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1 Institute of Gerontology, University of Michigan, Ann Arbor, Michigan 48109-2007; and 2 Muscle Research Centre, Department of Medicine, University of Liverpool, Liverpool L69 3BX, United Kingdom
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Van der Meulen, Jack H., Anne McArdle, Malcolm J. Jackson,
and John A. Faulkner. Contraction-induced injury to the extensor
digitorum longus muscles of rats: the role of vitamin E. J. Appl. Physiol. 83(3): 817-823, 1997.
Three days after a protocol of 225 pliometric (lengthening)
contractions was administered to in situ extensor digitorum longus
muscles of rats, the force deficit was 64 ± 7% and the percentage
of damaged muscle fibers was 38 ± 5% of the control values. We
then tested the hypothesis that at 3 h and 3 days after the protocol an
elevation in the muscle vitamin E content would decrease the force
deficit, the percentage of damaged muscle fibers, and the serum
activities of creatine kinase and pyruvate kinase. The 5-8 days of
intravenous injections of 
-tocopherol increased muscle vitamin E
content threefold compared with vehicle (ethanol)-treated rats. Despite the difference in vitamin E content, the force deficit and number of
damaged fibers were not different. After the contraction
protocol, the serum creatine kinase and pyruvate kinase activities of
the vehicle-treated rats increased fourfold at 3 h and twofold at 3 days, whereas the vitamin E-treated rats showed no change. We conclude
that vitamin E treatment did not ameliorate either the induction of the
injury or the more severe secondary injury at 3 days.
Despite the absence of evidence for an antioxidant function, the lack
of any increase in serum enzyme activities for vitamin E-treated rats
at 3 h and 3 days supported a role for vitamin E in the prevention of
enzyme loss after muscle damage.
pliometric contractions; muscle damage; serum creatine kinase
activity; serum pyruvate kinase activity; eccentric
exercise
INTRODUCTION WHEN ADMINISTERED TO MUSCLES of mice in situ, protocols
of pliometric (lengthening) contractions are more likely to cause injury to skeletal muscle fibers than are isometric or miometric (shortening) contractions or passive lengthening (10, 15). During the hours, days, and weeks after contraction-induced injury, the
timing and magnitude of the injury have been assayed by the activity of
muscle enzymes in the serum, the percentage of damaged compared with
intact muscle fibers in a muscle cross section, and the loss in force
development expressed as a force deficit (8). Protocols of single or
repeated pliometric contractions produce an initial focal injury to
single sarcomeres or small groups of sarcomeres within specific fibers
that is discernable by electron microscopy or by a force deficit in the
absence of fatigue but is not observed with light microscopy (5, 11, 18). The initial injury produces a cascade of events leading to a
secondary injury several days later (for reviews, see Refs. 1, 8).
The observation that the secondary injury at 3 days was almost
completely blocked by prior treatment with a known antioxidant, polyethylene glycol-superoxide dismutase (PEG-SOD), supported a role of
free radicals in the generation of the secondary injury (24). In
contrast to the efficacy of PEG-SOD, the ability of vitamin E to
protect muscles from contraction-induced injury has been much less
predictable. In muscle fibers, vitamin E has the potential to act as a
lipid-soluble antioxidant and to stabilize membranes (21). After
vitamin E supplementation, whole body pliometric exercise by rats and
humans has produced quite variable results in terms of its effect on
the different indexes of muscle damage. For subjects who took vitamin E
orally and subsequently ran downhill on a motor-driven treadmill,
Meydani et al. (16) reported a protective effect based on a decreased
activity of creatine kinase (CK) in the serum of the vitamin E-treated
group at 5 days. In contrast, Jakeman and Maxwell (13) observed no effect of oral vitamin E treatment on either force deficit or the serum
activity of CK during 12 days after box stepping. After downhill
running performed by rats given a dietary supplement of vitamin E and
by untreated rats, the vitamin E-treated rats showed no differences
compared with untreated rats in the serum activity of CK, the force
deficit, or the number of intact fibers per square millimeter in soleus
muscles (23). In the latter study (23), a full interpretation is
prevented by the lack of any knowledge of the recruitment or loading of
the soleus muscle during downhill running, the short 48-h period of
evaluation, the small 20% force deficit, and the absence of any direct
morphological data. Consequently, our purpose was to
determine the role of vitamin E in both the initial and secondary
aspects of contraction-induced injury.
The in situ extensor digitorum longus (EDL) muscle preparation of the
mouse provides an accurate and reproducible model system for
investigations of the full time course of the changes in force deficit
and morphological damage with knowledge of the strain, average force,
and number of contractions for a single muscle (4, 15). Despite the
advantages of the preparation, the 8-mg mass of the mouse EDL muscle
provides insufficient mass for the biochemical assays that we wished to
undertake for investigations of free radical activity and the effects
of vitamin E. Consequently, we developed an in situ EDL muscle
preparation in the rat, which has a 15-fold greater muscle mass than
does the mouse. We assumed that maximally activated EDL muscles in rats
exposed to 225 stretches through a 20% strain would sustain a force
deficit 3 days after the pliometric contraction protocol that was not
significantly different from the 70% force deficit observed for the
EDL muscles of mice exposed to a comparable protocol (4).
We subsequently tested the hypothesis that at 3 days after a protocol
of pliometric contractions that at 3 days produced a ~70% force
deficit in untreated muscles, the EDL muscles of vitamin E-treated rats
would show 1) a smaller force
deficit, 2) a smaller percentage of
damaged muscle fibers, and 3) lower
serum activities of CK and pyruvate kinase (PK). A control group
consisted of EDL muscles of vehicle (ethanol)-treated rats.
METHODS
-tocopherol in ethanol. Five days
of intravenous injections produced a stable muscle vitamin E content
comparable to that achieved with 5 wk of dietary supplementation. The 5 days of vitamin E treatment produced increases in the vitamin E content
of 2.0-fold in EDL, 2.8-fold in gastrocnemius, and 3.2-fold in soleus
muscles. For the comparison of treatments, the rats
(n = 33) were randomly assigned to a vitamin E-treated group
(n = 18) injected intravenously with
200 µl of a 70% (wt/vol) solution of
-tocopherol in ethanol and a
vehicle-treated group (n = 15)
injected intravenously with an equivalent volume of ethanol. Thirteen
vitamin E-treated and 10 vehicle-treated rats received daily injections
into a tail vein for 5 days before the administration of the pliometric
contraction protocol and were then tested at 3 h afterward
(n = 6 and 5, respectively) or for an
additional 3 days after the protocol and then tested (n = 7 and 5, respectively).
Nonexercised control groups, with 5 rats in each treatment group,
received daily injections for 5 days.
Pliometric contraction protocol for in situ EDL muscles of rats.
The rats were anesthetized with pentobarbital sodium (65 mg/100 g body
mass ip). Additional anesthetic was administered to maintain a
depth of anesthesia that prevented responses to tactile stimuli. The
distal tendon of the left EDL muscle was dissected free, and
the peroneal nerve was exposed. The rat was placed on its side on a
platform. The leg was attached securely to the platform by pinning the
knee and taping the foot. The body temperature was maintained at
37°C by a heating pad. The intact distal tendon of the EDL muscle
was attached with a clamp to the arm of a servomotor- force transducer
(model 6650, Cambridge Technology). An electrode was
inserted under the peroneal nerve. Voltage and muscle length were
adjusted to provide maximum twitch force. The optimum muscle length for
maximum twitch force
(Lo) is also
the Lo for the
development of maximum isometric tetanic force
(Po). With the muscle at
Lo, the
Po was measured during 300 ms of
stimulation. During repeated contractions, the frequency of stimulation
was increased until the force plateaued at
Po. On the basis of anatomic
landmarks, the Lo
was estimated with a calipers, and the optimum fiber length (Lf) was
calculated by multiplying the
Lo by a
previously determined Lf/Lo
ratio of 0.4 (22). The validity of this ratio was checked periodically
with caliper measurements of bundles of fibers dissected from the EDL
muscle.
During each protocol of pliometric contractions, EDL muscles were set
at Lo and then
activated with a stimulation frequency of 100 Hz every 4 s. This
produced an isometric contraction ~90% of
Po. The isometric contraction was
held for 200 ms, and then the activated muscle was stretched through a
strain of 20% relative to
Lf at a velocity
of 1.5 Lf/s. The
stimulation ceased at the end of the stretch, and the relaxed muscle
was returned to
Lo. Each protocol
consisted of three 5-min bouts of 75 contractions, with a recovery
period of 5 min between bouts. After a rest period of 30 min, the
Po was measured again. The
anesthetized rats were then removed from the apparatus, the incisions
in the fascia and skin were closed separately, and the rats were placed
in recovery cages.
For the untreated rats, the specific effects of pliometric contractions
were compared with other types of contractions. Isometric contractions
(n = 3) or stretches of passive
muscles (n = 3) were substituted for
the pliometric contractions but with the same level of activation,
train rates, number of contractions, and rest periods used during the
pliometric contraction protocol.
Evaluation of Po.
For the untreated rats, the Po
values of the experimental and the contralateral control EDL muscles
were measured at 1 day (n = 6), 3 days
(n = 8), 7 days
(n = 7), 21 days
(n = 7), or 42 days
(n = 6) after the pliometric
contraction protocol, whereas, after protocols of isometric
contractions or stretches of passive muscles, the
Po values of the experimental and
the contralateral control muscles were measured only at 3 days. For all
vitamin E-treated and vehicle-treated rats, the
Po values of the experimental EDL
muscles were determined at either 3 h or 3 days. For EDL muscles in
each of the three groups, the Po
values measured after the contraction protocol are
presented as a force deficit (Fig.
1). For
Po values measured during the
first 7 days after a contraction protocol, the force deficit is the
postprotocol Po expressed as a
percentage of the preprotocol Po.
For the untreated rats, an increase in body mass, muscle mass, and
Po occurred during the 6 wk of
recovery. Consequently, after 7 days, the force deficit was calculated
from the Po of the contralateral
control muscle.
),
vehicle-treated (
), and vitamin E-treated (
) rats. Force deficits
after isometric contractions (
) and passive stretches (
) in
untreated rats are included. * Significant difference compared with initial force, P < 0.05.
Muscle and blood sampling. After the final measurements of force development in situ, with the EDL muscle completely exposed, the Lo was measured. Subsequently, both EDL muscles were removed from the rats. The estimated Lo and the measured Lo were within 3% of one another. The whole EDL muscles of untreated rats and the distal one-quarter of EDL muscles of vitamin E-treated and vehicle-treated rats were blotted, weighed, and frozen in isopentane cooled with dry ice for histological analysis. The remaining parts of the EDL muscles were frozen rapidly in liquid nitrogen for the additional biochemical assays. From each vitamin E-treated and vehicle-treated rat, part of the gastrocnemius muscle was removed and frozen rapidly in liquid nitrogen for vitamin E analysis. The gastrocnemius muscle was used for measurements of the muscle vitamin E content because the total masses of the exercised and control EDL muscles were required for biochemical analyses. Five milliters of blood were removed from the abdominal aorta to determine serum activities of the muscle-derived enzymes, CK and PK. The blood was centrifuged at 500 g, and the serum was removed and stored at
70°C. The anesthetized rat was euthanized with an
overdose of anesthetic.
Muscle histology.
Our direct assessments of muscle damage were made at 1 h in untreated
rats (n = 3) and at 3 days in
untreated, vehicle-treated, and vitamin E-treated rats. For the
assessment, cross sections were cut from each muscle and stained with
hematoxylin and eosin. In single sections of control and experimental
muscles, the number of damaged fibers was determined with a Leitz image
analyzer at a magnification of ×100. Fibers were classified as
intact or damaged. A damaged fiber was defined as a fiber that showed
excessive swelling, degenerative changes in the cytosol, or no
cytosolic elements with only a basement membrane remaining (15, 24). A
fiber was classified as intact if no evidence of damage was observed. The number of damaged fibers was expressed as a percentage of the total
number of fibers present in the cross-sectional area.
Biochemical analyses.
The serum CK and PK activities were determined spectrophotometrically
in the serum of nonexercised, vitamin E-treated, and vehicle-treated
rats as described previously (14). The vitamin E content of samples of
the gastrocnemius muscles was determined by using high-performance
liquid chromatography techniques as described by Phoenix et al. (20).
Definition of damage to muscles.
Following protocols of pliometric contractions, the severity of damage
has been assessed by a variety of morphological, biochemical, and
functional measures (8). We have assessed the magnitude of the damage
with a direct measure of the number of damaged fibers observed with
light microscopy of sections stained with hematoxylin and eosin and
with an indirect measure of the force deficit. Neither variable
provides an exact measure of the magnitude of the damage. Light
microscopy does not identify the focal damage to single sarcomeres
observed immediately after contraction-induced injury with electron
microscopy (2, 5, 11, 18) or with higher power microscopy of thick
sections (2). Furthermore, the focal nature of even the more severe
injury at 3 days results in an evaluation of damaged fibers in one
cross section underestimating the number of damaged fibers in all
possible cross sections (2, 8, 15). The force deficit provides a
measure of the totality of the functional impairment induced by all the
focal injuries to fibers throughout the muscle, but, immediately after
protocols of repeated pliometric contractions, the force deficit
reflects fatigue as well as injury. Recovery from fatigue is usually
complete within 3 h, well before the onset of secondary injury (10). Thereafter, the force deficit provides an indirect measure of the
totality of the damage, but if recovery from fatigue is delayed to 24 h
the force deficit may reflect both fatigue and secondary injury (8).
Statistical analysis.
For the untreated rats, differences in the force deficit after recovery
periods ranging from 30 min to 7 days were assessed by a one-way
analysis of variance. Significant differences among the
three groups in the body masses, contractile properties, and histological damage were determined at 3 h and 3 days after the pliometric contraction protocol by a one-way analysis of variance. A
two-way analysis of variance was used to test for significant differences in the serum CK and PK activities; the muscle vitamin E
content between the vitamin E-treated and the vehicle-treated groups;
and the force deficits of the untreated, vehicle-treated, and vitamin
E-treated rats at 30 min, 3 h, and 3 days after the protocol. In the
event of a significant F-statistic,
the Scheffé's post hoc test was used to test for significant
differences between means. The level of significance was set a priori
at P < 0.05. All values are
expressed as means ± SE.
RESULTS
For EDL muscles measured in situ in untreated, vehicle-treated, and vitamin E-treated 3- to 4-mo old Wistar rats, the absolute Po values were 3.7, 3.2, and 3.3 N, respectively. The values for the Po were in good agreement with previously published data on the EDL muscles of young Wistar rats measured in vitro (6). The higher absolute body masses, muscle lengths, and absolute Po values of the 4-mo-old untreated rats compared with the 3-mo-old treated rats simply reflect the normal growth of the rats during the 1-mo period (Table 1). Compared with the vehicle-treated and the vitamin E-treated groups, the slightly higher values for the absolute forces of the untreated group were proportional to the increases in body masses. The specific Po of 257 kN/m2 for the EDL muscles of young untreated rats measured in situ (Table 1) is not different from the values reported for EDL muscles in young mice measured in situ (4, 10) and in young rats measured in vitro (6). Specific Po values could not be calculated for the treated EDL muscles because of the need to immediately freeze the muscles for biochemical analyses.
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The pooled value for the vitamin E content of the gastrocnemius muscles of the vehicle-treated rats (n = 15) was 5.2 ± 0.6 µg/g wet wt and that of the vitamin E-treated rats (n = 18) was 14.7 ± 3.3 µg/g wet wt. No difference was observed between the values for the vitamin E-treated rats at 3 h (11.9 ± 2.5 µg/g wet wt) and 3 days (8.7 ± 2.0 µg/g wet wt). Our values for the vitamin E content of muscles from vehicle-treated and vitamin E-treated rats were slightly lower than the values for rats treated with 5 wk of dietary supplementation (23). Despite the lower absolute values, our value for a threefold increase after vitamin E treatment was in excellent agreement with the relative increase reported after dietary supplementation (23). We conclude that we have collected valid data on force and achieved adequate vitamin E supplementation.
In untreated rats, during the pliometric contraction protocol, the force deficit during the last pliometric contraction was 94 ± 1% (Fig. 1). By 30 min after the pliometric contraction protocol, the force deficit was 63 ± 2%. The force deficits were 54 ± 3, 64 ± 7, and 55 ± 9% at 1, 3, and 7 days, respectively. No differences were observed among the force deficits between 30 min and 7 days. Thereafter, the force deficit diminished gradually, reaching control values by 42 days. Thirty minutes after the protocols of isometric contractions and stretches of passive muscles, the force deficits were 14 ± 5 and 4 ± 4%, respectively. In contrast to the substantial force deficit after the pliometric contraction protocol, 3 days after either isometric contractions or stretches of passive muscles, the force deficits were not different from zero, with the Po values 100 ± 4 and 103 ± 3% of their respective control values. These observations on EDL muscles of rats are in agreement with the reports of McCully and Faulkner (15) and Faulkner et al. (10), who found that protocols of isometric contractions and of stretches of passive EDL muscles of mice, respectively, result in an immediate small force deficit due to fatigue but do not cause injury.
For the vehicle-treated and vitamin E-treated rats, no differences between the groups were observed in the force deficits developed at any time during the 5-min bouts of pliometric contractions. The force deficits at the end of the protocol, at 30 min, and at 3 days were not different among the three groups. In addition, no differences were observed between the force deficits of the vehicle-treated and vitamin E-treated rats at 3 h (Fig. 1).
For the contralateral control EDL muscles in each of the three groups (Fig. 2A) and in the EDL muscles 1 h after the pliometric contraction protocol (Fig. 2B), cross sections stained with hematoxylin and eosin did not show abnormalities. In contrast, by 3 days after the pliometric contraction protocol was administered to untreated, vehicle-treated, and vitamin E-treated rats, 38 ± 5, 32 ± 5, and 29 ± 5%, respectively, of the fibers were classified as damaged (Table 2, Fig. 2, C-E). By 21 and 42 days, the number of intact fibers in the experimental muscles of the untreated rats was not different from the control value, but 5% of the fibers had central nuclei.
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For the nonexercised rats, the serum CK activities of the vehicle-treated and vitamin E-treated rats were not different, but the serum PK activity of the vitamin E-treated rats was twofold greater than that of the vehicle-treated rats (Fig. 3). After the pliometric contraction protocol, the vehicle-treated rats showed a fourfold increase in the serum CK and PK activities at 3 h and a twofold increase at 3 days, whereas at both 3 h and 3 days after the protocol, the serum CK and PK activities of the vitamin E-treated rats were not different from those of the nonexercised rats (Fig. 3).
) and
vitamin E-treated (
) rats, either nonexercised or at 3 h or 3 days
after pliometric contractions. * Significant difference compared
with nonexercised rats, P < 0.05.
DISCUSSION
ACKNOWLEDGEMENTS
The authors thank Richard Hinkle and Cheryl Hassett for assistance.
FOOTNOTES
Address for reprint requests: J. A. Faulkner, Univ. of Michigan, Institute of Gerontology, Rm. 1056, 300 N. Ingalls, Ann Arbor, MI 48109-2007.
Received 4 March 1996; accepted in final form 6 May 1997.
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