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821.Full-Text.Pdf Diabetes Care Volume 37, March 2014 821 Structural and Functional Kyriakoula Marinou,1,2 Leanne Hodson,1 Senthil K. Vasan,1,3 Barbara A. Fielding,1,4 Properties of Deep Abdominal Rajarshi Banerjee,5 Kerstin Brismar,3 Michael Koutsilieris,2 Anne Clark,1 Subcutaneous Adipose Tissue Matt J. Neville,1,6 and Fredrik Karpe1,6 Explain Its Association With Insulin Resistance and Cardiovascular Risk in Men OBJECTIVE Fat distribution is an important variable explaining metabolic heterogeneity of obesity. Abdominal subcutaneous adipose tissue (SAT) is divided by the Scarpa’s fascia into a deep subcutaneous adipose tissue (dSAT) and a superficial subcuta- neous adipose tissue (sSAT) layer. This study sought to characterize functional differences between the two SAT layers to explore their relative contribution to metabolic traits and cardiovascular risk (CVR) profile. RESEARCH DESIGN AND METHODS 1Oxford Centre for Diabetes, Endocrinology, and We recruited 371 Caucasians consecutively from a local random, population- Metabolism, Radcliffe Department of Medicine, University of Oxford, Oxford, United Kingdom based screening project in Oxford and 25 Asian Indians from the local community. 2 Department of Experimental Physiology, Athens CARDIOVASCULAR AND METABOLIC RISK The depth of the SAT layers was determined by ultrasound (US), and adipose University School of Medicine, Athens, Greece tissue (AT) biopsies were performed under US guidance in a subgroup of 43 3Department of Molecular Medicine and Caucasians. Visceral adipose tissue (VAT) mass was quantified by dual-energy Surgery, Karolinska Institutet, Stockholm, X-ray absorptiometry scan. Sweden 4Faculty of Health and Medical Sciences, RESULTS University of Surrey, Guildford, United Kingdom 5Division of Cardiovascular Medicine, Radcliffe Male adiposity in both ethnic groups was characterized by a disproportionate Department of Medicine, University of Oxford, expansion of dSAT, which was strongly correlated with VAT mass. dSAT depth Oxford, United Kingdom 6 was a strong predictor of global insulin resistance (IR; homeostatic model as- National Institute for Health Research, Oxford fi Biomedical Research Centre, Oxford University sessment of IR), liver-speci c IR (insulin-like growth factor binding protein-1), and Hospital Trusts, Oxford, United Kingdom Framingham risk score independently of other measures of adiposity in men. Corresponding author: Fredrik Karpe, fredrik Moreover, dSAT had higher expression of proinflammatory, lipogenic, and lipo- [email protected]. lytic genes and contained higher proportions of saturated fatty acids. There was Received 6 June 2013 and accepted 21 October increased proportion of small adipocytes in dSAT. 2013. This article contains Supplementary Data online CONCLUSIONS at http://care.diabetesjournals.org/lookup/ SAT is heterogeneous; dSAT expands disproportionally more than sSAT with in- suppl/doi:10.2337/dc13-1353/-/DC1. creasing obesity in Caucasian males (confirmed also in Asian Indians). Its expan- The contents of this article reflect only the ’ sion is related to increased CVR independent of other adiposity measures, and it authors views and not the views of the European Commission. has biological properties suggestive of higher metabolic activity contributing to © 2014 by the American Diabetes Association. global IR. See http://creativecommons.org/licenses/by- Diabetes Care 2014;37:821–829 | DOI: 10.2337/dc13-1353 nc-nd/3.0/ for details. 822 Abdominal Fat Layers and Cardiometabolic Risk Diabetes Care Volume 37, March 2014 Abdominal obesity is associated with differences in the SAT layers, gene The study population recruitment the development of insulin resistance expression, and fatty acid (FA) profiles. algorithm is presented in (IR), type 2 diabetes, and coronary We hypothesized that dSAT is Supplementary Fig. 1. heart disease (1). The classical morphologically and biologically Study Primary End Points abdominal adipose tissue (AT) different than sSAT, with the deep layer The primary end points of the study compartmentalization into having a more proinflammatory, were 1) the measurement of the depth subcutaneous adipose tissue (SAT) and lipogenic, and lipolytic profile. We of dSAT and sSAT layers by US (linked visceral adipose tissue (VAT) has been also hypothesized that the relative with all the other study end points), widely studied in relation to obesity- expansion of dSAT against sSAT layer, 2) gene expression and FA profile of related complications (2–4). The as quantified by US, may be a more dSAT and sSAT, 3) circulating lipid profile anatomical distinction of SAT superior index than BMI and waist and IR, and 4) histological characteristics compartments into superficial circumference (WC) to characterize of dSAT and sSAT. subcutaneous adipose tissue (sSAT) and cardiovascular and diabetes risk. Study Secondary End Points deep subcutaneous adipose tissue (dSAT), divided by Scarpa’s fascia, is well RESEARCH DESIGN AND METHODS The secondary end points of the study documented in literature (5–9). A few were 1) measurement of dSAT and sSAT Clinical Protocol by MRI (as means to validate the US studies have shown that dSAT is strongly The study participants were enrolled measurements), 2)DEXAmeasurements related to IR in a manner nearly identical consecutively from a random and of abdominal obesity, 3)FRS,and to that of VAT, while sSAT follows population-based screening project of 4) circulating biomarkers. the pattern of lower-body SAT (1,10). Caucasian residents in Oxfordshire, the Of note, Golan et al. (11) recently Oxford Biobank (www.oxfordbiobank The study was approved by the demonstrated that sSAT was a .org.uk) (19). Because of the well-known Oxfordshire Clinical Research Ethics protective fat depot in patients with high diabetes risk and the tendency Committee, and all volunteers gave type 2 diabetes. toward IR, we also included a pilot written informed consent. The sSAT layer is organized in compact recruitment of 25 nondiabetic Asian Indian immigrants to the U.K. from the Ultrasonography of SAT fascial septa orientated perpendicular US measurements of the SAT layers to the skin, with the lobules being small local Asian Oxfordshire community (as described below). Then, from the main were performed using a 7.5 MHz linear and ovoid, whereas the dSAT layer Oxford Biobank study cohort, we array probe and two-dimensional contains larger lobules and less identified 25 Caucasians with identical imaging (Philips PDI 5000) in all organized and widely spaced Scarpa’s whole subcutaneous adipose tissue participants (n = 371). Measurements fascia septa (5,12–14). Studies in pigs (wSAT), age, and gender with the were taken with participants in the suggest that the SAT layers have recruited Asians (nested study). supine position during exhalation different embryological origin and that phase. All measurements were recorded the deeper layer expands during weight Caucasian Cohort 5 cm lateral to the umbilicus (a location gain (1,15). The situation in humans is The 371 Caucasian individuals (146 men, where the Scarpa’s fascia line is clearly less clear. 225 women) came to the clinical observed) on both sides. The probe was research unit after an overnight fast. held with 1–2 mm distance from the skin Importantly, fat distribution differs Anthropometric variables were measured, between males and females, and this (US gel layer giving contact) to ensure no blood samples were taken, and US pressure was put on the abdomen. Two has been related to differences in both measurements of the abdomen were cardiovascular and diabetes risk profile independent measurements were made. The distribution of cardiovascular fi between genders (3,16–18). recorded from each side, and the nal risk (CVR) was estimated by calculating the depth of the fat depots was obtained by The current cross-sectional study was Framingham risk score (FRS). The the average of all four measurements. undertaken with three primary Framingham calculations of 10-year CVR The sSAT distance was defined as the objectives: 1) to identify the depth of werebasedonthethirdreportofthe region of AT between the Scarpa’sfascia the different SAT layers by a novel and National Cholesterol Education Program and lower dermis, whereas wSAT was simple technique using ultrasound (US) Expert Panel on Detection, Evaluation, and defined as the AT occupying the space imaging, validated against magnetic Treatment of High Blood Cholesterol in between the anterior line of the rectus resonance imaging (MRI) and dual- Adults (Adult Treatment Panel III) (2). The abdominis muscle and lower dermis. energy X-ray absorptiometry (DEXA) study population did not include any The difference between wSAT and sSAT in healthy volunteers within a wide patient with prior diagnosis of coronary was defined as dSAT. To evaluate the fi variety of adiposity; 2)toconfirm the heart disease. AT biopsies were speci cally within-person measurement variability, differences between sSAT and dSAT and taken from sSAT and dSAT layers in a sub- four measurements taken 10 min apart their relation with metabolic markers set (n = 43) of the Caucasian individuals. were recorded in 24 subjects (12 males, associated with IR and cardiometabolic Asian Indians 12 females), and the intraobserver risk; and 3) to characterize the biological The 25 Asian Indian individuals attended variability was 0.18% for sSAT, 0.3% for differences between sSAT and dSAT by the clinical research unit for US dSAT, and 0.06% for wSAT. The evaluating whether there are structural characterization of sSAT and dSAT. intraclass correlation coefficient was care.diabetesjournals.org Marinou and Associates 823 0.99 for wSAT (P , 0.0001), 0.98 for of the sSAT using a different syringe and distribution in a sample, we took five dSAT (P , 0.0001), and 0.98 for sSAT needle. This technique yielded ;300 mg samples and counted 2,500 cells in each. (P , 0.0001). of fat from each layer. Samples were We then removed data 100 at a time and washed with saline and aliquoted in 4% observed that the coefficient of variation MRI formalin or in RNA-Later solution for started to increase when less than 100 SAT measured by US was validated using RNA extraction. cells were included in each biopsy.
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