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Int. J. Mol. Sci. 2013, 14, 19782-19791; doi:10.3390/ijms141019782 OPEN ACCESS

International Journal of

Molecular Sciences ISSN 1422-0067 www.mdpi.com/journal/ijms Article

Relationship between Serum Osteocalcin Levels and Non-Alcoholic Fatty Liver Disease in Adult Males, South China Jun-Jie Liu 1, Yuan-Yuan Chen 1, Zeng-Nan Mo 2,3, Gui-Xiang Tian 1, Ai-Hua Tan 4, Yong Gao 2, Xiao-Bo Yang 5, Hai-Ying Zhang 5 and Zhi-Xian Li 1,* 1

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Department of Ultrasound, First Affiliated Hospital of Guangxi Medical University, Nanning 530021, China; E-Mails: [email protected] (J.-J.L.); [email protected] (Y.-Y.C.); [email protected] (G.-X.T.) Center for Personalized and Genomic Medicine, Guangxi Medical University, Nanning 530021, China; E-Mails: [email protected] (Z.-N.M.); [email protected] (Y.G.) Institute of Urology and Nephrology, First Affiliated Hospital of Guangxi Medical University, Nanning 530021, China Center for Metabolic Disease and Diabetes, First Affiliated Hospital of Guangxi Medical University, Nanning 530021, China; E-Mail: [email protected] Department of occupational health and environmental health, school of public health of Guangxi Medical University, Nanning 530021, China; E-Mails: [email protected] (X.-B.Y.); [email protected] (H.-Y.Z.)

* Author to whom correspondence should be addressed; E-Mail: [email protected]; Tel./Fax: +86-771-5356706. Received: 31 July 2013; in revised form: 20 September 2013 / Accepted: 22 September 2013 / Published: 30 September 2013

Abstract: AIM: To determine serum osteocalcin levels in South Chinese males with non-alcoholic fatty liver disease (NAFLD) and to examine the relation between serum osteocalcin and NAFLD. METHODS: Data were collected from 1683 men attending the Fangchenggang Area Male Healthy and Examination Survey (FAMHES) from September 2009 to December 2009. Serum osteocalcin was measured with electrochemiluminescence immunoassay. An abdominal ultrasonographic examination for all individuals was performed by two experienced ultrasonographers. The associations of serum osteocalcin with NAFLD were evaluated. RESULTS: The levels of serum osteocalcin were lower in 364 NAFLD participants than in 1319 non-NAFLD participants (24.51 ± 1.38 ng/mL vs. 20.81 ± 1.33 ng/mL, p < 0.001). Serum osteocalin level was associated with the scale of NAFLD (r = −0.150, p < 0.01). Serum osteocalin level tended to decrease with the scale of

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NAFLD. Binary logistic regression analysis showed that decreased ORs for NAFLD were observed from the first to the fourth osteocalcin quartiles. CONCLUSIONS: Our findings suggest that a lower serum osteocalcin level is associated with the presence of NAFLD. Keywords: osteocalin; Insulin resistance; non-alcoholic fatty liver disease; ultrasonography

1. Introduction Non-alcoholic fatty liver disease (NAFLD) is a type of fatty liver disease when fat is deposited in the liver but not due to excessive alcohol use [1]. Some epidemiological surveys have showed that NAFLD has become a serious public health problem in China and even Asia [2–5]. To date, the mechanism of NAFLD is not fully understood. However, NAFLD is now considered to be a manifestation of metabolic syndrome (MetS) and it has been reported to relate to insulin resistance (IR) [6,7]. IR is almost a universal finding in NAFLD [8]. Osteocalcin, a hormone secreted by osteoblasts, can stimulate insulin expression in β-cells and protect animals from obesity and glucose intolerance [9]. Recent studies suggest that serum osteocalcin plays a key role in the pathogenesis of IR and energy expenditure [10,11]. Moreover, decreased serum osteocalcin levels have been reported in patients with metabolic syndrome [12]. Fernández-Real et al. thought that osteocalcin may play a role in the development of insulin resistance-associated fatty liver disease [13]. However, there are few studies that have explored the association between osteocalcin and NAFLD [14–16], which reported that in East Chinese men and Turkish patients, NAFLD patients were seen with a decreased serum osteocalcin level than in the controls. This prompted us to investigate the role of osteocalcin in the development of NAFLD. Therefore, we conducted a cross-sectional study to investigate serum osteocalcin levels in South Chinese males with abdominal ultrasonography proven NAFLD, and to examine the relation of serum osteocalin and NAFLD. 2. Results and Discussion Among 1683 individuals enrolled in this study, the prevalence of NAFLD was 21.74%. The characteristics of the participants were divided into non-NAFLD (n = 1319) and NAFLD (n = 364) groups shown in Table 1. Compared with participants in non-NAFLD group, those in NAFLD group had lower serum osteocalcin levels (p < 0.001) (Table 1). In non-NAFLD group, the mean of serum osteocalcin was 24.51 ng/mL with a SD of 1.38 ng/mL while in NAFLD group the mean of serum osteocalcin was 20.81 ng/mL with a SD of 1.33 ng/mL. All variables had statistical differences between these two groups (Table 1). Age-adjusted Spearman correlation coefficient between osteocalcin and variables was shown in Table 2. There was a statistical negative correlation between osteocalcin and WC, BMI, TC, LDL-C, glucose, TG and ALT after adjustment for age (all p < 0.001). However, there was no statistically significant correlation between osteocalcin and HDL-C (p = 0.437). The strongest correlation was observed between osteocalcin and BMI (r = −0.246). The important finding in our study was that

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serum osteocalcin levels were statistically associated with the scale of NAFLD after adjustment of age and physical activity. Osteocalcin showed a decreased trend with the scale (r = −0.150, p < 0.001). Table 1. Baseline characteristics of the subjects in non-NAFLD and non-alcoholic fatty liver disease (NAFLD) groups. Characteristic Age (years) Osteocalcin (ng/mL) WC (cm) BMI (kg/m2) ALT (U/L) Glucose (mmol/L) TC (mmol/L) TG (mmol/L) HDL-C (mmol/L) LDL-C (mmol/L) Physical activity (n, %) Low * Moderate * High *

Non-NAFLD (n = 1319) 36.69 ± 11.37 24.51 ± 1.38 77.74 ± 7.68 22.25 ± 2.67 36.90 ± 12.65 5.20 ± 0.82 5.60 ± 1.01 1.24 ± 0.92 1.43 ± 0.29 2.88 ± 0.79

NAFLD (n = 364) 40.52 ± 10.18 20.81 ± 1.33 89.29 ± 6.84 26.25 ± 2.74 48.82 ± 15.25 5.57 ± 1.30 6.05 ± 1.06 2.44 ± 1.40 1.30 ± 0.40 3.24 ± 0.78

p value