Skip to main content
SpringerLink
Log in

Accuracy of contrast-enhanced ultrasound liver imaging reporting and data system: a systematic review and meta-analysis

  • Original Article
  • Published:
Hepatology International Aims and scope Submit manuscript

Abstract

Background and aim

After the introduction of the contrast-enhanced ultrasound Liver Imaging Reporting and Data System (CEUS LI-RADS), several studies have reported on its performance, but the reported data vary considerably. Therefore, we performed a systematic review and meta-analysis to determine the diagnostic performance of CEUS LI-RADS in patients at risk for hepatocellular carcinoma (HCC) and investigate the causes of study heterogeneity.

Methods

Original studies published until May 30, 2020, investigating the diagnostic performance of CEUS LI-RADS were identified in the MEDLINE, EMBASE, and Cochrane library databases. Study quality was assessed using the QUADAS-2 tool. Meta-analytic summary sensitivity and specificity for the diagnosis of HCC were calculated using a bivariate random-effects model. Meta-regression analysis was performed to explore the causes of study heterogeneity.

Results

Of the 105 articles screened, eight studies were finally analyzed (5428 hepatic observations). The summary sensitivity and specificity of CEUS LI-RADS category 5 (LR-5) for diagnosing HCC were 73% [95% confidence interval (CI) 65–79%; I2 = 93%] and 95% (95% CI 91–97%; I2 = 89%), respectively. Substantial study heterogeneity was noted in both sensitivity and specificity. Study heterogeneity was significantly associated with the proportion of cases of HCC and the type of reference standard (p ≤ 0.05).

Conclusion

CEUS LI-RADS had high pooled specificity for diagnosing HCC but suboptimal pooled sensitivity. Substantial study heterogeneity was found, which was significantly associated with the proportion of cases of HCC and the type of 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

Similar content being viewed by others

Abbreviations

CEUS:

Contrast-enhanced ultrasound

CI:

Confidence interval

CT:

Computed tomography

HCC:

Hepatocellular carcinoma

HSROC:

Hierarchical summary receiver operating characteristics

LI-RADS:

Liver imaging reporting and data system

MRI:

Magnetic resonance imaging

QUADAS-2:

Quality assessment of diagnostic accuracy studies

References

  1. El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology. 2007;132(7):2557–76.

    Article  CAS  Google Scholar 

  2. Chernyak V, Fowler KJ, Kamaya A, Kielar AZ, Elsayes KM, Bashir MR, et al. Liver Imaging Reporting and Data System (LI-RADS) version 2018: imaging of hepatocellular carcinoma in at-risk patients. Radiology. 2018;289(3):816–30.

    Article  Google Scholar 

  3. Wilson SR, Lyshchik A, Piscaglia F, Cosgrove D, Jang HJ, Sirlin C, et al. CEUS LI-RADS: algorithm, implementation, and key differences from CT/MRI. Abdom Radiol (NY). 2018;43(1):127–42.

    Article  Google Scholar 

  4. American College of Radiology. CEUS LI-RADS v2017 core. https://www.acr.org/-/media/ACR/Files/RADS/LI-RADS/CEUS-LI-RADS-2017-Core.pdf. Accessed 14 July 2020.

  5. Schellhaas B, Görtz RS, Pfeifer L, Kielisch C, Neurath MF, Strobel D. Diagnostic accuracy of contrast-enhanced ultrasound for the differential diagnosis of hepatocellular carcinoma: ESCULAP versus CEUS-LI-RADS. Eur J Gastroenterol Hepatol. 2017;29(9):1036–44.

    Article  Google Scholar 

  6. Ling W, Wang M, Ma X, Qiu T, Li J, Lu Q, et al. The preliminary application of Liver Imaging Reporting and Data System (LI-RADS) with contrast-enhanced ultrasound (CEUS) on small hepatic nodules (≤ 2cm). J Cancer. 2018;9(16):2946–52.

    Article  Google Scholar 

  7. Terzi E, Iavarone M, Pompili M, Veronese L, Cabibbo G, Fraquelli M, et al. Contrast ultrasound LI-RADS LR-5 identifies hepatocellular carcinoma in cirrhosis in a multicenter restropective study of 1006 nodules. J Hepatol. 2018;68(3):485–92.

    Article  Google Scholar 

  8. Chen LD, Ruan SM, Lin Y, Liang JY, Shen SL, Hu HT, et al. Comparison between M-score and LR-M in the reporting system of contrast-enhanced ultrasound LI-RADS. Eur Radiol. 2019;29(8):4249–57.

    Article  Google Scholar 

  9. Li J, Ling W, Chen S, Ma L, Yang L, Lu Q, et al. The interreader agreement and validation of contrast-enhanced ultrasound liver imaging reporting and data system. Eur J Radiol. 2019;120:108685.

    Article  Google Scholar 

  10. Hu J, Bhayana D, Burak KW, Wilson SR. Resolution of indeterminate MRI with CEUS in patients at high risk for hepatocellular carcinoma. Abdom Radiol (NY). 2020;45(1):123–33.

    Article  Google Scholar 

  11. Huang JY, Li JW, Lu Q, Luo Y, Lin L, Shi YJ, et al. Diagnostic accuracy of CEUS LI-RADS for the characterization of liver nodules 20 mm or smaller in patients at risk for hepatocellular carcinoma. Radiology. 2020;294(2):329–39.

    Article  Google Scholar 

  12. Kang HJ, Kim JH, Joo I, Han JK. Additional value of contrast-enhanced ultrasound (CEUS) on arterial phase non-hyperenhancement observations (≥ 2 cm) of CT/MRI for high-risk patients: focusing on the CT/MRI LI-RADS categories LR-3 and LR-4. Abdom Radiol (NY). 2020;45(1):55–63.

    Article  Google Scholar 

  13. Makoyeva A, Kim TK, Jang HJ, Medellin A, Wilson SR. Use of CEUS LI-RADS for the accurate diagnosis of nodules in patients at risk for hepatocellular carcinoma: a validation study. Radiology: Imaging Cancer. 2020;2(2):e190014.

  14. Tan Z, Teoh WC, Wong KM, Wansaicheong GK, Sandrasegaran K. Analysis of comparative performance of CEUS and CECT/MR LI-RADS classification: Can CEUS dichotomize LI-RADS indeterminate lesions on CT or MRI? Clin Imaging. 2020;62:63–8.

    Article  Google Scholar 

  15. Wang JY, Feng SY, Yi AJ, Zhu D, Xu JW, Li J, et al. Comparison of contrast-enhanced ultrasound versus contrast-enhanced magnetic resonance imaging for the diagnosis of focal liver lesions using the Liver Imaging Reporting and Data System. Ultrasound Med Biol. 2020;46(5):1216–23.

    Article  Google Scholar 

  16. Wang JY, Feng SY, Xu JW, Li J, Chu L, Cui XW, et al. Usefulness of the contrast-enhanced ultrasound liver imaging reporting and data system in diagnosing focal liver lesions by inexperienced radiologists. J Ultrasound Med. 2020;39(8):1537–46.

    Article  Google Scholar 

  17. Zheng W, Li Q, Zou XB, Wang JW, Han F, Li F, et al. Evaluation of contrast-enhanced US LI-RADS version 2017: application on 2020 liver nodules in patients with hepatitis B infection. Radiology. 2020;294(2):299–307.

    Article  Google Scholar 

  18. van der Pol CB, Lim CS, Sirlin CB, McGrath TA, Salameh JP, Bashir MR, et al. Accuracy of the Liver Imaging Reporting and Data System in computed tomography and magnetic resonance image analysis of hepatocellular carcinoma or overall malignancy-a systematic review. Gastroenterology. 2019;156(4):976–86.

    Article  Google Scholar 

  19. Kim DH, Choi SH, Park SH, Kim KW, Byun JH, Kim SY, et al. Meta-analysis of the accuracy of Liver Imaging Reporting and Data System category 4 or 5 for diagnosing hepatocellular carcinoma. Gut. 2019;68(9):1719–21.

    Article  Google Scholar 

  20. 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.

    Article  Google Scholar 

  21. Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155(8):529–36.

    Article  Google Scholar 

  22. Reitsma JB, Glas AS, Rutjes AW, Scholten RJ, Bossuyt PM, Zwinderman AH. Bivariate analysis of sensitivity and specificity produces informative summary measures in diagnostic reviews. J Clin Epidemiol. 2005;58(10):982–90.

    Article  Google Scholar 

  23. Leeflang MM, Deeks JJ, Rutjes AW, Reitsma JB, Bossuyt PM. Bivariate meta-analysis of predictive values of diagnostic tests can be an alternative to bivariate meta-analysis of sensitivity and specificity. J Clin Epidemiol. 2012;65(10):1088–97.

    Article  Google Scholar 

  24. Rutter CM, Gatsonis CA. A hierarchical regression approach to meta-analysis of diagnostic test accuracy evaluations. Stat Med. 2001;20(19):2865–84.

    Article  CAS  Google Scholar 

  25. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539–58.

    Article  Google Scholar 

  26. Devillé WL, Buntinx F, Bouter LM, Montori VM, de Vet HC, van der Windt DA, et al. Conducting systematic reviews of diagnostic studies: didactic guidelines. BMC Med Res Methodol. 2002;2:9.

    Article  Google Scholar 

  27. Lee S, Kim SS, Roh YH, Choi JY, Park MS, Kim MJ. Diagnostic performance of CT/MRI Liver Imaging Reporting and Data System v2017 for hepatocellular carcinoma: a systematic review and meta-analysis. Liver Int. 2020;40(6):1488–97.

    Article  Google Scholar 

  28. Kim PN, Choi D, Rhim H, Rha SE, Hong HP, Lee J, et al. Planning ultrasound for percutaneous radiofrequency ablation to treat small (≤ 3 cm) hepatocellular carcinomas detected on computed tomography or magnetic resonance imaging: a multicenter prospective study to assess factors affecting ultrasound visibility. J Vasc Interv Radiol. 2012;23(5):627–34.

    Article  Google Scholar 

  29. Lim JH, Kim SH, Lee WJ, Choi D, Kim SH, Lim HK. Ultrasonographic detection of hepatocellular carcinoma: correlation of preoperative ultrasonography and resected liver pathology. Clin Radiol. 2006;61(2):191–7.

    Article  CAS  Google Scholar 

  30. Claudon M, Dietrich CF, Choi BI, Cosgrove DO, Kudo M, Nolsøe CP, et al. Guidelines and good clinical practice recommendations for contrast enhanced ultrasound (CEUS) in the liver–update 2012: a WFUMB-EFSUMB initiative in cooperation with representatives of AFSUMB, AIUM, ASUM, FLAUS and ICUS. Ultraschall Med. 2013;34(1):11–29.

    CAS  PubMed  Google Scholar 

  31. Jang JY, Kim MY, Jeong SW, Kim TY, Kim SU, Lee SH, et al. Current consensus and guidelines of contrast enhanced ultrasound for the characterization of focal liver lesions. Clin Mol Hepatol. 2013;19(1):1–16.

    Article  Google Scholar 

  32. Kim TK, Noh SY, Wilson SR, Kono Y, Piscaglia F, Jang HJ, et al. Contrast-enhanced ultrasound (CEUS) liver imaging reporting and data system (LI-RADS) 2017 - a review of important differences compared to the CT/MRI system. Clin Mol Hepatol. 2017;23(4):280–9.

    Article  Google Scholar 

  33. Wilson SR, Kim TK, Jang HJ, Burns PN. Enhancement patterns of focal liver masses: discordance between contrast-enhanced sonography and contrast-enhanced CT and MRI. AJR Am J Roentgenol. 2007;189(1):W7-w12.

    Article  Google Scholar 

  34. Zhang J, Yu Y, Li Y, Wei L. Diagnostic value of contrast-enhanced ultrasound in hepatocellular carcinoma: a meta-analysis with evidence from 1998 to 2016. Oncotarget. 2017;8(43):75418–26.

    Article  Google Scholar 

  35. Kim KW, Lee J, Choi SH, Huh J, Park SH. Systematic review and meta-analysis of studies evaluating diagnostic test accuracy: a practical review for clinical researchers-part I. General Guidance and Tips. Korean J Radiol. 2015;16(6):1175–1187.

  36. Sica GT. Bias in research studies. Radiology. 2006;238(3):780–9.

    Article  Google Scholar 

  37. Leeflang MM, Rutjes AW, Reitsma JB, Hooft L, Bossuyt PM. Variation of a test’s sensitivity and specificity with disease prevalence. CMAJ. 2013;185(11):E537–44.

    Article  Google Scholar 

Download references

Funding

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korean government (MSIT; grant number: NRF-2019R1G1A1099743).

Author information

Authors and Affiliations

  1. Department of Radiology, Haeundae Paik Hospital, Inje University College of Medicine, Haeundae-ro 875, Haeundae-gu, Busan, 48108, South Korea

    Jung Hee Son

  2. Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center, 88, Olympic-ro 43-gil, Songpa-gu, Seoul, 05505, South Korea

    Sang Hyun Choi, So Yeon Kim, So Jung Lee, Seong Ho Park, Kyung Won Kim, Hyung Jin Won, Yong Moon Shin & Pyo-Nyun Kim

Authors
  1. Jung Hee Son
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sang Hyun Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. So Yeon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. So Jung Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Seong Ho Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kyung Won Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hyung Jin Won
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yong Moon Shin
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Pyo-Nyun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SH Choi provided substantial contributions to the conception and design of the study. Material preparation, data collection, and analysis were performed by JH Son and SH Choi. The methodology of the study was revised by SH Park and KW Kim. The first draft of the manuscript was written by JH Son and SH Choi. The manuscript was reviewed and edited by SY Kim, SJ Lee, HJ Won, YM Shin, and PN Kim. SH Choi supervised the process of the study, and all authors read and approved the final manuscript.

Corresponding author

Correspondence to Sang Hyun Choi.

Ethics declarations

Conflicts of interest

SH Choi receives research funding from Bayer Healthcare. Jung Hee Son, So Yeon Kim, So Jung Lee, Seong Ho Park, Kyung Won Kim, Hyung Jin Won, Yong Moon Shin, Pyo‑Nyun Kim have no conflict of interest are financial ties to disclose.

Additional information

Publisher's Note

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

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Son, J.H., Choi, S.H., Kim, S.Y. et al. Accuracy of contrast-enhanced ultrasound liver imaging reporting and data system: a systematic review and meta-analysis. Hepatol Int 14, 1104–1113 (2020). https://doi.org/10.1007/s12072-020-10102-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12072-020-10102-5

Keywords

Search

Navigation