World J Surg (2012) 36:1354–1360 DOI 10.1007/s00268-012-1481-8
Prospective Electromyographic Evaluation of Functional Postthyroidectomy Voice and Swallowing Symptoms Celestino P. Lombardi • Lucia D’Alatri • Maria R. Marchese • Daria Maccora Mauro Lo Monaco • Carmela De Crea • Marco Raffaelli
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Published online: 2 March 2012 Ó Socie´te´ Internationale de Chirurgie 2012
Abstract Background Voice and swallowing symptoms following thyroidectomy in the absence of any demonstration of laryngeal nerves injury are usually considered a functional outcome of uncomplicated operations, mainly related to scar formation and emotional reaction. They could be related to unapparent laryngeal nerve or cricothyroid (CT) muscle injuries detectable only by laryngeal electromyography (LEMG). We correlated such symptoms with LEMG patterns. Methods A total of 33 consenting patients undergoing total thyroidectomy (TT) were enrolled. Video-strobolaryngoscopy (VSL), acoustic voice analysis (AVA), and maximum phonation time (MPT) were performed preoperatively and 3 months postoperatively. Subjective evaluation of voice (Voice Impairment Score, or VIS) and swallowing (Swallowing Impairment Score, or SIS) were obtained preoperatively and 1 and 3 months postoperatively. At 1 month postoperatively LEMG was performed
examining thyroarytenoid (TA) and CT muscles to evaluate the inferior laryngeal nerve (ILN) and the external branch of the superior laryngeal nerve (EBSLN), respectively. Results One patient experienced transient vocal cord palsy and was excluded. The remaining 32 patients completed the postoperative evaluation. No significant difference was found between preoperative and postoperative AVA and MPT parameters. Mean VIS was significantly worse than preoperatively 1 and 3 months after TT. No significant difference was found between preoperative and postoperative SIS. LEMG evaluation of TA muscle showed decreased voluntary activity and spontaneous fibrillation potentials in one patient. LEMG of the CT muscle did not reveal any sign of EBSLN injury. Conclusions Patients frequently complain of subjective symptoms early after TT. LEMG demonstrated the absence of subclinical laryngeal nerve injury in all but one patient, confirming their functional nature.
Introduction This article is based on work that was the subject of an oral presentation at the ISW 2011–IAES free paper session, August 28 through September 1, 2011, Pacifico Yokohama, Japan. C. P. Lombardi D. Maccora C. De Crea (&) M. Raffaelli Department of Surgery, Division of General and Endocrine Surgery, Universita` Cattolica del Sacro Cuore, L.go A. Gemelli 8, Rome 00168, Italy e-mail:
[email protected] L. D’Alatri M. R. Marchese Institute of Otolaryngology, Universita` Cattolica del Sacro Cuore, L.go A. Gemelli 8, Rome 00168, Italy M. L. Monaco Institute of Neurology, Universita` Cattolica del Sacro Cuore, L.go A. Gemelli 8, Rome 00168, Italy
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Voice disturbances and related swallowing impairment after thyroidectomy have traditionally been attributed to direct injury to laryngeal nerves, resulting in vocal cord dysfunction. Nevertheless, it is well known among endocrine surgeons that following thyroidectomy most patients complain of some voice and swallowing disturbances, even in the absence of laryngeal nerve injury and video-strobolaryngoscopy (VSL) alterations [1–8]. This functional postthyroidectomy syndrome includes a broad spectrum of symptoms that are highly variable from patient to patient. In the recent literature, great interest has been paid to the occurrence of these voice and swallowing impairments that are related to thyroidectomy in the absence of laryngeal
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nerve injury, with particular attention on their prevalence, pathogenesis, and functional, clinical, and medicolegal implications [1–6, 9–15]. The prevalence and severity of the voice and swallowing symptoms tend to resolve with time [3, 15]. Moreover, at long-term evaluation after thyroidectomy, patients usually experience subjective amelioration of preoperative voice and swallowing performances and symptoms, if present [15, 16]. These symptoms may arise from cordal or cricopharyngeal dysfunctions (including the inability to close the glottis completely) related to alterations of the motor and sensory branches of the inferior laryngeal nerve (ILN) to the inferior constrictor muscle and laryngeal mucosa [17]. Other causes have been suggested as well, including arytenoid trauma following endotracheal intubation [1], surgical trauma, modification of the vascular supply and venous drainage of the larynx [5], local pain in the neck [3], cricothyroid dysfunction [1, 2, 5], strap muscle malfunction or a lesion of the perithyroidal neural plexus [4–6], intraoperative injury of the fine anastomotic branches connecting the ILN and the external branch of the superior laryngeal nerve (EBSLN) and/or one of their anastomosis with the sympathetic cervical chain [3, 10, 18], laryngotracheal fixation with impairment of vertical movement [1, 4–6] and psychological reaction to the operation [3, 5]. Recently, ILN edema following dissection has been offered as a possible cause of voice changes following thyroidectomy in the absence of vocal cord paralysis [19]. Most voice and swallowing symptoms following thyroidectomy, in the absence of any demonstration of laryngeal nerve injury, are usually considered functional outcome of an otherwise uncomplicated operation, mainly related to scar formation and emotional reaction. Nonetheless, they could be related to clinically unapparent laryngeal nerves or cricothyroid (CT) muscle injury detectable only by means of laryngeal electromyography (LEMG). Despite increasing interest, prospective data about LEMG evaluation of the functional postthyroidectomy syndrome are lacking. The discrepancies between subjective and objective voice and swallowing analyses can be studied, and maybe better understood, through use of LEMG to confirm the integrity of the laryngeal nerves and muscles. LEMG can show nervous alterations that may not be detectable at laryngoscopic examination. The purpose of this study was to correlate prospectively voice and swallowing symptoms following thyroidectomy with LEMG patterns.
Materials and methods Patients scheduled to undergo total thyroidectomy (TT) from November 2009 to December 2010 were considered
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eligible for this study. Exclusion criteria were age \21 and [65 years, previous vocal fold paralysis, history of voice or laryngeal disease requiring therapy or of pulmonary disease; previous neck surgery; malignancy other than papillary thyroid carcinoma. Patients showing signs of ILN after thyroidectomy or EBSLN palsy at VSL examination were excluded from the study. Among 1,177 patients who underwent TT during this period, 80 met the inclusion criteria and were considered eligible and accepted as participants in the study. The recruited patients signed an informed consent. The local ethics committee approved the study protocol. Surgical technique Patients undergoing both conventional thyroidectomy (CoT) and video-assisted thyroidectomy (VAT) were included in the study. All the surgical procedures were performed by an experienced endocrine surgeon or by a resident operating under supervision. TT is defined as total bilateral extracapsular thyroidectomy. Surgical techniques for both CoT and VAT have been already described elsewhere [3]. During every thyroid operation, we recommend systematic and prompt identification of the ILN. After its identification, the surgeon should follow the ILN upward until it enters the larynx. The EBSLN is not routinely exposed. The superior thyroid artery and vein are individually ligated close to the thyroid capsule to avoid injury to the ESBLN. Lesions of the CT muscle due to electrocoagulation or manual retraction are avoided. Patients assessment Video-strobolaryngoscopy, acoustic voice analysis (AVA), maximum phonation time (MPT), and self-assessment of voice and swallowing function were evaluated in all patients. The VSL was conducted the day before operation, 2 days after surgery, and 3 months later. AVA and MPT were performed before TT and 3 months after surgery. Patients’ subjective voice and swallowing evaluations were conducted preoperatively and at 1 month and 3 months after surgery. One month after thyroidectomy, LEMG was performed examining the thyroarytenoid (TA) and CT muscles to evaluate both the ILN and the EBSLN, respectively. Video-strobolaryngoscopy Video-strobolaryngoscopy was performed using a 70° rigid laryngoscope (model RLS 9100 B; Kay Elemetrics, Lincoln Park, NJ, USA) to assess vocal folds motion impairment (ILN injury) as well as bowing, inferior displacement of the vocal fold, regularity and symmetry of the mucosal
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traveling wave, and degree of glottic closure (EBSLN injury).
World J Surg (2012) 36:1354–1360 Table 1 Subjective voice evaluation questionnaire Parameter
Never (0)
Almost never (1)
Sometimes (2)
Often (3)
Always (4)
Acoustic voice analysis Objective voice analysis was performed using the MultiDimensional Voice Program (MDVP), model 5105, and the Voice Range Profile (VRP) program, model 4326, as well as Computerized Speech Lab, model 4500B (all from Kay Elemetrics). Recording was done with a microphone (model SM48; Shure, Evanston IL, USA) positioned at an angle of 45° and at a distance of 20 cm from the patient’s mouth. The microphone saturation input was fixed at 6/9 of CH1, and the environmental noise was \30 dB SPL. For MDVP analysis, after three training emissions, a sustained vowel /a/, produced at a comfortable pitch and loudness level for at least 5 s, was recorded with a sampling rate of 50,000 Hz. We selected an interval of 3 s from the midportion of each vowel. The following parameters were analyzed: mean frequency (F0, Hz); noise-to-harmonic ratio (NHR), jitter (%), and shimmer (%). For the VRP analysis, patients were instructed to phonate using a sustained vowel /a/ as loud and as soft as possible from the lowest to the highest frequencies. An automated procedure was used to obtain a voice range profile. Measurements derived from the VRP were the assessment of the lowest (Flow) and the highest (Fhigh) frequencies and the number of semitones. Finally, the MPT was obtained by having the patient sustain the vowel /a/ for as long as possible on a single breath. The longest of three attempts was calculated as the MPT. Subjective voice and swallowing evaluation The patient was asked a series of questions related to the frequency of voice and swallowing abnormalities using two specifically designed questionnaires (Tables 1, 2). These questionnaires have been already described in detail and were used in previous studies [3, 12, 15]. The scores resulting from these questionnaires were defined as the Voice Impairment Score (VIS) and the Swallowing Impairment Score (SIS). The VIS varied from a minimum score of 0 (no voice alterations) to a maximum of 40 (greatest voice impairment). The SIS ranged from a minimum of 0 (no swallowing alterations) to a maximum of 24 (greatest swallowing impairment). Laryngeal electromyography One month after TT, patients underwent bilateral electromyography (EMG) examination of the TA muscle (Fig. 1) and CT muscle (Fig. 2) to evaluate the ILN and the
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1. My voice is hoarse 2. My voice is breathy and weak 3. I have difficulty singing and yelling 4. The pitch of my voice is lower 5. My voice is monotonous 6. I run out of breath when I talk 7. My voice changes during the day 8. It takes a great effort to speak 9. The clarity of my voice is unpredictable 10. I feel vocal fatigue VIS total VIS: voice impairment score VIS is the sum of all of the scoring on the questionnaire (lowest to highest possible scores: 0–40)
EBSLN, respectively. With the patient’s neck extended, the TA muscle was approached by inserting a needle through the cricothyroid ligament approximately 0.5 cm from the midline. The needle was then angled superiorly 30°–45° to an approximate depth of 1–2 cm. The position of the needle was validated by asking the patient to repeat a sustained vowel /i/, causing a simultaneous sharp and sustained increase in LEMG activity. The CT was identified 1 cm off the midline, angling directly toward the cricoid cartilage. The size and recruitment of motor unit potentials were evaluated to judge the loss of motor units. Denervation activity (i.e., the presence of sharp waves and fibrillation potentials) was investigated at rest to identify acute axonal injury.
World J Surg (2012) 36:1354–1360 Table 2 Subjective swallowing evaluation by questionnaire
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Parameter
Never (0)
Nearly never (1)
Sometimes (2)
Often (3)
Always (4)
1. I make a great effort to swallow 2. I feel a sensation of an hypopharyngeal obstacle during swallowing SIS: swallowing impairment score SIS is the sum of all of the scoring on the questionnaire (lowest to highest possible scores: 0–24)
3. I feel pharyngeal discomfort during bolus transit 4. I cough during bolus transit 5. I feel sensation of foreign body in pharynx 6. I have some difficulty swallowing fluids SIS total
Statistical analysis Statistical analysis was performed using a commercially available statistical software package (SPSS 15.0 for Windows; SPSS, Chicago, Il, USA). The analysis of variance (ANOVA) for repeated measures was used for continuous variables and the v2 test for categoric variables. A value of P \ 0.05 was considered significant.
included in our study. There were 7 (21.9%) men and 25 (78.1%) women, with a mean age of 44.5 ± 10.7 years (range 27–63 years). The final histologic examination of the resected tissue confirmed benign diseases in 19 patients (59.4%) and papillary thyroid carcinoma in 13 cases (40.6%). The mean weight of the surgical specimens was 27.8 ± 24.9 g (range 6–111 g). Acoustic analysis
Results Among the 80 selected patients, 1 (1.2%) experienced transient unilateral ILN palsy, documented by early postoperative VSL, and was excluded from the study. This patient recovered within 1 month after surgery. In all, 47 of the remaining 79 (59.5%) patients refused to undergo follow-up consultation because of the absence of any subjective symptoms and/or they lived far from the hospital and/or they were concerned about the LEMG examination. Overall, 32 patients completed the study protocol and were
The acoustic parameters obtained from the MDVP and VRP analyses are shown in Table 3. No significant differences were found among the preoperative and postoperative mean values of the MDVP and VRP parameters (P = NS) (Table 3). Subjective voice and swallowing evaluation The mean VIS was significantly increased at 1 and 3 months after the surgery versus the preoperative value (7.09 ± 10.03 and 4.37 ± 7.44 vs. 1.84 ± 2.93, respectively;
Fig. 1 Normal laryngeal electromyography (LEMG) pattern for thyroarytenoid muscle
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Fig. 2 Normal LEMG pattern for cricothyroid muscle
Table 3 Comparison of preoperative and postoperative results of various analyses
Table 4 Comparison of mean preoperative and postoperative VIS and SIS
Analysis
Preop.
At 3 months postop.
Parameter
Preop. (a)
F0 (Hz)
175.05 ± 29.94
179.33 ± 32.67
NS
0.58 ± 0.38)
NS
VIS
1.84 ± 2.93
Jitter (%)
0.63 ± 0.22
P*
Shimmer (%)
4.63 ± 0.74
3.98 ± 1.25
NS
NHR (dB)
0.11 ± 0.01
0.14 ± 0.01
NS
P** SIS P***
2.15 ± 3.48
At 1 month postop. (b)
4.37 ± 7.44 \0.05
2.81 ± 3.63 NS
1.65 ± 2.56 NS
17.80 ± 6.60
19.27 ± 6.14
NS
143.07 ± 30.03
154.62 ± 35.7
NS
Results are the mean ± SD
Fhigh (Hz) No. of semitones
413.07 ± 66.05) 13.04 ± 1.98
392.41 ± 63.77 15.02 ± 2.71
NS NS
* ANOVA test for repeated measurements
* Analysis of variance (ANOVA) test for repeated measures
P \ 0.05) (Table 4). At 3 months after surgery, the mean VIS was significantly improved with respect to that obtained 1 month after TT. The mean postoperative SIS at 1 and 3 months after surgery did not differ significantly from the preoperative SIS (2.81 ± 3.63 and 1.65 ± 2.56 vs. 2.15 ± 3.48, respectively; P = NS) (Table 4). Hence, swallowing alterations showed a tendency to increase at 1 month after TT and to have improved at 3 months (Table 4). Laryngeal electromyography A total of 31 patients presented a normal LEMG pattern for TA on both sides. In the remaining patient, the LEMG of
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\0.05
7.09 ± 10.03
MPT (s)
MDVP multidimensional voice program, MPT maximum phonation time, VRP voice range profile, NHR noise/harmonic ratio
P*
\0.05
Flow (Hz)
Results are the means ± SD
At 3 months postop. (c)
NS
** (a) vs. (b), P \ 0.05; (a) vs. (c), P \ 0.05 *** (a) vs. (b), NS; (a) vs. (c), NS
the TA muscle revealed diminished motor unit recruitment and the presence of some spontaneous activity as fibrillation potentials. No patient showed LEMG signs of EBSLN injury or CT muscle damage.
Discussion The results of the present study confirm that subjective perception of voice and swallowing alterations is frequent soon after an otherwise uncomplicated thyroidectomy. In other words, in the absence of laryngeal nerve injury detectable by means of VSL, patients frequently complained of some voice and vocal disturbances. This is in agreement with our previously published studies [3, 12, 15] and with reports from others [1–4, 7, 8, 10–12, 16, 20]. Such symptoms usually tend to ameliorate over time, usually resolving within 3 months after surgery [15, 20].
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We have recently demonstrated that at long-term follow-up ([1 year after the operation) thyroidectomized patients usually experience subjective amelioration of their voice and swallowing performances [15]. This outcome could be related to the resolution of mild preoperative compressive symptoms related to the thyroid disease. Several causes for voice alteration after uncomplicated thyroidectomy have been suggested. Unfortunately, the main limitation of previous studies was the lack of LEMG examination. As a consequence, in the absence of EMG demonstration of the integrity of laryngeal nerve function, it was not possible to exclude minor laryngeal nerve injury that is undetectable by VSL. Indeed, it has been demonstrated that selected objective voice measures are abnormal in patients with EBSLN injuries [21]. Also, AVA modifications generally reported early after thyroidectomy in patients complaining of vocal alterations without any VSL modification (i.e., reduction in the MPT, F0, Fhigh, Flow, number of semitones) [2, 4, 11, 13, 14, 21] have been demonstrated to be related to EBSLN injury [4, 21]. Conversely, it is well known that laryngoscopic findings of such injuries are typically subtle [22], and confirmatory LEMG of the CT muscle is considered the gold standard for diagnosing EBSLN injury [16]. It has been estimated that for a vocal cord palsy to occur, at least 50% of the motor axons must be nonfunctional in the ILN [19, 23]. ILN injury involving less than half of the nerve fibers is not detectable by laryngoscopic examination. To the best of our knowledge, this study is the first in which LEMG was performed in patients who underwent thyroidectomy without VSL evidence of laryngeal nerve injury. Its findings were correlated to voice and swallowing postoperative impairment. Surprisingly, only 1 of the 33 (3.0%) patients displayed LEMG modification of the TA muscle; and partial injury of less than a half of the nerve fibers was supposed. In all of the other cases (32/33, 97%), the LEMG examination was completely normal for both the CA and TA muscles. This finding strongly and unequivocally excludes any laryngeal nerve injury in almost all of the patients. In other words, subclinical inadvertent EBSLN or CA muscle lesions are unlike to be the unrecognized cause of such symptoms. Recently, it has been suggested that ILN edema related to surgical dissection (i.e., stretching) and consequent partial dysfunction related to neuroapraxia of \50% of nerve fibers play a role in the pathogenesis of functional voice alterations following thyroidectomy. Our study excluded such a mechanism, at least in most of the cases, as only one patient (3% of all the cases) showed LEMG signs of neuroapraxia. Consequently, we can assume that voice and swallowing modifications following thyroidectomy in the absence of
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VSL evidence of vocal cord dysfunction are absolutely functional in origin. This supports the hypothesis that such symptoms are usually determined by the normal healing process [3, 12, 15] or by a functional component related to local neck pain and emotional and psychological reaction to postoperative stress [3, 12, 15].
Conclusions The results of the present study confirm that following thyroidectomy patients complain of some voice and swallowing disturbances in the absence of objective voice modification. LEMG demonstrated the absence of subclinical laryngeal nerve injury in all but one of the patients in the present series. It excluded subclinical laryngeal nerve injury and inadvertent cricothyroid muscle lesions as the potential pathogenesis, unequivocally confirming the functional nature of these problems. As a consequence, we can consider this cohort of symptoms as a functional postthyroidectomy syndrome and a common consequence of thyroid surgery. However, related symptoms can dramatically influence the quality of life of patients who undergo thyroidectomy, especially if they are professional voice users. For this reason, physicians should be aware of this subjective discomfort and inform their patients about the frequency of this presentation. The patients can be reassured about the usually transient and self-limiting nature of the problems because of their functional origin. Conflict of interest article.
No competing interests are declared for this
References 1. Stojadinovic A, Shaha AR, Orlikoff RF et al (2002) Prospective functional voice assessment in patients undergoing thyroid surgery. Ann Surg 236:823–832 2. Sinagra DL, Montesinos MR, Tacchi VA et al (2004) Voice changes after thyroidectomy recurrent laryngeal nerve injury. J Am Coll Surg 199:556–560 3. Lombardi CP, Raffaelli M, D’Alatri L et al (2006) Voice and swallowing changes after thyroidectomy in patients without inferior laryngeal nerve injuries. Surgery 140:1026–1034 4. Hong KH, Kim YK (1997) Phonatory characteristics of patients undergoing thyroidectomy without laryngeal nerve injury. Otolaryngol Head Neck Surg 117:399–404 5. Debruyne F, Ostyn F, Delaere P et al (1997) Acoustic analysis of the speaking voice after thyroidectomy. J Voice 11:479–482 6. McIvor NP, Flint DJ, Gillibrand J et al (2000) Thyroid surgery and voice-related outcomes. Aust N Z J Surg 70:179–183 7. Henry LR, Pearl Salomon N, Howard R et al (2008) The functional impact on voice of sternothyroid muscle division during thyroidectomy. Ann Surg Oncol 15:2027–2033 8. Akyildiz S, Ogut F, Akyildiz M et al (2008) A multivariate analysis of objective voice changes after thyroidectomy without
123
1360
9.
10.
11.
12.
13.
14.
15.
laryngeal nerve injury. Arch Otolaryngol Head Neck Surg 134:596–602 Rosato L, Carlevato MT, De Toma G et al (2005) Recurrent laryngeal nerve damage and phonetic modifications after total thyroidectomy: surgical malpractice only or predictable sequence? World J Surg 29:780–784. doi:10.1007/s00268-005-7653-z Pereira JA, Girvent M, Sancho JJ et al (2003) Prevalence of longterm upper aero-digestive symptoms after uncomplicated bilateral thyroidectomy. Surgery 133:318–322 Stojadinovic A, Henry LR, Howard RS et al (2008) Prospective trial of voice outcome after thyroidectomy: evaluation of patients-reported voice assessments in identifyng postthyroidectomy dysfonia. Surgery 143:732–742 Lombardi CP, Raffaelli M, D’Alatri L et al (2008) Video-assisted thyroidectomy significantly reduces the risk of early postthyroidectomy voice and swallowing symptoms. World J Surg 32: 693–700. doi:10.1007/s00268-007-9443-2 Musholt TJ, Musholt PB, Garm J et al (2006) Changes of the speaking and singing voice after thyroid or parathyroid surgery. Surgery 140:978–989 Soylu L, Ozbas S, Uslu HY et al (2007) The evaluation of the causes of subjective voice disturbances after thyroid surgery. Am J Surg 194:317–322 Lombardi CP, Raffaelli M, De Crea C et al (2009) Long-term outcome of functional post-thyroidectomy voice and swallowing symptoms. Surgery 146:1074–1081
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World J Surg (2012) 36:1354–1360 16. Henry LR, Helou LB, Solomon NP et al (2010) Functional voice outcomes after thyroidectomy: an assessment of the Dysphonia Severity Index (DSI) after thyroidectomy. Surgery 147:861–870 17. Randolph GW (2003) Surgical anatomy of the recurrent laryngeal nerve. In: Randolph GW (ed) Surgery of the Thyroid and Parathyroid Glands. Saunders, Philadelphia, pp 300–342 18. Raffaelli M, Iacobone M, Henry JF (2000) The ‘‘false’’ nonrecurrent inferior laryngeal nerve. Surgery 128:1082–1087 19. Serpell JW, Woodruff S, Bailey M et al (2011) Recurrent laryngeal nerve diameter increases during thyroidectomy. Ann Surg Oncol 18:1742–1747 20. Van Lierde K, D’Haeseleer E, Wuyts FL et al (2010) Impact of thyroidectomy without laryngeal nerve injury on vocal quality characteristics: an objective multiparameter approach. Laryngoscope 120:338–345 21. Robinson JL, Mandel S, Sataloff RT (2005) Objective voice measures in nonsinging patients with unilateral superior laryngeal nerve paresis. J Voice 19:665–667 22. Sataloff RT, Praneetvatakul P, Heuer RJ et al (2010) Laryngeal electromyography: clinical application. J Voice 24:228–234 23. Mu L, Yang S (1991) An experimental study on the laryngeal electromyography and visual observations in varying types of surgical injuries to the unilateral recurrent laryngeal nerve in the neck. Laryngoscope 101:699–708
