Abstract
Background
Laparoscopy-assisted gastrectomy (LAG) has been indicated to be safe, feasible, and oncologically efficacious for the treatment of early gastric cancer by both retrospective and prospective studies. Although some reports have demonstrated that LAG was also a safe and technically feasible procedure for advanced gastric cancer (AGC), its oncologic outcomes have not yet been confirmed in a multicenter, large-scale study. The aim of this study was to evaluate the oncologic outcomes of LAG for AGC on a multicenter basis in China.
Methods
Data of 1,184 consecutive patients with locally AGC who underwent LAG with curative intent between February 2003 and December 2009 were collected from the Chinese Laparoscopic Gastrointestinal Surgery Study group database and retrospectively analyzed. Survival rates were estimated by the Kaplan–Meier method. Risk factors for recurrence and survival were evaluated by Cox regression models.
Results
Postoperatively, 121 patients (10.2 %) experienced complications, and 1 patient died (0.1 %). Median follow-up was 12 months. Recurrence was observed in 185 patients (16.7 %), including hematogenous (31 patients), peritoneal (52), locoregional (25), distant lymph node (LN) (8), mixed (63), and uncertain (6) recurrences. The cumulative 3-year overall survival and disease-free survival rates were 75.3 and 69.0 %, respectively. The 3-year overall survival and disease-free survival rates were 89.7 and 88.9 % for stage I tumors, 85.0 and 77.0 % for stage II, 60.5 and 59.3 % for stage III. Independent risk factors for recurrence were tumor size > 40 mm, intraoperative blood transfusion, and advanced tumor stage. For survival, age > 65 years, tumor size > 40 mm, and advanced tumor stage were independent risk factors.
Conclusions
In addition to being safe and technically feasible, LAG for locally AGC could also yield acceptable short-term oncologic outcomes.
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References
Kitano S, Iso Y, Moriyama M, Sugimachi K (1994) Laparoscopy-assisted Billroth I gastrectomy. Surg Laparosc Endosc 4:146–148
Pak KH, Hyung WJ, Son T, Obama K, Woo Y, Kim HI, An JY, Kim JW, Cheong JH, Choi SH, Noh SH (2012) Long-term oncologic outcomes of 714 consecutive laparoscopic gastrectomies for gastric cancer: results from the 7-year experience of a single institute. Surg Endosc 26:130–136
Kitano S, Shiraishi N, Uyama I, Sugihara K, Tanigawa N (2007) A multicenter study on oncologic outcome of laparoscopic gastrectomy for early cancer in Japan. Ann Surg 245:68–72
Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61:69–90
Han HS, Kim YW, Yi NJ, Fleischer GD (2003) Laparoscopy-assisted D2 subtotal gastrectomy in early gastric cancer. Surg Laparosc Endosc Percutan Tech 13:361–365
Kim MC, Kim KH, Kim HH, Jung GJ (2005) Comparison of laparoscopy-assisted by conventional open distal gastrectomy and extraperigastric lymph node dissection in early gastric cancer. J Surg Oncol 91:90–94
Vinuela EF, Gonen M, Brennan MF, Coit DG, Strong VE (2012) Laparoscopic versus open distal gastrectomy for gastric cancer: a meta-analysis of randomized controlled trials and high-quality nonrandomized studies. Ann Surg 255:446–456
Liang Y, Li G, Chen P, Yu J, Zhang C (2011) Laparoscopic versus open gastrectomy for early distal gastric cancer: a meta-analysis. ANZ J Surg 81:673–680
Kim YW, Baik YH, Yun YH, Nam BH, Kim DH, Choi IJ, Bae JM (2008) Improved quality of life outcomes after laparoscopy-assisted distal gastrectomy for early gastric cancer: results of a prospective randomized clinical trial. Ann Surg 248:721–727
Huscher CG, Mingoli A, Sgarzini G, Sansonetti A, Di Paola M, Recher A, Ponzano C (2005) Laparoscopic versus open subtotal gastrectomy for distal gastric cancer: five-year results of a randomized prospective trial. Ann Surg 241:232–237
Hur H, Jeon HM, Kim W (2008) Laparoscopy-assisted distal gastrectomy with D2 lymphadenectomy for T2b advanced gastric cancers: three years’ experience. J Surg Oncol 98:515–519
Hwang SI, Kim HO, Yoo CH, Shin JH, Son BH (2009) Laparoscopic-assisted distal gastrectomy versus open distal gastrectomy for advanced gastric cancer. Surg Endosc 23:1252–1258
do Park J, Han SU, Hyung WJ, Kim MC, Kim W, Ryu SY, Ryu SW, Song KY, Lee HJ, Cho GS, Kim HH (2012) Long-term outcomes after laparoscopy-assisted gastrectomy for advanced gastric cancer: a large-scale multicenter retrospective study. Surg Endosc 26:1548–1553
Li ZJJ (2013) Laparoscopic D2 dissection for locally advanced gastric cancer in China. Transl Gastrointest Cancer 2:100–101
Hu YF, Yu J, Zhang C, Wang YN, Cheng X, Huang F, Li GX (2010) Development and implementation of a clinical data mining system for gastric cancer surgery. Zhonghua Wei Chang Wai Ke Za Zhi 13:510–515
Li GX, Zhang C, Yu J, Wang YN, Hu YF (2010) A new order of D2 lymphadenectomy in laparoscopic gastrectomy for cancer: live anatomy-based dissection. Minim Invasive Ther Allied Technol 19:355–363
Nakajima T (2002) Gastric cancer treatment guidelines in Japan. Gastric Cancer 5:1–5
Japanese Gastric Cancer A (1998) Japanese classification of gastric carcinoma—2nd English edition. Gastric Cancer 1:10–24
Strasberg SM, Linehan DC, Hawkins WG (2009) The accordion severity grading system of surgical complications. Ann Surg 250:177–186
Cai J, Wei D, Gao CF, Zhang CS, Zhang H, Zhao T (2011) A prospective randomized study comparing open versus laparoscopy-assisted D2 radical gastrectomy in advanced gastric cancer. Dig Surg 28:331–337
Shinohara T, Satoh S, Kanaya S, Ishida Y, Taniguchi K, Isogaki J, Inaba K, Yanaga K, Uyama I (2013) Laparoscopic versus open D2 gastrectomy for advanced gastric cancer: a retrospective cohort study. Surg Endosc 27:286–294
Washington K (2010) 7th edition of the AJCC cancer staging manual: stomach. Ann Surg Oncol 17:3077–3079
Park CH, Song KY, Kim SN (2008) Treatment results for gastric cancer surgery: 12 years’ experience at a single institute in Korea. Eur J Surg Oncol 34:36–41
Brundell SM, Tucker K, Texler M, Brown B, Chatterton B, Hewett PJ (2002) Variables in the spread of tumor cells to trocars and port sites during operative laparoscopy. Surg Endosc 16:1413–1419
Shen MY, Huang IP, Chen WS, Chang JT, Lin JK (2008) Influence of pneumoperitoneum on tumor growth and pattern of intra-abdominal tumor spreading: in vivo study of a murine model. Hepatogastroenterology 55:947–951
Jeong SH, Lee YJ, Park ST, Choi SK, Hong SC, Jung EJ, Joo YT, Jeong CY, Ha WS (2011) Risk of recurrence after laparoscopy-assisted radical gastrectomy for gastric cancer performed by a single surgeon. Surg Endosc 25:872–878
Park HA, Park SH, Cho SI, Jang YJ, Kim JH, Park SS, Mok YJ, Kim CS (2013) Impact of age and comorbidity on the short-term surgical outcome after laparoscopy-assisted distal gastrectomy for adenocarcinoma. Am Surg 79:40–48
Kim EJ, Seo KW, Yoon KY (2012) Laparoscopy-assisted distal gastrectomy for early gastric cancer in the elderly. J Gastric Cancer 12:232–236
Hyung WJ, Noh SH, Shin DW, Huh J, Huh BJ, Choi SH, Min JS (2002) Adverse effects of perioperative transfusion on patients with stage III and IV gastric cancer. Ann Surg Oncol 9:5–12
Ojima T, Iwahashi M, Nakamori M, Nakamura M, Naka T, Katsuda M, Iida T, Hayata K, Yamaue H (2009) Association of allogeneic blood transfusions and long-term survival of patients with gastric cancer after curative gastrectomy. J Gastrointest Surg 13:1821–1830
Wu HS, Little AG (1988) Perioperative blood transfusions and cancer recurrence. J Clin Oncol 6:1348–1354
Sun CF, Hsieh YY, Ngan KW, Wang WT (2001) Search for immunomodulatory effects of blood transfusion in gastric cancer patients: flow cytometry of Th1/Th2 cells in peripheral blood. Ann Clin Lab Sci 31:171–178
Strong VE, Devaud N, Allen PJ, Gonen M, Brennan MF, Coit D (2009) Laparoscopic versus open subtotal gastrectomy for adenocarcinoma: a case-control study. Ann Surg Oncol 16:1507–1513
Lee JH, Ahn SH, do Park J, Kim HH, Lee HJ, Yang HK (2012) Laparoscopic total gastrectomy with D2 lymphadenectomy for advanced gastric cancer. World J Surg 36:2394–2399
Noshiro H, Nagai E, Shimizu S, Uchiyama A, Tanaka M (2005) Laparoscopically assisted distal gastrectomy with standard radical lymph node dissection for gastric cancer. Surg Endosc 19:1592–1596
Bonenkamp JJ, Hermans J, Sasako M, van de Velde CJ, Welvaart K, Songun I, Meyer S, Plukker JT, Van Elk P, Obertop H, Gouma DJ, van Lanschot JJ, Taat CW, de Graaf PW, von Meyenfeldt MF, Tilanus H (1999) Extended lymph-node dissection for gastric cancer. N Engl J Med 340:908–914
Ikeguchi M, Kaibara N (2004) Lymph node metastasis at the splenic hilum in proximal gastric cancer. Am Surg 70:645–648
Monig SP, Collet PH, Baldus SE, Schmackpfeffer K, Schroder W, Thiele J, Dienes HP, Holscher AH (2001) Splenectomy in proximal gastric cancer: frequency of lymph node metastasis to the splenic hilus. J Surg Oncol 76:89–92
Kosuga T, Ichikawa D, Okamoto K, Komatsu S, Shiozaki A, Fujiwara H, Otsuji E (2011) Survival benefits from splenic hilar lymph node dissection by splenectomy in gastric cancer patients: relative comparison of the benefits in subgroups of patients. Gastric Cancer 14:172–177
Shin SH, Jung H, Choi SH, An JY, Choi MG, Noh JH, Sohn TS, Bae JM, Kim S (2009) Clinical significance of splenic hilar lymph node metastasis in proximal gastric cancer. Ann Surg Oncol 16:1304–1309
De Manzoni G, Verlato G, Roviello F, Di Leo A, Marrelli D, Morgagni P, Pasini F, Saragoni L, Tomezzoli A (2003) Subtotal versus total gastrectomy for T3 adenocarcinoma of the antrum. Gastric Cancer 6:237–242
Acknowledgments
The study was supported by the National High Technology Research and Development Program of China (863 Program) issued by the Ministry of Science and Technology of China (2012AA021103); the Development Center for Medical Science and Technology, Ministry of Health of China (W2011WAI44); the Research Fund of Public welfare in Health Industry, Health Ministry of China (No. 201402015); and Guangdong Provincial Science and Technology Key Project (2012A030400012).
The authors are grateful to the Chinese Laparoscopic and Endoscopic Surgery Society, the Chinese Gastric Cancer Association, and Ethicon Endo-Surgery of Johnson & Johnson Medical (China) Ltd. for their support in establishing the CLASS group and nationwide database.
We also acknowledge the following contributors to the CLASS group: Zhongchen Liu, Department of Gastrointestinal Surgery, Zhongshan Hospital, Xiamen University (Xiamen); Ziwei Wang, Department of General Surgery, the First Affiliated Hospital of Chongqing Medical University (Chongqing); Dong Wei, Department of Anorectal Surgery, the 150th Center Hospital of PLA (Luoyang); Mingsheng Sun, Department of General Surgery, the First Hospital of Nanchang (Nanchang); Zonghai Huang, Department of General Surgery, Zhujiang Hospital, Southern Medical University (Guangzhou); Zhigang Jie, Department of General Surgery, the First Affiliated Hospital of Nanchang University (Nanchang); Zhenxiang Rong, Department of General Surgery, the First People’s Hospital of Shunde (Shunde); Yihong Sun, Department of General Surgery, Zhongshan Hospital, Fudan University (Shanghai); Kai Pan, Department of Gastrointestinal Surgery, Shenzhen People’s Hospital (Shenzhen); Shunrong Huang, Department of Gastrointestinal Surgery, the People’s Hospital of Guangxi Zhuang Autonomous Region (Nanning); Ziyu Li, Department of Gastrointestinal Surgery, Beijing Cancer Hospital, Peking University (Beijing); Kaixiong Tao, Department of Laparoscopic Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology (Wuhan); Chuyuan Hong, Department of Gastrointestinal Surgery, the Second Affiliated Hospital of Guangzhou Medical University (Guangzhou); Enders Kwok-wai Ng, Department of Surgery, Prince of Wales Hospital, Chinese University of Hong Kong (Hong Kong).
Disclosures
Drs. Yanfeng Hu, Mingang Ying, Changming Huang, Hongbo Wei, Zhiwei Jiang, Xiang Peng, Jiankun Hu, Xiaohui Du, Baolin Wang, Feng Lin, Jian Xu, Guanglong Dong, Tingyu Mou, and Guoxin Li have no conflicts of interest or financial ties to disclose.
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The first two authors contributed equally to this article, and both should be considered first author. Tingyu Mou and Guoxin Li also contributed equally, and both should be considered as co-corresponding author.
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Hu, Y., Ying, M., Huang, C. et al. Oncologic outcomes of laparoscopy-assisted gastrectomy for advanced gastric cancer: a large-scale multicenter retrospective cohort study from China. Surg Endosc 28, 2048–2056 (2014). https://doi.org/10.1007/s00464-014-3426-9
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DOI: https://doi.org/10.1007/s00464-014-3426-9