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Original Studies |
Departments of Internal Medicine (M.K., K.F.P., R.B., D.L., G.I.S.) and Diagnostic Radiology (T.P., D.L.R.) and the Howard Hughes Medical Institute (G.I.S.), Yale University School of Medicine, New Haven, Connecticut 06536; and the Division of Endocrinology and Metabolism, Department of Internal Medicine III (M.R.), University of Vienna, Vienna, Austria
Address all correspondence and requests for reprints to: Gerald I. Shulman, M.D., Ph.D., Howard Hughes Medical Institute Research Laboratories, Yale University School of Medicine, Boyer Center for Molecular Medicine, 295 Congress Avenue, P.O. Box 9812, New Haven, Connecticut 06536-8012. E-mail: gerald.shulman{at}yale.edu
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Abstract |
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 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
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lactate and the glucosealanine cycle
from the resting muscle (forearm) to recovering muscles (thigh and
calf) after running exercise . |
Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Hepatic glycogen mobilization and gluconeogenesis also play an important role as a source of glucose for the working muscle and glycogen replenishment of active and recovering muscle (19, 20, 21). However, the possible redistribution of glycogen stores from noncontracting to contracting muscles during both exercise and recovery is still questioned (3, 22, 23, 24, 25, 26). According to the proposed model, glycogenolysis coupled to nonaerobic glycolysis in nonactive muscles would provide the substrates for glucose production through gluconeogenesis in the liver and kidney, which could than be channeled to preexercised muscle for glycogen repletion during recovery from exercise
Although it has been demonstrated that fuel utilization shifts from carbohydrates to lipids with increasing duration of submaximal exercise (27, 28, 29), the specific contribution of the intramyocellular lipid (IMCL) pool as energy substrate also remains to be determined. Dynamic changes in IMCL during prolonged exercise and subsequent recovery have been evaluated by using an invasive approach. Some studies showed a significant depletion of intramuscular lipid stores during the exercise and an increase in these stores during the recovery phase (30, 31, 32, 33). Other studies found no changes in the intramuscular triglycerides after shorter exercise tests with alternating exercise intensities (34, 35).
Now that recent studies have presented and validated the nuclear magnetic resonance (NMR) spectroscopy methods for noninvasive quantification of IMCL (36, 37) and glycogen (38) contents, the present study was designed to examine 1) intracellular glycogen and lipid utilization in different muscle groups during prolonged exercise, 2) resynthesis of glycogen and IMCL of different muscles during recovery from exercise, and 3) whether there is redistribution of glycogen between nonexercising and exercising muscles during recovery.
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Subjects and Methods |
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Nine (seven males and two females) trained subjects (body mass index, 24.3 ± 1.2 kg/m2; VO2 peak, 54.2 ± 2.7 mL O2/kg·min) underwent the exercise protocol, and three of them [body mass index, 25.7 ± 3 kg/m2; VO2 peak (maximal oxygen consumption), 52.7 ± 2.5 mL O2/kg·min] underwent an additional control protocol. For 3 days before the study, subjects received an isocaloric diet consisting of 60% carbohydrates, 20% fat, and 20% proteins and were instructed not to participate in strenuous physical exercise. Experimental procedures were carried out in accordance with the guidelines of the human investigation committee of Yale University School of Medicine. All subjects gave informed consent after the purpose, nature, and potential risks of the study were explained to them.
Peak oxygen uptake test
Maximal aerobic power was determined during a preliminary running treadmill (series 2000 Treadmill, Marquette, WI) test session 10 days before the running experiment using incremental speeds (starting at 2.5 km/h1 and +1.0 km/h every minute) and grades (starting at 0° and +2° every minute) until exhaustion. Oxygen uptake was measured by indirect calorimetry based on continuous breath by breath analysis of expired gas and measurement of minute ventilation (Vmax29 Metabolic Monitor, Sensormedics, CA). Heart rate was monitored during the test using the Max1 (Marquette, WI). The VO2 peak was established when two of the following three criteria were met: 1) oxygen consumption plateaued with increasing workload, 2) heart rate was greater than the age-predicted maximal value, and 3) respiratory exchange ratio (RER) exceeded 1.1.
Experimental design
The subjects were admitted to the Yale University New Haven Hospital General Clinical Research Center (GCRC) the evening before the study. They received a light breakfast at 0500 h on the day of the study. The exercise protocol was started at 0900 h and consisted of 45-min bouts of running on a motor-driven treadmill (series 2000 Treadmill, Marquette, WI) at 65–70% of the athlete’s predetermined peak oxygen uptake until exhaustion. The rest intervals between the exercise bouts included NMR measurements of muscular glycogen concentration and lasted about 30 min. To verify that the subjects were working at the proper intensity, oxygen uptake was measured during the first 10 min of the first interval and during the last 5 min of each running interval. Subjects were encouraged to drink water during the exercise, but were fasted during the entire exercise session and the first 5 h of the recovery period. At 1900 h the subjects were given a standard meal and remained in the GCRC until 0600 h next morning.
Intramuscular glycogen (thigh, vastus lateralis; calf, gastrocnemius/soleus complex; forearm, flexores digitorum) and IMCL (soleus muscle) concentrations were measured before exercise (thigh, calf, and forearm muscle), after each bout of exercise (thigh muscle), at the end of the last bout of exercise (0–2 h after exercise), and during the recovery (thigh, calf, and forearm muscle) at 4–5 and 17–18 h after the exercise. Due to the length of each NMR measurement (30 min for each intramuscular glycogen determination, 15 min for IMCL measurement) the forearm muscle glycogen content could be measured only at 100 min after exercise in the first five subjects. To allow clear discrimination between the effects of exercise and early recovery on glycogen concentration in nonexercising muscle, an additional forearm glycogen concentration measurement was performed immediately after the last exercise bout before the remaining NMR measurements for the next four subjects. Although it is possible that some resynthesis of glycogen and IMCL content might have occurred during the 15- to 30-min period needed for the NMR spectroscopic measurements, if such resynthesis occurs, its extent would be negligible. Maehlum et al. showed that the resynthesis of glycogen from endogenous sources after prolonged submaximal exercise is less than 2 mmol/L·h (10), which is in accordance with the rates of glycogen synthesis measured in the first 5 h of recovery by our study and would result in an increase in muscle glycogen concentration by approximately 1 mmol/L. This change in glycogen concentration is below the detectability of the 13C NMR method.
Blood samples were collected before breakfast (-240 min), 5 min before the start of exercise (baseline), at the end of each exercise bout (45, 90, 135, and 180 min), every hour up to 5 h of recovery, and the next morning at 0530 h before breakfast (18 h of recovery).
The control protocol was designed to study a possible effect of fasting per se on IMCL and glycogen concentrations. The subjects were given the same diet 3 days before the study and were admitted to the GCRC the evening before the study. No physical activity was allowed during this part of experiment. Breakfast and dinner were given at 0500 and 1900 h, respectively. Four sets of muscle glycogen and IMCL concentration measurements were performed starting 0800, 1400, 1800, and 0700 h the next morning. Time points were chosen according to the time course of the NMR measurements in the exercise protocol. Blood samples were collected at 0500 (before breakfast), 1000, 1200, 1400, 1700, 1900, and 0500 h the next morning.
NMR measurements
The glycogen concentration was measured by 13C NMR spectroscopy on a 2.1-T/1-m BioSpec system (Bruker Instruments, Inc., Billerica, MA) for thigh and calf muscles and on a 4.7-T/30-cm BioSpec Products, Inc., system (Bruker Instruments, Inc.) for forearm muscle. The coils and pulse sequences used were as previously described (15, 37). Briefly, thigh muscle glycogen was measured using a 9-cm circular 13C coil in a transmitter/receiver regimen combined with a 12 x 14-cm coplanar butterfly proton coil, which was used for shimming, scout images, and proton decoupling during 13C acquisition. Similarly, calf muscle glycogen was measured using a 9-cm circular 13C coil and a 16-cm coplanar concentric proton coil, whereas forearm muscle glycogen concentration was measured using a 5.1-cm circular 13C coil with a 9 x 9 cm coplanar butterfly proton coil.
For thigh and calf muscle glycogen measurements, subjects were placed
in the 2.1T spectrometer in the supine position, with the volume of
interest (calf or thigh muscle) in the homogeneous region of magnet on
the top of the coil (calf muscle) or underneath it (thigh muscle). The
magnetic field was shimmed on nonlocalized water signal (usual
bandwidth at half peak height, 
40 Hz). Scout images were acquired to
position the volume of interest.13C spectra of
the thigh and calf muscles were obtained with a pulse-acquire sequence
in two 10-min blocks consisting of 5500 scans using a 90° pulse at
the coil center and a repetition time of 120 ms (38). Decoupling at a
power of 15 watts was applied at the glycogen C1 proton resonance
frequency during the 25.6-ms acquisition period. A 2-cm sphere
containing 13C-enriched formic acid was used as
pulse power and loading calibration between phantom and in
vivo measurements. The glycogen concentration was determined by
comparing the intensity of identically broadened peaks of each subject
vs. that in a phantom solution containing 150 mmol/L oyster
glycogen in a cast of the subject’s leg (calf muscle) or in a
rectangle container (thigh muscle). Spectra were line broadened, zero
filled, and manually phase corrected. The baseline was manually
corrected ±300 Hz, and the peak area was integrated ±150 Hz on either
side of the [1-13C]glycogen resonance. Thigh
muscle glycogen signal intensity was further corrected for the
sensitive volume of the 13C coil. An image of the
glycogen phantom solution was acquired using a dedicated proton coil of
the same size as the 13C coil (fully relaxed
gradient echo sequence with 90° excitation pulse). The sensitive
volume of the image was then compared to the set of images previously
recorded from each individual using the butterfly proton coil.
For measurements of forearm muscle glycogen, the right arm was
stretched into the magnet bore with the forearm muscle positioned
within the homogeneous volume of the magnet on top of the coil. The
magnetic field was shimmed on nonlocalized water signal (usual
bandwidth at half peak height, 50 Hz). Scout images were acquired to
position the volume of interest. The 13C spectra
of forearm muscles were obtained using a similar pulse sequence with
parameters adapted to the different (4.7-T) field strength (15). The
pulse-acquire sequence with a 90° pulse in the coil center was
applied; 2700 averages, with a repetition time of 120 ms and an
acquisition time of 87 ms were taken in 5.5 min (15). A 0.5-cm formate
sphere mounted in the coil center was used for pulse strength and
loading calibration. The absolute concentration of glycogen was then
calculated as described above.
The IMCL content was measured in the soleus muscle. Localized proton
NMR spectra were acquired on the 2.1-T/1-m BioSpec Products, Inc. system (Bruker Instruments, Inc.) by using a 16-cm circular
surface coil in a transmitter/receiver mode. The use of
1H NMR spectroscopy for the quantitation of IMCL
content was recently introduced (36) and validated in vivo
(37). Pulse sequence, data acquisition, and processing were used as
previously described (39). During the measurements, the subject
remained in the supine position within the spectrometer. The
gastrocnemius-soleus muscle complex of the right leg was positioned
within the homogeneous volume of the magnet on top of the coil. The
magnetic field was shimmed on nonlocalized water signal (usual
bandwidth, 40 Hz). Scout images were acquired to position the volume
of interest. The STEAM sequence (40) (echo time, 30 ms; repetition
time, 2 s; 128 averages; 2048 data points) complemented by a
spatially localized suppression pulse centered into the adipose tissue
layer was used on the volume of 1.5 x 1.5 x 1.5
cm3. Spectra were processed using the MacNuts-PPC
software package (AcornNMR, Inc., Fremont, CA). Spectra were
line broadened and phase and baseline corrected, and the resonances of
interest were quantified using a line-fitting procedure. After
correction for T1 and T2
relaxations, the quantitation of IMCL content was performed comparing
the intensity of (CH2)n=
(1.25 ppm) resonance to the water resonance intensity. The IMCL content
is expressed as the percentage of the intensity of the water
resonance.
Analytical procedures
Plasma concentrations of glucose and lactate were measured using a 2300 STAT Plus glucose and lactate analyzer (YSI, Inc., Yellow Springs, OH). Plasma immunoreactive insulin, glucagon, leptin, and ß-endorphin concentrations were measured using commercially available double antibody RIAs (insulin: Diagnostics Systems Laboratories, Inc., Webster, TX; glucagon: ICN Biomedicals, Inc., Costa Mesa, CA; leptin: Linco Research, Inc., St. Louis, MO; ß-endorphin: Nichols Institute Diagnostics, San Juan Capistrano, CA). Plasma concentrations of free fatty acid (FFA) were determined using a microfluorimetric method. Plasma creatine phosphokinase activity was measured using a colorimetric method (Sigma, St. Louis, MO). Oxygen consumption and CO2 production were measured using breath by breath indirect calorimetry (Vmax29 Metabolic Monitor, Sensomedics, CA).
Data analysis
Data are presented as the mean ± SEM. Statistical analysis was performed using one-way repeated measures ANOVA to analyze time-course changes in im glycogen concentration, IMCL content, and plasma metabolite and hormone concentrations. Two-way repeated measures ANOVA was used to analyze time-course differences in im glycogen concentrations among different muscle groups. In the case of significant differences over the time course, post-hoc comparisons were made using Fisher’s protected least significant difference test. Differences were considered significant at P < 0.05.
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Results |
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All of the subjects completed three or four bouts of exercise. The mean total length of the run until exhaustion was 25.5 ± 1.8 km in 146.2 ± 6.6 min. Exhaustion was defined by the subject’s inability to maintain his pace. Oxygen consumption averaged 67.4 ± 0.9% of the VO2 peak over the entire time of the exercise protocol, and the RER decreased slowly from 0.89 ± 0.02 in the first 10 min to 0.82 ± 0.02 (P < 0.005) at the end of exercise.
Metabolic and hormonal data
Time-course changes in plasma glucose, lactate, insulin, FFA,
glucagon, ß-endorphin, and leptin are summarized in Figs. 1
and 2. The plasma
glucose concentration (Fig. 1A) rose slightly from 4.66 ± 0.15
mmol/L at baseline to 5.53 ± 0.25 mmol/L (P <
0.05 vs. baseline) after the first bout of exercise.
Afterward it decreased during exercise and reached a nadir of 4.25
± 0.12 mmol/L (P < 0.0001 vs. first
exercise bout; P < 0.05 vs. baseline) by 60
min of the recovery period. Plasma glucose further decreased below
baseline during the first 4 h of recovery (P <
0.05 for first four recovery data points) and reached the fasting
concentration of 5.09 ± 0.10 mmol/L at 0600 h next day
(P = NS vs. baseline; P <
0.01 vs. 60 min of recovery).
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) rose continuously during the
exercise, from 0.27 ± 0.04 mmol/L before exercise to 1.25 ±
0.19 mmol/L (P < 0.0001) after the third bout of
exercise, increased further to 1.62 ± 0.26 mmol/L during the
first hour of recovery (P < 0.0001 vs.
baseline), and then slowly declined to 1.10 ± 0.19 mmol/L during
the next 4 h of recovery (P < 0.05 vs.
60 min of recovery). After the overnight fast, the plasma FFA
concentration returned to baseline values (0.40 ± 0.06 mmol/L;
P = NS vs. baseline; P <
0.0001 vs. 60 min of recovery).
The plasma lactate concentration (Fig. 1C) increased during the first
bout of exercise from 1.09 ± 0.11 to 2.38 ± 0.50 mmol/L
(P < 0.001), then decreased but remained elevated
during the exercise period and decreased quickly to fasting values of
approximately 1 mmol/L during the first 60 min of recovery and remained
lower than that during exercise during the whole recovery period
(P < 0.05 for each recovery time point vs.
all three exercise time points).
Plasma insulin concentrations (Fig. 2A) decreased from 50 ± 4
pmol/L at baseline to 31 ± 2 pmol/L after the first bout of
exercise (P < 0.005 vs. baseline) and
20 ± 2 pmol/L after the third bout of exercise (P
< 0.0001 vs. baseline). The insulin concentration remained
lower during the first 5 h of recovery (P < 0.05
for all recovery time point vs. baseline). After the 18-h
recovery period plasma insulin concentrations were back to baseline
values (P < 0.001 for all first five recovery time
points vs. 18 h of recovery time point).
Plasma glucagon concentrations (Fig. 2B) increased from 50.7 ±
7.1 pg/dL at baseline to 102.6 ± 20.1 pg/dL by the end of
exercise (P < 0.005) and decreased to approximately 70
pg/dL by 60 min of recovery (P < 0.05 for all recovery
time points vs. the end of exercise), then remained stable
during the first 5 h of the recovery period. After refeeding and
overnight fasting, plasma glucagon concentrations had reached the
baseline value (52.7 ± 7.8 pg/dL; P = NS
vs. baseline; P < 0.005 vs. end
of exercise).
The plasma leptin concentration (Fig. 2C) rose only slightly from
2.8 ± 0.5 µg/dL at baseline to 3.2 ± 0.7 µg/dL after
the first 45 min of exercise (P = NS) and then steadily
declined during the remaining time of exercise and recovery. The value
at 5 h of recovery (1.7 ± 0.5 µg/dL) was lower than that
after the first bout of exercise (P < 0.05). After
dinner and 12-h overnight recovery, the plasma leptin concentrations
returned to baseline. To exclude the impact of gender on leptin
concentration variability, only the data from the male subjects were
evaluated (41, 42).
Although no changes in serum ß-endorphin concentrations were observed
after the first two exercise bouts (Fig. 2D), ß-endorphin increased
to 59.5 ± 14.7 pg/mL at the time of exhaustion (P
< 0.001 vs. baseline). A rapid decrease to 10.7 ± 1.3
pg/mL was observed during the first 5 h of recovery
(P < 0.0001 for all recovery time points
vs. end of exercise; P = NS vs.
baseline and first two bouts of exercise).
As a result of apparent muscle damage through running, exercise increased the blood plasma creatine phosphokinase concentration from 8 ± 1 U/mL in the basal state to 15 ± 3 U/mL at the time of exhaustion, 18 ± 3 U/mL at 1 h, and 23 ± 5 U/mL at 5 h postexercise.
Skeletal muscle glycogen
Time-course changes in intramuscular glycogen concentrations in
different muscle groups during the exercise and recovery protocol are
summarized in Fig. 3A. Mean baseline glycogen
concentrations were 72.9 ± 4.7 mmol/L in the thigh, 83.4 ±
4.3 mmol/L in the calf, and 83.2 ± 6.5 mmol/L in the forearm
muscle.
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The thigh muscle glycogen concentration increased to 75% of the resting level after 4–5 h of recovery (P < 0.005 vs. baseline), whereas almost no resynthesis of calf muscle glycogen content was measured. A subsequent decrease in glycogen concentration to 73% of the resting level was measured in the forearm muscle (P < 0.05 vs. baseline) at this time point.
After 18 h of recovery, glycogen concentrations increased to 81% (P < 0.05 vs. baseline; P < 0.05 vs. end of the exercise), 67% (P < 0.001 vs. baseline; P < 0.005 vs. end of the exercise), and 81% (P = NS) of the resting levels in the thigh, calf, and forearm muscle, respectively.
One-way repeated measures ANOVA analysis confirmed that all three muscle glycogen profiles are time dependent (arm, P = 0.0001; thigh and calf, P < 0.0001). Two-way repeated measures ANOVA analysis revealed that all three glycogen profiles are different from each other (arm/calf, P < 0.0001; arm/thigh, P < 0.005; thigh/calf, P < 0.0001).
In the control study (n = 3) the glycogen concentration in all three studied muscle groups did not change significantly. Over the course of a 12-h fast glycogen concentrations varied from 81.9 ± 11.8 to 73.2 ± 11.3 mmol/L, from 92.3 ± 10.9 to 89.9 ± 13.3 mmol/L, and from 68.9 ± 7.1 to 70.8 ± 10.4 mmol/L in the thigh, calf, and forearm muscle groups, respectively.
IMCL
Time-course changes in IMCL content during the exercise and
recovery protocols are summarized in Fig. 3B. Running for 2–3 h
resulted in a decrease in IMCL
(CH2)n= resonance from
1.37 ± 0.14% of water resonance peak intensity in the basal
state to 0.91 ± 0.09% of water resonance peak intensity
(P < 0.05 vs. baseline). During the
recovery period the IMCL content returned to 1.15 ± 0.11% after
about 4 h and to 1.23 ± 0.15% (P = NS
vs. baseline) after 17 h of recovery. A similar pattern
was observed by using the CH3- resonance peak
intensity of IMCL for quantitation. The decrease observed at the end of
exercise was also significant in this case (P < 0.05).
One-way repeated measures ANOVA analysis confirmed that both IMCL
profiles are time dependent
[(CH2)n= resonance,
P < 0.001; CH3- resonance,
P < 0.001], whereas two-way repeated measures ANOVA
analysis found no differences between these two profiles. Comparing
soleus IMCL content and leg glycogen concentration time courses
revealed a significant difference only in the case of the calf muscle
glycogen (P < 0.05, by two-way repeated measures
ANOVA).
In the control study the IMCL content in soleus muscle remained unchanged [1.02 ± 0.21% of water resonance peak intensity at baseline vs. 1.11 ± 0.20% of water resonance peak intensity at 12 h fast for the (CH2)n= resonance).
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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These data also demonstrate that glycogen depletion is different in various working muscle groups and that it may not be the major limiting factor for exercise performance. All of the subjects terminated the exercise due to physical exhaustion, although significant glycogen concentrations (>30 mM) were left in the active muscle groups (calf and thigh). Together with psychological fatigue, obvious muscle damage caused by running plays a role in the onset of exhaustion (17, 18). Consistent with this latter possibility, we observed a 3-fold increase in plasma creatine phosphokinase concentrations. In addition, differences in absolute glycogen depletion reflect differences in the relative workloads for active muscle groups during level running (43). The difference in the grade of depletion found in this study is in good agreement with the results of the only invasive study on this topic (7), which showed that glycogen depletion after level running is more pronounced in the gastrocnemius than in the vastus lateralis muscle.
The observed low rates of glycogen resynthesis (calf, 0.5 mmol/L·h; thigh, 2.9 mmol/L·h) during the first 5 h of recovery compared to other postexercise studies performed under hyperinsulinemic/hyperglycemic conditions (Ref. 15, 15 .8 mmol/L·h; Ref. 44, 7 .2 mmol/L·h) can probably be explained by low plasma glucose and insulin concentrations as well as by damaged muscle cell structure resulting from exercise.
The forearm glycogen measurements demonstrate a significant decrease in
glycogen content throughout the first part of the recovery period,
whereas thigh and calf muscles replenished their glycogen stores. These
data suggest that there is transfer of glycogen by the
glucoselactate and the glucosealanine cycle from the resting
muscle (forearm) to recovering muscles (thigh and calf) and are
consistent with the arterio-venous balance studies of Wahren et
al. that demonstrated a net release of lactate and alanine from
the resting muscles after exercise (3, 22, 23, 24, 25, 26).
We also assessed IMCL utilization in the calf muscles during exercise using a novel 1H NMR approach (36, 37, 39) and demonstrated a significant decrease in IMCL content after 2–3 h of exercise. These are the first data, to our knowledge, demonstrating the utilization of IMCL during exercise noninvasively and are consistent with the respiratory exchange ratio data showing a progressive shift toward increased fat oxidation with increasing duration of exercise. No measurements of thigh muscle IMCL content were performed because of time resolution constraints. However, Costill et al. reported an approximately 30% decrease in the vastus lateralis triglyceride content during prolonged submaximal running (43). These data are in contrast to the recent study of Rico-Sainz et al. (34), which found no change in IMCL content in the muscle after exercise using 1H NMR spectroscopy. It is likely that these differences can be explained by the different type, intensity, and duration of the exercise protocols.
In summary, we found, using 13C and
1H NMR spectroscopy techniques to noninvasively
measure muscle glycogen and IMCL content during a prolonged submaximal
running protocol and subsequent recovery, 1) significantly greater
muscle glycogen utilization in the calf muscle group than in the thigh
muscle group, 2) significant utilization of IMCL in the soleus muscle,
and 3) a decrease in glycogen content in nonexercising muscle and an
increase in glycogen content in recovering muscles during the
postexercise phase. These latter data are consistent with the
hypothesis that there is transfer of glycogen by the glucoselactate
and the glucosealanine cycle from the resting muscle (forearm) to
recovering muscles (thigh and calf) after running exercise.
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Acknowledgments |
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Footnotes |
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2 On leave from the Institute for Medical Physics, University of
Vienna, Austria and supported by the Joseph Skoda Award 1996 from the
Austrian Society for Internal Medicine and the Austrian National Bank
(ÖNB Grant 6438) (both awarded to M.R.).
3 Recipient of NIH Clinical Associate Physician Award
PA-90–30-CAP.
4 Investigator with the Howard Hughes Medical Institute.
Received July 8, 1999.
Revised September 15, 1999.
Accepted October 27, 1999.
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|
|
B. H Goodpaster, V A. Stenger, F. Boada, T. McKolanis, D. Davis, R. Ross, and D. E Kelley Skeletal muscle lipid concentration quantified by magnetic resonance imaging Am. J. Clinical Nutrition, May 1, 2004; 79(5): 748 - 754. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Neumann-Haefelin, A. Beha, J. Kuhlmann, U. Belz, M. Gerl, M. Quint, G. Biemer-Daub, M. Broenstrup, M. Stein, E. Kleinschmidt, et al. Muscle-Type Specific Intramyocellular and Hepatic Lipid Metabolism During Starvation in Wistar Rats Diabetes, March 1, 2004; 53(3): 528 - 534. [Abstract] [Full Text] [PDF]
|
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 S. R. Stannard and N. A. Johnson Insulin resistance and elevated triglyceride in muscle: more important for survival than 'thrifty' genes? J. Physiol., February 1, 2004; 554(3): 595 - 607. [Abstract] [Full Text] [PDF]
|
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L. J. White, M. A. Ferguson, S. C. McCoy, and H. Kim Intramyocellular Lipid Changes in Men and Women during Aerobic Exercise: A 1H-Magnetic Resonance Spectroscopy Study J. Clin. Endocrinol. Metab., December 1, 2003; 88(12): 5638 - 5643. [Abstract] [Full Text] [PDF]
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V. B. Schrauwen-Hinderling, L. J. C. van Loon, R. Koopman, K. Nicolay, W. H. M. Saris, and M. E. Kooi Intramyocellular lipid content is increased after exercise in nonexercising human skeletal muscle J Appl Physiol, December 1, 2003; 95(6): 2328 - 2332. [Abstract] [Full Text]
|
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L. J. C. van Loon, V. B. Schrauwen-Hinderling, R. Koopman, A. J. M. Wagenmakers, M. K. C. Hesselink, G. Schaart, M. E. Kooi, and W. H. M. Saris Influence of prolonged endurance cycling and recovery diet on intramuscular triglyceride content in trained males Am J Physiol Endocrinol Metab, October 1, 2003; 285(4): E804 - E811. [Abstract] [Full Text] [PDF]
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 S. K. Gan, A. D. Kriketos, B. A. Ellis, C. H. Thompson, E. W. Kraegen, and D. J. Chisholm Changes in Aerobic Capacity and Visceral Fat but not Myocyte Lipid Levels Predict Increased Insulin Action After Exercise in Overweight and Obese Men Diabetes Care, June 1, 2003; 26(6): 1706 - 1713. [Abstract] [Full Text] [PDF]
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V. B. Schrauwen-Hinderling, P. Schrauwen, M. K. C. Hesselink, J. M. A. van Engelshoven, K. Nicolay, W. H. M. Saris, A. G. H. Kessels, and M. E. Kooi The Increase in Intramyocellular Lipid Content Is a Very Early Response to Training J. Clin. Endocrinol. Metab., April 1, 2003; 88(4): 1610 - 1616. [Abstract] [Full Text] [PDF]
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), calf (
), and forearm (
) muscle
groups. B, Time course of IMCL depletion and repletion in the
soleus muscle. The results of the quantitation using the
(CH2)n= group resonance (