Purse-indigitation mechanical anastomosis vs. traditional mechanical anastomosis undergoing McKeown esophagectomy: a retrospective comparative cohort study
Introduction
In esophageal cancer, resection with immediate reconstruction—usually with the stomach—is currently considered the standard surgical treatment for curative or palliative measures. Unfortunately, leakage of the esophagogastric anastomosis after esophagectomy, with an average incidence rate of 10%, remains the most challenging complication. Leakage from an esophagogastric anastomosis can have serious implications for patient morbidity, as it prolongs fasting time and hospital stay, worsens financial burden, and increases the risk of reoperation and mortality (1,2).
The esophagogastric anastomosis can typically be performed in the chest or neck and several reports have described various anastomotic techniques including hand sewn, circular stapled, linear stapled and the modified Collard approach (combined linear and transverse stapled anastomosis) (3). There are certain notable factors associated with anastomotic leak including the absence of serosa layer, longitudinal orientation of the muscle fibers, the segmental blood supply, and tension of anastomosis. It has been demonstrated that wrapping the pedicled omental flap for esophagogastric anastomosis and using fibrin glue may help to promote sealing and decrease the leak rate (4,5). Stapling techniques during esophagectomy have often been employed. However, an esophagogastric anastomosis can be performed using a variety of techniques (6,7). Further investigation of esophagogastric anastomosis should be discussed and shared among experts in order to identify those incremental changes that may further improve outcomes (8,9).
Minimally invasive esophagectomy (MIE) has become a viable option in the surgical treatment of esophageal cancer. In our center, we adopted a circular stapled anastomotic technique because it has the advantage of a short learning curve and is more popular in McKeown esophagectomy worldwide. Since 2020, our purpose has been to investigate if improved treatment of the esophageal stump could decrease the occurrence of anastomotic leak. We made a minor modification based on traditional mechanical anastomosis (TMA). In the present study, we introduce an improved method of cervical esophagogastric anastomosis, referred to as purse-indigitation mechanical anastomosis (PIMA), and compare its feasibility, efficacy, and safety with those of TMA. We hypothesize that novel methods, like PIMA, can improve upon TMA by reducing postoperative anastomosis-related complications. We present the following article in accordance with the STROBE reporting checklist (available at https://atm.amegroups.com/article/view/10.21037/atm-22-3865/rc).
Methods
Study design and participants
This study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). This study was approved by the Ethics Committee of Fujian Cancer Hospital (No. SQ2021-072-01), and informed consent was taken from all the patients. A total of 318 patients with esophageal cancer, hospitalized between September 2020 to January 2022 in the Fujian Cancer Hospital, were preoperatively evaluated for eligibility for surgical resection. The inclusion criteria included patients who underwent esophageal cancer surgery for thoracic esophageal cancer for pathologic cT1–4aN0–2M0 [American Joint Committee on Cancer (AJCC) eighth edition]. The exclusion criteria for participation in this study were the following: (I) extended total gastrectomy; (II) colonic interposition or small bowel jejunal interposition reconstructions; (III) emergency resections; (IV) 2-stage Sweet and Ivor Lewis esophagectomy; (V) resections for benign disease; (VI) mediastinoscopy-assisted esophagectomy; (VII) completely hand-sewn anastomosis; and (VIII) open esophagectomy. Of the 318 patients, 264 met the criteria and were enrolled into the study. Resections were carried out by 2 different surgical teams (PIMA by S. Liu, F. Wang and P. Wang and TMA by D. Zhang, Y. Chen and H. Zhou). PIMA or TMA was performed after thoracoscopic and laparoscopic esophagectomy of esophageal cancer and cervical esophagogastrostomy in these patients, with 195 receiving PIMA and the other 69 receiving TMA (Figure 1). Three grades of anastomotic leak were defined (10). Demographic data including patient age, sex, diagnosis, neoadjuvant chemotherapy/radiation therapy in cases of malignancy, and comorbidities were collected (available at https://cdn.amegroups.cn/static/public/atm-22-3865-1.xlsx).
Surgical approaches
The operations were performed using thoracoscopy and laparoscopy, consisting of 3 stages: the thoracic, abdominal, and cervical stages. The thoracic stage and abdominal stage were performed in a manner previously described (7,11,12). No pyloroplasty was performed during the operation. Feeding tubes were inserted during the abdominal stage. The gastric conduit (3-cm wide) was achieved in the routine manner.
Cervical esophageal mobilization and esophagogastric anastomosis were performed during the cervical stage. The formed gastric tube was drawn up to the left neck through the posterior mediastinal route. For the TMA group, after an appropriate size of anvil (size of stapler: no. 21 or no. 25; Johnson & Johnson) was inserted and well placed, an incision was made at the lesser curvature side on the esophagogastric junction for the entrance of the stapler shaft. A circular end-to-end stapled anastomosis within 5-cm distal to the right gastroepiploic artery was then completed with the anastomotic site on the posterior wall of the gastric conduit and close to the greater curvature to ensure better blood flow (Figure 2A-2D). The remnant gastric conduit was transected about 1–2 cm from the anastomotic line, ensuring an adequate blood supply (Figure 2E).
For the PIMA group, the esophageal stump was sutured by interrupted horizontal mattress suture, while the anastomotic line near to the ischemic point was sutured by the purse-string technique. It is worth noting that the string at the proximal end of the esophagus should be 1 cm away from the anastomosis line and about 1–1.5 cm from the distal end of the slender gastric conduit to ensure coverage of the ischemic point, from which leakage can easily occur (Figure 2F-2H). The purpose of this suture method is to strengthen the anastomosis and the serous membrane of the anastomosis, such that if anastomotic fistula occurs, it remains an internal one. The scheme of PIMA is illustrated in Figure 3.
Postoperative treatment and follow-up
Anti-infection, nutritional support, and other treatments were routinely administered postoperatively. The cervical drainage tube was removed after 72 hours’ observation of no postoperative bleeding. Enteral nutrition was initiated after 24 hours of surgery. Esophageal radiography using diatrizoate meglumine was performed to confirm the integrity of the esophagogastric anastomosis postoperatively. An oral soft-food diet was initiated at the third postoperative week. Patients were followed for up to 3 months after discharge, and all patients underwent upper gastrointestinal examination to test the integrity of the anastomosis. The primary outcome was the incidence of anastomotic leak within 3 months after surgery to evaluate the safety and efficacy of the new technique.
Variables and statistical analysis
The basic demographic data of patients were recorded including sex, age, tumor location, neoadjuvant therapy, pathological type, pathological stage, nerve involvement, vascular invasion, total operation time, time of anastomosis, estimated blood loss, and type of postoperative complication (anastomotic leakage, anastomotic stricture, pulmonary complication). The quantitative data are expressed as the mean ± standard deviation (SD). Statistical analyses to evaluate variables included Pearson χ2 test, Fisher exact test, and univariate logistic regression. Baseline demographic and treatment date were compared between patients who underwent PIMA and those who underwent TMA. The statistical significance (alpha value) threshold was fixed at 0.05. Odds ratios (ORs) were estimated from logistic regression models. All P values were two-sided, and 95% confidence intervals (CIs) are provided. All data were analyzed with GraphPad Prism version 5.0 (GraphPad Software, San Diego, CA, USA).
Results
Patient characteristics
Characteristics of the patients, including sex, age, tumor location, neoadjuvant therapy, pathological type, T stage, N stage, pathologic stage, nerve involvement, and vascular invasion are shown in Table 1. In all, 264 patients with thoracic esophageal cancer were enrolled and underwent thoracoscopic and laparoscopic esophagectomy of esophageal cancer, followed by cervical esophagogastrostomy. No statistical differences were found among the abovementioned characteristics (Table 1, all P values >0.05).
Table 1
| Variables | PIMA (n=195) | TMA (n=69) | P value |
|---|---|---|---|
| Sex | 0.32 | ||
| Male | 154 | 50 | |
| Female | 41 | 19 | |
| Age (years) | 0.76 | ||
| <60 | 61 | 20 | |
| ≥60 | 134 | 49 | |
| Tumor location | 0.65 | ||
| Upper | 22 | 8 | |
| Middle | 96 | 38 | |
| Lower | 77 | 23 | |
| Neoadjuvant therapy | 0.54 | ||
| NCRT | 23 | 5 | |
| NCT | 58 | 20 | |
| Noa | 114 | 44 | |
| Pathological type | 0.43 | ||
| Squamous cell carcinomas | 190 | 66 | |
| Non-squamous cell carcinomasb | 5 | 3 | |
| Pathological T stage | 0.2 | ||
| Tis/T0/T1/T2 | 91 | 26 | |
| T3/T4 | 104 | 43 | |
| Pathological N stage | 0.31 | ||
| N0/N1 | 153 | 50 | |
| N2/N3 | 42 | 19 | |
| Pathologic stage | 0.89 | ||
| 0–II | 93 | 34 | |
| III–IV | 102 | 35 | |
| Nerve involvement | 0.61 | ||
| Yes | 64 | 25 | |
| No | 131 | 44 | |
| Vascular invasion | 0.588 | ||
| Yes | 100 | 38 | |
| No | 95 | 31 |
a, no treatment before surgery; b, adenocarcinoma, small-cell carcinoma, melanoma, spindle cell carcinoma. NCRT, neoadjuvant chemoradiotherapy; NCT, neoadjuvant chemotherapy; PIMA, purse-indigitation mechanical anastomosis; TMA, traditional mechanical anastomosis.
Operative and postoperative outcomes
All patients received the McKeown procedure with a variety of anastomotic techniques. Table 2 presents the operative and short-term postoperative outcomes, showing that the overall incidence of postoperative anastomotic leak in the PIMA group was lower than that in the TMA group (4.10% vs. 11.59%, P=0.04). No significant difference was found between the PIMA and TMA group for the following measures: total operation time (243.94 ±21.98 vs. 238.70±28.45 min, P=0.13), estimated blood loss (201.10±67.83 vs. 197.39±65.13 mL, P=0.68), postoperative hospital stay (8.83±2.77 vs. 9.35±3.78 days, P=0.22), pulmonary complications (8.21% vs. 11.59%, P=0.47), or anastomotic stricture (1.03% vs. 1.45%, P=1.00). Surprisingly, 3 patients in the PIMA group who only had subcutaneous emphysema after discharge had leak grade I, while the others had leak grade II; meanwhile, in the TMA group, 8 patients had leak grade II (P=0.20). One patient in the PIMA group died after the operation because of severe pulmonary complications, while in the TMA group no 90-day mortalities occurred (P=1.00).
Table 2
| Parameters | PIMA (n=195) | TMA (n=69) | P value |
|---|---|---|---|
| Total operation time (min), mean ± SD | 243.94±21.98 | 238.70±28.45 | 0.13 |
| Estimated blood loss (mL), mean ± SD | 201.10±67.83 | 197.39±65.13 | 0.68 |
| Postoperative hospital stay (days), mean ± SD | 8.83±2.77 | 9.35±3.78 | 0.22 |
| Pulmonary complications, n (%) | 16 (8.21) | 8 (11.59) | 0.47 |
| Anastomotic leak, n (%) | 8 (4.10) | 8 (11.59) | 0.04 |
| Anastomotic stricture, n (%) | 2 (1.03) | 1 (1.45) | 1.00 |
| In-hospital and 90-day mortality, n (%) | 1 (0.50) | 0 (0.00) | 1.00 |
SD, standard deviation; PIMA, purse-indigitation mechanical anastomosis; TMA, traditional mechanical anastomosis.
Factors associated with anastomotic leak
Overall, 16 patients (6.06%) experienced an anastomotic leak. Among the patients in the TMA group, those who underwent TMA had higher leak rates (n=8; 11.59%) compared with those who underwent PIMA (n=8; 4.10%; P=0.04). We also found that the incidence of postoperative pulmonary complications (3.44% vs. 50%) was significantly associated with an increased rate of anastomotic leak (OR: 15.50; 95% CI: 4.81–43.71; P<0.01). In the patients who underwent neoadjuvant chemoradiotherapy, there tended to be an increased rate of anastomotic leak compared with those who underwent esophagectomy alone (OR: 3.60; 95% CI: 0.98–13.22; P=0.06). However, there was no significant difference in the incidence of anastomotic leak in patients with neoadjuvant chemotherapy compared with those who underwent surgery alone (OR: 1.48; 95% CI: 0.45–4.82; P=0.53; Table 3).
Table 3
| Variables | No leak (n=248) | Leak (n=16) | OR | 95% CI | P value |
|---|---|---|---|---|---|
| Sex | 1.00 | ||||
| Male | 191 | 13 | 1.00 | ||
| Female | 57 | 3 | 1.29 | 0.36–4.70 | |
| Age (years) | 0.78 | ||||
| <60 | 77 | 4 | 1.00 | ||
| ≥60 | 171 | 12 | 1.35 | 0.42–4.32 | |
| Tumor location | 0.19 | ||||
| Upper | 30 | 0 | – | ||
| Middle | 122 | 11 | – | – | |
| Lower | 96 | 5 | – | – | |
| Neoadjuvant therapy | |||||
| Noa | 151 | 7 | 1.00 | ||
| NCRT | 24 | 4 | 3.60 | 0.98–13.22 | 0.06 |
| NCT | 73 | 5 | 1.48 | 0.45–4.82 | 0.53 |
| Pathological T stage | 0.31 | ||||
| Tis/T0/T1/T2 | 112 | 5 | 1.00 | ||
| T3/T4 | 136 | 11 | 1.81 | 0.61–5.37 | |
| Pathological N stage | 0.77 | ||||
| N0/N1 | 191 | 12 | 1.00 | ||
| N2/N3 | 57 | 4 | 1.12 | 0.35–3.60 | |
| Pathologic stage | 0.45 | ||||
| 0–II | 121 | 6 | 1.00 | ||
| III–IV | 127 | 10 | 1.59 | 0.56–4.50 | |
| Nerve involvement | 0.42 | ||||
| No | 166 | 9 | 1.00 | ||
| Yes | 82 | 7 | 1.58 | 0.57–4.38 | |
| Vascular invasion | 0.8 | ||||
| No | 129 | 9 | 1.00 | ||
| Yes | 119 | 7 | 0.84 | 0.30–2.33 | |
| Pulmonary complication | <0.01 | ||||
| No | 232 | 8 | 1.00 | ||
| Yes | 16 | 8 | 15.50 | 4.81–43.71 | |
| Anastomotic type | 0.04 | ||||
| PIMA | 187 | 8 | 1.00 | ||
| TMA | 61 | 8 | 3.07 | 1.10–8.52 |
a, no treatment before surgery. NCRT, neoadjuvant chemoradiotherapy; NCT, neoadjuvant chemotherapy; OR, odds ratio; CI, confidence interval; PIMA, purse-indigitation mechanical anastomosis; TMA, traditional mechanical anastomosis.
Discussion
Anastomotic leak is a common complication after McKeown esophagectomy and cervical anastomosis. Over the past decades, a variety of anastomotic techniques have been used, among which a uniform technique has not been agreed upon (7,13,14). Recent studies have demonstrated that MIE promotes postoperative recovery by decreasing complications (15,16). In this study, our data revealed a significantly decreased anastomotic leak rate when the cervical anastomosis employed the novel PIMA as compared with TMA.
Risk factors for anastomotic leak after radical McKeown esophagectomy include tension or ischemia at the anastomosis, extent of the mobilization of esophagus, lack of surgical experience, surgical technique, the compression of the conduit at the thoracic inlet, malnutrition, tumor stage, involvement at the anastomotic margin, neoadjuvant therapy, and patient comorbidities, among others (17,18). Previous studies have reported that a 3-cm wide gastric conduit is superior in providing blood supply and tube length compared to a 5-cm wide gastric conduit. Moreover, one multivariable analysis found a wider gastric conduit to involve a higher risk of developing anastomotic leakage (17,19). In the present study, PIMA and TMA were all performed with a 3-cm wide gastric conduit.
There are several requirements for the application of PIMA: (I) to ensure better blood supply, the anastomotic site should be within 5 cm from the top of the right gastroepiploic artery; (II) a longer gastric conduit in PIMA compared with TMA is needed, and the width of the gastric conduit should be approximately 3 cm and (III) the ischemic point between the right gastroepiploic artery and anastomosis should be covered by purse-string suture, as the greater the distance is from the distal end of the right gastroepiploic artery, the more likely anastomotic leak is to occur. The cardinal principle of the PIMA is to re-embed the ischemic area. If an anastomotic leak does occur, the digestive fluid can be restricted within an internally closed space, preventing leakage beyond this stage. Indeed, in the PIMA group of our study, 3 patients with grade I leak had delayed leakage and no abnormalities present in the upper gastrointestinal examination.
Anastomotic stenosis and esophageal reflux are frequent complications after McKeown esophagectomy (20). Anastomotic stenosis presents as dysphagia needing one or more endoscopic dilatations. Perhaps due to the short follow-up period in our study, only 1 patient experienced anastomotic stenosis. PIMA did not increase the rate of anastomotic stenosis. Clinically, we found that this novel technique might decrease the occurrence of postoperative reflux although we cannot explain these findings given limited data and low incidence of postoperative reflux in our study.
It should be noted that the addition of chemoradiation may increase the chance for toxicity, including anastomotic leak after surgery. Our findings are consistent with those in previously published studies (21-23). In our study, neoadjuvant chemoradiotherapy tended to be associated with a higher rate of anastomotic leak compared with surgery alone. Moreover, neoadjuvant chemotherapy did not increase the rate of anastomotic leak. It thus seems that radiotherapy has a greater contribution to the occurrence of anastomotic leak than does chemotherapy.
Owing to the application of pleural flaps in covering the upper mediastinum, leak related to cervical anastomosis mainly presents as a local infection, subcutaneous emphysema, and abscess (24). In our study, when a leak did occur, there was no leakage into the pleural cavity leading to potential subsequent pulmonary complications. Pulmonary complications are frequent postoperative complications of McKeown esophagectomy. We found that when pulmonary complications did occur, the incidence of anastomotic leak significantly increased (P<0.01).
Several limitations to this study should be noted. First, our design was restricted to being a retrospective analysis, which cannot account for all the potential factors that could help explain some of our findings. Second, the sample size of our study was relatively small and there were not an equal number of patients between groups with this being particularly subject to selection bias; because we adopted PIMA recently and the review only went back to 2020. Third, we only included patients who underwent cervical anastomosis via McKeown esophagectomy, and other surgical approaches were not considered. Finally, due to the short follow-up period and limited data obtained, we lack sufficient evidence to evaluate the long-term survival between techniques.
In conclusion, we believe that our novel anastomotic method is a feasible, safe, and viable alternative procedure for esophagogastric anastomosis, as it may significantly reduce the incidence of postoperative anastomosis leak in patients undergoing McKeown MIE for cancer.
Acknowledgments
The authors appreciate the academic support from AME Esophageal Surgery Collaborative Group.
Funding: This study was supported by funding from the National Natural Science Foundation of China (No. 82002497); the Science and Technology Program of Fujian Province (Nos. 2020J05072, 2020J011125, 2021J01442); and the Fujian Provincial Health and Family Planning Research Talent Training Project (No. 2018-CXB-3).
Footnote
Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://atm.amegroups.com/article/view/10.21037/atm-22-3865/rc
Data Sharing Statement: Available at https://atm.amegroups.com/article/view/10.21037/atm-22-3865/dss
Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://atm.amegroups.com/article/view/10.21037/atm-22-3865/coif). Dr. ISS has received honoraria for education/speaking and/or consulting from Intuitive Surgical, CMR, Stryker, and AMSI. The other 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 conducted in accordance with the Declaration of Helsinki (as revised in 2013). This study was approved by the Ethics Committee of Fujian Cancer Hospital (No. SQ2021-072-01), and informed consent was taken from all the patients.
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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(English Language Editor: J. Gray)
