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The evaluation of the causes of subjective voice disturbances after thyroid surgery
The American Journal of Surgery 194 (2007) 317–322
Clinical surgery–International
The evaluation of the causes of subjective voice disturbances after thyroid surgery Lutfi Soylu, M.D.a, Serdar Ozbas, M.D.b,*, Hatim Yahya Uslu, M.D.c, Savas Kocak, M.D.d a
General Surgery Department, Ankara University Medical School, Sýhhýye, 06430, Ankara, Turkey General Surgery Department, Adnan Menderes University Medical School, 09100, Aydin, Turkey c General Surgery Department, Ufuk University Medical School, Balgat, 06520, Ankara, Turkey d General Surgery Department, Division of Endocrine Surgery and Breast Diseases, Ankara University Medical School, Sýhhýye, 06430, Ankara, Turkey b
Manuscript received February 23, 2006; revised manuscript October 24, 2006
Abstract Background: Voice changes following thyroidectomy is a rare form of morbidity not infrequently encountered. Injury to the recurrent laryngeal nerve or external branch of the superior laryngeal nerve is the most well-known cause of post-thyroidectomy voice disturbances. However, voice dysfunction is a more complex entity. The aim of the current study was to assess the possible factors that influence voice changes after thyroidectomy. Methods: Forty-eight consecutive patients who had undergone thyroidectomy were studied. The acoustic voice analysis (mean vocal fundamental frequency [Fo], mean percentage vocal jitter and shimmer, and noise-to-harmonic ratio) and videolaryngostroboscopic examination of these patients were performed preoperatively, on the second postoperative day, and 3 months after the operation. The presence of subjective voice changes was recorded prospectively based on a symptom scale. Results: No major complications occurred perioperatively or in the postoperative period. Videolaryngostroboscopic examinations were normal in all patients before and after thyroidectomy. Eighteen (37.5%) patients complained of subjective voice changes in the early postoperative period and 7 (14.6%) of these were still uncomfortable after 3 months. Although the difference was significant by means of all acoustic voice parameters measured in the early postoperative period, Fo is the only parameter that continues to be significant after 3 months. Conclusions: Irrespective from recurrent laryngeal nerve and/or injuries to the external branch of the superior laryngeal nerve, voice may temporarily be affected by thyroidectomy. Most of the subjective complaints and acoustic voice parameters return to normal in a few months after surgery. © 2007 Excerpta Medica Inc. All rights reserved. Keywords: Thyroidectomy; Videolaryngostroboscopy; Voice; Acoustic voice parameters
Vocal dysfunction is one of the most important complications of thyroid surgery. Although recurrent laryngeal nerve (RLN) injury traditionally has been the most well-known neurogenic cause, 50% of patients with unilateral RLN palsy can be asymptomatic [1]. It is not always possible to preserve normal postoperative voice function, even though the identification and preservation of the RLNs has become a routine approach in modern thyroid surgery [2]. Another neurogenic voice-altering complication of thyroid surgery is * Corresponding author. Adnan Menderes University Medical School, General Surgery Department, 09100, Aydin, Turkey. Tel.: ⫹90 256 4441256, ⫹90 533 6880266 (mobile); fax: ⫹90 256 2146495. E-mail address: [email protected]
the injury to the external branch of the superior laryngeal nerve (EBSLN). The symptoms of EBSLN injury can be nonspecific, but significant incidences of this morbidity have been documented (5–28%) by advanced diagnostic techniques [3–5]. Severe damage to the EBSLN impairs the production of high tones and alters the speaking fundamental frequency, especially in women and professional singers [6]. Preservation of both RLN and EBSLN is important in sustaining voice function; however, all post-thyroidectomy voice alterations are not related to nerve injury [7]. Although the mechanism of post-thyroidectomy voice disturbances in patients with preserved nerve functions is not yet fully understood, it can be attributed to surgical trauma, laryngotracheal fixation of the prelaryngeal strap muscles
0002-9610/07/$ – see front matter © 2007 Excerpta Medica Inc. All rights reserved. doi:10.1016/j.amjsurg.2006.10.009
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Table 1 Patient characteristics, treatment modalities, and pathologic data Variables
n
% of total
Sex (male:female) Median age (y) Extent of resection Lobectomy Total thyroidectomy Presence of pyramidal lobe Use of a drain Histology Benign (NG:FA:DG:LT) Malign (papillary carcinoma)
6:42 47 (19–72)
12.5:87.5
8 40 18 19
16.7 83.3 37.5 39.6
38 (32:2:2:2) 10
79.2 (66.7:4.2:4.2:4.2) 20.8
NG ⫽ nodular goiter; FA ⫽ folicular adenom; DG ⫽ diffuse goiter; LT ⫽ lymphocytic thyroiditis.
[8], endotracheal intubation [9], or trauma to the arytenoids during intubation. Videolaryngostroboscopic (VLS) evaluation of the larynx facilitates visualization of the vocal folds vibrations and gives qualitative as well as quantitative data about vocal function and/or dysfunction. It is especially effective in the diagnosis of functional, organic, and neurogenic voice disturbances and in determining the treatment options. The stroboscopic findings of permanent paralysis of the RLN are well known [10,11]. Acoustic voice analysis also gives important objective data on voice disturbances, especially those with organic and functional origins. The aim of the current study was to investigate whether thyroidectomy might have some impact on voice parameters in the absence of RLN and/or EBSLN injury and the relationship between the subjective complaints of patients and objective voice analysis. Materials and Methods Fifty patients who underwent thyroid surgery for benign or malignant thyroid pathology at the Ankara University Ibni Sina Hospital between April 2002 and July 2004 were evaluated prospectively. Patients who had hyperthyroidism, previous thyroidectomy, and radiotherapy or surgery to the neck, those with systemic or neurogenic diseases that affected voice quality, those who had a pathology in the VLS examination before operation, or those in whom the examination could not be performed for some reason were excluded from the study. All of the patients were euthyroid at the time of operation and VLS examinations were normal preoperatively. The preoperative voice tests were used as the patients’ own controls.
The demographic features of the patients, treatment modalities, and pathologic data are presented in Table 1. In 19 patients, hemovac drains were used. All of these patients were in the total thyroidectomy group and drains were taken out after 24 hours. Thyroidectomy technique During surgery the strap musculature was retracted laterally from the midline but not completely divided in any of the cases. Total thyroidectomy was performed by extracapsular dissection to remove both thyroid lobes and the pyramidal lobe when it was present. Recurrent laryngeal nerves were identified and followed in both directions: caudally to the mediastinum and cranially to the cricothyroid junction. All vessels were ligated close to the thyroid gland. The superior thyroid artery and vein were individually ligated on thyroid capsule to avoid injury to the EBSLN. When the EBSLN could not be readily identified, no further dissection was performed. Parathyroid glands were also identified and preserved. Nonviable parathyroid glands were auto transplanted immediately. The cricothyroid muscle was protected from injury with electrocoagulation or manual retraction even when pyramidal lobe dissection was performed. Wound drainage with a closed suction catheter was used at the discretion of the operating surgeon. Patients were asked for any voice changes or disturbances 48 hours and 3 months after the surgery, and acoustic voice analysis and VLS examinations were performed simultaneously in the Ear, Nose and Throat Department of Ankara University Medical School. Videolaryngostroboscopy VLS examinations were done with a Storz 8010 machine (Karl Storz GmbH & Co., KG, Tuttlingen, Germany) by using a 90 degree–angled rigid endoscope. Acoustic voice analysis Acoustic voice analysis was performed by using MDVP (Multi Dimensional Voice Program; Kay Elemetrics Corp, Lincoln Park, NJ) version 2.02 voice analysis program with a Pentium IV computer (1.60 GHz), a voice card (Sound Blaster Live Value; Creative Labs, USA), and a microphone (Shure model 16A; Shure Inc, Niles, IL). The microphone was set at a distance of 15 cm from the oral cavity and a vowel of “a” was recorded for 3 seconds. For the statistical analysis, 4 parameters of the MDVP were used: mean vocal fundamental frequency (Fo, Hz), mean percentage vocal jitter and shimmer, and noise-to-harmonic ratio (NHR, dB).
Table 2 Comparison of the objective acoustic voice measurements according to pre- and postoperative periods Variable
Preop median (range)
Early postop median (range)
After 3 months median (range)
P1
P2
F0 Female F0 Male Jitter (%) Shimmer (%) NHR (dB)
239.65 (102.31) 166.570 (115.37) 0.572 (1.994) 2.529 (5.44) 0.120 (0.103)
221.87 (103.87) 143.950 (79.39) 0.750 (3.726) 2.827 (8.551) 0.130 (0.096)
227.30 (152.63) 139.608 (74.65) 0.598 (1.575) 2.475 (4.997) 0.122 (0.07)
⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001
⬍.01 ⬍.01 ⬎.05 ⬎.05 ⬎.05
P1 ⫽ comparison of preoperative and early postoperative periods; P2 ⫽ comparison of preoperative and late postoperative periods.
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Table 3 Pre- and postoperative comparisons of objective voice parameters according to extent of surgery Preoperative
Early postoperative
Late postoperative
Total lobectomy Total thyroidectomy P Median (range) Median (range)
Total lobectomy Total thyroidectomy P Median (range) Median (range)
Total lobectomy Total thyroidectomy P Median (range) Median (range)
236.54 (169.38) F0 (Hz) Jitter (%) 0.605 (1.994) Shimmer (%) 2.552 (5.44) NHR (dB) 0.121 (0.103)
237.71 (132.03) 0.397 (1.105) 2.441 (2.15) 0.113 (0.03)
.98 217.88 (171.86) .47 0.769 (3.726) .42 2.861 (8.551) .05 0.129 (0.09)
Mean percentage vocal jitter and shimmer are indices of the cycle-to-cycle variability of vocal period and amplitude, respectively. Fo and NHR were derived from the middle two seconds of each vowel prolongation. Statistical evaluation Data were analyzed in the Biostatistics Department of Ankara University Medical School by SPSS version 11.5 (Chicago, IL). Friedman’s test, Mann-Whitney U test, and chi-square tests were used for statistical analysis and P ⬍ .05 was accepted as the significance level. Results Of the 50 patients enrolled in this study, 2 patients did not return for late follow-up and were excluded. There was no operative mortality and no major complications after thyroidectomy. No patients required urgent re-exploration. VLS revealed no vocal cord paralysis in any of the patients after thyroidectomy. Subjective voice disturbances Eighteen patients (37%) revealed voice changes compared to preoperative status. After 3 months, 7 (14.6%) of 18 patients were still complaining of voice disturbances. Acoustic voice analysis Comparison of the acoustic voice parameters of preoperative, early postoperative (after 48 hours), and late postoperative (3 months after surgery) period are presented in Table 2. The only parameter that continues to be statistically significant after 3 months is Fo, both for male and female patients. The statistical comparison of the acoustic voice parameters related to the extent of surgery revealed no statistically significant difference (Table 3).
221.64 (126.37) 0.701 (1.016) 2.470 (3.959) 0.135 (0.03)
.05 225.54 (157.18) .48 0.591 (1.556) .28 2.505 (4.997) 1 0.123 (0.07)
213.95 (118.97) 0.657 (1.046) 2.407 (1.995) 0.121 (0.02)
.37 .75 .23 .88
The differences in acoustic voice measurements were not significant according to the final histopathology report (Table 4) and the presence of pyramidal lobe (Table 5). Comparisons of patients who complained of voice disturbances in the early postoperative period (Table 6) and after 3 months (Table 7) showed no statistically significant difference in terms of acoustic voice measurements. The only significant parameter related to the subjective voice complaints in the early postoperative period was the extent of surgery (total thyroidectomy) (Tables 8 and 9). Comments Preservation of voice is an important concern for patients undergoing thyroid surgery. However, vocal and laryngeal symptoms appear to be common following thyroidectomy. The outcomes of injury to RLN and EBSLN are well known and preservation of these nerves is the major point in modern thyroid surgery. However, the etiology of post-thyroidectomy voice disturbances for patients with preserved nerve function has not been widely studied. Our study reports that apart from neurogenic trauma, voice might temporarily be influenced following thyroid surgery. The present data suggest that the alterations of objective acoustic voice measures are associated with early postoperative voice symptoms. Vocal fundamental frequency was found to decrease and vocal jitter, shimmer, and NHR were found to increase on postoperative day 2 (P ⬍ .01). Although all patients had significant alterations of objective voice parameters, only 37% of patients reported voice symptoms early after thyroidectomy and only 14.6% of the overall were still complaining in the 3-month follow-up. However, none of the patients had abnormal VLS postoperatively. All patients who were found to be asymptomatic 2 days after thyroidectomy remained symptom-free in the 3-month follow-up. Another important finding in this study is the correlation
Table 4 Comparison of the acoustic voice parameters according to the final histopathology report Preoperative
F0 (Hz) Jitter (%) Shimmer (%) NHR (dB)
Early postoperative
Late postoperative
Benign Median (range)
Malign Median (range)
P
Benign Median (range)
Malign Median (range)
P
Benign Median (range)
Malign Median (range)
P
238.066 (169.38) 0.605 (1.23) 2.507 (2.76) 0.120 (0.07)
229.921 (136.32) 0.515 (1.89) 2.873 (5.08) 0.118 (0.10)
.68 .89 .15 .73
221.640 (171.86) 0.749 (1.76) 2.801 (5.49) 0.131 (0.09)
208.811 (123.05) 0.750 (3.57) 3.021 (7.62) 0.128 (0.05)
.10 .68 .47 .75
222.027 (157.18) 0.613 (1.35) 2.464 (3.28) 0.123 (0.05)
227.301 (132.45) 0.570 (1.46) 2.963 (4.49) 0.120 (0.07)
.75 .91 .11 .52
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Table 5 Comparison of the voice disturbances according to the presence of pyramidal lobe Preoperative
F0 (Hz) Jitter (%) Shimmer (%) NHR (dB)
Early postoperative
Late posoperative
Pyramidale lobe (⫹) Median (range)
Pyramidale lobe (⫺) Median (range)
P
Pyramidale lobe (⫹) Median (range)
Pyramidale lobe (⫺) Median (range)
P
Pyramidale lobe (⫹) Median (range)
Pyramidale lobe (⫺) Median (range)
P
241.85 (168.27) 0.571 (1.94) 2.556 (5.2) 0.121 (0.09)
234.13 (88.91) 0.572 (1.53) 2.412 (3.02) 0.117 (0.05)
.83 .72 .5 .51
217.98 (171.86) 0.882 (3.57) 2.905 (8.55) 0.132 (0.08)
221.13 (86.48) 0.597 (1.76) 2.523 (5.02) 0.126 (0.06)
.45 .1 .11 .29
218.68 (157.18) 0.681 (1.35) 2.522 (4.93) 0.119 (0.03)
227.951 (73.1) 0.558 (1.55) 2.395 (3.28) 0.120 (0.07)
.50 .13 .56 .14
between voice symptoms and the extent of thyroidectomy in the early postoperative period. It is now generally accepted that identifying the course of the recurrent nerve is the best way to avoid injury. Rates of paralysis do not increase according to the extent of thyroidectomy [12–17]. However, when the RLN arborizes prior to its entrance into the larynx at the cricothyroid joint, injury to a small branch may contribute to the changes in voice without significant changes in vocal fold motion [2]. There are several technical approaches to preserve the integrity of the EBSLN, including isolation and individual ligation of the superior pole vessels adjacent to the thyroid capsule, identification of the EBSLN prior to securing the vasculature in the same manner, and neuromonitoring of the EBSLN during thyroidectomy [18,19]. In a prospective trial, careful distal ligation of the superior thyroid vessels was reported to be a safe technique to preserve the EBSLN, making its routine exposure unnecessary during surgery [18]. We also believe that the surgical strategy should focus on to ligate the superior thyroid vasculature or their individual branches on the thyroid capsule and perform no further dissection unless EBSLN could be readily identified. The incidence of EBSLN injury in this study is 0% and it is 0% to 14% in other modern published series [18 –22]. Complete and incomplete injuries to the RLN and EBSLN can be identified with VLS. VLS provides useful information about the nature of vibration and presence of any abnormality, and gives a permanent record from which it is possible to assess improvement. The vocal fold is immobile and has no muscle tone in complete paralysis of the RLN. The glottis does not close completely. The movements of the bilateral folds are asymmetrical. The mucosal wave is absent or reduced on the paralytic vocal fold [20]. In contrast, in incomplete paralysis the vocal fold is slightly mobile and has some muscular tonus. Glottic closure is better. The mucosal wave is reduced in the affected fold and
the bilateral waves are again asymmetrical [11]. Abnormalities in the vibratory pattern become more apparent as the number of affected neurons increase. In superior laryngeal nerve paralysis, the anterior glottis moves to the affected side because of the tonus of the unaffected cricothyroid muscle. The mucosal wave is asymmetrical as the wave is late on the affected fold [11]. The displacement of the anterior glottis was reported to occur in severe cases of superior laryngeal nerve paralysis [23,24]. An asymmetria in the mucosal wave may be the only finding in mild cases. None of the patients in this study suffered from RLN and/or EBSLN injury as checked with VLS postoperatively. Laryngeal electromyography (EMG) also supplies valuable information about the innervation of the cricothyroid muscles. It is the most accurate test for postoperative assessment of superior laryngeal nerve paralysis. The correlation of laryngeal EMG with physical examination findings allows a definite diagnosis of superior laryngeal nerve paresis or paralysis. EMG may define the physiology of postthyroidectomy dysphonia but it is an invasive technique of voice testing and patients are usually reluctant to undergo such a procedure. Since the VLS examinations of the patients were normal, we didn’t consider performing laryngeal EMG because the subjective voice alterations did not seem to be related to neurogenic trauma. VLS has certain advantages when compared to indirect laryngoscopy, both regarding the differential diagnosis of the vocal disturbances and the prediction of the outcome of the paralysis [25]. It detects elusive symptoms of EBSLN palsy better than the other methods. It is considered to be an important noninvasive diagnostic tool for evaluating signs of cricothyroid muscle dysfunction [8,11,20,21]. A prospective study evaluating post-thyroidectomy voice function employing acoustic, videostroboscopic, and laryngeal elec-
Table 6 Comparison of the subjective voice changes between pre- and early post-operative period Preoperatıve
F0 (Hz) Jitter (%) Shimmer (%) NHR (dB)
Early postoperatıve
Voice disturbance (⫺) Median (range)
Voice disturbance (⫹) Median (range)
P
Voice disturbance (⫺) Median (range)
Voice disturbance (⫹) Median (range)
P
232.37 (169.38) 0.605 (1.94) 2.552 (5.2) 0.126 (0.09)
244.511 (87.80) 0.538 (1.15) 2.444 (2.4) 0.115 (0.08)
.02 .88 .34 .07
219.80 (171.86) 0.715 (3.68) 2.787 (8.55) 0.130 (0.09)
219.06 (90.02) 0.927 (1.76) 2.879 (5.08) 0.127 (0.06)
.56 .86 .25 .94
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Table 7 Comparison of the subjective voice changes between pre- and late postoperative period Preoperatıve
F0 (Hz) Jitter (%) Shimmer (%) NHR (dB)
After 3 months
Voice disturbance (⫺) Median (range)
Voice disturbance (⫹) Median (range)
P
Voice disturbance (⫺) Median (range)
Voice disturbance (⫹) Median (range)
P
235.49 (169.38) 0.536 (1.99) 2.510 (5.44) 0.120 (0.1)
237.60 (87.80) 0.825 (1.02) 2.735 (1.35) 0.122 (0.06)
.71 .43 .81 .95
222.36 (157.18) 0.598 (1.55) 2.465 (4.99) 0.123 (0.07)
224.74 (132.54) 0.581 (1.18) 2.518 (1.98) 0.116 (0.03)
.77 .88 .88 .10
tromyographic analysis found EBSLN palsy in 3 of 21 (14%) patients with postoperative voice symptoms [21]. When we compared the subgroups of patients who complained of voice disturbances in terms of the extent of thyroid surgery, by the presence of pyramidal lobe and final histopathology, the only statistically significant difference was found in the thyroidectomy technique. However, after 3 months from surgery, this difference was no more significant. Total thyroidectomy seemed to affect the subjective voice satisfaction in the early postoperative period. Early postoperative voice disturbances also were found to occur 41% to 47% of patients in other prospective studies [21,26]. Sinagra et al [27] found that Fo gradually recovered in the fourth and sixth postoperative months but did not reach preoperative values. They concluded that the decrease in Fo might be related to a decrease in the cordal tension by alteration in the functional character of the cricothyroid muscle or the SLN. Hong and Kim also reported that the speaking Fo and range of speaking Fo were significantly decreased 1 and 3 months after thyroid surgery but not at 6 months [8]. The present data suggest that clinically significant postoperative changes in all parameters of acoustic measurements in the early postoperative period are associated with voice symptoms. However, it is not possible to prove it with VLS. All patients who were asymptomatic 2 days after the thyroidectomy remained symptom-free at the 3-month follow-up. Other possible causes of post-thyroidectomy voice alterations have been described. Endotracheal intubation alone is associated with a 5% risk of voice impairment [9]. Division of strap muscles, which plays an important role in phonation [28,29], also might lead to discreet changes in tension and
Table 8 Distribution of patients with/without voice disturbances in the early post-operative period
Subjective voice disturbance (⫹) (n:18) Subjective voice disturbance (⫺) (n:30) P
Pyramidal lobe n (%)
Drain n (%)
Total thyroidectomy n (%)
Sex (female) n (%)
9 (50)
10 (55)
18 (100)
18 (100)
9 (30)
9 (30)
22 (73)
24 (80)
.018
.071
.122
.080
motility of the internal and external laryngeal muscles. In a study where the effect of division of strap muscles was evaluated in a study by VLS and EMG, the authors hypothesized that laryngotracheal fixation of the extralaryngeal strap musculature might result in post-thyroidectomy voice alterations following thyroidectomy [8]. To what degree sternohyoid and/or sternothyroid muscular division influences voice function is unknown. There was no iatrogenic damage to strap muscles in this patient cohort. Signs of cricothyroid dysfunction, whether by nervous or direct muscular injury, are subtle and variable. Normally, the cricothyroid muscle actively tightens during phonation to increase the tension in the vocal folds. When this function is lost, pitch decrease, fatigue during phonation, hoarseness, and loss of voice projection become apparent [27]. Removal of the thyroid gland modifies the vascular supply and venous drainage of the larynx. Together with the orotracheal intubation, this could cause alterations of the mucosa as a slight congestion that may help to explain the lower pitch [7]. It is also important to keep in mind that human voice and acoustic voice parameters also may be affected by emotional and behavioral conditions [30]. Therefore, all of these factors may work synergistically. The results of this study indicate that apart from RLN and/or EBSLN injuries, voice and objective acoustic measures may be temporarily influenced after thyroidectomy. These changes are temporary for the shimmer, jitter, and NHR and more lasting for the Fo. The extent of surgery is the most prominent factor in this study group that affects the acoustic measures in the early postoperative period. The changes found in the acoustic characteristics do not describe the postoperative voice changes of the patients. Therefore, the data should be interpreted cautiously as the overall study population was small.
Table 9 Distribution of patients with/without voice disturbances after 3 months Pyramidal lobe n (%) Subjective voice disturbance (⫹) (n:7) Subjective voice disturbance (⫺) (n:41) P
Drain n (%)
Total thyroidectomy n (%) 7 (100)
Sex (female) n (%)
3 (57)
2 (28)
7 (100)
16 (39)
17 (41)
31 (75)
35 (85)
1
.687
.583
.573
322
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Clinical surgery–International
The evaluation of the causes of subjective voice disturbances after thyroid surgery Lutfi Soylu, M.D.a, Serdar Ozbas, M.D.b,*, Hatim Yahya Uslu, M.D.c, Savas Kocak, M.D.d a
General Surgery Department, Ankara University Medical School, Sýhhýye, 06430, Ankara, Turkey General Surgery Department, Adnan Menderes University Medical School, 09100, Aydin, Turkey c General Surgery Department, Ufuk University Medical School, Balgat, 06520, Ankara, Turkey d General Surgery Department, Division of Endocrine Surgery and Breast Diseases, Ankara University Medical School, Sýhhýye, 06430, Ankara, Turkey b
Manuscript received February 23, 2006; revised manuscript October 24, 2006
Abstract Background: Voice changes following thyroidectomy is a rare form of morbidity not infrequently encountered. Injury to the recurrent laryngeal nerve or external branch of the superior laryngeal nerve is the most well-known cause of post-thyroidectomy voice disturbances. However, voice dysfunction is a more complex entity. The aim of the current study was to assess the possible factors that influence voice changes after thyroidectomy. Methods: Forty-eight consecutive patients who had undergone thyroidectomy were studied. The acoustic voice analysis (mean vocal fundamental frequency [Fo], mean percentage vocal jitter and shimmer, and noise-to-harmonic ratio) and videolaryngostroboscopic examination of these patients were performed preoperatively, on the second postoperative day, and 3 months after the operation. The presence of subjective voice changes was recorded prospectively based on a symptom scale. Results: No major complications occurred perioperatively or in the postoperative period. Videolaryngostroboscopic examinations were normal in all patients before and after thyroidectomy. Eighteen (37.5%) patients complained of subjective voice changes in the early postoperative period and 7 (14.6%) of these were still uncomfortable after 3 months. Although the difference was significant by means of all acoustic voice parameters measured in the early postoperative period, Fo is the only parameter that continues to be significant after 3 months. Conclusions: Irrespective from recurrent laryngeal nerve and/or injuries to the external branch of the superior laryngeal nerve, voice may temporarily be affected by thyroidectomy. Most of the subjective complaints and acoustic voice parameters return to normal in a few months after surgery. © 2007 Excerpta Medica Inc. All rights reserved. Keywords: Thyroidectomy; Videolaryngostroboscopy; Voice; Acoustic voice parameters
Vocal dysfunction is one of the most important complications of thyroid surgery. Although recurrent laryngeal nerve (RLN) injury traditionally has been the most well-known neurogenic cause, 50% of patients with unilateral RLN palsy can be asymptomatic [1]. It is not always possible to preserve normal postoperative voice function, even though the identification and preservation of the RLNs has become a routine approach in modern thyroid surgery [2]. Another neurogenic voice-altering complication of thyroid surgery is * Corresponding author. Adnan Menderes University Medical School, General Surgery Department, 09100, Aydin, Turkey. Tel.: ⫹90 256 4441256, ⫹90 533 6880266 (mobile); fax: ⫹90 256 2146495. E-mail address: [email protected]
the injury to the external branch of the superior laryngeal nerve (EBSLN). The symptoms of EBSLN injury can be nonspecific, but significant incidences of this morbidity have been documented (5–28%) by advanced diagnostic techniques [3–5]. Severe damage to the EBSLN impairs the production of high tones and alters the speaking fundamental frequency, especially in women and professional singers [6]. Preservation of both RLN and EBSLN is important in sustaining voice function; however, all post-thyroidectomy voice alterations are not related to nerve injury [7]. Although the mechanism of post-thyroidectomy voice disturbances in patients with preserved nerve functions is not yet fully understood, it can be attributed to surgical trauma, laryngotracheal fixation of the prelaryngeal strap muscles
0002-9610/07/$ – see front matter © 2007 Excerpta Medica Inc. All rights reserved. doi:10.1016/j.amjsurg.2006.10.009
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Table 1 Patient characteristics, treatment modalities, and pathologic data Variables
n
% of total
Sex (male:female) Median age (y) Extent of resection Lobectomy Total thyroidectomy Presence of pyramidal lobe Use of a drain Histology Benign (NG:FA:DG:LT) Malign (papillary carcinoma)
6:42 47 (19–72)
12.5:87.5
8 40 18 19
16.7 83.3 37.5 39.6
38 (32:2:2:2) 10
79.2 (66.7:4.2:4.2:4.2) 20.8
NG ⫽ nodular goiter; FA ⫽ folicular adenom; DG ⫽ diffuse goiter; LT ⫽ lymphocytic thyroiditis.
[8], endotracheal intubation [9], or trauma to the arytenoids during intubation. Videolaryngostroboscopic (VLS) evaluation of the larynx facilitates visualization of the vocal folds vibrations and gives qualitative as well as quantitative data about vocal function and/or dysfunction. It is especially effective in the diagnosis of functional, organic, and neurogenic voice disturbances and in determining the treatment options. The stroboscopic findings of permanent paralysis of the RLN are well known [10,11]. Acoustic voice analysis also gives important objective data on voice disturbances, especially those with organic and functional origins. The aim of the current study was to investigate whether thyroidectomy might have some impact on voice parameters in the absence of RLN and/or EBSLN injury and the relationship between the subjective complaints of patients and objective voice analysis. Materials and Methods Fifty patients who underwent thyroid surgery for benign or malignant thyroid pathology at the Ankara University Ibni Sina Hospital between April 2002 and July 2004 were evaluated prospectively. Patients who had hyperthyroidism, previous thyroidectomy, and radiotherapy or surgery to the neck, those with systemic or neurogenic diseases that affected voice quality, those who had a pathology in the VLS examination before operation, or those in whom the examination could not be performed for some reason were excluded from the study. All of the patients were euthyroid at the time of operation and VLS examinations were normal preoperatively. The preoperative voice tests were used as the patients’ own controls.
The demographic features of the patients, treatment modalities, and pathologic data are presented in Table 1. In 19 patients, hemovac drains were used. All of these patients were in the total thyroidectomy group and drains were taken out after 24 hours. Thyroidectomy technique During surgery the strap musculature was retracted laterally from the midline but not completely divided in any of the cases. Total thyroidectomy was performed by extracapsular dissection to remove both thyroid lobes and the pyramidal lobe when it was present. Recurrent laryngeal nerves were identified and followed in both directions: caudally to the mediastinum and cranially to the cricothyroid junction. All vessels were ligated close to the thyroid gland. The superior thyroid artery and vein were individually ligated on thyroid capsule to avoid injury to the EBSLN. When the EBSLN could not be readily identified, no further dissection was performed. Parathyroid glands were also identified and preserved. Nonviable parathyroid glands were auto transplanted immediately. The cricothyroid muscle was protected from injury with electrocoagulation or manual retraction even when pyramidal lobe dissection was performed. Wound drainage with a closed suction catheter was used at the discretion of the operating surgeon. Patients were asked for any voice changes or disturbances 48 hours and 3 months after the surgery, and acoustic voice analysis and VLS examinations were performed simultaneously in the Ear, Nose and Throat Department of Ankara University Medical School. Videolaryngostroboscopy VLS examinations were done with a Storz 8010 machine (Karl Storz GmbH & Co., KG, Tuttlingen, Germany) by using a 90 degree–angled rigid endoscope. Acoustic voice analysis Acoustic voice analysis was performed by using MDVP (Multi Dimensional Voice Program; Kay Elemetrics Corp, Lincoln Park, NJ) version 2.02 voice analysis program with a Pentium IV computer (1.60 GHz), a voice card (Sound Blaster Live Value; Creative Labs, USA), and a microphone (Shure model 16A; Shure Inc, Niles, IL). The microphone was set at a distance of 15 cm from the oral cavity and a vowel of “a” was recorded for 3 seconds. For the statistical analysis, 4 parameters of the MDVP were used: mean vocal fundamental frequency (Fo, Hz), mean percentage vocal jitter and shimmer, and noise-to-harmonic ratio (NHR, dB).
Table 2 Comparison of the objective acoustic voice measurements according to pre- and postoperative periods Variable
Preop median (range)
Early postop median (range)
After 3 months median (range)
P1
P2
F0 Female F0 Male Jitter (%) Shimmer (%) NHR (dB)
239.65 (102.31) 166.570 (115.37) 0.572 (1.994) 2.529 (5.44) 0.120 (0.103)
221.87 (103.87) 143.950 (79.39) 0.750 (3.726) 2.827 (8.551) 0.130 (0.096)
227.30 (152.63) 139.608 (74.65) 0.598 (1.575) 2.475 (4.997) 0.122 (0.07)
⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001
⬍.01 ⬍.01 ⬎.05 ⬎.05 ⬎.05
P1 ⫽ comparison of preoperative and early postoperative periods; P2 ⫽ comparison of preoperative and late postoperative periods.
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Table 3 Pre- and postoperative comparisons of objective voice parameters according to extent of surgery Preoperative
Early postoperative
Late postoperative
Total lobectomy Total thyroidectomy P Median (range) Median (range)
Total lobectomy Total thyroidectomy P Median (range) Median (range)
Total lobectomy Total thyroidectomy P Median (range) Median (range)
236.54 (169.38) F0 (Hz) Jitter (%) 0.605 (1.994) Shimmer (%) 2.552 (5.44) NHR (dB) 0.121 (0.103)
237.71 (132.03) 0.397 (1.105) 2.441 (2.15) 0.113 (0.03)
.98 217.88 (171.86) .47 0.769 (3.726) .42 2.861 (8.551) .05 0.129 (0.09)
Mean percentage vocal jitter and shimmer are indices of the cycle-to-cycle variability of vocal period and amplitude, respectively. Fo and NHR were derived from the middle two seconds of each vowel prolongation. Statistical evaluation Data were analyzed in the Biostatistics Department of Ankara University Medical School by SPSS version 11.5 (Chicago, IL). Friedman’s test, Mann-Whitney U test, and chi-square tests were used for statistical analysis and P ⬍ .05 was accepted as the significance level. Results Of the 50 patients enrolled in this study, 2 patients did not return for late follow-up and were excluded. There was no operative mortality and no major complications after thyroidectomy. No patients required urgent re-exploration. VLS revealed no vocal cord paralysis in any of the patients after thyroidectomy. Subjective voice disturbances Eighteen patients (37%) revealed voice changes compared to preoperative status. After 3 months, 7 (14.6%) of 18 patients were still complaining of voice disturbances. Acoustic voice analysis Comparison of the acoustic voice parameters of preoperative, early postoperative (after 48 hours), and late postoperative (3 months after surgery) period are presented in Table 2. The only parameter that continues to be statistically significant after 3 months is Fo, both for male and female patients. The statistical comparison of the acoustic voice parameters related to the extent of surgery revealed no statistically significant difference (Table 3).
221.64 (126.37) 0.701 (1.016) 2.470 (3.959) 0.135 (0.03)
.05 225.54 (157.18) .48 0.591 (1.556) .28 2.505 (4.997) 1 0.123 (0.07)
213.95 (118.97) 0.657 (1.046) 2.407 (1.995) 0.121 (0.02)
.37 .75 .23 .88
The differences in acoustic voice measurements were not significant according to the final histopathology report (Table 4) and the presence of pyramidal lobe (Table 5). Comparisons of patients who complained of voice disturbances in the early postoperative period (Table 6) and after 3 months (Table 7) showed no statistically significant difference in terms of acoustic voice measurements. The only significant parameter related to the subjective voice complaints in the early postoperative period was the extent of surgery (total thyroidectomy) (Tables 8 and 9). Comments Preservation of voice is an important concern for patients undergoing thyroid surgery. However, vocal and laryngeal symptoms appear to be common following thyroidectomy. The outcomes of injury to RLN and EBSLN are well known and preservation of these nerves is the major point in modern thyroid surgery. However, the etiology of post-thyroidectomy voice disturbances for patients with preserved nerve function has not been widely studied. Our study reports that apart from neurogenic trauma, voice might temporarily be influenced following thyroid surgery. The present data suggest that the alterations of objective acoustic voice measures are associated with early postoperative voice symptoms. Vocal fundamental frequency was found to decrease and vocal jitter, shimmer, and NHR were found to increase on postoperative day 2 (P ⬍ .01). Although all patients had significant alterations of objective voice parameters, only 37% of patients reported voice symptoms early after thyroidectomy and only 14.6% of the overall were still complaining in the 3-month follow-up. However, none of the patients had abnormal VLS postoperatively. All patients who were found to be asymptomatic 2 days after thyroidectomy remained symptom-free in the 3-month follow-up. Another important finding in this study is the correlation
Table 4 Comparison of the acoustic voice parameters according to the final histopathology report Preoperative
F0 (Hz) Jitter (%) Shimmer (%) NHR (dB)
Early postoperative
Late postoperative
Benign Median (range)
Malign Median (range)
P
Benign Median (range)
Malign Median (range)
P
Benign Median (range)
Malign Median (range)
P
238.066 (169.38) 0.605 (1.23) 2.507 (2.76) 0.120 (0.07)
229.921 (136.32) 0.515 (1.89) 2.873 (5.08) 0.118 (0.10)
.68 .89 .15 .73
221.640 (171.86) 0.749 (1.76) 2.801 (5.49) 0.131 (0.09)
208.811 (123.05) 0.750 (3.57) 3.021 (7.62) 0.128 (0.05)
.10 .68 .47 .75
222.027 (157.18) 0.613 (1.35) 2.464 (3.28) 0.123 (0.05)
227.301 (132.45) 0.570 (1.46) 2.963 (4.49) 0.120 (0.07)
.75 .91 .11 .52
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Table 5 Comparison of the voice disturbances according to the presence of pyramidal lobe Preoperative
F0 (Hz) Jitter (%) Shimmer (%) NHR (dB)
Early postoperative
Late posoperative
Pyramidale lobe (⫹) Median (range)
Pyramidale lobe (⫺) Median (range)
P
Pyramidale lobe (⫹) Median (range)
Pyramidale lobe (⫺) Median (range)
P
Pyramidale lobe (⫹) Median (range)
Pyramidale lobe (⫺) Median (range)
P
241.85 (168.27) 0.571 (1.94) 2.556 (5.2) 0.121 (0.09)
234.13 (88.91) 0.572 (1.53) 2.412 (3.02) 0.117 (0.05)
.83 .72 .5 .51
217.98 (171.86) 0.882 (3.57) 2.905 (8.55) 0.132 (0.08)
221.13 (86.48) 0.597 (1.76) 2.523 (5.02) 0.126 (0.06)
.45 .1 .11 .29
218.68 (157.18) 0.681 (1.35) 2.522 (4.93) 0.119 (0.03)
227.951 (73.1) 0.558 (1.55) 2.395 (3.28) 0.120 (0.07)
.50 .13 .56 .14
between voice symptoms and the extent of thyroidectomy in the early postoperative period. It is now generally accepted that identifying the course of the recurrent nerve is the best way to avoid injury. Rates of paralysis do not increase according to the extent of thyroidectomy [12–17]. However, when the RLN arborizes prior to its entrance into the larynx at the cricothyroid joint, injury to a small branch may contribute to the changes in voice without significant changes in vocal fold motion [2]. There are several technical approaches to preserve the integrity of the EBSLN, including isolation and individual ligation of the superior pole vessels adjacent to the thyroid capsule, identification of the EBSLN prior to securing the vasculature in the same manner, and neuromonitoring of the EBSLN during thyroidectomy [18,19]. In a prospective trial, careful distal ligation of the superior thyroid vessels was reported to be a safe technique to preserve the EBSLN, making its routine exposure unnecessary during surgery [18]. We also believe that the surgical strategy should focus on to ligate the superior thyroid vasculature or their individual branches on the thyroid capsule and perform no further dissection unless EBSLN could be readily identified. The incidence of EBSLN injury in this study is 0% and it is 0% to 14% in other modern published series [18 –22]. Complete and incomplete injuries to the RLN and EBSLN can be identified with VLS. VLS provides useful information about the nature of vibration and presence of any abnormality, and gives a permanent record from which it is possible to assess improvement. The vocal fold is immobile and has no muscle tone in complete paralysis of the RLN. The glottis does not close completely. The movements of the bilateral folds are asymmetrical. The mucosal wave is absent or reduced on the paralytic vocal fold [20]. In contrast, in incomplete paralysis the vocal fold is slightly mobile and has some muscular tonus. Glottic closure is better. The mucosal wave is reduced in the affected fold and
the bilateral waves are again asymmetrical [11]. Abnormalities in the vibratory pattern become more apparent as the number of affected neurons increase. In superior laryngeal nerve paralysis, the anterior glottis moves to the affected side because of the tonus of the unaffected cricothyroid muscle. The mucosal wave is asymmetrical as the wave is late on the affected fold [11]. The displacement of the anterior glottis was reported to occur in severe cases of superior laryngeal nerve paralysis [23,24]. An asymmetria in the mucosal wave may be the only finding in mild cases. None of the patients in this study suffered from RLN and/or EBSLN injury as checked with VLS postoperatively. Laryngeal electromyography (EMG) also supplies valuable information about the innervation of the cricothyroid muscles. It is the most accurate test for postoperative assessment of superior laryngeal nerve paralysis. The correlation of laryngeal EMG with physical examination findings allows a definite diagnosis of superior laryngeal nerve paresis or paralysis. EMG may define the physiology of postthyroidectomy dysphonia but it is an invasive technique of voice testing and patients are usually reluctant to undergo such a procedure. Since the VLS examinations of the patients were normal, we didn’t consider performing laryngeal EMG because the subjective voice alterations did not seem to be related to neurogenic trauma. VLS has certain advantages when compared to indirect laryngoscopy, both regarding the differential diagnosis of the vocal disturbances and the prediction of the outcome of the paralysis [25]. It detects elusive symptoms of EBSLN palsy better than the other methods. It is considered to be an important noninvasive diagnostic tool for evaluating signs of cricothyroid muscle dysfunction [8,11,20,21]. A prospective study evaluating post-thyroidectomy voice function employing acoustic, videostroboscopic, and laryngeal elec-
Table 6 Comparison of the subjective voice changes between pre- and early post-operative period Preoperatıve
F0 (Hz) Jitter (%) Shimmer (%) NHR (dB)
Early postoperatıve
Voice disturbance (⫺) Median (range)
Voice disturbance (⫹) Median (range)
P
Voice disturbance (⫺) Median (range)
Voice disturbance (⫹) Median (range)
P
232.37 (169.38) 0.605 (1.94) 2.552 (5.2) 0.126 (0.09)
244.511 (87.80) 0.538 (1.15) 2.444 (2.4) 0.115 (0.08)
.02 .88 .34 .07
219.80 (171.86) 0.715 (3.68) 2.787 (8.55) 0.130 (0.09)
219.06 (90.02) 0.927 (1.76) 2.879 (5.08) 0.127 (0.06)
.56 .86 .25 .94
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Table 7 Comparison of the subjective voice changes between pre- and late postoperative period Preoperatıve
F0 (Hz) Jitter (%) Shimmer (%) NHR (dB)
After 3 months
Voice disturbance (⫺) Median (range)
Voice disturbance (⫹) Median (range)
P
Voice disturbance (⫺) Median (range)
Voice disturbance (⫹) Median (range)
P
235.49 (169.38) 0.536 (1.99) 2.510 (5.44) 0.120 (0.1)
237.60 (87.80) 0.825 (1.02) 2.735 (1.35) 0.122 (0.06)
.71 .43 .81 .95
222.36 (157.18) 0.598 (1.55) 2.465 (4.99) 0.123 (0.07)
224.74 (132.54) 0.581 (1.18) 2.518 (1.98) 0.116 (0.03)
.77 .88 .88 .10
tromyographic analysis found EBSLN palsy in 3 of 21 (14%) patients with postoperative voice symptoms [21]. When we compared the subgroups of patients who complained of voice disturbances in terms of the extent of thyroid surgery, by the presence of pyramidal lobe and final histopathology, the only statistically significant difference was found in the thyroidectomy technique. However, after 3 months from surgery, this difference was no more significant. Total thyroidectomy seemed to affect the subjective voice satisfaction in the early postoperative period. Early postoperative voice disturbances also were found to occur 41% to 47% of patients in other prospective studies [21,26]. Sinagra et al [27] found that Fo gradually recovered in the fourth and sixth postoperative months but did not reach preoperative values. They concluded that the decrease in Fo might be related to a decrease in the cordal tension by alteration in the functional character of the cricothyroid muscle or the SLN. Hong and Kim also reported that the speaking Fo and range of speaking Fo were significantly decreased 1 and 3 months after thyroid surgery but not at 6 months [8]. The present data suggest that clinically significant postoperative changes in all parameters of acoustic measurements in the early postoperative period are associated with voice symptoms. However, it is not possible to prove it with VLS. All patients who were asymptomatic 2 days after the thyroidectomy remained symptom-free at the 3-month follow-up. Other possible causes of post-thyroidectomy voice alterations have been described. Endotracheal intubation alone is associated with a 5% risk of voice impairment [9]. Division of strap muscles, which plays an important role in phonation [28,29], also might lead to discreet changes in tension and
Table 8 Distribution of patients with/without voice disturbances in the early post-operative period
Subjective voice disturbance (⫹) (n:18) Subjective voice disturbance (⫺) (n:30) P
Pyramidal lobe n (%)
Drain n (%)
Total thyroidectomy n (%)
Sex (female) n (%)
9 (50)
10 (55)
18 (100)
18 (100)
9 (30)
9 (30)
22 (73)
24 (80)
.018
.071
.122
.080
motility of the internal and external laryngeal muscles. In a study where the effect of division of strap muscles was evaluated in a study by VLS and EMG, the authors hypothesized that laryngotracheal fixation of the extralaryngeal strap musculature might result in post-thyroidectomy voice alterations following thyroidectomy [8]. To what degree sternohyoid and/or sternothyroid muscular division influences voice function is unknown. There was no iatrogenic damage to strap muscles in this patient cohort. Signs of cricothyroid dysfunction, whether by nervous or direct muscular injury, are subtle and variable. Normally, the cricothyroid muscle actively tightens during phonation to increase the tension in the vocal folds. When this function is lost, pitch decrease, fatigue during phonation, hoarseness, and loss of voice projection become apparent [27]. Removal of the thyroid gland modifies the vascular supply and venous drainage of the larynx. Together with the orotracheal intubation, this could cause alterations of the mucosa as a slight congestion that may help to explain the lower pitch [7]. It is also important to keep in mind that human voice and acoustic voice parameters also may be affected by emotional and behavioral conditions [30]. Therefore, all of these factors may work synergistically. The results of this study indicate that apart from RLN and/or EBSLN injuries, voice and objective acoustic measures may be temporarily influenced after thyroidectomy. These changes are temporary for the shimmer, jitter, and NHR and more lasting for the Fo. The extent of surgery is the most prominent factor in this study group that affects the acoustic measures in the early postoperative period. The changes found in the acoustic characteristics do not describe the postoperative voice changes of the patients. Therefore, the data should be interpreted cautiously as the overall study population was small.
Table 9 Distribution of patients with/without voice disturbances after 3 months Pyramidal lobe n (%) Subjective voice disturbance (⫹) (n:7) Subjective voice disturbance (⫺) (n:41) P
Drain n (%)
Total thyroidectomy n (%) 7 (100)
Sex (female) n (%)
3 (57)
2 (28)
7 (100)
16 (39)
17 (41)
31 (75)
35 (85)
1
.687
.583
.573
322
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