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Endoscopic submucosal dissection for early neoplastic lesions in the surgically altered stomach: a systematic review and meta-analysis

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Abstract

Introduction and aim

Endoscopic submucosal dissection (ESD) for early gastric cancer is highly effective and well established. Performing ESD in the surgically altered stomach (SAS) is challenging. The aim of this meta-analysis is to assess the safety and efficacy of ESD for patients with early neoplastic lesions occurring in the SAS with a subgroup analysis of lesions occurring on the suture line compared to non-suture line lesions and outcomes in the remnant stomach compared to the gastric tube.

Methods

We performed a literature search of the PubMed, Embase, and CINAHL electronic databases from January 2000 to November 2017 for articles reporting the safety and efficacy of ESD in the surgically altered stomach. SAS was defined as the remnant stomach following gastrectomy and gastric tube following esophagectomy. Meta-analysis was performed using Review Manager version 5.3 software.

Results

A total of 21 articles, with 903 lesions occurring in the remnant stomach or gastric tube, were included in this study. There was no significant difference between en bloc (RR 0.99, 95% CI 0.91–1.08), curative resection (RR 1.03, 95% CI 0.84–1.26), or bleeding rates (RR 1.40, 95% CI 0.18–10.72) between lesions in the remnant stomach and gastric tube. However, perforation was significantly higher in the gastric tube (RR 5.19, 95% 1.27–21.25). Suture line lesions had a significantly higher risk of perforation (RR 4.55, 95% CI 2.13–9.74).

Conclusion

ESD for early neoplastic lesions occurring in the SAS is a safe and efficacious with similar en bloc and curative resection rates compared to the anatomically normal stomach. ESD for lesions on the suture line or in the gastric tube is associated with an increased risk of perforation which can be managed endoscopically.

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References

  1. Ojima T, Iwahashi M, Nakamori M, Nakamura M, Naka T, Katsuda M et al (2010) Clinicopathological characteristics of remnant gastric cancer after a distal gastrectomy. J Gastrointest Surg Off J Soc Surg Aliment Tract 14(2):277–281

    Article  Google Scholar 

  2. Nozaki I, Kurita A, Nasu J, Kubo Y, Aogi K, Tanada M et al (2007) Higher incidence of gastric remnant cancer after proximal than distal gastrectomy. Hepatogastroenterology 54(77):1604–1608

    PubMed  Google Scholar 

  3. Greene FL (1996) Management of gastric remnant carcinoma based on the results of a 15-year endoscopic screening program. Ann Surg 223(6):701–706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Nasu J, Doi T, Endo H, Nishina T, Hirasaki S, Hyodo I (2005) Characteristics of metachronous multiple early gastric cancers after endoscopic mucosal resection. Endoscopy 37(10):990–993

    Article  CAS  PubMed  Google Scholar 

  5. Motoyama S, Saito R, Kitamura M, Ogawa J (2003) Outcomes of active operation during intensive followup for second primary malignancy after esophagectomy for thoracic squamous cell esophageal carcinoma. J Am Coll Surg 197(6):914–920

    Article  PubMed  Google Scholar 

  6. Poon RT, Law SY, Chu KM, Branicki FJ, Wong J (1998) Multiple primary cancers in esophageal squamous cell carcinoma: incidence and implications. Ann Thorac Surg 65(6):1529–1534

    Article  CAS  PubMed  Google Scholar 

  7. Ono H, Kondo H, Gotoda T, Shirao K, Yamaguchi H, Saito D et al (2001) Endoscopic mucosal resection for treatment of early gastric cancer. Gut 48(2):225–229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Oka S, Tanaka S, Kaneko I, Mouri R, Hirata M, Kawamura T et al (2006) Advantage of endoscopic submucosal dissection compared with EMR for early gastric cancer. Gastrointest Endosc 64(6):877–883

    Article  PubMed  Google Scholar 

  9. Onozato Y, Ishihara H, Iizuka H, Sohara N, Kakizaki S, Okamura S et al (2006) Endoscopic submucosal dissection for early gastric cancers and large flat adenomas. Endoscopy 38(10):980–986

    Article  CAS  PubMed  Google Scholar 

  10. Facciorusso A, Antonino M, Di Maso M, Muscatiello N (2014) Endoscopic submucosal dissection vs endoscopic mucosal resection for early gastric cancer: a meta-analysis. World J Gastrointest Endosc 6(11):555–563

    Article  PubMed  PubMed Central  Google Scholar 

  11. Sugiura T, Kato H, Tachimori Y, Igaki H, Yamaguchi H, Nakanishi Y (2002) Second primary carcinoma in the gastric tube constructed as an esophageal substitute after esophagectomy. J Am Coll Surg 194(5):578–583

    Article  PubMed  Google Scholar 

  12. Gotoda T, Yanagisawa A, Sasako M, Ono H, Nakanishi Y, Shimoda T et al (2000) Incidence of lymph node metastasis from early gastric cancer: estimation with a large number of cases at two large centers. Gastric Cancer Off J Int Gastric Cancer Assoc Jpn Gastric Cancer Assoc 3(4):219–225

    Google Scholar 

  13. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JPA et al (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 339:b2700

    Article  PubMed  PubMed Central  Google Scholar 

  14. Song BG, Kim GH, Lee BE, Jeon HK, Baek DH, Song GA (2017) Endoscopic submucosal dissection of gastric epithelial neoplasms after partial gastrectomy: a single-center experience. Gastroenterol Res Pract 2017:6395283

    Article  PubMed  PubMed Central  Google Scholar 

  15. Jung JH, Shin I, Lee H, Min B-H, Lee JH, Rhee P-L et al (2016) Mo1334 endoscopic submucosal dissection for metachronous early gastric cancer in remnant stomach after gastrectomy for early gastric cancer. Gastrointest Endosc 83(5):AB460–AB461

    Article  Google Scholar 

  16. Lee JY, Min B-H, Lee JG, Noh D, Lee JH, Rhee P-L et al (2016) Endoscopic submucosal dissection for early gastric neoplasia occurring in the remnant stomach after distal gastrectomy. Clin Endosc 49(2):182–186

    Article  PubMed  PubMed Central  Google Scholar 

  17. Mukasa M, Takedatsu H, Matsuo K, Sumie H, Yoshida H, Hinosaka A et al (2015) Clinical characteristics and management of gastric tube cancer with endoscopic submucosal dissection. World J Gastroenterol 21(3):919–925

    Article  PubMed  PubMed Central  Google Scholar 

  18. Nishimura J, Nishikawa J, Hamabe K, Nakamura M, Goto A, Okamoto T et al (2014) Efficacy of endoscopic submucosal dissection for cancer of the operated stomach. J Gastrointest Cancer 45(1):27–33

    Article  PubMed  Google Scholar 

  19. Niwa Y, Ishihara M, Tajika M, Tanaka T, Fujiyoshi T, Tsutsumi E et al (2014) Sa1659 endoscopic submucosal resection for remnant early gastric cancer versus U region early gastric cancer. Gastrointest Endosc 79(5):AB291

    Article  Google Scholar 

  20. Nonaka S, Oda I, Sato C, Abe S, Suzuki H, Yoshinaga S et al (2014) Endoscopic submucosal dissection for gastric tube cancer after esophagectomy. Gastrointest Endosc 79(2):260–270

    Article  PubMed  Google Scholar 

  21. Ojima T, Takifuji K, Nakamura M, Nakamori M, Katsuda M, Iida T et al (2014) Endoscopic submucosal dissection for gastric tumors in various types of remnant stomach. Endoscopy 46(8):645–649

    Article  PubMed  Google Scholar 

  22. Suzuki H, Oda I, Sekiguchi M, Sato C, Makazu M, Sato Y et al (2014) Sa1636 factors associated with perforation and delayed perforation induced by endoscopic submucosal dissection for early gastric cancer: a large consecutive patients series. Gastrointest Endosc 79(5):AB283–AB284

    Article  Google Scholar 

  23. Tanaka S, Toyonaga T, Morita Y, Fujita T, Yoshizaki T, Kawara F et al (2014) Endoscopic submucosal dissection for early gastric cancer in anastomosis site after distal gastrectomy. Gastric Cancer Off J Int Gastric Cancer Assoc Jpn Gastric Cancer Assoc 17(2):371–376

    Google Scholar 

  24. Tawaraya S, Jin M, Matsuhashi T, Suzuki Y, Sawaguchi M, Watanabe N et al (2014) Advanced feasibility of endoscopic submucosal dissection for the treatment of gastric tube cancer after esophagectomy. Gastrointest Endosc 79(3):525–530

    Article  PubMed  Google Scholar 

  25. Lee HJ, Kim S, Shim CN, Park JC, Lee H, Lee SK et al (2013) Sa1600 is total gastrectomy the only treatment modality for early neoplasm at remnant stomach? Gastrointest Endosc 77(5):AB263–AB264

    Google Scholar 

  26. Nonaka S, Oda I, Makazu M, Haruyama S, Abe S, Suzuki H et al (2013) Endoscopic submucosal dissection for early gastric cancer in the remnant stomach after gastrectomy. Gastrointest Endosc 78(1):63–72

    Article  PubMed  Google Scholar 

  27. Nishide N, Ono H, Kakushima N, Takizawa K, Tanaka M, Matsubayashi H et al (2012) Clinical outcomes of endoscopic submucosal dissection for early gastric cancer in remnant stomach or gastric tube. Endoscopy 44(6):577–583

    Article  CAS  PubMed  Google Scholar 

  28. Bamba T, Kosugi S, Takeuchi M, Kobayashi M, Kanda T, Matsuki A et al (2010) Surveillance and treatment for second primary cancer in the gastric tube after radical esophagectomy. Surg Endosc 24(6):1310–1317

    Article  PubMed  Google Scholar 

  29. Hoteya S, Iizuka T, Kikuchi D, Yahagi N (2010) Clinical advantages of endoscopic submucosal dissection for gastric cancers in remnant stomach surpass conventional endoscopic mucosal resection. Dig Endosc Off J Jpn Gastroenterol Endosc Soc 22(1):17–20

    Google Scholar 

  30. Lee JY, Choi IJ, Cho S-J, Kim CG, Kook M-C, Lee JH et al (2010) Endoscopic submucosal dissection for metachronous tumor in the remnant stomach after distal gastrectomy. Surg Endosc 24(6):1360–1366

    Article  PubMed  Google Scholar 

  31. Mochizuki S, Yano T, Tsuruta S, Minashi K, Ikematsu H, Kaneko K et al (2009) Case series of endoscopic submucosal dissection (ESD) for early remnant gastric cancer after subtotal gastrectomy. Gastrointest Endosc 69(5):AB310

    Article  Google Scholar 

  32. Osumi W, Fujita Y, Hiramatsu M, Kawai M, Sumiyoshi K, Umegaki E et al (2009) Endoscopic submucosal dissection allows less-invasive curative resection for gastric tube cancer after esophagectomy—a case series. Endoscopy 41(9):777–780

    Article  CAS  PubMed  Google Scholar 

  33. Hirasaki S, Kanzaki H, Matsubara M, Fujita K, Matsumura S, Suzuki S (2008) Treatment of gastric remnant cancer post distal gastrectomy by endoscopic submucosal dissection using an insulation-tipped diathermic knife. World J Gastroenterol 14(16):2550–2555

    Article  PubMed  PubMed Central  Google Scholar 

  34. Takenaka R, Kawahara Y, Okada H, Tsuzuki T, Yagi S, Kato J et al (2008) Endoscopic submucosal dissection for cancers of the remnant stomach after distal gastrectomy. Gastrointest Endosc 67(2):359–363

    Article  PubMed  Google Scholar 

  35. Jeong JY, Oh Y-H, Yu YH, Park HS, Lee HL, Eun CS et al (2012) Does submucosal fibrosis affect the results of endoscopic submucosal dissection of early gastric tumors? Gastrointest Endosc 76(1):59–66

    Article  PubMed  Google Scholar 

  36. Piso P, Meyer HJ, Edris C, Jähne J (1999) Surgical therapy of gastric stump carcinoma—a retrospective analysis of 109 patients. Hepatogastroenterology 46(28):2643–2647

    CAS  PubMed  Google Scholar 

  37. Sasako M, Maruyama K, Kinoshita T, Okabayashi K (1991) Surgical treatment of carcinoma of the gastric stump. Br J Surg 78(7):822–824

    Article  CAS  PubMed  Google Scholar 

  38. Xi HQ, Cui JX, Hu C, Ma LG, Wei B, Chen L (2016) Retrospective clinical analysis of surgical treatment for gastric stump carcinoma. Zhonghua Wai Ke Za Zhi 54(3):182–186

    CAS  PubMed  Google Scholar 

  39. Iguchi K, Kunisaki C, Sato S, Tanaka Y, Miyamoto H, Kosaka T et al (2018) Evaluation of optimal lymph node dissection in remnant gastric cancer based on initial distal gastrectomy. Anticancer Res 38(3):1677–1683

    PubMed  Google Scholar 

  40. Li F, Zhang R, Liang H, Liu H, Quan J, Zhao J (2012) The pattern of lymph node metastasis and the suitability of 7th UICC N stage in predicting prognosis of remnant gastric cancer. J Cancer Res Clin Oncol 138(1):111–117

    Article  CAS  PubMed  Google Scholar 

  41. Son S-Y, Kong S-H, Ahn HS, Park YS, Ahn S-H, Suh Y-S et al (2017) The value of N staging with the positive lymph node ratio, and splenectomy, for remnant gastric cancer: a multicenter retrospective study. J Surg Oncol 116(7):884–893

    Article  PubMed  Google Scholar 

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Contributions

Literature search was performed by MB and MA. Data collection was performed by MB and MS. Data analysis was performed by AO and MB. The manuscript was written by MB. The manuscript was edited and revised by DCL and MO. Overall supervision was done by DCL and MO.

Corresponding author

Correspondence to Mohamed Barakat.

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Disclosure

Dr. David L. Carr-Locke is a consultant for Boston Scientific, Maura Kea Technologies and receives royalties from Telemed and Steris. Dr. Mohamed Othman is a consultant for Boston Scientific and Olympus. Doctors Mohamed Barakat, Mohamed Seif, Mohamed Abdelfatah, and Andrew Ofosu have no conflicts of interest or financial ties to disclose.

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Barakat, M., Seif, M., Abdelfatah, M.M. et al. Endoscopic submucosal dissection for early neoplastic lesions in the surgically altered stomach: a systematic review and meta-analysis. Surg Endosc 33, 2381–2395 (2019). https://doi.org/10.1007/s00464-019-06778-y

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