Carbohydrate Intake and Muscle Soreness / 171
International Journal of Sport Nutrition and Exercise Metabolism, 2004, 14, 171-184
© 2004 Human Kinetics Publishers, Inc.
Inadequate Carbohydrate Intake Following
Prolonged Exercise Does Not Increase Muscle
Soreness After 15 Minutes of Downhill Running
Matthew R. Nelson, Robert K. Conlee,
and Allen C. Parcell
In Delayed Onset Muscle Soreness (DOMS), muscles become sore 24 to 48
hours after eccentric and unaccustomed activity. Fiber stiffness, due to decreased muscle glycogen, may predispose muscle to greater damage during
eccentric exercise. This study sought to determine if inadequate carbohydrate
intake following a protocol to decrease muscle glycogen would increase DOMS
after 15 min of downhill running. Thirty-three male subjects (age, 18–35 years)
were randomized into 3 groups for testing over a 7-day period. The depletion
(DEP) group (n = 12) underwent a glycogen depletion protocol prior to a 15min downhill run designed to induce DOMS. The repletion (FED) group (n =
10) underwent a glycogen depletion protocol followed by a carbohydrate repletion protocol (>80% CHO) prior to downhill running. The third (ECC) group
(n = 11) performed only the downhill running protocol. Subjective muscle
soreness, isometric force production, relaxed knee angle, and thigh circumference were measured pretreatment and on days 1, 2, 3, 4, and 6 post treatment.
Subjective muscle soreness for all groups increased from 0 cm pretreatment to
3.05 ± 0.72 cm (on a 10-cm scale) on day 1 post treatment (p < .05). All groups
were significantly different from baseline measurements until day 4 post treatment. Each group experienced a decline in isometric force from 281 ± 45 N preto 253 ± 13 N on day 1 post treatment (p < .05). The decrease in isometric force
persisted in all groups for 4 days post treatment. Increases in thigh circumference and relaxed knee angle elevations in all 3 groups were statistically different (p < .05) from pretreatment until day 4. No differences were noted between
groups for any of the parameters examined. In the current study, 15 min of
downhill running is sufficient to cause DOMS with the associated functional
and morphological changes; however, inadequate carbohydrate intake after a
glycogen depleting exercise does not appear to exacerbate DOMS and the
associated symptoms.
Key Words: muscle damage, carbohydrate, DOMS
Introduction
Delayed onset muscle soreness (DOMS) is the muscular pain that occurs 24 to 48
hours following eccentric and unaccustomed activity of moderate intensity and
The authors are with the Human Performance Research Center at Brigham Young
University, Provo, UT 84602.
171
172 / Nelson, Conlee, and Parcell
duration (24). Muscles exhibit warmth, become painful to the touch, and swell, and
joints undergo a decreased range of motion (7, 18). Histological preparations from
muscle biopsy samples show mechanical damage as revealed by Z-band streaming
and disruption of the A-band in muscle fibers (15, 16, 27). Myoproteins increase in
the plasma (3), and an inflammatory response occurs in the damaged muscle fibers
(18, 35).
As common as DOMS is, little is known regarding the specific cellular mechanisms that induce muscle soreness (1, 2). Lieber and Friden have postulated that
fiber oxidative capacity may be a key to understanding the mechanism responsible
for DOMS (27, 29). Using a rabbit model, they observed that muscle fibers, after
eccentric treatments, displayed structural abnormalities primarily in fast-twitch
muscle and stained negative for glycogen. Human models have also shown selective
damage to fast-twitch muscle fibers after eccentric exercise protocols (17, 25).
Metabolic studies of human muscle further indicates that eccentric activity rapidly
depletes fast-twitch fibers of glycogen when performed above VO2max (15, 23), uses
significantly more muscle glycogen than concentric activity at similar intensities
(38), and impairs glycogen uptake post-exercise compared to muscle depleted by
concentric activity (9, 10, 38, 44).
Lieber and Friden proposed that fast-twitch fibers, which lack the higher
oxidative capacities of slow-twitch fibers, fatigue early in an exercise period and
become unable to generate enough adenosine triphosphate (ATP) to support the
contractile mechanism. According to the current theories of muscle contraction, the
release of the myosin head from the actin filament requires the addition of a new
ATP. Insufficient ATP causes this release mechanism to fail, and the fiber enters a
rigid or highly stiff state (11). Lieber and Friden theorized that subsequent eccentric
stretch of stiff fibers would mechanically disrupt the sarcolemma, sarcoplasmic
reticulum, and myofilaments, resulting in the observable cytoskeletal and myofibrillar damage leading to an inflammatory response and the concomitant delayed
muscle soreness.
Because Lieber and Friden noted that injured fast glycolytic muscle fibers
were depleted of glycogen, we hypothesized that fasted subjects, following a protocol to decrease muscle glycogen, might be more predisposed to DOMS than subjects with decreased muscle glycogen who had been fed a diet high in carbohydrates.
Theoretically, drastically decreasing muscle glycogen would lead to a decrease in
the availability of ATP, which would compromise the release of myosin crossbridges from the actin filaments, resulting in stiffness, injury, soreness, and dysfunction (22, 33, 34). The present study was designed to test the hypothesis that there
would be greater muscle soreness, stiffness, injury, and dysfunction in glycogendepleted subjects compared to subjects with normal muscle glycogen content.
Methods
Subjects
Thirty-three male subjects between the ages of 18 to 35 were recruited from the local
population. Subjects were excluded on the basis of a questionnaire if they responded
yes to any of the following: lower extremity pain, history of knee surgery, used
medications that would prevent an inflammatory response, involved in a lower
Carbohydrate Intake and Muscle Soreness / 173
extremity strength training program in the past 6 months, eccentric damage of their
lower extremities in the past 90 days, had Type I or II diabetes, or were avid cyclists
or runners. An informed consent document consistent with the university policy for
the protection of human subjects was given to the subjects, and written consent was
obtained.
Experimental Design
Subjects were randomized into three groups (Figure 1). The depletion group (DEP)
underwent a glycogen depletion protocol (21), fasted for 12 hours, and then performed an eccentric exercise protocol (5). The repletion group (FED) underwent a
glycogen depletion protocol, followed immediately by the consumption of a meal,
designed to replenish glycogen, before undergoing the eccentric treatment 12 hours
later. The third group (ECC) was a control and only participated in the eccentric
treatment.
All subjects were tested for maximal oxygen consumption using a cycle
ergometer to determine cycling resistance levels for the glycogen depletion protocol that followed 1 week later. The DEP and FED groups performed the glycogen
depletion protocol before the eccentric exercise protocol. The DEP group consumed
only water during the 12 hours between the depletion and eccentric protocols.
Following the depletion protocol, the FED group consumed a meal consisting of
80% carbohydrates, 10% fat, and 10% protein. Food consisted of pasta, sauce,
breads, and Gatorade®. Portions were determined by calculating 2 g of carbohydrates per kilogram of bodyweight (6, 23) from the Recommended Dietary Allowances packaging label on each food item. Portions were fed to the subjects within an
hour of the depletion protocol. The ECC group performed the maximal test of
oxygen consumption and, 1 week later, the downhill running protocol.
All groups underwent muscle damage marker assessment 1 day prior to, and
on days 1, 2, 3, 4, and 6 after, the eccentric exercise bout. Subjects refrained from any
activity that would induce muscle soreness during the experiment.
Figure 1 — VO2max tests were performed by all subjects 1 week prior to a glycogen
depletion protocol. The study groups DEP and FED both performed the depletion
protocol. The DEP group fasted between the depletion protocol and the downhill run,
while the FED group consumed 2 g CHO/kg body weight before their downhill run. The
ECC group performed only the VO2max test and the eccentric protocol. Each group
received DOMS assessment on days 1, 2, 3, 4, and 6 post eccentric activity.
174 / Nelson, Conlee, and Parcell
Test of Maximal Oxygen Consumption
All groups performed a graded exercise test to exhaustion to determine maximal
oxygen consumption. The VO2max test was performed on an electromagnetically
braked cycle ergometer (Lode Excalibur, Lode, Groningen, Netherlands). The cycling protocol was a concentric activity that would not induce DOMS.
Each subject began cycling at a resistance of 125 W. The resistance was
increased by 50 W every 3 min until volitional exhaustion. Each subject met three
criteria to determine VO2max. First, oxygen consumption plateaued during the last
minutes of the test, rising no more than 2 ml · kg–1 · min–1 in between the final test
stages. Second, the respiratory exchange ratio increased to 1.15 or higher. Last, each
subject’s heart rate increased to within 10 beats of the age-predicted maximum. The
last three VO2 readings were averaged to determine a maximal oxygen uptake value.
Expired volume was determined by a Fleish pneumotach, and exhaled O2 and CO2
were determined by a mass spectrometer (Marquette Inc.). Oxygen uptake and
carbon dioxide production were analyzed every 30 s by an online computer program
(Consentius Inc.). The mass spectrometer was calibrated prior to testing using
certified medical gases of known concentration. Heart rates were monitored by
radiotelemetry (Polar Electro Inc., Port Washington, NY, USA), and a rating of
perceived exertion (RPE) was recorded at 2-min intervals.
Depletion Protocol
Muscle glycogen depletion was induced with the protocol of Gollnick et al. (20).
This protocol depleted both slow- and fast-twitch fibers of glycogen in the anterior
thigh muscles (vastus lateralis, vastus medialis, and rectus femoris). Subjects rode
an electromagnetically braked cycle ergometer (Lode Excalibur, Lode, Groningen,
Netherlands) for 1.5 hours at a workload corresponding to 60% of their maximal
oxygen uptake. Subjects then performed six 1-min sprints at 150% of their VO2max.
Ten-minute rests were interposed between each sprint. This depletion protocol and
others comparable to it have shown to result in glycogen depletion in similar subjects (6, 23).
Eccentric Exercise Protocol to Induce DOMS
To induce muscle soreness, all subjects performed a downhill running protocol (5)
on a treadmill (Quinton Instruments, Seattle, WA, USA). Downhill running activates the anterior thigh muscles measured for glycogen depletion in the Gollnick
cycling protocol (4, 12, 13, 40). Subjects in the DEP and FED groups reported to the
lab 12 hours after the glycogen depletion cycle protocol. Subjects in the ECC group
performed the protocol at the same time of day as the other two groups. The subjects
familiarized themselves with the treadmill by running for 5 min at a 0% grade at a
target pace that elicited a heart rate of 170 bpm. After 5 min at 170 bpms, the slope of
the treadmill was changed to –10%, while the speed remained at the target pace, and
subjects ran continuously for 15 min. Subjects’ heart rate was recorded every 5 min.
Since muscle damage occurs early in the eccentric exercise period and to prevent
severe DOMS, the protocol in this study was modified by having subjects exercise
for 15 min. This modification was verified during our pilot study in which 5 subjects,
who exercised for 15 min, demonstrated an average muscle soreness of 5.3 on a 10cm subjective pain scale.
Carbohydrate Intake and Muscle Soreness / 175
Dependent Variables
Perceived muscle soreness, maximal isometric force, relaxed limb angles, and circumference of the lower anterior thigh were used as indirect muscle damage indicators (43). Each variable was collected on days 0, 1, 2, 3, 4, and 6.
Perceived Muscle Soreness
Each subject assessed pain of the contracted muscles of the anterior thigh (vastus
medialis, vastus lateralis, and rectus femoris) with the knee joint at 90° using a
horizontal visual analogue scale with a continuous, unmarked 10-cm line. The 0-cm
end represented no soreness, and the 10-cm end represented very, very sore (41).
Each subject was seated on a table with his or her knees at 90° angles and legs unable
to touch the floor. Each subject performed a maximal isometric knee extension at
90° against an immovable fixture, after which subjects were asked to rate their
perceived muscle pain by marking the 10-cm line.
Maximal Isometric Force
Isometric force measurements were obtained using a BIODEX System 3 Isokinetic
Dynanometer (Biodex Medical Systems, Shirley, NY, USA). Subjects were secured on the BIODEX with leg, thigh, waist, and shoulder straps. Seat and limb
positions were recorded to maintain the same position in all trials. Knee angle was
set at 60°. Subjects were given three periods of 10 s in which to develop maximal
isometric torque. Peak torque generated during each period was taken, and all three
maximum isometric peak torque measurements were averaged. The average derived from the three contractions was used as peak torque. Subjects rested for 2 min
between maximal isometric contraction periods.
Relaxed Limb Angle
The anatomic reference points for goniometer placement on the leg were taken from
Norkin and White (36). They included the lateral malleolus, the lateral head of the
tibia, and the anterior inferior iliac spine. Anatomical reference points of the left leg
were marked with a permanent marker and were remarked if fading occured between tests. Subjects sat on a table with their left knee joint relaxed and both feet
even above the ground. Initially, a mark was made 2 in. from the knee joint, where
the posterior thigh and the edge of the table met. Subjects were told to relax their
quadriceps. Knee angle measurements were performed in duplicate.
Thigh Circumference
Thigh circumference was determined with a Gulick tape measure at one fourth and
one half the distance up the thigh from the top of the patella to the inguinal line while
the subject was in a standing position. Corresponding marks were made on the
anterior and posterior thigh at both distances and were remarked between tests as
needed. Subjects were asked to stand with their weight evenly distributed on both
feet and to relax as a Gulick tape measure (accuracy to 1/16 in.) was placed around
their thighs, lining up at the anterior and posterior marks. The tape was then removed
and the measurement repeated.
176 / Nelson, Conlee, and Parcell
Statistical Analysis
Data were analyzed with repeated measures ANOVA. The dependent variables
were subjective muscle soreness, maximal isometric force, relaxed knee angle, and
thigh circumference. Independent variables were Time and Group. Between group
differences were checked by the Wilks’ Lambda test. Group and Time significance
were accepted at a p < .05. Data were analyzed using SAS 8.0 (SAS Institute Inc.,
North Carolina, USA).
Results
No significant differences existed between groups in any of the measured variables
at any time point. Muscle soreness, thigh circumference, and relaxed knee angle
were significantly different from baseline on days 1, 2, and 3 post exercise. Maximal
isometric force was statistically different from baseline measurements for 4 days
post treatment.
Perceived Muscle Soreness
Baseline muscle soreness for all groups was zero (Figure 2). DEP soreness peaked at
24 hours at 3.68 ± 0.67 cm (p < .05). FED and ECC peaked the 1st day as well, with
means of 2.27 ± 0.76 and 3.21 ± 0.75, respectively (p < .05). At 48 hours post
eccentric activity, all groups were still significantly different (p < .05) from baseline,
with DEP at 2.84 ± 0.54, FED at 2.23 ± 0.34, and ECC at 2.68 ± 0.63. Each subject
returned to baseline by the end of the measuring period. Interaction effect was nonsignificant (F10, 145 = 0.92, p = .51), indicating no differences between groups. Group
effects were non-significant (F2, 29 = 0.55, p = .58), while Time effects were significant (F5, 145 = 39.89, p < .05).
Maximal Isometric Force
Baseline isometric force values were 275 ± 35, 283 ± 56, and 285 ± 45 N for DEP,
FED, and ECC, respectively (p > .05; Figure 3). Twenty-four hours following the
eccentric exercise, each group showed maximal force decreases ranging from 22–
31 N (p < .05). On the 2nd day post treatment, FED decreased 5 N, and ECC
remained the same (p < .05). All groups after the day 2 measurement increased in
force from their maximal force deficit and returned to baseline values by the end of
the 6th day. Interaction effect was non-significant (F10, 145 = 0.83, p = .60). Group
effect was non-significant (F2, 29 = 0.16, p = .85). Time effects were significant
(F5, 145 = 57.22, p < .05).
Thigh Circumference
Thigh circumference baseline values were 17.25 ± 1.54, 17.25 ± 1.48, and 18.45 ±
2.66 in. for DEP, FED, and ECC, respectively (p > .05; Figure 4). Circumference
increased significantly in all groups by day 2 but returned to baseline values by day
6. Interaction effect was significant (F10, 145 = 2.27, p < .05), indicating differences
between Groups over Time. Group effect was non-significant (F2, 29 = 1.42, p = .25).
Time effect was significant (F5, 145 = 37.46, p < .05).
Carbohydrate Intake and Muscle Soreness / 177
Figure 2 — Perceived muscle soreness prior to (0) and 6 days following the downhill
running protocol. This graph compares the muscle soreness scores (cm) among the
depleted (DEP), repleted (FED), and control (ECC) groups. *Significant differences of
all three groups from baseline measurements (p < .05). There were no significant differences between groups.
Relaxed Knee Angle
Baseline knee angle values were 110.3 ± 1.06°, 111.1 ± 0.91°, and 108.0 ± 0.92° for
DEP, FED, and ECC, respectively, with no significant differences between baseline
values (Figure 5). DEP and ECC had maximum angle values at day 2 post treatment,
while FED had its maximum value on day 1 post treatment. All groups decreased to
baseline levels by the end of the measurement period; however, changes over time
were not different between groups. Interaction effect was non-significant (F10, 145 =
0.58, p = .82), indicating no differences between groups. Group effect was nonsignificant (F2, 29 = 2.31, p = .11). Time effect was significant (F5, 145 = 46.06, p < .05).
178 / Nelson, Conlee, and Parcell
Figure 3 — Maximal isometric strength prior to (0) and 6 days following the downhill
running protocol. This graph compares DEP, FED, and ECC group strength loss over
the measuring period. *Significant differences of all three groups from baseline measurements (p < .05). There is no significant difference between any of the groups.
Discussion
The present study sought to determine if inadequate carbohydrate intake after exercise to decrease muscle glycogen would increase the degree of DOMS in subjects
after a downhill run. The results of the indirect measures of muscle damage indicate
that DOMS did occur in all subjects. The loss of maximal isometric force, perceived
muscle soreness, decrease in relaxed knee angle, and increase in thigh circumference is consistent with DOMS as seen in other studies (7, 8, 18, 34). The etiology of
each of the above responses to muscle damage has been discussed further in other
studies (26, 34, 37, 42).
Lieber and Friden suggested that fast-twitch fibers fatigue during the early
phases of intense exercise (5–15 min) and, based upon their inability to regenerate
Carbohydrate Intake and Muscle Soreness / 179
Figure 4 — Measurement of thigh circumference prior to (0) and 6 days following the
downhill running protocol. Average DEP, FED, and ECC group thigh circumferences
are shown over the measuring period. *Significant difference of all three groups from
baseline measurements (p < .05). Statistical analysis failed to show any differences
between groups.
ATP, enter a rigid and highly stiff state (28). Further stretching of these stiff fibers
during eccentric contraction disrupts the fiber membranes, allowing an influx of
destructive metabolites into the cell, resulting in the observed cytoskeletal and
myofibrillar damage of DOMS (27, 28). Since glycogen depletion is a well-known
cause of fatigue, and since Lieber and Friden showed that fatigued and damaged
muscles were also depleted of glycogen, we hypothesized that a diet deficient in
carbohydrate would predispose whole muscle with decreased muscle glycogen to
greater damage from eccentric exercise than muscle allowed to increase glycogen
stores through ample carbohydrate intake. We also hypothesized that these subjects
would also experience a greater degree of DOMS and its associated symptoms.
180 / Nelson, Conlee, and Parcell
Figure 5 — Relaxed knee angle measurements prior to (0) and 6 days following the
downhill running protocol. The graph shows the DEP, FED, and ECC group angle
measurements over the measuring period. *Significant difference of the three group
measurements over baseline values (p < .05). There are no significant differences between groups.
Our results indicate that 15 min of downhill running in an untrained population is sufficient to induce DOMS; however, decreased muscle glycogen of whole
muscles followed by a state of fasting did not increase muscle soreness. Thigh
circumference measures revealed a significant difference at one time point between
the DEP group and the other two groups. The other three measures indicated no
Carbohydrate Intake and Muscle Soreness / 181
differences between groups at this time point; therefore, we question the physiological significance of circumference differences at a single time point. Interestingly,
Lieber and Friden postulated that eccentric damage to muscles occurs in the first 5–
15 min of eccentric exercise. Therefore, considering the state of the decreased
muscle glycogen of the subjects, the downhill running time of 15 min should have
been sufficient to invoke significant differences of muscle soreness.
Byrnes and his colleagues (5) showed that running on a –10° slope for 30 min
produced DOMS in all 22 trained college-age subjects. These subjects were maximally sore at 40 hours post treatment and, on a subjective pain questionnaire, rated
their muscle soreness at specific body sites over time on a scale of 1 to 10. Our
protocol was modified for untrained individuals to run for 15 min instead of 30 min
(19). This change allowed the protocol to be completed by untrained subjects and to
prevent potentially severe DOMS that would obscure any possible differences due
to treatments. Our modified protocol produced soreness similar to the Byrnes study,
but did not produce any significant differences in subjective muscle soreness between groups. Subject soreness peaked at 24 hours, with an average of 3.05 out of 10
on a subjective soreness scale.
Two possible limitations to the study were that we did not directly measure
muscle glycogen levels in our subjects and that the muscle fibers depleted of glycogen via the bicycle protocol were not recruited during the treadmill protocol. In
response to both limitations, we followed the same protocol as Gollnick et al. (20), in
which subjects experienced nearly complete depletion of glycogen in both slowand fast-twitch muscle fibers of the vastus lateralis muscle. Hickner et al. (23) used
a similar protocol with untrained subjects and also obtained severe glycogen depletion in the quadriceps femoris muscle of both slow- and fast-twitch fibers. Not only
are the same muscles utilized in the downhill run as the bicycle protocol (4, 12, 13,
40), but it is also the fast-twitch fibers that are preferentially depleted in this type of
eccentric activity (16, 17, 27, 29). Concerning the depleted muscle fibers, Hickner
as well as others (6, 30, 32) have shown that untrained subjects, 12 hours after
depleting exercise on a high carbohydrate diet (>80%), were mostly repleted with
muscle glycogen. Therefore, we believe that glycogen repletion occurred in the
FED group in response to the high carbohydrate meal consumed immediately following the depletion exercise. Fasted subjects undergoing depleting protocols show
extremely minimal increases in muscle glycogen levels up to 4 hours post activity
but show no further increases from the 4-hour time point to the 12-hour time point
(31, 39, 44). Therefore, based on the literature, we are confident that significant
muscle glycogen repletion did not occur in the DEP group.
An underlying assumption of our work is that fatigued muscle fibers became
stiff due to decreased glycogen, decreasing the amount of ATP that is necessary for
the release of the myosin cross bridge from the actin active site (11). This assumption can be contested. There is considerable evidence that suggests that fatigued
muscle still has a normal concentration of ATP (14, 22). If that is the case, then even
though decreased glycogen may predispose a muscle to be more susceptible to
fatigue, it may not be more susceptible to damage, because it may not be ATP
depleted.
The hypothesis of our study also fails to address the issue that fiber recruitment patterns are not altered by eccentric exercises (38). In eccentric activity below
VO2max, it is the slow-twitch muscle fibers that show the greatest decrease in glycogen levels, yet it is the fast-twitch fibers that demonstrate the greatest damage. These
182 / Nelson, Conlee, and Parcell
studies also indicate that muscle glycogen uptake is impaired in all fibers posteccentric activity (9, 10, 38, 44), and some even suggest that this lack of glycogen
repletion could be responsible for the ultrastructural changes seen in damaged
muscle (38). The current results provide no additional insight into the mechanisms
responsible for muscle soreness, but they do indicate that soreness is not related to
manipulations of glycogen levels by carbohydrate intake and glycogen depleting
activity.
Conclusion
In the current study, 15 min of downhill running was sufficient to induce DOMS.
Furthermore, muscle strength, relaxed knee angle, thigh circumference, and perceived muscle soreness indirectly demonstrated muscle damage. We proposed that
subjects who underwent a glycogen depletion protocol, followed by a 12-hour fast,
would be prone to a greater degree of stretch-induced injury compared to subjects
who had increased their intake of carbohydrates after a glycogen depletion protocol.
The data, however, reveal that was not the case. We conclude therefore that an
inadequate diet of carbohydrate after glycogen-depleting exercise does not predispose one to muscle dysfunction or soreness.
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