Skip to main content
Log in

Evaluation of liver parenchyma stiffness in patients with liver tumours: optimal strategy for shear wave elastography

  • Ultrasound
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

To determine the methodology of non-invasive test for evaluation of liver stiffness (LS) with tumours using two-dimensional (2D) shear wave elastography (SWE).

Methods

One hundred and twenty-seven patients with liver tumours underwent 2D-SWE before surgery to measure liver and spleen stiffness (SS). Two-dimensional SWE values were obtained in the liver at 0–1 cm, 1–2 cm and >2 cm from the tumour edge (PLS-1, PLS-2 and RLS, respectively). The influence of tumour-associated factors was evaluated. The area under the receiver operating characteristic curve (AUC) for each value was analysed to diagnose cirrhosis.

Results

PLS-1 was higher than PLS-2, which was even higher than RLS (p < 0.001). The AUCs of PLS-1, PLS-2, RLS and SS for diagnosing cirrhosis were 0.760, 0.833, 0.940 and 0.676, with the specificity of 75.7%, 67.6%, 90.3% and 77.4%, respectively. Tumour sizes, locations or types showed no apparent influence on 2D-SWE values except for RLS, which was higher in patients with primary hepatic carcinomas (p < 0.05).

Conclusions

LS with tumours is best measured at >2 cm away from the tumour edge. SS measurement could be used as an alternative to LS measurement in the event of no available liver for detection.

Key Points

• Tumour-associated factors impact background liver stiffness assessment.

• Background liver stiffness is best measured at >2 cm from tumour edge.

• Spleen stiffness can be an alternative to assess background liver stiffness.

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

Abbreviations

2D-SWE:

Two-dimensional shear wave elastography

ALB:

Albumin

ALP:

Alkaline phosphatase

ALT:

Glutamate pyruvate transaminase

AST:

Glutamic oxaloacetic transaminase

CCC:

Cholangiocellular carcinoma

CV:

Coefficient of variation

DBIL:

Direct bilirubin

EFSUMB:

European Federation of Societies for Ultrasound in Medicine and Biology

GGT:

Glutamyl transpeptidase

HBV:

Hepatitis B virus

HCC:

Hepatocellular carcinoma

LS:

Liver stiffness

MHC:

Metastatic hepatic carcinoma

PHLF:

Post-hepatectomy liver failure

PLS :

Peritumoural liver stiffness,

PLS-1 :

Peritumoural liver stiffness measured at 0–1 cm from the tumour edge

PLS-2:

Peritumoural liver stiffness measured at 1–2 cm from the tumour edge

PT:

Prothrombin time

RLS:

Remnant liver stiffness

SS:

Spleen stiffness

SSI:

Supersonic shear imaging

TBIL:

Total bilirubin

TE:

Transient elastography

References

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

    Article  Google Scholar 

  2. Guglielmi A, Ruzzenente A, Conci S, Valdegamberi A, Iacono C (2012) How much remnant is enough in liver resection? Dig Surg 29:6–17

    Article  Google Scholar 

  3. Shoup M, Gonen M, D'Angelica M et al (2003) Volumetric analysis predicts hepatic dysfunction in patients undergoing major liver resection. J Gastrointest Surg 7:325–330

    Article  Google Scholar 

  4. Tanabe G, Sakamoto M, Akazawa K, Al E (1995) Intraoperative risk factors associated with hepatic resection. Br J Surg 82:1262–1265

    Article  CAS  Google Scholar 

  5. Hemming AW, Gallinger S, Greig PD et al (2001) The hippurate ratio as an indicator of functional hepatic reserve for resection of hepatocellular carcinoma in cirrhotic patients. J Gastrointest Surg 5:316–321

    Article  CAS  Google Scholar 

  6. Nagasue N, Yukaya H, Ogawa Y, Kohno H, Nakamura T (1987) Human liver regeneration after major hepatic resection. A study of normal liver and livers with chronic hepatitis and cirrhosis. Ann Surg 206:30–39

    Article  CAS  Google Scholar 

  7. Hu H, Han H, Han XK, Wang WP, Ding H (2018) Nomogram for individualised prediction of liver failure risk after hepatectomy in patients with resectable hepatocellular carcinoma: the evidence from ultrasound data. Eur Radiol 28:877–885

    Article  Google Scholar 

  8. Ferraioli G, Filice C, Castéra L et al (2015) WFUMB guidelines and recommendations for clinical use of ultrasound elastography: Part 3: liver. Ultrasound Med Biol 41:1161–1179

    Article  Google Scholar 

  9. Tsochatzis EA, Gurusamy KS, Ntaoula S, Cholongitas E, Davidson BR, Burroughs AK (2011) Elastography for the diagnosis of severity of fibrosis in chronic liver disease: a meta-analysis of diagnostic accuracy. J Hepatol 54:650–659

    Article  CAS  Google Scholar 

  10. Yoshioka K, Hashimoto S (2012) Can non-invasive assessment of liver fibrosis replace liver biopsy? Hepatol Res 42:233–240

    Article  Google Scholar 

  11. Shiina T, Nightingale KR, Palmeri ML et al (2015) WFUMB guidelines and recommendations for clinical use of ultrasound elastography: Part 1: basic principles and terminology. Ultrasound Med Biol 41:1126–1147

    Article  Google Scholar 

  12. Dietrich CF, Bamber J, Berzigotti A et al (2017) EFSUMB Guidelines and Recommendations on the Clinical Use of Liver Ultrasound Elastography, update 2017 (long version). Ultraschall Med 38:e16–e47

    PubMed  Google Scholar 

  13. European Association for the Study of the Liver (2012) EASL Clinical Practice Guidelines: management of chronic hepatitis B virus infection. J Hepatol 57:167–185

    Article  Google Scholar 

  14. European Association for Study of Liver; Asociacion Latinoamericana para el Estudio del Higado (2015) EASL-ALEH Clinical Practice Guidelines: non-invasive tests for evaluation of liver disease severity and prognosis. J Hepatol 63:237–264

  15. Castéra L, Foucher J, Bernard PH et al (2010) Pitfalls of liver stiffness measurement: a 5-year prospective study of 13,369 examinations. Hepatology 51:828–835

    Google Scholar 

  16. Ferraioli G, Tinelli C, Zicchetti M et al (2012) Reproducibility of real-time shear wave elastography in the evaluation of liver elasticity. Eur J Radiol 81:3102–3106

    Article  Google Scholar 

  17. Tada T, Kumada T, Toyoda H et al (2015) Utility of real-time shear wave elastography for assessing liver fibrosis in patients with chronic hepatitis C infection without cirrhosis: comparison of liver fibrosis indices. Hepatol Res 45:E122–E129

    Article  CAS  Google Scholar 

  18. Ferraioli G, Tinelli C, Dal Bello B, Zicchetti M, Filice G, Filice C (2012) Accuracy of real-time shear wave elastography for assessing liver fibrosis in chronic hepatitis C: a pilot study. Hepatology 56:2125–2133

    Article  Google Scholar 

  19. Leung VY, Shen J, Wong VW et al (2013) Quantitative elastography of liver fibrosis and spleen stiffness in chronic hepatitis B carriers: comparison of shear-wave elastography and transient elastography with liver biopsy correlation. Radiology 269:910–918

    Article  Google Scholar 

  20. Muller M, Gennisson JL, Deffieux T, Tanter M, Fink M (2009) Quantitative viscoelasticity mapping of human liver using supersonic shear imaging: preliminary in vivo feasibility study. Ultrasound Med Biol 35:219–229

    Article  Google Scholar 

  21. Dietrich CF, Bamber J, Berzigotti A et al (2017) EFSUMB Guidelines and Recommendations on the Clinical Use of Liver Ultrasound Elastography, update 2017 (short version). Ultraschall Med 38:377–394

    Article  Google Scholar 

  22. Zeng J, Liu GJ, Huang ZP et al (2014) Diagnostic accuracy of two-dimensional shear wave elastography for the non-invasive staging of hepatic fibrosis in chronic hepatitis B: a cohort study with internal validation. Eur Radiol 24:2572–2581

    Article  Google Scholar 

  23. Wang CZ, Zheng J, Huang ZP et al (2014) Influence of measurement depth on the stiffness assessment of healthy liver with real-time shear wave elastography. Ultrasound Med Biol 40:461–469

    Article  Google Scholar 

  24. Huang Z, Zheng J, Zeng J, Wang X, Wu T, Zheng R (2014) Normal liver stiffness in healthy adults assessed by real-time shear wave elastography and factors that influence this method. Ultrasound Med Biol 40:2549–2555

    Article  Google Scholar 

  25. Huang ZP, Zhang XL, Zeng J, Zheng J, Wang P, Zheng RQ (2014) Study of detection times for liver stiffness evaluation by shear wave elastography. World J Gastroenterol 20:9578–9584

    Article  Google Scholar 

  26. Huang Z, Zheng W, Zhang YJ et al (2017) Assessing hepatic fibrosis using 2-d shear wave elastography in patients with liver tumors: a prospective single-center study. Ultrasound Med Biol 43:2522–2529

    Article  Google Scholar 

  27. Nishio T, Taura K, Koyama Y et al (2016) Prediction of posthepatectomy liver failure based on liver stiffness measurement in patients with hepatocellular carcinoma. Surgery 159:399–408

    Article  Google Scholar 

  28. Han H, Hu H, Xu YD, Wang WP, Ding H, Lu Q (2017) Liver failure after hepatectomy: a risk assessment using the pre-hepatectomy shear wave elastography technique. Eur J Radiol 86:234–240

    Article  Google Scholar 

  29. Elkrief L, Rautou PE, Ronot M et al (2015) Prospective comparison of spleen and liver stiffness by using shear-wave and transient elastography for detection of portal hypertension in cirrhosis. Radiology 275:589–598

    Article  Google Scholar 

  30. Scheuer PJ (1991) Classification of chronic viral hepatitis: a need for reassessment. J Hepatol 13:372–374

    Article  CAS  Google Scholar 

  31. Thiele M, Madsen BS, Procopet B et al (2017) Reliability criteria for liver stiffness measurements with real-time 2D shear wave elastography in different clinical scenarios of chronic liver disease. Ultraschall Med 38:648–654

    Article  Google Scholar 

  32. DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 3:837–845

    Article  Google Scholar 

  33. Ling W, Lu Q, Quan J, Ma L, Luo Y (2013) Assessment of impact factors on shear wave based liver stiffness measurement. Eur J Radiol 82:335–341

    Article  Google Scholar 

  34. Samir AE, Dhyani M, Vij A et al (2015) Shear-wave elastography for the estimation of liver fibrosis in chronic liver disease: determining accuracy and ideal site for measurement. Radiology 274:888–896

    Article  Google Scholar 

  35. Tian WS, Lin MX, Zhou LY et al (2016) Maximum value measured by 2-D shear wave elastography helps in differentiating malignancy from benign focal liver lesions. Ultrasound Med Biol 42:2156–2166

    Article  Google Scholar 

  36. Hoshida Y, Villanueva A, Kobayashi M et al (2008) Gene expression in fixed tissues and outcome in hepatocellular carcinoma. N Engl J Med 359:1995–2004

    Article  CAS  Google Scholar 

  37. Lu Q, Ling W, Lu C et al (2015) Hepatocellular carcinoma: stiffness value and ratio to discriminate malignant from benign focal liver lesions. Radiology 275:880–888

    Article  Google Scholar 

  38. Stefanescu H, Grigorescu M, Lupsor M, Procopet B, Maniu A, Badea R (2011) Spleen stiffness measurement using Fibroscan for the noninvasive assessment of esophageal varices in liver cirrhosis patients. J Gastroenterol Hepatol 26:164–170

    Article  Google Scholar 

  39. Sharma P, Kirnake V, Tyagi P et al (2013) Spleen stiffness in patients with cirrhosis in predicting esophageal varices. Am J Gastroenterol 108:1101–1107

    Article  Google Scholar 

  40. Grgurevic I, Puljiz Z, Brnic D et al (2015) Liver and spleen stiffness and their ratio assessed by real-time two dimensional-shear wave elastography in patients with liver fibrosis and cirrhosis due to chronic viral hepatitis. Eur Radiol 25:3214–3221

    Article  Google Scholar 

Download references

Funding

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

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Xiao-qing Pei or Fu-jun Zhang.

Ethics declarations

Guarantor

The scientific guarantor of this publication is An-hua Li.

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 obtained from all subjects (patients) in this study.

Ethical approval

Institutional review board approval was obtained.

Methodology

• prospective

• diagnostic or prognostic study

• performed at one institution

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zheng, W., Zhou, Zg., Wong, Ch. et al. Evaluation of liver parenchyma stiffness in patients with liver tumours: optimal strategy for shear wave elastography. Eur Radiol 29, 1479–1488 (2019). https://doi.org/10.1007/s00330-018-5676-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-018-5676-8

Keywords

Navigation