European Radiology

, Volume 29, Issue 3, pp 1479–1488 | Cite as

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

  • Wei Zheng
  • Zhong-guo Zhou
  • Chong-hei Wong
  • Xiao-qing PeiEmail author
  • Shu-lian Zhuang
  • Qing Li
  • Min-Shan Chen
  • An-hua Li
  • Fu-jun ZhangEmail author



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


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.


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).


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.


Elasticity imaging techniques Ultrasonography Liver neoplasms Liver cirrhosis Spleen 



Two-dimensional shear wave elastography




Alkaline phosphatase


Glutamate pyruvate transaminase


Glutamic oxaloacetic transaminase


Cholangiocellular carcinoma


Coefficient of variation


Direct bilirubin


European Federation of Societies for Ultrasound in Medicine and Biology


Glutamyl transpeptidase


Hepatitis B virus


Hepatocellular carcinoma


Liver stiffness


Metastatic hepatic carcinoma


Post-hepatectomy liver failure


Peritumoural liver stiffness,


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


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


Prothrombin time


Remnant liver stiffness


Spleen stiffness


Supersonic shear imaging


Total bilirubin


Transient elastography



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

Compliance with ethical standards


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.


• prospective

• diagnostic or prognostic study

• performed at one institution


  1. 1.
    Clavien PA, Petrowsky H, DeOliveira ML, Graf R (2007) Strategies for safer liver surgery and partial liver transplantation. N Engl J Med 356:1545–1559Google Scholar
  2. 2.
    Guglielmi A, Ruzzenente A, Conci S, Valdegamberi A, Iacono C (2012) How much remnant is enough in liver resection? Dig Surg 29:6–17Google Scholar
  3. 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 7:325–330Google Scholar
  4. 4.
    Tanabe G, Sakamoto M, Akazawa K, Al E (1995) Intraoperative risk factors associated with hepatic resection. Br J Surg 82:1262–1265Google Scholar
  5. 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 5:316–321Google Scholar
  6. 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 206:30–39Google Scholar
  7. 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 28:877–885Google Scholar
  8. 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 41:1161–1179Google Scholar
  9. 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 54:650–659Google Scholar
  10. 10.
    Yoshioka K, Hashimoto S (2012) Can non-invasive assessment of liver fibrosis replace liver biopsy? Hepatol Res 42:233–240Google Scholar
  11. 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 41:1126–1147Google Scholar
  12. 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–e47Google Scholar
  13. 13.
    European Association for the Study of the Liver (2012) EASL Clinical Practice Guidelines: management of chronic hepatitis B virus infection. J Hepatol 57:167–185Google Scholar
  14. 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 63:237–264Google Scholar
  15. 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 51:828–835Google Scholar
  16. 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 81:3102–3106Google Scholar
  17. 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–E129Google Scholar
  18. 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 56:2125–2133Google Scholar
  19. 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 269:910–918Google Scholar
  20. 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 35:219–229Google Scholar
  21. 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 38:377–394Google Scholar
  22. 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 24:2572–2581Google Scholar
  23. 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 40:461–469Google Scholar
  24. 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 40:2549–2555Google Scholar
  25. 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 20:9578–9584Google Scholar
  26. 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 43:2522–2529Google Scholar
  27. 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 159:399–408Google Scholar
  28. 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 86:234–240Google Scholar
  29. 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 275:589–598Google Scholar
  30. 30.
    Scheuer PJ (1991) Classification of chronic viral hepatitis: a need for reassessment. J Hepatol 13:372–374Google Scholar
  31. 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 38:648–654Google Scholar
  32. 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 3:837–845Google Scholar
  33. 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 82:335–341Google Scholar
  34. 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 274:888–896Google Scholar
  35. 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 42:2156–2166Google Scholar
  36. 36.
    Hoshida Y, Villanueva A, Kobayashi M et al (2008) Gene expression in fixed tissues and outcome in hepatocellular carcinoma. N Engl J Med 359:1995–2004Google Scholar
  37. 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 275:880–888Google Scholar
  38. 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 26:164–170Google Scholar
  39. 39.
    Sharma P, Kirnake V, Tyagi P et al (2013) Spleen stiffness in patients with cirrhosis in predicting esophageal varices. Am J Gastroenterol 108:1101–1107Google Scholar
  40. 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 25:3214–3221Google Scholar

Copyright information

© European Society of Radiology 2018

Authors and Affiliations

  • Wei Zheng
    • 1
  • Zhong-guo Zhou
    • 2
  • Chong-hei Wong
    • 2
    • 3
  • Xiao-qing Pei
    • 1
    Email author
  • Shu-lian Zhuang
    • 4
  • Qing Li
    • 1
  • Min-Shan Chen
    • 2
  • An-hua Li
    • 1
  • Fu-jun Zhang
    • 5
    Email author
  1. 1.Department of UltrasoundSun Yat-sen University Cancer Centre, State Key Laboratory of Oncology in South China; Collaborative Innovation Centre for Cancer MedicineGuangzhouPeople’s Republic of China
  2. 2.Department of Hepatobiliary OncologySun Yat-sen University Cancer Centre, State Key Laboratory of Oncology in South China; Collaborative Innovation Centre for Cancer MedicineGuangzhouPeople’s Republic of China
  3. 3.Department of OncologyCentro Hospitalar Conde de S. Januario (CHCSJ)MacaoPeople’s Republic of China
  4. 4.Department of Ultrasonographythe Second Affiliated Hospital of Guangzhou University of Traditional Chinese MedicineGuangzhouPeople’s Republic of China
  5. 5.Minimally Invasive Interventional CentreSun Yat-sen University Cancer Centre, State Key Laboratory of Oncology in South China; Collaborative Innovation Centre for Cancer MedicineGuangzhouPeople’s Republic of China

Personalised recommendations