Factors Predictive of Non-Alcoholic Fatty Liver Disease in Non-Obese Pakistani Population
Article Sidebar
Main Article Content
Abstract
Background: Non-alcoholic fatty liver disease (NAFLD) is one of the most prevalent causes of chronic liver disease worldwide, with a rising incidence in developing countries. In Pakistan, the estimated prevalence ranges from 14-47%. Studies have shown that NAFLD is also not uncommon among the non-obese lean population.
Objective: The aim of this study was to evaluate the factors predictive of non-alcoholic fatty liver disease in a non-obese Pakistani population, defined by a body mass index (BMI) of less than 23 kg/m².
Methods: This cross-sectional study was conducted at the Department of Hepatogastroenterology, Sindh Institute of Urology and Transplantation from November 1, 2020, to October 31, 2021. A total of 194 patients with BMI < 23 kg/m² presenting with abdominal pain were included. Exclusion criteria were viral hepatitis, significant alcohol intake, hepatocellular carcinoma, or other malignancies. Data collection involved recording demographic information, medical history, and clinical parameters. Ultrasound abdomen examinations were performed after 8-10 hours of fasting to diagnose NAFLD. Clinical assessments included history of hypertension and smoking, and laboratory tests such as liver function tests, fasting blood sugar levels, and lipid profiles. The primary outcome was the presence of fatty liver on ultrasound. Statistical analysis was conducted using SPSS version 25.0. Continuous variables were analyzed using the Student t-test and categorical variables using the Chi-square test. Significant variables in univariate analysis underwent multivariate logistic regression to identify independent predictors of lean NAFLD. A p-value ≤ 0.05 was considered significant.
Results: Out of the 194 patients, 107 (55.2%) were females. The mean age was 36.1 ± 9.6 years, and the mean BMI was 21 ± 1.7 kg/m². NAFLD was detected in 48 (24.7%) patients. Among the study population, 78 (40.2%) were hypertensive, 40 (20.6%) were diabetic, 49 (25.3%) were smokers, and 54 (27.8%) had increased triglyceride levels. Decreased HDL-C levels were observed in 72 (37.1%) patients. Univariate analysis identified hypertension (p ≤ 0.001), diabetes (p ≤ 0.001), smoking (p ≤ 0.001), hypertriglyceridemia (p ≤ 0.001), and decreased HDL-C levels (p ≤ 0.001) as significant factors. Multivariate logistic regression showed that diabetes (OR: 9.4, p = 0.037), smoking (OR: 46.4, p ≤ 0.001), hypertriglyceridemia (OR: 4.75, p = 0.016), and decreased HDL-C levels (OR: 36.8, p ≤ 0.001) were independently associated with lean NAFLD.
Conclusion: Non-obese individuals with a BMI less than 23 kg/m² can develop NAFLD and related complications. The study identified diabetes, smoking, hypertriglyceridemia, and decreased HDL-C levels as significant predictors of lean NAFLD. Further studies are needed to enhance the understanding of the disease's risk factors and behavior in this population.
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
References
Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, et al. The Diagnosis and Management of Non-Alcoholic Fatty Liver Disease: Practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology. 2012 Jun;55:2005-23.
Matteoni CA, Younossi ZM, Gramlich T, Boparai N, Liu YC, McCullough AJ. Nonalcoholic Fatty Liver Disease: A Spectrum of Clinical and Pathological Severity. Gastroenterology. 1999 Jun 1;116:1413-9.
Farrell GC, Wong VW, Chitturi S. NAFLD in Asia - As Common and Important as in the West. Nat Rev Gastroenterol Hepatol. 2013 May;10:307-18.
Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M. Global Epidemiology of Non-Alcoholic Fatty Liver Disease - Meta-Analytic Assessment of Prevalence, Incidence and Outcomes. Hepatology. 2016 Jul 1;64:73-84.
Abbas ZA, Zaheer R. Non-Alcoholic Fatty Liver Disease a Real Threat in Pakistan. J Pak Med Assoc. 2020 Dec 1;70(12(B)):2437-40.
Onitsuka Y, Takeshima F, Ichikawa T, Kohno S, Nakao K. Estimation of Visceral Fat and Fatty Liver Disease Using Ultrasound in Patients with Diabetes. Intern Med. 2014;53(6):545-53.
Pan WH, Yeh WT. How to Define Obesity? Evidence-Based Multiple Action Points for Public Awareness, Screening, and Treatment: An Extension of Asian-Pacific Recommendations. Asia Pac J Clin Nutr. 2008;17(3):370-4.
Diagnosis and Classification of Diabetes Mellitus. Diabetes Care. 2005 Jan 1;28(S37)
.
Milić S, Lulić D, Štimac D. Non-Alcoholic Fatty Liver Disease and Obesity: Biochemical, Metabolic and Clinical Presentations. World J Gastroenterol. 2014 Jul 28;20(28):9330.
Ha Y, Seo N, Shim JH, Kim SY, Park JA, Han S, et al. Intimate Association of Visceral Obesity with Non-Alcoholic Fatty Liver Disease in Healthy Asians: A Case-Control Study. J Gastroenterol Hepatol. 2015 Nov;30:1666-72.
Wang L, Guo J, Lu J. Risk Factor Compositions of Nonalcoholic Fatty Liver Disease Change with Body Mass Index in Males and Females. Oncotarget. 2016 Jun 14;7(24):35632.
Rush E, Plank L, Chandu V, Laulu M, Simmons D, Swinburn B, et al. Body Size, Body Composition, and Fat Distribution: A Comparison of Young New Zealand Men of European, Pacific Island, and Asian Indian Ethnicities. N Z Med J. 2004;117(1207):1-9.
Deurenberg-Yap M, Chew SK, Deurenberg P. Elevated Body Fat Percentage and Cardiovascular Risks at Low Body Mass Index Levels Among Singaporean Chinese, Malays and Indians. Obes Rev. 2002 Aug;3(3):209-15.
Wang J, Thornton JC, Russell M, Burastero S, Heymsfield SB, Pierson RN. Asians Have Lower Body Mass Index but Higher Percent Body Fat Than Do Whites: Comparisons of Anthropometric Measurements. Am J Clin Nutr. 1994 Jul 1;60:23-8.
Deurenberg-Yap M, Schmidt G, Staveren van WA, Deurenberg P. The Paradox of Low Body Mass Index and High Body Fat Percent Among Chinese, Malays and Indians in Singapore. Int J Obes. 2000 Aug;24:1011-7.
Grasgruber P, Sebera M, Hrazdíra E, Cacek J, Kalina T. Major Correlates of Male Height: A Study of 105 Countries. Econ Hum Biol. 2016 May 1;21:172-95.
Das K, Mukherjee PS, Ghosh A, Ghosh S, Mridha AR, Mukhopadhyay P, et al. Nonobese Population in a Developing Country Has a High Prevalence of Nonalcoholic Fatty Liver and Significant Liver Disease. Hepatology. 2010 May;51(5):1593-602.
Khan RTY, Hussain SZ, Shahzad S, et al. Frequency of Non-Alcoholic Fatty Liver Disease Among the Non-Obese Population Presenting to the Gastrointestinal Outpatient Clinic. J Liaquat Natl Hosp. 2024;2(1):117-121.
Wong RJ, Liu B, Bhuket T. Significant Burden of Nonalcoholic Fatty Liver Disease with Advanced Fibrosis in the US: A Cross-Sectional Analysis of 2011-2014 National Health and Nutrition Examination Survey. Aliment Pharmacol Ther. 2017 Nov;46(10):974-80.
Kwon YM, Oh SW, Hwang SS, Lee C, Kwon H, Chung GE. Association of Nonalcoholic Fatty Liver Disease with Components of Metabolic Syndrome According to Body Mass Index in Korean Adults. Am J Gastroenterol. 2012;107:1852–8.
Lee CM, Huxley RR, Wildman RP, Woodward M. Indices of Abdominal Obesity Are Better Discriminators of Cardiovascular Risk Factors Than BMI: A Meta-Analysis. J Clin Epidemiol. 2008 Jul;61(7):646-53.
Xu C, Yu C, Ma H, Xu L, Miao M, Li Y. Prevalence and Risk Factors for the Development of Nonalcoholic Fatty Liver Disease in a Nonobese Chinese Population: The Zhejiang Zhenhai Study. Am J Gastroenterol. 2013;108:1299–304.
Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M. Global Epidemiology of Non-Alcoholic Fatty Liver Disease: Meta-Analytic Assessment of Prevalence, Incidence, and Outcomes. Hepatology. 2016;64:73–84.
Zheng RD, Chen ZR, Chen JN, Lu YH, Chen J. Role of Body Mass Index, Waist-To-Height and Waist-To-Hip Ratio in Prediction of Nonalcoholic Fatty Liver Disease. Gastroenterol Res Pract. 2012;2012:1-8.
WHO Expert Consultation. Appropriate Body-Mass Index for Policy and Intervention Strategies. Lancet. 2004;363:157–63.
Park YW, Allison DB, Heymsfield SB, Gallagher D. Larger Amounts of Visceral Adipose Tissue in Asian Americans. Obes Res. 2001;9:381–7.
Younossi ZM, Stepanova M, Negro F, et al. Nonalcoholic Fatty Liver Disease in Lean Individuals in the United States. Medicine (Baltimore). 2012;91:319–27.
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.
Lankarani KB, Ghaffarpasand F, Mahmoodi M, Lotfi M, Zamiri N, Hyderi ST, et al. Non Alcoholic Fatty Liver Disease in Shiraz. Hepat Mon. 2013;13
.
Okamoto M, Miyake T, Kitai K, Furukawa S, Yamamoto S, Senba H, et al. Cigarette Smoking Is a Risk Factor for the Onset of Fatty Liver Disease in Nondrinkers: A Longitudinal Cohort Study. PLoS One. 2018;13
.
Hamabe A, Uto H, Imamura Y, Kusano K, Mawatari S, Kumagai K, et al. Impact of Cigarette Smoking on Onset of Nonalcoholic Fatty Liver Disease Over a 10-Year Period. J Gastroenterol. 2011;46:769–78.
Liu Y, Dai M, Bi Y, Xu M, Xu Y, Li M, et al. Active Smoking, Passive Smoking, and Risk of Nonalcoholic Fatty Liver Disease: A Population-Based Study in China. J Epidemiol. 2013;23:115–21.
Chen Z, Qin H, Qiu S, Chen G, Chen Y. Correlation of Triglyceride to High-Density Lipoprotein Cholesterol Ratio with Nonalcoholic Fatty Liver Disease Among the Non-Obese Chinese Population with Normal Blood Lipid Levels: A Retrospective Cohort Research. Lipids Health Dis. 2019 Aug 9;18(1):162.
Zhang YN, Wang QQ, Chen YS, Shen C, Xu CF. Association Between Serum Uric Acid to HDL-Cholesterol Ratio and Nonalcoholic Fatty Liver Disease in Lean Chinese Adults. Int J Endocrinol. 2020 Mar 23;2020:5953461.
Mathiesen U, Franzén L, Aselius H, Resjö M, Jacobsson L, Foberg U, et al. Increased Liver Echogenicity at Ultrasound Examination Reflects Degree of Steatosis but Not of Fibrosis in Asymptomatic Patients with Mild/Moderate Abnormalities of Liver Transaminases. Dig Liver Dis. 2002;34:516-22.
Joseph AE, Saverymuttu SH, al-Sam S, Cook MG, Maxwell JD. Comparison of Liver Histology with Ultrasonography in Assessing Diffuse Parenchymal Liver Disease. Clin Radiol. 1991;43:26-31.
Palmentieri B, de Sio I, La Mura V, Masarone M, Vecchione R, Bruno S, et al. The Role of Bright Liver Echo Pattern on Ultrasound B-Mode Examination in the Diagnosis of Liver Steatosis. Dig Liver Dis. 2006;38:485-9.