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Reduced Scd36 Following Weight Loss Corresponds to Improved Insulin Sensitivity, Dyslipidemia and Liver Fat in Obese Children

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Reduced Scd36 Following Weight Loss Corresponds to Improved Insulin Sensitivity, Dyslipidemia and Liver Fat in Obese Children European Journal of Clinical Nutrition (2016) 70, 1073–1077 © 2016 Macmillan Publishers Limited, part of Springer Nature. All rights reserved 0954-3007/16 www.nature.com/ejcn ORIGINAL ARTICLE Reduced sCD36 following weight loss corresponds to improved insulin sensitivity, dyslipidemia and liver fat in obese children L Knøsgaard1, K Kazankov2, NH Birkebæk3, P Holland-Fischer3, A Lange3, J Solvig4, A Hørlyck4, K Kristensen3, S Rittig3, H Vilstrup2, H Grønbæk2 and A Handberg1,5 BACKGROUND/OBJECTIVES: Childhood obesity is a major health problem with serious long-term metabolic consequences. CD36 is important for the development of obesity-related complications among adults. We aimed to investigate circulating sCD36 during weight loss in childhood obesity and its associations with insulin resistance, dyslipidemia, hepatic fat accumulation and low-grade inflammation. SUBJECTS/METHODS: The impact of a 10-week weight loss camp for obese children (N = 113) on plasma sCD36 and further after a 12-month follow-up (N = 68) was investigated. Clinical and biochemical data were collected, and sCD36 was measured by an in- house assay. Liver fat was estimated by ultrasonography and insulin resistance by the homeostasis model assessment (HOMA-IR). RESULTS: Along with marked weight loss, sCD36 was reduced by 21% (P = 0.0013) following lifestyle intervention, and individual sCD36 reductions were significantly associated with the corresponding decreases in HOMA-IR, triglycerides and total cholesterol. The largest sCD36 decrease occurred among children who reduced HOMA-IR and liver fat. After 12 months of follow-up, sCD36 was increased (P = 0.014) and the metabolic improvements were largely lost. CONCLUSIONS: Weight-loss-induced sCD36 reduction, coincident with improved insulin resistance, circulating lipids and hepatic fat accumulation, proposes that sCD36 may be an early marker of long-term health risk associated with obesity-related complications. European Journal of Clinical Nutrition (2016) 70, 1073–1077; doi:10.1038/ejcn.2016.88; published online 8 June 2016 INTRODUCTION both adipocytes and macrophages in diet-induced obesity.16 Physical inactivity and unhealthy diet are major causes of Recently, a circulating non-cell-bound form of CD36 (sCD36) was 17,18 obesity.1,2 The threat to public health is particularly related to identified and proposed to reflect tissue CD36 expression. obesity-associated insulin resistance preceding type 2 diabetes Associations of sCD36 with insulin resistance, body mass index mellitus, as well as cardiovascular diseases, hepatic steatosis and (BMI), hepatic fat accumulation, obesity-driven low-grade inflam- certain cancers.2,3 Childhood obesity is a serious public health mation and bariatric surgery-induced weight loss and metabolic – problem, as fat accumulation in children and adolescents carries improvements have previously been reported.17,19 23 Further- an increased risk of premature metabolic complications.2–4 Intra- more, sCD36 is suggested to be a marker of lipid accumulation in abdominal visceral fat is a major contributor to obesity-related arterial walls.24 metabolic complications. High lipolytic activity results in increased Weight reduction, particularly if due to physical activity and portal-free fatty acid flow and possibly contributes to increased caloric restriction, improves insulin sensitivity, and thus reduces 25–27 ectopic hepatic fat accumulation.2,5 A state of low-grade metabolic complications of obesity in adults and children. As inflammation has an important role in obesity-related metabolic childhood obesity is a major health problem, leading to serious complications.6,7 A well-known hypothesis is that the enlargement long-term metabolic consequences, all aspects of these inap- of fat cells causes hypoxia, which leads to a pro-inflammatory propriate metabolic conditions need attention. In the present response, and thus may contribute to the low-grade inflammatory study, we aimed to investigate sCD36 in childhood obesity during condition related to obesity and its complications.8 lifestyle intervention and at follow-up, and in particular, to study The multifunctional membrane receptor CD36 is involved in sCD36 as a marker of obesity-induced insulin resistance, many biological processes.9 Besides scavenging of oxidized low- dyslipidemia, hepatic fat accumulation and low-grade inflamma- density lipoproteins (oxLDLs),9–11 CD36 has an important function tion. We hypothesized that sCD36 in childhood obesity is in the facilitation of fatty acid uptake. In case of fatty acid associated with measures of insulin resistance, dyslipidemia, overload, this uptake contributes to ectopic fat accumulation and hepatic fat accumulation and low-grade inflammation, and that insulin resistance, in muscle, fat and liver cells, respectively.12–15 weight loss along with metabolic improvements causes a In addition, CD36 is involved in the inflammatory responses in reduction in the circulating levels of sCD36. 1Department of Clinical Biochemistry, Aalborg University Hospital, Aalborg, Denmark; 2Department of Hepatology and Gastroenterology, Aarhus University Hospital, Aarhus, Denmark; 3Department of Pediatrics, Aarhus University Hospital, Aarhus, Denmark; 4Department of Radiology, Aarhus University Hospital, Aarhus, Denmark and 5Department of Clinical Medicine, Faculty of Medicine, Aalborg University, Aalborg, Denmark. Correspondence: Professor A Handberg, Department of Clinical Biochemistry, Aalborg University Hospital, Hobrovej 18-22, Aalborg, DK-9000, Denmark. E-mail: [email protected] Received 23 November 2015; revised 24 February 2016; accepted 24 April 2016; published online 8 June 2016 sCD36 is reduced by weight loss in obese children L Knøsgaard et al 1074 MATERIALS AND METHODS nonparametric Spearman's rank correlations test, and described by Study population and clinical examinations Spearman’s rho (ρ) and P-values. The change in sCD36 during intervention was related to corresponding changes in various parameters by repeated One hundred and thirteen children from a weight loss camp at the Danish measurements, determined as differences or ratios depending on visual Christmas Seal Home (Julemærkehjemmet, Hobro, Denmark) were testing with scatter plots and Bland–Altman plots. To assess differences in included in this study. The Danish Christmas Seal Home is an opportunity proportions, the χ2-test or Fisher’s exact test was used. Statistical analyses for overweight school children between 7 and 14 years of age, and the were two-sided and P-values ⩽ 0.05 considered statistically significant. All children are referred by their school physician and offered a 10-week stay analyses were performed using the statistical software package STATA free of charge. The main purpose of the program was weight loss. The version 12.0 (StataCorp LP, College Station, TX, USA). children attended regular school classes, were physically active for at least 1 h every day and followed a fixed diet plan with focus on reduced intake 28–30 of calories. This study population was previously described in details. RESULTS Of the original 117 participants, baseline plasma for sCD36 measurement was available in 113 participants. Anthropometrical and biochemical characteristics of the study Clinical examinations and fasting blood samples were obtained at population baseline (N = 113), after the 10-week stay at the Danish Christmas Seal The anthropometrical and biochemical data of the participating Home (N = 113) and after 12 months of follow-up (N = 68). Body mass index children are presented in Table 1. In brief, after 10 weeks of (BMI) and BMI-standard deviation score (BMI-SDS) were calculated. lifestyle intervention, the children obtained a significant weight Multifrequency electrical bioimpedance analysis (Quadscan 4000, Bodystat Ltd, Isle of Man, UK) was used to estimate body composition, particularly loss. They reduced BMI by 11%, BMI-SDS by 21%, body content of the amount of body fat. fat by 23% and waist circumference by 11%. Furthermore, insulin The study was approved by the Ethics Committee of Region Midtjylland resistance, estimated by HOMA-IR, decreased by 33%, and (1–10–72–114–15). Prior to inclusion, the children and their parents were dyslipidemia improved. At the follow-up visit after 12 months, informed about the purpose, risks and drawbacks of the study and related the children had in average gained 10.8 kg and increased their procedures. Subsequently, they all gave informed written declaration of BMI-SDS by 9%; however, 24% had maintained or even further consent. reduced their BMI-SDS. Mean body content of fat and HOMA-IR increased, and the dyslipidemic state was aggravated. Biochemical analyses Alanine aminotransferase, gamma-glutamyltransferase, triglycerides, total Circulating sCD36 decreased during lifestyle intervention and cholesterol, high-density lipoprotein cholesterol, low-density lipoprotein increased during follow-up cholesterol, glucose, leukocytes and high sensitivity C-reactive protein were measured on automated analysis platforms in the routine laboratory Circulating sCD36 decreased by 21% after 10 weeks of lifestyle at Aarhus University Hospital. intervention (P = 0.0013) and was increased by 32% (P = 0.014) Circulating sCD36 in plasma was measured by an in-house enzyme- during the 12 months of follow-up (Figure 1). No gender linked immunosorbent assay as previously described,17 with an interassay differences were observed (P = 0.69). sCD36 was not associated coefficient of variation of 16.4%. Serum insulin (N = 112) was measured
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