Late gadolinium MRI enhancement of colorectal liver metastases is associated with overall survival among nonsurgical patients

  • Helen M. C. CheungEmail author
  • Jin K. Kim
  • John Hudson
  • Natalie Coburn
  • Paul J. Karanicolas
  • Calvin Law
  • Laurent Milot



To determine if late gadolinium MRI enhancement of colorectal liver metastases (CRCLM) is associated with overall survival among nonsurgical patients.

Materials and methods

This retrospective study was approved by the institutional research ethics board. Late gadolinium enhancement was measured using target tumour enhancement (TTE) in all nonsurgical patients with CRCLM who received a 10-min delayed phase gadobutrol-enhanced liver MRI between March 1, 2006, and August 31, 2014. A total of 122 patients met inclusion/exclusion criteria. Patients were dichotomized into strong and weak TTE. Kaplan-Meier and Cox regression statistics were used to determine whether TTE was associated with overall survival. Noncontributory potential confounding variables (age, sex, number and size of metastases, carcinoembryonic (CEA) level, and presence of extrahepatic disease) were excluded from the final Cox regression model using the backward Wald elimination. Subgroup Kaplan-Meier survival analyses were performed on patients who were chemotherapy-naïve and chemotherapy-treated at the time of MRI.


Strong TTE had increased survival compared with those with weak TTE on Kaplan-Meier analysis (2-year survival: 69.8% vs. 43.5%, p = 0.002). Among 96 patients where data was available for multivariable analysis, weak TTE was associated with death (adjusted hazard ratio 0.25, 95% CI 0.11–0.59, p = 0.002), after adjusting for CEA level. Other potential confounders were noncontributory. Subgroup analyses demonstrated that strong TTE had increased survival compared with those with weak TTE in both the chemotherapy-naïve (p = 0.047) and chemotherapy-treated (p = 0.008) groups.


Strong late gadolinium MRI enhancement of CRCLM is associated with overall survival among nonsurgical patients.

Key Points

• MRI enhancement of colorectal liver metastases is associated with overall survival in nonsurgical patients.

• MRI enhancement of colorectal liver metastases is associated with overall survival in both chemotherapy-naïve and chemotherapy-treated subgroups.


Magnetic resonance imaging Contrast media Neoplasm metastasis Colorectal neoplasms Biomarkers, tumour 

Abbreviations and acronyms


Carcinoembryonic antigen


Contrast-to-noise ratio


Colorectal liver metastases


Magnetic resonance imaging


Research ethics board


Response Evaluation Criteria in Solid Tumours 1.1


Region of interest


Standard deviation


Signal intensity


Target tumour enhancement



The authors state that this work has not received any funding.

Compliance with ethical standards


The scientific guarantor of this publication is Dr. Laurent Milot.

Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

Written informed consent was waived by the Institutional Review Board.

Ethical approval

Institutional Review Board approval was obtained.


• retrospective

• cross-sectional study

• performed at one institution


  1. 1.
    Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J et al (2013) Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer 49(6):1374–1403CrossRefGoogle Scholar
  2. 2.
    American Cancer Society (2018) Cancer Facts & Figures 2018. American Cancer Society, AtlantaGoogle Scholar
  3. 3.
    Fakih MG (2015) Metastatic colorectal cancer: current state and future directions. J Clin Oncol 33(16):1809–1824CrossRefGoogle Scholar
  4. 4.
    Wanebo HJ, LeGolvan M, Paty PB et al (2012) Meeting the biologic challenge of colorectal metastases. Clin Exp Metastasis 29(7):821–839CrossRefGoogle Scholar
  5. 5.
    Jones OM, Rees M, John TG, Bygrave S, Plant G (2005) Biopsy of resectable colorectal liver metastases causes tumour dissemination and adversely affects survival after liver resection. Br J Surg 92(9):1165–1168CrossRefGoogle Scholar
  6. 6.
    Gerlinger M, Rowan AJ, Horswell S et al (2012) Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 366(10):883–892CrossRefGoogle Scholar
  7. 7.
    Jamal-Hanjani M, Quezada SA, Larkin J, Swanton C (2015) Translational implications of tumor heterogeneity. Clin Cancer Res 21(6):1258–1266CrossRefGoogle Scholar
  8. 8.
    Punt CJ, Koopman M, Vermeulen L (2017) From tumour heterogeneity to advances in precision treatment of colorectal cancer. Nat Rev Clin Oncol 14(4):235–246CrossRefGoogle Scholar
  9. 9.
    Swanton C (2012) Intratumor heterogeneity: evolution through space and time. Cancer Res 72(19):4875–4882CrossRefGoogle Scholar
  10. 10.
    Sebagh M, Allard MA, Bosselut N et al (2016) Evidence of intermetastatic heterogeneity for pathological response and genetic mutations within colorectal liver metastases following preoperative chemotherapy. Oncotarget. 7(16):21591–21600CrossRefGoogle Scholar
  11. 11.
    Watanabe T, Kobunai T, Yamamoto Y et al (2011) Heterogeneity of KRAS status may explain the subset of discordant KRAS status between primary and metastatic colorectal cancer. Dis Colon Rectum. 54(9):1170–1178CrossRefGoogle Scholar
  12. 12.
    Tirkes T, Hollar MA, Tann M, Kohli MD, Akisik F, Sandrasegaran K (2013) Response criteria in oncologic imaging: review of traditional and new criteria. Radiographics. 33(5):1323–1341CrossRefGoogle Scholar
  13. 13.
    Cheung HMC, Karanicolas PJ, Hsieh E et al (2018) Late gadolinium enhancement of colorectal liver metastases post-chemotherapy is associated with tumour fibrosis and overall survival post-hepatectomy. Eur Radiol 28(8):3505–3512CrossRefGoogle Scholar
  14. 14.
    Eisenhauer EA, Therasse P, Bogaerts J et al (2009) New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 45(2):228–247CrossRefGoogle Scholar
  15. 15.
    Dietrich O, Raya JG, Reeder SB, Reiser MF, Schoenberg SO (2007) Measurement of signal-to-noise ratios in MR images: influence of multichannel coils, parallel imaging, and reconstruction filters. J Magn Reson Imaging 26(2):375–385CrossRefGoogle Scholar
  16. 16.
    Youden WJ (1950) Index for rating diagnostic tests. Cancer 3(1):32–35CrossRefGoogle Scholar
  17. 17.
    Tirumani SH, Kim KW, Nishino M et al (2014) Update on the role of imaging in management of metastatic colorectal cancer. Radiographics 34(7):1908–1928CrossRefGoogle Scholar
  18. 18.
    Poultsides GA, Bao F, Servais EL et al (2012) Pathologic response to preoperative chemotherapy in colorectal liver metastases: fibrosis, not necrosis, predicts outcome. Ann Surg Oncol 19(9):2797–2804CrossRefGoogle Scholar
  19. 19.
    Reddy SK, Parker RJ, Leach JW, Hill MJ, Burgart LJ (2016) Tumor histopathology predicts outcomes after resection of colorectal cancer liver metastases treated with and without pre-operative chemotherapy. J Surg Oncol 113(4):456–462CrossRefGoogle Scholar
  20. 20.
    Dietrich O, Raya JG, Reeder SB, Ingrisch M, Reiser MF, Schoenberg SO (2008) Influence of multichannel combination, parallel imaging and other reconstruction techniques on MRI noise characteristics. Magn Reson Imaging 26(6):754–762CrossRefGoogle Scholar
  21. 21.
    Oshinski JN, Yang Z, Jones JR, Mata JF, French BA (2001) Imaging time after Gd-DTPA injection is critical in using delayed enhancement to determine infarct size accurately with magnetic resonance imaging. Circulation 104(23):2838–2842CrossRefGoogle Scholar
  22. 22.
    Cheung HMC, Karanicolas PJ, Coburn N, Seth V, Law C, Milot L (2018) Delayed tumour enhancement on gadoxetate-enhanced MRI is associated with overall survival in patients with colorectal liver metastases. Eur Radiol.

Copyright information

© European Society of Radiology 2019

Authors and Affiliations

  • Helen M. C. Cheung
    • 1
    Email author
  • Jin K. Kim
    • 1
  • John Hudson
    • 1
  • Natalie Coburn
    • 2
  • Paul J. Karanicolas
    • 2
  • Calvin Law
    • 2
  • Laurent Milot
    • 1
  1. 1.Department of Medical Imaging, Sunnybrook Health Sciences CentreUniversity of TorontoTorontoCanada
  2. 2.Department of Surgery, Sunnybrook Health Sciences CentreUniversity of TorontoTorontoCanada

Personalised recommendations