Significance of “Four-Step Procedure” of laparoscopic exploration in diagnosis of peritoneal metastasis of gastric cancer_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

YAN Menghua , CHEN Xiaolong , ZHANG Weihan , YANG Kun , CHEN Xinzu , LIU Kai , ZHAO Linyong ,  HU Jiankun

Department of Gastrointestinal Surgery/Laboratory of Gastric Cancer, West China Hospital of Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

HU Jiankun, Email: hujkwch@126.com

Keywords：

gastric cancer; Four-Step Procedure; laparoscopic exploration; peritoneal metastasis; abdominal exfoliative cytology; staging

DOI：

10.7507/1007-9424.202102041

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Objective To explore the diagnostic value of “Four-Step Procedure” of laparoscopic exploration in patients with peritoneal metastasis of gastric cancer.Methods We retrospectively collected the data of 409 gastric adenocarcinoma patients from July 2016 to August 2020 who underwent “Four-Step Procedure” of laparoscopic exploration in West China Hospital. The descriptive case series study was conducted to analyze the outcome of laparoscopic exploration combined with CY (cytology test), stepwise treatment plans, and the rates of CY1 and P1 (peritoneal metastasis) among cT3–4 patients during different periods. SPSS 22.0 software was used to conduct the univariate and multivariate logistic regression to analyze the high risk factors associated with P1 and (or) CY1.Results A total of 409 gastric adenocarcinoma patients who underwent laparoscopic exploration were enrolled in our study. Among them, 65 patients were confirmed to be P1 and (or) CY1. Stratified analysis by cT and cN staging showed that there were 7 (7.4%) and 55 (27.9%) patients with peritoneal metastasis in cT3 staging and cT4 staging, respectively. After laparoscopic exploration, 168 patients received laparoscopic gastrectomy, 35 patients received laparotomy, 143 patients received neo-adjuvant chemotherapy, and 63 patients received conversion therapy. The bar chart showed an ascending tendency in the diagnosis rate of P1 over time among cT3–4 patients. Multivariate logistic regression analysis showed that ascites was an independent risk factor of CY1 and (or) P1 (P<0.001). Additionally, the postoperative complication rate was 2.9% in the patients who merely underwent laparoscopic exploration, including 4 patients with pulmonary infection and 2 patients with urinary retention.Conclusions “Four-Step Procedure” of laparoscopic exploration is reliable and feasible for gastric cancer. “Four-Step Procedure” of laparoscopic exploration has high diagnostic value for peritoneal metastasis of gastric cancer. Our study shows that most of peritoneal metastasis distribute in cT3 and cT4 patients. For these patients, laparoscopic exploration should be recommended to identify if peritoneal metastasis exists and avoid unnecessary laparotomy.

Citation： YAN Menghua, CHEN Xiaolong, ZHANG Weihan, YANG Kun, CHEN Xinzu, LIU Kai, ZHAO Linyong, HU Jiankun. Significance of “Four-Step Procedure” of laparoscopic exploration in diagnosis of peritoneal metastasis of gastric cancer. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2021, 28(5): 580-586. doi: 10.7507/1007-9424.202102041 Copy

1.	Chen W, Sun K, Zheng R, et al. Cancer incidence and mortality in China, 2014. Chin J Cancer Res, 2018, 30(1): 1-12.
2.	Nashimoto A, Akazawa K, Isobe Y, et al. Gastric cancer treated in 2002 in Japan: 2009 annual report of the JGCA nationwide registry. Gastric Cancer, 2013, 16(1): 1-27.
3.	Rau B, Brandl A, Piso P, et al. Peritoneal metastasis in gastric cancer: results from the German database. Gastric Cancer, 2020, 23(1): 11-22.
4.	Mirza A, Galloway S. Laparoscopy, computerised tomography and fluorodeoxyglucose positron emission tomography in the management of gastric and gastro-oesophageal junction cancers. Surg Endosc, 2016, 30(7): 2690-2696.
5.	丁平安, 刘洋, 郭洪海, 等. 腹腔镜探查联合腹腔脱落细胞学检查在局部进展期胃癌诊治中的应用. 中华胃肠外科杂志, 2020, 23(2): 170-176.
6.	Liu K, Chen XZ, Zhang WH, et al. “Four-Step Procedure” of laparoscopic exploration for gastric cancer in West China Hospital: a retrospective observational analysis from a high-volume institution in China. Surg Endosc, 2019, 33(5): 1674-1682.
7.	陈心足, 刘凯, 张维汉, 等. 胃癌腹腔镜探查. 中华胃肠外科杂志, 2018, 21(5): 497.
8.	Fukuya T, Honda H, Hayashi T, et al. Lymph-node metastases: efficacy for detection with helical CT in patients with gastric cancer. Radiology, 1995, 197(3): 705-711.
9.	Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer, 2011, 14(2): 101-112.
10.	Sano T, Coit DG, Kim HH, et al. Proposal of a new stage grouping of gastric cancer for TNM classification: International Gastric Cancer Association staging project. Gastric Cancer, 2017, 20(2): 217-225.
11.	Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2014(ver. 4). Gastric Cancer, 2017, 20(1): 1-19.
12.	邱海波, 周志伟. NCCN胃癌临床实践指南2017年第五版更新要点解读. 中华胃肠外科杂志, 2018, 21(2): 160-164.
13.	Irino T, Sano T, Hiki N, et al. Diagnostic staging laparoscopy in gastric cancer: a prospective cohort at a cancer institute in Japan. Surg Endosc, 2018, 32(1): 268-275.
14.	Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2018 (5th edition). Gastric Cancer, 2021, 24(1): 1-21.
15.	Cunningham D, Allum WH, Stenning SP, et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med, 2006, 355(1): 11-20.
16.	Yamamoto M, Rashid OM, Wong J. Surgical management of gastric cancer: the East vs. West perspective. J Gastrointest Oncol, 2015, 6(1): 79-88.
17.	Karanicolas PJ, Elkin EB, Jacks LM, et al. Staging laparoscopy in the management of gastric cancer: a population-based analysis. J Am Coll Surg, 2011, 213(5): 644-651.
18.	Miki Y, Tokunaga M, Tanizawa Y, et al. Staging laparoscopy for patients with cM0, type 4, and large type 3 gastric cancer. World J Surg, 2015, 39(11): 2742-2747.
19.	Ramos RF, Scalon FM, Scalon MM, et al. Staging laparoscopy in gastric cancer to detect peritoneal metastases: A systematic review and meta-analysis. Eur J Surg Oncol, 2016, 42(9): 1315-1321.
20.	Bentrem D, Wilton A, Mazumdar M, et al. The value of peritoneal cytology as a preoperative predictor in patients with gastric carcinoma undergoing a curative resection. Ann Surg Oncol, 2005, 12(5): 347-353.
21.	Ribeiro U, Safatle-Ribeiro AV, Zilberstein B, et al. Does the intraoperative peritoneal lavage cytology add prognostic information in patients with potentially curative gastric resection? J Gastrointest Surg, 2006, 10(2): 170-176.
22.	Wang YD, Wu P, Mao JD, et al. Relationship between vascular invasion and microvessel density and micrometastasis. World J Gastroenterol, 2007, 13(46): 6269-6273.
23.	Ru Y, Zhang L, Chen Q, et al. Detection and clinical significance of lymph node micrometastasis in gastric cardia adenocarcinoma. J Int Med Res, 2012, 40(1): 293-299.
24.	Hori Y; SAGES Guidelines Committee. Diagnostic laparoscopy guidelines: This guideline was prepared by the SAGES Guidelines Committee and reviewed and approved by the Board of Governors of the Society of American Gastrointestinal and Endoscopic Surgeons (SAGES), November 2007. Surg Endosc, 2008, 22(5): 1353-1383.
25.	Burke EC, Karpeh MS, Conlon KC, et al. Laparoscopy in the management of gastric adenocarcinoma. Ann Surg, 1997, 225(3): 262-267.
26.	Santa-Maria AF, Valadão M, Iglesias AC. The role of staging laparoscopy in treatment of locally advanced gastric cancer. Surg Laparosc Endosc Percutan Tech, 2014, 24(5): 434-439.
27.	D’Ugo DM, Pende V, Persiani R, et al. Laparoscopic staging of gastric cancer: an overview. J Am Coll Surg, 2003, 196(6): 965-974.
28.	Yoshikawa T, Tsuburaya A, Kobayashi O, et al. Peritoneal cytology in patients with gastric cancer exposed to the serosa–a proposed new classification based on the local and distant cytology. Hepatogastroenterology, 2003, 50(52): 1183-1186.
29.	Tokumitsu Y, Yoshino S, Iida M, et al. Intraoperative dissemination during gastrectomy for gastric cancer associated with serosal invasion. Surg Today, 2015, 45(6): 746-751.
30.	Ikeguchi M, Oka A, Tsujitani S, et al. Relationship between area of serosal invasion and intraperitoneal free cancer cells in patients with gastric cancer. Anticancer Res, 1994, 14(5B): 2131-2134.
31.	安杰, 刘伟, 刘艳丽, 等. 腹腔冲洗细胞学检查对胃癌预后的临床评估及意义. 中国普通外科杂志, 2009, 18(10): 1013-1018.

1. Chen W, Sun K, Zheng R, et al. Cancer incidence and mortality in China, 2014. Chin J Cancer Res, 2018, 30(1): 1-12.
2. Nashimoto A, Akazawa K, Isobe Y, et al. Gastric cancer treated in 2002 in Japan: 2009 annual report of the JGCA nationwide registry. Gastric Cancer, 2013, 16(1): 1-27.
3. Rau B, Brandl A, Piso P, et al. Peritoneal metastasis in gastric cancer: results from the German database. Gastric Cancer, 2020, 23(1): 11-22.
4. Mirza A, Galloway S. Laparoscopy, computerised tomography and fluorodeoxyglucose positron emission tomography in the management of gastric and gastro-oesophageal junction cancers. Surg Endosc, 2016, 30(7): 2690-2696.
5. 丁平安, 刘洋, 郭洪海, 等. 腹腔镜探查联合腹腔脱落细胞学检查在局部进展期胃癌诊治中的应用. 中华胃肠外科杂志, 2020, 23(2): 170-176.
6. Liu K, Chen XZ, Zhang WH, et al. “Four-Step Procedure” of laparoscopic exploration for gastric cancer in West China Hospital: a retrospective observational analysis from a high-volume institution in China. Surg Endosc, 2019, 33(5): 1674-1682.
7. 陈心足, 刘凯, 张维汉, 等. 胃癌腹腔镜探查. 中华胃肠外科杂志, 2018, 21(5): 497.
8. Fukuya T, Honda H, Hayashi T, et al. Lymph-node metastases: efficacy for detection with helical CT in patients with gastric cancer. Radiology, 1995, 197(3): 705-711.
9. Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer, 2011, 14(2): 101-112.
10. Sano T, Coit DG, Kim HH, et al. Proposal of a new stage grouping of gastric cancer for TNM classification: International Gastric Cancer Association staging project. Gastric Cancer, 2017, 20(2): 217-225.
11. Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2014(ver. 4). Gastric Cancer, 2017, 20(1): 1-19.
12. 邱海波, 周志伟. NCCN胃癌临床实践指南2017年第五版更新要点解读. 中华胃肠外科杂志, 2018, 21(2): 160-164.
13. Irino T, Sano T, Hiki N, et al. Diagnostic staging laparoscopy in gastric cancer: a prospective cohort at a cancer institute in Japan. Surg Endosc, 2018, 32(1): 268-275.
14. Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2018 (5th edition). Gastric Cancer, 2021, 24(1): 1-21.
15. Cunningham D, Allum WH, Stenning SP, et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med, 2006, 355(1): 11-20.
16. Yamamoto M, Rashid OM, Wong J. Surgical management of gastric cancer: the East vs. West perspective. J Gastrointest Oncol, 2015, 6(1): 79-88.
17. Karanicolas PJ, Elkin EB, Jacks LM, et al. Staging laparoscopy in the management of gastric cancer: a population-based analysis. J Am Coll Surg, 2011, 213(5): 644-651.
18. Miki Y, Tokunaga M, Tanizawa Y, et al. Staging laparoscopy for patients with cM0, type 4, and large type 3 gastric cancer. World J Surg, 2015, 39(11): 2742-2747.
19. Ramos RF, Scalon FM, Scalon MM, et al. Staging laparoscopy in gastric cancer to detect peritoneal metastases: A systematic review and meta-analysis. Eur J Surg Oncol, 2016, 42(9): 1315-1321.
20. Bentrem D, Wilton A, Mazumdar M, et al. The value of peritoneal cytology as a preoperative predictor in patients with gastric carcinoma undergoing a curative resection. Ann Surg Oncol, 2005, 12(5): 347-353.
21. Ribeiro U, Safatle-Ribeiro AV, Zilberstein B, et al. Does the intraoperative peritoneal lavage cytology add prognostic information in patients with potentially curative gastric resection? J Gastrointest Surg, 2006, 10(2): 170-176.
22. Wang YD, Wu P, Mao JD, et al. Relationship between vascular invasion and microvessel density and micrometastasis. World J Gastroenterol, 2007, 13(46): 6269-6273.
23. Ru Y, Zhang L, Chen Q, et al. Detection and clinical significance of lymph node micrometastasis in gastric cardia adenocarcinoma. J Int Med Res, 2012, 40(1): 293-299.
24. Hori Y; SAGES Guidelines Committee. Diagnostic laparoscopy guidelines: This guideline was prepared by the SAGES Guidelines Committee and reviewed and approved by the Board of Governors of the Society of American Gastrointestinal and Endoscopic Surgeons (SAGES), November 2007. Surg Endosc, 2008, 22(5): 1353-1383.
25. Burke EC, Karpeh MS, Conlon KC, et al. Laparoscopy in the management of gastric adenocarcinoma. Ann Surg, 1997, 225(3): 262-267.
26. Santa-Maria AF, Valadão M, Iglesias AC. The role of staging laparoscopy in treatment of locally advanced gastric cancer. Surg Laparosc Endosc Percutan Tech, 2014, 24(5): 434-439.
27. D’Ugo DM, Pende V, Persiani R, et al. Laparoscopic staging of gastric cancer: an overview. J Am Coll Surg, 2003, 196(6): 965-974.
28. Yoshikawa T, Tsuburaya A, Kobayashi O, et al. Peritoneal cytology in patients with gastric cancer exposed to the serosa–a proposed new classification based on the local and distant cytology. Hepatogastroenterology, 2003, 50(52): 1183-1186.
29. Tokumitsu Y, Yoshino S, Iida M, et al. Intraoperative dissemination during gastrectomy for gastric cancer associated with serosal invasion. Surg Today, 2015, 45(6): 746-751.
30. Ikeguchi M, Oka A, Tsujitani S, et al. Relationship between area of serosal invasion and intraperitoneal free cancer cells in patients with gastric cancer. Anticancer Res, 1994, 14(5B): 2131-2134.
31. 安杰, 刘伟, 刘艳丽, 等. 腹腔冲洗细胞学检查对胃癌预后的临床评估及意义. 中国普通外科杂志, 2009, 18(10): 1013-1018.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Significance of “Four-Step Procedure” of laparoscopic exploration in diagnosis of peritoneal metastasis of gastric cancer

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