Resection of colorectal liver metastases and extra-hepatic disease: a systematic review and proportional meta-analysis of survival outcomes

William J Hadden, Philip R de Reuver, Kai Brown, Anubhav Mittal, Jaswinder S Samra, Thomas J Hugh, William J Hadden, Philip R de Reuver, Kai Brown, Anubhav Mittal, Jaswinder S Samra, Thomas J Hugh

Abstract

Background: Colorectal cancer (CRC) accounts for 9.7% of all cancers with 1.4 million new cases diagnosed each year. 19-31% of CRC patients develop colorectal liver metastases (CRLM), and 23-38% develop extra-hepatic disease (EHD). The aim of this systematic review was to determine overall survival (OS) in patients resected for CRLM and known EHD.

Methods: A systematic review was undertaken to identify studies reporting OS after resection for CRLM in the presence of EHD. Proportional meta-analyses and relative risk of death before five years were assessed between patient groups.

Results: A total of 15,144 patients with CRLM (2308 with EHD) from 52 studies were included. Three and 5-year OS were 58% and 26% for lung, 37% and 17% for peritoneum, and 35% and 15% for lymph nodes, respectively. The combined relative risk of death by five years was 1.49 (95% CI = 1.34-1.66) for lung, 1.59 (95% CI = 1.16-2.17) for peritoneal and 1.70 (95% CI = 1.57-1.84) for lymph node EHD, in favour of resection in the absence of EHD.

Conclusion: This review supports attempts at R0 resection in selected patients and rejects the notion that EHD is an absolute contraindication to resection.

Copyright © 2016 International Hepato-Pancreato-Biliary Association Inc. Published by Elsevier Ltd. All rights reserved.

Figures

Figure 1
Figure 1
Search strategy applied to PubMed database
Figure 2
Figure 2
Proportional meta-analyses of three and 5-year overall survival in patients resected for CRLM and EHD in the (a) lung,, , , , , , , , (b) peritoneum, , , , , , , , , , and (c) lymph nodes, , , , , , , , , ,
Figure 3
Figure 3
Forest plot comparing 5-year overall survival in patients resected for CRLM without EHD versus patients resected for both CRLM and EHD in the (a) lung,, , (b) peritoneum, , , and (c) lymph nodes, , , , , ,
https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4814625/bin/fx1.jpg

References

    1. Ferlay J., Soerjomataram I., Dikshit R., Eser S., Mathers C., Rebelo M. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136:E359–E386.
    1. Kune G.A., Kune S., Field B., White R., Brough W., Schellenberger R. Survival in patients with large-bowel cancer. A population-based investigation from the Melbourne Colorectal Cancer Study. Dis Colon Rectum. 1990;33:938–946.
    1. Manfredi S., Lepage C., Hatem C., Coatmeur O., Faivre J., Bouvier A.M. Epidemiology and management of liver metastases from colorectal cancer. Ann Surg. 2006;244:254–259.
    1. van der Geest L.G., Lam-Boer J., Koopman M., Verhoef C., Elferink M.A., de Wilt J.H. Nationwide trends in incidence, treatment and survival of colorectal cancer patients with synchronous metastases. Clin Exp Metastasis. 2015;32:457–465.
    1. Kohne C.H., van Cutsem E., Wils J., Bokemeyer C., El-Serafi M., Lutz M.P. Phase III study of weekly high-dose infusional fluorouracil plus folinic acid with or without irinotecan in patients with metastatic colorectal cancer: European Organisation for Research and Treatment of Cancer Gastrointestinal Group Study 40986. J Clin Oncol. 2005;23:4856–4865.
    1. Giantonio B.J., Catalano P.J., Meropol N.J., O'Dwyer P.J., Mitchell E.P., Alberts S.R. Bevacizumab in combination with oxaliplatin, fluorouracil, and leucovorin (FOLFOX4) for previously treated metastatic colorectal cancer: results from the Eastern Cooperative Oncology Group Study E3200. J Clin Oncol. 2007;25:1539–1544.
    1. Van Cutsem E., Kohne C.H., Hitre E., Zaluski J., Chang Chien C.R., Makhson A. Cetuximab and chemotherapy as initial treatment for metastatic colorectal cancer. N Engl J Med. 2009;360:1408–1417.
    1. Gallagher D.J., Kemeny N. Metastatic colorectal cancer: from improved survival to potential cure. Oncology. 2010;78:237–248.
    1. Adam R., Vinet E. Regional treatment of metastasis: surgery of colorectal liver metastases. Ann Oncol. 2004;15(Suppl. 4):iv103–iv106.
    1. Elias D., Ouellet J.F., Bellon N., Pignon J.P., Pocard M., Lasser P. Extrahepatic disease does not contraindicate hepatectomy for colorectal liver metastases. Br J Surg. 2003;90:567–574.
    1. Hugh T.J., Kinsella A.R., Poston G.J. Management strategies for colorectal liver metastases–Part II. Surg Oncol. 1997;6:31–48.
    1. Pawlik T.M., Schulick R.D., Choti M.A. Expanding criteria for resectability of colorectal liver metastases. Oncologist. 2008;13:51–64.
    1. Poston G.J., Adam R., Alberts S., Curley S., Figueras J., Haller D. OncoSurge: a strategy for improving resectability with curative intent in metastatic colorectal cancer. J Clin Oncol. 2005;23:7125–7134.
    1. Scheele J., Stangl R., Altendorf-Hofmann A. Hepatic metastases from colorectal carcinoma: impact of surgical resection on the natural history. Br J Surg. 1990;77:1241–1246.
    1. Narita M., Oussoultzoglou E., Bachellier P., Jaeck D., Uemoto S. Post-hepatectomy liver failure in patients with colorectal liver metastases. Surg Today. 2015;45:1218–1226.
    1. Carpizo D.R., Are C., Jarnagin W., Dematteo R., Fong Y., Gonen M. Liver resection for metastatic colorectal cancer in patients with concurrent extrahepatic disease: results in 127 patients treated at a single center. Ann Surg Oncol. 2009;16:2138–2146.
    1. Hughes K.S., Simon R., Songhorabodi S., Adson M.A., Ilstrup D.M., Fortner J.G. Resection of the liver for colorectal carcinoma metastases: a multi-institutional study of patterns of recurrence. Surgery. 1986;100:278–284.
    1. van Ooijen B., Wiggers T., Meijer S., van der Heijde M.N., Slooff M.J., van de Velde C.J. Hepatic resections for colorectal metastases in The Netherlands. A multiinstitutional 10-year study. Cancer. 1992;70:28–34.
    1. Adams R.B., Aloia T.A., Loyer E., Pawlik T.M., Taouli B., Vauthey J.N. Selection for hepatic resection of colorectal liver metastases: expert consensus statement. HPB. 2013;15:91–103.
    1. Siriwardena A.K., Mason J.M., Mullamitha S., Hancock H.C., Jegatheeswaran S. Management of colorectal cancer presenting with synchronous liver metastases. Nat Rev Clin Oncol. 2014;11:446–459.
    1. Moher D., Liberati A., Tetzlaff J., Altman D.G. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg. 2010;8:336–341.
    1. Stroup D.F., Berlin J.A., Morton S.C., Olkin I., Williamson G.D., Rennie D. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000;283:2008–2012.
    1. Phillips B., Ball C., Sackett D., Badenoch D., Straus S., Haynes B. CEBM; 2009. Oxford Centre for evidence-based medicine – levels of evidence (March 2009)
    1. Downs S.H., Black N. The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J Epidemiol Community Health. 1998;52:377–384.
    1. Freeman M.F., Tukey J.W. Transformations related to the angular and the square root. Ann Math Stat. 1950:607–611.
    1. DerSimonian R., Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177–188.
    1. Mantel N., Haenszel W. Statistical aspects of the analysis of data from retrospective studies. J Natl Cancer Inst. 1959;22:719–748.
    1. Elias D., Liberale G., Vernerey D., Pocard M., Ducreux M., Boige V. Hepatic and extrahepatic colorectal metastases: when resectable, their localization does not matter, but their total number has a prognostic effect. Ann Surg Oncol. 2005;12:900–909.
    1. Elias D., Benizri E., Pocard M., Ducreux M., Boige V., Lasser P. Treatment of synchronous peritoneal carcinomatosis and liver metastases from colorectal cancer. Eur J Surg Oncol. 2006;32:632–636.
    1. Minagawa M., Yamamoto J., Miwa S., Sakamoto Y., Kokudo N., Kosuge T. Selection criteria for simultaneous resection in patients with synchronous liver metastasis. Arch Surg. 2006;141:1006–1012. discussion 1013.
    1. Figueras J., Torras J., Valls C., Llado L., Ramos E., Marti-Rague J. Surgical resection of colorectal liver metastases in patients with expanded indications: a single-center experience with 501 patients. Dis Colon Rectum. 2007;50:478–488.
    1. Kianmanesh R., Scaringi S., Sabate J.M., Castel B., Pons-Kerjean N., Coffin B. Iterative cytoreductive surgery associated with hyperthermic intraperitoneal chemotherapy for treatment of peritoneal carcinomatosis of colorectal origin with or without liver metastases. Ann Surg. 2007;245:597–603.
    1. Aoki T., Umekita N., Tanaka S., Noda K., Warabi M., Kitamura M. Prognostic value of concomitant resection of extrahepatic disease in patients with liver metastases of colorectal origin. Surgery. 2008;143:706–714.
    1. Byam J., Reuter N.P., Woodall C.E., Scoggins C.R., McMasters K.M., Martin R.C. Should hepatic metastatic colorectal cancer patients with extrahepatic disease undergo liver resection/ablation? Ann Surg Oncol. 2009;16:3064–3069.
    1. Chua T.C., Yan T.D., Zhao J., Morris D.L. Peritoneal carcinomatosis and liver metastases from colorectal cancer treated with cytoreductive surgery perioperative intraperitoneal chemotherapy and liver resection. Eur J Surg Oncol. 2009;35:1299–1305.
    1. Oussoultzoglou E., Romain B., Panaro F., Rosso E., Pessaux P., Bachellier P. Long-term survival after liver resection for colorectal liver metastases in patients with hepatic pedicle lymph nodes involvement in the era of new chemotherapy regimens. Ann Surg. 2009;249:879–886.
    1. Varban O., Levine E.A., Stewart J.H., McCoy T.P., Shen P. Outcomes associated with cytoreductive surgery and intraperitoneal hyperthermic chemotherapy in colorectal cancer patients with peritoneal surface disease and hepatic metastases. Cancer. 2009;115:3427–3436.
    1. Elias D., Gilly F., Boutitie F., Quenet F., Bereder J.M., Mansvelt B. Peritoneal colorectal carcinomatosis treated with surgery and perioperative intraperitoneal chemotherapy: retrospective analysis of 523 patients from a multicentric French study. J Clin Oncol. 2010;28:63–68.
    1. Adam R., de Haas R.J., Wicherts D.A., Vibert E., Salloum C., Azoulay D. Concomitant extrahepatic disease in patients with colorectal liver metastases: when is there a place for surgery? Ann Surg. 2011;253:349–359.
    1. Pulitano C., Bodingbauer M., Aldrighetti L., de Jong M.C., Castillo F., Schulick R.D. Liver resection for colorectal metastases in presence of extrahepatic disease: results from an international multi-institutional analysis. Ann Surg Oncol. 2011;18:1380–1388.
    1. Allard M.A., Adam R., Ruiz A., Vibert E., Paule B., Levi F. Is unexpected peritoneal carcinomatosis still a contraindication for resection of colorectal liver metastases? Combined resection of colorectal liver metastases with peritoneal deposits discovered intra-operatively. Eur J Surg Oncol. 2013;39:981–987.
    1. Maggiori L., Goere D., Viana B., Tzanis D., Dumont F., Honore C. Should patients with peritoneal carcinomatosis of colorectal origin with synchronous liver metastases be treated with a curative intent? A case-control study. Ann Surg. 2013;258:116–121.
    1. Tanaka K., Shimada H., Nagano Y., Endo I., Sekido H., Togo S. Outcome after hepatic resection versus combined resection and microwave ablation for multiple bilobar colorectal metastases to the liver. Surgery. 2006;139:263–273.
    1. Favero A., Benzoni E., Zompicchiatti A., Rossit L., Bresadola F., De Anna D. Surgery in hepatic and extrahepatic colorectal metastases. G Chir. 2007;28:307–311.
    1. Kornprat P., Jarnagin W.R., Gonen M., DeMatteo R.P., Fong Y., Blumgart L.H. Outcome after hepatectomy for multiple (four or more) colorectal metastases in the era of effective chemotherapy. Ann Surg Oncol. 2007;14:1151–1160.
    1. Takahashi S., Nagai K., Saito N., Konishi M., Nakagohri T., Gotohda N. Multiple resections for hepatic and pulmonary metastases of colorectal carcinoma. Jpn J Clin Oncol. 2007;37:186–192.
    1. Zakaria S., Donohue J.H., Que F.G., Farnell M.B., Schleck C.D., Ilstrup D.M. Hepatic resection for colorectal metastases: value for risk scoring systems? Ann Surg. 2007;246:183–191.
    1. Adam R., de Haas R.J., Wicherts D.A., Aloia T.A., Delvart V., Azoulay D. Is hepatic resection justified after chemotherapy in patients with colorectal liver metastases and lymph node involvement? J Clin Oncol. 2008;26:3672–3680.
    1. Bennett J.J., Schmidt C.R., Klimstra D.S., Grobmyer S.R., Ishill N.M., D'Angelica M. Perihepatic lymph node micrometastases impact outcome after partial hepatectomy for colorectal metastases. Ann Surg Oncol. 2008;15:1130–1136.
    1. Rees M., Tekkis P.P., Welsh F.K., O'Rourke T., John T.G. Evaluation of long-term survival after hepatic resection for metastatic colorectal cancer: a multifactorial model of 929 patients. Ann Surg. 2008;247:125–135.
    1. Maithel S.K., Ginsberg M.S., D'Amico F., DeMatteo R.P., Allen P.J., Fong Y. Natural history of patients with subcentimeter pulmonary nodules undergoing hepatic resection for metastatic colorectal cancer. J Am Coll Surg. 2010;210:31–38.
    1. Pulitano C., Bodingbauer M., Aldrighetti L., Choti M.A., Castillo F., Schulick R.D. Colorectal liver metastasis in the setting of lymph node metastasis: defining the benefit of surgical resection. Ann Surg Oncol. 2012;19:435–442.
    1. Ishibashi K., Ishida H., Ohsawa T., Okada N., Kumamoto K., Haga N. Impact of hepatic lymph node metastasis on survival of patients with synchronous resectable or unresectable liver metastases of colorectal cancer. Tech Coloproctol. 2013;17:51–57.
    1. Mavros M.N., Hyder O., Pulitano C., Aldrighetti L., Pawlik T.M. Survival of patients operated for colorectal liver metastases and concomitant extra-hepatic disease: external validation of a prognostic model. J Surg Oncol. 2013;107:481–485.
    1. Liu W., Yan X.L., Wang K., Bao Q., Sun Y., Xing B.C. The outcome of liver resection and lymphadenectomy for hilar lymph node involvement in colorectal cancer liver metastases. Int J Colorectal Dis. 2014;29:737–745.
    1. House M.G., Ito H., Gonen M., Fong Y., Allen P.J., DeMatteo R.P. Survival after hepatic resection for metastatic colorectal cancer: trends in outcomes for 1,600 patients during two decades at a single institution. J Am Coll Surg. 2010;210:744–752. 752–745.
    1. Tamandl D., Gruenberger B., Herberger B., Schoppmann S., Bodingbauer M., Schindl M. Selective resection of colorectal liver metastases. Eur J Surg Oncol. 2007;33:174–182.
    1. Adson M.A. Resection of liver metastases–when is it worthwhile? World J Surg. 1987;11:511–520.
    1. Simmonds P.C., Primrose J.N., Colquitt J.L., Garden O.J., Poston G.J., Rees M. Surgical resection of hepatic metastases from colorectal cancer: a systematic review of published studies. Br J Cancer. 2006;94:982–999.
    1. de Jong M.C., Pulitano C., Ribero D., Strub J., Mentha G., Schulick R.D. Rates and patterns of recurrence following curative intent surgery for colorectal liver metastasis: an international multi-institutional analysis of 1669 patients. Ann Surg. 2009;250:440–448.
    1. Fong Y., Fortner J., Sun R.L., Brennan M.F., Blumgart L.H. Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg. 1999;230:309–318. discussion 318–321.
    1. Ferrarotto R., Pathak P., Maru D., Agarwal A., Overman M., Hoff P.M. Durable complete responses in metastatic colorectal cancer treated with chemotherapy alone. Clin Colorectal Cancer. 2011;10:178–182.
    1. Simmonds P.C. Palliative chemotherapy for advanced colorectal cancer: systematic review and meta-analysis. Colorectal Cancer Collaborative Group. BMJ. 2000;321:531–535.
    1. Chua T.C., Saxena A., Liauw W., Chu F., Morris D.L. Hepatectomy and resection of concomitant extrahepatic disease for colorectal liver metastases–a systematic review. Eur J Cancer. 2012;48:1757–1765.
    1. Hwang M., Jayakrishnan T.T., Green D.E., George B., Thomas J.P., Groeschl R.T. Systematic review of outcomes of patients undergoing resection for colorectal liver metastases in the setting of extra hepatic disease. Eur J Cancer. 2014;50:1747–1757.
    1. Mise Y., Kopetz S., Mehran R.J., Aloia T.A., Conrad C., Brudvik K.W. Is complete liver resection without resection of synchronous lung metastases justified? Ann Surg Oncol. 2014;22:1218–1226.
    1. Robinson B.J., Rice T.W., Strong S.A., Rybicki L.A., Blackstone E.H. Is resection of pulmonary and hepatic metastases warranted in patients with colorectal cancer? J Thorac Cardiovasc Surg. 1999;117:66–75. discussion 75–66.
    1. Center VUUM. Chemotherapy and Maximal Tumor Debulking of Multi-organ Colorectal Cancer Metastases – Full Text View – 2015. Available from: .
    1. Beppu T., Sakamoto Y., Hasegawa K., Honda G., Tanaka K., Kotera Y. A nomogram predicting disease-free survival in patients with colorectal liver metastases treated with hepatic resection: multicenter data collection as a Project Study for Hepatic Surgery of the Japanese Society of Hepato-Biliary-Pancreatic Surgery. J Hepatobiliary Pancreat Sci. 2012;19:72–84.
    1. Edwards J., Scoggins C., McMasters K., Martin R. Combined pancreas and liver therapies: resection and ablation in hepato-pancreatico-biliary malignancies. J Surg Oncol. 2013;107:709–712.
    1. Gomez D., Kamali D., Dunn W.K., Beckingham I.J., Brooks A., Cameron I.C. Outcomes in patients with indeterminate pulmonary nodules undergoing resection for colorectal liver metastases. HPB. 2012;14:448–454.
    1. Hattori N., Kanemitsu Y., Komori K., Shimizu Y., Sano T., Senda Y. Outcomes after hepatic and pulmonary metastasectomies compared with pulmonary metastasectomy alone in patients with colorectal cancer metastasis to liver and lungs. World J Surg. 2013;37:1315–1321.
    1. Hemming A.W., Magliocca J.F., Fujita S., Kayler L.K., Hochwald S., Zendejas I. Combined resection of the liver and pancreas for malignancy. J Am Coll Surg. 2010;210:808–814. 814–806.
    1. Karanjia N.D., Lordan J.T., Fawcett W.J., Quiney N., Worthington T.R. Survival and recurrence after neo-adjuvant chemotherapy and liver resection for colorectal metastases: a ten year study. Eur J Surg Oncol. 2009;35:838–843.
    1. Kawano D., Takeo S., Tsukamoto S., Katsura M., Masuyama E., Nakaji Y. Prediction of the prognosis and surgical indications for pulmonary metastectomy from colorectal carcinoma in patients with combined hepatic metastases. Lung Cancer. 2012;75:209–212.
    1. Lordan J.T., Riga A., Worthington T.R., Karanjia N.D. Early and long-term outcomes of patients undergoing liver resection and diaphragm excision for advanced colorectal liver metastases. Ann R Coll Surg Engl. 2009;91:483–488.
    1. Marin C., Robles R., Lopez Conesa A., Torres J., Flores D.P., Parrilla P. Outcome of strict patient selection for surgical treatment of hepatic and pulmonary metastases from colorectal cancer. Dis Colon Rectum. 2013;56:43–50.
    1. Marudanayagam R., Ramkumar K., Shanmugam V., Langman G., Rajesh P., Coldham C. Long-term outcome after sequential resections of liver and lung metastases from colorectal carcinoma. HPB. 2009;11:671–676.
    1. Meimarakis G., Angele M., Conrad C., Schauer R., Weidenhagen R., Crispin A. Combined resection of colorectal hepatic-pulmonary metastases shows improved outcome over chemotherapy alone. Langenbecks Arch Surg. 2013;398:265–276.
    1. Miller G., Biernacki P., Kemeny N.E., Gonen M., Downey R., Jarnagin W.R. Outcomes after resection of synchronous or metachronous hepatic and pulmonary colorectal metastases. J Am Coll Surg. 2007;205:231–238.
    1. Neeff H., Horth W., Makowiec F., Fischer E., Imdahl A., Hopt U.T. Outcome after resection of hepatic and pulmonary metastases of colorectal cancer. J Gastrointest Surg. 2009;13:1813–1820.
    1. Niu R., Yan T.D., Zhu J.C., Black D., Chu F., Morris D.L. Recurrence and survival outcomes after hepatic resection with or without cryotherapy for liver metastases from colorectal carcinoma. Ann Surg Oncol. 2007;14:2078–2087.
    1. Reissfelder C., Rahbari N.N., Koch M., Ulrich A., Pfeilschifter I., Waltert A. Validation of prognostic scoring systems for patients undergoing resection of colorectal cancer liver metastases. Ann Surg Oncol. 2009;16:3279–3288.
    1. Shah S.A., Haddad R., Al-Sukhni W., Kim R.D., Greig P.D., Grant D.R. Surgical resection of hepatic and pulmonary metastases from colorectal carcinoma. J Am Coll Surg. 2006;202:468–475.
    1. Tanaka K., Shimada H., Matsumoto C., Matsuo K., Takeda K., Nagano Y. Impact of the degree of liver resection on survival for patients with multiple liver metastases from colorectal cancer. World J Surg. 2008;32:2057–2069.
    1. Tanaka K., Shimada H., Ueda M., Matsuo K., Endo I., Togo S. Long-term characteristics of 5-year survivors after liver resection for colorectal metastases. Ann Surg Oncol. 2007;14:1336–1346.
    1. Tsukioka T., Nishiyama N., Iwata T., Nagano K., Izumi N., Mizuguchi S. Pulmonary metastasis from colorectal carcinoma with hepatic metastasis. Gen Thorac Cardiovasc Surg. 2007;55:455–460.
    1. van der Pool A.E., Lalmahomed Z.S., Ozbay Y., de Wilt J.H., Eggermont A.M., Jzermans J.N. ‘Staged’ liver resection in synchronous and metachronous colorectal hepatic metastases: differences in clinicopathological features and outcome. Colorectal Dis. 2010;12:e229–235.
    1. Wicherts D.A., Miller R., de Haas R.J., Bitsakou G., Vibert E., Veilhan L.A. Long-term results of two-stage hepatectomy for irresectable colorectal cancer liver metastases. Ann Surg. 2008;248:994–1005.

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