Age as a Confounding Factor for the Accurate Non-Invasive Diagnosis of Advanced NAFLD Fibrosis

American Journal of Gastroenterology

Volumn 112, Issue 5, 2017, Pages 740-751

  McPherson, Stuart ^a,b   Hardy, Tim ^a,b   Dufour, Jean Francois ^c   Petta, Salvatore ^d   Romero Gomez, Manuel ^e   Allison, Mike ^f   Oliveira, Claudia P ^g   Francque, Sven ^h   Van Gaal, Luc ^h   Schattenberg, Jörn M ⁱ   Tiniakos, Dina ^a,b   Burt, Alastair ^j   Bugianesi, Elisabetta ^k   Ratziu, Vlad ^l   Day, Christopher P ^a,b   Anstee, Quentin M ^a,b,m  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b FREEMAN HOSPITAL   (United Kingdom)

^c UNIVERSITY OF BERN   (Switzerland)

^d UNIVERSITY OF PALERMO   (Italy)

^e HOSPITAL UNIVERSITARIO VIRGEN MACARENA   (Spain)

^f ADDENBROOKE S HOSPITAL   (United Kingdom)

^g UNIVERSITY OF SÃO PAULO   (Brazil)

^h ANTWERP UNIVERSITY HOSPITAL   (Belgium)

ⁱ UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^j UNIVERSITY OF ADELAIDE   (Australia)

^k UNIVERSITY OF TURIN   (Italy)

^l PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^m NEWCASTLE UNIVERSITY   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ALBUMIN; ASPARTATE AMINOTRANSFERASE;

ADULT; AGE; AGED; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALBUMIN BLOOD LEVEL; AREA UNDER THE CURVE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CONFOUNDING VARIABLE; DIAGNOSTIC ACCURACY; DIGESTIVE SYSTEM DISEASE ASSESSMENT; FEMALE; FIBROSIS 4 SCORE; HUMAN; LIVER BIOPSY; LIVER EXAMINATION; LIVER FIBROSIS; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; NON INVASIVE MEASUREMENT; NONALCOHOLIC FATTY LIVER; NONALCOHOLIC FATTY LIVER FIBROSIS SCORE; PREDICTIVE VALUE; PRIORITY JOURNAL; RECEIVER OPERATING CHARACTERISTIC; REFERENCE VALUE; SCORING SYSTEM; SENSITIVITY AND SPECIFICITY; BIOPSY; BLOOD; COMPLICATION; FALSE POSITIVE RESULT; LIVER; LIVER CIRRHOSIS; PATHOLOGY; THROMBOCYTE COUNT;

ADULT; AGE FACTORS; AGED; ALANINE TRANSAMINASE; AREA UNDER CURVE; ASPARTATE AMINOTRANSFERASES; BIOPSY; FALSE POSITIVE REACTIONS; FEMALE; HUMANS; LIVER; LIVER CIRRHOSIS; MALE; MIDDLE AGED; NON-ALCOHOLIC FATTY LIVER DISEASE; PLATELET COUNT; PREDICTIVE VALUE OF TESTS; REFERENCE VALUES; ROC CURVE;

EID: 84990946236     PISSN: 00029270     EISSN: 15720241     Source Type: Journal    
DOI: 10.1038/ajg.2016.453     Document Type: Article

References (52)

1. Anstee QM, McPherson S, Day CP. How big a problem is non-alcoholic fatty liver disease? BMJ 2011; 343: d3897.
2. Chalasani N, Younossi Z, Lavine JE et al. The diagnosis and management of non-alcoholic fatty liver disease: practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology 2012; 55: 2005-23.
3. 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: 1387-95.
4. Bedogni G, Nobili V, Tiribelli C. Epidemiology of fatty liver: an update. World J Gastroenterol 2014; 20: 9050-4.
5. Anstee QM, Targher G, Day CP. Progression of NAFLD to diabetes mellitus, cardiovascular disease or cirrhosis. Nat Rev Gastroenterol Hepatol 2013; 10: 330-44.
6. Wong VW, Wong GL, Choi PC et al. Disease progression of non-alcoholic fatty liver disease: a prospective study with paired liver biopsies at 3 years. Gut 2010; 59: 969-74.
7. Pais R, Charlotte F, Fedchuk L et al. A systematic review of follow-up biopsies reveals disease progression in patients with non-alcoholic fatty liver. J Hepatol 2013; 59: 550-6.
8. McPherson S, Hardy T, Henderson E et al. Evidence of NAFLD progression from steatosis to fibrosing-steatohepatitis using paired biopsies: implications for prognosis and clinical management. J Hepatol 2015; 62: 1148-55.
9. Ekstedt M, Franzen LE, Mathiesen UL et al. Long-term follow-up of patients with NAFLD and elevated liver enzymes. Hepatology 2006; 44: 865-73.
10. Bhala N, Angulo P, van der Poorten D et al. The natural history of nonalcoholic fatty liver disease with advanced fibrosis or cirrhosis: an international collaborative study. Hepatology 2011; 54: 1208-16.
11. Ekstedt M, Hagstrom H, Nasr P et al. Fibrosis stage is the strongest predictor for disease-specific mortality in NAFLD aft er up to 33 years of follow-up. Hepatology 2015; 61: 1547-54.
12. Angulo P, Kleiner DE, Dam-Larsen S et al. Liver fibrosis, but no other histologic features, is associated with long-term outcomes of patients with nonalcoholic fatty liver disease. Gastroenterology 2015; 149: 389-97.e310.
13. Dyson JK, McPherson S, Anstee QM. Non-alcoholic fatty liver disease: non-invasive investigation and risk stratification. J Clin Pathol 2013; 66: 1033-45.
14. Machado MV, Cortez-Pinto H. Non-invasive diagnosis of non-alcoholic fatty liver disease. A critical appraisal. J Hepatol 2013; 58: 1007-19.
15. Williams AL, Hoofnagle JH. Ratio of serum aspartate to alanine aminotransferase in chronic hepatitis. Relationship to cirrhosis. Gastroenterology 1988; 95: 734-9.
16. 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: 846-54.
17. McPherson S, Henderson E, Burt AD et al. Serum immunoglobulin levels predict fibrosis in patients with non-alcoholic fatty liver disease. J Hepatol 2014; 60: 1055-62.
18. Shah AG, Lydecker A, Murray K et al. Comparison of noninvasive markers of fibrosis in patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 2009; 7: 1104-12.
19. McPherson S, Stewart SF, Henderson E et al. Simple non-invasive fibrosis scoring systems can reliably exclude advanced fibrosis in patients with non-alcoholic fatty liver disease. Gut 2010; 59: 1265-9.
20. McPherson S, Anstee QM, Henderson E et al. Are simple noninvasive scoring systems for fibrosis reliable in patients with NAFLD and normal ALT levels? Eur J Gastroenterol Hepatol 2013; 25: 652-8.
21. Dyson JK, Anstee QM, McPherson S. Non-alcoholic fatty liver disease: a practical approach to diagnosis and staging. Frontline Gastroenterol 2014; 5: 211-8.
22. Williams R, Aspinall R, Bellis M et al. Addressing liver disease in the UK: a blueprint for attaining excellence in health care and reducing premature mortality from lifestyle issues of excess consumption of alcohol, obesity, and viral hepatitis. Lancet 2014; 384: 1953-97.
23. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2004; 27 Suppl 1: S5-10.
24. 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: 1313-21.
25. Yeh MM, Brunt EM. Pathological features of fatty liver disease. Gastroenterology 2014; 147: 754-64.
26. 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: 1317-25.
27. Vallet-Pichard A, Mallet V, Nalpas B et al. FIB-4: an inexpensive and accurate marker of fibrosis in HCV infection. comparison with liver biopsy and fibrotest. Hepatology 2007; 46: 32-6.
28. Ratziu V, Bellentani S, Cortez-Pinto H et al. A position statement on NAFLD/NASH based on the EASL 2009 special conference. J Hepatol 2010; 53: 372-84.
29. Francque SM, Verrijken A, Mertens I et al. Noninvasive assessment of nonalcoholic fatty liver disease in obese or overweight patients. Clin Gastroenterol Hepatol 2012; 10: 1162-8; quiz e1187.
30. Petta S, Vanni E, Bugianesi E et al. The combination of liver stiffness measurement and NAFLD fibrosis score improves the noninvasive diagnostic accuracy for severe liver fibrosis in patients with nonalcoholic fatty liver disease. Liver Int 2015; 35: 1566-73.
31. Adams LA, George J, Bugianesi E et al. Complex non-invasive fibrosis models are more accurate than simple models in non-alcoholic fatty liver disease. J Gastroenterol Hepatol 2011; 26: 1536-43.
32. Demir M, Lang S, Nierhoff D et al. Stepwise combination of simple noninvasive fibrosis scoring systems increases diagnostic accuracy in nonalcoholic fatty liver disease. J Clin Gastroenterol 2013; 47: 719-26.
33. Dong MH, Bettencourt R, Brenner DA et al. Serum levels of alanine aminotransferase decrease with age in longitudinal analysis. Clin Gastroenterol Hepatol 2012; 10: 285-290.e281.
34. Dong MH, Bettencourt R, Barrett-Connor E et al. Alanine aminotransferase decreases with age: the Rancho Bernardo Study. PLoS One 2010; 5: e14254.
35. Goh GB, Pagadala MR, Dasarathy J et al. Age impacts ability of aspartatealanine aminotransferase ratio to predict advanced fibrosis in nonalcoholic fatty liver disease. Dig Dis Sci 2015; 60: 1825-31.
36. Balduini CL, Noris P. Platelet count and aging. Haematologica 2014; 99: 953-5.
37. Perez-Gutierrez OZ, Hernandez-Rocha C, Candia-Balboa RA et al. Validation study of systems for noninvasive diagnosis of fibrosis in nonalcoholic fatty liver disease in Latin population. Ann Hepatol 2013; 12: 416-24.
38. Xun YH, Fan JG, Zang GQ et al. Suboptimal performance of simple noninvasive tests for advanced fibrosis in Chinese patients with nonalcoholic fatty liver disease. J Dig Dis 2012; 13: 588-95.
39. Noureddin M, Yates KP, Vaughn IA et al. Clinical and histological determinants of nonalcoholic steatohepatitis and advanced fibrosis in elderly patients. Hepatology 2013; 58: 1644-54.
40. Ratziu V, Massard J, Tahiri M et al. Diagnostic value of biochemical markers (FibroTest-FibroSURE) for the prediction of liver fibrosis in patients with non-alcoholic fatty liver disease. BMC Gastroenterol 2006; 6: 6.
41. Guha IN, Parkes J, Roderick P et al. Noninvasive markers of fibrosis in nonalcoholic fatty liver disease: validating the European Liver Fibrosis Panel and exploring simple markers. Hepatology 2008; 47: 455-60.
42. Fagan KJ, Pretorius CJ, Horsfall LU et al. ELF score >/=9.8 indicates advanced hepatic fibrosis and is influenced by age, steatosis and histological activity. Liver Int 2015; 35: 1673-81.
43. 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: 454-62.
44. Myers RP, Pomier-Layrargues G, Kirsch R et al. Discordance in fibrosis staging between liver biopsy and transient elastography using the fibroscan xl probe. J Hepatol 2011; 56: 564-70.
45. Castera L, Foucher J, Bernard PH et al. Pitfalls of liver stiffness measurement: a 5-year prospective study of 13,369 examinations. Hepatology 2010; 51: 828-35.
46. Koehler EM, Plompen EP, Schouten JN et al. Presence of diabetes mellitus and steatosis is associated with liver stiffness in a general population: the Rotterdam study. Hepatology 2015; 63: 138-47.
47. Jansen PL. Liver disease in the elderly. Best Pract Res Clin Gastroenterol 2002; 16: 149-58.
48. McLean AJ, Cogger VC, Chong GC et al. Age-related pseudocapillarization of the human liver. J Pathol 2003; 200: 112-7.
49. Fiel MI, Deniz K, Elmali F et al. Increasing hepatic arteriole wall thickness and decreased luminal diameter occur with increasing age in normal livers. J Hepatol 2011; 55: 582-6.
50. Ratziu V, Bruckert E, Grimaldi A et al. Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology 2005; 128: 1898-906.
51. Levene AP, Kudo H, Armstrong MJ et al. Quantifying hepatic steatosis-more than meets the eye. Histopathology 2012; 60: 971-81.
52. Burt AD, Lackner C, Tiniakos DG. Diagnosis and assessment of NAFLD: definitions and histopathological classification. Semin Liver Dis 2015; 35: 207-20.