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01-11-2014 | Original Article

Response to Preoperative Chemotherapy Predicts Survival in Patients Undergoing Hepatectomy for Liver Metastases from Gastric and Esophageal Cancer

Authors: Andreas Andreou, Luca Viganò, Giuseppe Zimmitti, Daniel Seehofer, Martin Dreyer, Andreas Pascher, Marcus Bahra, Wenzel Schoening, Volker Schmitz, Peter C. Thuss-Patience, Timm Denecke, Gero Puhl, Jean-Nicolas Vauthey, Peter Neuhaus, Lorenzo Capussotti, Johann Pratschke, Sven-Christian Schmidt

Published in: Journal of Gastrointestinal Surgery | Issue 11/2014

Abstract

Background

The role of hepatectomy for patients with liver metastases from gastric and esophageal cancer (GELM) is not well defined. The present study examined the morbidity, mortality, and long-term survivals after liver resection for GELM.

Methods

Clinicopathological data of patients who underwent hepatectomy for GELM between 1995 and 2012 at two European high-volume hepatobiliary centers were assessed, and predictors of overall survival (OS) were identified. In addition, the impact of preoperative chemotherapy for GELM on OS was evaluated.

Results

Forty-seven patients underwent hepatectomy for GELM. The primary tumor was located in the stomach, cardia, and distal esophagus in 27, 16, and 4 cases, respectively. Twenty patients received preoperative chemotherapy before hepatectomy. After a median follow-up time of 76 months, 1-, 3-, and 5-year OS rates were 70, 37, and 24 %, respectively. Postoperative morbidity and mortality rates were 32 and 4 %, respectively. Outcomes were comparable between the two centers. Preoperative chemotherapy for GELM (5-year OS: 45 vs 9 %, P = .005) and the lack of posthepatectomy complications (5-year OS: 34 vs 0 %, P < .0001) were significantly associated with improved OS in univariate and multivariate analyses. When stratifying OS by radiologic response of GELM to preoperative chemotherapy, patients with progressive disease despite preoperative treatment had significantly worse OS (5-year OS: 0 vs 70 %, P = .045).

Conclusion

For selected patients with GELM, liver resection is safe and should be regarded as a potentially curative approach. A multimodal treatment strategy including systemic therapy may provide better patient selection resulting in prolonged survival in patients with GELM undergoing hepatectomy.

Poon RT, Fan ST, Lo CM, Ng IO, Liu CL, Lam CM, Wong J. Improving survival results after resection of hepatocellular carcinoma: a prospective study of 377 patients over 10 years. Ann Surg 2001;234:63–70.PubMedCentralCrossRefPubMed

Abdalla EK, Vauthey JN, Ellis LM, Ellis V, Pollock R, Broglio KR, Hess K, Curley SA. Recurrence and outcomes following hepatic resection, radiofrequency ablation, and combined resection/ablation for colorectal liver metastases. Ann Surg 2004;239:818–825.PubMedCentralCrossRefPubMed

Truant S, Huglo D, Hebbar M, Ernst O, Steinling M, Pruvot FR. Prospective evaluation of the impact of [18 F]fluoro-2-deoxy-D-glucose positron emission tomography of resectable colorectal liver metastases. Br J Surg 2005;92:362–369.CrossRefPubMed

Aloia TA, Zorzi D, Abdalla EK, Vauthey JN. Two-surgeon technique for hepatic parenchymal transection of the noncirrhotic liver using saline-linked cautery and ultrasonic dissection. Ann Surg 2005;242:172–177.PubMedCentralCrossRefPubMed

Donadon M, Abdalla EK, Vauthey JN. Liver hanging maneuver for large or recurrent right upper quadrant tumors. J Am Coll Surg 2007;204:329–333.CrossRefPubMed

Azoulay D, Castaing D, Smail A, Adam R, Cailliez V, Laurent A, Lemoine A, Bismuth H. Resection of nonresectable liver metastases from colorectal cancer after percutaneous portal vein embolization. Ann Surg 2000;231:480–486.PubMedCentralCrossRefPubMed

Jaeck D, Oussoultzoglou E, Rosso E, Greget M, Weber JC, Bachellier P. A two-stage hepatectomy procedure combined with portal vein embolization to achieve curative resection for initially unresectable multiple and bilobar colorectal liver metastases. Ann Surg 2004;240:1037–1049; discussion 1049–1051.PubMedCentralCrossRefPubMed

Strasberg SM. Nomenclature of hepatic anatomy and resections: a review of the Brisbane 2000 system. J Hepatobiliary Pancreat Surg 2005;12:351–355.CrossRefPubMed

Makino H, Kunisaki C, Izumisawa Y, Tokuhisa M, Oshima T, Nagano Y, Fujii S, Kimura J, Takagawa R, Kosaka T, Ono HA, Akiyama H, Tanaka K, Endo I. Indication for hepatic resection in the treatment of liver metastasis from gastric cancer. Anticancer Res 2010;30:2367–2376.PubMed

10.

Okano K, Maeba T, Ishimura K, Karasawa Y, Goda F, Wakabayashi H, Usuki H, Maeta H. Hepatic resection for metastatic tumors from gastric cancer. Ann Surg 2002;235:86–91.PubMedCentralCrossRefPubMed

11.

Sakamoto Y, Ohyama S, Yamamoto J, Yamada K, Seki M, Ohta K, Kokudo N, Yamaguchi T, Muto T, Makuuchi M. Surgical resection of liver metastases of gastric cancer: an analysis of a 17-year experience with 22 patients. Surgery 2003;133:507–511.CrossRefPubMed

12.

Takemura N, Saiura A, Koga R, Arita J, Yoshioka R, Ono Y, Hiki N, Sano T, Yamamoto J, Kokudo N, Yamaguchi T. Long-term outcomes after surgical resection for gastric cancer liver metastasis: an analysis of 64 macroscopically complete resections. Langenbecks Arch Surg 2012;397:951–957.CrossRefPubMed

13.

Ajani JA. Evolving chemotherapy for advanced gastric cancer. Oncologist 2005;10 Suppl 3:49–58.CrossRefPubMed

14.

Cunningham D, Starling N, Rao S, Iveson T, Nicolson M, Coxon F, Middleton G, Daniel F, Oates J, Norman AR. Capecitabine and oxaliplatin for advanced esophagogastric cancer. N Engl J Med 2008;358:36–46.CrossRefPubMed

15.

Bang YJ, Van Cutsem E, Feyereislova A, Chung HC, Shen L, Sawaki A, Lordick F, Ohtsu A, Omuro Y, Satoh T, Aprile G, Kulikov E, Hill J, Lehle M, Ruschoff J, Kang YK. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet 2010;376:687–697.CrossRefPubMed

16.

Thelen A, Jonas S, Benckert C, Lopez-Hanninen E, Neumann U, Rudolph B, Schumacher G, Neuhaus P. Liver resection for metastatic gastric cancer. Eur J Surg Oncol 2008;34:1328–1334.CrossRefPubMed

17.

Stockmann M, Lock JF, Riecke B, Heyne K, Martus P, Fricke M, Lehmann S, Niehues SM, Schwabe M, Lemke AJ, Neuhaus P. Prediction of postoperative outcome after hepatectomy with a new bedside test for maximal liver function capacity. Ann Surg 2009;250:119–125.CrossRefPubMed

18.

Imamura H, Sano K, Sugawara Y, Kokudo N, Makuuchi M. Assessment of hepatic reserve for indication of hepatic resection: decision tree incorporating indocyanine green test. Journal of Hepato-Biliary-Pancreatic Surgery 2005;12:16–22.CrossRefPubMed

19.

Ribero D, Abdalla EK, Madoff DC, Donadon M, Loyer EM, Vauthey JN. Portal vein embolization before major hepatectomy and its effects on regeneration, resectability and outcome. Br J Surg 2007;94:1386–1394.CrossRefPubMed

20.

Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, Verweij J, Van Glabbeke M, van Oosterom AT, Christian MC, Gwyther SG. New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst 2000;92:205–216.CrossRefPubMed

21.

Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004;240:205–213.PubMedCentralCrossRefPubMed

22.

Mullen JT, Ribero D, Reddy SK, Donadon M, Zorzi D, Gautam S, Abdalla EK, Curley SA, Capussotti L, Clary BM, Vauthey JN. Hepatic insufficiency and mortality in 1,059 noncirrhotic patients undergoing major hepatectomy. J Am Coll Surg 2007;204:854–862.CrossRefPubMed

23.

Andreou A, Aloia TA, Brouquet A, Dickson PV, Zimmitti G, Maru DM, Kopetz S, Loyer EM, Curley SA, Abdalla EK, Vauthey JN. Margin status remains an important determinant of survival after surgical resection of colorectal liver metastases in the era of modern chemotherapy. Ann Surg 2013;257:1079–1088.PubMedCentralCrossRefPubMed

24.

Blazer DG, 3rd, Kishi Y, Maru DM, Kopetz S, Chun YS, Overman MJ, Fogelman D, Eng C, Chang DZ, Wang H, Zorzi D, Ribero D, Ellis LM, Glover KY, Wolff RA, Curley SA, Abdalla EK, Vauthey JN. Pathologic response to preoperative chemotherapy: a new outcome end point after resection of hepatic colorectal metastases. J Clin Oncol 2008;26:5344–5351.CrossRefPubMed

25.

Ychou M, Boige V, Pignon JP, Conroy T, Bouche O, Lebreton G, Ducourtieux M, Bedenne L, Fabre JM, Saint-Aubert B, Geneve J, Lasser P, Rougier P. Perioperative chemotherapy compared with surgery alone for resectable gastroesophageal adenocarcinoma: an FNCLCC and FFCD multicenter phase III trial. J Clin Oncol 2011;29:1715–1721.CrossRefPubMed

26.

Thuss-Patience PC, Hofheinz RD, Arnold D, Florschutz A, Daum S, Kretzschmar A, Mantovani-Loffler L, Bichev D, Breithaupt K, Kneba M, Schumacher G, Glanemann M, Schlattmann P, Reichardt P, Gahn B. Perioperative chemotherapy with docetaxel, cisplatin and capecitabine (DCX) in gastro-oesophageal adenocarcinoma: a phase II study of the Arbeitsgemeinschaft Internistische Onkologie (AIO){dagger}. Ann Oncol 2012;23:2827–2834.CrossRefPubMed

27.

Yoshida M, Ohtsu A, Boku N, Miyata Y, Shirao K, Shimada Y, Hyodo I, Koizumi W, Kurihara M, Yoshida S, Yamamoto S. Long-term survival and prognostic factors in patients with metastatic gastric cancers treated with chemotherapy in the Japan Clinical Oncology Group (JCOG) study. Jpn J Clin Oncol 2004;34:654–659.CrossRefPubMed

28.

Koizumi W, Narahara H, Hara T, Takagane A, Akiya T, Takagi M, Miyashita K, Nishizaki T, Kobayashi O, Takiyama W, Toh Y, Nagaie T, Takagi S, Yamamura Y, Yanaoka K, Orita H, Takeuchi M. S-1 plus cisplatin versus S-1 alone for first-line treatment of advanced gastric cancer (SPIRITS trial): a phase III trial. Lancet Oncol 2008;9:215–221.CrossRefPubMed

29.

Boku N, Yamamoto S, Fukuda H, Shirao K, Doi T, Sawaki A, Koizumi W, Saito H, Yamaguchi K, Takiuchi H, Nasu J, Ohtsu A. Fluorouracil versus combination of irinotecan plus cisplatin versus S-1 in metastatic gastric cancer: a randomised phase 3 study. Lancet Oncol 2009;10:1063–1069.CrossRefPubMed

30.

Koga R, Yamamoto J, Ohyama S, Saiura A, Seki M, Seto Y, Yamaguchi T. Liver resection for metastatic gastric cancer: experience with 42 patients including eight long-term survivors. Jpn J Clin Oncol 2007;37:836–842.CrossRefPubMed

31.

Morise Z, Sugioka A, Hoshimoto S, Kato T, Ikeda M, Uyama I, Horiguchi A, Miyakawa S. The role of hepatectomy for patients with liver metastases of gastric cancer. Hepatogastroenterology 2008;55:1238–1241.PubMed

32.

Shirabe K, Shimada M, Matsumata T, Higashi H, Yakeishi Y, Wakiyama S, Ikeda Y, Ezaki T, Fukuzawa S, Takenaka K, Kishikawa K, Ikeda T, Taguchi K, Maehara Y, Sugimachi K. Analysis of the prognostic factors for liver metastasis of gastric cancer after hepatic resection: a multi-institutional study of the indications for resection. Hepatogastroenterology 2003;50:1560–1563.PubMed

33.

Sakamoto Y, Sano T, Shimada K, Esaki M, Saka M, Fukagawa T, Katai H, Kosuge T, Sasako M. Favorable indications for hepatectomy in patients with liver metastasis from gastric cancer. J Surg Oncol 2007;95:534–539.CrossRefPubMed

34.

Qiu JL, Deng MG, Li W, Zou RH, Li BK, Zheng Y, Lao XM, Zhou K, Yuan YF. Hepatic resection for synchronous hepatic metastasis from gastric cancer. Eur J Surg Oncol 2013;39:694–700.CrossRefPubMed

35.

Zacherl J, Zacherl M, Scheuba C, Steininger R, Wenzl E, Muhlbacher F, Jakesz R, Langle F. Analysis of hepatic resection of metastasis originating from gastric adenocarcinoma. J Gastrointest Surg 2002;6:682–689.CrossRefPubMed

36.

Ambiru S, Miyazaki M, Ito H, Nakagawa K, Shimizu H, Yoshidome H, Shimizu Y, Nakajima N. Benefits and limits of hepatic resection for gastric metastases. Am J Surg 2001;181:279–283.CrossRefPubMed

37.

Adam R. Developing strategies for liver metastases from colorectal cancer. Semin Oncol 2007;34:7–11.CrossRef

38.

Nordlinger B, Sorbye H, Glimelius B, Poston GJ, Schlag PM, Rougier P, Bechstein WO, Primrose JN, Walpole ET, Finch-Jones M, Jaeck D, Mirza D, Parks RW, Collette L, Praet M, Bethe U, Van Cutsem E, Scheithauer W, Gruenberger T. Perioperative chemotherapy with FOLFOX4 and surgery versus surgery alone for resectable liver metastases from colorectal cancer (EORTC Intergroup trial 40983): a randomised controlled trial. Lancet 2008;371:1007–1016.PubMedCentralCrossRefPubMed

39.

Kopetz S, Chang GJ, Overman MJ, Eng C, Sargent DJ, Larson DW, Grothey A, Vauthey JN, Nagorney DM, McWilliams RR. Improved survival in metastatic colorectal cancer is associated with adoption of hepatic resection and improved chemotherapy. J Clin Oncol 2009;27:3677–3683.PubMedCentralCrossRefPubMed

40.

Chun YS, Vauthey JN, Boonsirikamchai P, Maru DM, Kopetz S, Palavecino M, Curley SA, Abdalla EK, Kaur H, Charnsangavej C, Loyer EM. Association of computed tomography morphologic criteria with pathologic response and survival in patients treated with bevacizumab for colorectal liver metastases. JAMA 2009;302:2338–2344.PubMedCentralCrossRefPubMed

41.

Shindoh J, Loyer EM, Kopetz S, Boonsirikamchai P, Maru DM, Chun YS, Zimmitti G, Curley SA, Charnsangavej C, Aloia TA, Vauthey JN. Optimal morphologic response to preoperative chemotherapy: an alternate outcome end point before resection of hepatic colorectal metastases. J Clin Oncol 2012;30:4566–4572.PubMedCentralCrossRefPubMed

42.

Brouquet A, Zimmitti G, Kopetz S, Stift J, Julie C, Lemaistre AI, Agarwal A, Patel V, Benoist S, Nordlinger B, Gandini A, Rivoire M, Stremitzer S, Gruenberger T, Vauthey JN, Maru DM. Multicenter validation study of pathologic response and tumor thickness at the tumor-normal liver interface as independent predictors of disease-free survival after preoperative chemotherapy and surgery for colorectal liver metastases. Cancer 2013;119:2778–2788.PubMedCentralCrossRefPubMed

43.

Thuss-Patience PC, Kretzschmar A, Dogan Y, Rothmann F, Blau I, Schwaner I, Breithaupt K, Bichev D, Grothoff M, Grieser C, Reichardt P. Docetaxel and capecitabine for advanced gastric cancer: investigating dose-dependent efficacy in two patient cohorts. Br J Cancer 2011;105:505–512.PubMedCentralCrossRefPubMed

44.

Stein A, Arnold D, Thuss-Patience PC, Moehler M, Grothe W, Seufferlein T, Reinacher-Schick A, Geissler M, Hofheinz RD, Schmoll HJ. Docetaxel, oxaliplatin and capecitabine (TEX regimen) in patients with metastatic gastric or gastro-esophageal cancer: results of a multicenter phase I/II study. Acta Oncol 2014;53:392–398.CrossRefPubMed

45.

Viganò L, Vellone M, Ferrero A, Giuliante F, Nuzzo G, Capussotti L. Liver Resection for Gastric Cancer Metastases. Hepatogastroenterology 2013;60:557–562.

46.

Geisel D, Denecke T, Collettini F, Grieser C, Wust P, Thuss-Patience P, Hamm B, Gebauer B. Treatment of hepatic metastases from gastric or gastroesophageal adenocarcinoma with computed tomography-guided high-dose-rate brachytherapy (CT-HDRBT). Anticancer Res 2012;32:5453–5458.PubMed

47.

Chen J, Tang Z, Dong X, Gao S, Fang H, Wu D, Xiang D, Zhang S. Radiofrequency ablation for liver metastasis from gastric cancer. Eur J Surg Oncol 2013;39:701–706.CrossRefPubMed

48.

Kerkar SP, Kemp CD, Duffy A, Kammula US, Schrump DS, Kwong KF, Quezado M, Goldspiel BR, Venkatesan A, Berger A, Walker M, Toomey MA, Steinberg SM, Giaccone G, Rosenberg SA, Avital I. The GYMSSA trial: a prospective randomized trial comparing gastrectomy, metastasectomy plus systemic therapy versus systemic therapy alone. Trials 2009;10:121.PubMedCentralCrossRefPubMed

49.

Fujitani K, Yang HK, Kurokawa Y, Park do J, Tsujinaka T, Park BJ, Fukuda H, Noh SH, Boku N, Bang YJ, Sasako M, Lee JI. 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;38:504–506.CrossRefPubMed

50.

Correa-Gallego C, Gonen M, Fischer M, Grant F, Kemeny NE, Arslan-Carlon V, Kingham TP, Dematteo RP, Fong Y, Allen PJ, D'Angelica MI, Jarnagin WR. Perioperative complications influence recurrence and survival after resection of hepatic colorectal metastases. Ann Surg Oncol 2013;20:2477–2484.CrossRefPubMed

51.

Mavros MN, de Jong M, Dogeas E, Hyder O, Pawlik TM. Impact of complications on long-term survival after resection of colorectal liver metastases. Br J Surg 2013;100:711–718.CrossRefPubMed

52.

Farid SG, Aldouri A, Morris-Stiff G, Khan AZ, Toogood GJ, Lodge JP, Prasad KR. Correlation between postoperative infective complications and long-term outcomes after hepatic resection for colorectal liver metastasis. Ann Surg 2010;251:91–100.CrossRefPubMed

53.

Ito H, Are C, Gonen M, D'Angelica M, Dematteo RP, Kemeny NE, Fong Y, Blumgart LH, Jarnagin WR. Effect of postoperative morbidity on long-term survival after hepatic resection for metastatic colorectal cancer. Ann Surg 2008;247:994–1002.CrossRefPubMed

54.

Tokunaga M, Tanizawa Y, Bando E, Kawamura T, Terashima M. Poor survival rate in patients with postoperative intra-abdominal infectious complications following curative gastrectomy for gastric cancer. Ann Surg Oncol 2013;20:1575–1583.CrossRefPubMed

55.

Li QG, Li P, Tang D, Chen J, Wang DR. Impact of postoperative complications on long-term survival after radical resection for gastric cancer. World J Gastroenterol 2013;19:4060–4065.PubMedCentralCrossRefPubMed

56.

Rizk NP, Bach PB, Schrag D, Bains MS, Turnbull AD, Karpeh M, Brennan MF, Rusch VW. The impact of complications on outcomes after resection for esophageal and gastroesophageal junction carcinoma. J Am Coll Surg 2004;198:42–50.CrossRefPubMed

57.

Lerut T, Moons J, Coosemans W, Van Raemdonck D, De Leyn P, Decaluwe H, Decker G, Nafteux P. Postoperative complications after transthoracic esophagectomy for cancer of the esophagus and gastroesophageal junction are correlated with early cancer recurrence: role of systematic grading of complications using the modified Clavien classification. Ann Surg 2009;250:798–807.CrossRefPubMed

58.

Schiesser M, Chen JW, Maddern GJ, Padbury RT. Perioperative morbidity affects long-term survival in patients following liver resection for colorectal metastases. J Gastrointest Surg 2008;12:1054–1060.CrossRefPubMed

59.

Tanaka K, Kumamoto T, Nojiri K, Matsuyama R, Takeda K, Endo I. Impact of Postoperative morbidity on long-term survival after resection for colorectal liver metastases. Ann Surg Oncol 2010; [Epub ahead of print].

60.

Sietses C, Beelen RH, Meijer S, Cuesta MA. Immunological consequences of laparoscopic surgery, speculations on the cause and clinical implications. Langenbecks Arch Surg 1999;384:250–258.CrossRefPubMed

61.

Goldfarb Y, Sorski L, Benish M, Levi B, Melamed R, Ben-Eliyahu S. Improving postoperative immune status and resistance to cancer metastasis: a combined perioperative approach of immunostimulation and prevention of excessive surgical stress responses. Ann Surg 2011;253:798–810.CrossRefPubMed

62.

Chauhan A, House MG, Pitt HA, Nakeeb A, Howard TJ, Zyromski NJ, Schmidt CM, Ball CG, Lillemoe KD. Post-operative morbidity results in decreased long-term survival after resection for hilar cholangiocarcinoma. HPB (Oxford) 2011;13:139–147.CrossRef

Title: Response to Preoperative Chemotherapy Predicts Survival in Patients Undergoing Hepatectomy for Liver Metastases from Gastric and Esophageal Cancer
Authors: Andreas Andreou
Luca Viganò
Giuseppe Zimmitti
Daniel Seehofer
Martin Dreyer
Andreas Pascher
Marcus Bahra
Wenzel Schoening
Volker Schmitz
Peter C. Thuss-Patience
Timm Denecke
Gero Puhl
Jean-Nicolas Vauthey
Peter Neuhaus
Lorenzo Capussotti
Johann Pratschke
Sven-Christian Schmidt
Publication date: 01-11-2014
Publisher: Springer US
Published in: Journal of Gastrointestinal Surgery / Issue 11/2014
Print ISSN: 1091-255X
Electronic ISSN: 1873-4626
DOI: https://doi.org/10.1007/s11605-014-2623-0

At a glance: The STEP trials

Springer Medicine

Response to Preoperative Chemotherapy Predicts Survival in Patients Undergoing Hepatectomy for Liver Metastases from Gastric and Esophageal Cancer

Abstract

Background

Methods

Results

Conclusion

At a glance: The STEP trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

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