Department of Human Physiology, Copenhagen Muscle Research Centre, University of Copenhagen, DK-2100 Copenhagen, Denmark
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ABSTRACT |
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The resting content and use of
myocellular triacylglycerol (MCTG) during 90 min of submaximal exercise
[60% of peak oxygen uptake
(O2 peak)] were studied in 21 eumenorrheic female and 21 male subjects at different training levels
[untrained (UT), moderately trained (MT), and endurance trained
(END)]. Males and females were matched according to their
O2 peak expressed relative to lean body
mass, physical activity level, and training history. All subjects
ingested the same controlled diet for 8 days, and all females were
tested in the midfollicular phase of the menstrual cycle. Resting MCTG,
measured with the muscle biopsy technique, averaged 48.4 ± 4.2, 48.5 ± 8.4, and 52.2 ± 5.8 mmol/kg dry wt in UT, MT, and
END females, respectively, and 34.1 ± 4.9, 31.6 ± 3.3, and
38.4 ± 3.0 mmol/kg dry wt in UT, MT, and END males, respectively
(P < 0.001, females vs. males in all groups). Exercise decreased MCTG content in the female subjects by an average of 25%,
regardless of training status, whereas in the male groups MCTG content
was unaffected by exercise. The arterial plasma insulin concentration
was higher (P < 0.05) and the arterial plasma
epinephrine concentration was lower (P < 0.05) in the
females than in the males at rest and during exercise. MCTG use was
correlated to the resting concentration of MCTG (P < 0.001). We conclude that resting content and use of MCTG during
exercise are related to gender and furthermore are independent of
training status.
muscle substrate; training; triglycerides
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INTRODUCTION |
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IT HAS PREVIOUSLY BEEN SHOWN (25) that myocellular triacylglycerol (MCTG) is utilized during the postexercise period. MCTG stores also represent a potentially large energy source during exercise. However, the extent to which MCTG is used during exercise and the possible existence of differences in its use between trained and untrained (UT) subjects are still under debate. In studies (27, 37) using stable isotope techniques combined with indirect calorimetry, it was estimated that MCTG accounted for 20-25% of the oxidative metabolism during submaximal exercise. However, when direct measurements of MCTG concentration in muscle biopsies have been used, some studies (4, 19, 34) have found a decrease in MCTG concentration during submaximal exercise, whereas others (1, 21, 22, 25, 44) have observed no change. In all of the above-mentioned studies, only male subjects have participated. Thus it is unknown whether gender differences exist in the utilization of MCTG during exercise. Some studies (18, 45, 46) have shown that females utilize lipids to a greater extent than males during submaximal exercise, but to our knowledge it has not been investigated whether this increased lipid utilization in females is primarily from MCTG or other lipid sources. Other studies (3, 6, 32) have not been able to find gender differences in lipid utilization during exercise. This could be due to differences in training status and exercise mode in the experimental designs. The aim of the present study was therefore to evaluate the contribution of MCTG during prolonged submaximal exercise, performed at the same relative workload, in female and male subjects at different training levels. The present study is part of a larger project evaluating metabolism in females and males during exercise at different training levels. The current study, however, focuses only on the effects of gender and training on MCTG levels and utilization.
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MATERIALS AND METHODS |
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Twenty-one female and twenty-one male subjects were recruited to
participate in the study. All subjects were young and healthy (although
not screened for family history of type 2 diabetes) and were nonsmokers
(Table 1). All subjects were fully
informed about the nature of the study and the possible risks
associated with it before they volunteered to participate, and written
consent was given. The study was approved by the Copenhagen Ethics
Committee and conformed to the code of ethics of the World Medical
Association (Declaration of Helsinki).
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Preexperimental protocol.
All subjects initially performed an incremental exercise test on a
Krogh bicycle ergometer to determine the peak oxygen uptake (O2 peak). In addition, all subjects
filled out a questionnaire and a training log regarding habitual
physical activity and training frequency, intensity, and duration as
well as competition history to establish these variables. To measure
lean body mass (LBM), a three-compartment model (9) was
used. Thus total body composition was assessed by hydrostatic weighing
(43), the pulmonary residual volume was determined by the
oxygen-dilution method (31), and total bone mineral
content was measured by dual-energy X-ray absorptiometry (DPX-IQ
scanner, software version 4.6.6; Lunar, Madison, WI). These
measurements were carried out under strictly controlled conditions. The
subjects were studied 3-4 h after the last meal and had defecated
and urinated beforehand. Furthermore, the subjects refrained from any
physical activities on the day before the test, which was carried out
in the midfollicular phase of the menstrual cycle in all the female subjects.
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Experimental protocol.
All subjects reported to the laboratory by either bus or car at 8 AM
after an overnight fast. All subjects abstained from any physical
activity for 2 days before the exercise experiment. After the subjects
rested for 30 min in the supine position, resting pulmonary oxygen
uptake (O2) and CO2
excretion (
CO2) were measured, and the
respiratory exchange ratio (RER) was calculated. Thereafter, a catheter
was inserted into the femoral artery under local anesthesia by use of
aseptic techniques, and the tip was advanced proximally 2 cm above the
inguinal ligamentum for blood sampling. After the catheter was
inserted, the subjects rested for 60 min in the supine position before
a second measurement of resting
O2 and
CO2 and subsequent calculation of RER.
Resting blood samples were drawn, and a muscle biopsy was obtained from the vastus lateralis muscle with suction under local anesthesia before
the subjects started to exercise on a Krogh bicycle ergometer for 90 min. All subjects exercised at the same relative workload (60%
O2 peak). Expired air was
collected in Douglas bags every 15 min during exercise for measurement
of
O2 and
CO2 and calculation of RER. Blood
samples were drawn at 15, 30, 60, 75, and 90 min of exercise. Heart
rate was monitored throughout the experiment with a heart rate monitor
(Vantage XL, Polar Electro). During exercise, subjects were allowed
water ad libitum and were cooled by an electric fan. At the termination
of exercise, another muscle biopsy was obtained through the same skin
incision but with the needle pointing in a different direction.
Pulmonary oxygen uptake and RER. Pulmonary oxygen uptake and RER were measured and calculated, respectively, during rest and exercise from the collection of expired air in the Douglas bags. The air volume in each Douglas bag was measured in a Collins bell spirometer (Tissot principle), and the O2 and CO2 content of the expired air was determined with a paramagnetic (Servomex) and an infrared (Beckman LB-2) system, respectively. Two gases of known composition were used to calibrate both systems regularly.
Muscle analysis.
In the present study, the biopsies were obtained from the same depth of
the vastus lateralis muscle to prevent differences in fiber type
composition between the biopsies obtained before and at the termination
of exercise (30). The biopsy samples were divided in two.
One part was frozen in liquid nitrogen within 10-15 s and stored
at 80°C for subsequent biochemical analysis. The other part was
mounted in embedding medium and frozen in precooled isopentane and then
stored at
80°C for subsequent histochemical analysis. Serial
transverse sections (10 µm) were cut and stained for myofibrillar
ATPase to identify the different fiber types (2). Before
biochemical analysis, ~30 mg wet wt of muscle tissue were freeze
dried and dissected free of all visible adipose tissue, connective
tissue, and blood with the use of a stereo microscope, leaving the
muscle fibers for further analysis. The muscle fibers were mixed, and
~1 mg dry wt of the pooled fibers was used for measurement of the
MCTG concentration according to the method of Kiens and Richter
(24). Glycerol from the degraded triacylglycerol was
assayed fluorometrically as described previously by Kiens and Richter
(24). A coefficient of variation (CV) of 4% for the MCTG
concentration was obtained between five samples from the mixed
freeze-dried pool of fibers as described above. In contrast, when five
small samples of wet muscle were dissected and analyzed separately, a
CV of 31% resulted between the samples. As suggested by
Wendling et al. (47), the relatively high variability in MCTG concentration between different locations in the muscle is a
concern when detecting expected differences of 20-30%. To
circumvent this potential problem, two or more biopsies might be
obtained. However, the large number of subjects and the consistency in
our findings regardless of training status indicate that our findings are not masked by methodological errors. To further avoid the impact of
methodological errors as well as day-to-day variation in the analysis,
we analyzed muscle tissue from both female and male subjects in one
assay run.
Blood analysis.
Blood was sampled in heparinized syringes, immediately transferred to
plastic test tubes containing EGTA, and centrifuged. Plasma was
immediately frozen at 80°C until further analysis. Blood for the
analysis of progesterone and estradiol was sampled in dry syringes and
transferred to dry test tubes in which the blood coagulated for a few
hours before it was centrifuged. Serum was frozen at
80°C until
further analysis. The plasma concentration of insulin was determined
using an RIA kit (insulin RIA 100, Pharmacia and Upjohn Diagnostics,
Uppsala, Sweden). The plasma concentrations of epinephrine and
norepinephrine were also determined using an RIA kit (KatCombi RIA,
Immuno-Biological Laboratories, Hamburg, Germany) as were the serum
concentrations of progesterone (progesterone 125I RIA, DGR
Instruments) and estradiol (estradiol ultrasensitive RIA, DGR Instruments).
Statistical evaluation.
Results are given as means ± SE. A three-way ANOVA with repeated
measures for the time factor was used to determine whether variables
were influenced by gender, training status, or time as well as to test
for a possible interaction between these three factors. For the
variables independent of time, a two-way ANOVA was used to determine
any influences of gender and training status and a possible interaction
between these two factors. Because females and males were not pairwise
matched, gender was not considered to be a repeated factor. In the case
of a significant main effect of one or more factors, Tukey's post hoc
test was used to detect pairwise differences between the means.
Correlations were evaluated by means of linear regression analysis
(Pearson product moment correlations). In all cases, an of 0.05 was
used as the level of significance.
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RESULTS |
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Diet. As we intended, the actual experimental diet averaged 65.5 E% carbohydrates, 19 E% fat, and 15.5 E% protein in all groups (Table 2). There were no differences in energy intake in any groups for habitual vs. experimental diet. The energy intake was significantly higher in males than in females and in END vs. UT and MT subjects. In UT and MT females and males, the nutrient composition of the habitual diet was similar and slightly but significantly different from the experimental diet. In END females and males, the energy percentages of carbohydrates and fat in the habitual diet were similar to those of the experimental diet. Furthermore, the energy percentage from dietary carbohydrates was higher for END than for UT subjects.
Workload.
The average workloads during the bicycle exercise test were expressed
relative to O2 peak and as
O2 per kilogram of LBM (Table 1). All
subjects completed the 90-min bicycle exercise test at a workload
corresponding to 59% of
O2 peak
Furthermore, at each training level no gender differences were observed
in
O2 expressed relative to LBM.
However, in females as well as males, the UT, MT, and END groups
differed significantly in
O2 expressed
relative to LBM (P < 0.01).
RER.
At rest, RER was similar in all groups (0.80 ± 0.02, 0.81 ± 0.02, and 0.79 ± 0.02 in UT, MT, and END females, respectively, and 0.85 ± 0.05, 0.80 ± 0.03, and 0.79 ± 0.01 in UT,
MT, and END males, respectively; Fig.
1). RER remained constant throughout the
exercise period in UT and MT subjects, averaging 0.87 ± 0.02 and
0.89 ± 0.02 in UT females and males, respectively, and 0.87 ± 0.02 and 0.89 ± 0.02 in MT females and males, respectively. However, RER remained constant during the first 60 min of exercise in
END subjects (0.90 ± 0.02 and 0.91 ± 0.02 at 60 min in
females and males, respectively) and subsequently decreased
(P < 0.05) to 0.87 ± 0.02 and 0.88 ± 0.01 at 90 min in females and males, respectively. No gender differences or
effects of training status were observed at any time point.
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Pulmonary O2.
O2 remained constant throughout the
exercise period, averaging 1.56 ± 0.07, 1.70 ± 0.05, and
2.19 ± 0.11 in UT, MT, and END females, respectively, and
2.17 ± 0.13, 2.31 ± 0.10, and 2.7 ± 0.08 in UT, MT,
and END males, respectively. The average
O2 during exercise was higher in END
subjects compared with UT and MT subjects (P < 0.001). Furthermore, the average
O2 during exercise was lower in females
than in males within each training group (P < 0.001).
MCTG.
At rest, the MCTG content in the vastus lateralis muscle was
significantly higher in the female subjects vs. the male subjects, regardless of training status (48.4 ± 4.2, 48.5 ± 8.4, and
52.2 ± 5.8 mmol/kg dry wt in UT, MT, and END females,
respectively, and 34.1 ± 4.9, 31.6 ± 3.3, and 38.4 ± 3.0 mmol/kg dry wt in UT, MT, and END males, respectively;
P < 0.001; Fig. 2). At
the termination of exercise, a mean decrease (P < 0.001) of 25% in MCTG content was observed in the female
subjects, regardless of training status. However, in the male subjects
the MCTG content remained unchanged after vs. before exercise,
regardless of training level. Thus a significant gender difference was
observed in MCTG utilization during exercise. A positive correlation
existed between MCTG content at rest and the degree of MCTG utilization
during exercise (r = 0.61, P < 0.001, Fig. 3).
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Fiber type distribution.
The fiber type distribution in the vastus lateralis muscle was not
different between UT and MT females (Table
3). However, in END females the
percentage of type I fibers was higher (P < 0.001) and
the percentage of type IIB fibers was lower (P < 0.001) compared with UT and MT females. Differences were not observed in the percentage of type IIA fibers.
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Circulating hormones.
At rest, the arterial plasma concentration of insulin averaged 8.3 ± 0.9, 8.3 ± 1.2, and 5.9 ± 0.9 µU/ml in UT, MT, and END females, respectively, and 7.1 ± 1.2, 6.2 ± 0.7, and
5.9 ± 0.8 µU/ml in UT, MT, and END males, respectively (Fig.
4A). The arterial plasma
insulin concentration decreased continuously throughout exercise to
5.4 ± 0.6, 6.2 ± 2.1, and 4.3 ± 1.1 µU/ml at 90 min in UT, MT, and END females, respectively, and 3.2 ± 0.4, 3.1 ± 0.4, and 3.1 ± 0.5 µU/ml at 90 min in UT, MT, and END males,
respectively (P < 0.001). The arterial plasma insulin
concentration was significantly higher in females than in males at rest
and during exercise regardless of training status (P < 0.05).
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DISCUSSION |
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The results of the present study demonstrate significant gender-based differences in resting content and utilization of MCTG during prolonged submaximal exercise at the same relative workload. At rest, the content of MCTG was significantly higher in females compared with males. During exercise, females utilized MCTG, whereas males did not. The observations of a higher resting content and MCTG use during exercise in females vs. males were made under conditions in which several parameters that could potentially affect substrate oxidation, including the pretest diet and the menstrual status and cycle phase of the female subjects, were standardized and carefully controlled.
MCTG content at rest. It has previously been demonstrated (23) that diet influences the MCTG content in human skeletal muscle, i.e., the consumption of a fat-rich diet increases MCTG content at rest. The higher MCTG content at rest in the female subjects compared with the male subjects in the present study is presumably not ascribed to the diet as all subjects ingested the same carbohydrate-rich diet for 8 days preceding the exercise experiment. Actually, due to their larger energy intake, males consumed a larger absolute amount of fat compared with females. However, when expressed relative to LBM, the fat ingestion was similar in females and males.
To explain the finding of a higher resting MCTG content in females compared with males, we examined the muscle fiber composition, since it has previously been shown (7) in male subjects that type I fibers contain more MCTG than type II fibers. Furthermore, in a group of females and males, it has recently been shown (20) that MCTG content in soleus, tibialis anterior, and tibialis posterior muscles varied consistently with the expected fraction of type I fibers in these muscles. One might also consider the possibility that females have a higher content of MCTG in type I fibers and/or other fiber types than males. To our knowledge, this has not yet been investigated. END females and males had more type I fibers compared with both MT and UT females and males. There was no effect of gender in the percentage of type I fibers in MT and END subjects. However, UT females had a higher percentage of type I fibers than UT males. Previously, a similar fiber type composition in females and males has been found in UT subjects (5, 35, 39) as well as in physical education students (40). Other studies have found that in UT subjects (42), middle-distance runners (5), trained cyclists (11), and subjects representing a wide range of physical activity levels (33), females had a higher percentage of type I fibers than males. At all training levels in the present study, the area of all the fiber types was smaller in females than in males, especially for type II fibers, which is in accordance with previous observations (5, 35, 39, 40, 42). As a consequence, the calculated fiber composition expressed relative to fiber area revealed that type I fibers accounted for a relatively larger area in females than in males. Thus the higher percentage of type I fibers expressed relative to area might partly explain the higher resting content of MCTG in females. This is further supported by the findings in the present study of a modest but significant correlation between the percentage of type I fibers relative to area and the resting concentration of MCTG (P < 0.05, r = 0.39). In the present study, no effect of training status on MCTG concentrations at rest was observed in females or males. Previous studies in males have reported inconsistent results, with some studies (22, 34) showing an increase in resting MCTG with training and others (19) showing no such increase. The strict dietary control may explain why an effect of training status on the resting MCTG concentrations was not observed in the present study. The experimental diet was a low-fat diet and differed from the diet in our (22) previous study. The possibility that the low-fat diet has concealed a training effect on MCTG concentration in the present study can therefore not be excluded. Another possible explanation of the increase in MCTG concentration with training in our (22) previous study might be that the subjects had exercised the day before the measurements were done. Because MCTG has been shown (25) to be utilized in the postexercise period, the difference in the reported resting concentration between trained and UT muscle (22) might be influenced by different degrees of postexercise MCTG use in trained and UT muscle.MCTG utilization during exercise. A major novel finding in the present study was that female subjects, regardless of training status, utilized a significant amount of MCTG during prolonged exercise, whereas male subjects did not. The fact that male subjects did not utilize MCTG during exercise to any measurable extent is in accord with our (22, 25) previous findings as well as other studies (1, 12, 21, 44) but does contrast with some studies (4, 19, 34) in which MCTG utilization was determined by applying the muscle biopsy technique. In recent studies (17, 38) in females in which a combination of isotope tracer technique and indirect calorimetry was used, it was suggested that the additional source of fatty acids oxidized during exercise at the same absolute workload after training (vs. before training) was provided by MCTG. Applying the same indirect methodology, several studies (27, 37) in males have indicated a similar significant utilization of MCTG during exercise. However, recent investigations in our laboratory revealed that combining isotope tracer technique and indirect calorimetry does not provide an accurate measure of MCTG use in males (13, 36) but does in females (36). This suggests that fat utilized during exercise is recruited from different sources in females and males (36).
To our knowledge, this study is the first to compare MCTG utilization in matched females and males at different training levels during prolonged exercise by applying the muscle biopsy technique. Recently, Guo et al. (12) evaluated the kinetics of intramuscular triacylglycerol fatty acids during exercise. Even though both female and male subjects participated in the study (12), a gender comparison was not made. Furthermore, net breakdown of MCTG in the vastus lateralis muscle was not observed during exercise, supporting our finding in male subjects. However, that study (12) revealed simultaneous esterification of plasma fatty acids to MCTG and MCTG hydrolysis when subjects exercised at 45% of ![]() |
ACKNOWLEDGEMENTS |
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We thank I. B. Nielsen, B. Bolmgren, and W. Taagerup for providing skilled technical assistance. We also thank Prof. Erik A. Richter for performing the invasive procedures.
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FOOTNOTES |
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This study was supported by Danish National Research Foundation Grant 504-12 and by the Danish Sports Research Council.
Address for reprint requests and other correspondence: B. Kiens, Copenhagen Muscle Research Centre, Dept. of Human Physiology, Universitetsparken 13, DK-2100 Copenhagen, Denmark (E-mail: Bkiens{at}aki.ku.dk).
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.
10.1152/ajpendo.00078.2001
Received 27 February 2001; accepted in final form 2 November 2001.
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REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
1.
Bergman, BC,
Butterfield GE,
Wolfel EE,
Casazza GA,
Lopaschuk GD,
and
Brooks GA.
Evaluation of exercise and training on muscle lipid metabolism.
Am J Physiol Endocrinol Metab
276:
E106-E117,
1999
2.
Brooke, MH,
and
Kaiser KK.
Three "myosin adenosine triphosphatase" systems: the nature of their pH lability and sulfhydryl dependence.
J Histochem Cytochem
18:
670-672,
1970[ISI][Medline].
3.
Burguera, B,
Proctor D,
Dietz N,
Guo Z,
Joyner M,
and
Jensen MD.
Leg free fatty acid kinetics during exercise in men and women.
Am J Physiol Endocrinol Metab
278:
E113-E117,
2000
4.
Carlson, LA,
Ekelund LG,
and
Froberg SO.
Concentration of triglycerides, phospholipids and glycogen in skeletal muscle and of free fatty acids and beta-hydroxybutyric acid in blood in man in response to exercise.
Eur J Clin Invest
1:
248-254,
1971[ISI][Medline].
5.
Costill, DL,
Daniels J,
Evans W,
Fink W,
Krahenbuhl G,
and
Saltin B.
Skeletal muscle enzymes and fiber composition in male and female track athletes.
J Appl Physiol
40:
149-154,
1976
6.
Costill, DL,
Fink WJ,
Getchell LH,
Ivy JL,
and
Witzmann FA.
Lipid metabolism in skeletal muscle of endurance-trained males and females.
J Appl Physiol
47:
787-791,
1979
7.
Essen, B,
Jansson E,
Henriksson J,
Taylor AW,
and
Saltin B.
Metabolic characteristics of fibre types in human skeletal muscle.
Acta Physiol Scand
95:
153-165,
1975[ISI][Medline].
8.
Essen-Gustavsson, B,
and
Tesch PA.
Glycogen and triglyceride utilization in relation to muscle metabolic characteristics in men performing heavy-resistance exercise.
Eur J Appl Physiol
61:
5-10,
1990.
9.
Forslund, AH,
Johansson AG,
Sjodin A,
Bryding G,
Ljunghall S,
and
Hambraeus L.
Evaluation of modified multicompartment models to calculate body composition in healthy males.
Am J Clin Nutr
63:
856-862,
1996[Abstract].
10.
Fröberg, SO,
Hultman E,
and
Nilsson LH.
Effect of noradrenaline on triglyceride and glycogen concentrations in liver and muscle from man.
Metabolism
24:
119-126,
1975[ISI][Medline].
11.
Goedecke, JH,
Gibson AS,
Grobler L,
Collins M,
Noakes TD,
and
Lambert EV.
Determinants of the variability in respiratory exchange ratio at rest and during exercise in trained athletes.
Am J Physiol Endocrinol Metab
279:
E1325-E1334,
2000
12.
Guo, Z,
Burguera B,
and
Jensen MD.
Kinetics of intramuscular triglyceride fatty acids in exercising humans.
J Appl Physiol
89:
2057-2064,
2000
13.
Helge, JW,
Watt PW,
Richter EA,
Rennie MJ,
and
Kiens B.
Fat utilization during exercise; adaptation to a fat-rich diet increases utilization of plasma fatty acids and very low density lipoprotein-triacylglycerol in humans.
J Physiol (Lond)
537:
1009-1020,
2001
14.
Hellström, L,
Blaak E,
and
Hagström-Toft E.
Gender differences in adrenergic regulation of lipid mobilization during exercise.
Int J Sports Med
17:
439-447,
1996[ISI][Medline].
15.
Holm, C,
Belfrage P,
and
Fredrikson G.
Immunological evidence for the presence of hormone-sensitive lipase in rat tissues other than adipose tissue.
Biochem Biophys Res Commun
148:
99-105,
1987[ISI][Medline].
16.
Holm, C,
Kirchgessner TG,
Svenson KL,
Fredrikson G,
Nilsson S,
Miller CG,
Shively JE,
Heinzmann C,
Sparkes RS,
and
Mohandas T.
Hormone-sensitive lipase: sequence, expression, and chromosomal localization to 19 cent-q13.3.
Science
241:
1503-1506,
1988[ISI][Medline].
17.
Horowitz, JF,
Leone TC,
Feng W,
Kelly DP,
and
Klein S.
Effect of endurance training on lipid metabolism in women: a potential role for PPAR in the metabolic response to training.
Am J Physiol Endocrinol Metab
279:
E348-E355,
2000
18.
Horton, TJ,
Pagliassotti MJ,
Hobbs K,
and
Hill JO.
Fuel metabolism in men and women during and after long-duration exercise.
J Appl Physiol
85:
1823-1832,
1998
19.
Hurley, BF,
Nemeth PM,
Martin WH,
Hagberg JM, III,
Dalsky GP,
and
Holloszy JO.
Muscle triglyceride utilization during exercise: effect of training.
J Appl Physiol
60:
562-567,
1986
20.
Hwang, JH,
Pan JW,
Heydari S,
Hetherington HP,
and
Stein DT.
Regional differences in intramyocellular lipids in humans observed by in vivo 1H-MR spectroscopic imaging.
J Appl Physiol
90:
1267-1274,
2001
21.
Jansson, E,
and
Kaijser L.
Effect of diet on the utilization of blood-borne and intramuscular substrates during exercise in man.
Acta Physiol Scand
115:
19-30,
1982[ISI][Medline].
22.
Kiens, B,
Essen-Gustavsson B,
Christensen NJ,
and
Saltin B.
Skeletal muscle substrate utilization during submaximal exercise in man: effect of endurance training.
J Physiol (Lond)
469:
459-478,
1993[Abstract].
23.
Kiens, B,
Essen-Gustavsson B,
Gad P,
and
Lithell H.
Lipoprotein lipase activity and intramuscular triglyceride stores after long-term high-fat and high-carbohydrate diets in physically trained men.
Clin Physiol
7:
1-9,
1987[ISI][Medline].
24.
Kiens, B,
and
Richter EA.
Types of carbohydrate in an ordinary diet affect insulin action and muscle substrates in humans.
Am J Clin Nutr
63:
47-53,
1996[Abstract].
25.
Kiens, B,
and
Richter EA.
Utilization of skeletal muscle triacylglycerol during postexercise recovery in humans.
Am J Physiol Endocrinol Metab
275:
E332-E337,
1998[Abstract].
26.
Kjær, M,
Howlett K,
Langfort J,
Zimmerman-Belsing T,
Lorentsen J,
Bülow J,
Ihlemann J,
Feldt-Rasmussen U,
and
Galbo H.
Adrenaline and glycogenolysis in skeletal muscle during exercise: a study in adrenalectomised humans.
J Physiol (Lond)
528:
371-378,
2000
27.
Klein, S,
Coyle EF,
and
Wolfe RR.
Fat metabolism during low-intensity exercise in endurance-trained and untrained men.
Am J Physiol Endocrinol Metab
267:
E934-E940,
1994
28.
Langfort, J,
Ploug T,
Ihlemann J,
Enevoldsen LH,
Stallknecht B,
Saldo M,
Kjær M,
Holm C,
and
Galbo H.
Hormone-sensitive lipase (HSL) expression and regulation in skeletal muscle.
Adv Exp Med Biol
441:
219-228,
1998[ISI][Medline].
29.
Langfort, J,
Ploug T,
Ihlemann J,
Saldo M,
Holm C,
and
Galbo H.
Expression of hormone-sensitive lipase and its regulation by adrenaline in skeletal muscle.
Biochem J
340:
459-465,
1999[ISI][Medline].
30.
Lexell, J,
Henriksson-Larsen K,
and
Sjostrom M.
Distribution of different fibre types in human skeletal muscles. II. A study of cross-sections of whole m. vastus lateralis.
Acta Physiol Scand
117:
115-122,
1983[ISI][Medline].
31.
Lundsgaard, C,
and
van Slyke DD.
Relation between thorax size and lung volume in normal adults.
J Exp Med
27:
65-85,
1918.
32.
Marliss, EB,
Kreisman SH,
Manzon A,
Halter JB,
Vranic M,
and
Nessim SJ.
Gender differences in glucoregulatory responses to intense exercise.
J Appl Physiol
88:
457-466,
2000
33.
Miller, AE,
MacDougall JD,
Tarnopolsky MA,
and
Sale DG.
Gender differences in strength and muscle fiber characteristics.
Eur J Appl Physiol
66:
254-262,
1993.
34.
Phillips, SM,
Green HJ,
Tarnopolsky MA,
Heigenhauser GJ,
and
Grant SM.
Progressive effect of endurance training on metabolic adaptations in working skeletal muscle.
Am J Physiol Endocrinol Metab
270:
E265-E272,
1996
35.
Prince, FP,
Hikida RS,
and
Hagerman FC.
Muscle fiber types in women athletes and non-athletes.
Pflügers Arch
371:
161-165,
1977[ISI][Medline].
36.
Roepstorff, C,
Steffensen CH,
Madsen M,
Stallknecht B,
Kanstrup IL,
Richter EA,
and
Kiens B.
Gender differences in substrate utilization during submaximal exercise in endurance trained subjects.
Am J Physiol Endocrinol Metab
282:
435-447,
2002.
37.
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
38.
Romijn, JA,
Coyle EF,
Sidossis LS,
Rosenblatt J,
and
Wolfe RR.
Substrate metabolism during different exercise intensities in endurance-trained women.
J Appl Physiol
88:
1707-1714,
2000
39.
Sale, DG,
MacDougall JD,
Alway SE,
and
Sutton JR.
Voluntary strength and muscle characteristics in untrained men and women and male bodybuilders.
J Appl Physiol
62:
1786-1793,
1987
40.
Schantz, P,
Randall-Fox E,
Hutchison W,
Tyden A,
and
Åstrand PO.
Muscle fibre type distribution, muscle cross-sectional area and maximal voluntary strength in humans.
Acta Physiol Scand
117:
219-226,
1983[ISI][Medline].
41.
Severson, DL.
Regulation of lipid metabolism in adipose tissue and heart.
Can J Physiol Pharmacol
57:
923-937,
1979[ISI][Medline].
42.
Simoneau, JA,
Lortie G,
Boulay MR,
Thibault MC,
Theriault G,
and
Bouchard C.
Skeletal muscle histochemical and biochemical characteristics in sedentary male and female subjects.
Can J Physiol Pharmacol
63:
30-35,
1985[ISI][Medline].
43.
Siri, WE.
The Gross Composition of the Body. Advances in Biological and Medical Physics. New York: Academic, 1956, p. 239-280.
44.
Starling, RD,
Trappe TA,
Parcell AC,
Kerr CG,
Fink WJ,
and
Costill DL.
Effects of diet on muscle triglyceride and endurance performance.
J Appl Physiol
82:
1185-1189,
1997
45.
Tarnopolsky, LJ,
MacDougall JD,
Atkinson SA,
Tarnopolsky MA,
and
Sutton JR.
Gender differences in substrate for endurance exercise.
J Appl Physiol
68:
302-308,
1990
46.
Tarnopolsky, MA,
Atkinson SA,
Phillips SM,
and
MacDougall JD.
Carbohydrate loading and metabolism during exercise in men and women.
J Appl Physiol
78:
1360-1368,
1995
47.
Wendling, PS,
Peters SJ,
Heigenhauser GJ,
and
Spriet LL.
Variability of triacylglycerol content in human skeletal muscle biopsy samples.
J Appl Physiol
81:
1150-1155,
1996
48.
World Health Organization.
Energy and Protein Requirements: Report of a Joint FAO/WHO/UNU Expert Consultation. Geneva: WHO, 1985. (Tech Rep Ser 724)