the only one that performs this surgery for patients with
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UVFP. In the present study centre, the LR was mainly performed by MMB, whereas for thyroplasty, three surgeons were involved including MMB. Thus, the comparison outcomes may not be able to be inferred globally but may represent a single centre experience instead. For perceptual evaluation of voice outcomes using the GRBAS scale focusing on the breathiness component, it may be confounded by its subjectivity. In order to minimise this issue, the audio of voices was recommended to be anonymised and randomized prior to the evaluation, so the evaluators are blinded. This was lacking in the present study. With regards to examining the acoustic parameters of the patient’s voices, the analysis of data of male and female is recommended to be done separately as both genders have a different normal range of measurements. This was not possible for the present study as there was only one male subject in each group. Another limitation of this study was that the baseline severity of VHI-10 and MPT was not well distributed between the two groups in which the parameters were better in the LR group as compared to the thyroplasty group. This may be caused by the normal voices of three patients included who had undergone the LR in the same setting as a thyroidectomy when the RLN was transected. Thus, there was no significant difference in the improvement of MPT demonstrated. However, these cases were included due to the main aim of the study which was to evaluate the voice outcomes between the two groups at 12 months postoperative. RECOMMENDATION FOR FUTURE STUDIES Should another RCT with adequate power is not able to conclude which of the two surgical intervention is superior in achieving good voice quality, a future larger study with longitudinal data comparing the outcomes between these two surgical interventions is necessary to confirm the present study’s findings. CONCLUSION The present case series showed that selected patients with UVFP who had undergone nonselective reinnervation (LR) may have better voice outcomes than type I thyroplasty. The VHI-10 and MPT were significantly better in the patients undergoing LR as compared to the thyroplasty procedure. DECLARATION OF INTEREST None. Acknowledgment We would like to extend our sincere thanks to Professor Dr Martin Anthony Birchall of the University College of London, who taught the corresponding author on the
technique of nonselective laryngeal reinnervation during the author’s PhD project. SUPPLEMENTARY MATERIALS Supplementary material associated with this article can be found in the online version at https://doi.org/10.1016/j. jvoice.2019.09.017. REFERENCES 1. Gandhi S, Rai S, Bhowmick N. Etiological profile of unilateral vocal cord paralysis: a single institutional experience over 10 years. J Laryngol Voice. 2014;4:58. 2. Singh JM, Kwartowitz G. Vocal Fold Paralysis Unilateral. StatPearls. Treasure Island (FL): StatPearls Publishing; 2018. 3. Misono S, Merati AL. Evidence-based practice: evaluation and management of unilateral vocal fold paralysis. Otolaryngol Clin North Am. 2012;45:1083–1108. 4. Universiti Kebangsaan Malaysia Medical Centre, Mat Baki M, Universiti Kebangsaan Malaysia Medical Centre. Non-selective laryngeal reinnervation for unilateral vocal fold paralysis. J Surg Acad. 2016;6:1–3. 5. Wang W, Chen D, Chen S, et al. Laryngeal reinnervation using ansa cervicalis for ahyroid surgery-related unilateral vocal fold paralysis: a long-term outcome analysis of 237 cases. PLOS ONE. 2011;6:e19128. 6. Miyauchi A, Inoue H, Tomoda C, et al. Improvement in phonation after reconstruction of the recurrent laryngeal nerve in patients with thyroid cancer invading the nerve. Surgery. 2009;146:1056–1062. 7. Neel HB, Harner SG, Benninger MS, et al. Evaluation and treatment of the unilateral paralyzed vocal fold. Otolaryngol Neck Surg. 1994;111:497–508. 8. Paniello RC, Edgar JD, Kallogjeri D, et al. Medialization versus reinnervation for unilateral vocal fold paralysis: a multicenter randomized clinical trial. Laryngoscope. 2011;121:2172–2179. 9. Isshiki N, Okamura H, Ishikawa T. Thyroplasty type I (lateral compression) for dysphonia due to vocal cord paralysis or atrophy. Acta Otolaryngol (Stockh). 1975;80:465–473. 10. Crumley RL. Update: ansa cervicalis to recurrent laryngeal nerve anastomosis for unilateral laryngeal paralysis. Laryngoscope. 1991;101:384–388. 11. Rosen CA, Lee AS, Osborne J, et al. Development and validation of the voice handicap index-10. Laryngoscope. 2004;114:1549–1556. 12. Ong FM, Husna Nik Hassan NF, Azman M, et al. Validity and reliability study of Bahasa Malaysia version of voice handicap index-10. J Voice.. 2018. 13. Hirano M, Hibi S, Yoshida T, et al. Acoustic Analysis of pathological voice: some results of clinical application. Acta Otolaryngol (Stockh). 1988;105:432–438. 14. Mattei A, Desuter G, Roux M, et al. International consensus (ICON) on basic voice assessment for unilateral vocal fold paralysis. Eur Ann Otorhinolaryngol Head Neck Dis. 2018;135:S11–S15. 15. Baki MM, Wood G, Alston M, et al. Reliability of OperaVOX against multidimensional voice program (MDVP). Clin Otolaryngol. 2015;40:22–28. 16. Blackshaw H, Carding P, Jepson M, et al. Does laryngeal reinnervation or type I thyroplasty give better voice results for patients with unilateral vocal fold paralysis (VOCALIST): study protocol for a feasibility randomised controlled trial. BMJ Open. 2017;7: e016871. 17. Li M, Chen S, Wang W, et al. Effect of duration of denervation on outcomes of ansa-recurrent laryngeal nerve reinnervation. Laryngoscope. 2014;124:1900–1905. 18. Li M, Chen D, Song X, et al. The effect of patient age on the success of laryngeal reinnervation. Eur Arch Otorhinolaryngol. 2014;271:3241–3247.
Nonselective Laryngeal Reinnervation versus Type 1 Thyroplasty in Patients with Unilateral Vocal Fold Paralysis: A Single Tertiary Centre Experience Azlina Ab Rani, Mawaddah Azman, Muhammad Azhan Ubaidah, Mohd Razif Mohamad Yunus, Abdullah Sani, and Marina Mat Baki, Cheras, Malaysia Summary: Objective. This study compared the voice outcomes of selected patients with unilateral vocal fold palsy (UVFP) who underwent either nonselective laryngeal reinnervation (LR) or Type 1 thyroplasty (thyroplasty) in a Malaysian tertiary centre using multidimensional voice assessments. Participants. The study included 16 patients with UVFP who underwent either LR (9 patients) or thyroplasty (7 patients) between 2015 and 2018 who fulfilled the inclusion criteria. Main Outcome Measures. The outcomes were measured subjectively and objectively with: (1) voice handicap index-10 (VHI-10- Malay version); (2) auditory perceptual evaluation using the breathiness component of Grade, Roughness, Breathiness, Asthenia, Strain scale; (3) maximum phonation time (MPT); and (4) acoustic analysis (jitter%, shimmer%, and NHR) using OperaVOXTM. The outcomes were measured at baseline, 6 and 12-months postoperative. The comparison of outcomes between pre and postoperative of each group was evaluated using one-way ANOVA test. Mann-Whitney test was used to compare the outcomes between the two groups. Results. Comparison of each group at different time points showed significant improvement of VHI-10 and MPT of LR group between baseline and 12 months (P ≤ 0.05) whereas, the improvement in thyroplasty group was observed at all time points (P ≤ 0.05). When comparing between the two groups at 12 months, the VHI-10 and MPT was significantly better in the LR group than thyroplasty group with P = 0.004 and P = 0.001 respectively. Other outcome measures did not reveal significant difference between the two groups. Conclusion. This observational study showed that LR may be better than thyroplasty in improving VHI-10 and MPT in selected patients with UVFP. Key Words: Vocal fold−Paralysis−Thyroplasty−Laryngeal reinnervation.
INTRODUCTION Unilateral vocal fold palsy (UVFP) occurs as a result of insults or injuries to the recurrent laryngeal nerve (RLN). One of the common causes of UVFP is surgical complications (iatrogenic) which can be further divided into occurrence during the head, neck and thoracic procedures.1 Patients with UVFP frequently complain of hoarseness with or without aspiration symptoms. The severity of the hoarseness would usually depend on the phonatory gap contributed by the position of the paralysed vocal fold, presence of atrophy as well as the arytenoid position.2 A big phonatory gap causes breathy and an easily fatigued voice due to glottis insufficiency.3 This voice abnormality affects the quality of life especially in those with a high voice demand, making voice rehabilitation pertinent.4 Conventionally, voice therapy is the first line of treatment while waiting for the RLN function to recover within 6 months.5 However, there is a recommendation for early temporary medialisation that may give a rapid and improved voice outcome.6 Patients who persist to have voice issues Accepted for publication September 26, 2019. From the Faculty of Medicine, Universiti Kebangsaan Malaysia Medical Centre, Cheras, Kuala Lumpur, Malaysia. Address correspondence and reprint requests to Marina Mat Baki, Department of Otorhinolaryngology, Universiti Kebangsaan Malaysia Medical Centre, Jalan Yaacob Latiff, Bandar Tun Razak, 56000 Cheras, Kuala Lumpur, Malaysia. E-mail: [email protected] Journal of Voice, Vol. &&, No. &&, pp. &&−&& 0892-1997 © 2019 The Voice Foundation. Published by Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jvoice.2019.09.017
even after 6 months of the RLN nerve insult may be offered other surgical interventions such as Type 1 thyroplasty, with or without arytenoid adduction, as well as nonselective laryngeal reinnervation.7 To the best of our knowledge, there is a still ongoing research on the best surgical options to improve the glottal function in chronic UVFP.8 Nonselective laryngeal reinnervation is a relatively new surgical procedure in South East Asia. The present study was aimed to compare the voice outcomes of selected patients with UVFP who underwent either nonselective laryngeal reinnervation (LR) or Type 1 thyroplasty (thyroplasty) in a Malaysian tertiary centre using multidimensional voice assessments.
MATERIALS AND METHODS This investigation was an observational study among patients with UVFP who had undergone either nonselective LR or a type 1 thyroplasty at Universiti Kebangsaan Malaysia Medical Centre from 2015 to 2018, performed by multiple surgeons (three surgeons). The nonselective laryngeal reinnervation was mainly performed by MMB, while the type 1 thyroplasty was performed by either MMB, MA or AS. A retrospective analysis of longitudinal data was done to evaluate the voice outcomes at baseline, 6 and 12 month postsurgical intervention.
ARTICLE IN PRESS 2 Patients between the ages of 18 to 60 years old with a duration of UVFP within 36 months upon surgical intervention as well as have completed a minimum of 12 months postoperative assessment was included in this study. The exclusion criteria were patients with concomitant other lower cranial nerve palsies, severe cardiopulmonary diseases, high vagal paralysis or duration of UVFP of more than 3 years. SURGICAL TECHNIQUE Type 1 thyroplasty (thyroplasty) The patient was positioned in the supine position and local anaesthesia was infiltrated. A transverse skin incision was made over the thyroid cartilage followed by an elevation of the platysma. The strap muscles attached to the ipsilateral thyroid cartilage lamina were then released and the outer perichondrium was elevated. A window was then created using a cutting burr size 4.0 at the estimated level of the vocal cord, which is halfway between the thyroid notch and lower border of the thyroid cartilage (imaginary line). This thyroid window was routinely performed superior to the thyroid tubercle in an ovoid shape and below the imaginary line, whereby the largest axis measured 6 to 7mm and the distance from the middle ranges from 13 to 17mm.9 The intact inner perichondrium was then elevated anteriorly, inferiorly, and posteriorly to create pockets in the paraglottic space where the polytetrafluoroethylene ribbon implant was inserted. The adequacy of the medialisation was determined endoscopically as well as through the patient’s ability in counting 1 to 10 in a single breath. Haemostasis was then secured and the wound was closed in layers.
Nonselective laryngeal reinnervation (LR) This surgical technique used in this study was described by Crumley,10 with slight modification from Wang et al.5 A horizontally oblique incision was made at the mid-thyroid cartilage level. The fascia between the strap muscles and the sternocleidomastoid muscles was opened to identify the ansa cervalis nerve superficial to the internal jugular vein. The main, sternohyoid or sternothyroid branch of the ansa cervicalis was identified and dissected to its termination in the muscle. The RLN was then identified at the tracheo-oesophageal groove. In post-thyroidectomy cases, the RLN was identified by doing an intralaryngeal dissection, whereby the nerve was found a few millimetres medial to the cricothyroid joint, overlying the posterior cricoarytenoid muscle. In intraoperative thyroidectomy cases where the RLN was accidentally transected, the distal stump of RLN was repaired to the ansa cervicalis. If the proximal part of the RLN was identified and tension free repair was possible, end-to-end neurorrhaphy was performed instead. The ansa cervicalis (proximally) and RLN (distally) were transected, retaining sufficient length for a tension free neurorrhaphy which was then performed using an operating microscope and 9/0 ethilon sutures, reinforced by fibrin glue. Temporary augmentation of the paralysed
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vocal fold was done by injecting hyaluorinic acid endoscopically in the same setting. VOICE ASSESSMENT Subjective evaluation Patients’ voice-related, self-reported outcomes were evaluated using the local language of voice handicap index-10 (malayVHI-10: mVHI-10).11,12 These questionnaires were filled in by the patients to determine how badly the voice disorder caused by UVFP has affected their lives. Perceptual evaluation by a laryngologist was done using the Grade, Roughness, Breathiness, Asthenia, Strain (GRBAS) scale as proposed by Hirano et al.13 In the current study, breathiness component of the GRBAS scale was documented as proposed by Mattei et al.14 Objective evaluation Objective evaluation of voices was done by performing acoustic analysis and measuring maximum phonation time (MPT). Acoustic analysis is noninvasive computer software that measures the quality of recorded voices. It was performed using OperaVOXTM (On Person RApid VOice eXaminer), portable voice analysis software running on iPod touch 6th generation (Apple, USA) to measure the fundamental frequency (F0), jitter % (cycle-to-cycle variation in pitch), shimmer % (cycleto-cycle variation in amplitude), and noise-to-harmonic ratio (NHR).15 MPT was used to assess the glottis efficiency by measuring the longest duration (seconds) of the patients’ ability to sustain a phonation /a/. STATISTICAL ANALYSIS The comparison of outcomes between pre- and postoperative of each group was evaluated using the one-way ANOVA test. For comparison of outcomes between both groups at 12 months postoperative, the Mann-Whitney test was used. P value ≤ 0.05 was considered to be statistically significant. RESULTS Demography A total of 31 patients with UVFP were identified for this study, whereby 10 patients underwent LR and 21 patients underwent thyroplasty. Among the 31 patients, 16 patients were included in the present study according to the inclusion and exclusion criteria. For the LR group, the mean age was of 41.4, ranging from 28 to 59 years old (8 females and 1 male). The aetiologies were iatrogenic (thyroidectomy) except one patient (old left upper lobe pulmonary tuberculosis). Three patients had the LR in the same setting as a thyroidectomy. Therefore, these three patients had normal voice parameters at baseline (preoperative). Out of 14 patients who were excluded in the thyroplasty group, four patients had the duration of palsy for more than 3 years, two had concurrent lower cranial nerve palsies,
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Nonselective LR vs Type 1 Thyroplasty in Patients with UVFP
TABLE 1. Summary of the Demography of the Patients Included for Review Nonselective Laryngeal Reinnervation (n = 9) Age Gender
Mean (SD) 44.29 (13.70)
Min, Max 28, 59
Mean (SD) 44.43 (10.05)
Min, Max 33, 60
Male
Female
Male
Female
1
Duration of palsy (Mean), months Aetiology
Type I Thyroplasty (n = 7)
8 0.4 Iatrogenic: 88.9%% (n = 8), Lobar tuberculosis: 0.11%% (n = 1)
three had a severe cardiopulmonary disease, three were exceeding the age limit and two had incomplete data. One patient was excluded from the LR group as the LR was performed in the same setting as vagal paraganglioma excision that resulted in a high vagal paralysis and multiple lower cranial nerve paralysis. For the thyroplasty group, the mean age was of 44.4, ranging from 33 to 60 years old. Six patients were female and one patient was male. The aetiologies were iatrogenic 71.4% (n = 5), neck trauma 0.14% (n = 1) and thyroid carcinoma 0.14% (n = 1). Simple t test was performed and noted that the age distribution for both groups was not statistically significant (P = 0.982). The patients’ demographic data are summarized in Table 1. Subjective evaluation (VHI-10 and breathiness component of the GRBAS scale) For the LR group, the mean (standard deviation [SD]) of VHI-10 at baseline was 18.57 (18.08). At 6 and 12 months postoperatively, the VHI-10 was of 8.43 (7.25) and 1.57 (2.572), respectively. The breathiness of the GRBAS scale percentage for a score of two or more (moderate to severe) at baseline was 71.4% while at 6 and 12 months were both 0%. However, when comparing the breathiness percentage value in both groups, it was not statistically significant, indicating both groups have near-normal voice perception. For the thyroplasty group, the mean (SD) of VHI-10 at baseline was 31.29 (3.35). At 6 and 12 months postoperatively, they were of 16.86 (11.64) and 10.29 (5.88), respectively. The breathiness of the GRBAS scale percentage for a score of two or more at baseline was 85.71% and at 6 and 12 months were 0% and 14.29%, respectively. Objective evaluation (MPT and acoustic analysis) For the LR group, the mean (SD) of MPT and acoustic analysis which comprises jitter, shimmer, and NHR were of 11.58 (4.88), 2.24 (2.06), 8.11 (5.01), and 0.32 (0.53), respectively. At 6 and 12 months, the values were of 15.21 (7.77) and 15.29 (5.82) for MPT; 1.77 (1.76) and 1.20 (0.76) for
1
6 9.1 Iatrogenic: 71.4% (n = 5), Neck trauma: 0.14% (n = 1), Thyroid carcinoma: 0.14% (n = 1)
jitter; 6.28 (3.77) and 5.97 (1.92) for shimmer; and 0.16 (0.25) and 0.06 (0.11) for NHR, respectively. For the thyroplasty group, the mean (SD) of MPT and acoustic analysis were of 4.79 (1.95), 6.08 (2.57), 9.27 (6.66) and 0.81 (0.86), respectively. At 6 and 12 months, the values were of 7.37 (1.59) and 8.70 (0.87) for MPT; 3.70 (1.56) and 3.18 (2.10) for jitter; 8.05 (4.25) and 8.23 (4.73) for shimmer; and 0.21 (0.38) and 0.29 (0.46) for NHR, respectively. Comparison between pre- and postoperative outcomes of each group The multidimensional voice outcomes were compared between preoperative and postoperative at different time points. For the LR group, comparison of VHI-10 showed a significant improvement between the baseline and 12 months postoperative (P = 0.038). (Figure 1). As for the thyroplasty group, the VHI-10 was significantly improved at 6 months (P = 0.036) and 12 months (P = 0.001) when compared to the baseline. (Figure 2). There were no significant changes of MPT between the baseline when compared with 6 months
FIGURE 1. One-way ANOVA test for Voice Handicap Index-10 (VHI-10) score of the nonselective laryngeal innervation group over 12 months from the baseline which showed significant improvement. **P ≤ 0.05.
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Thyroplasty
VHI-10 Score
40 30 20 10
6
B
as
el
in e M on 12 th s M on th s
0
Time FIGURE 2. One-way ANOVA test for Voice Handicap Index-10 (VHI-10) score of the thyroplasty group over 12 months from the baseline which showed significant improvement. **P ≤ 0.05. (P = 0.219) and 12 months (P = 0.078) postoperative in the LR group. (Figure 3). For the thyroplasty group, the MPT was significantly increased when comparing the baseline to 6 months (P = 0.04) and 12 months (P = 0.001) postoperative (Figure 4). Comparison at 12 months between 2 groups Comparison of voice parameters between the LR and the thyroplasty group showed that both VHI-10 was better and MPT was longer in the LR (P = 0.001) than the thyroplasty group (P = 0.004 and P = 0.001 respectively). There was no significant difference between both groups with regards
FIGURE 3. One-way ANOVA test for assessing maximum phonation time (MPT) of the nonselective laryngeal innervation group over 12 months which showed no significant difference. **P > 0.05.
FIGURE 4. One-way ANOVA test for assessing maximum phonation time (MPT) of the thyroplasty group over 12 months from the baseline which showed significant improvement. **P ≤ 0.05.
to breathiness component of the GRBAS scale and acoustic analysis (jitter, shimmer and NHR). The summary is tabulated in Table 2. DISCUSSION Overview The need to restore normal or near-normal voice in patients with unilateral vocal fold paralysis is a challenge. Surgical procedures proposed to enable this have their own set of advantages and disadvantages. As to which of the surgical option has a better chance of improving UVFP patients’ voice is still a matter under consideration in a number of researches.16 Here, results from a series of cases that fit the inclusion criteria comparing the voice outcomes of 2 promising surgical techniques, nonselective laryngeal reinnervation or Type 1 thyroplasty, were reported.
Synopsis of key findings There was a significant improvement in the mean of VHI-10 in each group as well as the mean of MPT in the thyroplasty group when comparing pre- and postoperative outcomes. Significantly better VHI-10 and MPT scores were present in the LR group as compared to the thyroplasty group at 12 months postoperative. In the LR group, three patients
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Nonselective LR vs Type 1 Thyroplasty in Patients with UVFP
TABLE 2. The Mann Whitney U Test to Compare the Outcomes of Both Objective and Subjective Assessments in Both Groups at 12 Months Post-op Nonselective Laryngeal Reinnervation
Type 1 Thyroplasty
Outcome Measure
Mean (SD)
Median (IQR)
Mean (SD)
Median (IQR)
p Value
VHI-10 MPT Jitter Shimmer Noise-Harmonic Ratio
1.57 (2.57) 15.29 (5.87) 1.20 (0.76) 7.35 (2.23) 0.06 (0.11)
0.00 (0.00, 2.00) 14.30 (10.50, 16.50) 0.79 (0.70, 2.11) 7.07 (6.24, 9.98) 0.02 (0.01, 0.05)
10.29 (5.88) 8.70 (0.86) 3.18 (2.10) 8.22 (4.73) 39.34 (103.90)
10.00 (5.00, 13.00) 8.90 (7.60, 9.30) 2.16 (2.06, 5.77) 7.41 (5.14, 8.49) 0.06 (0.06, 0.14)
0.004* 0.001* 0.128 0.383 0.071
* p ≤ 0.05.
had nonselective reinnervation performed in the same setting as the iatrogenic transection of the RLN, thus the preoperative assessment of these patients’ voice was considered to be the baseline, revealing a completely normal voice. This may explain why the mean of VHI-10 and MPT at baseline was better in the LR than the thyroplasty group as well as the absence of a statistically significant improvement in MPT between baseline and 12 months postoperative. The breathiness component on the GRBAS scale percentage for a score of two or more (moderate to severe) in the LR group at baseline was 71.4% and improved to 0% after 12 months. This showed that at the beginning there were patients with a near-normal or normal voice in this group; the voice of all of the patients in this group improved to near normal or normal after 12 months. The breathiness component of the GRBAS scale percentage for a score of two or more for the thyroplasty group at baseline was 85.71%. This value showed an improvement of up to 6 months where the percentage was from 85.71% to 0%. However, for the subsequent 6 months, the percentage of patients with breathiness increased to 14.29%. The acoustic analysis parameters (jitter, shimmer and NHR) of both groups showed improvement between pre- and postoperative and were comparable between both groups at 12 months.
Comparison with previous studies Studies comparing LR with other recommended surgical intervention for UVFP was limited. In a large observational study, Wang et al5 compared the voice outcomes of 237 patients with UVFP who underwent LR with voices of 237 normal members of a similar population. The study demonstrated that the voices of UVFP patients who had undergone LR were similar to voices of healthy people. Although the comparison between both groups was made, the study did not evaluate the effectiveness of the two different surgical techniques to treat UVFP. A randomised controlled trial (RCT) was performed in the US by Paniello et al8 comparing LR and type I thyroplasty. The results documented that there was no significant difference of voice outcomes between the two groups. This may suggest that LR is as effective as thyroplasty in rehabilitating UVFP patients’ voices. However, it was suspended
prematurely with only 20% of subjects enrolled. Another similar study was planned by a UK group of researchers aiming to replicate and complete the RCT study accordingly. Predicaments in recruiting and randomizing were inherent in surgical trials due to the strong surgical preference of patients as well as surgeons. Therefore, a feasibility study was carried out first to predict the success of the main trial and explore steps that need to be taken to minimise issues of recruitment and randomization of patients.16 At the time of writing, the report on the findings from this study has yet to be published. Meng Li et al studied the effect of denervation duration on the outcomes of LR.17 This study investigated paralysed intrinsic laryngeal muscles specimen from UVFP patients undergoing LR with median denervation period of 16.1 months and maximum denervation period of 45 months. The study demonstrated that the number of acetylcholine receptors negatively correlated with duration of palsy. Hence, better voice outcomes may be achieved if the LR procedure was performed within 2 years.17 In another study, Meng Li et al. also investigated the effect of age on the success of LR.18 The mean age of patients’ was 44.0, ranging from 17−69 years. The results demonstrated that age may play an important factor in the voice outcomes of patients with UVFP following LR in which it is maybe less effective in patients older than 60 years of age.18 The present study was observational with longitudinal data which excluded patients older than 60 years old or duration of palsy of more than 3 years when the surgical intervention, either LR or thyroplasty, was performed. Multidimensional voice outcome measures were employed (VHI-10, MPT and perceptual evaluation- breathiness component of GRBAS scale) to demonstrate that near normal to normal voice was achievable in the LR group; significantly better than the thyroplasty group. STUDY LIMITATION The main limitation of the present study was the retrospective nature and the small number of patients recruited. The LR surgery was relatively new in the South East Asian region and to the authors’ knowledge, the study centre was the only one that performs this surgery for patients with
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UVFP. In the present study centre, the LR was mainly performed by MMB, whereas for thyroplasty, three surgeons were involved including MMB. Thus, the comparison outcomes may not be able to be inferred globally but may represent a single centre experience instead. For perceptual evaluation of voice outcomes using the GRBAS scale focusing on the breathiness component, it may be confounded by its subjectivity. In order to minimise this issue, the audio of voices was recommended to be anonymised and randomized prior to the evaluation, so the evaluators are blinded. This was lacking in the present study. With regards to examining the acoustic parameters of the patient’s voices, the analysis of data of male and female is recommended to be done separately as both genders have a different normal range of measurements. This was not possible for the present study as there was only one male subject in each group. Another limitation of this study was that the baseline severity of VHI-10 and MPT was not well distributed between the two groups in which the parameters were better in the LR group as compared to the thyroplasty group. This may be caused by the normal voices of three patients included who had undergone the LR in the same setting as a thyroidectomy when the RLN was transected. Thus, there was no significant difference in the improvement of MPT demonstrated. However, these cases were included due to the main aim of the study which was to evaluate the voice outcomes between the two groups at 12 months postoperative. RECOMMENDATION FOR FUTURE STUDIES Should another RCT with adequate power is not able to conclude which of the two surgical intervention is superior in achieving good voice quality, a future larger study with longitudinal data comparing the outcomes between these two surgical interventions is necessary to confirm the present study’s findings. CONCLUSION The present case series showed that selected patients with UVFP who had undergone nonselective reinnervation (LR) may have better voice outcomes than type I thyroplasty. The VHI-10 and MPT were significantly better in the patients undergoing LR as compared to the thyroplasty procedure. DECLARATION OF INTEREST None. Acknowledgment We would like to extend our sincere thanks to Professor Dr Martin Anthony Birchall of the University College of London, who taught the corresponding author on the
technique of nonselective laryngeal reinnervation during the author’s PhD project. SUPPLEMENTARY MATERIALS Supplementary material associated with this article can be found in the online version at https://doi.org/10.1016/j. jvoice.2019.09.017. REFERENCES 1. Gandhi S, Rai S, Bhowmick N. Etiological profile of unilateral vocal cord paralysis: a single institutional experience over 10 years. J Laryngol Voice. 2014;4:58. 2. Singh JM, Kwartowitz G. Vocal Fold Paralysis Unilateral. StatPearls. Treasure Island (FL): StatPearls Publishing; 2018. 3. Misono S, Merati AL. Evidence-based practice: evaluation and management of unilateral vocal fold paralysis. Otolaryngol Clin North Am. 2012;45:1083–1108. 4. Universiti Kebangsaan Malaysia Medical Centre, Mat Baki M, Universiti Kebangsaan Malaysia Medical Centre. Non-selective laryngeal reinnervation for unilateral vocal fold paralysis. J Surg Acad. 2016;6:1–3. 5. Wang W, Chen D, Chen S, et al. Laryngeal reinnervation using ansa cervicalis for ahyroid surgery-related unilateral vocal fold paralysis: a long-term outcome analysis of 237 cases. PLOS ONE. 2011;6:e19128. 6. Miyauchi A, Inoue H, Tomoda C, et al. Improvement in phonation after reconstruction of the recurrent laryngeal nerve in patients with thyroid cancer invading the nerve. Surgery. 2009;146:1056–1062. 7. Neel HB, Harner SG, Benninger MS, et al. Evaluation and treatment of the unilateral paralyzed vocal fold. Otolaryngol Neck Surg. 1994;111:497–508. 8. Paniello RC, Edgar JD, Kallogjeri D, et al. Medialization versus reinnervation for unilateral vocal fold paralysis: a multicenter randomized clinical trial. Laryngoscope. 2011;121:2172–2179. 9. Isshiki N, Okamura H, Ishikawa T. Thyroplasty type I (lateral compression) for dysphonia due to vocal cord paralysis or atrophy. Acta Otolaryngol (Stockh). 1975;80:465–473. 10. Crumley RL. Update: ansa cervicalis to recurrent laryngeal nerve anastomosis for unilateral laryngeal paralysis. Laryngoscope. 1991;101:384–388. 11. Rosen CA, Lee AS, Osborne J, et al. Development and validation of the voice handicap index-10. Laryngoscope. 2004;114:1549–1556. 12. Ong FM, Husna Nik Hassan NF, Azman M, et al. Validity and reliability study of Bahasa Malaysia version of voice handicap index-10. J Voice.. 2018. 13. Hirano M, Hibi S, Yoshida T, et al. Acoustic Analysis of pathological voice: some results of clinical application. Acta Otolaryngol (Stockh). 1988;105:432–438. 14. Mattei A, Desuter G, Roux M, et al. International consensus (ICON) on basic voice assessment for unilateral vocal fold paralysis. Eur Ann Otorhinolaryngol Head Neck Dis. 2018;135:S11–S15. 15. Baki MM, Wood G, Alston M, et al. Reliability of OperaVOX against multidimensional voice program (MDVP). Clin Otolaryngol. 2015;40:22–28. 16. Blackshaw H, Carding P, Jepson M, et al. Does laryngeal reinnervation or type I thyroplasty give better voice results for patients with unilateral vocal fold paralysis (VOCALIST): study protocol for a feasibility randomised controlled trial. BMJ Open. 2017;7: e016871. 17. Li M, Chen S, Wang W, et al. Effect of duration of denervation on outcomes of ansa-recurrent laryngeal nerve reinnervation. Laryngoscope. 2014;124:1900–1905. 18. Li M, Chen D, Song X, et al. The effect of patient age on the success of laryngeal reinnervation. Eur Arch Otorhinolaryngol. 2014;271:3241–3247.