Am J C/in Nutr 1993:58:463-7. Printed in USA. © 1993 American Society for Clinical Nutrition 463

Sex differences in the relation of visceral adipose tissueaccumulation to total body fatness�3

Sirnone Lemieux, Denis Prud’homme, Claude Bouchard, Angelo Tremblay, and Jean-Pierre Despr#{233}s

ABSTRACT The associations between the amount of ab-

dominal adipose tissue (AT) measured by computed tomography

(CT) or estimated with predictive equations and the amount of

total body fat were compared in samples of 89 men and 75

women. After correction for total body fat mass, men had sig-

nificantly higher values ofvisceral AT volume (P < 0.0001) and

also higher abdominal visceral AT areas, measured by CT or

estimated by predictive equations than women (P < 0.0001). In

addition, an increase in total fat mass was associated with a

significantly greater increase in visceral AT volume in men than

in women (P < 0.000 1 ). In conclusion, these results suggest that

the greater health hazards associated with excess fatness in men

than in women may be explained by the fact that premenopausal

women can accumulate more body fat than men of the same

age before reaching the amounts of visceral AT found in men.

.4tii J Clin Nutr 1993:58:463-7.

KEY WORDS Sex differences, regional fat distribution,

visceral fat, computed tomography, obesity

Introduction

Abdominal obesity is associated with greater risk for hyper-

tension, dyslipidemia, non-insulin-dependent diabetes, and cor-

onary heart disease (1-6). Obese subjects with peripheral adipose

tissue (AT) deposition are generally not at greater risk than are

nonobese individuals, whereas the prevalence of cardiovascular

disease is clearly increased among individuals with an excessive

accumulation of AT in the abdominal region. Moreover, the

amount of abdominal visceral AT has been demonstrated to be

strongly correlated with metabolic alterations (7-16). It is also

well recognized that there are sex differences in body-fat distri-

bution (17-19); men are prone to accumulate upper-body and

abdominal fat, whereas women generally present a pattern of

predominant gluteofemoral fat deposition.

Furthermore, a striking difference between men and women

is found when the visceral accumulation of AT is examined.

Results from Kvist et a! (20) have shown that, on average, men’s

visceral depots represent 2 1% ofthe total body fat mass whereas,

on average, 8% of the total body fat mass is deposited in the

intraabdominal depots in women (21). However, sex differences

in visceral AT deposition have not been systematically investi-

gated among subjects with wide ranges of total body fat, from

leanness to obesity, and several questions remain unanswered.

Indeed, we do not know whether the amount of visceral AT

increases linearly with increases in body fat and whether this

relationship is the same in men and women. To the best of our

knowledge, the only cross-sectional study available on sex dif-

ferences in visceral AT deposition has been performed by Kvist

et al ( 18), who demonstrated a linear relationship in men, ie, an

increase in total body fat mass was associated with an increase

in the total visceral AT volume. On the other hand, it has been

suggested that there was a nonlinear relationship in women be-

cause no increase in visceral AT was observed until women had

accumulated 30 L total body fat.

Therefore, the objective of the present study was to examine

the relationships between total body fatness and several indexes

of body-fat distribution, either measured by computed tomog-

raphy (CT) or estimated by predictive equations, in both men

and women. These analyses were performed on large samples

of men and women, covering a wide range of body fat mass, to

better understand the potential sex differences in the interaction

between visceral AT accumulation and total body fatness.

Subjects and methods

Subjects

Eighty-nine men aged 30-42 y and 75 premenopausal women

aged 23-50 y were recruited from the Qu#{233}becCity area by so-

licitation through the media. Subjects were free from metabolic

diseases that would require treatment (diabetes, hypertension,

coronary heart disease). All participants were subjected to a

medical examination and were also asked to sign an informed-

consent document. This study was approved by the Medical

Ethics Committee of Laval University.

Body composition, anthropometr.v, and computed tomography

Body density was measured by the hydrostatic weighing tech-

nique (22) and the mean of six measurements was used in the

� From the Lipid Research Center, Laval University Medical Research

Center, and the Physical Activity Sciences Laboratory, Laval University,Qu#{233}bec.

2 Supported by the Canadian Diabetes Association, the Qu#{233}becHeartand Stroke Foundation, the Medical Research Council (MRC) of Canada,and the Fonds de Ia recherche en sante du Qu#{233}bec(FRSQ).

3Address reprint requests to J-P Despr#{233}s,Lipid Research Center, Laval

University Medical Research Center, CHUL, 2705 Boulevard Laurier,

Ste-Foy, Qu#{233}bec,Canada GIV 4G2.Received October 6, 1992.Accepted for publication April 23, 1993.

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464 LEMIEUX ET AL

+ 200.9726 (WHR) + 1.7 137 (age) - 292.1026

calculation of body density. Pulmonary residual volume was

measured before immersion in the hydrostatic tank by using the

helium-dilution method of Meneely and Kaltreider (23). Total

fat mass was derived from body density by using the equation

of Siri (24). Body weight, subcutaneous skinfold thickness, and

waist and hip circumferences were also measured by using stan-

dardized procedures (25).

CT was performed on a Siemens Somatom DRH scanner

(Erlanger, Germany) by using the procedures of Sj#{246}str#{246}met al

(26), as previously described (27). Briefly, subjects were examined

in the supine position with both arms stretched above their heads.

An abdominal scan was obtained at the L4-L5 level by using a

radiograph ofthe skeleton as a reference to establish the position

of the scan to the nearest millimeter. Total abdominal AT was

calculated by delineating this area with a graph pen and then

computing the AT surface by using an attenuation range of -190

to -30 Hounsfield units (2 1). The visceral AT area was deter-

mined by delineating the abdominal cavity within the muscle

wall surrounding the area. The abdominal subcutaneous AT

area was calculated by subtracting the amount of visceral ab-

dominal AT from the total fat area. The sagittal diameter was

obtained from the image ofthe abdomen generated by the com-

puter following the recommendations of Sj#{246}str#{246}m(28).

Predictive equations

Predictive equations previously published by Kvist et al (18)

were used to evaluate the association between the estimated total

volume of visceral AT and total body fat mass in our sample,

for men and women separately. These equations are based on

CT-derived measurements of sagittal diameter. Equations used

for men and women are as follow (18):

Men: Total visceral AT volume

= 0.73 1 (sagittal diameter) - 1 1.5

Women: Total visceral AT volume

= 0.37 (sagittal diameter) - 4.85

Explained variance in total visceral AT volume obtained by these

equations were 8 1% in men and 79.6% in women when they

were first derived from samples of I 7 men and 10 women (I 8).

We were also interested in verifying whether values obtained

by the prediction of the level of abdominal visceral AT area

would show significant relationships with total body fatness. The

equation used for men was first developed in our laboratory and

included age, waist-to-hip ratio (WHR), and sagittal diameter

(29):

Abdominal visceral AT area = 1 .563 (age)

+ 160.662 (WHR) + 8.358 (sagittal diameter) - 274.05

This model explained 77% of abdominal visceral AT area vari-

ance when first developed with 110 subjects (29).We also used a predictive equation elaborated in our labo-

ratory to estimate the level of abdominal visceral AT area in

women (27). This equation included weight, abdominal and

subscapular skinfold thickness, WHR, and age as independent

variables:

Abdominal visceral AT area

= 1.0652 (wt) + 1.6649 (abdominal skinfold thickness)

+ 1.6934 (subscapular skinfold thickness)

This model explained 74% of abdominal visceral AT area vari-

ance in a group of 5 1 premenopausal women (27).

Statistical analyses

The unpaired Student’s t test was used to compare men and

women. Pearson’s correlation coefficients were used to quantify

the univariate associations among variables. Linear-regression

analysis was performed, and slopes and intercepts of the regres-

sion lines were compared (30). All these analyses were performed

on the SAS(Statistical Analysis System) statistical package (SAS

Institute, Cary, NC).

Results

On average, both groups of 89 men and 75 premenopausal

women were overweight but these subjects represented a wide

range of body fatness, ranging from lean to very obese (Table

1 ). Women had higher mean values for body mass index, total

body fat, and abdominal subcutaneous AT area than did men.

No difference for sagittal diameter was observed between the

two groups.

Despite the fact that they had, on average, lower amounts of

total body fat than did women, men displayed significantly higher

values of abdominal visceral AT areas either estimated by pre-

dictive equations or directly measured by CT. Men also had

significantly higher values for estimated total visceral AT volume.

Sagittal diameter, which is the anthropometric variable used

in equations predicting the total volume of visceral AT (18),

was strongly and significantly related to total fat mass in both

men (r = 0.88) and women (r = 0.95). Figure 1 shows the re-

lationship of estimated total visceral AT volume to total body

fat mass. For both men and women body fat mass was associated

with total visceral AT volume. In addition, the regression line

in men ((3 = 0.269) was significantly steeper (P < 0.0001) than

in women (/3 = 0.122).

The relationship between measured (by CT) abdominal vis-

ceral AT area and total body fat mass is presented in Figure 2.

Positive correlations were observed for both men and women.

In addition, the regression line was significantly steeper in men

(�3 = 4.32) than in women (�3 = 3.06) (P < 0.05). Also, the

interindividual variation was particularly large in men and some

subjects had values of abdominal visceral AT area quite remote

from the regression line, especially for high values of body fat

mass. We therefore performed a log10 transformation of scores

of abdominal visceral AT areas in an attempt to reduce the

variation; results obtained were essentially similar to those de-

rived from untransformed data (results not shown). As for direct

measurements obtained by CT, the predicted (estimated) values

of abdominal visceral AT were positively associated with total

body fat mass in men and in women (Fig 2). The intercept of

the regression line of men (34.56) was significantly higher than

that ofwomen (-26.62) (P < 0.0001), but the slopes were not

statistically different. Negative values of estimated abdominal

visceral AT have been considered to be equal to zero.

Finally, Figure 3 illustrates the relation of abdominal sub-cutaneous AT area measured by CT to total body fat mass. High

correlations were observed in both men and women. In contrast

to abdominal visceral AT area, estimated or measured by CT,

men displayed a significantly lower intercept value (-12.731)

than women (1.345) (P < 0.0001) whereas the slopes were not

statistically different.

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substantially increase their amount of visceral AT until they

have accumulated some 30 L ofAT (or �27.5 kg when we use

the density of triolein to calculate the total AT weight from the

Discussion

The study ofsex differences in body-fat distribution has been

the topic of several investigations (1 7-19). More than 40 y ago.

Vague (3 1) documented the metabolic implications of regional

AT distribution and was first to emphasize the health hazards

related to an android fat pattern. The present study clearly sup-

ports the well-established notion that premenopausal women

display a regional fat distribution profile that differs considerably

from that of men of the same age. In fact, after correcting for

total fat mass, men had higher values for visceral AT than women

whereas women displayed higher values for subcutaneous AT

than men.

The main objective ofthis study was to compare among men

and women the relation of some regional AT variables to total

body fat mass. The present results are partly at variance with

those of Kvist et al (1 8), who suggested that women do not

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TABLE 1

Body-fat-distribution variables in men and women*

SEX DIFFERENCES IN VISCERAL FAT 465

Men(n=89)

Women(n=75)

Age (y) 36.07 ± 3.32 (29.60-41.80) 35.38 ± 4.88 (22.77-49.50)

Body weight (kg) 83.06 ± 12.12 (59.50-108.10) 78.01 ± 19.89 (44.90-120.60)Body mass indext 27.56 ± 3.80 (19.37-34.17) 29.92 ± 7.46� (17.53-46.49)

Fat mass (kg) 22.60 ± 7.79 (6.40-37.30) 33.18 ± 14.86� (8.03-66.77)Abdominal subcutaneous AT area (cm2) 253.96 ± 100.76 (59.10-535.00) 427.90 ± 200.52f (54.33-8 12.00)Abdominal visceral AT area (cm2) 122.93 ± 48.96 (27.96-253.00) 103.71 ± 53.77f (23.67-234.00)

Estimated abdominal visceral AT area (cm2)II 124.24 ± 36.43 (45.00-190.82) 96.97 ± 59.5 It (-6.69-2 19.93)

Sagittal diameter (cm) 22.88 ± 3.26 (15.80-29.70) 22.88 ± 5.17 (13.70-32.70)

Estimated total visceral AT (L)1T 5.23 ± 2.39 (0.05-10.21) 3.61 ± l.9l** (0.22-7.25)

* .�: � SD: range in parentheses. AT. adipose tissue.

t In kg/m2.

f�** Significantly different from men: fP < 0.05. §P < 0.0001, **� < 0.01.� Predictive equations for men from Despr#{233}set al (29) and for women from Ferland et al (27).

#{182}Predictive equations for men and women from Kvist et al (18).

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FIG 2. Relationships between total body fat mass and abdominalvisceral adipose tissue (AT) area measured by CT or estimated by using

predictive equations in 89 men and 75 premenopausal women. Bothcorrelation coefficients for measured and estimated values were signifi-

cant. P < 0.0001.

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U

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466 LEMIEUX ET AL

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FIG 3. Relationships between total body fat mass and abdominal

subcutaneous adipose tissue area measured by CT in 89 men and 75premenopausal women.

total volume of body fat). According to their results, the ratio

of visceral to total fat storage would be the same above this

amount for both men and women. Therefore, they concludedthat women are protected against visceral AT accumulation until

they reach a certain amount of total body fat, above which they

begin to accumulate visceral AT at the same rate as do men.

Our results indicate that, on average, for a similar increase inthe amount of total body fat, a smaller increase in the amount

of visceral AT is noted in women than in men, and that such adifference is constant over the whole range of body-fat-mass

values. Results ofthe present study therefore indicate that women

display a lower ratio of visceral to total body fat deposition for

any value of total body fat mass. The apparent discrepancy be-

tween the conclusions reached by Kvist et al ( 1 8) and results of

the present study could potentially be attributed to differencesin sample size because we studied a sample of 89 men and 75

women whereas Kvist et al used a smaller sample (24 men and

19 women). In addition, most of their subjects, especially the

women, displayed a total body fat mass < 30 kg. In contrast,

our sample included a large proportion of obese subjects with

total body fat mass values > 30 kg.

After correction for total body fat mass, men presented sig-

nificantly higher amounts of visceral AT than did women. These

results suggest that, on average, women can accumulate higher

amounts of total body fat mass before reaching amounts of vis-ceral AT that are similar to amounts in men. In addition, the

slopes ofthe regression lines ofabdominal visceral AT area and

of total visceral AT volume to body fat mass were greater in

men than in women. In fact, there is not much descriptive data

available on the amount of total visceral AT despite the fact

that visceral obesity is a significant health hazard (8-16). There-

fore, the greater increase in abdominal visceral AT area in men

than in women, for similar increases in total body fat mass,

suggests that obesity will be more detrimental to the health of

men than to that of women. From the substantial significant

alterations in plasma glucose-insulin homeostasis and in plasma

lipoprotein concentrations that have been related to visceral

obesity. the high proportion of visceral AT in men clearly rep-

resents a health burden.

Abdominal AT areas either directly measured by CT or es-

timated by predictive equations were highly correlated with total

body fat mass in both men and women. However. there was no

difference in the slopes between men and women when the es-

timated abdominal visceral AT area was plotted against total

body fat mass, whereas the slope ofthe regression of abdominal

visceral AT area measured by CT against the amount of total

body fat was steeper in men than in women. From Figure 2 it

is obvious that a group of male subjects deviated considerably

from the regression ofabdominal visceral AT area measured by

CT over total body fat mass. Therefore. for these male subjects

it appeared very difficult to precisely predict abdominal visceral

AT area. especially in the obese men. Other variables beside

those used in the predictive equation could influence visceral

AT deposition. eg, sex steroid and glucocorticoid concentrations,

stress, physical inactivity, and genetic variation (16, 32-35). Al-

though our equation for the prediction of abdominal visceral

AT deposition has been validated by others and was found toproduce no significant difference between estimated and mea-

sured abdominal visceral AT areas (36), we are fully aware of

the limitations ofsuch predictive equations for individual cases.

Nevertheless, anthropometric measurements such as the sagittal

diameter. the waist circumference. the WHR, and some sub-

cutaneous skinfold thicknesses could be useful in the identifi-

cation ofobese patients potentially at increased risk for metabolic

alterations related to visceral obesity. It is also important to

mention that we have used the sagittal diameter obtained from

CT scans to estimate men’s abdominal AT area and to predict

the total volume ofvisceral AT. The validity ofsagittal diameter

obtained by anthropometry has been tested by Koester et al

(36), and the correlation of anthropometric sagittal diameter

with sagittal diameter derivated from CT images was highly sig-

nificant (r = 0.94).

The accumulation of abdominal subeutaneous AT has been

shown to be proportionally similar in both sexes. Indeed, for a

same increase in total body fat mass, men accumulated more

AT in visceral depots than did women but men and women

stored equal amounts of AT in the abdominal subcutaneous

compartment. These results suggest that, in women, deposition

of abdominal subcutaneous AT does not compensate for the

decreased AT accumulation in the visceral depots, supporting

the notion that other regions, such as the gluteofemoral region,

may represent important sites of preferential AT deposition in

premenopausal women.

Among potential limitations that need to be considered in

the interpretation of our data, the single-scan approach for the

measurement ofvisceral AT deposition deserves some discussion.Obviously, because there is some variation within the abdomen

in the cross-sectional areas of visceral AT (19), it is possible that

a single L4-L5 scan procedure could have generated a greater

measurement error, explaining the lower correlation observed

between body fat mass and the measured visceral AT area in

comparison with the estimated visceral AT area. Although this

possibility remains likely, a clear dissociation between responses

of the visceral and the subcutaneous abdominal adipose depots

has been reported after overfeeding (37). This latter finding sup-

ports the notion that considerable individual variation in the

amount of visceral AT truly exists for a given amount of total

body fat in both men and women.

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SEX DIFFERENCES IN VISCERAL FAT 467

In summary, results of the present study indicate that the

proportion of visceral AT is different among the sexes, even

after correction for sex differences in the amount of total body

fat. We also demonstrated that obesity is associated with a greater

proportion ofvisceral AT accumulation in men than in women.

Finally, our results suggest that the preferential accumulation

of AT in visceral depots found in men when compared with

premenopausal women may be a determinant factor for the

greater health hazards of obesity in men than in women. El

We are grateful to the subjects for their excellent cooperation and tothe dedicated staff of the Physical Activity Sciences Laboratory. Sincerethanks are expressed to J Maheux. J Hovington. S Brulotte, H Bessette,and C Leblanc for their help in the collection and analysis of the data.

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