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Am J Physiol Endocrinol Metab 290: E355-E362, 2006. First published October 11, 2005; doi:10.1152/ajpendo.00259.2005
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Lipid metabolism response to a single, prolonged bout of endurance exercise in healthy young men

Faidon Magkos,1,2 David C. Wright,1 Bruce W. Patterson,1 B. Selma Mohammed,1 and Bettina Mittendorfer1

1Washington University School of Medicine, St. Louis, Missouri; and 2Department of Nutrition and Dietetics, Harokopio University, Athens, Greece

Submitted 9 June 2005 ; accepted in final form 29 September 2005


   ABSTRACT
TOP
 ABSTRACT
RESEARCH DESIGN AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
 REFERENCES
 
To discover the alterations in lipid metabolism linked to postexercise hypotriglyceridemia, we measured lipid kinetics, lipoprotein subclass distribution and lipid transfer enzymes in seven healthy, lean, young men the day after 2 h of cycling and rest. Compared with rest, exercise increased fatty acid rate of appearance and whole body fatty acid oxidation by ~65 and 40%, respectively (P < 0.05); exercise had no effect on VLDL-triglyceride (TG) secretion rate, increased VLDL-TG plasma clearance rate by 40 ± 8%, and reduced VLDL-TG mean residence time by ~40 min and VLDL-apolipoprotein B-100 (apoB-100) secretion rate by 24 ± 8% (all P < 0.05). Exercise also reduced the number of VLDL but almost doubled the number of IDL particles in plasma (P < 0.05). Muscle lipoprotein lipase content was not different after exercise and rest, but plasma lipoprotein lipase concentration increased by ~20% after exercise (P < 0.05). Plasma hepatic lipase and lecithin:cholesterol acyltransferase concentrations were not affected by exercise, whereas cholesterol ester transfer protein concentration was ~10% lower after exercise than after rest (P = 0.052). We conclude that 1) greater fatty acid availability after exercise does not stimulate VLDL-TG secretion, probably because of the increase in fatty acid oxidation and possibly also fatty acid use for restoration of tissue TG stores; 2) reduced secretion of VLDL-apoB-100 lowers plasma VLDL particle concentration; and 3) increased VLDL-TG plasma clearance maintains low plasma TG concentration but is not accompanied by similar increases in subsequent steps of the delipidation cascade. Acutely, therefore, the cardioprotective lowering of plasma TG and VLDL concentrations by exercise is counteracted by a proatherogenic increase in IDL concentration.

lipoprotein; fatty acid; stable isotope; metabolism

ALTERATIONS IN LIPOPROTEIN METABOLISM, manifested by increased plasma triglyceride (TG) and low-density lipoprotein (LDL) cholesterol and decreased high-density lipoprotein (HDL) cholesterol concentrations, are associated with a greater risk for the development of cardiovascular disease (CVD) (27), the leading cause of death in the US (31). Exercise has long been recognized as an effective means to improve insulin sensitivity (12, 36) and prevent CVD; in fact, one-third of CVD-related deaths are attributable to physical inactivity (35).

The cardioprotective effects of regular exercise are, to some extent at least, related to its effects on plasma lipoprotein profile: exercise lowers plasma TG concentration, raises plasma HDL cholesterol concentration, and possibly also reduces total and LDL cholesterol concentrations (53). The hypotriglyceridemic effect appears to be the most powerful and was first recognized four decades ago (26). The immediate effect of exercise on plasma TG concentration remains controversial: some investigators report a decrease during and immediately after exercise (39), whereas others show no change (3, 7, 9). However, there is compelling evidence for a "delayed-onset" hypotriglyceridemic effect ~12 h after a bout of exercise (3, 7, 9, 17, 20). Furthermore, the hypotriglyceridemic effect of exercise is transient and is unlikely to result in long-term adaptations with repeated bouts of exercise (i.e., training). Plasma TG concentrations are reduced after a single bout of exercise in untrained subjects for ~24–36 h (20, 26, 56, 61, 62); similarly, they are lower in trained than in untrained subjects when measurements are made within 24–36 h of the last bout of exercise (22, 23); after that, differences in plasma TG concentrations are no longer apparent (22, 23, 25). Also, the available literature suggests that the magnitude of the effect is the same in both conditions (13). HDL cholesterol concentrations change concomitantly with TG concentrations, but the magnitude of change is much smaller (~5–15% vs. ~20–50% for TG), and chronic exercise training may be required to elicit this effect (13, 57). Exercise training seldom alters total and LDL cholesterol (13). The initial phase of low plasma TG concentrations appears to coincide with the time window during which muscle lipoprotein lipase (LPL) activity is likely increased after exercise (30, 47, 48) and probably mediates the accelerated rate of postprandial TG removal at that time (2, 22). However, the exercise-induced reduction in total plasma TG concentration, during both fasted and fed conditions, is predominantly due to a decrease in VLDL-TG concentration (17, 20) and extends beyond the time frame of increased LPL activity, which would suggest that exercise also lowers the rate of VLDL-TG secretion. The changes in VLDL kinetics that accompany postexercise hypotriglyceridemia have not been investigated previously.

The purpose of our study was to assess the changes in lipid metabolism that coincide with the hypotriglyceridemic period following endurance exercise. We measured VLDL-TG, VLDL-apolipoprotein B-100 (apoB-100), and plasma fatty acid kinetics by using stable isotope-labeled tracers, plasma lipoprotein profile by nuclear magnetic resonance (NMR) spectroscopy, whole body fat oxidation by indirect calorimetry, muscle LPL content by Western blot analysis, and the plasma concentration of key enzymes involved in lipoprotein metabolism [i.e., LPL, hepatic lipase (HL), lecithin:cholesterol acyltransferase (LCAT), and cholesterol ester transfer protein (CETP)] with enzyme-linked immunosorbent assays (ELISA) in healthy young men in the morning after rest and after a single bout of exercise on the preceding evening.


   RESEARCH DESIGN AND METHODS
TOP
 ABSTRACT
 RESEARCH DESIGN AND METHODS
RESULTS
 DISCUSSION
 GRANTS
 REFERENCES
 
Subjects and preliminary testing. Seven healthy, recreationally active but untrained, men (age 28 ± 2 yr; body wt 71 ± 4 kg; BMI 22 ± 1 kg/m2; means ± SE) participated in this project. Written informed consent was obtained from all subjects before their participation in the study, which was approved by the Human Studies Committee and the General Clinical Research Center (GCRC) Advisory Committee at Washington University School of Medicine in St. Louis, MO. All participants were considered to be in good health after completing a medical evaluation, which included a history and physical examination and blood tests. They were instructed to adhere to their regular diet and to refrain from vigorous exercise for three days before the tracer infusion studies.

Approximately 1 wk before the beginning of the experiment, each subject's body composition was assessed by dual-energy X-ray absorptiometry (Delphi-W densitometer; Hologic, Waltham, MA), and peak oxygen consumption (VO2 peak) was determined. Subjects warmed up with cycling (Ergoline 800S ergometer; SensorMedics, Yorba Linda, CA) at 50 W and were familiarized with breathing through the apparatus used for metabolic measurements for 4 min. After warm-up, the work rate was increased every minute by ~25 W until volitional exhaustion or a plateau in VO2, despite increasing workload, and a respiratory exchange ratio (RER) ≥1.1 over ≥1 min was achieved. VO2 and carbon dioxide production (VCO2) were measured continuously by online expiratory gas exchange analysis (TrueOne 2400 Metabolic Measurement System; ParvoMedics, Salt Lake City, UT).

Experimental protocol. Each subject completed two stable isotope-labeled tracer infusion studies (~2 wk apart, in randomized order): once after resting and once after cycling on the preceding afternoon. For each study (rest and exercise), subjects were admitted to the GCRC the afternoon before the isotope infusion study. For the exercise study, subjects cycled on a semirecumbent cycle ergometer (EC-C400R Ergometer; Cateye Fitness, Source Distributors, Dallas, TX) for 2 h starting at 1730; the workload was set to elicit a VO2 equivalent to 60% VO2 peak. VO2 was measured (TrueOne 2400 Metabolic Measurement System; ParvoMedics) for 5–10 min at the beginning of the exercise and at 30-min intervals during exercise; the workload was adjusted as necessary to maintain (within ±5%) the desired VO2. After completion of the exercise, subjects took a shower and then rested in a chair. For both studies, subjects consumed a standard meal containing 16 kcal/kg body wt and 57% of total energy carbohydrates, 28% fat, and 15% protein at 2000, then fasted, except for water, and rested in bed until completion of the study the next day.

At 0530 the following morning, one catheter was inserted into a forearm vein to administer stable isotope-labeled tracers, and a second catheter was inserted into a contralateral hand vein; the hand was heated to 55°C with a thermostatically controlled box to obtain arterialized blood samples. Catheters were kept open with slow, controlled infusion of 0.9% NaCl solution (30 ml/h). At 0700 (time 0), after a blood sample for determination of plasma substrate, insulin, and enzyme concentrations and background glycerol, palmitate, and leucine tracer-to-tracee ratios (TTR) in plasma and VLDL-TG and apoB-100 was obtained, a bolus of [1,1,2,3,3-2H5]glycerol (75 µmol/kg body wt), dissolved in 0.9% NaCl solution, was administered through the catheter in the forearm vein, and constant infusions of [2,2-2H2]palmitate (0.03 µmol·kg body wt–1·min–1), dissolved in 25% albumin solution, and [5,5,5-2H3]leucine (0.12 µmol·kg body wt–1·min–1; priming dose 7.2 µmol/kg body wt), dissolved in 0.9% NaCl solution, were started and maintained for 12 h. Blood samples were obtained at 5, 15, 30, 60, 90, and 120 min and then every hour until completion of the study to determine glycerol and palmitate TTR in plasma and VLDL-TG, and leucine TTR in plasma and VLDL-apoB-100. VO2 and VCO2 were measured (Deltatrac Metabolic Monitor, SensorMedics) for 30 min starting at 2 and 5.5 h after the beginning of the isotope infusion, and the data were averaged. A muscle biopsy from the lateral portion of the quadriceps femoris muscle was obtained at 4 h (i.e., 15.5 h after the completion of exercise/rest on the preceding day) after lidocaine (2%) was applied to the area. Alternate legs were used to obtain muscle biopsies on different study days.

Sample collection and storage. Blood samples were collected in chilled tubes containing EDTA to determine substrate concentrations, and EDTA plus trasylol to determine insulin and enzyme concentrations. Samples were placed in ice, and plasma was separated by centrifugation within 30 min of collection. Aliquots of plasma (~2 ml) were kept in the refrigerator for immediate isolation of VLDL. The remaining plasma samples were stored at –80°C until final analyses were performed. To determine glucose concentration, blood was collected in tubes containing heparin, plasma was separated immediately by centrifugation, and the glucose was analyzed. Biopsy samples were cleansed with ice-cold saline, trimmed of any visible fat, blotted dry and frozen in liquid nitrogen, and stored at –80°C until final analysis.

Sample preparation and analyses. VLDL were prepared as previously described (38). Briefly, 2 ml of plasma were transferred into Opti Seal tubes (Beckman Instruments, Palo Alto, CA), overlaid with an NaCl-EDTA solution (1.006 kg/l) and centrifuged in a 50.4 Ti rotor (Beckman Instruments) at 100,000 g for 16 h at 10°C. The top layer, containing VLDL, was removed by tube slicing (Beckman Instruments) and stored at –80°C until final analyses were performed.

Plasma glucose concentration was determined on an automated glucose analyzer (Yellow Spring Instruments, Yellow Springs, OH). Plasma insulin concentration was measured by radioimmunoassay. Total plasma TG and VLDL-TG concentrations were determined with a spectrophotometric enzymatic kit (Sigma Chemicals, St. Louis, MO). Plasma fatty acid concentrations were quantified by gas chromatography (Hewlett-Packard 5890-II, Palo Alto, CA) after heptadecanoic acid was added to plasma as an internal standard (42). Total plasma and VLDL-apoB-100 concentrations were measured with an immunoturbidity assay (Wako Pure Chemical Industries, Osaka, Japan). Concentrations of LPL, LCAT, and CETP in plasma were determined with ELISA kits (Daiichi Pure Chemicals, Tokyo, Japan); the kit used for LPL does not cross-react with HL or pancreatic lipase. Plasma HL protein mass was determined by A. Bensadoun (Cornell University, Ithaca, NY) using ELISA with monoclonal antibodies generated against human HL (5).

Plasma free glycerol, palmitate, and leucine TTR and the TTR of glycerol, palmitate, and leucine present in VLDL-TG and apoB-100 were determined by gas chromatography-mass spectrometry (GC-MS; MSD 5973 System, Hewlett-Packard) (38, 42). Heptafluorobutyric (HFB) anhydride was used to form an HFB derivative of glycerol in plasma and VLDL-TG. The t-butyldimethylsilyl derivative was prepared for the analysis of plasma leucine and N-heptafluorobutyryl n-propyl ester for leucine in apoB-100. Plasma free palmitate and palmitate in VLDL-TG were analyzed as methyl esters.

Plasma lipoprotein particle concentrations were determined by 1H-NMR spectroscopy (40) on an AVANCE INCA NMR Chemical Analyzer equipped with an UltraShield superconducting magnet (Bruker BioSpin, Billerica, MA).

To determine total muscle LPL, ~20 mg of tissue were homogenized in a 10:1 volume-to-weight ratio of ice-cold modified radioimmumoprecipitation (RIPA) buffer (58), the homogenate was spun at 2,500 g for 15 min, and the supernatant was removed. Cytosolic and particulate (total membrane) fractions from ~80 mg of tissue were isolated as previously described (29). Total, cytosolic, and particulate fractions were stored at –80°C until further processing. Sixty micrograms of protein were separated by SDS-PAGE (10% resolving gel), blotted to nitrocellulose membranes, and incubated overnight at 4°C with primary antibody (Research Diagnostics, Flanders, NJ) diluted 1:500 in Tris-buffered saline with 0.1% tween-5% nonfat dry milk. The antibody-bound protein was visualized by enhanced chemiluminescence (Amersham Pharmacia Biotech, Piscataway, NJ) and quantified normalized to GADPH by densitometry.

Calculations. Palmitate rate of appearance (Ra) in plasma was calculated by dividing the palmitate tracer infusion rate by the average plasma palmitate TTR value from 60 to 180 min (steady state); total free fatty acid Ra was derived on the basis of the proportional contribution of palmitate to total free fatty acid concentration in plasma (37). The rate of whole body fat oxidation was calculated on the basis of VO2 and VCO2 measurements (15).

A metabolic steady state existed with regard to VLDL kinetics because the plasma VLDL-TG and apoB-100 concentrations remained constant throughout the sampling period. The fractional turnover rate (FTR) of VLDL-TG was determined by fitting the glycerol TTR time course in plasma and in VLDL-TG to a compartmental model (41). The absolute rate of VLDL-TG secretion was calculated as 1) total VLDL-TG secretion rate, which represents the total amount of VLDL-TG secreted by the liver; and 2) VLDL-TG secretion rate per unit of plasma as follows:


where CVLDL-TG is the concentration of VLDL-TG in plasma and PV is the plasma volume, which was estimated to be 0.055 l/kg fat-free mass (6). We assumed that the VLDL-TG volume of distribution is equal to PV because VLDL is restricted to plasma (44). The conclusions from our findings were the same regardless of whether the data were expressed in micromoles per minute or micromoles per liter of plasma per minute; we therefore elected to present data only expressed as micromoles per minute.

The relative contribution of systemic plasma free fatty acids to VLDL-TG-bound fatty acids was calculated by fitting the palmitate TTR in plasma and VLDL-TG to a compartmental model (38). The systemic plasma fatty acid pool includes fatty acids from the systemic circulation that are taken up by the liver and directly incorporated into VLDL-TG or temporarily incorporated into rapidly turning over intrahepatic and intraperitoneal TG stores before incorporation into VLDL-TG. The remaining fatty acids in VLDL-TG are derived from pools of fatty acids that are not labeled with tracer during the infusion period, including: 1) preexisting lipid stores in the liver and retroperitoneal fat depots, 2) lipolysis of plasma lipoproteins taken up by the liver, and 3) hepatic de novo lipogenesis.

The rate of whole body VLDL-TG clearance from plasma (an index of the efficiency of VLDL-TG removal) was calculated by dividing the rate of VLDL-TG disappearance from plasma (in µmol/min) by the plasma VLDL-TG concentration (in µmol/ml). The mean residence time of VLDL-TG was calculated as 1/FTR.

The FTR of VLDL-apoB-100 (in pools/h) was assessed on the basis of a compartmental model and the TTR of plasma free leucine and leucine bound to VLDL-apoB-100 (38). The total rate of VLDL-apoB-100 secretion (indicative of the secretion rate of VLDL particles) was calculated on the basis of plasma VLDL-apoB-100 concentration and VLDL-apoB-100 turnover rate as described above for VLDL-TG. The mean residence time of VLDL-apoB-100 (indicative of the mean residence time of a VLDL particle) was calculated as 1/FTR.

Statistical analysis. Results are presented as means ± SE. Comparisons between rest and exercise were made by Student's paired t-test; data were tested for normality and, if necessary, logarithmically transformed for analysis. A P value of ≤0.05 was considered statistically significant.


   RESULTS
TOP
 ABSTRACT
 RESEARCH DESIGN AND METHODS
 RESULTS
DISCUSSION
 GRANTS
 REFERENCES
 
VO2 peak and exercise workload and intensity. The average VO2 peak was 3.3 ± 0.3 l/min. Absolute power output and VO2 were constant between 10 and 120 min of exercise (data not shown): subjects exercised at an average of 117 ± 12 W, which corresponded to 61 ± 4% of their VO2 peak.

Plasma insulin and substrate concentrations. Plasma insulin, glucose, VLDL-TG, and VLDL-apoB-100 concentrations were significantly lower after evening exercise than after rest (all P < 0.05), and plasma fatty acid concentration was significantly higher (P < 0.05; Table 1).


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  		Table 1. Plasma insulin, glucose, and lipid concentrations after evening rest and evening exercise for 2 h at 60% VO2 peak

 
Substrate oxidation and fatty acid Ra. Basal VO2, and therefore resting energy expenditure, was ~10% higher (P < 0.05) after evening exercise (244 ± 12 ml O2/min) compared with rest (222 ± 11 ml O2/min), and RER tended to be lower after exercise (0.76 ± 0.01) than after rest (0.79 ± 0.02; P = 0.057). Evening exercise increased whole body fat oxidation by 40 ± 13% (P < 0.05; Fig. 1). Palmitate Ra increased by 64 ± 17% after exercise compared with rest (P < 0.05), and the increase in total fatty acid Ra (125 ± 28 µmol/min) was approximately twice as big as the increase in whole body fatty acid oxidation (74 ± 24 µmol/min; Fig. 1).



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  		Fig. 1. Whole body fatty acid oxidation and fatty acid rate of appearance (Ra) after evening rest (filled bars) and evening exercise for 2 h at 60% VO2 peak (open bars). *Value significantly different (P < 0.05) from value after rest.

 
VLDL-TG and apoB-100 kinetics. VLDL-TG FTR increased from 0.43 ± 0.03 pools/h after evening rest to 0.60 ± 0.06 pools/h after evening exercise (P < 0.05). Evening exercise had no effect on the rate of VLDL-TG secretion into plasma (Fig. 2) or the relative contribution of systemic and nonsystemic fatty acid sources to total VLDL-TG production; systemic plasma fatty acids contributed 76 ± 5% after rest and 68 ± 3% after exercise to total VLDL-TG production. The clearance rate of VLDL-TG, however, was ~40% greater (P < 0.05) after evening exercise (34 ± 4 ml/min) than evening rest (24 ± 2 ml/min), which resulted in a significant drop of the mean residence time of VLDL-TG in the blood stream by ~40 min (P < 0.05; Fig. 3). In contrast, VLDL-apoB-100 FTR was not different after evening rest (0.37 ± 0.04 pools/h) and exercise (0.38 ± 0.04 pools/h), and the rate of VLDL-apoB-100 secretion was significantly lower in response to exercise (P < 0.05; Fig. 2), whereas the time it takes to clear VLDL-apoB-100 (i.e., the VLDL particle) did not change (Fig. 3).



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  		Fig. 2. Rates of very-low-density lipoprotein-triglyceride (VLDL-TG; top) and VLDL-apolipoprotein B-100 (apoB-100; bottom) secretion into plasma after evening rest (filled bars) and evening exercise for 2 h at 60% VO2 peak (open bars). *Value significantly different (P < 0.05) from value after rest.

 


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  		Fig. 3. Mean residence times for VLDL-TG and VLDL-apoB-100 (top) and VLDL-TG plasma clearance rate (bottom) after evening rest (filled bars) and evening exercise for 2 h at 60% VO2 peak (open bars). *Value significantly different (P < 0.05) from value after rest.

 
Plasma lipoprotein NMR profile. Evening exercise significantly lowered the total number of VLDL particles in plasma (P < 0.05), due to ~50% fewer medium size particles. The concentration of intermediate-density lipoprotein (IDL) particles after exercise was almost double that after evening rest (P < 0.05). Exercise had no significant effect on LDL and HDL particle concentrations (Table 2).


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  		Table 2. Plasma lipoprotein particle concentrations after evening rest and evening exercise for 2 h at 60% VO2 peak

 
Muscle LPL and plasma LPL, HL, LCAT, and CETP. Muscle LPL content was not different after evening exercise compared with rest, whereas plasma LPL concentration increased by ~20% (P < 0.05) in response to exercise in six of the seven subjects; data from one subject was excluded because plasma LPL concentration was about fourfold higher than the average value of the other six subjects (Fig. 4). Plasma HL and LCAT concentrations were not affected by exercise, whereas plasma CETP concentration was ~10% lower after exercise than rest (P = 0.052; Fig. 5).



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  		Fig. 4. Musclea (top) and plasmab (bottom) lipoprotein lipase (LPL) protein masses after evening rest and evening exercise for 2 h at 60% VO2 peak. Top: representative blot for muscle LPL protein in 1 subject is shown (R, rest; EX, exercise). *Value significantly different (P < 0.05) from value after rest. aMean values for cytosolic and particulate fractions were derived from 6 subjects, due to limited muscle tissue from 1 subject. bMean value includes only 6 of the 7 subjects; in 1 subject, plasma LPL concentration was ~4-fold higher than in the other 6 subjects; he was, therefore, excluded from the analysis.

 


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  		Fig. 5. Plasma hepatic lipase (HL; top), lecithin:cholesterol acyltransferase (LCAT; middle) and cholesterol ester transfer protein (CETP; bottom) concentrations after evening rest (filled bars) and evening exercise for 2 h at 60% VO2 peak (open bars).

 

   DISCUSSION
TOP
 ABSTRACT
 RESEARCH DESIGN AND METHODS
 RESULTS
 DISCUSSION
GRANTS
 REFERENCES
 
We investigated the effects of a single vigorous bout of endurance exercise, which markedly lowered fasting plasma TG concentrations, on VLDL kinetics and plasma fatty acid availability, lipoprotein subclass distribution, and the protein mass of key enzymes involved in lipoprotein metabolism in healthy, lean young men. The most significant and novel findings from our study were that 1) exercise had no effect on the rate of VLDL-TG secretion despite significantly greater availability of plasma fatty acids after exercise, likely because of a simultaneous increase in fatty acid oxidation but also, we suspect, the use of fatty acids for replenishing tissue TG stores; 2) exercise lowered the rate of VLDL-apoB-100 secretion, an index of the secretion rate of VLDL particles, resulting in fewer VLDL particles in plasma; 3) exercise enhanced the efficiency of VLDL-TG removal from plasma without a simultaneous increase in muscle LPL protein content; however, increased plasma LPL concentration after exercise likely indicates greater release and possibly availability of muscle endothelial-bound LPL; and 4) faster VLDL-TG plasma clearance maintains low plasma TG concentration but is not accompanied by a similar increase in the next step of the delipidation cascade (i.e., IDL to LDL conversion). So, acutely after exercise, the cardioprotective lowering of plasma TG and VLDL concentrations is counteracted by a proatherogenic increase in IDL concentration.

The availability of plasma fatty acids is thought to be a major regulator of the rate of VLDL-TG secretion by the liver (33). However, we did not detect a change in the rate of VLDL-TG secretion the day after exercise, although plasma fatty acid availability was markedly increased and the increase in fatty acid Ra was not matched by the simultaneous increase in whole body fatty acid oxidation, which was less pronounced. The lack of detecting a change in VLDL-TG secretion in the presence of greater fatty acid availability is unlikely due to methodological limitations. If all of the nonoxidative fatty acid disposal were directed toward VLDL-TG secretion, it would have caused more than a doubling of the rate of VLDL-TG secretion, which we did not observe. Even if the amount of excess fatty acids available for VLDL-TG synthesis were smaller, considering that part of the nonoxidative use of fatty acids occurred in other (i.e., peripheral) tissues and that we may have overestimated the difference between fatty acid Ra and oxidation because of potential disagreement in the accuracy of the two measurements, we would expect the magnitude of the effect large enough to be measurable. It is also unlikely that exercise caused a regional redistribution of fatty acid uptake, with more fatty acids being directed toward muscle to help replenish intramuscular TG stores that were likely reduced by the exercise in our study (55). There is no evidence that blood flow to and fatty acid extraction by muscle (peripheral tissues in general) are greater the day after exercise; they return to resting values within 3 h after cessation of exercise (54). Finally, it is unlikely that fatty acid oxidation was stimulated by exercise to a greater extent in liver than in other tissues. Therefore, the "excess" fatty acids delivered to the liver after exercise are probably used to replenish hepatic TG stores that were likely depleted during the exercise as well. It is of interest to note that, in addition to the lack of change in the total rate of VLDL-TG production, there was also no change in the relative contribution of fatty acids from systemic plasma and other (presumably intrahepatic and visceral TG) sources despite the greater availability of systemic plasma fatty acids due to exercise. This finding disputes the current thought that a direct relationship exists between fatty acid availability in plasma and VLDL-TG secretion. This concept was originally established by measuring VLDL-TG turnover during infusion of Intralipid and heparin (33). The results from those studies are likely flawed because heparin stimulates LPL, which in itself could increase VLDL-TG turnover; also, plasma fatty acid availability was increased to values severalfold above normal. In accordance with our findings, Carpentier et al. (8) recently found no association between the insulin-induced suppression of plasma fatty acid availability and the rate of VLDL-TG secretion. We therefore suggest that, during normal physiological conditions, free fatty acid flux from extrahepatic tissues to the liver is not an important regulator of the absolute rate of VLDL-TG secretion. However, excess fatty acid availability postexercise may have maintained the VLDL-TG secretion rate despite a reduced rate of VLDL-apoB-100 secretion.

The suppression of VLDL-apoB-100 secretion after a single bout of exercise in our study is in accordance with the chronic effect of exercise described in a recent study in type 2 diabetic subjects (1), except that the magnitude of the lowering effect of exercise appeared to be greater after regular training than after a single bout. However, this could also be due to the faster baseline VLDL-apoB-100 secretion rate in the diabetic group compared with our subjects. The mechanisms responsible for the decrease in VLDL-apoB-100 secretion after exercise are not clear. It is possible that increased hepatic sensitivity to insulin after exercise (12, 36) is involved. VLDL-apoB-100 production is inhibited by experimentally induced hyperinsulinemia (34) and increased in insulin-resistant subjects (10). The reduced rate of VLDL-apoB-100 secretion after exercise, an index of the rate of secretion of VLDL particles, is consistent with fewer circulating VLDL particles revealed by NMR spectroscopy.

The markedly higher rate of VLDL-TG plasma clearance after exercise compared with rest occurred in the absence of a simultaneous change in muscle LPL content. Although muscle LPL content does not provide a direct measurement of LPL activity, changes in muscle LPL protein mass after exercise have been found to closely match the changes in muscle LPL activity in healthy men (47). Therefore, either exercise elicited an increase in LPL activity that is independent of an increase in muscle LPL protein mass [e.g., via posttranslational changes (50) or changes in inhibitory and stimulatory factors] or, alternatively, increased VLDL-TG plasma clearance following exercise was mediated via a muscle LPL-independent mechanism (e.g., direct uptake by the liver or other tissues). Furthermore, it is possible that we may have "missed" the effect because we measured muscle LPL content ~16 h after the cessation of exercise and it is known that the exercise-induced increase in muscle LPL mass and activity is transient and may have returned to baseline levels at the time of the biopsy in our study. In some studies, muscle LPL protein mass (48) and activity (24) 16–20 h after exercise are not different from resting conditions, whereas in others both muscle LPL protein mass (19, 47) and activity (30) are higher at that time. Although it is possible that the increase in muscle LPL was simply too small to be detected, it is more likely that muscle LPL synthesis (and mass) was indeed upregulated by exercise (probably via improved insulin sensitivity), and LPL then associated with the vascular endothelium, its site of action, and was then released into the bloodstream after VLDL-TG hydrolysis (21, 43, 45, 49). Release of newly synthesized LPL into the bloodstream makes it impossible to detect an increase in muscle LPL mass even if LPL synthesis is up-regulated. The increase in plasma LPL concentration in our study likely resulted from a greater release of the enzyme from the vascular endothelium in skeletal muscle because adipose tissue LPL is not affected by exercise (47).

The greater VLDL-TG clearance rate from plasma during the hypotriglyceridemic phase of recovery from exercise compared with resting conditions may also have resulted from changes in VLDL-TG content. The decrease in the rate of VLDL-apoB-100 secretion without a change in VLDL-TG secretion after exercise suggests secretion of VLDL particles that contain more TG. TG-rich VLDL (and similarly chylomicrons) have a greater affinity for LPL than TG-poor particles (14, 46). The accumulation of IDL particles after exercise compared with rest implies that the stimulatory effect of exercise on the initial step in the delipidation cascade is not matched by a similar change in the next one. This is probably because exercise does not increase HL concentration or activity (present study and Refs. 18 and 28), which mediates the conversion of IDL to LDL (11, 60). Alternatively, alterations in hepatic clearance of VLDL and IDL due to exercise may also contribute to the observed changes in their plasma concentration.

Changes in plasma lipoprotein subclass distribution in response to a single bout of vigorous exercise are ambiguous with regard to their clinically beneficial nature. We observed fewer VLDL, specifically medium-size VLDL, but more IDL particles and no change in LDL or HDL particle concentrations. Although much of the focus on the importance of lipoprotein subclass distribution for CVD has been on LDL, there is now considerable evidence that large VLDL and IDL and small HDL are predictors of CVD as well (32). It is difficult to evaluate our results in the context of available data in the literature because of conflicting reports, probably because of differences in study design (4, 52, 59). Also, it is possible that, because of the much slower turnover of HDL and LDL compared with VLDL, changes occur later after exercise or may require repeated bouts of exercise to manifest, and we therefore did not detect them in the present study.

We did not adjust dietary energy intake after exercise (at dinner) to compensate for the energy expended during exercise. Therefore, subjects were likely in a more negative energy balance after exercise than after rest. Consequently, we cannot determine the effect of contractile acitivity per se on the outcome measurements. However, our goal was to determine the lipid metabolism response to exercise during the hypotriglyceridemic time period after a single bout of exercise. Currently, it is not known to what extent the hypotriglyceridemic response to exercise is due to exercise-induced modification of energy balance or contractile activity per se. Most, if not all, of the studies that investigated the effect of exercise on plasma TG concentrations did not control for the negative energy balance induced by exercise. However, in one study, physical activity decreased plasma TG concentrations in subjects with type IV hyperlipoproteinemea independently of whether or not there was a compensatory increase in food intake (20). And a study in postmenopausal women demonstrated that a single 90-min bout of treadmill walking reduced fasting plasma TG concentrations the next day, whereas an energy deficit induced by diet restriction had no effect (16); however, the diet-induced energy deficit was considerably (~20%) smaller. In any case, compensatory food intake is not a normal physiological response to a single bout of exercise (51).

In summary, the major changes in lipid kinetics elicited by a single bout of exercise include a reduced VLDL-apoB-100 secretion rate without a change in the rate of VLDL-TG secretion despite greater fatty acid flux through the circulation. Plasma clearance of VLDL-TG, however, is significantly enhanced by exercise and maintains low plasma TG concentrations. Assessment of static variables of lipid metabolism indicated that exercise acutely changes the plasma lipid profile both for better (lower TG concentration, fewer VLDL particles) and for worse (more IDL particles, higher fatty acid concentration) regarding risk factors for CVD.


   GRANTS
TOP
 ABSTRACT
 RESEARCH DESIGN AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
REFERENCES
 
This study was supported by US National Institutes of Health Grants HD-01459, AR-49869, AG-00078, DK-56341 (Clinical Nutrition Research Unit), RR-00954 (Biomedical Mass Spectrometry Resource), and RR-00036 (General Clinical Research Center) and bygrants from the American Heart Association, the Novo Nordisk Foundation, and the Danish National Research Foundation (Center for Inflammation and Metabolism, Grant 02-512-55).


   ACKNOWLEDGMENTS
 
We thank Dr. Samuel Klein for medical supervision of the project, Megan Steward for subject recruitment, Junyoung Kwon for technical assistance, and the study subjects for their participation.


   FOOTNOTES
 

Address for reprint requests and other correspondence: B. Mittendorfer, Washington Univ. School of Medicine, Div. of Geriatrics and Nutritional Sciences, 660 South Euclid Ave., Campus Box 8031, St. Louis, MO 63110 (e-mail:mittendb{at}wustl.edu)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
TOP
 ABSTRACT
 RESEARCH DESIGN AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
 REFERENCES
 

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