The trans-cartilage recording system has yielded many novel surgical applications of IONM technology in recent years. Since vocal fold muscles are innervated only by the RLN and are attached to the anterior inner surface of the thyroid cartilage (TC), surface recording electrodes placed on the outer surface of TC should enable access to EMG signals evoked in vocal fold muscles during IONM ( Figure 1 and Figure 2A ) ( 14). To test this hypothesis, Wu et al. (14) performed an animal study using 12 male piglets under standard IONM settings. Adhesive pre-gelled EMG electrodes were attached to the outer surface of the TC for transcartilage AL recording. Evoked EMG signals detected by TC electrodes were compared with those detected by ET electrodes. Typical evoked laryngeal EMG waveforms for the vagus nerve (VN) and RLN were obtained under 1 mA stimulation. Experimental displacements and surgical manipulations of the trachea confirmed the stability and consistency of transcartilage method. Additionally, RLN traction experiments confirmed that transcartilage method accurately reflected neurophysiologic events (14). Zhao et al. (18) investigated the feasibility, EMG stability, and optimal location and size of adhesive surface arrays attached to the TC for use in IONM. Their experiments confirmed that, during surgical manipulations, EMG profiles obtained by transcartilage recording method were more stable than those obtained by ET recording method.

Similarly, Zhao et al. (16) performed an experimental porcine model to test the transcartilage recording by placing needle electrodes on the TC in a porcine model. They confirmed that a perichondral needle electrode can be safely inserted into the avascular area of the TC. Comparing to ET electrodes, TC electrodes registered earlier changes in EMG amplitudes when the nerve is in traction injury. Additionally, TC electrodes obtained higher and more stable EMG amplitudes. Their findings indicate that transcartilage recording electrodes have superior function, easier placement, and lower cost compared to ET electrodes (16). Researchers are increasingly discussing clinical applications of transcartilage AL recording in IONM, and several methods of affixing electrodes to the TC have been reported. For example, one proposed method is to perform transcartilage AL recording using a commercially available 12mm subdermal single needle electrode. Chiang et al. (19) analyzed 205 at-risk RLNs in 110 patients in a clinical comparison of EMG signals recorded by ET and TC surface electrodes in the standardized monitored thyroidectomy. A pair of one-channel electrodes were inserted into the perichondrium of the TC lamina on bilateral side. According to their comparisons, transcartilage AL recording and ET recording had comparable efficacy and reliability during monitored thyroidectomy. In contrast with the complicated and time-consuming procedures for adjusting ET electrodes and verifying their proper position, the setup procedure for transcartilage AL electrodes can be performed quicker (approximately 2 minutes) and easier. Additionally, compared to ET recording, transcartilage AL recording obtains higher and more stable EMG signals during IONM as well as fewer false EMG results. Chiang et al. (22) developed a technique for using two-channel paired subdermal needle electrodes for transcartilage AL recording. Based on their experience in performing the technique in 100 consecutive monitored total thyroidectomies, the authors concluded that, in clinical practice, the technique can be performed without ET electrodes and that it provides high sensitivity and stability of EMG signals. Therefore, it improves the safety and reliability of thyroid surgery and is particularly suitable for use in C-IONM. Another recent study by Jung et al. (23) reported the efficacy of transcartilage recording during standardized monitored thyroidectomy. A pair of 22-mm twisted needle electrodes was attached to the TC in 38 patients with 54 at-risk RLNs. The positive predictive values of loss of signal were 40% and 100% for ET and TC electrodes, respectively. In 2021, Lee et al. (24) reported the advantage of minimizing exposure of one side of the TC by applying a single ipsilateral transcartilage needle electrode during unilateral monitored hemithyroidectomy. Additionally, Türk et al. (27) reported the first case-control study to compare ET and TC electrodes and concluded that TC electrodes are an inexpensive and effective alternative to ET electrodes.

In a prospective clinical cohort study of 25 patients, Van Slycke et al. (21) affixed electrodes directly to the TC perichondrium with two stitches. Compared to ET electrodes, the TC electrodes obtained higher EMG amplitudes induced by stimulation of the VN, RLN and external branch of the superior laryngeal nerve (EBSLN). Liddy et al. (20) proposed and evaluated the use of adhesive dragonfly bipolar surface electrodes (Neurovision Medical, Inomed, Medtronic & Stryker) in 15 consecutive patients undergoing monitored thyroid and parathyroid surgery. Their approach entailed cutting the adhesive electrode in half to create two recording surfaces and then positioning the electrodes over the TC on either side of the midline. The electrodes were then secured by suturing them to the perichondrium. Their experiments again demonstrated that, compared to ET electrodes, adhesive transcartilage AL electrodes provide EMG signals with comparable stability and amplitude and have comparable sensitivity in recording evoked responses during IONM. Additionally, since adhesive transcartilage AL electrodes are accessible in the operative field, they are easily monitored and controlled by the surgeon, and they are unaffected by potential ET displacement during surgery (20). Finally, since transcartilage AL electrodes enable robust EBSLN monitoring, they reduce the risk of high-pitched voice function loss in thyroid and parathyroid surgery (30).

In pediatric patients, anatomical characteristics, e.g., smaller RLN diameter compared to adults, can make IONM challenging. One consensus statement suggested that IONM is beneficial in pediatric patients with a bulky thyroid and lymph node disease (31). Since the larynx and trachea are relatively small in pediatric patients, the limited selection of commercially available ET electrode sizes combined with the increased difficulty of confirming ET electrode position in pediatric patients may result in unstable and inconsistent contact between the ET electrode and the vocal fold (28, 32). Huang et al. (28) compared electrode types in 33 pediatric patients who had received neuromonitored thyroid surgery and concluded that, compared to EMG signals obtained by ET electrodes, signals obtained by TC electrodes had superior amplitude, stability, and quality, which greatly facilitates the meticulous RLN dissection required in pediatric thyroidectomies, especially in pediatric patients with thyroid cancer.

The feasibility of using TC perichondral needle electrodes as recording electrodes and their good signal stability have been well established in many animal and clinical studies. However, these electrodes require a standard neck incision for open exposure of the TC. That is, TC perichondral needle electrodes are inapplicable when invasiveness must be minimized and in remotely-performed endoscopic or robotic thyroidectomy. To overcome this limitation, Huang et al. (17) designed a novel IONM percutaneous recording method for remotely performed thyroid surgery ( Figure 1 and Figure 2B ) in which pairs of insulated needle electrodes (lengths, 25 mm and 38 mm) were inserted percutaneously into the TC perichondrium to within 5 mm of the tip. The four most widely used remote thyroidectomy techniques (bilateral axillary-breast, transoral, transaxillary, and retroauricular approaches) were evaluated in animal experiments and in their initial case series. They concluded that percutaneous TC recording technique is feasible and can be modified according to the approach used for remote access. This technique reduces interruption of the surgical procedure while still providing reliable EMG signals (17).

Percutaneous AL recording during IONM in minimally invasive parathyroidectomy was recently reported by Li, et al. (25). The authors used paired 12mm long needle electrodes for percutaneous recording in 20 patients and successfully detected typical EMG signals. Based on their findings, the authors concluded that their technique is feasible, convenient, reliable, and cost-effective when IONM is used to assist minimally invasive thyroid or parathyroid surgery (25).

In addition to transcartilage AL recording, transcutaneous AL recording is another innovative procedure that is proposed for modern IONM technology (15). Figure 1 shows that transcartilage recording is effective for evaluating vocal fold muscle function and RLN function in TC, and transcutaneous recording may be effective for the same purpose.

Technical advances in epidermal electronics now enable fabrication of sensors in the ideal form can be affixed as an electronic second skin. In 2018, Wu et al. used a porcine model with well-established applicability in IONM research to verify the hypothesis of transcutaneous AL recording. Electrically evoked EMGs were recorded from surface electrodes attached to the ET and from adhesive pre-gelled surface electrodes (Neotrode II^®-ConMed) attached to the anterior neck skin. In their experiments, ET electrodes and neck adhesive skin electrodes successfully recorded typical evoked laryngeal EMG waveforms from RLNs and VNs under 1 mA stimulation. Additionally, both electrode types accurately detected adverse EMG events under experimentally induced RLN traction stress. Under experimentally induced tracheal displacement, however, EMG signals obtained by ET electrodes widely varied whereas EMG signals obtained by transcutaneous electrodes were stable (15). Although this proof-of-concept study confirmed the stability and accuracy of EMG signals obtained by transcutaneous approach, it also revealed the need for new electrode designs that provide more consistent and accurate EMG amplitudes before practical clinical application of this approach.

In 2020, Lee et al. (26) performed the first clinical study to evaluate the efficacy of transcutaneous AL recording during monitored thyroidectomy. A disposable pre-gelled adhesive surface electrode (1.5 cm x 2.0 cm x 2.5 cm; DSE3125; Medtronic Xomed; Jacksonville, FL, USA) was attached to each of the two upper margins of the TC surface. The setup time for the skin electrodes was less than 1 minute in all cases. Their experimental results confirmed the effectiveness of IONM for recording evoked biphasic EMG signals of acceptable quality in all at-risk nerves.

Recently, Shin et al. (29) investigated the optimal attachment location of transcutaneous adhesive skin electrodes for IONM. In porcine animal model, the mean amplitude obtained using laterally attached transcutaneous electrodes was significantly higher than that obtained using medially attached skin surface electrodes. However, there was no significant difference in amplitude according to vertical levels (upper/middle/lower). In human patients, they reported that the ET electrode (716.25 ± 543.35 µV) showed a significantly higher mean amplitude than laterally attached transcutaneous electrodes (258.48 ± 77.31 µV), and the laterally attached transcutaneous electrodes showed a significantly higher mean amplitude than the medially attached skin electrodes (185.22 ± 66.56 µV) on RLN stimulation. Therefore, they concluded that transcutaneous recording is feasible and the lateral side of the thyroid cartilage lamina may be better than the medial side for electrode attachment to obtain better EMG signals from the intrinsic laryngeal muscles.

Although thyroid surgery is now a commonly performed procedure worldwide, RLN injuries are still common complications and a major cause of low satisfaction with thyroid surgery outcomes and medical malpractice litigation. Use of IONM in thyroid surgery has become well established in the past two decades, and surgical applications of IONM are increasingly accepted throughout the world. Recent registry-based studies performed in Sweden (SQRTPA) (33), Europe (EUROCRINE^®) (34), United Kingdom (UKRETS) (35), and other regions (36) provide insight into current IONM practices. Most studies agree that a large and growing majority of thyroid surgeons currently use IONM for anatomical identification of the RLN and for evaluating RLN injury. Another common motivation for using IONM is to reduce the risk of temporary and permanent RLN paralysis.

The most important issue when IONM is performed using an ETT as the recording side is that IONM has a high negative predictive value (92%-100%) but a relatively low and variable positive predictive value (10%-90%) (37). The IONM recording quality (i.e., stability and consistency) depends on the stability of contact between the ET electrodes and the vocal folds, and contact quality may vary widely during surgical manipulations. Therefore, alternative electrode types such as transcartilage, percutaneous, and transcutaneous AL recording electrodes have been extensively studied in recent years to minimize factors that negatively affect ET-IONM accuracy and efficacy. This article presents a complete overview of state-of-the-art transcartilage, percutaneous, and transcutaneous AL recording techniques used in IONM and compares their contribution to improved voice outcomes in modern thyroid surgery.

This is the first comprehensive review in the literature of IONM with transcartilage (14, 16, 18–24, 27, 28), percutaneous (17, 25), and transcutaneous (15, 26) AL recording electrodes. The techniques are illustrated ( Figure 1 ), major findings of each study are summarized and highlighted ( Table 1 ), and the pros and cons of each method are discussed and compared ( Figure 2 , Figure 3 and Table 2 ). In comparison with conventional ET recording IONM, advantages of AL recording IONM reported in both animal and clinical studies include lower invasiveness, better quality and stability of EMG signals, and avoidance of time-consuming disturbances such as the need to verify the ET position. In addition, the high reliability and quality of EMG response making these recording methods not only useful during routine ordinary thyroid and parathyroid surgery, but also practical during thyroid surgery with small incision, remote access, and in specific (e.g., pediatric) populations. In addition to ensuring stable EMG signals, AL recording IONM has several advantages. First, the equipment setup is user-friendly; reported setup times approximate 2 minutes for transcartilage needle electrodes (19) and less than 1 minute for transcutaneous electrodes (26). Second, only a short setup time is required for rapid implementation when an unexpected need for IONM occurs during surgery. Third, dislodged electrodes can be identified and managed intraoperatively. Finally, AL electrodes are apparently more cost effective than ET electrodes (28). A pair of adhesive pre-gelled electrodes or needle electrodes can be purchased for the equivalent of less than 100 USD, which is at least five-fold lower than the cost of EMG ET electrodes.

Whereas these novel techniques are apparently practicable and have no major disadvantages in most clinical applications, disadvantages of transcartilage electrodes include the higher skin flap elevation required to expose the TC ( Figure 2A ), and the difficulty of manipulating the electrodes in procedures performed within a limited operative space, e.g., in endoscopic thyroidectomy or in procedures in which the size of the incision is minimized to improve cosmetic outcome. Additionally, a needle electrode insertion may be complicated by scar tissue caused by revision surgery or, in older adults, by calcified TC, both of which can substantially impair recording of compound muscle action potential responses (14). Finally, patients undergoing such procedures have a low but still risk of laryngeal hematoma, laceration, infection, or rupture of an endotracheal cuff, especially in procedures performed with needle electrodes. Therefore, the recommendation is to insert the needle gently into the subperichondrium of the middle thyroid lamina from the anterior margin of the thyrohyoid muscle with a 10- to 15-degree slope on each side (22).

Although percutaneous AL electrodes are applicable in small incision thyroid and parathyroid surgery and in remote thyroidectomy, insertion of needle electrodes into the TC should be performed with extreme caution to avoid inadvertent injury to the cricothyroid muscle or EBSLN, which can cause muscular hematoma or scar tissue formation and subsequent alterations in vocal pitch. Additionally, percutaneous needle recording electrodes can inadvertently record far field potentials. Therefore, the recommended practices are confirming the stimulation site and comparing corresponding VN, RLN, or EBSLN waveforms, and adjusting the current intensity to minimize recording of far field potentials. Finally, excessive skin retraction or the use of skin retraction for counter-traction during remote thyroidectomy (17) could cause percutaneous needle displacement ( Figure 2B ).

Although transcutaneous AL recording in IONM has proven feasible and reliable, further technical refinement is needed to address some technical flaws. The skin electrode could be affected by patient characteristics such as obese or short neck, degree of subplatysmal flap elevation, and large tumor size. During surgery, subplatysmal flap and retraction of the strap muscle during dissection of the thyroid upper pole may hinder neural signal transmission. The EMG signals actually recorded after upper pole dissection might also be diminished (38). Therefore, this technique may not be useful in procedures that require a large incision or involve a large tumor size (15). Additionally, since both animal and clinical studies agree that low amplitude remains the major limitation of this technique, further research is needed to improve electrode designs and recording quality. Shin et al. (29) suggest that the lower amplitude could be overcome by attaching the skin electrodes more laterally and close to the cricoarytenoid joint. Therefore, the authors of this review suggest the surgeons may consider using ultrasonography to decide the optimal location of the AL electrodes preoperatively ( Figure 3 ).

In summary, this review of the recent literature regarding the feasibility, stability, safety, and efficiency of new and emerging techniques for obtaining transcartilage, percutaneous, or transcutaneous AL recordings during IONM found that recently developed techniques increase the potential applications of IONM as a high-quality quantitative tool in thyroid and parathyroid surgery. However, this review also revealed that most clinical studies have enrolled a relatively small number of patients. Therefore, future prospective studies in larger populations are needed to explore and verify the applicability and benefits of these techniques. Several novel techniques that can further improve AL recordings have been recently reported in the literature. One study uses a nanosheet-based microneedle for EMG recording, which minimizes the risk of laryngeal injury caused by needle insertion (39). Instead of using electrophysiologic laryngeal EMG to evaluate muscle movement, several recent animal studies have also evaluated the use of novel devices that use a piezo-electric surface pressure sensor (40, 41) or an accelerometer sensor (42) to measure muscle twitch. Another interesting development is an ‘‘electronic skin’’ (e-skin) fabricated by embedding various serpentine sensors in a highly stretchable net sandwiched between two protective layers of equal thickness (43). Like a bandage, the device can be attached to the skin surface to acquire physiological information that may be applicable in transcutaneous AL recording. In the future, these sensors may be integrated in various transcutaneous, transcartilage or ET-base surface electrode designs for IONM recording during thyroid surgery.

In the current era in which quality of life is increasingly included as a surgical outcome measure, voice outcome after thyroidectomy is an important consideration for both patients and any clinician involved in managing such patients. Several methods and technologies are being developed to overcome the limitations and disadvantages of the current IONM system that relies on EMG ET recording. This article reviews major recent developments and progress in new and emerging transcartilage, percutaneous, and transcutaneous AL recording techniques used during IONM. In comparison with the conventional ET recording method, many experimental and clinical studies have shown that these up-to-date AL recording methods have advantages of lower invasiveness, better EMG quality and stability, and avoidance of time-consuming disturbances for ET position verification. In addition, these methods are not only feasible for routine ordinary thyroid and parathyroid surgery, but also practical during thyroid or parathyroid surgery with a small incision, remote access, and in pediatric operations. Additional advantages of AL recordings include a cost-effective and surgeon-friendly set-up, allow for rapid implementation when an unexpected need, and the dislodged electrodes can be easily identified and managed intraoperatively. Although there are still some limitations of each recording method, we believe the continuous practical application and implementation of these developments will further optimize IONM to the ultimate benefit of thyroid surgery patients.

CL, TY-H, CW-W, and GD conceived and designed the study. Administrative support was obtained by LF-W, HY-T, and YC-L. Provision of study materials by JW, L-PC, H-YT, Y-CL had collected and assembled the data. Data analysis and interpretation was done by F-YC, T-YH, and CL. All authors contributed to the article and approved the submitted version.

This study was supported by grants from Kaohsiung Medical University Hospital (KMUH109-9M44), Kaohsiung Municipal Siaogang Hospital/Kaohsiung Medical University Research Center grants (KMHK-DK (C)110009, I-109-04, H-109-05, I-108-02) and Ministry of Science and Technology (MOST 108-2628-B-037-006, MOST 109-2628-B-037-014, MOST 110-2314-B-037-104-MY2, MOST 110-2314-B-037-120), Taiwan.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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