Standardization of bilateral upper mediastinal lymph node dissection using microanatomical concepts in minimally invasive esophagectomy

INTRODUCTION

Esophageal cancer (EC) is one of the most common gastrointestinal malignancies, mainly in Asian countries, and has a poor prognosis^[1]. Even today, primary treatment is still radical esophagectomy with regional lymphadenectomy^[2]. The surgical strategy for EC though has been shifting towards minimally invasive esophagectomy (MIE). Currently, thoracoscopic esophagectomy is the most common type of MIE. In 1992, the world’s first thoracoscopic esophagectomy was performed in the lateral decubitus position^[3]. For a period of time after, thoracoscopic esophagectomy in the lateral decubitus position (TELP) was the standard in MIE, and much progress was made, especially in Japan^[4,5]. Although thoracoscopic esophagectomy in the prone position (TEPP) was reported slightly later than TELP^[6,7], this procedure had not been used for a while. However, in 2006, Palanivelu et al.^[8] reported about 130 cases of TEPP and showed both decreased operative time and the frequency of respiratory complications compared with TELP and open esophagectomy. It was also reported that the main reasons for TEPP’s usefulness were due to the advantages of good exposure of the surgical field and improved ergonomics for the surgeon. Since then, TEPP has increasingly been adopted all over the world, including here in Japan, and there have been several reports of the tolerability and efficacy of this procedure^[9-12].

Upper mediastinal lymph node dissection (UMLND) remains the most important procedure in esophageal cancer surgery. However, this has also been the most difficult and time-consuming part, especially in TEPP. Although there have been technical reports about UMLND in TEPP, the longer thoracoscopic operative times and the higher recurrent laryngeal nerve (RLN) palsy rates of 10%-28% represent persistent challenges^[9,13,14]. Recently, progress in the development of endoscopic optical instruments [2K full high-definition (HD), 4K ultra-HD, and 3-dimensional] has been remarkable. Using them, we have been able to identify the fine microanatomy of membranes and layers that were not previously visualized, and there have been some reports on this new concept of surgical microanatomy and its usefulness in esophageal cancer surgery^[13-18].

In our institution, we have performed more than 500 cases of TEPP. Since reaching around 350 cases, we have been able to use a 4K ultra-HD system for our surgeries. Therefore, we started microanatomy-based standardization of UMLND using this endoscopically magnified view and established it when we reached around 400 cases. Previously, we have reported the concept of this standardization on the left side and its usefulness for safe and efficient surgery, especially for decreasing recurrent laryngeal nerve palsy rates^[19]. Concurrently, we have also standardized UMLND on the right side with the same concept as on the left within the same period.

The aim of this study was to investigate the outcomes of our microanatomy-based standardized procedure for UMLND on both sides using a 4K ultra-HD system, with a focus on decreasing operative time.

METHODS

Microanatomy-based standardization of left upper mediastinal lymph node dissection

In our procedure, the concepts of the meso-esophagus and visceral sheath are important. The meso-esophagus contains the lymph nodes around the recurrent laryngeal nerve, and the visceral sheath wraps the esophagus, trachea, and bilateral meso-esophagus [Figure 1A]^[19]. First, we peel off the dorsal and lateral sides of the esophagus, preserving the visceral sheath. On the lateral side, adhesions around the visceral sheath are so tight that we always have to peel it off together with branches of the sympathetic nerve [Figure 1B and 3A]. Furthermore, on the right side, we also peel it off together with the vascular sheath [Figure 1B]. Next, we detach the esophagus and the meso-esophagus from the trachea and aggregate the lymphatic chain to the esophageal side [Figures 2A, D and 3B]. Next, we proceed with lymph node dissection along the recurrent laryngeal nerve from the central to the peripheral part. On the left side especially, we flip up the lymphatic chain on the inner surface of the visceral sheath and slide the nerve down to the natural position [Figures 2B, E, F and 3C, D]. Finally, we cut the visceral sheath on the dorsal side of the nerve [Figure 2C, G].

Figure 1. A: the microanatomical concept in the upper mediastinum; B: detaching the meso-esophagus while preserving the visceral sheath

Figure 2. Microanatomy-based standardization of upper mediastinal lymph node dissection. A, D: detaching the esophagus together with the lymphatic chain from the trachea and aggregating the lymphatic chain to the esophageal side; B, E, F: identifying the recurrent laryngeal nerve and lymph node dissection along the nerve from the central part to the peripheral part; C, G: final findings of upper mediastinal lymph node dissection

Figure 3. Thoracoscopic 4K ultra-high-definition view. A: detaching the meso-esophagus on the left side while preserving the visceral sheath; B: aggregating the lymphatic chain to the esophageal side on the left side; C: upper mediastinal lymph node dissection on the right side; D: upper mediastinal lymph node dissection on the left side

RESULTS

Change in thoracoscopic operative time

There was a significant difference in thoracoscopic operative time between the pre-standardization group and the post-standardization group [n = 91, 232.0 (202.8-264.0) min vs.n = 83, 209.0 (176.0-235.0) min, (P < 0.001)] [Table 2]. The moving average curve showed that the thoracoscopic operative time decreased markedly during the phase of microanatomy-based standardization of UMLD (from 350 cases to 400 cases) and stabilized [Figure 4].

Figure 4. Twenty-case moving average of thoracoscopic operative time

DISCUSSION

When most MIEs were performed via TELP, there were reports that precise mediastinal lymph node dissection by MIE was as feasible as that by open thoracotomy with the added advantages of lesser decrease in respiratory function and lower respiratory complication rates^[4,5]. However, even now, it is important in TELP to have a special team composed of three experts (i.e., surgeon, assistant, and endoscopist) to perform the procedure smoothly. On the other hand, an excellent surgical field contributed simply by gravity and artificial pneumothorax without the need for an assistant is one advantage of TEPP. Furthermore, the improved ergonomics for the surgeon in TEPP is another advantage.

In the early phase of introducing TEPP in this decade, there were some reports about its conferred advantages for lymph node dissection, especially in the upper mediastinum^[9-12]. Along with the recent, remarkable progress of endoscopic optical instruments such as 3D and 4K ultra-HD, there have also been reports about the microanatomy-based surgical concept for MIE, similar to total meso-rectal excision in rectal cancer surgery^[13-18]. More recently, we have established the microanatomy-based standardization using the concept of the meso-esophagus wrapped with the visceral and vascular sheaths and reported its usefulness for left UMLND^[19]. Although we thought that this concept could also be applied for right UMLND, the asymmetrical anatomical structure in the upper mediastinum was an issue. The branching patterns of the arteries are different and the points of recurrence of the recurrent laryngeal nerves and their running direction and length are also different. However, for both the right and left sides, the recurrent laryngeal nerves originate from each main trunk of the vagal nerve within the vascular sheath and transit to the inner aspect of the visceral sheath after turning back at an artery. The nerves then run to the larynx as their target organ through the meso-esophagus. In addition, lymph nodes around the recurrent laryngeal nerve that should be dissected as regional lymph nodes are located within the meso-esophagus on both sides. In the first step of our standardization of UMLND, it is most important not to destroy the visceral sheath enveloping the lymphatic chain in the meso-esophagus, although the vascular sheath on each side should be detached in a different manner and range. After that, we proceed to en bloc lymph node dissection while preserving the visceral sheath and nerve.

Regarding thoracoscopic operative time, the first learning curve occurred due to the initial standardization of the lower mediastinal procedure of TEPP^[20]. After the initial standardization, the indication was expanded for thoracoscopic surgery. The thoracoscopic operative time again lengthened, followed by a second gentle, natural learning curve. However, after that, no obvious learning curve effect was achieved until more than 300 cases. Nevertheless, the microanatomy-based standardization during this time from case 350 to 400 contributed to a marked decrease in thoracoscopic operative time (by almost 30 min), even though the number of surgeries performed by less experienced operators increased. We believe that accurate understanding of the microanatomy involved contributed towards defining the surgical planes more easily for quick dissection of tissues including the lymph nodes with without extra bleeding. On the other hand, young surgeons could also learn the microanatomy from experienced surgeons through the clear 4K HD images and could re-watch the operation many times. Furthermore, there was also a concurrent decrease in postoperative complication rates. Therefore, our microanatomy-based concept appears to be useful not only for accurate and quick UMLD, but also for young surgeons to master the procedure efficiently.

Now, in our institution, we can conduct three types of MIE [thoracoscopic surgery, mediastinoscopic surgery, and robotic-assisted surgery (RAMIE)], and the rate of RAMIE has recently been increasing. We believe that RAMIE is an advanced form of thoracoscopic surgery and our microanatomy-based standardization approach could be similarly applied. Furthermore, we expect that this standardization will make much progress using the joint function and shake reduction system unique to RAMIE.

In conclusion, microanatomy-based standardization using a 4K ultra-HD system enabled quicker and more precise UMLD despite an increase in the number of surgeries performed by less experienced operators.