Innervation of the Cricothyroid Muscle by the Recurrent Laryngeal Nerve and Implications for Clinical Practice

Tom M. Kaffenberger, MD1; Leila J. Mady, MD, PhD, MPH1; Mathew Geltzeiler, MD2; Marlana D. Malcotti, MS, CNIM3; Carly Kleynen, CNIM4; Shaum Sridharan, MD1; Donald J. Crammond, PhD4, Partha Thirumala, MD, MS4; Jeffrey R. Balzer, PhD4; Umamaheswar Duvvuri, MD PhD1

1Department of Otolaryngology, University of Pittsburgh; 2Department of Otolaryngology, Oregon Health Science University; 3Procirca, University of Pittsburgh Medical Center; 4Department of Neurological Surgery, University of Pittsburgh

Umamaheswar Duvvuri, MD PhDEmail: DuvvuriU@upmc.edu

Corresponding Author

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460-466.3. Tschopp KP, et al. 2002. Comparison of various methods of electromyographic monitoring of the recurrent laryngeal nerve in thyroid surgery. Ann Otol Rhinol Laryngol 111: 811-816.4. Sanudo JR, et al., 1999. An anatomical study of anastomoses between the laryngeal nerves. Laryngoscope 109: 983-9875. Wu BL, et al. 1994. The human communicating nerve. An extension of the external superior laryngeal nerve that innervates the vocal cord. Arch Otolaryngol Head Neck Surg, 120:

1321-1328.6. Barczynski M, et al. 2012. Randomized controlled trial of visualization versus neuromonitoring of the external branch of the superior laryngeal nerve during thyroidectomy. World J

Surg 36: 1340-1347.7. Masuoka H, et al.2016. Innervation of the cricothyroid muscles by the recurrent laryngeal nerve. Head Neck 38: 441-445.8. Martin-Oviedo C et al 2011. Functional role of human laryngeal nerve connections. Head Neck 121: 2338-2343.9. Miyauchi A et al. 2016. Innervation of the cricothyroid muscle by extralaryngeal branches of the recurrent laryngeal nerve. Laryngoscope 126: 1157-62.10. Sosa JA et al 2013. Increases in thyroid nodule fine-needle aspirations, operations, and diagnoses of thyroid cancer in the United States. Surgery 154:1420–1426.

References

Objective: Intraoperative neurophysiological monitoring (IONM) is frequently used to identify the recurrent laryngeal nerve (RLN). Canonically, the external branch of the superior laryngeal nerve (EBSLN) innervates the cricothyroid muscle (CTM). Our study, based on recent observations showing CTM innervation by the RLN, sought to further investigate this innervation and utilize it clinically for a possible alternative and less expensive IONM of the RLN.

Study Design: Prospective study of thyroid surgery patients at a tertiary care hospital

Subjects and Methods: Fifty-seven at-risk RLNs in 44 patients were included. IONM was performed by a neurophysiology technologist with professional oversight provided by a board-certified neurophysiologist using an XLTEK monitoring system. Triggered electromyography (tEMG) was recorded using a Dragonfly laryngeal surface electrodes and intramuscular needle electrodes placed sterilely into the CTM. tEMG thresholds, onset latency , and onset-to-peak amplitude were recorded.

Results: CTM tEMG in response to ipsilateral RLN stimulation was observed in all patients. This tEMG response was comparable to the laryngeal surface recordings made in the same patients. CTM recordings had similar thresholds (1.49 mA vs. 1.41 mA) compared to laryngeal surface electrodes and was not statistically significant. We observed significant positive correlations between the two monitoring techniques in threshold, and onset latency parameters (r=0.545, p<0.0001; r=0.37, p=0.0004, respectively). No other clinical or statistical differences were noted.

Conclusions: All patients demonstrated RLN innervation of the CTM. IONM using tEMGs recorded from intramuscular needle electrodes in the CTM is comparable to laryngeal electrodes. Using intramuscular electrodes may result in increased utilization of RLN IONM based on the less expensive price of needle electrodes and the need to not use an endotracheal electrode.

Abstract

Introduction

After approval was obtained from our institution’s Quality Assurance Committee. Prospective data was collected from 44 thyroid surgeries carried out by a single surgeon and tEMGthresholds were measured at pre- and post-resection. Patients with incomplete data collection of tEMG parameters were excluded. In total, we obtained data from 57 RLNs at-risk with 84 total RLN tEMG measurements completed.

IONM was performed using the XLTEK (Natus Medical) system with two distinct types of EMG recording electrodes: laryngeal surface (Dragonfly, Neurovision) and intramuscular needle electrodes (Rhythmlink). These electrodes were used to record tEMGs after direct RLN stimulation from the vocal folds and CTM, respectively (CTM tEMG setup shown in Figure 1). The tEMG characteristics, thresholds, onset latency, and onset to peak amplitudes were measured.

Statistical analysis was carried out using Graphpad Prism (La Jolla, CA, USA).

Methods and Materials

• During stimulation of the RLN, all patients were observed to have ipsilateral CTM contraction

• There is significant positive correlation between tEMGsobtained from CTM needle electrodes and laryngeal endotracheal surface electrodes

• There were three transient RLN injuries which recovered by their first post-operative visit. Their IONM were reviewed and neither the needle electrodes or laryngeal surface electrodes showed an injury

• Clinically, this is useful given significant cost differences between electrode types: $2 for needle electrodes and $100 for laryngeal endotracheal electrodes at our institution

• CTM needle electrodes can easily be used intraoperative to troubleshoot signal loss that can be encountered using laryngeal surface electrodes

Conclusions

Conventionally, the RLN innervates the intrinsic muscles of the larynx and the EBSLN innervates the CTM. However this is overly simplistic as there are various anastomosis and interconnection between the RLN and superior laryngeal nerves including the human communicating nerve, Galen’s anastomosis, and more recently, a connection between the RLN and the CTM.

IONM is a common tool used to help identify the RLN. This is done via laryngeal electrodes placed on endotracheal tubes or needle electrodes placed directly into laryngeal muscles. We sought to expand on the previously shown RLN innervation of the CTM and assess its clinical utility during thyroid surgery by testing the tEMG profiles of needle electrodes in the CTM versus the laryngeal endotracheal electrodes during RLN stimulation.

Results

Figure 1. Dissection and exposure of the recurrent laryngeal nerve (RLN) with needle electrodes inserted into the cricothyroid muscle.

Figure 2: Average tEMG characteristics from 84 data points across 57 recurrent laryngeal nerves (RLN). RLN stimulation was recorded using laryngeal endotracheal surface tube electrodes (RLN-L) and needle electrodes placed into the cricothyroid muscle (RLN-N). We collected data on three tEMG characteristics: A. Stimulation threshold [milli-Amperes (mA)] (p=0.06); B. Onset to peak amplitude [micro-Volts (uVolt)] (p=0.76) C. Onset latency [milliseconds (msec)] (p=0.91)

Figure 3: Correlation comparison and analysis of recurrent laryngeal nerves (RLN) tEMG data with two separate recording systems: laryngeal surface electrodes (RLN-L) and cricothyroid muscle needle electrodes (RLN-N). Spearman coefficients of intra-operative recurrent laryngeal nerve stimulation using Dragonfly (RLN-L) and needle (RLN-N) electrodes were calculated for three EMG parameters: A. Threshold in milli-amperes (r=0.545; p<0.0001); B. Onset to peak Amplitude in micro-Volts (r=0.096; p=0.38); C. Onset Latency in milli-seconds (r=0.37; p=0.0004).

Table 1: Patient Demographics Total Patients 44 Number of female patients 34 (77.3%) Average age at procedure in years (SD) 51.6 (17.6%) Average time from procedure to first follow up in days (SD) 14.3 (9.1%) Primary Procedure Total Thyroidectomy 23 (52.3%) Thyroid lobectomy 21 (47.7%) Central neck dissection 12 (27%) Lateral neck dissection 7 (16%) Indication Papillary thyroid carcinoma 24 (54.9%) Thyroid nodule 8 (17.8%) Goiter 7 (15.9%) Graves disease 4 (9.1%) Anaplastic carcinoma 1 (2.3%)

Average laryngeal (RLN-L) and needle cricothyroid (RLN-N) electrodes have similar tEMG profiles with RLN stimulation

Correlation of laryngeal (RLN-L) and needle cricothyroid (RLN-N) electrode tEMGs

AcknowledgementsThe authors would like to thank the University of Pittsburgh Center for Clinical Neurophysiology and Department of Otolaryngology for their support in this study.

RLN-L

RLN- N

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Threshold

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RLN-L

RLN- N

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Onset to Peak Amplitude

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olt

RLN-L

RLN- N

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0.5

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Onset Latency

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e (m

sec)

A. B. C.