Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

A population-based study investigating the association between metabolic syndrome and Hepatitis B/C infection (Keelung Community-based Integrated Screening Study No. 10)

Abstract

Objectives:

We aimed to assess the association between metabolic syndrome (MS) and hepatitis B/C virus infection using a large population-based study.

Design and methods:

A population-based cross-sectional study design was adopted with a total of 53 528 subjects being enrolled from the integrated multiple diseases screening program in Keelung, Taiwan. Evidence of past hepatitis B/C infection, acquired during childhood or as a young adult, was identified during the two-stage liver cancer screening part of the process. Information on biochemical markers and anthropometric measures related to MS, such as fasting blood sugar, triglyceride and high-density lipoprotein (HDL), abdominal circumference and blood pressure (BP), were collected routinely while screening for hypertension, type 2 diabetes, and hyperlipidemia. Logistic regression was used to estimate odds ratios and related 95% confidence intervals for the associations between MS and hepatitis B/C infection.

Results:

High blood pressure (SBP135 mmHg or DBP85 mmHg) (adjusted odd ratio: 0.89 (0.83–0.94)) and high triglyceride (150 mg/dl) (adjusted odds ratio: 0.65 (0.60–0.69)) were, after adjusting for gender and age, inversely associated with being HBsAg positive (P<0.05). The likelihood of developing MS was lower in the HBsAg positive than the HBsAg negative (adjusted odds ratio: 0.84 (0.76–0.93)). A positive association between being anti-HCV positive and having low serum HDL (male <40 mg/dl, female <50 mg/dl) was also noted (adjusted odds ratio: 1.61 (1.37–1.88) after controlling for gender and age). High triglyceride was inversely associated with being anti-HCV positive (adjusted odds ratio: 0.63 (0.55–0.71).

Conclusions:

There is an inverse association between MS and hepatitis B virus infection whereas the association was heterogeneous for HCV infection with a positive association with abnormal serum HDL but an inverse association with hypertriglyceridemia.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Eckel RH, Grundy SM, Zimmet PZ . The metabolic syndrome. Lancet 2005; 365: 1415–1428.

    Article  CAS  Google Scholar 

  2. Kanel GC, Radvan G, Peters RL . High-density lipoprotein cholesterol and liver disease. Hepatology 1983; 3: 343–348.

    Article  CAS  Google Scholar 

  3. Cicognani C, Malavolti M, Morselli-Labate AM et al. Serum lipid and lipoprotein patterns in patients with liver cirrhosis and chronic active hepatitis. Arch Intern Med 1997; 157: 792–796.

    Article  CAS  Google Scholar 

  4. Su TC, Lee YT, Cheng TJ, Chien HP, Wang JD . Chronic hepatitis B virus infection and dyslipidemia. J Formos Med Assoc 2004; 103: 286–291.

    PubMed  Google Scholar 

  5. Voisset C, Callens N, Blanchard E, Op De Beeck A, Dubuisson J, Vu-Dac N . High density lipoproteins facilitate hepatitis C virus entry through the Scavenger receptor class B type I. J Biol Chem 2005; 280: 7793–7799.

    Article  CAS  Google Scholar 

  6. Huo TI, Wu JC, Lee PC, Tsay SH, Chang FY, Lee SD . Diabetes mellitus as a risk factor of liver cirrhosis in patients with chronic hepatitis B virus infection. J Clin Gastroenterol 2000; 30: 250–254.

    Article  CAS  Google Scholar 

  7. Sangiorgio L, Attardo T, Gangemi R, Rubino C, Barone M, Lunetta M . Increased frequency of HCV and HBV infection in type 2 diabetic patients. Diabetes Res Clin Pract 2000; 48: 147–151.

    Article  CAS  Google Scholar 

  8. Lao TT, Tse KY, Chan LY, Tam KF, Ho LF . HBsAg carrier status and the association between gestational diabetes with increased serum ferritin concentration in Chinese women. Diabetes Care 2003; 26: 3011–3016.

    Article  Google Scholar 

  9. Fraser GM, Harman I, Meller N, Niv Y, Porath A . Diabetes mellitus is associated with chronic hepatitis C but not chronic hepatitis B infection. Isr J Med Sci 1996; 32: 526–530.

    CAS  PubMed  Google Scholar 

  10. Okan V, Araz M, Aktaran S, Karsligil T, Meram I, Bayraktaroglu Z et al. Increased frequency of HCV but not HBV infection in type 2 diabetic patients in Turkey. Int J Clin Pract 2002; 56: 175–177.

    CAS  PubMed  Google Scholar 

  11. Bedarida G, D'Agostino F, Bianchi M, Susani G, Sangalli F, Fattorini A et al. Unexpected lower prevalence of HBsAg in diabetics than in controls (A study on 2465 patients). Ric Clin Lab 1982; 12: 409–415.

    CAS  PubMed  Google Scholar 

  12. Ozyilkan E, Ozyilkan O, Firat D, Telatar H . Hepatitis C virus antibody in patients with primary liver cancer (hepatocellular carcinoma, cholangiocarcinoma, and combined hepatocellular-cholangiocarcinoma) in Japan. Cancer 1994; 73: 2002–2003.

    Article  CAS  Google Scholar 

  13. Grimbert S, Valensi P, Levy-Marchal C, Perret G, Richardet JP, Raffoux C et al. High prevalence of diabetes mellitus in patients with chronic hepatitis C. A case–control study. Gastroenterol Clin Biol 1996; 20: 544–548.

    CAS  PubMed  Google Scholar 

  14. Knobler H, Schihmanter R, Zifroni A, Fenakel G, Schattner A . Increased risk of type 2 diabetes in noncirrhotic patients with chronic hepatitis C virus infection. Mayo Clinic Proc 2000; 75: 355–359.

    Article  CAS  Google Scholar 

  15. Wang CS, Wang ST, Yao WJ, Chang TT, Chou P . Community-based study of hepatitis C virus infection and type 2 diabetes: an association affected by age and hepatitis severity status. Am J Epidemiol 2003; 158: 1154–1160.

    Article  Google Scholar 

  16. Arao M, Murase K, Kusakabe A, Yoshioka K, Fukuzawa Y, Ishikawa T et al. Prevalence of diabetes mellitus in Japanese patients infected chronically with hepatitis C virus. J Gastroenterol 2003; 38: 355–360.

    Article  Google Scholar 

  17. Mehta SH, Brancati FL, Sulkowski MS, Strathdee SA, Szklo M, Thomas DL . Prevalence of type 2 diabetes mellitus among persons with hepatitis C virus infection in the United States. Ann Intern Med 2000; 133: 592–599.

    Article  CAS  Google Scholar 

  18. Lecube A, Hernandez C, Genesca J, Esteban JI, Jardi R, Simo R . High prevalence of glucose abnormalities in patients with hepatitis C virus infection: a multivariate analysis considering the liver injury. Diabetes Care 2004; 27: 1171–1175.

    Article  CAS  Google Scholar 

  19. Mangia A, Schiavone G, Lezzi G, Marmo R, Bruno F, Villani MR et al. HCV and diabetes mellitus: evidence for a negative association. Am J Gastroenterol 1998; 93: 2363–2367.

    Article  CAS  Google Scholar 

  20. Sung JL, Chen DS, Lai MY, Yu JY, Wang TH, Wang CY et al. Epidemiological study on hepatitis B virus infection in Taiwan. Chinese J Gastroenterol 1984; 1: 1–9.

    Google Scholar 

  21. Chang MH, Lee CY, Chen DS . Minimal role of hepatitis C virus infection in childhood liver diseases in an area hyperendemic for hepatitis B infection. J Med Virol 1993; 40: 322–325.

    Article  CAS  Google Scholar 

  22. Chen THH, Chiu YH, Luh DL, Yen MF, Wu HM, Chen LS et al. Taiwan Community-Based Integrated Screening Group Community-based multiple screening model: design, implementation, and analysis of 42,387 participants. Cancer 2004; 100: 1734–1743.

    Article  Google Scholar 

  23. Beisel WR . Metabolic response to infection. Annu Rev Med 1975; 26: 9–20.

    Article  CAS  Google Scholar 

  24. Grunfeld C, Feingold KR . Tumor necrosis factor, interleukin, and interferon induced changes in lipid, metabolism as part of host defense. Proc Soc Exp Biol Med 1992; 200: 224–227.

    Article  CAS  Google Scholar 

  25. Fabris C, Federico E, Soardo G, Falleti E, Pirisi M . Blood lipids of patients with chronic hepatitis: differences related to viral etiology. Clin Chim Acta 1997; 261: 159–165.

    Article  CAS  Google Scholar 

  26. Iannello S, Cavaleri A, Milazzo P, Cantarella S, Belfiore F . Low fasting serum triglyceride level as a precocious marker of autoimmune disorders. Med Gen Med 2003; 5: 20.

    Google Scholar 

  27. Takemura Y, Kobayashi H, Kamachi M, Sekiguchi S, Shioikari M, Tamura M . Pathogenesis-screening tests for liver dysfunction in the asymptomatic patients with elevated ALT values and their diagnostic efficacies in primary care medcine. Rinsho Byori 1996; 44: 261–266.

    CAS  PubMed  Google Scholar 

  28. Wang CS, Chang TT, Chou P . Differing characteristics of hepatitis B and C risk factors among elders in a rural area in Taiwan. J Gerontol A Biol Sci Med Sci 1998; 53: M107–M111.

    Article  CAS  Google Scholar 

  29. Angelico F, Del Ben M, Conti R, Francioso S, Feole K, Maccioni D et al. Non-alcoholic fatty liver syndrome: a hepatic consequence of common metabolic diseases. J Gastroenterol Hepatol 2003; 18: 588–594.

    Article  Google Scholar 

  30. Kang SK, Chung TW, Lee JY, Lee YC, Morton RE, Kim CH . The hepatitis B virus X protein inhibits secretion of apolipoprotein B by enhancing the expression of N-acetylglucosaminyltransferase III. J Biol Chem 2004; 279: 28106–28112.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T H-H Chen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jan, CF., Chen, CJ., Chiu, YH. et al. A population-based study investigating the association between metabolic syndrome and Hepatitis B/C infection (Keelung Community-based Integrated Screening Study No. 10). Int J Obes 30, 794–799 (2006). https://doi.org/10.1038/sj.ijo.0803204

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.ijo.0803204

Keywords

This article is cited by

Search

Quick links