research article low cd36 and lox-1 levels and cd36 gene...

Research ArticleLow CD36 and LOX-1 Levels and CD36 GeneSubexpression Are Associated with Metabolic Dysregulation inOlder Individuals with Abdominal Obesity

Perla-Monserrat Madrigal-Ruiacutez123 Rosa-Elena Navarro-Hernaacutendez123

Sandra-Luz Ruiacutez-Quezada34 Fernanda-Isadora Corona-Meraz23

Moacutenica Vaacutezquez-Del Mercado1256 Eduardo Goacutemez-Bantildeuelos236

Jorge Castro-Albarran23 Flavio Sandoval-Garciacutea27

Luis-Javier Flores-Alvarado13 and Beatriz-Teresita Martiacuten-Marquez126

1Departamento de Biologıa Molecular y Genomica Centro Universitario de Ciencias de la Salud Universidad de GuadalajaraSierra Mojada No 950 Colonia Independencia 44340 Guadalajara JAL Mexico2Instituto de Investigacion en Reumatologıa y del Sistema Musculo Esqueletico Centro Universitario de Ciencias de la SaludUniversidad de Guadalajara Sierra Mojada No 950 Colonia Independencia 44340 Guadalajara JAL Mexico3UDG-CA-701 Grupo de Investigacion Inmunometabolismo en Enfermedades Emergentes (GIIEE) Centro Universitario deCiencias de la Salud Universidad de Guadalajara Sierra Mojada No 950 Colonia Independencia 44340 Guadalajara JAL Mexico4Departamento de Farmacobiologıa Centro Universitario de Ciencias Exactas e Ingenierıas Universidad de GuadalajaraBoulevard Marcelino Garcıa Barragan No 1421 44430 Guadalajara JAL Mexico5Servicio de Reumatologıa Division de Medicina Interna Hospital Civil ldquoDr Juan I Menchacardquo Universidad de GuadalajaraSalvador de Quevedo y Zubieta No 750 44340 Guadalajara JAL Mexico6UDG-CA-703 Grupo de Investigacion en Inmunologıa y Reumatologıa Centro Universitario de Ciencias de la SaludUniversidad de Guadalajara Sierra Mojada No 950 Colonia Independencia 44340 Guadalajara JAL Mexico7Departamento de Clınicas Medicas Antiguo Hospital Civil de Guadalajara Calle Hospital No 320Colonia El Retiro 44360 Guadalajara JAL Mexico

Correspondence should be addressed to Beatriz-Teresita Martın-Marquez bethymarhotmailcom

Received 5 February 2016 Revised 17 June 2016 Accepted 19 June 2016

Academic Editor Hiroshi Okamoto

Copyright copy 2016 Perla-Monserrat Madrigal-Ruız et al This is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

Background Obesity study in the context of scavenger receptors has been linked to atherosclerosis CD36 and LOX-1 are importantsince they have been associated with atherogenic and metabolic disease but not fat redistribution The aim of our study wasto determinate the association between CD36 and LOX-1 in presence of age and abdominal obesity Methods This is a cross-sectional study that included 151 healthy individuals clinically and anthropometrically classified into two groups by age (lt30 andge30 years old) and abdominal obesity (according to World Health Organization guidelines) We excluded individuals with anychronic andmetabolic illness use of medication or smoking Fasting blood samples were taken to perform determination of CD36mRNA expression by real-time PCR lipid profile and metabolic and low grade inflammation markers by routine methods andsoluble scavenger receptors (CD36 and LOX-1) by ELISA Results Individuals ge30 years old with abdominal obesity presentedhigh atherogenic index lower soluble scavenger receptor levels and subexpression of CD36mRNA (54 less) On the other handindividuals lt30 years old with abdominal adiposity presented higher levels in the same parameters except LOX-1 soluble levelsConclusion In this study individuals over 30 years of age presented low soluble scavenger receptors levels pattern and CD36 genesubexpression which suggest the chronic metabolic dysregulation in abdominal obesity

Hindawi Publishing CorporationJournal of Diabetes ResearchVolume 2016 Article ID 5678946 10 pageshttpdxdoiorg10115520165678946

2 Journal of Diabetes Research

1 Introduction

Obesity is characterized by progressive enlargement of adi-pose tissue [1 2] It has been shown that the fat distributionrather than total amount of fat is associated with increasedcardiovascular disease (CVD) risk [3] Since CD36 is a cellsurface glycoprotein that belongs to class B scavenger recep-tor family it is considered as multifunctional receptor inadipocyte it acts as a fatty acid translocase of long-chain fattyacids however in monocytemacrophage it regulates oxLDLuptake [4] On the other hand LOX-1 is classified amongE-type scavenger receptor family is expressed in vascularendothelium and recognizes oxLDL cellular debris and sev-eral structurally unrelated molecules as a ligand it is highlyexpressed in the cardiovascular system by proinflammatoryand prooxidative stimuli [5 6]

LOX-1 and CD36 favor the development of atheroscle-rosis through their ability to bind and internalize modifiedLDL facilitating formation of macrophage foam cells andtheir location to subendothelial space promoting endothelialdysfunction and CVD

Additionally several studies associate an increase of solu-ble form of CD36 (sCD36) in symptomatic carotid stenosiswith metabolic disorders such as type 2 diabetes mellitus(T2DM) Meanwhile the soluble form of LOX-1 (sLOX-1)has been mainly associated with diverse atherogenic diseaseslike arterial stiffness T2DM and myocardial infarction andit is even proposed as a biomarker for acute coronarysyndrome [7ndash18] Several studies showed an inflammatoryparacrine interaction between adipocytes and macrophageswhich could be dependent on scavenger receptors thispathogenic process involves a state of dysmetabolic profileand chronic inflammation which contributes to abdominalobesity development [19 20]

However the association of sCD36 and sLOX-1 levelswith fat redistribution and metabolic markers is not knownThe aim of our study was to determine the associationbetween CD36 and LOX-1 in presence of age and abdominalobesity

2 Materials and Methods

21 Subjectsrsquo Selection and Classification In this cross-sectional study we recruited 151 adults aged between 20and 59 years of general population of Mexico They wereclassified according to the recommendations ofWorldHealthOrganization Expert Consultation by WC waist-hip ratio(WHR) and waist-to-height ratio (WHtR) into two groupsthe first group includes individuals with abdominal obesity ifany of the following conditions were present WC ge 900 cmWHR ge 090 and WHtR ge 0525 in men and WC ge 800 cmWHR ge 080 andWHtR ge 0530 in women the second groupincludes individuals without abdominal obesity a groupwhich has lower values of these measurements In relation toage an age of 30 years was established as a cutoff and twogroups were stablished lt30 years old and ge30 years old

We consider additional criteria for disease risk asso-ciations BMI from 1850 to 2499 kgm2 was considered

without disease risk for increased disease risk BMI 2500to 2999 kgm2 plus WC lt1020 cm (in men) or lt880 cm (inwomen) was considered for high disease risk we considerWC ge1020 cm (in men) or ge880 cm (in women) and BMIge300 kgm2 plus anyWCmeasurement was classified as veryhigh disease risk [21ndash23]

We included individuals who at the time of the studydid not present with glucose intolerance infectious diseaseshypertension pregnancy anemia diagnosis of CVD malig-nancy and renal and metabolic diseases such as T2DMWe excluded subjects with current medication smoking ordrugs use

For ethics conduct before enrolment participants wereinformed about the study and signed a consent form follow-ingHelsinki Declaration guidelines [24] and the institutional(Guadalajara University) review boards committees ensuredappropriate ethical and biosecurity conduct

22 Subjectsrsquo Medical History and Physical Examination Allindividuals who satisfied inclusion criteria were clinicallyevaluated by a physician who performed a complete medicalhistory assessment of general health status and vital signswere included blood pressure (executed 3 times with thesubject in the sitting position and relaxing for 15 minutesbefore the measurement) heart respiratory rate and bodytemperature

23 Subjectsrsquo Body Fat Storage Measurements We evaluatedthe following body measurements height was measured tothe nearest 1mm by using a stadiometer (seca GmbH amp CoKG Hamburg Germany) and body weight total body fatmass and trunk body fat mass (absolute kg and relative )were determined by using bioelectrical impedance analysis(TANITA BC-418 segmental body composition analyzerTokyo Japan) to the nearest 01 kg WC hip circumference(HC) and coronal abdominal diameter were measured byusing an anthropometric fiberglass tape (GULICK length 0ndash180 cm precision plusmn01 USA) At the level of the iliac crest (L4-5) sagittal abdominal diameter wasmeasured using a sliding-beam abdominal caliper (precision plusmn01 cm Holtain LtdCrosswell Crymych Pembs SA41 3UF UK) with the patientlying in a supine position in the examination table [25ndash29]Five measures of skinfold thicknesses (ie biceps tricepssubscapular suprailiac and abdominal) were obtained on theright side of the body by using a Harpenden skinfold caliper(opened 80mm and precision of plusmn02mm constant pressure10 gmm2 Holtain Ltd Crosswell Crymych Pembs SA413UF UK) All these measurements were carried out by thesame anthropometrist in duplicate following the proceduresrecommended by anthropometric indicators measurementguide [30 31]

To determine obesity and adiposity indexes the followingmath calculations were used BMI kgm2 = weight (kg)height2 (m)WHR=WCcmHCcmWHtR=WCcmheight(cm) conicity index (CI) = WC (cm)0109radicweight (kg)height (cm) total adipose area (TAA cm2) = WC24120587visceral area (VA cm2) = 120587(WC2120587 minus abdominal skinfold)2

Journal of Diabetes Research 3

subcutaneous abdominal area (cm2) = TAA minus VA [26]visceral adipose index (VAI) for males VAI = (WC3658 +(1896 lowast BMI))6(TG081)6(152HDLc) and for femalesVAI = (WC3968+(1886lowastBMI))6(TG103)6(131HDLc)abdominal volume index (AVI L) = [2 times WC2 +(07 cm)(WC minus HC)21000] [32] and homeostasis modelassessment-insulin resistance (HOMA-IR) = [basal glucosemgdL times (basal insulin 120583UImL)405] [33 34] in addition tothe sum of the 5 skin fold thicknesses (ST5) [35]

24 Metabolic and Inflammatory Markers and ScavengerReceptors Levels Measurements We confirmed overnightfast of 12 hours in all subjects and obtained two venousblood samples with and without anticoagulant (PAXgeneBlood RNA Tube CAT 762165 and BD SST Plus minus13mmCAT 368159 BD Diagnostic Systems Montenegro 1402(C1427AND) Buenos Aires Argentina resp) Samples wereallowed to clot for 30 minutes at 20∘C before centrifugationfor 10 minutes20∘C at 1509 RCF (Rotanta 460R AndreasHettich GmbH amp Co KG) serum was collected and storedimmediately at minus86∘C until further analysis

We quantified serum concentration of basal glucosemgdL and lipid profile mgdL which included triglyc-erides total cholesterol HDLc LDLc and VLDLc [36] (highlow and very low density lipoprotein cholesterols resp)apolipoproteins A1 and B (Apo-A1 and Apo-B) mgdLfree fatty acids (FFA mmolmL) serum C3 mgdL highsensitivity CRP with a limit of detection of 015mgL withroutine colorimetric enzymatic and immunoturbidimetrymethods (Randox Laboratories 55 Diamond Road CrumlinCo Antrim Northern Ireland UK) and erythrocyte sedi-mentation rate (ESR mmh) by Wintrobe method [37]

Through using commercial enzyme-linked immunosor-bent assays (ELISA) we determined soluble levels of insulinsensitivity of 0399120583UImL (ALPCO 26-GKeewaydinDriveSalem NH 03079) sCD36 sensitivity of 3125 ngmL andsLOX-1 sensitivity of 50 pgmL (AVISCERA BIOSCENCEINC 2348 Walsh Avenue Suite C Santa Clara CA 95051)Based on the lipid profile measurements we calculatedthe following atherogenic indexes TCHDLc LDLcHDLcTGHDLc and Apo-A1Apo-B

25 CD36 mRNA Expression Analysis Mononuclear cellsfrom the subjects were isolated by density gradient mediawith separating solution Lymphoprep (AXIS-SHIELD POBox 6863 Rodelokka 0504 Oslo Norway) [38] Purifiedmononuclear cells were used directly for total RNA isolationit was performed according to the manufacturerrsquos procedureusing TRIzol LS Reagent (Ambion Invitrogen by LifeTechnologies 5791 Van Allen Way Carlsbad CA 92008)based on the single-step RNA isolation modified methodreported by Chomczynski and Sacchi [39 40] The comple-mentary DNA synthesis (cDNA) was performed with 2 120583gof each total RNA sample using a reaction size of 20 120583Lwith oligo (dT) 18-primer (100 ng120583L) RNase-free DEPCtreated water and Moloney Murine Leukemia Virus ReverseTranscriptase (M-MLV RT) kit (Applied Biosystems 850Lincoln Centre Drive Foster City CA 94404) and stored atminus20∘C until being used for expression analyses

Real-time quantitative polymerase chain reaction(qPCR) was conducted using the StepOne detection systemEXPRESS SYBR GreenER qPCR SuperMix Universaland sequence detector software (Applied Biosystems 850Lincoln Centre Drive Foster City CA 94404) was used fordata analysis A threshold cycle (CT) value was determinedfrom each amplification plot

In brief CD36 mRNA expression was performed in afinal reaction volume of 20mL (40 120583M forward and reverseprimer 50 nM ROX 2x SYBR Green qPCR master mixand cDNA 100 ng) The conditions of the reaction were asfollows holding at 95∘C10min cycling (35 cycles of 95∘C15 sand 60∘C60 s) and melt curve at 95∘C15 s 60∘C60 s and95∘C15 s Expression of target genes was normalized bythe endogenous reference gene GAPDH sequence specificprimers were forward 51015840-GGAGCGAGATCCCTCCAA-AAT-31015840 [41] and reverse 51015840-GGCTGTTGTCATACTTCT-CATGG-31015840 and for CD36 target gene they were forward 51015840-CTATGCTGTATTTGAATCCGACGTT-31015840 [42] and reverse51015840-CCTGTGTACATTTCACTTCCTCATT-31015840

The relative expression fold changes of target genes werecalculated using the comparative CT method with 2minusΔΔCT

equation [43] For quality control a blank and samplespreviously confirmed as positive for each gene were used ascontrols In addition all samples were identified in duplicateby two different analysts The expression success rate was100

26 Statistical Analysis Data were analyzed with statisticssoftware SPSS v21 (IBM Inc Chicago IL USA) and withGraphPad Prism v601 (2014 Inc 2236 Beach Avenue JollaCA 92037) Results are given as mean plusmn standard devia-tion (SD) The data distribution of clinical and laboratoryvariables was evaluated with 119885 Kolmogorov-Smirnov testparametric and nonparametric tests were performed asappropriate An age and gender (male or female) adjustedANCOVA analysis was made in individuals included inthe study The clinical and laboratory characteristics of thestudy group were analyzed with unpaired Studentrsquos 119905-testor Mann-Whitney 119880 test to compare quantitative data intwo groups Data from serum concentrations of scavengerreceptors laboratorial assessment and adiposity variableswere subjected to Pearsonrsquos correlation tests A two-tailed 119875value less than 005 was considered statistically significant

3 Results

31 Study Subjects Show Increased Body Fat Storage andCardiovascular Disease Risk We included 151 individualsthat were classified by age and presence of abdominal obesity70 were females The anthropometric measures are shownin Table 1 Seventy percent presented overweight (mean BMI2988plusmn 33 kgm2) 37 of these individuals were categorizedwith CVD risk almost 70 of the group were older thange30 years (data no shown) and 78 were identified with anincreased body fat storage

When comparing subgroups with abdominal obesitywe observed a similar distribution of trunk fat storage inyoung and older individuals while older subjects presented


Table 1 Body dimensions and distribution of body fat storage according to age and abdominal obesity

Study grouplt30 years old ge30 years old

Without abdominalobesity

With abdominalobesity



119899 21 24 12 94Female () 14 (67) 11 (45) 10 (83) 71 (75)Age (years) 23 plusmn 3 24 plusmn 3 41 plusmn 9 45 plusmn 8

BMI (kgm2) 228 plusmn 24 285 plusmn 38 244 plusmn 17 300 plusmn 33MeasurementsHeight (cm) 1697 plusmn 86 1705 plusmn 90 1606 plusmn 62 1632 plusmn 91

Body weight (kg)lowast 659 plusmn 96 833 plusmn 151 629 plusmn 60 803 plusmn 124Total body fat mass (kg)lowast 152 plusmn 62 263 plusmn 78 195 plusmn 42 287 plusmn 70Body fat mass ()lowast 232 plusmn 86 319 plusmn 81 308 plusmn 22 356 plusmn 68Waist circumference (cm)lowast 797 plusmn 69 985 plusmn 84 794 plusmn 43 1010 plusmn 87Hip circumference (cm)lowast 991 plusmn 56 1084 plusmn 59 994 plusmn 48 1095 plusmn 76Trunk body fat mass (kg)lowast 75 plusmn 35 145 plusmn 41 94 plusmn 24 145 plusmn 38Trunk body fat mass ()lowast 113 plusmn 46 174 plusmn 34 147 plusmn 33 180 plusmn 35Total adipose area (cm2)lowast 510 plusmn 85 778 plusmn 135 503 plusmn 54 817 plusmn 145Subcutaneous abdominal area (cm2)lowast 381 plusmn 140 579 plusmn 185 489 plusmn 45 604 plusmn 253Visceral area (cm2) 301 plusmn 586 267 plusmn 277 456 plusmn 769 435 plusmn 699

Sagittal abdominal diameter (cm)lowast 178 plusmn 21 217 plusmn 26 186 plusmn 11 230 plusmn 37Coronal abdominal diameter (cm)lowast 282 plusmn 41 338 plusmn 49 289 plusmn 38 315 plusmn 67Skinfold thickness (mm)

Biceps 78 plusmn 45 95 plusmn 42 94 plusmn 44 129 plusmn 52

Tricepslowast 160 plusmn 51 291 plusmn 303 178 plusmn 41 216 plusmn 63Subscapularlowast 152 plusmn 53 204 plusmn 86 171 plusmn 51 239 plusmn 128

Suprailiaclowast 136 plusmn 57 196 plusmn 81 150 plusmn 71 208 plusmn 67Abdominal 185 plusmn 79 189 plusmn 95 205 plusmn 92 238 plusmn 88

ST5lowast 705 plusmn 250 977 plusmn 472 800 plusmn 260 1033 plusmn 297119899 = 151 Data are presented as mean plusmn SD Mann-Whitney 119880 test with lowast119875 lt 0001 comparing groups by age individuals with abdominal obesity versusindividuals without abdominal obesity BMI body mass index ST5 sum of five measures of skinfold thicknesses (ie biceps triceps subscapular suprailiacand abdominal)

higher measurements on triceps subscapular and suprailiacskinfold thickness compared to younger subjects (Table 1)

Additionally in the abdominal obesity subgroup weobserved increased WHtR in older (0619 plusmn 0054) versusyounger (0574 plusmn 0042) individuals (119875 = 0019)

32 Individuals with Abdominal Obesity Presented SubclinicalInflammatory State and Alterations of Lipids Profile Wefound that individuals below 30 years of age with abdominalobesity showed alterations on basal glucose total cholesterolHDLc levels and proinflammatory profile this same scenariowas seen in older individuals with similar adiposity char-acteristics in which a decreased level of Apo-A1 and HDLcwas also found (Table 2) Those individuals with abdominalobesity regardless of age presented higher measurements ofabdominal adiposity and atherogenic indexes (Figure 1)

33 Age and the Presence of Abdominal Obesity Have aDetrimental Effect on sCD36 and sLOX-1 Levels and Increaseof Metabolic Markers The subgroup of individuals below30 years of age compared with the subgroup of individuals

over 30 years of age showed an increase in accumulationof abdominal fat deposits in association with a dyslipidemicprofile which was in accordance with an increase in athero-genic indexes and metabolic markers (Figures 1(a) and 1(c)and Table 2)

We observed that individuals over 30 years of age withabdominal obesity presented lower sCD36 levels comparedto individuals without abdominal obesity while individualsaged below 30 years showed higher levels (Figure 2(a)) Onthe other hand levels of sLOX-1 were lower in both groups(Figure 2(b)) A more detailed analysis was performed inwhich 21 (120573 = 67802625 119875 = 0001) of sCD36 levels areaffected by sex and 35 (120573 = minus389121 119875 = 0006) areaffected by the combination of sex and abdominal skinfoldthickness on an age adjusted ANCOVA

34 CD36 Relative Expression Is Associated with AbdominalObesity We observed in young individuals with abdominalobesity a slight increase in relative expression (111 fold timesversus individuals without abdominal obesity) on the otherhand the group over 30 years of age with abdominal obesityshowed subexpression (54 less Figure 2(c))


Table 2 Metabolic and inflammation markers in individuals included in the study

Measurements






119899 21 24 12 94Basal glucose (mgdL)lowast 86 plusmn 12 97 plusmn 15 88 plusmn 9 98 plusmn 13Basal insulin (120583UImL) 135 plusmn 98 187 plusmn 106 175 plusmn 128 161 plusmn 150

Triglycerides (mgdL) 90 plusmn 41 122 plusmn 65 120 plusmn 55 146 plusmn 76

Total cholesterol (mgdL)lowast 166 plusmn 30 191 plusmn 38 235 plusmn 53 206 plusmn 40HDLc (mgdL)lowast 490 plusmn 66 427 plusmn 63 518 plusmn 45 462 plusmn 73LDLc (mgdL) 894 plusmn 345 1014 plusmn 332 1261 plusmn 364 1191 plusmn 373

VLDLc (mgdL) 180 plusmn 83 244 plusmn 131 240 plusmn 110 292 plusmn 152

Apo-A1 (mgdL)lowast 1372 plusmn 460 1235 plusmn 354 1821 plusmn 403 1436 plusmn 357Apo-B (mgdL)lowast 800 plusmn 311 1205 plusmn 475 1272 plusmn 511 1498 plusmn 895

FFA (mmolmL) 25 plusmn 10 31 plusmn 22 31 plusmn 23 31 plusmn 19

CRP (mgL)lowast 447 plusmn 211 683 plusmn 352 629 plusmn 383 74 plusmn 37

C3 (mgdL)lowast 110 plusmn 30 137 plusmn 38 116 plusmn 25 135 plusmn 26ESR (mmh) 6 plusmn 4 10 plusmn 7 12 plusmn 8 12 plusmn 5

119899 = 151 Data are presented as mean plusmn SD lowastMann-Whitney 119880 test with 119875 lt 005 comparing the groups by age individuals with abdominal obesity versusindividuals without abdominal obesity HDLc LDLc andVLDLc high density lipoprotein cholesterol low density lipoprotein cholesterol and very low densitylipoprotein cholesterol respectively Apo apolipoprotein CRP C reactive protein FFA free fatty acids ESR erythrocyte sedimentation rate

35 Adiposity Is Associated with Scavenger Receptors LevelsLow-Grade Systemic Inflammatory Markers and Body FatStorage Indexes In the case of sLOX-1 and FFA levels apositive correlation with sCD36 was observed in contrastwith the negative correlations in both scavenger receptorswith abdominal adiposity and body fat mass distribution andinflammatory and metabolic markers which are displayed inTable 3

4 Discussion

Abdominal obesity is generatedwhen there is excess accumu-lation of adipose tissue in a progressive manner preferably inthe central region of the body In this setting we evaluatedscavenger receptors production with metabolic inflamma-tory and adiposity profiles in two groups of adults withoutclinical manifestations of disease We found a significantpercent of individuals with high risk of CVD associated withthe presence of abdominal obesity [44] Although BMI isa useful tool to identify individuals at risk there are othercriteria that help recognize earlier CVD risk in an age-independent manner [22 23]

In the context of this study clinical and anthropometricprofile in individuals below 30 years of age versus individ-uals over 30 years of age suggests that abdominal obesityis independent of aging which involves different phenotypesobserved in several clinical stages during development of thepathogenic process

In our study all individuals with abdominal obesityshowed increased adiposity indexes and low-grade inflam-mation status with dyslipidemic profile It has been reportedthat accumulation of fat mass in abdominal area presents

diverse subclinical alterations characterized by changes onlipid and carbohydratemetabolism [25 45] All these changesare due to the development of low-grade inflammationThis process starts an abnormal mechanism with the fol-lowing sequential steps the monocytes from the blood-stream migrate to adipose tissue these cells polarize to M1macrophages and secrete proinflammatory cytokines thatcan act locally in paracrine way favoring the low-gradeinflammation which is redundantly perpetuated [20 45]

Although age is an important factor in the developmentof metabolic alterations a remarkable observation is that inpresence of abdominal obesity our younger group presentedhigh atherogenic indexes compared to its correspondingolder group

We also noticed that the accumulation of abdominal fatleads to higher fasting glucose and dyslipidemia observed inindividuals with abdominal obesityThese evidences confirmthat the abdominal obesity can be amodifiable cardiovascularrisk factor unlike othermetabolic diseases such as atheroscle-rosis hypertension and T2DM [46]

Soluble CD36 levels have been reported not only inpatients with carotid stenosis and unstable atheromatousplaque but also in chronic inflammatory related states such asdiabetic nephropathy polycystic ovary syndrome and sever-ity of hepatic steatosis and insulin resistance and individualswith morbid obesity [47ndash50]

In our study we observed in individuals below 30 yearsof age increased levels of sCD36 in parallel with body fatdeposits predominately on abdominal area These resultscontrast with the opposite case observed in older individ-uals where sCD36 levels decreases with age and presenceof abdominal obesity A consistent elevation of sCD36 in


0

2

4

6

8

TCH

DLc

Mag

nitu

de

LDLc

HD

Lc

TGH

DLc

Apo-

A1

Apo-

B

HO

MA-

IRWithout abdominal obesityWith abdominal obesity

P = 0003

P = 0049

P = 0005

P = 0040

(a)M

agni

tude

00

05

10

1510

20

30

40

BMI

WH

R

WH

tR CI AVI

VAI

Without abdominal obesityWith abdominal obesity

P = 0040

P lt 0001

P lt 0001P lt 0001

P lt 0001

P lt 0001

(b)

Mag

nitu

de


0

2

4

6

8

TCH

DLc

LDLc

HD

Lc

TGH

DLc

Apo-

A1

Apo-

B

HO

MA-

IR

P = 0023

(c)

Mag

nitu

de

00

05

10

15

2010

20

30

40

BMI

WH

R

WH

tR CI AVI

VAI


P = 0011

P lt 0001

P lt 0001

P lt 0001

P lt 0001

P lt 0001

(d)

Figure 1 Metabolic and adiposity indexes in study group Subjects without abdominal obesity 119899 = 33 subjects with abdominal obesity 119899 =118 Data are presented as mean plusmn SD (a) and (b) Individuals lt30 years old Mann-Whitney 119880 test comparing the groups with abdominalobesity versus individuals without abdominal obesity (c) and (d) Individuals ge30 years old with abdominal obesity versus individuals withoutabdominal obesity TC total cholesterol HDLc LDLc and VLDLc high density lipoprotein cholesterol low density lipoprotein cholesteroland very low density lipoprotein cholesterol respectively Apo apolipoprotein HOMA-IR homeostasis model assessment-insulin resistanceBMI body mass index BFR body fat ratio WHtR waist-to-height ratio CI conicity index AVI abdominal volume index VAI visceraladipose index

patients with T2DM insulin resistance and obesity has beendocumented after bariatric surgery in adults sCD36 levelsdecline and metabolic markers improve [8 10 14] mean-while there are reports of low receptor membrane expressionon peripheral blood mononuclear cells in women withobesity and pharmacologically treated rheumatoid arthritispatients with subclinical atherosclerosis [51 52] Based on

these reports we decided to measure scavenger receptorlevels in individuals with abdominal obesity

Our results showed two subsets of CD36 expressionin soluble levels related to age below and above 30 yearswhile a low soluble LOX-1 pattern in older individualswith abdominal adiposity negative correlates with severaladiposity indexes On the contrary we observed positive


0

50

100


Solu

ble l

evels

of s

CD36

(ng

mL)

Individuals aged lt30 years Individuals aged ge30 years

P = 00200

P = 00220

(a)

0

300

600

900

1200

1500

1800



P = 00020

Solu

ble l

evels

of s

LOX-

1(p

gm

L)

(b)


00

05

10

15

20

25

11 foldtimes

54less


Relat

ive e

xpre

ssio

n of

CD36

(2minusΔΔ

C T)

(c)

Figure 2 Scavenger receptors LOX-1 and sCD36 expression levels in study group Subjects without abdominal obesity 119899 = 86 subjects withabdominal obesity 119899 = 54 Data are presented as mean plusmn SD in individuals below 30 years of age and individuals above 30 years of age (a)Soluble levels of CD36 (b) Soluble levels of LOX-1 (c) mRNA expression levels of CD36 LOX-1 lectin like oxidized low density lipoproteinreceptor 1

correlations between FFA and sLOX-1 levels with sCD36which suggest the interaction of these scavenger receptors instates of pathological adipose tissue distribution

Increased sLOX-1 levels have been associated with acutecoronary syndrome or T2DM patients that denote theircontribution in atherosclerosis development [53ndash55] In our

study we showed an alternative scenario to what is reportedin previous studies in subjects with metabolic diseases ourfindings could be explained in part by a strict compliance onthe inclusion criteria used in our study and by taking intoaccount abdominal obesity indicators Even though there is afunctional redundancy in scavenger receptors it seems that in


Table 3 Correlation of adiposity with scavenger receptors markersand systemic low-grade inflammatory state along body fat storage

Measurements Pearsonrsquos correlation testsCD36 119875 LOX-1 119875

LOX-1 (pgmL) 0249 0042 mdash mdashBody mass index (BMI) 0359 0003 minus0359 0027Waist circumference (cm) minus0285 0008 minus0276 0025Hip circumference (cm) minus0217 0045 minus0188 NSTotal body fat mass () minus0334 0020 minus0221 NSTrunk body fat mass (kg) minus0229 0036 minus0225 NSTotal adipose area (cm2) minus0280 0009 minus0262 0034Visceral area (cm2) minus0282 0009 minus0251 0042Sagittal diameter (cm) minus0265 0014 minus0261 0033Body fat index minus0301 0038 minus0612 0001Waist-to-height ratio (WHtR) minus0313 0004 minus0378 0019Conicity index minus0256 0019 minus0371 0022Skinfold thickness (mm)

Bicipital minus0283 0008 minus0255 0037Subscapular minus0308 0004 minus0235 NSSuprailiac minus0305 0004 minus0251 0040Abdominal minus0325 0002 minus0258 0036ST5 (mm) minus0257 0017 minus0245 0048

Basal glucose (mgdL) minus0189 NS minus0258 0038Total cholesterol (mgdL) minus0255 0017 0001 NSHDLc (mgdL) minus0292 0044 0089 NSLDLc (mgdL) minus0247 0021 minus0027 NSVLDLc (mgdL) minus0379 0009 minus0406 0013LDLcHDLc minus0251 0019 minus0053 NSApo-A1 (mgL) 0463 0001 minus0383 0018Apo-A1Apo-B minus0225 0039 minus0048 NSFFA (mmolmL) 0377 0020 0167 NSCRP (mgL) minus0325 0002 minus0072 NSC3 (mgdL) minus0324 0024 minus0431 0007ESR (mmh) minus0107 NS minus0396 0014119899 = 151 HDLc LDLc and VLDLc high density lipoprotein cholesterol lowdensity lipoprotein cholesterol and very low density lipoprotein cholesterolrespectively Apo apolipoprotein CRP C reactive protein FFA free fattyacids ESR erythrocyte sedimentation rate

undefined circumstances they work as coreceptors to displayseveral responses in different clinical context this interplaybetween receptors has not been completely elucidated [56]

While CD36 soluble receptor levels are considered anearly marker of insulin resistance it could also be consideredthat modulation of scavenger receptor could represent aprecompensation mechanism in individuals with an alteredmetabolism Based on our results we could hypothesize thatlow soluble CD36 levels and their gene subexpression maybe an early homeostatic state previous to the establishmentof metabolic syndrome thereby reinforcing the central roleof dysfunctional adipose tissue as a trigger for the metaboliccomplications associated with long-term obesity The multi-ple functions and the heterogeneity of cells that express thisreceptor make it difficult to isolate the exact role of thesereceptors in diverse clinical contexts

5 Conclusions

In this study individuals over 30 years of age presented lowsoluble scavenger receptors levels pattern and CD36 genesubexpression which suggest the chronic metabolic dysreg-ulation in abdominal adiposity

Competing Interests

The authors declare that there are no competing interestsregarding the publication of this paper

Acknowledgments

This work was supported by Grant no 220214 to UDG-CA-701 Academic group ldquoAging Immuno-metabolism andOxidative Stressrdquo

References

[1] World Health Organization Obesity Preventing and Managingthe Global Epidemic Report of a WHO Consultation WHO2000

[2] J M Crow ldquoObesity insensitive issuerdquo Nature vol 486 no7403 pp S12ndashS13 2012

[3] J P Despres I Lemieux J Bergeron et al ldquoAbdominal obe-sity and the metabolic syndrome contribution to global car-diometabolic riskrdquo Arteriosclerosis Thrombosis and VascularBiology vol 28 no 6 pp 1039ndash1049 2008

[4] S Collot-Teixeira J Martin CMcDermott-Roe R Poston andJ L McGregor ldquoCD36 and macrophages in atherosclerosisrdquoCardiovascular Research vol 75 no 3 pp 468ndash477 2007

[5] R Yoshimoto Y Fujita A Kakino S Iwamoto T Takaya andT Sawamura ldquoThe discovery of LOX-1 its ligands and clinicalsignificancerdquo Cardiovascular Drugs and Therapy vol 25 no 5pp 379ndash391 2011

[6] M Piechota A Banaszewska J Dudziak M Slomczynski andR Plewa ldquoHighly upregulated expression of CD36 and MSR1in circulating monocytes of patients with acute coronary syn-dromesrdquo Protein Journal vol 31 no 6 pp 511ndash518 2012

[7] N Rasouli A Yao-Borengasser V Varma et al ldquoAssociation ofscavenger receptors in adipose tissue with insulin resistance innondiabetic humansrdquo Arteriosclerosis Thrombosis and Vascu-lar Biology vol 29 no 9 pp 1328ndash1335 2009

[8] L Knoslashsgaard S BThomsenM Stoslashckel H Vestergaard andAHandberg ldquoCirculating sCD36 is associated with unhealthy fatdistribution and elevated circulating triglycerides in morbidlyobese individualsrdquo Nutrition and Diabetes vol 4 article e1142014

[9] A Tuten B AydemirMOncul et al ldquoThe association of lectin-like oxidized LDL receptor 1 (LOX-1) K167N and 31015840UTR188CTpolymorphisms with maternal plasma soluble LOX-1 levelsand preeclampsia risk in Turkish populationrdquo Archives ofGynecology and Obstetrics vol 291 no 3 pp 563ndash571 2015

[10] A Handberg K Levin K Hoslashjlund and H Beck-NielsenldquoIdentification of the oxidized low-density lipoprotein scav-enger receptor CD36 in plasma a novel marker of insulinresistancerdquo Circulation vol 114 no 11 pp 1169ndash1176 2006

[11] A Handberg A Lopez-Bermejo J Bassols J Vendrell WRicart and J M Fernandez-Real ldquoCirculating soluble CD36


is associated with glucose metabolism and interleukin-6in glucose-intolerant menrdquo Diabetes and Vascular DiseaseResearch vol 6 no 1 pp 15ndash20 2009

[12] M Balin A Celik and M A Kobat ldquoThe association betweensoluble lectin-like oxidized low-density lipoprotein receptor-1levels andpatientswith isolated coronary artery ectasiardquo JournalofThrombosis andThrombolysis vol 33 no 3 pp 239ndash245 2012

[13] M Balin A Celik M A Kobat and A Baydas ldquoCirculatingsoluble lectin-like oxidized low-density lipoprotein receptor-1 levels predict percutaneous coronary intervention-relatedperiprocedural myocardial infarction in stable patients under-going elective native single-vessel PCIrdquo Journal of Thrombosisand Thrombolysis vol 34 no 4 pp 483ndash490 2012

[14] A Handberg M Norberg H Stenlund G Hallmans J Atter-mann and J W Eriksson ldquoSoluble CD36 (sCD36) clusters withmarkers of insulin resistance and high sCD36 is associatedwithincreased type 2 diabetes riskrdquo Journal of Clinical Endocrinologyand Metabolism vol 95 no 4 pp 1939ndash1945 2010

[15] T E Brinkley N Kume H Mitsuoka D A Phares and J MHagberg ldquoElevated soluble lectin-like oxidized LDL receptor-1(sLOX-1) levels in obese postmenopausal womenrdquo Obesity vol16 no 6 pp 1454ndash1456 2008

[16] T Otsuki S Maeda J Mukai M Ohki M Nakanishi and TYoshikawa ldquoAssociation between plasma sLOX-1 concentrationand arterial stiffness in middle-aged and older individualsrdquoJournal of Clinical Biochemistry and Nutrition vol 57 no 2 pp151ndash155 2015

[17] M Fukui M Tanaka T Senmaru et al ldquoLOX-1 is a novelmarker for peripheral artery disease in patients with type 2diabetesrdquoMetabolism vol 62 no 7 pp 935ndash938 2013

[18] Y Nomata N Kume H Sasai et al ldquoWeight reduction candecrease circulating soluble lectin-like oxidized low-densitylipoprotein receptor-1 levels in overweight middle-aged menrdquoMetabolism Clinical and Experimental vol 58 no 9 pp 1209ndash1214 2009

[19] A Chawla K D Nguyen and Y P S Goh ldquoMacrophage-mediated inflammation in metabolic diseaserdquo Nature ReviewsImmunology vol 11 no 11 pp 738ndash749 2011

[20] D J Kennedy S Kuchibhotla K M Westfall R L SilversteinR E Morton and M Febbraio ldquoA CD36-dependent pathwayenhances macrophage and adipose tissue inflammation andimpairs insulin signallingrdquo Cardiovascular Research vol 89 no3 pp 604ndash613 2011

[21] A Berber R Gomez-Santos G Fanghanel and L Sanchez-Reyes ldquoAnthropometric indexes in the prediction of type 2diabetes mellitus hypertension and dyslipidaemia in aMexicanpopulationrdquo International Journal of Obesity vol 25 no 12 pp1794ndash1799 2001

[22] S R Millar I J Perry and C M Phillips ldquoAssessing car-diometabolic risk in middle-aged adults using body mass indexand waist-height ratio are two indices better than one A cross-sectional studyrdquoDiabetology andMetabolic Syndrome vol 7 no1 article 73 2015

[23] C Nishida G T Ko and S Kumanyika ldquoBody fat distributionand noncommunicable diseases in populations overview of the2008 WHO Expert Consultation on Waist Circumference andWaist-HipRatiordquoEuropean Journal of Clinical Nutrition vol 64no 1 pp 2ndash5 2010

[24] (WHO) and CfIOoMSCicwtWHO International EthicalGuidelines for Biomedical Research Involving Human Subjects2002

[25] H S Kahn ldquoChoosing an index for abdominal obesity anopportunity for epidemiologic clarificationrdquo Journal of ClinicalEpidemiology vol 46 no 5 pp 491ndash494 1993

[26] M Garaulet J J Hernandez-Morante F J Tebar S Zamoraand M Canteras ldquoTwo-dimensional predictive equation toclassify visceral obesity in clinical practicerdquo Obesity vol 14 no7 pp 1181ndash1191 2006

[27] H S Kahn Q Gu KM Bullard D S Freedman N Ahluwaliaand C L Ogden ldquoPopulation distribution of the sagittalabdominal diameter (SAD) from a representative sample of USadults comparison of SAD waist circumference and bodymassindex for identifying dysglycemiardquo PLoS ONE vol 9 no 10Article ID e108707 2014

[28] P Pajunen H Rissanen M A Laaksonen M Heliovaara AReunanen and P Knekt ldquoSagittal abdominal diameter as a newpredictor for incident diabetesrdquoDiabetes Care vol 36 no 2 pp283ndash288 2013

[29] World Health Organization Waist Circumference and Waist-Hip Ratio Report of a WHO Expert Consultation World HealthOrganization Geneva Switzerland 2008

[30] (NHANES) NHaNES Antropometry Procedures Manual2013

[31] R Ness-Abramof and C M Apovian ldquoWaist circumferencemeasurement in clinical practicerdquoNutrition in Clinical Practicevol 23 no 4 pp 397ndash404 2008

[32] M C Amato C Giordano M Galia et al ldquoVisceral AdiposityIndex a reliable indicator of visceral fat function associatedwithcardiometabolic riskrdquoDiabetes Care vol 33 no 4 pp 920ndash9222010

[33] D R Matthews J P Hosker A S Rudenski B A Naylor DF Treacher and R C Turner ldquoHomeostasis model assessmentinsulin resistance and 120573-cell function from fasting plasmaglucose and insulin concentrations in manrdquo Diabetologia vol28 no 7 pp 412ndash419 1985

[34] T M Wallace and D R Matthews ldquoThe assessment of insulinresistance in manrdquoDiabetic Medicine vol 19 no 7 pp 527ndash5342002

[35] F-I Corona-Meraz R-E Navarro-Hernandez S-L Ruız-Quezada et al ldquoInverse relationship of the CMKLR1 rela-tive expression and chemerin serum levels in obesity withdysmetabolic phenotype and insulin resistancerdquo Mediators ofInflammation vol 2016 Article ID 3085390 9 pages 2016

[36] W T Friedewald R I Levy and D S Fredrickson ldquoEstimationof the concentration of low-density lipoprotein cholesterol inplasma without use of the preparative ultracentrifugerdquo ClinicalChemistry vol 18 no 6 pp 499ndash502 1972

[37] MMWintrobe and JW Landsberg ldquoA standardized techniquefor the blood sedimentation test 1935rdquoTheAmerican Journal ofthe Medical Sciences vol 346 no 2 pp 148ndash153 2013

[38] A Boyum ldquoSeparation of leukocytes from blood and bonemarrow Introductionrdquo Scandinavian Journal of Clinical andLaboratory Investigation Supplementum vol 97 article 7 1968

[39] P Chomczynski ldquoA reagent for the single-step simultaneousisolation of RNA DNA and proteins from cell and tissuesamplesrdquo BioTechniques vol 15 no 3 pp 532ndash537 1993

[40] P Chomczynski and N Sacchi ldquoSingle-step method of RNAisolation by acid guanidinium thiocyanate-phenol-chloroformextractionrdquo Analytical Biochemistry vol 162 no 1 pp 156ndash1591987

[41] Q Tang W Wu X Xu et al ldquomiR-141 contributes to fetalgrowth restriction by regulating PLAG1 expressionrdquo PLoS ONEvol 8 no 3 Article ID e58737 2013


[42] A Das T K Das U Sahu B P Das S K Kar and M R Ran-jit ldquoCD36 T188G gene polymorphism and severe falciparummalaria in Indiardquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 103 no 7 pp 687ndash690 2009

[43] K J Livak and T D Schmittgen ldquoAnalysis of relative geneexpression data using real-time quantitative PCR and the 2-ΔΔCT methodrdquoMethods vol 25 no 4 pp 402ndash408 2001

[44] J-P Despres and I Lemieux ldquoAbdominal obesity andmetabolicsyndromerdquo Nature vol 444 no 7121 pp 881ndash887 2006

[45] A Tchernof and J-P Despres ldquoPathophysiology of humanvisceral obesity an updaterdquo Physiological Reviews vol 93 no1 pp 359ndash404 2013

[46] K C Zalesin B A FranklinWMMiller E D Peterson and PA McCullough ldquoImpact of obesity on cardiovascular diseaserdquoEndocrinology Metabolism Clinics of North America vol 37 no3 pp 663ndash684 2008

[47] T M Shiju V Mohan M Balasubramanyam and PViswanathan ldquoSoluble CD36 in plasma and urine a plausibleprognostic marker for diabetic nephropathyrdquo Journal ofDiabetes and its Complications vol 29 no 3 pp 400ndash406 2015

[48] D Glintborg K Hoslashjlund M Andersen J E Henriksen HBeck-Nielsen and A Handberg ldquoSoluble CD36 and risk mark-ers of insulin resistance and atherosclerosis are elevated inpolycystic ovary syndrome and significantly reduced duringpioglitazone treatmentrdquo Diabetes Care vol 31 no 2 pp 328ndash334 2008

[49] C Garcıa-Monzon O Lo Iacono J Crespo et al ldquoIncreasedsoluble CD36 is linked to advanced steatosis in nonalcoholicfatty liver diseaserdquo European Journal of Clinical Investigationvol 44 no 1 pp 65ndash73 2014

[50] J-M Fernandez-Real A Handberg F Ortega K Hoslashjlund JVendrell and W Ricart ldquoCirculating soluble CD36 is a novelmarker of liver injury in subjects with altered glucose tolerancerdquoJournal of Nutritional Biochemistry vol 20 no 6 pp 477ndash4842009

[51] J Kuliczkowska-Płaksej G Bednarek-Tupikowska andA FilusldquoReceptor CD36 expression on peripheral blood monocytes inwomen with visceral obesityrdquo Endokrynologia Polska vol 59no 6 pp 483ndash489 2008

[52] E Gomez-Banuelos B T Martın-Marquez E A Martınez-Garcıa et al ldquoLow levels of CD36 in peripheral blood mono-cytes in subclinical atherosclerosis in rheumatoid arthritisa cross-sectional study in a Mexican populationrdquo BioMedResearch International vol 2014 Article ID 736786 6 pages2014

[53] K C B Tan S W M Shiu Y Wong L Leng and R BucalaldquoSoluble lectin-like oxidized low density lipoprotein receptor-1in type 2 diabetesmellitusrdquo Journal of Lipid Research vol 49 no7 pp 1438ndash1444 2008

[54] K Hayashida N Kume T Murase et al ldquoSerum solublelectin-like oxidized low-density lipoprotein receptor-1 levels areelevated in acute coronary syndrome a novel marker for earlydiagnosisrdquo Circulation vol 112 no 6 pp 812ndash818 2005

[55] T Murase N Kume H Kataoka et al ldquoIdentification of solubleforms of lectin-like oxidized LDL receptor-1rdquo ArteriosclerosisThrombosis and Vascular Biology vol 20 no 3 pp 715ndash7202000

[56] J Canton D Neculai and S Grinstein ldquoScavenger receptors inhomeostasis and immunityrdquo Nature Reviews Immunology vol13 no 9 pp 621ndash634 2013

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014


MEDIATORSINFLAMMATION

of


Behavioural Neurology

EndocrinologyInternational Journal of



Disease Markers


BioMed Research International

OncologyJournal of



Oxidative Medicine and Cellular Longevity


PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of



Computational and Mathematical Methods in Medicine

OphthalmologyJournal of


Diabetes ResearchJournal of



Research and TreatmentAIDS


Gastroenterology Research and Practice


Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom


1 Introduction

Obesity is characterized by progressive enlargement of adi-pose tissue [1 2] It has been shown that the fat distributionrather than total amount of fat is associated with increasedcardiovascular disease (CVD) risk [3] Since CD36 is a cellsurface glycoprotein that belongs to class B scavenger recep-tor family it is considered as multifunctional receptor inadipocyte it acts as a fatty acid translocase of long-chain fattyacids however in monocytemacrophage it regulates oxLDLuptake [4] On the other hand LOX-1 is classified amongE-type scavenger receptor family is expressed in vascularendothelium and recognizes oxLDL cellular debris and sev-eral structurally unrelated molecules as a ligand it is highlyexpressed in the cardiovascular system by proinflammatoryand prooxidative stimuli [5 6]

LOX-1 and CD36 favor the development of atheroscle-rosis through their ability to bind and internalize modifiedLDL facilitating formation of macrophage foam cells andtheir location to subendothelial space promoting endothelialdysfunction and CVD

Additionally several studies associate an increase of solu-ble form of CD36 (sCD36) in symptomatic carotid stenosiswith metabolic disorders such as type 2 diabetes mellitus(T2DM) Meanwhile the soluble form of LOX-1 (sLOX-1)has been mainly associated with diverse atherogenic diseaseslike arterial stiffness T2DM and myocardial infarction andit is even proposed as a biomarker for acute coronarysyndrome [7ndash18] Several studies showed an inflammatoryparacrine interaction between adipocytes and macrophageswhich could be dependent on scavenger receptors thispathogenic process involves a state of dysmetabolic profileand chronic inflammation which contributes to abdominalobesity development [19 20]

However the association of sCD36 and sLOX-1 levelswith fat redistribution and metabolic markers is not knownThe aim of our study was to determine the associationbetween CD36 and LOX-1 in presence of age and abdominalobesity

2 Materials and Methods

21 Subjectsrsquo Selection and Classification In this cross-sectional study we recruited 151 adults aged between 20and 59 years of general population of Mexico They wereclassified according to the recommendations ofWorldHealthOrganization Expert Consultation by WC waist-hip ratio(WHR) and waist-to-height ratio (WHtR) into two groupsthe first group includes individuals with abdominal obesity ifany of the following conditions were present WC ge 900 cmWHR ge 090 and WHtR ge 0525 in men and WC ge 800 cmWHR ge 080 andWHtR ge 0530 in women the second groupincludes individuals without abdominal obesity a groupwhich has lower values of these measurements In relation toage an age of 30 years was established as a cutoff and twogroups were stablished lt30 years old and ge30 years old

We consider additional criteria for disease risk asso-ciations BMI from 1850 to 2499 kgm2 was considered

without disease risk for increased disease risk BMI 2500to 2999 kgm2 plus WC lt1020 cm (in men) or lt880 cm (inwomen) was considered for high disease risk we considerWC ge1020 cm (in men) or ge880 cm (in women) and BMIge300 kgm2 plus anyWCmeasurement was classified as veryhigh disease risk [21ndash23]

We included individuals who at the time of the studydid not present with glucose intolerance infectious diseaseshypertension pregnancy anemia diagnosis of CVD malig-nancy and renal and metabolic diseases such as T2DMWe excluded subjects with current medication smoking ordrugs use

For ethics conduct before enrolment participants wereinformed about the study and signed a consent form follow-ingHelsinki Declaration guidelines [24] and the institutional(Guadalajara University) review boards committees ensuredappropriate ethical and biosecurity conduct

22 Subjectsrsquo Medical History and Physical Examination Allindividuals who satisfied inclusion criteria were clinicallyevaluated by a physician who performed a complete medicalhistory assessment of general health status and vital signswere included blood pressure (executed 3 times with thesubject in the sitting position and relaxing for 15 minutesbefore the measurement) heart respiratory rate and bodytemperature

23 Subjectsrsquo Body Fat Storage Measurements We evaluatedthe following body measurements height was measured tothe nearest 1mm by using a stadiometer (seca GmbH amp CoKG Hamburg Germany) and body weight total body fatmass and trunk body fat mass (absolute kg and relative )were determined by using bioelectrical impedance analysis(TANITA BC-418 segmental body composition analyzerTokyo Japan) to the nearest 01 kg WC hip circumference(HC) and coronal abdominal diameter were measured byusing an anthropometric fiberglass tape (GULICK length 0ndash180 cm precision plusmn01 USA) At the level of the iliac crest (L4-5) sagittal abdominal diameter wasmeasured using a sliding-beam abdominal caliper (precision plusmn01 cm Holtain LtdCrosswell Crymych Pembs SA41 3UF UK) with the patientlying in a supine position in the examination table [25ndash29]Five measures of skinfold thicknesses (ie biceps tricepssubscapular suprailiac and abdominal) were obtained on theright side of the body by using a Harpenden skinfold caliper(opened 80mm and precision of plusmn02mm constant pressure10 gmm2 Holtain Ltd Crosswell Crymych Pembs SA413UF UK) All these measurements were carried out by thesame anthropometrist in duplicate following the proceduresrecommended by anthropometric indicators measurementguide [30 31]

To determine obesity and adiposity indexes the followingmath calculations were used BMI kgm2 = weight (kg)height2 (m)WHR=WCcmHCcmWHtR=WCcmheight(cm) conicity index (CI) = WC (cm)0109radicweight (kg)height (cm) total adipose area (TAA cm2) = WC24120587visceral area (VA cm2) = 120587(WC2120587 minus abdominal skinfold)2












3 Results



























Measurements
















4 Discussion










0

2

4

6

8

TCH

DLc

Mag

nitu

de

LDLc

HD

Lc

TGH

DLc

Apo-

A1

Apo-

B

HO

MA-


P = 0003

P = 0049

P = 0005

P = 0040

(a)M

agni

tude

00

05

10

1510

20

30

40

BMI

WH

R

WH

tR CI AVI

VAI


P = 0040

P lt 0001

P lt 0001P lt 0001

P lt 0001

P lt 0001

(b)

Mag

nitu

de


0

2

4

6

8

TCH

DLc

LDLc

HD

Lc

TGH

DLc

Apo-

A1

Apo-

B

HO

MA-

IR

P = 0023

(c)

Mag

nitu

de

00

05

10

15

2010

20

30

40

BMI

WH

R

WH

tR CI AVI

VAI


P = 0011

P lt 0001

P lt 0001

P lt 0001

P lt 0001

P lt 0001

(d)






0

50

100


Solu

ble l

evels

of s

CD36

(ng

mL)


P = 00200

P = 00220

(a)

0

300

600

900

1200

1500

1800



P = 00020

Solu

ble l

evels

of s

LOX-

1(p

gm

L)

(b)


00

05

10

15

20

25

11 foldtimes

54less


Relat

ive e

xpre

ssio

n of

CD36

(2minusΔΔ

C T)

(c)













5 Conclusions


Competing Interests


Acknowledgments


References

































































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of



























3 Results



























Measurements
















4 Discussion










0

2

4

6

8

TCH

DLc

Mag

nitu

de

LDLc

HD

Lc

TGH

DLc

Apo-

A1

Apo-

B

HO

MA-


P = 0003

P = 0049

P = 0005

P = 0040

(a)M

agni

tude

00

05

10

1510

20

30

40

BMI

WH

R

WH

tR CI AVI

VAI


P = 0040

P lt 0001

P lt 0001P lt 0001

P lt 0001

P lt 0001

(b)

Mag

nitu

de


0

2

4

6

8

TCH

DLc

LDLc

HD

Lc

TGH

DLc

Apo-

A1

Apo-

B

HO

MA-

IR

P = 0023

(c)

Mag

nitu

de

00

05

10

15

2010

20

30

40

BMI

WH

R

WH

tR CI AVI

VAI


P = 0011

P lt 0001

P lt 0001

P lt 0001

P lt 0001

P lt 0001

(d)






0

50

100


Solu

ble l

evels

of s

CD36

(ng

mL)


P = 00200

P = 00220

(a)

0

300

600

900

1200

1500

1800



P = 00020

Solu

ble l

evels

of s

LOX-

1(p

gm

L)

(b)


00

05

10

15

20

25

11 foldtimes

54less


Relat

ive e

xpre

ssio

n of

CD36

(2minusΔΔ

C T)

(c)













5 Conclusions


Competing Interests


Acknowledgments


References

































































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of








































Measurements
















4 Discussion










0

2

4

6

8

TCH

DLc

Mag

nitu

de

LDLc

HD

Lc

TGH

DLc

Apo-

A1

Apo-

B

HO

MA-


P = 0003

P = 0049

P = 0005

P = 0040

(a)M

agni

tude

00

05

10

1510

20

30

40

BMI

WH

R

WH

tR CI AVI

VAI


P = 0040

P lt 0001

P lt 0001P lt 0001

P lt 0001

P lt 0001

(b)

Mag

nitu

de


0

2

4

6

8

TCH

DLc

LDLc

HD

Lc

TGH

DLc

Apo-

A1

Apo-

B

HO

MA-

IR

P = 0023

(c)

Mag

nitu

de

00

05

10

15

2010

20

30

40

BMI

WH

R

WH

tR CI AVI

VAI


P = 0011

P lt 0001

P lt 0001

P lt 0001

P lt 0001

P lt 0001

(d)






0

50

100


Solu

ble l

evels

of s

CD36

(ng

mL)


P = 00200

P = 00220

(a)

0

300

600

900

1200

1500

1800



P = 00020

Solu

ble l

evels

of s

LOX-

1(p

gm

L)

(b)


00

05

10

15

20

25

11 foldtimes

54less


Relat

ive e

xpre

ssio

n of

CD36

(2minusΔΔ

C T)

(c)













5 Conclusions


Competing Interests


Acknowledgments


References

































































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of

















0

2

4

6

8

TCH

DLc

Mag

nitu

de

LDLc

HD

Lc

TGH

DLc

Apo-

A1

Apo-

B

HO

MA-


P = 0003

P = 0049

P = 0005

P = 0040

(a)M

agni

tude

00

05

10

1510

20

30

40

BMI

WH

R

WH

tR CI AVI

VAI


P = 0040

P lt 0001

P lt 0001P lt 0001

P lt 0001

P lt 0001

(b)

Mag

nitu

de


0

2

4

6

8

TCH

DLc

LDLc

HD

Lc

TGH

DLc

Apo-

A1

Apo-

B

HO

MA-

IR

P = 0023

(c)

Mag

nitu

de

00

05

10

15

2010

20

30

40

BMI

WH

R

WH

tR CI AVI

VAI


P = 0011

P lt 0001

P lt 0001

P lt 0001

P lt 0001

P lt 0001

(d)






0

50

100


Solu

ble l

evels

of s

CD36

(ng

mL)


P = 00200

P = 00220

(a)

0

300

600

900

1200

1500

1800



P = 00020

Solu

ble l

evels

of s

LOX-

1(p

gm

L)

(b)


00

05

10

15

20

25

11 foldtimes

54less


Relat

ive e

xpre

ssio

n of

CD36

(2minusΔΔ

C T)

(c)













5 Conclusions


Competing Interests


Acknowledgments


References

































































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of

















0

50

100


Solu

ble l

evels

of s

CD36

(ng

mL)


P = 00200

P = 00220

(a)

0

300

600

900

1200

1500

1800



P = 00020

Solu

ble l

evels

of s

LOX-

1(p

gm

L)

(b)


00

05

10

15

20

25

11 foldtimes

54less


Relat

ive e

xpre

ssio

n of

CD36

(2minusΔΔ

C T)

(c)













5 Conclusions


Competing Interests


Acknowledgments


References

































































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of
























5 Conclusions


Competing Interests


Acknowledgments


References

































































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of





































































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of
















research article low cd36 and lox-1 levels and cd36 gene...

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