Skip to main content
Top
Published in: Digestive Diseases and Sciences 1/2013

01-01-2013 | Original Article

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

Authors: Ramesh Kumar, Archana Rastogi, Manoj Kumar Sharma, Vikram Bhatia, Pankaj Tyagi, Praveen Sharma, Hitendra Garg, K. N. Chandan Kumar, Chhagan Bihari, Shiv Kumar Sarin

Published in: Digestive Diseases and Sciences | Issue 1/2013

Login to get access

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.
Literature
1.
go back to reference McCullough AJ. Pathophysiology of nonalcoholic steatohepatitis. J Clin Gastroenterol. 2006;40:S17–S29.PubMed McCullough AJ. Pathophysiology of nonalcoholic steatohepatitis. J Clin Gastroenterol. 2006;40:S17–S29.PubMed
2.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
3.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
4.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
6.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
7.
go back to reference Rosenberg WM, Voelker M, Thiel R, et al. Serum markers detect the presence of liver fibrosis: a cohort study. Gastroenterology. 2004;127:1704–1713.PubMedCrossRef Rosenberg WM, Voelker M, Thiel R, et al. Serum markers detect the presence of liver fibrosis: a cohort study. Gastroenterology. 2004;127:1704–1713.PubMedCrossRef
8.
go back to reference 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 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
9.
go back to reference Foucher J, Chanteloup E, Vergniol J, et al. Diagnosis of cirrhosis by transient elastography (FibroScan): a prospective study. Gut. 2006;55:403–408.PubMedCrossRef Foucher J, Chanteloup E, Vergniol J, et al. Diagnosis of cirrhosis by transient elastography (FibroScan): a prospective study. Gut. 2006;55:403–408.PubMedCrossRef
10.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
11.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
12.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
13.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
14.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
15.
go back to reference 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 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
16.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
17.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
18.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
19.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
20.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
21.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
22.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
23.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
24.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
25.
go back to reference 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.CrossRef 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.CrossRef
26.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
27.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
28.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
29.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
30.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
31.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
32.
go back to reference Arena U, Vizzutti F, Corti G, et al. Acute viral hepatitis increases liver stiffness values measured by transient elastography. Hepatology. 2008;47:380–384.PubMedCrossRef Arena U, Vizzutti F, Corti G, et al. Acute viral hepatitis increases liver stiffness values measured by transient elastography. Hepatology. 2008;47:380–384.PubMedCrossRef
33.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
34.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
35.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
36.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
37.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
38.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
39.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
40.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
Metadata
Title
Liver Stiffness Measurements in Patients with Different Stages of Nonalcoholic Fatty Liver Disease: Diagnostic Performance and Clinicopathological Correlation
Authors
Ramesh Kumar
Archana Rastogi
Manoj Kumar Sharma
Vikram Bhatia
Pankaj Tyagi
Praveen Sharma
Hitendra Garg
K. N. Chandan Kumar
Chhagan Bihari
Shiv Kumar Sarin
Publication date
01-01-2013
Publisher
Springer US
Published in
Digestive Diseases and Sciences / Issue 1/2013
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-012-2306-1

Other articles of this Issue 1/2013

Digestive Diseases and Sciences 1/2013 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.