Specific complications related to the approach in minivasive gastric surgery and impact on survival: a narrative review

Introduction

Gastric cancer is one of the leading causes of death worldwide (1,2). Despite improvements in non-surgical procedures, radical gastrectomy surgery associated with lymphadenectomy is still a very important step in the treatment process (3).

Gastric surgery has always been fundamental to general surgery (4). That is why the concept of centralisation has only been developed and accepted in a few countries; consequently, many surgical centres (especially in Western countries) report less than 10 cases per year of radical gastrectomy. Historically, a significant morbidity-mortality rate encumbers this operation (5,6), second only to oesophageal surgery and above pancreatic and liver surgery, which are more frequently centralised.

For many years now, the field of gastric surgery has also embraced the introduction of minimally invasive surgery, thanks to a scientifically irrefutable demonstration of oncological non-inferiority in terms of the most commonly performed surgery: partial gastrectomy. Many experienced surgeons have crossed the barrier of total gastrectomy in daily practice, which has thus become a routine operation (7). However, this transition has also been accompanied by worsening short-term post-surgical outcomes compared to other sectors, such as colorectal surgery (8-12). The rationale of this review is analyzing the controversies and the complication caused by the introduction of the mininvasive technique, how those issues could affect the oncological outcome and how and which of those criticalities have been overcome in the last years. We present the following article in accordance with the Narrative Review reporting checklist (available at https://ales.amegroups.com/article/view/10.21037/ales-21-43/rc).

Methods

This narrative review analyses the critical surgical steps in radical gastrectomy and lymphadenectomy for cancer focusing on problems and complications introduced by the mini-invasive technique, describing the critical aspects and the strategies used to obtain the best oncological result.

A MEDLINE and PubMed research was performed using the terms “laparoscopic gastrectomy”, “gastric cancer” and “outcomes” from 1990 through July 2021; only articles in English were considered.

Discussion

The unstoppable avalanche: how the minimally invasive procedure has conquered gastric surgery.

When investigating complications in mininvasive gastric surgery two main limitations emerge: the lack of prospective controlled studies and the fact that surgical complications after gastric surgery are occasionally not recorded in a standardized fashion (13).

Minimally invasive surgery first entered into the field of gastrointestinal cancer surgery through colorectal surgery. In particular, due to the technical difficulty of performing a correct lymphadenectomy, gastric surgery has been the most difficult area to conquer. The first attempts of minimally invasive gastric cancer surgery date back to the 90’s (14), but these were sporadic reports by pioneering surgeons with particular expertise. Since 2010, minimally invasive stomach cancer surgery has been completely normalised following the publication of works by the Japanese (Japan Clinical Oncology Group) (15,16), the Korean group KLASS (Korean Laparoendoscopic Gastrointestinal Surgery Study) (17) and the Chinese group CLASS (Chinese Laparoscopic Gastrointestinal Surgery Study) (18). KLASS is a group of very well coordinated South Korean surgeons who, after a period of rigorously certified training via the re-evaluation of unedited videos by a centralised panel, collected scientifically solid data on post-surgical morbidity-mortality rates and the oncological surgery quality of distal gastrectomy, firstly in early gastric cancer (EGC) and then in advanced gastric cancer (AGC) (19). Data collection for total gastrectomy is still ongoing (19,20). The same work team has launched an interesting study on organ-sparing surgery in EGC. A few years later, prospective controlled and non-controlled studies on minimally invasive gastrectomy have also started in the West (21,22). A second powerful push for the development of minimally invasive gastric cancer surgery later came from the standardisation and dissemination of enhanced recovery after surgery (ERAS) protocols, which are also based on a minimally invasive approach. Thanks to solid data, distal gastrectomy for EGC is now a standard treatment, and many guidelines even include the possibility of treating advanced neoplasms with the minimally invasive technique. With that said, minimally invasive total gastrectomy is still considered experimental.

Problem number 1: esophagojejunal anastomosis

Until 2015, minimally invasive total gastrectomy with esophagojejunal anastomosis was the prerogative of only a few particularly skilled surgeons; from a scientific point of view, almost exclusively Oriental publications were recorded, all of which included retrospective analyses of individual cases (23). In the following years, a couple of prospective studies were released and then published in the last 2 years. We discuss at least four of such studies, respectively the Japanese, Korean, Chinese and Dutch ones (JCOG-1401, Klass03, Class02, Stomach trial). The percentage of anastomotic leak was less than 2% in the first 3 trials at Eastern centres and 8.5% in the Dutch trial; however, another Japanese study with results recorded in a national registry rather than in a prospective study like JCOG-1401 reports an anastomotic leak rate of 5.6% (24). Similarly, a Dutch study provides a snapshot of reality outside these prospective studies by reporting a leak percentage of as much as 17% (25).

The personal experience of many surgeons in real life shows a high complication rate for minimally invasive esophagojejunal anastomosis. The incidence of anastomotic leaks varies between 5–6% and 20–25%, with average values of around 10–15%. This percentage is significantly higher than historically accepted parameters for open surgery, which are around 5%. Many laparoscopic and robotic reconstruction techniques show that the ideal technical solution has not yet been identified. A meta-analysis (26) evaluates 9 comparison works, 3 of which are prospective of the totally minimally invasive technique and the laparoscopic-assisted technique, and no difference is reported. Another interesting literature review (27) analyses the different techniques of esophagojejunal anastomosis in 25 papers for 1,170 patients. It concludes that the functional end-to-end anastomosis (FETEA) and Overlap techniques have a lower complication rate (1.1% and 2.3%) than the single stapling technique (SST), double stapling technique (DST), hemi-double stapling technique (HDST), hand sewn (HS), which vary between 6% and 7%. However, only a few hundred cases are involved in each technique, which means that there are only a handful of complicated patients.

Another dehiscence: duodenal stump and its surroundings

Dehiscence of the duodenal stump after a total or partial gastrectomy is a rare, yet feared occurrence of gastrectomy. In fact, the duodenum is not a very mobile organ as it is retroperitoneal with a thick wall and receives a large amount of highly corrosive secretions, such as bile and pancreatic juice. The incidence of duodenal stump leakage is historically less than 2%. The minimally invasive approach to cancer gastrectomy is not a risk factor in itself, since the section and suture techniques are substantially similar to those commonly used in open surgery (28). The introduction of the minimally invasive approach has led to a greater use of linear tri-staplers, known for their improved technical features compared to classic linear staplers, which are more commonly used in open surgery due to their cost. At the same time, the minimally invasive procedure makes it more difficult to add manual reinforcement to the mechanical suture, a technique normally used by many surgeons in open surgery. Furthermore, there are some reports on the increased risk of pancreatitis from direct trauma caused by laparoscopic instruments to the pancreatic gland, which could result in a leakage of pancreatic enzymes, thus increasing the risk of enzymatic digestion of the duodenal suture (29). Other possible sources of biliary fistula during minimally invasive surgery include burns to the biliary tract during lymphadenectomy of the hepatic pedicle with Energy Devices or traumatic lesions to the posterior aspect of the pancreatic head during a Kocher manoeuvre, which is notoriously less comfortable with a minimally invasive approach than with open surgery (30). In any case, there is no available literature showing an increased risk of duodenal leak or biliary fistula associated with minimally invasive surgery (31).

The other leaks: once upon a time, there was a safe gastro-entero anastomosis

For many years, the gastro-jejunum anastomosis has been considered to have a low-risk for leaks. However, there was a higher incidence of leaks and stenosis in the initial phase of the minimally invasive experience than in the past (31). Nonetheless, more recent reports, influenced by increased experience and improved technique, return to report an extremely low risk of anastomotic complications.

The pancreas puzzle

At the moment, the trauma of the pancreatic gland is a topic with a debated and unclear literature (32). In fact, some early Eastern papers reported an increased number of acute post-surgical pancreatitis and “biochemical leaks” due to the evidence of an increased dosage of pancreatic enzymes in the post-surgical period (33). A possible explanation could be related to the pancreas body mobilisation during the lymphadenectomy of stations 8 and 11 (34); another possible explanation could be referred to the difficulty often encountered during the separation of the layers near the pancreatic head, the transverse mesocolon, the lymphatic tissue, the fat tissue near station 6, and the pancreatic capsule (35,36). However, some more recent series have disavowed this trend and, in some cases, even overturned it (37,38).

Some incredible (but true) things

Anecdotal cases describe complete transections of the hepatic and splenic arteries during lymphadenectomy with a minimally invasive technique, evidently linked to the safe use of Energy Devices. On the other hand, numerous case report of late pseudoaneurysms from heat injury (39,40). Cases of intestinal short circuit have also been described due to an error in the choice of the jejunal tract to be anastomosed to the stomach, especially in obese patients in whom the minimally invasive seeking of the Treitz angle can be difficult.

The unpleasant question of re-interventions: open vs. redo laparoscopy

After a surgery conducted with a minimally invasive technique, if the patient needs a re-operation for major complications, is it sensible to start the re-operation employing again a minimally invasive technique or, in principle, is it more appropriate to switch to an open technique? This question has no sure answer. Over time and with the accumulation of experience, more and more surgeons venture with a minimally invasive approach even in the case of re-surgery (41). Certainly, this attitude cannot be criticised a priori, especially where the problem can be easily recognized as well as solved, and the minimally invasive technique offers the patient fewer respiratory complications, fewer wound complications, and an adequate toilet of the peritoneal cavity.

Back to the past?

For a long time, using the Roux-en-Y technique with transmesocolic passage of the jejunal loop was considered ideal for the reconstruction of gastrointestinal continuity after subtotal gastrectomy. With the advent of minimally invasive gastrectomy, it was realized that the reconstruction with antecolic passage of the jejunal loop according to Billroth II represents an easier solution and bears fewer complications; this technique, formerly used for fast reconstructions in open surgery, is thus back in vogue (42-45). However, such technique is accompanied by an internal anastomosis to prevent biliary reflux (46). A newly introduced technique, the “uncut” technique, also provides the terminalisation of the loop without a section of the meso (47).

Long-term oncological results of complicated patients

As in other areas of gastrointestinal cancer surgery, post-surgical complications inevitably lead to the worsening of mean and long-term oncological results. This could be linked to relatively transient immunosuppression, but also to reduced or delayed accessibility to adjuvant therapies (48,49). On the contrary, in patients with a regular postoperative course, it is shown that the oncological results are ultimately comparable to those of open surgery (50).

Cui prodest? And who loses?

In reality, we must consider that the real goals of a surgically treated patient suffering from stomach cancer are a radical cure of the disease, as well as an intervention with no residual disease both on the tissue and in the lymph nodes. Whether these goals are achieved with an open or a minimally invasive technique, in the long term it does not matter, and even less for the specific needs of this type of patient than in other areas of abdominal pathology. To date, there are no certain demonstrations of the superiority of the minimally invasive approach compared to the open one on the truly relevant parameters, such as global survival and quality of life with particular reference to nutrition. Precisely because having a smaller incision is not the goal, it is not frequent among gastric cancer patients to specifically ask for a minimally invasive approach.

Do not forget: time and cost

Certainly, in the initial phase of the laparoscopic experience the minimally invasive intervention increases the operating times by at least 30%, and at the same time it certainly does not reduce the costs of the material. On the contrary, these costs are more frequently increased by the minimally invasive approach regarding the use of Energy Devices and the preparation of the anastomoses, which invariably happens by mechanical suturing machines and high-cost self-locking stitches (51). On the other hand, it is certainly true that in the context of an ERAS protocol, the minimally invasive approach allows a partial reduction in costs related to postoperative hospitalisation, as it is demonstrated that, in the absence of complications, on average it allows discharge one day earlier than an open intervention (52,53).

Despite the increase in experience, mininvasive gastric surgery remains burdened by a high rate of complications, especially when total gastrectomy is required (54).

Further studies are required to assess the length of the learning curve for minivasive gastrectomy, in order to understand when a surgeon is proficient in performing mininvasive gastric surgery without proctoring.

Conclusions

There is no doubt that the topic of gastric cancer surgery has also been fully conquered by minimally invasive surgery. To date, the only critical element remains the jejunal oesophagus anastomosis, while all the other technical steps have proven to be easily reproducible with the same results, without involving specific complications.

Acknowledgments

Funding: None.

Footnote

Provenance and Peer Review: This article was commissioned by the Guest Editors (Stefano Rausei and Simone Giacopuzzi) for the series “Minimally Invasive Surgery and Gastric Cancer: Where Are We Now?” published in Annals of Laparoscopic and Endoscopic Surgery. The article has undergone external peer review.

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://ales.amegroups.com/article/view/10.21037/ales-21-43/rc

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://ales.amegroups.com/article/view/10.21037/ales-21-43/coif). The series “Minimally Invasive Surgery and Gastric Cancer: Where Are We Now?” was commissioned by the editorial office without any funding or sponsorship. The authors have no other 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.

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. Ferlay J, Colombet M, Soerjomataram I, et al. Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int J Cancer 2019;144:1941-53. [Crossref] [PubMed]
2. Crew KD, Neugut AI. Epidemiology of gastric cancer. World J Gastroenterol 2006;12:354-62. [Crossref] [PubMed]
3. Terashima M. The 140 years' journey of gastric cancer surgery: From the two hands of Billroth to the multiple hands of the robot. Ann Gastroenterol Surg 2021;5:270-7. [Crossref] [PubMed]
4. Samrat R, Naimish M, Samiran N. Post-Gastrectomy Complications - An Overview. Chirurgia (Bucur) 2020;115:423-31. [Crossref] [PubMed]
5. Baiocchi GL, Giacopuzzi S, Marrelli D. Cutoff values of major surgical complications rates after gastrectomy. Updates Surg 2018;70:251-5. [Crossref] [PubMed]
6. Ritchie WP Jr, Perez AR. Postgastrectomy syndromes. In: Moody FG, Carey LC, Jones RS. et al, editors. Surgical treatment of digestive disease. Chicago: Year Book Medical Publishers; 1986:264-73.
7. Lianos GD, Hasemaki N, Glantzounis GK, et al. Assessing safety and feasibility of 'pure' laparoscopic total gastrectomy for advanced gastric cancer in the West. Review article. Int J Surg 2018;53:275-8. [Crossref] [PubMed]
8. Baiocchi GL, Giacopuzzi S, Reim D, et al. Incidence and Grading of Complications After Gastrectomy for Cancer Using the GASTRODATA Registry: A European Retrospective Observational Study. Ann Surg 2020;272:807-13. [Crossref] [PubMed]
9. Yoshida K, Honda M, Kumamaru H, et al. Surgical outcomes of laparoscopic distal gastrectomy compared to open distal gastrectomy: A retrospective cohort study based on a nationwide registry database in Japan. Ann Gastroenterol Surg 2017;2:55-64. [Crossref] [PubMed]
10. Etoh T, Honda M, Kumamaru H, et al. Morbidity and mortality from a propensity score-matched, prospective cohort study of laparoscopic versus open total gastrectomy for gastric cancer: data from a nationwide web-based database. Surg Endosc 2018;32:2766-73. [Crossref] [PubMed]
11. Shibasaki S, Suda K, Nakauchi M, et al. Non-robotic minimally invasive gastrectomy as an independent risk factor for postoperative intra-abdominal infectious complications: A single-center, retrospective and propensity score-matched analysis. World J Gastroenterol 2020;26:1172-84. [Crossref] [PubMed]
12. Kim MC, Choi HJ, Jung GJ, et al. Techniques and complications of laparoscopy-assisted distal gastrectomy (LADG) for gastric cancer. Eur J Surg Oncol 2007;33:700-5. [Crossref] [PubMed]
13. Baiocchi GL, Giacopuzzi S, Marrelli D, et al. International consensus on a complications list after gastrectomy for cancer. Gastric Cancer 2019;22:172-89. [Crossref] [PubMed]
14. Kitano S, Iso Y, Moriyama M, et al. Laparoscopy-assisted Billroth I gastrectomy. Surg Laparosc Endosc 1994;4:146-8. [PubMed]
15. Katai H, Sasako M, Fukuda H, et al. Safety and feasibility of laparoscopy-assisted distal gastrectomy with suprapancreatic nodal dissection for clinical stage I gastric cancer: a multicenter phase II trial (JCOG 0703). Gastric Cancer 2010;13:238-44. [Crossref] [PubMed]
16. Katai H, Mizusawa J, Katayama H, et al. Survival outcomes after laparoscopy-assisted distal gastrectomy versus open distal gastrectomy with nodal dissection for clinical stage IA or IB gastric cancer (JCOG0912): a multicentre, non-inferiority, phase 3 randomised controlled trial. Lancet Gastroenterol Hepatol 2020;5:142-51. [Crossref] [PubMed]
17. Kim HH, Han SU, Kim MC, et al. Effect of Laparoscopic Distal Gastrectomy vs Open Distal Gastrectomy on Long-term Survival Among Patients With Stage I Gastric Cancer: The KLASS-01 Randomized Clinical Trial. JAMA Oncol 2019;5:506-13. [Crossref] [PubMed]
18. Yu J, Huang C, Sun Y, et al. Effect of Laparoscopic vs Open Distal Gastrectomy on 3-Year Disease-Free Survival in Patients With Locally Advanced Gastric Cancer: The CLASS-01 Randomized Clinical Trial. JAMA 2019;321:1983-92. [Crossref] [PubMed]
19. Hyung WJ, Yang HK, Park YK, et al. Long-Term Outcomes of Laparoscopic Distal Gastrectomy for Locally Advanced Gastric Cancer: The KLASS-02-RCT Randomized Clinical Trial. J Clin Oncol. 2020;38:3304-13. [Crossref] [PubMed]
20. Katai H, Mizusawa J, Katayama H, et al. Single-arm confirmatory trial of laparoscopy-assisted total or proximal gastrectomy with nodal dissection for clinical stage I gastric cancer: Japan Clinical Oncology Group study JCOG1401. Gastric Cancer 2019;22:999-1008. [Crossref] [PubMed]
21. Haverkamp L, Brenkman HJ, Seesing MF, et al. Laparoscopic versus open gastrectomy for gastric cancer, a multicenter prospectively randomized controlled trial (LOGICA-trial). BMC Cancer 2015;15:556. [Crossref] [PubMed]
22. van der Wielen N, Straatman J, Daams F, et al. Open versus minimally invasive total gastrectomy after neoadjuvant chemotherapy: results of a European randomized trial. Gastric Cancer 2021;24:258-71. [Crossref] [PubMed]
23. Kunisaki C, Makino H, Takagawa R, et al. A systematic review of laparoscopic total gastrectomy for gastric cancer. Gastric Cancer 2015;18:218-26. [Crossref] [PubMed]
24. Kodera Y, Yoshida K, Kumamaru H, et al. Introducing laparoscopic total gastrectomy for gastric cancer in general practice: a retrospective cohort study based on a nationwide registry database in Japan. Gastric Cancer 2019;22:202-13. [Crossref] [PubMed]
25. Gertsen EC, Brenkman HJF, Seesing MFJ, et al. Introduction of minimally invasive surgery for distal and total gastrectomy: a population-based study. Eur J Surg Oncol 2019;45:403-9. [Crossref] [PubMed]
26. Liao GX, Xie GZ, Li R, et al. Meta-analysis of outcomes compared between robotic and laparoscopic gastrectomy for gastric cancer. Asian Pac J Cancer Prev 2013;14:4871-5. [Crossref] [PubMed]
27. Umemura A, Koeda K, Sasaki A, et al. Totally laparoscopic total gastrectomy for gastric cancer: literature review and comparison of the procedure of esophagojejunostomy. Asian J Surg 2015;38:102-12. [Crossref] [PubMed]
28. He H, Li H, Ye B, et al. Single Purse-String Suture for Reinforcement of Duodenal Stump During Laparoscopic Radical Gastrectomy for Gastric Cancer. Front Oncol 2019;9:1020. [Crossref] [PubMed]
29. Tang HN, Hu JH. A comparison of surgical procedures and postoperative cares for minimally invasive laparoscopic gastrectomy and open gastrectomy in gastric cancer. Int J Clin Exp Med 2015;8:10321-9. [PubMed]
30. Gu L, Zhang K, Shen Z, et al. Risk Factors for Duodenal Stump Leakage after Laparoscopic Gastrectomy for Gastric Cancer. J Gastric Cancer 2020;20:81-94. [Crossref] [PubMed]
31. Baiocchi GL, Giacopuzzi S, Marrelli D, et al. Complications after gastrectomy for cancer: Italian perspective. Updates Surg 2017;69:285-8. [Crossref] [PubMed]
32. Hiki N, Honda M, Etoh T, et al. Higher incidence of pancreatic fistula in laparoscopic gastrectomy. Real-world evidence from a nationwide prospective cohort study. Gastric Cancer 2018;21:162-70. [Crossref] [PubMed]
33. Sato Y, Inokuchi M, Otsuki S, et al. Risk Factor of Pancreatic Fistula after Radical Gastrectomy from the Viewpoint of Fatty Pancreas. Dig Surg 2017;34:455-61. [Crossref] [PubMed]
34. Guerra F, Giuliani G, Iacobone M, et al. Pancreas-related complications following gastrectomy: systematic review and meta-analysis of open versus minimally invasive surgery. Surg Endosc 2017;31:4346-56. [Crossref] [PubMed]
35. Migita K, Matsumoto S, Wakatsuki K, et al. The anatomical location of the pancreas is associated with the incidence of pancreatic fistula after laparoscopic gastrectomy. Surg Endosc 2016;30:5481-9. [Crossref] [PubMed]
36. Kobayashi N, Shinohara H, Haruta S, et al. Process of Pancreas Head as a Risk Factor for Postoperative Pancreatic Fistula in Laparoscopic Gastric Cancer Surgery. World J Surg 2016;40:2194-201. [Crossref] [PubMed]
37. Washio M, Yamashita K, Niihara M, et al. Postoperative pancreatic fistula after gastrectomy for gastric cancer. Ann Gastroenterol Surg 2020;4:618-27. [Crossref] [PubMed]
38. Tokunaga M, Tanizawa Y, Bando E, et al. Poor survival rate in patients with postoperative intra-abdominal infectious complications following curative gastrectomy for gastric cancer. Ann Surg Oncol 2013;20:1575-83. [Crossref] [PubMed]
39. Chen L, Ming X, Gu R, et al. Treatment experience of delayed massive gastrointestinal bleeding caused by intra-abdominal arteriointestinal fistula in gastric cancer patients after radical gastrectomy. World J Surg Oncol 2019;17:201. [Crossref] [PubMed]
40. Li Z, Jie Z, Liu Y, et al. Management of delayed hemorrhage following radical gastrectomy for gastric carcinoma patients. Hepatogastroenterology 2012;59:2016-9. [Crossref] [PubMed]
41. Chang KH, Bourke MG, Kavanagh DO, et al. A systematic review of the role of re-laparoscopy in the management of complications following laparoscopic colorectal surgery. Surgeon 2016;14:287-93. [Crossref] [PubMed]
42. Ma Y, Li F, Zhou X, et al. Four reconstruction methods after laparoscopic distal gastrectomy: A systematic review and network meta-analysis. Medicine (Baltimore) 2019;98:e18381. [Crossref] [PubMed]
43. Namikawa T, Kitagawa H, Okabayashi T, et al. Roux-en-Y reconstruction is superior to billroth I reconstruction in reducing reflux esophagitis after distal gastrectomy: special relationship with the angle of his. World J Surg 2010;34:1022-7. [Crossref] [PubMed]
44. Ishikawa M, Kitayama J, Kaizaki S, et al. Prospective randomized trial comparing Billroth I and Roux-en-Y procedures after distal gastrectomy for gastric carcinoma. World J Surg 2005;29:1415-20. [Crossref] [PubMed]
45. Fein M, Fuchs KH, Thalheimer A, et al. Long-term benefits of Roux-en-Y pouch reconstruction after total gastrectomy: a randomized trial. Ann Surg 2008;247:759-65. [Crossref] [PubMed]
46. Ren Z, Wang WX. Comparison of Billroth I, Billroth II, and Roux-en-Y Reconstruction After Totally Laparoscopic Distal Gastrectomy: A Randomized Controlled Study. Adv Ther 2019;36:2997-3006. [Crossref] [PubMed]
47. Yang L, Xu H, Zhang DC, et al. Uncut Roux-en-Y Reconstruction in a Laparoscopic Distal Gastrectomy: A Single-Center Study of 228 Consecutive Cases and Short-Term Outcomes. Surg Innov 2019;26:698-704. [Crossref] [PubMed]
48. Tokunaga M, Kondo J, Tanizawa Y, et al. Postoperative intra-abdominal complications assessed by the Clavien-Dindo classification following open and laparoscopy-assisted distal gastrectomy for early gastric cancer. J Gastrointest Surg 2012;16:1854-9. [Crossref] [PubMed]
49. Shimada H, Fukagawa T, Haga Y, et al. Does postoperative morbidity worsen the oncological outcome after radical surgery for gastrointestinal cancers? A systematic review of the literature. Ann Gastroenterol Surg 2017;1:11-23. [Crossref] [PubMed]
50. Kim KH, Kim MC, Jung GJ, et al. Comparative analysis of five-year survival results of laparoscopy-assisted gastrectomy versus open gastrectomy for advanced gastric cancer: a case-control study using a propensity score method. Dig Surg 2012;29:165-71. [Crossref] [PubMed]
51. Gosselin-Tardif A, Abou-Khalil M, Mata J, et al. Laparoscopic versus open subtotal gastrectomy for gastric adenocarcinoma: cost-effectiveness analysis. BJS Open 2020;4:830-9. [Crossref] [PubMed]
52. Li MZ, Wu WH, Li L, et al. Is ERAS effective and safe in laparoscopic gastrectomy for gastric carcinoma? A meta-analysis. World J Surg Oncol 2018;16:17. [Crossref] [PubMed]
53. Beamish AJ, Chan DS, Blake PA, et al. Systematic review and meta-analysis of enhanced recovery programmes in gastric cancer surgery. Int J Surg 2015;19:46-54. [Crossref] [PubMed]
54. Kostakis ID, Alexandrou A, Armeni E, et al. Comparison Between Minimally Invasive and Open Gastrectomy for Gastric Cancer in Europe: A Systematic Review and Meta-analysis. Scand J Surg 2017;106:3-20. [Crossref] [PubMed]