Glucose uptake patterns in exercised skeletal muscles of elite male long-distance and short-distance runners.

Abstract

The aim of this study was to determine glucose uptake patterns in exercised skeletal muscles of elite male long-distance and short-distance runners. Positron emission tomography (PET) using 18F-fluoro-2-deoxyglucose (FDG) was performed to determine the patterns of glucose uptake in lower limbs of short-distance (SD group, n=8) and long-distance (LD group, n=8) male runners after a modified 20 min Bruce treadmill test. Magnetic resonance imaging (MRI) was used to delineate the muscle groups in lower limbs. Muscle groups from hip, knee, and ankle movers were measured. The total FDG uptake and the standard uptake value (SUV) for each muscle group were compared between the 2 groups. For the SD and LD runners, the 2 major muscle groups utilizing glucose during running were knee extensors and ankle plantarflexors, which accounted for 49.3 +/- 8.1% (25.1 +/- 4.7% and 24.2 +/- 6.0%) of overall lower extremity glucose uptake for SD group, and 51.3 +/- 8.0% (27.2 +/- 2.7% and 24.0 +/- 8.1%) for LD group. No difference in muscle glucose uptake was noted for other muscle groups. For SD runners, the SUVs for the muscle groups varied from 0.49 +/- 0.27 for the ankle plantarflexors, to 0.20 +/- 0.08 for the hip flexor. For the LD runners, the highest and lowest SUVs were 0.43 +/- 0.15 for the ankle dorsiflexors and 0.21 +/- 0.19 for the hip. For SD and LD groups, no difference in muscle SUV was noted for the muscle groups. However, the SUV ratio between the ankle dorsiflexors and plantarflexors in the LD group was significantly greater than that in the SD group. We thus conclude that the major propelling muscle groups account for approximately 50% of lower limb glucose utilization during running. Thus, the other muscle groups involving maintenance of balance, limb deceleration, and shock absorption utilize an equal amount. This result provides a new insight into glucose distribution in skeletal muscle, suggesting that propellers and supporters are both energetically important during running. Furthermore, for each unit muscle volume, movers of ankle are more glucose-demanding than those of hip.

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Corresponding author: Chi-Hsien Chen, M.D., Ph.D., Department of Physical Medicine and Rehabilitation, Taipei Medical University-Wan
Fang Hospital, Taipei 11696, Taiwan, Republic of China. Fax: +886-2-29333025, E-mail: chihsen.chen@msa.hinet.net
Received: February 26, 2009; Revised: May 3, 2009; Accepted: July 17, 2009.
2010 by The Chinese Physiological Society. ISSN : 0304-4920. http://www.cps.org.tw
Chinese Journal of Physiology 53(×): ×××-×××, 2010
DOI: 10.4077/CJP.2010.AMK016
1
Glucose Uptake Patterns in Exercised Skeletal
Muscles of Elite Male Long-Distance and
Short-Distance Runners
Suh-Jun Tai, Ren-Shyan Liu, Ya-Chen Kuo, Chi-Yang Hsu, and Chi-Hsien Chen
Department of Physical Medicine and Rehabilitation
Taipei Medical University-Wan Fang Hospital
Taipei 11696, Taiwan, Republic of China
Abstract
The aim of this study was to determine glucose uptake patterns in exercised skeletal muscles of
elite male long-distance and short-distance runners. Positron emission tomography (PET) using 18F-
fluoro-2-deoxyglucose (FDG) was performed to determine the patterns of glucose uptake in lower limbs
of short-distance (SD group, n = 8) and long-distance (LD group, n = 8) male runners after a modified
20 min Bruce treadmill test. Magnetic resonance imaging (MRI) was used to delineate the muscle groups
in lower limbs. Muscle groups from hip, knee, and ankle movers were measured. The total FDG uptake
and the standard uptake value (SUV) for each muscle group were compared between the 2 groups. For
the SD and LD runners, the 2 major muscle groups utilizing glucose during running were knee extensors
and ankle plantarflexors, which accounted for 49.3 ± 8.1% (25.1 ± 4.7% and 24.2 ± 6.0%) of overall lower
extremity glucose uptake for SD group, and 51.3 ± 8.0% (27.2 ± 2.7 and 24.0 ± 8.1%) for LD group. No
difference in muscle glucose uptake was noted for other muscle groups. For SD runners, the SUVs for
the muscle groups varied from 0.49 ± 0.27 for the ankle plantarflexors, to 0.20 ± 0.08 for the hip flexor.
For the LD runners, the highest and lowest SUVs were 0.43 ± 0.15 for the ankle dorsiflexors and 0.21 ±
0.19 for the hip. For SD and LD groups, no difference in muscle SUV was noted for the muscle groups.
However, the SUV ratio between the ankle dorsiflexors and plantarflexors in the LD group was
significantly greater than that in the SD group. We thus conclude that the major propelling muscle
groups account for ~50% of lower limb glucose utilization during running. Thus, the other muscle
groups involving maintenance of balance, limb deceleration, and shock absorption utilize an equal
amount. This result provides a new insight into glucose distribution in skeletal muscle, suggesting that
propellers and supporters are both energetically important during running. Furthermore, for each unit
muscle volume, movers of ankle are more glucose-demanding than those of hip.
Key Words: FDG, PET, muscle recruitment, glucose uptake, exercise
Introduction
Slow twitch (ST) muscle fibers and fast twitch
(FT) fibers are mixed in a muscle, with different
ratios in different muscles. For example, the average
cross section areas of ST fibers are 43.5% and 73.4%
for the surface of the lateral head of gastrocnemius
and the surface of the tibialis anterior muscles, re-
spectively, in young male adults (10). However, the
mixing ratio varies with subjects. It has also been
demonstrated that endurance athletes have predom-
inantly ST fiber populations in their gastrocnemius
and vastus lateralis muscles, whereas strength athletes
have a higher percentage of FT fibers (1). In addi-
tion, endurance training improves exercise perfor-
mance through the increase of muscle GLUT-4 content
CJP E-prepublication Ahead of Print

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Tai, Liu, Kuo, Hsu and Chen
and hexokinase activity, and the decrease of muscle
glucose-6-phosphatase activity. All of these adap-
tations lead to enhanced glucose uptake and phospho-
rylation (2, 7, 16).
Because electromyography and magnetic reso-
nance imaging (MRI) techniques, which have been
used to analyze the in vivo motion and contraction of
skeletal muscle (4, 13), are not useful for evaluating
muscle metabolism, positron emission tomography
(PET) with [18F]-fluorodeoxyglucose (FDG) has been
employed to determine metabolic activity of the domi-
nant side and posterior compartment of legs in runners
by Tashiro and colleagues (17). Recently, Ohnuma
et al. investigated glucose uptake during a dash with
FDG-PET, and found that “posterior thigh muscles
were especially active” (15).
Since running is a basic skill of almost all ath-
letes, which requires combined and accurately coor-
dinated muscle contraction in every stride (17), the
purpose of this study was to investigate if the glucose
uptake pattern of the leg muscles differs between
long-distance (LD) and short- distance (SD) runners
at relatively higher exercise intensity. We hypothe-
sized that glucose uptake is higher in LD runners
because of their more abundant ST fibers and intense
endurance training.
Materials and Methods
Subjects
Sixteen healthy young male elite short-distance
(SD) (n = 8) and long-distance (LD) (n = 8) runners
participated in the study. Most of the LD runners
were competing in men’s 5,000 meter or 10,000 meter
runs, while the SD runners were competing in men’s
110 meter hurdles. The demographic data of the
runners are presented in Table 1. Written informed
consent was obtained after the nature, purpose, and
potential risks of the study were explained to the
subjects. The study protocol was performed in ac-
cordance with Declaration of Helsinki and approved
by the Institute of Research Board of the Taipei
Medical University-Wan Fang Hospital.
Exercise Protocol
Every subject was fasting for at least 8 h before
the exercise testing. A cup of 18F-FDG solution (ra-
dioactivity approximately 0.5 MBq/subject/kg) was
ingested (5, 14) as fast as possible by each subject
immediately before a Bruce Multistage Continuous
Protocol (8) on a treadmill (Takasuma X-fit 7; Chi-
Tai Health, Kaohsiung, Taiwan, ROC) under the
supervision of a licensed physical therapist (PT). The
test was modified so that the total test duration was 20
min, but the speed and slope remained the same if the
subject felt uncomfortable to go to the next stage. A
one minute cool down was allowed after the test, and
then the subject rested in the supine position for 59
min before the PET scan.
FDG-PET
Multiple-frame step and pelvis-to-ankle PET
imaging was performed using a dedicated PET scanner
(SCANDITRONIX 4096 15WB Plus; General Electric,
Milwaukee, WI, USA) with a 97.5 mm axial FOV.
The acquisition time for each step was 5 min. Trans-
mission scan then was done with the same area of the
emission scan. All image data were reconstructed by
a vendor-provided iterative reconstruction algorithm
with correction of transmission scan.
MRI
One subject who had the nearest body weight
and height to the average weight and height of all
subjects was also scanned in a supine position in a
1.5 T Horizon scanner (General Electric) using a
standard body coil with conventional T1-weighted
spin echo MR pulse sequences. Continuous 4 mm
axial slices were taken from the iliac crest to just
below the ankle. Each display matrix was 256 × 256
Table 1. Basic information of the runners
Runner Group NumberAge
(year)
Body Height
(cm)†
Body Weight
(kg)*
FDG Taken
(M Bq)
Treadmill
Protocol
Completed*
100.0 ± 0.0%Long-Distance
Runner
Short-Distance
Runner
*Statistically significant difference found between the two runner groups.
†P < 0.1 found for the corresponding values between the two runner groups.
8 22.4 ± 3.2171.0 ± 5.759.9 ± 5.132.8 ± 4.7
821.0 ± 1.5 176.6 ± 5.071.8 ± 6.034.4 ± 6.0 88.0 ± 7.5%

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Muscle Glucose Uptake in Elite Male Runners
3
with a pixel size of 1.56 × 1.56 mm.
Image Procedures
Both the reconstructed PET and MRI data were
transferred to a personal computer in native and
DICOM (Digital Imaging and Communications in
Medicine) format, respectively. The multi-frame
images were then stacked together and converted to
the Mayo Clinic Analyze 7.5 format by programs
written by one of the authors (C-H Chen) using IDL
6.3 (available from ITT Corporation, White Plains,
NY, USA). In addition, PET images were decay-
corrected to the start of the first scan step.
The MRI image set (Fig. 1) was first manually
registered to the PET image set with a public-domain
medical image processing tool, AMIDE (12), by a PT.
The amount of FDG uptake in different muscle groups
for each subject were then manually analyzed with
AMIDE based on the registered MRI image set by the
same PT, as shown in Fig. 2. The muscle groups
included the extensors and flexors of the hips and
knees, the abductors and adductors of the hips, ankle
dorsiflexors, and ankle plantarflexors. The muscles
included in each muscle group are listed in Table 2.
Statistical Analyses
Two-tailed t-test was applied on demographic
data, percentage FDG (%FDG) uptake, standard
uptake value (SUV), and antagonist ratios. The SUV
is the most often used PET index, and is described
elsewhere (11, 17). The antagonist ratios are ratios
between absolute FDG uptake in MBq of hip adductors
coronal 1
transverse 1
sagittal 1
Fig. 1. An example of muscle group delineation from the magnetic resonance (MR) image set. A manually drawn region of interest
(ROI) for the ankle plantar flexor group is shown in white. The interface of AMIDE shows, from left to right, axial, coronal,
and sagital views of the lower legs of a subject.
coronal 1
transverse 1
sagittal 1
Fig. 2. The registered MR and PET image sets of the same subject shown in Fig. 1 are presented in a gray and red color spectrum,
respectively. The manually drawn ROI of the ankle plantar flexor group is also shown in white as in Fig. 1.

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Tai, Liu, Kuo, Hsu and Chen
and abductors, hip flexors and extensors, knee flexors
and extensors, and ankle dorsiflexors and plantar-
flexors. We also applied two-way analysis of variance
(ANOVA) using a free statistical software program,
R (18). The two factors were joint mover and sport
type. The former had 8 levels (hip adductor, hip
abductor, hip flexor, hip extensor, knee flexor, knee
extensor, ankle dorsiflexor, and ankle plantarflexor),
while the latter had only 2 levels (SD and LD).
Therefore, it was an 8 × 2 factorial experimental
design. We applied the analysis to both %FDG and
SUV to see if any of the factors had a significant
effect on them. If a factor was shown to have a
significant effect, the different effects among different
levels of that factor were checked by the Tukey test
(19), again, using the freeware R. Data were presented
as mean ± standard deviation (SD) or number and
percent. A P value of < 0.05 was considered to in-
dicate statistical significance.
Results
The mean body weight of the LD group was
significantly different than that of the SD group
(59.9 ± 5.1 kg vs. 71.8 ± 6.0 kg, respectively, P <
0.05). There were no statistical differences in the
comparison of other demographic data between the
2 groups (Table 1). Although there appears to be a
difference in body height (171.0 ± 5.7 cm vs. 176.6 ±
5.0 cm), there was only a “weak” difference (P < 0.1).
[Note: This is not really appropriate or correct. If P
is set as < 0.05, and P value of the comparison is not
below that level, then there is no difference. The term
“weak” difference is not accurate or appropriate.
The percent of runners completing the Bruce
treadmill protocol (100.0 ± 0.0 LD vs. 88.0 ± 7.5%
SD) was significantly different (P < 0.05). Data are
presented in Table 1. The data of the completion of
the treadmill protocol for the SD group implies that
most SD runners reached 16% or more inclination,
and all of them reached an inclination of at least 14%.
For those who completed the protocol, the estimated
VO2 was approximately 60 ml/kg/min. The VO2 for
those who reached inclinations of 14% and 18% was
approximately 35 ml/kg/min and 52 ml/kg/min (also
the average for SD group), respectively.
The absolute and relative FDG uptake, the SUV,
and the antagonist ratio for each muscle group are
shown in Tables 3 and 4 for LD and SD runners,
respectively. Table 3 indicates that the FDG uptake
of the knee extensors and ankle plantarflexors for the
LD group are 632 ± 246 kBq (27.2 ± 2.7% of the total
FDG uptake of the 8 joint movers) and 508 ± 86 kBq
(24.0 ± 8.1%), respectively. For SD runners, these
values are 597 ± 321 kBq (25.1 ± 4.7%) and 584 ± 367
kBq (24.2 ± 6.0%), as shown in Table 4. The sum
of knee extensor and ankle plantarflexor %FDG up-
take for the LD and SD groups are 51.3 ± 8.0% and
49.3 ± 8.1%, respectively. The FDG uptake for the
other muscle groups in descending order are knee
flexor, hip extensor, hip adductor, hip abductor, ankle
dorsiflexors, and hip flexor, as shown in Tables 3 and
4, and Fig. 3. Using the two-tailed t-test, no statistical
differences in muscle glucose uptake and antagonist
Table 2. Muscles in each muscle group
Joint
Hip
Abductor
Gluteus
medius
Gluteus
minimus
Piriformis
Adductor
Adductor magnus
Adductors brevis
Adductor longus
Pectineus
Gracilis
Extensor/Plantarflex
Gluteus maximus
Flexor/Dorsiflexor
Psoas major
Iliacus
Tensor fasciae latae
Adductor brevis
Adductor longus
Pectineus
KneeRectus femoris
Vastus intermedius
Vastus lateralis
Vastus medialis
Biceps femoris
Semimembranosus
Semitendinosus
AnkleGastrocnemius
Peroneus brevis
Peroneus longus
Plantaris
Soleus
Tibialis posterior
Tibialis anterior
The ankle plantarflexors are considered extensors and the dorsiflexors flexors.

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Muscle Glucose Uptake in Elite Male Runners
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FDG ratio were found for any muscle groups or
ratios between the 2 runner groups. This result is also
supported by the two-way ANOVA results. The
significant factor that determines FDG uptake in a
muscle group is the different joint movers (P <
0.001), as shown in Fig. 3, and not the different type
of running. Note Fig. 3 indicates median and quartiles
instead of mean and standard deviation. The Tukey
test showed that the %FDG of hip flexors was sig-
nificantly lower than that of hip extensors, knee
flexors, ankle plantarflexors, and knee extensors.
There was no statistical difference of %FDG among
other muscle group pairs.
The SUV for each muscle group, as shown in
Tables 3 and 4, falls between 0.21 ± 0.19 (hip flexor)
and 0.43 ± 0.15 (ankle dorsiflexor) for LD runners,
while values for SD runners are 0.20 ± 0.08 (hip
flexor) and 0.49 ± 0.27 (ankle plantarflexor). Note
that the highest muscle group SUV is different for the
2 groups. However, the two-tailed t-test failed to
show a significant difference of SUV for any muscle
groups between the 2 groups of runners. Two-way
ANOVA testing again revealed that the significant
factor affecting SUV in a muscle group was the
different joint movers (P < 0.001), instead of the type
of running.
Figure 4 shows the combined SUV for each
muscle group for all the subjects. The Tukey test
showed that the SUVs of both ankle dorsiflexors and
plantarflexors were significantly higher than that of
hip flexors. No statistical difference in SUV was
found between other muscle group pairs. However,
the P values of the comparison between the SUVs of
hip extensors and the ankle movers were < 0.1.
Table 4. The FDG uptake pattern of short-distance runners
Joint MoversFDG Uptake
(kBq)
201 ± 98
184 ± 114
44 ± 19
237 ± 126
342 ± 179
597 ± 321
78 ± 50
584 ± 367
2,267 ± 1,214
FDG Uptake
(%)
8.6 ± 1.3%
7.7 ± 3.5%
2.0 ± 0.5%
10.2 ± 1.6%
14.1 ± 3.3%
25.1 ± 4.7%
3.3 ± 0.8%
24.2 ± 6.0%
Antagonists FDG
Ratio
1.3 ± 0.5
SUV Antagonists
SUV Ratio
1.1 ± 0.4 Hip Adductor
Abductor
Flexor
Extensor
0.29 ± 0.12
0.30 ± 0.18
0.20 ± 0.08
0.26 ± 0.12
0.35 ± 0.16
0.33 ± 0.15
0.42 ± 0.24
0.49 ± 0.27
0.2 ± 0.00.8 ± 0.2
KneeFlexor
Extensor
0.6 ± 0.1 1.1 ± 0.2
AnkleDorsiflexor
Plantarflexor
0.1 ± 0.0†
0.9 ± 0.2*
Total
FDG: 18F-fluror-2-deoxy glucose SUV: standard uptake value.
*Statistically significant difference (P < 0.05) found for the corresponding values between the two runner groups.
†P < 0.1 found for the corresponding values between the two runner groups.
Table 3. The FDG uptake pattern of long-distance runners
Joint MoversFDG Uptake
(kBq)
214 ± 98
187 ± 175
53 ± 46
290 ± 142
332 ± 149
632 ± 246
90 ± 25
508 ± 86
2,307 ± 816
FDG Uptake
(%)
9.2 ± 1.7%
7.0 ± 4.9%
2.0 ± 1.4%
12.2 ± 4.5%
14.0 ± 1.9%
27.2 ± 2.7%
4.4 ± 2.2%
24.0 ± 8.1%
Antagonists FDG
Ratio
2.3 ± 1.9
SUVAntagonists
SUV Ratio
2.1 ± 1.7HipAdductor
Abductor
Flexor
Extensor
0.26 ± 0.08
0.26 ± 0.27
0.21 ± 0.19
0.27 ± 0.14
0.30 ± 0.14
0.30 ± 0.10
0.43 ± 0.15
0.38 ± 0.08
0.1 ± 0.10.6 ± 0.5
KneeFlexor
Extensor
0.5 ± 0.11.0 ± 0.2
AnkleDorsiflexor
Plantarflexor
0.2 ± 0.0†
1.1 ± 0.2*
Total
FDG: 18F-fluror-2-deoxy glucose SUB: standard uptake value.
*Statistically significant difference (P < 0.05) found for the corresponding values between the two runner groups.
†P < 0.1 found for the corresponding values between the two runner groups.