A novel technique for lymphadenectomy along the left recurrent laryngeal nerve during minimally invasive esophagectomy: a retrospective cohort study

Esophageal cancer is one of the most prevalent malignant tumors worldwide, with a high morbidity and mortality rate in Asia [1, 2]. Poor prognosis primarily stems from lymph node metastases, notably in proximity to the recurrent laryngeal nerves (RLN). Notably, patients with thoracic esophageal cancer exhibit the highest incidence of RLN lymph node metastasis [3]. Studies conducted by Shiozaki et al. reported a substantial 49.1% rate of RLN lymph node metastasis [4], while Zhang et al. documented a metastasis rate of 28% along the left RLN [5]. Consequently, undertaking radical lymphadenectomy along the left RLN emerges as a crucial intervention. This procedure not only enhances postoperative survival but also ensures precise nodal staging, thereby providing invaluable guidance for postoperative treatments.

The total two-field lymphadenectomy, performed concomitantly with esophagectomy using the Mckeown procedure, has gained widespread acceptance among surgeons for the treatment of patients diagnosed with thoracic esophageal squamous cell carcinoma [6‐8]. Nevertheless, executing lymphadenectomy along the RLN poses considerable challenges. These challenges arise from several limitations, including the heightened sensitivity of nerves due to thermal damage, intricate anatomical structures within the superior mediastinum, and the restricted working space available in the superior mediastinal area [9]. In comparison to the right RLN, the left RLN proves to be more challenging to expose and is susceptible to injuries during lymphadenectomy due to its deep-seated location and extended course. Studies by Koterazawa et al. and Oshikiri et al. indicated significant rates of RLN injury, with 26% and 28% incidences, respectively, during minimally invasive esophagectomy [10, 11]. Scholars have experimented with a limited array of techniques for lymphadenectomy along the left RLN in the past [11, 12]. Despite these efforts, there still lacks a universally accepted standard method for conducting lymphadenectomy along the left RLN.

We implemented a novel technique called “elastic suspension of left RLN (ESLR)” for lymphadenectomy along the left RLN with the aim of reducing nerve injury rates and enhancing lymph node dissection rates. In this study, we delineated the surgical procedure and conducted a retrospective analysis to evaluate the safety and efficacy of this technique. This evaluation involved comparing the outcomes of the ESLR method with those of the conventional method for lymphadenectomy.

Zheng et al. previously introduced an esophageal suspension method aimed at reducing postoperative hoarseness following esophagectomy [9]. However, this approach did not demonstrate any advantages concerning the number of harvested lymph nodes along the recurrent laryngeal nerves (RLNs) when compared to the non-suspension group, as observed in prior studies [14‐16]. Additionally, Oshikiri et al. employed the "Bascule Method" for lymph node dissection along the left RLN during esophagectomy [11]. Despite its efficacy, the prone position utilized in this method posed challenges in emergency situations, such as sudden massive bleeding or when urgent conversion to thoracotomy was necessary [17]. Furthermore, the Bascule Method is unsuitable for patients with tumors located across the aortic arch. In the pursuit of minimizing RLN injury, Otsuka et al. placed greater impetus on micro-anatomical layers [18]. However, this approach demands additional time during lymphadenectomy compared to the conventional method. Moreover, the procedure involves two distinct parts, the thoracic and cervical procedures, to accomplish the lymphadenectomy process. In our efforts to achieve radical lymph node dissection along the left RLN while safeguarding its integrity, we introduced the innovative ESLR method. This approach not only enhanced the number of dissected lymph nodes along the left RLN but also significantly reduced the incidence of postoperative RLN injury, all without prolonging the duration of surgery. Importantly, this novel method proved to be versatile, applicable to tumors located at various positions within the thoracic region. Moreover, in comparison to alternative techniques, our novel method was found to be more accessible and easier to master.

Esophageal cancer is predominantly prevalent in Asia and East Africa. In the progression of esophageal cancer, lymph node metastasis occurs early and is frequently characterized as skips or bi-directional metastasis [3, 19]. Lymph nodes along RLNs are highly involved. Tan et al. reported a lymph node metastasis rate along the RLN of 26%, with 20.9% occurring along the right side and 8.7% along the left side [20]. Tachimori et al. reported the incidence of RLN lymph node metastasis as 13.6% along the left side [21]. Radical lymphadenectomy along RLNs could improve the prognosis [22, 23]. In this study, the implementation of the novel ESLR method led to a higher number of dissected lymph nodes along the left RLN compared to the conventional method. Furthermore, patients in the ESLR group exhibited a superior 5-year OS rate in comparison to patients in the conventional group. In the multivariate Cox regression analysis, the number of harvested lymph nodes along the left RLN emerged as a significant factor associated with OS. Specifically, the removal of a greater number of lymph nodes along the left RLN correlated with a more favorable prognosis in this study. These results are consistent with findings from previous studies [22, 23].

Achieving adequate operative exposure is the first step in the lymphadenectomy along RLNs. Compared to the right RLN, the left RLN was more difficult to expose and mobilize through the right thorax. The left RLN resides within a confined and deep space, and its trajectory is longer compared to the right RLN [24]. When patients assumed the left lateral position, the prolapsed right lung and mediastinal structures and organs naturally shifted toward the left side, further deepening the location of the left RLN. During the chest procedure in the ESLR method, patients were positioned in the left semi-prone posture with a 30° ventral rotation of the body axis. In this specific posture, the right lung descended toward the ventral side, enhancing the visibility and accessibility of the operative field. This novel method involved the use of single lumen endotracheal intubation and artificial pneumothorax for all patients. The single lumen endotracheal tube, characterized by its smaller diameter and softer composition compared to a double lumen endotracheal tube, facilitated maneuverability. Unlike double lumen endotracheal intubation, the trachea could be more effectively pushed toward the ventral side by an assistant when utilizing the single lumen endotracheal intubation approach [25, 26]. Preceding the lymphadenectomy, the suspension of the esophagus and the ventral push of the trachea collectively widened the space surrounding the left RLN. The synergistic implementation of these techniques in this novel method significantly enhanced the operative exposure along the left RLN, thereby facilitating the lymphadenectomy procedure. Furthermore, following elastic suspension of the left RLN, the path of the left RLN became distinctly visible compared to the conventional method. This enhanced clarity allowed for a more meticulous and radical dissection of the lymph nodes along the left RLN.

In the postoperative phase, RLN injury stands out as a significant complication [27, 28]. This injury leads to incomplete closure of the vocal cord folds, limiting patients' ability to cough effectively. Moreover, RLN injury heightens the risk of pulmonary complications due to an increased likelihood of aspiration pneumonia. Beyond hoarseness, RLN injury can cause symptoms such as stridor, aspiration pneumonia, severe cough, and even apnea, severely impairing patients' overall quality of life. Oshikiri et al. reported an incidence of 28% for left RLN injury when employing the "Bascule method" for lymphadenectomy [11]. In the ESLR group in this study, 31 patients experienced postoperative RLN injury. The rate of RLN injury associated with this novel method was 10.65%, which was lower than that in the conventional group. Additionally, this injury rate was also lower when compared to rates reported in other studies [10, 19, 29]. Among the patients in the ESLR group who experienced hoarseness, three individuals demonstrated partial recovery within two months following surgery. It is noteworthy that the nerve tissue is highly susceptible to stretching damage [18, 30]. In our approach, we utilized an elastic rope to suspend the left RLN. The effect of elastic traction exerted by the rope on the left RLN mimicked the physiological tension from the surrounding peripheral tissues, possibly enhancing safety during the procedure. Notably, nerves are highly sensitive to clamping and thermal damage [9, 30]. Following the suspension of the left RLN, it was simultaneously "marked" using an elastic rope, providing a distinct visual indicator for surgeons to differentiate the left RLN from the surrounding connective tissues. Employing this novel method ensured a sufficient distance between the suspended left RLN and the adjacent tissues. Consequently, the nerve remained safeguarded against thermal damage during the lymphadenectomy procedure.

It is essential to acknowledge the limitations of this study. The retrospective nature of the study design imposed constraints on randomization, leading to potential bias in the selection of surgical techniques. Moreover, our study solely focused on OS, without delving into disease-free survival rates and tumor-related deaths. To address these limitations, future studies should consider adopting a prospective and randomized approach to provide more robust and comprehensive insights into the effectiveness of the surgical techniques employed.

The utilization of the ESLR method in lymph node dissection along the left RLN during minimally invasive esophagectomy has been demonstrated to be both safe and effective. This innovative approach not only enhances the quantity of dissected lymph nodes along the left RLN but also significantly reduces the incidence of postoperative RLN injury, all without causing a prolongation of operative time. Moreover, patients subjected to this method may experience improved long-term survival rates. Considering these advantages, the ESLR method holds the potential for widespread adoption in esophagectomy procedures.