Skip to main content
Top
Published in: World Journal of Surgical Oncology 1/2019

Open Access 01-12-2019 | Metastasis | Research

Synchronous and metachronous liver metastases in patients with colorectal cancer—towards a clinically relevant definition

Authors: Jennie Engstrand, Cecilia Strömberg, Henrik Nilsson, Jacob Freedman, Eduard Jonas

Published in: World Journal of Surgical Oncology | Issue 1/2019

Login to get access

Abstract

Background

Approximately 25% of patients with colorectal cancer (CRC) will have liver metastases classified as synchronous or metachronous. There is no consensus on the defining time point for synchronous/metachronous, and the prognostic implications thereof remain unclear. The aim of the study was to assess the prognostic value of differential detection at various defining time points in a population-based patient cohort and conduct a literature review of the topic.

Methods

All patients diagnosed with CRC in the counties of Stockholm and Gotland, Sweden, during 2008 were included in the study and followed for 5 years or until death to identify patients diagnosed with liver metastases. Patients with liver metastases were followed from time of diagnosis of liver metastases for at least 5 years or until death. Different time points defining synchronous/metachronous detection, as reported in the literature and identified in a literature search of databases (PubMed, Embase, Cochrane library), were applied to the cohort, and overall survival was calculated using Kaplan-Meier curves and compared with log-rank test. The influence of synchronously or metachronously detected liver metastases on disease-free and overall survival as reported in articles forthcoming from the literature search was also assessed.

Results

Liver metastases were diagnosed in 272/1026 patients with CRC (26.5%). No statistically significant difference in overall survival for synchronous vs. metachronous detection at any of the defining time points (CRC diagnosis/surgery and 3, 6 and 12 months post-diagnosis/surgery) was demonstrated for operated or non-operated patients. In the literature search, 41 publications met the inclusion criteria. No clear pattern emerged regarding the prognostic significance of synchronous vs. metachronous detection.

Conclusion

Synchronous vs. metachronous detection of CRC liver metastases lacks prognostic value. Using primary tumour diagnosis/operation as standardized cut-off point to define synchronous/metachronous detection is semantically correct. In synchronous detection, it defines a clinically relevant group of patients where individualized multimodality treatment protocols will apply.
Literature
1.
go back to reference Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JW, Comber H, et al. Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer. 2013;49(6):1374–403.PubMedCrossRef Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JW, Comber H, et al. Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer. 2013;49(6):1374–403.PubMedCrossRef
2.
go back to reference Sjovall A, Jarv V, Blomqvist L, Singnomklao T, Cedermark B, Glimelius B, et al. The potential for improved outcome in patients with hepatic metastases from colon cancer: a population-based study. Eur J Surg Oncol. 2004;30(8):834–41.PubMedCrossRef Sjovall A, Jarv V, Blomqvist L, Singnomklao T, Cedermark B, Glimelius B, et al. The potential for improved outcome in patients with hepatic metastases from colon cancer: a population-based study. Eur J Surg Oncol. 2004;30(8):834–41.PubMedCrossRef
3.
go back to reference Hackl C, Neumann P, Gerken M, Loss M, Klinkhammer-Schalke M, Schlitt HJ. Treatment of colorectal liver metastases in Germany: a ten-year population-based analysis of 5772 cases of primary colorectal adenocarcinoma. BMC Cancer. 2014;14:810.PubMedPubMedCentralCrossRef Hackl C, Neumann P, Gerken M, Loss M, Klinkhammer-Schalke M, Schlitt HJ. Treatment of colorectal liver metastases in Germany: a ten-year population-based analysis of 5772 cases of primary colorectal adenocarcinoma. BMC Cancer. 2014;14:810.PubMedPubMedCentralCrossRef
4.
go back to reference Engstrand J, Nilsson H, Stromberg C, Jonas E, Freedman J. Colorectal cancer liver metastases - a population-based study on incidence, management and survival. BMC Cancer. 2018;18(1):78.PubMedPubMedCentralCrossRef Engstrand J, Nilsson H, Stromberg C, Jonas E, Freedman J. Colorectal cancer liver metastases - a population-based study on incidence, management and survival. BMC Cancer. 2018;18(1):78.PubMedPubMedCentralCrossRef
5.
go back to reference de Jong MC, Pulitano C, Ribero D, Strub J, Mentha G, Schulick RD, et al. 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(3):440–8.PubMed de Jong MC, Pulitano C, Ribero D, Strub J, Mentha G, Schulick RD, et al. 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(3):440–8.PubMed
6.
go back to reference Pawlik TM, Schulick RD, Choti MA. Expanding criteria for resectability of colorectal liver metastases. Oncologist. 2008;13(1):51–64.PubMedCrossRef Pawlik TM, Schulick RD, Choti MA. Expanding criteria for resectability of colorectal liver metastases. Oncologist. 2008;13(1):51–64.PubMedCrossRef
7.
go back to reference Settmacher U, Dittmar Y, Knosel T, Schone U, Heise M, Jandt K, et al. Predictors of long-term survival in patients with colorectal liver metastases: a single center study and review of the literature. Int J Color Dis. 2011;26(8):967–81.CrossRef Settmacher U, Dittmar Y, Knosel T, Schone U, Heise M, Jandt K, et al. Predictors of long-term survival in patients with colorectal liver metastases: a single center study and review of the literature. Int J Color Dis. 2011;26(8):967–81.CrossRef
8.
go back to reference Spelt L, Andersson B, Nilsson J, Andersson R. Prognostic models for outcome following liver resection for colorectal cancer metastases: a systematic review. Eur J Surg Oncol. 2012;38(1):16–24.PubMedCrossRef Spelt L, Andersson B, Nilsson J, Andersson R. Prognostic models for outcome following liver resection for colorectal cancer metastases: a systematic review. Eur J Surg Oncol. 2012;38(1):16–24.PubMedCrossRef
9.
go back to reference Adam R, de Gramont A, Figueras J, Kokudo N, Kunstlinger F, Loyer E, et al. Managing synchronous liver metastases from colorectal cancer: a multidisciplinary international consensus. Cancer Treat Rev. 2015;41(9):729–41.PubMedCrossRef Adam R, de Gramont A, Figueras J, Kokudo N, Kunstlinger F, Loyer E, et al. Managing synchronous liver metastases from colorectal cancer: a multidisciplinary international consensus. Cancer Treat Rev. 2015;41(9):729–41.PubMedCrossRef
10.
go back to reference Reddy SK, Barbas AS, Clary BM. Synchronous colorectal liver metastases: is it time to reconsider traditional paradigms of management? Ann Surg Oncol. 2009;16(9):2395–410.PubMedCrossRef Reddy SK, Barbas AS, Clary BM. Synchronous colorectal liver metastases: is it time to reconsider traditional paradigms of management? Ann Surg Oncol. 2009;16(9):2395–410.PubMedCrossRef
11.
go back to reference Schwarz RE, Berlin JD, Lenz HJ, Nordlinger B, Rubbia-Brandt L, Choti MA. Systemic cytotoxic and biological therapies of colorectal liver metastases: expert consensus statement. HPB (Oxford). 2013;15(2):106–15.CrossRef Schwarz RE, Berlin JD, Lenz HJ, Nordlinger B, Rubbia-Brandt L, Choti MA. Systemic cytotoxic and biological therapies of colorectal liver metastases: expert consensus statement. HPB (Oxford). 2013;15(2):106–15.CrossRef
12.
go back to reference Jones RP, Malik HZ, Fenwick SW, Poston GJ. Perioperative chemotherapy for resectable colorectal liver metastases: where now? Eur J Surg Oncol. 2013;39(8):807–11.PubMedCrossRef Jones RP, Malik HZ, Fenwick SW, Poston GJ. Perioperative chemotherapy for resectable colorectal liver metastases: where now? Eur J Surg Oncol. 2013;39(8):807–11.PubMedCrossRef
13.
go back to reference Brouquet A, Nordlinger B. Neoadjuvant therapy of colorectal liver metastases: lessons learned from clinical trials. J Surg Oncol. 2010;102(8):932–6.PubMedCrossRef Brouquet A, Nordlinger B. Neoadjuvant therapy of colorectal liver metastases: lessons learned from clinical trials. J Surg Oncol. 2010;102(8):932–6.PubMedCrossRef
14.
go back to reference Kodeda K, Nathanaelsson L, Jung B, Olsson H, Jestin P, Sjovall A, et al. Population-based data from the Swedish Colon Cancer Registry. Br J Surg. 2013;100(8):1100–7.PubMedCrossRef Kodeda K, Nathanaelsson L, Jung B, Olsson H, Jestin P, Sjovall A, et al. Population-based data from the Swedish Colon Cancer Registry. Br J Surg. 2013;100(8):1100–7.PubMedCrossRef
15.
go back to reference McInnes MDF, Moher D, Thombs BD, McGrath TA, Bossuyt PM, Clifford T, et al. Preferred Reporting Items for a Systematic Review and Meta-analysis of Diagnostic Test Accuracy Studies: the PRISMA-DTA statement. JAMA. 2018;319(4):388–96.PubMedCrossRef McInnes MDF, Moher D, Thombs BD, McGrath TA, Bossuyt PM, Clifford T, et al. Preferred Reporting Items for a Systematic Review and Meta-analysis of Diagnostic Test Accuracy Studies: the PRISMA-DTA statement. JAMA. 2018;319(4):388–96.PubMedCrossRef
16.
go back to reference Mutsaerts EL, van Ruth S, Zoetmulder FA, Rutgers EJ, Hart AA, van Coevorden F. Prognostic factors and evaluation of surgical management of hepatic metastases from colorectal origin: a 10-year single-institute experience. J Gastrointest Surg. 2005;9(2):178–86.PubMedCrossRef Mutsaerts EL, van Ruth S, Zoetmulder FA, Rutgers EJ, Hart AA, van Coevorden F. Prognostic factors and evaluation of surgical management of hepatic metastases from colorectal origin: a 10-year single-institute experience. J Gastrointest Surg. 2005;9(2):178–86.PubMedCrossRef
17.
go back to reference Leporrier J, Maurel J, Chiche L, Bara S, Segol P, Launoy G. A population-based study of the incidence, management and prognosis of hepatic metastases from colorectal cancer. Br J Surg. 2006;93(4):465–74.PubMedCrossRef Leporrier J, Maurel J, Chiche L, Bara S, Segol P, Launoy G. A population-based study of the incidence, management and prognosis of hepatic metastases from colorectal cancer. Br J Surg. 2006;93(4):465–74.PubMedCrossRef
18.
go back to reference Minagawa M, Yamamoto J, Miwa S, Sakamoto Y, Kokudo N, Kosuge T, et al. Selection criteria for simultaneous resection in patients with synchronous liver metastasis. Arch Surg. 2006;141(10):1006–12.PubMedCrossRef Minagawa M, Yamamoto J, Miwa S, Sakamoto Y, Kokudo N, Kosuge T, et al. Selection criteria for simultaneous resection in patients with synchronous liver metastasis. Arch Surg. 2006;141(10):1006–12.PubMedCrossRef
19.
go back to reference Taniai N, Yoshida H, Mamada Y, Matsumoto S, Mizuguchi Y, Suzuki H, et al. Outcome of surgical treatment of synchronous liver metastases from colorectal cancer. J Nippon Med School. 2006;73(2):82–8.CrossRef Taniai N, Yoshida H, Mamada Y, Matsumoto S, Mizuguchi Y, Suzuki H, et al. Outcome of surgical treatment of synchronous liver metastases from colorectal cancer. J Nippon Med School. 2006;73(2):82–8.CrossRef
20.
go back to reference Shimizu Y, Yasui K, Sano T, Hirai T, Kanemitsu Y, Komori K, et al. Treatment strategy for synchronous metastases of colorectal cancer: is hepatic resection after an observation interval appropriate? Langenbeck's Arch Surg. 2007;392(5):535–8.CrossRef Shimizu Y, Yasui K, Sano T, Hirai T, Kanemitsu Y, Komori K, et al. Treatment strategy for synchronous metastases of colorectal cancer: is hepatic resection after an observation interval appropriate? Langenbeck's Arch Surg. 2007;392(5):535–8.CrossRef
21.
go back to reference Tsai MS, Su YH, Ho MC, Liang JT, Chen TP, Lai HS, et al. Clinicopathological features and prognosis in resectable synchronous and metachronous colorectal liver metastasis. Ann Surg Oncol. 2007;14(2):786–94.PubMedCrossRef Tsai MS, Su YH, Ho MC, Liang JT, Chen TP, Lai HS, et al. Clinicopathological features and prognosis in resectable synchronous and metachronous colorectal liver metastasis. Ann Surg Oncol. 2007;14(2):786–94.PubMedCrossRef
22.
go back to reference Wang X, Hershman DL, Abrams JA, Feingold D, Grann VR, Jacobson JS, et al. Predictors of survival after hepatic resection among patients with colorectal liver metastasis. Br J Cancer. 2007;97(12):1606–12.PubMedPubMedCentralCrossRef Wang X, Hershman DL, Abrams JA, Feingold D, Grann VR, Jacobson JS, et al. Predictors of survival after hepatic resection among patients with colorectal liver metastasis. Br J Cancer. 2007;97(12):1606–12.PubMedPubMedCentralCrossRef
23.
go back to reference Bockhorn M, Frilling A, Fruhauf NR, Neuhaus J, Molmenti E, Trarbach T, et al. Survival of patients with synchronous and metachronous colorectal liver metastases - is there a difference? J Gastrointest Surg. 2008;12(8):1399–405.PubMedCrossRef Bockhorn M, Frilling A, Fruhauf NR, Neuhaus J, Molmenti E, Trarbach T, et al. Survival of patients with synchronous and metachronous colorectal liver metastases - is there a difference? J Gastrointest Surg. 2008;12(8):1399–405.PubMedCrossRef
24.
go back to reference Hamady ZZR, Malik HZ, Alwan N, Wyatt JI, Prasad RK, Toogood GT, et al. Surgeon’s awareness of the synchronous liver metastases during colorectal cancer resection may affect outcome. Eur J Surg Oncol. 2008;34(2):180–4.PubMedCrossRef Hamady ZZR, Malik HZ, Alwan N, Wyatt JI, Prasad RK, Toogood GT, et al. Surgeon’s awareness of the synchronous liver metastases during colorectal cancer resection may affect outcome. Eur J Surg Oncol. 2008;34(2):180–4.PubMedCrossRef
25.
go back to reference Vigano L, Ferrero A, Lo Tesoriere R, Capussotti L. Liver surgery for colorectal metastases: results after 10 years of follow-up. Long-term survivors, late recurrences, and prognostic role of morbidity. Ann Surg Oncol. 2008;15(9):2458–64.PubMedCrossRef Vigano L, Ferrero A, Lo Tesoriere R, Capussotti L. Liver surgery for colorectal metastases: results after 10 years of follow-up. Long-term survivors, late recurrences, and prognostic role of morbidity. Ann Surg Oncol. 2008;15(9):2458–64.PubMedCrossRef
26.
go back to reference Konopke R, Kersting S, Distler M, Dietrich J, Gastmeier J, Heller A, et al. Prognostic factors and evaluation of a clinical score for predicting survival after resection of colorectal liver metastases. Liver Int. 2009;29(1):89–102.PubMedCrossRef Konopke R, Kersting S, Distler M, Dietrich J, Gastmeier J, Heller A, et al. Prognostic factors and evaluation of a clinical score for predicting survival after resection of colorectal liver metastases. Liver Int. 2009;29(1):89–102.PubMedCrossRef
27.
go back to reference Ng WWC, Cheung YS, Wong J, Lee KF, Lai PBS. A preliminary analysis of combined liver resection with new chemotherapy for synchronous and metachronous colorectal liver metastasis. Asian Journal of Surgery. 2009;32(4):189–97.PubMedCrossRef Ng WWC, Cheung YS, Wong J, Lee KF, Lai PBS. A preliminary analysis of combined liver resection with new chemotherapy for synchronous and metachronous colorectal liver metastasis. Asian Journal of Surgery. 2009;32(4):189–97.PubMedCrossRef
28.
go back to reference Xu J, Wei Y, Zhong Y, Fan J, Zhou J, Qin L, et al. Hepatectomy for liver metastasis of colorectal cancer. Int J Color Dis. 2009;24(4):419–25.CrossRef Xu J, Wei Y, Zhong Y, Fan J, Zhou J, Qin L, et al. Hepatectomy for liver metastasis of colorectal cancer. Int J Color Dis. 2009;24(4):419–25.CrossRef
29.
go back to reference Tonelli F, Leo F, Nobili S, Mini E, Batignani G. Prognostic factors in primary and iterative surgery of colorectal liver metastases. J Chemother. 2010;22(5):358–63.PubMedCrossRef Tonelli F, Leo F, Nobili S, Mini E, Batignani G. Prognostic factors in primary and iterative surgery of colorectal liver metastases. J Chemother. 2010;22(5):358–63.PubMedCrossRef
30.
go back to reference van der Pool AEM, Lalmahomed ZS, Ozbay Y, de Wilt JHW, Eggermont AMM, Jzermans JNM, et al. ‘Staged’ liver resection in synchronous and metachronous colorectal hepatic metastases: differences in clinicopathological features and outcome. Color Dis. 2010;12(10):e229–e35.CrossRef van der Pool AEM, Lalmahomed ZS, Ozbay Y, de Wilt JHW, Eggermont AMM, Jzermans JNM, et al. ‘Staged’ liver resection in synchronous and metachronous colorectal hepatic metastases: differences in clinicopathological features and outcome. Color Dis. 2010;12(10):e229–e35.CrossRef
31.
go back to reference Brouquet A, Overman MJ, Kopetz S, Maru DM, Loyer EM, Andreou A, et al. Is resection of colorectal liver metastases after a second-line chemotherapy regimen justified? Cancer. 2011;117(19):4484–92.PubMedCrossRef Brouquet A, Overman MJ, Kopetz S, Maru DM, Loyer EM, Andreou A, et al. Is resection of colorectal liver metastases after a second-line chemotherapy regimen justified? Cancer. 2011;117(19):4484–92.PubMedCrossRef
32.
go back to reference Swan PJ, Welsh FK, Chandrakumaran K, Rees M. Long-term survival following delayed presentation and resection of colorectal liver metastases. Br J Surg. 2011;98(9):1309–17.PubMedCrossRef Swan PJ, Welsh FK, Chandrakumaran K, Rees M. Long-term survival following delayed presentation and resection of colorectal liver metastases. Br J Surg. 2011;98(9):1309–17.PubMedCrossRef
33.
go back to reference Furukawa K, Shiba H, Haruki K, Fujiwara Y, Iida T, Mitsuyama Y, et al. The Glasgow prognostic score is valuable for colorectal cancer with both synchronous and metachronous unresectable liver metastases. Oncol Lett. 2012;4(2):324–8.PubMedPubMedCentralCrossRef Furukawa K, Shiba H, Haruki K, Fujiwara Y, Iida T, Mitsuyama Y, et al. The Glasgow prognostic score is valuable for colorectal cancer with both synchronous and metachronous unresectable liver metastases. Oncol Lett. 2012;4(2):324–8.PubMedPubMedCentralCrossRef
34.
go back to reference Vigano L, Russolillo N, Ferrero A, Langella S, Sperti E, Capussotti L. Evolution of long-term outcome of liver resection for colorectal metastases: analysis of actual 5-year survival rates over two decades. Ann Surg Oncol. 2012;19(6):2035–44.PubMedCrossRef Vigano L, Russolillo N, Ferrero A, Langella S, Sperti E, Capussotti L. Evolution of long-term outcome of liver resection for colorectal metastases: analysis of actual 5-year survival rates over two decades. Ann Surg Oncol. 2012;19(6):2035–44.PubMedCrossRef
35.
go back to reference Dexiang Z, Li R, Ye W, Haifu W, Yunshi Z, Qinghai Y, et al. Outcome of patients with colorectal liver metastasis: analysis of 1,613 consecutive cases. Ann Surg Oncol. 2012;19(9):2860–8.PubMedCrossRef Dexiang Z, Li R, Ye W, Haifu W, Yunshi Z, Qinghai Y, et al. Outcome of patients with colorectal liver metastasis: analysis of 1,613 consecutive cases. Ann Surg Oncol. 2012;19(9):2860–8.PubMedCrossRef
36.
go back to reference Gur I, Diggs BS, Wagner JA, Vaccaro GM, Lopez CD, Sheppard BC, et al. Safety and outcomes following resection of colorectal liver metastases in the era of current perioperative chemotherapy. J Gastrointest Surg. 2013;17(12):2133–42.PubMedCrossRef Gur I, Diggs BS, Wagner JA, Vaccaro GM, Lopez CD, Sheppard BC, et al. Safety and outcomes following resection of colorectal liver metastases in the era of current perioperative chemotherapy. J Gastrointest Surg. 2013;17(12):2133–42.PubMedCrossRef
37.
go back to reference Nanji S, Cleary S, Ryan P, Guindi M, Selvarajah S, Grieg P, et al. Up-front hepatic resection for metastatic colorectal cancer results in favorable long-term survival. Ann Surg Oncol. 2013;20(1):295–304.PubMedCrossRef Nanji S, Cleary S, Ryan P, Guindi M, Selvarajah S, Grieg P, et al. Up-front hepatic resection for metastatic colorectal cancer results in favorable long-term survival. Ann Surg Oncol. 2013;20(1):295–304.PubMedCrossRef
38.
go back to reference Ribeiro HS, Stevanato-Filho PR, Costa WL Jr, Diniz AL, Herman P, Coimbra FJ. Prognostic factors for survival in patients with colorectal liver metastases: experience of a single brazilian cancer center. Arq Gastroenterol. 2012;49(4):266–72.PubMedCrossRef Ribeiro HS, Stevanato-Filho PR, Costa WL Jr, Diniz AL, Herman P, Coimbra FJ. Prognostic factors for survival in patients with colorectal liver metastases: experience of a single brazilian cancer center. Arq Gastroenterol. 2012;49(4):266–72.PubMedCrossRef
39.
go back to reference John SK, Robinson SM, Rehman S, Harrison B, Vallance A, French JJ, et al. 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(4-6):293–301.PubMedCrossRef John SK, Robinson SM, Rehman S, Harrison B, Vallance A, French JJ, et al. 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(4-6):293–301.PubMedCrossRef
40.
go back to reference Kumar R, Price TJ, Beeke C, Jain K, Patel G, Padbury R, et al. Colorectal cancer survival: an analysis of patients with metastatic disease synchronous and metachronous with the primary tumor. Clin Colorectal Cancer. 2014;13(2):87–93.PubMedCrossRef Kumar R, Price TJ, Beeke C, Jain K, Patel G, Padbury R, et al. Colorectal cancer survival: an analysis of patients with metastatic disease synchronous and metachronous with the primary tumor. Clin Colorectal Cancer. 2014;13(2):87–93.PubMedCrossRef
41.
go back to reference Kuo IM, Huang SF, Chiang JM, Yeh CY, Chan KM, Chen JS, et al. Clinical features and prognosis in hepatectomy for colorectal cancer with centrally located liver metastasis. World J Surg Oncol. 2015;13:92.PubMedPubMedCentralCrossRef Kuo IM, Huang SF, Chiang JM, Yeh CY, Chan KM, Chen JS, et al. Clinical features and prognosis in hepatectomy for colorectal cancer with centrally located liver metastasis. World J Surg Oncol. 2015;13:92.PubMedPubMedCentralCrossRef
42.
go back to reference Ali MA, Di Sandro S, Lauterio A, Concone G, Mangoni I, Ferla F, et al. Repeat hepatectomy for recurrent colorectal liver metastases: is it worth the challenge? J Gastrointest Surg. 2015;19(12):2192–8.PubMedCrossRef Ali MA, Di Sandro S, Lauterio A, Concone G, Mangoni I, Ferla F, et al. Repeat hepatectomy for recurrent colorectal liver metastases: is it worth the challenge? J Gastrointest Surg. 2015;19(12):2192–8.PubMedCrossRef
44.
go back to reference Lemke J, Cammerer G, Ganser J, Scheele J, Xu P, Sander S, et al. Survival and prognostic factors of colorectal liver metastases after surgical and nonsurgical treatment. Clin Colorectal Cancer. 2016;15(4):e183–e92.PubMedCrossRef Lemke J, Cammerer G, Ganser J, Scheele J, Xu P, Sander S, et al. Survival and prognostic factors of colorectal liver metastases after surgical and nonsurgical treatment. Clin Colorectal Cancer. 2016;15(4):e183–e92.PubMedCrossRef
45.
go back to reference Miller CL, Taylor MS, Qadan M, Deshpande V, Worthington S, Smalley R, et al. Prognostic significance of surgical margin size after neoadjuvant FOLFOX and/or FOLFIRI for colorectal liver metastases. J Gastrointest Surg. 2017;21(11):1831–40.PubMedCrossRef Miller CL, Taylor MS, Qadan M, Deshpande V, Worthington S, Smalley R, et al. Prognostic significance of surgical margin size after neoadjuvant FOLFOX and/or FOLFIRI for colorectal liver metastases. J Gastrointest Surg. 2017;21(11):1831–40.PubMedCrossRef
46.
go back to reference Angelsen JH, Horn A, Sorbye H, Eide GE, Løes IM, Viste A. Population-based study on resection rates and survival in patients with colorectal liver metastasis in Norway. Br J Surg. 2017;104(5):580–9.PubMedCrossRef Angelsen JH, Horn A, Sorbye H, Eide GE, Løes IM, Viste A. Population-based study on resection rates and survival in patients with colorectal liver metastasis in Norway. Br J Surg. 2017;104(5):580–9.PubMedCrossRef
47.
go back to reference Bartolini I, Ringressi MN, Melli F, Risaliti M, Brugia M, Mini E, et al. Analysis of prognostic factors for resected synchronous and metachronous liver metastases from colorectal cancer. Gastroenterol Res Pract. 2018;2018. Bartolini I, Ringressi MN, Melli F, Risaliti M, Brugia M, Mini E, et al. Analysis of prognostic factors for resected synchronous and metachronous liver metastases from colorectal cancer. Gastroenterol Res Pract. 2018;2018.
48.
go back to reference Margonis GA, Buettner S, Andreatos N, Kim Y, Wagner D, Sasaki K, et al. Association of BRAF mutations with survival and recurrence in surgically treated patients with metastatic colorectal liver cancer. JAMA Surg. 2018;153(7):e180996.PubMedPubMedCentralCrossRef Margonis GA, Buettner S, Andreatos N, Kim Y, Wagner D, Sasaki K, et al. Association of BRAF mutations with survival and recurrence in surgically treated patients with metastatic colorectal liver cancer. JAMA Surg. 2018;153(7):e180996.PubMedPubMedCentralCrossRef
49.
go back to reference Marques MC, CR HS, Costa WL Jr, VHF d J, de Macedo MP, Diniz AL, et al. Is primary sidedness a prognostic factor in patients with resected colon cancer liver metastases (CLM)? J Surg Oncol. 2018;117(5):858–63.PubMedCrossRef Marques MC, CR HS, Costa WL Jr, VHF d J, de Macedo MP, Diniz AL, et al. Is primary sidedness a prognostic factor in patients with resected colon cancer liver metastases (CLM)? J Surg Oncol. 2018;117(5):858–63.PubMedCrossRef
50.
go back to reference Memeo R, de Blasi V, Adam R, Goéré D, Piardi T, Lermite E, et al. Margin status is still an important prognostic factor in hepatectomies for colorectal liver metastases: a propensity score matching analysis. World J Surg. 2018;42(3):892–901.PubMedCrossRef Memeo R, de Blasi V, Adam R, Goéré D, Piardi T, Lermite E, et al. Margin status is still an important prognostic factor in hepatectomies for colorectal liver metastases: a propensity score matching analysis. World J Surg. 2018;42(3):892–901.PubMedCrossRef
51.
go back to reference Quireze Junior C, Brasil AMS, Morais LK, Campion ERL, Taveira EJF, Rassi MC. Metachronous colorectal liver metastases has better prognosis – is it true? Arq Gastroenterol. 2018;55(3):258–63.PubMedCrossRef Quireze Junior C, Brasil AMS, Morais LK, Campion ERL, Taveira EJF, Rassi MC. Metachronous colorectal liver metastases has better prognosis – is it true? Arq Gastroenterol. 2018;55(3):258–63.PubMedCrossRef
52.
go back to reference Suthananthan AE, Bhandari M, Platell C. Influence of primary site on metastatic distribution and survival in stage IV colorectal cancer. ANZ J Surg. 2018;88(5):445–9.PubMedCrossRef Suthananthan AE, Bhandari M, Platell C. Influence of primary site on metastatic distribution and survival in stage IV colorectal cancer. ANZ J Surg. 2018;88(5):445–9.PubMedCrossRef
53.
go back to reference Strandberg Holka P, Eriksson S, Eberhard J, Bergenfeldt M, Lindell G, Sturesson C. Significance of poor performance status after resection of colorectal liver metastases. World J Surg Oncol. 2018;16(1):3.PubMedPubMedCentralCrossRef Strandberg Holka P, Eriksson S, Eberhard J, Bergenfeldt M, Lindell G, Sturesson C. Significance of poor performance status after resection of colorectal liver metastases. World J Surg Oncol. 2018;16(1):3.PubMedPubMedCentralCrossRef
54.
go back to reference Zhao Y, Deng Y, Peng J, Sui Q, Lin J, Qiu M, et al. Does the preoperative prognostic nutritional index predict survival in patients with liver metastases from colorectal cancer who underwent curative resection? J Cancer. 2018;9(12):2167–74.PubMedPubMedCentralCrossRef Zhao Y, Deng Y, Peng J, Sui Q, Lin J, Qiu M, et al. Does the preoperative prognostic nutritional index predict survival in patients with liver metastases from colorectal cancer who underwent curative resection? J Cancer. 2018;9(12):2167–74.PubMedPubMedCentralCrossRef
55.
go back to reference Veereman G, Robays J, Verleye L, Leroy R, Rolfo C, Van Cutsem E, et al. Pooled analysis of the surgical treatment for colorectal cancer liver metastases. Crit Rev Oncol Hematol. 2015;94(1):122–35.PubMedCrossRef Veereman G, Robays J, Verleye L, Leroy R, Rolfo C, Van Cutsem E, et al. Pooled analysis of the surgical treatment for colorectal cancer liver metastases. Crit Rev Oncol Hematol. 2015;94(1):122–35.PubMedCrossRef
56.
go back to reference Lam VW, Laurence JM, Pang T, Johnston E, Hollands MJ, Pleass HC, et al. A systematic review of a liver-first approach in patients with colorectal cancer and synchronous colorectal liver metastases. HPB. 2014;16(2):101–8.PubMedCrossRef Lam VW, Laurence JM, Pang T, Johnston E, Hollands MJ, Pleass HC, et al. A systematic review of a liver-first approach in patients with colorectal cancer and synchronous colorectal liver metastases. HPB. 2014;16(2):101–8.PubMedCrossRef
57.
go back to reference Siriwardena AK, Mason JM, Mullamitha S, Hancock HC, Jegatheeswaran S. Management of colorectal cancer presenting with synchronous liver metastases. Nat Rev Clin Oncol. 2014;11(8):446–59.PubMedCrossRef Siriwardena AK, Mason JM, Mullamitha S, Hancock HC, Jegatheeswaran S. Management of colorectal cancer presenting with synchronous liver metastases. Nat Rev Clin Oncol. 2014;11(8):446–59.PubMedCrossRef
58.
go back to reference Slesser AA, Simillis C, Goldin R, Brown G, Mudan S, Tekkis PP. A meta-analysis comparing simultaneous versus delayed resections in patients with synchronous colorectal liver metastases. Surg Oncol. 2013;22(1):36–47.PubMedCrossRef Slesser AA, Simillis C, Goldin R, Brown G, Mudan S, Tekkis PP. A meta-analysis comparing simultaneous versus delayed resections in patients with synchronous colorectal liver metastases. Surg Oncol. 2013;22(1):36–47.PubMedCrossRef
59.
go back to reference Van den Eynden GG, Majeed AW, Illemann M, Vermeulen PB, Bird NC, Hoyer-Hansen G, et al. The multifaceted role of the microenvironment in liver metastasis: biology and clinical implications. Cancer Res. 2013;73(7):2031–43.PubMedCrossRef Van den Eynden GG, Majeed AW, Illemann M, Vermeulen PB, Bird NC, Hoyer-Hansen G, et al. The multifaceted role of the microenvironment in liver metastasis: biology and clinical implications. Cancer Res. 2013;73(7):2031–43.PubMedCrossRef
60.
go back to reference Hagness M, Foss A, Egge TS, Dueland S. Patterns of recurrence after liver transplantation for nonresectable liver metastases from colorectal cancer. Ann Surg Oncol. 2014;21(4):1323–9.PubMedCrossRef Hagness M, Foss A, Egge TS, Dueland S. Patterns of recurrence after liver transplantation for nonresectable liver metastases from colorectal cancer. Ann Surg Oncol. 2014;21(4):1323–9.PubMedCrossRef
61.
go back to reference Hagness M, Foss A, Line PD, Scholz T, Jorgensen PF, Fosby B, et al. Liver transplantation for nonresectable liver metastases from colorectal cancer. Ann Surg. 2013;257(5):800–6.PubMedCrossRef Hagness M, Foss A, Line PD, Scholz T, Jorgensen PF, Fosby B, et al. Liver transplantation for nonresectable liver metastases from colorectal cancer. Ann Surg. 2013;257(5):800–6.PubMedCrossRef
62.
go back to reference Kartalis N, Brismar TB, Mihocsa L, Isaksson B, Albiin N. The added value of contrast-enhanced ultrasound in patients with colorectal cancer undergoing preoperative evaluation with extensive gadobenate dimeglumine liver MRI. Eur Radiol. 2011;21(10):2067–73.PubMedCrossRef Kartalis N, Brismar TB, Mihocsa L, Isaksson B, Albiin N. The added value of contrast-enhanced ultrasound in patients with colorectal cancer undergoing preoperative evaluation with extensive gadobenate dimeglumine liver MRI. Eur Radiol. 2011;21(10):2067–73.PubMedCrossRef
63.
go back to reference Zech CJ, Korpraphong P, Huppertz A, Denecke T, Kim MJ, Tanomkiat W, et al. Randomized multicentre trial of gadoxetic acid-enhanced MRI versus conventional MRI or CT in the staging of colorectal cancer liver metastases. Br J Surg. 2014;101(6):613–21.PubMedPubMedCentralCrossRef Zech CJ, Korpraphong P, Huppertz A, Denecke T, Kim MJ, Tanomkiat W, et al. Randomized multicentre trial of gadoxetic acid-enhanced MRI versus conventional MRI or CT in the staging of colorectal cancer liver metastases. Br J Surg. 2014;101(6):613–21.PubMedPubMedCentralCrossRef
64.
go back to reference Zech CJ, Justo N, Lang A, Ba-Ssalamah A, Kim MJ, Rinde H, et al. Cost evaluation of gadoxetic acid-enhanced magnetic resonance imaging in the diagnosis of colorectal-cancer metastasis in the liver: results from the VALUE Trial. Eur Radiol. 2016;26(11):4121–30.PubMedPubMedCentralCrossRef Zech CJ, Justo N, Lang A, Ba-Ssalamah A, Kim MJ, Rinde H, et al. Cost evaluation of gadoxetic acid-enhanced magnetic resonance imaging in the diagnosis of colorectal-cancer metastasis in the liver: results from the VALUE Trial. Eur Radiol. 2016;26(11):4121–30.PubMedPubMedCentralCrossRef
65.
go back to reference Zech CJ, Grazioli L, Jonas E, Ekman M, Niebecker R, Gschwend S, et al. Health-economic evaluation of three imaging strategies in patients with suspected colorectal liver metastases: Gd-EOB-DTPA-enhanced MRI vs. extracellular contrast media-enhanced MRI and 3-phase MDCT in Germany, Italy and Sweden. Eur Radiol. 2009;19 Suppl 3:S753-S763.CrossRef Zech CJ, Grazioli L, Jonas E, Ekman M, Niebecker R, Gschwend S, et al. Health-economic evaluation of three imaging strategies in patients with suspected colorectal liver metastases: Gd-EOB-DTPA-enhanced MRI vs. extracellular contrast media-enhanced MRI and 3-phase MDCT in Germany, Italy and Sweden. Eur Radiol. 2009;19 Suppl 3:S753-S763.CrossRef
Metadata
Title
Synchronous and metachronous liver metastases in patients with colorectal cancer—towards a clinically relevant definition
Authors
Jennie Engstrand
Cecilia Strömberg
Henrik Nilsson
Jacob Freedman
Eduard Jonas
Publication date
01-12-2019
Publisher
BioMed Central
Published in
World Journal of Surgical Oncology / Issue 1/2019
Electronic ISSN: 1477-7819
DOI
https://doi.org/10.1186/s12957-019-1771-9

Other articles of this Issue 1/2019

World Journal of Surgical Oncology 1/2019 Go to the issue