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ORIGINAL ARTICLE -Muscle Pedicle Flap Implantation Combined With Arytenoid Adduction

Eiji Yumoto, MD; Tetsuji Sanuki, MD; Yutaka Toya, MD; Narihiro Kodama; Yoshihiko Kumai, MD

Objectives: To describe a new technique of nerve- Main Outcome Measures: The maximum phonation muscle pedicle (NMP) flap implantation combined with time, mean airflow rate, pitch range, and acoustic para- arytenoid adduction (AA) to treat dysphonia due to uni- meters (jitter, shimmer, and harmonics to noise ratio) were lateral vocal fold paralysis and to examine postoperative evaluated before surgery and twice after surgery. vocal function. Results: All parameters improved significantly after sur- Study Design: Retrospective review of clinical gery (PϽ.01). The measurements for maximum phonation records. time, mean airflow rate, and harmonics to noise ratio were within normal ranges after surgery. Furthermore, the maxi- Setting: Tertiary academic center. mum phonation time and jitter were significantly improved after long-term follow-up compared with early postopera- Patients: Twenty-two consecutive patients underwent tive measurements (PϽ.01 and PϽ.05, respectively). NMP flap implantation with AA and were followed up short term over a period of 1 to 6 months (mean, 2.9 Conclusions: Precise harvest of an NMP flap and its place- months) and long term over a period of 7 to 36 months ment directly onto the thyroarytenoid muscle combined (mean, 21.4 months). with AA provided excellent vocal function. The NMP Interventions: An NMP flap was made using an ansa cer- method may have played a certain role in the improve- vicalis branch and a piece of the sternohyoid muscle. A win- ment of postoperative vocal function, although further study dow was opened in the thyroid ala at the level of the vocal with electromyographic examination is required to clarify fold. Then, AA was performed and the NMP flap was se- the innervation status of the thyroarytenoid muscle. curely implanted onto the thyroarytenoid muscle through the window under microscopic guidance. Arch Otolaryngol Head Surg. 2010;136(10):965-969

MPROVEMENT IN BREATHY DYSPHO- muscle pedicle (NMP) flap implantation nia due to unilateral vocal fold pa- onto the TA muscle through a window in ralysis (UVFP) is usually achieved the thyroid ala. May and Beery4 also re- by implementing various kinds of ported positive effects of NMP implanta- phonosurgical procedures, in- tion onto the lateral cludingI intracordal injection, type I thy- on breathy dysphonia. However, to our roplasty, arytenoid adduction (AA), and knowledge, no studies, except those noted combinations thereof. However, some pa- above, have reported further results regard- tients do not recover “normal” voices af- ing the use of the NMP method. Although ter surgery.1,2 Normal voices can be at- immediate reconstruction of the severed re- tained by providing the immobile vocal current laryngeal nerve (RLN) can result in fold with the median location and the excellent vocal function,5 immediate recon- struction is not feasible in most patients be- cause they usually seek treatment only af- Video available online at ter the onset of paralysis. We examined the www.archoto.com effects of an NMP method in rats and con- firmed the effectiveness of the method to re- symmetrical bulk and tension of the unaf- verse or repair atrophic changes in the long- fected vocal fold. Because the phonosurgi- term denervated TA muscle.6,7 We refined cal procedures offer “static” adjustment of the technique of NMP flap implantation these features, the thyroarytenoid muscle onto the TA muscle and have applied this Author Affiliations: Department of (TA) does not work as the body of the im- innovative method, together with AA, in the Otolaryngology–Head and Neck mobile vocal fold, resulting in little contri- treatment of breathy dysphonia due to Surgery, Graduate School of bution to voice production and tuning. UVFP since July 2002. We also refined the Medicine, Kumamoto To restore tonus of the immobile vocal original AA method of Isshiki et al.8 The University, Kumamoto, Japan. fold, Tucker3 described a method of nerve- goals of the present study were to describe

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©2010 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/01/2021 Cranial side Thyroid notch Cranial side

10-12 mm 2 mm 5-7 mm

3-5 mm

Inferior tubercle

Figure 3. An operative view after completion of arytenoid adduction in the same patient as in Figure 1. The dotted line indicates the estimated level of Inferior tubercle the vocal fold. The asterisks indicate the silicone shim; arrowheads, the exposed thyroarytenoid muscle. Figure 1. Location and design of the window in the thyroid ala (58-year-old man, left side). The dotted line indicates the estimated level of the vocal fold. respectively. The use of a relatively thin tube allows the vocal fold to adduct passively through the anteroinferior pull of the Cranial side muscular process of the . An incision is made horizontally from the midline to the anterior margin of the sternocleidomastoid muscle at the level of the inferior one-fourth of the . The space anterior to the sternocleidomastoid muscle is opened, expos- ing the internal jugular vein where the (AC) nerve (superior root) and its branch to the are iden- tified. The omohyoid muscle is transected, and the AC nerve is followed until it enters the sternohyoid (SH) muscle. Elec- trical stimulation is applied to confirm the presence of nerve fibers innervating the SH muscle. A relatively thick AC branch to the SH muscle is harvested together with a 3ϫ3-mm piece of the muscle at the point of nerve entrance to the muscle to form a NMP flap. The NMP flap is elevated with meticulous care, and the course is reversed cranially so that the NMP flap Nerve-muscle pedicle flap reaches the midportion of the thyroid ala with no tension. The Figure 2. A nerve-muscle pedicle flap, which reached the window without inferior root of the AC nerve is usually preserved. tension in the same patient as in Figure 1. Cartilage is not yet drilled out. Arytenoid adduction is performed according to the method of Isshiki et al.8 The cricoarytenoid joint is not opened in our technique. Care is taken to preserve the external branch of the our refined technique in detail and to report patient data superior laryngeal nerve and to avoid injury to the pyriform from vocal function tests. The study was approved by the sinus mucosa. The muscular process is grasped with a pair of institutional review board of the Graduate School of Medi- Adson forceps to confirm the passive mobility of the aryte- cine, Kumamoto University. noid. This step is necessary to estimate the degree of traction of the muscular process. Two 3-0 nylon threads are then placed METHODS through the muscular process and tied for later use. The location and design of a window in the thyroid ala is shown in Figure 1. The window base is set 2 to 3 mm cranial PATIENTS to the lower edge of the thyroid ala. Diamond-tip drills are used under microscopic control to make a window with the inner Twenty-four consecutive patients with breathy dysphonia due perichondrium intact. Figure 2 shows the NMP flap, which to UVFP underwent NMP flap implantation together with AA reaches the window without tension. After the cartilage in the between July 2002 and September 2007 at Kumamoto Univer- window is drilled out, the perichondrium is excised with elec- sity Hospital, Kumamoto, Japan. Two patients, however, were trocautery, and the TA muscle is carefully exposed as wide as excluded. One patient with left vocal fold paralysis underwent possible to secure contact of the NMP flap with the TA muscle. total thyroidectomy simultaneously; the next day, she under- The nylon thread tied to the muscular process is intro- went a tracheostomy because of paralysis of the preopera- duced to the anterior surface of the thyroid ala medially from tively mobile right vocal fold. Another patient was not fol- the inferior tubercle, with one end through the lower edge of lowed up for the requisite time. Therefore, our study included the window and the other end through the cricothyroid mem- 22 patients who were followed up for more than 6 months. brane. Another thread is also introduced in the same way, slightly more medially. These threads pull the muscular process in a SURGICAL PROCEDURE direction similar to the lateral cricoarytenoid muscle and are secured using a silicone shim. Figure 3 shows a picture after General anesthesia with endotracheal intubation is adminis- completion of AA. The TA muscle bundle is widely exposed tered. The patient lies in the supine position with a pillow un- (Figure 3, arrowheads). der the shoulder. Generally, an endotracheal tube with an in- The muscle piece of the NMP flap is positioned in the win- ner diameter of 6 or 7 mm is used for female or male patients, dow to make as wide contact as possible with the TA muscle

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©2010 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/01/2021 and is secured with the surrounding tissues using 8-0 nylon threads. This step is crucial and is performed under micro- Cranial side scopic guidance. Subsequently, the window is covered with the outer perichondium (Figure 4). Meticulous hemostasis is un- dertaken throughout the operation. Two Penrose drains are placed in the wound, one at the site of the NMP flap harvest and the other toward the paraglottic space.

ASSESSMENT OF VOCAL FUNCTION

The vocal function of each patient was assessed before surgery and within and after 6 months after surgery. To measure the maxi- mum phonation time (MPT) and mean airflow rate (MFR), each patient was asked to sustain the vowel /a/ at a comfortable pitch AC nerve and loudness for as long as possible. Of the 2 consecutive mea- surements, the longer performance was analyzed. Pitch range was Figure 4. An operative view after completion of nerve-muscle pedicle flap also measured and expressed in semitone scale. These para- implantation (51-year-old woman, left side). The asterisks indicate the outer perichondrium, which covers the window; AC, ansa cervicalis. meters were measured using a phonation analyzer (SK-99; Na- gashima, Tokyo, Japan). The preoperative and postoperative voices were recorded on a cassette tape recorder (TCD5M; Sony, Tokyo, The preoperative voice recording was missing in one pa- Japan) or a digital recorder (PMD670; Marantz, Kanagawa, Ja- tient, and the vocal function test was not carried out be- pan) in a soundproof room using a dynamic microphone (FP280; fore surgery in another patient because she underwent a Sony) at a mouth-to-microphone distance of 30 cm. For the acous- tracheostomy. Acoustic analysis was not possible in 4 pre- tic analysis, each patient was asked to sustain the vowel /a/ at a comfortable pitch and loudness. Jitter, shimmer, and harmonics operative voice samples because of poor voice quality and to noise ratio (HNR) were measured from a relatively stable part short duration. Three patients did not undergo vocal func- of the recording using the Multi-Dimensional Voice Program tion testing within 6 months after surgery. (MDVP; KayPentax, Lincoln Park, New Jersey). The HNR was Figure 5 summarizes the results of preoperative and ϫ calculated in the following way: HNR=10 log10(1/NHR), where postoperative vocal function tests. All parameters im- NHR is the noise to harmonics ratio. proved significantly after surgery. For reference, the Table shows the mean (SD) ranges obtained from healthy STATISTICAL ANALYSIS Japanese men and women in their 50s for MPT, MFR, and pitch range.9 The normal ranges for jitter (Ͻ1.04%), All measurements are shown as mean (SD). The paired t test shimmer (Ͻ3.81%), and HNR (Ͻ7.21 dB) were calcu- was used to compare the measurements of 3 different occa- lated according to the MDVP software assessment by Kay- sions: before surgery, at short-term follow-up, and at long- Pentax. The measurements for MPT, MFR, and HNR were term follow-up (StatView; SAS Institute, Cary, North Caro- lina). The significance level was set at PϽ.05. within normal ranges after surgery. Furthermore, the MPT and jitter were significantly improved after long-term fol- low-up compared with early postoperative measure- RESULTS ments (PϽ.01 and PϽ.05, respectively). The video (avail- able at http://www.archoto.com) shows preoperative and The study included 10 men and 12 women (age range, postoperative stroboscopic images of a representative case. 28-82 years; mean [SD], 56.6 [16.4] years). The left side One patient complained of sudden inspiratory dys- was affected in 16 patients; the right, in 6. The period pnea on postoperative day 1 and immediately under- from onset to surgery ranged from 1 to 48 months (mean went a tracheostomy. However, laryngofiberscopy re- [SD], 15.6 [10.8] months); the short-term follow-up vealed that her glottis was wide on postoperative day 2, ranged from 1 to 6 months (mean [SD], 2.9 [1.2 months]); and the cause was considered to be paradoxical adduc- and the long-term follow-up ranged from 7 to 36 months tion of the healthy vocal fold as a result of vocal fold dys- (mean [SD], 21.4 [7.1] months). The cause of UVFP in function.10 Her stoma was subsequently closed; her con- the study patients is shown below. dition has not changed since then. In another patient, inspiratory dyspnea occurred suddenly on postopera- Cause No. of Patients tive day 3 as a result of laryngeal edema. A tracheos- Iatrogenic (postoperative) tomy was performed on an emergency basis. Her stoma Thyroid cancer 5 was closed a few days later, and her condition has not Graves disease 1 changed since then. No other postoperative complica- Aortic aneurysm 3 tion occurred. tumor 2 Cerebral aneurysm 2 Meningioma 1 COMMENT Vagal schwannoma 1 Lung cancer 1 Thyroid cancer 1 Laryngeal reinnervation can provide the affected vocal Subarachnoid hemorrhage 1 fold with bulk and tension. Procedures aiming at the re- Aortic aneurysm 1 innervation include direct anastomosis of the severed Idiopathic 3 stumps of the RLN, anastomosis between the RLN stumps Total 22 by interposition of a foreign nerve section, anastomosis

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Preoperative 5.2 (2.1) 713 (680) 7.6 ± (7.2) 7.67 (4.84) 12.28 (7.17) 5.42 (3.27) P < .001 P < .01 P < .01 P < .001 P < .01 P < .01 Short-term follow-up 13.1 (5.1) P < .001 145 (58) P < .01 14.0 ± (4.2) P < .01 2.08 (1.25) P < .001 6.70 (4.14) P < .01 8.00 (1.64) P < .01 P < .01 P = .57 P =.69 P < .05 P = .96 Long-term follow-up 17.5 (8.8) 150 (73) 14.9 ± (4.6) 1.54 (1.41) 6.04 (3.27) P = .50 8.02 (1.18)

Figure 5. Results of preoperative and postoperative phonatory function testing. The number of patients compared between preoperative and short-term follow-up measurements was 19 for aerodynamics and 14 for acoustic analysis; between preoperative and long-term follow-up measurements, 21 for aerodynamics and 16 for acoustic analysis; and between short- and long-term follow-up measurements, 19 for aerodynamics and 19 for acoustic analysis. HNR indicates harmonics to noise ratio; MFR, mean airflow rate; and MPT, maximum phonation time.

and its AC branch. The lower portion of the SH muscle is Table. Ranges for MPT, MFR, and Pitch Range Obtained invariably innervated by a prominent branch from the loop From Healthy Japanese Men and Women in Their 50s9 of the AC nerve. It branches farther, and 1 major branch is wider and contains more nerve fibers than the omohy- Parameter Men Women oid branch.20 Therefore, a larger number of regenerating MPT, s 12.5-30.4 14.2-19.8 axons are expected to reach the target muscle. Electrical MFR, mL/s 113-262 99-173 Pitch range, semitone 18.2-28.6 18.7-30.4 stimulation was always applied to confirm the presence of nerve fibers innervating the SH muscle. Second, the TA Abbreviations: HNR, harmonics to noise ratio; MFR, mean airflow rate; muscle was the target muscle in the present series and in MPT, maximum phonation time. Tucker’s 15 technique. In contrast, May and Beery4 sought to reinnervate the lateral cricoarytenoid muscle to medi- between the peripheral RLN stump and the AC nerve,11-14 alize the affected vocal fold. Seven of 29 patients in their and NMP flap implantation.3,4 The former 3 methods can- series experienced no improvement in their voices. Third, not usually be applied in patients with UVFP that is re- window opening, incising the inner perichondrium, ex- lated to neck operations because the peripheral stump posure of the TA muscle, and fixation of the NMP flap were of the RLN is buried in the cicatricial tissue. In contrast, crucial steps and were performed with great care under the NMP method provides a practical way of reinnervat- microscopic control in the present series. Fourth, AA was ing laryngeal muscles because the peripheral stump of performed together with NMP flap implantation to lo- the RLN is not required. cate the affected vocal fold at the median position, while Tucker3 first described an NMP method to reinner- Tucker15 performed a type I thyroplasty and May and Beery4 vate the unilaterally paralyzed and later com- did not combine another method. All patients in the pres- bined the NMP method with a type I thyroplasty.15 May ent series had relatively wide glottal gaps and required AA. and Beery4 also implanted a NMP flap onto the lateral Type I thyroplasty may not be indicated for combination cricoarytenoid muscle. To our knowledge, there are no with the NMP method because successful reinnervation other clinical reports on this subject. This paucity of data of the TA muscle provides the affected vocal fold with in- may be ascribed to a lack of consistent effects of the NMP creased bulk and tension. method reported in animal experiments. Some studies Kimura et al1 performed intracordal collagen injec- have used the NMP method successfully,16,17 whereas oth- tion in 40 patients who had undergone AA and whose ers have reported difficulty in achieving reliable results vocal fold geometry as observed with videostroboscopy with the procedure.18,19 Using a rat UVFP model, we found was inadequate. They reported that the mean MPT and that the NMP method was effective in repairing the atro- MFR were 15 seconds and 223 mL/s, respectively, after phic changes of the TA muscle, even in long-term de- injection. However, the perceptual quality of postinjec- nervated animals.6,7 Miyamaru et al7 also reported that tion voice remained G1 according to the Grade of the Se- stimulation of the AC nerve elicited action potentials of verity of Dysphonia, Roughness, Breathiness, Asthenic- the TA muscle. The occurrence of the evoked potentials ity, and Strain scale.21 Mortensen et al2 compared vocal of the TA muscle was attributable to successful reinner- function after AA combined with type I thyroplasty with vation via the transferred AC nerve through reconstruc- that after intracordal injection or type I thyroplasty alone tion of the neuromuscular junction. Formation and im- and found that there was a statistically significant differ- plantation of an NMP flap were carefully performed under ence between the 2 groups. The patients who under- microscopic control, and direct contact of the muscle flap went AA with type I thyroplasty had worse preoperative with the TA muscle fibers was later histologically ascer- function and better postoperative function. The postop- tained. Based on these experimental results, we have re- erative mean MPT and MFR in patients who underwent fined the technique of the NMP method and combined AA with type I thyroplasty were 14.8 seconds and 219 it with AA in the treatment of UVFP. mL/s, respectively. Mortensen and colleagues’ results dem- There are major differences between our surgical tech- onstrated that postoperative vocal function improved, but niques using the NMP method and combined surgery and not to “normal,” according to their description.2 In con- those of Tucker15 and May and Beery.4 First, we har- trast, in the present series, not only the mean values of vested an NMP flap from the SH muscle and its major AC all parameters measured improved significantly after sur- branch, although Tucker3,15 and May and Beery4 used an gery, but also the MPT, MFR, and HNR were within nor- NMP flap from the superior belly of the omohyoid muscle mal ranges (Figure 5 and Table). Furthermore, the MPT

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©2010 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/01/2021 and jitter improved significantly beyond 6 months after nical, and material support: Yumoto and Toya. Study su- surgery. These results suggested that an addition of the pervision: Yumoto. NMP method may have played a certain role in the im- Financial Disclosure: None reported. provement of postoperative vocal function. Online-Only Material: The video is available at http: Further study focusing on electromyographic exami- //www.archoto.com. nation is required to clarify the innervation status of the TA muscle. Also, long-term follow-up of vocal function, including aerodynamics, acoustic analysis, strobo- REFERENCES scopic assessment, and patients’ self evaluation, is in progress, and the results will be reported separately. 1. Kimura M, Nito T, Imagawa H, Tayama N, Chan RW. 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