We previously reported our procedure for thoracoscopic esophagectomy in the left lateral decubitus position and suggested the benefits of minimally invasive esophagectomy and use of the technique to limit morbidity [
5]. Intraoperative nerve injury is caused by thermal damage, stretching, cutting, compression, and vascular compromise to the nerve. These mechanisms more frequently affect the left recurrent laryngeal nerve compared to the right, because of its longer course and vulnerability within the mediastinum. Minimally invasive esophagectomy is particularly beneficial to reduce the incidence of postoperative respiratory complications, but may be associated with a higher incidence of left recurrent nerve palsy according to one large Japanese study [
6]. In this study, we present our lymph node dissection technique, with specific attention to the micro-anatomical layer to avoid recurrent laryngeal nerve injury.
Discussion
By avoiding direct nerve injury, unreasonable traction, thermal damage, and other factors associated with RLNP, the incidence of RLNP should be minimized. Herein, we have reviewed the dissection techniques used to limit the occurrence of RLNP, with specific focus on the anatomical layer around the recurrent laryngeal nerve. This new technique for limiting the incidence of RLNP is based on the simple concept of preserving the thin layer of tissue on the left recurrent laryngeal nerve. We refer to this as the native tissue preservation technique. Although we dissected the recurrent laryngeal nerve lymph nodes bilaterally, we did not note any incidence of RLNP (Clavien-Dindo classification > grade II) in this series of patients. This novel technique enabled an extended radical lymphadenectomy with retrieval of a mean of 26.5 lymph nodes from the mediastinum and 58.6 total lymph nodes.
Thoracic esophageal cancer accounts for approximately 90% of esophageal cancers in Japan, with a relatively high risk of metastases to upper mediastinal lymph nodes along the recurrent laryngeal nerves bilaterally [
10]. Moreover, we clinically suspected metastasis in the recurrent laryngeal nerve lymph nodes in 51 cases (58.6%). Right recurrent laryngeal nerve lymph node metastasis was noted in 47 cases (54%) and left recurrent laryngeal nerve lymph node metastasis was noted in 19 cases (21.8%); bilateral recurrent laryngeal nerve lymph node metastasis was observed in 15 cases (17.2%) in our study. We chose neoadjuvant chemotherapy for 89% cases in this study, and a total of 24 cases (27.6%) of lymph node metastasis around the recurrent laryngeal nerve was diagnosed. Based on the pathological findings, lymph node metastasis on the right side was detected in 18 cases (20.7%), while lymph node metastasis on the left side was detected in 12 cases (13.8%); bilateral metastasis was detected in 6 cases (6.9%). Given the nature of the disease, extended radical lymphadenectomy including the upper mediastinal lymph nodes along both recurrent laryngeal nerves is considered a standard surgical approach in Japan [
11‐
13]. Although it depends on the extent of lymph node dissection performed, the incidence of RLNP after esophagectomy with radical lymph node dissection is reported to range from 8.3 to 40.9% [
2‐
4]. This rate of RLNP after a three-field lymph node dissection is unacceptably high following esophagectomy. Radical lymphadenectomy including the upper mediastinal nodes after neoadjuvant chemotherapy for patients with advanced esophageal cancer improved the overall 5-year survival rate from 50 to 70% in our institution [
5].
The resection of esophageal cancer has recently been performed thoracoscopically for many patients [
6]. We use thoracoscopic magnification during lymph node dissection and divide the branches of the recurrent laryngeal nerve carefully to avoid thermal damage, stretching, cutting, compression, and vascular compromise. Placing a tape around the recurrent laryngeal nerve during lymphadenectomy is usually performed during radical esophagectomy performed through a thoracotomy [
11,
13]. However, minimally invasive esophagectomy has a higher rate of recurrent nerve palsy compared with open surgery (10.3% vs. 8.1%), suggesting the need to more carefully avoid RLNP when performing resection of esophageal cancer [
6]. Minimally invasive esophagectomy has good outcomes usually with little bleeding, but we noticed thermal damage and stretching of the recurrent laryngeal nerve during the lymphadenectomy. We believe these factors contribute to the development of RLNP and care must be taken to avoid these actions intraoperatively.
Most dissections were performed with an ultrasonic surgical device when performing the upper mediastinal lymphadenectomy along the recurrent laryngeal nerves during minimally invasive esophagectomy. Special care is taken to avoid thermal damage and cavitation. There is evidence that the use of electrosurgical devices may lead to inadvertent damage to nearby structures such as the bowel, nerves, or blood vessels through the lateral spread of thermal energy [
14‐
17]. Studies also show a correlation of the degree of thermal injury with lateral thermal spread [
18,
19]. A study of the Harmonic Scalpel device demonstrated that it may be used without a substantial rise in the temperature of adjacent tissues. An increase in tissue temperature above 42 °C results in both damage to cell membranes and protein denaturation [
20]. Sutton et al. suggested that the use of electrosurgical instruments is associated with a significant rise in temperature at the tip of the instrument, proportional to the power and length of time of application [
21]. We are vigilant regarding the duration of application and use the short pitch dissection technique within 1–2 s when dissecting connective tissue and small vessels. These precautions may limit thermal damage to the recurrent laryngeal nerve.
To investigate the influence of distance from the instrument on damage to the recurrent laryngeal nerve, Megan et al. compared thermal spread and recurrent laryngeal nerve function with the THUNDERBEAT Open Fine Jaw device, the bipolar Ligasure Small Jaw, and the ultrasonic Harmonic Focus for open thyroidectomy [
22]. This study concluded that RLN injury did not occur if the devices were used approximately 2 mm away from the nerve. We did not maintain this 2 mm margin from the nerve because of existing adipose and lymph node tissue that must be radically resected inside that margin. Although we cannot conclude a specific safe distance from the nerve based on this study, we believe that attention to meticulous dissection during lymphadenectomy around the nerve with magnification can avoid RLNP due to thermal damage.
Stretching of the recurrent laryngeal nerve during lymphadenectomy must be avoided. We believe that excessive stretching is the most common mechanism of recurrent laryngeal nerve injury. The left recurrent laryngeal nerve is more frequently involved, probably because the longer course of the nerve creates additional vulnerability, especially within the mediastinum. However, this native tissue preservation technique was used around not only the left recurrent laryngeal nerve area but also the right recurrent laryngeal nerve lymph node. Thyroid surgeons suggest that excessive traction is the most common mechanism of recurrent laryngeal nerve injury and suggest that intraoperative nerve monitoring may be a useful adjunct to decrease the rate of injury [
23‐
25]. We used intraoperative nerve monitoring in the past, but it was difficult to prevent injury because the monitoring was not continuous. We could only determine the incidence of recurrent laryngeal nerve palsy, but continuous intraoperative nerve monitoring was useful to decrease the injury in thyroid surgery [
24]. In a recent animal study, Deguchi et al. studied approaches to decrease the incidence of RLN damage during esophageal surgery [
26] and suggested that continuous intraoperative nerve monitoring may be useful to decrease the incidence of nerve injury in esophageal surgery. The underlying concept of this native tissue preservation technique is to maintain the recurrent laryngeal nerve in its normal anatomical position without stretching, thermal damage, or touching the nerve, and this approach limits the incidence of RLNP, as there was no incidence of RLNP in 87 consecutive patients in this study. The native tissue preservation technique also limits the incidence of vascular compromise to the recurrent laryngeal nerve. Blood flow affects nerve function and regeneration [
27,
28]. We believe that the thin layer of connective tissue around the recurrent laryngeal nerve also preserves the small blood vessels that supply the recurrent laryngeal nerve.
Although it has been suggested that neoadjuvant chemo-radiation therapy increases postoperative complications and mortality compared to surgery alone [
29], we performed neoadjuvant chemo-radiation (40 Gy) followed by minimally invasive esophagectomy using the native tissue preservation technique after 4 weeks in four cases. We did not note a significant difference in the thoracic operation time (175.5 min), thoracic blood loss (68 ml), and postoperative length of stay (16.5 days) compared to the other techniques. There were no complications in our patients. Therefore, our procedure can be performed safely for patients who receive neoadjuvant chemo-radiation therapy.
Postoperative bleeding was observed in two patients (2.3%) in this study. One patient showed bleeding from a branch of the right bronchial artery on postoperative day 2 and required reoperation. Another patient presented with postoperative bleeding from a branch of the right gastroepiploic artery after gastric tube reconstruction on postoperative day 0 and required reoperation. These bleeding events were not related to lymphadenectomy, and the patients were discharged following an extended standard perioperative course. Pneumonia was observed in three patients (3.4%) in this study, which is a lower incidence than previously reported [
2,
3,
6]. Among these three patients, one patient had previous experienced postoperative bleeding, and he developed atelectasis, anastomotic leakage, and pneumonia. Two elderly patients (over 85 years old) developed aspiration pneumonia, which suggests that this technique may limit the development of aspiration pneumonia. We believe that this approach helps limit the incidence of recurrent laryngeal nerve palsy and is a simple technique based on anatomical structures, facilitating its use by most esophageal surgeons.
This study has limitations. It is a single-institution retrospective study, and all operations were performed by a highly experienced team. These results may not be generalizable but are encouraging and support further study of the native tissue preservation technique. These results are expected to contribute to the prevention of recurrent laryngeal nerve palsy during minimally invasive esophagectomy with radical lymph node dissection.
In conclusion, the native tissue preservation technique maintains the normal anatomical position of the recurrent laryngeal nerve, avoiding stretching, thermal damage, and direct contact to the nerve. This technique was used in 87 consecutive patients who underwent minimally invasive radical esophagectomy with radical lymph node dissection, and there was no incidence of RLNP. This native tissue preservation technique may reduce the incidence of recurrent laryngeal nerve paralysis after minimally invasive esophagectomy with radical lymph node dissection.
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