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Abstract

Objective

A retrospective cohort study to develop a classification scheme for abnormal vocal cord movement (AVCM) before and after thyroid surgery.

Methods

Clinical and laryngoscopic data from patients who underwent partial or total thyroidectomy were analysed. AVCM was classified as mild (type I), moderate (type II) or severe (type III), according to laryngoscopic findings.

Results

The study included 1619 patients, of whom 39 had preoperative AVCM and 65 had postoperative AVCM. Recovery rates for preoperative, postoperative and total type I AVCM were higher than the corresponding type III AVCM. Recovery rates for total type II AVCM were higher than those for type III AVCM at 1, 3 and 6 months postoperatively. Asymptomatic patients had better recovery rates than symptomatic patients.

Conclusion

We have developed a useful classification system for patients with AVCM after thyroidectomy. Pre- and postoperative laryngoscopy can identify asymptomatic AVCM and is essential to evaluate the extent of recurrent laryngeal nerve injury in these patients.

Keywords

Thyroid surgery recurrent laryngeal nerve injury laryngoscopy

Introduction

Thyroid surgery is a common procedure that is frequently used to treat thyroid cancer, goitre, and overactive thyroid.^1,2 The most common complications after thyroid surgery include bleeding, hypoparathyroidism, infection, recurrent laryngeal nerve injury (RLNI) and hypothyroidism.^3,4 Rare complications, such as damage to the sympathetic trunk, are occasionally reported, although most can be avoided while performing surgery.⁵

The reported rate of RLNI after thyroid surgery ranges between 1.4% and 15%.^6–8 RLNI symptoms may include postoperative hoarseness and dysphonia, and can lead to abnormal vocal cord movement (AVCM). Bilateral RLNI may also be accompanied by breathlessness and life-threatening upper airway obstruction.⁹ These clinical manifestations are often subacute. Generally, the vocal fold initially remains in the paramedian position, and definite vocal changes may develop over days or weeks.¹⁰ The incidence of RLNI is highest during re-explorations, Graves’ disease or thyroid carcinoma procedures.^11,12 Injury can occur as a result of stretch injury, pressure, crush injury, electrocautery, suction trauma or ischaemia,^13,14 but it is difficult to determine the cause of RLNI during surgery as these injuries are not visually discernible. To reduce the incidence of RNLI, the anatomical structure should be carefully assessed. The integrity of the recurrent laryngeal nerve can be guaranteed by careful identification and assessment during the surgical procedure, as visual identification may decrease the risk of permanent nerve palsy after thyroid surgery.¹⁵

Perioperative vocal fold paralysis can be assessed using functional voice assessment (via endoscopy) and vocal function assessment (e.g., maximum phonation time, pitch range, perceptual voice quality, etc.).¹⁶ There are no validated laryngoscopic standards available for vocal cord function assessment after thyroidectomy, however. Such standards would allow assessment of the presence and extent of nerve damage, and the risk of aspiration or respiratory compromise due to vocal cord impairment. The aim of the present study was to develop a new classification scheme for AVCM before and after thyroid surgery. Such a scheme could be used to evaluate the extent of pre- and postoperative RLNI in patients with thyroid disease, and predict the prognosis of RLNI.

Patients and methods

Study population

This retrospective cohort study included all patients (including those with vocal cord dysfunction caused by thyroid disease) who underwent partial or total thyroidectomy and perioperative laryngoscopic examination at the Department of Thyroid Surgery, China–Japan Union Hospital, Changchun, China, between January 2010 and January 2011. Exclusion criteria were: other vocal cord disease; laryngeal disease; laryngeal surgery.

The study was approved by the institutional review board of China–Japan Union Hospital, Changchun, China, and all patients (or their next-of‐kin if aged <18 years) provided written informed consent.

IONM

In all patients, the recurrent laryngeal nerve was exposed during thyroidectomy, and its functional integrity was determined using intraoperative neuromonitoring (IONM), as described.^11,17 The four-step IONM procedure obtains electromagnetic signals from the vagus nerve and recurrent laryngeal nerve before and after resection of the thyroid lobe. All IONM procedures were performed by the same physician (J.X.).

Laryngoscopy

All patients underwent routine laryngoscopic examination to assess vocal cord movement (VCM) before and 1 day after surgery (ENF-P4 laryngoscope; Olympus, Tokyo, Japan). All laryngoscopic examinations were performed by the same physician (J.X.), and abnormal vocal cord movements were confirmed by an experienced otolaryngologist. Pre- and postoperative laryngoscopy findings were compared.

Patients were stratified between three groups: control (normal pre- and postoperative findings); preoperative abnormal (abnormal preoperative findings); and postoperative abnormal (normal preoperative but abnormal postoperative findings).

In the case of normal postoperative laryngoscopy findings, no further examinations were performed. In all other cases, laryngoscopy was repeated at 7 days and 1, 3 and 6 months after surgery, or until normal VCMs were observed (to a maximum of 1 year). Patients were considered to have permanent vocal cord damage if their laryngoscopy findings were abnormal 6 months after surgery. Patients with postoperative AVCM were given standard treatment, with intravenous dexamethasone and oral vitamin B.

Recurrent laryngeal nerve monitoring

The NIM® II monitoring system (Medtronic, Minneapolis, MN, USA) was used to monitor, test and confirm visual identification of the recurrent laryngeal nerve. After its intraoperative visual identification, the nerve stimulator settings were 1 mA and 100 µV. Nerve testing was repeated at the most distal part of the dissected recurrent laryngeal nerve to the entry point. The stimulus necessary to generate a response at the cricoarytenoid joint and distal dissection was recorded for each nerve. Vagal stimulation was performed with a current of 1 mA after direct anatomical exposure of the vagus nerve. Pathological reports and information regarding patients’ pre- and postoperative vocal cord mobility were reviewed and documented.

AVCM classification

Normal VCM was defined as bilaterally symmetrical and fast, with normal amplitude. AVCM was classified as mild (type I), moderate (type II), or severe (type III), based on laryngoscopic findings and neuromonitoring (Table 1).

Table 1.

Classification of abnormal vocal cord movements (VCM).

Classification	VCM	Hoarseness	Dysphasia	Choking	Neuromonitoring
Type I	Slow with decreased amplitude on the impaired side. Movement remains opposite to that of the normal vocal cord	No	No	No	Normal, decreased, or absent
Type II	Extremely slow with obviously decreased amplitude. Bilateral VCM is asymmetrical	Probable	Probable	Probable	Decreased
Type III	Absent and asymmetrical	Probable	Probable	Probable	Absent

Statistical analyses

Data were presented as n (%) and compared using χ²-test. Statistical analyses were performed using SPSS^® version 16.0 (SPSS Inc., Chicago, IL, USA) for Windows®. P-values < 0.05 were considered statistically significant.

Results

The study enrolled 1842 patients, of whom 223 were lost to follow-up due to lack of subsequent laryngoscopic examinations. The final analysis therefore included 1619 patients (374 male/1245 female; median age 46 years, age range 19–72 years). A total of 39 patients were stratified into the preoperative abnormal group, 65 were stratified into the postoperative abnormal group, and the remaining 1515 patients were stratified into the control group.

Patients presented with papillary thyroid carcinoma of both lobes (n = 218, 436 recurrent laryngeal nerves at risk) or a single lobe (n = 679, 679 recurrent laryngeal nerves at risk); nodular goitre (n = 624, 1248 recurrent laryngeal nerves at risk); follicular adenoma of both lobes (n = 13, 26 recurrent laryngeal nerves at risk) or a single lobe (n = 40, 40 recurrent laryngeal nerves at risk); Hurthle cell follicular adenoma (n = 7, seven recurrent laryngeal nerves at risk); lymphocytic thyroiditis (n = 28, four recurrent laryngeal nerves at risk); medullary thyroid carcinoma (n = 9, 18 recurrent laryngeal nerves at risk); and primary squamous cell carcinoma of the thyroid (n = 1, two recurrent laryngeal nerves at risk). In total, 2460 recurrent laryngeal nerves were at risk. Demographic and clinical data of the study population stratified according to laryngoscopy findings are given in Table 2.

Table 2.

Demographic and clinical characteristics of patients undergoing partial or total thyroidectomy and perioperative laryngoscopic examination included in a study to develop a new classification scheme for abnormal vocal cord movement before and after thyroid surgery.

Characteristic	Control group n = 1515	Abnormal group
Characteristic	Control group n = 1515	Preoperatively abnormal n = 39	Postoperatively abnormal n = 65
Age range, years	19–69	21–72	23–57
Sex, male/female	350/1165	9/30	15/50
Diagnosis
Papillary thyroid carcinoma	839	11	47
Nodular goitre	591	24	9
Follicular adenoma	53	0	0
Hurthle cell follicular adenoma	7	0	0
Lymphocytic thyroiditis	18	4	6
Medullary thyroid carcinoma	7	0	2
Primary squamous cell carcinoma of the thyroid	0	0	1

Data presented as range or n.

The failure rate of IONM for detecting functional integrity in the recurrent laryngeal nerve was 10.8% (175/1619) in the total study population and 52.9% (55/104) in patients with AVCM. In the 1515 patients with normal VCM, 120 showed abnormal signals during the operation, and 1395 patients showed normal signals. The use of IONM for detecting functional integrity in the recurrent laryngeal nerve detection had sensitivity 47.1%, specificity 92.1%, positive predictive value 29.0%, and negative predictive value 96.2%.

Data regarding the clinical recovery of patients with AVCM, stratified according to classification, are given in Table 3. A significantly higher percentage of patients with preoperative type I AVCM recovered from RLNI within 1 or 7 days after surgery than those with preoperative type III AVCM (23/27 [85.3%] and 27/27 [100%] vs 1/12 [8.3%] and 1/12 [8.3%]; P < 0.001 for both comparisons). Of the 39 patients with preoperative AVCM, 34 were asymptomatic. A significantly higher percentage of asymptomatic patients than symptomatic patients recovered within 7 days (28/36 [77.8%] vs 0/5 [0%]; P = 0.001). Of the 65 patients with postoperative AVCM, 36 were asymptomatic and 29 were symptomatic. A significantly higher percentage of asymptomatic patients than symptomatic patients recovered within 7 days (28/36 [77.8%] vs 14/29 [48.3%]; P = 0.013; Table 3).

Table 3.

Clinical recovery of patients with abnormal vocal cord movement (AVCM), stratified according to type of AVCM.

Clinical parameter	AVCM Classification
Clinical parameter	Preoperative I n = 27	Preoperative III n = 12	Postoperative I n = 21	Postoperative II n = 12	Postoperative III n = 32
Asymptomatic	27	7	21	5	10
Recovery	23 (day 1) 4 (day 7)	1 (day 1)	18 (day 7) 3 (1 month)	4 (day 7) 1 (1 month)	6 (day 7) 4 (1 month)
No recovery	0	6
Symptomatic	0	5	0	7	22
Recovery	–	0	–	4 (day 7) 2 (1 month) 1 (3 months)	10 (day 7) 4 (1 month) 4 (3 months) 2 (6 months)
No recovery	–	5	–	0	2

Data presented as n.

Data regarding causes of and recovery from AVCM are given in Table 4. The 7-day recovery rate was significantly lower in patients with postoperative type II AVCM than in those with postoperative type I (8/12 [66.7%] vs 18/21 [85.7%]; P = 0.198). In addition, the 7-day and 1-month recovery rates were significantly lower in patients with postoperative type III AVCM than those with postoperative type I AVCM (16/32 [50.0%] vs 18/21 [85.7%]; P = 0.008, and 24/32 [75.0%] vs 21/21 [100%]; P = 0.013, respectively). There were no significant differences between postoperative type II and postoperative type III AVCM groups in 7-day or 1-month recovery rates.

Table 4.

Cause of and recovery from pre- or postoperative abnormal vocal cord movement (AVCM) in patients undergoing partial or total thyroidectomy.

AVCM Classification	n	Laryngeal nerve signal	Cause, n	Recovered patients, n (recovery time)
Preoperative I	27	Normal	Tumour compression, 23	23 (day 1)
Preoperative I	27	Normal	Adhesion, 4	4 (day 7)
Preoperative III	12	Normal	Primary palsy, 1	1 (day 1)
Preoperative III	12	Abnormal	Tumour invasion, 11	0
Postoperative I	21	Normal	Unclear, 10	10 (day 7)
		Abnormal	Excessive traction, 5	5 (day 7)
		Abnormal	Contusion, 5	2 (day 7) 3 (1 month)
		Abnormal	Forceps injury, 1	1 (day 7)
Postoperative II	12	Abnormal	Contusion, 7	6 (day 7) 1 (1 month)
		Normal	Unclear, 3	1 (day 7) 1 (1 month) 1 (3 months)
		Abnormal	Forceps injury, 2	1 (day 7) 1 (1 month)
Postoperative III	32	Abnormal	Tumour adhesion, 14	9 (day 7) 3 (1 month) 1 (3 months) 1 (6 months)
		Abnormal	Contusion, 7	4 (day 7) 2 (1 month) 1 (3 months)
		Normal	Unclear, 5	2 (day 7) 1 (1 month) 1 (3 months) 1 (6 months)
		Abnormal	Forcible traction, 2	1 (day 7) 1 (1 month)
		Abnormal	Dissection, 2	0
		Abnormal	Prolonged exposure, 1	1 (1 month)
		Abnormal	Forceps injury, 1	1 (3 months)

The 7-day recovery rate of combined pre- and postoperative type I AVCM was significantly higher than that of combined type II AVCM (93.8% vs 66.7%; P = 0.009) and combined type III AVCM (38.6%; P < 0.001). There was no significant difference in 7-day recovery rate between combined type II and type III AVCM, however. The recovery rate was significantly higher in combined type II AVCM than type III AVCM at 1 month (91.7% vs 56.8%,;P = 0.039), 3 months (100% vs 65.9%; P = 0.024) and 6 months (100% vs 70.5%; P = 0.049) postoperatively.

Discussion

The surgical management of thyroid disease has markedly improved during the past century.¹⁸ In the last 20 years, total thyroidectomy has become the preferred option for managing bilateral benign goitre, Graves’ disease and some thyroid cancers. The recurrent laryngeal nerves may be injured during thyroidectomy, however,¹⁹ due to complete or partial transection, traction, contusion, crush, burn, misplaced ligature or compromised blood supply. RLNI is generally unilateral and transient, but is sometimes bilateral and permanent, causing paralysis of the vocal cords or true vocal-fold paresis.^12,20 Surgeons can prevent permanent injury to the RLN during surgery by identifying and carefully tracing the recurrent laryngeal nerve’s path²¹ or using nerve-monitoring devices, but the most effective method for protecting the nerve remains unclear. Although the incidence of permanent recurrent laryngeal nerves paralysis after thyroidectomy is relatively low (0.2–2%)^1,3,9, it remains an important complication that may affect a patient’s health-related quality-of-life.

Perioperative laryngeal examinations are necessary to determine RLN function, but normal vocal quality does not ensure symmetrical VCM. The results of the current study underline the importance of laryngoscopy for visual identification of VCM. Patients with preoperative type I AVCM were at a high risk of developing RLNI during surgery in the present study, but all recovered within 7 days after surgery. Of the patients with type III preoperative AVCM in the current study, the vast majority had RLN involvement due to cancer invasion and none recovered from the injury. The prognosis for patients with type I AVCM was better than that for those with type III AVCM. In addition, the majority (87.2%) of patients in the present study with preoperative AVCM were asymptomatic. Taken together, our findings indicate that preoperative laryngoscopy is necessary in patients undergoing thyroidectomy, in order to identify the underlying cause of AVCM and aid in determining prognosis.

Repeated laryngoscopic examination may provide essential information regarding AVCM recovery. Compared with day 1 findings, laryngoscopic findings were significantly improved at day 7 after surgery in patients with type I AVCM in the present study. Recovery was slower in patients with type II or III AVCM. Timely laryngoscopic examinations are therefore extremely important for the assessment of type II and type III patients.

The present finding that 87.2% of patients with preoperative AVCM and 55.4% of those with laryngoscopically-observed postoperative AVCM were asymptomatic concurs with others who have suggested that it is arbitrary to judge VCM purely on the basis of clinical symptoms.^22–25 We suggest that regular pre- and postoperative laryngoscopic examinations should be performed in all patients scheduled to undergo thyroid surgery, in order to offer timely medical treatment, shorten recovery time and improve the outcome of patients with perioperative AVCM.

Asymptomatic patients with pre- or postoperative AVCM had significantly better outcomes than symptomatic patients, in the present study. It is possible that RLNI was less severe in asymptomatic patients than symptomatic ones, resulting in more rapid recovery. The presence of clinical symptoms may therefore be an indicator of poor outcome in patients with RLNI.

The present study is limited by the follow-up schedule, since it was not possible to determine precise recovery times for RLNI. The relationship between recovery time and RLN electrophysiological signals also requires further investigation.

In conclusion, we have developed a useful classification system for patients with RLNI after thyroidectomy. Pre- and postoperative laryngoscopy can identify asymptomatic AVCM and is essential to evaluate the extent of RLNI in these patients.

Footnotes

Declaration of conflicting interest

The authors declare that there are no conflicts of interest.

Funding

This research was supported by funding from the Changes in Spectrum of Thyroid Diseases in Jilin Province Before and After Universal Salt Iodization and its Diagnosis and Treatment Strategies (Grant No. 20110449) from the Jilin Province Science and Technology Department.

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A laryngoscopy-based classification system for perioperative abnormal vocal cord movement in thyroid surgery

Abstract

Objective

Methods

Results

Conclusion

Keywords

Introduction

Patients and methods

Study population

IONM

Laryngoscopy

Recurrent laryngeal nerve monitoring

AVCM classification

Statistical analyses

Results

Discussion

Footnotes

Declaration of conflicting interest

Funding

References