This study was approved by the Institutional Review Board of Cancer Hospital, Chinese Academy of Medical Science. The medical records of 445 consecutive patients who underwent minimally invasive McKeown esophagectomy between January 2009 and July 2015 at the Cancer Hospital of Chinese Academy of Medical Sciences were retrospectively reviewed. In the same period, 103 patients received open McKeown esophagectomy. The clinical variables of the paired groups were compared, including age, sex, body mass index (BMI), neoadjuvant therapy, tumor location, duration of operation, intraoperative blood loss, number of harvested lymph nodes, differentiation, American Joint Committee on Cancer (AJCC) stage, morbidity rate, rate of anatomic leakage, pulmonary morbidity rate, mortality rate and length of hospital stay. Esophageal cancer staging was carried out according to the AJCC 2009 cancer staging system[15]. All involved patients gave their informed consent prior to study inclusion. A randomized, controlled trial of neoadjuvant treatment has shown a survival benefit in locally advanced esophageal carcinoma as compared with esophagectomy alone in 2012[16]. Since then, we adopted chemotherapy or chemoradiotherapy as an alternative for locally advanced esophageal cancer.

MIE includes total minimally invasive McKeown esophagectomy and hybrid minimally invasive McKeown esophagectomy[8]. The former consists of thoracoscopic esophagectomy, laparoscopic gastric preparation and gastroesophageal cervical anastomosis, while there are thoracoscopic esophagectomy plus open gastric preparation or laparoscopic gastric preparation plus open esophagectomy in the hybrid minimally invasive McKeown esophagectomy group. Since 2009, total minimally invasive McKeown esophagectomy has been introduced and in use. The selection criteria for patients to either total MIE, hybrid MIE or open esophagectomy were mainly based on the clinical stage and the experiences of surgeons. Patients with early stage esophageal cancer received more minimally invasive esophagectomies than open esophagectomies, and surgeons who received training in minimally invasive thoracic surgery more performed minimally invasive esophagectomies than open esophagectomies.

Thoracoscopic phase: The patient was placed in the left lateral decubitus position. The position of the double-lumen tube was verified, and single-lung ventilation was used. Four thoracoscopic ports were established. A 10 mm port was placed at the seventh intercostal space, just along the anterior axillary line, for the camera. Another 10 mm port was placed at the eighth or ninth intercostal space, posterior to the axillary line, for the dissection instrument (ultrasonic coagulating shears) and passage of the end-to-end circular stapler (EEA; Covidien or Johnson) or Hem-lock. A 5 mm port was placed in the anterior axillary line, at the third or fourth intercostal space, and this was used to pass a fan-shaped retractor to retract the lung anteriorly and allow exposure of the esophagus. A 5 mm port was placed just below the subscapular tip to place the instruments for retraction and counter traction. The inferior pulmonary ligament was divided. The mediastinal pleura overlying the esophagus was divided and opened to the level of the azygous vein to expose the thoracic esophagus. The azygous vein was then dissected and divided with an endoscopic vascular stapler or Hem-lock. The thoracic esophagus, alone with the periesophageal tissue and mediastinal lymph nodes, was circumferentially mobilized from the diaphragm to the level of inlet of the thorax. Mediastinal lymphadenectomy was done for every patient, and the resected lymph nodes included left recurrent and right subclavian,paratracheal, subcarinal, left and right bronchial, lower posterior mediastinum, para-aortic, and para-oesophageal lymph nodes. The chest was inspected closely, and hemostasis was verified. Chest tube was routinely placed.

Laparoscopic phase: The patient was placed in a supine position. A pneumoperitoneum (12-14 cm H₂O) was established by CO₂ injection through an umbilical port. A total of five abdominal ports (three 5 mm and two 10 mm) were used. After placement of the ports, the first step of the laparoscopic phase was an exploration of the abdomen to rule out advanced disease. The mobilization of the stomach was started with the division of the greater curvature using a Harmonic scalpel (Ethicon Endo-Surgery, OH, United States). The short gastric vessels were then divided. The gastrocolic omentum was then divided, with care taken to preserve the right gastroepiploic artery. The posterior attachments of the stomach were then divided after retraction of the stomach anteriorly. The left gastric vessel was divided at its origin from the celiac trunk with an endoscopic gastrointestinal anastomosis (GIA) stapler or Hem-lock. Lymphatic tissues around vessels were included in the resection. Subsequently, the right crus was visualized and dissected, followed by dissecting and defining the left crura of the diaphragm. The abdominal/distal esophagus was dissected as far as possible toward the distal end. The gastric conduit was made extracorporeally. Pyloroplasty or gastric drainage procedure was not routinely performed in our study. We inserted duodenal nutrition tube before anastomosis in the operation. The abdomen was inspected to make sure that hemostasis was adequate and the incisions were closed.

Cervical anastomosis: After laparoscopic phase and thoracoscopic phase, a 4 to 6 cm horizontal neck incision was made to expose the cervical esophagus. Careful dissection was performed down until the thoracic dissection plane was encountered, generally quite easily since the VATS dissection was continued well into the thoracic inlet. The esophagogastric specimen was pulled out of the neck incision and the cervical esophagus divided high. The specimen was removed from the field. An anastomosis was performed between the cervical esophagus and gastric tube using standard techniques (mechanical stapled or handsewn anastomosis in an end-to-side fashion).

Open Mckeown esophagectomy: The first stage was started with a right posterolateral thoracotomy. The mediastinal pleura overlying the esophagus were divided with electrotome. The thoracic esophagus, alone with the periesophageal tissue and mediastinal lymph nodes, was circumferentially mobilized from the diaphragm to the level of the inlet of the thorax.

The second stage is the mobilization of the stomach which was started with the division of the greater curvature using ultrasonic coagulating shears. The short gastric vessels were divided with ultrasonic coagulating shears as well. The gastrocolic omentum was then divided, with care taken to preserve the right gastroepiploic artery. The posterior attachments of the stomach were then divided after retraction of the stomach anteriorly. The left gastric vessel was divided at its origin from the celiac trunk with sutures. Lymphatic tissues around vessels were included in the resection. Subsequently, the abdominal esophagus was dissected as far as possible toward the distal end. Pyloroplasty was not routinely performed. The abdomen is inspected to make sure that hemostasis was adequate and the incisions were closed. For the last stage, the cervical incision was made and then anastomosis was performed like minimally invasive esophagectomy.

Postoperative care: The patients were placed in an intensive care unit or discharged to ward directly from operation room according to the judgement of anesthetist. Assessment of recurrent laryngeal nerve injury was done on the 1^st d postoperatively. Postoperative respiratory tract management included chest physiotherapy and early ambulation. Patient-controlled analgesia was given to every patient to control postoperative pain.

In order to study the learning curve of total minimally invasive McKeown esophagectomy, we selected data of 180 patients who underwent total minimally invasive McKeown esophagectomy in the early period which was performed by five senior thoracic oncologic surgeons who majored in thoracic surgical oncology over 20 years. All 180 patients were divided into three groups according to time sequence from January 2009 to August 2013 as group 1 (n = 60), from September 2013 to November 2013 as group 2 (n = 60) and from December 2013 to group 3 (n = 60).

The SPSS software package 16.0 for Windows was used for statistical analyses. Data are presented as median value (interquartile range) for continuous variables, and percentages for dichotomous variables. Continuous variables were analyzed using ANOVA test or nonparametric test, and categorical variables were analyzed using Fisher exact test. Survival was estimated using Kaplan-Meier method and log-rank tests were used to analyze differences between curves. The significant level was set as a P value less than 0.05.

From January 2009 to June 2015, 445 cases of minimally invasive McKeown esophagectomy were conducted at our hospital. In this cohort, the median age was 60 years (range, 36-79 years) and there were 341 males and 104 females. Twenty-one patients underwent neoadjuvant radiotherapy, and 30 patients underwent neoadjuvant chemotherapy. Other clinical variables are displayed in Table 1. Five patients were converted into open thoracotomy and laparotomy and the reasons for conversion are displayed in Table 2.

The cohort was divided into three groups based on operative technique used. Of 548 McKeown esophagectomies, there were 375 total minimally invasive McKeown esophagectomies, 70 hybrid minimally invasive McKeown esophagectomies and 103 open McKeown esophagectomies. The selection of which approach was based on the opinion of surgeons. Patients who underwent minimally invasive McKeown esophagectomy were older than patients who underwent open Mckeown esophagectomy. Patients who underwent open McKeown esophagectomy were more in the proximal third of the esophagus and more received neoadjuvant chemotherapy and radiotherapy (Table 3) .

As shown in Table 4, patients who underwent total minimally invasive McKeown esophagectomy had significantly less intraoperative blood loss than patients who underwent hybrid minimally invasive McKeown esophagectomy and open McKeown esophagectomy. However, there were no significant differences in duration of operation, number of harvested lymph nodes, or postoperative morbidity including incidence of pulmonary complication and anastomotic leak between total minimally invasive McKeown esophagectomy, hybrid minimally invasive McKeown esophagectomy and open McKeown esophagectomy groups.

Kaplan-Meier plots depict the long term survival of patients who underwent three types of operation: total minimally invasive McKeown esophagectomy, hybrid minimally invasive McKeown esophagectomy and open McKeown esophagectomy (Figure 1). There were no significant differences in 5-year survival between these three types (60.3% vs 47.9% vs 35.3%, P = 0.579).

Open in New Tab   Full Size Figure   Download Figure

Figure 1 Kaplan-Meier analysis of three types of operation. There were no significant differences in 5-yr survival between total minimally invasive McKeown esophagectomy, hybrid minimally invasive McKeown esophagectomy and open Mckeown esophagectomy (60.3% vs 47.9% vs 35.3%, P = 0.579). MIME: Minimally invasive McKeown esophagectomy.

Patients in group 1 (n = 60) had significantly longer duration of operation than those in groups 2 (n = 60) and 3 (n = 60). There were no significant differences in intraoperative blood loss, number of harvested lymph nodes, or postoperative morbidity including incidence of pulmonary complication and anastomotic leak between groups 1, 2 and 3 (Table 5). Five surgeons performed 180 total minimally invasive McKeown esophagectomies. There were no significant differences in the short term outcomes or oncologic clearance between these three groups. The duration of operation got steady after the first 60 cases for 5 surgeons, suggesting that 12 cases were needed for a senior surgeon to master total minimally invasive McKeown esophagectomy at our hospital, a high volume cancer center. Then we analyzed the learning curve for each of 5 surgeons and found that all surgeons had a trend of reduction of duration of operation. Of 5 surgeons, there were significant differences in duration of operation between surgeons A and B, while there were no significant differences in duration of operation between surgeons C, D and E (Figure 2).

Open in New Tab   Full Size Figure   Download Figure

Figure 2 Learning curve of total minimally invasive McKeown esophagectomy of five surgeons. Durations of operation for five surgeons in three periods are as follows: surgeon A (340 ± 57 min vs 395 ± 105 min vs 310 ± 61 min, P = 0.037); surgeon B (413 ± 109 min vs 387 ± 110 min vs 272 ± 58 min, P = 0.002); surgeon C (418 ± 65 min vs 339 ± 116 min vs 367 ± 74 min, P = 0.098); surgeon D (383 ± 105 min vs 359 ± 82 min vs 317 ± 116 min, P = 0.287); and surgeon E (355 ± 123 min vs 337 ± 77 min vs 320 ± 159 min, P = 0.789).

Open McKeown esophagectomy is a complex surgery for upper third esophageal cancer with higher morbidity rate than open Ivor Lewis and Sweet esophagectomy. Minimally invasive esophagectomy is a new technique which aims to reduce systematic inflammatory response syndrome and perioperative morbidity rate.

In the past 5 years, several studies including one randomized controlled trial reported reduced postoperative pulmonary complication rates, comparable oncologic clearance and similar long term survival. However, few studies focused on the comparison of open McKeown esophagectomy and minimally invasive McKeown esophagectomy.

This study again reinforced the feasibility of minimally invasive McKeown esophagectomy and extended previous study of learning curve of minimally invasive McKeown esophagectomy that at least 12 cased are needed to reach the plateau of this technique.

The results of this study may provide new data for thoracic surgeons who majored in esophageal surgery that minimally invasive McKeown esophagectomy is feasible and is associated with less intraoperative blood loss. Most importantly, performing 12 cases of minimally invasive McKeown esophagectomies may reach the plateau of this technique.

This manuscript compared totally minimally invasive esophagectomy (MIE), hybrid MIE and open three stage (McKeowm) oesophagectomy. The authors found the procedure ontologically safe in terms of lymph node yield and long term survival and technically safe in terms of blood loss, operating time, morbidity and mortality. This is an interesting manuscript and clearly written and organized.