Skip to main content

Advertisement

SpringerLink
Log in

Liver Stiffness Measurements in Patients with Different Stages of Nonalcoholic Fatty Liver Disease: Diagnostic Performance and Clinicopathological Correlation

  • Original Article
  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

Background

The present study evaluated performance characteristics of liver stiffness measurement (LSM) by FibroScan in patients with different stages of nonalcoholic fatty liver disease (NAFLD).

Patients and Methods

A total of 307 subjects (120 NAFLD, 85 NAFLD related cirrhosis, and 102 healthy controls) were studied.

Results

In NAFLD patients, LSM had significant correlation with fibrosis (r = 0.68, p < 0.001), and increased progressively with increasing fibrosis (p < 0.001). However, the difference between stage 1 and stage 2 fibrosis was not significant (p = 0.07). The LSM in NAFLD without fibrosis and healthy controls was similar (p = 0.37). The areas under receiver-operating characteristics (AUROC) curve of LSM for stages ≥1, ≥2, ≥3, and 4 were 0.82, 0.85, 0.94, and 0.96, respectively. The best LSM (kPa) cut-offs for fibrosis stages ≥1, ≥2, ≥3 and 4 were 6.1, 7.0, 9.0, and 11.8, respectively. The negative predictive value of LSM for excluding advanced fibrosis was 95 %. For advanced fibrosis, the AUROC curve of LSM was 0.94, followed by FIB-4 (0.75), BARD score (0.68), NAFLD fibrosis score (0.66), and aspartate platelet ratio index (0.60). In multivariate analysis, LSM was the only independent predictor of advanced fibrosis (odds ratio 1.47). In patients with NAFLD cirrhosis, LSM correlated significantly with Child-Pugh score (r = 0.40, p < 0.001), serum bilirubin (r = 0.34, p = 0.02), and grades of esophageal varices (r = 0.23, p = 0.04).

Conclusion

LSM is a useful tool for evaluation of patients with NAFLD, and is the best among other non-invasive predictors of liver fibrosis.

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

Abbreviations

NAFLD:

Nonalcoholic fatty liver disease

NASH:

Nonalcoholic steatohepatitis

LSM:

Liver stiffness measurement

TE:

Transient elastography

AST:

Aspartate transaminase

ALT:

Alanine transaminase

IQR:

Interquartile range

APRI:

AST platelet ratio index

ROC:

Receiver operating characteristic

BMI:

Body mass index

AUROC:

Areas under ROC

APRI:

AST platelet ration index

RCS:

Red color sign

INR:

International normalized ratio

References

  1. McCullough AJ. Pathophysiology of nonalcoholic steatohepatitis. J Clin Gastroenterol. 2006;40:S17–S29.

    PubMed  CAS  Google Scholar 

  2. Das K, Das K, Mukherjee PS, et al. Nonobese population in a developing country has a high prevalence of nonalcoholic fatty liver and significant liver disease. Hepatology. 2010;51:1593–1602.

    Article  PubMed  CAS  Google Scholar 

  3. Amarapurkar DN, Hashimoto E, Lesmana LA, Sollano JD, Chen PJ. Asia–Pacific Working Party on NAFLD. How common is non-alcoholic fatty liver disease in the Asia–Pacific region and are there local differences? J Gastroenterol Hepatol. 2007;22:788–793.

    Article  PubMed  Google Scholar 

  4. Rafiq N, Bai C, Fang Y, et al. Long-term follow-up of patients with nonalcoholic fatty liver. Clin Gastroenterol Hepatol. 2009;7:234–238.

    Article  PubMed  Google Scholar 

  5. Bravo AA, Sheth SG, Chopra S. Liver biopsy. N Engl J Med. 2001;344:495–500.

    Article  PubMed  CAS  Google Scholar 

  6. Regev A, Berho M, Jeffers LJ, et al. Sampling error and intraobserver variation in liver biopsy in patients with chronic HCV infection. Am J Gastroenterol. 2002;97:2614–2618.

    Article  PubMed  Google Scholar 

  7. Rosenberg WM, Voelker M, Thiel R, et al. Serum markers detect the presence of liver fibrosis: a cohort study. Gastroenterology. 2004;127:1704–1713.

    Article  PubMed  Google Scholar 

  8. Vizzutti F, Arena U, Nobili V, et al. Non-invasive assessment of fibrosis in non-alcoholic fatty liver disease. Ann Hepatol. 2009;8:89–94.

    PubMed  Google Scholar 

  9. Foucher J, Chanteloup E, Vergniol J, et al. Diagnosis of cirrhosis by transient elastography (FibroScan): a prospective study. Gut. 2006;55:403–408.

    Article  PubMed  CAS  Google Scholar 

  10. Friedrich-Rust M, Ong MF, Martens S, et al. Performance of transient elastography for the staging of liver fibrosis: a meta-analysis. Gastroenterology. 2008;134:960–974.

    Article  PubMed  Google Scholar 

  11. Vizzutti F, Arena U, Romanelli RG, et al. Liver stiffness measurement predicts severe portal hypertension in patients with HCV-related cirrhosis. Hepatology. 2007;45:1290–1297.

    Article  PubMed  Google Scholar 

  12. Kazemi F, Kettaneh A, N’kontchou G, et al. Liver stiffness measurement selects patients with cirrhosis at risk of bearing large oesophageal varices. J Hepatol. 2006;45:230–235.

    Article  PubMed  Google Scholar 

  13. Yoneda M, Yoneda M, Mawatari H, et al. Noninvasive assessment of liver fibrosis by measurement of stiffness in patients with nonalcoholic fatty liver disease (NAFLD). Dig Liver Dis. 2008;40:371–378.

    Article  PubMed  CAS  Google Scholar 

  14. Wong VW, Vergniol J, Wong GL, et al. Diagnosis of fibrosis and cirrhosis using liver stiffness measurement in nonalcoholic fatty liver disease. Hepatology. 2010;51:454–462.

    Article  PubMed  CAS  Google Scholar 

  15. Madan K, Batra Y, Gupta SD, et al. Non-alcoholic fatty liver disease may not be a severe disease at presentation among Asian Indians. World J Gastroenterol. 2006;12:3400–3405.

    PubMed  Google Scholar 

  16. Duseja A, Das A, Das R, et al. The clinicopathological profile of Indian patients with nonalcoholic fatty liver disease (NAFLD) is different from that in the West. Dig Dis Sci. 2007;52:2368–2374.

    Article  PubMed  Google Scholar 

  17. Petersen KF, Dufour S, Feng J, et al. Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men. Proc Nat Acad Sci. 2006;103:18273–18277.

    Article  PubMed  CAS  Google Scholar 

  18. Caldwell SH, Oelsner DH, Iezzoni JC, Hespenheide EE, Battle EH, Driscoll CJ. Cryptogenic cirrhosis: clinical characterization and risk factors for underlying disease. Hepatology. 1999;29:664–669.

    Article  PubMed  CAS  Google Scholar 

  19. Hui JM, Kench JG, Chitturi S, et al. Long-term outcomes of cirrhosis in nonalcoholic steatohepatitis compared with hepatitis C. Hepatology. 2003;38:420–427.

    Article  PubMed  Google Scholar 

  20. Kleiner DE, Brunt EM, Van Natta M, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005;41:1313–1321.

    Article  PubMed  Google Scholar 

  21. Wai CT, Greenson JK, Fontana RJ, et al. A simple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C. Hepatology. 2003;38:518–526.

    Article  PubMed  Google Scholar 

  22. Sterling RK, Lissen E, Clumeck N, et al. Development of a simple noninvasive index to predict significant fibrosis in patients with HIV/HCV coinfection. Hepatology. 2006;43:1317–1325.

    Article  PubMed  CAS  Google Scholar 

  23. Angulo P, Hui JM, Marchesini G, et al. The NAFLD fibrosis score: a noninvasive system that identifies liver fibrosis in patients with NAFLD. Hepatology. 2007;45:846–854.

    Article  PubMed  CAS  Google Scholar 

  24. Harrison SA, Oliver D, Arnold HL, Gogia S, Neuschwander-Tetri BA. Development and validation of a simple NAFLD clinical scoring system for identifying patients without advanced disease. Gut. 2008;57:1441–1447.

    Article  PubMed  CAS  Google Scholar 

  25. DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometric. 1998;44:837–845.

    Article  Google Scholar 

  26. Gómez-Domínguez E, Mendoza J, Rubio S, Moreno-Monteagudo JA, García-Buey L, Moreno-Otero R. Transient elastography: a valid alternative to biopsy in patients with chronic liver disease. Aliment Pharmacol Ther. 2006;24:513–518.

    Article  PubMed  Google Scholar 

  27. Nahon P, Kettaneh A, Tengher-Barna I, et al. Assessment of liver fibrosis using transient elastography in patients with alcoholic liver disease. J Hepatol. 2008;49:1062–1068.

    Article  PubMed  Google Scholar 

  28. Ganne-Carrié N, Ziol M, de Ledinghen V, et al. Accuracy of liver stiffness measurement for the diagnosis of cirrhosis in patients with chronic liver diseases. Hepatology. 2006;44:1511–1517.

    Article  PubMed  Google Scholar 

  29. Ziol M, Handra-Luca A, Kettaneh A, et al. Noninvasive assessment of liver fibrosis by measurement of stiffness in patients with chronic hepatitis C. Hepatology. 2005;41:48–54.

    Article  PubMed  Google Scholar 

  30. Ziol M, Kettaneh A, Ganne-Carrié N, Barget N, Tengher-Barna I, Beaugrand M. Relationships between fibrosis amounts assessed by morphometry and liver stiffness measurements in chronic hepatitis or steatohepatitis. Eur J Gastroenterol Hepatol. 2009;21:1261–1268.

    Article  PubMed  Google Scholar 

  31. Coco B, Oliveri F, Maina AM, et al. Transient elastography: a new surrogate marker of liver fibrosis influenced by major changes of transaminases. J Viral Hepat. 2007;14:360–369.

    Article  PubMed  CAS  Google Scholar 

  32. Arena U, Vizzutti F, Corti G, et al. Acute viral hepatitis increases liver stiffness values measured by transient elastography. Hepatology. 2008;47:380–384.

    Article  PubMed  CAS  Google Scholar 

  33. Petta S, Di Marco V, Cammà C, Butera G, Cabibi D, Craxì A. Reliability of liver stiffness measurement in non-alcoholic fatty liver disease: the effects of body mass index. Aliment Pharmacol Ther. 2011;33:1350–1360.

    Article  PubMed  CAS  Google Scholar 

  34. Castéra L, Le Bail B, Roudot-Thoraval F, et al. Early detection in routine clinical practice of cirrhosis and esophageal varices in chronic hepatitis C: comparison of transient elastography (FibroScan) with standard laboratory tests and non-invasive scores. J Hepatol. 2009;50:59–68.

    Article  PubMed  Google Scholar 

  35. Bureau C, Metivier S, Peron JM, et al. Transient elastography accurately predicts presence of significant portal hypertension in patients with chronic liver disease. Aliment Pharmacol Ther. 2008;27:1261–1268.

    Article  PubMed  CAS  Google Scholar 

  36. Myers RP, Pomier-Layrargues G, Kirsch R, et al. Feasibility and diagnostic performance of the FibroScan XL probe for liver stiffness measurement in overweight and obese patients. Hepatology. 2012;55:199–208.

    Article  PubMed  Google Scholar 

  37. Rifai K, Cornberg J, Mederacke I, et al. Clinical feasibility of liver elastography by acoustic radiation force impulse imaging (ARFI). Dig Liver Dis. 2011;43:491–497.

    Article  PubMed  Google Scholar 

  38. Lucidarme D, Foucher J, Le Bail B, et al. Factors of accuracy of transient elastography (fibroscan) for the diagnosis of liver fibrosis in chronic hepatitis C. Hepatology. 2009;49:1083–1089.

    Article  PubMed  Google Scholar 

  39. Myers RP, Crotty P, Pomier-Layrargues G, Ma M, Urbanski SJ, Elkashab M. Prevalence, risk factors and causes of discordance in fibrosis staging by transient elastography and liver biopsy. Liver Int. 2010;30:1471–1480.

    Article  PubMed  Google Scholar 

  40. Kim SU, Seo YS, Cheong JY, et al. Factors that affect the diagnostic accuracy of liver fibrosis measurement by Fibroscan in patients with chronic hepatitis B. Aliment Pharmacol Ther. 2010;32:498–505.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

We are thankful to Mr Sandeep Kumar from the Information Technology Department of the Institute of Liver and Biliary Sciences for providing computer and technical assistance.

Conflict of interest

None.

Author information

Authors and Affiliations

  1. Department of Hepatology, Institute of Liver and Biliary Sciences (ILBS), Sector D1, Vasant Kunj, New Delhi, 110070, India

    Ramesh Kumar, Manoj Kumar Sharma, Vikram Bhatia, Pankaj Tyagi, Praveen Sharma, Hitendra Garg, K. N. Chandan Kumar & Shiv Kumar Sarin

  2. Department of Pathology, Institute of Liver and Biliary Sciences (ILBS), New Delhi, 110070, India

    Archana Rastogi & Chhagan Bihari

Authors
  1. Ramesh Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Archana Rastogi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Manoj Kumar Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vikram Bhatia
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pankaj Tyagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Praveen Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hitendra Garg
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. K. N. Chandan Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Chhagan Bihari
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Shiv Kumar Sarin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shiv Kumar Sarin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kumar, R., Rastogi, A., Sharma, M.K. et al. Liver Stiffness Measurements in Patients with Different Stages of Nonalcoholic Fatty Liver Disease: Diagnostic Performance and Clinicopathological Correlation. Dig Dis Sci 58, 265–274 (2013). https://doi.org/10.1007/s10620-012-2306-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10620-012-2306-1

Keywords

Search

Navigation