- Email: [email protected]
Does Dysphagia Improve Following Laryngeal Reinnervation for Treatment of Hoarseness in Unilateral Vocal Fold Paralysis?
ARTICLE IN PRESS
Does Dysphagia Improve Following Laryngeal Reinnervation for Treatment of Hoarseness in Unilateral Vocal Fold Paralysis? *Zahide C. Buyukatalay, †Simon Brisebois, ‡Seher Sirin, and §Albert L. Merati, *Ankara, and zKocaeli, Turkey, ySherbrooke, Canada, and xSeattle, Washington
Abstract: Purpose. There are many reports of the efficacy of laryngeal reinnervation on voice, but there is a paucity of literature regarding its impact on swallowing function. The goal of this study was to explore the impact of laryngeal reinnervation on swallowing outcomes among unilateral vocal fold paralysis (UVFP) patients. Methods. We reviewed 22 UVFP cases treated with laryngeal reinnervation at our institution. Ten patients had complete datasets, including Eating Assessment Tool (EAT-10) scores and appropriate follow-up. Wilcoxon signed-rank test was used to compare pre- and postoperative scores. Results. Over the study period, 10 cases (mean age 45.7 § 13.3 years; 6/10 men) with UVFP underwent ansa cervicalis to recurrent laryngeal nerve anastomosis (6/10) or nerve-muscle pedicle procedure (4/10). The median time between injury and surgical reinnervation was 12.4 months (range 2.7−88.5 months). Based on EAT-10 scores 6/10 patients were found to have dysphagia. Of these, four improved their score after surgery, one remained stable, and one deteriorated. The median EAT-10 score of these patients improved from 13 to 7 after surgery, but this difference was not statistically significant (P = 0.138). Conclusion. Laryngeal reinnervation procedure has the potential for restoring a near normal voice in UVFP. Laryngeal reinnervation of the vocal fold may be associated with a tendency toward improvement in the EAT-10 score in patients after surgery for hoarseness in the setting of UVFP. Key Words: Laryngeal reinnervation−Vocal fold paralysis−Swallowing−Dysphagia.
INTRODUCTION Unilateral vocal fold paralysis (UVFP) has many underlying etiologies. In many large series, the most common reported etiology is iatrogenic in up to 48% of cases of vocal fold motion impairment,1−5 usually from neck surgery, such as spine or thyroid surgery. In most cases, this results in a varying degree of glottic insufficiency depending on the resting position of the impaired vocal fold, as well as potential synkinesis and a possible degree of pharyngeal dysfunction. Indeed, the recurrent laryngeal nerve (RLN) has been shown to contribute, at least to some degree, to the innervation of the inferior pharyngeal constrictor and cricopharyngeal muscle.6−8 Thus, patients will typically report dysphonia, but might also complain of dysphagia.9 According to various reports using functional endoscopic evaluation of swallowing or videofluoroscopic swallow studies, the rate of aspiration in patient with unilateral vocal fold motion impairment (UVFMI) can be anywhere between 23% and 56%.3,4,9−12 Accepted for publication August 6, 2019. Funding: No financial supporter of this study. Conflict of Interests: The authors declare that they have no conflict of interest. Meeting: Presented at ALA meeting, COSM 2018, National Harbor, MD, April 18−20. From the *Department of Otorhinolaryngology, Head and Neck Surgery, Ibni Sina Hospital, Ankara University School of Medicine, Ankara, Turkey; yDepartment of Surgery, Division of Otolaryngology, Head and Neck Surgery, Centre Hospitalier Universitaire de Sherbrooke, Sherbrooke, Quebec, Canada; zDepartment of Otorhinolaryngology, Head and Neck Surgery, Kocaeli University School of Medicine, Kocaeli, Turkey; and the xDepartment of Otolaryngology, Head and Neck Surgery, University of Washington Medical Center, Seattle, Washington. Address correspondence and reprint requests to Zahide C. Buyukatalay, 8th Floor, Alt{nda g, Ankara 06660, Turkey. 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.2019.08.005
Leder et al also reports that patients with UVFMI have about 2.5 times the odds of aspirating when compared with controls without motion impairment.10 There has been extensive research on the impact of UVFP on voice and phonation. However, if both dysphonia and dysphagia are present after UVFP, then the underlying pathophysiology for the swallowing impairment should be clarified for each patient since no two patients are identical in severity of recurrent nerve injury, extent of nerve regeneration, synkinesis posthealing, compensatory changes of the unaffected larynx, etc. Ineffective airway protection is suggested as being the primary cause of swallowing dysfunction in patients with UVFMI.4,5 At least three other deficits besides ineffective airway protection may accompany UVFP and cause or increase the severity of dysphagia and/ or aspiration. A study by Domer et al showed increase in the pharyngeal transit time and pharyngeal constriction ratio suggesting that pharyngeal weakness can also be present. Also, they found that the opening diameter of the upper esophageal sphincter (UES) was diminished, although not statistically different.12 Still, this might suggest that the loss of efferent input from the RLN impairs the ability of the UES to relax during the pharyngeal phase of deglutition (delayed relaxation of the UES), therefore contributing to the dysphagia. Finally, decreased sensation has been shown as a contributing factor of dysphagia in patients with UVFMI.4 Glottic insufficiency from UVFMI leads to reduced cough efficacy with impaired airway clearing after aspiration. Increased cough efficiency may be accomplished vocal fold augmentation, as demonstrated by trials indicating an increase in airflow measurements during voluntary
ARTICLE IN PRESS 2 cough after a vocal fold augmentation.13,14 Indeed, dysphagia seen with RLN injury may be more often than not multifactorial. Still, most treatment options for UVFP, vocal fold augmentation, laryngeal framework surgery, or laryngeal reinnervation, focus on optimizing glottic competence. The rates of penetration and aspiration have been found to improve on fluoroscopy after both injection medialization and type I thyroplasty, although in a limited manner.3,15 Laryngeal reinnervation using ansa cervicalis to RLN anastomosis was first reported by Frazier in 1924 in patients with bilateral vocal fold paralysis after a thyroidectomy.16 In 1986, Crumley and Izdebski published their surgical technique, which served as the basis for contemporary work on reinnervation.17 Although efficacy on objective and subjective voice-related outcomes of reinnervation has been shown in many studies,18−23 dysphagia outcomes have not been thoroughly studied. One study conducted by Zur and Carroll, looked at swallowing function after reinnervation surgery was performed for aspiration in three pediatric patients with UVFMI. Improved swallowing function on postoperative MBS was found 6 months after surgery.24 The aim of this study was to investigate the impact of laryngeal reinnervation, performed due to dysphonia, on swallowing outcomes in patients with UVFP. MATERIALS AND METHODS The charts of patients who underwent a reinnervation procedure for a UVFP at the University of Washington Medical Center between 2008 and 2017 were retrospectively reviewed. This research protocol was approved by the University of Washington Institutional Review Board. In addition to demographic characteristics, preoperative and postoperative patient reported outcomes questionnaires were collected. Dysphagia was assessed using the Eating Assessment Tool (EAT-10).25 The EAT-10 score closest to the one-year mark after surgery was used as the postoperative value. However, in order to discard the effect of the simultaneously performed injection laryngoplasty on the results, EAT-10 scores taken postoperatively before 6 months were not considered for the patients who did receive an injection. Patients with incomplete sets of data, any history of radiation therapy or insufficient follow-up were excluded. Voice Handicap Index (VHI-10)26 were also collected for descriptive purposes and again, scores taken before 6 months were not considered for patient having received an injection laryngoplasty. Statistical comparisons were made on the patients who described dysphagia and/or aspiration prior to reinnervation and whose preoperative EAT 10 scores were three and higher. The primary outcome was defined as a reduction in EAT-10 score. Descriptive statistics are shown as the mean (standard deviation) for normally distributed variables, a median (range) for non-normally distributed and as the number of cases (%) for nominal variables. Pre- and postoperative score analysis was done using Wilcoxon signed-rank test. A P < 0.05 value was accepted as statistically significant.
Journal of Voice, Vol. &&, No. &&, 2019
RESULTS Study population The charts of 22 patients diagnosed with UVFP and treated with a laryngeal reinnervation procedure were reviewed. Ten patients (6 men and 4 women) were found to have adequate data on swallowing before and after the laryngeal reinnervation. The mean age of our population at the time of diagnosis was 45.7 years (SD 13.3) and the paralysis was left-sided in seven patients. In all cases, the etiology was iatrogenic. Paralysis occurred after neck surgery (thyroidectomy, cervical spine, or paraganglioma) in seven patients, after thoracic surgery in two patients and intubation in one patient. The median duration of UVFP from symptom onset to date of surgery was 12.4 months (range\ 2.7−88.5 months). A total of six patients underwent ansa cervicalis to RLN anastomosis, while the remaining four patients had a neuromuscular pedicle. In six of the patients, an injection laryngoplasty with hyaluronic acid was done at the same time as the reinnervation surgery. The median follow-up time after procedure was 21.2 months (range 5.0−38.5 months) (Table 1).
EAT-10 EAT-10 scores of 6/10 patients were found to be three or higher before the reinnervation surgery and thus used in the analysis. Median EAT-10 scores of these six patients were 13 (3−23) in the preoperatively and seven (2−12) in the postoperative period. The decrease in the median score after surgery did not reach statistical significance (P = 0.138) (Figure 1).
VHI-10 The median preoperative VHI-10 score was 30 (range 18−40), and postoperative score was 10.5 (range 1−34). There was statistically significant improvement (P= 0.008) in median VHI-10 score after surgery. DISCUSSION The purpose of laryngeal reinnervation is to restore tone, bulk, and variable repositioning of the vocal fold.27,28 When compared to static medialization interventions such as injection augmentation or anterior thyroplasty, reinnervation may provide active resting tone to whichever muscle(s) becomes reinnervated, active air stream resistance on both inhalation and exhalation, and prevention of muscle atrophy.29 The laryngeal reinnervation procedure is considered safe30 and offers positive effects on UVFP in terms of acoustic, perceptual, electromyographic, and visual outcomes.22 Laryngeal reinnervation is potentially more successful if the procedure is performed within 2 years following nerve injury19 or in patients less than 60 years old.18 Although it is considered as being an effective and reliable surgical procedure, it is not as widely performed as other medialization techniques, such as framework surgery, due to the longer
ARTICLE IN PRESS
12 25 5 34 9 19 9 8 1 25
3
Abbreviations: A-to-R, ansa cervicalis to recurrent laryngeal nerve; F, female; L, left; M, male; NMP, nerve-muscle pedicle; N, no; R, right; Y, yes.
21 40 18 34 40 23 26 25 34 35 6 12 0 2 0 8 0 3 0 12 6 22 0 4 0 3 1 23 2 19 M M F F M M M M F F 1 2 3 4 5 6 7 8 9 10
53 44 44 43 35 23 33 60 66 56
Thoracic surgery Spine surgery Thyroid surgery Thyroid surgery Thyroid surgery Thoracic surgery Intubation Spine surgery Thyroid surgery Neck surgery
L R L R L L L R L L
88.5 14.5 2.7 19.6 9.1 6.5 17.0 36.6 10.4 5.5
A-to-R NMP NMP A-to-R A-to-R A-to-R A-to-R A-to-R NMP NMP
N N Y Y Y Y Y Y N N
Post EAT-10 Injection Augmentation Reinnervation Type Sex Patient
Age
Etiology
Side
Denervation Duration (Months)
TABLE 1. Patient Characteristics, Preoperative, and Postoperative Outcomes Scores
Dysphagia After Laryngeal Reinnervation
Pre EAT-10
Pre VHI-10
Post VHI-10
Zahide C. Buyukatalay, et al
FIGURE 1. Preoperative and postoperative EAT-10 scores. *, P = 0.138.
surgical time, the disadvantage of general anesthesia, and the long-term effect. The most common patient complaint in UVFP is dysphonia. However, it may also be associated with significant swallowing impairments and potential aspiration. Prior research shows that factors such as pharyngeal muscle weakness, delayed relaxation of the UES, and decreased laryngeal sensation also impact swallowing in these patients, along with glottal incompetence.31 These factors are much more common in central brainstem deficits or high vagal paralysis.32,33 Four patients in our study group who had postoperative paralysis due to cervical spine surgery or paraganglioma had much higher EAT-10 scores compared with patients with other etiologies (Table 1). Swallowing dysfunction and aspiration decreases the quality of life and may cause serious complications. This study retrospectively evaluated the effect of reinnervation for an indication of dysphonia on swallowing function by means of patient-reported outcomes. All surgeries were successful in the sense that the VHI-10 was significantly improved after the procedure. Although this surgical procedure was not actually planned for the treatment of swallowing disorder in these patients, their postoperative EAT-10 scores also improved. However, this improvement was not statistically significant, probably due to the small number of patients in our study. Interestingly, the improvement was more striking for these patients with a central etiology to their UVFP in which the preoperative score suggested a more profound dysphagia, probably due to the presence of all the aforementioned factors. Unfortunately, the paucity of patients does not allow for reliable subgroup analysis. Only one patient had a worsening of his EAT-10 score after the surgery, despite an improvement in his VHI-10. It is to note that this patient had been operated for an extensive mediastinal germ cell tumor at which time the left RLN was injured. Thus, it is possible that the reported worsening of dysphagia
ARTICLE IN PRESS 4 in this patient was secondary to an added esophageal issue, more so than from a change in the pharyngoesophageal segment. This study also adds to the safety profile of the procedure by suggesting that patients do not experience worsening dysphagia despite the theoretical loss of function associated with denervation of strap muscles from harvesting the ansa cervicalis. Obviously, this study presents some limitations. Firstly, this is a retrospective cohort with a small number of patients and thus, potential for sampling error. Secondly, only a patient reported outcomes questionnaire was used. Unfortunately, since laryngeal reinnervation is typically focused on the treatment of dysphonia, complete dysphagia workup was not routinely done, thereby limiting the dataset. Finally, hyaluronic acid injection augmentation was used concomitantly in many patients, which might have had an impact on short-term function. However, the clinical longevity of the filler material used in those patients (hyaluronic acid) was considered by excluding all patients with follow-up less than 6 months. A well-designed prospective study with a larger sample size and objective functional assessment of swallowing could help support the role of laryngeal reinnervation in the treatment of dysphagia in patients with UVFP.
Journal of Voice, Vol. &&, No. &&, 2019
7.
8.
9.
10. 11. 12.
13.
14.
15.
16. 17.
CONCLUSION Even though laryngeal reinnervation is not designed to be a treatment for dysphagia, our study shows a tendency for improvement of the EAT-10 score in UVFP patients after reinnervation surgery. SUPPLEMENTARY MATERIALS Supplementary material associated with this article can be found in the online version at https://doi.org/10.1016/j.jvoice. 2019.08.005.
18.
19.
20.
21.
22.
23.
REFERENCES 1. Merati AL, Shemirani N, Smith TL, et al. Changing trends in the nature of vocal fold motion impairment. Am J Otolaryngol. 2006;27:106–108. 2. Rosenthal LHS, Benninger MS, Deeb RH. Vocal fold immobility: a longitudinal analysis of etiology over 20 years. Laryngoscope. 2007;117:1864–1870. 3. Bhattacharyya N, Kotz T, Shapiro J. Dysphagia and aspiration with unilateral vocal cord immobility: incidence, characterization, and response to surgical treatment. Ann Otol Rhinol Laryngol. 2002;111:672–679. 4. Tabaee A, Murry T, Zschommler A, et al. Flexible endoscopic evaluation of swallowing with sensory testing in patients with unilateral vocal fold immobility: incidence and pathophysiology of aspiration. Laryngoscope. 2005;115:565–569. 5. Heitmiller RF, Tseng E, Jones B. Prevalence of aspiration and laryngeal penetration in patients with unilateral vocal fold motion impairment. Dysphagia. 2000;15:184–187. 6. Uludag M, Aygun N, Isgor A. Innervation of the human cricopharyngeal muscle by the recurrent laryngeal nerve and external branch of
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the superior laryngeal nerve. Langenbeck’s Arch Surg. 2017;402: 683–690. Sakamoto Y. Interrelationships between the innervations from the laryngeal nerves and the pharyngeal plexus to the inferior pharyngeal constrictor. Surg Radiol Anat. 2013;35:721–728. Brok HA, Copper MP, Stroeve RJ, et al. Evidence for recurrent laryngeal nerve contribution in motor innervation of the human cricopharyngeal muscle. Laryngoscope. 1999;109:705–708. Flint PW, Purcell LL, Cummings CW. Pathophysiology and indications for medialization thyroplasty in patients with dysphagia and aspiration. Otolaryngol Head Neck Surg. 1997;116:349–354. Leder SB, Suiter DM, Duffey D, et al. Vocal fold immobility and aspiration status: a direct replication study. Dysphagia. 2012;27:265–270. Leder SB, Ross DA. Incidence of vocal fold immobility in patients with dysphagia. Dysphagia. 2005;20:163–167. Domer AS, Leonard R, Belafsky PC. Pharyngeal weakness and upper esophageal sphincter opening in patients with unilateral vocal fold immobility. Laryngoscope. 2014;124:2371–2374. Ruddy BH, Pitts TE, Lehman J, et al. Improved voluntary cough immediately following office-based vocal fold medialization injections. Laryngoscope. 2014;124:1645–1647. Dion GR, Achlatis E, Teng S, et al. Changes in peak airflow measurement during maximal cough after vocal fold augmentation in patients with glottic insufficiency. JAMA Otolaryngol Head Neck Surg. 2017;143:1141–1145. Cates DJ, Venkatesan NN, Strong B, et al. Effect of vocal fold medialization on dysphagia in patients with unilateral vocal fold immobility. Otolaryngol Head Neck Surg. 2016;155:454–457. Frazier CH. The treatment of paralysis of the recurrent laryngeal nerve by nerve anastomosis. Ann Surg. 1924;79:161–171. Crumley RL, Izdebski K. Voice quality following laryngeal reinnervation by ansa hypoglossi transfer. Laryngoscope. 1986;96:611–616. 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. 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. Lee WT, Milstein C, Hicks D, et al. Results of ansa to recurrent laryngeal nerve reinnervation. Otolaryngol Head Neck Surg. 2007;136: 450–454. Lee S, Park K. A long-term comparative prospective study between reinnervation and injection laryngoplasty. Laryngoscope. 2018;128: 1893–1897. Aynehchi BB, McCoul ED, Sundaram K. Systematic review of laryngeal reinnervation techniques. Otolaryngol Head Neck Surg. 2010;143: 749–759. Su WF, Hsu YD, Chen HC, et al. Laryngeal reinnervation by ansa cervicalis nerve implantation for unilateral vocal cord paralysis in humans. J Am Coll Surg. 2007;204:64–72. Zur KB, Carroll LM. Recurrent laryngeal nerve reinnervation for management of aspiration in a subset of children. Int J Pediatr Otorhinolaryngol. 2018;104:104–107. Belafsky PC, Mouadeb DA, Rees CJ, et al. Validity and reliability of the eating assessment tool (EAT-10). Ann Otol Rhinol Laryngol. 2008;117:919–924. Rosen CA, Lee AS, Osborne J, et al. Development and validation of the voice handicap index-10. Laryngoscope. 2004;114:1549–1556. Zheng H, Li Z, Zhou S, et al. Laryngeal reinnervation for unilateral vocal cord paralysis with the ansa cervicalis. Laryngoscope. 1996;106: 1522–1527. Crumley RL. Update: ansa cervicalis to recurrent laryngeal nerve anastomosis for unilateral laryngeal paralysis. Laryngoscope. 1991;101:384–387. discussion 388. Chhetri DK, Blumin JH. Laryngeal reinnervation for unilateral vocal fold paralysis using ansa cervicalis nerve to recurrent laryngeal nerve anastomosis. Oper Tech Otolaryngol Neck Surg. 2012;23: 173–177.
ARTICLE IN PRESS Zahide C. Buyukatalay, et al
Dysphagia After Laryngeal Reinnervation
30. Blumin JH, Merati AL. Laryngeal reinnervation with nerve-nerve anastomosis versus laryngeal framework surgery alone: a comparison of safety. Otolaryngol Head Neck Surg. 2008;138:217–220. 31. Aviv JE, Mohr J, Blitzer A, et al. Restoration of laryngopharyngeal sensation by neural anastomosis. Arch Otolaryngol Head Neck Surg. 1997;123:154–160.
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32. Jang YY, Lee SJ, Lee SJ, et al. Analysis of video fluoroscopic swallowing study in patients with vocal cord paralysis. Dysphagia. 2012;27:185–190. 33. Fang TJ, Tam YY, Courey MS, et al. Unilateral high vagal paralysis: relationship of the severity of swallowing disturbance and types of injuries. Laryngoscope. 2011;121:245–249.
Does Dysphagia Improve Following Laryngeal Reinnervation for Treatment of Hoarseness in Unilateral Vocal Fold Paralysis? *Zahide C. Buyukatalay, †Simon Brisebois, ‡Seher Sirin, and §Albert L. Merati, *Ankara, and zKocaeli, Turkey, ySherbrooke, Canada, and xSeattle, Washington
Abstract: Purpose. There are many reports of the efficacy of laryngeal reinnervation on voice, but there is a paucity of literature regarding its impact on swallowing function. The goal of this study was to explore the impact of laryngeal reinnervation on swallowing outcomes among unilateral vocal fold paralysis (UVFP) patients. Methods. We reviewed 22 UVFP cases treated with laryngeal reinnervation at our institution. Ten patients had complete datasets, including Eating Assessment Tool (EAT-10) scores and appropriate follow-up. Wilcoxon signed-rank test was used to compare pre- and postoperative scores. Results. Over the study period, 10 cases (mean age 45.7 § 13.3 years; 6/10 men) with UVFP underwent ansa cervicalis to recurrent laryngeal nerve anastomosis (6/10) or nerve-muscle pedicle procedure (4/10). The median time between injury and surgical reinnervation was 12.4 months (range 2.7−88.5 months). Based on EAT-10 scores 6/10 patients were found to have dysphagia. Of these, four improved their score after surgery, one remained stable, and one deteriorated. The median EAT-10 score of these patients improved from 13 to 7 after surgery, but this difference was not statistically significant (P = 0.138). Conclusion. Laryngeal reinnervation procedure has the potential for restoring a near normal voice in UVFP. Laryngeal reinnervation of the vocal fold may be associated with a tendency toward improvement in the EAT-10 score in patients after surgery for hoarseness in the setting of UVFP. Key Words: Laryngeal reinnervation−Vocal fold paralysis−Swallowing−Dysphagia.
INTRODUCTION Unilateral vocal fold paralysis (UVFP) has many underlying etiologies. In many large series, the most common reported etiology is iatrogenic in up to 48% of cases of vocal fold motion impairment,1−5 usually from neck surgery, such as spine or thyroid surgery. In most cases, this results in a varying degree of glottic insufficiency depending on the resting position of the impaired vocal fold, as well as potential synkinesis and a possible degree of pharyngeal dysfunction. Indeed, the recurrent laryngeal nerve (RLN) has been shown to contribute, at least to some degree, to the innervation of the inferior pharyngeal constrictor and cricopharyngeal muscle.6−8 Thus, patients will typically report dysphonia, but might also complain of dysphagia.9 According to various reports using functional endoscopic evaluation of swallowing or videofluoroscopic swallow studies, the rate of aspiration in patient with unilateral vocal fold motion impairment (UVFMI) can be anywhere between 23% and 56%.3,4,9−12 Accepted for publication August 6, 2019. Funding: No financial supporter of this study. Conflict of Interests: The authors declare that they have no conflict of interest. Meeting: Presented at ALA meeting, COSM 2018, National Harbor, MD, April 18−20. From the *Department of Otorhinolaryngology, Head and Neck Surgery, Ibni Sina Hospital, Ankara University School of Medicine, Ankara, Turkey; yDepartment of Surgery, Division of Otolaryngology, Head and Neck Surgery, Centre Hospitalier Universitaire de Sherbrooke, Sherbrooke, Quebec, Canada; zDepartment of Otorhinolaryngology, Head and Neck Surgery, Kocaeli University School of Medicine, Kocaeli, Turkey; and the xDepartment of Otolaryngology, Head and Neck Surgery, University of Washington Medical Center, Seattle, Washington. Address correspondence and reprint requests to Zahide C. Buyukatalay, 8th Floor, Alt{nda g, Ankara 06660, Turkey. 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.2019.08.005
Leder et al also reports that patients with UVFMI have about 2.5 times the odds of aspirating when compared with controls without motion impairment.10 There has been extensive research on the impact of UVFP on voice and phonation. However, if both dysphonia and dysphagia are present after UVFP, then the underlying pathophysiology for the swallowing impairment should be clarified for each patient since no two patients are identical in severity of recurrent nerve injury, extent of nerve regeneration, synkinesis posthealing, compensatory changes of the unaffected larynx, etc. Ineffective airway protection is suggested as being the primary cause of swallowing dysfunction in patients with UVFMI.4,5 At least three other deficits besides ineffective airway protection may accompany UVFP and cause or increase the severity of dysphagia and/ or aspiration. A study by Domer et al showed increase in the pharyngeal transit time and pharyngeal constriction ratio suggesting that pharyngeal weakness can also be present. Also, they found that the opening diameter of the upper esophageal sphincter (UES) was diminished, although not statistically different.12 Still, this might suggest that the loss of efferent input from the RLN impairs the ability of the UES to relax during the pharyngeal phase of deglutition (delayed relaxation of the UES), therefore contributing to the dysphagia. Finally, decreased sensation has been shown as a contributing factor of dysphagia in patients with UVFMI.4 Glottic insufficiency from UVFMI leads to reduced cough efficacy with impaired airway clearing after aspiration. Increased cough efficiency may be accomplished vocal fold augmentation, as demonstrated by trials indicating an increase in airflow measurements during voluntary
ARTICLE IN PRESS 2 cough after a vocal fold augmentation.13,14 Indeed, dysphagia seen with RLN injury may be more often than not multifactorial. Still, most treatment options for UVFP, vocal fold augmentation, laryngeal framework surgery, or laryngeal reinnervation, focus on optimizing glottic competence. The rates of penetration and aspiration have been found to improve on fluoroscopy after both injection medialization and type I thyroplasty, although in a limited manner.3,15 Laryngeal reinnervation using ansa cervicalis to RLN anastomosis was first reported by Frazier in 1924 in patients with bilateral vocal fold paralysis after a thyroidectomy.16 In 1986, Crumley and Izdebski published their surgical technique, which served as the basis for contemporary work on reinnervation.17 Although efficacy on objective and subjective voice-related outcomes of reinnervation has been shown in many studies,18−23 dysphagia outcomes have not been thoroughly studied. One study conducted by Zur and Carroll, looked at swallowing function after reinnervation surgery was performed for aspiration in three pediatric patients with UVFMI. Improved swallowing function on postoperative MBS was found 6 months after surgery.24 The aim of this study was to investigate the impact of laryngeal reinnervation, performed due to dysphonia, on swallowing outcomes in patients with UVFP. MATERIALS AND METHODS The charts of patients who underwent a reinnervation procedure for a UVFP at the University of Washington Medical Center between 2008 and 2017 were retrospectively reviewed. This research protocol was approved by the University of Washington Institutional Review Board. In addition to demographic characteristics, preoperative and postoperative patient reported outcomes questionnaires were collected. Dysphagia was assessed using the Eating Assessment Tool (EAT-10).25 The EAT-10 score closest to the one-year mark after surgery was used as the postoperative value. However, in order to discard the effect of the simultaneously performed injection laryngoplasty on the results, EAT-10 scores taken postoperatively before 6 months were not considered for the patients who did receive an injection. Patients with incomplete sets of data, any history of radiation therapy or insufficient follow-up were excluded. Voice Handicap Index (VHI-10)26 were also collected for descriptive purposes and again, scores taken before 6 months were not considered for patient having received an injection laryngoplasty. Statistical comparisons were made on the patients who described dysphagia and/or aspiration prior to reinnervation and whose preoperative EAT 10 scores were three and higher. The primary outcome was defined as a reduction in EAT-10 score. Descriptive statistics are shown as the mean (standard deviation) for normally distributed variables, a median (range) for non-normally distributed and as the number of cases (%) for nominal variables. Pre- and postoperative score analysis was done using Wilcoxon signed-rank test. A P < 0.05 value was accepted as statistically significant.
Journal of Voice, Vol. &&, No. &&, 2019
RESULTS Study population The charts of 22 patients diagnosed with UVFP and treated with a laryngeal reinnervation procedure were reviewed. Ten patients (6 men and 4 women) were found to have adequate data on swallowing before and after the laryngeal reinnervation. The mean age of our population at the time of diagnosis was 45.7 years (SD 13.3) and the paralysis was left-sided in seven patients. In all cases, the etiology was iatrogenic. Paralysis occurred after neck surgery (thyroidectomy, cervical spine, or paraganglioma) in seven patients, after thoracic surgery in two patients and intubation in one patient. The median duration of UVFP from symptom onset to date of surgery was 12.4 months (range\ 2.7−88.5 months). A total of six patients underwent ansa cervicalis to RLN anastomosis, while the remaining four patients had a neuromuscular pedicle. In six of the patients, an injection laryngoplasty with hyaluronic acid was done at the same time as the reinnervation surgery. The median follow-up time after procedure was 21.2 months (range 5.0−38.5 months) (Table 1).
EAT-10 EAT-10 scores of 6/10 patients were found to be three or higher before the reinnervation surgery and thus used in the analysis. Median EAT-10 scores of these six patients were 13 (3−23) in the preoperatively and seven (2−12) in the postoperative period. The decrease in the median score after surgery did not reach statistical significance (P = 0.138) (Figure 1).
VHI-10 The median preoperative VHI-10 score was 30 (range 18−40), and postoperative score was 10.5 (range 1−34). There was statistically significant improvement (P= 0.008) in median VHI-10 score after surgery. DISCUSSION The purpose of laryngeal reinnervation is to restore tone, bulk, and variable repositioning of the vocal fold.27,28 When compared to static medialization interventions such as injection augmentation or anterior thyroplasty, reinnervation may provide active resting tone to whichever muscle(s) becomes reinnervated, active air stream resistance on both inhalation and exhalation, and prevention of muscle atrophy.29 The laryngeal reinnervation procedure is considered safe30 and offers positive effects on UVFP in terms of acoustic, perceptual, electromyographic, and visual outcomes.22 Laryngeal reinnervation is potentially more successful if the procedure is performed within 2 years following nerve injury19 or in patients less than 60 years old.18 Although it is considered as being an effective and reliable surgical procedure, it is not as widely performed as other medialization techniques, such as framework surgery, due to the longer
ARTICLE IN PRESS
12 25 5 34 9 19 9 8 1 25
3
Abbreviations: A-to-R, ansa cervicalis to recurrent laryngeal nerve; F, female; L, left; M, male; NMP, nerve-muscle pedicle; N, no; R, right; Y, yes.
21 40 18 34 40 23 26 25 34 35 6 12 0 2 0 8 0 3 0 12 6 22 0 4 0 3 1 23 2 19 M M F F M M M M F F 1 2 3 4 5 6 7 8 9 10
53 44 44 43 35 23 33 60 66 56
Thoracic surgery Spine surgery Thyroid surgery Thyroid surgery Thyroid surgery Thoracic surgery Intubation Spine surgery Thyroid surgery Neck surgery
L R L R L L L R L L
88.5 14.5 2.7 19.6 9.1 6.5 17.0 36.6 10.4 5.5
A-to-R NMP NMP A-to-R A-to-R A-to-R A-to-R A-to-R NMP NMP
N N Y Y Y Y Y Y N N
Post EAT-10 Injection Augmentation Reinnervation Type Sex Patient
Age
Etiology
Side
Denervation Duration (Months)
TABLE 1. Patient Characteristics, Preoperative, and Postoperative Outcomes Scores
Dysphagia After Laryngeal Reinnervation
Pre EAT-10
Pre VHI-10
Post VHI-10
Zahide C. Buyukatalay, et al
FIGURE 1. Preoperative and postoperative EAT-10 scores. *, P = 0.138.
surgical time, the disadvantage of general anesthesia, and the long-term effect. The most common patient complaint in UVFP is dysphonia. However, it may also be associated with significant swallowing impairments and potential aspiration. Prior research shows that factors such as pharyngeal muscle weakness, delayed relaxation of the UES, and decreased laryngeal sensation also impact swallowing in these patients, along with glottal incompetence.31 These factors are much more common in central brainstem deficits or high vagal paralysis.32,33 Four patients in our study group who had postoperative paralysis due to cervical spine surgery or paraganglioma had much higher EAT-10 scores compared with patients with other etiologies (Table 1). Swallowing dysfunction and aspiration decreases the quality of life and may cause serious complications. This study retrospectively evaluated the effect of reinnervation for an indication of dysphonia on swallowing function by means of patient-reported outcomes. All surgeries were successful in the sense that the VHI-10 was significantly improved after the procedure. Although this surgical procedure was not actually planned for the treatment of swallowing disorder in these patients, their postoperative EAT-10 scores also improved. However, this improvement was not statistically significant, probably due to the small number of patients in our study. Interestingly, the improvement was more striking for these patients with a central etiology to their UVFP in which the preoperative score suggested a more profound dysphagia, probably due to the presence of all the aforementioned factors. Unfortunately, the paucity of patients does not allow for reliable subgroup analysis. Only one patient had a worsening of his EAT-10 score after the surgery, despite an improvement in his VHI-10. It is to note that this patient had been operated for an extensive mediastinal germ cell tumor at which time the left RLN was injured. Thus, it is possible that the reported worsening of dysphagia
ARTICLE IN PRESS 4 in this patient was secondary to an added esophageal issue, more so than from a change in the pharyngoesophageal segment. This study also adds to the safety profile of the procedure by suggesting that patients do not experience worsening dysphagia despite the theoretical loss of function associated with denervation of strap muscles from harvesting the ansa cervicalis. Obviously, this study presents some limitations. Firstly, this is a retrospective cohort with a small number of patients and thus, potential for sampling error. Secondly, only a patient reported outcomes questionnaire was used. Unfortunately, since laryngeal reinnervation is typically focused on the treatment of dysphonia, complete dysphagia workup was not routinely done, thereby limiting the dataset. Finally, hyaluronic acid injection augmentation was used concomitantly in many patients, which might have had an impact on short-term function. However, the clinical longevity of the filler material used in those patients (hyaluronic acid) was considered by excluding all patients with follow-up less than 6 months. A well-designed prospective study with a larger sample size and objective functional assessment of swallowing could help support the role of laryngeal reinnervation in the treatment of dysphagia in patients with UVFP.
Journal of Voice, Vol. &&, No. &&, 2019
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10. 11. 12.
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CONCLUSION Even though laryngeal reinnervation is not designed to be a treatment for dysphagia, our study shows a tendency for improvement of the EAT-10 score in UVFP patients after reinnervation surgery. SUPPLEMENTARY MATERIALS Supplementary material associated with this article can be found in the online version at https://doi.org/10.1016/j.jvoice. 2019.08.005.
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