American Journal of Otolaryngology - Head and Neck Medicine and Surgery
Volume 33, Issue 1 , Pages 1-5, January 2012

Detecting and identifying nonrecurrent laryngeal nerve with the application of intraoperative neuromonitoring during thyroid and parathyroid operation☆☆☆★

  • Feng-Yu Chiang, MD

      Affiliations

    • Department of Otolaryngology, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan
    • Faculty of Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan
    • ,
  • I-Cheng Lu, MD

      Affiliations

    • Faculty of Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan
    • Department of Anesthesiology, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan
    • ,
  • Cheng-Jing Tsai, MD

      Affiliations

    • Department of Anesthesiology, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan
    • ,
  • Pi-Jung Hsiao, MD

      Affiliations

    • Faculty of Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan
    • Department of Endocrinology and Metabolism Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan
    • ,
  • Ka-Wo Lee, MD

      Affiliations

    • Department of Otolaryngology, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan
    • Faculty of Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan
    • ,
  • Che-Wei Wu, MD

      Affiliations

    • Department of Otolaryngology, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan
    • Department of Otolaryngology, Kaohsiung Municipal Hsaio-Kang Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan
    • Institute of Clinical Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan
    • Corresponding Author InformationCorresponding author. Department of Otolaryngology-Head and Neck Surgery, Kaohsiung Medical University Hospital, No.100, Tzyou First Road, Kaohsiung City 807, Taiwan. Tel.: +886 7 3121101x5009; fax: +886 7 3208264.

Received 28 August 2010 published online 09 February 2011.

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Article Outline

Abstract 

Purpose

The nonrecurrent laryngeal nerve (NRLN) is a rare anatomical variant but associated with high risk of nerve injury during thyroid and parathyroid operations. Therefore, intraoperative detection and verification of NRLN are necessary.

Method

A total of 390 consecutive patients who underwent thyroid and parathyroid operations (310 RLNs dissected on the right side and 293 nerves on the left side) were enrolled. Electrically evoked electromyography was recorded from the vocalis muscles via an endotracheal tube with glottis surface recording electrodes. At an early stage of operation, vagal nerve was routinely stimulated at the level of inferior thyroid pole to ensure normal path of RLN. If there is a negative response from lower position but positive response from upper vagal stimulation, it indicates the occurrence of a NRLN, and we localize its separation point and path.

Results

Four right NRLNs (1.3%) without preoperative recognition were successfully detected at an early stage of operation. Three patients were operated on for thyroid disease, one for parathyroid adenoma and all were associated with right aberrant subclavian artery. All NRLNs were localized and identified precisely with intraoperative neuromonitoring. Functional integrity of all nerves was confirmed by the intraoperative neuromonitoring and postoperative laryngeal examination.

Conclusions

Vagal stimulation at the early stage of operation is a simple, useful, and reliable procedure to detect and identify the NRLN.

 

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1. Introduction 

The nonrecurrent laryngeal nerve (NRLN) is a rare anatomical variant, with an incidence of 0.3% to 1.6% on the right side and 0.04% on the left side [1], [2]. The risk of nerve injury was reported with very high rate up to 75% in case the occurrence of NRLN was not recognized preoperatively [3].

Most NRLNs were reported to be associated with a right aberrant subclavian artery. Therefore, some methods such as the symptom of dysphagia, chest x-ray, barium swallow test, esophageal endoscopy, computed tomography, magnetic resonance imaging, angiography, and neck ultrasonography were reported to be used to predict the presence of NRLN preoperatively by discovering the aberrant subclavian artery [3], [4], [5], [6], [7], [8]. However, the NRLN was reported very difficult to identify preoperatively: 0% in the series of Toniato et al [2], [9] and Brauckhoff et al [10], 6% diagnosed with certainty, and 24% merely suspected in the series of Henry et al [1]. Furthermore, NRLN can occur without subclavian artery anomaly [11] or occur on the left side [1], [12]. During the operation, a large sympathetic RLN anastomotic branch can be mistaken as NRLN [13], [14], and the NRLN may be associated with a second smaller right RLN in the normal RLN position that may be mistaken as the entire RLN [15], [16]. Therefore, intraoperative detection and verification of NRLN are necessary.

Intraoperative neuromonitoring (IONM) has been commonly applied in thyroid and parathyroid operation as a means to localized and identify RLN, to predict the outcome of vocal function and to elucidate the mechanism of RLN injury [17], [18], but the usefulness of IONM for detecting and identifying NRLN was only described by Brauckhoff et al [10] in 2002. This study aimed to verify the value of vagal neurostimulation at an early stage of operation in detecting and identifying NRLN during thyroid and parathyroid operations.

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2. Materials and methods 

From April 2006 to May 2010, 390 consecutive patients who underwent thyroid or parathyroid operations with the application of IONM were enrolled. There were 163 unilateral and 227 bilateral procedures. Fourteen nerves were excluded from this study due to preoperative palsy and/or cancer invasion noted intraoperatively. Thus, in all, 603 RLNs (310 right, 293 left) were at risk in this study. All patients were intubated with Nerve Integrity Monitor (NIM) Standard Reinforced EMG Endotracheal Tube (6.0 mm for women and 7.0 mm ID for men) (Medtronic Xomed, Jacksonville, FL) for general anesthesia. The middle of the exposed electrodes was placed in contact with the true vocal cords. A Pass monopolar stimulation probe (Medtronic Xomed) was used for nerve stimulation during the operation. Electromyography (EMG) activity was recorded and displayed on a NIM-response 2.0 monitor (Medtronic Xomed). At the early stage of operation, the vagus nerve was routinely tested to ensure functional monitoring system and the normal pathway of RLN after the space between the thyroid and carotid sheath was open. The vagus was typically stimulated at the level of inferior thyroid pole with current of 2 mA for direct stimulation or 3 mA for indirect stimulation (without dissection of carotid sheath). A case of negative EMG signals at lower position and positive EMG signals at upper position indicates the occurrence of a NRLN. The separation point and path of NRLN will be localized and identified precisely at upper trachea-esophageal groove (Video).

All patients received preoperative and postoperative laryngofibroscopic examination of cord mobility. During the operation, functional nerve integrity is documented and confirmed with the registration of EMG signals, and all exposed RLNs or NRLNs are routinely photographically documented to show visual nerve integrity. The study was approved by the institutional review board of Kaohsiung Medical University Hospital and the ClinicalTrials.gov (http://www.clinicaltrials.gov. [identifier: NCT00629746]). Written informed consent was obtained from each patient. Patients were informed of the intent to use this monitoring system potentially to aid in the localization and identification of the RLNs and in the assessment of their function during operation. There was no financial or professional association between the authors and the commercial company whose nerve-monitoring product was used.

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3. Results 

Four right NRLNs (1.3% in the right and 0% in the left side) without preoperative recognition were detected due to negative response from the lower portion vagal stimulation but positive response from the upper portion vagal stimulation. The separation point and path of the NRLNs were localized and identified precisely at upper trachea-esophageal groove with IONM. One nerve was type I anomaly (Fig. 1) in which the nerve directly arises from the vagus nerve above the laryngotracheal junction and descends into the larynx, running parallel to the trunk of superior thyroid artery. Coexisting small nerve branches in the normal RLN position was also found; they could be small collateral branches to the trachea and the esophagus and could be mistaken as the normal RLN if no IONM was applied. Another 3 were type II anatomical variant (Fig. 2, Fig. 3, Fig. 4) arising from the vagus nerve below the laryngotracheal junction and running parallel to the trunk of inferior thyroid artery. Two patients were operated on for thyroid cancer, one for multiple nodular goiter and the other for right superior parathyroid adenoma (Table 1). All patients were further confirmed to have right aberrant subclavian artery on computed tomography scan, so-called arteria lusoria, but none of them reported the symptoms preoperatively. Visual and functional integrity of all NRLNs was confirmed during the operation, and symmetric vocal cord movement was also confirmed after the operation.

  • View full-size image.
  • Fig. 1. 

    Type I NRLN (case 1). The patient was operated on for papillary thyroid cancer. The NRLN (arrow) directly arises from the vagus nerve (star) at upper neck position. There are still some small nerve branches (triangle) in the normal RLN position of the tracheoesophageal groove.

  • View full-size image.
  • Fig. 2. 

    Type II NRLN (case 2). The patient was operated on for papillary thyroid cancer. The NRLN (arrow) arising from the vagus nerve (star) below the laryngotracheal junction and running parallel to the path of inferior thyroid artery.

  • View full-size image.
  • Fig. 3. 

    Type II NRLN (case 3). The patient was operated on for right upper parathyroid adenoma (triangle). (A) The right NRLN (arrow) ran below the carotid artery (circle) after arising from the vagus nerve and ran between the parathyroid adenoma (triangle) and thyroid lobe before entering into the larynx. (B) The direct root of the NRLN (arrow) branching directly off the vagus nerve (circle) can be visualized after the retraction of the carotid artery laterally and mobilizing the parathyroid adenoma (triangle).

  • View full-size image.
  • Fig. 4. 

    Type II NRLN (case 4). The patient was operated on for multinodular goiter. The NRLN (arrow) arises from the vagus nerve at lower neck position near the inferior thyroid pole. The NRLN could be misrecognized if the initial vagal stimulation level is too high.

Table 1. Characteristics of the patients with a nonrecurrent inferior laryngeal nerve
PatientAge (y)SexPathologyOperationTypeRight or leftArteria lusoriaSymptoms of arteria lusoria
169MalePTCTTIIRightYesNo
254FemalePTCTTIIRightYesNo
352FemalePTAPTEIIRightYesNo
468FemaleGoiterTTIRightYesNo

PTC indicates papillary thyroid carcinoma; TT, total thyroidectomy; PTA, parathyroid adenoma; PTE, parathyroidectomy.

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4. Discussion 

Brauckhoff and colleagues [10] first described the method of using vagal stimulation to detect the occurrence of NRLN during IONM in 2002. They performed neurostimulation of the vagus opposite the lower and the upper thyroid poles. In 9 patients with a NRLN, they found positive EMG signals proximally and negative EMG signals distally. However, this method was seldom called attention to in the literature, although IONM has been more popularly applied in thyroid and parathyroid operation. We have been using IONM in our thyroid and parathyroid operations since 2006, and we have been including vagal stimulation before and after dissection of RLN as our standardized IONM procedure [17], [19]. Because the space between thyroid lobe and carotid artery is opened, we routinely perform vagal stimulation at the level of inferior thyroid pole to confirm a working monitoring system and normal path of RLN. In this study, we experienced 9 patients with negative response from initial vagal stimulation. Among these patients, 4 NRLNs were detected due to positive response from vagal stimulation at upper position, another 5 patients were detected without positive response from proximal vagal stimulation, and all encountered equipment failure due to malposition of EMG endotracheal tube.

Based on our experience in using IONM in this study, we find that vagal stimulation is a simple and safe procedure. It can easily uncover most kinds of artifacts. It also provides the following useful data: (1) the stimulating level used to elicit an EMG response from vagus nerve can definitely elicit response from RLN, and the intensity of signal will be always greater; (2) the original data can be used to compare the results after complete dissection of RLN; and (3) the data can be used to judge a proper position of electrodes. In our experience, a stimulation level of 1 mA is adequate to elicit a maximum response on the bare vagus nerve, and it should be elevated to 2 mA in case of some fascia on the nerve. In this study, we found that it is not necessary to dissect carotid sheath and expose vagus nerve routinely. We exposed vagus nerve in the first 2 NRLNs, but in the recently 2 cases, we performed vagal stimulation without dissection of carotid sheath. We just put the nerve stimulator between carotid artery and internal jugular vein with stimulus current of 3 mA, and we could localize the separation point of NRLN and map the path of NRLN precisely (Video).

The separation of NRLN from the vagus may occur as high as the superior thyroid pole or as low as the inferior thyroid artery. Avisse et al [20] divided the courses of NRLN into types I and II: a type I anomaly in which the nerve stems from the vagus nerve above the laryngotracheal junction and descends into the larynx, running together with the vessels of the superior thyroid peduncle and a type II anatomical variant in which the nerve stems from the vagus nerve on a level with the lower thyroid artery and then follows a transversal path parallel to the inferior thyroid artery. In their series of 17 NRLN, 7 patients were type I (41%) and 10 patients were type II (59%). Toniato and colleagues reported 5 (16%) type I and 26 (84%) type II NRLNs. However, in the series of 9 NRLNs by Brauckhoff et al [10], all belonged to type I anomaly. Toniato et al [2] emphasized that type I anomaly had a higher risk of injury. In their 4 nerve injuries, 3 occurred in type I but only 1 nerve injury in type II anomaly. They claimed that ligation of upper pole vessels of the thyroid gland may consequently carry a severe risk of damaging the nerve and should be performed with great caution. In this study, we had 1 type I (Fig. 1) and 3 type II NRLNs (Fig. 2, Fig. 3, Fig. 4), and all were successfully detected and preserved at the early stage of operation with the help of IONM and vagal stimulation routinely. In addition, we find that the level of initial vagal stimulation is very important, to detect and avoid injury of the NRLN. The 3 type II NRLNs of this study could be misrecognized and had been injured if the initial vagal stimulation level is higher to the separation point. Therefore, we recommend that the initial vagal stimulation level during IONM procedures should not be proximal to the level of inferior thyroid artery.

The combination of the parathyroid tumor and NRLN was rarely reported in the literature [21]. In this study, we encountered 1 NRLN in a patient who was operated on for superior parathyroid adenoma. The right NRLN ran behind the carotid artery and ran between the parathyroid adenoma and thyroid lobe before entering the larynx (Fig. 3A). The NRLN can more easily be injured if no early localization and identification of the nerve are performed in this situation, especially when small skin incision was applied to the parathyroidectomy.

In summary, vagal stimulation at the early stage of operation is a simple, useful, and reliable IONM procedure to detect the occurrence of NRLN and to localize its separation point and path precisely during thyroid and parathyroid operations.

The following are the supplementary materials related to this article.

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Acknowledgments 

This study was supported by grants from Kaohsiung Medical University Research Foundation and (KMU-M099001) and the National Science Council (NSC 99-2314-B-037-015-MY2). We thank the study participants for their contribution to this study.

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☆ Trial registration: Clinicaltrials.gov. Identifier: NCT00629746.

☆☆ Part of this work was presented at the Fourth World Congress of International Federation of Head and Neck Oncologic Societies in Seoul, Korea, June 15–19, 2010.

★ There are no conflicts of interest or financial support from any company.

PII: S0196-0709(10)00243-7

doi:10.1016/j.amjoto.2010.11.011

American Journal of Otolaryngology - Head and Neck Medicine and Surgery
Volume 33, Issue 1 , Pages 1-5, January 2012

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