Modern Surgical Considerations for Gastric Cancer

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Quan P. Ly From the Department of Surgery, University of Nebraska Medical Center, and Eppley Cancer Center, Omaha, Nebraska.

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Aaron R. Sasson From the Department of Surgery, University of Nebraska Medical Center, and Eppley Cancer Center, Omaha, Nebraska.

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Surgical resection remains the mainstay of treatment for localized gastric adenocarcinoma. The type and extent of resection depends on tumor location. Although the incidence of gastric cancer has been declining, a shift has occurred to more tumors involving the proximal compared with the distal stomach. Appropriate treatment depends on a thorough staging process to exclude the presence of distant metastatic disease. Current staging modalities include high-quality CT scan, endoscopic ultrasound, PET, and laparoscopy. The value of peritoneal lavage to detect occult peritoneal disease is under investigation. The principles of surgical resection have always included negative resection margins and adequate lymph node examination. Controversial topics requiring further study include laparoscopic resections and hepatic metastasectomy. This review highlights the salient points of current surgical management of gastric adenocarcinoma.

Correspondence: Aaron R. Sasson, MD, Department of Surgery, University of Nebraska Medical Center, 984030 Nebraska Medical Center, Omaha, NE 68198-4030. E-mail: asasson@unmc.edu
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  • 1.

    Jemal A, Siegel R, Ward E et al.. Cancer statistics, 2008. CA Cancer J Clin. 2008;58:7196.

  • 2.

    Wilkinson NW, Howe J, Gay G et al.. Differences in the pattern of presentation and treatment of proximal and distal gastric cancer: results of the 2001 gastric patient care evaluation. Ann Surg Oncol 2008;15:16441650.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Bentrem D, Gerdes H, Tang L et al.. Clinical correlation of endoscopic ultrasonography with pathologic stage and outcome in patients undergoing curative resection for gastric cancer. Ann Surg Oncol 2007;14:18531859.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Malheiros CA, Ardengh JC, Santo GC et al.. Endoscopic ultrasound in the preoperative staging of gastric cancer: correlation with the surgical and/or pathological findings. Arq Gastroenterol 2008;45:2227 [in Portuguese].

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Ganpathi IS, So JB, Ho KY. Endoscopic ultrasonography for gastric cancer: does it influence treatment? Surg Endosc 2006;20:559562.

  • 6.

    Jones DB. Role of endoscopic ultrasound in staging upper gastrointestinal cancers. ANZ J Surg 2007;77:166172.

  • 7.

    Chen J, Cheong JH, Yun MJ et al.. Improvement in preoperative staging of gastric adenocarcinoma with positron emission tomography. Cancer 2005;103:23832390.

  • 8.

    Lerut T, Flamen P, Ectors N et al.. Histopathologic validation of lymph node staging with FDG-PET scan in cancer of the esophagus and gastroesophageal junction: a prospective study based on primary surgery with extensive lymphadenectomy. Ann Surg 2000;232:743752.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Yun M, Lim JS, Noh SH et al.. Lymph node staging of gastric cancer using (18)F-FDG PET: a comparison study with CT. J Nucl Med 2005;46:15821588.

  • 10.

    Lim JS, Kim MJ, Yun MJ et al.. Comparison of CT and 18F-FDG pet for detecting peritoneal metastasis on the preoperative evaluation for gastric carcinoma. Korean J Radiol 2006;7:249256.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Kinkel K, Lu Y, Both M et al.. Detection of hepatic metastases from cancers of the gastrointestinal tract by using noninvasive imaging methods (US, CT, MR imaging, PET): a meta-analysis. Radiology 2002;224:748756.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Ott K, Herrmann K, Lordick F et al.. Early metabolic response evaluation by fluorine-18 fluorodeoxyglucose positron emission tomography allows in vivo testing of chemosensitivity in gastric cancer: long-term results of a prospective study. Clin Cancer Res 2008;14:20122018.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Song KY, Kim SN, Park CH. Tailored-approach of laparoscopic wedge resection for treatment of submucosal tumor near the esophagogastric junction. Surg Endosc 2007;21:22722276.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Nakagawa S, Nashimoto A, Yabusaki H. Role of staging laparoscopy with peritoneal lavage cytology in the treatment of locally advanced gastric cancer. Gastric Cancer 2007;10:2934.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Blackshaw GR, Barry JD, Edwards P et al.. Laparoscopy significantly improves the perceived preoperative stage of gastric cancer. Gastric Cancer 2003;6:225229.

  • 16.

    Sarela AI, Miner TJ, Karpeh MS et al.. Clinical outcomes with laparoscopic stage M1, unresected gastric adenocarcinoma. Ann Surg 2006;243:189195.

  • 17.

    Bozzetti F, Marubini E, Bonfanti G et al.. Subtotal versus total gastrectomy for gastric cancer: five-year survival rates in a multicenter randomized Italian trial. Italian Gastrointestinal Tumor Study Group. Ann Surg 1999;230:170178.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Gouzi JL, Huguier M, Fagniez PL et al.. Total versus subtotal gastrectomy for adenocarcinoma of the gastric antrum. A French prospective controlled study. Ann Surg 1989;209:162166.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Davies J, Johnston D, Sue-Ling H et al.. Total or subtotal gastrectomy for gastric carcinoma? A study of quality of life. World J Surg 1998;22:10481055.

  • 20.

    Harrison LE, Karpeh MS, Brennan MF. Total gastrectomy is not necessary for proximal gastric cancer. Surgery 1998;123:127130.

  • 21.

    Kim JH, Park SS, Kim J et al.. Surgical outcomes for gastric cancer in the upper third of the stomach. World J Surg 2006;30:18701876; discussion 1877–1878.

  • 22.

    Katsoulis IE, Robotis I, Kouraklis G, Yannopoulos P. Duodenogastric reflux after esophagectomy and gastric pull-up: the effect of the route of reconstruction. World J Surg 2005;29:174181.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Hsu CP, Chen CY, Hsieh YH et al.. Esophageal reflux after total or proximal gastrectomy in patients with adenocarcinoma of the gastric cardia. Am J Gastroenterol 1997;92:13471350.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Ito H, Clancy TE, Osteen RT et al.. Adenocarcinoma of the gastric cardia: what is the optimal surgical approach? J Am Coll Surg 2004;199:880886.

  • 25.

    Bozzetti F, Bonfanti G, Bufalino R et al.. Adequacy of margins of resection in gastrectomy for cancer. Ann Surg 1982;196:685690.

  • 26.

    Cascinu S, Giordani P, Catalano V et al.. Resection-line involvement in gastric cancer patients undergoing curative resections: implications for clinical management. Jpn J Clin Oncol 1999;29:291293.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Cho BC, Jeung HC, Choi HJ et al.. Prognostic impact of resection margin involvement after extended (D2/D3) gastrectomy for advanced gastric cancer: a 15-year experience at a single institute. J Surg Oncol 2007;95:461468.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Kim SH, Karpeh MS, Klimstra DS et al.. Effect of microscopic resection line disease on gastric cancer survival. J Gastrointest Surg 1999;3:2433.

  • 29.

    Kajitani T. The general rules for the gastric cancer study in surgery and pathology. Part I. Clinical classification. Jpn J Surg 1981;11:127139.

  • 30.

    D'Ugo D, Pacelli F, Persiani R et al.. Impact of the latest TNM classification for gastric cancer: retrospective analysis on 94 D2 gastrectomies. World J Surg 2002;26:672677.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Marrelli D, Pedrazzani C, Neri A et al.. Complications after extended (D2) and superextended (D3) lymphadenectomy for gastric cancer: analysis of potential risk factors. Ann Surg Oncol 2007;14:2533.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Hartgrink HH, van de Velde CJ, Putter H et al.. Extended lymph node dissection for gastric cancer: who may benefit? Final results of the randomized dutch gastric cancer group trial. J Clin Oncol 2004;22:20692077.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Cuschieri A, Weeden S, Fielding J et al.. Patient survival after D1 and D2 resections for gastric cancer: long-term results of the MRC randomized surgical trial. Surgical Co-operative Group. Br J Cancer 1999;79:15221530.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Hartgrink HH, van de Velde CJ. Status of extended lymph node dissection: locoregional control is the only way to survive gastric cancer. J Surg Oncol 2005;90:153165.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Fatouros M, Roukos DH, Lorenz M et al.. Impact of spleen preservation in patients with gastric cancer. Anticancer Res 2005;25:30233030.

  • 36.

    Biffi R, Chiappa A, Luca F et al.. Extended lymph node dissection without routine spleno-pancreatectomy for treatment of gastric cancer: low morbidity and mortality rates in a single center series of 250 patients. J Surg Oncol 2006;93:394400.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Gil-Rendo A, Hernandez-Lizoain JL, Martinez-Regueira F et al.. Risk factors related to operative morbidity in patients undergoing gastrectomy for gastric cancer. Clin Transl Oncol 2006;8:354361.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Kulig J, Popiela T, Kolodziejczyk P et al.. Standard D2 versus extended D2 (D2+) lymphadenectomy for gastric cancer: an interim safety analysis of a multicenter, randomized, clinical trial. Am J Surg 2007;193:1015.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Yu W, Choi GS, Chung HY. Randomized clinical trial of splenectomy versus splenic preservation in patients with proximal gastric cancer. Br J Surg 2006;93:559563.

  • 40.

    Zhang CH, Zhan WH, He YL et al.. Spleen preservation in radical surgery for gastric cardia cancer. Ann Surg Oncol 2007;14:13121319.

  • 41.

    Kunisaki C, Makino H, Suwa H et al.. Impact of splenectomy in patients with gastric adenocarcinoma of the cardia. J Gastrointest Surg 2007;11:10391044.

  • 42.

    Degiuli M, Sasako M, Ponti A, Calvo F. Survival results of a multicentre phase II study to evaluate D2 gastrectomy for gastric cancer. Br J Cancer 2004;90:17271732.

  • 43.

    Karpeh MS, Leon L, Klimstra D, Brennan MF. Lymph node staging in gastric cancer: is location more important than number? An analysis of 1,038 patients. Ann Surg 2000;232:362371.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Greene FL, Page DL, Fleming ID et al.., eds. AJCC Cancer Staging Manual. 6th ed. New York: Springer; 2002:421.

  • 45.

    Lee HK, Yang HK, Kim WH et al.. Influence of the number of lymph nodes examined on staging of gastric cancer. Br J Surg 2001;88:14081412.

  • 46.

    Bouvier AM, Haas O, Piard F et al.. How many nodes must be examined to accurately stage gastric carcinomas? Results from a population based study. Cancer 2002;94:28622866.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47.

    Smith DD, Schwarz RR, Schwarz RE. Impact of total lymph node count on staging and survival after gastrectomy for gastric cancer: data from a large US-population database. J Clin Oncol 2005;23:71147124.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48.

    Saito H, Fukumoto Y, Osaki T et al.. Prognostic significance of the ratio between metastatic and dissected lymph nodes (n ratio) in patients with advanced gastric cancer. J Surg Oncol 2008;97:132135.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 49.

    Marchet A, Mocellin S, Ambrosi A et al.. The ratio between metastatic and examined lymph nodes (N ratio) is an independent prognostic factor in gastric cancer regardless of the type of lymphadenectomy: results from an Italian multicentric study in 1853 patients.. Ann Surg 2007;245:543552

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 50.

    Iivonen MK, Mattila JJ, Nordback IH, Matikainen MJ. Long-term follow-up of patients with jejunal pouch reconstruction after total gastrectomy. A randomized prospective study. Scand J Gastroenterol 2000;35:679685.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51.

    McAleese P, Calvert H, Ferguson WR, Laird J. Evaluation of ``gastric'' emptying time in the J pouch compared with a standard esophagojejunal anastomosis. World J Surg 1993;17:595599; discussion 599–600.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 52.

    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;247:759765.

  • 53.

    Kono K, Iizuka H, Sekikawa T et al.. Improved quality of life with jejunal pouch reconstruction after total gastrectomy. Am J Surg 2003;185:150154.

  • 54.

    Iivonen MK, Koskinen MO, Ikonen TJ, Matikainen MJ. Emptying of the jejunal pouch and Roux-en-Y limb after total gastrectomy— a randomised, prospective study. Eur J Surg 1999;165:742747.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 55.

    Nakane Y, Okumura S, Akehira K et al.. Jejunal pouch reconstruction after total gastrectomy for cancer. A randomized controlled trial. Ann Surg 1995;222:2735.

  • 56.

    Kitano S, Iso Y, Moriyama M, Sugimachi K. Laparoscopy-assisted billroth I gastrectomy. Surg Laparosc Endosc 1994;4:146148.

  • 57.

    Fujiwara M, Kodera Y, Misawa K et al.. Longterm outcomes of early-stage gastric carcinoma patients treated with laparoscopy-assisted surgery. J Am Coll Surg 2008;206:138143.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 58.

    Pugliese R, Maggioni D, Sansonna F et al.. Outcomes and survival after laparoscopic gastrectomy for adenocarcinoma. Analysis on 65 patients operated on by conventional or robot-assisted minimal access procedures. Eur J Surg Oncol 2008, in press.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 59.

    Kitano S, Shiraishi N, Uyama I et al.. A multicenter study on oncologic outcome of laparoscopic gastrectomy for early cancer in Japan. Ann Surg 2007;245:6872.

  • 60.

    Ryu KW, Kim YW, Lee JH et al.. Surgical complications and the risk factors of laparoscopy-assisted distal gastrectomy in early gastric cancer. Ann Surg Oncol 2008;15:16251631.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 61.

    Lee JH, Kim YW, Ryu KW et al.. A phase-II clinical trial of laparoscopy-assisted distal gastrectomy with D2 lymph node dissection for gastric cancer patients. Ann Surg Oncol 2007;14:31483153.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 62.

    Song KY, Park SM, Kim SN, Park CH. The role of surgery in the treatment of recurrent gastric cancer. Am J Surg 2008;196:1922.

  • 63.

    Nakajima T, Harashima S, Hirata M, Kajitani T. Prognostic and therapeutic values of peritoneal cytology in gastric cancer. Acta Cytol 1978;22:225229.

  • 64.

    Abe S, Yoshimura H, Tabara H et al.. Curative resection of gastric cancer: limitation of peritoneal lavage cytology in predicting the outcome. J Surg Oncol 1995;59:226229.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 65.

    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;12:347353.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 66.

    Kim MM, Mansfield PF, Das P et al.. Chemoradiation therapy for potentially resectable gastric cancer: clinical outcomes among patients who do not undergo planned surgery. Int J Radiat Oncol Biol Phys 2008;71:167172.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 67.

    Bando E, Yonemura Y, Endou Y et al.. Immunohistochemical study of MT-MMP tissue status in gastric carcinoma and correlation with survival analyzed by univariate and multivariate analysis. Oncol Rep 1998;5:14831488.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 68.

    Burke EC, Karpeh MS Jr, Conlon KC, Brennan MF. Peritoneal lavage cytology in gastric cancer: an independent predictor of outcome. Ann Surg Oncol 1998;5:411415.

  • 69.

    Asao T, Fukuda T, Yazawa S, Nagamachi Y. Carcinoembryonic antigen levels in peritoneal washings can predict peritoneal recurrence after curative resection of gastric cancer. Cancer 1991;68:4447.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 70.

    Nishiyama M, Takashima I, Tanaka T et al.. Carcinoembryonic antigen levels in the peritoneal cavity: useful guide to peritoneal recurrence and prognosis for gastric cancer. World J Surg 1995;19:133137; discussion 137.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 71.

    Kodera Y, Nakanishi H, Ito S et al.. Quantitative detection of disseminated free cancer cells in peritoneal washes with real-time reverse transcriptase-polymerase chain reaction: a sensitive predictor of outcome for patients with gastric carcinoma. Ann Surg 2002;235:499506.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 72.

    Katsuragi K, Yashiro M, Sawada T et al.. Prognostic impact of PCR-based identification of isolated tumour cells in the peritoneal lavage fluid of gastric cancer patients who underwent a curative R0 resection. Br J Cancer 2007;97:550556.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 73.

    Saidi RF, ReMine SG, Dudrick PS, Hanna NN. Is there a role for palliative gastrectomy in patients with stage IV gastric cancer? World J Surg 2006;30:2127.

  • 74.

    Lim S, Muhs BE, Marcus SG et al.. Results following resection for stage IV gastric cancer; are better outcomes observed in selected patient subgroups? J Surg Oncol 2007;95:118122.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 75.

    Hartgrink HH, Putter H, Klein Kranenbarg E et al.. Value of palliative resection in gastric cancer. Br J Surg 2002;89:14381443.

  • 76.

    Ouchi K, Sugawara T, Ono H et al.. Therapeutic significance of palliative operations for gastric cancer for survival and quality of life. J Surg Oncol 1998;69:4144.

  • 77.

    Lin SZ, Tong HF, You T et al.. Palliative gastrectomy and chemotherapy for stage IV gastric cancer. J Cancer Res Clin Oncol 2008;134:187192.

  • 78.

    Fujitani K, Yang HK, Kurokawa Y et al.. Randomized controlled trial comparing gastrectomy plus chemotherapy with chemotherapy alone in advanced gastric cancer with a single non-curable factor: Japan Clinical Oncology Group Study JCOG 0705 and Korea Gastric Cancer Association Study KGCA01. Jpn J Clin Oncol 2008;38:504506.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 79.

    Linhares E, Monteiro M, Kesley R et al.. Major hepatectomy for isolated metastases from gastric adenocarcinoma. HPB (Oxford) 2003;5:235237.

  • 80.

    Cheon SH, Rha SY, Jeung HC et al.. Survival benefit of combined curative resection of the stomach (D2 resection) and liver in gastric cancer patients with liver metastases. Ann Oncol 2008;19:11461153.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 81.

    Koga R, Yamamoto J, Ohyama S et al.. Liver resection for metastatic gastric cancer: experience with 42 patients including eight long-term survivors. Jpn J Clin Oncol 2007;37:836842.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 82.

    Okano K, Maeba T, Ishimura K et al.. Hepatic resection for metastatic tumors from gastric cancer. Ann Surg 2002;235:8691.

  • 83.

    Shirabe K, Wakiyama S, Gion T et al.. Hepatic resection for the treatment of liver metastases in gastric carcinoma: review of the literature. HPB (Oxford) 2006;8:8992.

  • 84.

    Ambiru S, Miyazaki M, Ito H et al.. Benefits and limits of hepatic resection for gastric metastases. Am J Surg 2001;181:279283.

  • 85.

    Hermans J, Bonenkamp JJ, Boon MC et al.. Adjuvant therapy after curative resection for gastric cancer: meta-analysis of randomized trials. J Clin Oncol 1993;11:14411447.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 86.

    Mari E, Floriani I, Tinazzi A et al.. Efficacy of adjuvant chemotherapy after curative resection for gastric cancer: a meta-analysis of published randomised trials. A study of the GISCAD (Gruppo Italiano per lo Studio dei Carcinomi dell'Apparato Digerente). Ann Oncol 2000;11:837843.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 87.

    Macdonald JS, Smalley SR, Benedetti J et al.. Chemoradiotherapy after surgery compared with surgery alone for adenocarcinoma of the stomach or gastroesophageal junction. N Engl J Med 2001;345:725730.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 88.

    Medical Research Council Oesophageal Cancer Working Group. Surgical resection with or without preoperative chemotherapy in oesophageal cancer: a randomised controlled trial. Lancet 2002;359:17271733.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 89.

    Cunningham D, Allum WH, Stenning SP et al.. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med 2006;355:1120.

  • 90.

    Kunisaki C, Takahashi M, Makino H et al.. The influence of stage migration on the comparison of surgical outcomes between D2 gastrectomy and D3 gastrectomy (para-aortic lymph node dissection): a multi-institutional retrospective study. Am J Surg 2008;196:358363.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 91.

    Ajani JA, Barthel JS, Bekaii-Saab T et al.. NCCN Clinical Practice Guidelines in Oncology: Gastric Cancer. Version 1.2009. Available at: http://www.nccn.org/professionals/physician_gls/PDF/gastric.pdf. Accessed 23 September 2008.

    • PubMed
    • Search Google Scholar
    • Export Citation
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