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Clinical, anthropometric, biochemical, and histological characteristics of nonobese nonalcoholic fatty liver disease patients of Bangladesh

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Abstract

Background

Nonalcoholic fatty liver disease (NAFLD) is considered to be a disease of obese individuals, yet lean patients are increasingly susceptible to have NAFLD. The aim of this study was to evaluate the profile of nonobese patients by comparing with obese NAFLD patients.

Methods

We have included 465 patients of NAFLD after exclusion of other diseases, and 220 with elevated alanine aminotransferase (ALT) were biopsied. Patients were biochemically and clinically evaluated: blood pressure, body mass index (BMI), and waist circumference (WC) were recorded for every patient. A BMI  ≥ 25 kg/m2 was defined as obese, and those with a BMI of <25 kg/m2 were labeled as nonobese. Histological activity was expressed with NAFLD activity score (NAS).

Results

Of 465 cases, 119 (25.6 %) were nonobese. Diabetes was noted in 122 (26.2 %) and hypertension in 122 (26.2 %). Metabolic syndrome was present in 253 (59.7 %), low HDL cholesterol in 228 (64.8 %), hypertriglyceridemia in 297 (73.2 %), and WC above normal in 308 (70.2 %). Males were predominating in the nonobese compared to females in the obese (p = 0.001). Hypertriglyceridemia and low high-density lipoprotein was similar in the obese and nonobese (76.2 % vs. 72.3 %, p = 0.5 and 65.2 % vs. 64.6 %, p = 1.0, respectively). The grades of steatosis, lobular inflammation, ballooning, NAS, and the stage of fibrosis did not also significantly differ between obese and nonobese patients. Nonalcoholic steatohepatitis (NASH) was 53.1 % in nonobese.

Conclusion

Nonobese was 25.6 % among NAFLD patients of Bangladesh, and 53.1 % of nonobese NAFLD cases were NASH. Though they were nonobese by BMI grade, they were metabolically similar to obese. Males were predominant in the nonobese, whereas females in the obese. NASH and fibrosis were similar in the obese and nonobese.

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References

  1. Adams LA, Lindor KD. Nonalcoholic fatty liver disease. Ann Epidemiol. 2007;17:863–5.

    Article  PubMed  Google Scholar 

  2. Angulo P. Nonalcoholic fatty liver disease. N Engl J Med. 2002;346:1226–31.

    Article  Google Scholar 

  3. Clark JM, Brancati FL, Dieh AM. Nonalcoholic fatty liver disease. Gastroenterology. 2002;122:1649–57.

    Article  PubMed  Google Scholar 

  4. Amarpurkar DN, Hashimoto E, Lesman LA, Sollano JD, Chan PJ, Goh KL. Asia-pacific working party on nonalcoholic fatty liver disease. How common is NAFLD in the Asia-pacific region and are there local differences? J Gastroenterol Hepatol. 2007;22:788–93.

    Article  Google Scholar 

  5. Younossi ZM, Stepanovo M, Fang Y, Younossi Y, Mir H, Shrishard M. Changes in prevalence of the most common causes of chronic liver disease in United States from 1988 to 2008. Clin Gastroenterol Hepatol. 2011;9:524–30.

    Article  PubMed  Google Scholar 

  6. Amarpurkar D, Kumani P, Patel N, et al. Prevalence of nonalcoholic fatty liver disease, population based study. Ann Hepatol. 2007;61:161–3.

    Google Scholar 

  7. Fabbini E, Sullivan S, Klein S. Obesity and nonalcoholic fatty liver disease biochemical, metabolic and clinical implications. Hepatology. 2010;51:679–89.

    Article  Google Scholar 

  8. 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;34:274–85.

    Article  PubMed  CAS  Google Scholar 

  9. Bonora E, Targher G, Alberiche M, et al. Homeostasis model assessment closely mirrors the glucose clamp technique in the assessment of insulin sensitivity: studies in subject with various degrees of glucose tolerance and insulin sensitivity. Diabetes Care. 2000;23:57–63.

    Article  PubMed  CAS  Google Scholar 

  10. Das K, Das K, Mukherjee PS, et al. Nonobese population in a developing country has a high prevalence of nonalcoholic fatty liver disease and significant liver disease. Hepatology. 2010;51:1593–602.

    Article  PubMed  CAS  Google Scholar 

  11. Merra F, Bertolani C. Adipokines in liver diseases. Hepatology. 2009;50:957–69.

    Article  Google Scholar 

  12. Choudhary NS, Duseja A, Kalra N, Das A, Dhiman RK, Chawla YK. Correlation of adipose tissue with liver histology in Asian Indian patients with nonalcoholic fatty liver disease (NAFLD). Ann Hepatol. 2012;11:478–86.

    PubMed  Google Scholar 

  13. Francazani AL, Valenti L, Buigianesi E, et al. Risk of NASH and fibrosis in patients with nonalcoholic fatty liver disease and low visceral adiposity. J Hepatol. 2011;54:1244–49.

    Article  Google Scholar 

  14. Gholam PM, Flancbaum L, Machan JT, Charney DA, Kotler DP. Nonalcoholic fatty liver disease in severely obese subjects. Am J Gastroenterol. 2007;102:399–408.

    Article  PubMed  CAS  Google Scholar 

  15. Madan K, Batra Y, Gupta SD, et al. Nonalcoholic fatty liver disease may not be a severe disease at apresentation among Asian Indians. World J Gastroenterol. 2006;12:3400–5.

    PubMed  PubMed Central  Google Scholar 

  16. Belleantini S, Marino M. Epidemiology and natural history of nonalcoholic fatty liver disease. Ann Hepatol. 2009;8 Suppl 1:S4–8.

    Google Scholar 

  17. Sing DK, Sakhuja P, Malhotra V, Gondal R, Sarin SK. Independent predictors of steatohepatitis and fibrosis in Asian Indian patients with NASH. Dig Dis Sci. 2007;52:2368–74.

    Article  Google Scholar 

  18. Succuro E, Marini MA, Frontini S, et al. Insulin secretion in metabolically healthy but obese individuals. Obesity (Silver Spring). 2008;16:1881–6.

    Article  Google Scholar 

  19. Heng D, Ma S, Lee JJ, et al. Modification of the NCEP ATP III definitions of the metabolic syndrome for use in Asians identifies individuals at risk of ischemic heart disease. Atherosclerosis. 2006;186:367–73.

    Article  PubMed  CAS  Google Scholar 

  20. Expert WHO. Consultation. appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet. 2004;363:157–63.

    Article  Google Scholar 

  21. Brunt EM, Janney CG, Di Bisceglie AM, et al. Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions. Am J Gastroenterol. 1999;94:2467–74.

    Article  PubMed  CAS  Google Scholar 

  22. Kleiner DE, Brunt EM, Van Natta M, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005;41:1313–21.

    Article  PubMed  Google Scholar 

  23. Szczepaniak LS, Nurenberg P, Leonard D, et al. Magnetic resonance spectroscopy to measure hepatic triglyceride content: prevalence of hepatic steatosis in the general population. Am J Physiol Endocrinol Metab. 2005;288:E462–8.

    Article  PubMed  CAS  Google Scholar 

  24. Fracanzani AL, Valenti L, Bugianesi E, et al. Risk of severe liver disease in nonalcoholic fatty liver disease with normal aminotransferase levels: a role for insulin resistance and diabetes. Hepatology. 2008;48:792–8.

    Article  PubMed  CAS  Google Scholar 

  25. Duseja A, Das A, Das R, et al. The clinicopathological profile of Indian patients with nonalcoholic fatty liver disease (NAFLD) is different from that in the West. Dig Dis Sci. 2007;52:2368–74.

  26. Bajaj S, Nigam P, Luthra A, et al. A case–control study on insulin resistance, metabolic co-variates and prediction score in non-alcoholic fatty liver disease. Indian J Med Res. 2009;129:285–92.

    PubMed  CAS  Google Scholar 

  27. Agarwal AK, Jain V, Singla S, et al. Prevalence of non-alcoholic fatty liver disease and its correlation with coronary risk factors in patients with type 2 diabetes. J Assoc Physicians India. 2011;59:351–4.

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  29. Petersen KF, Dufour S, Feng J, et al. Increased prevalence of insulin resistance and nonalcoholic fatty liver disease in Asian-Indian men. Proc Natl Acad Sci. 2006;103:18273–27.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  30. Kumar R, Rastogi A, Sharma MK, et al. Clinicopathological characteristics and metabolic profile of nonalcoholic fatty liver disease in Indian patients with normal body mass index: do they differ from obese or overweight non-alcoholic fatty liver disease? Indian J Endocr Metab. 2013;17:665–71.

    Article  Google Scholar 

  31. 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 

  32. Uchil D, Pipalia D, Chawla M, et al. Non-alcoholic fatty liver disease (NAFLD): the hepatic component of metabolic syndrome. J Assoc Physicians India. 2009;57:201–4.

    PubMed  Google Scholar 

  33. Das SK, Balakrishnan V. Role of cytokines in the pathogenesis of non-alcoholic fatty liver disease. Indian J Clin Biochem. 2011;26:202–9.

  34. Viswanathan V, Kadiri M, Medipudi S, Kumpatla S. Association of non-alcoholic fatty liver disease with microvascular and macrovascular complications in south Indian diabetic subjects. Int J Diabetes Dev C. 2010;30:208–12.

    Article  Google Scholar 

  35. Farrell GC, Larter CZ. Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology. 2006;43:S99–S112.

    Article  PubMed  CAS  Google Scholar 

  36. Marchesini G, Brizi M, Bianchi G, et al. Nonalcoholic fatty liver disease: a feature of the metabolic syndrome. Diabetes. 2001;50:1844–50.

    Article  PubMed  CAS  Google Scholar 

  37. Kim HJ, Kim HJ, Lee KE, et al. Metabolic significance of nonalcoholic fatty liver disease in nonobese, nondiabetic adults. Arch Intern Med. 2004;164:2169–75.

    Article  PubMed  Google Scholar 

  38. Hooper AJ, Adams LA, Burnett JR. Genetic determinants of hepatic steatosis in man. J Lipid Res. 2011;52:593–617.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  39. Santoro N, Kursawe R, D’Adamo E, et al. A common variant in the patatin-like phospholipase 3 gene (PNPLA3) is associated with fatty liver disease in obese children and adolescents. Hepatology. 2010;52:1281–90.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  40. Alam SL, Noor-E-Alam SM, Chowdhury ZR, Alam M, Kabir J. Nonalcoholic steatohepatitis in nonalcoholic fatty liver disease patients of Bangladesh. World J Hepatol. 2013;5:281–7.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Wong VW, Wong GL, Tsang SW, et al. Metabolic and histological features of non-alcoholic fatty liver disease patients with different serum alanine aminotransferase levels. Aliment Pharmacol Ther. 2009;29:387–96.

    Article  PubMed  CAS  Google Scholar 

  42. Neuschwander-Tetri BA, Clark JM, Bass NM, et al. NASH clinical research network. clinical, laboratory and histological associations in adults with nonalcoholic fatty liver disease. Hepatology. 2010;52:913–24.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  43. Alam S, Ahmad N, Mustafa G, et al. Evaluation of normal or minimally elevated alanine transaminase, age and DNA level in predicting liver histological changes in chronic hepatitis B. Liver Int. 2011;31:824–30.

    Article  PubMed  CAS  Google Scholar 

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Conflict of interest

SA, UDG, MA, JK, ZRC, and AKMKA all declare that they have no conflict of interest.

Ethics statement

The authors declare that the study was performed in a manner that conforms with the Helsinki Declaration of 1975, as revised in 2000 and 2008 concerning Human and Animal Rights, and the authors followed the policy concerning informed consent as shown on Springer.com.

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Correspondence to Shahinul Alam.

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Alam, S., Gupta, U.D., Alam, M. et al. Clinical, anthropometric, biochemical, and histological characteristics of nonobese nonalcoholic fatty liver disease patients of Bangladesh. Indian J Gastroenterol 33, 452–457 (2014). https://doi.org/10.1007/s12664-014-0488-5

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  • DOI: https://doi.org/10.1007/s12664-014-0488-5

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