Traction injury of the recurrent laryngeal nerve: Results of continuous intraoperative neuromonitoring in a swine model

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1 ORIGINAL ARTICLE Traction injury of the recurrent laryngeal nerve: Results of continuous intraoperative neuromonitoring in a swine model Hye Yoon Lee, MD, PhD, 1 Young Geon Cho, MD, 2 Ji Young You, MD, 1 Byoung Ho Choi, MD, PhD, 2 Joon Yub Kim, MD, PhD, 3 Che-Wei Wu, MD, PhD, 4 Feng-Yu Chiang, MD, PhD, 4 Hoon Yub Kim, MD, PhD 1 * 1 Department of Surgery, Korea University Anam Hospital, Korea University College of Medicine, Seoul, Korea, 2 Advanced Materials Characterization Laboratory at School of Mechanical Engineering, Korea University, Seoul, Korea, 3 Department of Orthopaedic Surgery, Myongji Hospital, Seoul, Korea, 4 Department of Otolaryngology Head and Neck Surgery, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Taiwan. Accepted 4 December 2014 Published online 20 June 2015 in Wiley Online Library (wileyonlinelibrary.com). DOI /hed ABSTRACT: Background. Recurrent laryngeal nerve (RLN) palsy is the most serious complication after thyroidectomy. However, little is known about the degree of traction injury that causes loss of signal. The purpose of this study was to evaluate traction injuries in the swine RLN using continuous intraoperative neuromonitoring (IONM) and determine the traction power that results in loss of signal. Methods. Thirteen swine underwent traction injury to the RLNs with continuous IONM, and stress-strain curves were determined for 8 nerves using the universal material testing machine in an ex vivo model. Results. Traction injury at a mean power of 2.83 MPa caused loss of signal. The mean physiologic limit strain and tensile strength of the swine RLNs were found to be 15.0% and 4.9 MPa, respectively. Histological analysis showed no abnormal structural findings. Conclusion. Traction injury of swine RLNs causes loss of signal at a power of 2.83 MPa. However, all injured nerves recovered within 7 days with no observed structural damage. VC 2015 Wiley Periodicals, Inc. Head Neck 38: , 2016 KEY WORDS: intraoperative neuromonitoring, recurrent laryngeal nerve, traction injury, swine model, thyroidectomy INTRODUCTION Recurrent laryngeal nerve (RLN) palsy is a potential serious complication after thyroid surgery. RLN dysfunction causes voice impairment that can significantly reduce the lifelong quality of life. 1 The gold standard procedure for protection from RLN injury is routine visual identification. 2,3 Several studies have shown that routine visual identification of the RLN with or without intraoperative neuromonitoring (IONM) results in decreased rates of permanent RLN palsy. 2 5 However, inadvertent RLN injury occurs even though most surgeons must confirm the visual integrity of the RLN during the operation. 5 Furthermore, most of these injuries are not recognized intraoperatively. Several studies have reported that some types of RLN injury, such as inadvertent transection, clamping, or ligature entrapment, have become rare with the use of IONM. However, injury caused by medial traction of the thyroid still occurs and is the most common mechanism of intraoperative RLN injury This type of injury cannot be completely avoided because the thyroid must be mobi- *Corresponding author: H. Y. Kim, Department of Surgery, Korea University Anam Hospital, Korea University College of Medicine, 73 Inchon-ro, Seongbukgu, Seoul , Korea. hoonyubkim@gmail.com lized and retracted medially during preparation of the RLN. The RLN could be over-stretched and compressed on the trachea by a dense fibrous band or a crossing artery (especially at the region of Berry s ligament), during this surgical maneuver. 6 The compressive forces on the nerve could prolong and cause injury before the RLN is identified for dissection. Recently, several studies have shown that IONM can assist with RLN identification without imposing additional risks. 7,11 During the last decade, surgeons have accepted IONM as an adjunct to help localize and identify the RLN intraoperatively in order to predict vocal cord function after thyroid resection 2,12 and to elucidate the mechanism(s) of RLN injury. 6,7 Conventional IONM is now used to evaluate the function of the RLN during stimulation, but the nerve is still at risk for injury when it is not being stimulated. 2,8,10,13 Consequently, several varieties of electrodes for stimulation of the vagus nerve have been designed for continuous IONM, which is reported to offer more seamless monitoring of the nerve s functional integrity during surgery However, the electromyography (EMG) evolution and thresholds indicative of RLN injury are still uncertain. The purpose of this study was to investigate EMG signals during traction injury of the RLN in a swine model using continuous IONM and to determine the force and strain that cause traction injury of the RLN using an ex vivo model. 582 HEAD & NECK DOI /HED APRIL 2016

2 TRACTION INJURY OF THE RECURRENT LARYNGEAL NERVE IN A SWINE MODEL FIGURE 1. Traction experiment of the recurrent laryngeal nerve (RLN) in a swine model. (A) Anatomy of the swine neck. The automated periodic stimulation (APS) electrode was positioned on the left vagus nerve (arrow), and the left RLN (arrowhead) was stretched using a 5-mm-wide piece of fabric. (B) The right RLN was stretched using a string scale. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] MATERIALS AND METHODS In vivo experiment Subjects and anesthesia. Permission to perform this experiment was obtained from the Korea University Institutional Animal Care and Use Committee (Seoul, Korea KUIACUC , ). Thirteen live swine weighing 30 to 40 kg (breed: country pig-large black- Hampshire) were used in this prospective experiment. Preoperatively, the swine were fasted for 12 hours. After preanesthetic medication with intramuscular 1 mg/ kg Rompun (Bayer Health Care, Pittsburgh, PA) and 7 mg/kg Zoletil (Virbac, Carros, France), the swine were placed on an operating table in the supine position with their necks extended. Rompun is xylazine hydrochloride, which is a short-acting muscle relaxant. Neuromonitoring began 30 minutes after preanesthetic medication. A pulse oximeter and electrocardiogram leads were attached. The swine were intravenously cannulated at the auricular vein and received a continuous intravenous infusion of lactated Ringer s solution at 5 ml/kg/hr throughout the operation. The swine were intubated with a nerve integrity monitor (NIM) EMG endotracheal tube (Medtronic, Jacksonville, FL) without administration of a neuromuscular blocking agent. The size of the EMG endotracheal tube was determined by visual inspection of the larynx and was confirmed by the ability to pass the tube without resistance. We used a 6-mm internal diameter endotracheal tube in all cases. Tidal volume and respiratory rate were set at 8 ml/kg and 15 breaths per minute, respectively. After oral intubation, intravenous prophylactic antibiotics were administered in the form of a single shot of 1500 mg cefuroxime. Intraoperative neuromonitoring. To investigate real-time EMG changes during traction injury of the RLN, we used continuous IONM via automated periodic stimulation (APS; APS Electrode Stimulator probe [2.0 mm; Medtronic]) of the vagus nerve. For EMG monitoring, we used NIM 3.0 Nerve Monitoring Systems (Medtronic). APS is a pulse generator for continuous stimulation (1/ 6 s, 100 us, 1 ma). A conventional monopolar stimulation probe (4 pulse/s, 100 us, 1 ma; Medtronic) was used for identification and intermittent stimulation of the RLN. After determining the APS baseline for amplitude and latency of the evoked response, continuous stimulated EMG signals were recorded during traction of the RLN. An upper threshold for latency (110%) and a lower threshold for amplitude (250%) were set as separate alarm thresholds. In addition, acoustic and optic signals alerted the surgeon if a preset threshold had been crossed or electrode had been dislocated. Operation and experimental design. After surgical disinfection, a low collar incision was made for exposure of the neck and larynx. Bilateral vagus nerves and RLNs were identified using a handheld stimulation probe. Bilateral vagus nerves were completely isolated from the main surgical field to apply the APS probe. The APS electrode was carefully positioned on the vagus nerve, keeping the enclosure tabs open with forceps. After connecting the APS electrode to the NIM 3.0 system, baselines for latency and amplitude were automatically calibrated. To minimize potential bias, all testing was conducted without manipulation or traction of the trachea in order to avoid altering the electrode contacts. The surgical field was maintained bloodless, and the nerves to be stimulated were dissected from the fascia. RLN traction injury experiments were performed in 13 swine (26 RLNs). After preparing the RLN, a 5-mm-wide fabric strip made of a surgical drape was wrapped around the nerve, and the nerve was retracted with a force between 1 N (newton) and 6 N (see Figure 1) at the level of the third or fourth tracheal ring. This traction injury was caused by direct distress on the nerve by stretching the ligament, and it created a point of injury on the HEAD & NECK DOI /HED APRIL

3 LEE ET AL. nerve. 6 Therefore, we evaluated the type 1 stretch injury of Chiang s classification in this swine model. 6 In 1 subject, 1 RLN was retracted until loss of signal was observed, and the other RLN was retracted with a force 1 N lower than the force causing loss of signal of the contralateral RLN. The nerves that had loss of signal were designated to the loss of signal group, and the others to the no loss of signal group. Induced EMG changes and recovery were displayed and recorded continuously with the continuous IONM system throughout the experiment. We calculated the mean traction power that caused loss of signal using the equation: r5f=d 2 The mean traction power(r) is measured in megapascal (MPa), where F is the loading force at the time of loss of signal and d is the diameter of the recurrent laryngeal nerve. The loading force (F) is measured in newton (N). Electron microscopic examination. All nerves in the loss of signal group were examined by electron microscopy. We sutured the nerve at the point of traction with 6-0 nylon and observed the point of traction by electron microscopy. Ex vivo experiment After the in vivo experiments, we harvested the RLNs from the no loss of signal group for stress-strain evaluation. The nerves were gradually stretched in the universal material testing machine (MTS Systems, Minneapolis, MN) at the rate of 1 cm/min (strain of 0.5%/s) in order to evaluate the stress-strain correlation. All 13 RLNs were harvested, but ex vivo experiments were performed for only 8 nerves because we were unable to attach the thin nerves to the universal material testing machine. Load deformation and strain-stress curves of the RLN were determined for the 8 nerves examined. We measured the physiologic limit strain and tensile strength as well as the ultimate strain and the tensile strength by the strain-stress curve. We define physiologic limit strain as the degree of maximum strain produced by the RLN while maintaining its physiological structure. Up to the physiologic limit strain, the strain-stress curve corresponds to extension of the epineurium and straightening of the funiculi. 17 Nerves can stretch even beyond the physiologic limit strain and reach the ultimate strain. From physiologic limit to ultimate strain, morphology changes are not grossly apparent and the stretched nerve is elastic and obeys Hooke s law. 17 However, after the ultimate strain, we observed breakage of tiny fibers around the nerve, resulting in nerve thinning and leading to tensile failure. The strain parameters are measured in percentiles (%), which are calculated using the following equation: ((Length of the RLN with tensile stress) 2 (Length of the RLN without traction force)) / (Length of the RLN without traction force) (%) The ultimate tensile strength equates to the force at the limit state of tensile stress that leads to tensile failure. We calculated the tensile strength at the physiologic limit strain and the ultimate tensile strength at the limit of tensile stress using the equation: r5f=d 2 The tensile strength at the physiologic limit strain and ultimate tensile strength is measured in megapascal (MPa), where F is the loading force at the limit state of tensile stress, and d is the diameter of the recurrent laryngeal nerve. The loading force (F) is measured in newton (N). RESULTS Continuous intraoperative neuromonitoring during traction injury of the recurrent laryngeal nerve The mean diameter of the 26 RLNs was 1.5 mm (range, mm). The mean baseline amplitude of the EMG for the 26 RLNs was mv, and the mean baseline latency was 7.2 ms (Table 1). Among the 26 RLNs, 13 were stretched until loss of signal, and this was performed unilaterally in each swine. In the loss of signal group, the mean traction power that caused loss of signal was 4.0 N and 2.83 MPa. One case showed EMG signal recovery just after the traction study. The left nerve of swine #8 showed latency recovery 42 seconds and amplitude recovery 54 seconds after loss of signal (Figure 2A). The other 12 nerves showed no EMG signal recovery during the traction study (Figure 2B). Seven days after the traction study, all 13 nerves in the loss of signal group showed EMG signal recovery (Table 2). On the seventh postoperative day, recovery of EMG signal was evaluated by continuous IONM. The mean percentage of EMG amplitude recovery was 72.2% , and the mean percentage of latency recovery was 105.6%. Every nerve in the loss of signal group recovered >50% of its amplitude and <110% of its latency within 7 days. The percentage of amplitude recovery differed significantly between the loss of signal and no loss of signal groups (amplitude % vs 92.54% ; p <.001; 95% confidence interval to 29.96). However, there was no significant difference in latency recovery between the 2 groups (latency vs ; p 5.784; Table 3). In the no loss of signal group, four nerves showed >110% increase in latency only during the traction study (Figure 2C), with <50% change in amplitude. One nerve had >50% decrease in amplitude during the traction study without any changes in latency (Table 3). Stress-strain study of the recurrent laryngeal nerve A stress-strain graph was obtained by stretching the nerves using the universal material testing machine (see Figure 3). For the first nerve, the curve illustrated a stress-strain relationship during straightening of the nerve, the bundles of which are usually undulated. Linear stiffness was achieved at the point (a) in Figure 3. From the point (a), the curve shows a linear relationship between stress and strain of the nerve, which is characteristic of an elastic material. The slope of the stress-strain curve remained unchanged from (a) to (b), however, the load decreased suddenly at point (c), indicating the limit of elasticity of the nerve trunk. Elongation continued with a steadily diminishing load. 584 HEAD & NECK DOI /HED APRIL 2016

4 TRACTION INJURY OF THE RECURRENT LARYNGEAL NERVE IN A SWINE MODEL TABLE 1. Electromyography signal change in traction injury of swine recurrent laryngeal nerves. Baseline EMG EMG after traction injury EMG on postoperative 7th day Subject # (side) Weight, kg Nerve diameter, mm uv ms uv ms Loss of signal Maximum traction power, N uv % ms % 1 (L) No (R) Loss of signal (L) Loss of signal (R) Latency only (L) Loss of signal (R) Latency only (L) Loss of signal (R) No (L) No (R) Loss of signal (L) Loss of signal (R) No (L) Loss of signal (R) No (L) Loss of signal (R) No (L) Latency only (R) Loss of signal (L) Amplitude only (R) Loss of signal (L) Loss of signal (R) Latency only (L) Loss of signal (R) No (L) Loss of signal (R) No Mean Abbreviations: EMG, electromyography; L, left; R, right. From (a) to (b) in Figure 3, morphology changes were not grossly apparent. At point (b), we observed breakage of tiny fibers around the nerve, resulting in nerve thinning. Up to point (a), the physiologic limit strain, the nerve stretched within its physiological range. Therefore, we evaluated the physiologic limit strain and tensile strength at physiologic limit strain in 8 nerves. The mean physiologic strain limit and corresponding tensile strength of the swine RLNs were found to be 15.0% and 4.9 MPa, respectively. Ultimate strain occurred at point (b), and we evaluated ultimate strain and ultimate tensile strength in the 8 nerves. The mean ultimate strain and ultimate tensile strength of the swine RLNs were found to be 21.5% and 6.6 MPa, respectively. Electron microscopic findings All nerves in the loss of signal group were examined by electron microscopy. All components of the nerve trunk were present throughout the process of stretching. The epineurium, perineurium, and endoneurium remained intact throughout the test (see Figure 4). In this study, there was no visual injury of RLNs in the loss of signal group, either grossly or microscopically. DISCUSSION Using continuous IONM, we evaluated EMG signal changes and the traction power that causes loss of signal during traction injury of swine RLNs. We showed that EMG signals of RLNs experiencing loss of signal recovered within 7 days. In 1 case, after only 54 seconds, the EMG signal recovered to >50% of the original amplitude and <110% of the latency. We also showed that the percentage of EMG recovery was significantly different between the loss of signal group and the no loss of signal group. If traction did not induce loss of signal, the EMG showed nearly full recovery (92.5% amplitude, 103.3% latency) within 7 days. For surgeons who perform thyroid operations using continuous IONM, our findings may be relevant with regard to the surgical maneuvers that may stretch the RLNs, with the ultimate goal of reducing the occurrence of RLN dysfunction and preventing permanent RLN palsy. Recent continuous IONM clinical studies report that surgical maneuvers, particularly traction on the thyroid, correlate well with depression of the EMG response. 10,18 In the present in vivo study using a swine model, traction injury caused reversible EMG changes or loss of signal. When loss of signal was observed, traction was terminated. The RLNs were stretched over a very short time and all 26 nerves recovered EMG signals within 7 days. Our findings indicate that a short duration of traction injury can be reversible. However, the safe traction duration is still unknown. In this study, APS was a continuous pulse stimulation over 6 seconds. Therefore, the duration of manageable traction might be shorter than 6 seconds. HEAD & NECK DOI /HED APRIL

5 LEE ET AL. FIGURE 2. Electromyography (EMG) signal change of the recurrent laryngeal nerve (RLN) during traction in swine models. (A) EMG signal of the left RLN of swine #8 in the loss of signal group. Loss of signal occurred after 36 seconds of traction. Latency recovered after 42 seconds, and amplitude recovered after 54 seconds. (B) EMG signal change of the right RLN of swine #10 in the loss of signal group. Amplitude and latency did not recover within 168 seconds. After 30 minutes, intermittent stimulation was performed to evaluate the EMG signal of the nerve, but neither amplitude nor latency recovered. On the seventh postoperative day, the EMG signal of this nerve recovered 59% of its amplitude and 107.1% of its latency. (C) EMG signal change of the left RLN of swine #9 in the no loss of signal group. After 54 seconds, the EMG signal showed >10% increase in latency without a change in amplitude. Latency recovered within 36 seconds. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] Further investigation is needed to evaluate the safe duration of traction of RLNs during thyroid surgery. In the no loss of signal group, latency changed in 4 cases and amplitude changed in 1 case. Previous studies suggest amplitude change is a better parameter for monitoring EMG signals of RLNs. 19 However, our findings are not consistent with those studies, possibly because of our small sample size. Nevertheless, our results suggest that a change in the latency of the RLN may be as important a parameter for assessing RLN injuries as a change in amplitude. In this animal study, we focused on evaluating the traction power that caused loss of signal in RLNs. In the current in vivo study, we showed that the mean traction power that caused loss of signal was 2.83 MPa. One MPa represents the force of 10 kg per cm In the ex vivo stress-strain study, the physiologic strain limit and traction power were 15.0% and 4.9 MPa, respectively. We hypothesize that the physiologic strain limit and traction power result in loss of signal because of the morphologic changes of the RLN that occur at those limits. However, the power that resulted in loss of signal was different between the in vivo and the ex vivo studies. This difference might be due to additional stretching of the nerves by surrounding structures in the in vivo study. Indeed, a lower traction power was needed to cause loss of TABLE 2. Electromyography signal change and maximum traction power in traction injury of thirteen recurrent laryngeal nerves in loss of signal group. Subject # (side) Nerve diameter, mm Baseline EMG EMG after traction injury Maximum traction power, uv ms uv ms EMG on postoperative 7th day N MPa uv % ms % 1 (R) (L) (L) (L) (R) (L) (L) (L) (R) (R) (L) (L) (L) Mean % Abbreviations: EMG, electromyography; L, left; R, right. 586 HEAD & NECK DOI /HED APRIL 2016

6 TRACTION INJURY OF THE RECURRENT LARYNGEAL NERVE IN A SWINE MODEL TABLE 3. Electromyography signal change and maximum traction power of 13 recurrent laryngeal nerves in no loss of signal group. Baseline EMG EMG after traction injury EMG on postoperative 7th day Subject # (side) Nerve diameter, mm uv ms uv ms Loss of signal Maximum traction power, newton uv % ms % 1 (L) No (R) Latency only (R) Latency only (R) No (L) No (R) No (R) No (R) No (L) Latency only (L) Amplitude only (R) Latency only (R) No (R) No Mean 92.54% Abbreviations: EMG, electromyography; L, left; R, right. signal in the in vivo study. These findings suggest that a traction power lower than 4.9 MPa may cause loss of signal in thyroid operations in humans. Previous studies on stretch injury of peripheral nerves have reported that elasticity of the whole nerve trunk depends mainly upon the epineurium. 17 If the epineurium is not injured, nerve function is preserved. In the present study, electron microscopy revealed an intact epineurium in all 13 nerves in the loss of signal group. Therefore, reversible traction injury did not change the epineurium of the RLNs. However, even in reversible traction injury, IONM and continuous IONM can detect loss of signal. Thus, both may be useful for monitoring loss of signal and preventing RLN injuries during thyroid surgery. This study had several limitations. First, the duration of stimulation by APS was 6 seconds, which might be too long to evaluate the continuous monitoring of RLN injury. Second, the study was conducted in an animal model, which affects its generalizability to humans. Although reversible traction injury did not induce structural damage in the swine RLNs, this may not be the case in humans. In conclusion, traction of swine RLNs caused loss of signal at a mean power of 2.83 MPa. All nerves that experienced loss of signal at a mean traction power of FIGURE 3. Stress-strain relationship in traction of the recurrent laryngeal nerve (RLN) in the ex vivo study. From the first point (a), the curve shows a linear relationship between stress and strain of the nerve. The slope of the stress-strain curve remains unchanged from (a) to (b), then the load decreases suddenly at (c), the limit of elasticity of the nerve trunk. Until point (a), the nerve stretched within its physiological range; the physiologic strain limit occurred at point (a). Ultimate strain occurred at point (b). From this stress-strain curve, we evaluated the physiologic strain limit and ultimate strain and the power at the time of limit and ultimate strain. Gross features of the stretched nerve at each point are shown in the inset box. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] FIGURE 4. Electron-microscopic examination of the swine recurrent laryngeal nerve (RLN) in a traction model. All components of the nerve, including the epineurium, perineurium, and endoneurium, remained intact at the stretched point. HEAD & NECK DOI /HED APRIL

7 LEE ET AL MPa showed recovery of EMG signals within 7 days. However, there was a significant difference in the degree of recovery between the loss of signal and no loss of signal groups. Therefore, surgical procedures involving the thyroid should aim to minimize stretching of the RLN in order to prevent loss of signal and RLN dysfunction. Additionally, all nerves with or without loss of signal were observed to recover EMG signals within 7 days. In summary, this study showed that reversible traction injury might not induce structural damage of swine RLNs. REFERENCES 1. Smith E, Taylor M, Mendoza M, Barkmeier J, Lemke J, Hoffman H. Spasmodic dysphonia and vocal fold paralysis: outcomes of voice problems on work-related functioning. Journal of voice: official journal of the Voice Foundation 1998;12(2): Dralle H, Sekulla C, Lorenz K, Brauckhoff M, Machens A; German IONM Study Group. Intraoperative monitoring of the recurrent laryngeal nerve in thyroid surgery. World J Surg 2008;32: Randolph GW. Surgical anatomy of the recurrent laryngeal nerve. In: Randolph GW, editor. Surgery of the thyroid and parathyroid glands. Philadelphia, PA: Saunders; pp Dralle H, Sekulla C, Haerting J, et al. Risk factors of paralysis and functional outcome after recurrent laryngeal nerve monitoring in thyroid surgery. Surgery 2004;136: Chiang FY, Wang LF, Huang YF, Lee KW, Kuo WR. Recurrent laryngeal nerve palsy after thyroidectomy with routine identification of the recurrent laryngeal nerve. Surgery 2005;137: Chiang FY, Lu IC, Kuo WR, Lee KW, Chang NC, Wu CW. The mechanism of recurrent laryngeal nerve injury during thyroid surgery the application of intraoperative neuromonitoring. Surgery 2008;143: Snyder SK, Lairmore TC, Hendricks JC, Roberts JW. Elucidating mechanisms of recurrent laryngeal nerve injury during thyroidectomy and parathyroidectomy. J Am Coll Surg 2008;206: Chiang FY, Lee KW, Chen HC, et al. Standardization of intraoperative neuromonitoring of recurrent laryngeal nerve in thyroid operation. World J Surg 2010;34: Dionigi G, Alesina PF, Barczynski M, et al. Recurrent laryngeal nerve injury in video-assisted thyroidectomy: lessons learned from neuromonitoring. Surg Endosc 2012;26: Schneider R, Randolph GW, Sekulla C, et al. Continuous intraoperative vagus nerve stimulation for identification of imminent recurrent laryngeal nerve injury. Head Neck 2013;35: Snyder SK, Hendricks JC. Intraoperative neurophysiology testing of the recurrent laryngeal nerve: plaudits and pitfalls. Surgery 2005;138: ; discussion Randolph GW, Dralle H, International Intraoperative Monitoring Study Group, et al. Electrophysiologic recurrent laryngeal nerve monitoring during thyroid and parathyroid surgery: international standards guideline statement. Laryngoscope 2011;121 Suppl 1:S1 S Wu CW, Dionigi G, Sun H, et al. Intraoperative neuromonitoring for the early detection and prevention of RLN traction injury in thyroid surgery: a porcine model. Surgery 2014;155(2): Lamade W, Ulmer C, Seimer A, et al. A new system for continuous recurrent laryngeal nerve monitoring. Minim Invasive Ther Allied Technol 2007; 16(3): Ulmer C, Koch KP, Seimer A, et al. Real-time monitoring of the recurrent laryngeal nerve: an observational clinical trial. Surgery 2008;143(3): Schneider R, Przybyl J, Hermann M, Hauss J, Jonas S, Leinung S. A new anchor electrode design for continuous neuromonitoring of the recurrent laryngeal nerve by vagal nerve stimulations. Langenbecks Arch Surg 2009; 394(5): Haftek J. Stretch injury of peripheral nerve. Acute effects of stretching on rabbit nerve. J Bone Joint Surg Br 1970;52(2): Schneider R, Bures C, Lorenz K, Dralle H, Freissmuth M, Hermann M. Evolution of Nerve Injury with Unexpected EMG Signal Recovery in Thyroid Surgery Using Continuous Intraoperative Neuromonitoring. World J Surg 2013;37(2): Lo CY, Kwok KF, Yuen PW. A prospective evaluation of recurrent laryngeal nerve paralysis during thyroidectomy. Arch Surg 2000;135(2): Coghill AM, Garson LR, American Chemical Society. The ACS style guide: effective communication of scientific information. 3rd ed. Washington, DC, Oxford; New York: American Chemical Society; Oxford University Press; xiv, 430 p. p. 588 HEAD & NECK DOI /HED APRIL 2016