(Circulation. 2000;102:179.)
© 2000 American Heart Association, Inc.
Clinical Investigation and Reports |
Hypertriglyceridemic Waist
A Marker of the Atherogenic Metabolic Triad (Hyperinsulinemia; Hyperapolipoprotein B; Small, Dense LDL) in Men?
From the Quebec Heart Institute, Laval Hospital Research Center; the Lipid Research Center, CHUL Research Center; the Physical Activity Sciences Laboratory, Laval University; the Diabetes Research Unit, CHUL Research Center, Ste-Foy; and the Lipid Clinic, Chicoutimi Hospital, Chicoutimi, Québec, Canada.
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Abstract |
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Background—The present study tested the hypothesis that simple variables, such as waist circumference and fasting plasma triglyceride (TG) concentrations, could be used as screening tools for the identification of men characterized by a metabolic triad of nontraditional risk factors (elevated insulin and apolipoprotein [apo] B and small, dense LDL particles).
Methods and Results—Results of the metabolic study
(study 1) conducted on 185 healthy men indicate that a large proportion
(>80%) of men with waist circumference values 
90 cm and with
elevated TG levels (2.0 mmol/L) were characterized by the
atherogenic metabolic triad. Validation of the model in an
angiographic study (study 2) on a sample of 287 men with and without
coronary artery disease (CAD) revealed that only men with both
elevated waist and TG levels were at increased risk of CAD (odds ratio
of 3.6, P<0.03) compared with men with low waist and TG
levels.
Conclusions—It is suggested that the simultaneous measurement and interpretation of waist circumference and fasting TG could be used as inexpensive screening tools to identify men characterized by the atherogenic metabolic triad (hyperinsulinemia, elevated apo B, small, dense LDL) and at high risk for CAD.
Key Words: apolipoproteins • insulin • lipoproteins • lipids • coronary disease • waist circumference
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Introduction |
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There is increasing evidence that variables other than the traditional lipoprotein-lipid profile may further improve the discrimination of individuals at high risk for coronary heart disease (CHD). In this regard, it has been suggested that apolipoprotein (apo) B concentration could be an important predictor of CHD risk.1 2 In addition, fasting hyperinsulinemia, used in nondiabetic subjects as a crude marker of insulin resistance, may be a relevant correlate of metabolic abnormalities exacerbating CHD risk in men.3 4 Furthermore, small, dense LDL particles have been reported to be more prevalent in CHD patients than in healthy control subjects.5 6
Although recent analyses of the prospective Québec Cardiovascular Study have shown that the lipid triad (elevated plasma LDL cholesterol and triglyceride [TG] levels and reduced HDL cholesterol) was associated with a substantial increase in the 5-year risk of CHD, we found that hyperinsulinemia, hyperapolipoprotein B (hyperapo B), and small, dense LDL were even more powerful tools to predict CHD in men when these variables were considered simultaneously.7 We have therefore suggested that this triad of "unconventional" metabolic risk variables (metabolic triad) could be a powerful predictor of CHD risk.
In this regard, we have also shown that this atherogenic metabolic triad is highly prevalent among abdominally obese men, especially when a high accumulation of visceral adipose tissue is present.8 However, the costs associated with the measurement of visceral adipose tissue accumulation and with the measurement of insulin, apo B, and LDL particle diameter represent major barriers to their widespread use in clinical practice. Because we had previously reported that the waist circumference was a good crude correlate of visceral adipose tissue and of related metabolic complications9 and because fasting TG concentration has been shown to be the best predictor of LDL size assessed by gradient gel electrophoresis,10 we tested in 2 different samples the ability of these 2 simple measurements (waist circumference and fasting TG) to (1) identify men with the atherogenic triad of "unconventional" risk variables and (2) predict coronary artery disease (CAD) assessed by angiography.
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Methods |
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Subjects
Metabolic Study Sample (Study 1)
One hundred eighty-five men were recruited from the Québec City metropolitan area by solicitation through the media. All subjects were sedentary but healthy nonsmoking volunteers and were not under treatment for CHD, diabetes, dyslipidemias, or endocrine disorders. Blood samples were drawn after a 12-hour overnight fast. Plasma TG11 and cholesterol12 concentrations in the plasma and in the lipoprotein subfractions were measured with a Technicon RA-500 analyzer (Bayer Corp). Plasma VLDLs (d<1.006 g/L) were isolated by ultracentrifugation,13 and the HDL fraction was obtained after precipitation of LDL in the infranatant (d>1.006 g/L) with heparin and MnCl2.14 Apo B concentrations were measured in the fasting plasma by the rocket immunoelectrophoretic method of Laurell15 as previously described.16 LDL peak particle diameter was assessed with nondenaturing 2% to 16% polyacrylamide gel electrophoresis of whole plasma as previously described.10 Fasting plasma insulin was measured by radioimmunoassay with polyethylene glycol separation.17 Body weight, height, and waist circumference were measured by standardized procedures.18 Abdominal adipose tissue areas were measured by CT with a Siemens Somatom DHR scanner as previously described.19 All participants signed an informed consent document approved by the Laval University Medical Ethics Committee.
Angiographic Study Sample (Study 2)
This study sample included unrelated adults who underwent an
angiographic procedure for the investigation of retrosternal pain at
the Saguenay–Lac-St-Jean regional hospital in Chicoutimi. Patients
with type 2 diabetes as well as those known to be affected by familial
hypercholesterolemia, type III
dyslipidemia, or partial lipoprotein lipase deficiency were
excluded. Coronary angiographic disease was assessed by
angiography according to previously published
procedures.20 21 Briefly, 4 coronary arteries were
considered for the assessment of coronary stenosis:
left main coronary, left anterior descending, circumflex, and
right coronary. Patients with 1 lesion leading to a minimum
50% lumen narrowing of any of these 4 coronary
arterial segments were included in the CAD(+) group.
Patients not fulfilling this criterion were classified in the CAD(-)
group. Blood samples were obtained in the morning after a 12-hour fast.
Plasma total cholesterol, TG, and HDL
cholesterol levels were measured by enzymatic
assays.14 22 23 Total cholesterol was
determined in plasma, and HDL cholesterol was measured in
the supernatant after precipitation of VLDL and LDL with dextran
sulfate and magnesium chloride.23 Plasma LDL
cholesterol levels were estimated with the Friedewald
formula24 when TG concentrations were <5.0 mmol/L.
Plasma apo B levels were measured according to the rocket
immunoelectrophoretic method of Laurell.15 Fasting
insulinemia was measured by radioimmunoassay with polyethylene glycol
separation.17 Body weight, height, and waist girth were
assessed according to the procedures recommended by the Airlie
Conference.18 Patients gave their written consent to
participate in the study, which was approved by the Chicoutimi Hospital
Ethics Committee.
Statistical Analyses
Comparisons among subgroups of men classified on the basis of
waist and fasting TG values were performed by either Student’s
unpaired t test or ANOVA with the general linear model, and
the Duncan post hoc test was used when a significant group effect was
observed.
Metabolic Study (Study 1)
The prevalence of men with the metabolic triad was
compared among various subgroups stratified on the basis of waist
circumference and TG concentrations. Comparison of prevalence data
among subgroups was performed by 
2
analysis. Pearson correlation coefficients were computed to
quantify the relationships among variables. All statistical
analyses were conducted with SAS software (SAS
Institute).
Angiographic Study (Study 2)
Multiple logistic regression models were used for modeling
relationships between waist girth and triglyceridemia and
CAD. Patients were divided into 4 groups according to waist girth (<90
cm or 90 cm) and TG levels (<2.0 mmol/L or 2.0 mmol/L),
and the group characterized by both low waist circumference and low TG
concentration was considered the reference group, to which a CAD odds
ratio of 1.0 was assigned for comparison purposes. Analyses
were carried out with the SPSS package (release 6.1, SPSS Inc).
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Results |
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All nonobese volunteers (n=38) of the metabolic study (study 1) with body mass index values <25 kg/m2 were used to arbitrarily determine, by use of the 50th percentile of variables, reference values for the metabolic triad (high apo B and insulin levels and small, dense LDL particles) (Table 1
). The 50th percentile values in
nonobese men for fasting insulin, apo B, and LDL peak particle diameter
corresponded to 48.5 pmol/L, 0.96 g/L, and 255.5 Å, respectively.
Among these nonobese men, 21% were characterized by the
metabolic triad.
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To examine the relationship of waist circumference to the features of
the metabolic triad, the entire cohort of the
metabolic study (study 1) was divided into deciles of waist
girth. Figure 1A shows that apo B
concentrations increased rapidly to 
100 cm of waist circumference
and then remained stable among higher deciles of waist girth. Fasting
insulin levels, conversely, increased progressively as a function
increasing waist girth (Figure 1B).
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As expected from numerous studies,6 10 25 a highly
significant correlation was noted between the LDL peak particle
diameter determined by gradient gel electrophoresis and fasting TG
concentrations (r=-0.56, P<0.0001). Figure 1C
presents LDL peak particle diameter values among deciles
of fasting TG levels. It appears that most of the reduction in LDL peak
particle size was observed at a value somewhere between 1.82 and
2.11 mmol/L. According to our previous analyses, which
suggested that a TG value of 1.9 mmol/L was associated with the
best sensitivity/specificity to detect the small, dense LDL
phenotype from TG levels,10 these results
suggested that a TG concentration of 2.0 mmol/L may be a useful
and easy-to-remember reference value to screen for the small, dense LDL
phenotype.
Specificity (percentage of adequately classified subjects without the
new atherogenic metabolic triad) and sensitivity
(percentage of adequately classified subjects with the new atherogenic
metabolic triad) analyses were performed to verify
whether our TG and waist girth cutoff points were appropriate. Plasma
TG cutoff points of 1.9 or 2.0 mmol/L, combined with a waist
circumference of 85 or 90 cm, corresponded to values at which both
optimal sensitivity (73% to 78%) and specificity (78% to 81%) were
obtained (results not shown). To keep our algorithm as simple as
possible for clinicians, we selected values of 2.0 mmol/L for TG
and 90 cm for waist girth as critical cutoff points to screen for the
nontraditional metabolic triad. Figure 2 illustrates the working model we used,
in which the waist circumference was considered a proxy variable
for apo B and fasting insulin levels, whereas TG concentrations were
used to screen for the presence of small, dense LDL particles.
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The frequency of men characterized by the atherogenic
metabolic triad in each subgroup of waist girth and TG
levels is presented in Figure 3.
The subgroup of men having small waist girth values (<90 cm) and
elevated TG levels (2.0 mmol/L) was not included in the
analyses because too few such men (n=5) were found for
meaningful comparisons. Figure 3 shows that a high proportion of
men with waist circumference values 90 cm and with elevated TG
concentrations (>80%) were characterized by the atherogenic
metabolic triad, irrespective of whether they had a
moderately elevated (90 cm but <100 cm) or a substantially increased
(100 cm) waist circumference. However, moderately or substantially
elevated waist circumferences alone (90 cm but <100 cm and 100 cm)
in the absence of TG2.0 mmol/L were not enough to adequately
discriminate men with the metabolic triad (only 12% and
53% of men had the triad for moderately and substantially elevated
waist girths, respectively). Thus, the simultaneous
presence of an increased waist circumference and elevated TG
concentrations is necessary to substantially increase the likelihood of
finding individuals characterized by the metabolic
triad.
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Characteristics of subgroups classified on the basis of waist girth and
TG levels are presented in Table 2. The cholesterol/HDL
cholesterol ratio was substantially elevated in subgroups
with both a high waist girth and elevated TG values. The
cholesterol/HDL cholesterol ratio was also
elevated in men presenting a high waist circumference value but low
TG concentrations. However, this ratio was 1 unit lower than in the 2
groups with both elevated waist and TG levels. Fasting insulin
concentrations were higher with increasing waist girth values. However,
elevated TG concentrations were associated with further elevations in
insulin levels (P<0.0001). Apo B concentrations
progressively increased from the low waist and low TG levels to the
intermediate waist girth and high TG level group. As expected, LDL peak
particle diameter appeared to be largely influenced by TG levels rather
than by waist circumference (P<0.0001). Men with the
highest waist circumference values and elevated TG concentrations had
similar apo B concentrations and LDL peak particle size than men with
medium waist girth and high TG levels, but the former group was
characterized by higher fasting insulin levels (P<0.0001).
In the absence of elevated TG levels, men with increased waist
circumference had intermediate LDL peak particle diameter and apo B
levels but elevated fasting insulin concentrations.
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We then performed a validation study by studying the
performance of our simple waist-TG algorithm in a sample of
male patients who had coronary angiographic procedures for
symptoms of CAD (study 2). Characteristics of subjects according to CAD
status are presented in Table 3.
Overall, patients in the CAD(+) group showed a deteriorated
lipoprotein-lipid profile compared with patients in the CAD(-) group.
Figure 4 presents multiple logistic
regression analyses performed to determine the relationships of
waist circumference and TG levels to CAD. The relative odds of being
affected by CAD were increased significantly, by 3.6-fold
(P<0.03), among men with elevated waist circumference and
TG concentrations compared with men in the reference group (low waist
girth and TG levels).
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Discussion |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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The objective of the present study was to test whether simple variables, such as waist circumference and TG concentrations, could be used as screening tools for the identification of men characterized by a cluster of new metabolic risk variables for CHD, such as hyperinsulinemia and elevated apo B and small, dense LDL particles. In a prospective case-control analysis of men of the Québec Cardiovascular Study, we recently reported that the simultaneous measurement of insulinemia, apo B, and LDL particle diameter could improve our ability to identify men at high risk for CHD beyond the traditional lipid triad (increased TG and LDL cholesterol and reduced HDL cholesterol levels).7
Although there are considerable data linking the traditional lipid
triad to CHD risk, we believe that the high risk of CHD noted among men
with the metabolic triad of nontraditional risk factors
makes sense from a pathophysiological standpoint.
However, because most physicians do not have access to these new
metabolic markers of CHD risk, there was a need to develop
simple and inexpensive screening procedures that could improve the
ability of general physicians and other health professionals to
identify, at low cost, potential carriers of this atherogenic
metabolic triad. Analyses conducted in our study
sample 1 revealed that a large proportion of men with intermediate
(90 but <100 cm) and large (100 cm) waist girth values and with TG
concentrations >2.0 mmol/L were characterized by the triad of
nontraditional metabolic risk factors. They were also
characterized by substantial elevations in their
cholesterol/HDL cholesterol ratio (a
well-accepted predictor of CHD risk)26 and by increased
levels of visceral adipose tissue, which were far above our previously
suggested critical value (130
cm2).27 Conversely, it is
also important to point out that 50% of men with TG levels <2.0
mmol/L but with high waist circumference values (100 cm) were
characterized by the atherogenic triad; yet, they had very high levels
of visceral adipose tissue. Moreover, only 12% of men with an
intermediate waist girth (90 but <100 cm) but with TG levels
<2.0 mmol/L had the atherogenic triad. Results of the
angiographic study (study 2) also revealed that only men with elevated
waist girth and TG levels were at greater risk for CAD. Thus, results
of both our metabolic and angiographic studies suggest that
an elevated waist girth is, by itself, not enough to identify men with
the atherogenic metabolic triad and that considering the
presence of a moderate hypertriglyceridemia
(2.0 mmol/L) could further improve the screening procedure.
Results from published prospective studies have also shown that apo B
is a significant predictor of CHD, although this is not a uniform
finding.2 28 In the present study, we found a positive
association between apo B levels and waist circumference as apo B
concentrations progressively increased with waist girth. We observed a
rapid increase in apo B levels up to 100 cm of waist circumference.
Above this value, a further increase in waist girth was not associated
with substantial changes in apo B concentrations. Therefore, it seems
that apo B levels are very sensitive to an increase in waist girth
resulting from an accumulation of visceral adipose tissue.
Analyses on sensitivity and specificity revealed that 90 cm of
waist circumference was the critical cutoff point in screening for the
nontraditional lipid triad, which included elevated apo B
concentrations.
Our previous work has also demonstrated a positive association between waist girth and fasting as well as postglucose insulin levels.9 In our metabolic study (study 1), men with elevated waist girth were also characterized by higher levels of visceral adipose tissue and by elevated fasting insulin concentrations. Thus, in the present cohort of men, fasting insulin levels increased consistently with waist circumference. We have suggested that this hyperinsulinemic state in nondiabetic abdominally obese men was a marker of insulin resistance and a risk factor for CHD,4 21 although this issue is still controversial.
There is also evidence that the small, dense LDL phenotype is quite prevalent among patients with CHD. In the Québec Cardiovascular Study, we reported that the concomitant variation in apo B level was critical in the determination of CHD risk among men with small, dense LDL particles.6 Thus, TG concentrations are the best predictors of the dense LDL phenotype, but the presence of small, dense LDL particles alone may not be sufficient to substantially increase CHD risk. This is therefore why we believe that the measurement of waist girth (as a correlate of elevated insulin and apo B levels), in addition to fasting TG levels, is important in the assessment of CHD risk in men.
In summary, we tested, in 2 independent study samples, the ability of simple and inexpensive tools to screen for high-risk patients. It is suggested that the simultaneous interpretation of waist girth and fasting TG levels may contribute to a better identification of individuals characterized by the simultaneous presence of hyperinsulinemia, hyperapo B, and the small, dense LDL phenotype who are at increased risk of CHD. This "hypertriglyceridemic waist" concept may prove to be a helpful approach for the cost-effective screening of the population.
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Acknowledgments |
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This study was supported by the Medical Research Council of Canada and by the Heart and Stroke Foundation of Canada. Isabelle Lemieux is recipient of a fellowship from the Heart and Stroke Foundation of Canada; André Tchernof is recipient of a postdoctoral fellowship from the American Heart Association; Benoît Lamarche is a research scholar from the Medical Research Council of Canada; and Jean Bergeron is a clinical research scholar from the Fonds de la Recherche en Santé du Québec. Jean-Pierre Després is chair professor of human nutrition and lipidology, which is supported by Parke-Davis/Warner-Lambert and Provigo.
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Footnotes |
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Reprint requests to Jean-Pierre Després, PhD, Professor and Director of Research, Pavilion Mallet, 2nd Floor, 2725, chemin Sainte-Foy, Sainte-Foy, Québec, Canada G1V 4G5.
Received September 29, 1999; revision received January 28, 2000; accepted February 8, 2000.
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L. Guize, F. Thomas, B. Pannier, K. Bean, B. Jego, and A. Benetos All-Cause Mortality Associated With Specific Combinations of the Metabolic Syndrome According to Recent Definitions Diabetes Care, September 1, 2007; 30(9): 2381 - 2387. [Abstract] [Full Text] [PDF]
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A. J.G. Hanley, L. E. Wagenknecht, A. Festa, R. B. D'Agostino Jr., and S. M. Haffner Alanine Aminotransferase and Directly Measured Insulin Sensitivity in a Multiethnic Cohort: The Insulin Resistance Atherosclerosis Study Diabetes Care, July 1, 2007; 30(7): 1819 - 1827. [Abstract] [Full Text] [PDF]
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J. L Kuk, P. M Janiszewski, and R. Ross Body mass index and hip and thigh circumferences are negatively associated with visceral adipose tissue after control for waist circumference Am. J. Clinical Nutrition, June 1, 2007; 85(6): 1540 - 1544. [Abstract] [Full Text] [PDF]
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G. Pambianco, T. Costacou, and T. J. Orchard The Prediction of Major Outcomes of Type 1 Diabetes: a 12-Year Prospective Evaluation of Three Separate Definitions of the Metabolic Syndrome and Their Components and Estimated Glucose Disposal Rate: The Pittsburgh Epidemiology of Diabetes Complications Study experience Diabetes Care, May 1, 2007; 30(5): 1248 - 1254. [Abstract] [Full Text] [PDF]
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B. Richelsen, S. Tonstad, S. Rossner, S. Toubro, L. Niskanen, S. Madsbad, P. Mustajoki, and A. Rissanen Effect of Orlistat on Weight Regain and Cardiovascular Risk Factors Following a Very-Low-Energy Diet in Abdominally Obese Patients: A 3-year randomized, placebo-controlled study Diabetes Care, January 1, 2007; 30(1): 27 - 32. [Abstract] [Full Text] [PDF]
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J.-P. Despres Abdominal obesity: the most prevalent cause of the metabolic syndrome and related cardiometabolic risk Eur. Heart J. Suppl., May 1, 2006; 8(suppl_B): B4 - B12. [Abstract] [Full Text] [PDF]
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H.-U. Wittchen, B. Balkau, C. Massien, A. Richard, S. Haffner, J.-P. Despres, and on behalf of the IDEA Steering Committee International Day for the Evaluation of Abdominal obesity: rationale and design of a primary care study on the prevalence of abdominal obesity and associated factors in 63 countries Eur. Heart J. Suppl., May 1, 2006; 8(suppl_B): B26 - B33. [Abstract] [Full Text] [PDF]
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