Implication of normal liver enzymes in liver disease

Journal of Viral Hepatitis

Volumn 16, Issue 8, 2009, Pages 529-536

  Calvaruso, Vincenza ^a   Craxì, Antonio ^a  

^a UNIVERSITY OF PALERMO   (Italy)

Author keywords

Aminotransferases; Chronic hepatitis; Liver fibrosis

Indexed keywords

ALANINE AMINOTRANSFERASE; HEPATITIS B SURFACE ANTIGEN; LIVER ENZYME; VIRUS DNA;

BODY MASS; CHRONIC HEPATITIS; GROUPS BY AGE; HEPATITIS B VIRUS; HEPATITIS C VIRUS; HUMAN; LIVER DISEASE; NONALCOHOLIC FATTY LIVER; POPULATION RESEARCH; PRIORITY JOURNAL; REVIEW;

ALANINE TRANSAMINASE; HUMANS; LIVER; LIVER DISEASES; SENSITIVITY AND SPECIFICITY;

EID: 68749085069     PISSN: 13520504     EISSN: 13652893     Source Type: Journal    
DOI: 10.1111/j.1365-2893.2009.01150.x     Document Type: Review

References (85)

1. Hoofnagle JH. Hepatitis C: the clinical spectrum of disease. Hepatology 1997 3 (Suppl 1 15S 20S.
2. Okanoue T, Makiyama A, Nakayama M et al. A follow-up study to determine the value of liver biopsy and need for antiviral therapy for hepatitis C virus carriers with persistently normal serum aminotransferase. J Hepatol 2005 43 (4 599 605.
3. Lai CL, Yuen MF. The natural history and treatment of chronic hepatitis B: a critical evaluation of standard treatment criteria and end points. Ann Intern Med 2007 147 (1 58 61.
4. Dufour DR, Lott JA, Nolte FS et al. Diagnosis and monitoring of hepatic injury. I. Performance characteristics of laboratory tests. Clin Chem 2000 46 : 2027 2049.
5. Puoti C, Castellacci R, Montagnese F et al. Histological and virological features and follow-up of hepatitis C virus carriers with normal aminotransferase levels: the Italian prospective study of the asymptomatic C carriers (ISACC). J Hepatol 2002 37 : 117 123.
6. Marcellin P, Levy S, Erlinger S. Therapy of hepatitis C: patients with normal aminotransferase levels. Hepatology 1997 26 : 133S 136S.
7. Shindo M, Arai K, Sokawa Y et al. The virological and histological states of anti-hepatitis C virus-positive subjects with normal liver biochemical values. Hepatology 1995 22 : 418 425.
8. Rumi MG, De Filippi F, La Vecchia C et al. Hepatitis C reactivation in patients with chronic infection with genotypes 1b and 2c: a retrospective cohort study of 206 untreated patients. Gut 2005 54 (3 402 406.
9. Esteban JI, Lopez-Talavera JC, Genesca J et al. High rate of infectivity and liver disease in blood donors with antibodies to hepatitis C virus. Ann Intern Med 1991 115 : 443 449.
10. Mathurin P, Moussalli J, Cadranel JF et al. Slow progression rate of fibrosis in hepatitis C virus patients with persistently normal alanine transaminase activity. Hepatology 1998 27 : 868 872.
11. Prati D, Taioli E, Zanella A et al. Updated definitions of healthy ranges for serum alanine aminotransferase levels. Ann Intern Med 2002 137 : 1 10.
12. Pradat P, Alberti A, Poynard T et al. Predictive value of ALT levels for histologic findings in chronic hepatitis C: a European collaborative study. Hepatology 2002 36 (pt 1 973 977.
13. Shiffman ML, Diago M, Tran A et al. Chronic hepatitis C in patients with persistently normal alanine transaminaselevels. Clin Gastroenterol Hepatol 2006 4 : 645 652.
14. Hui CK, Belaye T, Montegrande K, Wright TL. A comparison in the progression of liver fibrosis in chronic hepatitis C between persistently normal and elevated transaminases. J Hepatol 2003 38 : 511 517.
15. Alberti A, Noventa F, Benvegnù L et al. Prevalence of liver disease in a population of asymptomatic persons with hepatitis C virus infection. Ann Intern Med 2002 137 (12 961 964.
16. Strader DB, Wright T, Thomas DL, Seeff LB. Diagnosis, management, and treatment of Hepatitis C. Hepatology 2004 39 : 1147.
17. Colletta C, Smirne C, Fabris C et al. Value of two noninvasive methods to detect progression of fibrosis among HCV carriers with normal aminotransferases. Hepatology 2005 42 : 838 845.
18. Poynard T, Munteanu M, Ngo Y et al. Diagnostic value of FibroTest with normal serum aminotransferases. Hepatology 2006 43 : 374 375.
19. Koda M, Matunaga Y, Kawakami M et al. FibroIndex, a practical index for predicting significant fibrosis in patients with chronic hepatitis C. Hepatology 2007 45 : 297 306.
20. Fabris C, Smirne C, Toniutto P et al. Assessment of liverfibrosis progression in patients with chronic hepatitis C andnormal alanine aminotransferase values: the role of AST to the platelet ratio index. Clin Biochem 2006 39 : 339 343.
21. Sebastiani G, Vario A, Guido M et al. Stepwise combination algorithms of noninvasive markers to diagnose significant fibrosis in chronic hepatitis C. J Hepatol 2006 44 : 686 693.
22. Sebastiani G, Vario A, Guido M, Alberti A. Performance of noninvasive markers for liver fibrosis is reduced in chronic hepatitis C with normal transaminases. J Viral Hepat 2008 15 : 212 218. (Pubitemid 351143742)
23. Maida I, Soriano V, Barreiro P et al. Liver fibrosis stage and HCV genotype distribution in HIV-HCV coinfected patients with persistently normal transaminases. AIDS Res Hum Retroviruses 2007 23 (6 801 804.
24. Sandrin L, Tanter M, Gennisson JL et al. Shear elasticity probe for soft tissues with 1-D transient elastography. IEEE Trans Ultrason Ferroelectr Freq Control 2002 49 : 436 446.
25. 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 (5 360 369.
26. Arena U, Vizzutti F, Corti G et al. Acute viral hepatitis increases liver stiffness values measured by transient elastography. Hepatology 2008 47 : 380 384.
27. 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 : 592 597.
28. Calvaruso V, Cammà C, Di Marco V et al. Error factors for transient elastography in chronic Hepatitis C. Hepatology 2008 48 : 65A.
29. Prieto M, Olaso V, Verdu C et al. Does the healthy hepatitis C virus carrier state really exist? An analysis using polymerase chain reaction. Hepatology 1995 22 : 413 417.
30. Shakil AO, Conry-Cantilena C, Alter HJ et al. Volunteer blood donors with antibody to hepatitis C virus: clinical, biochemical, virologic, and histologic features. The Hepatitis C Study Group. Ann Intern Med 1995 123 : 330 337.
31. Bacon BR. Treatment of patients with hepatitis C and normal serum aminotransferase levels. Hepatology 2002 36 : S179 S184.
32. EASL International Consensus Conference on Hepatitis C. EASL International Consensus Conference on Hepatitis C: Consensus Statement. J Hepatol 1999 30 : 956 961.
33. Puoti C, Guido M, Mangia A et al. (Committee on HCV carriers with normal alanine aminotransferase levels of the Italian Association for The Study of the Liver). Clinical management of HCV carriers with normal aminotransferase levels. Dig Liver Dis 2003 35 : 362 369.
34. Marcellin P, Levy S, Erlinger S. Therapy of hepatitis C: patients with normal aminotransferase levels. Hepatology 1997 26 (Suppl 1 133S 136S.
35. Zeuzem S, Diago M, Gane E et al. International, multicenter, randomized, controlled study for the treatment of patients with chronic hepatitis C and persistently normal ALT levels with PegInterferon Alfa-2a (40 Kd) (Pegasys) and Ribavirin (copegus). Hepatology 2003 38 (4 10635.
36. National Institutes of Health. National Institutes of Health Consensus Development Conference Statement: Management of hepatitis C: 2002 - June 10-12. Hepatology 2002 36 : S3 S20.
37. Alberti A. Towards more individualised management of hepatitis C virus patients with initially or persistently normal alanineaminotransferase levels. J Hepatol 2005 42 : 266 274.
38. Keeffe EB, Dieterich DT, Han SHB et al. A treatment algorithm for the management of chronic hepatitis B virus infection in the United States: an update. Clin Gastroenterol Hepatol 2006 4 : 936 962.
39. Lok ASF, McMahon BJ. Chronic hepatitis B. Hepatology 2007 45 : 507 539.
40. Hoofnagle JH, Doo E, Liang TJ et al. Management of hepatitis B: summary of a clinical research workshop. Hepatology 2007 45 : 1056 1075.
41. Chen CJ, Yang HI, Su J et al. Risk of hepatocellular carcinoma across a biological gradient of serum hepatitis B virus DNA level. JAMA 2006 295 : 65 73.
42. Iloeje UH, Yang HI, Su J et al. Predicting cirrhosis risk based on the level of circulating hepatitis B viral load. Gastroenterology 2006 130 : 678 686.
43. Yuen MF, Yuan HJ, Wong DKH et al. Prognostic determinants for chronic hepatitis B in Asians: therapeutic implications. Gut 2005 54 : 1610 1614.
44. Yim HJ, Lok AS-F. Natural history of chronic hepatitis B virus infection: what we knew in 1981 and what we know in 2005. Hepatology 2006 43 : S173 S181.
45. Hui C-K, Leung N, Yuen S-T et al. Natural history and disease progression in Chinese chronic hepatitis B patients in immunetolerant phase. Hepatology 2007 46 : 395 401. (Pubitemid 47344774)
46. Nguyen MH, Trinh H, Garcia RT et al. Significant histologic disease in HBV-infected patients with normal to minimally elevated ALT levels at initial evaluation (abstract). Hepatology 2005 42 : 593A.
47. Terrault N, Kim WR, Lim SG et al. Presence of biopsy-proven histologic damage (necroinflammation and fibrosis) is common even when ALT is less than 2x ULN in patients with chronic hepatitis B (CHB) (abstract). Gastroenterology 2007 132 : A729 A730.
48. McGill D, Rakela J, Zinsmeister A et al. A 21-year experience with major hemorrhage after percutaneous liver biopsy. Gastroenterology 1990 99 : 1396 1400.
49. Bravo AA, Sheth SG, Chopra S. Liver biopsy. N Engl J Med 2001 344 : 495 500.
50. Lok ASF, McMahon BJ. Chronic hepatitis B. Hepatology 2007 45 : 507 539.
51. Lin CL, Liao LY, Liu CJ et al. Hepatitis B viral factors in HbeAg negative carriers with persistently normal serum alanine aminotransferase levels. Hepatology 2007 45 : 1193 1198.
52. Lai M, Hyatt B, Afdhal N. Role of liver biopsy in patients with normal ALT and high HBV DNA (abstract). Hepatology 2005 42 : 720A.
53. Wang C, Deubner H, Shuhart M et al. High prevalence of significant fibrosis in patients with immunotolerance to chronic hepatitis B infection [Abstract]. Hepatology 2005 42 : 573A.
54. Brunetto MR, Oliveri F, Coco B et al. Outcome of anti-HBe positive chronic hepatitis B in alpha-interferon treated and untreated patients: a long term cohort study. J Hepatol 2002 36 : 263 270.
55. Chu CJ, Hussain M, Lok AS. Quantitative serum HBV DNA levels during different stages of chronic hepatitis B infection. Hepatology 2002 36 : 1408 1415.
56. Lebensztejn DM, Kaczmarski M, Sobaniec-Lotowska M et al. Serum laminin-2 and hyaluronan predict severe liver fibrosis in children with chronic hepatitis B. Hepatology 2004 39 : 868 869. (Pubitemid 38337673)
57. Hui AY, Chan HL, Wong VW et al. Identification of chronic hepatitis B patients without significant liver fibrosis by a simple noninvasive predictive model. Am J Gastroenterol 2005 100 : 616 623.
58. Myers RP, Tainturier MH, Ratziu V et al. Prediction of liver histologicalle-Prediction of liver histological lesions with biochemical markers in patients with chronic hepatitis B. J Hepatol 2003 39 : 222 230.
59. Poynard T, Zoulim F, Ratziu V et al. Longitudinal assessment of histology surrogate markers (FibroTest-ActiTest) during lamivudine therapy in patients with chronic hepatitis B infection. Am J Gastroenterol 2005 100 : 1970 1980.
60. Sebastiani G, Vario A, Guido M, Alberti A. Sequential algorithms combining non-invasive markers and biopsy for the assessment of liver fibrosis in chronic hepatitis B. World J Gastroenterol 2007 13 (4 525 531.
61. Chan HL-Y, Wong GL-H, Choi PC-L et al. 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.
62. Farrell CG, Larter CZ. Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology 2006 43 : S99 S112.
63. Neuschwander-Tetri BA, Caldwell SH. Nonalcoholic steatohepatitis: summary of an AASLD single topic conference. Hepatology 2003 37 : 1202 1219.
64. Farrell GC, George J, dela M, Hall P, McCullough AJ (eds). Fatty Liver Disease: NASH and Related Disorders. Malden, MA : Blackwell Publishing, 2005 : 1 319.
65. Bellentani S, Saccoccio G, Masatti F et al. Prevalence of and risk factors for hepatic steatosis in Northern Italy. Ann Intern Med 2000 132 : 112 117.
66. Chitturi S, Abeygunasekera S, Farrell GC et al. NASH and insulin resistance: insulin hypersecretion and specific association with the insulin resistance syndrome. Hepatology 2002 35 : 373 379.
67. Pagano G, Pacini G, Musso G et al. Nonalcoholic steatohepatitis, insulin resistance, and metabolic syndrome: further evidence for an etiologic association. Hepatology 2002 35 : 367 372.
68. Marchesini G, Bugianesi E, Forlani G et al. Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology 2003 37 : 917 923.
69. Sonsuz A, Basaranoglu M, Ozbay G. Relationship between aminotransferase levels and histopathological findings in patients with nonalcoholic steatohepatitis (letter). Am J Gastroenterol 2000 95 : 1370 1371.
70. Bacon BR, Farahvash MJ, Janney CG, Neuschwander Tetri BA. Nonalcoholic steatohepatitis: an expanded clinical entity. Gastroenterology 1994 107 : 1103 1109.
71. Powell EE, Cooksley WG, Hanson R et al. The natural history of nonalcoholic steatohepatitis: a follow-up study of forty-two patients for up to 21 years. Hepatology 1990 11 : 74 80.
72. Browning JD, Szczepaniak LS, Dobbins R et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 2004 40 : 1387 1395.
73. Mofrad P, Contos MJ, Haque M et al. Clinical and histologic spectrum of nonalcoholic fatty liver disease associated with normal ALT values. Hepatology 2003 37 : 1286 1292.
74. Matteoni CA, Younossi ZM, Gramlich T et al. Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity. Gastroenterology 1999 116 : 1413 1419.
75. Marcos A, Fisher RA, Ham JM et al. Selection and outcome of living donors for adult to adult right lobe transplantation. Transplantation 2000 69 : 2410 2415. (Pubitemid 30409013)
76. Minervini MI, Ruppert K, Fontes P et al. Liver biopsy findings from healthy potential living liver donors: Reasons for disqualification, silent diseases and correlation with liver injury tests. J Hepatol 2009 50 (3 501 510.
77. Fracanzani AL, Valenti L, Bugianesi E et al. Risk of severe liver disease in nonalcoholic fatty liver disease with normal aminotransferase levels: A role for insulin resistance and diabetes. Hepatology 2008 48 : 792 798.
78. Gaidos JKJ, Hillner BE, Sanyal AJ. A decision analysis study of the value of a liver biopsy in nonalcoholic steatohepatitis. Liver Int 2008 28 : 650 658.
79. Sakugawa H, Nakayoshi T, Kobashigawa K et al. Clinical usefulness of biochemical markers of liver fibrosis in patients with nonalcoholic fatty liver disease. World J Gastroenterol 2005 11 : 255 259.
80. Lindqvist U, Laurent TC. Serum hyaluronan and aminoterminal propeptide of type III procollagen: variation with age. Scand J Clin Lab Invest 1992 52 : 613 621.
81. Ueno T, Inuzuka S, Torimura T et al. Significance of serum type-IV collagen levels in various liver diseases. Measurement with a one-step sandwich enzyme immunoassay using monoclonal antibodies with specificity for pepsin-solubilized type-IV collagen. Scand J Gastroenterol 1992 27 : 513 520.
82. 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). Digest Liver Dis 2008 40 : 371 378.
83. Castera L, Forns X, Alberti A. Non-invasive evaluation of liver fibrosis using transient elastography. J Hepatol 2008 48 : 835 847.
84. Karmen A, Wroblewski F, LaDue JS. Transaminase activity in human blood. J Clin Invest 1955 34 : 126 133.
85. Kallei L, Hahn A, Roder VZ. Correlation between histological findings and serum transaminase values in chronic diseases of the liver. Acta Med Scand 1964 175 : 49 56.