Donate Help Contact The AHA Sign In Home
American Heart Association
Arteriosclerosis, Thrombosis, and Vascular Biology
Search: search_blue_button Advanced Search
Arteriosclerosis, Thrombosis, and Vascular Biology. 1999;19:2448-2455

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowRequest Permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Couillard, C.
Right arrow Articles by Després, J.-P.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Couillard, C.
Right arrow Articles by Després, J.-P.
Related Collections
Right arrow Nutrition
Right arrow Risk Factors
Right arrow Lipid and lipoprotein metabolism
(Arteriosclerosis, Thrombosis, and Vascular Biology. 1999;19:2448-2455.)
© 1999 American Heart Association, Inc.


Atherosclerosis and Lipoproteins

Gender Difference in Postprandial Lipemia

Importance of Visceral Adipose Tissue Accumulation

Charles Couillard; Nathalie Bergeron; Denis Prud'homme; Jean Bergeron; Angelo Tremblay; Claude Bouchard; Pascale Mauriège; Jean-Pierre Després

*    Abstract
up arrowTop
*Abstract
down arrowIntroduction
down arrowMethods
down arrowResults
down arrowDiscussion
down arrowReferences
 
Abstract—Insulin resistance, hyperinsulinemia, hypertriglyceridemia, and low HDL-cholesterol concentrations are common features of a plurimetabolic syndrome, which increases the risk of coronary artery disease. Although it has been proposed that the development of atherosclerosis through alterations in plasma lipid levels could be a postprandial phenomenon, most studies on gender differences in plasma lipoprotein-lipid concentrations have reported fasting levels. Therefore, the aim of our study was to examine the response of postprandial triglyceride-rich lipoproteins to a standardized meal in 63 men and 25 women. In addition to the measurement of fasting and postprandial plasma lipid levels, numerous physical and metabolic variables were assessed, including body composition by underwater weighing and body fat distribution by computed tomography. Although no gender difference was noted in total body fat mass, men were characterized by a preferential accumulation of abdominal adipose tissue as revealed by an increased waist circumference and a greater visceral adipose tissue accumulation (50% difference) compared with women (P<0.001). Men also showed a greater plasma triglyceride response (P<0.005) as well as increased postprandial insulin and free fatty acid levels compared with women (P<0.01). Visceral adipose tissue was significantly associated with the postprandial triglyceride response in both genders (men: r=0.49, P<0.0001; women: r=0.43, P<0.05). Finally, when men and women were matched for visceral adipose tissue accumulation, the gender difference in postprandial plasma triglyceride response was eliminated. Thus results of the present study suggest that the well known gender difference in visceral adipose tissue accumulation is an important contributing factor involved in the exaggerated postprandial triglyceride-rich lipoprotein response noted in men compared with women.


Key Words: postprandial lipemia • gender differences • visceral obesity • free fatty acids


*    Introduction
up arrowTop
up arrowAbstract
*Introduction
down arrowMethods
down arrowResults
down arrowDiscussion
down arrowReferences
 
Alterations in plasma lipoprotein-lipid concentrations are known to increase the risk of coronary artery disease (CAD) in both men and women.1 2 However, at all ages, the prevalence of CAD in women is lower than in men, and the gender difference in plasma lipoprotein-lipid levels as well as in the prevalence of type II diabetes are believed to be responsible, at least in part, for the higher CAD risk observed in men. Indeed, men are characterized by an overall less favorable plasma lipid profile, which includes high fasting triglyceride (TG) and low HDL-cholesterol concentrations compared with women.3 Men and women also show marked differences in indices of plasma glucose-insulin homeostasis.4 5 Furthermore, an increased visceral adipose tissue (AT) accumulation has been reported in men compared with women and this factor could also contribute to the gender difference in the CAD risk profile.6 7

Although the contribution of altered plasma lipoprotein-lipid levels to the increased risk of CAD is well known, most studies reporting such a relationship have examined fasting concentrations. However, Zilversmit8 has suggested that the development of atherosclerosis could be a postprandial phenomenon, and the renewed interest for postprandial studies has allowed the identification of various physiological conditions that influence postprandial lipoprotein metabolism. It has therefore been reported that age,9 10 diet,11 physical activity,12 13 14 non–insulin dependent diabetes mellitus15 16 as well as obesity,17 and body fat distribution18 19 20 21 all affect dietary fat clearance. In addition, a gender dimorphism has been reported in postprandial lipoprotein-lipid metabolism, as women generally show a lower postprandial triglyceride response to a dietary fat challenge compared with men.10 22 However, little is known about the physiological mechanisms responsible for this gender dimorphism.

Therefore, the aim of the present study was to examine the contribution of the gender difference in visceral AT accumulation to the variation in postprandial lipoprotein-lipid levels. For that purpose, 63 men and 25 women were investigated and their plasma triglyceride-rich protein (TRL) responses measured over a period of 8 hours after the ingestion of a standardized meal.


*    Methods
up arrowTop
up arrowAbstract
up arrowIntroduction
*Methods
down arrowResults
down arrowDiscussion
down arrowReferences
 
Subjects
Sixty-three men (mean age±SD: 45.0±10.0 years) and twenty-five premenopausal women (41.6±10.9 years) were recruited through the media and selected to cover a wide range of body fatness values. All women were tested during the follicular phase (between days 5 and 12) of their menstrual cycle. None of the women were using oral contraceptives. Subjects gave their written consent to participate in the study, which was approved by the Medical Ethics Committee of Laval University. Subjects with diabetes or with coronary heart disease were excluded from the present study. None of the subjects were on medication known to affect insulin action or plasma lipoprotein levels.

Anthropometric and Body Composition Measurements
Body weight, height, waist, and hip circumferences were measured following standardized procedures,23 and the waist-to-hip ratio was calculated. Body density was measured by the hydrostatic weighing technique.24 The mean of 6 measurements was used in the calculation of percent body fat from body density using the equation of Siri.25 Fat mass was obtained by multiplying body weight by percent body fat.

Computed Tomography
Visceral AT accumulation was assessed by CT, which was performed on a Siemens Somatom DRH scanner using previously described procedures.26 27 Briefly, the subjects were examined in the supine position with both arms stretched above the head. The scan was performed at the abdominal level (between L4 and L5 vertebrae) using an abdominal scout radiograph to standardize the position of the scan to the nearest millimeter. The total AT area was calculated by delineating the abdominal scan with a graph pen and then computing the AT surface with attenuation range of -190 to -30 Hounsfield units.26 27 28 The abdominal visceral AT area was measured by drawing a line within the muscle wall surrounding the abdominal cavity. The abdominal subcutaneous AT area was calculated by subtracting the visceral AT area from the total abdominal AT area.

Oral Lipid Tolerance Test
After a 12-hour overnight fast, an intravenous catheter was inserted into a forearm vein for blood sampling. Each participant was given a test meal containing 60g fat/m2 body surface area.18 The meal consisted of eggs, cheese, toasts, peanut butter, peaches, whipped cream, and milk. The meal provided 64% of calories from fat, 18% from carbohydrates, and 18% from protein. The test meal was well tolerated by all subjects. After the meal, subjects were not allowed to eat for the 8 hours after meal intake but were given free access to water. Blood samples were drawn before the meal and every 2 hours after the meal over an 8-hour period.

Fasting and Postprandial Plasma Lipoprotein Concentrations
Plasma was separated immediately after blood collection by centrifugation at 3000 rpm for 10 minutes at 4°C. Triglyceride and cholesterol concentrations in total plasma were determined enzymatically on a RA-500 Auto-Analyzer (Bayer Corporation Inc), as previously described.29 Each plasma sample (4 mL) was then subjected to a 12-hour ultracentrifugation (50 000 rpm) in a Beckman 50.3Ti rotor at 4°C in 6 mL Beckman Quickseal tubes, which yielded 2 fractions: the top fraction containing TRL (d<1.006 g/mL; total) and the bottom fraction consisting of triglyceride-poor lipoproteins (d>1.006 g/mL). Using the distilled water layering technique and modified method of Ruotolo et al,30 the total-TRL fraction was further separated by a 5-minute spin (40 000 rpm) at 4°C using the same tubes and rotor into 3 subclasses of TRL namely: large, medium, and small. A small volume (100 µL) of a d=1.019 g/mL saline solution was added to the total-TRL fraction to facilitate water layering. The large-TRL fraction was collected by tube slicing and made up to a final volume of 1 mL with 0.15 mol/L NaCl. The next 3 mL of the middle layer were collected by aspiration as medium-TRL, and the final 2 mL were considered as the small-TRL fraction. Large-TRL consist of lipoproteins of Sf>400, whereas the medium- and small-TRL are within a spectrum of particles of Sf 20 to 400.30 Furthermore, in a pilot study (n=5) conducted in our laboratory (Bergeron et al, unpublished observations, 1998) in which apo B-48 and apo B-100 concentrations were measured, it was found that although the protein concentration of the fraction designated large-TRL is very low, it is predominantly rich in apo B-48, with a minor contribution of apo B-100 particles. In contrast, the predominant apolipoprotein found in the fraction designated small-TRL was apo B-100 (>95% of total apo B). Finally, the fraction designated medium contained both apo B-48 and apo B-100. HDL particles were isolated from the bottom fraction (d>1.006 g/mL) after precipitation of apo B–containing lipoproteins with heparin and MnCl2.31 The triglyceride and cholesterol contents of each fraction, ie, large-, medium-, and small-TRL, as well as HDL, were quantified on the Auto-Analyzer. All lipoprotein isolation procedures were completed within 2 to 3 days of the fat load. Plasma free fatty acid (FFA) levels were also measured at 0, 2, 4, 6, and 8 hours using an enzymatic method.32 Total apo B concentration was measured in plasma by the rocket immunoelectrophoretic method, as previously described.33 The lyophilized serum standard for apo B measurement was prepared in our laboratory and calibrated with reference standards obtained from the Centers for Disease Control.

Glucose and Insulin Concentrations
Fasting and postprandial plasma glucose concentrations were determined using the glucose oxidase assay34 (SIGMA). Plasma insulin levels were measured by a commercial double antibody radioimmunoassay (LINCO Research) that shows little cross-reactivity (<0.02%) with proinsulin.35

Statistical Analyses
Pearson product-moment correlation coefficients were used to quantify associations between variables. Differences between men and women were tested for significance using the Student's t test. The different areas under the curve of TG, FFA, insulin, and glucose concentrations were determined by the trapezoid method. Multiple regression analyses were performed to quantify the independent contributions of age, gender, fat mass, abdominal visceral, and subcutaneous AT to the variance of postprandial plasma triglyceride response. Fasting TG, HDL-cholesterol, insulin, and FFA levels, as well as postprandial insulin and FFA responses, were also included in the statistical model. All analyses were conducted on the SAS statistical package (SAS Institute).


*    Results
up arrowTop
up arrowAbstract
up arrowIntroduction
up arrowMethods
*Results
down arrowDiscussion
down arrowReferences
 
Physical characteristics and fasting metabolic profiles of men and women are presented in Table 1Down. Although both genders had the same amount of total body fat, there were significant differences in body fat distribution. Indeed, men were characterized by an increased abdominal AT accumulation as expressed by higher waist circumference and waist-to-hip ratio values compared with women. Furthermore, men displayed a greater amount of visceral AT than women. In contrast, significantly higher levels of abdominal subcutaneous AT were noted in women compared with men. Gender differences in the fasting metabolic risk profile were also observed as men were characterized by increased plasma cholesterol, triglyceride, and glucose levels, as well as by decreased plasma HDL-cholesterol concentrations compared with women. Men also showed higher fasting plasma insulin levels than women, but this difference did not reach statistical significance.


View this table:
[in this window]
[in a new window]
 
Table 1. Physical Characteristics and Fasting Metabolic Profile of the Subjects

Figure 1Down illustrates plasma TG as well as the triglyceride content of the various TRL subfractions of men and women throughout the entire postprandial period. Men showed significantly higher triglyceride levels at all times compared with women. These higher plasma triglyceride levels noted during the postprandial period resulted in a greater triglyceride response in men compared with women and were also reflected by significantly higher TG levels in all TRL fractions (total, large, medium, small) at all time points. Furthermore, gender differences were also observed in postprandial insulin and FFA concentrations, as men displayed higher postprandial insulin and FFA levels compared with women (Figure 2Down).



View larger version (31K):
[in this window]
[in a new window]
 
Figure 1. Postprandial plasma (A), as well as total- (B), large- (C), medium- (D), and small-TRL (B) triglycerides concentrations in men (M; n=63; black circles and bars) and women (W; n=25; white circles and bars). Bars represent the areas under the incremental curves (responses). Values are expressed as means±SEM. Significantly different from women at *P<0.05; {dagger}P<0.01; {ddagger}P<0.005.



View larger version (17K):
[in this window]
[in a new window]
 
Figure 2. Postprandial glucose (A), insulin (B), and FFA (C) concentrations in men (M; n=63; black circles and bars) and women (W; n=25; white circles and bars). Bars represent the areas under the incremental curves (responses). Values are expressed as means±SEM. Significantly different from women at *P<0.05; {dagger}P<0.01; {ddagger}P<0.005.

In both genders, increased adiposity was associated with a greater postprandial lipemia, as body fat mass as well as abdominal visceral and subcutaneous AT were positively correlated with the plasma triglyceride response (Figure 3Down). In addition, we noted that for a similar accumulation of abdominal subcutaneous AT, women had a lower postprandial triglyceride response compared with men (Figure 3BDown). However, the relationship of visceral AT to plasma triglyceride response did not appear to differ between men and women (Figure 3CDown). We also found that in men, abdominal visceral AT, but not subcutaneous AT, was positively associated with the postprandial FFA response (Figure 4Down). However, this association was not observed in women.



View larger version (21K):
[in this window]
[in a new window]
 
Figure 3. Associations between fat mass (A), as well as abdominal subcutaneous (B) and visceral AT (C), and the postprandial plasma triglyceride response in men (n=63; black circles and solid lines) and women (n=25; white circles and dotted lines).



View larger version (24K):
[in this window]
[in a new window]
 
Figure 4. Associations between abdominal visceral (A), as well as subcutaneous AT accumulation (B), and postprandial plasma FFA response in men (n=63; black circles and solid line) and women (n=25; white circles).

As shown in Table 2Down, some variables of the fasting metabolic profile were associated more closely with the postprandial plasma triglyceride response than adiposity indices. Indeed, increased fasting plasma triglyceride and insulin levels were predictive of a greater triglyceride response in both men and women. We also found that low fasting HDL-cholesterol levels were associated with an increased triglyceride response and that elevated fasting apo B concentrations were correlated with higher postprandial triglyceride levels. However, these latter relationships were only noted in men.


View this table:
[in this window]
[in a new window]
 
Table 2. Correlations Between Fasting Metabolic Profile Variables and the Postprandial Triglyceride Response in Men and Women

To further examine the importance of visceral AT accumulation to the gender difference in postprandial lipemia, we matched men and women on the basis of visceral AT (Table 3Down) regardless of total body fat mass and examined their respective postprandial triglyceride responses. Despite having identical levels of visceral AT, women were characterized by increased overall adiposity and abdominal subcutaneous AT accumulation. After the matching procedure, the difference in postprandial plasma triglyceride levels was no longer significant between men and women (Figure 5Down). We also compared the plasma triglyceride responses of men and women who were matched for total body fat mass and abdominal subcutaneous AT. These comparisons revealed a greater postprandial plasma triglyceride response in men than in women (Figure 5Down). We also examined the impact of matching subjects for visceral AT on the triglyceride responses in the various TRL subfractions (Figure 6Down). We found no significant difference in total-, large-, and medium-TRL triglyceride responses between men and women. On the other hand, the matching procedure failed to eliminate the difference in small-TRL levels as women were characterized by a lower triglyceride response in this subfraction compared with men. Matching men and women for visceral AT also affected postprandial plasma glucose and insulin responses as shown both genders were characterized by similar glucose and insulin responses after pairing men and women for visceral AT accumulation (Figure 7Down). However, women were still characterized by a lower FFA response after the fat load compared with men.


View this table:
[in this window]
[in a new window]
 
Table 3. Body Fatness and Adipose Tissue Distribution of Men and Women Matched for A) Total Body Fat Mass, B) Abdominal Subcutaneous Adipose Tissue, or C) Visceral Adipose Tissue



View larger version (19K):
[in this window]
[in a new window]
 
Figure 5. Postprandial plasma triglyceride concentrations in men (M; black circles and bars) and women (W; white circles and bars) matched for body fat mass (20 pairs) (A), as well as abdominal subcutaneous (16 pairs) (B) and visceral AT accumulation (19 pairs) (C). Bars represent the areas under the incremental curves (responses). Values are expressed as means±SEM. Significantly different from women at *P<0.05; {dagger}P<0.01; {ddagger}P<0.005.



View larger version (16K):
[in this window]
[in a new window]
 
Figure 6. Postprandial triglyceride concentrations of total- (A), as well as large- (B), medium- (C), and small-TRL (D) in men (M; n=19; black circles and bars) and women (W; n=19; white circles and bars) matched for visceral AT accumulation. Bars represent the areas under the incremental curves (responses). Values are expressed as means±SEM. Significantly different from women at *P<0.05; {dagger}P<0.01.



View larger version (18K):
[in this window]
[in a new window]
 
Figure 7. Postprandial plasma glucose (A), insulin (B), and FFA (C) concentrations in men (M; n=19; black circles and bars) and women (W; n=19; white circles and bars) matched for visceral AT accumulation. Bars represent the areas under the incremental curves (responses). Values are expressed as means±SEM. Significantly different from women at *P<0.05.

Finally, we conducted multiple regression analyses to quantify the independent contributions of age, gender, and adiposity indices, as well as fasting and postprandial metabolic profile variables to the variance of the postprandial plasma triglyceride response (Table 4Down). Fasting triglyceride concentration was by far the best predictor of plasma triglyceride response, accounting for more than 61% of its variance (Model 1). However, when fasting TG level was removed from the model (Model 2), fasting apo B level showed the greatest contribution to the plasma triglyceride response (37%). In Model 3, both fasting TG and apo B levels were excluded on purpose from the statistical model. In this restricted model, 27% of the variance of the plasma triglyceride response was attributed to visceral AT accumulation. It seems important to point out that, in all models, postprandial FFA response and fasting insulin concentration were significant predictors of the postprandial plasma triglyceride response. However, gender per se did not contribute to the variation in postprandial triglyceride levels after control for visceral AT accumulation and related fasting metabolic variables (TG, apo B, FFA, and insulin).


View this table:
[in this window]
[in a new window]
 
Table 4. Multivariate Regression Analyses Showing the Independent Contributions of Physical and Metabolic Characteristics to the Postprandial Plasma Triglyceride Response


*    Discussion
up arrowTop
up arrowAbstract
up arrowIntroduction
up arrowMethods
up arrowResults
*Discussion
down arrowReferences
 
Gender differences in fasting plasma lipoprotein-lipid concentrations have already been reported.3 36 In the present study, we also found that men were characterized by increased fasting plasma cholesterol and triglyceride levels as well as by decreased HDL-cholesterol concentrations compared with women. In addition, men also displayed higher fasting plasma glucose and insulin levels than women, although the gender difference in fasting insulinemia did not reach statistical significance. These metabolic alterations are considered as features of the insulin-resistance syndrome.37 On the other hand, it has been suggested that differences in adiposity, especially in body fat distribution, between men and women may be involved in the gender dimorphism noted in plasma lipoprotein-lipid levels. Indeed, men are known to present a preferential accumulation of AT in the abdominal visceral depot, whereas women are characterized by a more peripheral AT distribution.38 In the present study, we found that despite having similar levels of total body fat in kg compared with women, men were characterized by an increased abdominal fat accumulation as indicated by higher waist circumference and visceral AT values.

Significant gender differences were also noted in postprandial lipemia men being characterized by a greater postprandial plasma triglyceride response compared with women. This result is concordant with previous observations that reported higher postprandial triglyceride levels in men than in women.10 22 In the present study, gender differences in the postprandial triglyceride response profile were also noted. In men, plasma triglyceride levels peaked later during the postprandial period than in women. Because the increase in triglycerides (from 2 to 4 hours) after meal consumption mainly reflects dietary TG absorption, whereas the return to fasting levels (from 6 to 9 hours postprandially) is presumably a function of TRL clearance,11 our results of a delayed postprandial TG peak in men suggest an impaired postprandial clearance of TRL compared with women.

The strong association between fasting TG and the postprandial plasma triglyceride response indicates that fasting triglyceridemia is an important correlate of the gender difference in postprandial lipemia. Indeed, on their entry into the circulation, both newly synthesized and endogenous TRL compete for lipoprotein lipase (LPL) to be hydrolyzed.39 Thus, in men, the increased quantity of TRL before the meal as indicated by their fasting hypertriglyceridemic state may contribute to the delayed clearance of postprandial triglycerides from the plasma. This accumulation of TRL related to the presumed "saturation" of LPL would also postpone the postprandial peak plasma triglyceride concentration. The gender difference in TRL clearance after a meal could also be the result of an increase in the contribution of hepatic TRL to total-TRL at the late stages of the postprandial period. Under insulin-resistant conditions, the antilipolytic effect of insulin on AT is very weak,40 which would explain the raised FFA levels observed postprandially in subjects with visceral obesity.18 This increased flux of FFA to the liver would promote the synthesis and secretion of VLDL. This model is supported by results presented in Figure 2Up. Indeed, we noted that, in men, there was a progressive increase in plasma FFA levels, which resulted in 8-hour plasma FFA concentrations that remained well above fasting values, whereas in women, plasma FFA levels at the end of the postprandial period were near fasting concentrations. Furthermore, our results are supported by a previous study41 in which men and women had been shown to differ significantly in the postprandial regulation of AT lipolysis. Indeed, men were characterized by an AT nonesterified fatty acid release that was more resistant to the postprandial antilipolytic effect of insulin.41 On the other hand, the increase in postprandial FFA concentrations may also be resulting from an increased lipolysis of TRL by LPL paralleled by an inadequate esterification of FFA into triglycerides by the AT.42 However, the present study did not allow us to quantify the contribution of both physiological processes, ie, increased AT or TRL lipolysis, to the increased postprandial FFA response in men. Further studies in this area are clearly warranted.

Nevertheless, our results indicate that visceral AT accumulation plays a major role in the gender difference in postprandial lipemia. Accordingly, we found no difference in postprandial lipemia among men and women matched for visceral AT accumulation. We also have examined the impact of the matching procedure on the different TRL subclasses. We found that there was no difference in total- as well as in large- and medium-TRL triglyceride responses between men and women with similar levels of visceral AT. However, a gender difference remained in the small-TRL triglyceride response as men had higher 2-, 4-, and 6-hour small-TRL triglyceride concentrations compared with women matched for similar visceral AT accumulation. It is suggested that the remaining increased postprandial FFA response noted in men, after the matching procedure, may have contributed to their higher small-TRL triglyceride response compared with women. Particle size has also been suggested to affect the rate of TRL clearance, with large particles being better substrates for lipolysis by LPL than smaller particles.43 Our finding of a more prolonged accumulation of small-TRL triglycerides but not of large- and medium-TRL in men than women matched for visceral AT is concordant with this observation.

Multiple regression analyses revealed that the fasting triglyceride levels were by far the best predictors of the plasma triglyceride response to the fat load (Model 1). The contribution of apo B–containing lipoproteins to postprandial lipemia was also highlighted as fasting apo B concentration became the strongest predictor of plasma triglyceride response after fasting triglyceridemia was eliminated from the statistical model. Because apo B found in the fasting plasma is secreted through lipoproteins of hepatic origin, our results provide further support to the concept of a hepatic contribution to the delayed clearance of TRL in men.44 However, further studies are needed to support this notion and measurements of apo B-48 and apo B-100 containing TRL, which are respectively used as markers of TRL of intestinal and hepatic origin, will have to be performed in future studies.

It is known that visceral obesity is associated with metabolic abnormalities such as fasting hypertriglyceridemia, hyperinsulinemia, and increased apo B concentrations as well as lower HDL-cholesterol levels.6 45 Recently, we have reported that visceral obese men are characterized by an impaired postprandial TRL clearance compared with obese men with low levels of visceral AT.18 In the present study, when both fasting TG and apo B concentrations were eliminated on purpose from the multiple regression analyses, the amount of visceral AT was found to be the best predictor of TRL triglyceride response. Furthermore, we also quantified (data not shown) the independent contributions of total body fat mass and AT distribution variables (including subcutaneous abdominal fat measured by CT) to the fasting TG and apo B levels. In both cases, visceral AT accumulation was the best and only significant predictor of these metabolic variables. As women have less visceral AT than men,39 we tested the hypothesis that their preferential accumulation of subcutaneous AT would be associated with a more favorable postprandial TRL metabolism. Results of the present study provide further support to such an hypothesis. Indeed, for a similar abdominal subcutaneous AT accumulation, women had a lower postprandial triglyceride response compared with men (Figure 3Up). Although we were not able to study the physiological mechanisms responsible for this phenomenon, previous results have indicated that subcutaneous AT may have a greater capacity for FFA esterification into adipose cell TG than omental AT.46 This peculiar metabolic behavior of subcutaneous fat is concordant with the faster clearance of TG-rich lipoproteins after a meal in women who have more subcutaneous AT than men. However, results of the present study support the notion that visceral AT may be more critical to the gender difference in postprandial lipemia than subcutaneous AT. Indeed, when men and women were matched on the basis of visceral AT accumulation, women remained characterized by a substantially greater subcutaneous AT depot compared with men (409 versus 234 cm2, respectively). Thus, had subcutaneous AT had a greater impact on postprandial lipemia than visceral AT, a significant difference in postprandial TRL levels between men and women would have been expected even after they were matched for visceral AT accumulation. In the present study, such a difference in TRL response was minimal after men and women were matched for visceral AT despite the fact that matched women had more subcutaneous AT than matched men.

Although matching men and women for the level of visceral AT eliminated the gender difference in plasma triglyceride response, there was a tendency for men to display a greater triglyceridemic response compared with women. This gender difference was evident for the response of the small-TRL fraction. Other factors have been proposed to explain the lower postprandial lipemia in women than in men. For instance, estrogens have been suggested to have a favorable impact on postprandial triglyceridemia.47 Variation in LPL activity between men and women47 48 may also be implicated in the gender difference in postprandial lipemia. Once again, the greater accumulation of subcutaneous fat in women than in men could play a role in the gender difference noted in the clearance of TRL after a dietary fat challenge.

In summary, results from the present study indicate that there is a gender difference in postprandial lipemia as men show a greater postprandial triglyceridemic response to a meal than women. Although this difference is likely to result from the influence of several factors, our results suggest that the increased visceral AT accumulation in men makes an important contribution to this delayed dietary fat clearance. Concomitant impairment of postprandial FFA metabolism after meal consumption and a reduced ability to store lipids in subcutaneous AT may be responsible, at least in part, for this exaggerated lipemic response observed in men compared with women.


*    Acknowledgments
 
This study was supported by the Medical Research Council of Canada and by the Québec Heart and Stroke Foundation. We would like to thank the staff of the Physical Activity Sciences Laboratory for data collection and the personnel of the Lipid Research Center for their excellent and dedicated work.

Received November 12, 1998; accepted February 22, 1999.


*    References
up arrowTop
up arrowAbstract
up arrowIntroduction
up arrowMethods
up arrowResults
up arrowDiscussion
*References
 
1. Lerner DJ, Kannel WB. Patterns of coronary heart disease morbidity and mortality in the genderes: A 26-year follow-up to the Framingham population. Am Heart J. 1986;11:383–390.

2. Wingard DL, Suarez L, Barrett-Connor E. The gender differential in mortality from all causes and ischemic heart disease. Am J Epidemiol. 1983;117:165–172.[Abstract/Free Full Text]

3. Godsland IF, Wynn V, Crook D, Miller NE. Sex, plasma lipoproteins and atherosclerosis: Prevailing assumptions and outstanding questions. Am Heart J. 1987;114:1467–1503.[Medline] [Order article via Infotrieve]

4. Modan M, Or J, Karasik A, Drory Y, Fuchs Z, Lusky A, Chetrit A, Halkin H. Hyperinsulinemia, gender and risk of atherosclerotic cardiovascular disease. Circulation. 1991;84:1165–1175.[Abstract/Free Full Text]

5. Krotkiewski M, Björntorp P, Sjöström L, Smith U. Impact of obesity on metabolism in men and women: Importance of regional adipose tissue distribution. J Clin Invest. 1983;72:1150–1162.

6. Lemieux S, Després JP, Moorjani S, Nadeau A, Theriault G, Prud'homme D, Tremblay A, Bouchard C, Lupien PJ. Are gender differences in cardiovascular disease risk factors explained by the level if visceral adipose tissue. Diabetologia. 1994;37:757–764.[Medline] [Order article via Infotrieve]

7. Lemieux S, Després JP. Metabolic complications of visceral obesity: Contribution to the etiology of type II diabetes and implications for prevention and treatment. Diabete Metab. 1994;20:375–393.[Medline] [Order article via Infotrieve]

8. Zilversmit DB. Atherogenesis. A postprandial phenomenon. Circulation. 1979;60:473–485.[Abstract/Free Full Text]

9. Krasinski SD, Cohn JS, Schaefer EJ, Russell RM. Postprandial plasma retinyl ester response is greater in older subjects compared with younger subjects. Evidence for a delayed plasma clearance of intestinal lipoproteins. J Clin Invest. 1990;85:883–892.

10. Cohn JS, McNamara JR, Cohn SD, Ordovas JM, Schaefer EJ. Postprandial plasma lipoprotein changes in human subjects of different ages. J Lipid Res. 1988;29:469–479.[Abstract]

11. Bergeron N, Havel RJ. Assessment of postprandial lipemia: Nutritional influences. Curr Opin Lipidol. 1997;8:43–52.[Medline] [Order article via Infotrieve]

12. Weintraub MS, Rosen Y, Otto R, Eisenberg S, Breslow JL. Physical exercise conditioning in the absence of weight loss reduces fasting and postprandial triglyceride-rich lipoprotein levels. Circulation. 1989;79:1007–1014.[Abstract/Free Full Text]

13. Aldred HE, Hardman AE, Taylor S. Influence of 12 weeks of training by brisk walking on postprandial lipemia and insulinemia in sedentary middle-aged women. Metabolism. 1995;44:390–397.[Medline] [Order article via Infotrieve]

14. Ziogas GG, Thomas TR, Harris WS. Exercise training, postprandial hypertriglyceridemia and LDL subfraction distribution. Med Sci Sports Exerc. 1997;29:986–991.[Medline] [Order article via Infotrieve]

15. Ida-Chen YD, Swami S, Skowronski R, Coulston AM, Reaven GM. Differences in postprandial lipemia between patients with normal glucose tolerance and non-insulin dependent diabetes mellitus. J Clin Endocrinol Metab. 1993;76:172–177.[Abstract]

16. Lewis GF, O'Meara NM, Soltys PA, Blackman JD, Iverius PH, Pugh WL, Getz GS, Polonsky KS. Fasting hypertriglyceridemia in non-insulin-dependent diabetes mellitus is an important predictor of postprandial lipid and lipoprotein abnormalities. J Clin Endocrinol Metab. 1991;72:934–944.[Abstract/Free Full Text]

17. Lewis GF, O'Meara NM, Soltys PA, Blackman JD, Iverius PH, Druetzler AF, Getz GS, Polonsky KS. Postprandial lipoprotein metabolism in normal and obese subjects: Comparison after the vitamin A fat-loading test. J Clin Endocrinol Metab. 1990;71:1041–1050.[Abstract/Free Full Text]

18. Couillard C, Bergeron N, Prud'homme D, Bergeron J, Tremblay A, Bouchard C, Mauriège P, Despres JP. Postprandial triglyceride response in visceral obesity in men. Diabetes. 1998;47:953–960.[Abstract]

19. Wideman L, Kaminsky LA, Whaley MH. Postprandial lipemia in obese men with abdominal fat patterning. J Sports Med Phys Fitness. 1996;36:204–210.[Medline] [Order article via Infotrieve]

20. Ryu JE, Craven TE, MacArthur RD, Hinson WH, Bond MG, Hagaman AP, Crouse JR. Relationship of intraabdominal fat as measured by magnetic resonance imaging to postprandial lipemia in middle-aged subjects. Am J Clin Nutr. 1994;60:586–591.[Abstract/Free Full Text]

21. Mekki N, Christofilis MA, Charbonnier M, Atlan-Gepner C, Defoort C, Juhel C, Borel P, Portugal H, Pauli AM, Vialettes B, Lairon D. Influence of obesity and body fat distribution on postprandial lipemia and triglyceride-rich lipoproteins in adult women. J Clin Endocrinol Metab. 1999;84:184–191.[Abstract/Free Full Text]

22. Georgopoulos A, Rosengard AM. Abnormalities in the metabolism of postprandial and fasting triglyceride-rich lipoprotein subfractions in normal and insulin-dependent diabetic subjects: Effects of gender. Metabolism. 1989;38:781–789.[Medline] [Order article via Infotrieve]

23. The Airlie (VA) Consensus Conference. In: Lohman T, Roche A, Martorel R, eds. Standardization of Anthropometric Measurements. Champaign, IL: Human Kinetics Publ; 1988:39–80.

24. Benhke AR, Wilmore JH. Evaluation and regulation of body build and composition Englewood Cliffs; Prentice-Hall; 1974:20–37.

25. Siri WE. The gross composition of the body. Adv Biol Med Phys. 1956;4:239–280.[Medline] [Order article via Infotrieve]

26. Després JP, Prud'homme D, Pouliot MC, Tremblay A, Bouchard C. Estimation of deep abdominal adipose-tissue accumulation from simple anthropometric measurements in men. Am J Clin Nutr. 1991;54:471–477.[Abstract/Free Full Text]

27. Ferland M, Després JP, Tremblay A, Pinault S, Nadeau A, Moorjani S, Lupien PJ, Theriault G, Bouchard C. Assessment of adipose tissue distribution by computed tomography in obese women: Association with body density and anthropometric measurements. Br J Nutr. 1989;61:139–148.[Medline] [Order article via Infotrieve]

28. Kvist H, Tylen U, Sjöström L. Adipose tissue volume determinations in women by computed tomography: Technical considerations. Int J Obesity. 1986;10:53–67.[Medline] [Order article via Infotrieve]

29. Moorjani S, Dupont A, Labrie F, Lupien PJ, Brun D, Gagné C, Giguère M, Bélanger A. Increase in plasma high-density lipoprotein concentration following complete androgen blockade in men with prostatic carcinoma. Metabolism. 1987;36:244–250.[Medline] [Order article via Infotrieve]

30. Ruotolo G, Zhang H, Bentsianov B, Le NA. Protocol for the study of the metabolism of retinyl esters in plasma lipoproteins during postprandial lipemia. J Lipid Res. 1992;33:1541–1549.[Abstract]

31. Burstein M, Samaille J. Sur un dosage rapide du cholestérol lié aux ß-lipoprotéines du sérum. Clin Chim Acta. 1960;5:609–610.[Medline] [Order article via Infotrieve]

32. Noma A, Okabe H, Kita M. A new colorimetric microdetermination of free fatty acids in serum. Clin Chim Acta. 1973;43:317–320.[Medline] [Order article via Infotrieve]

33. Avogaro P, Bittolo Bon G, Cazzolato G, Quinci GB. Are apolipoprotein better discriminators than lipids for atherosclerosis? Lancet 1979;1:901–903.

34. Raabo E, Terkildsen TC. On the enzymatic determination of blood glucose. Scand J Clin Lab Invest. 1960;12:402–407.[Medline] [Order article via Infotrieve]

35. Morgan CR, Lazarow A. Immunoassay of insulin: Two antibody system. Plasma insulin levels in normal, subdiabetic rats. Diabetes. 1963;12:115–126.

36. Couillard C, Lemieux S, Moorjani S, Lupien PJ, Thériault G, Prud'homme D, Tremblay A, Bouchard C, Després JP. Associations between 12-year changes in body fatness and lipoprotein-lipid levels in men and women of the Québec Family Study. Int J Obesity. 1996;20:1081–1088.

37. Reaven GM. Role of insulin resistance in human disease. Diabetes. 1988;37:1595–1607.[Abstract]

38. Lemieux S, Prud'homme D, Bouchard C, Tremblay A, Després JP. Sex differences in the relation of visceral adipose tissue to total body fatness. Am J Clin Nutr. 1993;58:463–467.[Abstract/Free Full Text]

39. Brunzell JD, Hazzard WR, Porte D, Bierman EL. Evidence for a common, saturable, triglyceride removal mechanism for chylomicrons and very-low density lipoprotein in man. J Clin Invest. 1973;52:1578–1585.

40. Rebuffé-Scrive M, Lönnorth P, Marin P, Wesslau C, Björntorp P, Smith U. Regional adipose tissue metabolism in men and postmenopausal women. Int J Obes. 1987;11:347–355.[Medline] [Order article via Infotrieve]

41. Jensen MD. Gender differences in regional fatty acid metabolism before and after meal ingestion. J Clin Invest. 1995;96:2297–2303.

42. Sniderman AD, Cianflone K, Arner P, Summers LKM, Frayn KN. The adipocyte, fatty acid trapping and atherogenesis. Aretrioscler Thromb Vasc Biol. 1998;18:147–151.

43. Björkegren J, Packard CJ, Hamsten A, Bedford D, Caslake M, Foster L, Shepherd J, Stewart P, Karpe F. Accumulation of large very low density lipoprotein in plasma during intravenous infusion of a chylomicron-like triglyceride emulsion reflects competition for a common lipolytic pathway. J Lipid Res. 1996;37:76–86.[Abstract]

44. Lewis GF. Fatty acid regulation of very-low-density lipoprotein production. Curr Opin Lipidol. 1997;8:146–153.[Medline] [Order article via Infotrieve]

45. Kissebah AH, Krakower GR. Regional adiposity and morbidity. Physiol Rev. 1994;74:761–811.[Free Full Text]

46. Maslowska MH, Sniderman AD, MacLean LD, Cianflone K. Regional differences in triacylglycerol synthesis in adipose tissue and in cultured preadipocytes. J Lipid Res. 1993;34:219–228.[Abstract]

47. Westerveld HT, Meyer E, de Bruin TWA, Erkelens DW. Oestrogens and postprandial lipid metabolism. Biochem Soc Trans. 1997;25:45–49.[Medline] [Order article via Infotrieve]

48. St-Amand J, Després JP, Lemieux S, Lamarche B, Moorjani S, Prud'homme D, Bouchard C, Lupien PJ. Does lipoprotein or hepatic lipase activity explain the protective lipoprotein profile of premenopausal women? Metabolism.. 1995;44:491–498.[Medline] [Order article via Infotrieve]




This article has been cited by other articles:


Home page
Annals of Clinical & Laboratory ScienceHome page
G. Kolovou, D. Damaskos, K. Anagnostopoulou, and D. V. Cokkinos
Apolipoprotein E Gene Polymorphism and Gender
Ann. Clin. Lab. Sci., January 1, 2009; 39(2): 120 - 133.
[Abstract] [Full Text] [PDF]


Home page
ANGIOLOGYHome page
G. D. Kolovou and H. G. Bilianou
Influence of Aging and Menopause on Lipids and Lipoproteins in Women
Angiology, August 1, 2008; 59(2_suppl): 54S - 57S.
[Abstract] [PDF]


Home page
Arterioscler. Thromb. Vasc. Bio.Home page
J.-P. Despres, I. Lemieux, J. Bergeron, P. Pibarot, P. Mathieu, E. Larose, J. Rodes-Cabau, O. F. Bertrand, and P. Poirier
Abdominal Obesity and the Metabolic Syndrome: Contribution to Global Cardiometabolic Risk
Arterioscler. Thromb. Vasc. Biol., June 1, 2008; 28(6): 1039 - 1049.
[Abstract] [Full Text] [PDF]


Home page
J. Nutr.Home page
N. D. Knuth and J. F. Horowitz
The Elevation of Ingested Lipids within Plasma Chylomicrons Is Prolonged in Men Compared with Women
J. Nutr., June 1, 2006; 136(6): 1498 - 1503.
[Abstract] [Full Text] [PDF]


Home page
J. Nutr.Home page
B. Mittendorfer
Sexual Dimorphism in Human Lipid Metabolism
J. Nutr., April 1, 2005; 135(4): 681 - 686.
[Abstract] [Full Text] [PDF]


Home page
J. Lipid Res.Home page
R. Elosua, J. M. Ordovas, L. A. Cupples, C. S. Fox, J. F. Polak, P. A. Wolf, R. A. D'Agostino Sr., and C. J. O'Donnell
Association of APOE genotype with carotid atherosclerosis in men and women: the Framingham Heart Study
J. Lipid Res., October 1, 2004; 45(10): 1868 - 1875.
[Abstract] [Full Text] [PDF]


Home page
J. Lipid Res.Home page
K. Cianflone, R. Zakarian, C. Couillard, B. Delplanque, J.-P. Despres, and A. Sniderman
Fasting acylation-stimulating protein is predictive of postprandial triglyceride clearance
J. Lipid Res., January 1, 2004; 45(1): 124 - 131.
[Abstract] [Full Text] [PDF]


Home page
Arterioscler. Thromb. Vasc. Bio.Home page
C.J.M. Halkes, H. van Dijk, C. Verseyden, P.P.Th. de Jaegere, H.W.M Plokker, S. Meijssen, D.W. Erkelens, and M. C. Cabezas
Gender Differences in Postprandial Ketone Bodies in Normolipidemic Subjects and in Untreated Patients With Familial Combined Hyperlipidemia
Arterioscler. Thromb. Vasc. Biol., October 1, 2003; 23(10): 1875 - 1880.
[Abstract] [Full Text] [PDF]


Home page
StrokeHome page
T. C. Wascher, B. Paulweber, L. Malaimare, A. Stadlmayr, B. Iglseder, I. Schmoelzer, and W. Renner
Associations of a Human G Protein {beta}3 Subunit Dimorphism With Insulin Resistance and Carotid Atherosclerosis
Stroke, March 1, 2003; 34(3): 605 - 609.
[Abstract] [Full Text] [PDF]


Home page
DiabetesHome page
P. Shah, A. Vella, A. Basu, R. Basu, A. Adkins, W. F. Schwenk, C. M. Johnson, K. S. Nair, M. D. Jensen, and R. A. Rizza
Elevated Free Fatty Acids Impair Glucose Metabolism in Women: Decreased Stimulation of Muscle Glucose Uptake and Suppression of Splanchnic Glucose Production During Combined Hyperinsulinemia and Hyperglycemia
Diabetes, January 1, 2003; 52(1): 38 - 42.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Endocrinol. Metab.Home page
T. J. Horton, S. R. Commerford, M. J. Pagliassotti, and D. H. Bessesen
Postprandial leg uptake of triglyceride is greater in women than in men
Am J Physiol Endocrinol Metab, December 1, 2002; 283(6): E1192 - E1202.
[Abstract] [Full Text] [PDF]


Home page
J. Nutr.Home page
R. D. Mattes
Oral Fat Exposure Increases the First Phase Triacylglycerol Concentration Due to Release of Stored Lipid in Humans
J. Nutr., December 1, 2002; 132(12): 3656 - 3662.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Clin. Nutr.Home page
C. Couillard, N. Bergeron, A. Pascot, N. Almeras, J. Bergeron, A. Tremblay, D. Prud'homme, and J.-P. Despres
Evidence for impaired lipolysis in abdominally obese men: postprandial study of apolipoprotein B-48- and B-100-containing lipoproteins
Am. J. Clinical Nutrition, August 1, 2002; 76(2): 311 - 318.
[Abstract] [Full Text] [PDF]


Home page
Cardiovasc ResHome page
J. E Roeters van Lennep, H.T. Westerveld, D.W. Erkelens, and E. E van der Wall
Risk factors for coronary heart disease: implications of gender
Cardiovasc Res, February 15, 2002; 53(3): 538 - 549.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
G. Perseghin, P. Scifo, E. Pagliato, A. Battezzati, S. Benedini, L. Soldini, G. Testolin, A. Del Maschio, and L. Luzi
Gender Factors Affect Fatty Acids-Induced Insulin Resistance in Nonobese Humans: Effects of Oral Steroidal Contraception
J. Clin. Endocrinol. Metab., July 1, 2001; 86(7): 3188 - 3196.
[Abstract] [Full Text] [PDF]


Home page
Scand J Public HealthHome page
M. Barnekow-Bergkvist, G. Hedberg, U. Janlert, and E. Jansson
Adolescent determinants of cardiovascular risk factors in adult men and women
Scand J Public Health, July 1, 2001; 29(3): 208 - 217.
[Abstract] [PDF]


Home page
DiabetesHome page
J. P. Frias, G. B. Macaraeg, J. Ofrecio, J. G. Yu, J. M. Olefsky, and Y. T. Kruszynska
Decreased Susceptibility to Fatty Acid-Induced Peripheral Tissue Insulin Resistance in Women
Diabetes, June 1, 2001; 50(6): 1344 - 1350.
[Abstract] [Full Text]


Home page
Arterioscler. Thromb. Vasc. Bio.Home page
J. M. Bard, M. A. Charles, I. Juhan-Vague, P. Vague, P. Andre, M. Safar, J. C. Fruchart, E. Eschwege, and o. b. o. t. BIGPRO Study Group
Accumulation of Triglyceride-Rich Lipoprotein in Subjects With Abdominal Obesity : The Biguanides and the Prevention of the Risk of Obesity (BIGPRO) 1 Study
Arterioscler. Thromb. Vasc. Biol., March 1, 2001; 21(3): 407 - 414.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
C. Couillard, N. Bergeron, J. Bergeron, A. Pascot, P. Mauriège, A. Tremblay, D. Prud’homme, C. Bouchard, and J.-P. Després
Metabolic Heterogeneity Underlying Postprandial Lipemia among Men with Low Fasting High Density Lipoprotein Cholesterol Concentrations
J. Clin. Endocrinol. Metab., December 1, 2000; 85(12): 4575 - 4582.
[Abstract] [Full Text]


This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowRequest Permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Couillard, C.
Right arrow Articles by Després, J.-P.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Couillard, C.
Right arrow Articles by Després, J.-P.
Related Collections
Right arrow Nutrition
Right arrow Risk Factors
Right arrow Lipid and lipoprotein metabolism