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Published in: Indian Journal of Gastroenterology 1/2020

01-02-2020 | Obesity | Original Article

Metabolic syndrome is not uncommon among lean non-alcoholic fatty liver disease patients as compared with those with obesity

Authors: Nirmalya Sinha, Saptarshi Mukhopadhyay, Manabendra Sau

Published in: Indian Journal of Gastroenterology | Issue 1/2020

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Abstract

Background

Non-alcoholic fatty liver disease (NAFLD) is associated with obesity, which is known to be associated with metabolic syndrome (MS). However, the risk factors for NAFLD in absence of obesity (leanness) is not well-studied. This study aimed to investigate and compare the clinical characteristics, metabolic associations, and cardiovascular risk factors among patients having NAFLD with (body mass index [BMI] ≥ 23 kg/m2) or without obesity (BMI < 23 kg/m2).

Methods

The cross-sectional study was conducted among the outdoor and indoor patients diagnosed as NAFLD by ultrasonography in a tertiary care teaching hospital in eastern India. Relevant anthropometric measurements, laboratory investigations, and imaging were performed. Metabolic syndrome was classified by the “International Diabetes Federation, 2005” criteria.

Results

Among 120 NAFLD patients, 37 (30.8%) were lean, while 83 (69.2%) were obese. The components of MS such as systolic blood pressure (lean, 138.0 ± 17.6 mmHg; obese, 137.9 ± 15.3 mmHg), diastolic blood pressure (lean, 88.9 ± 6.5 mmHg; obese, 87.3 ± 6.1 mmHg), fasting blood sugar (lean, 127.8 ± 30.8 mg/dL; obese, 135.1 ± 29.5 mg/dL), and serum triglyceride (lean, 170.5 ± 34.2 mg/dL; obese, 186.4 ± 43.8 mg/dL) were comparable among patients with obese and lean NAFLD and were more often abnormal among both the groups of NAFLD as compared with controls.

Conclusion

The overall prevalence of MS among NAFLD study population was 64.2%. Lean NAFLD was also associated with the component of MS like obese NAFLD.
Literature
1.
go back to reference Kim D, Kim WR. Nonobese fatty liver disease. Clin Gastroenterol Hepatol. 2017;15:474–85. Kim D, Kim WR. Nonobese fatty liver disease. Clin Gastroenterol Hepatol. 2017;15:474–85.
2.
go back to reference Ghoshal UC, Baba CS, Ghoshal U, et al. Low-grade small intestinal bacterial overgrowth is common in patients with non-alcoholic steatohepatitis on quantitative jejunal aspirate culture. Indian J Gastroenterol. 2017;36:390–9. Ghoshal UC, Baba CS, Ghoshal U, et al. Low-grade small intestinal bacterial overgrowth is common in patients with non-alcoholic steatohepatitis on quantitative jejunal aspirate culture. Indian J Gastroenterol. 2017;36:390–9.
3.
go back to reference Duseja A. Nonalcoholic fatty liver disease in India - a lot done, yet more required! Indian J Gastroenterol. 2010;29:217–25. Duseja A. Nonalcoholic fatty liver disease in India - a lot done, yet more required! Indian J Gastroenterol. 2010;29:217–25.
4.
go back to reference Alam S, Islam MS, Islam S, Mustafa G, Saleh AA, Ahmad N. Association of single nucleotide polymorphism at PNPLA3 with fatty liver, steatohepatitis, and cirrhosis of liver. Indian J Gastroenterol. 2017;36:366–72. Alam S, Islam MS, Islam S, Mustafa G, Saleh AA, Ahmad N. Association of single nucleotide polymorphism at PNPLA3 with fatty liver, steatohepatitis, and cirrhosis of liver. Indian J Gastroenterol. 2017;36:366–72.
5.
go back to reference Araujo AR, Rosso N, Bedogni G, Tiribelli C, Bellentani S. Global epidemiology of non-alcoholic fatty liver disease/non-alcoholic steatohepatitis: what we need in the future. Liver Int. 2018;38 Suppl 1:47–51. Araujo AR, Rosso N, Bedogni G, Tiribelli C, Bellentani S. Global epidemiology of non-alcoholic fatty liver disease/non-alcoholic steatohepatitis: what we need in the future. Liver Int. 2018;38 Suppl 1:47–51.
6.
go back to reference Younossi Z, Anstee QM, Marietti M, et al. Global burden of NAFLD and NASH: trends, predictions, risk factors and prevention. Nat Rev Gastroenterol Hepatol. 2018;15:11–20. Younossi Z, Anstee QM, Marietti M, et al. Global burden of NAFLD and NASH: trends, predictions, risk factors and prevention. Nat Rev Gastroenterol Hepatol. 2018;15:11–20.
7.
go back to reference Machado MV, Cortez-Pinto H. Fatty liver in lean patients: is it a different disease? Ann Gastroenterol. 2012;25:1–2. Machado MV, Cortez-Pinto H. Fatty liver in lean patients: is it a different disease? Ann Gastroenterol. 2012;25:1–2.
8.
go back to reference Perumpail BJ, Khan MA, Yoo ER, Cholankeril G, Kim D. Ahmed A. Clinical epidemiology and disease burden of nonalcoholic fatty liver disease. World J Gastroenterol. 2017;23:8263–76. Perumpail BJ, Khan MA, Yoo ER, Cholankeril G, Kim D. Ahmed A. Clinical epidemiology and disease burden of nonalcoholic fatty liver disease. World J Gastroenterol. 2017;23:8263–76.
9.
go back to reference Ballestri S, Lonardo A, Bonapace S, Byrne CD, Loria P, Targher G. Risk of cardiovascular, cardiac and arrhythmic complications in patients with non-alcoholic fatty liver disease. World J Gastroenterol. 2014;20:1724–45. Ballestri S, Lonardo A, Bonapace S, Byrne CD, Loria P, Targher G. Risk of cardiovascular, cardiac and arrhythmic complications in patients with non-alcoholic fatty liver disease. World J Gastroenterol. 2014;20:1724–45.
10.
go back to reference Bhat G, Baba CS, Pandey A, Kumari N, Choudhuri G. Insulin resistance and metabolic syndrome in nonobese Indian patients with non-alcoholic fatty liver disease. Trop Gastroenterol. 2013;34:18–24. Bhat G, Baba CS, Pandey A, Kumari N, Choudhuri G. Insulin resistance and metabolic syndrome in nonobese Indian patients with non-alcoholic fatty liver disease. Trop Gastroenterol. 2013;34:18–24.
11.
go back to reference Shin JA, Lee JH, Lim SY, et al. Metabolic syndrome as a predictor of type 2 diabetes, and its clinical interpretations and usefulness. J Diabetes Investig. 2013;4:334–43. Shin JA, Lee JH, Lim SY, et al. Metabolic syndrome as a predictor of type 2 diabetes, and its clinical interpretations and usefulness. J Diabetes Investig. 2013;4:334–43.
12.
go back to reference Ginsberg HN, MacCallum PR. The obesity, metabolic syndrome, and type 2 diabetes mellitus pandemic: part I. Increased cardiovascular disease risk and the importance of atherogenic dyslipidemia in persons with the metabolic syndrome and type 2 diabetes mellitus. J Cardiometab Syndr. 2009;4:113–9. Ginsberg HN, MacCallum PR. The obesity, metabolic syndrome, and type 2 diabetes mellitus pandemic: part I. Increased cardiovascular disease risk and the importance of atherogenic dyslipidemia in persons with the metabolic syndrome and type 2 diabetes mellitus. J Cardiometab Syndr. 2009;4:113–9.
13.
go back to reference Bahrami A, Teymoori F, Eslamparast T, et al. Legume intake and risk of nonalcoholic fatty liver disease. Indian J Gastroenterol. 2019;38:55–60. Bahrami A, Teymoori F, Eslamparast T, et al. Legume intake and risk of nonalcoholic fatty liver disease. Indian J Gastroenterol. 2019;38:55–60.
14.
go back to reference Kumar S, Khandelwal N, Kumar A, et al. Simultaneous living donor liver transplant with sleeve gastrectomy for metabolic syndrome and NASH-related ESLD-First report from India. Indian J Gastroenterol. 2017;36:243–7. Kumar S, Khandelwal N, Kumar A, et al. Simultaneous living donor liver transplant with sleeve gastrectomy for metabolic syndrome and NASH-related ESLD-First report from India. Indian J Gastroenterol. 2017;36:243–7.
15.
go back to reference Wells JC, Pomeroy E, Walimbe SR, Popkin BM, Yajnik CS. The elevated susceptibility to diabetes in India: an evolutionary perspective. Front Public Health. 2016;4:145.CrossRef Wells JC, Pomeroy E, Walimbe SR, Popkin BM, Yajnik CS. The elevated susceptibility to diabetes in India: an evolutionary perspective. Front Public Health. 2016;4:145.CrossRef
16.
go back to reference Prasad DS, Kabir Z, Dash AK, Das BC. Prevalence and risk factors for metabolic syndrome in Asian Indians: a community study from urban eastern India. J Cardiovasc Dis Res. 2012;3:204–11. Prasad DS, Kabir Z, Dash AK, Das BC. Prevalence and risk factors for metabolic syndrome in Asian Indians: a community study from urban eastern India. J Cardiovasc Dis Res. 2012;3:204–11.
17.
go back to reference Swain M, Nath P, Parida PK, et al. Biochemical profile of nonalcoholic fatty liver disease patients in eastern India with histopathological correlation. Indian J Clin Biochem. 2017;32:306–14. Swain M, Nath P, Parida PK, et al. Biochemical profile of nonalcoholic fatty liver disease patients in eastern India with histopathological correlation. Indian J Clin Biochem. 2017;32:306–14.
18.
go back to reference Li Q, Dhyani M, Grajo JR, Sirlin C, Samir AE. Current status of imaging in nonalcoholic fatty liver disease. World J Hepatol. 2018;10:530–42. Li Q, Dhyani M, Grajo JR, Sirlin C, Samir AE. Current status of imaging in nonalcoholic fatty liver disease. World J Hepatol. 2018;10:530–42.
19.
go back to reference Mishra P, Younossi ZM. Abdominal ultrasound for diagnosis of nonalcoholic fatty liver disease (NAFLD). Am J Gastroenterol. 2007;102:2716–7. Mishra P, Younossi ZM. Abdominal ultrasound for diagnosis of nonalcoholic fatty liver disease (NAFLD). Am J Gastroenterol. 2007;102:2716–7.
20.
go back to reference 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. 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.
21.
go back to reference Annex 2 Recommended measurement protocols and derivations of indices. In: Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee. Geneva: World Health Organization; 1995:424–38 (WHO Technical Report Series, No. 854; http://apps.who.int/iris/ bitstream/10665/37003/ 1/WHO_TRS_854.pdf, accessed 10 February 2016) Annex 2 Recommended measurement protocols and derivations of indices. In: Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee. Geneva: World Health Organization; 1995:424–38 (WHO Technical Report Series, No. 854; http://​apps.​who.​int/​iris/​ bitstream/10665/37003/ 1/WHO_TRS_854.pdf, accessed 10 February 2016)
22.
go back to reference Trinder P. Determination of glucose in blood using glucose oxidase with an alternative oxygen acceptor. Ann Clin Biochem. 1969;6:24–7. Trinder P. Determination of glucose in blood using glucose oxidase with an alternative oxygen acceptor. Ann Clin Biochem. 1969;6:24–7.
24.
go back to reference WHO expert consultation. Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet. 2004;363:157–63. WHO expert consultation. Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet. 2004;363:157–63.
25.
go back to reference Gaharwar R, Trikha S, Margekar SL, Jatav OP, Ganga PD. Study of clinical profile of patients of non alcoholic fatty liver disease and its association with metabolic syndrome. J Assoc Physicians India. 2015;63:12–6. Gaharwar R, Trikha S, Margekar SL, Jatav OP, Ganga PD. Study of clinical profile of patients of non alcoholic fatty liver disease and its association with metabolic syndrome. J Assoc Physicians India. 2015;63:12–6.
26.
go back to reference 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. 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.
27.
go back to reference Bajaj S, Nigam P, Luthra A, et al. A case-control study on insulin resistance, metabolic co-variates & prediction score in non-alcoholic fatty liver disease. Indian J Med Res. 2009;129:285–92. Bajaj S, Nigam P, Luthra A, et al. A case-control study on insulin resistance, metabolic co-variates & prediction score in non-alcoholic fatty liver disease. Indian J Med Res. 2009;129:285–92.
28.
go back to reference Iqbal U, Perumpail BJ, Akhtar D, Kim D, Ahmed A. The epidemiology, risk profiling and diagnostic challenges of nonalcoholic fatty liver disease. Medicines (Basel). 2019;6. pii: E41. Iqbal U, Perumpail BJ, Akhtar D, Kim D, Ahmed A. The epidemiology, risk profiling and diagnostic challenges of nonalcoholic fatty liver disease. Medicines (Basel). 2019;6. pii: E41.
29.
go back to reference Kumar R, Mohan S. Non-alcoholic fatty liver disease in lean subjects: characteristics and implications. J Clin Transl Hepatol. 2017;5:216–23. Kumar R, Mohan S. Non-alcoholic fatty liver disease in lean subjects: characteristics and implications. J Clin Transl Hepatol. 2017;5:216–23.
30.
go back to reference Fan JG, Kim SU, Wong VW. New trends on obesity and NAFLD in Asia. J Hepatol. 2017;67:862–73. Fan JG, Kim SU, Wong VW. New trends on obesity and NAFLD in Asia. J Hepatol. 2017;67:862–73.
31.
go back to reference Khov N. Bedside ultrasound in the diagnosis of nonalcoholic fatty liver disease. World J Gastroenterol. 2014;20:6821–5. Khov N. Bedside ultrasound in the diagnosis of nonalcoholic fatty liver disease. World J Gastroenterol. 2014;20:6821–5.
32.
go back to reference Tana C, Ballestri S, Ricci F, et al. Cardiovascular risk in non-alcoholic fatty liver disease: mechanisms and therapeutic implications. Int J Environ Res Public Health. 2019;16:pii: E3104. Tana C, Ballestri S, Ricci F, et al. Cardiovascular risk in non-alcoholic fatty liver disease: mechanisms and therapeutic implications. Int J Environ Res Public Health. 2019;16:pii: E3104.
33.
go back to reference Olubunmi OO, Virtanen JK, Pihlajamaki J, Tuomainen TP. Association of fatty liver index with risk of incident type 2 diabetes by metabolic syndrome status in an Eastern Finland male cohort: a prospective study. BMJ Open. 2019;9:e026949.CrossRef Olubunmi OO, Virtanen JK, Pihlajamaki J, Tuomainen TP. Association of fatty liver index with risk of incident type 2 diabetes by metabolic syndrome status in an Eastern Finland male cohort: a prospective study. BMJ Open. 2019;9:e026949.CrossRef
34.
go back to reference Misra A, Khurana L. The metabolic syndrome in South Asians: epidemiology, determinants, and prevention. Metab Syndr Relat Disord. 2009;7:497–514. Misra A, Khurana L. The metabolic syndrome in South Asians: epidemiology, determinants, and prevention. Metab Syndr Relat Disord. 2009;7:497–514.
35.
go back to reference Alam S, Gupta UD, Alam M, Kabir J, Chowdhury ZR, Alam AK. Clinical, anthropometric, biochemical, and histological characteristics of nonobese nonalcoholic fatty liver disease patients of Bangladesh. Indian J Gastroenterol. 2014;33:452–7. Alam S, Gupta UD, Alam M, Kabir J, Chowdhury ZR, Alam AK. Clinical, anthropometric, biochemical, and histological characteristics of nonobese nonalcoholic fatty liver disease patients of Bangladesh. Indian J Gastroenterol. 2014;33:452–7.
36.
go back to reference Kumar R, Rastogi A, Sharma MK, et al. Clinicopathological characteristics and metabolic profiles of non-alcoholic 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 Endocrinol Metab. 2013;17:665–71. Kumar R, Rastogi A, Sharma MK, et al. Clinicopathological characteristics and metabolic profiles of non-alcoholic 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 Endocrinol Metab. 2013;17:665–71.
37.
go back to reference Das K, Das K, Mukherjee PS, et al. Nonobese population in a developing country has a high prevalence of nonalcoholic fatty liver and significant liver disease. Hepatology. 2010;51:1593–602. Das K, Das K, Mukherjee PS, et al. Nonobese population in a developing country has a high prevalence of nonalcoholic fatty liver and significant liver disease. Hepatology. 2010;51:1593–602.
38.
go back to reference Wei JL, Leung JC, Loong TC, et al. Prevalence and severity of nonalcoholic fatty liver disease in non-obese patients: a population study using proton-magnetic resonance spectroscopy. Am J Gastroenterol. 2015;110:1306–14, quiz 1315. Wei JL, Leung JC, Loong TC, et al. Prevalence and severity of nonalcoholic fatty liver disease in non-obese patients: a population study using proton-magnetic resonance spectroscopy. Am J Gastroenterol. 2015;110:1306–14, quiz 1315.
39.
go back to reference 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. 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.
40.
go back to reference Leung JC, Loong TC, Wei JL, et al. Histological severity and clinical outcomes of nonalcoholic fatty liver disease in nonobese patients. Hepatology. 2017;65:54–64. Leung JC, Loong TC, Wei JL, et al. Histological severity and clinical outcomes of nonalcoholic fatty liver disease in nonobese patients. Hepatology. 2017;65:54–64.
Metadata
Title
Metabolic syndrome is not uncommon among lean non-alcoholic fatty liver disease patients as compared with those with obesity
Authors
Nirmalya Sinha
Saptarshi Mukhopadhyay
Manabendra Sau
Publication date
01-02-2020
Publisher
Springer India
Published in
Indian Journal of Gastroenterology / Issue 1/2020
Print ISSN: 0254-8860
Electronic ISSN: 0975-0711
DOI
https://doi.org/10.1007/s12664-020-01020-3

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