Skip to main content

Advertisement

SpringerLink
Log in

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

  • Magnetic Resonance
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

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

Methods

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.

Results

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.

Conclusions

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

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Steele G Jr, Ravikumar TS (1989) Resection of hepatic metastases from colorectal cancer. Biologic perspective. Ann Surg 210:127–138

    Article  PubMed  PubMed Central  Google Scholar 

  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 13:1261–1268

    Article  PubMed  Google Scholar 

  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 17:1225–1239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 64:551–558

    CAS  PubMed  Google Scholar 

  5. Goere D, Elias D (2008) Resection of liver metastases from non-colorectal non-endocrine primary tumours. Eur J Surg Oncol 34:281–288

    Article  CAS  PubMed  Google Scholar 

  6. Bipat S, van Leeuwen MS, Comans EF et al (2005) Colorectal liver metastases: CT, MR imaging, and PET for diagnosis—meta-analysis. Radiology 237:123–131

    Article  PubMed  Google Scholar 

  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 31:19–31

    Article  PubMed  Google Scholar 

  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 257:674–684

    Article  PubMed  Google Scholar 

  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 49:572–584

    Article  PubMed  Google Scholar 

  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:e48681

  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 85:980–989

    Article  PubMed  PubMed Central  Google Scholar 

  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 82:822–828

    Article  PubMed  Google Scholar 

  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 30:648–658

    Article  PubMed  Google Scholar 

  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 23:739–747

    Article  PubMed  Google Scholar 

  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 47:159–166

    CAS  PubMed  Google Scholar 

  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 37:74–82

    Article  PubMed  Google Scholar 

  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 34:345–353

    Article  PubMed  Google Scholar 

  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 274:712–722

    Article  PubMed  Google Scholar 

  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 101:613–621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 155:529–536

    Article  PubMed  Google Scholar 

  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 58:982–990

    Article  PubMed  Google Scholar 

  22. van Houwelingen HC, Arends LR, Stijnen T (2002) Advanced methods in meta-analysis: multivariate approach and meta-regression. Stat Med 21:589–624

    Article  PubMed  Google Scholar 

  23. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560

    Article  PubMed  PubMed Central  Google Scholar 

  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: http://srdta.cochrane.org/

  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 14:70

    Article  PubMed  PubMed Central  Google Scholar 

  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 58:882–893

    Article  PubMed  Google Scholar 

  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

    PubMed Central  Google Scholar 

  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. 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 371:1007–1016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 80:524–531

    Article  CAS  PubMed  Google Scholar 

  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 28:691–697

    Article  PubMed  Google Scholar 

  32. Nasu K, Kuroki Y, Nawano S et al (2006) Hepatic metastases: diffusion-weighted sensitivity-encoding versus SPIO-enhanced MR imaging. Radiology 239:122–130

    Article  PubMed  Google Scholar 

  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 246:812–822

    Article  PubMed  Google Scholar 

  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 18:903–910

    Article  CAS  PubMed  Google Scholar 

  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 191:1421–1429

    Article  PubMed  Google Scholar 

  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 72:432–439

    Article  PubMed  Google Scholar 

  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 51:692–699

    Article  PubMed  Google Scholar 

  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 20:2690–2698

    Article  PubMed  Google Scholar 

  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 73:131–136

    Article  PubMed  Google Scholar 

  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 46:548–555

    Article  CAS  PubMed  Google Scholar 

  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 66:489–496

    Article  PubMed  Google Scholar 

  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 80:245–252

    Article  PubMed  Google Scholar 

  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 21:832–840

    Article  CAS  PubMed  Google Scholar 

  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 34:326–335

    Article  PubMed  Google Scholar 

  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 21:2336–2343

    Article  PubMed  Google Scholar 

  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 4:302–310

    Article  PubMed  PubMed Central  Google Scholar 

  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 181:499–509

    Article  CAS  PubMed  Google Scholar 

  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 38:670–676

    Article  CAS  PubMed  Google Scholar 

  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 85:539–547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 35:635–643

    Article  PubMed  Google Scholar 

  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 35:132–139

    Article  PubMed  Google Scholar 

  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 30:554–561

    Article  CAS  PubMed  Google Scholar 

  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 81:1016–1023

    Article  PubMed  Google Scholar 

  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 82:453–458

    Article  PubMed  Google Scholar 

  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 14:894–904

    Article  PubMed  PubMed Central  Google Scholar 

  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 23:2187–2196

    Article  CAS  PubMed  Google Scholar 

  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 111:667–673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 38:273–278

    Article  PubMed  Google Scholar 

  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 83:1626–1630

    Article  PubMed  Google Scholar 

  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 55:515–523

    Article  PubMed  Google Scholar 

  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 25:2428–2436

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Department of Radiology, Assistance Publique—Hôpitaux de Paris, University Hospitals Paris Nord Val de Seine, Beaujon, Clichy, Hauts-de-Seine, France

    Valérie Vilgrain & Maxime Ronot

  2. University Paris Diderot, Sorbonne Paris Cité, Paris, France

    Valérie Vilgrain & Maxime Ronot

  3. INSERM U1149, Centre de Recherche Biomédicale Bichat-Beaujon, CRB3, Paris, France

    Valérie Vilgrain & Maxime Ronot

  4. Hôpital européen Georges-Pompidou, Unité d’Épidémiologie et de Recherche Clinique, 75015, Paris, France

    Maxime Esvan, Aurore Caumont-Prim & Gilles Chatellier

  5. INSERM, Centre d’Investigation Clinique 1418, module Épidémiologie Clinique, 75015, Paris, France

    Maxime Esvan, Aurore Caumont-Prim & Gilles Chatellier

  6. Department of Radiology, CHU d’Angers, Angers, France

    Christophe Aubé

  7. Laboratoire HIFIH, LUNAM, Université d’Angers, Angers, France

    Christophe Aubé

  8. Université Paris Descartes, Sorbonne Paris Cité, Faculté de Médecine, 75006, Paris, France

    Gilles Chatellier

Authors
  1. Valérie Vilgrain
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maxime Esvan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maxime Ronot
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Aurore Caumont-Prim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Christophe Aubé
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gilles Chatellier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Valérie Vilgrain.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vilgrain, V., Esvan, M., Ronot, M. et al. A meta-analysis of diffusion-weighted and gadoxetic acid-enhanced MR imaging for the detection of liver metastases. Eur Radiol 26, 4595–4615 (2016). https://doi.org/10.1007/s00330-016-4250-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-016-4250-5

Keywords

Search

Navigation