Effects of patient factors on noninvasive liver stiffness measurement using acoustic radiation force impulse elastography in patients with chronic hepatitis C

BMC Gastroenterology

I-Ping Chiang²  Wen-Pang Su⁵  Po-Heng Chuang⁵  Cheng-Yuan Peng¹  Jung-Ta Kao⁵  Hsueh-Chou Lai⁴  Yu-Fen Li³  Sheng-Hung Chen⁵ 

[1] School of Medicine, China Medical University, Taichung, 40402, Taiwan;Department of Pathology, China Medical University Hospital, Taichung, 40402, Taiwan;Institute of Biostatistics Center, China Medical University, Taichung, 40402, Taiwan;College of Chinese Medicine, China Medical University, Taichung, 40402, Taiwan;China Medical University, Taichung, 40402, Taiwan

关键词: Chronic hepatitis C;    ActiTest;    FibroTest;    Acoustic radiation force impulse;    Cirrhosis;    Liver fibrosis;   

Others  :  1121894
DOI  :  10.1186/1471-230X-12-105

 received in 2012-02-24, accepted in 2012-08-02,  发布年份 2012

【 摘 要 】

Background

Previous research has shown variation in the effects of patient factors, including hepatic necroinflammatory activity, on liver stiffness measurement (LSM). This prospective study attempts to identify explanatory factors for LSM in patients with chronic hepatitis C (CHC) using acoustic radiation force impulse (ARFI) technology.

Methods

A cohort of 127 Taiwanese patients with CHC underwent ARFI LSM and immediate percutaneous liver biopsy. This study compares the concurrent diagnostic performances of LSM and FibroTest using receiver operating characteristic (ROC) curves. Three multiple linear regression models were used to evaluate the significance of concurrent patient factors in explaining LSM.

Results

To classify METAVIR fibrosis (F) stages, the areas under ROC curves (AUCs) were ARFI LSM, 0.847 (95% confidence interval (CI), 0.779-0.914) and FibroTest, 0.823 (95% CI, 0.748-0.898), for F1 versus F2-4; ARFI LSM, 0.902 (95% CI, 0.835-0.970) and FibroTest, 0.812 (95% CI, 0.735-0.888), for F1-2 versus F3-4; ARFI LSM, 0.831 (95% CI, 0.723-0.939) and FibroTest, 0.757 (95% CI, 0.648-0.865), for F1-3 versus F4. After adjusting for other demographic and biological covariates, biochemical and histological necroinflammatory factors consistently explained LSM. Factors included serum alanine aminotransferase (ALT)/upper limit of normal (ULN) categories (model R² = 0.661, adjusted R² = 0.629), ActiTest A scores (R² = 0.662, adjusted R² = 0.636), and METAVIR activity (A) grades (R² = 0.651, adjusted R² = 0.620). METAVIR F stages, body mass index, and platelet count were also independently associated with LSM. Necroinflammatory degrees, including ALT/ULN, ActiTest A scores, and METAVIR A grades, explained the false positivity of liver fibrosis staging using ARFI LSM.

Conclusions

The degree of hepatic necroinflammatory activity independently and significantly exaggerated liver fibrosis evaluation using ARFI LSM. However, comparisons with concurrent FibroTest indicate that ARFI LSM may be a promising alternative, or adjunctive single indicator, for liver fibrosis evaluation in patients with CHC.

【 授权许可】

   
2012 Chen et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Fig. 1.

【 参考文献 】

• [1]Yu ML, Chuang WL: Treatment of chronic hepatitis C in Asia: when East meets West. J Gastroenterol Hepatol 2009, 24:336-345.
• [2]Bizollon T, Ahmed SN, Radenne S, Chevallier M, Chevallier P, Parvaz P, Guichard S, Ducerf C, Baulieux J, Zoulim F, Trepo C: Long term histological improvement and clearance of intrahepatic hepatitis C virus RNA following sustained response to interferon-ribavirin combination therapy in liver transplanted patients with hepatitis C virus recurrence. Gut 2003, 52:283-287.
• [3]Wang JH, Changchien CS, Hung CH, Tung WC, Kee KM, Chen CH, Hu TH, Lee CM, Lu SN: Liver stiffness decrease after effective antiviral therapy in patients with chronic hepatitis C: longitudinal study using FibroScan. J Gastroenterol Hepatol 2010, 25:964-969.
• [4]Moreira RK: Hepatic stellate cells and liver fibrosis. Arch Pathol Lab Med 2007, 131:1728-1734.
• [5]Lai M, Afdhal NH: Editorial: staging liver fibrosis in hepatitis C: a challenge for this decade. Am J Gastroenterol 2011, 106:2121-2122.
• [6]Regev A, Berho M, Jeffers LJ, Milikowski C, Molina EG, Pyrsopoulos NT, Feng ZZ, Reddy KR, Schiff ER: Sampling error and intraobserver variation in liver biopsy in patients with chronic HCV infection. Am J Gastroenterol 2002, 97:2614-2618.
• [7]Friedrich-Rust M, Nierhoff J, Lupsor M, Sporea I, Fierbinteanu-Braticevici C, Strobel D, Takahashi H, Yoneda M, Suda T, Zeuzem S, Herrmann E: Performance of Acoustic Radiation Force Impulse imaging for the staging of liver fibrosis: a pooled meta-analysis. J Viral Hepat 2012, 19:e212-e219.
• [8]Friedrich-Rust M, Wunder K, Kriener S, Sotoudeh F, Richter S, Bojunga J, Herrmann E, Poynard T, Dietrich CF, Vermehren J, Zeuzem S, Sarrazin C: Liver fibrosis in viral hepatitis: noninvasive assessment with acoustic radiation force impulse imaging versus transient elastography. Radiology 2009, 252:595-604.
• [9]Fierbinteanu-Braticevici C, Andronescu D, Usvat R, Cretoiu D, Baicus C, Marinoschi G: Acoustic radiation force imaging sonoelastography for noninvasive staging of liver fibrosis. World J Gastroenterol 2009, 15:5525-5532.
• [10]Lupsor M, Badea R, Stefanescu H, Sparchez Z, Branda H, Serban A, Maniu A: Performance of a new elastographic method (ARFI technology) compared to unidimensional transient elastography in the noninvasive assessment of chronic hepatitis C Preliminary results. J Gastrointestin Liver Dis 2009, 18:303-310.
• [11]Takahashi H, Ono N, Eguchi Y, Eguchi T, Kitajima Y, Kawaguchi Y, Nakashita S, Ozaki I, Mizuta T, Toda S, Kudo S, Miyoshi A, Miyazaki K, Fujimoto K: Evaluation of acoustic radiation force impulse elastography for fibrosis staging of chronic liver disease: a pilot study. Liver Int 2010, 30:538-545.
• [12]Rizzo L, Calvaruso V, Cacopardo B, Alessi N, Attanasio M, Petta S, Fatuzzo F, Montineri A, Mazzola A, L'abbate L, Nunnari G, Bronte F, Di Marco V, Craxì A, Cammà C: Comparison of transient elastography and acoustic radiation force impulse for non-invasive staging of liver fibrosis in patients with chronic hepatitis C. Am J Gastroenterol 2011, 106:2112-2120.
• [13]Colombo S, Buonocore M, Del Poggio A, Jamoletti C, Elia S, Mattiello M, Zabbialini D, Del Poggio P: Head-to-head comparison of transient elastography (TE), real time tissue elastography (RTE), and acoustic radiation force impulse (ARFI) imaging in the diagnosis of liver fibrosis. J Gastroenterol 2012, 47:461-469.
• [14]Sporea I, Sirli RL, Deleanu A, Popescu A, Focsa M, Danila M, Tudora A: Acoustic radiation force impulse elastography as compared to transient elastography and liver biopsy in patients with chronic hepatopathies. Ultraschall Med 2011, 32:S46-S52.
• [15]Yoon KT, Lim SM, Park JY, Kim DY, Ahn SH, Han KH, Chon CY, Cho M, Lee JW, Kim SU: Liver stiffness measurement using acoustic radiation force impulse (ARFI) elastography and effect of necroinflammation. Dig Dis Sci 2012, 57:1682-1691.
• [16]DeLong ER, DeLong DM, Clarke-Pearson DL: Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 1988, 44:837-845.
• [17]Toshima T, Shirabe K, Takeishi K, Motomura T, Mano Y, Uchiyama H, Yoshizumi T, Soejima Y, Taketomi A, Maehara Y: New method for assessing liver fibrosis based on acoustic radiation force impulse: a special reference to the difference between right and left liver. J Gastroenterol 2011, 46:705-711.
• [18]Goertz RS, Zopf Y, Jugl V, Heide R, Janson C, Strobel D, Bernatik T, Haendl T: Measurement of liver elasticity with acoustic radiation force impulse (ARFI) technology: an alternative noninvasive method for staging liver fibrosis in viral hepatitis. Ultraschall Med 2010, 31:151-155.
• [19]Bota S, Sporea I, Sirli R, Popescu A, Dănilă M, Sendroiu M: Factors that influence the correlation of acoustic radiation force impulse (ARFI), elastography with liver fibrosis. Med Ultrason 2011, 13:135-140.
• [20]Arena U, Vizzutti F, Corti G, Ambu S, Stasi C, Bresci S, Moscarella S, Boddi V, Petrarca A, Laffi G, Marra F, Pinzani M: Acute viral hepatitis increases liver stiffness values measured by transient elastography. Hepatology 2008, 47:380-384.
• [21]Sagir A, Erhardt A, Schmitt M, Häussinger D: Transient elastography is unreliable for detection of cirrhosis in patients with acute liver damage. Hepatology 2008, 47:592-595.
• [22]Coco B, Oliveri F, Maina AM, Ciccorossi P, Sacco R, Colombatto P, Bonino F, Brunetto MR: Transient elastography: a new surrogate marker of liver fibrosis influenced by major changes of transaminases. J Viral Hepat 2007, 14:360-369.
• [23]da Lee M, Moon EJ, Hwang JA, Lee MS, Cheong JY, Cho SW, Kim YB, Kim DJ, Hwang SG, Yang JM: Factors associated with liver stiffness in chronic liver disease. Korean J Hepatol 2009, 15:464-473.
• [24]Chan HL, Wong GL, Choi PC, Chan AW, Chim AM, Yiu KK, Chan FK, Sung JJ, Wong VW: Alanine aminotransferase-based algorithms of liver stiffness measurement by transient elastography (Fibroscan) for liver fibrosis in chronic hepatitis B. J Viral Hepat 2009, 16:36-44.
• [25]Seo YS, Lee KG, Jung ES, An H, Park S, Keum B, Yim HJ, Jeen YT, Chun HJ, Kim CD, Ryu HS, Um SH: Dynamic changes in liver stiffness during the course of acute hepatitis A. Scand J Gastroenterol 2010, 45:449-456.
• [26]Fung J, Lai CL, Chan SC, But D, Seto WK, Cheng C, Wong DK, Lo CM, Fan ST, Yuen MF: Correlation of liver stiffness and histological features in healthy persons and in patients with occult hepatitis B, chronic active hepatitis B, or hepatitis B cirrhosis. Am J Gastroenterol 2010, 105:1116-1122.
• [27]Kim BK, Han KH, Park JY, Ahn SH, Chon CY, Kim JK, Paik YH, Lee KS, Park YN, Kim do Y: A novel liver stiffness measurement-based prediction model for cirrhosis in hepatitis B patients. Liver Int 2010, 30:1073-1081.
• [28]Cardoso AC, Carvalho-Filho RJ, Stern C, Dipumpo A, Giuily N, Ripault MP, Asselah T, Boyer N, Lada O, Castelnau C, Martinot-Peignoux M, Valla DC, Bedossa P, Marcellin P: Direct comparison of diagnostic performance of transient elastography in patients with chronic hepatitis B and chronic hepatitis C. Liver Int 2012, 32:612-621.
• [29]Myers RP, Pomier-Layrargues G, Kirsch R, Pollett A, Beaton M, Levstik M, Duarte-Rojo A, Wong D, Crotty P, Elkashab M: Discordance in fibrosis staging between liver biopsy and transient elastography using the FibroScan XL probe. J Hepatol 2012, 56:564-570.
• [30]Tapper EB, Cohen EB, Patel K, Bacon B, Gordon S, Lawitz E, Nelson D, Nasser IA, Challies T, Afdhal N: Levels of alanine aminotransferase confound use of transient elastography to diagnose fibrosis in patients with chronic HCV infection. Clin Gastroenterol Hepatol 2012. Epub ahead of print
• [31]Millonig G, Reimann FM, Friedrich S, Fonouni H, Mehrabi A, Büchler MW, Seitz HK, Mueller S: Extrahepatic cholestasis increases liver stiffness (FibroScan) irrespective of fibrosis. Hepatology 2008, 48:1718-1723.
• [32]Harata M, Hashimoto S, Kawabe N, Nitta Y, Murao M, Nakano T, Arima Y, Shimazaki H, Ishikawa T, Okumura A, Ichino N, Osakabe K, Nishikawa T, Yoshioka K: Liver stiffness in extrahepatic cholestasis correlates positively with bilirubin and negatively with alanine aminotransferase. Hepatol Res 2011, 41:423-429.
• [33]Lebray P, Varnous S, Charlotte F, Varaut A, Poynard T, Ratziu V: Liver stiffness is an unreliable marker of liver fibrosis in patients with cardiac insufficiency. Hepatology 2089, 2008:48.
• [34]Poynard T, Munteanu M, Ngo Y, Castera L, Halfon P, Ratziu V, Imbert-Bismut F, Thabut D, Bourliere M, Cacoub P, Messous D, de Ledinghen V: ActiTest accuracy for the assessment of histological activity grades in patients with chronic hepatitis C, an overview using Obuchowski measure. Gastroenterol Clin Biol 2010, 34:388-396.
• [35]Yin M, Chen J, Glaser KJ, Talwalkar JA, Ehman RL: Abdominal magnetic resonance elastography. Top Magn Reson Imaging 2009, 20:79-87.
• [36]Wong F: Management of ascites in cirrhosis. J Gastroenterol Hepatol 2012, 27:11-20.
• [37]Ngo Y, Munteanu M, Messous D, Charlotte F, Imbert-Bismut F, Thabut D, Lebray P, Thibault V, Benhamou Y, Moussalli J, Ratziu V, Poynard T: A prospective analysis of the prognostic value of biomarkers (FibroTest) in patients with chronic hepatitis C. Clin Chem 2006, 52:1887-1896.
• [38]Poynard T, Ngo Y, Perazzo H, Munteanu M, Lebray P, Moussalli J, Thabut D, Benhamou Y, Ratziu V: Prognostic value of liver fibrosis biomarkers: a meta-analysis. Gastroenterol Hepatol (N Y) 2011, 7:445-454.
• [39]Palmeri ML, Wang MH, Dahl JJ, Frinkley KD, Nightingale KR: Quantifying hepatic shear modulus in vivo using acoustic radiation force. Ultrasound Med Biol 2008, 34:546-558.
• [40]Tozaki M, Isobe S, Fukuma E: Preliminary study of ultrasonographic tissue quantification of the breast using the acoustic radiation force impulse (ARFI) technology. Eur J Radiol 2011, 80:e182-187.
• [41]Theise ND: Liver biopsy assessment in chronic viral hepatitis: a personal, practical approach. Mod Pathol 2007, 20(Suppl 1):S3-14.
• [42]Poynard T, Ratziu V, McHutchison J, Manns M, Goodman Z, Zeuzem S, Younossi Z, Albrecht J: Effect of treatment with peginterferon or interferon alfa-2b and ribavirin on steatosis in patients infected with hepatitis C. Hepatology 2003, 38:75-85.
• [43]Youden WJ: Index for rating diagnostic tests. Cancer 1950, 3:32-35.
• [44]Kim BH, Lee JM, Lee YJ, Lee KB, Suh KS, Han JK, Choi BI: MR elastography for noninvasive assessment of hepatic fibrosis: experience from a tertiary center in Asia. J Magn Reson Imaging 2011, 34:1110-1116.
• [45]Mueller S, Sandrin L: Liver stiffness: a novel parameter for the diagnosis of liver disease. Hepatic Medicine: Evidence and Research 2010, 2:49-65.
• [46]Motosugi U, Ichikawa T, Niitsuma Y, Araki T: Acoustic radiation force impulse elastography of the liver: can fat deposition in the liver affect the measurement of liver stiffness? Jpn J Radiol 2011, 29:639-643.
• [47]Yin M, Woollard J, Wang X, Torres VE, Harris PC, Ward CJ, Glaser KJ, Manduca A, Ehman RL: Quantitative assessment of hepatic fibrosis in an animal model with magnetic resonance elastography. Magn Reson Med 2007, 58:346-353.
• [48]Roulot D, Czernichow S, Le Clésiau H, Costes JL, Vergnaud AC, Beaugrand M: Liver stiffness values in apparently healthy subjects: influence of gender and metabolic syndrome. J Hepatol 2008, 48:606-613.
• [49]Baba M, Furuya K, Bandou H, Kasai K, Sadaoka K: Discrimination of individuals in a general population at high-risk for alcoholic and non-alcoholic fatty liver disease based on liver stiffness: a cross section study. BMC Gastroenterol 2011, 11:70. BioMed Central Full Text
• [50]Talwalkar JA, Yin M, Venkatesh S, Rossman PJ, Grimm RC, Manduca A, Romano A, Kamath PS, Ehman RL: Feasibility of in vivo MR elastographic splenic stiffness measurements in the assessment of portal hypertension. Am J Roentgenol 2009, 193:122-127.
• [51]Wai CT, Greenson JK, Fontana RJ, Kalbfleisch JD, Marrero JA, Conjeevaram HS, Lok AS: A simple non-invasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C. Hepatology 2003, 38:518-526.
• [52]Skripenova S, Trainer TD, Krawitt EL, Blaszyk H: Variability of grade and stage in simultaneous paired liver biopsies in patients with hepatitis C. J Clin Pathol 2007, 60:321-324.
• [53]Yang HI, Yuen MF, Chan HL, Han KH, Chen PJ, Kim DY, Ahn SH, Chen CJ, Wong VW, Seto WK, REACH-B Working Group: Risk estimation for hepatocellular carcinoma in chronic hepatitis B (REACH-B): development and validation of a predictive score. Lancet Oncol 2011, 12:568-574.
• [54]Kim SU, Kim Do Y, Park JY, Lee JH, Ahn SH, Kim JK, Paik YH, Lee KS, Chon CY, Choi EH, Song KJ, Park YN, Han KH: How can we enhance the performance of liver stiffness measurement using FibroScan in diagnosing liver cirrhosis in patients with chronic hepatitis B? J Clin Gastroenterol 2010, 44:66-71.
• [55]Poynard T, Halfon P, Castera L, Munteanu M, Imbert-Bismut F, Ratziu V: Standardization of ROC curve areas for diagnostic evaluation of liver fibrosis markers based on prevalences of fibrosis stages. Clin Chem 2007, 53:1615-1622.