Clinical application of liver stiffness measurement using transient elastography: A surgical perspective

Digestion

Volumn 88, Issue 4, 2013, Pages 258-265

  Kim, Seung Up ^a,b   Kim, Beom Kyung ^a,b   Han, Kwang Hyub ^a,b  

^a Yonsei University College of Medicine   (South Korea)

^b Liver Cirrhosis Clinical Research Centre   (South Korea)

Author keywords

Liver stiffness; Outcome; Resection; Transient elastography; Transplantation

Indexed keywords

INDOCYANINE GREEN;

CANCER RECURRENCE; CAUSE OF DEATH; DISEASE SEVERITY; ELASTOGRAPHY; GRAFT DYSFUNCTION; GRAFT RECIPIENT; HEPATITIS C; HEPATOBILIARY PARAMETERS; HUMAN; LIVER CELL CARCINOMA; LIVER FAILURE; LIVER FIBROSIS; LIVER GRAFT; LIVER RESECTION; LIVER STIFFNESS; LIVER TRANSPLANTATION; MONITORING; PORTAL HYPERTENSION; PORTAL VEIN BLOOD PRESSURE; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; REVIEW; TRANSIENT ELASTOGRAPHY; ECHOGRAPHY; HEPATITIS C VIRUS; IMMUNOSUPPRESSIVE TREATMENT; LONG TERM CARE; PHYSICAL PARAMETERS; PROGNOSIS; RECURRENT DISEASE; VENOUS PRESSURE;

ELASTICITY IMAGING TECHNIQUES; FIBROSIS; HEPATECTOMY; HUMANS; LIVER; LIVER CIRRHOSIS; LIVER TRANSPLANTATION; PREDICTIVE VALUE OF TESTS; TREATMENT OUTCOME;

EID: 84892189445     PISSN: 00122823     EISSN: 14219867     Source Type: Journal    
DOI: 10.1159/000355948     Document Type: Review

References (86)

1. Jang JW: Current status of liver diseases in Korea: liver cirrhosis. Korean J Hepatol 2009; 15(suppl 6):S40-S49.
2. Lok AS: Hepatitis B: Liver fibrosis and hepatocellular carcinoma. Gastroenterol Clin Biol 2009; 33: 911-915.
3. McGill DB, Rakela J, Zinsmeister AR, Ott BJ: A 21-year experience with major hemorrhage after percutaneous liver biopsy. Gastroenterology 1990; 99: 1396-1400.
4. Jin SY: Role of liver biopsy in the assessment of hepatic fibrosis -its utility and limitations (in Korean). Korean J Hepatol 2007; 13: 138-145.
5. 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.
6. Abraldes JG, Araujo IK, Turon F, Berzigotti A: Diagnosing and monitoring cirrhosis: liver biopsy, hepatic venous pressure gradient and elastography. Gastroenterol Hepatol 2012; 35: 488-495.
7. Castera L, Forns X, Alberti A: Non-invasive evaluation of liver fibrosis using transient elastography. J Hepatol 2008; 48: 835-847.
8. Sandrin L, Fourquet B, Hasquenoph JM, Yon S, Fournier C, Mal F, Christidis C, Ziol M, Poulet B, Kazemi F, Beaugrand M, Palau R: Transient elastography: a new noninvasive method for assessment of hepatic fibrosis. Ultrasound Med Biol 2003; 29: 1705-1713.
9. Talwalkar JA, Kurtz DM, Schoenleber SJ, West CP, Montori VM: Ultrasound-based transient elastography for the detection of hepatic fibrosis: systematic review and metaanalysis. Clin Gastroenterol Hepatol 2007; 5: 1214-1220.
10. Kim SU, Seo YS, Cheong JY, Kim MY, Kim JK, Um SH, Cho SW, Paik SK, Lee KS, Han KH, Ahn SH: 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.
11. Kim SU, Han KH, Ahn SH: Transient elastography in chronic hepatitis B: an Asian perspective. World J Gastroenterol 2010; 16: 5173-5180.
12. Jung KS, Kim SU: Clinical applications of transient elastography. Clin Mol Hepatol 2012; 18: 163-173.
13. Kim SU, Park JY, Kim do Y, Ahn SH, Choi EH, Seok JY, Lee JM, Park YN, Chon CY, Han KH: Non-invasive assessment of changes in liver fibrosis via liver stiffness measurement in patients with chronic hepatitis B: impact of antiviral treatment on fibrosis regression. Hepatol Int 2010; 4: 673-680.
14. Scott DR, Levy MT: Liver transient elastography (Fibroscan ® ): a place in the management algorithms of chronic viral hepatitis. Antivir Ther 2010; 15: 1-11.
15. Stebbing J, Farouk L, Panos G, Anderson M, Jiao LR, Mandalia S, Bower M, Gazzard B, Nelson M: A meta-analysis of transient elastography for the detection of hepatic fibrosis. J Clin Gastroenterol 2010; 44: 214-219.
16. Han KH, Yoon KT: New diagnostic method for liver fibrosis and cirrhosis. Intervirology 2008; 51(suppl 1):11-16.
17. Smith JO, Sterling RK: Systematic review: non-invasive methods of fibrosis analysis in chronic hepatitis C. Aliment Pharmacol Ther 2009; 30: 557-576.
18. Friedrich-Rust M, Ong MF, Martens S, Sarrazin C, Bojunga J, Zeuzem S, Herrmann E: Performance of transient elastography for the staging of liver fibrosis: a meta-analysis. Gastroenterology 2008; 134: 960-974.
19. Chon YE, Choi EH, Song KJ, Park JY, Kim do Y, Han KH, Chon CY, Ahn SH, Kim SU: Performance of transient elastography for the staging of liver fibrosis in patients with chronic hepatitis B: a meta-analysis. PLoS One 2012; 7:e44930.
20. Kim SU, Han KH, Ahn SH: Non-invasive assessment of liver fibrosis: time to move from cross-sectional studies to longitudinal ones. J Gastroenterol Hepatol 2010; 25: 1472-1473.
21. Kim SU, Ahn SH, Park JY, Kim do Y, Chon CY, Choi JS, Kim KS, Han KH: Prediction of postoperative hepatic insufficiency by liver stiffness measurement (Fibroscan ® ) before curative resection of hepatocellular carcinoma: a pilot study. Hepatol Int 2008; 2: 471-477.
22. Cescon M, Colecchia A, Cucchetti A, Peri E, Montrone L, Ercolani G, Festi D, Pinna AD: Value of transient elastography measured with Fibroscan ® in predicting the outcome of hepatic resection for hepatocellular carcinoma. Ann Surg 2012; 256: 706-713.
23. Jung KS, Kim SU, Choi GH, Park JY, Park YN, Kim DY, Ahn SH, Chon CY, Kim KS, Choi EH, Choi JS, Han KH: Prediction of recurrence after curative resection of hepatocellular carcinoma using liver stiffness measurement (Fibroscan ® ). Ann Surg Oncol 2012; 19: 4278-4286.
24. Wong JS, Wong GL, Chan AW, Wong VW, Cheung YS, Chong CN, Wong J, Lee KF, Chan HL, Lai PB: Liver stiffness measurement by transient elastography as a predictor on posthepatectomy outcomes. Ann Surg 2013; 257: 922-928.
25. Rigamonti C, Donato MF, Fraquelli M, Agnelli F, Ronchi G, Casazza G, Rossi G, Colombo M: Transient elastography predicts fibrosis progression in patients with recurrent hepatitis C after liver transplantation. Gut 2008; 57: 821-827.
26. Carrion JA, Navasa M, Bosch J, Bruguera M, Gilabert R, Forns X: Transient elastography for diagnosis of advanced fibrosis and portal hypertension in patients with hepatitis C recurrence after liver transplantation. Liver Transpl 2006; 12: 1791-1798.
27. Harada N, Soejima Y, Taketomi A, Yoshizumi T, Ikegami T, Yamashita Y, Itoh S, Kuroda Y, Maehara Y: Assessment of graft fibrosis by transient elastography in patients with recurrent hepatitis C after living donor liver transplantation. Transplantation 2008; 85: 69-74.
28. Corradi F, Piscaglia F, Flori S, D'Errico-Grigioni A, Vasuri F, Tame MR, Andreone P, Boni P, Gianstefani A, Bolondi L: Assessment of liver fibrosis in transplant recipients with recurrent HCV infection: usefulness of transient elastography. Dig Liver Dis 2009; 41: 217-225.
29. Lee JG, Kang CM, Park JS, Kim KS, Yoon DS, Choi JS, Lee WJ, Kim BR: The actual five-year survival rate of hepatocellular carcinoma patients after curative resection. Yonsei Med J 2006; 47: 105-112.
30. Lai EC, Fan ST, Lo CM, Chu KM, Liu CL, Wong J: Hepatic resection for hepatocellular carcinoma. An audit of 343 patients. Ann Surg 1995; 221: 291-298.
31. Shuto T, Hirohashi K, Kubo S, Tanaka H, Tsukamoto T, Yamamoto T, Ikebe T, Kinoshita H: Changes and results of surgical strategies for hepatocellular carcinoma: results of a 15-year study on 452 consecutive patients. Surg Today 1998; 28: 1124-1129.
32. Torzilli G, Makuuchi M, Inoue K, Takayama T, Sakamoto Y, Sugawara Y, Kubota K, Zucchi A: No-mortality liver resection for hepatocellular carcinoma in cirrhotic and noncirrhotic patients: is there a way? A prospective analysis of our approach. Arch Surg 1999; 134: 984-992.
33. Kim SU, Kim YC, Choi JS, Kim KS, Choi GH, Park JY, Kim do Y, Ahn SH, Choi EH, Park YN, Chon CY, Han KH, Kim MJ: Can preoperative diffusion-weighted MRI predict postoperative hepatic insufficiency after curative resection of HBV-related hepatocellular carcinoma? A pilot study. Magn Reson Imaging 2010; 28: 802-811.
34. Lewin M, Poujol-Robert A, Boelle PY, Wendum D, Lasnier E, Viallon M, Guechot J, Hoeffel C, Arrive L, Tubiana JM, Poupon R: Diffusion-weighted magnetic resonance imaging for the assessment of fibrosis in chronic hepatitis C. Hepatology 2007; 46: 658-665.
35. Koinuma M, Ohashi I, Hanafusa K, Shibuya H: Apparent diffusion coefficient measurements with diffusion-weighted magnetic resonance imaging for evaluation of hepatic fibrosis. J Magn Reson Imaging 2005; 22: 80-85.
36. Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, de Santibanes E, Pekolj J, Slankamenac K, Bassi C, Graf R, Vonlanthen R, Padbury R, Cameron JL, Makuuchi M: The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg 2009; 250: 187-196.
37. Dindo D, Demartines N, Clavien PA: Classification of surgical complications: a new proposal with evaluation in a cohort of 6,336 patients and results of a survey. Ann Surg 2004; 240: 205-213.
38. Poon RT, Fan ST, Lo CM, Liu CL, Lam CM, Yuen WK, Yeung C, Wong J: Extended hepatic resection for hepatocellular carcinoma in patients with cirrhosis: is it justified? Ann Surg 2002; 236: 602-611.
39. Fan ST, Lai EC, Lo CM, Ng IO, Wong J: Hospital mortality of major hepatectomy for hepatocellular carcinoma associated with cirrhosis. Arch Surg 1995; 130: 198-203.
40. Kim MS, Lee JR: Assessment of liver stiffness measurement: novel intraoperative blood loss predictor? World J Surg 2013; 37: 185-191.
41. 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.
42. Sagir A, Erhardt A, Schmitt M, Haussinger D: Transient elastography is unreliable for detection of cirrhosis in patients with acute liver damage. Hepatology 2008; 47: 592-595.
43. Inoue Y, Sugawara Y, Tamura S, Ohtsu H, Taguri M, Makuuchi M, Kokudo N: Validity and feasibility of transient elastography for the transplanted liver in the peritransplantation period. Transplantation 2009; 88: 103-109.
44. Lee SH, Joo DJ, Kim SU, Kim MS, Lee AL, Choi GH, Choi JS, Han KH, Kim SI: Graft function measured by transient elastography in living donor liver transplantation: preliminary. Transplant Proc 2013;45:3028-3031.
45. Hubscher SG: What is the long-term outcome of the liver allograft? J Hepatol 2011; 55: 702-717
46. Sebagh M, Rifai K, Feray C, Yilmaz F, Falissard B, Roche B, Bismuth H, Samuel D, Reynes M: All liver recipients benefit from the protocol 10-year liver biopsies. Hepatology 2003; 37: 1293-1301.
47. Slapak GI, Saxena R, Portmann B, Gane E, Devlin J, Calne R, Williams R: Graft and systemic disease in long-term survivors of liver transplantation. Hepatology 1997; 25: 195-202.
48. Seo S, Maganti K, Khehra M, Ramsamooj R, Tsodikov A, Bowlus C, McVicar J, Zern M, Torok N: De novo nonalcoholic fatty liver disease after liver transplantation. Liver Transpl 2007; 13: 844-847.
49. Scheenstra R, Peeters PM, Verkade HJ, Gouw AS: Graft fibrosis after pediatric liver transplantation: ten years of follow-up. Hepatology 2009; 49: 880-886.
50. Gor NV, Levy RM, Ahn J, Kogan D, Dodson SF, Cohen SM: Biliary cast syndrome following liver transplantation: predictive factors and clinical outcomes. Liver Transpl 2008; 14: 1466-1472.
51. Frizell E, Abraham A, Doolittle M, Bashey R, Kresina T, Van Thiel D, Zern MA: FK506 enhances fibrogenesis in in vitro and in vivo models of liver fibrosis in rats. Gastroenterology 1994; 107: 492-498.
52. Khanna A, Kapur S, Sharma V, Li B, Suthanthiran M: In vivo hyperexpression of transforming growth factor-? 1 in mice: stimulation by cyclosporine. Transplantation 1997; 63: 1037-1039.
53. Carrion JA, Torres F, Crespo G, Miquel R, Garcia-Valdecasas JC, Navasa M, Forns X: Liver stiffness identifies two different patterns of fibrosis progression in patients with hepatitis C virus recurrence after liver transplantation. Hepatology 2010; 51: 23-34.
54. Rigamonti C, Donato MF, Colombo M: Transient elastography in the early prediction of progressive recurrent hepatitis C following liver transplantation. Hepatology 2010; 52: 800-801.
55. Testa G, Crippin JS, Netto GJ, Goldstein RM, Jennings LW, Brkic BS, Brooks BK, Levy MF, Gonwa TA, Klintmalm GB: Liver transplantation for hepatitis C: recurrence and disease progression in 300 patients. Liver Transpl 2000; 6: 553-561.
56. Hubscher SG: Transplantation pathology. Semin Liver Dis 2009; 29: 74-90.
57. Gane EJ, Portmann BC, Naoumov NV, Smith HM, Underhill JA, Donaldson PT, Maertens G, Williams R: Long-term outcome of hepatitis C infection after liver transplantation. N Engl J Med 1996; 334: 815-820.
58. Garcia-Retortillo M, Forns X, Llovet JM, Navasa M, Feliu A, Massaguer A, Bruguera M, Fuster J, Garcia-Valdecasas JC, Rimola A: Hepatitis C recurrence is more severe after living donor compared to cadaveric liver transplantation. Hepatology 2004; 40: 699-707.
59. Dickson RC, Caldwell SH, Ishitani MB, Lau JY, Driscoll CJ, Stevenson WC, McCullough CS, Pruett TL: Clinical and histologic patterns of early graft failure due to recurrent hepatitis C in four patients after liver transplantation. Transplantation 1996; 61: 701-705.
60. Berenguer M, Ferrell L, Watson J, Prieto M, Kim M, Rayon M, Cordoba J, Herola A, Ascher N, Mir J, Berenguer J, Wright TL: HCV-related fibrosis progression following liver transplantation: increase in recent years. J Hepatol 2000; 32: 673-684.
61. Neumann UP, Berg T, Bahra M, Seehofer D, Langrehr JM, Neuhaus R, Radke C, Neuhaus P: Fibrosis progression after liver transplantation in patients with recurrent hepatitis C. J Hepatol 2004; 41: 830-836.
62. Chalasani N, Manzarbeitia C, Ferenci P, Vogel W, Fontana RJ, Voigt M, Riely C, Martin P, Teperman L, Jiao J, Lopez-Talavera JC: Peginterferon alfa-2a for hepatitis C after liver transplantation: two randomized, controlled trials. Hepatology 2005; 41: 289-298.
63. Berenguer M, Aguilera V, Prieto M, Ortiz C, Rodriguez M, Gentili F, Risalde B, Rubin A, Canada R, Palau A, Rayon JM: Worse recent efficacy of antiviral therapy in liver transplant recipients with recurrent hepatitis C: impact of donor age and baseline cirrhosis. Liver Transpl 2009; 15: 738-746.
64. Beckebaum S, Iacob S, Klein CG, Dechene A, Varghese J, Baba HA, Sotiropoulos GC, Paul A, Gerken G, Cicinnati VR: Assessment of allograft fibrosis by transient elastography and noninvasive biomarker scoring systems in liver transplant patients. Transplantation 2010; 89: 983-993.
65. Rigamonti C, Fraquelli M, Bastiampillai AJ, Caccamo L, Reggiani P, Rossi G, Colombo M, Donato MF: Transient elastography identifies liver recipients with nonviral graft disease after transplantation: a guide for liver biopsy. Liver Transpl 2012; 18: 566-576.
66. Syn WK, Nightingale P, Gunson B, Hubscher SG, Neuberger JM: Natural history of unexplained chronic hepatitis after liver transplantation. Liver Transpl 2007; 13: 984-989.
67. Mells G, Mann C, Hubscher S, Neuberger J: Late protocol liver biopsies in the liver allograft: a neglected investigation? Liver Transpl 2009; 15: 931-938.
68. Fraquelli M, Rigamonti C, Casazza G, Conte D, Donato MF, Ronchi G, Colombo M: Reproducibility of transient elastography in the evaluation of liver fibrosis in patients with chronic liver disease. Gut 2007; 56: 968-973.
69. Arena U, Vizzutti F, Abraldes JG, Corti G, Stasi C, Moscarella S, Milani S, Lorefice E, Petrarca A, Romanelli RG, Laffi G, Bosch J, Marra F, Pinzani M: Reliability of transient elastography for the diagnosis of advanced fibrosis in chronic hepatitis C. Gut 2008; 57: 1288-1293.
70. 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.
71. Wong GL, Wong VW, Choi PC, Chan AW, Chim AM, Yiu KK, Chan FK, Sung JJ, Chan HL: Increased liver stiffness measurement by transient elastography in severe acute exacerbation of chronic hepatitis B. J Gastroenterol Hepatol 2009; 24: 1002-1007.
72. Kim SU, Kim JK, Park YN, Han KH: Discordance between liver biopsy and Fibroscan ® in assessing liver fibrosis in chronic hepatitis B: risk factors and influence of necroinflammation. PLoS One 2011; 7:e32233.
73. Fung J, Lai CL, But D, Hsu A, Seto WK, Cheng C, Wong DK, Yuen MF: Reduction of liver stiffness following resolution of acute flares of chronic hepatitis B. Hepatol Int 2010; 4: 716-722.
74. 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.
75. Millonig G, Reimann FM, Friedrich S, Fonouni H, Mehrabi A, Buchler MW, Seitz HK, Mueller S: Extrahepatic cholestasis increases liver stiffness (Fibroscan ® ) irrespective of fibrosis. Hepatology 2008; 48: 1718-1723.
76. Foucher J, Castera L, Bernard PH, Adhoute X, Laharie D, Bertet J, Couzigou P, de Ledinghen V: Prevalence and factors associated with failure of liver stiffness measurement using Fibroscan ® in a prospective study of 2,114 examinations. Eur J Gastroenterol Hepatol 2006; 18: 411-412.
77. De Ledinghen V, Wong VW, Vergniol J, Wong GL, Foucher J, Chu SH, Le Bail B, Choi PC, Chermak F, Yiu KK, Merrouche W, Chan HL: Diagnosis of liver fibrosis and cirrhosis using liver stiffness measurement: comparison between M and XL probe of Fibroscan ® . J Hepatol 2011; 56: 833-839.
78. Chung JH, Ahn HS, Kim SG, Lee YN, Kim YS, Jeong SW, Jang JY, Lee SH, Kim HS, Kim BS: The usefulness of transient elastography, acoustic-radiation-force impulse elastography, and real-time elastography for the evaluation of liver fibrosis. Clin Mol Hepatol 2013; 19: 156-164.
79. Ye XP, Ran HT, Cheng J, Zhu YF, Zhang DZ, Zhang P, Zheng YY: Liver and spleen stiffness measured by acoustic radiation force impulse elastography for noninvasive assessment of liver fibrosis and esophageal varices in patients with chronic hepatitis B. J Ultrasound Med 2013; 31: 1245-1253.
80. 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, Craxi A, Camma 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.
81. Tamaki N, Kurosaki M, Matsuda S, Nakata T, Muraoka M, Suzuki Y, Yasui Y, Suzuki S, Hosokawa T, Nishimura T, Ueda K, Tsuchiya K, Nakanishi H, Itakura J, Takahashi Y, Matsunaga K, Taki K, Asahina Y, Izumi N: Prospective comparison of real-time tissue elastography and serum fibrosis markers for the estimation of liver fibrosis in chronic hepatitis C patients. Hepatol Res 2013, DOI:10.1111/hepr.12179.
82. Chin JL, Chan G, McCormick PA: Spleen stiffness: the new kid on the block for diagnosing portal hypertension? Gastroenterology 2013; 144: 1152-1153.
83. Sharma P, Kirnake V, Tyagi P, Bansal N, Singla V, Kumar A, Arora A: Spleen stiffness in patients with cirrhosis in predicting esophageal varices. Am J Gastroenterol 2013; 108: 1101-1107.
84. Furuichi Y, Moriyasu F, Taira J, Sugimoto K, Sano T, Ichimura S, Miyata Y, Imai Y: Noninvasive diagnostic method for idiopathic portal hypertension based on measurements of liver and spleen stiffness by ARFI elastography. J Gastroenterol 2013; 48: 1061-1068.
85. Park H, Park JY, Kim do Y, Ahn SH, Chon CY, Han KH, Kim SU: Characterization of focal liver masses using acoustic radiation force impulse elastography. World J Gastroenterol 2013; 19: 219-226.
86. Yu H, Wilson SR: Differentiation of benign from malignant liver masses with acoustic radiation force impulse technique. Ultrasound Q 2011; 27: 217-223.