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��ࡱ�>��	tw����qrs�����������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������[�	���mbjbj����	7zΐΐ3�+��������	�	��SSS����ggg8��<g�jp�:///LiNiNiNiNiNiNi$	m��o:ri�Sw{ri��//HSj000��/8/Li0Li00H(i�;�J/�����h�Q��g�,�4I8iij0�jNI��oI/p�o4�J�J�oS�O`0riri�/X�j���������������������������������������������������������������������o�		�:	Vitamin D deficiency in relation to insulin resistance associated with nonalcoholic fatty liver disease among Bangladeshi prediabetic subjects
Israt A Hossain1, Mijanur R Shah2, Sayela Afroz3, Liaquat Ali1 
Running title: Hypovitaminosis D in prediabetic NAFLD 
1Department of Biochemistry and Cell Biology, Bangladesh University of Health Sciences, Dhaka, Bangladesh
2Department of Microbiology and Immunology, Bangabandhu Sheikh Mujib Medical University, Dhaka, Bangladesh
3Department of Biochemistry and Molecular Biology, Rajshahi University, Rajshahi, Bangladesh 
*Corresponding author:
Israt A Hossain, Department of Biochemistry and Cell Biology, Bangladesh University of Health Sciences, Dhaka, Bangladesh. Email:  HYPERLINK "mailto:israt.ru84@buhs.ac.bd" israt.ru84@buhs.ac.bd, Tel: +88-02-9010654, Fax: +88-02-8055312.
Abstract
Objectives: The present study was aimed to examine the association of hypovitaminosis D with nonalcoholic fatty liver disease (NAFLD) with concomitant prediabetes and to explore whether this association is mediated by insulin resistance during this disorder.
Methods: We studied 151 prediabetic subjects consisting of 55 impaired fasting glycemia (IFG) and 96 impaired glucose tolerance (IGT) who came in Bangladesh Institute of Health Sciences General Hospital, Dhaka, Bangladesh to diagnose their metabolic evaluation from April 2012 to June 2013. Prediabetes was confirmed by 2-sample OGTT based on WHO Group Study Criteria. NAFLD was examined by upper abdomen ultrasonography comprising into non NAFLD (n = 84; M/F, 47/37) and NAFLD (n = 67; M/F, 38/29) groups. Serum insulin and 25-hydroxyvitamin D [25(OH)D] were analyzed by ELISA. Insulin resistance (HOMA-IR) was calculated by the homeostasis model assessment.
Results: Compared to the non NAFLD counterparts, NAFLD subjects had significantly lower levels of [25(OH)D] (P < 0.001) as well as significantly higher levels of HOMA-IR (P < 0.001). On binary logistic regression analysis, HOMA-IR (OR: 2.103, 95% CI: 1.011-4.376, P = 0.047) and [25(OH)D] (0.897, 0.857-0.939, P < 0.001) were found to be significant determinants of NAFLD when adjusted the major confounders of age, waist circumference, HbA1c, and triglyceride respectively. Pearson�s correlation analysis showed significant negative correlation of [25(OH)D] with HOMA-IR  in both NAFLD (r = -0.276, P = 0.032) and non NAFLD (r = -0.160, P = 0.049) subjects. Multiple linear regression analysis showed significant negative association of HOMA-IR with [25(OH)D] (� = -0.371, P = 0.001) in NAFLD subjects after adjusting potential cofounders of age, waist circumference, HbA1c and serum triglyceride respectively. 
Conclusions: Hypovitaminosis D seem to have an association with NAFLD and this relationship is mediated by insulin resistance which considered the pathophysiological determinant of prediabetes.
Keywords
NAFLD; 25-hydroxyvitamin D; Prediabetes; IFG; IGT; HOMA-IR; Metabolic Syndrome 
Introduction
Low levels of vitamin D synthesis occur due to impaired insulin action results in alteration of glucose and lipid metabolism. Recent studies revealed that vitamin D deficiency is strongly associated with features of insulin resistance relating to obesity, type 2 diabetes mellitus (T2DM) and metabolic syndrome (MetS) [1]. Prior epidemiological and interventional studies revealed that vitamin D supplementation reduces the free fatty acid induced insulin resistance in the peripheral tissues among subjects with baseline glucose intolerance [2,3]. A more recent mechanism reveals that low vitamin D reduces the lipolysis activity in the liver that may predispose to excessive accumulation of triglycerides within the hepatocytes leading to nonalcoholic fatty liver disease (NAFLD) [4].
	NAFLD is a clinicopathological condition caused by abnormal lipid metabolism due to impaired insulin signaling within the hepatocytes. It is a consequence of insulin resistance that enhances the excessive accumulation of triglyceride originated from peripheral FFAs via denovolipogenesis or dietary sources in the liver. In a secondary event, oxidative stress occurs due to mitochondrial dysfunction and inflammation leading to hepatocellular damage. These two pathogenic mechanisms are closely linked to vitamin D deficiency because of its anti-inflammatory, antiproliferative and anti-fibrotic activities in the liver [5]. The insulin-sensitizing action of vitamin D exerts its function by binding to its specific receptor VDR expressed in a wide range of insulin sensitizing tissues and are involved in cell proliferation, differentiation, immune modulation, and apoptosis. 
	A recent meta-analysis on NAFLD subjects suggests that decreased serum [25(OH)D] concentrations are strongly associated with NAFLD emerging 26% of these subjects are in a condition of hypovitaminosis D thereby stratifying its pathogenic role in the development of NAFLD [6]. Another clinical study on 607 NAFLD cases evaluates the association of serum [25(OH)D] levels with increased severity of ultrasound detected NAFLD suggesting its relationship with concomitant progression to liver injury [7]. Conversely, a clinical study from Chinese adults after abdominal ultrasound examination found no significant association of vitamin D deficiency with NAFLD [8]. In the same line, another clinical perspective including young adolescent with NAFLD did not find any independent association of hypovitaminosis D with NAFLD based on the elevation of ALT levels after adjustment of obesity [9]. However, the differences of the results between the associations of vitamin D with varying degrees of NAFLD in different studies based on a number of intervening factors such as races, geography, environmental factors and the VDR allelic variation. 
	Research demonstrated NAFLD that affects 10-24% of the general population from different countries and recognized increasingly as a major cause of liver related morbidity and mortality [6]. Numerous studies have been identified relating the possible effect of [25(OH)D] deficiency in the development of NAFLD and T2DM [2,10]. Nevertheless, very limited data are in a range of prediabetes- an earlier state of type 2 diabetes where insulin resistance considered as a common detriment of the disorder. Since vitamin D plays important role in the reduction of insulin resistance in hepatocytes exerting its inhibitory action in the development of NAFLD/NASH, glucose intolerance, and their metabolic consequences. In this context, the present study has been undertaken to investigate the levels of [25(OH)D]  in NAFLD who are prediabetes and to explore whether this association is mediated by insulin resistance during this disorder.
Materials and Methods
Study design and subjects 
In this cross-sectional study, we investigated 151 (one hundred and fifty one) consecutive prediabetic subjects consisting of 55 impaired fasting glycemia (IFG) and 96 impaired glucose tolerance (IGT) who came in Bangladesh Institute of Health Sciences General Hospital, Dhaka, Bangladesh to diagnose their metabolic evaluation from April 2012 to June 2013. Diabetes and prediabetes were diagnosed following WHO Group Study criteria [11] and after upper abdomen ultrasonographic examination, the prediabetic subjects is further divided into non NAFLD (n = 84) and NAFLD (n = 67) groups. Subjects suffering from concomitant acute and chronic diseases of hepatic, cardiac, renal, and respiratory systems, history of alcohol addiction, cancer, stroke, type 1 diabetes, autoimmune liver disease, presence of hepatitis B surface antigen and hepatitis C virus, any type of malignancy, intake of glucose and lipid lowering drugs, vitamin and mineral supplementation that known to influence vitamin D status and pregnant subjects were excluded from the study. Anthropometric measurements including waist and hip circumference (WC and HC), weight, height and clinical measures (systolic and diastolic blood pressure) were recorded by standard procedures. Body mass index (BMI) was calculated as weight (kg) divided by height (m) squared. Prior enrollment, each participant provided written informed consent where they were thoroughly appraised about nature, purpose, and implications of the study. The study protocol was approved by the local ethics committee (BADAS, ref no: BADAS-ERC/13/00106).
Sample collection 
After overnight fasting (8-10 hours), a total of ~6.00 ml blood sample was obtained by venipuncture of the participants following standard procedure. Subjects were then allowed to drink glucose (75 g in 300 ml of water) and requested not to take any food and be rested for two hours. After 2 hours of glucose intake, the second draw of a blood sample (~3.00 ml venous blood) was taken. Fasting and postprandial blood samples were taken into the plain tube (~6 cc), allowed to clot for 30 minutes and serum was separated by centrifugation for 10 min at 3000 rpm and collected at least 600 �l in each of the three aliquots. Blood samples were maintained at 40c until separation and serum were frozen at -300c within an hour of sample collection. One aliquot was used for measuring fasting serum glucose, lipid profile, liver enzymes, total calcium, creatinine, second aliquot for postprandial serum glucose and serum insulin, third aliquot for fasting serum insulin, high-sensitivity C-reactive protein (hsCRP) and [25(OH)D] measurement respectively. Whole blood (~2 ml) was taken in a 2 mg/ml EDTA vial for measurement of HbA1c. Serum was not allowed to be thawed until the assay is performed.
Biochemical measurements 
Fasting and postprandial serum glucose were measured by the glucose-oxidase method, total cholesterol, triglyceride, and HDL-cholesterol, alanine aminotransferase, aspartate aminotransferase, gamma-glutamyl transferase and alkaline phosphatase were measured by enzymatic colorimetric method and total calcium by O-Cresolphthalein Complexone/Colorimetric method using a conventional automated analyzer (Dimension RxL clinical chemistry system, Siemens Healthcare Diagnostics Inc. USA). LDL-cholesterol was calculated by the Friedewald equation [12] and HbA1c was measured by the HPLC technique, using an autoanalyzer (Bio-Rad Variant, Hercules, CA, USA). Serum insulin, hsCRP and [25(OH)D] were quantified using commercial ELISA kits (DRG International, Inc., USA) and their optical density was measured by ELISA plate reader (MultiskanTM FC Microplate Photometer, Thermo Scientific, USA). When considering the precision of laboratory performances the intra- and inter-assay %CV for serum insulin was 5.4% and 6.7% and for [25(OH)D] the values were 5.7% and 7.1% respectively. Insulin secretory function (HOMA%B) and insulin sensitivity (HOMA%S) was calculated by homeostasis model assessment (HOMA) taking values of fasting serum glucose and fasting serum insulin. An index of insulin resistance was calculated according to the homeostatic model assessment of insulin resistance (HOMA-IR) formula: HOMA-IR = (fasting insulin (�IU/ml) � fasting glucose (mmol/l)) / 22.5 [13]. Total body fat was determined by bioimpedometry. 
NAFLD evaluation 
The ultrasonographic examination of the liver was performed by a well-trained radiologist who was masked about the aims of the study and unaware the clinical characteristics and laboratory test values of the participants using a 3.5 MHz linear transducer (Philips Ultrasound-Ay-MNT-15 TTK, HDI-4000, Netherland) sonogram machine. The presence of NAFLD was confirmed by the degree of fatty liver in the absence of alcohol intake. The grading and staging of NAFLD was classified by using a semiquantitative point scale based on standard ultrasonographic criteria as Grade 0: normal liver echo-texture; Grade 1 (mild steatosis): slightly increased echoes in the liver parenchyma where the diaphragm and vessel borders within the hepatocytes is visualized; Grade 2 (moderate steatosis): slightly increased liver echoes with partial visualization of the diaphragm and vessel borders; Grade 3 (severe steatosis): marked increased liver echoes with no visualization of the diaphragm and vessel borders and heavy posterior attenuation [14].
Assessment of noninvasive markers of NAFLD 
We calculated several surrogate noninvasive indicators of liver steatosis to identify subjects with liver related morbidity and mortality. This included fatty liver index (FLI) [15] =  [e 0.953�loge (TG)+0.139�BMI+0.718�loge (GGT)+0.053�waistcircumference-15.745)]/[1+e 0.953�loge (TG)+0.139�BMI+0.718�loge  (GGT)+0.053�waist circumference�15.745]�100- with a cut-off value < 30 as normal and > 30 as moderate and e" 60 as severe steatosis, hepatic steatosis index (HSI) [16] = 8 x ALT/AST ratio + BMI + 2 (if diabetic) + 2 (if female)- with a cut-off value of 36, NAFLD fibrosis score (NFS) [17] = [-1.675 + 0.037 � age (years) + 0.094 � BMI (kg/m2) + 1.13 � IFG/diabetes (yes = 1, no = 0) + 0.99 � AST/ALT ratio � 0.013 � platelet (�109/L) � 0.66 � albumin (g/dL)]-with a cut-off value of NFS > 0.676 as advanced fibrosis, fibrosis4 (FIB4) score [18] = (Age � AST)/(PLT � "ALT)- with a cut-off value of FIB4 score >2.67 as advanced fibrosis, BARD score [19] = 1 (if BMI > 28) + 2 (if AST/ALT ratio > 0.8) + 1 (if diabetic)- with a cut-off value of BARD score is e" 2 points, it is regarded as significant fibrosis, and BAAT score [20] = BMI e" 28 -1 point+ Age e" 50 -1 point+ ALT e" 2 � ULN -1 point+ TG e" 150 mg/dl-1 point- with a cut-off value of point e" 2 is regarded as significant fibrosis.
Definition of metabolic syndrome (MetS) 
The presence of MetS among the study participants was assessed according to the revised criteria of National Cholesterol Education Program Adult Treatment Panel III (NCEP ATP III) for Asians in a modified form with the presence of three or more of the following risk factor [21]: 
1. WC e" 90 cm for males and e" 80 cm for females; 
2. Systolic blood pressure e" 130 mmHg or diastolic blood pressure e" 85 mmHg or antihypertensive medication; 
3. Fasting plasma glucose e" 5.6 mmol/l or on medication for high blood glucose; 
4. HDL-cholesterol < 40 mg/dl for males and < 50 mg/dl for females; 
5. Triglycerides e" 150 mg/dl
Statistical analysis 
Statistical package for the social sciences (SPSS) for windows version 17.0 was used for all statistical analysis (SPSS Inc., Chicago, IL, USA). Data with normal distribution were expressed as mean � SD and an absolute number (percentages) where appropriate and their comparison between two independent groups was done using Student�s unpaired t-test. Binary logistic regression analysis was carried out considering group (NAFLD and non NAFLD as reference) as dependent variable and age, waist circumference, HbA1c, serum triglyceride, HOMA-IR and [25(OH)D] as independent variables to assess significant predictors and adjusted OR estimated by controlling the above significant predictors of NAFLD. The relationship of [25(OH)D] with significant variables of the study subjects was evaluated by bivariate Pearson�s correlation testing. Multiple linear regression analysis was done to see the independent association between HOMA-IR and [25(OH)D] in NAFLD subjects considering HOMA-IR as the dependent variable and age, waist circumference, HbA1c, serum triglyceride and [25(OH)D] as the independent variables. To see the levels [25(OH)D], HOMA-IR, other insulinemic indices and noninvasive markers among different grades of NAFLD was performed by ANOVA. Regression curve analysis was performed to see the relationship of [25(OH)D] and HOMA-IR  with noninvasive markers among different grades of NAFLD. The relationship between serum [25(OH)D] and HOMA-IR levels with noninvasive markers among different grades of NAFLD was performed by regression curve analysis. The sample size was calculated by using the regression model for individual predictors and it depends on the desired power (l- �), significance level (�), the number of predictors and the expected effect sizes. Sampling weights were used by using the formula of n e" 50 + 8 m, where m is the number of independent variables (IVs) for testing the multiple correlation and n > 104 + m for testing IVs. In our study there was six IVs (Table 3) and the calculated sample number was 50 + 8 (6) = 98 cases and 104 + 6 = 110 cases for testing IVs. These calculations were based on significance level of 5% (� = 0.05) and 80% power (P = 0.20) [22]. A P value less than 0.05 was considered statistically significant. 
RESULTS
Characteristics of the study subjects 
The general characteristics of the prediabetic subjects are shown in Table 1. Age was significantly higher in IFG group compared to the IGT group (P = 0.001). Compared to the IGT counterparts, IFG subjects had significantly lower levels of postprandial serum insulin (P < 0.001) and HOMA%B (P < 0.001) and alanine aminotransferase (P = 0.012). 
Characteristics of the prediabetic subjects after liver ultrasonography 
The sociodemographic, anthropometric, clinical and biochemical characteristics of the prediabetic subjects according to their fatty liver group are presented in Table 2. The NAFLD subjects were 79.1% (n = 53), 16.4% (n = 11) and 4.5% (n = 3) in the group of grade 1, grade 2 and grade 3 respectively. Based on prediabetes, the NAFLD group had 32.8% (n = 22) IFG and 67.2% (n = 45) IGT while, the non NAFLD group had 39.3% (n = 33) IFG and 60.7% (n = 51) IGT. The MetS was 57.1% (n = 48) in non NAFLD group and 77.6% (n = 52) was in NAFLD group and the presence of MetS was significantly higher in NAFLD subjects compared to the non NAFLD counterparts (P < 0.001). Compared to their non NAFLD counterparts, NAFLD subjects had significantly higher levels of waist to hip ratio (P = 0.026), systolic and diastolic blood pressure (P = 0.004 and P = 0.004), total cholesterol (P = 0.015), triglyceride (P = 0.010), gamma-glutamyl transferase (P = 0.001), aspartate aminotransferase (P = 0.024), hsCRP (P < 0.001), fasting serum insulin (P = 0.001), postprandial serum insulin (P < 0.001), HOMA%B (P = 0.003), HOMA-IR (P = 0.001), fatty liver index (P < 0.001), BARD score (P < 0.001) and NAFLD fibrosis score (P < 0.001) whereas, they had significantly lower levels of HDL-cholesterol (P = 0.047), HOMA%S (P = 0.049) and [25(OH)D] (P < 0.001) respectively.
Levels of [25(OH)D] and HOMA-IR in different grades of NAFLD 
Compared to grade 0 group, [25(OH)D] was significantly lower in grade 1, grade 2 and grade 3  subjects (42.05 � 14.7 vs. 31.18 � 8.88, 27.50 � 8.36, 27.60 � 2.29). However, compared to the grade 0 group, HOMA-IR was increased concomitantly with increasing the severity of NAFLD (1.80 � 0.51 vs. 2.27 � 1.12, 2.15 � 0.69, 2.35 � 1.34) (Figure 1). 
Association of [25(OH)D] and HOMA-IR with NAFLD 
To evaluate the contribution of [25(OH)D] and HOMA-IR on NAFLD group taking non NAFLD as a reference after adjusting the effects of major confounders are shown in Table 3. In binary logistic regression analysis, [25(OH)D] (OR 0.897, 95% CI 0.857-0.939, P < 0.001) and HOMA-IR (OR 2.103, 95% CI 1.011-4.376, P = 0.047) were found to be significant determinants of NAFLD after adjusting the effects of age, waist circumference, HbA1C and triglyceride respectively. 
Correlation of [25(OH)D] with significant variables of HOMA-IR in NAFLD subjects 
Bivariate Pearson�s correlation analysis showed significant negative correlation of [25(OH)D] with weight (r = -0.284, P = 0.020), BMI (r = -0.435, P < 0.001), HbA1C (r = -0.326, P = 0.007), fasting serum insulin (r = -0.259, P = 0.034), hepatic steatosis index (r = -0.364, P = 0.002) and HOMA-IR (r = -0.262, P = 0.032) as well as significant positive correlation with HOMA%S (r = 0.284, P = 0.020) in NAFLD subjects (Table 4). On regression analysis, [25(OH)D] showed significant negative correlation with fatty liver index, hepatic steatosis index, BARD score, NAFLD fibrosis score and fibrosis4 score in grade 0 subjects however, in grade 1 subjects, it showed significant negative correlation with fatty liver index and hepatic steatosis index while, positive correlation with fibrosis4 score (Figure 2). Conversely, HOMA-IR showed significant positive correlation with fatty liver index and hepatic steatosis index in grade 0 and grade 1 subjects whereas, it only showed significant positive correlation with fibrosis4 score in grade 0 subjects (Figure 3). 
Independent association of HOMA-IR with [25(OH)D] levels in NAFLD subjects 
To explore the association of HOMA-IR with [25(OH)D] among NAFLD subjects after adjusting the effects of pertinent variables considering HOMA-IR as dependent and age, waist circumference, HbA1C, triglyceride and [25(OH)D] as independent variables are demonstrated in Table 5. In NAFLD subjects, multiple linear regression analysis showed a significant negative association of HOMA-IR with [25(OH)D] (� = -0.371, P = 0.001) after adjusting the effects of age, waist circumference, HbA1C, and triglyceride respectively. 
Discussion
This study demonstrates that prediabetic individuals with NAFLD have reduced levels of [25(OH)D] as compared to the non NAFLD subjects. A number of clinical studies revealed the association of vitamin D deficiency with NAFLD and other metabolic disorders in a different population [10,23]. Prior epidemiological evidence proposed the role of [25(OH)D] deficiency in the pathogenesis of NAFLD and suggested the clinical utility of [25(OH)D] supplement in the treatment and management of NAFLD, which is also related to type 2 diabetes, obesity and insulin resistance [23]. In accordance with our results, recently published data of a meta-analysis by Eliades et al. studied on U.S. adults in an integrated healthcare delivery system using the database of PubMed and EMBASE. In this analysis, they used seventeen cross-sectional and case-control studies of NAFLD subjects after confirmed by liver biopsy, CT scan and based on elevated liver enzymes and found a linking relationship of vitamin D deficiency with the consequence of NAFLD development. They conclude that NAFLD patients were 1.26 times more likely to be [25(OH)D] deficient suggesting its role in the development and progression to NAFLD [6]. In the same line by Kucukazman et al. studied on 211 consecutive Turkish subjects to examine the presence of NAFLD after liver ultrasonography and its association with [25(OH)D] status. This study demonstrated a lower serum [25(OH)D] levels in NAFLD subjects compared to without NAFLD [24]. Accordingly, study on Korean Cohort of healthy adult men by HYPERLINK "http://www.ncbi.nlm.nih.gov/pubmed/?term=Rhee%20EJ%5BAuthor%5D&cauthor=true&cauthor_uid=23411507"Rhee et al. found a reduced risk of NAFLD among subjects with higher tertiles of 25 (OH)D3 compared to the lower 25 (OH)D3 groups independent of obesity and MetS. In this cross-sectional study, they found a higher prevalence of NAFLD (43.6%) among the study participants after confirmed by abdominal ultrasonogram [25]. Furthermore, in a cross-sectional study by HYPERLINK "http://www.ncbi.nlm.nih.gov/pubmed/?term=Barchetta%20I%5BAuthor%5D&cauthor=true&cauthor_uid=21749681"Barchetta et al. on 262 consecutive subjects where NAFLD was confirmed by upper abdomen ultrasonogram (US) with persistent normal liver enzymes and various degrees of insulin resistance and related metabolic disorders and found a direct association of hypovitaminosis D in subjects with NAFLD. They showed significant reduction of serum [25(OH)D] levels in NAFLD subjects compared to without NAFLD subjects and reported that low [25(OH)D] levels are associated with the presence of NAFLD independent of MetS, type 2 diabetes and insulin resistance profile [26]. Apart from ultrasound scanning, a number of clinical studies after liver biopsy also revealed low plasma [25(OH)D] levels as a significant risk factor for the histopathological features of NAFLD [27,28]. In contrast, Jeong et al. performed a cross-sectional gender specific study including 558 Korean adults and found no significant association of vitamin D deficiency with the severity of US-NAFLD [29]. In accordance, another study by Ha et al. after using the noninvasive methods of NAFLD detection in a Cohort of 1812 Korean adults and found no significant association of vitamin D with NAFLD [30]. Accordingly, Li et al. in 1248 Chinese Cohort did not find any significant association of [25(OH)D] with abdominal ultrasound examined NAFLD subjects [8]. However, the inconsistency of the results and the median cut-off values of vitamin D in the previous studies vary due to a number of influencing factors (e.g. sun exposure behavior, culture behavior, lifestyle, diet, aging, skin pigmentation, and laboratory methods of vitamin D measurement respectively).
	Following the Prospective study, Darasathy et al. performed an observational study on biopsy proven NAFLD subjects with baseline hypovitaminosis D who after treatment with a daily dose of 2000 IU vitamin D3 for 6 months and did not find any improvement of vitamin D status among the study participants [31]. In the same line by Barchetta et al. performed a randomized clinical trial (RCT) on the US detected NAFLD subjects over 4 weeks with a daily dose of 2000 IU vitamin D3 and at the endpoint, they observed no significant improvement in NASH or other metabolic disorders [32]. Another RCT observed by Sharif et al. and found no improvements in terms of liver enzymes, oxidative stress and inflammation among the US detected NAFLD subjects after treatment with vitamin D3 for 4 months [33].
	It is clearly evident that NAFLD is a multifactorial disease where insulin resistance considered as a key factor in its pathogenesis. In our settings, we found a significantly higher level of insulin resistance in NAFLD subjects compared to the non NAFLD counterparts. Our study data also reveals a significantly higher level of postprandial serum insulin, HOMA%B as well as a significantly lower level of HOMA%S among the NAFLD subjects. Accumulating evidence suggest that NAFLD is significantly associated with reduced insulin sensitivity due to impaired insulin signaling [6]. In our study, we found a lower level of HOMA-IR and [25(OH)D] in IFG subjects compared to IGT counterparts which are in line with a cross-sectional study of 542 Arab Americans by Pinelli et al. and showed significant association of hypovitaminosis D with insulin resistance, components of the metabolic syndrome, and glucose intolerance in men suggesting the status of  vitamin D deficiency among varying degrees of glycemic levels [34]. In contrary, a meta-analysis from randomized controlled trials revealed no beneficial effect of vitamin D supplementation in patients with impaired fasting glucose and impaired glucose tolerance or insulin resistance [16]. 
	To explore the relationship of [25(OH)D] with different grades of fatty liver we found a significant decrease of [25(OH)D] concomitantly with increasing the various steps of disease progression and fatty liver severity. This finding is in agreement with Targher et al. who found circulating [25(OH)D] was reduced in biopsy proven NAFLD adults with increasing histological severity, independent of any metabolic abnormalities [28]. In contrast, Patel et al. investigated on biopsy proven NAFLD Cohort and found no significant association of vitamin D deficiency and its related genes expressed in the hepatocytes with increasing histological severity of NAFLD [35].
	Our binary logistic regression analysis showed a strong association between [25(OH)D] and HOMA-IR with NAFLD after adjusting the pertinent confounders. Prior studies revealed the insulin-sensitizing action of [25(OH)D] suggesting its role in glucose and lipid metabolism [26,34]. In Pearson�s correlation analysis, we found a significant negative correlation of [25(OH)D] with HOMA-IR as well as a significant positive correlation with HOMA%S in NAFLD subjects. This is in line with Pirgon et al. where the NAFLD adolescent subjects were stratified into an obese and lean group and found a significant negative correlation of [25(OH)D] with HOMA-IR among the obese NAFLD subjects stratifying the potential role of vitamin D against the insulin resistance syndrome [36]. 
	In accordance with the previous studies, we also evaluated noninvasive indicators to explore their relationship with different grades of NAFLD for prediction of liver complications where we found a significant negative correlation of [25(OH)D] with fatty liver index, hepatic steatosis index, BARD score, BAAT score, NAFLD fibrosis score, and fibrosis4 score in NAFLD subjects which are in line with other studies [9,26]. In accordance a cross-sectional study by Lee et al. who investigated over 10,000 Korean adults and found the sensitivity and specificity of HSI for detection of NAFLD was 93.1% and 92.4% respectively [16]. This study concludes the validation of HSI as an effective tool for screening of NAFLD that could recommend the subjects for liver ultrasonography or other measures to control the disease condition. In multiple linear regression analysis, we found a significant negative association of HOMA-IR with [25(OH)D] in NAFLD subjects after adjusting the effects of age, waist circumference, triglyceride, and HbA1c. This is in line with Barchetta et al. who showed an independent association of adiposity, glycemia, and HOMA-IR with NAFLD [26]. 
	Our study has several limitations. Firstly, NAFLD was confirmed by imaging technique of upper abdominal ultrasonography though, liver biopsy considered the gold standard method. Secondly, it was an analytical study with a cross-sectional design that limits its strength to find a causal association between [25(OH)D] and other interacting molecules of HOMA-IR with NAFLD.
Conclusions
In conclusion, we found significantly lower levels of [25(OH)D] among NAFLD individuals with persistent prediabetes. Hypovitaminosis D due to insulin resistance might have an independent role in the development of prediabetes and its subsequent progression to NAFLD. The data also indicate that vitamin D deficiency and insulin resistance are associated with each other and those, in turn, are affected by obesity and alteration of glucose metabolism in prediabetic subjects. Prospective studies with large sample size are warranted to evaluate the causal association between hypovitaminosis D and NAFLD among Bangladeshi prediabetic subjects.
Acknowledgements
The authors would like to thank all laboratory team members and volunteers, staffs of OPD of BIHS General Hospital for their cooperation and helping attitudes and for assisting the conduction of the study.
Disclosures
The authors declare that they have no conflict of interest associated with this paper.
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