Skip to main content
Log in

A Study of Carotid Atherosclerosis in Patients with Non-alcoholic Fatty Liver Disease

  • Original Article
  • Published:
Indian Journal of Clinical Biochemistry Aims and scope Submit manuscript

Abstract

Non-alcoholic fatty liver disease shares many features of metabolic syndrome and its presence could signify a substantial cardiovascular risk above and beyond that conferred by individual risk factors. This study is an attempt to investigate the association of non-alcoholic fatty liver disease with carotid intima-media thickness and plaque as surrogate measures of increased cardiovascular risk. The study was conducted on 645 non diabetic, non alcoholic subjects in the age range of 20–60 years. Metabolic syndrome was assessed by using ATP III and ADA (2005) criteria. Anthropometric factors—waist circumference and blood pressure were measured. Fasting serum samples were analyzed for glucose, triglyceride, cholesterol and its fractions, insulin, alanine and aspartate transaminases, gamma glutamyl transferase and free fatty acids. Insulin resistance and secretion were calculated by homeostasis model and insulin sensitivity by QUICKI index. Liver ultrasonographic scanning was used for assessing fatty liver. Carotid atherosclerosis was assessed by B-mode ultrasonography of common carotid artery and internal carotid artery. The prevalence of non-alcoholic fatty liver disease was 15.6 % in non alcoholic population and 68.5 % of non-alcoholic fatty liver disease had metabolic syndrome, which was associated with hyperinsulinemia, insulin resistance, insulin insensitivity along with elevated levels of waist circumference, blood pressure, triglyceride, FFA and decreased HDL cholesterol. NAFLD patients had markedly greater carotid intima media thickness than non NAFLD subjects with MCIMT of 591.6 ± 108 and 489.5 ± 132.4 μm (P < 0.001) and plaque prevalence of 19.2 and 2.2 %, respectively, thus the carotid intima media thickness is associated with NAFLD.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Angulo P. Nonalcoholic fatty liver disease. N Engl J Med. 2002;346:1221–31.

    Article  PubMed  CAS  Google Scholar 

  2. Neuschwander Tetri BA, Caldwell SH. Nonalcoholic steatohepatitis: summary of an AASLD single topic conference. Hepatology. 2003;37:1202–19.

    Article  PubMed  Google Scholar 

  3. Sharma P, Mishra S, Ajmera P, Mathur S. Oxidative stress in metabolic syndrome. Indian J Clin Biochem. 2005;20(1):145–9.

    Article  PubMed  CAS  Google Scholar 

  4. Mishra S, Yadav D, Gupta M, Mishra H, Sharma P. Hyperinsulinemia predisposes to NAFLD. Indian J Clin Biochem. 2008;23(2):130–5.

    Article  PubMed  Google Scholar 

  5. Targher G, Marra F, Marchesini G. Increased risk of cardiovascular disease in nonalcoholic fatty liver disease: causal effect or epiphenomenon? Diabetologia. 2008;51(11):1947–53.

    Article  PubMed  CAS  Google Scholar 

  6. Raitakari OT, Juonala M, Kahonen M, Taittonen L, Laitinen T, Maki-Torkko N, et al. Cardiovascular risk factors in childhood and carotid artery intima-media thickness in adulthood: the Cardiovascular Risk in Young Finns Study. JAMA. 2003;290(17):2277–83.

    Article  PubMed  CAS  Google Scholar 

  7. Expert Panel on Detection, Evaluation and Treatment of High Blood Cholesterol in Adults. Executive Summary of the Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). JAMA. 2001;285:2486–97.

    Google Scholar 

  8. Alberti KGMM, Zimmet P, Shaw J, IDF Epidemiology Task Force Consensus Group. The metabolic syndrome: a new worldwide definition. Lancet. 2005;366:1059–62.

    Article  PubMed  Google Scholar 

  9. Trinder P. Enzymatic method of glucose estimation. J Clin Pathol. 1969;22:246.

    Article  PubMed  CAS  Google Scholar 

  10. Trinder P. Enzymatic method of triglyceride estimation. Ann Clin Biochem. 1969;6:24–7.

    CAS  Google Scholar 

  11. The Expert Panel Report of the National Cholesterol Education Programme, Expert Panel on Detection, Evaluation and Treatment of high blood cholesterol in adults. Arch Intern Med. 1988;148:36–69.

    Google Scholar 

  12. Myers GL, Cooper GR, Henderson LO, Hassemer DJ, Kimberly MM. Standardization of lipid and lipoprotein measurement. In: Rifai N, Warnick GR, Dominiczak MH, editors. Handbook of lipoprotein testing. Washington, DC: AACC Press; 2000. p. 717–48.

    Google Scholar 

  13. Bergmeyer HU, Scheibe P, Wahlefeld AW. Optimization of methods for aspartate aminotransferase and alanine aminotransferase. Clin Chem. 1978;24:1.

    Google Scholar 

  14. Saris NE. Revised IFCC method for aspartate aminotransferase. Clin Chem. 1978;24:720–1.

    Google Scholar 

  15. Shaw LM, Stromme JH, London JL, Theodorsen L. IFCC methods for the determination of enzymes part 4. IFCC method for gamma-glutamyl transferase [(gamma-glutamyl)-peptide; amino acid gamma-glutamyl transferase, EC 2.3.2.2.]. Clin Chem Acta. 1983;135:315F–38F.

    CAS  Google Scholar 

  16. Shimizu S, Inoue K, Tani Y, Yamada H. Enzymatic determination of serum-free fatty acids: a colorimetric method. Anal Biochem. 1979;98:341–5.

    Article  PubMed  CAS  Google Scholar 

  17. Andersen L, Dinesen B, Jørgensen PN, Poulsen F, Røder ME. Enzyme immunoassay for intact human insulin in serum or plasma. Clin Chem. 1993;38:578–82.

    Google Scholar 

  18. Matthews DR, Hosker JP, Rudenski AS. Homeostasis model assessment: insulin resistance and b-cell function from fasting plasma glucose and insulin concentration. Diabetologia. 1985;28:412–9.

    Article  PubMed  CAS  Google Scholar 

  19. Levy JC, Matthews DR, Herman MP. Correct homeostasis model assessment (HOMA) evaluation uses the computer program. Diabetes Care. 1998;21:2191–2.

    Article  PubMed  CAS  Google Scholar 

  20. Katz A, Nambi SS, Mather K, Baron AD, Follmann DA, Sullivan G, Quon MJ. Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. J Clin Endocrinol Metab. 2000;85:2402–10.

    Article  PubMed  CAS  Google Scholar 

  21. Saverymuttu SH, Joseph AEA, Amxwell JD. Ultrasound scanning in the detection of hepatic fibrosis and steatosis. Br Med J. 1986;292:13–5.

    Article  CAS  Google Scholar 

  22. Lim TK, Lim E, Dwivedi G, Kooner J, Senior R. Normal value of carotid intima-media thickness—a surrogate marker of atherosclerosis: quantitative assessment by B-mode carotid ultrasound. J Am Soc Echocardiogr. 2008;21(2):112–6.

    Article  PubMed  Google Scholar 

  23. Brunt EM. Nonalcoholic steatohepatitis. Semin Liver Dis. 2004;24:3–20.

    PubMed  Google Scholar 

  24. Younossi Z, Diehl AM, Ong JP. Nonalcoholic fatty liver disease: an agenda for clinical research. Hepatology. 2002;35:746–52.

    Article  PubMed  Google Scholar 

  25. Bellentani S, Saccoccio G, Masutti F, Croce LS, Brandi G, Sasso F, et al. Prevalence of and risk factors for hepatic steatosis in Northern Italy. Ann Intern Med. 2000;132:112–7.

    PubMed  CAS  Google Scholar 

  26. Donati G, Stagni B, Piscaglia F, Venturoli N, Morselli-Labate AM, Rasciti L, et al. Increased prevalence of fatty liver in arterial hypertensive patients with normal liver enzymes: role of insulin resistance. Gut. 2004;53:1020–3.

    Article  PubMed  CAS  Google Scholar 

  27. Diehl AM. Fatty liver, hypertension and the metabolic syndrome. Gut. 2004;53:923–4.

    Article  PubMed  CAS  Google Scholar 

  28. Assy N, Kaita K, Mymin D, Levy C, Rosser B, Minuk G. Fatty infiltration of liver in hyperlipidemic patients. Dig Dis Sci. 2000;45:1929–34.

    Article  PubMed  CAS  Google Scholar 

  29. Gupte P, Amarapurkar D, Agal S, Baijal R, Kulshrestha P, Pramanik S, et al. Non-alcoholic steatohepatitis in type 2 diabetes mellitus. J Gastroenterol Hepatol. 2004;19:854–8.

    Article  PubMed  Google Scholar 

  30. Alexander CM, Landsman PB, Teutch SM, Haffner SM. NCEP-defined metabolic syndrome, diabetes and prevalence of coronary heart disease among NHANES III participants aged 50 years and older. Diabetes. 2003;52:1210–4.

    Article  PubMed  CAS  Google Scholar 

  31. Cortez Pinto H, Camilo ME, Baptista A, De Oliveira AG, De Moura MC. Non-alcoholic fatty liver: another feature of the metabolic syndrome? Clin Nutr. 1999;18:353–8.

    Article  PubMed  CAS  Google Scholar 

  32. Angelico F, Del Ben M, Conti R, Francioso S, Feole K, Maccioni D, Antonini TM, Alessandri C. Non-alcoholic fatty liver syndrome: a hepatic consequence of common metabolic diseases. J Gastroenterol Hepatol. 2003;18:588–94.

    Article  PubMed  Google Scholar 

  33. Marchesini G, Bugianesi E, Forlani G, Cerelli F, Lenzi M, Manini R, Rizzetto M, Melchionda N. Nonalcoholic fatty liver, steatohepatitis and the metabolic syndrome. Hepatology. 2003;37:917–23.

    Article  PubMed  Google Scholar 

  34. del Sol IA, Bots ML, Grobbee DE, Hofman A, Witteman JC. Carotid intima-media thickness at different sites: relation to incident myocardial infarction. The Rotterdam study. Eur Heart J. 2002;23(12):934–40.

    Article  Google Scholar 

  35. Kablak-Ziembicka A, Tracz W, Przewlocki T, Pieniazek P, Sokolowski A, Konieczynska M. Association of increased carotid intima-media thickness with the extent of coronary artery disease. Heart. 2004;90(11):1286–90.

    Article  PubMed  CAS  Google Scholar 

  36. Aygun C, Kocaman O, Sahin T, Uraz S, Hulagu S. Evaluation of METS frequency and carotid artery intima media thickness as risk factors for a atherosclerosis in patients with non-alcoholic fatty liver disease. Dig Dis Sci. 2008;53(5):1352–7.

    Article  PubMed  Google Scholar 

  37. Lewis GF, Carpentier A, Adeli K, Giacca A. Disordered fat storage and mobilization in the pathogenesis of insulin resistance and type 2 diabetes. Endocr Rev. 2002;23:201–29.

    Article  PubMed  CAS  Google Scholar 

  38. Unger RH. Minireview: weapons of lean body mass destruction: the role of ectopic lipids in the metabolic syndrome. Endocrinology. 2003;144:5159–65.

    Article  PubMed  CAS  Google Scholar 

  39. Volzke H, Robinson DM, Kleine V, Deutscher R, Hoffmann W, Ludemann J. Hepatic steatosis is associated with an increased risk of carotid atherosclerosis. World J Gastroenterol. 2005;11(12):1848–53.

    PubMed  Google Scholar 

  40. Caserta CA, Pendino GM, Alicante S, Amante A, Amato F, Fiorillo M, et al. Body mass index, cardiovascular risk factors, and carotid intima-media thickness in a pediatric population in southern Italy. J Pediatr Gastroenterol Nutr. 2010;51(2):216–20.

    Article  PubMed  Google Scholar 

  41. Cotichini R, Zuin M, Rosmini F, Mele A, Marcucci F. Cardiovascular risk factors, nonalcoholic fatty liver disease, and carotid artery intima-media thickness in an adolescent population in southern Italy. Am J Epidemiol. 2010;171(11):1195–202.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mishra, S., Yadav, D., Gupta, M. et al. A Study of Carotid Atherosclerosis in Patients with Non-alcoholic Fatty Liver Disease. Ind J Clin Biochem 28, 79–83 (2013). https://doi.org/10.1007/s12291-012-0286-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12291-012-0286-8

Keywords

Navigation