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Metabolic profiles in patients with chronic hepatitis C: a case–control study

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Abstract

Background

The clinical implications of metabolic profiles in patients with chronic hepatitis C remain controversial. To study the association of metabolic abnormalities with chronic hepatitis C, we conducted a case–control study with special emphasis on serum lipid pattern, fasting blood glucose, and adiponectin.

Methods

We enrolled 500 patients with chronic hepatitis C and 536 sex and age-matched controls. Unadjusted and adjusted associations of demographic and metabolic variables were estimated.

Results

Chronic hepatitis C patients had higher alanine aminotransferase (ALT) and high-density lipoprotein-cholesterol levels, but lower total cholesterol (TC), triglyceride (TG), and low-density lipoprotein-cholesterol levels than controls. Stratifying ALT level according to its upper limit of normal, HCV infection was associated with younger age, female gender, and higher TC levels in chronic hepatitis C patients with normal ALT levels, but with lower TC and lower TG levels in those with abnormal ALT levels. By using multiple linear regression analyses for subjects with available adiponectin data, presence of HCV infection was independently associated with higher serum adiponectin levels.

Conclusions

Metabolic profiles of chronic hepatitis C patients are affected by age, gender, serum adiponectin, and ALT levels. Further longitudinal studies are needed to clarify the complex interplay between HCV infection and metabolic profiles.

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Abbreviations

HCV:

Hepatitis C virus

ALT:

Alanine aminotransferase

TG:

Triglyceride

TC:

Total cholesterol

HDL:

High-density lipoprotein-cholesterol

LDL:

Low-density lipoprotein-cholesterol

ULN:

Upper limit of normal

ADN:

Adiponectin

References

  1. Chen DS, Wang JT, Chen PJ, Wang TH, Sung JL. Hepatitis C virus infection in Taiwan. Gastroenterol Jpn. 1991;26 Suppl 3:164–6.

    PubMed  CAS  Google Scholar 

  2. Allison ME, Wreghitt T, Palmer CR, Alexander GJ. Evidence for a link between hepatitis C virus infection and diabetes mellitus in a cirrhotic population. J Hepatol. 1994;21:1135–9.

    Article  PubMed  CAS  Google Scholar 

  3. Mangia A, Schiavone G, Lezzi G, et al. HCV and diabetes mellitus: evidence for a negative association. Am J Gastroenterol. 1998;93:2363–7.

    Article  PubMed  CAS  Google Scholar 

  4. Mason AL, Lau JY, Hoang N, et al. Association of diabetes mellitus and chronic hepatitis C virus infection. Hepatology. 1999;29:328–33.

    Article  PubMed  CAS  Google Scholar 

  5. Caronia S, Taylor K, Pagliaro L, et al. Further evidence for an association between non-insulin-dependent diabetes mellitus and chronic hepatitis C virus infection. Hepatology. 1999;30:1059–63.

    Article  PubMed  CAS  Google Scholar 

  6. 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 Clin Proc. 2000;75:355–9.

    Article  PubMed  CAS  Google Scholar 

  7. Thuluvath PJ, John PR. Association between hepatitis C, diabetes mellitus, and race: a case–control study. Am J Gastroenterol. 2003;98:438–41.

    PubMed  Google Scholar 

  8. Zein CO, Levy C, Basu A, Zein NN. Chronic hepatitis C and type II diabetes mellitus: a prospective cross-sectional study. Am J Gastroenterol. 2005;100:48–55.

    Article  PubMed  Google Scholar 

  9. Antonelli A, Ferri C, Fallahi P, Pampana A, Ferrari SM, Goglia F, et al. Hepatitis C virus infection: evidence for an association with type 2 diabetes. Diabetes Care. 2005;28:2548–50.

    Article  PubMed  Google Scholar 

  10. Jarmay K, Karacsony G, Nagy A, Schaff Z. Changes in lipid metabolism in chronic hepatitis C. World J Gastroenterol. 2005;11:6422–8.

    PubMed  CAS  Google Scholar 

  11. Siagris D, Kouraklis-Symeonidis A, Christofidou M, et al. Serum lipid profile and hepatic steatosis of adult beta-thalassaemia patients with chronic HCV infection. Eur J Gastroenterol Hepatol. 2005;17:345–50.

    Article  PubMed  CAS  Google Scholar 

  12. Siagris D, Christofidou M, Theocharis GJ, et al. Serum lipid pattern in chronic hepatitis C: histological and virological correlations. J Viral Hepat. 2006;13:56–61.

    Article  PubMed  CAS  Google Scholar 

  13. Behrendt CE, Ruiz RB. Hyperglycemia among persons with hepatitis C: not the classical diabetic phenotype. Diabetes Res Clin Pract. 2006;71:68–74.

    Article  PubMed  CAS  Google Scholar 

  14. Petit JM, Benichou M, Duvillard L, et al. Hepatitis C virus-associated hypobetalipoproteinemia is correlated with plasma viral load, steatosis, and liver fibrosis. Am J Gastroenterol. 2003;98:1150–4.

    PubMed  CAS  Google Scholar 

  15. Serfaty L, Andreani T, Giral P, Carbonell N, Chazouilleres O, Poupon R. Hepatitis C virus induced hypobetalipoproteinemia: a possible mechanism for steatosis in chronic hepatitis C. J Hepatol. 2001;34:428–34.

    Article  PubMed  CAS  Google Scholar 

  16. 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;261:159–65.

    Article  PubMed  CAS  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;133:592–9.

    PubMed  CAS  Google Scholar 

  18. 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 (Lond). 2006;30:794–9.

    Article  Google Scholar 

  19. Shaheen M, Echeverry D, Oblad MG, Montoya MI, Teklehaimanot S, Akhtar AJ. Hepatitis C, metabolic syndrome, and inflammatory markers: results from the Third National Health and Nutrition Examination Survey [NHANES III]. Diabetes Res Clin Pract. 2007;75:320–6.

    Article  PubMed  Google Scholar 

  20. Hui JM, Hodge A, Farrell GC, Kench JG, Kriketos A, George J. Beyond insulin resistance in NASH: TNF-alpha or adiponectin? Hepatology. 2004;40:46–54.

    Article  PubMed  CAS  Google Scholar 

  21. Fumeron F, Aubert R, Siddiq A, et al. Adiponectin gene polymorphisms and adiponectin levels are independently associated with the development of hyperglycemia during a 3-year period: the epidemiologic data on the insulin resistance syndrome prospective study. Diabetes. 2004;53:1150–7.

    Article  PubMed  CAS  Google Scholar 

  22. Berg AH, Combs TP, Scherer PE. ACRP30/adiponectin: an adipokine regulating glucose and lipid metabolism. Trends Endocrinol Metab. 2002;13:84–9.

    Article  PubMed  CAS  Google Scholar 

  23. Masaki T, Chiba S, Tatsukawa H, Yasuda T, Noguchi H, Seike M, et al. Adiponectin protects LPS-induced liver injury through modulation of TNF-alpha in KK-Ay obese mice. Hepatology. 2004;40:177–84.

    Article  PubMed  CAS  Google Scholar 

  24. Liu CJ, Chen PJ, Jeng YM, et al. Serum adiponectin correlates with viral characteristics but not histologic features in patients with chronic hepatitis C. J Hepatol. 2005;43:235–42.

    Article  PubMed  CAS  Google Scholar 

  25. Liu CJ, Jeng YM, Chen PJ, et al. Influence of metabolic syndrome, viral genotype and antiviral therapy on superimposed fatty liver disease in chronic hepatitis C. Antivir Ther. 2005;10:405–15.

    PubMed  CAS  Google Scholar 

  26. Yeh SH, Tsai CY, Kao JH, et al. Quantification and genotyping of hepatitis B virus in a single reaction by real-time PCR and melting curve analysis. J Hepatol. 2004;41:659–66.

    Article  PubMed  CAS  Google Scholar 

  27. Strader DB, Wright T, Thomas DL, Seeff LB. Diagnosis, management, and treatment of hepatitis C. Hepatology. 2004;39:1147–71.

    Article  PubMed  Google Scholar 

  28. Kao JH, Lin HH, Chen PJ, Lai MY, Wang TH, Mizokami M, et al. Serotyping of hepatitis C virus in chronic type C hepatitis in Taiwan: correlation with genotypes. J Gastroenterol. 1996;31:224–7.

    Article  PubMed  CAS  Google Scholar 

  29. Ohno O, Mizokami M, Wu RR, et al. New hepatitis C virus (HCV) genotyping system that allows for identification of HCV genotypes 1a, 1b, 2a, 2b, 3a, 3b, 4, 5a, and 6a. J Clin Microbiol. 1997;35:201–7.

    PubMed  CAS  Google Scholar 

  30. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2006;29 Suppl 1:S43–8.

  31. Kim HC, Nam CM, Jee SH, Han KH, Oh DK, Suh I. Normal serum aminotransferase concentration and risk of mortality from liver diseases: prospective cohort study. BMJ. 2004;328:983.

    Article  PubMed  CAS  Google Scholar 

  32. Prati D, Shiffman ML, Diago M, et al. Viral and metabolic factors influencing alanine aminotransferase activity in patients with chronic hepatitis C. J Hepatol. 2006;44:679–85.

    Article  PubMed  CAS  Google Scholar 

  33. Kaser S, Moschen A, Cayon A, et al. Adiponectin and its receptors in non-alcoholic steatohepatitis. Gut. 2005;54:117–21.

    Article  PubMed  CAS  Google Scholar 

  34. Yamaguchi A, Tazuma S, Nishioka T, Ohishi W, Hyogo H, Nomura S, et al. Hepatitis C virus core protein modulates fatty acid metabolism and thereby causes lipid accumulation in the liver. Dig Dis Sci. 2005;50:1361–71.

    Article  PubMed  CAS  Google Scholar 

  35. Tsutsumi T, Suzuki T, Shimoike T, et al. Interaction of hepatitis C virus core protein with retinoid X receptor alpha modulates its transcriptional activity. Hepatology. 2002;35:937–46.

    Article  PubMed  CAS  Google Scholar 

  36. Larter CZ, Farrell GC. Insulin resistance, adiponectin, cytokines in NASH: which is the best target to treat? J Hepatol. 2006;44:253–61.

    Article  PubMed  Google Scholar 

  37. Favre D, Muellhaupt B. Potential cellular receptors involved in hepatitis C virus entry into cells. Lipids Health Dis. 2005;4:9.

    Article  PubMed  CAS  Google Scholar 

  38. 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;280:7793–9.

    Article  PubMed  CAS  Google Scholar 

  39. von Hahn T, Lindenbach BD, Boullier A, Quehenberger O, Paulson M, Rice CM, et al. Oxidized low-density lipoprotein inhibits hepatitis C virus cell entry in human hepatoma cells. Hepatology. 2006;43:932–42.

    Article  CAS  Google Scholar 

  40. Gopal K, Johnson TC, Gopal S, et al. Correlation between beta-lipoprotein levels and outcome of hepatitis C treatment. Hepatology. 2006;44:335–40.

    Article  PubMed  CAS  Google Scholar 

  41. Barba G, Harper F, Harada T, et al. Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. Proc Natl Acad Sci USA. 1997;94:1200–5.

    Article  PubMed  CAS  Google Scholar 

  42. Marchesini G, Bugianesi E, Forlani G, et al. Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology. 2003;37:917–23.

    Article  PubMed  Google Scholar 

  43. Jonsson JR, Moschen AR, Hickman IJ, et al. Adiponectin and its receptors in patients with chronic hepatitis C. J Hepatol. 2005;43:929–36.

    Article  PubMed  CAS  Google Scholar 

  44. Hsu C-S, Liu C-J, Liu C-H, et al. High hepatitis C viral load is associated with insulin resistance in patients with chronic hepatitis C. Liver Int. 2008;28:271–277.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by grants from the National Taiwan University Hospital, the Department of Heath, and the National Science Council, Executive Yuan, Taiwan. We thank Dr. Huang SP at the Health Management Center of National Taiwan University Hospital for providing data of non-HCV controls.

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Authors and Affiliations

  1. Division of Gastroenterology, Buddhist Tzu Chi General Hospital, Taipei Branch, Taipei, Taiwan, ROC

    Ching-Sheng Hsu

  2. Department of Internal Medicine, Buddhist Tzu Chi General Hospital, Taipei Branch, Taipei, Taiwan, ROC

    Ching-Sheng Hsu

  3. Department of Internal Medicine, National Taiwan University College of Medicine and National Taiwan University Hospital, Taipei, Taiwan, ROC

    Chun-Jen Liu, Chen-Hua Liu, Ming-Yang Lai, Pei-Jer Chen, Ding-Shinn Chen & Jia-Horng Kao

  4. Graduate Institute of Clinical Medicine, National Taiwan University College of Medicine and National Taiwan University Hospital, Taipei, Taiwan, ROC

    Chi-Ling Chen, Pei-Jer Chen, Ding-Shinn Chen & Jia-Horng Kao

  5. Department of Medical Research, National Taiwan University College of Medicine and National Taiwan University Hospital, Taipei, Taiwan, ROC

    Ming-Yang Lai, Pei-Jer Chen & Jia-Horng Kao

  6. Hepatitis Research Center, National Taiwan University Hospital, 1 Chang-Te St., Taipei, 100, Taiwan, ROC

    Jia-Horng Kao

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  1. Ching-Sheng Hsu
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Correspondence to Jia-Horng Kao.

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Hsu, CS., Liu, CJ., Liu, CH. et al. Metabolic profiles in patients with chronic hepatitis C: a case–control study. Hepatol Int 2, 250–257 (2008). https://doi.org/10.1007/s12072-008-9064-3

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  • DOI: https://doi.org/10.1007/s12072-008-9064-3

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