Comparisons between minimally invasive and open esophagectomy for esophageal cancer with cervical anastomosis: a retrospective study

Esophageal carcinoma is a kind of digestive system tumor with high malignancy and poor prognosis. It has been reported that the overall survival rate of esophageal cancer in 5 years is only 15–20% [1], which turns into the sixth leading cause of cancer-related death worldwide [2]. Squamous cell carcinoma (SCC) and adenocarcinoma (AC) present to be the most common pathological types of esophageal cancer, among which squamous cell carcinoma develops as a principal pathological type. The distribution of esophageal cancer demonstrates significant regional differences [3]. The incidence of SCC mostly occurred in Asia, especially in China (more than half of global SCC cases), while the highest burden of AC was found in Western countries [4]. The incidence of AC in the Western world has been a marked and steady increase over recent decades which takes predominantly in esophagectomy patients [5]. Current treatment strategies for esophageal cancer have developed into two main directions: local-regional therapy and systemic treatment. At the same time, optimized individual therapeutic protocol should be achieved for patients with esophageal cancer based on the type of tumor, location, local infiltration, and individual physiological conditions. However, esophagectomy with radical lymph nodes dissection is recognized as one of the standard treatments for patients with localized and locally advanced disease [6]. Due to the complexity of surgical procedures, huge trauma, severe postoperative complications (especially pulmonary infection), and poor quality of life after operation [7], surgical treatment still has risks in a high mortality rate andother disadvantages as well, along with advances in both medical technology and postoperative care.

As medical technologies advance rapidly, extensive attention and application of video-assisted thoracoscopic surgery with trauma reduction have gainedfrom thoracic surgeons, especially in China [8]. Numerous comparative studies on MIE and OE have revealed that MIE has produced satisfactory results in lower rate of postoperative complications, better relieved pain, less blood loss, more lymph nodes retrieved, shorter hospital stay, better postoperative short-term quality of life and lower overall mortality rates [9, 10]. However, no consensus has been reached on the indications for MIE treatment yet, which is generally determined by the surgeon’s clinical experience currently. More comparative studies between MIE and OE have been carried out focusing on safety of procedures, rate of the tumor resection, postoperative survival rate, and quality of life.

Data associated with MIE and OE has been obtained for the treatment of middle or upper esophageal carcinoma in this study. Analysis on the safety of procedures, rate of tumor resection, postoperative complications and quality of life has been performed in order to provide relevant references for MIE on esophageal cancer therapy.

For patients with esophageal cancer, surgical resection with the combination of neoadjuvant chemoradiotherapy or chemotherapy was considered as the only potential path for a radical cure currently [11, 12]. However, patients underwent OE were extremely traumatic and suffered from severe postoperative complications, including pulmonary infection and poor quality of life [7]. Since 1992 Cuschieri et al have reported [13] the first application of minimally invasive technique adopted for resection of esophageal cancer. As it produced great potential in minimizing invasions and accelerating rehabilitation, the application of this technique gained popularity in the medical front. However, many scholars hold a conservative attitude on MIE including the complexity of the procedure, adequacy of resection and nodal clearance in upper third tumors, and availability of MIE in patients who performed chemoradiotherapy [14]. As science and technology advance over the past 30 years, technologyies including high-definition imaging, novel energy devices, and enhanced stapling had been widely used in modern medicine. Meanwhile, a variety of modified MIE procedures had been widely implemented in major medical centers all over the world. No consensus has been reached on whether MIE tends to be superior to OE or notamong centers. However, many comparative studies on the clinical effects of MIE and OE, namely the clinical randomized controlled researches [10], Meta analyses [15] and retrospective studies [16], confirmed that there were no significant differences in both techniques. Contrary to general expectations, results in comparing MIE with OE had shown that MIE was associated with lower operative blood loss, shorter ICUand hospital stays, fewer postoperative respiratory complications, better relieved pain and short-term postoperative quality of life [17]. The outcome of postoperative hospital stay in MIE was significantly shorter than in OE (9.68 ± 2.97 vs 15.64 ± 6.05, P < 0.0001) in our study. A growing number of clinical trials of esophagectomy showed that MIE could shorten hospital stay [18‐20].

A natural channel for early lymphatic returns and distant skip metastases were provided due to the extensive submucosal lymphatic plexus under the esophageal wall (i.e., lymph nodes adjacent to the primary tumor are not affected, but more distant-located lymph nodes contain metastases) [21]. Thus, the early metastases of lymph nodes were one of the characteristics of esophageal cancer. Studies had reported that about 20–40% of patients with submucosal esophageal cancer developed local lymph node metastasis [22, 23]. Consequently, extensive lymph nodes dissection can maximize the clearance of malignant lymph nodes which played an essential role in inhibiting tumor recurrence and facilicating a long survival time for patients with esophageal cancer. A retrospective study on 3572 cases of esophageal carcinoma from Worldwide Esophageal Cancer Collaboration Group (WECC) found that, patients with complete tumor R0 resection, the more lymph nodes extracted, the higher survival rate exhibited in patients. In addition, the total number of lymph nodes was an independent risk factor prognosticating patients’ survivals [24]. In our study, the number of lymph nodes, intraoperative blood loss, and operative time were significantly ameliorated in MIE when compared with OE. Research by Dhamija et al. emphasized that the extent and effect of lymph nodes dissection in MIE were closely linked with learning curve and surgeons’ experiences [25]. Our surgical team initiated the thoracic minimally invasive surgery combined with open surgery for resection of esophageal cancer since July 2012. Total minimally invasive esophagectomy was finally been developed in March 2013. We maintained that the learning curve had a practical impact on the lymph nodes resection (p < 0.0001), operation time (p < 0.0001) and intraoperative blood loss (p < 0.0001) in early stages of MIE. Recently, a clinical comparative study between HMIE (Hybrid minimally invasive esophagectomy) and OE has revealed that there were no significant differences on the number of lymph nodes resection (22 vs. 20, p = 0.459) and R0 resection rate (95 vs 93%, p = 0.500) [26]. However, the operation time (329 vs 407 min, p < 0.001), blood transfusion rate (18 vs 50%, p < 0.001), and length of hospital stay (14 vs 18 days, p = 0.002) in HMIE were significantly better than those in OE. We made a 4–5 cm longitudinal incision below the xiphoid process to pull out the stomach and a 4- to 5-cm-wide gastric conduit was built, which helped shorten the total operation time significantly with the best record of 88 min. However, both complexity and prolonged operation time of MIE procedures increased when patients were associated with pleural adhesions, enormous tumor mass and preoperative chemoradiotherapy. Patients who underwent OE and MIE for esophageal cancer in the Society of Thoracic Surgeons General Thoracic Surgery Database (STS Database) showed that approximately 50% of patients had preoperative radiation therapy, which contrasted dramatically with only 5.66% (OE) and 8.05% (MIE) of patients by esophagectomy in our study [27]. The procedure duration of OE (312.0 min) and MIE (443.0 min) in the STS Database was also higher than the operation time (OE vs MIE, 200.34 ± 14.51 vs 146.08 ± 17.35 min, P < 0.0001) in our study. We speculated that the absence of preoperative radiation therapy probably was the reason for the shortened operation time. The STS Database Task Force reported that most US patients with esophageal cancer had a BMI greater than 25.0 (66.2%, N = 4321) [28], while Chinese patients presented a BMI less than 25.0. Esophageal resection in overweight patients was associated with increased operative time [29]. This also indicated another possibility which significantly influenced outcomes of shorter operative time.

A lot of studies have reported significantly lower pulmonary complications for those who underwent MIE versus OE [17, 18, 30]. Of note, there are several factors linked to pulmonary complications post procedure, including preoperative status, intraoperative details, and postoperative details [31]. In this study, rates of pulmonary infection in MIE were slightly higher than those in OE, although there was no significant difference demonstrated. And that the pulmonary infection rate of patients who underwent MIE (31.3%) was higher than that reported in other studies (17.1%) [18]. One reason may be that the location of the tumor was in the middle or upper segment of the esophagus. This probably enhanced the pain associated with their MIE procedure and produced a negative effect on the incidence of pulmonary complications. Another reason may be that the differences in BMI ranges between Asian and Western populations generating higher pulmonary infection. Mitzman et al. (2018) reported that among patients who were overweight BMI (25.0 to 34.9, accounting for 55% of all patients), there was a lower risk of having any major, pulmonary, infectious, or other complications when compared with BMI 21.5 [29]. In addition, the extensive lymph nodes dissection in MIE (OE vs MIE, 18.42 ± 3.66 vs 38.89 ± 4.31, P < 0.0001) may be considered as another cause. Researches discovered that [32, 33] extensive lymph nodes dissection significantly increased postoperative respiratory complications and delayed patients’ rehabilitation. However, contrary opinions proved that extensive lymph nodes dissection neither elevated the risk of postoperative morbidity nor affected the life quality of patients [34, 35]. Therefore, the relationship between the number of lymph nodes resection and postoperative complications may deserve further investigations.

Results from our retrospective analysis between MIE and OE showed that the clinical outcomes were similar in both procedures. While the number of lymph nodes and intraoperative blood loss were significantly ameliorated in MIE. Moreover, a 4–5 cm longitudinal incision below the xiphoid process was made to create the gastric conduit under direct vision helped to shorten the total operation time significantly.