Elevated plasma triglyceride (TG) concentrations are associated with increased risk of CHD, particularly in women (16). Therefore, interventions that decrease or prevent an increase in plasma TG concentrations, such as exercise and diet, may help reduce CHD risk (1). It has long been known that exercise reduces total plasma TG concentration (17), almost exclusively because of the reduced concentration of TG in VLDL (3). This effect is not the result of repeated exercise sessions (i.e., training) (14) but instead is acute and short lived because plasma TG concentrations are decreased 12–18 h after a single bout of exercise and remain lower than preexercise values for 2–3 d (8,39). Exercise-induced hypotriglyceridemia manifests above a certain threshold of exercise energy expenditure (7), independent of duration and intensity (41) and plateaus with progressively more exercise (9). In a series of studies in healthy nonobese men, we have shown that a single bout of aerobic exercise reduces fasting plasma TG concentrations the next day by increasing the clearance rate of VLDL-TG from the circulation, without affecting VLDL-TG secretion rate from the liver (23,25,26,40). The exercise-induced increase in VLDL-TG plasma clearance rate also requires a certain energy expenditure threshold and plateaus thereafter (20). However, the mechanism by which a single bout of exercise reduces fasting plasma TG concentrations in women (12) remains elusive (24). Previous studies have revealed major sex differences in basal VLDL-TG kinetics (22,31). For example, women have a much greater basal VLDL-TG secretion rate than men. It is thus possible that exercise-induced hypotriglyceridemia in women manifests via a different mechanism (e.g., reduced hepatic VLDL-TG secretion) than that in men.
Recent data indicate that negative energy balance is a critical factor for exercise-induced TG lowering. Acutely increasing dietary energy intake to compensate for the energy expended during exercise abolishes the reduction in fasting total plasma TG concentration (6), whereas a single day of calorie restriction to induce a similar energy deficit as that caused by exercise decreases fasting plasma VLDL-TG concentration to the same extent (28). Still, although changes in energy balance seem to account for most of the exercise-induced TG-lowering, there are data suggesting that exercise is somewhat superior to calorie restriction in inducing hypotriglyceridemia (11,29,43). These observations suggest that the hypotriglyceridemic effect of exercise may be mediated by a mechanism other than, or in addition to, the negative energy balance and that dietary energy deficit may have an independent effect on the mechanisms regulating VLDL-TG homeostasis. Chronic dietary energy restriction leading to weight loss is accompanied by a reduction in hepatic VLDL-TG secretion rate (13,32). However, the effects of acute dietary-induced negative energy balance on VLDL-TG kinetics are not known.
The overall aim of the present study was to assess the acute effects of exercise and calorie restriction, each tailored to induce the same negative energy balance, on VLDL-TG metabolism in women. The specific study purposes were 1) to assess the mechanisms leading to exercise-induced hypotriglyceridemia in women and 2) to assess the independent hypotriglyceridemic effect of negative energy balance.
Eleven healthy, lean, sedentary women (age = 23.5 ± 2.7 yr; body mass index = 21.6 ± 1.4 kg·m−2; peak oxygen consumption [V˙O2peak] = 1.6 ± 0.4 L·min−1; mean ± SD) volunteered for the study. The selection of healthy lean volunteers was made to avoid influence of medication and obesity-related comorbidities. Exclusion criteria included contraindication to aerobic exercise, irregular menses, amenorrhea, polycystic ovary syndrome, pregnancy, acute or chronic illness, use of medications (including oral contraceptives) or dietary supplements, smoking, regular alcohol consumption (>1 drink per day), regular exercise participation (>1 time per week), and being on a special diet or having experienced weight fluctuations ≥2 kg at any time during the last 6 months. The Ethics Committee of Harokopio University approved the study protocol, and all subjects gave written informed consent.
All preliminary tests were carried out during screening, approximately 1–2 wk before the beginning of the experiment. Weight and height were measured, and an overnight fasting blood sample was drawn for hematological and biochemical evaluations. Subjects were healthy on the basis of medical examination and routine laboratory tests; all were normoglycemic and normolipidemic. Total body fat mass and fat-free mass were determined with dual energy x-ray absorptiometry (model DPX-MD; Lunar, Madison, WI). Resting energy expenditure (REE) was measured by indirect calorimetry (Vmax229D; Sensormedics, Yorba Linda, CA) in the morning, after subjects remained rested for at least 30 min (27). V˙O2peak was assessed with a submaximal incremental brisk walking exercise test based on the Balke treadmill protocol (2). Briefly, after a 5-min warm-up, subjects walked on a treadmill (Technogym Runrace, Gambettola, Italy) at constant speed, and grade was increased by 2% every 3 min. Expiratory gases were collected (Vmax229D; Sensormedics), and heart rate was monitored continuously. The test was terminated at 80% of maximal heart rate, and V˙O2peak was predicted from the oxygen consumption–heart rate relationship (2).
We used a paired crossover design, in which all subjects performed three trials, that is, control, exercise-induced energy deficit, and dietary-induced energy deficit, in random order and at least 1 wk apart, without considering the phase of the menstrual cycle, because we have previously shown that basal VLDL-TG kinetics are not affected by menstrual cycle phase (21). A stable isotopically labeled tracer infusion was performed on the day after each trial, after an overnight fast. Subjects were instructed to refrain from exercise for 2 d and avoid alcohol and caffeine consumption for 1 d before each trial. In addition, they were asked to record their diet during the day preceding the first trial and to replicate this diet on the day preceding the subsequent trials (i.e., purchase the same type and brand of food, use the same cooking methods and portions, etc.) to avoid prestudy differences in nutrient intake.
Control (isocaloric diet and rest).
Subjects were asked to abstain from exercise and carry out only the activities of daily living. During the afternoon of the day preceding the isotope infusion study, they remained rested at home. Subjects were instructed to follow a prescribed isocaloric diet (50% of energy from carbohydrate, 20% from protein and 30% from fat), which provided their estimated daily energy needs for weight maintenance, calculated by multiplying the measured REE with an activity factor of 1.4 representative of their very light to light physical activity habits (19). Subjects were thus assumed to be on zero energy balance during the control trial.
Subjects were asked to abstain from exercise and carry out only the activities of daily living, with the exception of an exercise session performed at the laboratory in the afternoon. Each subject attended the laboratory midway between lunch and dinner and walked briskly on the treadmill (Technogym Runrace) at 60% of her V˙O2peak. Gas sampling was performed for 10 min every 20 min during exercise to estimate total exercise energy expenditure. The exercise bout was stopped when subjects reached an estimated exercise-induced net energy deficit of approximately 2 MJ, calculated by subtracting REE from the total energy expenditure of exercise. The duration of the bout was 123 ± 18 min (mean ± SD). Subjects were also instructed to follow a prescribed isocaloric diet, which provided their estimated daily energy needs for weight maintenance without accounting for the exercise-induced energy deficit, that is, the same diet as in the control trial.
Diet (hypocaloric diet and rest).
Subjects were asked to abstain from exercise and carry out only the activities of daily living. They were instructed to follow a prescribed hypocaloric diet (50% of energy from carbohydrate, 20% from protein and 30% from fat), which provided their estimated daily energy needs for weight maintenance minus 2 MJ (∼500 kcal). The restriction of energy intake occurred at lunch, afternoon snack, and dinner so that the energy deficit occurred at similar times of the day in the diet and exercise trials (11,28).
For each trial (on the day before the infusion study), subjects recorded their dietary intake with a food diary (type of food, brand, portion, etc.), and a 24-h food recall was obtained on the following day (during the infusion study). Subjects were allowed to make their own selections of brands on the basis of a prescribed diet for the first trial and were then instructed to consume the same type of foods (i.e., purchase the same brand, use the same cooking methods, etc.) with prescribed portions for the remaining trials. Food records were analyzed by using Diet Analysis Plus 8 (Cengage Learning, Florence, KY).
Tracer Infusion Study
The morning following each of the three experimental trials (control, exercise, and diet), subjects arrived at the laboratory at approximately 0800 h, after an overnight fast. A catheter was inserted in a forearm vein to administer stable isotopically labeled tracers, and a second catheter was inserted in a contralateral hand vein for blood sampling, which was kept warm with a heating pad until the end of the metabolic study. Subjects were given 1 h to relax and familiarize with the catheters; during this time, a 24-h diet recall was taken. At 0900 h, a baseline blood sample was obtained and immediately after a bolus of [1,1,2,3,3-2H5]glycerol (75 μmol·kg−1 body weight; Goss Scientific Instruments, Essex, UK), dissolved in normal saline, was administered through the catheter in the forearm vein. Blood samples were taken every 15 min during the first hour after tracer administration and hourly thereafter for another 7 h. Catheters were flushed with saline every 30 min to maintain patency. Subjects remained fasted (except for water) in a sitting position until the end of the metabolic study.
Sample Collection, Processing, and Analysis
Blood samples were collected in precooled potassium-EDTA Monovettes (Sarstedt, Leicester, UK) and immediately placed on ice. Plasma was separated by centrifugation within 30 min of collection. A 3-mL aliquot of plasma was transferred into plastic culture tubes and kept in the refrigerator for immediate isolation of VLDL, and the remaining plasma samples were stored at −80°C until analyses. The VLDL fraction was prepared by density-gradient ultracentrifugation, the VLDL-TG were isolated by thin-layer chromatography, hydrolyzed, and the VLDL-TG-bound glycerol was derived with heptafluorobutyric anhydride, as previously described (25,40). The tracer-to-tracee ratio of glycerol in VLDL-TG was measured by gas chromatography-mass spectrometry (MSD 5973 system; Hewlett-Packard, Palo Alto, CA) by selectively monitoring the ions at mass-to-charge ratios 467 and 472 (25,40).
The determination of plasma glucose, total plasma TG, and VLDL-TG concentrations was performed by enzymatic colorimetric methods using commercially available kits (Alfa Wassermann Diagnostics, Woerden, the Netherlands) on an automated analyzer (ACE Schiapparelli Biosystems, Fairfield, NJ). Plasma free fatty acid (FFA) concentrations were measured by using a commercially available diagnostic kit (Waco Diagnostics, Richmond, VA). VLDL, intermediate-density lipoprotein, LDL, and HDL particle concentrations and HDL-cholesterol concentration were determined by using proton nuclear magnetic resonance spectroscopy (LipoScience, Raleigh, NC) (34). A separate blood sample was collected into nonheparinized serum tubes (Sarstedt), allowed to clot, spun in a centrifuge, and then aliquoted and frozen immediately at −80°C, until measurement of insulin with a commercially available immunoenzymetric fluorescent method (ST AIA-PACK IRI; Tosoh Medics, Inc., San Francisco, CA) on an automated analyzer (Tosoh AIA 600II, Tosoh Medics, Inc.). All samples from each subject’s trials were analyzed in the same batch.
The gross energy expenditure of exercise was calculated by using the Weir (42) equation and nonprotein respiratory quotient (36). Net energy expenditure was calculated by subtracting REE for an equivalent period of rest. The fractional turnover rate (FTR; pools per hour) of VLDL-TG was determined by monoexponential analysis of VLDL-TG-glycerol tracer-to-tracee ratio data (18,35). The hepatic secretion rate of VLDL-TG (μmol·min−1) was calculated as FTR × C × PV / 60, where C is the concentration of VLDL-TG in plasma and PV is the plasma volume (55 mL·kg−1 of fat-free mass (4)). It was assumed that the VLDL-TG volume of distribution equals PV because VLDL particles are restricted to the plasma compartment (38). The plasma clearance rate of VLDL-TG (mL·min−1), which is an index of the efficiency of VLDL-TG removal from the circulation via all possible routes, was calculated by dividing the rate of VLDL-TG disappearance (which equals the secretion rate at steady state) by the plasma concentration of VLDL-TG.
All data sets were tested for normality by using the Kolmogorov–Smirnov criterion. Normally distributed variables are presented as mean ± SD, whereas nonnormally distributed variables were log-transformed for analyses and back-transformed and presented as mean values with 95% confidence intervals. Generalized estimating equations were fitted to evaluate differences among the three experimental trials (encoded as dummy variables). For all the dependent variables, the normal distribution was used for fitting generalized estimating equations, with the identity as the link function. The unstructured formation of the correlation matrix was used after comparing various scenarios using the corresponding quasi-likelihood under the independence criterion for model’s goodness of fit. Post hoc analysis for comparing mean values among trials was applied by using the Bonferroni correction rule to adjust for the inflation of type I error due to multiple comparisons. All statistical analyses were carried out using the Statistical Package for the Social Sciences for Windows (Version 19; IBM SPSS, Chicago, IL).
Dietary Energy Intake and Exercise Energy Expenditure
The gross energy expenditure of exercise was 2.53 ± 0.08 MJ. Compared with the control condition (rest and isocaloric feeding; zero energy balance), subjects were in a negative energy balance of approximately 2 MJ during the exercise and hypocaloric diet trials (Table 1).
Fasting plasma glucose concentration was not different among trials, but fasting serum insulin concentration was significantly lower after dietary energy restriction than after the control trial (P = 0.005) (Table 2). Plasma FFA concentration was not different after exercise or diet compared with the control condition but was significantly greater after exercise compared with hypocaloric diet (P = 0.006). Total plasma TG (P = 0.007), VLDL-TG (P < 0.001), and total and all VLDL subclass particle concentrations (P < 0.015) were significantly lower after exercise compared with control (Tables 2 and 3). Dietary energy restriction did not significantly affect total plasma TG (P = 1.000) and VLDL-TG (P = 0.297) concentrations but significantly reduced large (P = 0.019) and small (P = 0.013) VLDL particle concentrations relative to the control condition (Tables 2 and 3). Exercise did not affect total LDL particle concentration, but HDL-cholesterol concentration (P = 0.028) (Table 2) and total HDL particle concentration (P = 0.017) (Table 3) were greater after the exercise trial than after hypocaloric diet trial.
The FTR of VLDL-TG was 0.60 (0.54, 0.67) pools per hour after the control trial (zero energy balance), and was significantly increased after the exercise-induced energy deficit (0.73 (0.62, 0.86) pools per hour, P = 0.001 vs control) but did not change after the diet-induced energy deficit (0.66 (0.60, 0.71) pools per hour, P = 0.213 vs control). Compared with the control trial, hepatic VLDL-TG secretion rate was reduced by approximately 17% (P = 0.042) (Fig. 1) and plasma clearance rate of VLDL-TG was increased by approximately 22% after exercise (P = 0.001) (Fig. 2). Hypocaloric diet had no effect on the hepatic secretion rate (P = 1.000) or the plasma clearance rate (P = 0.227) of VLDL-TG.
We evaluated the effects of aerobic exercise and dietary energy restriction of equivalent energy deficit (∼2 MJ or 500 kcal) on basal VLDL-TG kinetics in healthy, lean, sedentary women. Compared with a control day of isocaloric feeding and rest, we found that exercise decreased fasting plasma VLDL-TG concentration by approximately 30%, owing to a 17% reduction in hepatic VLDL-TG secretion rate and a 22% increase in the plasma clearance rate of VLDL-TG, whereas diet had no effect on VLDL-TG concentration and kinetics. The findings from our study indicate that (i) exercise-induced hypotriglyceridemia in women manifests through a different mechanism (increased clearance and decreased secretion of VLDL-TG) than that described previously in men (increased clearance of VLDL-TG only) (26,40), and (ii) exercise affects TG homeostasis by eliciting changes in VLDL-TG kinetics that are independent of negative energy balance and specific to muscular contraction.
Studies measuring total plasma TG concentrations after single bouts of aerobic exercise indicate that exercise-induced hypotriglyceridemia in the basal state requires a certain amount of energy to be expended during exercise (7). The duration and intensity of exercise are interchangeable (increasing duration while decreasing intensity and vice versa) when it comes to eliciting hypotriglyceridemia, provided that the total energy expenditure is held constant (41). In previous studies, we have shown that 60 min of exercise at 60% of V˙O2peak does not lead to hypotriglyceridemia in either men (23) or women (24). Results from several studies in healthy normolipidemic men indicate that the threshold of exercise required for hypotriglyceridemia to manifest lies near or around 500–600 kcal (20,33). However, a single bout of prolonged moderate-intensity endurance exercise (90–120 min at 60% of V˙O2peak with an energy expenditure of 800–1200 kcal) reduced VLDL-TG concentrations by 25%–30% in young healthy men (26,40), consistent with the results from this study. Therefore, men and women are equally sensitive to a single bout of endurance exercise (12), although the absolute energy expended during exercise is much lower for women than for men owing to their lower body weight and V˙O2peak.
We have shown previously that basal hypotriglyceridemia after a single bout of prolonged moderate-intensity endurance exercise (90–120 min at 60% of V˙O2peak) results from increased plasma clearance rate of VLDL-TG in healthy nonobese men (26,40). The present results demonstrate that, in women, exercise-induced hypotriglyceridemia manifests via both an increase in VLDL-TG plasma clearance rate and a decrease in the hepatic VLDL-TG secretion rate. This sexually dimorphic response of VLDL-TG metabolism in response to acute exercise is consistent with previous studies showing considerable sex differences in basal VLDL metabolism. Women have significantly greater VLDL-TG plasma clearance rates but also greater hepatic VLDL-TG secretion rates than men (22,31). Given that the mechanisms of TG removal from the circulation are saturable (5) and that the stimulatory effect of exercise on VLDL-TG clearance appears to level off (20), it is possible that exercise has lesser of an effect on VLDL-TG plasma clearance rate in women (∼20%, present study) than that in men (∼40% (26,40)) because women already exhibit very high rates of VLDL-TG removal from the circulation (22,31). This hypothesis is consistent with data from studies showing that women exhibit considerably smaller exercise-induced increases in skeletal muscle LPL activity compared with men (37). Therefore, exercise in women lowers fasting plasma TG concentrations only partly by increasing VLDL-TG clearance. Our results demonstrate that approximately half of this effect is attributed to a reduction in VLDL-TG secretion from the liver, which is also considerably greater in women than that in men at rest (22,31). Unfortunately, the nature of our study cannot further describe the mechanisms responsible for this observation.
We found that a part of the exercise-induced decrease in VLDL-TG concentration in women was due to reduced secretion of VLDL-TG from the liver. Although this contributes to a beneficial effect (i.e., reduction in plasma TG concentrations), it can be argued that it might also have negative consequences because VLDL-TG secretion buffers the excess amount of plasma FFA, which generally increases after exercise and would otherwise be cytotoxic (10). However, we did not observe an increase in plasma FFA concentration after exercise in women. Also, other studies have shown that women exhibit lower exercise-induced increases in plasma FFA than men, and values after exercise return to baseline more readily in women than that in men (15,23,24). This suggests that the increase in hepatic fatty acid availability after exercise might be lower in women, or that hepatic fatty acids are used more toward oxidation or tissue replenishment in women than in men. A previous study has shown that in response to another lipolytic stimuli (prolonged fasting), women have a greater ability to partition systemic fatty acids toward ketone body production rather than VLDL-TG synthesis compared with young men, resulting in a more advantageous metabolic profile (30). It can be hypothesized that a similar difference might exist after exercise. Furthermore, the exercise-induced decrease in hepatic glycogen availability might have been higher for our subjects compared with other studies conducted in men (26,40), thus resulting in a further increase in the use of hepatic fatty acids for oxidation and a limited use for TG synthesis and secretion.
Our results show that the dietary energy restriction of a similar magnitude as the exercise-induced energy deficit does not reproduce the effects of exercise on VLDL-TG metabolism. However, we observed a great variability in the diet-induced changes (relative to the control trial) in VLDL-TG concentration among our subjects. VLDL-TG concentration decreased by 20%–50% in six subjects, did not change in three subjects (±6%), and increased in two subjects by 40%. We have previously shown that a similar intervention was successful in decreasing fasting and postprandial triglyceridemia (29), and another study has shown that a greater diet-induced energy deficit (∼900 kcal) for a longer period (5 d) reduced fasting plasma TG concentrations (43), although in both instances exercise appeared to cause a somewhat greater effect than diet (29,43). Another study, however, found that a lower diet-induced calorie restriction (∼1.4 MJ) had no effect on fasting plasma TG concentrations (11). It is thus possible that there is an energy deficit threshold for diet-induced TG lowering, at approximately 2 MJ (500 kcal). Thus, acute dietary interventions near this threshold may (29) or may not (present study) induce a hypotriglyceridemic effect. Nevertheless, our results indicate that exercise affects VLDL-TG concentration and kinetics, which is specific to muscular contraction and independent of exercise-induced negative energy balance.
Our study has several limitations. First, we only studied healthy young normotriglyceridemic women; hence, we cannot exclude the possibility that our results may be different in obese subjects or those with increased plasma TG concentrations. Second, we did not evaluate VLDL-apolipoprotein B-100 kinetics in this study, which is indicative of the metabolic behavior of the VLDL particle itself, as opposed to the metabolic behavior of core TG; this would have been helpful to better characterize the effects of diet and exercise on VLDL metabolism. Lastly, we did not perform a trial with less exercise; hence, we cannot speculate whether less exercise, such as that recommended to the general public, has a similarly beneficial effect on TG homeostasis and VLDL metabolism.
In summary, we found that a single bout of moderate-intensity aerobic exercise lowers fasting plasma VLDL-TG concentrations in women via a combination of reduced VLDL-TG secretion from the liver and increased VLDL-TG clearance from plasma. Calorie restriction tailored to induce the same energy deficit (∼2 MJ/500 kcal) had no effect on VLDL-TG concentration and kinetics. Therefore, exercise affects TG homeostasis in women by eliciting changes in VLDL-TG kinetics that are specific to muscular contraction and independent of the accompanying negative energy balance. Our study underpins the existence of sex differences in the regulation of postexercise TG metabolism and the possibility of developing sex-specific interventions to improve plasma TG homeostasis.
This work was supported by the Graduate Program, Department of Nutrition and Dietetics of Harokopio University, the Hellenic Heart Foundation, and the Greek Governmental Institute of Scholarships (E.B.). Support also came from the Institute for Translational Sciences at the University of Texas Medical Branch, supported in part by a Clinical and Translational Science Award (UL1TR000071) from the National Center for Advancing Translational Sciences, National Institutes of Health, the Shriners Hospital for Children (SSF 84090), and from the Sealy Center on Aging, University of Texas Medical Branch at Galveston. We are indebted to the subjects for their interest and participation in the study.
The authors have no conflicts of interest.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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