Sports Med 2004; 34 (1): 49-69
0112-1642/04/0001-0049/$31.00/0
REVIEW ARTICLE
 2004 Adis Data Information BV. All rights reserved.
Neuromuscular Function After
Exercise-Induced Muscle Damage
Theoretical and Applied Implications
Christopher Byrne,1 Craig Twist2,3 and Roger Eston3
1
2
3
Centre for Human Performance, Defence Medical and Environmental Research Institute, DSO
National Laboratories, Republic of Singapore
Department of Sport & Exercise Sciences, North East Wales Institute of Higher Education,
Wrexham, UK
School of Sport Health and Exercise Sciences, University of Wales, Bangor, UK
Contents
Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49
1. Effects of Exercise-Induced Muscle Damage on Muscle Function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52
1.1 Effects on the Joint Angle-Torque Relationship . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52
1.2 Effects on the Torque-Angular Velocity Relationship . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53
1.3 Effects on Athletic Performance Measures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56
1.3.1 Power-Generating Ability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56
1.3.2 Vertical Jump Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57
1.3.3 Sprinting Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57
1.3.4 Endurance Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58
1.4 Effects on Neuromuscular Control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58
2. Theoretical Implications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59
2.1 Central Fatigue . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59
2.2 Excitation-Contraction Coupling Impairment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 60
2.3 Redistribution of Sarcomere Lengths . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 60
2.4 Selective Fibre Type Damage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
2.5 Impaired Metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62
3. Applied Implications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
3.1 Strength and Power Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
3.2 Endurance Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
3.3 Intermittent High-Intensity Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
4. Future Directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64
5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64
Abstract
Exercise-induced muscle damage is a well documented phenomenon particularly resulting from eccentric exercise. When eccentric exercise is unaccustomed
or is performed with an increased intensity or duration, the symptoms associated
with muscle damage are a common outcome and are particularly associated with
participation in athletic activity. Muscle damage results in an immediate and
prolonged reduction in muscle function, most notably a reduction in force-generating capacity, which has been quantified in human studies through isometric and
dynamic isokinetic testing modalities. Investigations of the torque-angular velocity relationship have failed to reveal a consistent pattern of change, with inconsistent reports of functional change being dependent on the muscle action and/or
angular velocity of movement. The consequences of damage on dynamic, mul-
50
Byrne et al.
ti-joint, sport-specific movements would appear more pertinent with regard to
athletic performance, but this aspect of muscle function has been studied less
often. Reductions in the ability to generate power output during single-joint
movements as well as during cycling and vertical jump movements have been
documented. In addition, muscle damage has been observed to increase the
physiological demand of endurance exercise and to increase thermal strain during
exercise in the heat. The aims of this review are to summarise the functional
decrements associated with exercise-induced muscle damage, relate these decrements to theoretical views regarding underlying mechanisms (i.e. sarcomere
disruption, impaired excitation-contraction coupling, preferential fibre type damage, and impaired muscle metabolism), and finally to discuss the potential impact
of muscle damage on athletic performance.
Exercise-induced muscle damage is a common
phenomenon resulting from the performance of unaccustomed exercise or exercise with an increased
intensity or duration. In this review, we classify
muscle damage as a state when one or more of the
direct or indirect indicators is present. The well
documented symptoms of muscle damage include
disruption of intracellular muscle structure, sarcolemma and extracellular matrix,[1-10] prolonged impairment of muscle function,[1,7,8,11-87] and delayed-onset muscle soreness (DOMS), stiffness and
swelling.[13,21,22,30,88-97] A particular component of
exercise, eccentric muscle action, is the principle
factor responsible for muscle damage. Active muscles may be referred to as performing isometric
(constant length), concentric (shortening) or eccentric (lengthening) actions.[91] Several early studies
clearly demonstrated that eccentric muscle actions
result in greater evidence of muscle damage than
isometric or concentric actions.[2,11,13,18,24] Subsequently, eccentric actions in the form of submaximal
and maximal voluntary- or electrically-stimulated
actions, with either a passive or unloaded active
(concentric) return to the start position, have been
employed in many studies to experimentally induce
muscle damage.
These forms of eccentric muscle action rarely
occur in isolation in natural human movement. Instead, natural muscle function occurs in a sequence
of active eccentric action followed by an active
concentric action, known as the stretch-shortening
cycle (SSC).[98,99] This natural form of muscle function is utilised when body segments are subjected to
impact or stretch, due to external forces such as
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gravity, and is utilised in non-sporting functional
activities and most sporting activities such as, running, jumping, throwing and weightlifting. The SSC
has a well recognised purpose: enhancement of performance during the final propulsive (concentric)
action when compared with the performance of an
isolated concentric action.[98,99] The mechanisms underlying performance enhancement during the SSC
and their relative contributions are highly debatable,
but four mechanisms have been identified: (i) the
time available to develop force; (ii) storage and
reutilisation of elastic energy; (iii) potentiation of
the contractile machinery; and (iv) contribution of
reflexes.[100,101] Eccentric actions actively contribute
to the SSC and, therefore, it is not surprising that
muscle damage is a common occurrence during
prolonged or intense exercise involving the SSC,
such as distance running,[14,48,102-105] plyometrics[37,53,106] and resistance training.[7,24,78,79,107]
It is estimated that approximately 10 000 SSC
muscle actions take place during a marathon race.[57]
Running downhill increases the contribution of eccentric actions to performance and is a greater stimulus for damage than level or uphill running.[108]
Intense or prolonged running, plyometrics and resistance exercise are inherent components of training
and competition for most athletes. Moreover, exercise-induced muscle damage occurs frequently in
athletic populations, especially during periods of
overreaching or overtraining.[109-111] Of greatest concern to the athlete is the loss of muscle function that
accompanies muscle damage and will result in under-performance. The aims of this review are to
summarise the functional decrements associated
Sports Med 2004; 34 (1)
Neuromuscular Function After Exercise-Induced Muscle Damage
with exercise-induced muscle damage, relate these
decrements to theoretical views regarding underlying mechanisms, and finally to discuss the potential
impact of muscle damage on athletic performance.
Eccentric muscle actions possess several unique
features,[112] which potentially explain why performance of these actions often results in damage to the
muscle. The classic in vitro force-velocity relationship of maximally activated muscle indicates that
force generated during an eccentric action is 1.5–1.9
times greater than isometric force.[113-117] Although
the in vivo torque-velocity relationship of human
muscle differs due to neural inhibition of maximal
eccentric actions,[115,116] well motivated individuals
can achieve greater torques during a maximal voluntary eccentric versus an isometric or concentric action.[112] Furthermore, motor unit activation (as assessed by electromyography) is lower for maximal
eccentric versus isometric or concentric actions and
less motor unit activation is required for a given
force under eccentric conditions.[112,116,118,119] This
combination of high force and low fibre recruitment
places a high mechanical stress on the involved
structures and has been implicated as a causative
factor in muscle damage.[112] Enoka[112] suggested
that such a loading profile might take the form of a
lower level of activation distributed across the entire
population of motoneurons or the activation of only
a subset of the entire population (e.g. type II fibres,
see section 2.4). Although differences in the recruitment order of motor units between concentric and
eccentric actions have been observed,[120,121] an alteration in the recruitment order of motor units does
not appear to be a general control strategy for eccentric actions.[122] The mechanism of force generation
during an eccentric action also differs, whereby the
cross-bridges are detached mechanically rather than
undergoing a detachment that involves adenosine
triphosphate (ATP) splitting, as with concentric actions.[122,123] The compliant portion of individual
cross-bridges is also stretched further during an eccentric versus an isometric action.[122,123] There also
seems to be a length-dependent factor involved in
the damaging process, since eccentric actions performed at long muscle length result in greater evidence of damage than those performed at short
muscle length.[17,49]
 2004 Adis Data Information BV. All rights reserved.
51
It is widely believed that eccentric exercise-induced muscle damage is initiated by
mechanical factors.[6,9,10,18,124-126] Force produced
during eccentric actions and magnitude of strain (i.e.
change in length as a function of initial length [%])
appear important mechanical factors determining
muscle damage. This concept is straightforward
when considering the loading profile and range of
motion associated with high force eccentric actions,
such as those used in plyometrics and resistance
training. However, other factors (e.g. metabolic depletion, calcium influx, generation of reactive oxygen species, musculo-tendonous stiffness regulation) may initiate or contribute to the damaging
process,[99,127,128] particularly when considering
damage resulting from prolonged low force eccentric actions, such as with distance running. Initial
manifestations of damage are disrupted sarcomeres
and damage to components of the excitation-contraction (E-C) coupling system.[125,126,129] After these
initial events there follows a process of muscle fibre
degeneration and regeneration, which has been described in detail elsewhere.[3,91-95,97,124,128] During
these stages, the transient symptoms of DOMS,
muscle stiffness, and muscle swelling appear and
subside. These symptoms are mediated by the inflammatory response that accompanies muscle fibre
damage and causes a transfer of fluid and cells to the
affected muscles for the removal of damaged contractile proteins and cellular debris, before regeneration begins.[36,94,130]
Muscle soreness is the most commonly used
marker of exercise-induced muscle damage in
human studies,[131] is probably the most well recognised indicator of damage among athletic populations, and yet shares a poor temporal relationship
with histological evidence of muscle damage[3] and
measures of muscle function.[13,30,83] Objective measures of soreness have been gained by using a ‘myometer’ to measure the applied force to a muscle
group at the pain threshold[13,17,18,22,51,90] and subjective measures of soreness have been gained by numerical scales, questionnaires and visual analogue
scales.[21,25,28,30,82] Both forms of measurement have
demonstrated that muscle soreness following eccentric exercise has a characteristic time course. Exercised muscles are pain-free for approximately 8
hours and then soreness increases and peaks over the
Sports Med 2004; 34 (1)
52
Byrne et al.
next 24–48 hours.[13,17,18,21,22,90] Jones and Round[123]
observed that after intense eccentric exercise, a person will go to bed with only minor discomfort but
will wake the next morning with severe, and in some
cases almost disabling pain, first appreciated when
trying to get out of bed. All discomfort usually
subsides within 96 hours.[90,93] Thus, the term
‘DOMS’ is appropriate in describing the typical
time course of the sensation but conveys little about
the nature of the sensation.[90] The sensation of
soreness comprises muscle tenderness, pain on palpation, and also mechanical stiffness in the muscle
that results in pain when the muscle is passively
stretched or activated.[21,90,93]
DOMS should not be used as an indicator of the
magnitude of muscle damage or functional impairment, since function is impaired before soreness
arises and damage becomes worse when soreness
has dissipated.[3,30,83] Muscle function can also remain impaired when soreness has dissipated and this
could lead to practical problems if the dissipation of
DOMS is used as a signal to resume normal training
when the muscle is in a weakened state. DOMS is
believed to arise from damage and inflammation of
non-contractile connective tissue,[18,90] which gives
rise to painful sensations when the muscle is palpated, stretched or activated.
1. Effects of Exercise-Induced Muscle
Damage on Muscle Function
In a recent review of the measurement tools used
in the study of eccentric exercise-induced muscle
damage, Warren et al.[131] suggested that measures
of muscle function provide the most effective means
of evaluating the magnitude and time course of
damage resulting from eccentric muscle actions.
Functional impairments (e.g. reductions in strength
and power) are immediate, prolonged, and perhaps
the most important symptom of damage when considering athletic performance in the presence of
muscle damage.
1.1 Effects on the Joint
Angle-Torque Relationship
Measures of isometric strength have been the
most widely used method of determining muscle
function after eccentric exercise.[131] The method
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involves the study participant performing a maximal
voluntary contraction (MVC) of a muscle group at a
fixed joint angle for 2–5 seconds to determine
muscle strength. In general, isometric strength is
reduced immediately post-eccentric exercise and recovery is gradual and prolonged. The magnitude and
time course of strength loss appear dependent on the
training history of the muscle group, with the greatest and longest lasting strength loss consistently
observed in the relatively inactive elbow flexors[22,28,76] versus the locomotory muscles of the
lower limbs.[11,12,49]
Clarkson et al.[21] reported that a typical response
to maximal eccentric exercise of the elbow flexors
was an immediate 50–60% reduction in strength
followed by a linear recovery to baseline by 2 weeks
post-exercise. However, further studies have reported much longer time courses of recovery. Howell et
al.[28] reported an immediate 35% loss of strength
following submaximal eccentric exercise of the elbow flexors and suggested that the half-time of
recovery may be as long as 5–6 weeks. More recently, Sayers and Clarkson[76] measured strength loss
and recovery of the elbow flexors in 192 volunteers
(98 males, 94 females) after 50 maximal voluntary
eccentric muscle actions of the non-dominant arm.
On average, strength was reduced by 57% immediately post-exercise and remained 33% lower at 5.5
days. No differences were apparent between males
and females. Approximately 20% (n = 32) of the
sample demonstrated strength loss exceeding 70%,
with the majority of these study participants demonstrating some recovery by 5.5 days, but not fully
recovering strength by 26 days post-exercise. Interestingly, 24 out of the 32 study participants were
female, suggesting that some females may be more
susceptible to greater initial reductions in strength
than males. However, these same females recovered
strength more rapidly than males with an equivalent
strength deficit. A minority of the sample (n = 9)
demonstrated severe strength loss (>70%) and little
recovery by 5.5 days. When these study participants
were monitored until full recovery, the time course
varied between 33 and 89 days. Of note, two male
study participants recorded the longest recovery of
strength (61 and 89 days). These results demonstrate
that for relatively inactive muscle groups, such as
the elbow flexors, the magnitude of strength loss
Sports Med 2004; 34 (1)
Neuromuscular Function After Exercise-Induced Muscle Damage
following eccentric exercise-induced muscle damage can be dramatic and recovery can take up to 12
weeks. Sayers and Clarkson[76] suggested that some
individuals displaying protracted recovery periods
may be predisposed to a prolonged inflammatory
response that may contribute directly to the prolonged impairment of muscle function.
The knee and ankle extensors also demonstrate
immediate and prolonged reductions in isometric
strength following exercise-induced muscle damage, although the magnitude of strength loss is usually less than that observed for the elbow flexors.
Early work by Komi and Viitasalo[11] demonstrated
a 35% reduction in knee extensor strength and a
decrease in the rate of force development, which had
not recovered 2 days after 40 maximal eccentric
actions performed on a leg press apparatus. Recent
work by Byrne and Eston[79] demonstrated a
30–40% reductions in knee extensor strength with
recovery incomplete (approximately 95%) 7 days
after 100 repetitions of the eccentric phase of the
barbell squat exercise performed with a load of 80%
of concentric one repetition maximum. Following
marathon running, Avela et al.[53] reported a 30%
reduction in ankle extensor strength and rate of force
development with full recovery by 2 and 4 days
post-race, respectively. Other studies have documented the acute fatigue effects of long-distance
endurance exercise on isometric strength but have
not monitored recovery.[132-137] For example, reductions of 10%, 26% and 30% have been reported in
the knee extensors immediately following an 85km
cross-country ski race,[132] a 42.2km marathon,[134]
and a 65km ultramarathon race,[137] respectively.
The consistent findings from research investigating
the effects of eccentric exercise or prolonged SSC
exercise on locomotory muscle groups are an immediate and prolonged reduction in strength and a
decreased rate of force development. The apparent
inconsistencies in the magnitude of strength loss and
length of recovery between the elbow flexor and
knee extensor muscle groups is possibly due to the
severity of the initial damage, as a result of more
severe damage-inducing exercise (maximal versus
submaximal eccentric), and less natural activation of
the elbow flexors during everyday activity.
Examination of isometric strength as a function
of joint angle has revealed that relative strength loss
 2004 Adis Data Information BV. All rights reserved.
53
is not uniform across joint angles. Several investigations have revealed a disproportionate loss of
strength at joint angles corresponding to short versus
optimal or long muscle lengths.[39,49,66,79] Furthermore, a shift to the right of the optimal angle for
torque generation has been shown to occur after
eccentric exercise, providing direct evidence of a
shift in the length-tension relationship towards longer muscle lengths for maximal force generation.[43,52] Such findings lend support to the concept
that a longer muscle length is needed to achieve the
same myofilament overlap and hence force production after eccentric exercise due to an increase in
series compliance as a result of overextended
sarcomeres.[125,126] It is unclear whether the shift in
optimal angle persists as long as the reduction in
strength[39] or reverses whilst strength remains reduced.[43,49,79] Nevertheless, these consistent findings suggest that strength loss will be exacerbated
when muscle groups are activated at shortened
lengths after eccentric exercise. For example, when
the knee extensors are activated and the knee joint is
close to full extension or when the elbow flexors are
activated and the elbow joint is close to full flexion.
1.2 Effects on the Torque-Angular
Velocity Relationship
Several studies have used isokinetic dynamometry to investigate whether strength loss after eccentric exercise-induced muscle damage is dependent
on the muscle action being performed (i.e. isometric, concentric, eccentric; see table I).[8,24,78,80] When
isometric strength and concentric and eccentric
strength at a single angular velocity of movement
are compared, there appears to be no significant or
meaningful differences in the magnitude of strength
loss or the rate of recovery across muscle actions.[8,78,80] Isokinetic dynamometry has also been
employed to examine whether strength loss and rate
of recovery are dependent on the angular velocity of
movement (see table I). Conflicting results have
emerged from these studies, with several authors
reporting strength at higher angular velocities of
movement to be affected to a lesser extent than
either slower angular velocities of movement or
isometric strength. For example, Michaut et al.[80]
reported that immediately after 50 maximal eccentric actions of the elbow flexors, isokinetic concenSports Med 2004; 34 (1)
54
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Table I. Studies investigating dynamic muscle function by isokinetic dynamometry after exercise-induced muscle damage
Study
Muscle group
Study
participants
Activity
Muscle action
Angular velocity
(rad/sec)
Recovery
Comments
Friden et al.[1]
Knee extensors
12M
30 min eccentric cycle
ergometer
Isometric,
concentric
1.57, 3.14, 5.24
Isometric and
concentric 1.57 and
3.14 rad/sec recovered
by D6. Strength at 5.24
rad/sec not recovered
by D6
Slower recovery at
higher angular velocity.
Biopsy evidence of
selective type II fibre
damage
Sherman et
al.[14]
Knee extensors
10M runners
42.2km marathon 175.7 ± 20.4
min
Concentric
1.1, 3.2, 5.3
Greater than 7 days for
all velocities
Recovery more rapid
with rest vs exercise in
week after marathon
Golden and
Dudley[24]
Knee extensors
8M
100 eccentric actions at 85% of
eccentric 1RM (10 sets × 10
reps)
Isometric,
concentric,
eccentric
1.05, 3.14
Isometric and eccentric
at 1.05 and 3.14 rad/
sec by D7. Concentric
1.05 rad/sec by D10,
concentric 3.14 rad/sec
not recovered by D10
Slower recovery for
concentric actions
particularly at high
angular velocity
Gibala et al.[7]
Elbow flexors
8M untrained
64 eccentric actions at 80% of
concentric 1RM (8 sets × 8
reps)
Isometric,
concentric
0.52, 3.14
By D4 for 3.14 but not
0.52 rad/sec
Slower recovery at
lower angular velocity
Knee extensors
10M
40 min downhill (–10%
gradient) running (5 × 8 min) at
80% HRmax
Concentric,
eccentric
0.52, 2.83
By D4 for eccentric
0.52 rad/sec. By D7 for
eccentric 2.83 rad/sec
Slower recovery of
eccentric strength at
higher angular velocity
Hortobagyi et
al.[8]
Knee extensors
12 (6M, 6F)
moderately
active
100 eccentric actions at 80% of
eccentric 1RM (10 sets × 10
reps)
Isometric,
concentric,
eccentric
1.04
No difference in rate of
recovery. Greatest
deficit at D2, complete
recovery by D7
Greater decline in
isotonic eccentric
versus concentric (58%
vs 39%) 1RM at D2
post-exercise
Deschnes et
al.[60]
Knee extensors
9M untrained
100 maximal isokinetic
concentric/eccentric actions at
0.53 rad/sec (4 sets × 25 reps)
Isometric,
concentric
1.09, 3.14
Concentric 3.14 rad/sec
not affected. Isometric
by D7, concentric 1.09
rad/sec by D2
Muscle function
preserved at high
angular velocity
Byrne et al.[66]
Knee extensors
8 (5M, 3F)
moderately
active
100 maximal isokinetic
eccentric actions at 1.57 rad/
sec (10 sets × 10 reps)
Isometric,
concentric
0.52, 3.14
No differences in
recovery. Approx. 90%
for isometric, 0.52 and
3.14 at D7
No muscle action- or
velocity-dependent
effect observed
Eston et al.
[35]
Byrne et al.
Sports Med 2004; 34 (1)
Continued next page
Immediate postexercise measurements
only
(–22.3 ± 8.1%)
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D = day post-eccentric exercise; F = females; HRmax = maximum heart rate; M = males; reps = repetitions; RM = repetition maximum.
Muscle function
preserved at high
angular velocity
Concentric 4.19 rad/sec
reduced to a lesser
extent (–12.5 ± 8.9%)
vs concentric 1.05 rad/
sec (–18.5 ± 6.1%),
isometric (–20.8 ±
11.2%), and eccentric
1.05 rad/sec
Concentric
1.05, 4.19.
Eccentric 1.05
Isometric,
concentric,
eccentric
50 maximal isokinetic eccentric
actions at 1.05 rad/sec (5 sets
× 10 reps)
10M active
Michaut et al.[80] Elbow flexors
No muscle actiondependent effect
observed
No differences in
recovery. Complete by
D7
1.57
Isometric,
concentric,
eccentric
100 eccentric actions at 70%
body mass load (10 sets × 10
reps)
Knee extensors
Byrne and
Eston[78]
8 (5M, 3F)
moderately
active
Muscle group
Study
Table I. Contd
Study
participants
Activity
Muscle action
Angular velocity
(rad/sec)
Recovery
Comments
Neuromuscular Function After Exercise-Induced Muscle Damage
55
tric strength at 4.19 rad/sec was reduced to a lesser
extent (12.5 ± 8.9%) than either concentric (18.5 ±
6.1%) or eccentric strength (22.3 ± 8.1%) at 1.05
rad/sec and isometric strength (20.8 ± 11.2%). Similarly, Deschnes et al.[60] reported that following eccentric exercise of the knee extensors, isokinetic
concentric strength at 3.14 rad/sec was not significantly reduced whereas concentric strength at 1.09
rad/sec was reduced until 2 days post-exercise and
isometric strength reduced until 7 days post-exercise. Gibala et al.[7] reported a faster restoration of
isokinetic concentric strength at a higher angular
velocity (3.14 rad/sec) than either a slower angular
velocity (0.52 rad/sec) or isometric strength following eccentric exercise of the elbow flexors.
In contrast to the studies demonstrating a preservation of strength at higher angular velocities of
movement, several studies have reported either no
differences or a slower restoration of strength at
higher angular velocities of movement. Byrne et
al.[66] reported that isometric strength and concentric
strength at 0.52 and 3.14 rad/sec were affected to a
similar extent in terms of magnitude and rate of
recovery following eccentric exercise of the knee
extensors. Also, following a marathon race, Sherman et al.[14] reported no differences in the magnitude of strength loss or rate of recovery of knee
extensor concentric strength at 1.1, 3.2, and 5.3 rad/
sec. However, Golden and Dudley[24] reported that
despite similar initial strength decrements, isometric
and concentric and eccentric strength at 1.05 and
3.14 rad/sec demonstrated contrasting recovery patterns. Concentric strength was slower to return to
baseline and this was most evident at the higher
angular velocity of 3.14 rad/sec. For isokinetic eccentric strength, Eston et al.[35] reported a slower
restoration of strength at 2.79 versus 0.52 rad/sec.
Earlier work by Friden et al.[1] suggested a slower
restoration of strength only at a very high angular
velocity of movement. Following eccentric exercise
of the knee extensors, isometric strength and concentric strength at 1.57 and 3.14 rad/sec had returned to baseline by day 6 post-exercise, whereas
concentric strength at 5.24 rad/sec was still significantly reduced.
At present, the torque-velocity relationship appears to be affected in one of three possible ways: (i)
similar relative decreases in isometric strength and
Sports Med 2004; 34 (1)
56
Byrne et al.
concentric and eccentric strength across angular velocities; (ii) velocity-dependent strength loss with
high angular velocity torque being affected to a
greater extent than isometric and low angular velocity torque; or (iii) velocity-dependent strength loss
with high angular velocity torque being affected to a
lesser extent than isometric and low angular velocity
torque. Evidence that strength decrements are greatest at higher angular velocities[1,24,35] supports the
notion that type II fibres may be selectively damaged during eccentric exercise (see section 2.4).
However, evidence that strength decrements are less
at higher,[7,60,80] compared with lower angular velocities, contradicts this notion. The contrasting results
possibly reflect differences in damage-inducing protocols, whether selective damage occurred and/or
the sensitivity of isokinetic dynamometers to detect
functional changes in muscle composition. Although isokinetic dynamometry has provided a useful tool for the study of dynamic muscle function
after damaging exercise, the utility of the technique
is limited when we wish to extrapolate to the sporting context. Isokinetic dynamometers are compromised in their ability to replicate sport-specific
movement velocities and multi-joint movements,
being limited to angular velocities up to approximately 7 rad/sec and single joint movements, whereas movement velocities can be approximately 17
rad/sec for knee flexion during sprinting.[138]
1.3 Effects on Athletic
Performance Measures
1.3.1 Power-Generating Ability
The ability to generate power is an aspect of
human muscle function that has received limited
attention after exercise-induced muscle damage.
The major concern for the athlete is if a selective
loss of concentric and eccentric strength at high
angular velocities of movement occurs, as reported
by some studies of the torque-velocity relationship.[1,24,35] This would render the affected muscle(s)
markedly less powerful at the velocities of movement associated with athletic events.
Sherman et al.[14] were perhaps the first to measure maximal dynamic exercise performance after a
bout of damage-inducing exercise. These authors
employed a maximal work capacity test consisting
 2004 Adis Data Information BV. All rights reserved.
of 50 maximal leg extensions at 3.2 rad/sec and
reported a 47% reduction in work capacity immediately after a marathon race in ten trained male
runners. Interestingly, five study participants who
performed daily ‘recovery’ exercise in the week
post-marathon, consisting of 20–45 minutes of running per day at 50–60% maximal oxygen uptake
(V̇O2max), did not achieve full recovery of maximal
work capacity by day 7, whereas the five who performed no exercise recovered fully by day 3. The
practical question of whether to rest or perform
recovery exercise after muscle damage remains unresolved. Recent research using the elbow flexors
reported that recovery of isometric strength was
facilitated by both recovery exercise and immobilisation, suggesting that more than one mechanism of strength recovery may be operating after
damaging exercise.[64] Another early study by Sargeant and Dolan[16] measured knee extensor peak
power output during maximal 20-second isokinetic
cycling at 80 and 110 revolutions per minute (rpm).
Reductions in peak power of 15–20% were apparent
immediately after eccentric exercise and remained
for 2 days at 80 rpm and for over 4 days at 110 rpm.
The longer recovery period at the higher movement
velocity would seem to suggest a selective loss of
performance at high angular velocities of movement.
More recently, Byrne and Eston[79] reported immediate and prolonged reductions in peak power
during a 30-second Wingate cycle test. The reductions in power output were the direct result of an
inability to achieve a high pedal frequency since the
external load remained constant before and after
eccentric exercise. Moreover, the recovery pattern
of peak power was different to that of isometric
strength. Whereas isometric strength demonstrated a
linear recovery, peak power demonstrated further
decrements at days 1 and 2 post-exercise before
recovering linearly (figure 1). These results suggest
that muscle power, unlike strength, may be affected
by DOMS and the inflammatory response to exercise-induced muscle damage. In contrast, Malm et
al.[139] reported no significant change in Wingate
30-second cycle test performance and an unexpected improvement in intermittent maximal intensity
cycle performance (10 × 10 seconds of all-out cycling interspersed with 50-second rest periods) folSports Med 2004; 34 (1)
Strength/power (% of pre-exercise values)
Neuromuscular Function After Exercise-Induced Muscle Damage
100
90
Strength
Power
*
**
*
Post
D1
*
*
D2
D3
80
70
60
50
D7
Time after exercise
Fig. 1. Loss and recovery of isometric knee extensor strength and
Wingate peak power after eccentric exercise-induced muscle damage. Values are means (± standard error) expressed as a percentage of pre-exercise values (reproduced from Byrne and Eston,[79]
with permission). D = day post-eccentric exercise; Post = 1h post
muscle-damaging exercise; * indicates a significant difference for
both strength and power from pre-exercise values, p < 0.05; **
indicates a significant difference between the loss of strength and
power, p < 0.05.
lowing eccentric exercise of the knee extensors.
However, the eccentric exercise protocol employed
in this study may not have been sufficiently intense
to produce functional changes, judging by the absence of an increase in creatine kinase and only
moderate muscle soreness.
Miles et al.[44] reported an immediate and prolonged impairment of the ability of damaged muscle
to generate rapid force. During unloaded maximal
velocity concentric movements of the elbow flexors
in response to a light stimulus, increases were observed for movement time and the time to reach
peak velocity, with a gradual slowing of peak velocity. Peak velocity slowed by approximately 3.5 rad/
sec (25%) at 4 days post-exercise. Interestingly, premotor time, representing central processing time,
was unchanged. Such findings are consistent with a
change in the force-velocity relationship towards
slower muscle and the notion of selective type II
fibre damage.
1.3.2 Vertical Jump Performance
Komi and colleagues[37,53,57,99,132,134,135,140,141]
have extensively studied the effect of short- and
long-lasting SSC exercise on neuromuscular performance during a drop jump from approximately
 2004 Adis Data Information BV. All rights reserved.
57
50cm height (for review see Komi[99]). When muscle
damage was induced through intense plyometric
exercise or through marathon running, prolonged
reductions in maximal force and electromyographic
activity, ground reaction forces, stretch-reflex sensitivity, muscle and joint stiffness regulation and drop
jump performance were observed.[53,57,134,135] The
recovery process was shown to occur in a bimodal
pattern with an initial dramatic reduction in performance followed by an early recovery before secondary reductions in performance at 2–3 days postexercise.[53,57] The secondary decline in performance
observed in these studies was suggested as being
associated with the well documented inflammatory
response to muscle damage. These studies have
demonstrated that damaged muscle has a reduced
tolerance to impact forces during an SSC movement.[97] During a drop jump, there is an increased
contact time during breaking and push-off phases
due to decreased strength, reflex activity and initial
stiffness. Work is increased during the push-off
phase resulting in reduced efficiency and the potential to accelerate fatigue during repeated SSC actions.[53,57,134,135]
Byrne and Eston[79] recently investigated the effect of exercise-induced muscle damage on vertical
jumping performance with and without use of the
SSC. Reductions in vertical jumping performance
were immediate, long lasting (up to 4 days), and
dependent on the type of jump performed (see figure
2). Interestingly, jump performance was affected to
a greater extent under squat jump conditions (no
SSC) than in the countermovement or drop jump
(with SSC). Similar results have been observed after
intensive plyometric exercise[142] and after an ultramarathon foot race.[48] These results suggest that
the SSC possibly attenuates the detrimental performance effects associated with exercise-induced
muscle damage.
1.3.3 Sprinting Performance
Semark et al.[51] studied the effects of exerciseinduced muscle damage on sprint performance. Using a single sprint effort, assessed at 5, 10, 20 and
30m from a standing start, there was no evidence to
suggest that muscle damage had a detrimental effect
on sprint time or acceleration. Although muscle
soreness was evident, serum creatine kinase meaSports Med 2004; 34 (1)
58
Byrne et al.
Height (% of pre-exercise values)
100
*
*
CMJ
DJ
95
90
85
SJ
Fig. 2. Average reduction in squat jump (SJ), countermovement
jump (CMJ), and drop jump (DJ) performance (% of pre-exercise
values) over a 7-day period following eccentric exercise-induced
muscle damage. Vertical jumping performance was assessed with
(CMJ, DJ) and without (SJ) use of the stretch-shortening cycle.
Values are means (± standard error) [reproduced from Byrne and
Eston,[78] with permission] . * indicates a significantly greater preservation of CMJ and DJ than SJ performance.
surements demonstrated no significant change over
the assessed time period. It is therefore possible that
the protocol may not have induced sufficient muscle
damage to influence performance.
1.3.4 Endurance Performance
An elevated physiological response to endurance
exercise has been reported after muscle damaging
exercise.[143,144] When six untrained male study participants performed 15 minutes of sub-maximal
cycle ergometer exercise at 80% V̇O2max, exercise
values for minute ventilation, breathing frequency,
respiratory exchange ratio, heart rate, and rating of
perceived exertion were all significantly higher 2
days after eccentric exercise when compared with
the corresponding values 2 days after concentric
exercise.[143] Furthermore, post-exercise venous
blood lactate and plasma cortisol were also significantly higher when sub-maximal exercise was performed after eccentric versus concentric exercise.
The same authors also observed an elevated blood
lactate response to incremental cycle ergometer exercise performed 2 days after eccentric exercise;[144]
however, no differences were observed for V̇O2max
or endurance time. In both of these studies, no
difference in sub-maximal oxygen consumption
(V̇O2) was observed after eccentric exercise, suggesting that exercise efficiency was unaltered. These
 2004 Adis Data Information BV. All rights reserved.
results demonstrate that most, but not all, physiological responses to endurance exercise were amplified
when muscle damage was present. The loss of
muscle function and SSC efficiency through repetitive SSC actions, as occurs in the quadriceps and
calf muscles during running (see section 1.3.2), may
directly contribute to fatigue during prolonged exercise.[99,145]
Muscle damage has also been shown to alter
thermoregulation during exercise in the heat.[146] In
comparison to pre-exercise values, core temperature
was elevated by 0.2–0.3°C and heart rate by 12
beats/min during 50 minutes of treadmill walking at
an intensity of 45–50% V̇O2max and in environmental conditions of 40°C and 20% relative humidity,
performed 2 and 6–7 hours after lower body eccentric exercise. Exercise was also associated with
greater heat storage and energy expenditure, suggesting a decreased economy of walking. These
changes had subsided at 26 hours post-eccentric
exercise, although the elevated heart rate response
still remained. The authors suggested that the altered
thermoregulatory and cardiovascular responses
were modest and highlighted that the largest individual increase in core temperature (0.4°C) was equivalent to what would be expected from an individual
hypohydrated by 2–3% (bodyweight loss). However, the attainment of a critical core temperature
may be the rate-limiting factor when endurance exercise is performed in an uncompensable hot environment,[147,148] and thus even a modest elevation of
core temperature would reduce the capacity for heat
storage and be a potential disadvantage to the athlete.
1.4 Effects on Neuromuscular Control
A reduction in neuromuscular efficiency of the
knee extensors has been observed after eccentric
exercise.[11,60] This is reflected as a decrease in the
force : integrated electromyographic (iEMG) activity ratio, resulting in a greater central activation
(nervous stimulation) being required for the
achievement of a sub-maximal or maximal force.
Deschenes et al.[60] recently reported that the increased iEMG was localised to the rectus femoris
where soreness was focussed. Furthermore, the impairment in neuromuscular efficiency was demonstrated to outlast other symptoms of damage such as
Sports Med 2004; 34 (1)
Neuromuscular Function After Exercise-Induced Muscle Damage
strength loss, muscle soreness and increased circulating levels of myofibre proteins.
Proprioception (perception of voluntary force
and joint position) has recently been demonstrated
to be impaired after eccentric exercise. In forcematching tasks using the eccentrically exercised elbow flexors, study participants consistently undershot the target force being produced by the unexercised contralateral arm, thus perceiving they were
producing more force than was recorded.[34,40,44] The
error in force sense appears proportionate to the
extent of strength loss, suggesting that a central
compensatory mechanism is active. For example, a
50% strength loss would result in a given force postexercise being perceived equivalent to twice that
force pre-exercise. When study participants attempted to match joint angles being produced by the
non-exercised arm, the eccentrically exercised arm
has been reported to adopt either a more extended
position[40] or a more flexed position.[34] Thus, study
participants perceived the eccentrically exercised
muscles to be shorter or longer than they actually
were. Motor skill and learning during a one-dimensional visual pursuit tracking-task, was also shown
to be detrimentally affected by eccentric exercise of
the elbow flexors.[50] These studies demonstrate that
it is not only the force-generating capacity of muscle
that is affected by muscle damaging exercise but
also motor control.
2. Theoretical Implications
Sites and mechanisms of failure in the neuromuscular system responsible for altered muscle function
after eccentric exercise have been identified and
demonstrated to be located peripherally (i.e. E-C
coupling failure, redistribution of sarcomere
lengths, damage to contractile machinery, impaired
metabolism) rather than centrally. Potential mechanisms for the reduction in maximal force-generating capacity have been reviewed in detail elsewhere.[125,126,129] However, previous reviews have
made little or no attempt to relate the functional
decrements and the underlying mechanisms with
practical implications for athletic performance.
Moreover, rate-limiting mechanisms identified from
animal muscle preparations without neural input or
human muscle activated voluntarily at a fixed joint
angle may not directly translate to athletic perform 2004 Adis Data Information BV. All rights reserved.
59
ance, which requires the activation and co-ordination of the contractile machinery of many muscle
groups under dynamic conditions. Under such conditions, consideration must be given to the contribution of central fatigue and neuromuscular control.
Their contribution to the loss of muscle function is
likely to be greater than that previously determined
from single joint isometric actions.
2.1 Central Fatigue
A reduction in voluntary activation during the
performance of maximal exercise might be expected
after eccentric exercise, due to inhibition caused by
the presence of muscle soreness, swelling and stiffness. Voluntary activation after eccentric exercise
has been studied during isometric MVCs by using
the twitch interpolation technique.[15,39,149] This
technique involves the delivery of single electrical
impulses to the active muscles through surface electrodes over the muscle belly or motor nerve during
the performance of a MVC and when the muscle is
relaxed. Sensitive force measurement allows for the
determination of any additional force increment in
response to the electrical impulse and a measure of
voluntary activation can be gained by a simple ratio:[150,151]
Voluntary activation (%) = 100 (1 – Tinterpolated/
Tcontrol)
where T = twitch force (N). Any additional force
produced by the superimposed electrical impulse is
the result of incomplete (<100%) voluntary activation and highlights the presence of central fatigue.
Evidence from studies employing this technique
have suggested that full voluntary activation can be
achieved during isometric MVCs following eccentric exercise-induced muscle damage.[15,39,149]
Saxton and Donnelly[39] also reported that the disproportionate loss of strength at short muscle length
observed in their study was not due to a reduction in
voluntary activation. In the study of Gibala et al.,[7]
volunteers were unable to achieve full voluntary
activation before eccentric exercise; however, the
level of voluntary activation did not change in the
days following eccentric exercise. Therefore, these
findings suggest that the immediate and prolonged
loss of isometric strength after eccentric exercise is
caused by factors at or distal to the neuromuscular
junction (i.e. peripheral mechanisms). However,
Sports Med 2004; 34 (1)
60
Byrne et al.
caution should be expressed when interpreting the
results of twitch interpolation since the methodology employed in some studies may have lacked sufficient sensitivity to detect small increments in force
and thus small failures in voluntary drive.[150,151] It is
not known whether central fatigue contributes to the
reductions in isokinetic concentric and eccentric
strength observed after eccentric exercise. Recent
research suggests that maximal or near maximal
voluntary activation can be achieved in the fresh
state during concentric muscle actions of the elbow
flexors up to angular velocities of 5.24 rad/sec.[152]
In contrast, neural inhibition prevents full voluntary
activation during maximal eccentric actions.[115-118]
Whether full voluntary activation can be achieved or
whether inhibition occurs in the presence of muscle
damage during concentric and eccentric actions
across a range of angular velocities, remains to be
determined.
2.2 Excitation-Contraction
Coupling Impairment
E-C coupling is the sequence of events that starts
with the passage of the action potential along the
plasmalemma and ends with the release of calcium
from the sarcoplasmic reticulum.[153] A reduced efficiency of the E-C coupling process has been demonstrated after eccentric exercise in humans through
the use of the force frequency relationship. The
force frequency relationship, which is a plot of the
force produced (y-axis) when a muscle is stimulated
with a range of frequencies (x-axis), demonstrates
relatively greater losses of force at low frequencies
(10–20Hz) compared with high frequencies
(50–100Hz) following eccentric exercise.[154] This
low frequency fatigue has a time course of recovery
similar to isometric strength loss, taking hours, days
or even weeks.[12,13,16,18] Early explanations for lowfrequency fatigue suggested that less calcium is
released per action potential, possibly due to damage to components of the E-C coupling system.[155,156] More recent animal experiments have
focussed on the relationship between E-C coupling
failure and the loss of maximal force-generating
capacity.[153,157] These studies have confirmed a reduced rate of calcium release from the sarcoplasmic
reticulum and greater reductions in maximally activated tetanic force (P0) versus maximal caffeine 2004 Adis Data Information BV. All rights reserved.
activated force, indicating that a failure to fully
activate the contractile machinery rather than damage to the contractile machinery is the primary reason responsible for the loss of force after eccentric
muscle actions. Furthermore, these investigators estimated that at least 75% of the reduction in P0 was
due to E-C coupling failure immediately post-exercise, and although the contribution declined with
recovery, they estimated that E-C coupling failure
accounted for at least 57% of the reduction in P0 at 5
days post-exercise.
Failure of E-C coupling will impair maximal and
sub-maximal force generation. A loss of maximal
strength will have major implications for performance in strength and power events. A given absolute
sub-maximal force will require increased motor unit
recruitment and/or firing frequency that will increase the perception of effort. Furthermore, it is
expected that these effects will be exacerbated at
short muscle lengths, since the activation curve for
calcium shifts to higher calcium levels and high
firing frequencies are needed for maximum force at
short sarcomere (muscle) lengths.[158-161] In line with
this proposition, a number of studies have reported a
disproportionate loss of strength at short versus optimal or long muscle lengths following eccentric exercise.[39,49,66,79] It is possible that a pre-activation of
the muscle may counter the reduced availability of
calcium ions to the myofibrils by increasing the
intensity or duration of the active state. This may be
one explanation for the findings where vertical
jumping performance was affected to a lesser extent
in jumps that employed an active pre-stretch (i.e.
countermovement jump, drop jump) than jumps
without an active pre-stretch (i.e. squat jump) following muscle damaging exercise.[48,78,142]
2.3 Redistribution of Sarcomere Lengths
It has been suggested that eccentric muscle actions result in a redistribution of sarcomere lengths.
According to the ‘popping sarcomere’ hypothesis,[125,126,162] lengthening of active muscle does
not occur by uniform lengthening of all sarcomeres,
but by a non-uniform distribution of sarcomere
length change, with some sarcomeres rapidly overextending (‘popping’) beyond myofilament overlap
and failing to re-interdigitate upon relaxation. Such
over-extended sarcomeres would result in the reSports Med 2004; 34 (1)
Neuromuscular Function After Exercise-Induced Muscle Damage
maining functional sarcomeres adopting a shorter
length to compensate and a shift in the lengthtension relationship towards longer muscle lengths.
The practical implications are that a longer muscle
length is required to achieve the same myofilament
overlap after eccentric exercise compared with
before, resulting in a shift to the right of the optimal
angle for force generation and a disproportionate
loss of strength at short muscle lengths. Direct evidence for a shift in the optimal angle for strength has
been reported following eccentric exercise of the
ankle extensors[43,52] and several studies have reported a disproportionate loss of strength at short versus
optimal or long muscle lengths.[39,49,66,79]
tural differences between fast and slow twitch
muscle fibres may also predispose these fibres to
selective damage. Fast twitch fibres are characterised by narrower Z-lines which reflects a lower thick
and thin filament attachment and therefore weaker
sarcomere connection.[1,6,9,10]
Functional changes occurring in human muscle
after eccentric exercise also suggest a selective re-
1.0
 2004 Adis Data Information BV. All rights reserved.
Before
After
Slow
0.8
0.6
2.4 Selective Fibre Type Damage
0.4
0.2
0.0
2.0
Tension (N)
Several investigations have reported selective
damage to type II muscle fibres in human[1,3,47] and
animal muscle[6,163-166] after eccentric muscle actions. Animal studies have demonstrated significant
reductions in maximum tetanic tension, following
eccentric exercise protocols and have identified that
fast-twitch glycolytic fibres are preferentially damaged. Friden and Lieber[6,9,10] proposed a mechanism
to explain selective type II fibre damage, suggesting
that during the initial stages of eccentric exercise,
fast-twitch glycolytic fibres are instantaneously fatigued. Unable to regenerate ATP, these fibres enter
a state of rigor, resulting in mechanical disruption.
During active lengthening of a muscle fibre, the
further a muscle is stretched onto the descending
limb of the length-tension curve the greater the
potential for damage.[17,49,126,166] Brockett et al.[166]
proposed that in muscle of mixed fibre composition,
motor units differ in their vulnerability to active
lengthening because of differences in optimal
length-tension characteristics. They reported that
fast-twitch motor units show a greater shift in optimal muscle length compared with slow-twitch
motor units following eccentric actions (see figure
3). Subsequently, peak tension values were similar
in both types of motor unit, in contrast to baseline
values, which had shown fast-twitch force values to
be twice that of slow-twitch force. Therefore, it is
possible that as the ability of fast-twitch units to
exert a given force occurs at a shorter optimal
length, a resulting stretch of the muscle fibre may
lead to greater disruption of the type II fibres. Struc-
61
Fast
1.5
1.0
0.5
0.0
Fast
3.0
2.5
2.0
1.5
1.0
0.5
0.0
18
16
14
12
10
8
6
4
2
Length from Lmax (mm)
Fig. 3. Length tension curves before and after active lengthening.
Plots of tetanic length-tension curves for two fast-twitch and one
slow-twitch motor unit before and after ten active lengthenings. In
each panel, the dotted line and downwards directed arrow indicates
the whole-muscle optimal length. Gaussian curves have been fitted
to the data points. Curve fits indicated the optimum length for each
motor unit before and after the active lengthening (upwards directed arrows) [reproduced from Brockett et al.,[166] with permission].
Lmax = maximum physiological length.
Sports Med 2004; 34 (1)
62
Byrne et al.
600
Pre
DI
Torque (N
. m)
500
400
300
200
100
0
0
10
20
30
40
50
60
Time (sec)
Fig. 4. Knee-extensor rate of fatigue in a single study participant during a sustained 60-second isometric maximal voluntary contraction
before (Pre) and 1-day after (D1) eccentric exercise-induced muscle damage. Fatigue was quantified as the slope of a linear regression line
fitted to the 60 data points: the less negative the regression coefficient (b), the less fatigable the knee extensors were. Regression lines
fitted to the data represent b = –7.68 (Pre) and b = –4.58 (D1). Note the reduced starting torque, less fatigability, and task failure at D1
(reproduced from Byrne and Eston,[79] with permission).
cruitment or damage of type II fibres. During repeated electrically stimulated[12,27] or sustained maximal
voluntary[79] isometric actions, eccentrically exercised muscle appears weaker but less fatigable (see
figure 4). A similar response was observed during
30 seconds Wingate tests following eccentric exercise.[79] The fatigue responses appear without the
marked rise and rapid decline in force/power that is
associated with the activation and rapid fatigue of
type II fibres and therefore appear fatigue resistant.
2.5 Impaired Metabolism
Impaired muscle glycogen resynthesis following
exercise-induced muscle damage has been well documented.[47,104,105,167-170] Asp et al.[47] reported a significantly lower resting muscle glycogen content in
association with a 23% reduction in concentric exercise capacity of the knee extensors in comparison to
a control group 2 days after unaccustomed eccentric
exercise. This was attributed to eccentrically damaged muscle having to work at a higher relative
workload during concentric exercise, resulting in
increased glycogen utilisation and thus decreased
endurance capacity. Further analysis revealed that
the resting muscle glycogen content of type II fibres
was severely reduced, supporting the proposition
that type II fibres are selectively recruited and/or
damaged during eccentric exercise.
 2004 Adis Data Information BV. All rights reserved.
The muscle glucose transporter GLUT-4 has
been investigated as a source of impaired glycogen
resynthesis following exercise-induced muscle damage.[104,170] The findings have been equivocal, possibly because in two of the highlighted studies contrasting methods were used to induce muscle damage (i.e. eccentric actions in untrained males[170]
versus marathon running in well trained males[104]).
GLUT-4 content remained unchanged despite increased circulating levels of creatine kinase and
suppressed glycogen concentration 2 days after marathon running. Similar observations in GLUT-4
content were made in a later study,[104] although
glycogen depletion was predominant in type I rather
than type II fibres as had previously been suggested.[47] Interestingly, research that has identified a
decrease in GLUT-4 content has employed maximal
eccentric actions, which may be associated with
preferential recruitment of type II fibres. The type of
muscle-damaging exercise and the differences in
motor unit recruitment and glycogen utilisation
should therefore be considered when evaluating effects on metabolism. An impaired resynthesis of
muscle glycogen following damaging exercise represents an obvious challenge to athletes involved in
competition or athletic training where muscle glycogen content may be rate-limiting. Reduced glycogen
content in type II fibres also suggests that there are
Sports Med 2004; 34 (1)
Neuromuscular Function After Exercise-Induced Muscle Damage
similar implications for sports of a high intensity or
intermittent nature.
Warren et al.[171] examined the effect of creatine
supplementation on strength loss following muscledamaging exercise in 8-week-old mice. Although
the creatine-fed mice showed a 12% increase in
tibialis anterior creatine concentration, there were
no differences between control and experimental
groups in isometric strength loss at various concentric and eccentric angular velocities. Creatine supplementation did not attenuate strength loss following damaging exercise nor was it associated with an
increased potential for muscle injury, which had
previously been postulated.[172] In humans, a study
on 23 non-resistance trained males, 12 of whom
were supplemented with creatine 5 days prior to a
resistance training programme, demonstrated no
significant differences in circulating levels of myofibre proteins, soreness or muscle function measures
between the two groups following muscle damaging
exercise.[74]
Observed differences in response to exerciseinduced muscle damage between males and females
have been discussed in relation to the protective role
of the female sex hormone estrogen.[128] Through
estrogen’s high antioxidant capacity, membrane
stabilising properties or gene regulatory effect, or a
complex interaction of these properties, attempts
have been made to establish the role of this hormone
in muscle-damaging exercise.
The lower creatine kinase responses demonstrated by females following exercise-induced muscle
damage[172,173] does not unequivocally suggest that
estrogen moderates the muscle damaging process,
since functional measures have tended to suggest
that the hormone is ineffective at minimising muscle
damage.[174-176] Therefore, further research is needed
to quantify the role of estrogen in muscle damage.
For a more in-depth discussion on the effects of
estrogen and muscle damage, the reader is directed
towards a recent review by Kendall and Eston.[128]
3. Applied Implications
63
athletic pursuits that emphasise high power outputs
(e.g. sprinting, throwing, jumping). Similarly the
occurrence of reflex inhibition as a protective mechanism may hinder technique in performance of common training strategies (e.g. plyometrics, Olympic
lifts) and thus impair optimal performance. In attempting to moderate the effects of exercise-induced
muscle damage, the possibility of enhancing the
stretch-shortening capabilities of the muscle may
warrant further investigation. The performer and
coach should be aware of the potential implications
of exercise-induced muscle damage on performance
and the time course of recovery, such that the periodisation of training accounts for this phenomenon
in the days following eccentrically biased training
resulting in symptoms of muscle damage.
3.2 Endurance Exercise
Post-competition training must focus on adequate glycogen replenishment and appropriate recovery training intensities as exhaustive running has
been shown to impair muscle glycogen supercompensation.[177] In the days following a long-distance
event, such as a marathon, a carbohydrate-rich diet
will result in similar muscle glycogen storing regardless of whether athletes jog or rest.[14] Similarly,
athletes may need to pursue diets that are higher in
carbohydrate to ensure appropriate recovery.[167]
Endurance activities are also highly associated
with overtraining,[178] of which muscle damage has
been identified as a common symptom.[109] Highly
determined performers are driven to achieve success
resulting in excessive training, whereby the poor
temporal relationship between DOMS and the functional consequences of damage may lead performers
to believe that the absence of soreness indicates a
return to normal functional capacity.[179] There are
also similar consequences for those exposed to excessive competition with minimum recovery time.
With prevention identified as the most appropriate
approach to overtraining, again the role of appropriate planning of training and recovery is paramount.
3.3 Intermittent High-Intensity Exercise
3.1 Strength and Power Exercise
Selective alterations to the torque angular-velocity relationship would have serious implications for
 2004 Adis Data Information BV. All rights reserved.
Thompson et al.[180] examined the impact of prolonged intermittent high-intensity shuttle running on
muscle soreness and markers of muscle damage
Sports Med 2004; 34 (1)
64
Byrne et al.
with study participants unaccustomed to such activity. Results indicated significant increases in creatine kinase and aspartate aminotransferase, which
peaked at 24–48 hours post-exercise. In addition,
perceived muscle soreness was significantly elevated above baseline in the experimental group for 72
hours following the shuttle-running, peaking at
24–48 hours. Soreness was uniform across the
whole body musculature, although the hamstrings
demonstrated the greatest soreness rating, peaking at
24 hours. This research provides evidence to suggest
that sports in which there are brief periods of highintensity activity interrupted with periods of lowintensity work, such as soccer, rugby, and hockey
have the potential to induce muscle damage and
result in the functional alterations outlined in this
review.
Examples of work-to-rest ratios for high- to lowintensity activity in such sports has been quantified
as 1 : 6 to 1 : 8[181] and 1 : 1.5 to 1 : 2.9,[182] respectively. Although work by Byrne and Eston[79] has
considered the effects of exercise-induced muscle
damage on maximal-intensity performance over 30
seconds, none have as yet studied its effects on
maximal-intensity intermittent activity. Of particular concern is the approach to optimising recovery
following muscle-damaging exercise, allowing an
immediate return to training and further competition
as is commonly associated with intermittent highintensity activities. Evidence would suggest that following muscle-damaging activity, there would be an
immediate and prolonged reduction in maximal
strength and power, and thus training in the days
after such activity should not attempt to address the
development of these directly. Similarly, reduced
glycogen availability following muscle-damaging
exercise as discussed for endurance performance
(section 3.2) may have similar implications for intermittent high-intensity activity. Therefore, dietary
requirements and training intensity of the athlete
following competition may need to be given priority. However, further research focusing on the consequences of exercise-induced muscle damage on intermittent high-intensity exercise is required.
4. Future Directions
Clarkson and Newham[95] suggested that from a
functional standpoint, the effects of exercise-in 2004 Adis Data Information BV. All rights reserved.
duced muscle damage on the ability to generate
power and do work is more pertinent than on isometric force generation. However, this concept has been
studied infrequently. If, as suggested, type II fibres
are preferentially recruited and damaged during eccentric actions,[1,24,35,62,163,165,166] their contribution
to performance after damage will presumably be
compromised. The result of which would most probably be a decrease in speed and power. Reductions
in the muscles force-generating capacity and velocity of shortening are central to the reduction in
power output, which is most likely underestimated
by measurement of either one alone. In relation to
this, several, but not all, researchers have observed
greater impairment of muscle function at higher
angular velocities.[1,24,35] This has potential implications for sports or activities that are power orientated
and therefore must be studied in an appropriately
applied setting. For example, what are the effects of
exercise-induced muscle damage on single and repetitive sprint performance?
Vertical jump procedures have also been used to
study dynamic muscle function before and after
damaging exercise.[37,48,53,57,78,99] However, the effects of SSC on jump performance merits further
study. Similarly, the effects of reflex inhibition and
reduced muscle stiffness following muscle-damaging exercise are well documented but their influences on activities requiring sprinting and agility
warrants further investigation.
The role of exercise-induced muscle damage on
endurance performance is also of considerable interest. Further investigation of carbohydrate metabolism and storage following muscle-damaging exercise may be pertinent due to its association with
fatigue during prolonged exercise.
5. Conclusions
Eccentric exercise resulting in the symptoms of
exercise-induced muscle damage results in a well
documented reduction in isometric and dynamic
strength. Immediate and prolonged reductions in
power-generating ability have also been observed
during maximal cycling and vertical jump movements, suggesting that performance decrements observed in the laboratory are likely to transfer to an
applied athletic setting. Prolonged losses of strength
and power, impaired neuromuscular control, selecSports Med 2004; 34 (1)
Neuromuscular Function After Exercise-Induced Muscle Damage
tive type II fibre damage and reflex inhibition are
documented outcomes of muscle damage that have
the potential to adversely affect dynamic, multi-joint
movements that are associated with athletic activity.
Performing endurance exercise in the presence of
damage results in an elevated physiological response and an increase in subjective effort that would
likely impair training and performance. Whether the
phenomenon of exercise-induced muscle damage
represents a problem in an applied athletic setting is
unknown, but the potential for affecting performance is evident. For the coach and athlete, the challenge is to recognise the potential for damage in
various activities, to recognise the potential functional implications when the phenomenon arises,
and to structure training and competition to accommodate exposure to exercise-induced muscle damage.
Acknowledgements
No sources of funding were used to assist in the preparation of this manuscript. The views and opinions contained in
this review are those of the authors and should not be taken to
represent an official position of the Singapore Armed Forces
and the Ministry of Defence, Singapore.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
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 2004 Adis Data Information BV. All rights reserved.
Correspondence and offprints: Craig Twist, Department of
Sport and Exercise Sciences, North East Wales Institute of
Higher Education, Mold Road, Wrexham, LL11 2AW, UK.
E-mail: [email protected]
Sports Med 2004; 34 (1)