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Repeated high-force eccentric exercise:
effects on muscle pain and damage
D. J. NEWHAM, D. A. JONES, AND P. M. CLARKSON
Department
of
Medicine, University College London and Middlesex Hospital Medical School,
The Rayne Institute, London WClE 6JJ, United Kingdom; and Department
of
Exercise Science,
University
of
Massachusetts, Amherst, Massachusetts 01003
NEWHAM, D.J.,D. A. JONES, AND P. M. CLARKSON.R~-
peated high-force eccentric exercise: effects on muscle pain and
damage. J. Appl. Physiol. 63(4): 1381-1386,1987.-Five women
and three men (aged 24-43 yr) performed maximal eccentric
contractions of the elbow flexors (for 2Q min) on three occa-
sions, spaced 2 wk apart. Muscle pain, strength and contractile
properties, and plasma creatine kinase (CK) were studied before
and after each exercise bout. Muscle tenderness was greatest
after the first bout and thereafter progressively decreased. Very
high plasma CK levels (1,500-11,000 W/l) occurred after the
first bout, but the second and third bouts did not significantly
affect the plasma CK. After each bout the strength was reduced
by -50% and after 2 wk had only recovered to 80% of preex-
ercise values. Each exercise bout produced a marked shift of
the force-frequency curve to the right which took approximately
2 wk to recover. The recovery rate of both strength and force-
frequency characteristics was faster after the second and third
bouts. Since the adaptation occurred after the performance of
maximal contractions it cannot have been a result of changes
in motor unit recruitment. The observed training effect of
repeated exercise was not a consequence of the muscle becom-
ing either stronger or more resistant to fatigue.
training; fatigue; elbow flexors; creatine kinase
PREVIOUS STUDIES
have shown that exercise involving
high-force eccentric muscle contractions can produce
temporary muscle pain and damage. Evidence of damage
includes disruption of muscle fibers (8,
14,
Zl),
increased
circulating levels of muscle proteins (3,9,18,19), muscle
uptake of radionuclides
(17, 20,
25), and changes in
voluntary strength and contractile properties in the im-
mediate postexercise period (5, 22).
One interesting feature is the rapidity with which the
pain and muscle damage are reduced or abolished by
repeated exercise (2-4, 7, 11, 13). In our previous work
(ll),
release of creatine kinase (CK) and muscle tender-
ness were measured after one bout of exercise involving
contractions at 50% maximum force. When the exercise
was repeated 1 wk later both pain and
CK
release were
much reduced. This training effect was found to last -6
wk, indicating a considerable and long-lasting adaptation
(11). There are a number of possible explanations for the
training which include the following.
1)
There may be a change in the pattern of motor unit
recruitment. Previous studies have used submaximal
contractions that allow the possibility that training may
cause a change in the order of motor unit recruitment
such that either susceptible fibers are spared on the
second and subsequent occasions or more fibers are
recruited and the force-fiber ratio is reduced. This can
be investigated by using maximal contractions.
2) There may be some adaptation in the muscle fibers
such that they become more resistant to the fatiguing
and damaging effects of eccentric exercise. This might
be evident as a change in th’e strength and contractile
properties of the muscle.
3) It has been suggested that eccentric exercise pref-
erentially damages a population of fibers that are nearing
the end of the cycle of growth and replacement
(1).
In
this case, a decrement in force generation would occur
after the first exercise which would be absent on subse-
quent occasions.
The purpose of the present investigation was to test
these possibilities. To this end we have compared the
changes in strength and contractile properties with the
pain and plasma CK response after three bouts of max-
imal eccentric contractions of the elbow flexors spaced
at two weekly intervals.
METHODS
Subjects.
Eight subjects (5 females and 3 males) rang-
ing in age from 24 to 43 yr took part in the study. They
were healthy and active but none was participating in
any training programs, and they had not participated in
studies involving eccentric contractions for at least 3 mo.
Their physical characteristics are shown in Table
1.
All
were fully informed of the nature and risks of the pro-
cedures to be used. The study had the approval of the
Committee for the Ethics of Human Procedures at Uni-
versity College Hospital.
Exercise.
To exercise the elbow flexors the subject sat
in an adjustable chair with the upper arm supported on
a shelf, the height of which could be adjusted to bring
the upper arm to an angle of 90” with the body. An
inextensible cord passed from a wrist cuff to a pulley
attached to the wall in front of the subject and then to
the experimenter. The latter was able to forcibly extend
the elbow and overcome the maximal effort of the subject
by means of a winch with a mechanical advantage of
-1O:l. The signal from the strain gauge was amplified
and displayed on an ultraviolet recorder. Details of the
procedure have been given elsewhere (12).
0161-7567/87 $1.50 Copyright 0 1987 the American Physiological Society 1381
1382
REPEATED EXERCISE: MUSCLE PAIN AND DAMAGE
TABLE
1. Physical characteristics
of
the subjects
Subj. No. Sex &e Ht, m W kg
1 M 43 1.76 71.9
2 M 41 1.68 73.4
3 F 37 1.67 68.4
4 F 35 1.76 65.3
5 M 39 1.64 69.9
6 F 24 1.56 47.7
7 F 26 1.60 48.3
8 F 40 1.58 49.6
The subjects performed one eccentric maximal volun-
tary contraction every
15
s for 20 min. Each contraction
lasted -2 s. The range of elbow movement was from full
flexion to full extension with care being taken not to
hyperextend the elbow. The exercise was repeated on
three occasions that were separated by an interval of 2
wk.
Force measurement. Isometric maximum voluntary
contraction (MVC) force was measured before and im-
mediately after each exercise period and repeated at daily
intervals thereafter. Three attempts were made on each
occasion, and the highest was taken as the maximal force.
When recording force from voluntary contractions of
painful muscles there is the possibility that the contrac-
tions are submaximal, even with well-motivated subjects.
To determine whether this was the case electrical stim-
ulation (at both
1
and
100
Hz) was superimposed on the
voluntary contractions. With this technique additional
force is generated by the electrical stimulation only if
the voluntary contractions are submaximal (23).
The force-frequency relationship was determined by
percutaneous electrical stimulation of the biceps at
1
Hz
(for 5 s) and
10, 20, 50,
10, and
100
Hz for 2 s each.
Damp electrodes (8, cm”) were bandaged onto the upper
arm, over the proximal and distal ends of the biceps.
Square-wave pulses of 50 pus and up to
100
V were used
(Digitimer dual high-voltage stimulator, Hertfordshire,
UK). The force at each frequency was expressed as a
percent of that generated by stimulation at 100 Hz (l/
lOO%, lO/lOO%,
etc.). Care was taken to ensure that at
least 25% of the elbow flexors were stimulated, compar-
ing the stimulated contractions with the MVC.
.For all the isometric measurements the wrist was tied
and the upper arm supported to prevent movement of
the arm in any direction. The shoulder was prevented
from forward movement by being clamped to the back of
the chair. In our experience daily testing in this way
neither causes muscle pain or damage nor does it modify
the response to eccentric exercise.
Plasma CK. Blood was collected from an antecubital
vein into heparinized tubes before and at daily intervals
after each exercise period. CK activity was determined
by the Department of Chemical Pathology, University
College Hospital, using a Boehringer Mannheim kit
method with N-acetylcysteine activation. The normal
range using this method is 60-190 IU/l.
Muscle tenderness. This was measured daily after the
exercise by recording the force required to elicit tender-
ness at fixed sites on the skin over the biceps and
brachioradialis (22). Twelve test sites were spaced -2 cm
apart over the muscle surface and marked with indelible
ink. At each site a gradually increasing force was applied
through a flat plastic disc of 2 cm diam attached to a
force transducer with digital readout (Penny & Giles
Transducers, Christchurch, Dorset, UK). The subject
was asked to indicate when the sensation of pressure
changed to discomfort, and the force at that point was
recorded. Tenderness was recorded as absent if not re-
ported before 30 N. The value of the force (N) has been
subtracted from 30 to give a tenderness score.
Statistics. Data were analyzed using repeated-measures
analysis of variance. Statistical significance was set at P
c 0.05.
RESULTS
A4aximal voluntary force. Superimposition of electrical
stimulation on the voluntary contractions demonstrated
that all subjects were able to fully activate their muscles
during the isometric contractions despite any discomfort.
The values for MVC, expressed as a percent of the
initial preexercise force, are presented in Fig.
1.
There
was a large decrease in voluntary force (-50%) immedi-
ately after the three exercise periods. There was no
significant difference between the extent of force loss
after the three bouts. Recovery was slow and there were
differences between the rate of recovery from the first
compared with that from the second and third occasions.
After the first exercise force had hardly improved after
24 h (49% initial), whereas after exercise bouts 2 and 3
there was recovery to 66 and 69%, respectively. The
values for bouts 2 and 3 at this time differed significantly
from bout 1 but not from each other. After the first bout
of exercise the MVC remained significantly lower than
the initial force until
1
wk after the third and final
exercise. There was no evidence of an increase in strength
as a result of the exercise in any of the subjects.
ContractiZe properties. After exercise there was a sig-
nificant decrease in force generation at low frequencies
of stimulation. A representative index of this is the force
generated by 20 Hz stimulation expressed as a percent
of that at 100 Hz (20/100%). These values are presented
in Fig. 2. A large decrease in the 2O/lOO% value to -40%
was seen immediately after each exercise bout, there
being no significant difference between the decrement
seen on the three occasions. As with the MVC measure-
ments (Fig. 1) there was a faster recovery after the second
and third exercise bouts compared with the first. The
2O/lOO% value was significantly less than the initial
value until the 9th day after the first exercise but was
not significantly different from preexercise values by the
4th and 3rd days after the second and third bouts of
exercise.
Plasma CK. Although there was a large intersubject
variation in the CK response, all showed a substantial
increase after bout 1, the peak values ranging from 1,570
to 10,904 IU/l, which was much greater than the response
seen after bouts 2 and 3 (Fig. 3 and Table 2). The plasma
CK only showed a significant increase after the first
exercise.
MuscZe tenderness. Muscle tenderness values are pre-
sented in Fig. 4. A significant difference in tenderness
was found among the three bouts, with each resulting in
REPEATED EXERCISE: MUSCLE PAIN AND DAMAGE
1383
100
80 [ -
Ye
.- + 60-
.-
c
.- w
s
-
- 2 40 L
20 -
m
O-
Mean & sem
n=8
1 I 1 1 1 I
J
1
2 3 4 5 6 7
Time (weeks)
FIG. 1. Maximal isometric strength during training period. Exercise was performed in lst, 3rd, and 5th wk. MVC,
maximum voluntary contraction.
Mean & sem
n -8
Time keks)
progressively less tenderness. The peak pain, which oc-
curred on day 2 after the first exercise and day 1 after
the second and third occasions, was significantly less on
the second compared with the first occasion and less
again on the third compared with the second occasion.
The sums of the pain scores over the 4 days after exercise
were reduced, being 43 and 35% of the initial response
after the second and third bouts, respectively.
There were no obvious relationships among the vari-
ables measured such as the extent of force loss and
subsequent pain or increase in plasma CK. Changes in
force and contractile properties were similar in all the
subjects (Figs. 1 and Z), but there was considerable
variation in the pain and release of CK. There was no
obvious relationship between the extent of the response
and parameters such as age, sex, or general level of
physical fitness of the subjects (Tables 1 and 3).
FIG. 2. Force-frequency relationship
during training period. Exercise was per-
formed in lst, 3rd, and 5th wk.
5 6
DISCUSSION
The training effects of repeated high-force, eccentric
exercise were very obvious both from subjective reports
and objective measurements of pain and muscle damage.
Muscle pain and stiffness were much reduced after the
second and third bouts of exercise compared with the
first.
The most striking training response was seen in the
CK efflux. The enzyme release after the first exercise
was similar in magnitude and time course to those that
we have previously reported (14, 18, 19), being both very
large and characteristically delayed for several days after
eccentric exercise. Despite variation between individuals
in the extent of the release, the plasma levels were always
greatest, by up to two orders of magnitude, after the first
bout of exercise. Although the mechanism of the exercise-
REPEATED EXERCISE: MUSCLE PAIN AND DAMAGE
mean & sem
n=8
FIG.
3. Plasma creatine kinase (CK)
during training period. Note marked
training effect seen here in comparison
with force measurements. Exercise was
performed in lst, 3rd, and 5th wk.
Time hueeks)
TABLE
2. Range of plasma CK values before and after the three exercise bouts
Exercise Postexercise, days
Bout Preexercise 1 2 3 4 5 6 7 8
1
57-250 8%1,133 81-3,074 177-7,978 735-10,904 1,854-6,074 1,402-4,535 709-3,313 365-2,222
2 90-208 97-328 64-327 49-250 52-237 65-175
3 36-185 36-230 31-137 31-167
CK, creatine kinase, in IU/l.
Mean & sem
n= 8
FIG.
4. Muscle tenderness during
training period. Pain progressively de-
creased after each exercise bout. Exer-
cise was performed in lst, 3rd, and 5th
wk.
44
1 2 3 4 5 6
nrne (weeks)
induced enzyme efflux is unknown, it is generally as-
sumed to reflect some form of membrane damage.
Suprisingly, in view of the major changes in pain and
enzyme release, the training had no effect on the maxi-
mum isometric strength, the extent of force loss after
the exercise, or the changes in contractile properties of
the muscles. Other workers have reported similar reduc-
tions in the MVC immediately after a single bout of
submaximal eccentric contractions (5,
16)
and it has
often been assumed that the apparent force loss was
largely due to the pain preventing subjects from fully
activating their muscles (7, 15,
24).
In the present study
the strength measurements were shown to be from fully
activated muscles, and thus the force loss was the result
of changes in the contractile elements.
Although both the pain and CK release responded to
training, it is unlikely that these were causally related.
Whereas the CK response was virtually eliminated after
the first bout of exercise, the discomfort was only reduced
in a stepwise manner. Furthermore, the CK release and
pain are always separated in time (see Figs. 3 and
4)
and
are often dissociated in magnitude. Thus one individual
REPEATED EXERCISE: MUSCLE PAIN AND DAMAGE
1385
TABLE
3. Relationship between muscle strength, fatigue,
damage, and pain after eccentric contractions
MVC
Subj. No. 20/100%, Peak CK, Peak Tenderness
n % initial % initial IU/l Score
1 310 47.8 53.7 5,586 12.6
2 263 43.9 72.9 1,854 9.0
3 186 57.8 75.2 6,074 14.0
4 167 51.4 71.6 5,464 10.2
5 152 56.3 52.0 9,426 17.9
6 129 57.1 58.9 1,570 15.0
7 115 55.9 56.5 10,904 10.6
8 103 60.7 74.6 2,494 14.9
Relationship between initial strength of subjects and changes in
force generation, plasma creatine kinase (CK), and muscle pain after
first bout of exercise. Force measurements are those before and im-
mediately after exercise period. MVC, maximum voluntary contraction;
ZO/lOO%, force generated by 20 Hz of stimulation expressed as percent
of that at 100 Hz (% initial).
might have considerable pain but little or no evidence of
muscle membrane damage.
There is evidence that the pain and stiffness experi-
enced after eccentric contractions are a consequence of
shortening of the noncontractile material that is ar-
ranged in parallel with the contractile material (10, 13).
This may be a response to some form of damage to the
connective tissue, and if so the training could have caused
some adaptation of this tissue.
We have previously studied the training effect using
eccentric contractions at 50% maximum (11) and found
results similar to those reported here. With submaximal
contractions it was possible that changes might have
occurred in the recruitment pattern so that, after train-
ing, less susceptible motor units were used. Alternatively,
more motor units could be recruited, thereby reducing
the force per fiber. The results of the present study, using
maximum contractions, show that neither of these pos-
sibilities can be the entire explanation since maximal
contractions require the activation of all motor units so
there is no possibility of change in the extent or order of
recruitment.
The training program did not increase the voluntary
strength of the muscle, nor did it prevent the loss of force
or change in contractile properties (shown by the 20/
100% value, Fig. 2) that occurred to a similar extent after
each bout of exercise. This demonstrates that the adap-
tation did not involve any change in the strength or
contractile properties of the muscle or its ability to
withstand fatigue.
The present results provide some evidence in favor of
the possibility, suggested by Armstrong (l), that the first
bout of exercise causes damage and destruction to a
population of susceptible fibers, possibly those near the
end of their life cycle. There was a notable difference in
the time course of recovery of force generation after the
first exercise bout compared with the second and third,
being slower after the first bout (Figs. 1 and 5). This
difference in rate of recovery was also evident with the
20/100% value (Fig. 2). The slow recovery of force and
contractile properties was associated with the release of
CK from the muscle. It is possible that the loss of force
and release of soluble constituents represent the removal
1 a 1 1 a 1 1 4
0 1 2 3 4 5 6 7
Days after exercise
FIG. 5. Changes in maximum voluntary contraction (MVC) force
(means -+ SE) after first (squares) and second (diamonds) exercise
bouts. Values after second exercise bout were significantly greater than
after first at all times shown with exception of those on day 4.
and replacement of irreparably damaged fibers that may
have been particularly susceptible to damage, possibly
being near the end of the natural cycle of cell turnover.
This could equally well apply to either the entire fiber or
a part of it. After the initial damage they may fail to
repair and subsequently undergo degeneration, recover-
ing slowly and releasing soluble enzymes in the process.
The more resilient fibers, or parts of fibers, remain and
these are able to withstand the effects of eccentric exer-
cise without undergoing a process of degeneration and
enzyme release.
This seems to be the first report in which the time
course of the recovery of both strength and contractile
properties has been followed for more than a few days.
The MVC was very slow to recover, only returning to
-80% of the initial value in 2 wk. Interestingly, the
subjects were aware of impaired muscle function only
after the first exercise bout in which most pain was
experienced. They therefore felt that the training had
improved their performance, yet objective testing showed
appreciable and long-lasting weakness.
This study does not identify the mechanism by which
the pain and damage are reduced by training. However,
it does suggest that the prevention of enzyme release
with training may be due to the removal of contractile
material that is particularly sensitive to damage.
Received 19 December 1986; accepted in final form 1 May 1987.
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