Skip to main content

Advertisement

Log in

A meta-analysis evaluating contrast-enhanced intraoperative ultrasound (CE-IOUS) in the context of surgery for colorectal liver metastases

  • Hepatobiliary
  • Published:
Abdominal Radiology Aims and scope Submit manuscript

Abstract

Background

This study aimed to assess the outcomes of contrast-enhanced intraoperative ultrasound (CE-IOUS) for patients with colorectal liver metastases (CRLMs) undergoing surgery.

Method

A thorough literature search was performed in PubMed, Scopus, and Cochrane databases, in accordance with the PRISMA guidelines. The Odds Ratio, Weighted Mean Difference, and 95% Confidence Interval were evaluated, by means of Random-Effects model.

Results

Eleven articles met the inclusion criteria and incorporated 497 patients. The present study shows that CE-IOUS is associated with higher sensitivity and accuracy compared with multidetector computed tomography (MDCT), magnetic resonance imaging (MRI), and intraoperative ultrasound (IOUS) in identifying CRLMs (p < 0.05). The positive predictive value was similar among the different modalities. Furthermore, new CRLMs were identified by CE-IOUS, thus affecting the surgical plan in 128 patients (51.8% of the patients with new CRLMs). Moreover, 91 patients (71%) underwent a more extensive hepatectomy and 15 patients (11.7%) were considered non-operable. Two alternative contrast agents, Sonazoid and Sonovue, were employed with similar sensitivity (p > 0.05).

Conclusion

These outcomes suggest the superiority of the CE-IOUS over MDCT, MRI, and IOUS for the staging of patients with CRLMs undergoing surgery. However, they should be treated with caution given the small number of the included studies.

Graphic abstract

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

Data availability

Raw data and material are available upon request. Supplementary electronic material is provided.

Code availability

Review Manager 5.4 was employed for the present study.

References

  1. 1. Siegel RL, Miller KD, Goding Sauer A, Fedewa SA, Butterly LF, Anderson JC, Cercek A, Smith RA, Jemal A. Colorectal cancer statistics, 2020. CA Cancer J Clin. 2020 May;70(3):145-164. https://doi.org/10.3322/caac.21601. Epub 2020 Mar 5.

    Article  PubMed  Google Scholar 

  2. 2. Evrard S, Poston G, Kissmeyer-Nielsen P, Diallo A, Desolneux G, Brouste V, et al. Combined ablation and resection (CARe) as an effective parenchymal sparing treatment for extensive colorectal liver metastases. PLoS One 2014;9:e114404.

    Article  Google Scholar 

  3. 3. Mazzoni G, Napoli A, Mandetta S, Miccini M, Cassini D, Gregori M, et al. Intraoperative ultrasound for detection of liver metastases from colorectal cancer. Liver Int 2008;28:88e94.

    Google Scholar 

  4. 4. Hoch G, Croise-Laurent V, Germain A, Brunaud L, Bresler L, Ayav A. Is intraoperative ultrasound still useful for the detection of colorectal cancer liver metastases? HPB (Oxford) 2015;17:514e9.

    Article  Google Scholar 

  5. 5. Wagnetz U, Atri M, Massey C, Wei AC, Metser U. Intraoperative ultrasound of the liver in primary and secondary hepatic malignancies: comparison with preoperative 1.5-T MRI and 64-MDCT. AJR Am J Roentgenol 2011;196:562e8.

    Article  Google Scholar 

  6. 6. Torzilli G, Procopio F, Botea F, Marconi M, Del Fabbro D, Donadon M, et al. One-stage ultrasonographically guided hepatectomy for multiple bilobar colorectal metastases: a feasible and effective alternative to the 2-stage approach. Surgery 2009;146:60e71.

    Article  Google Scholar 

  7. 7. Choti MA, Kaloma F, de Oliveira MLet al. Patient variability in intraoperative ultrasonographic characteristics of colorectal liver metastases. Arch Surg 2008;143:29e34.

    Article  Google Scholar 

  8. 8. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JP, et al., The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration, PLoS Med. 6 (2009) e1000100. https://doi.org/10.1136/bmj.b2700

    Article  PubMed  PubMed Central  Google Scholar 

  9. Higgins JPT, Green S. Cochrane Handbook for systematic reviews of interventions version 5.1.0 [updated March 2011]. The Cochrane Collaboration. 2011 Available from www.cochrane-handbook.org

  10. 10. Lee J, Kim KW, Choi SH, Huh J, Park SH. Systematic Review and Meta-Analysis of Studies Evaluating Diagnostic Test Accuracy: A Practical Review for Clinical Researchers-Part II. Statistical Methods of Meta-Analysis. Korean J Radiol. 2015 Nov-Dec;16(6):1188-96. https://doi.org/10.3348/kjr.2015.16.6.1188. Epub 2015 Oct 26. PMID: 26576107

    Article  PubMed  PubMed Central  Google Scholar 

  11. 11. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 25 (2010), pp. 603–605. https://doi.org/10.1007/s10654-010-9491-z.

    Article  Google Scholar 

  12. 12. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629– 34. https://doi.org/10.1136/bmj.315.7109.629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. 13. Arita J, Ono Y, Takahashi M, Inoue Y, Takahashi Y, Matsueda K, et al. Routine Preoperative Liver-specific Magnetic Resonance Imaging Does Not Exclude the Necessity of Contrast-enhanced Intraoperative Ultrasound in Hepatic Resection for Colorectal Liver Metastasis. Ann Surg. 2015 Dec;262(6):1086-91. https://doi.org/10.1097/SLA.0000000000001085.

    Article  PubMed  Google Scholar 

  14. 14. Desolneux G, Isambert M, Mathoulin-Pelissier S, Dupré A, Rivoire M, Cattena V, et al. Contrast-enhanced intra-operative ultrasound as a clinical decision making tool during surgery for colorectal liver metastases: The ULIIS study. Eur J Surg Oncol. 2019 Jul;45(7):1212-1218. https://doi.org/10.1016/j.ejso.2019.03.002.

    Article  CAS  PubMed  Google Scholar 

  15. 15. Fioole B, de Haas RJ, Wicherts DA, Elias SG, Scheffers JM, van Hillegersberg R, et al. Additional value of contrast enhanced intraoperative ultrasound for colorectal liver metastases. Eur J Radiol. 2008 Jul;67(1):169-76. https://doi.org/10.1016/j.ejrad.2007.03.017.

    Article  PubMed  Google Scholar 

  16. 16. Hoareau J, Venara A, Lebigot J, Hamel JF, Lermite E, Caroli-Bosc FX, et al. Intraoperative Contrast-Enhanced Ultrasound in Colorectal Liver Metastasis Surgery Improves the Identification and Characterization of Nodules. World J Surg. 2016 Jan;40(1):190-7. https://doi.org/10.1007/s00268-015-3269-0.

    Article  PubMed  Google Scholar 

  17. 17. 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 Oct;21(10):2067-73. https://doi.org/10.1007/s00330-011-2156-9

    Article  PubMed  Google Scholar 

  18. 18. Leen E, Ceccotti P, Moug SJ, Glen P, MacQuarrie J, Angerson WJ, et al. Potential value of contrast-enhanced intraoperative ultrasonography during partial hepatectomy for metastases: an essential investigation before resection? Ann Surg. 2006 Feb;243(2):236-40. https://doi.org/10.1097/01.sla.0000197708.77063.07.

    Article  PubMed  PubMed Central  Google Scholar 

  19. 19. Oba A, Mise Y, Ito H, Hiratsuka M, Inoue Y, Ishizawa T, et al. Clinical implications of disappearing colorectal liver metastases have changed in the era of hepatocyte-specific MRI and contrast-enhanced intraoperative ultrasonography. HPB (Oxford). 2018 Aug;20(8):708-714. https://doi.org/10.1016/j.hpb.2018.02.377

    Article  PubMed  Google Scholar 

  20. 20. Ruzzenente A, Conci S, Iacono C, Valdegamberi A, Campagnaro T, Bertuzzo F, et al. Usefulness of contrast-enhanced intraoperative ultrasonography (CE-IOUS) in patients with colorectal liver metastases after preoperative chemotherapy. J Gastrointest Surg. 2013 Feb;17(2):281-7. https://doi.org/10.1007/s11605-012-2043-y.

    Article  PubMed  Google Scholar 

  21. 21. Schulz A, Dormagen JB, Drolsum A, Bjørnbeth BA, Labori KJ, Kløw NE. Impact of contrast-enhanced intraoperative ultrasound on operation strategy in case of colorectal liver metastasis. Acta Radiol. 2012 Dec 1;53(10):1081-7. https://doi.org/10.1258/ar.2012.120049

    Article  PubMed  Google Scholar 

  22. 22. Torzilli G, Botea F, Donadon M, Cimino M, Procopio F, Pedicini V, et al. Criteria for the selective use of contrast-enhanced intra-operative ultrasound during surgery for colorectal liver metastases. HPB (Oxford). 2014 Nov;16(11):994-1001. https://doi.org/10.1111/hpb.12272

    Article  PubMed  PubMed Central  Google Scholar 

  23. 23. Uchiyama K, Ueno M, Ozawa S, Kiriyama S, Shigekawa Y, Yamaue H. Combined use of contrast-enhanced intraoperative ultrasonography and a fluorescence navigation system for identifying hepatic metastases. World J Surg. 2010 Dec;34(12):2953-9. https://doi.org/10.1007/s00268-010-0764-1

    Article  PubMed  Google Scholar 

  24. 24. Ignatavicius P, Oberkofler CE, Chapman WC, DeMatteo RP, Clary BM, D’Angelica MI, et al. Choices of Therapeutic Strategies for Colorectal Liver Metastases Among Expert Liver Surgeons: A Throw of the Dice? Ann Surg. 2020 Nov;272(5):715-722. https://doi.org/10.1097/SLA.0000000000004331.

    Article  PubMed  Google Scholar 

  25. 25. Wang K, Liu W, Yan XL, Li J, Xing BC. Long-term postoperative survival prediction in patients with colorectal liver metastasis. Oncotarget. 2017;8:79927–79934.

    Article  Google Scholar 

  26. 26. Clavien PA, Petrowsky H, DeOliveira ML, Graf R. Strategies for safer liver surgery and partial liver transplantation. N Engl J Med. 2007;356:1545–1559.

    Article  Google Scholar 

  27. 27. Clavien PA. Hepatic Vein Embolization for Safer Liver Surgery. Insignificant novelty or a breakthrough? Ann Surg. 2020;272:206–209.

    Article  Google Scholar 

  28. 28. Liu W, Zhang ZY, Yin SS, Yan K, Xing BC. Contrast-Enhanced Intraoperative Ultrasound Improved Sensitivity and Positive Predictive Value in Colorectal Liver Metastasis: a Systematic Review and Meta-Analysis. Ann Surg Oncol. 2020 Nov 27. https://doi.org/10.1245/s10434-020-09365-x.

    Article  PubMed  PubMed Central  Google Scholar 

  29. 29. Granata V, Fusco R, di Castelguidone ED, Avallone A, Palaia R, Delrio P, et al. Diagnostic performance of gadoxetic acid-enhanced liver MRI versus multidetector CT in the assessment of colorectal liver metastases compared to hepatic resection. BMC Gastroenterol, 2019; 19(1):129

    Article  Google Scholar 

  30. 30. Marion-Audibert AM, Vullierme MP, Ronot M, Mabrut JY, Sauvanet A, Zins M, et al. Routine MRI With DWI Sequences to Detect Liver Metastases in Patients With Potentially Resectable Pancreatic Ductal Carcinoma and Normal Liver CT: A Prospective Multicenter Study. AJR Am J Roentgenol. 2018 Nov;211(5):W217-W225. https://doi.org/10.2214/AJR.18.19640.

    Article  PubMed  Google Scholar 

  31. 31. Choi SH, Kim SY, Park SH, Kim KW, Lee JY, Lee SS, et al. Diagnostic performance of CT, gadoxetate disodium-enhanced MRI, and PET/CT for the diagnosis of colorectal liver metastasis: systematic review and metaanalysis. J Magn Reson Imaging. 2018;47(5):1237-1250.

    Article  Google Scholar 

  32. 32. Hagen EK, Forsberg F, Aksnes AK, Merton DA, Liu JB, Tornes A, et al. Enhanced detection of blood flow in the normal canine prostate using an ultrasound contrast agent. Invest Radiol. 2000;35(2):118-124.

    Article  CAS  Google Scholar 

  33. 33. Yanagisawa K, Moriyasu F, Miyahara T, Yuki M, Iijima H. Phagocytosis of ultrasound contrast agent microbubbles by Kupffer cells. Ultrasound Med Biol. 2007;33(2):318-325.

    Article  Google Scholar 

  34. 34. Tsilimigras DI, Ntanasis-Stathopoulos I, Paredes AZ, Moris D, Gavriatopoulou M, Cloyd JM, et al. Disappearing liver metastases: a systematic review of the current evidence. Surg Oncol. 2019;29:7-13.

    Article  Google Scholar 

  35. 35. Hata S, Imamura H, Aoki T, Hashimoto T, Akahane M, Hasegawa K, et al. Value of visual inspection, bimanual palpation, and intraoperative ultrasonography during hepatic resection for liver metastases of colorectal carcinoma. World J Surg. 2011;35(12):2779-2787.

    Article  Google Scholar 

Download references

Funding

No funds, grants, or other support was received.

Author information

Authors and Affiliations

Authors

Contributions

MPF contributed to the conception and design of the work, the acquisition, analysis, and interpretation of data for the work, the drafting the work and revising it critically for important intellectual content, the final approval of the version to be published and is accountable for all aspects of the work. DEM contributed to the design of the work, the interpretation of data for the work, the revising of the work critically for important intellectual content, the final approval of the version to be published and is accountable for all aspects of the work. MV contributed to the acquisition and analysis of data for the work, the drafting the work and revising it critically for important intellectual content, the final approval of the version to be published and is accountable for all aspects of the work. CR contributed to the acquisition and analysis of data for the work, the drafting the work and revising it critically for important intellectual content, the final approval of the version to be published and is accountable for all aspects of the work. TA contributed to the design of the work, the acquisition and analysis of data for the work, the drafting the work and revising it critically for important intellectual content, the final approval of the version to be published and is accountable for all aspects of the work. DZ contributed to the conception and design of the work, the interpretation of data for the work, the revising of the work critically for important intellectual content, the final approval of the version to be published and is accountable for all aspects of the work.

Corresponding author

Correspondence to Dimitrios Zacharoulis.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare that are relevant to the content of this article.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fergadi, M.P., Magouliotis, D.E., Vlychou, M. et al. A meta-analysis evaluating contrast-enhanced intraoperative ultrasound (CE-IOUS) in the context of surgery for colorectal liver metastases. Abdom Radiol 46, 4178–4188 (2021). https://doi.org/10.1007/s00261-021-03096-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00261-021-03096-7

Keywords

Navigation