Hypertriglyceridemic Waist Phenotype

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Hypertriglyceridemic Waist PhenotypePredicts Increased Visceral Fat in Subjects

With Type 2 Diabetes

SUSAN SAM, MD1

STEVEN HAFFNER, MD2

MICHAEL H. DAVIDSON, MD3

RALPH B. DAGOSTINO SR., MD4

STEVEN FEINSTEIN, MD5

GEORGE KONDOS, MD6

ALFONSO PEREZ, MD7

THEODORE MAZZONE, MD1

OBJECTIVE Greater accumulationof visceral fat is stronglylinked to risk of cardiovasculardisease. However, elevated waist circumference by itself does not always identify individualswith increased visceral fat.

RESEARCH DESIGN AND METHODS We examined 375 subjects with type 2diabetes from the CHICAGO cohort for presence of hypertriglyceridemic waist phenotype (waistcircumference90 cm in men or85 cm in women, in conjunction with a plasma triglycerideconcentration of177mg/dl) to determine its usefulness for identifying subjects with increased

amounts of visceral fat. We divided subjects into three groups: group 1 (low waist circumferenceand low triglycerides; waist circumference90cminmenor85 cm in womenand triglyceride177 mg/dl, n 18), group 2 (high waist circumference and low triglycerides; waist circum-ference 90 cm in men or 85 cm in women and triglycerides 177 mg/dl, n 230), andgroup 3 (high waist circumference and high triglycerides; waist circumference 90 cm in menor85 cm in women and triglycerides 177 mg/dl, n 127).

RESULTS Subjects in group 3 had significantly higher visceral fat (P 0.0001), A1C (P0.01), and coronary artery calcium (P 0.05) compared with group 2, despite similar age, BMI,and waist circumference. The relationship of the phenotype to atherosclerosis, however, wasattenuated by adjustment for HDL cholesterol, triglyceride-rich lipoprotein cholesterol, apoli-poprotein B, or LDL particle number.

CONCLUSIONS The presence of hypertriglyceridemic waist phenotype in subjects withtype 2 diabetes identifies a subset with greater degree of visceral adiposity. This subset also has

greater degree of subclinical atherosclerosisthat may be related to the proatherogenic lipoproteinchanges.

Diabetes Care 32:19161920, 2009

Despite the strong association of obe-sity, especially abdominal obesity,to metabolic and cardiovascular

disease, not all obese individuals carry thesame metabolic and cardiovascular risk(1,2). The metabolic syndrome (a clusterof metabolic abnormalities that includeglucose intolerance, central obesity, dys-

lipidemia, and hypertension) has beenused to identify individuals at high riskfor type 2 diabetes and cardiovascular dis-ease (3,4). A hypertriglyceridemic waistphenotype defined as an elevated waistcircumference (90 cm in men or 85cm in women) along with an elevatedplasma triglyceride concentration (de-

fined as a level 177 mg/dl) has beenproposed and shown to be a strongermarker of cardiovascular risk and a betterpredictor of cardiovascular disease thanthe metabolic syndrome in nondiabeticsubjects (5,6). Deposition of visceral fatmay be most closely linked to the meta-bolic and cardiovascular risk associatedwith both the metabolic syndrome and thehypertriglyceridemic waist phenotype (6).

The CHICAGO cohort is a well-characterized group of men and womenwith type 2 diabetes who had measure-ments of abdominal fat depots by com-puted tomography (CT) and coronaryartery calcium (CAC) by electron-beamtomography (79). We evaluated theprevalence of hypertriglyceridemic waistphenotype in this cohort and report itsusefulness for identifying subjects withdiabetes who have higherlevels of visceralfat. We further examined the metabolicand cardiovascular impact of this pheno-type in subjects with type 2 diabetes.

RESEARCH DESIGN AND

METHODS Subjects for the current

analysis were non-Hispanic white (n 246) and non-Hispanic black participants(n 129) in the CHICAGO trial, a pro-spective study of the effects of pioglita-zone compared with glimepiride oncarotid intima-media thickness in sub-

jects with type 2 diabetes recruited from28 clinical sites in Chicago (79). The de-tails of the study have been previously re-ported (79). Data included in this reportwere obtained prior to randomization totreatment groups. All subjects wereasymptomatic for coronary artery disease

at baseline. The study was approved bycentral and local institutional reviewboard committees, and all participantsprovided written informed consent. Allsubjects underwent measurements ofheight, weight, and waist and hip circum-ference by a trained nurse at the baselinevisit. Waist circumference was mea-sured at the level of umbilicus to thenearest 0.1 cm. BMI was calculated asweight in kilograms divided by thesquare of height in meters.

Subjects underwent an abdominal CTscan for determination of visceral adipose

From the 1Department of Medicine, Section of Endocrinology, Diabetes and Metabolism, University ofIllinois, Chicago, Illinois; the 2Department of Medicine, University of Texas Health Science Center, San

Antonio, Texas; the 3Pritzker School of Medicine, University of Chicago, Chicago, Illinois; the 4Depart-ment of Mathematics, Statistics and Consulting Unit, Boston University, Boston, Massachusetts; the5Department of Medicine, Section of Cardiology, Rush University Medical Center, Chicago, Illinois; the6Department of Medicine, Section of Cardiology, University of Illinois College of Medicine, Chicago,Illinois; and 7Takeda Global Research and Development, Deerfield, Illinois.

Corresponding author: Susan Sam, [email protected] 3 March 2009 and accepted 7 July 2009.Published ahead of print at http://care.diabetesjournals.org on 10 July 2009. DOI: 10.2337/dc09-0412. 2009 by the American Diabetes Association. Readers may use this article as long as the work is properly

cited, the use is educational and not for profit, and the work is not altered. See http://creativecommons.org/licenses/by-nc-nd/3.0/ for details.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be herebymarked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

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tissue (VAT) and subcutaneous adiposetissue (SAT), as previously described (9).Fasting blood samples were obtained atthe baseline visit for measurements of

A1C, lipid panel, and LDL particle num-ber by previously described techniques(7,8). Triglyceride-rich lipoprotein (TRL)cholesterol was calculated by subtracting

the directly measured values for LDL andHDL cholesterol from total cholesterol.Non-HDL cholesterol was calculated bysubtracting the directly measured valuesfor HDL cholesterol from total choles-terol. CAC was determined using previ-ously described techniques (8).

Statistical methods

The cohort was divided into three pheno-types based on criteria for hypertriglycer-idemic waist: group 1 included subjectswith waist circumference90 cm in men

or

85 cm in women and triglyceride lev-els 177 mg/dl, group 2 included sub-jects with waist circumference90 cm inmen or 85 cm in women and triglycer-ide levels 177 mg/dl, and group 3 (hy-pertriglyceridemic waist) includedsubjects with waist circumference 90cm in men or 85 cm in women andtriglyceride levels177 mg/dl (5). Therewas only one subject who had an elevatedtriglyceride level and low waist circumfer-ence. Analyses were performed with in-clusion of thatsubject in group 2 (sincehehad intermediate phenotype) but were

also repeated after exclusion of that subject, which did not impact any of ourresults.

Log transformation of the data wasperformed when necessary to achieve ho-mogeneity of variance. Age, BMI, andwaist circumference were compared us-ing ANCOVA with Bonferonni post hocanalysis to evaluate the differences amongthe three groups. Categorical variablesamong the three groups were comparedusing 2 analysis. Differences in LDL,HDL, and TRL cholesterol and VAT, SAT,

total abdominal fat (TAT), A1C, and CACscores were examined using general linearmodel with Bonferonni analysis to com-pare the differences among the threegroups. These analyses were also adjustedfor age, BMI, sex, diabetes treatment,years of smoking, insulin use, duration ofdiabetes, and use of statins. Analyses for

VAT, SAT, and TAT were also performedseparately for each sex. Since racial differ-ences in VAT have been reported, withblacks having lower amount of VAT com-pared with whites (10), we examined theimpact of race on the usefulness of the

hypertriglyceridemic waist phenotype for

identifying subjects with increased vis-ceral fat. To do this, we examined the re-lationship between the phenotype andabdominal fat distribution separately foreach race and performed a test of hetero-geneity for the relation between race andhypertriglyceridemic waist phenotypeand body fat distribution. The analysesfor the relationship between body distri-bution and CAC score were further ad-

justed for A1C, HDL cholesterol, TRLcholesterol, non-HDL cholesterol, apoli-poprotein (apo) B, and LDL particle num-

ber. Analyses were performed using the11.0 PC package of SPSS statistical soft-ware (SPSS, Chicago, IL). A P 0.05 wasconsidered significant.

RESULTS The cohort was dividedinto three groups based on the criteria forhypertriglyceridemic waist (5). The base-line characteristics of the three groups aresummarized on Table 1. The mean age forgroup 1 was 67 years, for group 2 was 61years, and for group 3 was 60 years. Sub-

jectsin group 1 were older compared withsubjects in groups 2 and 3 (P 0.002).

The average BMI for group 1 was 24.7

2.8 kg/m2

, for group 2 was 33.0 4.9kg/m2, and for group 3 was 32.5 4.6kg/m2. The average waist circumferencefor group 1 was 81.4 5.0 cm, for group2 was 109.1 12.0 cm, and for group 3was 108.6 10.9 cm. Subjects in group 1were leaner (P 0.0001) and had lowerwaist circumference (P 0.0001) com-pared with subjects in groups 2 and 3.There were no differences in age, BMI, orwaist circumference between subjects ingroups 2 and 3.

Thirty-nine percent of subjects in

group 1 were men compared with 61% ingroup 2 and 65% in group 3, but thesedifferences were not statistically signifi-cant (Table 1). There were no differencesin smoking status, duration of diabetes, orstatin use among the three groups (Table1). There were differences in diabetestherapy among the three groups, with ahigher percentage of subjects in group 3not taking any diabetes medication (21%)compared with group 1 (11%) and group2 (12%). Furthermore, fewer subjects ingroup 3 were taking insulin (3%) com-pared with group 1 (22%) and with group

Table 1Baseline characteristics of study participants based on hypertriglyceridemic waist

phenotypes

Group 1 Group 2 Group 3

n 18 230 127

Age (years) 67 10* 61 8 60 7BMI (kg/m2) 24.7 2.8 33.0 4.9 32.5 4.6

Waist circumference (cm) 81.4 5.0 109.1 12.0 108.6 10.9Duration of type 2 diabetes (months) 121 159 94 83 86 79

A1C (%) 7.0 0.8 7.3 0.9 7.6 1.1Sex (%)

Men 39 61 65 Women 61 39 35

Smoking (%)Current 17 15 15

Former 50 48 54Never 33 37 31

Diabetes therapy (%)None 11 12 21

Sulfonylurea 17 16 15Metformin 28 25 36

Sulfonylurea and metformin 22 34 25Insulin 22 13 3

Statin use (%)On statin 50 53 60

No statin 50 47 40

Data are means SD or percent. Group 1 (low waist circumference and low triglycerides; waist circumfer-ence90 cm in men or 85 cm in women and triglycerides 177 mg/dl); group 2 (high waist circumfer-ence and low triglycerides; waist circumference 90 cm in men or 85 cm in women and triglycerides177 mg/dl, n 230); and group 3 (high waist circumference and high triglycerides; waist circumference90 cm in men or 85 cm in women and triglyceride 177 mg/dl, n 127). *P 0.05 vs. groups 2 and3; P 0.0001 vs. group 1; P 0.01 vs. groups 1 and 2; P 0.01 vs. group 2.

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2 (13%), and more subjects in group 3were taking metformin-only therapy(36%) compared with groups 1 (28%)

and 2 (25%).Differences in lipid profile are dem-onstrated in Table 2. Level of TRL choles-terol was higher in group 3 comparedwith group 1 (P 0.0001) and group 2(P 0.0001) (Table2). Level of non-HDLcholesterol and apoB were higher ingroup 3 compared with group 1 (P 0.001 for both non-HDL and apoB) andgroup 2 (P 0.0001 for both non-HDLand apoB) (Table 2). There were no dif-ferences in LDL cholesterol levels amongthe three groups (Table 2). HDL choles-terol levels were higher in group 1 com-

pared with group 2 (P 0.01) and group3 (P 0.0001). HDL cholesterol levelswere also significantly higher in group 2compared with group 3 (P 0.0001) (Ta-ble 2). LDL particle number was higher ingroup 3 (1,709 563) compared withgroup 2 (1,369 500; P 0.0001) andwith group 1 (1,254 450; P 0.001)(data not shown).

Table 3 summarizes the differences inbody fat distribution among the threegroups. Subjects in group 1 had signifi-

cantly lower TAT and VAT comparedwith subjects in both groups 2 and 3 (P0.0001 for all comparisons), while SATdid not differ among the three groups inadjusted analyses. Despite similar BMIand waist circumference in groups 2 and3 (Table 1), subjects in group 2 had sig-nificantly lower VAT (P 0.0001) com-pared with those in group 3 (Table 3).These differences in VAT and TAT amonggroups persisted after adjustment for

A1C, apoB levels, LDL particle number,HDL cholesterol, TRL cholesterol, andnon-HDL cholesterol. Furthermore, sim-

ilar results were obtained if each sex wasexamined separately. Since the racialmakeup of groups 2 and 3 were differentin our sample (42% of group 2 are blackvs. 16% of group 3) and race has beenreported to influence abdominal fat dis-tribution (10), we examined the differ-ences in VAT among groups separately foreach race. For whites and blacks exam-

ined separately, subjects in group 3 hadgreater amounts of visceral fat comparedwith those in group 2, even after adjust-ment for age, BMI, smoking years, dura-tion of diabetes, sex, and statin use(similar to findings for the combinedgroup). Furthermore, tests of heterogene-ity were not significant for the interaction

between race, hypertriglyceridemic waist,and visceral fat. These results indicate thatthe hypertriglyceridemic waist phenotypecan be useful for identifying both whiteand black subjects with increased visceralfat.

Subjects in group 3 had the highest A1C level (7.6 1.1) compared withgroup 2 (7.3 0.9; P 0.01) and group1 (7.0 0.8; P 0.01), after adjustmentfor age, BMI, diabetes therapy, insulinuse, duration of diabetes, years of smok-ing, and statin use. CAC scores were

higher in group 3 (255

77) comparedwith group 2 (218 48) (P 0.03), afteradjustments for age, BMI, diabetes ther-apy, insulin use, duration of diabetes,years of smoking, and statin use. Therewas no difference in CAC between group1 (202 168) and the other two groups,which is most likely related to the smallsample size. The difference in CAC scoresbetween groups 2 and 3 remained signif-icant after addition of A1C to the model(P 0.05, data not shown). However,differences in CACscores between groups2 and 3 were no longer present after fur-

ther adjustment for HDL cholesterol (P0.1), TRL cholesterol (P 0.6), non-HDLcholesterol (P 0.2), apoB levels (P 0.2), or LDL particle number (P 0.3)(data not shown). HDL cholesterol was apredictor of CAC in a model adjusted forage, BMI, diabetes therapy, insulin use,duration of diabetes, years of smoking,and statin use. However, its predictivevalue was lost after addition of hypertri-glyceridemic waist phenotype or TRLcholesterol to the model. TRL cholesterolwas a strong independent predictor of

CAC even after addition of hypertriglyc-eridemic waist phenotype and HDL cho-lesterol to the model (P 0.004, data notshown).

CONCLUSIONS In this study, wefound that in a large well-characterizedcohort of obese subjects with type 2 dia-betes, the presence of elevated triglycer-ides, along with an elevated waistcircumference (both defined as proposedfor the hypertriglyceridemic waist pheno-type in nondiabetic subjects) (5,6), iden-tifies a subgroup with higher amount of

Table 2Comparison of lipid profile based on hypertriglyceridemic phenotype

Group

Triglycerides

(mg/dl)

LDL

cholesterol(mg/dl)

HDL

cholesterol(mg/dl)

TRL

cholesterol(mg/dl)

Non-HDL

cholesterol(mg/dl)

ApoB(mg/dl)

1 (n 18) 114 381 109 156 61 58 19 17 129 34 80 302 (n 230) 117 111 110 45 51 17* 19 17 130 30 80 30

3 (n 127) 270 185 119 75 42 23 40 23 159 45 100 30Data are means SD. Group 1 (low waist circumference and low triglyceride; waist circumference 90 cmin men or 85 cm in women and triglycerides 177 mg/dl); group 2 (high waist circumference and lowtriglyceride; waist circumference 90 cm in men or85 cm in women and triglycerides 177 mg/dl, n230); and group 3 (high waist circumference and high triglyceride; waist circumference 90 cm in men or85 cm in women and triglycerides177 mg/dl, n 127). Analysis is adjusted for age, BMI, sex, diabetestreatment, years of smoking, insulin use, duration of diabetes, and use of statins. TRL cholesterol wascalculated by subtracting the directly measured values for LDL and HDL cholesterol from total cholesterol.Non-HDL cholesterol was calculated by subtracting the directly measured values for HDL cholesterol fromtotal cholesterol. *P 0.01 vs. group 1; P 0.0001 vs. groups 1 and 2; P 0.01 vs. groups 1 and 2.

Table 3Body fat distributions based on hypertriglyceridemic waist phenotypes

Group

TAT (cm3) TAT (cm3) VAT (cm3) VAT (cm3) SAT (cm3)SAT

(cm3)

Unadjusted Adjusted Unadjusted Adjusted Unadjusted Adjusted

1 (n 18) 173 47 292 780 62 24 95 54 112 36 204 622 (n 230) 330 101 316 85* 128 57 117 60* 205 84 204 71

3 (n 127) 337 85 340 94* 149 51 150 67 194 61 195 73

Data aremeans SD andadjustedmeansSD with P value only reported for adjusted means.Group1 (lowwaist circumference and low triglyceride; waist circumference 90 cm in men or 85 cm in women andtriglycerides177 mg/dl); group2 (highwaist circumference and low triglyceride; waistcircumference90cm in men or 85 cm in women and triglycerides 177 mg/dl, n 230); and group 3 (high waistcircumference and high triglyceride; waist circumference 90 cm in men or 85 cm in women andtriglycerides177 mg/dl, n 127). Analyses forTAT, VAT, andSAT areadjustedfor age, BMI, sex, diabetestreatment, years of smoking, insulin use, duration of diabetes, and use of statins. * P 0.0001 vs. group 1;P 0.0001 vs. groups 1 and 2.

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visceral fat. The relationship remained af-ter adjustment for multiple factors includ-ing age, sex, BMI, duration of diabetes,years of smoking, diabetes therapy, insu-lin, A1C, and statin use.

The existence of benign obesity oroverweight andobese individuals who aremetabolically healthy is well recognized

(1,2). A recent study indicates that amongthe National Health and Nutrition Exam-ination Survey cohort, 51% of overweightand 32% of the obese adults are metabol-ically healthy. Furthermore, in this study,waist circumference was not different be-tween the two obese subgroups (metabol-ically healthy versus those with metabolicabnormalities) (1). The relation of waistcircumference to abdominal adiposity iscomplicated as this measurement corre-lates well with theamount of total abdom-inal fat but cannot distinguish between

subcutaneous and visceral adiposity. Nu-merous epidemiologic, as well as physio-logic, studies have suggested that visceralfat is more strongly associated with meta-bolic risk factors as well as cardiovasculardisease than subcutaneous abdominal fat(6,11). For instance, individuals matchedfor subcutaneous abdominal fat, but withdifferent degrees of visceral fat, have beenshown to have markedly different levelsof insulin resistance and glucose tolerance(12). Surgical removal of abdominal sub-cutaneous fat in obese subjects did notresult in metabolic improvements or ben-

eficial changes in cardiovascular risk fac-tors (13). Conversely, removal of visceralfat has led to metabolic improvements(14). Adipose tissue has been shown tosecrete a number of inflammatory media-tors (15), and visceral adipose tissue hasbeen shown to secrete higher quantities ofthese inflammatory cytokines (15,16).Hence, visceral fat may be thedistinguish-ing factor separating metabolicallyhealthy obese individuals from obese in-dividuals who are not metabolicallyhealthy.

Several investigators, including us,have demonstrated that an increase in thesize of visceral fat depot is associated withmetabolic syndrome, inflammation, dys-lipidemia, and coronary artery disease(1720). Measurement of visceral fat de-pot requires imaging techniques such asCT or magnetic resonance imaging thatare not practical screening tools for thegeneral population due to cost and radia-tion exposure. The concept of a hypertri-glyceridemic waist has been proposed byDespres and colleagues (5,6) for identify-ing viscerally obese individuals at risk for

cardiovascular disease. This group advo-cates that a fasting plasma triglyceridelevel of177 mg/dl in conjunction withabdominal obesity (waist circumference90 cm in men and 85 cm in women)is a better predictor of metabolic and car-diovascular risk than the metabolic syn-drome (5,6). In a study by another group

of investigators (21), among the NationalCholesterol Education Program (NCEP)criteria for metabolic syndrome, waist cir-cumference and triglyceride levels bestcorrelated to visceral adiposity and insu-lin resistance. The results of the currentstudy confirm that simultaneous mea-surement of fasting triglycerides and waistcircumference is a useful approach foridentifying subjects with the greatestamount of visceral fat even among obesesubjects with type 2 diabetes.

CAC measured by electron-beam to-

mography is a measure of total coronaryatherosclerosis that has been validated bycoronary angiogram (22). The amount ofCAC has been shown to correlate wellwith the amount of atherosclerotic plaquein patients with type 2 diabetes (23). Inlarge prospective studies, CAC has beenfound to be a significant predictor of car-diovascular disease in symptomatic andasymptomatic subjects (24). In the cur-rent study, we demonstrate that subjectswith greater degree of visceral adipositybased on hypertriglyceridemic waist, in-dependent of many factors including gly-

cemic control, had the highest CACscore.The difference in CAC between groups 2and 3 was significant but perhaps not aslarge as might be expected given the moreprofound metabolic abnormalities in thelatter group (Table 2). This could be re-lated to an overall higher prevalence ofCAC in type 2 diabetes compared withnondiabetic subjects (25). Nonetheless,subjects in group 3 had significantlyhigher amount of CAC compared withthose in group 2, though both groups hadsimilar BMI and waist circumference.

However, the relationship between thehypertriglyceridemic phenotype andCAC was not present after adjustmentsfor HDL cholesterol, non-HDL choles-terol, TRL cholesterol, LDL particle num-ber, or apoB. In a previous study of theCHICAGO cohort (8), our group hasreported that visceral adipose tissuepredicted CAC but not after adjustmentfor TRL cholesterol. Due to the cross-sectional nature of this study, we are notable to make any conclusions regardingthe causal nature of the associationsobserved.

In this study, A1C was highest in thesubset with hypertriglyceridemic waist(group 3). These differences were presenteven after adjustment for a number ofconfounders including age, sex, BMI, di-abetes therapy, duration of diabetes, yearsof smoking, and use of insulin and statins.

A higher percentage of subjects with hy-

pertriglyceridemic waist phenotype weretreated with metformin, and fewer weretreated with either insulin or sulfonylureacompared with those with lower triglyc-eride levels and elevated waist circumfer-ence. The reasons for these differences intherapy are not clear; however, all of theanalyses in our report were adjusted fordiabetes therapy and insulin use.

In summary, our results indicate thateven in the presence of type 2 diabetes, anelevated waist circumference, by itself,does not identify subjects with the highest

accumulation of visceral fat. Addition offasting triglyceride levels to waist circum-ference is a simple and inexpensivemethod for clinicians to identify thosewith greatest amount of visceral fat andthus greatest metabolic and cardiovascu-lar risk. In diabetes, the association of thehypertriglyceridemic waist phenotypewith coronary atherosclerosis may be re-lated to the proatherogenic lipoproteinchanges associated with the phenotype.

Acknowledgments The CHICAGO study

was sponsored and funded by Takeda GlobalResearch and Development. The analysis inthis manuscript was supported by grant DK71711 from the National Institutes of Health(to T.M.), an unrestricted grant from TakedaGlobal and Development, and by an institu-tional award from the University of Illinois atChicago.S.S.hadfullaccessto all ofthe data inthe study and takes responsibility for the in-tegrity of the data and the accuracy of the dataanalysis.

S.F. has received honoraria from TakedaPharmaceuticals. A.P. is an employee ofTakeda Global Research and DevelopmentCenter, the institution that sponsored the

CHICAGO trial. No other potential conflictsof interest relevant to this article werereported.

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Hypertriglyceridemic waist in type 2 diabetes


Hypertriglyceridemic Waist Phenotype

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