Advertisement

Digestive Diseases and Sciences

, Volume 62, Issue 8, pp 2150–2158 | Cite as

Prevalence and Predictors of Significant Fibrosis Among Subjects with Transient Elastography-Defined Nonalcoholic Fatty Liver Disease

  • Hye Won Lee
  • Beom Kyung Kim
  • Seung Up Kim
  • Jun Yong Park
  • Do Young Kim
  • Sang Hoon Ahn
  • Kwang Joon Kim
  • Kwang-Hyub HanEmail author
Original Article

Abstract

Background/Aims

Transient elastography (TE) can be used to assess the degree of liver fibrosis and steatosis. We investigated the prevalence and predictors of nonalcoholic fatty liver disease (NAFLD) with or without significant liver fibrosis in the general population.

Methods

A total of 3033 subjects without alcoholic or chronic viral liver diseases who underwent a medical health check-up including TE were recruited from April 2013 to August 2014. TE-defined NAFLD was defined as a controlled attenuation parameter of ≥250 dB/m, and significant liver fibrosis was defined as a liver stiffness (LS) value of ≥8 kPa.

Results

Overall, 1178 (42.9%) subjects had NAFLD. Subjects with NAFLD had significantly higher alanine aminotransferase (ALT) levels and a higher prevalence of parameters related to metabolic syndrome, such as high blood pressure, a high body mass index (BMI), glucose intolerance, and dyslipidemia than did subjects without NAFLD (all P < 0.05). Age, male gender, ALT level, serum albumin, BMI, diabetes, hypertriglyceridemia, and LS values independently showed positive associations with the presence of NAFLD (all P < 0.05). In addition, concomitant significant liver fibrosis was identified in 60 (5.1%) subjects with NAFLD, and its independent predictors were age [odds ratio (OR) 1.054], ALT level (OR 1.019), BMI (OR 1.217), and diabetes (OR 1.987) (all P < 0.05).

Conclusions

We found that the prevalence of subjects with NAFLD was high (42.9%), and 5.1% of them had concomitant significant liver fibrosis. The risk factors found in this study can help identify which subjects with NAFLD are vulnerable to fibrosis progression.

Keywords

Transient elastography Nonalcoholic fatty liver disease Controlled attenuation parameter Fibrosis Steatosis 

Abbreviations

NAFLD

Nonalcoholic fatty liver disease

NASH

Nonalcoholic steatohepatitis

DM

Diabetes mellitus

TE

Transient elastography

CAP

Controlled attenuation parameter

AUROC

Area under receiver operating curve

LS

Liver stiffness

ALT

Alanine aminotransferase

LDL

Lower-density lipoprotein

HDL

High-density lipoprotein

IQR

Interquartile range

BMI

Body mass index

APRI

Aspartate aminotransferase (AST) to platelet ratio index

LAP

Lipid accumulation product

Notes

Acknowledgments

The authors are grateful to Dong-Su Jang (Medical Illustrator, Medical Research Support Section, Yonsei University College of Medicine, Seoul, Korea) for the help with this journal.

Funding

This study was supported by the Liver Cirrhosis Clinical Research Center, in part by a Grant from the Korea Healthcare Technology R&D Project, Ministry of Health and Welfare, Republic of Korea (No. HI10C2020). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The funding does not alter our adherence to all the journal policies on sharing data and materials.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Supplementary material

10620_2017_4592_MOESM1_ESM.docx (12 kb)
Supplementary material 1 (DOCX 11 kb)

References

  1. 1.
    Chitturi S, Wong VW, Farrell G. Nonalcoholic fatty liver in Asia: firmly entrenched and rapidly gaining ground. J Gastroenterol Hepatol. 2011;26:163–172.CrossRefPubMedGoogle Scholar
  2. 2.
    Farrell GC, Wong VW, Chitturi S. NAFLD in Asia—as common and important as in the West. Nat Rev Gastroenterol Hepatol. 2013;10:307–318.CrossRefPubMedGoogle Scholar
  3. 3.
    Oh H, Jun DW, Saeed WK, et al. Non-alcoholic fatty liver diseases: update on the challenge of diagnosis and treatment. Clin Mol Hepatol. 2016;22:327–335.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Anonymous. KASL clinical practice guidelines: management of nonalcoholic fatty liver disease. Clin Mol Hepatol. 2013;19:325–48.Google Scholar
  5. 5.
    Sorrentino P, Tarantino G, Conca P, et al. Silent non-alcoholic fatty liver disease—a clinical-histological study. J Hepatol. 2004;41:751–757.CrossRefPubMedGoogle Scholar
  6. 6.
    Ascha MS, Hanouneh IA, Lopez R, et al. The incidence and risk factors of hepatocellular carcinoma in patients with nonalcoholic steatohepatitis. Hepatology. 2010;51:1972–1978.CrossRefPubMedGoogle Scholar
  7. 7.
    Adams LA, Lymp JF, St Sauver J, et al. The natural history of nonalcoholic fatty liver disease: a population-based cohort study. Gastroenterology. 2005;129:113–121.CrossRefPubMedGoogle Scholar
  8. 8.
    Ekstedt M, Franzen LE, Mathiesen UL, et al. Long-term follow-up of patients with NAFLD and elevated liver enzymes. Hepatology. 2006;44:865–873.CrossRefPubMedGoogle Scholar
  9. 9.
    Ong JP, Pitts A, Younossi ZM. Increased overall mortality and liver-related mortality in non-alcoholic fatty liver disease. J Hepatol. 2008;49:608–612.CrossRefPubMedGoogle Scholar
  10. 10.
    Kim NH, Park J, Kim SH, et al. Non-alcoholic fatty liver disease, metabolic syndrome and subclinical cardiovascular changes in the general population. Heart. 2014;100:938–943.CrossRefPubMedGoogle Scholar
  11. 11.
    Lee JY, Kim KM, Lee SG, et al. Prevalence and risk factors of non-alcoholic fatty liver disease in potential living liver donors in Korea: a review of 589 consecutive liver biopsies in a single center. J Hepatol. 2007;47:239–244.CrossRefPubMedGoogle Scholar
  12. 12.
    Wong GL, Wong VW, Choi PC, et al. Assessment of fibrosis by transient elastography compared with liver biopsy and morphometry in chronic liver diseases. Clin Gastroenterol Hepatol. 2008;6:1027–1035.CrossRefPubMedGoogle Scholar
  13. 13.
    Kang W, Kim SU. Chasing after novel non-invasive markers to identify advanced fibrosis in NAFLD. Clin Mol Hepatol. 2013;19:255–257.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Chon YE, Jung KS, Kim SU, et al. Controlled attenuation parameter (CAP) for detection of hepatic steatosis in patients with chronic liver diseases: a prospective study of a native Korean population. Liver Int. 2014;34:102–109.CrossRefPubMedGoogle Scholar
  15. 15.
    Sasso M, Beaugrand M, de Ledinghen V, et al. Controlled attenuation parameter (CAP): a novel VCTE guided ultrasonic attenuation measurement for the evaluation of hepatic steatosis: preliminary study and validation in a cohort of patients with chronic liver disease from various causes. Ultrasound Med Biol. 2010;36:1825–1835.CrossRefPubMedGoogle Scholar
  16. 16.
    de Ledinghen V, Vergniol J, Capdepont M, et al. Controlled attenuation parameter (CAP) for the diagnosis of steatosis: a prospective study of 5323 examinations. J Hepatol. 2014;60:1026–1031.CrossRefPubMedGoogle Scholar
  17. 17.
    Myers RP, Pollett A, Kirsch R, et al. Controlled attenuation parameter (CAP): a noninvasive method for the detection of hepatic steatosis based on transient elastography. Liver Int. 2012;32:902–910.CrossRefPubMedGoogle Scholar
  18. 18.
    Kwok R, Choi KC, Wong GL, et al. Screening diabetic patients for non-alcoholic fatty liver disease with controlled attenuation parameter and liver stiffness measurements: a prospective cohort study. Gut. 2016;65:1359–1368.CrossRefPubMedGoogle Scholar
  19. 19.
    Park CC, Nguyen P, Hernandez C, et al. Magnetic resonance elastography vs transient elastography in detection of fibrosis and noninvasive measurement of steatosis in patients with biopsy-proven nonalcoholic fatty liver disease. Gastroenterology. 2017;152:e592.Google Scholar
  20. 20.
    Lee HW, Park SY, Kim SU, et al. Discrimination of nonalcoholic steatohepatitis using transient elastography in patients with nonalcoholic fatty liver disease. PLoS ONE. 2016;11:e0157358.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Anonymous. EASL-EASD-EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease. J Hepatol. 2016;64:1388–402.Google Scholar
  22. 22.
    Alberti KG, Eckel RH, Grundy SM, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009;120:1640–1645.CrossRefPubMedGoogle Scholar
  23. 23.
    Sandrin L, Fourquet B, Hasquenoph JM, et al. Transient elastography: a new noninvasive method for assessment of hepatic fibrosis. Ultrasound Med Biol. 2003;29:1705–1713.CrossRefPubMedGoogle Scholar
  24. 24.
    Karlas T, Petroff D, Sasso M, et al. Individual patient data meta-analysis of controlled attenuation parameter (CAP) technology for assessing steatosis. J Hepatol. 2017;66:1022–1030.CrossRefPubMedGoogle Scholar
  25. 25.
    Neuschwander-Tetri BA, Caldwell SH. Nonalcoholic steatohepatitis: summary of an AASLD Single Topic Conference. Hepatology. 2003;37:1202–1219.CrossRefPubMedGoogle Scholar
  26. 26.
    Ong JP, Younossi ZM. Epidemiology and natural history of NAFLD and NASH. Clin Liver Dis. 2007;11:1–16, vii.Google Scholar
  27. 27.
    Vernon G, Baranova A, Younossi ZM. Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther. 2011;34:274–285.CrossRefPubMedGoogle Scholar
  28. 28.
    Foster KJ, Dewbury KC, Griffith AH, et al. The accuracy of ultrasound in the detection of fatty infiltration of the liver. Br J Radiol. 1980;53:440–442.CrossRefPubMedGoogle Scholar
  29. 29.
    de Ledinghen V, Vergniol J, Foucher J, et al. Non-invasive diagnosis of liver steatosis using controlled attenuation parameter (CAP) and transient elastography. Liver Int. 2012;32:911–918.CrossRefPubMedGoogle Scholar
  30. 30.
    Kwok R, Choi KC, Wong GL, et al. Screening diabetic patients for non-alcoholic fatty liver disease with controlled attenuation parameter and liver stiffness measurements: a prospective cohort study. Gut. 2016;65:1359–1368.CrossRefPubMedGoogle Scholar
  31. 31.
    Chang Y, Jung HS, Yun KE, et al. Cohort study of non-alcoholic fatty liver disease, NAFLD fibrosis score, and the risk of incident diabetes in a Korean population. Am J Gastroenterol. 2013;108:1861–1868.CrossRefPubMedGoogle Scholar
  32. 32.
    Roulot D, Costes JL, Buyck JF, et al. Transient elastography as a screening tool for liver fibrosis and cirrhosis in a community-based population aged over 45 years. Gut. 2011;60:977–984.CrossRefPubMedGoogle Scholar
  33. 33.
    Lee S, Jin Kim Y, Yong Jeon T, et al. Obesity is the only independent factor associated with ultrasound-diagnosed non-alcoholic fatty liver disease: a cross-sectional case-control study. Scand J Gastroenterol. 2006;41:566–572.CrossRefPubMedGoogle Scholar
  34. 34.
    Verma S, Jensen D, Hart J, et al. Predictive value of ALT levels for non-alcoholic steatohepatitis (NASH) and advanced fibrosis in non-alcoholic fatty liver disease (NAFLD). Liver Int. 2013;33:1398–1405.CrossRefPubMedGoogle Scholar
  35. 35.
    Shima T, Seki K, Umemura A, et al. Influence of lifestyle-related diseases and age on the development and progression of non-alcoholic fatty liver disease. Hepatol Res. 2015;45:548–559.CrossRefPubMedGoogle Scholar
  36. 36.
    Matteoni CA, Younossi ZM, Gramlich T, et al. Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity. Gastroenterology. 1999;116:1413–1419.CrossRefPubMedGoogle Scholar
  37. 37.
    Neuschwander-Tetri BA, Clark JM, Bass NM, et al. Clinical, laboratory and histological associations in adults with nonalcoholic fatty liver disease. Hepatology. 2010;52:913–924.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Roulot D, Czernichow S, Le Clesiau H, et al. Liver stiffness values in apparently healthy subjects: influence of gender and metabolic syndrome. J Hepatol. 2008;48:606–613.CrossRefPubMedGoogle Scholar
  39. 39.
    Loaeza-del-Castillo A, Paz-Pineda F, Oviedo-Cardenas E, et al. AST to platelet ratio index (APRI) for the noninvasive evaluation of liver fibrosis. Ann Hepatol. 2008;7:350–357.PubMedGoogle Scholar
  40. 40.
    Bedogni G, Kahn HS, Bellentani S, et al. A simple index of lipid overaccumulation is a good marker of liver steatosis. BMC Gastroenterol. 2010;10:98.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Petta S, Wai-Sun Wong V, Camma C, et al. Improved noninvasive prediction of liver fibrosis by liver stiffness measurement in patients with nonalcoholic fatty liver disease accounting for controlled attenuation parameter values. Hepatology. 2017;65:1145–1155.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Hye Won Lee
    • 1
    • 2
    • 3
  • Beom Kyung Kim
    • 1
    • 2
    • 3
  • Seung Up Kim
    • 1
    • 2
    • 3
  • Jun Yong Park
    • 1
    • 2
    • 3
  • Do Young Kim
    • 1
    • 2
    • 3
  • Sang Hoon Ahn
    • 1
    • 2
    • 3
    • 4
  • Kwang Joon Kim
    • 1
    • 5
    • 6
  • Kwang-Hyub Han
    • 1
    • 2
    • 3
    • 4
    Email author
  1. 1.Department of Internal MedicineYonsei University College of MedicineSeoulSouth Korea
  2. 2.Institute of GastroenterologyYonsei University College of MedicineSeoulSouth Korea
  3. 3.Yonsei Liver CenterSeoulSouth Korea
  4. 4.Brain Korea 21 Project for Medical ScienceSeoulSouth Korea
  5. 5.Division of Endocrinology, Yonsei University College of MedicineSeoulSouth Korea
  6. 6.Severance Check-up Severance HospitalYonsei University Health SystemSeoulSouth Korea

Personalised recommendations