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Annals of The Royal College of Surgeons of England logoLink to Annals of The Royal College of Surgeons of England
. 2010 Aug 30;93(1):17–21. doi: 10.1308/003588410X12771863936963

Safety and application of laparoscopic gastrectomy for benign gastric disease and gastric cancer

MK Zia 1, G Morris-Stiff 1, A Luhmann 1, R Jeffries 1, O Ehsan 1, A Hassn 1
PMCID: PMC3293264  PMID: 20810021

Abstract

INTRODUCTION

Laparoscopic gastrectomy is rapidly expanding despite reservations by some surgeons regarding its safety and radicality. The aim of this study was to evaluate patients undergoing laparoscopic gastrectomy for both benign and malignant disease with particular emphasis on technical feasibility, safety, effectiveness and complications.

PATIENTS AND METHODS

Review of prospectively collected data of patients who underwent laparoscopic gastrectomy from May 2005 to September 2009 under the care of one consultant surgeon.

RESULTS

A total of 61 laparoscopic gastrectomies were performed (35 men and 26 women) with a median age of 68 years (range, 41–90 years). There were 39 distal gastrectomies (19 adenocarcinoma, 6 gastrointestinal stromal tumour [GIST], 4 benign gastric outlet obstruction, 4 high-grade dysplasia in gastric adenomas, 4 non-healing ulcers, 2 gastric antral vascular ectasia [GAVE]); 15 sub-total gastrectomies (13 adenocarcinomas, 2 GIST); and 7 total gastrectomies (5 adenocarcinomas, 1 GIST, 1 carcinoid). Median follow-up was for 48 months (range, 1–72 months). There was one death, two major and six minor complications. All patients with complications made a satisfactory recovery.

CONCLUSIONS

Laparoscopic gastrectomy is associated with a low mortality (1.75%) and major morbidity (3.50%). Although technically demanding, especially when a D2 lymphadenectomy is performed, our results have shown that tailored laparoscopic resection based on tumour characteristics with either D1 or D2 lymphadenectomy results in good surgical and oncological outcomes.

Keywords: Laparoscopic gastrectomy, Benign gastric disease, Gastric cancer, Audit


Gastric surgery, as other surgical disciplines, aims to achieve resection of the primary lesion and its draining lymph nodes (in cancers), with minimum complications and the best possible quality of life. Traditionally, it has been performed by open access and there is a general consensus regarding the satisfactory oncological safety of this approach. The role of laparoscopic gastric surgery has not yet been completely defined and doubts still remain about its ability to satisfy all the oncological criteria met during conventional open surgery.1

Nevertheless, in the past decade, laparoscopic techniques have gained clinical acceptance as they offer significant advantages compared with open surgery: reduced surgical stress, less intra-operative blood loss, less postoperative pain and accelerated recovery, earlier return to normal bowel function with earlier resumption of oral intake, early discharge from hospital, and overall lower financial costs.2-5 The same advantages have been reported after laparoscopic subtotal or total gastrectomy for benign tumours as well as early gastric cancers.6-9

Laparoscopic-assisted distal gastrectomy has been applied to the treatment of gastric cancer and there are now several publications regarding the safety and feasibility of this approach.10,11 However, both laparoscopic-assisted distal gastrectomy and laparoscopic-assisted subtotal gastrectomy for distal gastric cancer can only be justified and widely accepted as a safe alternative to open surgery if equal long-term results are obtained. This would include an equivalent radical oncological resection to open surgery. In contrast to laparoscopic-assisted distal gastrectomy, there have been few reports on laparoscopic-assisted total gastrectomy compared with open total gastrectomy.11

The aim of the present study was to analyse the results of laparoscopic gastric surgery with intracorporeal anastomosis, for both benign and malignant conditions, performed in our institution by one laparoscopic oesophagogastric surgeon and thereby evaluate its feasibility, safety and complications.

Patients and Methods

All patients who underwent laparoscopic gastrectomy under the care of a single laparoscopic upper gastrointestinal surgeon were identified from a prospectively maintained database. Data collected included: patient demographics; ASA status; pTNM stage; tumour histology; number of retrieved lymph nodes; type of gastrointestinal anastomosis; peri-operative outcome including blood loss, resumption of diet, morbidity and mortality; and overall and disease-free survival. Laparoscopic resectional surgery for oesophagogastric benign and malignant disease was approved by local governance committee in the trust and all operations were audited in local and regional meetings. Also, an early series was presented at an AUGIS (Association of Upper Gastrointestinal Surgery) meeting in 2006. The learning curve was included in this series. In the early part of the series, cases were carefully selected, i.e. early tumours, distal resections and slim patients. As experience advanced, procedures included subtotal and total gastrectomies at all operable stages. In the last 2.5 years, laparoscopic gastrectomy was offered to all patients regardless of stage, site of lesion and body mass index status.

Surgical procedures consisted of total gastrectomy with a Roux-en-Y oesophagojejunostomy for proximal and middle gastric cancers, subtotal/distal gastrectomy with a Roux-en-Y gastrojejunostomy for distal gastric cancers and antral/prepyloric lesions. The port site placements are shown in Figure 1. The first part of duodenum was divided with 60 mm vascular stapler and all gastrojejunostomies were constructed side-to-side intracorporeally using 60 mm vascular cartilage. After anastomosis, the remaining stapler entry site in the bowel wall was closed with a single layer 3/0 vicryl intracorporeal continuous suture. For oesophagojejunostomy, an Orvil (Covidien) 25 mm stapling gun was used constructing an end-to-side anastomosis. In addition, a D2 en-bloc lymphadenectomy was performed for carcinomas and a D1 en-bloc lymphadenectomy for patients with severe dysplasia. For benign lesions, a tailored gastric resection was devised which would adequately excise the ulcer or tumour bearing area. All operations were performed laparoscopically with intracorporeal anastomosis and the specimen was extracted through the umbilical port in an Endo Catch.

Figure 1.

Figure 1

Configuration of port site placements.

Results

A total of 61 patients underwent laparoscopic gastrectomy during the study period between May 2005 and Sept 2009. There were 35 men and 26 women with a median age of 68 years (range, 41–90 years). The median follow-up was for 48 months (range, 1–72 months). The median ASA grade was 3 (range, 1–4).

The indications and the operations performed are summarised in Figure 2. Thirty-nine patients underwent distal gastrectomy, 15 sub-total gastrectomy and seven total gastrectomy. Fifty-nine gastrectomies were successfully completed laparoscopically and two were converted to open operation. Among these conversions, one was a very large GIST in the proximal stomach with the dissection hampered by a larger left lobe of liver, and the other was a total gastrectomy converted due to instrument failure.

Figure 2.

Figure 2

Type of operation and pathology.

The median operating time was 2 h 40 min (range, 1 h 20 min to 6 h) and the estimated median blood loss was 45 ml (range, 30–74 ml). One patient required transfusion for a postoperative haemorrhage. The median time to resumption of food intake was 3 days (range, 2–5 days) with a median length of hospital stay of 12 days (range, 2–29 days).

Histological examination revealed 38 cancers, 14 benign lesions and nine low-grade GISTs (Table 1). Among the cancers, 37 were adenocarcinomas and one carcinoid. All proximal and distal resection margins were clear; however, the circumferential resection margin (CRM) was involved in two patients with advanced cancer. D1 lymphadenectomy was performed in 15 patients for early stage gastric cancer and D2 lymphadenectomy in 23 patients for high-risk cancers. A median of 17 lymph nodes were retrieved (range, 8–46). The pTNM showed 14 stage I, 13 stage II, 11 stage III and no stage IV lesions. Two patients with advanced cancer who had involved CRM developed tumour recurrence during follow-up, one at 5 months and the other after 14 months.

Table 1.

Tumour characteristics

Location of lesion Oesophagogastric junction (n = 0);
upper third (n = 7);
middle third (n = 12);
lower third (n = 42)
Total cancers n = 38
D1 lymphadenectomy For early stage cancers (n = 15)
D2 lymphadenectomy For high-risk cancers (n = 23)
No of retrieved lymph nodes Median 17, range (8–46)
Tumour histology 37 adenocarcinoma; 1 carcinoid
Margins Clear except 2 patients with locally advanced but respectable disease
pTNM I (n = 14)
II (n = 13)
III (n = 11)
IV (n = 0)

Complications

There was one death and two patients developed major complications (Table 2). The patient who died suffered a myocardial infarct on the 8th postoperative day following a sub-total gastrectomy. Among the two patients with major complications, one suffered a duodenal stump blow out which was managed by open repair and the other had a postoperative haemorrhage which was managed by re-laparoscopy, drainage and blood transfusion. There were six minor complications. All patients developing complications made a satisfactory recovery.

Table 2.

Complications

Complication Number Outcome
Myocardial infarction 1 Died
Blow out of duodenal stump 1 Patient. survived after open repair
Postoperative haemorrhage 1 Patient survived after re-laparoscopy, drainage and blood transfusion
Peri-umbilical laparoscopic port site infection 2 Treated with antibiotics
Chest infection 1 Treated with antibiotics
Renal failure 1 Renal impairment present before surgery. Renal function returned to baseline following surgery
Ascites 1 Patient with alcoholic cirrhosis
Exacerbation of psychosis 1 Treated with antipsychotics

Discussion

Gastric cancer is the seventh most common cancer in the UK and has an incidence of about 8000 new cases per annum. Men are affected at least twice as often as women and gastric cancer remains among the top ten causes of cancer-related deaths in either sex.12

Most authorities agree that the treatment of operable distal gastric cancer is a radical resection of the distal four-fifths of the stomach with a tumour-free margin of at least 5 cm.13,14 The extent of draining lymph node dissection is still contentious. In Japan, where gastric cancer is six times more common than the West, an extended dissection with routine involvement of D2 and D3 lymph nodes is performed because of perceived improved long-term survival, despite the higher postoperative morbidity and mortality.15-18 In contrast, a more conservative lymphadenectomy (D1) is favoured in the West due to the higher complications associated with extended lymphadenectomy (D2, D3)19-22 and owing to a paucity of long-term survival data following extensive lymph node resections.23-25

Goh et al.26 are credited with the first laparoscopic-assisted distal gastrectomy in 1992. It was performed for a peptic ulcer with a Billroth II gastrojejunostomy reconstruction. The first laparoscopic gastrectomy for cancer was performed in 1992 by Kitano et al.27 Again, the reconstruction was performed by a Billroth II gastrojejunostomy. Following this, a number of publications have appeared reporting the important advantages of laparoscopic total, sub-total and distal gastrectomy.28-32

Goh et al.28 reported early follow-up results of laparoscopic distal gastrectomies in 1997. A questionnaire was sent to surgeons in 12 countries regarding a total of 118 laparoscopic distal gastrectomies. Out of 16 respondents, 10 felt laparoscopic distal gastrectomy to be superior to open distal gastrectomy in terms of duration of recovery, pain and cosmesis. Another interesting study in 1999 by Shirasihi et al.29 published a report of 40 laparoscopic-assisted gastrectomies for early gastric cancer. At a mean follow-up of 21 months, there was no morbidity, mortality or recurrence.

In 1999 and then 2000 Adachi et al.30,31 reported superior results of laparoscopic distal gastrectomy as compared with open distal gastrectomy with respect to weight loss, early dumping syndrome, heart burn, surgical trauma, return of gastrointestinal function and duration of hospital stay.

An interesting, prospective, randomised, controlled trial comparing laparoscopic and open gastrectomy for malignant disease was published in 2003 by Weber et al.32 They compared the 5-year results of a series of 12 gastric cancer patients treated by laparoscopic subtotal gastrectomy with 13 patients who underwent open gastrectomy and acted as controls. This study concluded that the laparoscopic approach did not compromise the oncological safety or the 5-year overall and disease-free survival rates.32

In 2002, Kitano et al.10 published interim results of a randomised controlled trial comparing open distal gastrectomy with laparoscopy-assisted distal gastrectomy for early gastric cancer. A total of 28 patients were included in the trial and the results showed an earlier recovery, reduced pain and less impairment of pulmonary function following laparoscopic-assisted distal gastrectomy.

In 2005, Huscher et al.1 reported the results of a prospective, randomised, controlled trial with a total of 59 patients comparing laparoscopic (n = 30) versus open (n = 29) subtotal gastrectomy for distal gastric cancer. There was no difference in the mean number of resected lymph nodes at 33.4 ± 17.4 in the open group and 30.0 ± 14.9 in the laparoscopic group. Operative mortality was non-significantly higher at 6.7% (2 patients) in the open group compared to 3.3% (1 patient) in the laparoscopic group. Morbidity rates were also comparable at 27.6% and 26.7% in the open and laparoscopic groups, respectively (not significant). They concluded that laparoscopic subtotal gastrectomy for distal gastric cancer is feasible and safe with short- and long-term results similar to those obtained with an open approach. In addition, the laparoscopic group had less blood loss, shorter time to resumption of oral intake, earlier discharge from hospital and similar 5-year overall and disease-free survival. More recently, several other authors have found similar benefits from laparoscopic gastrectomy compared with open surgery.33-40

Our results have shown both low mortality (1.75%) and major morbidity (3.50%) rates for laparoscopic gastrectomy. This compares favourably with published literature regarding complications from open gastrectomy. The time to resumption of food intake was also favourable (median, 2 days; range, 1–4 days) with a median length of postoperative hospital stay of 12 days (range, 2–29 days). In this series, most of the patients who stayed in hospital for longer than 8 days did so due to social reasons and, again, a 12-day postoperative median stay compared favourably with open surgery. In addition, all proximal and distal resection margins were clear and the CRM was involved in only two patients who were known to have advanced, albeit resectable, cancer. Unfortunately, these two patients developed recurrence. D1 lymphadenectomy was performed in 15 patients for early stage gastric cancer and D2 lymphadenectomy in 23 patients with high-risk cancers. An acceptable median of 17 lymph nodes were retrieved (range, 8–46). The pTNM showed 14 stage I, 13 stage II, 11 stage III and no stage IV lesion. Two patients had tumour recurrence – one 5 months after surgery and the other 14 months after.

Conclusions

Laparoscopic gastrectomy for both benign and malignant disease has similar short-term outcomes to conventional surgery that testify to the oncological safety and radicality of the procedure in addition to all the advantages of minimally invasive access. It has a low complication rate and it is safe and feasible in the hands of experienced surgeons.

These results would suggest that laparoscopic gastric resections can be performed for malignant disease; however, long-term follow-up studies are required to validate oncological outcomes in these patients.

References

  • 1.Huscher CGS, Mingoli A, Sgarzini G, Sansonetti A, Di Paola M, et al. Laparoscopic versus open subtotal gastrectomy for distal gastric cancer. Ann Surg. 2005;241:232–7. doi: 10.1097/01.sla.0000151892.35922.f2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Schulze S, Thorup J. Pulmonary function, pain and fatigue after laparoscopic cholecystectomy. Eur J Surg. 1993;159:361–4. [PubMed] [Google Scholar]
  • 3.Iwanaka T, Arkovitz MS, Arya G, Ziegler MM. Evaluation of operative stress and peritoneal macrophage function in minimally invasive operations. J Am Coll Surg. 1997;184:357–63. [PubMed] [Google Scholar]
  • 4.Carter JJ, Whelan RL. The immunologic consequences of laparoscopy in oncology. Surg Oncol Clin North Am. 2001;10:655–77. [PubMed] [Google Scholar]
  • 5.Gupta A, Watson DI. Effect of laparoscopy on immune function. Br J Surg. 2001;88:1296–306. doi: 10.1046/j.0007-1323.2001.01860.x. [DOI] [PubMed] [Google Scholar]
  • 6.Azagra JS, Goergen M, De Simone P, Ibanez-Aguirre J. Minimally invasive surgery for gastric cancer. Surg Endosc. 1999;13:351–7. doi: 10.1007/s004649900988. [DOI] [PubMed] [Google Scholar]
  • 7.Asao T, Hosouchi Y, Nakabayashi T, Haga N, Mochiki E, Kuwano H. Laparoscopically assisted total or distal gastrectomy with lymph node dissection for early gastric cancer. Br J Surg. 2001;88:128–32. doi: 10.1046/j.1365-2168.2001.01618.x. [DOI] [PubMed] [Google Scholar]
  • 8.Reyes CD, Weber KJ, Gagner M, Divino CM. Laparoscopic vs open gastrectomy. A retrospective review. Surg Endosc. 2001;15:928–31. doi: 10.1007/s004640080185. [DOI] [PubMed] [Google Scholar]
  • 9.Yano H, Monden T, Kinuta M, Nakano Y, Tono T, et al. The usefulness of laparoscopy-assisted distal gastrectomy in comparison with that of open distal gastrectomy for early gastric cancer. Gastric Cancer. 2001;4:93–7. doi: 10.1007/pl00011730. [DOI] [PubMed] [Google Scholar]
  • 10.Kitano S, Shiraishi N, Fujii K, Yasuda K, Inomata M, Adachi Y. A randomized controlled trial comparing open vs laparoscopy-assisted distal gastrectomy for the treatment of early gastric cancer: an interim report. Surgery. 2002;131:306–11. doi: 10.1067/msy.2002.120115. [DOI] [PubMed] [Google Scholar]
  • 11.Jeong GA, Cho GS, Kim HH, Lee HJ, Ryu SW, Song KY. Laparoscopic-assisted total gastrectomy for gastric cancer: a multicenter retrospective analysis. Surgery. 2009;146:469–74. doi: 10.1016/j.surg.2009.03.023. [DOI] [PubMed] [Google Scholar]
  • 12.Siewert JR, Sendler A. The current management of gastric cancer. Adv Surg. 1999;33:69–93. [PubMed] [Google Scholar]
  • 13.Cuschieri A. Gastrectomy for gastric cancer: definitions and objectives. Br J Surg. 1986;73:513–4. doi: 10.1002/bjs.1800730702. [DOI] [PubMed] [Google Scholar]
  • 14.Hioki K, Nakane Y, Yamamoto M. Surgical strategy for early gastric cancer. Br J Surg. 1990;77:1330–4. doi: 10.1002/bjs.1800771205. [DOI] [PubMed] [Google Scholar]
  • 15.Noguchi Y, Imada T, Matsumoto A, Coit DG, Brennan MF. Radical surgery for gastric cancer: a review of the Japanese experience. Cancer. 1989;64:2053–62. doi: 10.1002/1097-0142(19891115)64:10<2053::aid-cncr2820641014>3.0.co;2-j. [DOI] [PubMed] [Google Scholar]
  • 16.Maruyama K, Okabayashi K, Kinoshita T. Progress in gastric cancer surgery in Japan and its limits of radicality. World J Surg. 1987;11:418–25. doi: 10.1007/BF01655804. [DOI] [PubMed] [Google Scholar]
  • 17.Maruyama K, Gunven P, Okabayashi K, Sasako M, Kinoshita T. Lymph node metastases of gastric cancer: general pattern in 1931 patients. Ann Surg. 1989;210:596–602. doi: 10.1097/00000658-198911000-00005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Cuschieri A, Weeden S, Fielding J, Bancewicz J, Craven J, et al. Patient survival after D1 and D2 resections for gastric cancer: long-term results of the MRC randomized surgical trials. Br J Cancer. 1999;79:1522–30. doi: 10.1038/sj.bjc.6690243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Bunt AM, Hermans J, Smit VT, van de Velde CJ, Fleuren GJ, Bruijn JA. Surgical/pathologic stage migration confounds comparisons of gastric cancer survival rates between Japan and Western countries. J Clin Oncol. 1995;13:19–25. doi: 10.1200/JCO.1995.13.1.19. [DOI] [PubMed] [Google Scholar]
  • 20.Bonenkamp JJ, Songun I, Hermans J, van de Velde CJH, Hermans J, et al. Randomized comparison of morbidity after D1 and D2 dissection of gastric cancer in 996 Dutch patients. Lancet. 1995;345:745–8. doi: 10.1016/s0140-6736(95)90637-1. [DOI] [PubMed] [Google Scholar]
  • 21.Wanebo HJ, Kennedy BJ, Wichester DP, Stewart AK, Fremgen AM. Role of splenectomy in gastric cancer surgery: adverse effect of elective splenectomy on long-term survival. J Am Coll Surg. 1997;185:177–84. [PubMed] [Google Scholar]
  • 22.Bonenkamp JJ, Hermans J, Sasako M, van de Velde CJ, Welvaart K, et al. Extended lymph-node dissection for gastric cancer. N Engl J Med. 1999;340:908–14. doi: 10.1056/NEJM199903253401202. [DOI] [PubMed] [Google Scholar]
  • 23.Bonenkamp JJ, van de Velde CJ. Lymph node dissection in gastric cancer. Br J Surg. 1995;82:867–9. doi: 10.1002/bjs.1800820703. [DOI] [PubMed] [Google Scholar]
  • 24.Cuschieri A, Fayers P, Fielding J, Craven J, Bancewicz J, et al. Postoperative morbidity and mortality after D1 and D2 resections for gastric cancer: preliminary results of the MRC randomized controlled surgical trial. Lancet. 1996;347:995–9. doi: 10.1016/s0140-6736(96)90144-0. [DOI] [PubMed] [Google Scholar]
  • 25.Sasako M. Risk factors for surgical treatment in the Dutch Gastric Cancer trial. Br J Surg. 1997;84:1567–71. doi: 10.1111/j.1365-2168.1997.02842.x. [DOI] [PubMed] [Google Scholar]
  • 26.Goh P, Tekant Y, Kum CK, Isaac J, Shang NS. Totally intra-abdominal laparoscopic Billroth II gastrectomy. Surg Endosc. 1992;6:160. doi: 10.1007/BF02309093. [DOI] [PubMed] [Google Scholar]
  • 27.Kitano S, Iso Y, Moriyama M, Sugimachi K. Laparoscopy-assisted Billroth I gastrectomy. Surg Laparosc Endosc. 1994;4:146–8. [PubMed] [Google Scholar]
  • 28.Goh PM, Alponat A, Mak K, Kum CK. Early international results of laparoscopic gastrectomies. Surg Endosc. 1997;11:650–2. doi: 10.1007/s004649900413. [DOI] [PubMed] [Google Scholar]
  • 29.Shiraishi N, Adachi Y, Kitano S, Bandoh T, Katsuta T, Morimoto A. Indication for and outcome of laparoscopic-assisted Billroth I gastrectomy. Br J Surg. 1999;86:541–4. doi: 10.1046/j.1365-2168.1999.01083.x. [DOI] [PubMed] [Google Scholar]
  • 30.Adachi Y, Suematsu T, Shiraishi N, Katsuta T, Morimoto A, et al. Quality of life after laparoscopic-assisted Billroth I gastrectomy. Ann Surg. 1999;229:49–54. doi: 10.1097/00000658-199901000-00006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Adachi Y, Shiraishi N, Shiromizu A, Bandoh T, Aramaki M, Kitano S. Laparoscopy-assisted Billroth I gastrectomy compared with conventional open gastrectomy. Arch Surg. 2000;135:806–10. doi: 10.1001/archsurg.135.7.806. [DOI] [PubMed] [Google Scholar]
  • 32.Weber KJ, Reyes CD, Gagner M, Divino CM. Comparison of laparoscopic and open gastrectomy for malignant disease. Surg Endosc. 2003;17:968–71. doi: 10.1007/s00464-002-8738-5. [DOI] [PubMed] [Google Scholar]
  • 33.Kawamura H, Yokota R, Homma S, Kondo Y. Comparison of invasiveness between laparoscopic-assisted total gastrectomy and open total gastrectomy. World J Surg. 2009;33:2389–95. doi: 10.1007/s00268-009-0208-y. [DOI] [PubMed] [Google Scholar]
  • 34.Tinoco RC, Tinoco A C, El-Kadre LJ, Sueth DM, Conde LM. Laparoscopic gastrectomy for gastric cancer. Surg Laparosc Endosc Percutan Tech. 2009;19:384–7. doi: 10.1097/SLE.0b013e3181ba4701. [DOI] [PubMed] [Google Scholar]
  • 35.Cho GS, Kim W, Kim HH, Ryu SW, Kim MC, Ryu SY. Multicentre study of the safety of laparoscopic subtotal gastrectomy for gastric cancer in the elderly. Br J Surg. 2009;96:1437–42. doi: 10.1002/bjs.6777. [DOI] [PubMed] [Google Scholar]
  • 36.Sasaki A, Koeda K, Obuchi T, Nakajima J, Nishizuka S, et al. Tailored laparoscopic resection for suspected gastric gastrointestinal stromal tumors. Surgery. 2010 doi: 10.1016/j.surg.2009.10.035. Epub ahead of print. [DOI] [PubMed] [Google Scholar]
  • 37.Shinohara T, Kanaya S, Taniguchi K, Fujita T, Yanaga K, Uyama I. Laparoscopic total gastrectomy with D2 lymph node dissection for gastric cancer. Arch Surg. 2009;144:1138–42. doi: 10.1001/archsurg.2009.223. [DOI] [PubMed] [Google Scholar]
  • 38.Varela JE, Hiyashi M, Nguyen T, Sabio A, Wilson SE, Nguyen NT. Comparison of laparoscopic and open gastrectomy for gastric cancer. Am J Surg. 2006;192:837–42. doi: 10.1016/j.amjsurg.2006.08.054. [DOI] [PubMed] [Google Scholar]
  • 39.Kharbutli B, Velanovich V. Gastrointestinal symptomatic outcomes of laparoscopic and open gastrectomy. World J Gastrointest Surg. 2009;1:56–8. doi: 10.4240/wjgs.v1.i1.56. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Kim HH, Hyung WJ, Cho GS, Kim MC, Han SU, et al. Morbidity and mortality of laparoscopic gastrectomy versus open gastrectomy for gastric cancer: an interim report – a phase III multicenter, prospective, randomized Trial (KLASS Trial) Ann Surg. 2010;251:417–20. doi: 10.1097/SLA.0b013e3181cc8f6b. [DOI] [PubMed] [Google Scholar]

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