The comparisons of three stapler placement methods for intrathoracic mechanistic circular stapling in Ivor Lewis minimally invasive esophagectomy

Introduction

Subtotal esophagectomy with radical lymph node dissection remains the mainstream choice for the treatment of esophageal cancer (EC) (1). In recent years, Ivor Lewis minimally invasive esophagectomy (ILMIE) has been increasingly performed in the treatment of middle and lower EC as it prevents complications related to cervical anastomosis and reduces the higher morbidity and mortality of conventional open esophagectomy (2,3).

The mechanistic circular stapled technique is the most frequently implemented approach for intrathoracic esophagogastric anastomosis in ILMIE (4). It requires insertion of the anvil into the proximal esophagus stump and anastomosis of the anvil rod with the stapler shaft. However, the appropriate placement of the anvil into the esophageal stump is a challenging step in the thoracoscopic operation (5). Depending on the manner of anvil introduction, the main methods of circular stapled intrathoracic anastomoses include a transoral Orvil technique (TOT) and a hand-sewn purse-string technique (PST). In recent years, the reversal penetrating technique (RPT), a modified anastomotic technique for ILMIE, has been reported to be a simple and effective approach, and its practice experience has been accumulating in some centers (5-7). However, no study has yet compared RPT and the former two methods in intrathoracic anastomoses for esophagogastrostomy.

Anastomotic failure in the form of stricture or leakage is common and critical (8,9). Anastomotic leakage is the main cause of postoperative morbidity, mortality, and prolonged hospitalization (10). Anastomotic stricture requires serial anastomotic dilatation and significantly impairs long-term quality of life. The anastomotic technique might be one major factor that influences anastomotic complications (11). Therefore, in this study, we retrospectively analyzed the impact of RPT on the incidence of anastomotic complications, and we also further identified the risk factors for the development of anastomotic leakage and stricture following ILMIE. We present the following article in accordance with the STROBE reporting checklist (available at https://dx.doi.org/10.21037/jgo-21-322).

Methods

Patients

The clinical data of the patients receiving total laparoscopic and thoracoscopic Ivor Lewis esophagectomy with intrathoracic esophagogastric mechanistic circular stapled anastomosis from Jan 2012 to Dec 2019 in our institution were collected. All patients were diagnosed with EC by gastroscopy and had received overall pre-operative assessment including clinical symptoms, physical examination, and auxiliary laboratory and imaging examinations, etc. Cardiopulmonary function was evaluated by pulmonary function, electrocardiogram, color Doppler echocardiography, and blood gas analysis. All patients underwent esophageal ultrasonography, supraclavicular lymph node ultrasonography, enhanced thoracoabdominal CT, cranial magnetic resonance imaging, or PET/CT for clinical staging. After surgery, all patients were staged according to the 8th edition staging system of the American Joint Committee on Cancer (AJCC) (12). We excluded patients with the upper thoracic esophageal carcinoma. The participants were divided into three groups, namely the RPT, TOT, and PST group according to the different stapler placement methods for intrathoracic mechanistic circular stapling. Clinical data were obtained and retrospectively analyzed from the electronic medical record database, including demographic characteristics, pathological data, anastomosis related conditions, and anastomosis complications, among others. This study was performed in accordance with the principles of the Declaration of Helsinki (as revised in 2013). This research project was approved by the Ethics Committee of the 2nd Affiliated Hospital, School of Medicine, Zhejiang University with approval number 2021-0802. Due to the retrospective design of the study, the local ethics committee confirmed that informed consent was not necessary from participants.

Surgery methods

ILMIE with intrathoracic mechanistic circular esophagogastric anastomosis, which was performed similarly to procedures described in previous literature (5,13), was conducted when the patient was under combined general-epidural anesthesia and double-lumen endotracheal intubation. A gastric conduit was created in most cases. The intrathoracic esophagogastric anastomosis was performed using a circular stapling device. The methods of anvil placement included the TOT, hand-sewn PST, and RPT.

TOT (14)

Esophageal dissection was performed with a linear stapler. Then, the Orvil anvil (DST Series EEA Orvil Device; Covidien) was attached to an orogastric tube, which was fully lubricated and inserted transorally by the anesthesiologist under laryngoscopy. The tube passed out through an incision created at the tip of the esophageal stump and the anvil was sent to and fixed at the predetermined position. The circular stapler was placed into the gastric conduit through gastrostomy. Then, the circular stapler was docked with the anvil to complete the intrathoracic esophagogastric anastomosis.

The hand-sewn PST (15,16)

A 3-0 suture was used to create a hand-sewn purse string through the muscular layer of the esophagus at least 5 cm proximal to the tumor. A transverse incision was made 2 cm distal to the purse-string suture of the esophagus and the anvil was inserted and fixed by tightening the purse string. Then, the esophagus was transected. The gastric conduit was pulled out from the abdominal cavity into the thoracic cavity and the circular stapler was introduced into the gastric conduit to dork with the anvil to construct the intrathoracic anastomosis. The bottom opening of the gastric conduit was closed with the linear stapler.

RPT (5,17)

The main operative steps of ILMIE are shown in Figure 1. A 2-0 prolene suture stitch was linked to the tip of the ancillary rod with a knot. A longitudinal incision was made more than 3.0 cm above the tumor margin on the esophageal wall. The anvil with the suture was inserted into the esophagus lumen through the incision. Then, the suture penetrated the esophagus wall reversely at the predetermined anastomosis position, roughly 5.0 cm above the tumor margin. The suture was pulled to guide the penetration and positioning of the anvil on the esophagus wall. Then, the linear stapler was used to transect the esophagus and obtain the sample. The circular stapler was placed in the gastric conduit through gastrostomy and docked with the anvil to complete the intrathoracic anastomosis. The bottom opening of the gastric conduit was sutured with absorbable line or closed with the linear stapler.

Figure 1 The main operative steps of the reverse penetrating technique in Ivor Lewis minimally invasive esophagectomy. (I) Establishment of an anvil set (A). (II) Placement of the anvil in the esophagus: making a longitudinal incision on the esophageal anterior wall (B); inserting the anvil set into the esophageal lumen (C); penetrating reversely the esophageal wall with a stitch (D) and pulling out the anvil rod (E); transecting the proximal esophagus with the linear stapler (F); detaching the ancillary trocar from the anvil rod and obtaining the anvil placement (G,H). (III) Completion of intrathoracic anastomosis: sending the shaft of the circular stapler into the gastric conduit through gastrostomy (I) and docking with the anvil to achieve anastomosis (J).

Postoperative management

All patients were treated with regular fast, gastrointestinal decompression, analgesia, antibiotics, and antacid therapy. Parenteral nutritional support started 24 h after the operation. The drainage tube was removed on the 3rd postoperative day. Upper gastrointestinal radiography with iodized oil and oral administration of methylene blue dilution were given on the 7th postoperative day to evaluate the integrity of the anastomosis. A fluid diet was resumed on the 6th postoperative day, and a semifluid diet commenced on the 8^th day. Patients with no manifestations of discomfort were discharged from the hospital on the 9–10^th postoperative day.

Perioperative variables and surgical complications

Clinical data were obtained and retrospectively analyzed from the electronic medical record database, including patient demographic characteristics, tumor features, anastomosis related conditions, and anastomosis complications, among others. The following anastomosis-related conditions were recorded: conversion rate, anastomosis position, surgical time, and number of lymph nodes harvested. The postoperative anastomosis complications included the following: anastomosis leakage, stricture, esophagotracheal leakage, and reflux esophagitis. Anastomosis leakage was defined as blue fluid outflowing from the drainage tube, or contrast leakage from the site of intrathoracic anastomosis or clinical suspected leakage requiring alteration of therapy. In our study, we further differentiated minor leakage and major leakage on the basis of the classification system of the Esophagectomy Complications Consensus Group (ECCG) (18). Minor leakage corresponds to type I leakage in the ECCG classification, which refers to leakage associated with no or minor clinical presentation and necessitating no additional intervention (19). Major leakage corresponds to type II and III leakage in the ECCG classification, which refers to leakage presenting signs of inflammation and necessitating related intervention (19). Anastomosis stricture was defined as the development of a feeding obstruction or anastomosis narrowing less than 1 cm under endoscopy or gastrointestinal radiograph and dysphagia requiring at least 1 endoscopic dilatation to relieve the symptom (20).

Statistical analysis

All statistical analyses were performed with SPSS 22.0 (SPSS Inc., Chicago, IL). All tests were two-sided with a significance level of 0.05. The continuous variables were shown as means ± standard deviation (SD) and compared by ANOVA or the Kruskal-Wallis test between more than two groups. The categorical variables were focused on frequencies and proportions, and compared by Chi-square or Fisher’s exact tests between groups. The non-parametric test was used if the one-way ordered R×C list (grade data) did not meet the chi-square test premise. Logistic regression models were used to analyze the influence of clinical and pathological factors on anastomotic leakage and stricture. Univariate analysis was used to determine the correlation between factors and anastomotic leakage or stricture. Candidate variables that showed a univariate relationship with outcome or that were considered clinically relevant were included in the multivariate logistic regression analysis to generate the multivariate logistic regression model. Additionally, 95% confidence intervals (CI) and odds ratio (OR) were calculated.

Results

A total of 316 patients with EC receiving ILMIE were included in the present analysis. There were 154 patients in the RPT group, 78 in the TOT group, and 84 in the PST group. The clinical characteristics of the patients in each study group are listed in Table 1. Except for the method of anvil placement, the perioperative treatment strategy was the same for all the included patients. The patients of the three groups were not statistically different with respect to demographics, comorbidities, preoperative therapy, tumor location, or 30-day mortality (all P>0.05).

The anastomosis-related conditions in esophagectomy are summarized in Table 2. The total conversion rate, the rate of conversion due to anastomosis, the number of total lymph nodes harvested, and the number of mediastinal lymph nodes harvested were not significantly different between groups (all P>0.05). However, the total surgical time and anastomosis time among the three groups were statistically significant (both P<0.05). Furthermore, multiple comparisons with Dunnett’s test (TOT vs. RPT and PST vs. RPT) showed that the total surgical time and anastomosis time in the RPT group were significantly shorter than those in both the PST group and TOT group (all P<0.05).

Table 3 shows the postoperative anastomotic complications in all patients, as well as the differences in anastomotic complications among the RPT, TOT, and PST groups. Anastomotic leakage occurred in 25 patients (7.91%), of which 19 cases had minor anastomotic leakage and 6 cases had major leakage. However, none of the anastomotic leakage rates, regardless of the total rate, minor anastomotic leakage rate, or major anastomotic leakage rate, were significantly different between the 3 experimental groups (all P>0.05). All included patients received postoperative endoscopic evaluation. In total, 49 patients (15.51%) presented with anastomotic stricture in all groups (Table 3). However, the stricture rates among the RPT, TOT, and PST groups were not significantly different (P>0.05). Furthermore, no significant difference among the three groups was noted in esophagotracheal leakage, reflux esophagitis (including anastomotic inflammation), and frequent dependence on anti-reflux medication (all P>0.05).

The results of univariate and multivariate analyses for the prediction of anastomotic leakage and stricture are listed in Tables 4 and 5, respectively. The multivariate logistic regression analyses using an enter model revealed that tumor location, and neoadjuvant therapy predicted anastomotic leakage, rather than the methods of anvil placement. Moreover, anastomotic stricture was significantly influenced by the presence of BMI, smoking history, conversion, and neoadjuvant therapy rather than by the methods of anvil placement.

Discussion

The RPT, a modified method of stapler placement applied in ILMIE, has been reported to be a simple and effective approach, and its practice experience has been accumulating in some centers in the past few years (4,21). We performed this retrospective study to investigate the influence of the RPT compared with the PST and TOT on anastomotic leakage and stricture. We also performed multivariate analysis to analyze the influence of risk factors on anastomotic leakage and stricture in patients undergoing ILMIE.

Our analysis results revealed that the surgery time and anastomosis time of the RPT group were significantly shorter than those of the TOT and PST group. However, other anastomosis-related conditions, including conversion rate and number of lymph nodes dissected, and anastomosis complications, including anastomosis leakage and stricture of the RPT group, were not significantly different from those in the TOT and PST groups.

The shorter surgery time and anastomosis time clearly indicated that the RPT was simpler and easier to perform than the TOT or PST. During the anastomosis procedure of the RPT, a small incision was made to allow for the introduction of the anvil into the esophageal lumen. The operation is easier than in the TOT. In the latter operation, the anvil was transorally introduced by guidance of an orogastric tube, and was performed by an anesthesiologist in cooperation with the surgeon. The penetration of the stitch, suture, and anvil rod in the RPT made the positions of the esophagus and anvil more fixed, thus avoiding excessive surgery and unnecessary esophageal injury. The demanding operation of purse-string hand sewing under endoscopy was avoided in the RPT, and was instead achieved by cutting and closure of a linear stapler. This modification made the operation easier and the cutting edge more regular. Moreover, we can speculate that the less demanding operation of the RPT may greatly shorten the learning curve of surgeons.

Anastomosis leakage is the most serious complication post esophagectomy. The rate of anastomosis leakage in this study was 7.91%, which is slightly higher than the pooled anastomosis leakage rate of 7.1% among 1,791 cases receiving stapler anastomosis for MIE (22) or 6% among 700 cases who received circular stapler anastomosis for MIE reported by Yang et al. (23). This inconsistency may be attributed to the diverse definitions used for anastomotic leakage after esophagectomy and the different surgeons performing the surgery in different studies. The standardized definitions for anastomosis leakage proposed by the ECCG (18) were adopted in our study and hopefully may standardize the anastomosis leakage definition in future studies. However, the major leakage rate in this study was 1.90%, which was slightly lower than the leakage rate of 5.7% requiring treatment after intrathoracic mechanical esophagogastric anastomosis in the study by Harustiak et al. (19).

Both minor and major leakage rates in the RPT, TOT, and PST groups were not significantly different. The multivariate analysis in our study revealed that the factors of tumor location, and neoadjuvant therapy rather than the methods of anvil placement may predict anastomotic leakage. This result was consistent with most previous studies, which suggested that anastomotic leakage may not be affected by the methods of anvil placement (22,23). Minor leakage was speculated to be affected mainly by the sewing skills of surgeons during manual anastomosis (19). In this study, the anastomosis was generated by a mechanical circular stapler, so the concerns regarding sewing skills can be ignored in the comparison among circular stapler anastomosis techniques. One factor that may increase anastomosis leakage after using the RPT is that the end-to-end anastomosis may cross the linear stapler line, potentially increasing the risk of anastomosis leakage. However, according to the analysis results, the anastomosis leakage rate in the RPT group was not increased but slightly lessened compared with the other groups, so this concern is also unnecessary. On the other hand, major leakage might be associated with tissue ischemia that occurs after altered blood perfusion. Therefore, major leakage may not be affected by the methods of anvil placement but by surgical skills and some systemic or intrinsic factors that may influence blood perfusion, such as esophageal separation location, stomach stretching, or diabetes (24,25). Our findings by multivariate analysis confirmed this presumption that the method of anvil placement is not a risk factor of anastomotic leakage.

Anastomosis stricture is a common long-term complication and seriously reduces the quality of life of patients. The rate of anastomotic stricture was 15.51% in our study, comparable with 13.6% reported by Tanaka et al. (26). The results of our study showed no difference with respect to anastomotic stricture between the experimental groups. Furthermore, the multivariate analysis revealed that the factors which may influence the development of anastomotic stricture included BMI, smoking history, and conversion rather than placement of the anvil. According to a previous study, the surgical factors associated with anastomotic stricture after esophagectomy may include small size of the anastomotic stapler, end-to-end anastomosis, excessive tension at the anastomosis, and local tissue pressing, among other factors (27). These results and our study suggest that these 3 methods of anvil placement might not be influencing factors for stricture.

The other anastomotic complication rates did not significantly differ between the RPT, TOT, and PST groups. Overall, these results indicated that using the RTP would not increase the risk of anastomosis-related complications; thus, it is as safe and feasible as TOT or PST.

Besides simplicity, easier operation, safety, and feasibility, the RPT may also have the following advantages in clinical application: (I) in the RPT, the technique can be applied after a small modification of the anvil. In the Orvil technique, a specific Orvil circular stapler and transoral anvil introduction tube are needed; thus, RPT is more economical than the Orvil method; (II) during the anastomosis procedure, involvement of excessive or inadequate esophageal tissues is bad for anastomosis and may cause leakage. Cases of esophageal dilation may be difficult for the PST, as the involvement of the whole circle of the esophageal stump will create redundant esophageal tissue rolled in anastomotic doughnuts, which makes the anastomosis less secure. In the RPT, only part of the stump is involved in anastomosis, so the anastomosis formation will be less influenced by the excessive esophageal tissues. Therefore, in this situation, the RPT has obvious superiority (5). Previously, one limitation of the RPT was that the RPT requires adequate length of normal esophageal tissue. In the RPT, the esophageal wall penetration site is 2 cm or more above the esophageal incision and the esophageal incision is 3 cm or more above the tumor margin. Thus, the anastomosis site is 5 cm or more from the tumor. However, using a flexible curved intraluminal stapler makes the RTP still applicable in cases of tumors in much higher locations.

This is the first study comparing the RPT with two other methods of anvil placement in ILMIE. However, the inherent limitation of the retrospective study design suggests that the patient demographics and baseline clinical parameters were not well balanced. In the future, well-designed randomized trials are warranted for further comparisons.

Conclusions

Compared with the TOT and PST methods of anvil placement for intrathoracic gastroesophageal circular stapling in ILMIE, the RPT method does not increase the risk of anastomotic leakage and stricture, but involves significantly shorter surgical time and anastomosis time. Therefore, the RPT method is a safe, effective, and easier-to-perform anastomotic technique, worthy of further application and popularization in ILMIE.

Acknowledgments

Funding: This study was funded by a grant from the Zhejiang Provincial Natural Science Foundation (grant number: LQ17H010002).

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://dx.doi.org/10.21037/jgo-21-322

Data Sharing Statement: Available at https://dx.doi.org/10.21037/jgo-21-322

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://dx.doi.org/10.21037/jgo-21-322). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. This study was performed in accordance with the principles of the Declaration of Helsinki (as revised in 2013). This research project was approved by the Ethics Committee of the 2nd Affiliated Hospital, School of Medicine, Zhejiang University with approval number 2021-0802. Due to the retrospective design of the study, the local ethics committee confirmed that informed consent was not necessary from participants.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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