Skip to main content
Erschienen in: Clinical and Translational Oncology 8/2020

08.01.2020 | Research Article

Different variables predict the outcome of patients with synchronous versus metachronous metastases of colorectal cancer

verfasst von: G. A. Colloca, A. Venturino, D. Guarneri

Erschienen in: Clinical and Translational Oncology | Ausgabe 8/2020

Einloggen, um Zugang zu erhalten

Abstract

Purpose

Timing of metastasis is a controversial prognostic factor for patients with metastatic colorectal cancer (mCRC), as well as the performance of the common prognostic variables within patients with synchronous (SMs) or metachronous metastases (MMs). The aim of the current study is to evaluate outcome by the timing of metastases and to explore different tumor characteristics associated with SMs and MMs.

Methods

Data were collected from the clinical records of patients with mCRC, which were referred to the Department of Oncology of the Ospedale Civile di Sanremo from 2006 to 2011. A comparison of the characteristics of tumors of patients, overall and by the timing of metastases, and a Cox regression analysis have been performed to select the most relevant prognostic factors. Finally, the characteristics of the variables associated with the outcome were analyzed through a logistic regression.

Results

Two hundreds fifteen patients with SMs and two hundreds ten with MMs were included. Patients with SMs reported a poor prognosis (18.5 versus 62.8 months; p value < 0.001). Among patients with SMs there was a significant difference in overall survival between patients with a CEA-positive or negative disease, while no difference was present among patients with MMs. After multivariate analysis, only within the SMs group the occurrence of liver metastases was related to a CEA-positive disease.

Conclusions

Within the cohort of SMs high CEA levels, occurrence of liver metastases and right-sided colon tumors were associated with a very poor prognosis, whereas no relationship was detectable in the group of patients with MMs.
Literatur
1.
Zurück zum Zitat Malvezzi M, Carioli G, Bertuccio P, Boffetta P, Levi F, La Vecchia C. European cancer mortality prediction for the year 2017, with focus on lung cancer. Ann Oncol. 2017;28:1117–23.PubMedCrossRef Malvezzi M, Carioli G, Bertuccio P, Boffetta P, Levi F, La Vecchia C. European cancer mortality prediction for the year 2017, with focus on lung cancer. Ann Oncol. 2017;28:1117–23.PubMedCrossRef
2.
Zurück zum Zitat Van der Geest LGM, Lam-Boer J, Koopman M, Verhoef C, Elferink MAG, de Wilt JHW. Nationwide trends in incidence, treatment and survival of colorectal cancer patients with synchronous metastases. Clin Exp Metastasis. 2015;32:457–65.PubMed Van der Geest LGM, Lam-Boer J, Koopman M, Verhoef C, Elferink MAG, de Wilt JHW. Nationwide trends in incidence, treatment and survival of colorectal cancer patients with synchronous metastases. Clin Exp Metastasis. 2015;32:457–65.PubMed
3.
Zurück zum Zitat Ghiringhelli F, Hennequin A, Drouillard A, Lepage C, Faivre J, Bouvier AM. Epidemiology and prognosis of synchronous and metachronous colon cancer metastases: a French population-based study. Dig Liver Dis. 2014;46:854–8.PubMedCrossRef Ghiringhelli F, Hennequin A, Drouillard A, Lepage C, Faivre J, Bouvier AM. Epidemiology and prognosis of synchronous and metachronous colon cancer metastases: a French population-based study. Dig Liver Dis. 2014;46:854–8.PubMedCrossRef
4.
Zurück zum Zitat Manfredi S, Lepage C, Hatem C, Coatmeur O, Faivre J, Bouvier AM. Epidemiology and management of liver metastases from colorectal cancer. Ann Surg. 2006;244:254–9.PubMedPubMedCentralCrossRef Manfredi S, Lepage C, Hatem C, Coatmeur O, Faivre J, Bouvier AM. Epidemiology and management of liver metastases from colorectal cancer. Ann Surg. 2006;244:254–9.PubMedPubMedCentralCrossRef
5.
Zurück zum Zitat Elferink MAG, de Jong KP, Klaase JM, Siemerink EJ, del Wilt JHW. Metachronous metastases from colorectal cancer: a population-based study in North-East Netherlands. Int J Colorectal Dis. 2014;30:205–12.PubMedCrossRef Elferink MAG, de Jong KP, Klaase JM, Siemerink EJ, del Wilt JHW. Metachronous metastases from colorectal cancer: a population-based study in North-East Netherlands. Int J Colorectal Dis. 2014;30:205–12.PubMedCrossRef
6.
Zurück zum Zitat Tan EK, Ooi LLPJ. Colorectal cancer liver metastases – understanding the differences in the management of synchronous and metachronous disease. Ann Acad Med Singap. 2010;39:709–15. Tan EK, Ooi LLPJ. Colorectal cancer liver metastases – understanding the differences in the management of synchronous and metachronous disease. Ann Acad Med Singap. 2010;39:709–15.
7.
Zurück zum Zitat Kumar R, Price TJ, Beeke C, Jain K, Patel G, Padbury R, Young GP, Roder D, Townsend A, Bishnoi S, Karapetis CS. Colorectal cancer survival: an analysis of patients with metastatic disease synchronous and metachronous with the primary tumor. Clin Colorectal Cancer. 2014;13:87–93.PubMedCrossRef Kumar R, Price TJ, Beeke C, Jain K, Patel G, Padbury R, Young GP, Roder D, Townsend A, Bishnoi S, Karapetis CS. Colorectal cancer survival: an analysis of patients with metastatic disease synchronous and metachronous with the primary tumor. Clin Colorectal Cancer. 2014;13:87–93.PubMedCrossRef
8.
Zurück zum Zitat Mitry E, Guiu B, Cosconea S, Jooste V, Faivre J, Bouvier AM. Epidemiology, management and prognosis of colorectal cancer with lung metastases: a 30-year population-based study. Gut. 2010;59:1383–8.PubMedCrossRef Mitry E, Guiu B, Cosconea S, Jooste V, Faivre J, Bouvier AM. Epidemiology, management and prognosis of colorectal cancer with lung metastases: a 30-year population-based study. Gut. 2010;59:1383–8.PubMedCrossRef
9.
Zurück zum Zitat Martin R, Paty P, Fong Y, Grace A, Cohen A, DeMatteo R, Jarnagin W, Blumgart L. Simultaneous liver and colorectal resections are safe for synchronous colorectal liver metastases. J Am Coll Surg. 2003;197:233–42.PubMedCrossRef Martin R, Paty P, Fong Y, Grace A, Cohen A, DeMatteo R, Jarnagin W, Blumgart L. Simultaneous liver and colorectal resections are safe for synchronous colorectal liver metastases. J Am Coll Surg. 2003;197:233–42.PubMedCrossRef
10.
Zurück zum Zitat Goey KKH, 't Lam-Boer J, de Wilt JHW, Punt CJA, van Oijen MGH, Koopman M. Significant increase of synchronous disease in first-line metastatic colorectal cancer trials: results of a systematic review. Eur J Cancer. 2016;69:166–77. Goey KKH, 't Lam-Boer J, de Wilt JHW, Punt CJA, van Oijen MGH, Koopman M. Significant increase of synchronous disease in first-line metastatic colorectal cancer trials: results of a systematic review. Eur J Cancer. 2016;69:166–77.
11.
Zurück zum Zitat Tsai MS, Su YH, Ho MC, Liang JT, Chen TP, Lai HS, Lee PH. Clinicopathological features and prognosis in resectable synchronous and metachronous colorectal liver metastasis. Ann Surg Oncol. 2007;14:786–94.PubMedCrossRef Tsai MS, Su YH, Ho MC, Liang JT, Chen TP, Lai HS, Lee PH. Clinicopathological features and prognosis in resectable synchronous and metachronous colorectal liver metastasis. Ann Surg Oncol. 2007;14:786–94.PubMedCrossRef
12.
Zurück zum Zitat Bockhorn M, Frilling A, Fruhauf NR, Neuhaus J, Molmenti E, Trarbech T, Malagò M, Lang H, Broelsch CE. Survival of patients with synchronous and metachronous colorectal liver metastases—is there a difference? J Gastrointest Surg. 2008;12:1399–405.PubMedCrossRef Bockhorn M, Frilling A, Fruhauf NR, Neuhaus J, Molmenti E, Trarbech T, Malagò M, Lang H, Broelsch CE. Survival of patients with synchronous and metachronous colorectal liver metastases—is there a difference? J Gastrointest Surg. 2008;12:1399–405.PubMedCrossRef
13.
Zurück zum Zitat Stillwell AP, Buettner PG, Ho YH. Meta-analysis of survival of patients with stage IV colorectal cancer managed with surgical resection versus chemotherapy alone. World J Surg. 2010;34(4):797–807.PubMedCrossRef Stillwell AP, Buettner PG, Ho YH. Meta-analysis of survival of patients with stage IV colorectal cancer managed with surgical resection versus chemotherapy alone. World J Surg. 2010;34(4):797–807.PubMedCrossRef
14.
Zurück zum Zitat van Rooijen KL, Shi Q, Goey KKH, Meyers J, Heinemann V, Diaz-Rubio E, Aranda E, Falcone A, Green E, de Gramont A, Sargent DJ, Punt CJA, Koopman M. Prognostic value of primary tumor resection in synchronous metastatic colorectal cancer: individual patient data analysis of first-line randomised trials from the ARCAD database. Eur J Cancer. 2018;91:99–106.PubMedCrossRef van Rooijen KL, Shi Q, Goey KKH, Meyers J, Heinemann V, Diaz-Rubio E, Aranda E, Falcone A, Green E, de Gramont A, Sargent DJ, Punt CJA, Koopman M. Prognostic value of primary tumor resection in synchronous metastatic colorectal cancer: individual patient data analysis of first-line randomised trials from the ARCAD database. Eur J Cancer. 2018;91:99–106.PubMedCrossRef
15.
Zurück zum Zitat Alawadi Z, Phatak UR, Hu CY, Bailey CE, You YN, Kao LS, Massarweh NN, Feig BW, Bigas MA, Skibber JM, Chang GJ. Comparative effectiveness of primary tumor resection in patients with stage IV colon cancer. Cancer. 2017;123:1124–33.PubMedCrossRef Alawadi Z, Phatak UR, Hu CY, Bailey CE, You YN, Kao LS, Massarweh NN, Feig BW, Bigas MA, Skibber JM, Chang GJ. Comparative effectiveness of primary tumor resection in patients with stage IV colon cancer. Cancer. 2017;123:1124–33.PubMedCrossRef
16.
Zurück zum Zitat Wong SF, Wong HL, Field KM, Kosmider S, Tie J, Wong R, Tacey M, Shapiro J, Nott L, Richardson G, Cooray P, Jones I, Croxford M, Gibbs P. Primary tumor resection and overall survival in patients with metastatic colorectal cancer treated with palliative intent. Clin Colorectal Cancer. 2016;15(3):e125–e132132.PubMedCrossRef Wong SF, Wong HL, Field KM, Kosmider S, Tie J, Wong R, Tacey M, Shapiro J, Nott L, Richardson G, Cooray P, Jones I, Croxford M, Gibbs P. Primary tumor resection and overall survival in patients with metastatic colorectal cancer treated with palliative intent. Clin Colorectal Cancer. 2016;15(3):e125–e132132.PubMedCrossRef
17.
Zurück zum Zitat Slesser AAP, Georgiou P, Brown G, Mudan S, Goldin R, Tekkis P. The tumor biology of synchronous and metachronous colorectal liver metastases: a systematic review. Clin Exp Metastasis. 2013;30:457–70.PubMedCrossRef Slesser AAP, Georgiou P, Brown G, Mudan S, Goldin R, Tekkis P. The tumor biology of synchronous and metachronous colorectal liver metastases: a systematic review. Clin Exp Metastasis. 2013;30:457–70.PubMedCrossRef
18.
Zurück zum Zitat Wanebo HJ, Rao B, Pinsky CM, Hoffman RG, Stearns M, Schwartz MK, Oettgen HF. Preoperative carcinoembryonic antigen level as prognostic indicator in colorectal cancer. N Engl J Med. 1978;299:448–51.PubMedCrossRef Wanebo HJ, Rao B, Pinsky CM, Hoffman RG, Stearns M, Schwartz MK, Oettgen HF. Preoperative carcinoembryonic antigen level as prognostic indicator in colorectal cancer. N Engl J Med. 1978;299:448–51.PubMedCrossRef
19.
Zurück zum Zitat Iizasa T, Suzuki M, Yoshida S, Motohashi S, Yasufuku K, Iyoda A, Shibuya K, Hiroshima K, Nakatani Y, Fujisawa T. Prediction of prognosis and surgical indications for pulmonary metastasectomy from colorectal cancer. Ann Thorac Surg. 2006;82:254–60.PubMedCrossRef Iizasa T, Suzuki M, Yoshida S, Motohashi S, Yasufuku K, Iyoda A, Shibuya K, Hiroshima K, Nakatani Y, Fujisawa T. Prediction of prognosis and surgical indications for pulmonary metastasectomy from colorectal cancer. Ann Thorac Surg. 2006;82:254–60.PubMedCrossRef
20.
Zurück zum Zitat John SKP, Tobinson SM, Rehman S, Harrison B, Vallance A, French JJ, Jaques BC, Charnley RM, Manas DM, White SA. Prognostic factors and survival after resection of colorectal liver metastasis in the era of preoperative chemotherapy: an 11-year single-centre study. Dig Surg. 2013;30:293–301.PubMedCrossRef John SKP, Tobinson SM, Rehman S, Harrison B, Vallance A, French JJ, Jaques BC, Charnley RM, Manas DM, White SA. Prognostic factors and survival after resection of colorectal liver metastasis in the era of preoperative chemotherapy: an 11-year single-centre study. Dig Surg. 2013;30:293–301.PubMedCrossRef
21.
Zurück zum Zitat Stremitzer S, Zhang W, Yang D, Ning Y, Stintzing S, Sunakawa Y, Sebio A, Yamauchi S, Matsusaka S, Parekh A, Barzi A, Khoueiry R, Stift J, Wrba F, Gruenberger T, Lenz HJ. Variation in genes involved in dormancy associated with outcome in patients with resected colorectal liver metastases. Ann Oncol. 2015;26:1728–33.PubMedPubMedCentralCrossRef Stremitzer S, Zhang W, Yang D, Ning Y, Stintzing S, Sunakawa Y, Sebio A, Yamauchi S, Matsusaka S, Parekh A, Barzi A, Khoueiry R, Stift J, Wrba F, Gruenberger T, Lenz HJ. Variation in genes involved in dormancy associated with outcome in patients with resected colorectal liver metastases. Ann Oncol. 2015;26:1728–33.PubMedPubMedCentralCrossRef
22.
Zurück zum Zitat Fong Y, Fortner J, Sun RL, Brennan MF, Blumgart LH. Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg. 1999;230:309–18.PubMedPubMedCentralCrossRef Fong Y, Fortner J, Sun RL, Brennan MF, Blumgart LH. Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg. 1999;230:309–18.PubMedPubMedCentralCrossRef
23.
Zurück zum Zitat Nordlinger B, Guiguet M, Vaillant JC, Balladur P, Boudjema K, Bachellier P, Jaeck D. Surgical resection of colorectal carcinoma metastases to the liver. A prognostic scoring system to improve case selection, based on 1568 patients. Association Francaise de Chirurgie. Cancer. 1996;77:1254–62.PubMedCrossRef Nordlinger B, Guiguet M, Vaillant JC, Balladur P, Boudjema K, Bachellier P, Jaeck D. Surgical resection of colorectal carcinoma metastases to the liver. A prognostic scoring system to improve case selection, based on 1568 patients. Association Francaise de Chirurgie. Cancer. 1996;77:1254–62.PubMedCrossRef
24.
Zurück zum Zitat Reissfelder C, Rahbari NN, Koch M, Ulrich A, Pfeilschifter I, Waltert A, Müller SA, Schemmer P, Büchler MW, Weitz J. Validation of prognostic scoring systems for patients undergoing resection of colorectal cancer liver metastases. Ann Surg Oncol. 2009;16:3279–88.PubMedCrossRef Reissfelder C, Rahbari NN, Koch M, Ulrich A, Pfeilschifter I, Waltert A, Müller SA, Schemmer P, Büchler MW, Weitz J. Validation of prognostic scoring systems for patients undergoing resection of colorectal cancer liver metastases. Ann Surg Oncol. 2009;16:3279–88.PubMedCrossRef
25.
Zurück zum Zitat Bajenova O, Gorbunoa A, Evsyukov I, Rayko M, Gapon S, Bozhokina E, Shishkin A, O'Brien SJ. The genome-wide analysis of carcinoembryonic antigen signaling by colorectal cancer cells using RNA sequencing. PLoS ONE One. 2016;11:e0161256.CrossRef Bajenova O, Gorbunoa A, Evsyukov I, Rayko M, Gapon S, Bozhokina E, Shishkin A, O'Brien SJ. The genome-wide analysis of carcinoembryonic antigen signaling by colorectal cancer cells using RNA sequencing. PLoS ONE One. 2016;11:e0161256.CrossRef
26.
Zurück zum Zitat Wang W, Li Y, Zhang X, Jing J, Zhao X, Wang Y, Han C. Evaluating the significance of expression of CEA mRNA and levels of CEA and its related proteins in colorectal cancer patients. J Surg Oncol. 2014;109:440–4.PubMedCrossRef Wang W, Li Y, Zhang X, Jing J, Zhao X, Wang Y, Han C. Evaluating the significance of expression of CEA mRNA and levels of CEA and its related proteins in colorectal cancer patients. J Surg Oncol. 2014;109:440–4.PubMedCrossRef
27.
Zurück zum Zitat Bramswig KH, Poettler M, Unseld M, Wrba F, Uhrin P, Zimmermann W, Zielinski CC, Prager GW. Soluble carcinoembryonic antigen activates endothelial cells and tumor angiogenesis. Cancer Res. 2013;73:6584–96.PubMedCrossRef Bramswig KH, Poettler M, Unseld M, Wrba F, Uhrin P, Zimmermann W, Zielinski CC, Prager GW. Soluble carcinoembryonic antigen activates endothelial cells and tumor angiogenesis. Cancer Res. 2013;73:6584–96.PubMedCrossRef
28.
Zurück zum Zitat Van der Wal GE, Gouw ASH, Kamps JAAM, Moorlag HE, Bulthuis MLC, Molema G, de Jong KP. Angiogenesis in synchronous and metachronous colorectal liver metastases. Ann Surg. 2012;255:86–94.PubMedCrossRef Van der Wal GE, Gouw ASH, Kamps JAAM, Moorlag HE, Bulthuis MLC, Molema G, de Jong KP. Angiogenesis in synchronous and metachronous colorectal liver metastases. Ann Surg. 2012;255:86–94.PubMedCrossRef
29.
Zurück zum Zitat Venderbosch S, de Wilt JH, Teerenstra S, Loosveld OJ, van Bochove A, Sinnige HA, Creemers GJ, Tesselaar ME, Mol L, Punt CJ, Koopman M. Prognostic value of resection of primary tumor in patients with stage IV colorectal cancer: retrospective analysis of two randomized studies and a review of the literature. Ann Surg Oncol. 2011;17:3252–60.CrossRef Venderbosch S, de Wilt JH, Teerenstra S, Loosveld OJ, van Bochove A, Sinnige HA, Creemers GJ, Tesselaar ME, Mol L, Punt CJ, Koopman M. Prognostic value of resection of primary tumor in patients with stage IV colorectal cancer: retrospective analysis of two randomized studies and a review of the literature. Ann Surg Oncol. 2011;17:3252–60.CrossRef
30.
Zurück zum Zitat Budd GT, Cristofanilli M, Ellis MJ, Stopeck A, Borden E, Miller MC, Matera J, Repollet M, Doyle GV, Terstappen LW, Hayes DF. Circulating tumor cells versus imaging-predicting overall survival in metastatic breast cancer. Clin Cancer Res. 2006;12(21):6403–9.PubMedCrossRef Budd GT, Cristofanilli M, Ellis MJ, Stopeck A, Borden E, Miller MC, Matera J, Repollet M, Doyle GV, Terstappen LW, Hayes DF. Circulating tumor cells versus imaging-predicting overall survival in metastatic breast cancer. Clin Cancer Res. 2006;12(21):6403–9.PubMedCrossRef
31.
Zurück zum Zitat Turner N, Tran B, Tran PV, Sinnathamby M, Wong HL, Jones I, Croxford M, Desai J, Tie J, Field KM, Kosmider S, Bae S, Gibbs P. Primary tumor resection in patients with metastatic colorectal cancer is associated with reversal of systemic inflammation and improved survival. Clin Colorectal Cancer. 2015;14:185–91.PubMedCrossRef Turner N, Tran B, Tran PV, Sinnathamby M, Wong HL, Jones I, Croxford M, Desai J, Tie J, Field KM, Kosmider S, Bae S, Gibbs P. Primary tumor resection in patients with metastatic colorectal cancer is associated with reversal of systemic inflammation and improved survival. Clin Colorectal Cancer. 2015;14:185–91.PubMedCrossRef
32.
Zurück zum Zitat Gavriilidis P, Sutcliffe RP, Hodson J, Marudanayagam R, Isaac J, Azoulay D, Roberts KJ. Simultaneous versus delayed hepatectomy for synchronous colorectal liver metastases: a systematic review and meta-analysis. HPB. 2018;20(1):11–9.PubMedCrossRef Gavriilidis P, Sutcliffe RP, Hodson J, Marudanayagam R, Isaac J, Azoulay D, Roberts KJ. Simultaneous versus delayed hepatectomy for synchronous colorectal liver metastases: a systematic review and meta-analysis. HPB. 2018;20(1):11–9.PubMedCrossRef
33.
Zurück zum Zitat Lambert LA, Colacchio TA, Barth RJ. Interval hepatic resection of colorectal metastases improves patient selection. Arch Surg. 2000;135:473–80.PubMedCrossRef Lambert LA, Colacchio TA, Barth RJ. Interval hepatic resection of colorectal metastases improves patient selection. Arch Surg. 2000;135:473–80.PubMedCrossRef
34.
Zurück zum Zitat Allen PJ, Kemeny N, Jarnagin W, DeMatteo R, Blumgart L, Fong Y. Importance of response to neoadjuvant chemotherapy in patients undergoing resection of synchronous colorectal liver metastases. J Gastrointest Surg. 2003;7:109–15.PubMedCrossRef Allen PJ, Kemeny N, Jarnagin W, DeMatteo R, Blumgart L, Fong Y. Importance of response to neoadjuvant chemotherapy in patients undergoing resection of synchronous colorectal liver metastases. J Gastrointest Surg. 2003;7:109–15.PubMedCrossRef
35.
Zurück zum Zitat Slesser AAP, Khan F, Chau I, Khan AZ, Mudan S, Tekkis PP, Brown G, Rao S. The effect of a primary tumor resection on the progression of synchronous colorectal liver metastases: an exploratory study. Eur J Surg Oncol. 2015;41:484–92.PubMedCrossRef Slesser AAP, Khan F, Chau I, Khan AZ, Mudan S, Tekkis PP, Brown G, Rao S. The effect of a primary tumor resection on the progression of synchronous colorectal liver metastases: an exploratory study. Eur J Surg Oncol. 2015;41:484–92.PubMedCrossRef
36.
Zurück zum Zitat Mekenkamp LJM, Koopman M, Teerenstra S, van Krieken JHJM, Mol L, Nagtegaal ID, Punt CJA. Clinicopathological features and outcome in advanced colorectal cancer patients with synchronous vs metachronous metastases. Brit J Cancer. 2010;103:159–64.PubMedCrossRefPubMedCentral Mekenkamp LJM, Koopman M, Teerenstra S, van Krieken JHJM, Mol L, Nagtegaal ID, Punt CJA. Clinicopathological features and outcome in advanced colorectal cancer patients with synchronous vs metachronous metastases. Brit J Cancer. 2010;103:159–64.PubMedCrossRefPubMedCentral
37.
Zurück zum Zitat Kohne CH, Poston G, Folprecht G, Ciardiello F, Ronga P, Beier F, Van Cutsem E. FOLFIRI plus cetuximab in patients with liver-limited or non-liver-limited RAS wild-type metastatic colorectal cancer: a retrospective subgroup analysis of the CRYSTAL study. Eur J Surg Oncol. 2016;42:1540–7.PubMedCrossRef Kohne CH, Poston G, Folprecht G, Ciardiello F, Ronga P, Beier F, Van Cutsem E. FOLFIRI plus cetuximab in patients with liver-limited or non-liver-limited RAS wild-type metastatic colorectal cancer: a retrospective subgroup analysis of the CRYSTAL study. Eur J Surg Oncol. 2016;42:1540–7.PubMedCrossRef
38.
Zurück zum Zitat Adam R, de Gramont A, Figueras J, Kokudo N, Kunstlinger F, Loyer E, Poston G, Rougier P, Rubbia-Brandt L, Sobrero A, Teh C, Tejpar S, Van Cutsem E, Vauthey JN, Påhlman L, of the EGOSLIM (Expert Group on, OncoSurgery, management of, LIver, Metastases) group. Managing synchronous liver metastases from colorectal cancer: a multidisciplinary international consensus. Cancer Treat Rev. 2015;41:729–41.PubMedCrossRef Adam R, de Gramont A, Figueras J, Kokudo N, Kunstlinger F, Loyer E, Poston G, Rougier P, Rubbia-Brandt L, Sobrero A, Teh C, Tejpar S, Van Cutsem E, Vauthey JN, Påhlman L, of the EGOSLIM (Expert Group on, OncoSurgery, management of, LIver, Metastases) group. Managing synchronous liver metastases from colorectal cancer: a multidisciplinary international consensus. Cancer Treat Rev. 2015;41:729–41.PubMedCrossRef
39.
Zurück zum Zitat Holch JW, Demmer M, Lamersdorf C, Michl M, Schulz C, von Einem JC, Modest DP, Heinemann V. Pattern and dynamics of distant metastases in metastatic colorectal cancer. Visc Med. 2017;33:70–5.PubMedPubMedCentralCrossRef Holch JW, Demmer M, Lamersdorf C, Michl M, Schulz C, von Einem JC, Modest DP, Heinemann V. Pattern and dynamics of distant metastases in metastatic colorectal cancer. Visc Med. 2017;33:70–5.PubMedPubMedCentralCrossRef
40.
Zurück zum Zitat Finlay IG, Meek D, Brunton F, McArdle CS. Growth rate of hepatic metastases in colorectal cancer. Br J Surg. 1988;75:641–4.PubMedCrossRef Finlay IG, Meek D, Brunton F, McArdle CS. Growth rate of hepatic metastases in colorectal cancer. Br J Surg. 1988;75:641–4.PubMedCrossRef
41.
Zurück zum Zitat Kawaguchi K, Uehara K, Nakayama G, Fukui T, Fukumoto K, Nakamura S, Yokoi K. Growth rate of chemotherapy-naive lung metastasis from colorectal cancer could be a predictor of early relapse after lung resection. Int J Clin Oncol. 2016;21:329–34.PubMedCrossRef Kawaguchi K, Uehara K, Nakayama G, Fukui T, Fukumoto K, Nakamura S, Yokoi K. Growth rate of chemotherapy-naive lung metastasis from colorectal cancer could be a predictor of early relapse after lung resection. Int J Clin Oncol. 2016;21:329–34.PubMedCrossRef
42.
Zurück zum Zitat Lenz HJ, Ou FS, Venook AP, Hochster HS, Niedzwiecki D, Goldberg RM, Mayer RJ, Bertagnolli MM, Blanke CD, Zemla T, Qu X, Wirapati P, Tejpar S, Innocenti F, Kabbarah O. Impact of consensus molecular subtype on survival in patients with metastatic colorectal cancer: results from CALGB/SWOG 80405 (Alliance). J Clin Oncol. 2019;37(22):1876–85.PubMedPubMedCentralCrossRef Lenz HJ, Ou FS, Venook AP, Hochster HS, Niedzwiecki D, Goldberg RM, Mayer RJ, Bertagnolli MM, Blanke CD, Zemla T, Qu X, Wirapati P, Tejpar S, Innocenti F, Kabbarah O. Impact of consensus molecular subtype on survival in patients with metastatic colorectal cancer: results from CALGB/SWOG 80405 (Alliance). J Clin Oncol. 2019;37(22):1876–85.PubMedPubMedCentralCrossRef
Metadaten
Titel
Different variables predict the outcome of patients with synchronous versus metachronous metastases of colorectal cancer
verfasst von
G. A. Colloca
A. Venturino
D. Guarneri
Publikationsdatum
08.01.2020
Verlag
Springer International Publishing
Erschienen in
Clinical and Translational Oncology / Ausgabe 8/2020
Print ISSN: 1699-048X
Elektronische ISSN: 1699-3055
DOI
https://doi.org/10.1007/s12094-019-02277-7

Weitere Artikel der Ausgabe 8/2020

Clinical and Translational Oncology 8/2020 Zur Ausgabe

Update Onkologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.