Clinical analysis of tubular stapler-assisted nested anastomosis in the prevention of postoperative esophageal cancer complications

Introduction

Esophageal cancer (EC), one of the most common malignant tumor types, ranks 8th in incidence rate and 6th in mortality rate. China has the highest incidence and mortality rates of EC in the world (1-4). Surgery is considered the treatment of choice for patients with early-stage and mid-stage EC (5-8). However, because of the traumatic nature of EC surgery and the need for gastrointestinal reconstruction, high rates of postoperative complications such as anastomotic leakage or stenosis, esophageal reflux, and pulmonary infection exist (9-12). Despite the wide use of mechanical anastomosis in clinical practice and a reduction in the incidence of anastomotic-related complications (13) with advances in science and technology, a high incidence of postoperative anastomotic-related complications persists (14) and presents a challenge to both Chinese and international thoracic surgeons (15,16). The first nested esophagogastric anastomosis assisted by tubular stapler in China was recently performed with a satisfactory clinical result, and the current clinical research results are as follows. In this study, we explored anastomosis techniques in McKeown operation for EC and the influence of different anastomosis methods on clinical efficacy. We present the following article in accordance with the STROBE reporting checklist (available at https://jgo.amegroups.com/article/view/10.21037/jgo-23-166/rc).

Methods

Patients

A total of 544 patients were diagnosed with esophageal squamous cell carcinoma or squamous adenocarcinoma by laparoscopic McKeown surgery in the Thoracic Department of The First Hospital of Lanzhou University between January 2017 and August 2020. All operations were performed by the chief surgeon and his team. According to the method of cervical anastomosis, participants were divided into a tubular stapler-assisted nested anastomosis group or a conventional tubular mechanical anastomosis group. The tubular stapler-assisted nested anastomosis was taken as the time node in this retrospective study. No neoadjuvant therapy was performed before surgery, and no severe cardiopulmonary dysfunction, severe coagulation dysfunction, or metastasis occurred. The inclusion criterion was McKeown operation for EC. Follow-up results and surgical indicators were used as comparison objects to evaluate the clinical efficacy of anastomosis methods in the 2 groups. In order to resolve the problem of deviation of research results, the operation methods were unified, the same person completed the operation, and the postoperative follow-up time was the same; the variables comprised follow-up results, postoperative complications, and surgical indicators. Patients backgrounds between the two groups (Table 1).

A total of 332 patients were in the tubular stapler-assisted nested anastomosis group, including 239 men and 93 women, with an average age of 56.58±4.83 years, an average weight of 67.17±7.15 kg, and an average tumor size of 4.78±1.03 cm. Patients with tumors located in the upper, middle, and lower thoracic segments numbered 85, 160, and 87, respectively. A total of 212 patients were in the conventional tubular mechanical anastomosis group, comprising 150 men and 62 women, with an average age of 57.74±7.56 years, an average weight of 65.69±7.56 kg, and an average tumor size of 4.97±1.04 cm. Patients with tumors located in the upper, middle, and lower thoracic segments numbered 47, 84, and 81, respectively. No significant difference in age, sex, body weight, tumor size, or tumor location was noted between the 2 groups (P>0.05). The diagnosis of esophageal squamous cell carcinoma was confirmed in all patients through preoperative pathology. Central venous catheters were placed by peripheral venipuncture prior to surgery. The purpose and specific steps of the catheterization procedure were explained to the patient and their family. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). Written informed consent was obtained from each participant. The research protocol of this clinical study was approved by the Medical Ethics Committee of The First Hospital of Lanzhou University (No. LDYYLL2022-475).

Surgical procedure

All patients underwent laparoscopic radical surgery for EC through the right thoracic-abdominal-neck 3-incision method. After the dissociation of the thoracic esophagus and the dissection of the thoracic lymph nodes, the patient was placed in a supine position. An incision was made in the anterior edge of the mastoid muscle, the cervical esophagus was separated and removed, and purse-string forceps were introduced into the purse-string suture. The purse-string forceps were then used to dissect the esophagus, and a tubular stapler anvil was placed at the proximal end of the esophagus. After the closure of the distal end and suturing of the traction tube (infusion set tube), laparoscopic dissociation of the stomach was performed. The stomach was lifted out of the abdominal cavity through a small incision under the xiphoid process, In the area superior to the pylorus, the right gastric artery and vein were transected. Utilizing a linear cutting stapler, the stomach was reshaped along the greater curvature from the lesser curvature side superior to the pylorus in an upward direction, creating a narrow tubular shape with a diameter of 3 cm; the gastric fundus was then fixed to the traction tube and the thoracic entrance was enlarged. The stomach fundus was pulled up to the neck by the posterior mediastinum route and a tension-free site on the greater curvature (as close to the right omental vascular arch as possible) was selected to puncture the connecting rod; the bottom nail anvil was finally connected to the anvil and adjusted to the effective stapling range. All patients underwent complete data collection during hospitalization, returned to the hospital according to regular time points after discharge, and completed postoperative follow-up data. All patients underwent a complete examination after admission to evaluate the opportunity for surgery. The clinical data of patients with surgical indications were included in this study. A detailed post-operative visit plan was developed to obtain complete follow-up data to prevent data loss.

Anastomosis method

In the routine anastomosis group, the anastomotic stoma was inspected directly and the esophageal and gastric seromuscular layers were intermittently sutured to embed the anastomosis. A tubular stapler was used to assist in the connection to the bottom nail anvil in the nested anastomosis group. The surgeon made adjustments to the effective stapling range, relied on the support of the stapler to pull the esophagus 3 cm into the stomach, and then intermittently sutured around the esophagus to embed it in the stomach wall. Anastomosis was completed after the suturing of the muscular and gastric seromuscular layers, the verification of stump integrity, and the closure of the gastric stump. The previously inserted gastroenteric feeding tube was removed in all patients. Anastomosis is illustrated in Figure 1. The final state after the gastroesophageal anastomotic site is nested within the gastric cavity in Figure 2. Final effect drawing after anastomosis is in Figure 3.

Figure 1 The process of nested anastomosis.

Figure 2 Gastroesophageal anastomotic site is nested within the gastric cavity.

Figure 3 Stapler cutting stitcher.

Diagnostic criteria for associated complications

The diagnostic criteria for postoperative complications were as follows: (I) anastomotic leakage, as confirmed by a positive methylene blue test or upper gastrointestinal angiography; (II) infection of the neck incision, as confirmed by a positive bacteria culture of the purulent secretion from the catheter placement site; (III) pulmonary infection, as detected by X-ray examination combined with postoperative bloodwork and a positive bacterial sputum culture; and (IV) gastroesophageal reflux, as determined by standard values in the Chinese population as reported in the literature (15)—which were >5 minutes of reflux more than 5 times in 24 hours; abnormal oropharyngeal swab color and pH level <4; and paroxysmal nocturnal dyspnea, asthma, belching, and acid regurgitation—(V) anastomotic inflammation, as confirmed by a 1 month postoperative gastroscopy; (VI) prolonged anastomosis time, defined as the length of time required to complete mechanical anastomosis and anastomotic embedding; (VII) anastomotic stenosis, as indicated by anastomotic stoma <1.0 cm in diameter as measured during a 3-month postoperative gastroscopy and accompanied by dysphagia.

Statistical analysis

The statistical analysis was conducted using SPSS 26.0 (IBM, Armonk, NY, USA). For demographic information, surgical anastomosis time, and incidence of complications, data were described using frequencies or percentages for categorical variables, and analyzed using the chi-square test or Fisher’s exact test. Continuous variables were presented as means ± standard deviation or median (interquartile range), and analyzed using the independent samples t-test or Wilcoxon rank-sum test. A P value less than 0.05 was considered statistically significant between the two groups.

Results

All patients underwent successful operations without conversion to thoracotomy or laparotomy. All surgeries involved the use of a linear cutter stapler to reconstruct the stomach into a thin tube shape approximately 3 cm in diameter. A postoperative 6-month follow-up rate of 100% was achieved. No deaths were reported. Compared with the conventional tubular mechanical anastomosis group, the tubular stapler-assisted nested anastomosis group exhibited a lower incidence of the following complications: anastomotic leakage rate [0 (0/332) vs. 5.2% (11/212)]; pulmonary infection rate [3.3% (11/332) vs. 11.8% (25/212)]; postoperative gastroesophageal reflux rate [6.9% (23/332) vs. 16.0% (34/212)]; anastomotic stricture rate [3.0% (10/332) vs. 10.4% (22/212)]; neck incision infection rate [0.9% (3/332) vs. 7.1% (15/212)]; prolonged surgical anastomosis time (11.02±1.54 vs. 18.53±3.20 min). No significant difference was detected in the incidence of the following complications: arrhythmia, recurrent laryngeal nerve injury, chylothorax, and anastomotic stomatitis (Table 2). In the conventional tubular mechanical anastomosis group, 4 patients with anastomotic leakage were successfully treated with a combination of unobstructed drainage and parenteral nutrition support and 9 patients with anastomotic stenosis experienced significant symptom alleviation after gastroscopic balloon dilation (3 patients) and radial anastomotic incision (6 patients).

Discussion

China has the highest global incidence of EC, of which most cases are located in the middle segment of the esophagus, followed by the lower segment and upper segment (16). Surgery is the preferred treatment method for early-stage and mid-stage EC. EC’s longitudinal infiltration pattern and sequence of growth along the esophageal submucosa necessitates adherence to strict surgical margins. The resection margin is generally located at least 5 cm away from the tumor, and some ECs present with multifocal lesions in clinical practice. Total thoracic esophagectomy with cervical anastomosis is widely regarded as the standard treatment for middle and upper EC (17,18). Clinician and patient expectations of and demand for minimally invasive EC surgery have grown with the continual development of video-assisted thoracoscopy, laparoscopic technology, and related surgical instruments. The advantages of laparoscopic minimally invasive surgery for EC include fewer complications, quicker postoperative recovery (19), and a lower level of pain and trauma, assets that have attracted growing attention and favor from thoracic surgeons (20-26). However, the incidence of anastomotic leakage and related postsurgical complications of cervical anastomosis is significantly higher than in intrathoracic anastomosis, which considerably limits the clinical application of total thoracic esophagectomy and cervical anastomosis. Therefore, the research of thoracic surgeons has long focused on reducing the incidence of oral leakage in cervical anastomosis. Promisingly, the incidence of anastomotic-related complications, including anastomotic leakage, stenosis, and regurgitation, has decreased due to the continual advancement of anastomotic technology and the application of staplers. Nevertheless, complications cannot be completely avoided (27,28). Studies from China and worldwide have reported an anastomotic leakage incidence of 3–26% (18,29-31) and an even higher incidence of stenosis and reflux (32,33), resulting in significantly prolonged hospitalization, increased hospitalization costs, and decreased postoperative quality of life. Therefore, the advancement of anastomosis techniques and reduction of surgery-related complications remain crucial research topics in EC surgery and constitute the focal points of our study. Appropriate anastomosis technology and anastomosis instruments can reduce the incidence of postoperative complications, reduce the physiological and psychological burden of patients, and accelerate the postoperative rehabilitation of patients, reflecting the concept of accelerated surgical rehabilitation.

This study observed a significantly lower incidence of complications in the stapler-assisted insertion anastomosis group than in the conventional anastomosis group, including anastomotic leakage, anastomotic stenosis, reflux, and postoperative pneumonia. Neck anastomotic leakage is a frequent complication of cervical anastomosis in EC. The common causes include excessive anastomotic tension, impaired blood circulation near the anastomotic stoma, local tissue contamination, infection, malnutrition, and inappropriate anastomotic methods. Alverdy et al. (34) noted that anastomotic fistulas may be bacteria-related pathophysiological processes. Bacteria easily migrate to the anastomotic stoma of patients who have large tumors; these patients experience difficult surgical separation and excessive blood loss; the local tissue collagenase activity then grows and eventually develops into anastomotic fistulas. The formation of an anastomotic fistula leads to delayed or non-healing of anastomosis, which is not conducive to the recovery of postoperative digestive tract reconstruction, affects the postoperative quality of patients, aggravates the burden, is not conducive to recovery, and may even result in death. Therefore, it is very important to reduce the occurrence of postoperative complications.

The incidence of anastomotic leakage in the experimental group was significantly lower than that in the conventional anastomosis group. We attribute this difference to the following. First, the embedding of the gastroesophageal anastomosis in the gastric cavity produces no postsurgical tension in the anastomotic stoma and acts as one of the key factors for anastomotic healing. Second, because the mechanical anastomosis was not completed during the first embedding, no risk of pulling or tearing the anastomotic stoma during embedding and suturing was present. Complete gastroesophageal end-to-side anastomosis in an entirely tension-free state constitutes a crucial measure of anastomotic leakage prevention. Third, the anastomosis can be evenly and deeply nested into the gastric cavity with the support force of the stapler. If a small fistula occurs, it can be drained to the gastric cavity without spreading the infection. Fourth, visible or invisible wounds are caused by unavoidable pulling and rotation of the anastomotic stoma during conventional anastomotic embedding due to the poor exposure of the operating field, especially when the posterior wall is embedded. The aforementioned characteristics of the conventional anastomosis group may contribute to the incidence of anastomotic leakage. The use of a stapler and anastomotic nesting can greatly reduce the difficulties encountered during anastomotic embedding, improve the quality and safety of anastomosis, and lower the incidence of postoperative coughing and expectoration (35-37). This anastomosis not only reduces the tear risk caused by the anastomotic tension, but also reduces the irritation to the respiratory tract, which is conducive to reducing the occurrence of postoperative complications and speeding up the recovery of patients.

Additional crucial measures for preventing anastomotic leakage during anastomosis include the following. The first is ensuring adequate blood supply to the stomach, maintaining the integrity of the right omental vascular arch, preserving the main trunk of the right gastric artery, and selecting an anastomotic site near the greater curvature of the vascular arch. The second is ensuring sufficient tubular stomach length, which is essential for tension-free anastomosis and anastomotic nesting. We endeavored to mould the stomach into a tubular shape approximately 3 cm in diameter and parallel to the greater curvature of the vascular arch. An excessively wide diameter would affect the length of the tubular stomach. The third is ensuring the correct reshaping of the tubular stomach. The shape of the stomach also plays a crucial role in the successful nesting of the stapler. The proximal diameter must be wider than the middle and lower parts to accommodate the nesting of the gastroesophageal anastomosis and part of the esophagus into the tubular stomach. Ensuring the smooth nesting of the anastomosis helps prevent tension on the esophageal lumen over the anastomosis, which could impair the esophageal blood supply and lead to postoperative dysphagia.

The incidence of postoperative anastomotic stenosis in the stapler-assisted nested anastomosis group was significantly lower than in the conventional anastomosis group. In the conventional anastomosis group, 4 patients exhibited anastomotic leakage, which acted as an independent factor in the formation of anastomotic stenosis (38-41). Inflammatory hyperplasia occurs during the recovery process of anastomotic leakage, and excessive scarring leads to anastomotic stenosis after healing. Although a study has indicated that anastomotic stenosis is related to gastroesophageal reflux, the reason for this relationship remains undetermined (42). Anastomotic edematous or cicatricial strictures may originate from chronic acidic or alkaline stimulation (43). Therefore, the reduction or prevention of anastomotic stenosis and gastroesophageal reflux are of critical concern.

The incidence of regurgitation in the stapler-assisted nested anastomosis group was significantly lower than in the conventional anastomosis group. This finding may have been due to the possibility that a structure similar to the gastric fundus formed around the anastomosis post surgically. The concurrent increased pressure over the esophageal anastomosis during reflux closes the esophageal cavity and prevents the reflux material from entering the esophagus (44), thereby reducing aspiration, reducing the incidence of aspiration pneumonia, and improving the quality of life of patients after surgery. Furthermore, a significantly lower incidence of postoperative pneumonia was observed in the nested anastomosis group than in the conventional anastomosis group, which also exhibited the antireflux characteristic that is characteristic of nested anastomosis. Our experiment adopted a tubular stomach diameter of 3 cm, which is similar to the artificial nipple insertion method (45). An overly long measurement affects the thoroughness of the resection, whereas an overly short measurement cannot achieve anastomotic decompression and antireflux effects. A significant difference in the incidence of stomatitis was not present in the data; although this indicates the anti-esophageal reflux characteristic of nested anastomosis, it also suggests an inability to reduce the erosion damage of the reflux fluid to the gastroesophageal anastomosis. The optimized design of the nested anastomosis process entails a simpler operation and a significantly shorter procedure relative to conventional anastomosis. The results of this study are roughly consistent with the expected results of our hypothesis, which verifies our hypothesis and further illustrates the advantages of this anastomosis method, which is suitable for application and promotion in the surgical treatment of EC.

Conclusions

In conclusion, in addition to being simple to implement, stapler-assisted nested anastomosis can effectively reduce the incidence of complications such as anastomotic leakage, anastomotic stenosis, reflux, and aspiration pneumonia compared with conventional anastomosis, and should thus be widely promoted.

Acknowledgments

Funding: This study was supported by the Gansu Provincial Youth Science and Technology Fund Program (Grant/Award Number: 18JR3RA305 & 21JR1RA107, to Ruijiang Lin); Natural Science Foundation of Gansu Province (Grant/Award Number: 21JR1RA092 & 21JR1RA118, to Biao Han).

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jgo.amegroups.com/article/view/10.21037/jgo-23-166/rc

Data Sharing Statement: Available at https://jgo.amegroups.com/article/view/10.21037/jgo-23-166/dss

Peer Review File: Available at https://jgo.amegroups.com/article/view/10.21037/jgo-23-166/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jgo.amegroups.com/article/view/10.21037/jgo-23-166/coif). RL reports funding support from the Gansu Provincial Youth Science and Technology Fund Program (Grant/Award Number: 18JR3RA305 & 21JR1RA107); BH reports funding support from the Natural Science Foundation of Gansu Province (Grant/Award Number: 21JR1RA092 & 21JR1RA118). 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. The research protocol of this clinical study was approved by the Medical Ethics Committee of The First Hospital of Lanzhou University (No. LDYYLL2022-475). The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). All patients provided written informed consent.

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/.

References

1. Wei WQ, Yang J, Zhang SW, et al. Analysis of the esophageal cancer mortality in 2004 - 2005 and its trends during last 30 years in China. Zhonghua Yu Fang Yi Xue Za Zhi 2010;44:398-402. [PubMed]
2. Li H, Yang S, Zhang Y, et al. Thoracic recurrent laryngeal lymph node metastases predict cervical node metastases and benefit from three-field dissection in selected patients with thoracic esophageal squamous cell carcinoma. J Surg Oncol 2012;105:548-52. [Crossref] [PubMed]
3. Li H, Li HQ. Progress in the epidemiology of esophageal cancer. Chinese Journal of Gastrointestinal Surgery 2009;12:96-7.
4. Meng F, Li Y, Ma H, et al. Comparison of outcomes of open and minimally invasive esophagectomy in 183 patients with cancer. J Thorac Dis 2014;6:1218-24. [PubMed]
5. Mao YS, He J, Gao SG, et al. Controversies in the surgical treatment for esophageal carcinoma and future investigation. Chin J Gastrointest Surg 2015;18:851-4. [PubMed]
6. Altorki N, Kent M, Ferrara C, et al. Three-field lymph node dissection for squamous cell and adenocarcinoma of the esophagus. Ann Surg 2002;236:177-83. [Crossref] [PubMed]
7. Wang F, Liu S, Wang J, et al. Comparison of the stapled suture with the manual suture in the application of minimally invasive esophagectomy. Zhonghua Wei Chang Wai Ke Za Zhi 2014;17:881-3. [PubMed]
8. Safranek PM, Cubitt J, Booth MI, et al. Review of open and minimal access approaches to oesophagectomy for cancer. Br J Surg 2010;97:1845-53. [Crossref] [PubMed]
9. Biere SS, Maas KW, Bonavina L, et al. Traditional invasive vs. minimally invasive esophagectomy: a multi-center, randomized trial (TIME-trial). BMC Surg 2011;11:2. [Crossref] [PubMed]
10. Kawakubo H, Takeuchi H, Kitagawa Y. Current status and future perspectives on minimally invasive esophagectomy. Korean J Thorac Cardiovasc Surg 2013;46:241-8. [Crossref] [PubMed]
11. Sun C, Shi WP, Shu YS, et al. Clinical application of tubular stomach in cervical esophageal reconstruction after esophagectomy for esophageal cancer . Chin J Clin Thorac Cardiovasc Surg 2012;19:148-50.
12. Ma MQ, Jiang HJ, Tang P, et al. Retrospective comparative study of preoperative complications and lymphadenectomy between thoraco-scopic esophagectomy and open procedure . Chin J Thorac Cardiovasc Surg 2015;31:260-3.
13. Lerut T, Coosemans W, Decker G, et al. Anastomotic complications after esophagectomy. Dig Surg 2002;19:92-8. [Crossref] [PubMed]
14. Atkins BZ, Shah AS, Hutcheson KA, et al. Reducing hospital morbidity and mortality following esophagectomy. Ann Thorac Surg 2004;78:1170-6; discussion 1170-6. [Crossref] [PubMed]
15. Jung MK, Schmidt T, Chon SH, et al. Current surgical treatment standards for esophageal and esophagogastric junction cancer. Ann N Y Acad Sci 2020;1482:77-84. [Crossref] [PubMed]
16. Morita M, Yoshida R, Ikeda K, et al. Advances in esophageal cancer surgery in Japan: an analysis of 1000 consecutive patients treated at a single institute. Surgery 2008;143:499-508. [Crossref] [PubMed]
17. Yang G, Chen JK, Wang XB, et al. A New Esophagogastric Anastomosis for McKeown Esophagectomy in Esophageal Cancer. Ann Thorac Surg 2022;113:e307-10. [Crossref] [PubMed]
18. Cheng L, Fu S, Liu J, et al. Modified layered hand-sewn cervical end-to-side anastomosis for minimally invasive McKeown esophagectomy. J Surg Oncol 2021;124:1031-9. [Crossref] [PubMed]
19. Expert committee on esophageal surgery of Chinese medical doctors association, Fang WT, Zhang X. Minimally invasive esophageal resection (minimally invasive esophagectomy, MIE) expert consensus. Chin J Thorac Cardiovasc Surg 2013;29:385-7.
20. Luketich JD, Pennathur A, Awais O, et al. Outcomes after minimally invasive esophagectomy: review of over 1000 patients. Ann Surg 2012;256:95-103. [Crossref] [PubMed]
21. Zingg U, Smithers BM, Gotley DC, et al. Factors associated with postoperative pulmonary morbidity after esophagectomy for cancer. Ann Surg Oncol 2011;18:1460-8. [Crossref] [PubMed]
22. Rajan PS, Vaithiswaran V, Rajapandian S, et al. Minimally invasive esophagectomy for carcinoma oesophagus- approaches and options in a high volume tertiary centre. J Indian Med Assoc 2010;108:642-4. [PubMed]
23. Zhang ZM, Wang Y, Gao YS, et al. Minimally invasive esophagectomy for esophageal carcinoma: clinical analysis of 160 cases. Chin J Gastrointest Surg 2012;15:934-7. [PubMed]
24. Lin JB, Kang MQ, Lin RB, et al. Thoracolaparoscopic esophagectomy with two-field lymph node dissection for esophageal carcinoma: report of 150 cases. Chin J Gastrointest Surg 2012;15:930-3. [PubMed]
25. Xie X, Fu JH, Wang JY, et al. Analysis of learning process of video-assisted minimally invasive esophagectomy for thoracic esophageal carcinoma. Chin J Gastrointest Surg 2012;15:918-21. [PubMed]
26. Wang H, Tan LJ, Li JP, et al. Evaluation of safety of video- assisted thoracoscopic esophagectomy for esophageal carcinoma. Chin J Gastrointest Surg 2012;15:926-9. [PubMed]
27. Lai Y, Zeng X, Zhou K, et al. End to end intussusception anastomosis decreases the risk of anastomotic leakage after neoadjvant chemoradiation and McKeown oesophagectomy. Radiother Oncol 2021;158:285-92. [Crossref] [PubMed]
28. Liu YZ, Cheng ZQ, Han WZ, et al. Clinical study on cervical esophagogastric anastomosis. Medical Journal of Chinese People's Health 2005;17:575-6.
29. Oshikiri T, Takiguchi G, Miura S, et al. Non-placement versus placement of a drainage tube around the cervical anastomosis in McKeown esophagectomy: study protocol for a randomized controlled trial. Trials 2019;20:758. [Crossref] [PubMed]
30. Michelet P, Djourno XB, Roch A, et al. Perioperative risk factors for anastomotic leakage after esophagectomy. Chest 2005;128:3461-6. [Crossref] [PubMed]
31. Tu DH, Qu R, Ping W, et al. Anastomosis oversewing technique to prevent leakage after oesophagectomy: a propensity score-matched analysis. Eur J Cardiothorac Surg 2022;61:990-8. [Crossref] [PubMed]
32. Qin YY, Ding XQ, Liu GZ, et al. The anti-reflux function of rebuilding His angle through artificially folding gastric fundus—a clinical study of 102 cases with esophagogastric junction cancer radical operation. Chin J Surg Oncol 2009;1:340-2.
33. Gao C, Xu G, Wang C, et al. Evaluation of preoperative risk factors and postoperative indicators for anastomotic leak of minimally invasive McKeown esophagectomy: a single-center retrospective analysis. J Cardiothorac Surg 2019;14:46. [Crossref] [PubMed]
34. Alverdy JC, Hyoju SK, Weigerinck M, et al. The gut microbiome and the mechanism of surgical infection. Br J Surg 2017;104:e14-e23. [Crossref] [PubMed]
35. Luo J, Zhuo ZG, Zhu YK, et al. Fixed in the neck or pushed back into the thorax?-Impact of cervical anastomosis position on anastomosis healing. J Thorac Dis 2020;12:2153-60. [Crossref] [PubMed]
36. Amaris M, Dua KS, Naini SR, et al. Characterization of the upper esophageal sphincter response during cough. Chest 2012;142:1229-36. [Crossref] [PubMed]
37. Cheng ZX, Li JS, Wang JJ, et al. Causes and diagnosis of delayed anastomotic fistula after resection of esophageal carcinoma. J Clin Surg 2014;22:458-9.
38. Sutcliffe RP, Forshaw MJ, Tandon R, et al. Anastomotic strictures and delayed gastric emptying after esophagectomy: incidence, risk factors and management. Dis Esophagus 2008;21:712-7. [Crossref] [PubMed]
39. Yoshida N, Eto K, Matsumoto T, et al. Omental Flap Wrapping Around the Esophagogastric Anastomosis and Association with Anastomotic Leak in Esophagectomy for Esophageal Cancer: A Propensity Score-Matching Analysis. J Am Coll Surg 2023;236:189-97. [Crossref] [PubMed]
40. van Heijl M, Gooszen JA, Fockens P, et al. Risk factors for development of benign cervical strictures after esophagectomy. Ann Surg 2010;251:1064-9. [Crossref] [PubMed]
41. Cao BX, Ren GG, Xiao B, et al. Causes of anastomotic stenosis after resection of esophageal carcinoma. Chin J Thorac Cardiovasc Surg 2013;29:138-9.
42. Orringer MB, Marshall B, Stirling MC. Transhiatal esophagectomy for benign and malignant disease. J Thorac Cardiovasc Surg 1993;105:265-76; discussion 276-7. [Crossref] [PubMed]
43. Fu MY, Huang T, Ren Q, et al. The relationship between charac-teristics of gastroesophageal reflux symptoms and related factors after gastroesophageal anastomosis. Chin J Clin Thorac Cardiovasc Surg 2007;14:476-7.
44. Mao CY, Yang YS, Yuan Y, et al. End-to-End Versus End-to-Side Hand-Sewn Anastomosis for Minimally Invasive McKeown Esophagectomy. Ann Surg Oncol 2019;26:4062-9. [Crossref] [PubMed]
45. Wang P, Zhang D, Lin X, et al. Purse-indigitation mechanical anastomosis vs. traditional mechanical anastomosis undergoing McKeown esophagectomy: a retrospective comparative cohort study. Ann Transl Med 2022;10:903. [Crossref] [PubMed]

(English Language Editor: J. Jones)