1 Human Muscle Metabolism Research Group, Department of Physical Education, Sports Science and Recreation Management, 2 Human Biology Research Group, Department of Human Sciences, Loughborough University, Loughborough, Leicestershire LE11 3TU; and 3 Oxford Lipid Metabolism Group, Sheikh Rashid Laboratory, The Radcliffe Infirmary, Oxford OX2 6HE, United Kingdom
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ABSTRACT |
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Prior exercise decreases postprandial plasma
triacylglycerol (TG) concentrations, possibly through changes to
skeletal muscle TG extraction. We measured postprandial substrate
extraction across the leg in eight normolipidemic men aged 21-46
yr. On the afternoon preceding one trial, subjects ran for 2 h at
64 ± 1% of maximal oxygen uptake (exercise); before the control
trial, subjects had refrained from exercise. Samples of femoral
arterial and venous blood were obtained, and leg blood flow was
measured in the fasting state and for 6 h after a meal (1.2 g fat,
1.2 g carbohydrate/kg body mass). Prior exercise increased time
averaged postprandial TG clearance across the leg (total TG: control,
0.079 ± 0.014 ml · 100 ml
tissue1 · min
1; exercise,
0.158 ± 0.023 ml · 100 ml
tissue
1 · min
1, P
<0.01), particularly in the chylomicron fraction, so that absolute TG
uptake was maintained despite lower plasma TG concentrations (control,
1.53 ± 0.13 mmol/l; exercise, 1.01 ± 0.16 mmol/l,
P < 0.001). Prior exercise increased postprandial leg
blood flow and glucose uptake (both P < 0.05). Mechanisms
other than increased leg TG uptake must account for the effect of prior
exercise on postprandial lipemia.
triacylglycerol; glucose; arteriovenous differences; leg blood flow
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INTRODUCTION |
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IMPAIRED CLEARANCE of triacylglycerol (TG)-rich lipoproteins constitutes an atherogenic influence on other lipoprotein species (16): when their residence time in the circulation is prolonged, these particles exchange their TG for cholesteryl ester from the cholesterol-rich lipoproteins. The result is a depletion of high-density lipoprotein (HDL) cholesterol and a preponderance of small, dense low-density lipoprotein particles, a combination known as the atherogenic lipoprotein phenotype (1). Case-control studies support the clinical relevance of these interactions, showing that indexes of postprandial lipemia are highly discriminatory in predicting the presence or absence of coronary artery disease (21, 32). Humans spend most of their lives in the postprandial state, so impaired processing of TG-rich lipoproteins, reflecting a poor metabolic capacity for TG, is likely to be one determinant of atherogenesis. Nevertheless, little is known about potential modulators of postprandial lipemia or their mechanisms of action.
Exercise may be such a modulator; a single session has been shown to reduce the lipemic response to a fatty meal consumed some hours afterwards by >20% (30, 35). One plausible mechanism is enhanced removal after exercise of TG from TG-rich lipoproteins into skeletal muscle. This speculation is supported by evidence for exercise-induced changes to the activity of skeletal muscle lipoprotein lipase (LPL), the rate-limiting enzyme of TG hydrolysis and, hence, removal. Exercise induces an increase in LPL gene expression in human skeletal muscle. This increase is transient and delayed, the peak LPL protein response occurring >8 h after exercise (25), which fits well with the findings of whole body studies where reduced lipemia was evident when the test meal was consumed 12-15 h after an exercise session (19, 30, 35).
Nevertheless, there is little direct evidence of the consequences of exercise-induced changes to muscle LPL activity for the postprandial partitioning of TG and their relation to reduced postprandial plasma TG concentrations. Thus the purpose of the present study was to examine the influence of a prolonged session of prior exercise on postprandial extraction of TG across the leg. We interpreted measurements of arteriovenous differences across the leg to reflect mainly skeletal muscle metabolism. There is evidence that chylomicron-TG is hydrolyzed by LPL in preference to very low density lipoprotein (VLDL)-TG (22); therefore, we determined TG extraction in individual lipoprotein fractions.
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SUBJECTS AND METHODS |
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Subjects.
Eight healthy men aged 21-46 yr with body mass index of 24.6 ± 1.8 kg/m2, body fat level of 17.6 ± 4.6%, and
maximal oxygen uptake (O2 max) of
56.8 ± 5.3 ml · kg
1 · min
1 (all
means ± SD) volunteered to participate. Lean tissue (muscle plus
bone) comprised 72.5% (range 67.1-77.1%) of their leg volumes, assessed as described below. The Ethical Advisory Committee of Loughborough University and the Central Oxford Research Ethics Committee approved the study protocol. The purpose of the study and the
risks involved in taking part were explained to the subjects before
their written informed consent was obtained. All subjects were
normolipidemic, with plasma concentrations in the fasted state of
3.54 ± 0.32 mmol/l for total cholesterol, 1.09 ± 0.07 mmol/l for HDL cholesterol, and 0.91 ± 0.09 mmol/l (all
means ± SD) for TG. They were all nonsmokers, and none used any
medication. Five took part in physically active recreations and three
in structured endurance training programs.
Preliminary exercise tests.
Two preliminary exercise tests were conducted. In the first,
O2 max was determined during uphill
running at a constant speed (range 2.9 to 3.8 m/s). In the second, the
steady-state relationship between submaximal
O2 and treadmill speed was established. The treadmill running speed, which elicited 60% of
O2 max was interpolated on an
individual basis.
Study design.
Each subject underwent two oral fat tolerance tests in a randomized
fully balanced design, with an interval of 2 or 3 wk and with different
preconditions. On one occasion (exercise trial), subjects ran on a
motorized treadmill for 2 h at 60%
O2 max. Approximately 3 h after
the run (and at the corresponding time on the control trial), they ate
a standard low-fat evening meal [5.35 ± 0.31 MJ (means ± SD), with 10% of energy from fat and 71% from carbohydrate]. The
next morning, they were taken to the laboratory for the oral fat
tolerance test. On the other occasion (control trial), no exercise was
performed, but other procedures were identical.
Treadmill runs.
Subjects began running at 1400, >1 h after a light lunch. Expired air
samples were collected every 15 min using Douglas bags. These were
analyzed for oxygen with a paramagnetic analyzer (570A; Taylor-Servomex, Crowborough, UK) and for carbon dioxide with an
infrared analyzer (Lira MSA model 303; Mines Safety Appliances Britain,
Coatbridge, Scotland). Gas volumes were measured by means of a
dry-gas meter (Harvard Apparatus, Edenbridge, Kent, UK) and corrected to STPD. O2 and carbon dioxide
production were calculated using the Haldane transformation. Heart rate
was monitored using short-range telemetry (Sport-Tester; Polar Electro,
Tampere, Finland).
Fat tolerance tests. Subjects reported to the laboratory at 0800 after a 12-h fast, 16 h after the end of exercise. They were placed in the supine position, and the right groin was exposed. Under aseptic conditions, the skin overlying the right femoral vessels was anesthetized with 1% lidocaine, and the femoral artery was cannulated via a guide-wire in a cephalad direction (20 Fr, 8 cm, Leadercath, Vygon, Ecouen, France). The ipsilateral femoral vein was then cannulated in a caudal direction with the same technique. Sterile physiological saline (0.9% wt/vol) without heparin was continuously infused through each cannula (femoral artery, 50 ml/h; femoral vein, 30 ml/h) to maintain patency. For sampling procedures, the vascular line dead space was aspirated before blood samples were removed and then flushed with saline.
Subjects then rested for 30 min before two basal blood samples were taken, simultaneously, from the femoral artery and the femoral vein, with an interval of 20 min. The test meal was then consumed over a maximum of 10 min. This consisted of whipping cream, cereal, coconut, nuts, chocolate, and fruit and was given according to body mass (per kg body mass: 1.2 g fat, 1.2 g carbohydrate, 0.2 g protein, and 61 kJ energy). For our subjects, this meant 98 ± 8 g fat, 98 ± 8 g carbohydrate, and 16 ± 1 g protein, with a total energy value of 4.95 ± 0.42 MJ (all means ± SD), 69% of which came from fat. Additional blood samples were obtained 20, 40, 60, 90, and 120 min after completion of the meal and then hourly for 6 h. Arterial blood pressure and leg and subcutaneous abdominal adipose tissue blood flows were measured immediately after each blood sample. Blood pressure was measured with an automated sphygmomanometer. Calf blood flow was determined by venous occlusion plethysmography below the right knee (10) and calculated according to the principle outlined by Sumner (29). This approach to the measurement of leg blood flow has been validated previously (28). Blood flow was measured in adipose tissue, a major site of postprandial TG uptake, by the 133Xe washout technique (18), using a CsI-scintillation detector as described previously (24). Subjects remained immobile for periods of 10 min during measurements of blood flows.Analytical methods.
Blood samples were dispensed into precooled EDTA, heparinized, and
plain Monovettes (Sarstedt, Leicester, UK). Heparinized blood was
immediately used to measure hematocrit and oxygen saturation (Co-oximeter, Instrumentation Laboratory, Warrington, UK). Blood samples in plain tubes were allowed to clot for 1 h at room
temperature before serum was separated. A portion of each EDTA blood
sample was rapidly deproteinized with perchloric acid (70 g/l) for
measurement of 3-hydroxybutyrate concentration, and the remainder was
used to prepare plasma within 15 min. Plasma was recovered after
low-speed centrifugation at 4°C. From samples obtained at the second
baseline and at 2, 3, 4, 5, and 6 h, one aliquot was kept
overnight on ice at 4°C until chylomicron- and VLDL-rich fractions
were prepared by density-gradient ultracentrifugation. Further aliquots
were stored at 20°C until analysis.
Lipoprotein fractionation by density-gradient ultracentrifugation. The chylomicron-rich fraction was prepared by layering 0.75 ml of plasma underneath NaCl solution [density 1.006 g/ml, with 0.01% (wt/vol) EDTA] in thin-walled open-topped centrifuge tubes (11 × 34 mm). The tubes were then centrifuged in an ultracentrifuge (Optima TLX, Beckman Instruments, High Wycombe, Bucks, UK) for 20 min in a swinging-bucket rotor (Beckman, TLS 55) at 30,000 rpm. The chylomicron-rich fraction was then separated by slicing. The VLDL-rich fraction was prepared using the infranatant from 0.75 ml of plasma, prepared as described above, which was transferred into bell-topped centrifuge tubes (13 × 51 mm). These tubes were filled with NaCl solution, sealed, and centrifuged for 2 h 30 min in a fixed angle rotor (Beckman, TLA 100 · 4) at 100,000 rpm. The VLDL-rich fraction was then separated by slicing. Both separated fractions were aspirated into preweighed glass tubes. Within-batch coefficients of variation for concentrations of TG in chylomicron- and VLDL-rich fractions were 4.8 and 5.2%, respectively.
Anthropometry. Height and body mass were determined by standard methods. Body density was predicted from the logarithm of the sum of skinfold thicknesses at four sites and used to estimate body fatness (6). Leg, muscle, and bone volumes were determined by anthropometry (14, 15) with ultrasound to measure subcutaneous fat thickness.
Calculations.
Variables for substrate extraction across the leg were calculated as
described previously (22). Concentrations of TG (total or
in lipoprotein fractions) and glucose in plasma (P) were converted to
those in whole blood (B) using the hematocrit (H): B = P × (1 H). The Dillon factor (5) was used to correct
for distribution of glucose between plasma and erythrocytes.
Arteriovenous (a-v) differences were calculated for whole blood
concentrations. Two measures of substrate extraction were calculated:
absolute extraction (uptake) as a-vsubstrate × leg
blood flow, and substrate clearance as uptake/arterial concentration.
Clearance, therefore, measures the "efficiency of removal."
Statistical analysis. Results are shown as means ± SE unless otherwise stated. Variables were compared between trials by repeated-measures ANOVA to examine the effects of trial, time, and (where appropriate) sampling site. In addition, basal values and summary measures of postprandial responses (time averaged areas under response vs. time curves) were compared by t-test for correlated data. Where data were not normally distributed (3-hydroxybutyrate), comparisons were performed after logarithmic transformation. Statistical procedures were performed using Statistica for Windows 95, version 5.0 (Stat Soft, Tulsa, OK).
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RESULTS |
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Cardiorespiratory and metabolic responses during running.
The average O2 during running, 37.0 ± 2.7 ml · kg
1 · min
1,
represented 64 ± 3% of
O2 max.
An estimated 53 ± 9 g of fat and 333 ± 49 g of
carbohydrate were oxidized, with a gross energy expenditure of
7.21 ± 0.87 MJ, 28 ± 4% from fat and 72 ± 4% from
carbohydrate. Average values for heart rate and respiratory exchange
ratio were 166 ± 14 beats/min and 0.91 ± 0.01 (all
means ± SD), respectively.
Plasma TG concentrations in basal and postprandial states.
Arterial and femoral venous plasma concentrations of total, VLDL- and
chylomicron-TG are shown in Fig. 1, with
summary statistics in Table 1. Basal
values of total and VLDL-TG were significantly lower in the exercise
trial than in the control trial. Basal values for the concentration of
TG measured in the fraction separated as chylomicrons were not
distinguishable from zero. Postprandial concentrations of total,
VLDL-TG, and chylomicron-TG were all significantly lower in the
exercise trial, as were the postprandial increases in these variables
above the basal level.
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Cardiovascular responses.
Neither leg blood flow nor leg vascular resistance was significantly
different in the basal state between trials (Fig.
2). Postprandially, leg blood flow was
significantly higher in the exercise trial, and leg vascular resistance
was significantly lower [time averaged areas under the response vs.
time curves: leg blood flow, control 1.6 ± 0.2 ml · 100 ml tissue1 · min
1, exercise
2.2 ± 0.3 ml · 100 ml
tissue
1 · min
1 (P < 0.01); leg vascular resistance, control 62.3 ± 4.9 mmHg · ml
1 · 100 ml
tissue
1 · min; exercise 46.8 ± 7.3 mmHg · ml
1 · 100 ml
tissue
1 · min (P = 0.03)]. Changes in mean arterial blood pressure were small and
did not differ between trials (average values: control, 84 ± 1 mmHg; exercise, 81 ± 2 mmHg). Average adipose tissue blood flow
in the postprandial state, calculated over the whole period between
basal and 6-h time points, was not significantly different between
trials (control, 4.0 ± 0.5 mm Hg ml
1 · 100 ml tissue
1 · min
1; exercise
4.3 ± 1.0 mm Hg ml
1 · 100 ml
tissue
1 · min
1).
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Substrate extraction across the leg.
Data comparing TG extraction across the leg are presented as
uptake (Table 2 and Fig.
3) and clearance (Table 2 and Fig. 4). In the basal state, none of these
measures differed significantly between trials. Postprandially, uptake
of total TG increased significantly from basal in both exercise and
control trials, but there was no such increase in the uptake of
VLDL-TG. There were no significant differences between trials in
postprandial uptake of TG (an absolute measure of extraction) (main
effect of trial: total TG, P = 0.21; VLDL-TG,
P = 0.32; chylomicron-TG, P = 0.20),
but postprandial clearance (a measure of fractional removal) was higher
in the exercise trial for total, VLDL-TG, and chylomicron-TG. TG
clearance was higher in the exercise trial for a given arterial TG
concentration (Fig. 5).
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Responses of glucose, insulin, NEFA, lactate, and
3-hydroxybutyrate.
Arterial concentrations of plasma glucose, plasma NEFA, plasma lactate,
blood 3-hydroxybutyrate, and serum insulin are shown in Fig.
6. There were no significant differences
in plasma NEFA concentrations, either in the basal state
(P = 0.07) or postprandially (P = 0.08), but the change over time differed significantly between trials
(interaction, P < 0.01). 3-Hydroxybutyrate concentration was higher in the exercise trial, both in the basal state
(P < 0.01) and postprandially (ANOVA,
P < 0.01; area under the concentration vs. time curve,
P < 0.01) with a different pattern of change over time
(interaction, P = 0.02). Plasma lactate concentration
was lower in the exercise trial in the basal state (P = 0.02) and in the postprandial state (ANOVA, P = 0.02).
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DISCUSSION |
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Prior exercise decreased plasma TG concentrations during the hours after consumption of a high-fat mixed meal by more than one-third. By contrast with earlier reports suggesting that exercise largely influences chylomicron-TG (2, 33), >70% of this decrease was attributable to the lower concentration of TG in VLDL. Our functional measures of substrate extraction across the leg during the postprandial period help elucidate the metabolic basis of these effects.
In the fasted state, plasma TG concentration was 0.25 mmol/l lower after exercise, as observed previously. This effect has often (26) been attributed to an increase in muscle LPL activity (17, 25), the assumption being that increased enzyme activity leads to greater muscle TG uptake. A new finding of our study was that, although prior exercise may have enhanced the efficiency of LPL action as measured by leg TG clearance (Table 2 and Fig. 4), the absolute uptake of TG across the leg in the fasted state was relatively unchanged in the fasted state.
Mechanisms other than increased leg TG uptake that might account
for the lower basal TG concentration in the exercise trial include
increased adipose tissue uptake or/and a suppressive effect on hepatic
VLDL secretion. The former seems unlikely for two reasons. First, we
were able to measure TG uptake across subcutaneous abdominal adipose tissue in three subjects with the use of methods described previously (9). For each individual, prior exercise
reduced, rather than increased, TG uptake [control 0.165 (range,
0.109-0.243) µmol · 100 g
tissue1 · min
1; exercise 0.092 (range, 0.027-0.164) µmol · 100 g
tissue
1 · min
1]. Second, adipose
tissue LPL activity has been reported to be unchanged by exercise in
fasted subjects (25).
By contrast, prior exercise may well have decreased VLDL-TG secretion rate in the fasting state. Blood 3-hydroxybutyrate concentration was higher after exercise, suggesting enhanced hepatic fatty acid oxidation. This would decrease the availability of fatty acids for re-esterification and thus decrease VLDL-TG secretion, in line with published data showing (in rats) that training decreases VLDL secretion (20, 27). To the authors' knowledge, no comparable data are available for humans.
These are the first data to describe the effects of prior exercise on leg TG uptake and clearance during the postprandial period. Although the decrease in TG concentrations was particularly clear during the postprandial period, there was no convincing evidence that prior exercise increased the rate of leg TG uptake. The main effect, as shown so clearly in Fig. 5, was to increase the efficiency of leg TG clearance, so that leg TG uptake was maintained despite a much lower plasma TG concentration.
The higher leg TG clearance can be assumed to reflect an effect of prior exercise on muscle LPL. Exercise increases mRNA for skeletal muscle LPL (25) and, hence, enzyme activity (17) over a time scale that fits well with our observations, i.e., maximal increase >8 h after exercise (26). Our data show that this is functionally important in postprandial leg TG clearance and is sufficient to override the inhibition of muscle LPL activity by insulin (7). The improvement of leg TG clearance by prior exercise was greater in the chylomicron fraction than in the VLDL fraction, probably because LPL appears to hydrolyze larger, more TG-rich lipoproteins better than smaller particles (22).
Assuming that the appearance rate of chylomicron-TG was not delayed by prior exercise (and we found no evidence for a later peak in concentration that might suggest this), then whole body chylomicron-TG uptake must have been increased. We can exclude a significant increase in muscle uptake, so (provided that myocardial uptake of chylomicron-TG was similar in both trials) uptake into adipose tissue may have been enhanced. Postprandial subcutaneous abdominal adipose tissue blood flow was not higher after exercise, however, so greater uptake would require an increase in adipose tissue LPL activity, but there is no evidence on this for the postprandial state.
Whole body chylomicron uptake may have been greater after exercise simply because VLDL-TG concentration was lower, reducing competition for hydrolysis by LPL. The major part of the difference between trials in postprandial TG concentration was attributable to VLDL-TG. As suggested for the fasted state, this might reflect a lower rate of VLDL-TG synthesis and secretion, secondary to greater oxidation in the liver of fatty acids. The higher postprandial 3-hydroxybutyrate response in the exercise trial provides indirect evidence for this.
The finding that prior exercise enhanced postprandial muscle blood flow measured the next day is intriguing and, to the authors' knowledge, novel. It is consistent with reports that leg blood flow is higher in endurance-trained men than in normally active controls (11). One mechanism may be that enhanced sensitivity to insulin in trained people reinforces its hemodynamic effects, which include decreasing vascular resistance (Fig. 2). A single session of exercise improves insulin sensitivity in physically active individuals (4), so this might explain our findings. A limitation to this reasoning is that concentrations of serum insulin and plasma glucose after the test meal were not influenced by exercise, but this does not preclude an effect on insulin action.
The higher leg blood flow in the exercise trial increased glucose
delivery, facilitating enhanced glucose uptake during hyperinsulinemia. It takes ~20 h for a 70-kg person having ingested 500-600 g of carbohydrate to replenish muscle glycogen depleted by exercise (3). In our study, where subjects exercised at 64% of
O2 max for 2 h, utilizing a total
of ~330 g of carbohydrate, both muscle and liver glycogen would have
been considerably reduced (23). The evening meal consumed
after exercise contained 250 g of carbohydrate, clearly
insufficient fully to restore these glycogen stores. Consequently, prior exercise led to enhanced leg glucose uptake for utilization in
muscle glycogen synthesis. Low muscle glycogen might also explain the
higher plasma NEFA concentrations after exercise (34). Low liver glycogen might explain the lower basal plasma lactate in the
exercise trial if hepatic uptake of lactate, an important gluconeogenic
precursor, was enhanced.
We have interpreted our measurements of a-v differences across the leg to reflect mainly changes to skeletal muscle metabolism. Some contamination of venous samples with drainage from adipose tissue may occur with these techniques, but if the venous cannula is inserted in a caudal direction, as in our study, this is minimal (31). Furthermore, the legs we studied were lean (15), muscle plus bone typically comprising 73% of leg volume. Consequently, we are confident that the measurements we present reflect mainly the metabolism of skeletal muscle.
In summary, prior exercise enhanced TG clearance across the leg, allowing postprandial tissue uptake of TG-derived fatty acids to be maintained despite a markedly lower arterial plasma TG concentration. Postprandial leg blood flow was higher after exercise, and this served to increase leg glucose uptake during the early part of the postprandial period, presumably to facilitate muscle glycogen replenishment.
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ACKNOWLEDGEMENTS |
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We thank the British Heart Foundation for support and the subjects for their participation. We thank Mo Clark for technical help, the Wellcome Trust and the Dunhill Medical Trust for specialist equipment, and Coca Cola UK for the provision of beverages for subjects after the studies.
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FOOTNOTES |
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Address for reprint requests and other correspondence: A. E. Hardman, Human Muscle Metabolism Research Group, Dept. of Sports Science, Loughborough Univ., Loughborough, Leicestershire LE11 3TU, UK (E-mail:a.e.hardman{at}lboro.ac.uk).
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.
Received 24 February 2000; accepted in final form 22 June 2000.
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REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
1.
Austin, MA,
King MC,
Vranizan KM,
and
Krauss RM.
Atherogenic lipoprotein phenotype: a proposed genetic marker for coronary heart disease risk.
Circulation
82:
495-506,
1990[Abstract].
2.
Cohen, JC,
Noakes TD,
and
Benade AJS
Postprandial lipemia and chylomicron clearance in athletes and sedentary men.
Am J Clin Nutr
49:
443-447,
1989[Abstract].
3.
Coyle, EF.
Substrate utilization during exercise in active people.
Am J Clin Nutr
61:
9685-9795,
1995.
4.
Dela, F,
Mikines KJ,
von Linstow M,
Secher NH,
and
Galbo H.
Effect of training on insulin-mediated glucose uptake in human muscle.
Am J Physiol Endocrinol Metab
263:
E1134-E1143,
1992.
5.
Dillon, R.
Importance of hematocrit in interpretation of blood sugar.
Diabetes
14:
672-678,
1974[ISI][Medline].
6.
Durnin, JVGA,
and
Womersley J.
Body fat assessed from total body density and its estimation from skinfold thicknesses: measurements on 481 men and women aged from 16 to 72 years.
Br J Nutr
32:
77-97,
1974[ISI][Medline].
7.
Farese, RV,
Yost TJ,
and
Eckel RH.
Tissue-specific regulation of lipoprotein lipase activity by insulin/glucose in normal-weight humans.
Metabolism
40:
214-216,
1991[ISI][Medline].
8.
Frayn, KN,
and
Macdonald IA.
Assessment of substrate and energy metabolism in vivo.
In: Clinical Research in Diabetes and Obesity. Part I: Methods, Assessment, and Metabolic Regulation, edited by Dranzin B,
and Rizza R. Totowa, NJ: Humana, 1997, p. 101-124.
9.
Frayn, KN,
Shadid S,
Hamilani R,
Humphreys SM,
Clarke ML,
Fielding BA,
Boland O,
and
Coppack SW.
Regulation of fatty acid movement in human adipose tissue in the postabsorptive to postprandial transition.
Am J Physiol Endocrinol Metab
266:
E308-E317,
1994
10.
Greenfield, ADM,
Whitney RJ,
and
Mowbray JF.
Methods for the investigation of peripheral blood flow.
Br Med Bull
19:
101-109,
1963[ISI].
11.
Hardin, DS,
Azzarelli B,
Edwards J,
Wigglesworth J,
Maianu L,
Brechtel G,
Johnson A,
Baron A,
and
Garvey WT.
Mechanisms of enhanced insulin sensitivity in endurance-trained athletes: effects on blood flow and differential expression of GLUT 4 in skeletal muscles.
J Clin Endocrinol Metab
80:
2437-2446,
1995[Abstract].
12.
Humphreys, SM,
Fisher RM,
and
Frayn KN.
Micro-method for measurement of sub-nanomole amounts of triacylglycerol.
Ann Clin Biochem
27:
597-598,
1990[ISI][Medline].
13.
Jannson, PA,
and
Lönnroth P.
Comparison of two methods to assess the tissue/blood partition coefficient for xenon in subcutaneous adipose tissue in man.
Clin Physiol
15:
45-55,
1995.
14.
Jones, PRM
Radiographic determination of leg fat, muscle and bone volumes in male and female adults.
J Physiol (Lond)
207:
1P-3P,
1969.
15.
Jones, PRM,
and
Pearson J.
Anthropometric determination of leg fat and muscle plus bone volumes in young male and female adults.
J Physiol (Lond)
204:
63P-66P,
1969[Medline].
16.
Karpe, F,
and
Hamsten A.
Postprandial lipoprotein metabolism and atherosclerosis.
Curr Opin Lipidol
6:
123-129,
1995[ISI][Medline].
17.
Kiens, B,
Lithell H,
Mikines KJ,
and
Richter E.
Effects of insulin and exercise on muscle lipoprotein lipase activity in man and its relation to insulin action.
J Clin Invest
84:
1124-1129,
1989[ISI][Medline].
18.
Larsen, OA,
Lassen NA,
and
Quaade F.
Blood flow through human adipose tissue determined with radioactive xenon.
Acta Physiol Scand
66:
337-345,
1966[ISI][Medline].
19.
Malkova, D,
Hardman AE,
Bowness RJ,
and
Macdonald IA.
The reduction in postprandial lipemia after exercise is independent of the relative contribution of fat and carbohydrate to energy metabolism during exercise.
Metabolism
48:
245-251,
1999[ISI][Medline].
20.
Mondon, CE,
Dolkas CB,
Tobey T,
and
Reaven GM.
Causes of the triglyceride-lowering effect of exercise training in the rat.
J Appl Physiol
57:
1455-1471,
1984.
21.
Patsch, JR,
Miesenböck G,
Hopferwieser T,
Muhlberger V,
Knapp E,
Dunn JK,
Gotto AM,
and
Patsch W.
Relation of triglyceride metabolism and coronary artery disease. Studies in the postprandial state.
Arterioscler Thromb
12:
1336-1345,
1992[Abstract].
22.
Potts, JL,
Fisher RM,
Humphreys SM,
Coppack SW,
Gibbons GF,
and
Frayn KN.
Peripheral triacylglycerol extration in the fasting and post-prandial states.
Clin Sci (Colch)
81:
621-626,
1991[ISI][Medline].
23.
Romijn, JA,
Coyle EF,
Sidossis LS,
Gastaldelli A,
Horowitz JF,
Endert E,
and
Wolfe RR.
Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration.
Am J Physiol Endocrinol Metab
265:
E380-E391,
1993
24.
Samra, JS,
Frayn KN,
Giddings JA,
Clark ML,
and
Macdonald IA.
Modification and validation of a commercially available portable detector for measurement of adipose tissue blood flow.
Clin Physiol
15:
241-248,
1995[ISI][Medline].
25.
Seip, RL,
Angelopoulos TJ,
and
Semenkovich CF.
Exercise induces human lipoprotein lipase gene expression in skeletal muscle but not adipose tissue.
Am J Physiol Endocrinol Metab
268:
E229-E236,
1995
26.
Seip, RL,
Mair D,
Cole TG,
and
Semenkovich CF.
Induction of human skeletal muscle lipoprotein lipase gene expression by short-term exercise is transient.
Am J Physiol Endocrinol Metab
272:
E255-E261,
1997
27.
Simonelli, C,
and
Eaton RP.
Reduced triglyeride secretion: a metabolic consequence of chronic exercise.
Am J Physiol
3:
E221-E227,
1978.
28.
Simonsen, L,
Ryge C,
and
Bülow J.
Glucose-induced thermogenesis in splanchnic and leg tissues in man.
Clin Sci (Colch)
88:
543-550,
1995[ISI][Medline].
29.
Sumner, DS.
Volume plethysmography in vascular disease: an overview.
In: Noninvasive Diagnostic Techniques in Vascular Disease, edited by Berstein EF. St. Louis, MO: Mosby, 1985, p. 97-118.
30.
Tsetsonis, NV,
Hardman AE,
and
Mastana SS.
Acute effects of exercise on postprandial lipemia: a comparative study in trained and untrained middle-aged women.
Am J Clin Nutr
65:
525-533,
1997[Abstract].
31.
Van Hall, G,
González-Alonso J,
Sacchetti M,
and
Saltin B.
Skeletal muscle substrate metabolism during exercise: methodological considerations.
Proc Nutr Soc
58:
899-912,
2000[ISI].
32.
Weintraub, MS,
Grosskopf I,
Rassin T,
Miller H,
Charach G,
Rotmensch HH,
Liron M,
Rubinstein A,
and
Iaina A.
Clearance of chylomicron remnants in normolipidaemic patients with coronary artery disease: case control study over three years.
Br Med J
312:
935-939,
1996
33.
Weintraub, MS,
Rosen Y,
Otto R,
Eisenberg S,
and
Breslow JL.
Physical conditioning in the absence of weight loss reduces fasting and postprandial triglyceride-rich lipoprotein levels.
Circulation
79:
1007-1014,
1989[Abstract].
34.
Weltan, SM,
Bosch AN,
Dennis SC,
and
Noakes TD.
Influence of muscle glycogen content on metabolic regulation.
Am J Physiol Endocrinol Metab
274:
E72-E82,
1998
35.
Zhang, JQ,
Thomas TR,
and
Ball SD.
Effect of exercise timing on postprandial lipemia and HDL cholesterol subfractions.
J Appl Physiol
85:
1516-1522,
1998