A non-recurrent laryngeal nerve (NRLN) is an inferior laryngeal nerve with an aberrant path that is due to the nerve coursing from the cervical VN to directly enter the larynx without first descending into the thorax [1,2,3,4]. The estimated incidence of an NRLN on the right side is quite low (0.2–1.5%), and the estimated incidence of an NRLN on the left side is even lower (0.04%) [5,6,7,8,9]. Intraoperative identification and preservation of the NRLN is challenging [7,8,9]. The importance of recognizing this anatomical variant preoperatively in the presence of an aberrant right subclavian artery (ARSA) or early during robotic cervical exploration is critical to avoiding injury to the nerve, which can occur in up to 10% of patients with an NRLN [3].

The procedures for identifying and preserving an NRLN through preoperative imaging, meticulous dissection, and standard intraoperative neural monitoring (IONM) techniques have been discussed extensively in the literature for open surgery [2, 7, 8]. However, there are no published descriptions for identifying and preserving an NRLN during robotic surgery. Therefore, we have presented a video description of two NRLN dissections in which robotic-assisted exploration and simultaneous intermittent nerve monitoring were effective. The goal of this report was to summarize our observations, evaluate the feasibility, provide detailed information concerning proper techniques, and address limitations associated with NRLN robotic dissection and release.

Materials and methods

This video report retrospectively detailed the robotic thyroidectomy procedures performed at the Division of Thyroid Surgery, China-Japan Union Hospital Of Jilin University, Jilin Provincial Key Laboratory of Surgical Translational Medicine, Changchun City, Jilin Province, China. The video specifically focused on two patients who underwent thyroidectomy that required full exposure of an NRLN. In both patients, vocal cord mobility was assessed using flexible laryngoscopy preoperatively and on postoperative day 1 (Video 1). Both patients had been informed that the IONM system would be used as an aid to localize and identify the laryngeal nerves and to assess nerve function during surgery.

The use of CT scans for NRLN preoperative prediction

Axial computed tomography (CT, Toshiba Aquilion ONE) of the neck was included as one of the routine tests performed before robotic thyroidectomy. CT was performed without contrast agents and visualized the area caudal from the thyroid cartilage to the sternoclavicular articulation with horizontal movement every 3 mm (Video 2).

Robot system

A fourth-generation da Vinci Surgical System (Intuitive, USA) was used.

BABA technique

Our group has previously provided detailed descriptions of the BABA approach and IONM in recently published studies (Fig. 1) [10, 11].

Fig. 1
figure 1

BABA approach. A Surgical incision and approach; B robotic arm placement and surgical scenarios

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NRLN definitions

Based on the classification system developed by Toniato et al., NRLNs were classified into three types (I through III). A Type I NRLN courses near the superior thyroid vessels. A Type II (also called Type-IIA) NRLN courses parallel to the inferior thyroid artery, and then courses transversely to and above the inferior thyroid artery. A Type III (also called a Type-IIB) NRLN courses parallel to the inferior thyroid artery, and then courses transversely to and between the branches of the artery or transversely to and under the artery [1].

Algorithm for detecting NRLNs using IONM

Intermittent IONM is performed routinely using standardized procedures and guidelines established by the International Neural Monitoring Study Group (INMSG). The published guidelines include procedures for equipment setup, induction and maintenance anesthesia, correct tube positioning and verification testing, and electromyography (EMG) definitions [12,13,14,15]. Neuromonitoring was performed using a commercially available system (NIM-Response 3.0, Medtronic Inc., Minneapolis, MN, USA) with surface electrode tubes to register the EMG signals from the vocal cords (Medtronic Xomed Inc., Jacksonville, FL, USA). The A–B point comparison algorithm for NRLN identification described by Chiang et al. was routinely performed during the surgeries (Fig. 2) [7]. The VN was routinely tested early in the surgeries to confirm the function of the monitoring system and to confirm the normal pathway of the RLN after the space between the thyroid and carotid sheath was opened. Typically, the VN was indirectly (i.e., without carotid sheath dissection) stimulated distal to the level of the inferior thyroid pole using a suprathreshold current of 3 mA. Point A on the VN was defined as the superior border of the thyroid cartilage. Point B on the VN was defined as the inferior border of the fourth tracheal ring. An NRLN is indicated by a positive EMG signal at point A and a negative EMG signal at point B. Based on the EMG signals, the course of the NRLN can be traced, and its separation point in the upper tracheoesophageal groove can be precisely localized [7, 12,13,14,15].

Fig. 2
figure 2

The A–B point comparison algorithm for NRLN identification using IONM

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IONM stimulation probes for NRLN monitoring

Figure 3 and Video 3 depict how to install the IONM stimulation probes in the robotic surgical unit to monitor the NRLN.

Fig. 3
figure 3

Neural monitoring in robotic surgery. A Selection of site for introducing the neuromonitoring probe through a puncture wound made with a syringe needle; B the intraoperative nerve monitoring is easily performed via percutaneous probe stimulation by inserting the conventional probe through the puncture site and into the working space

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Results

Two patients (38 and 26 years old, both female) presented with right NRLNs. The 3D CT scans revealed the presence of an ARSA, which arose from the descending aorta in both cases. Preoperative fine-needle aspirates confirmed the presence of papillary thyroid carcinoma in both patients. The surgeries were robot-assisted right thyroid lobectomy plus central lymph node dissection.

NRLN findings during surgery

Detailed observations from both surgeries are presented in Video 4 and Fig. 4. Both surgeries were performed by one of the authors (DZ). One NRLN was classed as a Type I and the other a Type II [1]. During surgery, the functional integrity of the NRLNs was documented and confirmed by registration of the EMG signals. The exposed NRLNs were documented with photographs and video imaging. Lymph node dissection was easier alongside the NRLN because no nerve was present in the tracheoesophageal sulcus. Thus, it was only necessary to protect the lower parathyroid gland, esophagus, and trachea (Fig. 4). Because the space between the larynx and nerve was exceedingly narrow, we were able to identify the NRLNs and complete the dissections safely, using magnifying endoscopy and the articulating robotic devices (Fig. 4). We determined that the right NRLN branched from the right VN trunk and ran directly to the larynx. The left recurrent laryngeal nerve was located in its normal position in the tracheoesophageal groove. Some connective tissue bands that crossed the NRLNs in the immediate vicinity could have been responsible for some nerve constriction. We also were able to dissect the proximal segment of the NRLNs to their origins.

Fig. 4
figure 4

Intraoperative image after thyroid lobectomy and central lymph node dissection with NRLN

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Clinical observations and outcomes

The postoperative course was uneventful for both patients. The postoperative laryngeal examination revealed normal vocal cord mobility. The patients were discharged on the third postoperative day. Histological examination revealed that the tumors were both small and invasive but had not spread to the lymph nodes (T1, N0, M0; Table 1).

Table 1 Basic characteristics
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Discussion

This video tutorial demonstrated the techniques used for NRLN management performed by video-assisted robotic thyroidectomy, using BABA. To our knowledge, this is the first video to present NRLN management using robotic thyroidectomy. These two cases are the first to be documented that successfully performed the surgeries using robotics without damaging the NRLN. The steps performed by the surgical team were shown in the video, and we paid particular attention to the description of the anatomy and functional integrity of the NRLN. To perform this type of nerve dissection safely, it was necessary to understand both the normal anatomy and the possible variants of the RLN.

This report included the following information: (1) A description of the aberrant anatomy and CT imaging needed to inform the surgeon of the presence and location of an NRLN. (2) A description of a technique using the nerve monitor with the robotic surgical equipment. (3) A description of the techniques needed to isolate and protect the NRLN during the robotic surgery. The robotic application contributed to the enhancement of the NRLN dissections due to the advantages of increased surgeon control and autonomy, superior instrument dexterity and tissue handling, improved three‐dimensional visualization, and wrist articulation.

Robotic thyroidectomy has become the approach of choice for thyroid resections in Asia, although the procedure is more complicated than open surgery and calls for extensive surgical experience [16,17,18]. Robotics requires a detailed understanding of neck anatomy and the range of possible surgical approaches [16,17,18]. This video tutorial provided a comprehensive description of the dynamic anatomy of the NRLN and demonstrated the optimal robotic approach.

During thyroidectomy and cervical lymphadenectomy performed with robotic surgery, the identification and preservation of an NRLN are essential. Without prediction of the presence of an NRLN preoperatively, surgeons must identify it intraoperatively. Although preoperative identification of an NRLN is difficult, it often accompanies the more readily evident ARSA. Thus, preoperative CT identification of ARSA could indicate the presence of an NRLN. Moreover, identifying an NRLN during robotic surgical neck procedures with IONM offers improved safety. Therefore, the precise dissection of an NRLN could be guided through IONM. We determined that in these cases, we identified the presence of a cervical NRLN early through the use of CT imaging and IONM, which allowed us to dissect the lymph nodes completely. Before beginning dissection of the RLN, the endoscopic surgeon could perform VN stimulation to predict the presence of an NRLN to optimize the efficiency of the subsequent surgical dissection. Brauckhoff et al. described a technique for using IONM to detect an NRLN based on the V1 latency profiles [4]. Chiang et al. introduced the A–B point comparison algorithm in 2012 (Fig. 5) [7].

Fig. 5
figure 5

Flow chart for NRLN management in robotic BABA

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The NRLN anomaly could result in severe difficulties when performing dissections due to the minimal working space. The robotic application clearly contributed several improvements in the NRLN dissections. These advantages included the surgeon’s ability to gain additional precision during the surgery through improved tissue handling, increased visualization of the narrow surgical area, and improved articulation of the surgical instrumentation.

Moreover, during the robotic dissection, we determined that using only the proximal to distal robotic dissection of the NRLN jeopardized the integrity of the nerve. For example, the BABA approach with the Type I NRLN is similar to the dissection of the RLN in transoral thyroidectomy. Also, the thyroid cartilage interferes with the endoscopic visualization of the surgical field. The Type I NRLN is more challenging to manage at the laryngeal entry point and its origin from the VN. For the Type II NRLN, it is essential to identify the point of origin and how the nerve reflects from the VN. Thus, we modified the protocol used for nerve dissection by implementing a hybrid method, similar to the protocol used in open surgery. Occasionally, the nerve was dissected from proximal to distal. In other cases, the dissection proceeded from distal to proximal. By combining the two techniques, we avoided placing any traction on the nerve.

In summary, there are anatomical and technical points that need to be addressed to allow easier and safer dissection of lymph nodes and the laryngeal nerve when an NRLN is present. These preoperative and intraoperative factors include technological and anatomical considerations.

Preoperative considerations (i.e., CT imaging)

An NRLN could be identified prior to surgery as all patients undergo neck and mediastinal CT scans preoperatively. The CT imaging allowed identification of the presence of any vascular anomalies, including an aberrant subclavian artery, which could be an indirect indication that an NRLN was present (please also refer to the ‘Materials and methods’ section). Thus, the surgeon would know that an anatomical variation was present prior to surgery and know before surgery that the RLN nerve was likely not to be located in the tracheoesophageal sulcus. Therefore, this anatomical region (Levels 6 and 7) would be "nerve-free" during lymph node dissection.

Intraoperative considerations (i.e., applied technologies)

IONM

The origin of the NRLN was identified and traced early in the dissection using V1 latency profiles and the A–B point algorithm of the IONM (detailed in the ‘Materials and methods’ section). When the nerve was identified early during surgery, dissection of the neck became less problematic.

Robotic-assisted surgery

The surgical robot allowed superior dissection of the lymph nodes located in the tracheoesophageal sulcus and the lymph nodes located in the vicinity of the NRLNs due to the advantages of increased surgeon control and autonomy, superior instrument dexterity and tissue handling, improved three‐dimensional visualization, and wrist articulation.

Anatomy

The absence of a recurrent laryngeal nerve in the tracheoesophageal sulcus certainly allowed a safer and more complete dissection of the lymph nodes in that anatomical region (i.e., Levels 6 and 7). Our videos and Fig. 4 detail the considerations described above. Without a RLN in the tracheoesophageal sulcus, it was only necessary to protect the lower parathyroid gland, esophagus, and trachea during the surgery (Fig. 4).

The question remains whether damage to the NRLN is more common, but addressing this specific question was not the purpose of this report. Analysis of a larger number of surgeries that involve NRLN nerves is required to address that question. Previously, the NRLN was not clearly recognized and managed during most surgeries. In the past, the only way to recognize an NRLN was through meticulous dissection and surgical experience. However, the current surgical circumstances have changed. Due to preoperative knowledge of the presence of any anatomical variations using CT imaging and the application of advanced technologies, including robotics and IONM, identification of the presence of an NRLN is easier and more specific.