Clinical Anatomy 00:00–00 (2014)
ORIGINAL COMMUNICATION
Superior Laryngeal Nerve Monitoring Using Laryngeal Surface Electrodes and Intraoperative Neurophysiological Monitoring During Thyroidectomy BENJAMIN L. HODNETT,1 NICOLE C. SCHMITT,1 DANIEL R. CLAYBURGH,2 ALEX BURKOWSKY,3 JEFFREY BALZER,4 PARTHASARATHY D. THIRUMALA,5 AND UMAMAHESWAR DUVVURI6* 1
Department of Otolaryngology, University of Pittsburgh Medical Center, Eye and Ear Institute, Pittsburgh, Pennsylvania 2 Department of Otolaryngology-Head and Neck Surgery, Oregon Health and Science University, Portland, Oregon 3 Clinical Neurophysiology Tech, Procirca—Center for Clinical Neurophysiology (CCN), UPMC Presbyterian Hospital, Pittsburgh, Pennsylvania 4 Neuroscience & Acute and Tertiary Care Nursing, Center for Clinical Neurophysiology (CCN), UPMC Presbyterian Hospital, Pittsburgh, Pennsylvania 5 Center for Clinical Neurophysiology (CCN), UPMC Presbyterian Hospital, Suite B-400, Pittsburgh, Pennsylvania 6 University of Pittsburgh Medical Center, VA Pittsburgh Health System, Eye and Ear Institute, Pittsburgh, Pennsylvania
The objective of this study is to establish normative waveform data for the external branch of the superior laryngeal nerve (SLN) utilizing laryngeal surface electrodes and intraoperative neurophysiological monitoring (IONM) in conjunction with a clinical neurophysiologist. A retrospective chart review of 91 consecutive at-risk SLN were identified in 51 patients in whom IONM using laryngeal surface electrodes was performed by a clinical neurophysiologist using Dragonfly (Neurovision Medical Products, Ventura, CA) recording electrodes and a Protektor (Natus Medical Inc., San Carlos, CA)16 channel- intraoperative nerve monitoring system. Inclusion criteria were met for 30 SLN. Data collected included preoperative diagnosis, surgical procedure, rates of nerve identification and stimulation, and waveform characteristics. Waveform analysis for 30 SLN yielded a peak latency of 4.0 6 0.2 ms, onset latency 2.3 6 0.1 ms, peak-to-peak amplitude of 220.4 6 31.1 mV, onset-to-peak amplitude of 186.0 6 25.0 mV, and stimulation current threshold of 0.55 6 0.03 mA (data5 mean 6 SEM). Two patients had abnormal SLN function documented clinically on postoperative laryngoscopic examination. Laryngeal surface electrodes were successfully utilized to identify and monitor SLN function intraoperatively. Abbreviations used: EMG, electromyography; IONM, intraoperative neurophysiological monitoring; SLN, superior laryngeal nerve. Contract Grant sponsor: Department of Veterans Affairs, BLSR&D, and the PNC Foundation (UD). *Correspondence to: University of Pittsburgh Medical Center, VA Pittsburgh Health System, Eye and Ear Institute, 200 Lothrop Street, Suite 500, Pittsburgh, PA 15213. E-mail: [email protected]
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2014 Wiley Periodicals, Inc.
Oral Presentation at Combined Otolaryngology Spring Meetings, May 14-18, 2014, Las Vegas, Nevada. Received 16 August 2014; Revised 18 October 2014; Accepted 19 October 2014 Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/ca.22487
2
Hodnett et al.
IONM using laryngeal surface electrodes enables analysis of waveform morphology and latency in addition to threshold and amplitude data obtained with the traditional NIM system, potentially improving the performance of nerve monitoring during thyroid surgery. Clin. Anat. 00:000–000, 2014. VC 2014 Wiley Periodicals, Inc.
Key words: external branch of superior laryngeal nerve; nerve monitoring and stimulation; thyroid surgery
INTRODUCTION The external branch of the superior laryngeal nerve (SLN) is responsible for motor innervation of the cricothyroid muscle. This muscle acts to tilt the thyroid cartilage and tense or elongate the vocal folds. Injury to this nerve may affect the ability to produce highfrequency sounds as well as impact the overall quality of voice and vocal projection (Sulica, 2004). The SLN is at risk during dissection of the superior pole during thyroidectomy. Previous studies have reviewed the surgical anatomy of the external branch of the SLN (Fig. 1) as well as its rate of identification intraoperatively (Lennquist, 1987; Kierner, 1998; Cernea, 1992; ski, 2012; Barczyn ski, 2013). Various techniBarczyn ques for intraoperative SLN monitoring exist. Normative data have been established for the SLN using intraoperative nerve monitoring with NIM tubes (a form of endotracheal tube-based surface electrodes) ski, 2012; Potenza, 2013; Darr, 2014). How(Barczyn ever, the use of continuous intraoperative neurophysiological monitoring (IONM) in conjunction with a clinical neurophysiologist during thyroidectomy has not been routinely utilized. The objective of this study was to further enhance standardization of intraoperative nerve monitoring by establishing normative waveform data for the SLN utilizing laryngeal surface electrodes and IONM in conjunction with a clinical neurophysiologist.
MATERIALS AND METHODS A retrospective review of patients undergoing thyroidectomy with intraoperative electromyography (EMG) monitoring from January 2012 to July 2013 was conducted. The patient list was initially queried for all procedures involving intraoperative nerve monitoring using Dragonfly laryngeal surface electrodes and the Protektor (Natus Medical, San Carlos, CA) IONM system from January 2012 to July 2013. This initial query included patients undergoing thyroidectomy, parathyroidectomy, and central/lateral neck dissection for thyroid carcinoma. This was later revised to include only thyroidectomy with or without associated procedures such as parathyroidectomy or neck dissection as SLN was not routinely performed for parathyroidectomy or neck dissection alone. All operations were performed by one surgeon who routinely identifies the external branch of the SLN. Operative reports were reviewed for each patient. Data collected included preoperative diagnosis, surgical procedure,
and whether the SLN was identified and/or stimulated during the case. Laterality of each nerve was recorded. Diagnostic and intraoperative factors were collected from preoperative and operative reports including information regarding surgery for large goiter, significant intraoperative retraction, Graves’ disease, Hashimoto’s thyroiditis, prior radioactive iodine ablation, prior radiation therapy, intraoperative inflammation/fibrosis, or extensive tumor. The final pathological diagnosis was also recorded for each case. Preand postoperative clinical notes were reviewed for each patient. Inclusion criteria included: (1) documented SLN identification in the operative report and (2) documented SLN identification in the neurophysiological case record. Excluded nerves were those in which incomplete records were identified or the laterality of the SLN nerve was not evident in the neurophysiological case record. All thyroidectomy and parathyroidectomy cases at our institution are performed utilizing Dragonfly (Neurovision Medical Products, Ventura, CA) laryngeal surface electrodes (Fig. 2) and continuous neurophysiological monitoring in conjunction with a clinical neurophysiologist. During the surgery, the monitoring is performed with a neurophysiology technologist in the operating room and a board-certified clinical neurophysiologist viewing the data remotely in real-time. The intraoperative EMG data is collected by the Center for Clinical Neurophysiology and also reviewed at the end of each case. For each of the patients in this study, EMG data were retrospectively reviewed. SLN waveforms were identified from the EMG data and used to calculate latencies and amplitudes. Onset latency and peak latency were measured in milliseconds (ms). Onset-to-peak amplitude and peak-to-peak amplitude were measured in microvolts (mV). Intensity of electrical stimulation was also recorded in milliamps (mA). Onset latency was defined as the time from the initial deflection at baseline to the waveform response. Peak latency was defined as the time from the electrical stimulus to the waveform response. Onset-to-peak amplitude was defined as the amplitude from the baseline to the peak of the waveform response. Peak-to-peak amplitude was defined as the amplitude from the positive deflection to the negative deflection. Figure 3 illustrates the waveform parameters. Final analysis of waveform parameters included only SLN waveforms that were positively identified from the collected EMG data. Data are reported as mean 6 SEM. Statistical analysis was performed using Student t-test or MannWhitney Rank Sum test where appropriate.
Superior Laryngeal Nerve Monitoring
Fig. 1. Schematic drawing of the SLN. Note the innervation of the cricothyroid muscle (CT) by the external branch of the superior laryngeal nerve (EBSLN). IBSLN, internal branch of superior laryngeal nerve; RLN, recurrent laryngeal nerve.
RESULTS Table 1 lists demographic data. A total of 54 operations on 51 patients were identified from the database during the time period. The mean age at time of surgery was 44 6 2 years, with a range from 8 to 85 years of age. Total thyroidectomy was the most common surgery accounting for 36 of 54 operations (67%). Of the remaining thyroid lobectomies, 3 of 18 were completion thyroid lobectomies (17%). The final pathological diagnosis was noted for the patients with the majority performed for thyroid malignancy (71%). Patient risk factors were also recorded from the clinic records with a large goiter or mass noted in 20% of the patients. Table 2 reviews operative findings. Based on the total number of operations and sides of the operations, 91 SLN were at risk during the operations. The positive identification rate per the operative reports was 67%. Intraoperative findings were also noted with extensive tumor or dissection noted in 12% and inflammation or fibrosis in 8% of cases. Postoperative flexible laryngoscopy noted two patients with decreased elongation of the true vocal folds suggesting possible SLN injury. Unfortunately, EMG data were not sufficient on these two SLN to perform accurate waveform analysis. Review of intraoperative EMG data allowed for analysis of 30 SLNs. Latency and amplitude data are presented in Table 3 for all SLN as well as right (n 5 18) and left (n 5 12) groups. There were no significant dif-
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Fig. 2. Videolaryngoscope monitor visualization of placement utilizing Dragonfly laryngeal surface electrodes. The left electrode is visible adjacent to the left vocal fold (LVF). RVF, right vocal fold. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary. com.]
ferences between the groups for latency, amplitude, or stimulation current parameters.
DISCUSSION IONM is commonly utilized during thyroidectomy to decrease the incidence of recurrent laryngeal nerve palsy. The most commonly utilized IONM systems rely on laryngeal surface electrodes (Randolph, 2011). Various monitoring systems include audio and/or visual identification features such as the NIM (Medtronic Inc.) system. At our university, recurrent laryngeal nerve monitoring is also performed using laryngeal surface electrodes. However, the IONM is performed in conjunction with a board-certified clinical neurophysiologist performing real-time monitoring. In addition, this system records waveform morphology and additional neurophysiologic parameters not recorded by other monitoring systems. The SLN may also be monitored intraoperatively. Injury to this nerve during thyroidectomy may result in impaired elongation of the true vocal fold, resulting in decreased pitch and vocal register, as well as increased vocal fatigue (Bevan, 1989; Cernea, 1992; ski, 2013). Direct EMG recordings of the Barczyn external branch of the SLN have been performed previously using electrodes placed in the cricothyroid muscle intraoperatively (Selvan, 2009). IONM using the NIM system and laryngeal surface electrodes has also been utilized in several studies for identification of the SLN (Dionigi, 2009; Lifante, 2009). Normative data have been collected in three studies using the ski, 2012; Potenza, 2013; Darr, NIM system (Barczyn 2014). To our knowledge, no studies have reported normative data for the SLN when IONM is performed
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Fig. 3. Waveform parameters and measurement. Panel A represents measurement of peak latency. Panel B represents onset latency. Panel C represents onset-topeak amplitude. Panel D represents peak-to-peak amplitude.
in conjunction with a clinical neurophysiologist. Our study sought to establish detailed normative data for SLN monitoring using laryngeal surface electrodes TABLE 1. Demographic Data Variable Number of patients Male Female Age at surgery Total operations Total thyroidectomy Thyroid lobectomy Final diagnosis Malignant Benign Risk Factors Large goiter/mass Grave’s disease Hashimoto’s thyroiditis Prior radioactive iodine ablation Prior neck irradiation
Data (n) 51 11 40 44 6 2 years (range 8–85 years) 54 36 18 (three completion)
when the monitoring is performed in conjunction with a clinical neurophysiologist. ksi et al. (2012) randomized 210 female Barczyn patients to two groups, one group having visual identification alone of the SLN and the second having IONM performed with the NIM monitoring system. The primary endpoint of their study was identification rate of the SLN with secondary endpoints noting anatomic variability and postoperative voice performance. Stimulation was performed with 1 mA of current, and the mean amplitude was noted to be 249.5 6 144.3 mV for 130 SLN positively identified. Potenza et al. (2013) performed IONM with the NIM monitoring system on
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TABLE 2. Operative Findings
10 1 3 1
Superior laryngeal nerves at risk Positively Identified Unknown or Not Identified Intraoperative inflammation or fibrosis Extensive tumor or dissection Significant retraction
1
Variable
Data (n) 91 61 30 4 6 1
Superior Laryngeal Nerve Monitoring
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TABLE 3. Superior Laryngeal Nerve Waveform Data Nerve All SLN (n 5 30) Right SLN (n 5 18) Left SLN (n 5 12)
Peak latency (ms)
Onset latency (ms)
Peak-to-peak amplitude (mV)
Onset-to-peak amplitude (mV)
Stimulation current (mA)
4.0 6 0.2 4.2 6 0.2 3.7 6 0.2 P 5 0.310
2.3 6 0.1 2.4 6 0.1 2.3 6 0.2 P 5 0.287
220.4 6 31.1 230.0 6 46.8 207.8 6 30.2 P 5 0.712
186.0 6 25.0 185.1 6 36.4 172.9 6 29.9 P 5 0.626
0.55 6 0.03 0.53 6 0.03 0.56 6 0.04 P 5 0.654
Data expressed as mean 6 SEM.
72 consecutive patients undergoing thyroidectomy. Endpoints for this study were response amplitudes, latencies, and thresholds. Stimulation was performed with 2 mA of current for initial nerve mapping and 1 mA for subsequent stimulations, and the mean amplitude 5 269.9 6 178.6 mV for 55 SLN positively identified. A significant difference was noted between the left (358.8 mV, n 5 24) and right (204.9 mV, n 5 31) SLN. The mean threshold was reported for five SLN and noted to be 0.5 6 0.1 mA. Latencies were also measured. The latency for the four left SLN was 5.75 ms, whereas the latency for the two right SLN was 3.5 ms. Darr et al. (2014) performed IONM with the NIM monitoring system on 22 patients undergoing thyroidectomy. This study utilized a novel endotracheal tube and bipolar stimulation probe in addition to the traditional Prass (monopolar) probe. Endpoints for this study were response amplitudes, latencies, and thresholds. Stimulation saturation was also reported in this study and is a measure of the stimulation current that elicits a maximum amplitude response. Neural stimulation was performed with both probes at currents of 1–2 mA. Mean initial and final amplitudes were 272.2 6 202.9 mV and 263.8 6 184.7 mV, respectively. No significant difference was noted between the left (260.2 6 218.3 mV) and right (289.1 6 186.9 mV) SLN. SLN mean latency, threshold current, and stimulation saturation were 3.36 ms, 0.68 mA, and 1.45 mA, respectively. In our study, two different amplitude measurements were performed: peak-to-peak amplitude and onset-to-peak amplitude. The difference in these measurements is important from a neurophysiological standpoint. Peak-to-peak amplitude is typically reported in other studies as the mean amplitude as in ksi et al. (2012), Potenza et al. (2013), the Barczyn and Darr et al. (2014) studies. However, in neurophysiological studies, the peak-to-peak amplitude may be more appropriate for sensory nerve action potential measurement (Freeman, 2004). The sensory nerve conduction test in electromyographic studies of peripheral nerves consists of an orthrodomic stimulation of a distal sensory nerve and recording proximal compound nerve action potential. The study may also be performed in an antidromic fashion in which the proximal nerve is stimulated and the distal nerve compound nerve action potential is recorded. For these studies latency is equal to nerve conduction velocity. The amplitude measurements in sensory nerve conduction studies are representative of the number of large nerve fibers activated by nerve stimulation (Lee, 2004). The onset-to-peak amplitude,
also known as the baseline-to-peak amplitude may be more appropriate for measurement of compound motor action potential (Freeman, 2004). In electromyographic studies of peripheral nerves, the compound motor action potential estimates the number of nerve fibers activated by a nerve stimulation which represents the number of muscle fibers that contract during stimulation. Low amplitude responses represent impairment of nerve conduction due to axonal loss (Lee, 2004). To our knowledge, the utility of onset-to-peak amplitude has not been explored in animal or human studies in relation to recurrent or SLN monitoring. An additional consideration is that in asymmetric, non-periodic waves, the onset-to-peak amplitude is a less ambiguous measurement than the peak-to-peak amplitude, which is more appropriate for symmetric, periodic waves. We also measured waveform latency in two different manners: onset latency and peak latency. Onset latency is recorded from the initial deflection from the baseline and represents conduction of the signal along the fastest axons of the nerve. Peak latency is recorded from the electrical stimulus to the peak of the waveform response and represents conduction of the signal along the majority of the axons of the nerve (Freeman, 2004). The utility of measuring onset and peak latencies in neurophysiological monitoring has not been established for thyroidectomy. Electromyographic studies in peripheral nerves often measure distal and proximal latencies, with these measurements being used to calculate conduction time (Lee, 2004; Kane, 2012). Currently, the clinical significance of measuring additional latencies (distal and proximal vs. onset and peak) has not been established for laryngeal nerve monitoring. The peak-to-peak amplitude measured from our study (220.4 mV) was obtained with mean stimulus amplitude of 0.5 mA. This value was less than the ksi et al. mean amplitudes reported by the Barczyn (2012), Potenza et al. (2013), and Darr et al. (2014) studies which utilized higher stimulation currents (249.5 mV and 1 mA, 269.9 mV and 2 mA, 272.2 mV and 1–2 mA, respectively). In our study, no difference was noted between the left and right SLN, in contrast to the study by Potenza et al. (2013) in which a larger mean amplitude was noted on the left when compared to the right (358.8 mV vs. 204.9 mV, respectively). The significance of this difference in the aforementioned study is unknown. In our study, the trend was actually reversed with a lower mean peak-to-peak amplitude for the left compared to the right (207.8 mV vs. 230.0 mV, respectively), though this difference was not stastically significant (P 5 0.712).
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The present study has several advantages over previous studies utilizing NIM monitoring. Performing neural monitoring in a real-time fashion in conjunction with a clinical neurophysiologist allows identification of nerves to be performed with not only audio and visual verification of neural stimulation as with NIM monitoring, but also contemporaneous intraoperative interpretation of the EMG data to determine whether the waveform is of a normal character and quality of the presumed stimulated nerve. In addition, the clinical neurophysiologist records and reviews all the cases allowing for post hoc EMG analysis. The NIM monitoring system does allow for monitoring intraoperatively by the surgeon; however, this information is not saved by the machine at the completion of the case. Another advantage is that this study recognizes that additional waveform parameters may need to be measured to ensure that the data accurately represent what is intended to be measured from a neurophysiological and electrical conduction standpoint. Amplitude and threshold data are recorded in two different fashions for this data set, which has not been previously been described. However, the clinical utility of these measurements, from either an intraoperative or prospective standpoint, is largely unknown. Several limitations are also present in this study. Intraoperative SLN identification rate was lower than that reported in previous studies. This may have been secondary to the high proportion of the thyroidectomies being performed for malignancy, as thyroidectomies performed in conjunction with central or lateral neck dissections were not excluded from initial analysis, and the SLN may not have been actively sought for identification in all of these studies. A review of these operative reports reveals that a large portion of the nerves at risk which were positively identified intraoperatively were excluded from final analysis. This was predominantly due to the retrospective nature of the study. Review of the waveforms entailed reviewing time logs and notations in the collected EMG data. In cases where it was unclear when the SLN was stimulated in relation to the procedure, the data point was excluded as an accurate measurement could not be obtained. In addition, if the data log and notations did not correlate with the operative report on whether the right or left nerve was identified or stimulated, the data were excluded to prevent ambiguity. Diagnostic and intraoperative factors were also collected with the plan to correlate these findings with EMG data. However, based on the final number of nerves analyzed these additional analyses could not be performed. Future directions include a similar study performed in a prospective fashion with meticulous logging and data recording intraoperatively. Accurate logging is improved when the surgeon and neurophysiology technologist communicate more effectively intraoperatively as to when and which nerve is being stimulated as the data are logged by the technician into the EMG record at the time of the surgery, and the surgeon may not review the EMG data until weeks later. Threshold data were not routinely collected prior to this study and would be an important adjunct to further establishing normative data for SLN monitoring
as well as being used as a potential pre- and postresection prognosticator of nerve function at the end of the procedure.
CONCLUSION In conclusion, this is the first study to present normative data for monitoring of the external branch of the SLN during thyroidectomy performed with laryngeal surface electrodes in conjunction with a clinical neurophysiologist. Normative data were established by performing amplitude and latency measurements using different electrophysiological measurement parameters. These data add to the existing normative data presented in other studies utilizing NIM monitoring performed by the surgeon alone as well as setting the stage for a comprehensive prospective study investigation amplitudes, latencies, thresholds and how they relate to clinical outcomes.
ACKNOWLEDGMENT The work does not represent the views of the US Government or the Department of Veterans Affairs. IRB approval was under the IRB for intraoperative neurophysiology monitoring from the Center for Clinical Neurophysiology (IRB PRO08120394 Analyses of Neurosurgery Operative Procedures). The authors acknowledge Trenita Finney for the anatomical figure for this manuscript.
REFERENCES ski M, Konurek A, Stopa M, Honowska A, Nowak W. 2012. Barczyn Randomized controlled trial of visualization versus neuromonitoring of the external branch of the superior laryngeal nerve during thyroidectomy. World J Surg 36:1340–1347. ski M, Randolph GW, Cernea CR, Dralle H, Dionigi G, Alesina Barczyn PF, Mihai R, Finck C, Lombardi D, Hartl DM, Miyauchi A, Serpell J, Snyder S, Volpi E, Woodson G, Kraimps JL, Hisham AN; International Neural Monitoring Study Group. 2013. External branch of the superior laryngeal nerve monitoring during thyroid and parathyroid surgery: International Neural Monitoring Study Group standards guideline statement. Laryngoscope 123 Suppl 4:S1–S14. Bevan K, Griffiths MV, Morgan MH. 1989. Cricothyroid muscle paralysis: Its recognition and diagnosis. J Laryngol Otol 103:191–195. Cernea CR, Ferraz AR, Furlani J, Monteiro S, Nishio S, Hojaij FC, nior A, Marques LA, Pontes PA, Bevilacqua RG. 1992. Dutra Ju Identification of the external branch of the superior laryngeal nerve during thyroidectomy. Am J Surg 164:634–639. Darr EA, Tufano RP, Ozdemir S, Kamani D, Hurwitz S, Randolph G. 2004. Superior laryngeal nerve quantitative intraoperative monitoring is possible in all thyroid surgeries. Laryngoscope 124: 1035–1041. Dionigi G, Boni L, Rovera F, Bacuzzi A, Dionigi R. 2009. Neuromonitoring and video-assisted thyroidectomy: A prospective, randomized case-control evaluation. Surg Endosc 23:996–1003. Freeman TL, Johnson E, Freeman ED, Brown DP. 2004. Nerve conduction studies (NCS) In: Cuccurullo S, editor. Physical Medicine and Rehabilitation Board Review. New York: Demos Medical Publishing. URL: http://www.ncbi.nlm.nih.gov/books/NBK27199, accessed June 2014. Kane NM, Oware A. 2012. Nerve conduction and electromyography studies. J Neurol 259:1502–1508.
Superior Laryngeal Nerve Monitoring Kierner AC, Aigner M, Burian M. 1998. The external branch of the superior laryngeal nerve: Its topographical anatomy as related to surgery of the neck. Arch Otolaryngol Head Neck Surg 124:301–303. Lee DH, Claussen GC, Oh S. 2004. Clinical nerve conduction and needle electromyography studies. J Am Acad Orthop Surg 12:276–287. Lennquist S, Cahlin C, Smeds S. 1987. The superior laryngeal nerve in thyroid surgery. Surgery 102:999–1008. Lifante JC, McGill J, Murry T, Aviv JE, Inabnet WB 3rd. 2009. A prospective, randomized trial of nerve monitoring of the external branch of the superior laryngeal nerve during thyroidectomy under local/ regional anesthesia and IV sedation. Surgery 146:1167–1173. Potenza AS, Phelan EA, Cernea CR, Slough CM, Kamani DV, Darr A, Zurakowski D, Randolph GW. 2013. Normative intra-operative electrophysiologic waveform analysis of superior laryngeal nerve external branch and recurrent laryngeal nerve in patients undergoing thyroid surgery. World J Surg 37:2336–2342.
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Randolph GW, Dralle H, International Intraoperative Monitoring Study Group, Abdullah H, Barczynski M, Bellantone R, Brauckhoff M, Carnaille B, Cherenko S, Chiang FY, Dionigi G, Finck C, Hartl D, Kamani D, Lorenz K, Miccolli P, Mihai R, Miyauchi A, Orloff L, Perrier N, Poveda MD, Romanchishen A, Serpell J, Sitges-Serra A, Sloan T, Van Slycke S, Snyder S, Takami H, Volpi E, Woodson G. 2011. Electrophysiologic recurrent laryngeal nerve monitoring during thyroid and parathyroid surgery: International standards guideline statement. Laryngoscope 121 Suppl 1:S1–S16. Selvan B, Babu S, Paul MJ, Abraham D, Samuel P, Nair A. 2009. Mapping the compound muscle action potentials of cricothyroid muscle using electromyography in thyroid operations: A novel method to clinically type the external branch of the superior laryngeal nerve. Ann Surg 250:293–300. Sulica L. 2004. The superior laryngeal nerve: Function and dysfunction. Otolaryngol Clin North Am 37:183–201.
ORIGINAL COMMUNICATION
Superior Laryngeal Nerve Monitoring Using Laryngeal Surface Electrodes and Intraoperative Neurophysiological Monitoring During Thyroidectomy BENJAMIN L. HODNETT,1 NICOLE C. SCHMITT,1 DANIEL R. CLAYBURGH,2 ALEX BURKOWSKY,3 JEFFREY BALZER,4 PARTHASARATHY D. THIRUMALA,5 AND UMAMAHESWAR DUVVURI6* 1
Department of Otolaryngology, University of Pittsburgh Medical Center, Eye and Ear Institute, Pittsburgh, Pennsylvania 2 Department of Otolaryngology-Head and Neck Surgery, Oregon Health and Science University, Portland, Oregon 3 Clinical Neurophysiology Tech, Procirca—Center for Clinical Neurophysiology (CCN), UPMC Presbyterian Hospital, Pittsburgh, Pennsylvania 4 Neuroscience & Acute and Tertiary Care Nursing, Center for Clinical Neurophysiology (CCN), UPMC Presbyterian Hospital, Pittsburgh, Pennsylvania 5 Center for Clinical Neurophysiology (CCN), UPMC Presbyterian Hospital, Suite B-400, Pittsburgh, Pennsylvania 6 University of Pittsburgh Medical Center, VA Pittsburgh Health System, Eye and Ear Institute, Pittsburgh, Pennsylvania
The objective of this study is to establish normative waveform data for the external branch of the superior laryngeal nerve (SLN) utilizing laryngeal surface electrodes and intraoperative neurophysiological monitoring (IONM) in conjunction with a clinical neurophysiologist. A retrospective chart review of 91 consecutive at-risk SLN were identified in 51 patients in whom IONM using laryngeal surface electrodes was performed by a clinical neurophysiologist using Dragonfly (Neurovision Medical Products, Ventura, CA) recording electrodes and a Protektor (Natus Medical Inc., San Carlos, CA)16 channel- intraoperative nerve monitoring system. Inclusion criteria were met for 30 SLN. Data collected included preoperative diagnosis, surgical procedure, rates of nerve identification and stimulation, and waveform characteristics. Waveform analysis for 30 SLN yielded a peak latency of 4.0 6 0.2 ms, onset latency 2.3 6 0.1 ms, peak-to-peak amplitude of 220.4 6 31.1 mV, onset-to-peak amplitude of 186.0 6 25.0 mV, and stimulation current threshold of 0.55 6 0.03 mA (data5 mean 6 SEM). Two patients had abnormal SLN function documented clinically on postoperative laryngoscopic examination. Laryngeal surface electrodes were successfully utilized to identify and monitor SLN function intraoperatively. Abbreviations used: EMG, electromyography; IONM, intraoperative neurophysiological monitoring; SLN, superior laryngeal nerve. Contract Grant sponsor: Department of Veterans Affairs, BLSR&D, and the PNC Foundation (UD). *Correspondence to: University of Pittsburgh Medical Center, VA Pittsburgh Health System, Eye and Ear Institute, 200 Lothrop Street, Suite 500, Pittsburgh, PA 15213. E-mail: [email protected]
C V
2014 Wiley Periodicals, Inc.
Oral Presentation at Combined Otolaryngology Spring Meetings, May 14-18, 2014, Las Vegas, Nevada. Received 16 August 2014; Revised 18 October 2014; Accepted 19 October 2014 Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/ca.22487
2
Hodnett et al.
IONM using laryngeal surface electrodes enables analysis of waveform morphology and latency in addition to threshold and amplitude data obtained with the traditional NIM system, potentially improving the performance of nerve monitoring during thyroid surgery. Clin. Anat. 00:000–000, 2014. VC 2014 Wiley Periodicals, Inc.
Key words: external branch of superior laryngeal nerve; nerve monitoring and stimulation; thyroid surgery
INTRODUCTION The external branch of the superior laryngeal nerve (SLN) is responsible for motor innervation of the cricothyroid muscle. This muscle acts to tilt the thyroid cartilage and tense or elongate the vocal folds. Injury to this nerve may affect the ability to produce highfrequency sounds as well as impact the overall quality of voice and vocal projection (Sulica, 2004). The SLN is at risk during dissection of the superior pole during thyroidectomy. Previous studies have reviewed the surgical anatomy of the external branch of the SLN (Fig. 1) as well as its rate of identification intraoperatively (Lennquist, 1987; Kierner, 1998; Cernea, 1992; ski, 2012; Barczyn ski, 2013). Various techniBarczyn ques for intraoperative SLN monitoring exist. Normative data have been established for the SLN using intraoperative nerve monitoring with NIM tubes (a form of endotracheal tube-based surface electrodes) ski, 2012; Potenza, 2013; Darr, 2014). How(Barczyn ever, the use of continuous intraoperative neurophysiological monitoring (IONM) in conjunction with a clinical neurophysiologist during thyroidectomy has not been routinely utilized. The objective of this study was to further enhance standardization of intraoperative nerve monitoring by establishing normative waveform data for the SLN utilizing laryngeal surface electrodes and IONM in conjunction with a clinical neurophysiologist.
MATERIALS AND METHODS A retrospective review of patients undergoing thyroidectomy with intraoperative electromyography (EMG) monitoring from January 2012 to July 2013 was conducted. The patient list was initially queried for all procedures involving intraoperative nerve monitoring using Dragonfly laryngeal surface electrodes and the Protektor (Natus Medical, San Carlos, CA) IONM system from January 2012 to July 2013. This initial query included patients undergoing thyroidectomy, parathyroidectomy, and central/lateral neck dissection for thyroid carcinoma. This was later revised to include only thyroidectomy with or without associated procedures such as parathyroidectomy or neck dissection as SLN was not routinely performed for parathyroidectomy or neck dissection alone. All operations were performed by one surgeon who routinely identifies the external branch of the SLN. Operative reports were reviewed for each patient. Data collected included preoperative diagnosis, surgical procedure,
and whether the SLN was identified and/or stimulated during the case. Laterality of each nerve was recorded. Diagnostic and intraoperative factors were collected from preoperative and operative reports including information regarding surgery for large goiter, significant intraoperative retraction, Graves’ disease, Hashimoto’s thyroiditis, prior radioactive iodine ablation, prior radiation therapy, intraoperative inflammation/fibrosis, or extensive tumor. The final pathological diagnosis was also recorded for each case. Preand postoperative clinical notes were reviewed for each patient. Inclusion criteria included: (1) documented SLN identification in the operative report and (2) documented SLN identification in the neurophysiological case record. Excluded nerves were those in which incomplete records were identified or the laterality of the SLN nerve was not evident in the neurophysiological case record. All thyroidectomy and parathyroidectomy cases at our institution are performed utilizing Dragonfly (Neurovision Medical Products, Ventura, CA) laryngeal surface electrodes (Fig. 2) and continuous neurophysiological monitoring in conjunction with a clinical neurophysiologist. During the surgery, the monitoring is performed with a neurophysiology technologist in the operating room and a board-certified clinical neurophysiologist viewing the data remotely in real-time. The intraoperative EMG data is collected by the Center for Clinical Neurophysiology and also reviewed at the end of each case. For each of the patients in this study, EMG data were retrospectively reviewed. SLN waveforms were identified from the EMG data and used to calculate latencies and amplitudes. Onset latency and peak latency were measured in milliseconds (ms). Onset-to-peak amplitude and peak-to-peak amplitude were measured in microvolts (mV). Intensity of electrical stimulation was also recorded in milliamps (mA). Onset latency was defined as the time from the initial deflection at baseline to the waveform response. Peak latency was defined as the time from the electrical stimulus to the waveform response. Onset-to-peak amplitude was defined as the amplitude from the baseline to the peak of the waveform response. Peak-to-peak amplitude was defined as the amplitude from the positive deflection to the negative deflection. Figure 3 illustrates the waveform parameters. Final analysis of waveform parameters included only SLN waveforms that were positively identified from the collected EMG data. Data are reported as mean 6 SEM. Statistical analysis was performed using Student t-test or MannWhitney Rank Sum test where appropriate.
Superior Laryngeal Nerve Monitoring
Fig. 1. Schematic drawing of the SLN. Note the innervation of the cricothyroid muscle (CT) by the external branch of the superior laryngeal nerve (EBSLN). IBSLN, internal branch of superior laryngeal nerve; RLN, recurrent laryngeal nerve.
RESULTS Table 1 lists demographic data. A total of 54 operations on 51 patients were identified from the database during the time period. The mean age at time of surgery was 44 6 2 years, with a range from 8 to 85 years of age. Total thyroidectomy was the most common surgery accounting for 36 of 54 operations (67%). Of the remaining thyroid lobectomies, 3 of 18 were completion thyroid lobectomies (17%). The final pathological diagnosis was noted for the patients with the majority performed for thyroid malignancy (71%). Patient risk factors were also recorded from the clinic records with a large goiter or mass noted in 20% of the patients. Table 2 reviews operative findings. Based on the total number of operations and sides of the operations, 91 SLN were at risk during the operations. The positive identification rate per the operative reports was 67%. Intraoperative findings were also noted with extensive tumor or dissection noted in 12% and inflammation or fibrosis in 8% of cases. Postoperative flexible laryngoscopy noted two patients with decreased elongation of the true vocal folds suggesting possible SLN injury. Unfortunately, EMG data were not sufficient on these two SLN to perform accurate waveform analysis. Review of intraoperative EMG data allowed for analysis of 30 SLNs. Latency and amplitude data are presented in Table 3 for all SLN as well as right (n 5 18) and left (n 5 12) groups. There were no significant dif-
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Fig. 2. Videolaryngoscope monitor visualization of placement utilizing Dragonfly laryngeal surface electrodes. The left electrode is visible adjacent to the left vocal fold (LVF). RVF, right vocal fold. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary. com.]
ferences between the groups for latency, amplitude, or stimulation current parameters.
DISCUSSION IONM is commonly utilized during thyroidectomy to decrease the incidence of recurrent laryngeal nerve palsy. The most commonly utilized IONM systems rely on laryngeal surface electrodes (Randolph, 2011). Various monitoring systems include audio and/or visual identification features such as the NIM (Medtronic Inc.) system. At our university, recurrent laryngeal nerve monitoring is also performed using laryngeal surface electrodes. However, the IONM is performed in conjunction with a board-certified clinical neurophysiologist performing real-time monitoring. In addition, this system records waveform morphology and additional neurophysiologic parameters not recorded by other monitoring systems. The SLN may also be monitored intraoperatively. Injury to this nerve during thyroidectomy may result in impaired elongation of the true vocal fold, resulting in decreased pitch and vocal register, as well as increased vocal fatigue (Bevan, 1989; Cernea, 1992; ski, 2013). Direct EMG recordings of the Barczyn external branch of the SLN have been performed previously using electrodes placed in the cricothyroid muscle intraoperatively (Selvan, 2009). IONM using the NIM system and laryngeal surface electrodes has also been utilized in several studies for identification of the SLN (Dionigi, 2009; Lifante, 2009). Normative data have been collected in three studies using the ski, 2012; Potenza, 2013; Darr, NIM system (Barczyn 2014). To our knowledge, no studies have reported normative data for the SLN when IONM is performed
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Fig. 3. Waveform parameters and measurement. Panel A represents measurement of peak latency. Panel B represents onset latency. Panel C represents onset-topeak amplitude. Panel D represents peak-to-peak amplitude.
in conjunction with a clinical neurophysiologist. Our study sought to establish detailed normative data for SLN monitoring using laryngeal surface electrodes TABLE 1. Demographic Data Variable Number of patients Male Female Age at surgery Total operations Total thyroidectomy Thyroid lobectomy Final diagnosis Malignant Benign Risk Factors Large goiter/mass Grave’s disease Hashimoto’s thyroiditis Prior radioactive iodine ablation Prior neck irradiation
Data (n) 51 11 40 44 6 2 years (range 8–85 years) 54 36 18 (three completion)
when the monitoring is performed in conjunction with a clinical neurophysiologist. ksi et al. (2012) randomized 210 female Barczyn patients to two groups, one group having visual identification alone of the SLN and the second having IONM performed with the NIM monitoring system. The primary endpoint of their study was identification rate of the SLN with secondary endpoints noting anatomic variability and postoperative voice performance. Stimulation was performed with 1 mA of current, and the mean amplitude was noted to be 249.5 6 144.3 mV for 130 SLN positively identified. Potenza et al. (2013) performed IONM with the NIM monitoring system on
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TABLE 2. Operative Findings
10 1 3 1
Superior laryngeal nerves at risk Positively Identified Unknown or Not Identified Intraoperative inflammation or fibrosis Extensive tumor or dissection Significant retraction
1
Variable
Data (n) 91 61 30 4 6 1
Superior Laryngeal Nerve Monitoring
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TABLE 3. Superior Laryngeal Nerve Waveform Data Nerve All SLN (n 5 30) Right SLN (n 5 18) Left SLN (n 5 12)
Peak latency (ms)
Onset latency (ms)
Peak-to-peak amplitude (mV)
Onset-to-peak amplitude (mV)
Stimulation current (mA)
4.0 6 0.2 4.2 6 0.2 3.7 6 0.2 P 5 0.310
2.3 6 0.1 2.4 6 0.1 2.3 6 0.2 P 5 0.287
220.4 6 31.1 230.0 6 46.8 207.8 6 30.2 P 5 0.712
186.0 6 25.0 185.1 6 36.4 172.9 6 29.9 P 5 0.626
0.55 6 0.03 0.53 6 0.03 0.56 6 0.04 P 5 0.654
Data expressed as mean 6 SEM.
72 consecutive patients undergoing thyroidectomy. Endpoints for this study were response amplitudes, latencies, and thresholds. Stimulation was performed with 2 mA of current for initial nerve mapping and 1 mA for subsequent stimulations, and the mean amplitude 5 269.9 6 178.6 mV for 55 SLN positively identified. A significant difference was noted between the left (358.8 mV, n 5 24) and right (204.9 mV, n 5 31) SLN. The mean threshold was reported for five SLN and noted to be 0.5 6 0.1 mA. Latencies were also measured. The latency for the four left SLN was 5.75 ms, whereas the latency for the two right SLN was 3.5 ms. Darr et al. (2014) performed IONM with the NIM monitoring system on 22 patients undergoing thyroidectomy. This study utilized a novel endotracheal tube and bipolar stimulation probe in addition to the traditional Prass (monopolar) probe. Endpoints for this study were response amplitudes, latencies, and thresholds. Stimulation saturation was also reported in this study and is a measure of the stimulation current that elicits a maximum amplitude response. Neural stimulation was performed with both probes at currents of 1–2 mA. Mean initial and final amplitudes were 272.2 6 202.9 mV and 263.8 6 184.7 mV, respectively. No significant difference was noted between the left (260.2 6 218.3 mV) and right (289.1 6 186.9 mV) SLN. SLN mean latency, threshold current, and stimulation saturation were 3.36 ms, 0.68 mA, and 1.45 mA, respectively. In our study, two different amplitude measurements were performed: peak-to-peak amplitude and onset-to-peak amplitude. The difference in these measurements is important from a neurophysiological standpoint. Peak-to-peak amplitude is typically reported in other studies as the mean amplitude as in ksi et al. (2012), Potenza et al. (2013), the Barczyn and Darr et al. (2014) studies. However, in neurophysiological studies, the peak-to-peak amplitude may be more appropriate for sensory nerve action potential measurement (Freeman, 2004). The sensory nerve conduction test in electromyographic studies of peripheral nerves consists of an orthrodomic stimulation of a distal sensory nerve and recording proximal compound nerve action potential. The study may also be performed in an antidromic fashion in which the proximal nerve is stimulated and the distal nerve compound nerve action potential is recorded. For these studies latency is equal to nerve conduction velocity. The amplitude measurements in sensory nerve conduction studies are representative of the number of large nerve fibers activated by nerve stimulation (Lee, 2004). The onset-to-peak amplitude,
also known as the baseline-to-peak amplitude may be more appropriate for measurement of compound motor action potential (Freeman, 2004). In electromyographic studies of peripheral nerves, the compound motor action potential estimates the number of nerve fibers activated by a nerve stimulation which represents the number of muscle fibers that contract during stimulation. Low amplitude responses represent impairment of nerve conduction due to axonal loss (Lee, 2004). To our knowledge, the utility of onset-to-peak amplitude has not been explored in animal or human studies in relation to recurrent or SLN monitoring. An additional consideration is that in asymmetric, non-periodic waves, the onset-to-peak amplitude is a less ambiguous measurement than the peak-to-peak amplitude, which is more appropriate for symmetric, periodic waves. We also measured waveform latency in two different manners: onset latency and peak latency. Onset latency is recorded from the initial deflection from the baseline and represents conduction of the signal along the fastest axons of the nerve. Peak latency is recorded from the electrical stimulus to the peak of the waveform response and represents conduction of the signal along the majority of the axons of the nerve (Freeman, 2004). The utility of measuring onset and peak latencies in neurophysiological monitoring has not been established for thyroidectomy. Electromyographic studies in peripheral nerves often measure distal and proximal latencies, with these measurements being used to calculate conduction time (Lee, 2004; Kane, 2012). Currently, the clinical significance of measuring additional latencies (distal and proximal vs. onset and peak) has not been established for laryngeal nerve monitoring. The peak-to-peak amplitude measured from our study (220.4 mV) was obtained with mean stimulus amplitude of 0.5 mA. This value was less than the ksi et al. mean amplitudes reported by the Barczyn (2012), Potenza et al. (2013), and Darr et al. (2014) studies which utilized higher stimulation currents (249.5 mV and 1 mA, 269.9 mV and 2 mA, 272.2 mV and 1–2 mA, respectively). In our study, no difference was noted between the left and right SLN, in contrast to the study by Potenza et al. (2013) in which a larger mean amplitude was noted on the left when compared to the right (358.8 mV vs. 204.9 mV, respectively). The significance of this difference in the aforementioned study is unknown. In our study, the trend was actually reversed with a lower mean peak-to-peak amplitude for the left compared to the right (207.8 mV vs. 230.0 mV, respectively), though this difference was not stastically significant (P 5 0.712).
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The present study has several advantages over previous studies utilizing NIM monitoring. Performing neural monitoring in a real-time fashion in conjunction with a clinical neurophysiologist allows identification of nerves to be performed with not only audio and visual verification of neural stimulation as with NIM monitoring, but also contemporaneous intraoperative interpretation of the EMG data to determine whether the waveform is of a normal character and quality of the presumed stimulated nerve. In addition, the clinical neurophysiologist records and reviews all the cases allowing for post hoc EMG analysis. The NIM monitoring system does allow for monitoring intraoperatively by the surgeon; however, this information is not saved by the machine at the completion of the case. Another advantage is that this study recognizes that additional waveform parameters may need to be measured to ensure that the data accurately represent what is intended to be measured from a neurophysiological and electrical conduction standpoint. Amplitude and threshold data are recorded in two different fashions for this data set, which has not been previously been described. However, the clinical utility of these measurements, from either an intraoperative or prospective standpoint, is largely unknown. Several limitations are also present in this study. Intraoperative SLN identification rate was lower than that reported in previous studies. This may have been secondary to the high proportion of the thyroidectomies being performed for malignancy, as thyroidectomies performed in conjunction with central or lateral neck dissections were not excluded from initial analysis, and the SLN may not have been actively sought for identification in all of these studies. A review of these operative reports reveals that a large portion of the nerves at risk which were positively identified intraoperatively were excluded from final analysis. This was predominantly due to the retrospective nature of the study. Review of the waveforms entailed reviewing time logs and notations in the collected EMG data. In cases where it was unclear when the SLN was stimulated in relation to the procedure, the data point was excluded as an accurate measurement could not be obtained. In addition, if the data log and notations did not correlate with the operative report on whether the right or left nerve was identified or stimulated, the data were excluded to prevent ambiguity. Diagnostic and intraoperative factors were also collected with the plan to correlate these findings with EMG data. However, based on the final number of nerves analyzed these additional analyses could not be performed. Future directions include a similar study performed in a prospective fashion with meticulous logging and data recording intraoperatively. Accurate logging is improved when the surgeon and neurophysiology technologist communicate more effectively intraoperatively as to when and which nerve is being stimulated as the data are logged by the technician into the EMG record at the time of the surgery, and the surgeon may not review the EMG data until weeks later. Threshold data were not routinely collected prior to this study and would be an important adjunct to further establishing normative data for SLN monitoring
as well as being used as a potential pre- and postresection prognosticator of nerve function at the end of the procedure.
CONCLUSION In conclusion, this is the first study to present normative data for monitoring of the external branch of the SLN during thyroidectomy performed with laryngeal surface electrodes in conjunction with a clinical neurophysiologist. Normative data were established by performing amplitude and latency measurements using different electrophysiological measurement parameters. These data add to the existing normative data presented in other studies utilizing NIM monitoring performed by the surgeon alone as well as setting the stage for a comprehensive prospective study investigation amplitudes, latencies, thresholds and how they relate to clinical outcomes.
ACKNOWLEDGMENT The work does not represent the views of the US Government or the Department of Veterans Affairs. IRB approval was under the IRB for intraoperative neurophysiology monitoring from the Center for Clinical Neurophysiology (IRB PRO08120394 Analyses of Neurosurgery Operative Procedures). The authors acknowledge Trenita Finney for the anatomical figure for this manuscript.
REFERENCES ski M, Konurek A, Stopa M, Honowska A, Nowak W. 2012. Barczyn Randomized controlled trial of visualization versus neuromonitoring of the external branch of the superior laryngeal nerve during thyroidectomy. World J Surg 36:1340–1347. ski M, Randolph GW, Cernea CR, Dralle H, Dionigi G, Alesina Barczyn PF, Mihai R, Finck C, Lombardi D, Hartl DM, Miyauchi A, Serpell J, Snyder S, Volpi E, Woodson G, Kraimps JL, Hisham AN; International Neural Monitoring Study Group. 2013. External branch of the superior laryngeal nerve monitoring during thyroid and parathyroid surgery: International Neural Monitoring Study Group standards guideline statement. Laryngoscope 123 Suppl 4:S1–S14. Bevan K, Griffiths MV, Morgan MH. 1989. Cricothyroid muscle paralysis: Its recognition and diagnosis. J Laryngol Otol 103:191–195. Cernea CR, Ferraz AR, Furlani J, Monteiro S, Nishio S, Hojaij FC, nior A, Marques LA, Pontes PA, Bevilacqua RG. 1992. Dutra Ju Identification of the external branch of the superior laryngeal nerve during thyroidectomy. Am J Surg 164:634–639. Darr EA, Tufano RP, Ozdemir S, Kamani D, Hurwitz S, Randolph G. 2004. Superior laryngeal nerve quantitative intraoperative monitoring is possible in all thyroid surgeries. Laryngoscope 124: 1035–1041. Dionigi G, Boni L, Rovera F, Bacuzzi A, Dionigi R. 2009. Neuromonitoring and video-assisted thyroidectomy: A prospective, randomized case-control evaluation. Surg Endosc 23:996–1003. Freeman TL, Johnson E, Freeman ED, Brown DP. 2004. Nerve conduction studies (NCS) In: Cuccurullo S, editor. Physical Medicine and Rehabilitation Board Review. New York: Demos Medical Publishing. URL: http://www.ncbi.nlm.nih.gov/books/NBK27199, accessed June 2014. Kane NM, Oware A. 2012. Nerve conduction and electromyography studies. J Neurol 259:1502–1508.
Superior Laryngeal Nerve Monitoring Kierner AC, Aigner M, Burian M. 1998. The external branch of the superior laryngeal nerve: Its topographical anatomy as related to surgery of the neck. Arch Otolaryngol Head Neck Surg 124:301–303. Lee DH, Claussen GC, Oh S. 2004. Clinical nerve conduction and needle electromyography studies. J Am Acad Orthop Surg 12:276–287. Lennquist S, Cahlin C, Smeds S. 1987. The superior laryngeal nerve in thyroid surgery. Surgery 102:999–1008. Lifante JC, McGill J, Murry T, Aviv JE, Inabnet WB 3rd. 2009. A prospective, randomized trial of nerve monitoring of the external branch of the superior laryngeal nerve during thyroidectomy under local/ regional anesthesia and IV sedation. Surgery 146:1167–1173. Potenza AS, Phelan EA, Cernea CR, Slough CM, Kamani DV, Darr A, Zurakowski D, Randolph GW. 2013. Normative intra-operative electrophysiologic waveform analysis of superior laryngeal nerve external branch and recurrent laryngeal nerve in patients undergoing thyroid surgery. World J Surg 37:2336–2342.
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Randolph GW, Dralle H, International Intraoperative Monitoring Study Group, Abdullah H, Barczynski M, Bellantone R, Brauckhoff M, Carnaille B, Cherenko S, Chiang FY, Dionigi G, Finck C, Hartl D, Kamani D, Lorenz K, Miccolli P, Mihai R, Miyauchi A, Orloff L, Perrier N, Poveda MD, Romanchishen A, Serpell J, Sitges-Serra A, Sloan T, Van Slycke S, Snyder S, Takami H, Volpi E, Woodson G. 2011. Electrophysiologic recurrent laryngeal nerve monitoring during thyroid and parathyroid surgery: International standards guideline statement. Laryngoscope 121 Suppl 1:S1–S16. Selvan B, Babu S, Paul MJ, Abraham D, Samuel P, Nair A. 2009. Mapping the compound muscle action potentials of cricothyroid muscle using electromyography in thyroid operations: A novel method to clinically type the external branch of the superior laryngeal nerve. Ann Surg 250:293–300. Sulica L. 2004. The superior laryngeal nerve: Function and dysfunction. Otolaryngol Clin North Am 37:183–201.
