UBC Faculty Research and Publications

The association between "hypertriglyceridemic waist" and sub-clinical atherosclerosis in a multiethnic… Gasevic, Danijela; Carlsson, Axel C; Lesser, Iris A; Mancini, GB J; Lear, Scott A Feb 23, 2014

Your browser doesn't seem to have a PDF viewer, please download the PDF to view this item.

Item Metadata


52383-12944_2013_Article_1040.pdf [ 304.63kB ]
JSON: 52383-1.0167785.json
JSON-LD: 52383-1.0167785-ld.json
RDF/XML (Pretty): 52383-1.0167785-rdf.xml
RDF/JSON: 52383-1.0167785-rdf.json
Turtle: 52383-1.0167785-turtle.txt
N-Triples: 52383-1.0167785-rdf-ntriples.txt
Original Record: 52383-1.0167785-source.json
Full Text

Full Text

RESEARCH Open AccessThe association between “hypertriglyceridemicwaist” and sub-clinical atherosclerosis in amultiethnic population: a cross-sectional studyDanijela Gasevic1*, Axel C Carlsson2,3, Iris A Lesser1, GB John Mancini4,5 and Scott A Lear1,5,6AbstractBackground: “Hypertriglyceridemic waist” (HTGW) phenotype, an inexpensive early screening tool for detection ofindividuals at risk for type 2 diabetes and cardiovascular disease was found to be associated with subclinicalatherosclerosis in various patient populations such as those with diabetes mellitus, chronic kidney disease, andthose infected with human immunodeficiency virus. However, less is known regarding an association betweenHTGW and subclinical atherosclerosis in the apparently healthy, multiethnic population. Therefore, the aim of thestudy was to explore the association between HTGW and sub-clinical atherosclerosis in an apparently healthy,multiethnic population; and to investigate whether the effect of HTGW on sub-clinical atherosclerosis persists overand above the traditional atherosclerosis risk factors.Methods: We studied 809 individuals of Aboriginal, Chinese, European and South Asian origin who were assessedfor indices of sub-clinical atherosclerosis (intima-media thickness (IMT), total area and presence of carotid plaques),socio-demographic and lifestyle characteristics, anthropometrics, lipids, glucose, blood pressure, and family historyof cardiovascular disease.Results: We found that, compared to individuals without HTGW and after adjusting for age, ethnicity, smoking, andphysical activity; men and women with HTGW had a significantly higher: IMT (men: B (95%CI = 0.084 (0.037, 1.133),p < 0.001; women: B (95%CI) = 0.041 (0.006, 0.077), p = 0.020); and total area (men: B (95%CI = 0.202 (0.058, 0.366),p = 0.005; women: B (95%CI) = 0.115 (0.006, 0.235), p = 0.037). The association between HTGW waist and presence ofplaques was significant for men (OR (95%CI) = 1.904 (1.040, 3.486), p = 0.037 vs. men without HTGW), but not forwomen (p = 0.284). Once analyses were adjusted for additional, traditional risk factors for atherosclerosis, the effectof HTGW on sub-clinical atherosclerosis was no longer significant.Conclusions: In conclusion, HTGW may serve as an early marker of subclinical atherosclerosis in men and women,irrespective of ethnicity. However, once individuals are assessed for all traditional risk factors for atherosclerosis, theadditional assessment for HTGW is not warranted.Keywords: Hypertriglyceridemic waist, Sub-clinical atherosclerosis, Intima-media thickness, Atherosclerotic plaque,Ethnicity* Correspondence: danijela.gasevic@gmail.com1Department of Biomedical Physiology and Kinesiology, Simon FraserUniversity, 2600-515 W Hastings Street, Vancouver V6B 5K3, BC, CanadaFull list of author information is available at the end of the article© 2014 Gasevic et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the CreativeCommons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, andreproduction in any medium, provided the original work is properly credited. The Creative Commons Public DomainDedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article,unless otherwise stated.Gasevic et al. Lipids in Health and Disease 2014, 13:38http://www.lipidworld.com/content/13/1/38BackgroundAtherosclerosis is a chronic progressive disease associatedwith high cardiovascular morbidity and mortality [1]. Thediagnosis of atherosclerosis in its subclinical stage (sub-clinical atherosclerosis) is important, as it would allow forearly implementation of lifestyle prevention programs thatmay help prevent further progression and cardiovascularevents [2]. Various invasive and non-invasive arterialimaging techniques (such as intravascular sonography,B-mode ultrasonography, computed tomography andmagnetic imaging) have been developed to detect anddiagnose sub-clinical atherosclerosis [1]. A commonlyused technique is a non-invasive B-mode ultrasonographythat can determine the thickness of the intima-medialayers (intima-media thickness, IMT) and characterizefocal plaques. Thus, IMT carotid ultrasound is an estab-lished non-invasive method for detection of early ath-erosclerotic disease [3]. Longitudinal studies have showna strong association between IMT and future risk of myo-cardial infarction and stroke [3,4], while in clinical trialsIMT is often used to evaluate the effects of coronaryheart disease risk factor interventions on atheroscleroticburden [5].Obesity, an independent predictor of cardiovasculardisease (CVD) [6,7] has been found to be associated withabnormal IMT. Namely, positive associations were re-ported between IMT and general obesity as measured bybody mass index (BMI) [8], as well as between IMT andabdominal obesity as depicted by waist circumference(WC) and waist-to-hip ratio [8-10] or visceral adipose tis-sue [11]. Moreover, “hypertriglyceridemic waist” (HTGW)phenotype, an inexpensive early screening tool for detec-tion of individuals at risk for type 2 diabetes and CVD thattakes into account WC and fasting triglycerides (TG)[12-14] was found to be associated with subclinical athero-sclerosis in various patient populations such as those withdiabetes mellitus [15,16], chronic kidney disease [17], andthose infected with human immunodeficiency virus [18].However, less is known regarding an association betweenHTGW and subclinical atherosclerosis in the apparentlyhealthy, multiethnic population. Therefore, the purpose ofthis study was to investigate whether HTGW is associatedwith measures of sub-clinical atherosclerosis (IMT, pres-ence of plaques, and total area (a composite of IMT andplaque area)) in a multi-ethnic primary prevention cohortof men and women without pre-existing diabetes orCVD; and to explore whether this association remainsafter taking into account the traditional risk factors foratherosclerosis.MethodsStudy populationIndividuals were recruited as part of the Multi-CulturalCommunity Health Assessment Trial (M-CHAT), a studyinitially designed to investigate ethnic differences in bodyfat accumulation and how these relate to diabetes andCVD risk [19]. Men and women of self-reported Abori-ginal, Chinese, European, and South Asian origin be-tween 30 and 65 years of age, with no weight change ofmore than 2 kg in three months before assessment date,and with no diagnosed CVD or on medications to treatCVD-related risk factors were eligible to participate inthe study. Individuals of Chinese, European, and SouthAsian origin had to be living in Canada for more thanthree years and had to be third-generation Canadian orless in order to limit possible differences in acculturationamong the immigrant groups. Individuals of Aboriginalorigin were eligible for the study if they reported to haveat least three grandparents of exclusive Aboriginal descent.Within each ethnic group, participants were recruitedacross ranges of BMI (≤24.9 (lower range), 25.0-29.9 (mid-dle range) and ≥30 (upper range)) to examine CVD associ-ations within a range of body sizes. However, there was adifficulty in identifying Aboriginal men with a BMI of lessthan 25, so Aboriginal men of any BMI were recruited.Similarly, we encountered a difficulty in the recruitmentof Chinese individuals with a BMI of 30 and over; there-fore, the target for the upper BMI range for Chinese studyparticipants was changed to a BMI ≥28. Despite thesemodifications, the study multiethnic cohort had suffi-cient variation in BMI values within each ethnic group.All participants provided written informed consent forthe study, and the study was approved by the SimonFraser University Research Ethics Board.Participant assessmentStudy participants were assessed for demographics, an-thropometry, health-related behaviours, lipids, and sub-clinical atherosclerosis. Body mass index was calculatedas weight in kilograms divided by height in metressquared. Waist circumference was measured at thepoint of maximal narrowing of the waist, and an averageof two measures was calculated and recorded in centi-metres. Smoking status (smoker vs. former smoker/neversmoker) was self-reported. Physical activity was deter-mined by self-report, measured using the ModifiablePhysical Activity questionnaire previously used in multi-ethnic populations [20,21], and reported as the averageminutes per week of leisure physical activity over the pre-vious year. A fasting blood sample was obtained from eachstudy participant, and TG were measured using a standardprotocol by the ADVIA 1650 analyzer (Bayer Health Care,Morristown, NJ). The HTGW phenotype was defined asWC ≥ 85 cm and TG ≥ 1.5 mmol/L in females, andWC ≥ 90 cm and TG ≥ 2.0 mmol/L in males [22].Average carotid IMT, total area, and presence of pla-ques were assessed as indices of sub-clinical athero-sclerosis as previously described [23]. Briefly, carotidGasevic et al. Lipids in Health and Disease 2014, 13:38 Page 2 of 10http://www.lipidworld.com/content/13/1/38IMT was assessed by a scan of carotid arteries per-formed at the Prevention Clinic/Healthy Heart Programat St. Paul’s Hospital in Vancouver, Canada. Carotid arter-ies were examined bilaterally using a 7.5 MHz to 10 MHzlinear-array transducer (Image Point HX, Hewlett Packard,Andover, MA), and individual IMT measurements weretaken over a 10 mm segment in the far wall of the rightand left common coronary carotid artery within 2 cmproximal to the carotid bulb. The region with the thickestIMT, excluding areas with focal lesions, was measured. Allscans were thereafter transferred to the CardiovascularImaging Research Core Laboratory at Vancouver GeneralHospital to be digitized for analysis (Vascular Imager5.0, Medical Imaging Applications, LLC, Coralville, IA).The average IMT (mm) was derived from the right andleft IMT measurements. Plaques in any of the carotidsegments were measured. Plaques were identified, byconsensus of at least 2 observers, as wall thickness thatwas increased focally compared with IMT on either sideof the focal area. Total area (mm2), a superior measureof atherosclerotic burden than IMT alone [23], was cal-culated as the sum of IMT area (20 mm length x averageIMT for the measured length (mm)) and plaque area.Plaque area was equal to the average lesion thickness(mm) multiplied by lesion length (mm)). In case of mul-tiple plaques, average plaque thickness was calculatedby dividing the area of plaques (area of plaque 1 + areaof plaque 2 +…) by the total length of plaques (lengthof plaque 1 + length of plaque 2 +…). The intraclass andinterobserver correlation values for this method were0.922 to 0.948 and 0.850 to 0.901, respectively [23]. Forrepeated measures in the same subject, the accuracyand precision were −0.001 mm (not significant com-pared to 0.00 mm) and 0.04 mm, respectively, for IMTand −0.21 mm2 (not significant compared to 0.00 mm2)and 3.61 mm2, respectively, for total area. Of importance,given that our study population consisted of apparentlyhealthy individuals, about 50 percent of participants had nodetectible plaques. Consequently, instead of plaque size, weused presence of plaques variable (any plaque presentvs. plaques not present) as an outcome variable to iden-tify whether HTGW shows any association with plaquepresence in this multiethnic study population.Statistical analysesOut of 822 participants initially recruited for the M-CHATstudy, 13 participants were missing data for measuresof sub-clinical atherosclerosis. These individuals wereexcluded from the study, and the final sample consistedof 809 participants. Distribution of all continuous variableswas explored for normality, and non-normally distributedvariables (IMT, total area, TG, physical activity, fastingblood glucose, and systolic blood pressure) were trans-formed using the natural logarithm. Sex differences instudy characteristics were explored using an independ-ent t-test for continuous variables and Chi-square testfor categorical variables. The differences in study char-acteristics among individuals were stratified as follows:1) Without HTGW (WC and TG not elevated); 2) ElevatedTG (not elevated WC); 3) Elevated WC (not elevated TG)and 4) HTGW (elevated both TG and WC). These wereanalyzed using general linear models and Chi-square testsfor continuous and categorical variables, respectively.Multiple linear regression analyses were used to explorethe association of the stratified HTGW components withIMT and total area. Logistic regression analysis was uti-lized to explore the association between the stratifiedHTGW components and presence of plaques. Given thatthere was a significant interaction between the effect ofsex and effect of HTGW on IMT (p = 0.013), all regressionmodels were performed for men and women separately.However, no significant interaction between the effectof ethnicity and effect of HTGW on IMT was observed(p = 0.329), therefore, the analyses were not additionallystratified by ethnic group. All regression models wereadjusted for age, ethnicity, smoking and physical activ-ity. In order to explore whether the association betweenHTGW and indices of sub-clinical atherosclerosis re-mains after the adjustment for additional, traditionalrisk factors for atherosclerosis, the analyses were furtheradjusted for total cholesterol, high-density lipoproteincholesterol (HDL-C), fasting blood glucose, systolic bloodpressure and BMI. Regression models were explored formulticollinearity, and variance inflation indices and toler-ance statistics indicate no multicollinearity in our data. Allanalyses were performed using Statistical Package forSocial Sciences 19 (SPSS, Chicago, IL). P values ≤ 0.05were considered significant.ResultsBaseline characteristics of male and female participantsare shown in Table 1. Significantly higher cardiovascularrisk was seen among men demonstrated by larger WC,higher levels of TG, fasting blood glucose and systolicblood pressure, greater prevalence of HTGW, HDL-C,greater average carotid IMT, and larger total area. Further-more, compared to women, men were more likely to haveplaques present in carotid arteries.Characteristics of participating men, stratified by thepresence of HTGW components, are presented in Table 2.In men, HTGW phenotype was most prevalent amongSouth Asians (32.1%) and least prevalent among Chinese(17.9%). Furthermore, the greatest percentage of menwithout HTGW was highest among Chinese (37.3%)which was more than three times higher than that ofAboriginals. However, prevalence of Elevated TG pheno-type was about 20 times higher in Chinese men comparedto their Aboriginal and European counterparts. HighestGasevic et al. Lipids in Health and Disease 2014, 13:38 Page 3 of 10http://www.lipidworld.com/content/13/1/38BMI, fasting blood glucose and systolic blood pressure,and lowest HDL-C were observed among men withHTGW. In addition, IMT and total area were signifi-cantly higher in men with HTGW and Elevated WCphenotypes compared to their counterparts withoutHTGW and those with Elevated TG.Characteristics of participating women, stratified bythe presence of HTGW components, are presented inTable 3. Ethnic differences in the distribution of HTGWcomponents in women were similar to those in men withthe highest prevalence of Without HTGW and lowestprevalence of HTGW phenotypes being among Chinesewomen. Women with HTGW were about 5 times morelikely to smoke compared to women without HTGW. Inaddition, BMI, fasting blood glucose, systolic blood pres-sure, IMT and total area were significantly higher, whileHDL-C was significantly lower, in women with HTGWthan in those without HTGW.The association of HTGW with indices of sub-clinicalatherosclerosis among men after adjusting for age, eth-nicity, smoking, and physical activity is presented inFigure 1. Intima-media thickness was significantly higherin men with Elevated WC (B (95%CI = 0.059 (0.017,0.102), p = 0.005) and with HTGW (B (95%CI = 0.084(0.037, 1.133), p < 0.001) compared to their counterpartswithout HTGW. Similarly, larger total area (a compositeof IMT and plaque area) was observed among men withElevated WC ((B (95%CI = 0.124 (0.001, 0.261), p = 0.047)and HTGW ((B (95%CI = 0.202 (0.058, 0.366), p = 0.005)then among men without HTGW. No statistically signifi-cant difference in IMT and total area was observed be-tween men with Elevated TG and those without HTGW.Moreover, while no difference in prevalence of carotidartery plaques was noted between men without HTGWand those with Elevated TG and Elevated WC; prevalenceof carotid artery plaques was significantly higher amongmen with HTGW than among their counterparts withoutHTGW (OR (95%CI) = 1.904 (1.040, 3.486), p = 0.037).However, after additional adjustment for total cholesterol,HDL-C, glucose, systolic blood pressure, BMI, and familyhistory of CVD, traditional risk factors for atherosclerosis,the association of HTGW with indices of atherosclerosiswas no longer significant (Additional file 1).Figure 2 features the association of HTGW with indicesof sub-clinical atherosclerosis in women. After adjustingfor age, ethnicity, smoking, and physical activity, IMTwas significantly higher in women with Elevated TG (B(95%CI) = 0.051 (0.013, 0.090), p = 0.007), Elevated WC(B (95%CI) = 0.045 (0.015, 0.077), p = 0.003), and HTGW(B (95%CI) = 0.041 (0.006, 0.077), p = 0.020) than in womenWithout HTGW. Furthermore, total area of women withHTGW was significantly larger than that among womenWithout HTGW (B (95%CI) = 0.115 (0.006, 0.235), p =0.037). However, no significant difference in total area wasfound between women with Elevated TG and ElevatedWC and women Without HTGW. Additionally, presenceof carotid artery plaques among women with Elevated TG,Elevated WC and HTGW did not significantly differ fromtheir counterparts Without HTGW. Once analyses wereadditionally adjusted for traditional risk factors for athero-sclerosis, HTGW phenotype was no longer associatedwith IMT and total area (Figure 2, Additional file 2).DiscussionIn an apparently healthy multi-ethnic population of Abori-ginal, Chinese, European and South Asian men andwomen, we explored the association between HTGWTable 1 Baseline characteristics of the study populationCharacteristic Menn = 391Womenn = 418Significance (p)Age 46.6 ± 8.7 47.5 ± 8.8 0.130Ethnicity 0.885Aboriginal 90 (23.0%) 101 (24.2%)Chinese 101 (25.8%) 115 (27.5%)European 98 (25.1%) 99 (23.7%)South Asian 102 (26.1%) 103 (24.6%)Current smoker 50 (12.8%) 38 (9.1%) 0.058Family history ofCVD present (%)171 (43.7%) 186 (44%) 0.827Physical activity(min/week)225 (97, 444) 208 (95, 413) 0.171BMI 27.6 ± 4.3 27.4 ± 5.2 0.520Waist circumference(cm)92.7 ± 11.1 85.3 ± 12.1 < 0.001Total cholesterol(mmol/L)5.25 ± 0.97 5.24 ± 1.03 0.925HDL-C (mmol/L) 1.13 ± 0.29 1.43 ± 0.36 < 0.001Triglycerides(mmol/L)1.47 (0.99, 2.23) 1.18 (0.83, 1.63) < 0.001Without HTGW 134 (35.5%) 168 (40.8%) 0.008Elevated TG 31 (8.2%) 57 (13.8%)Elevated WC 128 (34.0%) 117 (28.4%)HTGW 84 (22.3%) 70 (17%)Glucose (mmol/L) 5.30 (5.00, 5.60) 5.10 (4.80, 5.40) < 0.001Systolic bloodpressure (mm Hg)117 (110, 124) 115 (106, 125) 0.035Intima-mediathickness (mm)0.68 (0.60, 0.77) 0.63 (0.58, 0.70) < 0.001Total area (mm2) 16.60(13.14, 23.99)14.24(12.00, 20.51)< 0.001Presence of plaque 213 (54.5%) 191 (45.7%) 0.008Categorical variables presented as n (%). Normally distributed continuousvariables presented as mean ± SD. Skewed continuous variables presented asmedian (25%, 75%). Sex differences in continuous and categorical variablesexplored by independent t-test and Chi-square test, respectively. HDL-C: high-density lipoprotein cholesterol; CVD: cardiovascular disease.Gasevic et al. Lipids in Health and Disease 2014, 13:38 Page 4 of 10http://www.lipidworld.com/content/13/1/38and indices of subclinical atherosclerosis. The findingsof our study indicate that HTGW was significantly andpositively associated with IMT and total area in both menand women. The positive association between HTGW andpresence of plaques was significant for men; but it did notreach statistical significance for women. Significant associ-ations between HTGW and indices of subclinical athero-sclerosis were independent of age, ethnicity, smokingbehaviour, and levels of physical activity. However, onceanalyses were adjusted for all traditionally measured riskfactors for atherosclerosis, the associations of HTGWwith indices of subclinical atherosclerosis were no longersignificant.Our study is congruent with studies performed in pop-ulations with diabetes mellitus [15,16], chronic kidneydisease [17], and those infected with human immuno-deficiency virus [18] that found a positive associationbetween HTGW and subclinical atherosclerosis. In ourstudy, as indicated by total area and presence of plaques,individuals with either Elevated WC or Elevated TG hadmore carotid atherosclerosis than individuals withoutHTGW; while greatest carotid atherosclerosis was ob-served among men and women with HTGW suggestingthat the combination of a large WC and elevated TGresults in greater CVD risk. Indeed, the phenotype ofHTGW has previously been shown to be associated withelevated cardiometabolic risk factors [13,24-28]. Addition-ally, multiple prospective studies reported an increase inrisk of developing cardiovascular disease [22,29-31] anddiabetes [32,33] among individuals with HTGW pheno-type further highlighting the utility of HTGW as a pre-ventative screening tool.It has been proposed that elevated fasting TG, in thepresence of increased WC, represent a marker of indi-vidual’s relative inability to store energy surplus in thesubcutaneous adipose tissue (a protective metabolic sink);consequently, HTGW could be a simple marker of vis-ceral adipose tissue (dysfunctional adipose tissue) andits metabolic complications resulting from insulin re-sistance [14,34]. Indeed, it has recently been reportedthat, among subjects with type 2 diabetes, HTGW iden-tifies subset of individuals with greater degree of vis-ceral adiposity and subclinical atherosclerosis (15). Ofimportance, although there is an established link be-tween insulin resistance and coronary artery disease(CAD) [35], presence of HTGW was found to be asso-ciated with increased CAD risk in both normoglycemicand insulin resistant individuals [36].Table 2 Characteristics of participating men stratified by presence of HTGW components**Characteristic Without HTGWn = 134Elevated TGn = 31Elevated WCn = 128HTGWn = 84Overall significance (p)Age (years) 46.7 ± 8.9 46.1 ± 7.9 47.9 ± 8.7 45.5 ± 8.8 0.256Ethnicity < 0.001Aboriginal 15 (11.2%) 1 (3.2%) 38 (29.7%) 25 (29.8%)Chinese 50 (37.3%) 19 (61.3%) 16 (12.5%) 15 (17.9%)European 40 (29.9%) 1 (3.2%) 39 (30.5%) 17 (20.2%)South Asian 29 (21.6%) 10 (32.3%) 35 (27.3%) 27 (32.1%)Current smoker 10 (7.5%) 3 (9.7%) 14 (10.9%) 15 (17.9%) 0.125Family history of CVD present (%) 59 (44.0%) 14 (45.2%) 58 (45.3%) 36 (42.9%) 0.987Physical activity (min/week)*† 238 (194, 290) 153 (99, 236) 220 (179, 272) 183 (142, 236) 0.249Body mass index* 24.2 (23.6, 24.7) 24.7 (23.6, 25.8) 29.8 (29.2, 30.3) 30.7 (30.1, 31.4) < 0.001b, c, d, e, fTotal cholesterol (mmol/L)* 5.11 ± 0.95 5.81 ± 1.01 5.00 ± 0.87 5.66 ± 0.95 < 0.001a, c, d, fHDL-C (mmol/L)* 1.28 ± 0.30 0.97 ± 0.19 1.13 ± 0.27 0.94 ± 0.20 < 0.001a, b, c, d, fGlucose (mmol/L)* 5.10 (4.90, 5.43) 5.20 (5.00, 5.40) 5.30 (5.10, 5.70) 5.60 (5.20, 5.90) < 0.001b, c, e, fSystolic blood pressure (mm Hg)* 115 (108, 120) 116 (108, 124) 118 (112, 126) 120 (114, 131) 0.014cIntima-media thickness (mm)*† 0.67 (0.65, 0.69) 0.65 (0.61, 0.69) 0.71 (0.69, 0.73) 0.72 (0.70, 0.75) < 0.001b, c, d, eTotal area (mm2)*† 17.87 (16.53, 19.34) 18.56 (15.75, 21.85) 20.41 (18.84, 21.85) 21.05 (19.07, 23.27) < 0.001b, cPresence of plaque 66 (49.3%) 17 (54.8%) 74 (57.8%) 53 (63.1%) 0.225*Age adjusted, presented as mean (95%CI), † geometric means; age presented as mean ± SD; Differences in continuous variables across categories of HTGWcomponents variable explored by general linear modelling. Categorical variables presented as n (%). Associations between categorical variables and HTGWcomponents variable explored by Chi-square test.Pairwise comparisons: ap < 0.05, Normal WC/Normal TG vs. Elevated TG/Normal WC; bp < 0.05, Normal WC/Normal TG vs. Elevated WC/Normal TG; cp < 0.05,Normal WC/Normal TG vs. HTGW; dp < 0.05, Elevated TG/Normal WC vs. Elevated WC/Normal TG; ep < 0.05, Elevated TG/Normal WC vs. HTGW; fp < 0.05, ElevatedWC/Normal TG vs. HTGW.**Elevated waist circumference (WC) was ≥ 90 cm. Elevated triglyceride (TG) levels were ≥ 2 mmol/L. Fourteen male participants are missing data for one or bothhypertriglyceridemic waist (HTGW) components.Gasevic et al. Lipids in Health and Disease 2014, 13:38 Page 5 of 10http://www.lipidworld.com/content/13/1/38The rationale for measuring and interpreting WC alongwith TG when screening for individuals at increased car-diometabolic risk is due to a fact that not all individualswith increased WC have elevated VAT and are at in-creased risk for CAD (14). Indeed, it has been shown thatisolated increase in WC or isolated hypertriglycerideamiashowed no association with increase in CAD risk, whilesimultaneous presence of elevated WC and fasting TG(HTGW) was associated with a significant increase inCAD disease (13). Additionally, although cardiovascularrisk of men was significantly higher than that of women inour study, which is most likely due to differences in bodyfat accumulation between sexes [37,38], greatest athero-sclerosis was observed in both men and women withHTGW compared to their counterparts with isolated ele-vated WC or TG. Thus, simultaneous measurement andinterpretation of WC and fasting TG can be a powerfultool to identify both men and women characterized bythe atherogenic triade (hyperinsulinemia, elevated apo-lipoprotein B, and small, dense LDL-C) and at high riskfor CAD (13, 27).The strength of our study lies in exploring the associ-ation between HTGW and subclinical atherosclerosis inan apparently healthy and a multiethnic population, inusing several markers of subclinical atherosclerosis (IMT,total area and presence of carotid plaques), and exploringwhether the effect of HTGW on subclinical atheroscler-osis persists over and above traditional risk factors foratherosclerosis. Our findings that HTGW phenotype isassociated with subclinical atherosclerosis in apparentlyhealthy men and women, irrespective of ethnicity, suggestsan important role that HTGW may play in primary carepractice in identifying patients at risk for atherosclerosis.The use of HTGW would largely expedite and simplifytriaging of patients by identifying those “in need” of ag-gressive atherosclerosis prevention, thereby decreasing theamount of time and complex testing a primary health carepractitioner would spend screening for such patients andpotentially translate in lower health care costs. Moreover,this quick assessment would further allow a primary carehealth practitioner to spend more time in counselling apatient on how to decrease their risk for atherosclerosis.Patients seen by specialists often already have documen-tation of traditional risk factors and so further assessmentfor HTGW may not necessarily add information towardatherosclerosis risk since we observed the effect of HTGWon subclinical atherosclerosis was no longer significantonce all traditional atherosclerosis risk factors were addedTable 3 Characteristics of participating women stratified by presence of HTGW components**Characteristic Without HTGWn = 168Elevated TGn = 57Elevated WCn = 117HTGWn = 70Overall significance (p)Age (years) 48.1 ± 8.8 47.6 ± 9.7 47.3 ± 8.6 46.9 ± 8.8 0.795Ethnicity < 0.001Aboriginal 19 (11.3%) 12 (21.1%) 46 (39.3%) 21 (30.0%)Chinese 61 (36.3%) 21 (36.8%) 24 (20.5%) 9 (12.9%)European 43 (25.6%) 6 (10.5%) 27 (23.1%) 21 (30.0%)South Asian 45 (26.8%) 18 (31.6%) 20 (17.1%) 19 (27.1%)Current smoker 7 (4.2%) 4 (7.0%) 10 (8.5%) 14 (20.0%) 0.001Family history of CVD present (%) 79 (47.0%) 25 (43.9%) 48 (41.0%) 31 (44.3%) 0.798Physical activity (min/week)*† 214 (183, 252) 197 (148, 260) 178 (147, 216) 162 (127, 208) 0.124Body mass index* 23.8 (23.2, 24.3) 25.3 (24.3, 26.3) 31.0 (30.3, 31.7) 31.8 (30.9, 32.7) < 0.001a, b, c, d, eTotal cholesterol (mmol/L)* 5.11 ± 1.03 5.71 ± 1.13 4.99 ± 0.93 5.62 ± 0.87 < 0.001a, c, d, fHDL-C (mmol/L)* 1.58 ± 0.36 1.32 ± 0.36 1.40 ± 0.30 1.23 ± 0.27 < 0.001a, b, c, fGlucose (mmol/L)* 4.90 (4.70, 5.30) 5.10 (4.80, 5.40) 5.20 (4.90, 5.50) 5.30 (4.90, 5.60) < 0.001b, cSystolic blood pressure (mm Hg)* 111 (104, 122) 114 (107, 125) 119 (109, 131) 120 (113, 127) < 0.001b, cIntima-media thickness (mm)*† 0.63 (0.62, 0.64) 0.66 (0.64, 0.69) 0.65 (0.64, 0.67) 0.65 (0.64, 0.67) < 0.001a, b, cTotal area (mm2)*† 15.60 (14.76, 16.46) 16.76 (15.27, 18.41) 16.53 (15.49, 17.65) 17.46 (16.05, 18.99) < 0.001cPresence of plaque 75 (44.6%) 24 (42.1%) 52 (44.4%) 37 (52.9%) 0.595*Age adjusted, presented as mean (95%CI), †geometric means; age presented as mean ± SD; Differences in continuous variables across categories of HTGWcomponents variable explored by general linear modelling. Categorical variables presented as n (%). Associations between categorical variables and HTGWcomponents variable explored by Chi-square test.Pairwise comparisons: ap < 0.05, Normal WC/Normal TG vs. Elevated TG/Normal WC; bp < 0.05, Normal WC/Normal TG vs. Elevated WC/Normal TG; cp < 0.05,Normal WC/Normal TG vs. HTGW; dp < 0.05, Elevated TG/Normal WC vs. Elevated WC/Normal TG; ep < 0.05, Elevated TG/Normal WC vs. HTGW; fp < 0.05, ElevatedWC/Normal TG vs. HTGW.**Elevated waist circumference (WC) was ≥ 85 cm. Elevated triglyceride (TG) levels were ≥ 1.5 mmol/L. Six female participants are missing data for one or bothhypertriglyceridemic waist (HTGW) components.Gasevic et al. Lipids in Health and Disease 2014, 13:38 Page 6 of 10http://www.lipidworld.com/content/13/1/38to the model. However, given a strong association ofHTGW with cardiometabolic risk factors [12,13,24-28]and its ability to predict cardiovascular disease event[30], HTGW may be used as a simple and inexpensivetool in clinical practice to monitor patients’ changes(improvement/deterioration) in cardiometabolic risk.Additionally, this simple tool could also provide greaterincentive to patients for lifestyle change, as they can easilytrack the effect of lifestyle changes on their cardio-metabolic risk.ABCFigure 1 The association between HTGW phenotype andindices of subclinical atherosclerosis in men. Panel A: Theassociation HTGW phenotype and IMT; Panel B: The associationbetween HTGW phenotype and total area; Panel C: The associationbetween HTGW phenotype and presence of plaques; ↑TG: Elevatedtriglycerides, not elevated waist circumference; ↑WC: Elevated waistcircumference, not elevated triglycerides; HTGW: elevated bothtriglycerides and waist circumference; _1: Model 1, adjusted for age,ethnicity, smoking and physical activity; _2: Model 2 = Model 1 +additional adjustment for systolic blood pressure, total cholesterol,HDL-C, fasting blood glucose, family history of CVD, and BMI;B (95%CI): Beta unstandardized regression coefficient with acorresponding 95 percent confidence interval; OR (95%CI): oddsratio with a corresponding 95 percent confidence interval;*p < 0.05, **p < 0.01, ***p < 0.001.ABCFigure 2 The association between HTGW phenotype andindices of subclinical atherosclerosis in women. Panel A: Theassociation HTGW phenotype and IMT; Panel B: The associationbetween HTGW phenotype and total area; Panel C: The associationbetween HTGW phenotype and presence of plaques; ↑TG: Elevatedtriglycerides, not elevated waist circumference; ↑WC: Elevated waistcircumference, not elevated triglycerides; HTGW: elevated bothtriglycerides and waist circumference; _1: Model 1, adjusted for age,ethnicity, smoking and physical activity; _2: Model 2 = Model 1 +additional adjustment for systolic blood pressure, total cholesterol,HDL-C, fasting blood glucose, family history of CVD, and BMI;B (95%CI): Beta unstandardized regression coefficient with acorresponding 95 percent confidence interval; OR (95%CI): oddsratio with a corresponding 95 percent confidence interval; *p < 0.05,**p < 0.01, ***p < 0.001.Gasevic et al. Lipids in Health and Disease 2014, 13:38 Page 7 of 10http://www.lipidworld.com/content/13/1/38Despite its potential benefits in identifying individualsat increased risk for atherosclerosis, the widespread useof HTGW as a screening tool may be limited due to thelack of routine measurement of WC in clinical practice.Indeed, in a recently published study, Gupta et al. (2012)surveyed Canadian primary care physicians and foundthat WC was routinely measured by only 6% of physicians[39]. This finding contrasts with the knowledge that 80%of surveyed physicians considered WC to be a vital sign[39]. This discrepancy may be due to a notion amongstclinicians that WC is a tool for research purposes only;a lack of effort to continuously inform physicians aboutthe clinical usefulness of the routine WC measurements;and a lack of a standardized protocol for WC measure-ment [40]. There is a concern that a lack of standardizedprotocol for measurement of WC may influence clinicaldecision-making [41-43]. However, it has been reportedthat the reproducibility of WC measurement is high re-gardless of the measurement site [44] and that the WCmeasurement protocol has no significant influence on theassociation of WC with CVD, diabetes, all-cause and CVDmortality. Given the simplicity, high reproducibility of andlow costs associated with the WC measurement, it hasbeen argued that WC should be used by the medical com-munity more consistently [28].Ethnic-specific WC targets may pose an additional chal-lenge in identifying individuals with HTGW and hence atrisk for atherosclerosis [17]. While using current definitionfor HTGW [22], we found that ethnicity did not modify theassociation between HTGW and indices of atherosclerosis;however, our results indicate significant ethnic differencesin the distribution of HTGW components which is mostlikely driven by body fat accumulation shown to be differ-ent in distinct ethnic groups [45,46]. Thus, we believethat further exploration on the role of ethnicity in theassociation between HTGW and subclinical athero-sclerosis is warranted given the already established eth-nic differences in CVD risk [47,48].There are limitations to the study design as it is cross-sectional rather than prospective. Future research shouldemploy a prospective study design to determine causalrelationships. Our study sample may not be representativeof a general population given that our participants werebetween ages of 30 and 65 and purposely recruited acrossa range of BMI values. However, this approach to recruit-ment may be advantageous, as it allowed us to explore theassociation between HTGW and atherosclerosis in apopulation with diverse body sizes. Furthermore, due to adifficulty in identifying individuals of Chinese origin withBMI of 30 and higher, the target for the upper BMI rangeof Chinese individuals was changed to a BMI of 28 orhigher. However, we believe that this slight modificationin the recruitment strategy did not influence our study re-sults where Chinese individuals were shown to have lowerprevalence of HTGW and hence lower cardiovascular riskcompared to their ethnic counterparts; as already reportedin the literature [48,49].ConclusionsIn conclusion, in a multi-ethnic population of apparentlyhealthy individuals, in both men and women, the presenceof HTGW was positively associated with subclinical athero-sclerosis as depicted by carotid IMT and total area indicesafter adjustment for age, ethnicity, smoking and physicalactivity. However, in our study, HTGW did not show theassociation with subclinical atherosclerosis over and abovethe traditional risk factors for atherosclerosis. Our resultsfurther verify the importance of HTGW as a simple clinicaltool that may serve as an early marker of subclinical athero-sclerosis in men and women, irrespective of ethnicity. Theimplementation of HTGW as a preventative clinical toolwould allow for timely implementation of prevention pro-grams to reduce subclinical atherosclerosis and future CVDrisk. However, once individuals are assessed for all trad-itional risk factors for atherosclerosis, the results of ourstudy indicate that the additional assessment of men andwomen for HTGW is not warranted.Additional filesAdditional file 1: The association of HTGW with IMT, total area andpresence of carotid artery plaques in men.Additional file 2: The association of HTGW with IMT, total area andpresence of carotid artery plaques in women.AbbreviationsBMI: Body mass index; CAD: Coronary artery disease; CVD: Cardiovasculardisease; HDL-C: High density lipoprotein cholesterol;HTGW: Hypertriglyceridemic waist; IMT: Intima-media thickness;M-CHAT: Multi-Cultural Community Health Assessment Trial; TG: Triglycerides;WC: Waist circumference.Competing interestsThe authors declare that they have no competing interests.Authors’ contributionsDG performed statistical analyses, data interpretation and drafted themanuscript. ACC helped with the interpretation of data and drafting themanuscript. IAL participated in the discussion and critically revised themanuscript. GBJM and SAL have made substantial contributions toconception and design of the study, data interpretation and critically revisedthe manuscript. All authors read and approved the final manuscript.Author details1Department of Biomedical Physiology and Kinesiology, Simon FraserUniversity, 2600-515 W Hastings Street, Vancouver V6B 5K3, BC, Canada.2Center for Family and Community Medicine, Department of Neurobiology,Care Sciences and Society, Karolinska Institutet, Alfred Nobels allé 12,Huddinge 141 83, Sweden. 3Department of Public Health and CaringSciences/ Section of Geriatrics Uppsala University, Uppsala, Sweden.4Department of Medicine, University of British Columbia, 2775 Laurel Street,Vancouver, BC V5Z 1M9, Canada. 5Faculty of Health Sciences, Simon FraserUniversity, Burnaby, BC, Canada. 6Division of Cardiology, Providence HealthCare, Healthy Heart Program, 180 - 1081 Burrard Street, Vancouver, BC V6Z1Y6, Canada.Gasevic et al. Lipids in Health and Disease 2014, 13:38 Page 8 of 10http://www.lipidworld.com/content/13/1/38Received: 27 November 2013 Accepted: 19 February 2014Published: 23 February 2014References1. Toth PP: Subclinical atherosclerosis: what it is, what it means and whatwe can do about it. Int J Clin Prac 2008, 62:1246–1254.2. Miller M: An emerging paradigm in atherosclerosis: focus on subclinicaldisease. Postgrad Med 2009, 121:49–59.3. Bots ML, Hoes AW, Koudstaal PJ, Hofman A, Grobbee DE: Common carotidintima-media thickness and risk of stroke and myocardial infarction: theRotterdam Study. Circulation 1997, 96:1432–1437.4. O’Leary DH, Polak JF, Kronmal RA, Manolio TA, Burke GL, Wolfson SK Jr:Carotid-artery intima and media thickness as a risk factor for myocardialinfarction and stroke in older adults. Cardiovasc Health Study CollaborativeRes Group NEJM 1999, 340:14–22.5. Bots ML, Grobbee DE: Intima media thickness as a surrogate marker forgeneralised atherosclerosis. Cardiovasc Drugs Ther 2002, 16:341–351.6. Hubert HB, Feinleib M, McNamara PM, Castellj WP: Obesity as anindependent risk factor for cardiovascular disease: a 26-year follow-up ofparticipants in the Framingham Heart Study. Circulation 1983, 67:968–977.7. Rabkin SW, Mathewson FA, Hsu PH: Relation of body weight todevelopment of ischemic heart disease in a cohort of young NorthAmerican men after a 26 year observation period: the Manitoba Study.Am J Cardiol 1977, 39:452–458.8. De Michele M, Panico S, Iannuzzi A, Celentano E, Ciardullo AV, Galasso R,Saccheti L, Zarrilli F, Bond MG, Rubba P: Association of obesity and centralfat distribution with carotid artery wall thickening in middle-agedwomen. Stroke 2002, 33:2923–2928.9. Hassinen M, Lakka TA, Komulainen P, Haapala I, Nissinen A, Rauramaa R:Association of waist and hip circumference with 12-year progression ofcarotid intima-media thickness in elderly women. Int J Obes (Lond) 2007,31:1406–1411.10. Lakka TA, Lakka HM, Salonen R, Kaplan GA, Salonen JT: Abdominal obesityis associated with accelerated progression of carotid atherosclerosis inmen. Atherosclerosis 2001, 154:497–504.11. Lear SA, Humphries KH, Kohli S, Frohlich JJ, Birmingham CL, Mancini GB:Visceral adipose tissue, a potential risk factor for carotid atherosclerosis:results of the Multicultural Community Health Assessment Trial(M-CHAT). Stroke 2007, 38(9):2422–2429.12. Blackburn P, Lemieux I, Lamarche B, Bergeron J, Perron P, Tremblay G,Gaudet D, Despres JP: Hypertriglyceridemic waist: a simple clinicalphenotype associated with coronary artery disease in women.Metabolism 2012, 61:56–64.13. Lemieux I, Pascot A, Couillard C, Lamarche B, Tchernof A, Almeras N,Bergeron J, Gaudet D, Tremblay G, Prud’homme D, Nadeau A, Despres JP:Hypertriglyceridemic waist: A marker of the atherogenic metabolic triad(hyperinsulinemia; hyperapolipoprotein B; small, dense LDL) in men?Circulation 2000, 102:179–184.14. Lemieux I, Poirier P, Bergeron J, Almeras N, Lamarche B, Cantin B, DagenaisGR, Despres JP: Hypertriglyceridemic waist: a useful screening phenotypein preventive cardiology? Can J Cardiol 2007, 23(Suppl B):23B–31B.15. Sam S, Haffner S, Davidson MH, D’Agostino RB Sr, Feinstein S, Kondos G,Perez A, Mazzone T: Hypertriglyceridemic waist phenotype predictsincreased visceral fat in subjects with type 2 diabetes. Diabetes Care 2009,32:1916–1920.16. Lei Z, Dong Y, Xu M, Li J, Wang X, Wang N: The hypertriglyceridemic-waistphenotype in relation to carotid artery atherosclerosis in patients withtype 2 diabetes mellitus. Chin J Endocrinol Metab 2012, 28(1):21–23.17. Zhe X, Bai Y, Cheng Y, Xiao H, Wang D, Wu Y, Huang X, Tian X, Wang T:Hypertriglyceridemic waist is associated with increased carotidatherosclerosis in chronic kidney disease patients. Nephron 2012,122:146–152.18. Bernal E, Marin I, Munoz A, Saban J, Sarabia F, Garcia-Medina A, Vicente T,Cano A: Hypertriglyceridemic waist phenotype is a risk factor for subclin-ical atherosclerosis in human immunodeficiency virus-infected patients.Med Clin 2012, 139(13):561–565.19. Lear SA, Birmingham CL, Chockalingam A, Humphries KH: Study design ofthe Multicultural Community Health Assessment Trial (M-CHAT): acomparison of body fat distribution in four distinct populations. Ethn Dis2006, 16:96–100.20. Kriska AM, Knowler WC, LaPorte RE, Drash AL, Wing RR, Blair SN, Bennett PH,Kuller LH: Development of questionnaire to examine relationship ofphysical activity and diabetes in Pima Indians. Diabetes Care 1990,13:401–411.21. Pereira MA, Kriska AM, Joswiak ML, Dowse GK, Collins VR, Zimmet PZ,Gareeboo H, Chitson P, Hemrai F, Purran A: Physical inactivity and glucoseintolerance in the multiethnic island of Mauritius. Med Sci Sports Exerc1995, 27:1626–1634.22. Arsenault BJ, Lemieux I, Despres JP, Wareham NJ, Kastelein JJ, Khaw KT,Boekholdt SM: The hypertriglyceridemic-waist phenotype and the risk ofcoronary artery disease: results from the EPIC-Norfolk prospectivepopulation study. CMAJ 2010, 182:1427–1432.23. Aminbakhsh A, Frohlich J, Mancini GBJ: Detection of early atherosclerosiswith B mode carotid ultrasonography: assessment of a new quantitativeapproach. Clin Invest Med 1999, 22:265–274.24. Blackburn P, Lemieux I, Almeras N, Bergeron J, Cote M, Tremblay A,Lamarche B, Despres JP: The hypertriglyceridemic waist phenotype versusthe national cholesterol education program-adult treatment panel IIIand international diabetes federation clinical criteria to identify high-riskmen with an altered cardiometabolic risk profile. Metabolism 2009,58(8):1123–1130.25. Gazi IF, Filippatos TD, Tsimihodimos V, Saougos VG, Liberopoulos EN,Mikhailidis DP, Tselepis AD, Elisaf M: The hypertriglyceridemic waistphenotype is a predictor of elevated levels of small, dense LDLcholesterol. Lipids 2006, 41(7):657–654.26. Solati M, Ghanbarian A, Rahmani M, Sarbazi N, Allahverdian S, Azizi F:Cardiovascular risk factors in males with hypertriglyceridemic waist(Tehran Lipid and Glucose Study). Int J Obes Relat Metab Dis 2004, 28(5):706–709.27. LaMonte MJ, Ainsworth BE, DuBose KD, Grandiean PW, Davis PG, YanowitzFG, Durstine JL: The hypertriglyceridemic waist phenotype amongwomen. Atherosclerosis 2003, 171(1):123–130.28. Kahn HS, Valdez R: Metabolic risks identified by the combination ofenlarged waist and elevated triacylglycerol concentration. Am J Clin Nutr2003, 78:928–934.29. Tanko LB, Bagger YZ, Qin G, Alexanders P, Larsen PJ, Christiansen C:Enlarged waist combined with elevated triglycerides is a strongpredictor of accelerated atherogenesis and related cardiovascularmortality in postmenopausal women. Circulation 2005, 111(15):1883–1890.30. Czernichow S, Bruckert E, Bertrais S, Galan P, Hercberg S, Oppert JM:Hypertriglyceridemic wasit and 7.5-year prospective risk ofcardiovascular disease in asymptomatic middle-aged men. Int J Obes2007, 31(5):791–796.31. St-Pierre J, Lemieux I, Perron P, Brisson D, Santure M, Vohl MC, Despres JP,Gaudet D: Relation of the “hypertriglyceridemic waist” phenotype toearlier manifestations of coronary artery disease in patients with glucoseintolerance and type 2 diabetes mellitus. Am J Cardiol 2007,99(3):369–373.32. Zhang M, Gao Y, Chang H, Wang X, Liu D, Zhu Z, Huang G:Hypertriglyceridemic-waist phenotype predicts diabetes: a cohort studyin Chinese urban adults. BMC Public Health 2012, 12:1081.33. Carlsson AC, Riserus U, Arnlov J: Hypertriglyceridemic waist phenotype isassociated with decreased insulin sensitivity and incident diabets inelderly men. Obesity 2013. 10.1002/oby.20434.34. Despres JP, Lemieux I: Abdominal obesity and metabolic syndrome.Nature 2006, 444:881–887.35. Reaven G: Insulin resistance and coronary heart disease in nondiabeticindividuals. ATVB 2012, 32:1754–1759.36. St-Pierre J, Lemieux I, Vohl MC, Perron P, Tremblay G, Despres JP, Gaudet D:Contribution of abdominal obesity and hypertriglyceridemia to impairedfasting glucose and coronary artery disease. Am J Cardiol 2002, 90:15–18.37. Freedman DS, Jacobsen SJ, Barboriak JJ, Sobocinski KA, Anderson AJ,Kissebah AH, Sasse EA, Gruchow HW: Body fat distribution and male/female differences in lipids and lipoproteins. Circulation 1990,81:1498–1506.38. Larsson B, Bengtsson C, Bjorntorp P, Lapidus L, Sjostrom L, Syardsudd K,Tibblin G, Wedel H, Welin L, Wilhelmsen L: Is abdominal body fatdistribution a major explanation for the sex difference in the incidenceof myocardial infarction? The study of men born in 1913 and thestudy ow women, Goteborg, Sweden. Am J Epidemiology 1992,135(3):266–273.Gasevic et al. Lipids in Health and Disease 2014, 13:38 Page 9 of 10http://www.lipidworld.com/content/13/1/3839. Gupta M, Singh N, Tsiqoulis M, Kaiij M, Hirjikaka S, Quan A, Teoh H, Verma S:Perceptions of Canadian primary care physicians towards cardiovascularrisk assessment and lipid management. Can J Cardiology 2012,28(1):14–19.40. Wang J: Waist circumference: a simple, inexpensive, and reliable toolthat should be included as part of physical examinations in the doctor’soffice. Am J Clin Nutr 2003, 78:902–903.41. Yamada S, Tsukamoto Y, Irie J: Waist circumference in metabolicsyndrome. Lancet 2007, 370(9598):1541–1542.42. Mason C, Katzmarzyk PT: Effect of the site measurement of waistcircumference on the prevalence of the metabolic syndrome.Am J Cardiol 2009, 103(12):1716–1720.43. Lin CC, Yu SC, Wu BJ, Chang DJ: Measurement of waist circumference atdifferent sites affects the detection of abdominal obesity and metabolicsyndrome among psychiatric patients. Psychiatry Res 2012, 197(3):322–326.44. Wang J, Thornton JC, Bari S, Williamson B, Gallagher D, Heymsfield SB,Horlick M, Kotler D, Laferrere B, Mayer L, Pi-Sunver FX, Pierson RN Jr:Comparisons of waist circumferences measured at 4 sites. Am J Clin Nutr2003, 77(2):379–384.45. Lear SA, Humphries KH, Kohli S, Chockalingam A, Frohlich JJ, BirminghamCL: Visceral adipose tissue accumulation differs according to ethnicbackground: results of the Multicultural Community Health AssessmentTrial (M-CHAT). Am J Clin Nutr 2007, 86(2):353–359.46. Kohli S, Sniderman AD, Tchernof A, Lear SA: Ethnic-specific differences inabdominal subcutanepus tissue compartments. Obesity 2010,18(11):2177–2183.47. Kurian AK, Cardarelli KM: Racial and ethnic differences in cardiovasculardisease risk factors: a systematic review. Ethn Dis 2007, 17(1):143–152.48. Chiu M, Austin PC, Manuel DG, Tu JV: Comparison of cardiovascular riskprofiles among ethnic groups using population health surveys between1996 and 2007. CMAJ 2010, 182(8):E301–E310.49. Anand SS, Yusuf S, Vuksan V, Devanesen S, Teo KK, Montague PA, KelemenL, Yi C, Lonn E, Gerstein H, Hegele RA, McQueen M for the SHAREInvestigators: Differences in risk factors, atherosclerosis, andcardiovascular disease between ethnic groups in Canada: the Study ofHealth Assessment and Risk in Ethnic groups (SHARE). Lancet 2000,356:279–284.doi:10.1186/1476-511X-13-38Cite this article as: Gasevic et al.: The association between“hypertriglyceridemic waist” and sub-clinical atherosclerosis in amultiethnic population: a cross-sectional study. Lipids in Health andDisease 2014 13:38.Submit your next manuscript to BioMed Centraland take full advantage of: • Convenient online submission• Thorough peer review• No space constraints or color figure charges• Immediate publication on acceptance• Inclusion in PubMed, CAS, Scopus and Google Scholar• Research which is freely available for redistributionSubmit your manuscript at www.biomedcentral.com/submitGasevic et al. Lipids in Health and Disease 2014, 13:38 Page 10 of 10http://www.lipidworld.com/content/13/1/38


Citation Scheme:


Citations by CSL (citeproc-js)

Usage Statistics



Customize your widget with the following options, then copy and paste the code below into the HTML of your page to embed this item in your website.
                            <div id="ubcOpenCollectionsWidgetDisplay">
                            <script id="ubcOpenCollectionsWidget"
                            async >
IIIF logo Our image viewer uses the IIIF 2.0 standard. To load this item in other compatible viewers, use this url:


Related Items