Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Article
  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

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

References

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Anonymous. KASL clinical practice guidelines: management of nonalcoholic fatty liver disease. Clin Mol Hepatol. 2013;19:325–48.

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  13. Kang W, Kim SU. Chasing after novel non-invasive markers to identify advanced fibrosis in NAFLD. Clin Mol Hepatol. 2013;19:255–257.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Anonymous. EASL-EASD-EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease. J Hepatol. 2016;64:1388–402.

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  25. Neuschwander-Tetri BA, Caldwell SH. Nonalcoholic steatohepatitis: summary of an AASLD Single Topic Conference. Hepatology. 2003;37:1202–1219.

    Article  PubMed  Google Scholar 

  26. Ong JP, Younossi ZM. Epidemiology and natural history of NAFLD and NASH. Clin Liver Dis. 2007;11:1–16, vii.

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Department of Internal Medicine, Yonsei University College of Medicine, Seoul, South Korea

    Hye Won Lee, Beom Kyung Kim, Seung Up Kim, Jun Yong Park, Do Young Kim, Sang Hoon Ahn, Kwang Joon Kim & Kwang-Hyub Han

  2. Institute of Gastroenterology, Yonsei University College of Medicine, Seoul, South Korea

    Hye Won Lee, Beom Kyung Kim, Seung Up Kim, Jun Yong Park, Do Young Kim, Sang Hoon Ahn & Kwang-Hyub Han

  3. Yonsei Liver Center, Seoul, South Korea

    Hye Won Lee, Beom Kyung Kim, Seung Up Kim, Jun Yong Park, Do Young Kim, Sang Hoon Ahn & Kwang-Hyub Han

  4. Brain Korea 21 Project for Medical Science, Seoul, South Korea

    Sang Hoon Ahn & Kwang-Hyub Han

  5. Division of Endocrinology, Yonsei University College of Medicine, Seoul, South Korea

    Kwang Joon Kim

  6. Severance Check-up Severance Hospital, Yonsei University Health System, Seoul, South Korea

    Kwang Joon Kim

Authors
  1. Hye Won Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Beom Kyung Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Seung Up Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jun Yong Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Do Young Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sang Hoon Ahn
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kwang Joon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kwang-Hyub Han
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kwang-Hyub Han.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 11 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, H.W., Kim, B.K., Kim, S.U. et al. Prevalence and Predictors of Significant Fibrosis Among Subjects with Transient Elastography-Defined Nonalcoholic Fatty Liver Disease. Dig Dis Sci 62, 2150–2158 (2017). https://doi.org/10.1007/s10620-017-4592-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10620-017-4592-0

Keywords

Search

Navigation