European Radiology

, Volume 26, Issue 12, pp 4595–4615 | Cite as

A meta-analysis of diffusion-weighted and gadoxetic acid-enhanced MR imaging for the detection of liver metastases

  • Valérie Vilgrain
  • Maxime Esvan
  • Maxime Ronot
  • Aurore Caumont-Prim
  • Christophe Aubé
  • Gilles Chatellier
Magnetic Resonance



To obtain the diagnostic performance of diffusion-weighted (DW) and gadoxetic-enhanced magnetic resonance (MR) imaging in the detection of liver metastases.


A comprehensive search (EMBASE, PubMed, Cochrane) was performed to identify relevant articles up to June 2015. Inclusion criteria were: liver metastases, DW-MR imaging and/or gadoxetic acid-enhanced MR imaging, and per-lesion statistics. The reference standard was histopathology, intraoperative observation and/or follow-up. Sources of bias were assessed using the QUADAS-2 tool. A linear mixed-effect regression model was used to obtain sensitivity estimates.


Thirty-nine articles were included (1,989 patients, 3,854 metastases). Sensitivity estimates for DW-MR imaging, gadoxetic acid-enhanced MR imaging and the combined sequence for detecting liver metastases on a per-lesion basis was 87.1 %, 90.6 % and 95.5 %, respectively. Sensitivity estimates by gadoxetic acid-enhanced MR imaging and the combined sequence were significantly better than DW-MR imaging (p = 0.0001 and p < 0.0001, respectively), and the combined MR sequence was significantly more sensitive than gadoxetic acid-enhanced MR imaging (p < 0.0001). Similar results were observed in articles that compared the three techniques simultaneously, with only colorectal liver metastases and in liver metastases smaller than 1 cm.


In patients with liver metastases, combined DW-MR and gadoxetic acid-enhanced MR imaging has the highest sensitivity for detecting liver metastases on a per-lesion basis.

Key Points

• DW-MRI is less sensitive than gadoxetic acid-enhanced MRI for detecting liver metastases

• DW-MRI and gadoxetic acid-enhanced MRI is the best combination

• Same results are observed in colorectal liver metastases

• Same results are observed in liver metastases smaller than 1 cm

• Same results are observed when histopathology alone is the reference standard


Liver metastases, diagnosis Liver metastases, MR imaging Liver metastases, meta-analysis Liver MRI 



The scientific guarantor of this publication is Valérie Vilgrain. 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. This study has received funding by the French Ministry of Health, PHRC, AOM 08-114. The authors thank The Ligue Nationale Contre le Cancer for supporting meta-analysis in cancer.

One of the authors has significant statistical expertise. Institutional Review Board approval was not required because this study is a meta-analysis. Written informed consent was not required for this study because this study is a meta-analysis. Methodology: retrospective, meta-analysis, performed at one institution.


  1. 1.
    Steele G Jr, Ravikumar TS (1989) Resection of hepatic metastases from colorectal cancer. Biologic perspective. Ann Surg 210:127–138CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Charnsangavej C, Clary B, Fong Y, Grothey A, Pawlik TM, Choti MA (2006) Selection of patients for resection of hepatic colorectal metastases: expert consensus statement. Ann Surg Oncol 13:1261–1268CrossRefPubMedGoogle Scholar
  3. 3.
    Adam R, De Gramont A, Figueras J et al (2012) The oncosurgery approach to managing liver metastases from colorectal cancer: a multidisciplinary international consensus. Oncologist 17:1225–1239CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Ercolani G, Vetrone G, Grazi GL et al (2009) The role of liver surgery in the treatment of non-colorectal non-neuroendocrine metastases (NCRNNE). Analysis of 134 resected patients. Minerva Chir 64:551–558PubMedGoogle Scholar
  5. 5.
    Goere D, Elias D (2008) Resection of liver metastases from non-colorectal non-endocrine primary tumours. Eur J Surg Oncol 34:281–288CrossRefPubMedGoogle Scholar
  6. 6.
    Bipat S, van Leeuwen MS, Comans EF et al (2005) Colorectal liver metastases: CT, MR imaging, and PET for diagnosis—meta-analysis. Radiology 237:123–131CrossRefPubMedGoogle Scholar
  7. 7.
    Floriani I, Torri V, Rulli E et al (2010) Performance of imaging modalities in diagnosis of liver metastases from colorectal cancer: a systematic review and meta-analysis. J Magn Reson Imaging 31:19–31CrossRefPubMedGoogle Scholar
  8. 8.
    Niekel MC, Bipat S, Stoker J (2010) Diagnostic imaging of colorectal liver metastases with CT, MR imaging, FDG PET, and/or FDG PET/CT: a meta-analysis of prospective studies including patients who have not previously undergone treatment. Radiology 257:674–684CrossRefPubMedGoogle Scholar
  9. 9.
    Wu LM, Hu J, Gu HY, Hua J, Xu JR (2013) Can diffusion-weighted magnetic resonance imaging (DW-MRI) alone be used as a reliable sequence for the preoperative detection and characterisation of hepatic metastases? A meta-analysis. Eur J Cancer 49:572–584CrossRefPubMedGoogle Scholar
  10. 10.
    Chen L, Zhang J, Zhang L et al (2012) Meta-analysis of gadoxetic acid disodium (Gd-EOB-DTPA)-enhanced magnetic resonance imaging for the detection of liver metastases. PLoS One 7:e48681Google Scholar
  11. 11.
    Koh DM, Collins DJ, Wallace T, Chau I, Riddell AM (2012) Combining diffusion-weighted MRI with Gd-EOB-DTPA-enhanced MRI improves the detection of colorectal liver metastases. Br J Radiol 85:980–989CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Donati OF, Fischer MA, Chuck N, Hunziker R, Weishaupt D, Reiner CS (2012) Accuracy and confidence of Gd-EOB-DTPA enhanced MRI and diffusion-weighted imaging alone and in combination for the diagnosis of liver metastases. Eur J Radiol 82:822–828CrossRefPubMedGoogle Scholar
  13. 13.
    Tajima T, Akahane M, Takao H et al (2012) Detection of liver metastasis: is diffusion-weighted imaging needed in Gd-EOB-DTPA-enhanced MR imaging for evaluation of colorectal liver metastases? Jpn J Radiol 30:648–658CrossRefPubMedGoogle Scholar
  14. 14.
    Macera A, Lario C, Petracchini M et al (2013) Staging of colorectal liver metastases after preoperative chemotherapy. Diffusion-weighted imaging in combination with Gd-EOB-DTPA MRI sequences increases sensitivity and diagnostic accuracy. Eur Radiol 23:739–747CrossRefPubMedGoogle Scholar
  15. 15.
    Kim YK, Lee MW, Lee WJ et al (2012) Diagnostic accuracy and sensitivity of diffusion-weighted and of gadoxetic acid-enhanced 3-T MR imaging alone or in combination in the detection of small liver metastasis (≤1.5 cm in diameter). Invest Radiol 47:159–166PubMedGoogle Scholar
  16. 16.
    Holzapfel K, Eiber MJ, Fingerle AA, Bruegel M, Rummeny EJ, Gaa J (2012) Detection, classification, and characterization of focal liver lesions: value of diffusion-weighted MR imaging, gadoxetic acid-enhanced MR imaging and the combination of both methods. Abdom Imaging 37:74–82CrossRefPubMedGoogle Scholar
  17. 17.
    Chung WS, Kim MJ, Chung YE et al (2011) Comparison of gadoxetic acid-enhanced dynamic imaging and diffusion-weighted imaging for the preoperative evaluation of colorectal liver metastases. J Magn Reson Imaging 34:345–353CrossRefPubMedGoogle Scholar
  18. 18.
    Kim HJ, Lee SS, Byun JH et al (2014) Incremental value of liver MR imaging in patients with potentially curable colorectal hepatic metastasis detected at CT: a prospective comparison of diffusion-weighted imaging, gadoxetic acid-enhanced MR imaging, and a combination of both MR techniques. Radiology 274:712–722CrossRefPubMedGoogle Scholar
  19. 19.
    Zech CJ, Korpraphong P, Huppertz A et al (2014) Randomized multicentre trial of gadoxetic acid-enhanced MRI versus conventional MRI or CT in the staging of colorectal cancer liver metastases. Br J Surg 101:613–621CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Whiting PF, Rutjes AW, Westwood ME et al (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155:529–536CrossRefPubMedGoogle Scholar
  21. 21.
    Reitsma JB, Glas AS, Rutjes AW, Scholten RJ, Bossuyt PM, Zwinderman AH (2005) Bivariate analysis of sensitivity and specificity produces informative summary measures in diagnostic reviews. J Clin Epidemiol 58:982–990CrossRefPubMedGoogle Scholar
  22. 22.
    van Houwelingen HC, Arends LR, Stijnen T (2002) Advanced methods in meta-analysis: multivariate approach and meta-regression. Stat Med 21:589–624CrossRefPubMedGoogle Scholar
  23. 23.
    Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    MacAskill P GC, Deeks JJ, Harbord R, Takwoingi Y (2010) Chapter 10: analysing and presenting results. In: Deeks JJ, Bossuyt PM, Gatsonis C (eds) Cochrane handbook for systematic reviews of diagnostic test accuracy, version 1.0. The Cochrane Collaboration, 2010. Available from:
  25. 25.
    van Enst WA, Ochodo E, Scholten RJ, Hooft L, Leeflang MM (2014) Investigation of publication bias in meta-analyses of diagnostic test accuracy: a meta-epidemiological study. BMC Med Res Methodol 14:70CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Deeks JJ, Macaskill P, Irwig L (2005) The performance of tests of publication bias and other sample size effects in systematic reviews of diagnostic test accuracy was assessed. J Clin Epidemiol 58:882–893CrossRefPubMedGoogle Scholar
  27. 27.
    Neri E, Bali MA, Ba-Ssalamah A et al (2015) ESGAR consensus statement on liver MR imaging and clinical use of liver-specific contrast agents. Eur Radiol. doi: 10.1007/s00330-015-3900-3 PubMedCentralGoogle Scholar
  28. 28.
    Merkle EM, Zech CJ, Bartolozzi C et al (2015) Consensus report from the 7th International Forum for Liver Magnetic Resonance Imaging. Eur Radiol. doi: 10.1007/s00330-015-3873-2 Google Scholar
  29. 29.
    Nordlinger B, Sorbye H, Glimelius B et al (2008) 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 371:1007–1016CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Coenegrachts K, Delanote J, Ter Beek L et al (2007) Improved focal liver lesion detection: comparison of single-shot diffusion-weighted echoplanar and single-shot T2 weighted turbo spin echo techniques. Br J Radiol 80:524–531CrossRefPubMedGoogle Scholar
  31. 31.
    Goshima S, Kanematsu M, Kondo H et al (2008) Diffusion-weighted imaging of the liver: optimizing b value for the detection and characterization of benign and malignant hepatic lesions. J Magn Reson Imaging 28:691–697CrossRefPubMedGoogle Scholar
  32. 32.
    Nasu K, Kuroki Y, Nawano S et al (2006) Hepatic metastases: diffusion-weighted sensitivity-encoding versus SPIO-enhanced MR imaging. Radiology 239:122–130CrossRefPubMedGoogle Scholar
  33. 33.
    Parikh T, Drew SJ, Lee VS et al (2008) Focal liver lesion detection and characterization with diffusion-weighted MR imaging: comparison with standard breath-hold T2-weighted imaging. Radiology 246:812–822CrossRefPubMedGoogle Scholar
  34. 34.
    Koh DM, Brown G, Riddell AM et al (2008) Detection of colorectal hepatic metastases using MnDPDP MR imaging and diffusion-weighted imaging (DWI) alone and in combination. Eur Radiol 18:903–910CrossRefPubMedGoogle Scholar
  35. 35.
    Bruegel M, Gaa J, Waldt S et al (2008) Diagnosis of hepatic metastasis: comparison of respiration-triggered diffusion-weighted echo-planar MRI and five t2-weighted turbo spin-echo sequences. AJR Am J Roentgenol 191:1421–1429CrossRefPubMedGoogle Scholar
  36. 36.
    Coenegrachts K, Matos C, ter Beek L et al (2009) Focal liver lesion detection and characterization: comparison of non-contrast enhanced and SPIO-enhanced diffusion-weighted single-shot spin echo echo planar and turbo spin echo T2-weighted imaging. Eur J Radiol 72:432–439CrossRefPubMedGoogle Scholar
  37. 37.
    Donati OF, Hany TF, Reiner CS et al (2010) Value of retrospective fusion of PET and MR images in detection of hepatic metastases: comparison with 18F-FDG PET/CT and Gd-EOB-DTPA-enhanced MRI. J Nucl Med 51:692–699CrossRefPubMedGoogle Scholar
  38. 38.
    Shimada K, Isoda H, Hirokawa Y, Arizono S, Shibata T, Togashi K (2010) Comparison of gadolinium-EOB-DTPA-enhanced and diffusion-weighted liver MRI for detection of small hepatic metastases. Eur Radiol 20:2690–2698CrossRefPubMedGoogle Scholar
  39. 39.
    Kim YK, Lee YH, Kwak HS, Kim CS, Han YM (2010) Detection of liver metastases: Gadoxetic acid-enhanced three-dimensional MR imaging versus ferucarbotran-enhanced MR imaging. Eur J Radiol 73:131–136CrossRefPubMedGoogle Scholar
  40. 40.
    Seo HJ, Kim MJ, Lee JD, Chung WS, Kim YE (2011) Gadoxetate disodium-enhanced magnetic resonance imaging versus contrast-enhanced 18F-fluorodeoxyglucose positron emission tomography/computed tomography for the detection of colorectal liver metastases. Invest Radiol 46:548–555CrossRefPubMedGoogle Scholar
  41. 41.
    Kim YK, Kim CS, Han YM, Lee YH (2011) Detection of liver malignancy with gadoxetic acid-enhanced MRI: is addition of diffusion-weighted MRI beneficial? Clin Radiol 66:489–496CrossRefPubMedGoogle Scholar
  42. 42.
    Soyer P, Boudiaf M, Place V et al (2011) Preoperative detection of hepatic metastases: comparison of diffusion-weighted, T2-weighted fast spin echo and gadolinium-enhanced MR imaging using surgical and histopathologic findings as standard of reference. Eur J Radiol 80:245–252CrossRefPubMedGoogle Scholar
  43. 43.
    Lowenthal D, Zeile M, Lim WY et al (2011) Detection and characterisation of focal liver lesions in colorectal carcinoma patients: comparison of diffusion-weighted and Gd-EOB-DTPA enhanced MR imaging. Eur Radiol 21:832–840CrossRefPubMedGoogle Scholar
  44. 44.
    Muhi A, Ichikawa T, Motosugi U et al (2011) Diagnosis of colorectal hepatic metastases: comparison of contrast-enhanced CT, contrast-enhanced US, superparamagnetic iron oxide-enhanced MRI, and gadoxetic acid-enhanced MRI. J Magn Reson Imaging 34:326–335CrossRefPubMedGoogle Scholar
  45. 45.
    Sofue K, Tsurusaki M, Tokue H, Arai Y, Sugimura K (2011) Gd-EOB-DTPA-enhanced 3.0 T MR imaging: quantitative and qualitative comparison of hepatocyte-phase images obtained 10 min and 20 min after injection for the detection of liver metastases from colorectal carcinoma. Eur Radiol 21:2336–2343CrossRefPubMedGoogle Scholar
  46. 46.
    Palmucci S, Mauro LA, Messina M et al (2012) Diffusion-weighted MRI in a liver protocol: its role in focal lesion detection. World J Radiol 4:302–310CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Chan VO, Das JP, Gerstenmaier JF et al (2012) Diagnostic performance of MDCT, PET/CT and gadoxetic acid (Primovist(R))-enhanced MRI in patients with colorectal liver metastases being considered for hepatic resection: initial experience in a single centre. Ir J Med Sci 181:499–509CrossRefPubMedGoogle Scholar
  48. 48.
    Berger-Kulemann V, Schima W, Baroud S et al (2012) Gadoxetic acid-enhanced 3.0 T MR imaging versus multidetector-row CT in the detection of colorectal metastases in fatty liver using intraoperative ultrasound and histopathology as a standard of reference. Eur J Surg Oncol 38:670–676CrossRefPubMedGoogle Scholar
  49. 49.
    Kim YK, Park G, Kim CS, Yu HC, Han YM (2012) Diagnostic efficacy of gadoxetic acid-enhanced MRI for the detection and characterisation of liver metastases: comparison with multidetector-row CT. Br J Radiol 85:539–547CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Jeong HT, Kim MJ, Park MS et al (2012) Detection of liver metastases using gadoxetic-enhanced dynamic and 10- and 20-minute delayed phase MR imaging. J Magn Reson Imaging 35:635–643CrossRefPubMedGoogle Scholar
  51. 51.
    Haradome H, Grazioli L, Al Manea K et al (2012) Gadoxetic acid disodium-enhanced hepatocyte phase MRI: can increasing the flip angle improve focal liver lesion detection? J Magn Reson Imaging 35:132–139CrossRefPubMedGoogle Scholar
  52. 52.
    Kim H, Yu JS, Cho ES et al (2012) Diffusion-weighted imaging versus superparamagnetic iron oxide (SPIO)-enhanced MRI: exclusive and combined values in the assessment of hepatic metastases. Magn Reson Imaging 30:554–561CrossRefPubMedGoogle Scholar
  53. 53.
    Kenis C, Deckers F, De Foer B, Van Mieghem F, Van Laere S, Pouillon M (2012) Diagnosis of liver metastases: can diffusion-weighted imaging (DWI) be used as a stand alone sequence? Eur J Radiol 81:1016–1023CrossRefPubMedGoogle Scholar
  54. 54.
    Shimizu H, Isoda H, Fujimoto K et al (2013) Comparison of acquired diffusion weighted imaging and computed diffusion weighted imaging for detection of hepatic metastases. Eur J Radiol 82:453–458CrossRefPubMedGoogle Scholar
  55. 55.
    Lee KH, Lee JM, Park JH et al (2013) MR imaging in patients with suspected liver metastases: value of liver-specific contrast agent gadoxetic acid. Korean J Radiol 14:894–904CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Scharitzer M, Ba-Ssalamah A, Ringl H et al (2013) Preoperative evaluation of colorectal liver metastases: comparison between gadoxetic acid-enhanced 3.0-T MRI and contrast-enhanced MDCT with histopathological correlation. Eur Radiol 23:2187–2196CrossRefPubMedGoogle Scholar
  57. 57.
    Rojas Llimpe FL, Di Fabio F, Ercolani G et al (2014) Imaging in resectable colorectal liver metastasis patients with or without preoperative chemotherapy: results of the PROMETEO-01 study. Br J Cancer 111:667–673CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Ding Y, Rao SX, Meng T, Chen C, Li R, Zeng MS (2014) Preoperative evaluation of colorectal liver metastases: comparison of gadopentetate dimeglumine and gadoxetic-acid-enhanced 1.5-T MRI. Clin Imaging 38:273–278CrossRefPubMedGoogle Scholar
  59. 59.
    Furuta A, Isoda H, Yamashita R et al (2014) Comparison of monopolar and bipolar diffusion weighted imaging sequences for detection of small hepatic metastases. Eur J Radiol 83:1626–1630CrossRefPubMedGoogle Scholar
  60. 60.
    Schmid-Tannwald C, Thomas S, Ivancevic MK et al (2014) Diffusion-weighted MRI of metastatic liver lesions: is there a difference between hypervascular and hypovascular metastases? Acta Radiol 55:515–523CrossRefPubMedGoogle Scholar
  61. 61.
    Yu MH, Lee JM, Hur BY et al (2015) Gadoxetic acid-enhanced MRI and diffusion-weighted imaging for the detection of colorectal liver metastases after neoadjuvant chemotherapy. Eur Radiol 25:2428–2436CrossRefPubMedGoogle Scholar

Copyright information

© European Society of Radiology 2016

Authors and Affiliations

  • Valérie Vilgrain
    • 1
    • 2
    • 3
  • Maxime Esvan
    • 4
    • 5
  • Maxime Ronot
    • 1
    • 2
    • 3
  • Aurore Caumont-Prim
    • 4
    • 5
  • Christophe Aubé
    • 6
    • 7
  • Gilles Chatellier
    • 4
    • 5
    • 8
  1. 1.Department of Radiology, Assistance Publique—Hôpitaux de ParisUniversity Hospitals Paris Nord Val de Seine, BeaujonClichyFrance
  2. 2.University Paris Diderot, Sorbonne Paris CitéParisFrance
  3. 3.INSERM U1149, Centre de Recherche Biomédicale Bichat-Beaujon, CRB3ParisFrance
  4. 4.Hôpital européen Georges-Pompidou, Unité d’Épidémiologie et de Recherche CliniqueParisFrance
  5. 5.INSERM, Centre d’Investigation Clinique 1418, module Épidémiologie CliniqueParisFrance
  6. 6.Department of RadiologyCHU d’AngersAngersFrance
  7. 7.Laboratoire HIFIH, LUNAMUniversité d’AngersAngersFrance
  8. 8.Université Paris Descartes, Sorbonne Paris Cité, Faculté de MédecineParisFrance

Personalised recommendations