Relation Among the Plasma Triglyceride/High-Density Lipoprotein

Cholesterol Concentration Ratio, Insulin Resistance, and Associated

Cardio-Metabolic Risk Factors in Men and Women
Martin R. Salazar, MDa,*, Horacio A. Carbajal, MDa, Walter G. Espeche, MDa,
Carlos E. Leiva Sisnieguez, MDa, Eduardo Balbín, MDa, Carlos A. Dulbecco, MDa,
Marcelo Aizpurúa, MDb, Alberto G. Marillet, MDc, and Gerald M. Reaven, MDd
Results of recent studies using the ratio of plasma triglyceride (TG) to high-density
lipoprotein (HDL) cholesterol concentration to identify insulin-resistant patients at in-
creased cardiometabolic risk have emphasized that the cut point used for this purpose will
vary with race. Because TG and HDL cholesterol concentrations vary with gender, this
analysis was initiated to define gender-specific plasma TG/HDL cholesterol concentration
ratios that best identified high-risk subjects among women (n ⴝ 1,102) and men (n ⴝ 464)
of primarily European ancestry. Insulin resistance was defined as the 25% of the population
with the highest values for fasting plasma insulin concentration and homeostasis model
assessment of insulin resistance. Using TG/HDL concentration ratios >2.5 in women and
>3.5 in men identified subgroups of men and women that were comparable in terms of
insulin resistance and associated cardiometabolic risk, with significantly higher values for
fasting plasma insulin, homeostasis model assessment of insulin resistance, blood pressure,
body mass index, waist circumference, and glucose and TG concentrations and lower HDL
cholesterol concentrations than in women and men below these cut points. The sensitivity
and specificity of these gender-specific cut points to identify insulin-resistant subjects were
about 40% and about 80%, respectively. In conclusion, the plasma TG/HDL cholesterol
concentration ratio that identifies patients who are insulin resistant and at significantly
greater cardiometabolic risk varies between men and women. © 2012 Elsevier Inc. All
rights reserved. (Am J Cardiol 2012;109:1749 –1753)

Plasma triglyceride (TG) and high-density lipoprotein and non-Hispanic blacks have shown that the “best” ratio
(HDL) cholesterol concentrations are independently related will vary as a function of racial group.9 Epidemiologic
to insulin-mediated glucose disposal,1 and the plasma TG/ studies have conventionally taken gender differences into
HDL cholesterol concentration ratio is significantly related account,10 and a recent editorial in The Lancet11 reminded
to this measure of insulin action, as well as to plasma insulin investigators of the importance of “analyzing data by sex,
concentration, a commonly used surrogate estimate of in- not only when scientifically appropriate, but also as a matter
sulin action.2,3 Because measurements of TG and HDL of routine.” Given differences in TG and HDL cholesterol
cholesterol are standardized, whereas there is no standard metabolism between men and women,10,12 it seemed impor-
assay of plasma insulin concentration,4 we suggested that tant to see if the “best ratio” might vary as function of
the plasma concentration ratio of TG to HDL cholesterol gender as well as racial group. Because we were unaware of
might be a useful surrogate estimate of insulin action.2,3 any study in which that has been done, the present analysis
However, recent studies addressing this issue have come to was performed, in which the ability of the plasma concen-
disparate conclusions as to the utility of this ratio as a tration ratio of TG to HDL cholesterol to identify insulin-
surrogate estimate of insulin resistance, with particular em- resistant subjects was analyzed separately for men and
phasis on the impact of differences in racial background of women.
the populations being studied.5–9 Whether subsequent evi-
dence will establish the TG/HDL cholesterol concentration
ratio as a useful surrogate estimate of insulin resistance and Methods
associated cardiometabolic risk remains to be seen, but As part of community intervention programs on car-
comparisons in non-Hispanic whites, Mexican Americans, diovascular risk factors, epidemiologic studies on hyper-
tension, renal disease, and other cardiometabolic risk
a
factors were conducted in Rauch, in the province of
Hospital Universitario General San Martín, La Plata; bHospital Mu-
Buenos Aires, Argentina (the RAUCH project), and San
nicipal de Rauch; cHospital Municipal de San Andrés de Giles, Buenos
Aires, Argentina; and dStanford University School of Medicine, Stanford,
Andrés de Giles, also in the province of Buenos Aires
California. Manuscript received December 23, 2011; revised manuscript (the PROCER project). According to the last national
received and accepted February 5, 2012. census available, there were 8,246 and 13,922 inhabitants
*Corresponding author: Tel: 54-221-4242625; fax: 54-221-4129164. aged ⱖ15 years in the urban areas of Rauch and San
E-mail address: salazarlandea@gmail.com (M.R. Salazar). Andrés de Giles, respectively. The methods of the sam-

0002-9149/12/$ – see front matter © 2012 Elsevier Inc. All rights reserved. www.ajconline.org
doi:10.1016/j.amjcard.2012.02.016
1750 The American Journal of Cardiology (www.ajconline.org)

Table 1
Characteristics of the sample according to gender and origin
Variable Rauch San Andrés de Giles Both Samples

Women Men p Value* Women Men p Value* Women Men p Value*

(n ⫽ 465) (n ⫽ 209) (n ⫽ 637) (n ⫽ 255) (n ⫽ 1,102) (n ⫽ 464)

Age (years) 52 ⫾ 16 53 ⫾ 15 0.581 40 ⫾ 17 40 ⫾ 16 0.988 45 ⫾ 18 46 ⫾ 17 0.489

FPI (␮U/ml) 7.5 ⫾ 4.2 7.6 ⫾ 5.4 0.805 8.4 ⫾ 6.3 8.1 ⫾ 8.9 0.650 8.0 ⫾ 5.5 7.9 ⫾ 7.5 0.731
HOMA-IR 1.66 ⫾ 0.99 1.77 ⫾ 1.37 0.307 1.99 ⫾ 1.58 2.00 ⫾ 2.15 0.964 1.85 ⫾ 1.37 1.90 ⫾ 1.84 0.651
Body mass index (kg/m2) 25.5 ⫾ 4.8 26.4 ⫾ 3.7 0.010 27.9 ⫾ 6.5 27.5 ⫾ 5.1 0.272 26.9 ⫾ 6.0 27.0 ⫾ 4.6 0.770
Waist circumference (cm) 92 ⫾ 13 96 ⫾ 10 ⬍0.001 92 ⫾ 15 94 ⫾ 14 0.114 92 ⫾ 14 95 ⫾ 12 ⬍0.001
Systolic blood pressure 131 ⫾ 19 136 ⫾ 18 ⬍0.001 122 ⫾ 20 125 ⫾ 18 0.068 126 ⫾ 20 130 ⫾ 19 ⬍0.001
(mm Hg)
Diastolic blood pressure 81 ⫾ 11 85 ⫾ 12 ⬍0.001 73 ⫾ 13 74 ⫾ 13 0.099 76 ⫾ 13 79 ⫾ 14 ⬍0.001
(mm Hg)
Glucose (mg/dl) 88 ⫾ 10 92 ⫾ 12 ⬍0.001 95 ⫾ 11 99 ⫾ 10 ⬍0.001 92 ⫾ 11 96 ⫾ 12 ⬍0.001
TG (mg/dl) 123 ⫾ 61 150 ⫾ 79 ⬍0.001 119 ⫾ 50 139 ⫾ 76 ⬍0.001 120 ⫾ 55 144 ⫾ 78 ⬍0.001
HDL cholesterol (mg/dl) 61 ⫾ 12 55 ⫾ 12 ⬍0.001 64 ⫾ 15 57 ⫾ 14 ⬍0.001 63 ⫾ 14 56 ⫾ 13 ⬍0.001
TG/HDL cholesterol ratio 2.17 ⫾ 1.44 2.93 ⫾ 1.91 ⬍0.001 2.01 ⫾ 1.19 2.75 ⫾ 2.13 ⬍0.001 2.08 ⫾ 1.30 2.84 ⫾ 2.03 ⬍0.001

Data are expressed as mean ⫾ SD.

* Student’s t test for independent samples.

ples, the socioeconomic features, and the prevalence of avoid the potential confounding impact of extreme outliers,
cardiovascular risk factors of the 2 populations have been subjects with TG concentrations ⬎500 mg/dl and/or HDL
published previously.13,14 cholesterol concentrations ⬎100 mg/dl were excluded from
In brief, the surveys were performed on simple random the analysis,7 as were participants with positive histories of
samples of subjects aged 15 to 80 years who lived in the diabetes or fasting glucose concentrations ⱖ126 mg/dl. The
chosen blocks (RAUCH n ⫽ 1,307, PROCER n ⫽ 1,591). remaining 1,102 women (mean age 45 ⫾ 1 years) and 464
Blood pressure was measured sitting, after a minimum rest men (mean age 46 ⫾ 1 years) were those included in the
period of 5 minutes, using a mercury sphygmomanometer. analysis.
Phase I and V Korotkoff sounds were used to identify Men and women were divided into quartiles on the basis of
systolic blood pressure and diastolic blood pressure, respec- their TG/HDL cholesterol concentration ratios, and mean ⫾
tively, and values were averages of 3 different measure- SD values and ranges were estimated. Values of TG/HDL
ments separated by 2 minutes from one another. Weight was cholesterol concentration ratios were compared between
determined with subjects wearing light clothing and no women and men using Student’s t tests for independent
shoes. Height was also measured without shoes, using a samples. Values for age, FPI, HOMA-IR, systolic blood
metallic metric tape; waist circumference was measured pressure, diastolic blood pressure, body mass index, waist
with a relaxed abdomen using a metallic metric tape on a circumference, glucose, HDL cholesterol, TG, and TG/HDL
horizontal plane above the iliac crest. Body mass index was cholesterol ratio were compared between the quartile with
calculated, and concentrations of plasma glucose, TG, HDL the highest TG/HDL cholesterol ratio and the remaining
cholesterol, and fasting plasma insulin (FPI) were deter- quartiles using analysis of covariance with age and study
mined after an overnight (12-hour) fast. Plasma for the site (Rauch and San Andrés de Giles) as covariates.
insulin measurements was extracted by centrifugation (15 To define insulin resistance, the sample was divided into
minutes at 3,000 rpm) and frozen at ⫺20°C until assayed. FPI quartiles and HOMA-IR quartiles, and subjects in the
FPI concentrations in the Rauch population were deter- upper quartiles of the 2 variables were classified as insulin
mined using an immunoradiometric assay, with 2 monoclo- resistant on the basis of a prospective outcome study.16 To
nal antibodies against 2 different epitopes of the insulin evaluate agreement between the 2 definitions of IR, we used
molecule. The inter- and intra-assay coefficients of variation coefficient of concordance (␬). The sensitivity and specific-
were 8.0% and 3.8%, respectively, with the lowest detect- ity of TG/HDL cholesterol ratio to identify insulin resis-
able level of 1.4 pmol/L. FPI concentrations in the San tance were calculated using as a cut-off point the value that
Andrés de Giles population were determined using a solid- separated the upper 25% of the TG/HDL cholesterol ratio in
phase chemiluminescent assay, using commercially avail- women and men, separately.
able kits (Immunolite Diagnostic Products, Los Angeles, All significant tests were 2 tailed, and p values ⬍0.05
California), with an analytic sensitivity of 1.4 pmol/L, inter- were considered statistically significant. All statistical anal-
and intra-assay coefficients of variation ⬍8%, and proinsu- yses were performed using SPSS (SPSS, Inc., Chicago,
lin cross-reactivity ⬍8.5%. The homeostasis model assess- Illinois).
ment of insulin resistance (HOMA-IR) was calculated using
the formula {[insulin (␮U/ml) ⫻ glucose (mg/100 ml)/18]/ Results
22.5}.15 FPI was measured in 1,174 women (mean age 46 ⫾
1 years, range 15 to 80) and 501 men (mean age 47 ⫾ 1 Table 1 lists the demographic and metabolic character-
years, range 15 to 80). As in previously published studies, to istics of the experimental population, divided on the basis of
 Preventive Cardiology/Plasma TG/HDL-C Ratio and Cardiometabolic Risk 1751

Table 2
Mean, standard deviation, and range of the plasma triglyceride/high-density lipoprotein cholesterol concentration ratio quartiles by gender
TG/HDL Cholesterol Ratio Women (n ⫽ 1,102) Men (n ⫽ 464)

Mean ⫾ SD Minimum Maximum Mean ⫾ SD Minimum Maximum

Quartile 1 0.99 ⫾ 0.16 0.18 1.23 1.14 ⫾ 0.21 0.64 1.47

Quartile 2 1.46 ⫾ 0.15 1.24 1.75 1.83 ⫾ 0.23 1.47 2.26
Quartile 3 2.05 ⫾ 0.21 1.75 2.48 2.84 ⫾ 0.36 2.28 3.52
Quartile 4 3.81 ⫾ 1.47 2.48 14.65 5.53 ⫾ 2.27 3.54 15.43
Quartiles 1–4 2.08 ⫾ 1.30 0.18 14.65 2.84 ⫾ 2.03 0.64 15.43

Data are expressed as mean ⫾ SD.

Table 3
Comparison of the cardiometabolic risk profile in women with triglyceride/high-density lipoprotein cholesterol concentration ratios ⬎2.5 and ⱕ2.5 and
in men with triglyceride/high-density lipoprotein cholesterol concentration ratios ⬎3.5 and ⱕ3.5
Variable TG/HDL Cholesterol Ratio

Women Men

ⱕ2.5 ⬎2.5 p Value* ⱕ3.5 ⬎3.5 p Value*

(n ⫽ 834) (n ⫽ 268) (n ⫽ 346) (n ⫽ 118)

Age (years) 44 ⫾ 18 50 ⫾ 16 ⬍0.001 44 ⫾ 18 50 ⫾ 13 ⬍0.001

FPI (␮U/ml) 7.1 ⫾ 4.8 10.7 ⫾ 6.6 ⬍0.001 6.9 ⫾ 7.5 10.7 ⫾ 6.9 ⬍0.001
HOMA-IR 1.64 ⫾ 1.18 2.53 ⫾ 1.68 ⬍0.001 1.65 ⫾ 1.79 2.63 ⫾ 1.80 ⬍0.001
Body mass index (kg/m2) 26.1 ⫾ 5.7 29.3 ⫾ 6.0 ⬍0.001 26.4 ⫾ 4.7 28.8 ⫾ 3.8 ⬍0.001
Waist circumference (cm) 90 ⫾ 14 98 ⫾ 14 ⬍0.001 93 ⫾ 12 100 ⫾ 10 ⬍0.001
Systolic blood pressure (mm Hg) 124 ⫾ 19 132 ⫾ 20 ⬍0.001 129 ⫾ 18 134 ⫾ 20 0.151
Diastolic blood pressure (mm Hg) 75 ⫾ 13 80 ⫾ 13 ⬍0.001 78 ⫾ 13 83 ⫾ 14 0.028
Glucose (mg/dl) 91 ⫾ 10 94 ⫾ 12 0.001 95 ⫾ 11 98 ⫾ 13 0.021
TG (mg/dl) 98 ⫾ 28 191 ⫾ 58 ⬍0.001 111 ⫾ 37 241 ⫾ 84 ⬍0.001
HDL cholesterol (mg/dl) 66 ⫾ 12 52 ⫾ 12 ⬍0.001 60 ⫾ 12 45 ⫾ 10 ⬍0.001
TG/HDL cholesterol ratio 1.51 ⫾ 0.47 3.84 ⫾ 1.48 ⬍0.001 1.93 ⫾ 0.74 5.50 ⫾ 2.26 ⬍0.001

Data are expressed as mean ⫾ SD.

* Analysis of covariance using age and study site (Rauch and San Andrés de Giles) as covariates.

Table 4
study site and gender. In general, the values in the 2 pop- Triglyceride/high-density lipoprotein cholesterol concentration ratio
ulations were comparable, although the Rauch group was sensitivity and specificity to identify insulin-resistant subjects
somewhat older, with higher blood pressures. Given the
Insulin Resistance Women, TG/HDL Men, TG/HDL
relative comparability of the values at the 2 sites, the ex- Estimate Cholesterol Ratio ⬎2.5 Cholesterol Ratio ⬎3.5
perimental data are combined in the tables. It should be
noted that the men and women were not different in terms Sensitivity Specificity Sensitivity Specificity
of age, FPI, HOMA-IR, and body mass index, whereas every (%) (%) (%) (%)
other experimental variable varied as a function of gender. FPI 43 82 43 81
The study population was divided into quartiles on the HOMA-IR 44 82 42 80
basis of the TG/HDL cholesterol concentration ratios, and
the comparison between men and women is listed in Table
2. It can be seen that the TG/HDL cholesterol ratios were significance. Most experimental variables were relatively
higher in men (p ⬍0.001), irrespective of quartile. How- similar in the women and men in the highest TG/HDL
ever, the magnitude of the difference between the 2 genders cholesterol quartile (Table 3). Furthermore, the FPI and
became greater as the TG/HDL cholesterol concentrations HOMA-IR values were almost identical between women
increased. Finally, the cut points separating the upper quar- and men who were in the TG/HDL cholesterol top quartile
tile from the other 3 were different, with values of about 2.5 (FPI p ⫽ 0.963, HOMA-IR p ⫽ 0.584).
and about 3.5 in women and men, respectively. Table 4 lists the sensitivity and specificity with which
Table 3 compares the cardiometabolic risk profiles of TG/HDL cholesterol ratios of 2.5 and 3.5 identified insulin-
men and women in the highest TG/HDL cholesterol quartile resistant women and men, respectively, using either FPI or
with those of subjects in the lowest 3 quartiles. In women, HOMA-IR values to define insulin resistance. There was a
every experimental variable was significantly worse in those high level of concordance with the 2 estimates of insulin
whose TG/HDL cholesterol ratios were ⬎2.5. The findings resistance (␬ ⫽ 0.88 in women and 0.85 in men). The
in men were comparable in that all the cardiometabolic risk sensitivity and specificity were essentially identical in men
factors were worse in those with TG/HDL cholesterol ratios and women when the gender-specific TG/HDL cholesterol
⬎3.5, although the increase in SBP did not reach statistical ratios were used.
1752 The American Journal of Cardiology (www.ajconline.org)

Discussion a relatively small number of South Americans, primarily of

European origin. Second, we evaluated only cardiometabolic
The possibility that the plasma TG/HDL cholesterol con-
risk, not disease outcomes. Third, the relatively modest sensi-
centration ratio might be helpful in identifying subjects without
tivity of the TG/HDL cholesterol ratios used in this study
known disease, likely to be insulin resistant, with the associ-
detracts from their clinical utility. However, the results in
ated metabolic abnormalities that increase risk for coronary
Table 4 demonstrate that these TG/HDL cholesterol ratios
heart disease (CHD), seemed worth exploring for at least 5
provide a reasonable degree of specificity in identifying, in a
reasons. First, increases in plasma TG and decreases in HDL
general population, subjects who are insulin resistant and at
cholesterol concentration have been identified as risk factors
increased cardiometabolic risk. Furthermore, although much
for CHD.17,18 Second, the TG/HDL cholesterol ratio, often
simpler to assess, the sensitivity and specificity values for
elevated in insulin-resistant patients, has been shown to inde-
pendently predict cardiovascular events.19,20 Third, insulin re- identifying high-risk subjects with the TG/HDL cholesterol
sistance is an independent predictor of TG and HDL choles- ratio and these gender-specific cut points are comparable to
terol concentrations.1 Fourth, hyperinsulinemia, as a surrogate those previously described using metabolic syndrome diagnos-
marker of insulin resistance, has been shown to predict CHD tic criteria.24 –27 Consequently, if the metabolic syndrome cri-
risk.16,21–23 Thus, there is ample evidence of relations among teria are considered useful in identifying subjects at high car-
insulin resistance and high TG and low HDL cholesterol con- diometabolic risk, this much simpler approach seems worthy
centrations. Finally, in the absence of a standardized assay for of further evaluation in other populations of European origin.
measuring plasma insulin concentration,4 the ratio of TG/HDL Finally, it would be of interest to develop gender-specific
cholesterol may serve as a pragmatic way to identify that criteria for TG/HDL cholesterol cut points that most effec-
portion of a general population that is at greatly increased risk tively identify subjects at enhanced cardiometabolic risk in
for CHD because of insulin resistance and associated abnor- non-European racial groups.
malities.
1. Laws A, Reaven GM. Evidence for an independent relationship be-
In addition to supporting the notion that the plasma
tween insulin resistance and fasting plasma HDL-cholesterol, triglyc-
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risk, our findings underline the importance of taking gender Use of metabolic markers to identify overweight individuals who are
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3. McLaughlin T, Reaven G, Abbasi F, Lamendola C, Saad M, Waters D,
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