• Users Online: 131
  • Home
  • Print this page
  • Email this page
Home About us Editorial board Search Ahead of print Current issue Archives Submit article Instructions Subscribe Contacts Login 


 
 Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 31  |  Issue : 1  |  Page : 92-98

Prevalence of asymptomatic nonalcoholic fatty liver disease in nondiabetic participants: a study from South India


1 Department of Clinical Research, Nizams’s Institute of Medical Sciences; Department of Neurology, Nizams’s Institute of Medical Sciences, Hyderabad, Telangana, India
2 Department of Neurology, Nizams’s Institute of Medical Sciences, Hyderabad, Telangana, India
3 Department of Radiology, Nizams’s Institute of Medical Sciences, Hyderabad, Telangana, India
4 Department of Medicine, Yashoda Group of Hospitals, Hyderabad, Telangana, India

Date of Submission09-Sep-2018
Date of Acceptance28-Oct-2018
Date of Web Publication24-Apr-2019

Correspondence Address:
Kandadai R Mridula
Department of Neurology, Nizam’s Institute of Medical Sciences, Hyderabad 500082
India
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ejim.ejim_76_18

Rights and Permissions
  Abstract 

Background Nonalcoholic fatty liver disease (NAFLD) is a common chronic disease that is rapidly increasing worldwide.
Aim The aim of this study was to investigate the risk factors associated with NAFLD in nondiabetics from South India.
Participants and methods We recruited 345 asymptomatic participants consecutively, and the study period was between January 2014 and December 2017. All participants underwent risk factor evaluation, fasting serum lipid profile, C-reactive protein (CRP), hemoglobin A1c, liver function test, and abdominal ultrasound.
Results Of 345 participants, men represented 213 (71%). The mean age of the participants was 58.4±11.1 years, with age range from 24–68 years. Prevalence of NAFLD was seen in 22%. On risk factor evaluation, 107 (31%) were hypertensive, 89 (25.7%) smoked, 52 (15%) were overweight, 110 (24.9%) were obese, and 113 (32.7%) had dyslipidemia. The mean CRP was 12.7±9.5 mg/l. High γ-glutamyl transferase levels, elevated CRP levels, obesity (45, 59.2%), high total cholesterol (49, 64.4%), low levels of high-density lipoprotein (28, 36.8%), high levels of low-density lipoprotein (27, 35.5%), and high triglycerides (31, 40.7%) were significantly associated with NALFD compared with non-NAFLD. After adjustment using multiple regression analysis, obesity (odds ratio: 3.5; 95% CI: 2.18–6.16), high total cholesterol [odds ratio: 4.9; 95% confidence interval (CI): 2.91–9.43], low high-density lipoprotein (odds ratio: 2.3; 95% CI: 1.20–4.47), high low-density lipoprotein (odds ratio: 2.9; 95% CI: 1.58–6.17), high triglycerides (odds ratio: 2.4; 95% CI: 1.33–4.60), and elevated CRP levels (odds ratio: 2.0; 95% CI: 1.21–3.39) were significantly associated with NAFLD.
Conclusion Our study established obesity, CRP positivity, and dyslipidemia as independently associated with NAFLD in South Indian patients.

Keywords: asymptomatic diseases, C-reactive protein, dyslipidemia, nonalcoholic fatty liver disease, nondiabetics, obesity, South Indian patients


How to cite this article:
Bandaru VS, Chaudhury JR, Lalitha P, Reddy SN, Misra PK, Balaraju B, Mridula KR. Prevalence of asymptomatic nonalcoholic fatty liver disease in nondiabetic participants: a study from South India. Egypt J Intern Med 2019;31:92-8

How to cite this URL:
Bandaru VS, Chaudhury JR, Lalitha P, Reddy SN, Misra PK, Balaraju B, Mridula KR. Prevalence of asymptomatic nonalcoholic fatty liver disease in nondiabetic participants: a study from South India. Egypt J Intern Med [serial online] 2019 [cited 2019 Sep 19];31:92-8. Available from: http://www.esim.eg.net/text.asp?2019/31/1/92/256987




  Introduction Top


Nonalcoholic fatty liver disease (NAFLD) is a separate hepatic condition distinguished by abnormal fat deposits in liver cells causing chronic liver disease [1]. NAFLD is now recognized as one of the major chronic liver diseases in industrialized countries [2]. At present, NAFLD is an increasing major health problem worldwide [3]. At the time of diagnosis, most patients with NAFLD have minimal signs and symptoms of liver disease, even though some patients have discomfort or sensation of fullness on the right side of the upper abdomen; there is generalized fatigue with hepatomegaly in most of the patients. Prevalence of NAFLD is 15–40% in Western countries and 9–40% in Asia [4]. Recent studies from the Indian subcontinent recorded a NAFLD prevalence of 9–32% in the general population [5],[6]. Studies have established hypertension, type II diabetes, smoking, obesity, and dyslipidemia to be significantly associated with NAFLD [5],[6]. The aim of this study was to investigate NAFLD risk factors among nondiabetics in general population. Limited studies are available on this topic from Indian subcontinent.


  Participants and methods Top


We recruited consecutively, 345 asymptomatic participants from medical health check-up clinic at Yashoda Hospital and Nizam’s Institution of Medical Sciences, Hyderabad. The study period was from January 2014 to December 2017, and the study was approved by Institutional Ethics Committee.

Detailed medical history (present and past) was collected from all participants. Standardized questions were adapted from the behavioral risk factor surveillance system prescribed by the Centers for Disease Control and Prevention. All participants underwent glycosylated hemoglobin A1c (HbA1c), lipid profile, C-reactive protein (CRP), ultrasound abdominal and liver function test [alanine aminotransferase (ALT), aspartate aminotransferase (AST), γ-glutamyl transferase (GGT), and alkaline phosphatase], and viral screening (HIV and hepatitis B and C). NAFLD was diagnosed based on criteria defined by American Gastroenterology Association [7], and based on the ultrasonography, NAFLD was classified into grade I, grade II, and grade III [8].

Including and excluding criteria

Participants older than 18 years were included in the study. If participants having any present or past history of NAFLD; type I or type II diabetes; cardiovascular disease; cerebrovascular disease; other liver diseases like viral hepatitis, primary biliary cirrhosis, drug-induced liver damage, autoimmune hepatitis, biliary obstruction, alcoholic liver disease, and Wilson’s disease; α1-antitrypsin deficiency; HIV infection; alcohol intake more than 20 g/day; severe end organ damage; malignancy; previous gastrointestinal tract surgery; ingestion of drugs known to produce hepatic steatosis; patients taking corticosteroids, high-dose estrogens, methotrexate, tetracycline hydrochloride, amiodarone, or tamoxifen citrate in the previous 6 months; those who had received any prior therapies that may have been beneficial for NAFLD, such as vitamin E, pentoxifylline, and pioglitazone; and those prescribed diet and exercise for weight loss were excluded from the study.

Risk factor assessment

According to Joint National Committee VI–VII, hypertension was defined as a systolic blood pressure more than 140 mmHg and/or a diastolic blood pressure more than 90 mmHg based on the average of the two blood pressure measurements, or a patient’s self-reported history of hypertension or antihypertensive use, supported by documents. Diabetes was diagnosed if the patient was on antidiabetic medications. Smokers were defined as those reporting daily smoking, and exsmokers and occasional smokers were classified as nonsmokers. BMI value of 25.1–30 kg/m2 was considered overweight and more than 30 kg/m2 was measured as obese. Dyslipidemia was defined (ATP III) as one or more of the following: total cholesterol more than 200 mg/dl, low-density lipoprotein (LDL) cholesterol more than 130 mg/dl, high-density lipoprotein (HDL) cholesterol below 40 mg/dl, very low-density lipoprotein (VLDL) cholesterol more than 30 mg/dl, and triglycerides more than 150 mg/dl. The CRP was assessed by quantitative analysis, and more than 10.1 mg/l was considered positive [9],[10].

Statistical analysis

Statistical analysis was performed using statistical package for the social sciences 18.0 Windows Software (SPSS Inc., Chicago, Illinois, USA). Continuous variables were presented in titer of mean±SD. Categorical variables were expressed as proportions. The Student t-test was used to test the differences in continuous variables, and χ2-test was used to study the association in proportions. Multiple logistic regression was performed before and after adjustment for potential confounders. All tests were two sided, and P value less than 0.05 was considered statistically significant.


  Results Top


[Table 1] shows that men represented 213 (71%). The participants’ mean age was 58.4±11.1 years, with age range from 25 to 69 years. Hypertension was observed in 107 (31%), smoking in 89 (25.7%), alcoholism (<20 g/day) in 41 (11.8%), normal weight in 183 (53%), overweight in 52 (15%), and obesity in 110 (24.9%) participants. High total cholesterol levels were seen in 113 (32.7%), low HDL in 67 (19.4%), high LDL in 60 (17.3%), high VLDL in 25 (7.2%), high triglycerides in 83 (24%), and CRP positivity in 125 (36.2%) participants. Mean HbA1c was 5.9±2.1, mean ALT was 59.4±12.8 IU/l, mean AST was 40.5±8.9 IU/l, mean GGT 59.9±19.4 IU/l, and mean alkaline phosphatase was 98.6±21.5 IU/l. Prevalence of NAFLD in nondiabetics was seen in 76 (22%) (grade 1 was 11.5%, grade II 7.5%, and grade III 2.8%) ([Table 1]).
Table 1 Baseline characteristics

Click here to view


Older age (mean age: 59.9±12.2 years) (P=0.043), obesity (45, 59.2%) (P<0.0001), high total cholesterol (49, 64.4%) (P<0.0001), low HDL levels (28, 36.8%) (P<0.0001), high LDL levels (27, 35.5%) (P<0.0001), high triglycerides (31, 40.7%) (P<0.0001), obesity (45, 59.2%) (P<0.0001), elevated mean CRP levels (17.8±13.9) (P<0.0001), elevated mean ALT levels (72.8±14.8) (P<0.0001), AST (47.4±11.7) (P<0.0001) elevated mean GGT (68.4±12.7) (P<0.0001), and alkaline phosphatase levels (128.1±13.8) (P<0.0001) were significantly associated with NAFLD compared with participants without NAFLD ([Table 2]).
Table 2 Comparison between nonalcoholic fatty liver disease and non-nonalcoholic fatty liver disease

Click here to view


After adjustment using multiple logistic regression analysis, high total cholesterol levels [odds ratio: 4.9; 95% confidence interval (CI): 2.91–9.43], low HDL levels (odds ratio: 2.3; 95% CI: 1.20–4.47), high LDL levels (odds ratio: 2.9; 95% CI: 1.58–6.17), high triglycerides levels (odds ratio: 2.4; 95% CI: 1.33–4.60), obesity (odds ratio: 3.5; 95% CI: 2.18–6.16), and elevated CRP levels (odds ratio: 2.0; 95% CI: 1.21–3.39) were independently associated with NAFLD ([Table 3]).
Table 3 Predictors of nonalcoholic fatty liver disease (before and after adjustment in stepwise method)

Click here to view



  Discussion Top


In our study, we found a prevalence of 22% of NAFLD in asymptomatic participants from South India; other studies have found similar findings from 9.3 to 29.5% in Asian countries [11],[12], 17.1% in Mexico [13], 30% in Israel [14], 20% in Romania [15], and 22.6% in Italy [16]. Ethnicity and racial differences possibly account for the small changes in the prevalence of NAFLD and less prevalence of NAFLD in African Americans [17]. The difference may be owing to less visceral fat and a different lipoprotein metabolism in African Americans [18].

Recent studies have established increasing prevalence of NAFLD with age [1]. We found our study the mean age (59.9 years) had borderline significant association with NAFLD; other studies have noted slightly lower mean age (49.14+9.65) years [8] and 55.4 years [19].

Fatty liver occurs in all age groups. The liver regulates alcohol metabolism, and as the body ages, toxicity elevates owing to increased organ damage. These developments are related to a mitochondrial transport flaw rising with age and decrease in the smooth endoplasmic reticulum and metabolism of CYP2E1-dependent microsomal ethanol oxidation functions [20].

In our study, we noted that among patients with NAFLD, 43 (56.5%) were men, whereas other studies have noted in 53.3% of men [21]. Our study established no significant association between men and women with NAFLD. However, some studies have noted NAFLD being more predominant in women [1].

We found hypertension in 22 (28.9%) patients with NAFLD, with no significant association with NAFLD. However, some studies have found a significant association with NAFLD [22],[23].

This study found smoking was seen in 21 (27.6%) of patients with NAFLD, with no significant association with NAFLD. In contrast, other studies have noted smoking was association with NAFLD [24].

This study found obesity was present in 45 (59.2%) of patients with NAFLD, with a significant association with NAFLD. Our findings were advocated by other studies, which showed the prevalence ranges from 22–74% in obese children and adults [25],[26]. De Sousa et al. [26] found in a population-based study, central obesity was seen in 50.5% of men and 38.9% of women, and it had an independent association with NAFLD. Cotrim et al. showed in their study, 44.7% of patients with NAFLD had obesity [21]. Kim et al. [27] noted in his study 34.4% had NAFLD in the overweight group. Kalra et al. [1] noted in their study 54.9% of female patients with NAFLD had obesity.

Asian participants have a higher ratio of visceral fat and a minor lean body mass than Caucasian participants with the same BMI. Central obesity is an important factor for insulin resistance, and an increased visceral adiposity may cause pathogenesis of NAFLD. Visceral adipose tissue is strongly associated with insulin resistant and produces more free fatty acid than accomplish adipose tissue in other sites. In liver deposited of undeveloped lipogenesis causing to NAFLD [27].

Studies have reported that obesity is a major risk factor for NAFLD [27]. In our study, after adjustment of logistic regression analysis, obesity was an independent risk factor for NAFLD (odds ratio: 3.5; 95% CI: 2.18–6.16). Our findings were advocated by de Sousa and colleagues [26],[27],[28].

Studies have noted the prevalence of 20–92% of patients having dyslipidemia with NAFD [29]. Amarapurkar et al. [3] found in their study the prevalence of NAFLD among patients with dyslipidemia ranges between 25 and 60% in reports from the Asia–Pacific region. In our study, we showed hypercholesterolemia in 64.4%, high LDL in 35.5%, high triglycerides in 31 (40.7%), and low HDL in 36.8% in patients with NAFLD. Our findings were supported by other studies [8],[30],[31],[32]. Jali et al. [31] noted in their study, 52% of the patients with NAFLD had hypercholesterolemia, 27% had low HDL, 59% had high levels of LDL, and 67% had high levels of triglycerides. Mahaling et al. [8] found in their study hypertriglycerides in 67.1%, hypercholesterolemia in 45.7%, high LDL in 34.2%, and high VLDL in 25.7%. Agrawal et al. [32] showed in his study, 21.8% had hypercholesterolemia, 45.16% had low HDL, 25% had high LDL, 56.5% had elevated VLDL, and 63.7% had hypertriglyceridemia, and obesity association with NAFLD. Marchsini et al. [33] noted in their study, hypertriglyceridemia is present in 64% of patients with hepatic steatosis and 30–42% of HDL low levels. Cotrim et al. [21] reported the presence of hyperlipidemia in 66.8% of patients with NAFLD. Duseja et al. [34] found hypercholesterolemia in 32% of patients and hypertriglyceridemia 79 (63.7%) patients.

Differences in body fat distribution of patients with NAFLD may have a genetic predisposition. Deposits of lipids within hepatocytes, in the form of triglycerides, can lead to development of NAFLD. The primary metabolic abnormalities leading to lipid accumulation are not proper understood, but they may consist of alterations in the pathways of uptake, synthesis, degradation or secretion in hepatic lipid metabolism and finally from insulin resistance. Insulin resistance is one of the factor for development of NAFLD [8]. The pathophysiology of NAFLD is still incompletely understood. Storage of triglycerides in hepatocytes due to oxidative stress, lipid peroxidation, and proinflammatory cytokines [e.g. tumor necrosis factor α (TNF-α) and interleukin 6 (IL-6)]. Animal studies have shown elevated fatty acids in the liver, and it may cause higher levels of TNF-α. When hepatocytes get damaged, liver-specific macrophages (Kupffer cells) are activated and produce more TNF-α and IL-6 into the blood stream, which leads to the production of the acute-phase protein high-sensitivity CRP [35].

In our study, we established that elevated total cholesterol (odds ratio: 4.9; 95% CI: 2.91–9.43), LDL (odds ratio: 3.0; 95% CI: 1.55–6.07) triglycerides (odds ratio: 2.4; 95% CI: 1.33–4.60), and low HDL (odds ratio: 2.3; 95% CI: 1.20–4.47) are independent association with NAFLD; our findings are supported by Amirkalali et al. [36].In our study, we found elevated CRP levels were significant associated with NAFLD compared without NAFLD, and our findings are supported by Nigam et al. [35]. Very few studies have found elevated CRP levels are a useful diagnostic marker for NAFLD [37],[38]. Studies have noted CRP levels were higher in Asians Indians than Caucasians [39]. Park et al. [40] showed in their study that elevated high-sensitivity CRP level was associated with NAFLD in nonobese healthy men. The proposed mechanism between CRP and NAFLD is the rise in acute-phase cytokines. IL-6 is a strong booster and elevates CRP levels.

This study established elevated CRP levels as an independent risk factor for NAFLD (odds ratio: 2.1; 95% CI: 1.21–3.39), and these findings were advocated by Assy et al. [41].

Our study found that elevated ALT (72.8±14.8 IU/l), AST (47.4±11.7 IU/l), and alkaline phosphatase (128.1±13.8 IU/l) are significantly associated with NAFLD compared with without NAFLD. A similar finding was noted by Agrawal et al. [32], who noted in their study ALT had a mean value of 97.0±56.0 IU/l, AST had a mean value of 75.0±50 IU/l, and alkaline phosphatase had a mean value of 216.0±77 IU/l. Jali et al. [31] noted elevated levels of AST (30%) and ALT (22%) in NAFLD. Amirkalali et al. [36] showed in their study very low prevalence of AST (3.9%) and ALT (10.4%) in NAFLD. However, some studies have found no significant association AST and ALT with NAFLD [42],[43]. Studies have established GGT levels were significantly associated with NAFLD [44],[45]. Our study showed elevated GGT levels were significantly associated with NAFLD when compared with non-NAFLD; our findings are advocated by Saxena and colleagues [44],[45].

Limitations of study

The main drawback of the study was that we were unable to examine insulin resistance in our participants. The second drawback was that we were unable to analyze grade I to grade III with multiple logistic regression owing to small number. In our study, all asymptomatic participants underwent for one laboratory examination at the time of recruitment. Some studies have found liver biopsy as a gold standard for NAFLD diagnosis, but it is an invasiveness and painful procedure with complications, and sometimes, mortality also occurs. In this study, we performed ultrasonography, which is a noninvasiveness procedure and a promising tool for NAFLD in asymptomatic participants, and it also cost-effective. Ultrasonography has a sensitivity of 60–94% and specificity of 88–95% [46]. In our study, we assessed the relationship between CRP and NAFLD and analyzed multiple logistic regressions for potential risk factors to NAFLD.


  Conclusion Top


In this study, we established dyslipidemia, obesity, and CRP positivity as independent risk factors for NAFLD in asymptomatic nondiabetic South Indian participants. We need long-term follow-up studies from India on patients with NAFLD to understand the temporal evolution of NAFLD, metabolic syndrome, and coronary artery disease in our population. From our results, we suggest that every asymptomatic participant older than 40 years should undergo ultrasonography screening. Further studies should explore these findings.

Acknowledgements

The authors are grateful to Dr G.S. Rao, Managing Director, and Dr A. Lingaiah, Director of Medical Services Yashoda Group of Hospitals for their support to carry out this study in Yashoda Hospital, Hyderabad.

VCS Srinivasarao Bandaru was involved in data collection and manuscript writing; Jaydip R. Chaudhury in manuscript review and data analysis; Palle L. Reddy in manuscript writing and interpretation of data; Somala N. Reddy in data collection and statistical analysis; Pradeep K. Misra in manuscript review and data collection; Banda Balaraju in manuscript review and interpretation of data; and Kandadai R. Mridula in study design, manuscript preparation, data review, manuscript review, and statistical analysis. All authors have read the manuscript and approved it for submission.

This study was funded by Yashoda Research Foundation, Hyderabad, India.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Kalra S, Vithalani M, Gulati G, Kulkarni CM, Kadam Y, Pallivathukkal J et al. Study of prevalence of nonalcoholic fatty liver disease (NAFLD) in type 2 diabetes patients in India (SPRINT). J Assoc Physicians India 2013; 61:448–453.  Back to cited text no. 1
    
2.
Suzuki A, Angulo P, Lymp J, St Sauver J, Muto A, Okada T et al. Chronological development of elevated aminotransferases in a nonalcoholic population. Hepatology 2005; 41:64–71.  Back to cited text no. 2
    
3.
Amarapurkar DN, Hashimoto E, Lesmana LA, Sollano JD, Chen PJ, Goh KL. How common is non-alcoholic fatty liver disease in the Asia-Pacific region and are there local differences? J Gastroenterol Hepatol 2007; 22:788–793.  Back to cited text no. 3
    
4.
Bellentani S, Scaglioni F, Marino M, Bedogni G. Epidemiology of non-alcoholic fatty liver disease. Dig Dis 2010; 28:155–161.  Back to cited text no. 4
    
5.
Duseja A. Nonalcoholic fatty liver disease in India − a lot done, yet more required. Indian J Gastroenterol 2010; 29:217–225.  Back to cited text no. 5
    
6.
Uchil D, Pipalia D, Chawla M, Patel R, Maniar S, Narayani et al. Non-alcoholic fatty liver disease (NAFLD) − the hepatic component of metabolic syndrome. J Assoc Physicians India 2009; 57:201–204.  Back to cited text no. 6
    
7.
Bacon BR, Farahvash MJ, Janney CG, Neuschwander-Tetri BA. Nonalcoholic steatohepatitis: an expanded clinical entity. Gastroenterology 1994; 107:1103–1109.  Back to cited text no. 7
    
8.
Mahaling DU, Basavaraj MM, Bika AJ. Comparison of lipid profile in different grades of non-alcoholic fatty liver disease diagnosed on ultrasound. Asian Pac J Trop Biomed 2013; 3:907–912.  Back to cited text no. 8
    
9.
Chaudhuri JR, Mridula KR, Anamika A, Boddu DB, Misra PK, Lingaiah A et al. Deficiency of 25-hydroxyvitamin D and dyslipidemia in Indian subjects. J Lipids 2013; 2013:623420.  Back to cited text no. 9
    
10.
Chaudhuri JR, Mridula KR, Keerthi AS, Prakasham PS, Balaraju B, Bandaru VC. Association between Chlamydia pneumoniae and migraine: a study from a tertiary center in India. J Oral Facial Pain Headache 2016; 30:150–155.  Back to cited text no. 10
    
11.
Omagari K, Kadokawa Y, Masuda J, Egawa I, Sawa T, Hazama H et al. Fatty liver in non-alcoholic non-overweight Japanese adults: incidence and clinical characteristics. J Gastroenterol Hepatol 2002; 17:1098–1105.  Back to cited text no. 11
    
12.
Lin YC, Lo HM, Chen JD. Sonographic fatty liver, overweight and ischemic heart disease. World J Gastroenterol 2005; 11:4838–4842.  Back to cited text no. 12
    
13.
Lizardi-Cervera J, Laparra DI, Chavez-Tapia NC, Ostos ME, Esquivel MU. Prevalence of NAFLD and metabolic syndrome in asymtomatics subjects. Rev Gastroenterol Mex 2006; 71:453–459.  Back to cited text no. 13
    
14.
Zelber-Sagi S, Nitzan-Kaluski D, Halpern Z, Oren R. Prevalence of primary non-alcoholic fatty liver disease in a population-based study and its association with biochemical and anthropometric measures. Liver Int 2006; 26:856–863.  Back to cited text no. 14
    
15.
Radu C, Grigorescu M, Crisan D, Lupsor M, Constantin D, Dina L. Prevalence and associated risk factors of non-alcoholic fatty liver disease in hospitalized patients. J Gastrointestin Liver Dis 2008; 17:255–260.  Back to cited text no. 15
    
16.
Bedogni G, Miglioli L, Masutti F, Tiribelli C, Marchesini G, Bellentani S. Prevalence of and risk factors for nonalcoholic fatty liver disease: the Dionysos Nutrition and Liver Study. Hepatology 2005; 42:44–52.  Back to cited text no. 16
    
17.
Browning JD, Szczepaniak LS, Dobbins R, Nuremberg P, Horton JD, Cohen JC et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 2004; 40:1387–1395.  Back to cited text no. 17
    
18.
Caldwell SH, Ikura Y, Iezzoni JC, Liu Z. Has natural selection in human populations produced two types of metabolic syndrome (with and without fatty liver)? J Gastroenterol Hepatol 2007; 22(Suppl 1):S11–S19.  Back to cited text no. 18
    
19.
Amarapurkar DN, Amarapurkar AD. Nonalocholic steatohepatitis:clinicopathologic profile. J Assoc Physicians India 2000; 48:311–313.  Back to cited text no. 19
    
20.
Kim IH, Kisseleva T, Brenner DA. Aging and liver disease. Curr Opin Gastroenterol 2015; 31:184–191.  Back to cited text no. 20
    
21.
Cotrim HP, Parise ER, Oliveira CP, Leite N, Martinelli A, Galizzi J et al. Nonalcoholic fatty liver disease in Brazil: clinical and histological profile. Ann Hepatol 2011; 10:33–37.  Back to cited text no. 21
    
22.
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; 53:1020–1023.  Back to cited text no. 22
    
23.
Fallo F, Dalla PA, Sonino N, Lupia M, Tona F, Federspil G et al. Non-alcoholic fatty liver disease is associated with left ventricular diastolic dysfunction in essential hypertension. Nutr Metab Cardiovasc Dis 2009; 19:646–653.  Back to cited text no. 23
    
24.
Zein CO, Unalp A, Colvin R, Liu YC, McCullough AJ, Nonalcoholic Steatohepatitis Clinical Research Network. Smoking and severity of hepatic fibrosis in nonalcoholic fatty liver disease. J Hepatol 2011; 54:753–759.  Back to cited text no. 24
    
25.
Rivera CA. Risk factors and mechanisms of non-alcoholic steatohepatitis. Pathophysiology 2008; 15:109–114.  Back to cited text no. 25
    
26.
De Sousa TF, Nahas MV, Silva DA, del Duca GF, Peres MA. Factors associated with central obesity in adults from Florianópolis, Santa Catarina: a population based-study. Rev Bras Epidemiol 2011; 14:296–309.  Back to cited text no. 26
    
27.
Kim HJ, Kim HJ, Lee KE, Kim DJ, Kim SK, Ahn CW et al. Metabolic significance of nonalcoholic fatty liver disease in nonobese, nondiabetic adults. Arch Intern Med 2004; 164:2169–2175.  Back to cited text no. 27
    
28.
Bellentani S, Saccoccio G, Masutti F, Crocè LS, Brandi G, Sasso F et al. Prevalence of and risk factors for hepatic steatosis in NorthernItaly. Ann Intern Med 2000; 132:112–117.  Back to cited text no. 28
    
29.
Loria P, Carulli L, Bertolotti M, Lonardo A. Endocrine and liver interaction: the role of endocrine pathways in NASH. Nat Rev Gastroenterol Hepatol 2009; 6:236–247.  Back to cited text no. 29
    
30.
Prashanth M, Ganesh HK, Vima MV, John M, Bandgar T, Joshi SR et al. Prevalence of nonalcoholic fatty liver disease in patients with type 2 diabetes mellitus. J Assoc Physicians India 2009; 57:205–210.  Back to cited text no. 30
    
31.
Jali MV, Kambar S, Jali SM, Hiremath MB. Prevalence of non-alcoholic fatty liver disease among type-2 diabetes mellitus patients − a cross-sectional hospital based study. Al Ameen J Med Sci 2015; 8:50–54.  Back to cited text no. 31
    
32.
Agrawal R, Mishra S, Dixit VK, Rai S. Association of non-alcoholic fatty liver disorder with obesity. Indian J Prev Soc Med 2009; 40:126–129.  Back to cited text no. 32
    
33.
Marchesini G, Bugianesi E, Forlani G, Cerrelli F, Lenzi M, Manini R et al. Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology 2003; 37:917–923.  Back to cited text no. 33
    
34.
Duseja A, Das R, Nanda M, Das A, Garewal G, Chawla Y. Non alcoholic steatohepatitis in Asian Indians in neither associated with iron overload with HFE genemutations. World J Gastroenterol 2005; 11:393–395.  Back to cited text no. 34
    
35.
Nigam P, Bhatt SP, Misra A, Vaidya M, Dasgupta J, Chadha DS. Non-alcoholic fatty liver disease is closely associated with sub-clinical inflammation: a case-control study on Asian Indians in North India. PLoS ONE 2013; 8:e49286.  Back to cited text no. 35
    
36.
Amirkalali B, Poustchi H, Keyvani H, Khansari MR, Ajdarkosh H, Maadi M et al. Prevalence of non-alcoholic fatty liver disease and its predictors in north of Iran. Iran J Public Health 2014; 43:1275–1283.  Back to cited text no. 36
    
37.
Haukeland JW, Damås JK, Konopski Z, Loberg EM, Haaland T, Goverud I et al. Systemic inflammation in nonalcoholic fatty liver disease is characterized by elevated levels of CCL2. J Hepatol 2006; 44:1167–1174.  Back to cited text no. 37
    
38.
Oruc N, Ozutemiz O, Yuce G, Akarca US, Ersoz G, Gunsar F et al. Serum procalcitonin and CRP levels in non-alcoholic fatty liver disease: a case-control study. BMC Gastroenterol 2009; 9:16.  Back to cited text no. 38
    
39.
Chandalia M, Cabo-Chan AV Jr, Devaraj S, Jialal I, Grundy SM et al. Elevated plasma high-sensitivity C-reactive protein concentrations in Asian Indians living in the United States. J Clin Endocrinol Metab 2003; 88:3773–3776.  Back to cited text no. 39
    
40.
Park SH, Kim BI, Yun JW, Kim JW, Park DI, Cho YK et al. Insulin resistance and C-reactive protein as independent risk factors for non-alcoholic fatty liver disease in non-obese Asian men. J Gastroenterol Hepatol 2005; 19:694–698.  Back to cited text no. 40
    
41.
Assy N, Schlesinger S, Hussein O. Elevated plasma protein C correlates with the presence of fatty liver. Gut 2005; 54:729.  Back to cited text no. 41
    
42.
Syn WK, Nightingale P, Bateman JM. Non-alcoholic fatty liver disease in a district general hospital: clinical presentation and risk factors. Hepatol Int 2008; 2:190–195.  Back to cited text no. 42
    
43.
Taseer IH, Hussain L, Safdar S, Mirbahar AM, Ahmad I. Frequency of non-alcoholic fatty liver disease (NAFLD) and its biochemical derangements in type 2 diabetic patients. Pak J Med Sci 2009; 25:817–820.  Back to cited text no. 43
    
44.
Saxena T, Arya A, Rathore AJ, Rajak N, Naz S, Shah R. GGT and SGPT − a rising marker in diagnosis of non-alcoholic fatty liver disease. Biomed Pharmacol J 2014; 7:277–280.  Back to cited text no. 44
    
45.
Wang J, Li P, Jiang Z, Yang Q, Mi Y, Liu Y et al. Diagnostic value of alcoholic liver disease (ALD)/nonalcoholic fatty liver disease (NAFLD) index combined with γ-glutamyl transferase in differentiating ALD and NAFLD. Korean J Intern Med 2016; 31:479–487.  Back to cited text no. 45
    
46.
Joy D, Thava VR, Scot BB. Diagnosis of fatty liver disease: is biopsy necessary?. Eur J Gastroenterol Hepatol 2003; 15:539–543.  Back to cited text no. 46
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

Top
 
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

 
  In this article
Abstract
Introduction
Participants and...
Results
Discussion
Conclusion
References
Article Tables

 Article Access Statistics
    Viewed226    
    Printed20    
    Emailed0    
    PDF Downloaded43    
    Comments [Add]    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]