Hindawi Publishing Corporation
The Scientific World Journal
Volume 2013, Article ID 189149, 11 pages
http://dx.doi.org/10.1155/2013/189149
Review Article
Exercise-Induced Muscle Damage and
Running Economy in Humans
Cláudio de Oliveira Assumpção, Leonardo Coelho Rabello Lima, Felipe Bruno Dias
Oliveira, Camila Coelho Greco, and Benedito Sérgio Denadai
Human Performance Laboratory, UNESP, Avenue 24 A, Bela Vista-Rio, 13506-900 Rio Claro, SP, Brazil
Correspondence should be addressed to Benedito S´ergio Denadai; bdenadai@rc.unesp.br
Received 18 December 2012; Accepted 18 January 2013
Academic Editors: L. Guimar˜aes-Ferreira, H. Nicastro, J. Wilson, and N. E. Zanchi
Copyright © 2013 Cl´audio de Oliveira Assumpc¸˜ao et al. This is an open access article distributed under the Creative Commons
Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is
properly cited.
Running economy (RE), defined as the energy demand for a given velocity of submaximal running, has been identified as a critical
factor of overall distance running performance. Plyometric and resistance trainings, performed during a relatively short period
of time (∼15–30 days), have been successfully used to improve RE in trained athletes. However, these exercise types, particularly
when they are unaccustomed activities for the individuals, may cause delayed onset muscle soreness, swelling, and reduced muscle
strength. Some studies have demonstrated that exercise-induced muscle damage has a negative impact on endurance running
performance. Specifically, the muscular damage induced by an acute bout of downhill running has been shown to reduce RE during
subsequent moderate and high-intensity exercise (>65% VO2max). However, strength exercise (i.e., jumps, isoinertial and isokinetic
eccentric exercises) seems to impair RE only for subsequent high-intensity exercise (∼90% VO2max). Finally, a single session of
resistance exercise or downhill running (i.e., repeated bout effect) attenuates changes in indirect markers of muscle damage and
blunts changes in RE.
1. Introduction
Running economy (RE), defined as the energy demand for
a given velocity of submaximal running, is an important
predictor of aerobic running performance, particularly in
elite runners who have a similar aerobic power (i.e., max-
imal oxygen uptake, VO2max) [1]. Runners with high RE
demonstrate lower energetic cost at submaximal velocity and
consequently tend to run faster at given distance or longer at
a constant velocity.
A number of biomechanical (e.g., gait patterns, kinemat-
ics, and the kinetics of running) and physiological factors
(e.g., oxidative muscle capacity) seem to influence RE in
trained athletes [2, 3]. Moreover, some interventions (plyo-
metric, resistance and altitude training) performed during
relatively short periods of time (∼15–30 days) have been
successfully used to improve RE [4–6]. Plyometric and
resistance trainings lead to neuromuscular adaptations such
as increased neural drive to the muscles and changes in
muscle stiffness and muscle fiber composition, which might
reduce the energetic cost during submaximal exercise. How-
ever, plyometric and resistance trainings, especially when
they are unaccustomed activities, may cause delayed onset
muscle soreness (DOMS), swelling, and reduced muscle
strength. The negative effect of muscle-damaging exercises
on endurance running performance has been experimentally
demonstrated in both animal [7, 8] and human experi-
ments [9]. However, studies that have investigated the effect
of exercise-induced muscle damage (EIMD) on RE have
produced equivocal results [9–12]. This review discusses
the effects of EIMD induced by different exercise types
(strength, long-distance running, and downhill running) on
RE. Different recovery strategies aiming to enhance the RE
after EIMD are also addressed.
2. Running Economy
Aerobic fitness, as well as running performance, can be mea-
sured by different variables, for example, maximal oxygen
uptake (VO2max), lactate threshold (LT), onset of blood
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lactate accumulation (OBLA), movement economy (ME), or
running economy (RE). The VO2max, which reflects an indi-
vidual’s maximal rate of aerobic energy expenditure, has been
considered the gold standard for measuring aerobic power
[13]. Indeed, the VO2max has a positive association with
aerobic running performance obtained during middle- and
long-distance events (1,500 m–42,195 m) [14–16]. However,
some studies [17–20] have shown that subjects with similar
VO2max values may attain different aerobic running perfor-
mance or VO2 values during exercise of similar duration and
intensity. These differences are most likely due to variations
in ME among subjects.
The ME is defined as the amount of energy necessary
(Kcal⋅min−1) to perform a given task [21]. However, due to the
difficulty to determine the external work performed during
running, RE, expressed as the volume of oxygen uptake
(mL⋅Kg−1⋅min−1) during a specific submaximal running
intensity (Km⋅h−1), has been adopted. There is a strong asso-
ciation between RE and aerobic running performance, with
RE being a better predictor of performance than VO2max,
particularly in athletes who have similar VO2max [19, 22].
Several factors have been proposed to influence RE in
trained subjects. These include oxidative muscle capacity
and muscle stiffness. Muscle stiffness corresponds to the
ability of the muscles to store and release elastic energy.
Moreover, some interventions such as training, environment,
and muscle damage can modify the oxygen cost over a range
of running speeds [6, 11, 23–25].
Improved oxidative muscle capacity can be associated
with reduced oxygen consumption per mitochondrial respi-
ratory chain during submaximal exercise. Trained subjects
are known to have better RE than untrained individuals, and
long-distance runners are more economical than middle-
distance runners [26]. Additionally, a high weekly volume of
training has also been associated with better RE. However, a
short period (4–6 weeks) of high-intensity aerobic training
(near or above VO2max) can also lead to improvement in the
RE of trained runners [27].
In addition to aerobic characteristics and adaptations,
neuromuscular profile factors have also been considered
important aspects of RE. Type II muscle fibres seem to be
positively correlated with submaximal energy consumption,
especially at lower speeds [28]. Furthermore, both muscular
stiffness and the ability to rapidly develop muscular force
(i.e., rate of force development (RFD)) have demonstrated
significant correlations with RE [29, 30]. Stiffer muscle-
tendon complexes may increase elastic energy storage by
reducing the ground contact time, thus decreasing the
running oxygen cost. Similar to stiffness, a higher RFD is
associated with a shorter time to generate a contraction.
This effect could also diminish the ground contact time
and running oxygen cost. Heavy weight and plyometric
training associated with endurance training have improved
RE in well-trained runners [5, 31]. Basically, these types of
strength training induce neuromuscular adaptations such as
increased neural drive to the muscles, altered muscle-tendon
complex stiffness, and changed muscle fibre composition
(i.e., I → IIA ← IIX).
Environmental variables can also be used to reduce the
energetic cost of running. RE can be improved (2-3%) after
relative short periods (∼15–20 days) of altitude exposure
(∼2.000–4.500 m). Altitude exposure during daily activities,
sleeping, or training can enhance RE at sea level altitude
through haematological and muscle changes in favour of
oxygen transport [32–34]. Moreover, heat exposure during
training sessions can also improve RE by enhancing the
thermoregulatory process, thus reducing the cardiovascular
and muscle work for a given exercise intensity [23, 35, 36].
More recently, EIMD has also proposed to generate
important modifications in RE. Muscular damage induced by
an acute bout of downhill running has shown to reduce RE
in the days following the intervention (24–120 hours) [9, 11].
Specific aspects of this intervention are addressed hereafter.
3. Muscle Damage and the
Repeated Bout Effect
Skeletal muscle damage has been considered an important
factor contributing to DOMS and strength loss after eccentric
exercise [37]. Basically, the exercise conditions at which
muscle damage can be induced are unaccustomed exercises
and exercises with higher intensity or longer duration than
those to which the subject is adapted [37, 38]. The result-
ing metabolic overload and mechanical strain have been
suggested the main factors generating muscle damage [38].
Warren et al. [39] have suggested that measures of muscle
function such as strength and power are effective indicators
of both the magnitude and time course of muscle damage.
Depending on the magnitude of muscle damage, muscle
force at isometric, and dynamic testing conditions may be
impaired for 1–7 days after the exercise [40–43]. Other
important symptoms of muscle damage are disruption of
the sarcolemma and extracellular matrix [44, 45], increased
blood levels of creatine kinase (CK) and myoglobin (MB),
stiffness, and swelling [46–48].
In general, muscle damage can be induced by both static
(isometric) and dynamic (concentric and eccentric) muscle
contractions. However, there is substantial evidence that
eccentric muscle actions result in greater muscle damage than
isometric or concentric actions [49–52]. The magnitude of
strength loss after EIMD may vary between 5–10% and ∼60%
[43, 52], depending on the characteristics of the protocol
and the type of muscle actions (i.e., isometric, concentric
or eccentric) used during the posttest. The different effects
of eccentric versus isometric or concentric actions have also
been verified in the context of whole body exercises (i.e., run-
ning, cycling, and cross-country skiing) [43, 53]. For example,
muscle damage and strength loss are higher during running
(∼20–30%), which involves concentric and eccentric actions,
when compared with cycling (∼10–15%), which involves
mainly concentric actions [53]. In accordance with Millet
and Lepers [53], although concentric and eccentric actions
are present during cross-country skiing, muscular damage
is considerably lesser during this exercise than in running
because shock waves are present only during running. The
main factors attributed to the greater effect of eccentric
contractions on muscle damage are the higher peak torque
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3
values [54] and reduced motor unit activation for a given
force [54–56], both of which induce a higher mechanical
stress on the muscles [54]. Other important aspects of the
greater muscle damage induced by eccentric muscle actions
are that no energy (ATP) is necessary to detach the cross-
bridges formed during muscle contraction [57] and that the
longer length of the muscles during the contraction generates
greater muscle damage.
In addition to the main mechanical factors (i.e., the
force level produced and the change in muscle length) [37,
58, 59], some metabolic factors such as substrate depletion,
calcium influx, and reactive oxygen species have also been
proposed to influence muscle damage [38, 60]. The effects
of the different mechanical and metabolic factors that would
contribute to muscle damage do not occur at the same time.
The time course of the events involves damage in components
of excitation-contraction system and sarcomeres [59] and
degeneration and regeneration of muscle fibres, during which
DOMS, stiffness, and swelling occur [37]. Additionally, there
is an inflammatory response generating a transfer of fluid
and cells to remove damaged contractile proteins and cellular
debris from the damaged muscles [61]. Thereafter, the muscle
regeneration process is initiated [61]. Although some of these
effects may appear only some hours after the exercise, muscle
strength may be impaired during and immediately after the
exercise. Thus, mechanisms other than muscle damage can
also explain the muscle fatigue (i.e., strength loss).
It has been suggested that the magnitude of muscle
damage and the loss of muscle function might be attenuated
after one bout of eccentric exercise [62–64]. This concept is
known as the repeated bout effect (RBE). The RBE has been
demonstrated after both eccentric muscle actions [65] and
downhill running [66]. In general, this protective effect is
confirmed by the reduced decrements and faster recovery
of muscle strength, less swelling and DOMS, and attenuated
changes in CK and MB in the blood [62, 67, 68]. In addition,
alterations in muscle circumference or echo intensity (inflam-
mation) are also smaller after the first eccentric exercise bout
[68]. This protective effect has been demonstrated after a
few days of the eccentric exercise [66] and may last up to
6 months (circumference, DOMS, and inflammation) or 9
months (maximal isometric force, CK), depending on the
marker of muscle damage [65].
It has been hypothesized that the RBE is mediated by neu-
ral, cellular, and mechanical mechanisms [63, 64]. The neural
changes proposed to contribute to the RBE are increased
slow-twitch fibre recruitment and synchronisation of motor
unit firing, better distribution of the workload among muscle
fibres, higher participation of synergist muscles to torque
production, and increased motor unit activity relative to
torque produced [69–71]. Neural mechanisms have been
suggested based on the reduced median frequency [69],
which reflects some central aspects related to motor unit
recruitment. Howatson et al. [69] have demonstrated a 10%
decrease in median frequency 14 days after a bout consisting
of either 10 or 45 maximal eccentric actions. RBE has also
been observed in the untrained contralateral limb, referred
to as the contralateral RBE [72]. These studies [69, 72] con-
firm that, in addition to intramuscular adaptations, central
aspects regarding motor unit recruitment are also involved in
RBE.
The main mechanical adaptations associated with RBE
are increased muscle stiffness and intramuscular connective
tissue and changes in the intermediate filament system (main-
tenance of structural integrity of sarcomeres) [63]. Cellular
adaptations are associated with higher number of sarcom-
eres in myofibrils [59, 73], which might decrease myofib-
rillar disruption in the next exercise bout, strengthened
plasma membranes, increased protein synthesis, removal
of stress-susceptible fibres [59, 74, 75], and remodelling of
the cytoskeleton, including effects on proteins such as titin
and desmin, talin and vinculin [76], which might improve
the strength and the stability of sarcomeres and protect
muscle fibers against injuries. Other adaptation that has been
hypothesized to explain the RBE is the lesser inflammatory
response. Since the mechanical disruption is decreased after
the first eccentric exercise bout, the stimulus for the inflam-
matory response is also reduced after the exercise [73, 74].
Some of these alterations have been associated with reduced
muscle damage (strengthened extracellular matrix) and a
change in the optimal angle for torque production toward a
longer muscle length (increases in number of sarcomeres).
The magnitude of muscle damage induced by eccentric
exercise is greater at longer muscle lengths [65, 77]. When the
muscles are elongated, the sarcomere length is also greater.
Because the severity of muscle damage is influenced by the
muscle strain generated [73, 78], it has been suggested that
the RBE would be greater under conditions of longer muscle
lengths. Nosaka et al. [73] have investigated the effect of the
range of motion of the exercise used to induce muscle damage
on the RBE. The protocol used to induce muscle damage
involved 24 maximal eccentric contractions of the elbow
joint, using amplitudes of 50–100∘ or 130–180∘. Although
the changes (maximal isometric strength, range of motion,
upper arm circumference, muscle soreness, and CK) induced
by the first bout were significantly greater using the higher
amplitude, both exercise conditions induced RBE. However,
the effect generated by the short range of motion was lesser
than that promoted by the higher amplitude.
Other factor that can modify this protective effect (i.e.,
RBE) of eccentric exercise is the magnitude of muscle damage
[65, 66], which is influenced by the exercise intensity of the
first bout. Chen et al. [66] showed that 30 eccentric con-
tractions performed at 40% of maximal isometric strength
generated a smaller attenuation of the changes in indirect
markers of muscle damage (20–60%) than maximal eccentric
exercise (65–100%).
It has been also demonstrated that both the muscle
damage level (i.e., CK) and strength impairment and recovery
(i.e., isometric torque) are progressively greater with increases
in the number of bouts (1–4). However, Chen et al. [68] have
demonstrated that repetitive submaximal eccentric exercise
bouts (40% MVC) performed every two weeks promote a
protective effect similar to that induced by one maximal
eccentric exercise bout. In this study, the main indirect
markers of muscle damage were less affected by the second
to the fourth bouts of submaximal eccentric exercise than
the first; that is, the protective effect is promoted under
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Table 1: Comparison of the effects of the resistance exercise on running economy.
Study
Subjects
EIMD
Muscle damage
VO2max (%)
RE (%)
Paschalis et al.
[10]
10 healthy males
120 eccentric actions
↑ CK,
↑ DOMS, and
↓ ROM, and
↓ strength
55 and 75
√
Burt et al. [12]
9 healthy men
100 squats at 80%
body mass
√ CK,
↑ DOMS, and
↓ strength
90
↓ 4-5
Vassilis et al. [87]
24 young healthy
men
120 eccentric actions
↑ CK,
↑ DOMS,
↓ strength
70
√
Scott et al. [88]
8 active men and
8 active women
3-4 × 10 repetitions
of squat, lunges, step
up and step down,
and stiff-legged
deadlift
↑ DOMS
70
√
EIMD: exercise-induced muscle damage; %VO2max: exercise intensity at which running economy was measured; RE: running economy; CK: creatine kinase;
DOMS: delayed onset muscle soreness; ROM: range of motion; ↓ indicates decrease; √ indicates no change; ↑ indicates increase.
conditions of reduced levels of induced muscle damage.
Even after repeated submaximal bouts the magnitude of
muscle damage was still smaller than that induced by one
maximal bout. The authors suggested that the effect of
exercise intensity on the protective effect of the first bout
does not apply when some bouts of low-intensity exercise
are performed. Therefore, the magnitude of muscle damage
does not necessarily affect the protective effect of eccentric
exercise. Moreover, Howatson et al. [69] have compared two
protocols of maximal eccentric contractions to induce muscle
damage with 45 or 10 contractions. After 14 days, subjects
performed the same protocol with 45 contractions. Although
the effect of the higher volume of the first bout on damage
markers (CK, DOMS, and isometric torque) was greater, the
protective effects of both protocols were similar. Therefore,
the intensity of the first bout seems to be the main aspect of
the magnitude of muscle damage and RBE.
Because one exercise bout is enough to generate the
RBE, some studies have also investigated whether resistance
training could also reduce the effects of eccentric exercise
on muscle damage markers [67, 79]. Specifically, Newton et
al. [67] found that resistance-trained subjects demonstrated
smaller RBE when compared with untrained subjects. More-
over, Falvo et al. [79] did not find changes in indirect markers
of muscle damage (maximal isometric torque and CK) in
resistance-trained men. The authors attributed the absence
of RBE to a lack of neural adaptation. Thus, it is likely that
strength training induces to adaptations that reduce the RBE.
The majority of studies that have analysed the RBE used
relatively short time periods after the eccentric exercise (i.e.,
from approximately 7–14 days to 6–9 weeks). However, some
studies [80, 81] have reported that the RBE induced by 24
maximal eccentric actions of the elbow flexors may last up
to 6 months. Nosaka et al. [80] aimed to investigate the
responses of the main indirect markers of muscle damage
(CK, maximal isometric torque, DOMS, and swelling) five
days after the eccentric exercise bout, with sessions six, nine,
and twelve months apart. The main finding of this study was
that the RBE for strength, swelling, DOMS, and CK lasted up
to six months.
4. Strength Exercise, Muscle Damage,
and Running Economy
A variety of studies have investigated the influence of EIMD
and DOMS on neuromuscular performance indicators (i.e.,
strength and rate of force development) [82–84]. These
studies verified that the isomeric peak torque is compromised
immediately after the damaging exercise that causes DOMS,
with a gradual recovery in subsequent days. The magnitude
and the recovery rate from strength loss seem to be related
to the training history of the muscle group. For instance,
when performing maximal eccentric contractions, upper
limb muscles (less active) demonstrate greater loss of strength
(50–70%) and slower recovery (60–90 days) when compared
to lower limb muscles (locomotory muscles) (20–30% and
10–30 days, resp.) [37, 85]. However, only a few studies have
investigated the effects of EIMD and DOMS on aerobic per-
formance indexes (e.g., VO2max, lactate response to exercise,
VO2 kinetics, and movement economy) [86]. These studies
analysed the effects of EIMD on RE [10, 12] and VO2 kinetics
during submaximal cycling exercise [86]. In this context,
studies that investigated the effects of strength exercises (i.e.,
jumps, isoinertial and isokinetic eccentric exercises) on RE
will be addressed (Table 1).
Paschalis et al. [10] analysed the effects of eccentric
exercises on indirect muscle damage markers (CK, DOMS,
ROM, and isometric force) and RE in active individuals
who were not engaged in strength training programs. The
eccentric exercise protocol consisted of 120 (12 × 10) maximal
voluntary contractions (MVC) at an angular velocity of 1.05
rad⋅s−1. Although indirect muscle damage markers were
significantly altered in the subsequent days (24–72 h), the
RE (assessed at 55 and 75% VO2max) was not modified.
Similar data were obtained by Vassilis et al. [87], who analysed
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Table 2: Comparison of the effects of the downhill running on running economy.
Study
Subjects
EIMD
Muscle damage
VO2max (%)
RE (%)
Chen et al. [11]
50 male students
30 min DHR at
−15%
↑ CK,
↑ DOMS,
↓ strength, and
↑ LDH
70, 80, and
90
↓ 5
Hamill et al. [92]
10 recreational
female runners
30 min DHR at
−15%
↑ CK,
↑ DOMS
80
√
Braun and Dutto
[93]
9 endurance trained
men
30 min DHR at
−10%
↑ DOMS
65, 75, and 85
↓ 3
Chen et al. [94]
10 soccer trained
men
30 min DHR at
−15%
↑ CK,
↑ DOMS,
↓ strength, and
↑ MB
65, 75, and 85
↓ 4–7
EIMD: exercise-induced muscle damage; DHR: downhill running; %VO2max: exercise intensity at which running economy was measured; RE: running
economy; CK: creatine kinase; DOMS: delayed onset muscle soreness; MB: myoglobin; LDH: lactate dehydrogenase; ↓ indicates decrease; √ indicates no
change; ↑ indicates increase.
the effects of eccentric exercise (120 MVC at a 60∘⋅s−1) on
RE in recreational athletes with no previous experience in
resistance training. The RE (assessed at 70% VO2max) was
not changed 48 hours after the damaging bout. Therefore,
EIMD induced by isokinetic eccentric contractions do not
seem to interfere on RE measured at moderate intensities (55–
75% VO2max).
Using closed kinetic-chain exercises, Scott et al. [88]
have also analysed the effects of EIMD on RE. The vol-
unteers performed a series of lower extremity resistance
exercises designed to induce DOMS. RE was analysed at
70% VO2max, 24–30 hours after the EIMD. Although the
subjects demonstrated a higher rate of perceived exertion
values, RE was maintained unaltered throughout the days
after EIMD. In another study, Marcora and Bosio [9] did
not find any alteration in RE (70% VO2max) after 100 drop
jumps, although DOMS, CK, and knee extensors strength
were significantly affected by EIMD. Therefore, the evidence
suggests that muscle damage induced by both open and
closed kinetic-chain exercises dose not alter RE at moderate
intensities (55–75% VO2max).
However, in a recent study, Burt et al. [12] presented con-
flicting data regarding the effect of EIMD on RE. In this study,
indirect markers of muscle damage and RE were measured,
24–48 h after EIMD (10 sets of 10 squats at 80% body
mass). Significant increases in all indirect markers of muscle
damage, kinematic parameters (stride length and stride
frequency), and oxygen uptake during submaximal running
(∼90% VO2max) were observed at 24–48 h following the
initial bout of EIMD. Some authors [82, 89] have suggested
that the changes in RE are associated with decrements in
neuromuscular function (i.e., MVC) after EIMD. However,
both the magnitude and the time course of the changes in
muscular function (MVC) and RE can be different. Therefore,
changes during submaximal exercise (i.e., RE) may not be
strictly associated with neuromuscular function.
As a whole, these data suggest that the effects of muscle
damage induced by strength exercise (i.e., jumps, isoinertial
and isokinetic eccentric exercises) on RE are intensityd-
dependent. During moderate exercises (55–75% VO2max),
RE is not altered by EIMD. However, during high-intensity
exercise (∼90% VO2max), RE is impaired. During high
intensity exercise, additional type II fibres, which are the
most affected by EIMD, are recruited. Moreover, at these
intensities, the VO2 either attains a delayed steady state
(heavy domain) or continues to increase slowly (i.e., VO2
slow component (VO2SC)) reaching its maximal values at the
end of exercise (severe domain) [90]. Although the physio-
logical determinants of VO2SC remain poorly understood,
some authors have proposed that an increased ATP and/or
O2 cost of power production in fatigued fibres, rather than
the additional recruitment of poorly efficient muscle fibres,
is responsible for the VO2SC [91]. Therefore, the effects
of strength exercise-induced muscle damage on RE seem
to depend on the fibre recruitment pattern and/or on the
mechanisms determining the VO2SC.
5. Downhill and Long-Distance Running,
Muscle Damage, and Running Economy
Adopting a more specific approach, some studies have inves-
tigated the influence of muscle damage induced by strenuous
exercise (e.g., long-distance running) or downhill running on
neuromuscular parameters, and RE. This aspect and the effect
of some interventions on RE during the recovery period after
EIMD are also addressed in this topic (Table 2).
As mentioned previously, muscle damage is usually
induced by maximal and submaximal eccentric contractions,
but it can also be observed when a high volume of eccen-
tric/concentric contractions are performed, due to the eccen-
tric contractions per se [95] or because of metabolite accu-
mulation that may lead to stress and impairment of the
muscle fibres [96]. Because a high number of concentric and,
particularly, eccentric contractions are performed during
long-distance running, the symptoms of muscle damage
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are usually observed immediately and a few days after the
running bout.
In a study conducted by Millet et al. [97], changes in
muscle function and muscle damage markers from 22 expe-
rienced marathon runners were collected and analysed after
they had run an international extreme mountain ultrama-
rathon. The race consisted of a 166 km marathon through
mountainous terrain with the final destination set at 9500 m
below the starting point. This predominately downhill con-
figuration required a high number of eccentric contractions
particularly for the knee extensors. Indirect muscle damage
markers (strength, CK, LDH, and MB) were analysed before,
immediately after, and 2, 5, 7, 9, and 16 days after the
marathon. The authors found higher decreases in force
production immediately after the ultramarathon, most likely
because of the fatigue experienced during the race. However,
some of the strength markers remained altered until 5
days after exercise, as usually occurs after muscle damaging
activities. Blood markers also demonstrated the highest value
immediately after the race, returning to baseline values 5
days later. The authors found that even though this type of
activity can induce extreme muscle damage, after 16 days,
all the alterations induced by muscle damage and/or fatigue
had returned to normal. Considering that force production is
intimately related to RE, these findings may indicate that an
extremely damaging activity may induce high levels of force
loss and decreases in RE. Force production is usually fully
recovered 5 days after the damaging activity. However, RE
may recover at a faster rate than force.
To investigate factors that could influence RE, Kyrolainen
et al. [89] subjected 7 experienced runners to a protocol sim-
ulating a marathon. RE and kinematic variables (stride length
and frequency, mean contact time, external mechanical work
and power, and angular displacements and velocities of the
hip, knee, and ankle joints) were collected before, during (at
the 1st, 13th, 26th, and 42nd kilometres), two hours after, and
in the days (2, 4, and 6) after the marathon. Muscle damage
markers (CK and SOR) were also collected after the exercise.
The impairment of RE (i.e., higher oxygen consumption) was
observed only at the end of the marathon (42nd kilometre
and two hours afterward). CK and SOR were significantly
increased immediately after the marathon and returned to
baseline values only at the 6-day postexercise time point.
These data may indicate that alterations in RE after marathon
running may not be exclusively in the result of muscle damage
but may be affected by other factors such as thermal stress. To
better understand the time course of recovery of the various
parameters of muscle function following marathon running,
it is important to investigate other indirect EIMD markers,
such as force and inflammatory response.
Muscle damage induced by downhill running has also
been widely studied in the last decades. This type of exercise
has been proven to induce muscle damage even when
performed for relatively short periods (e.g., 30 minutes) due
to higher mechanical stress applied to the lower limb muscles
during the contact with the ground phase [95]. Some studies
have shown that downhill running can lead to muscle damage
of the same magnitude as plyometric or maximal eccen-
tric exercises [92, 98]. Considering that downhill running
induces muscle damage, a series of studies have investigated
its influence on neuromuscular and metabolic markers in
animals [99] and humans [11, 93, 94, 98]. In animals, downhill
running has been utilised to induce overtraining [100] as well
as a training method to increase the number of sarcomeres
[101]. In humans, this exercise model has been recently
studied in attempt to understand its influence on specific
running and aerobic parameters, such as RE [93, 98] and
running kinematics.
To the best of our knowledge, Hamill et al. [92] performed
the first study investigating the influence of downhill run-
ning on RE. In this study, 10 recreational female runners
underwent a 30 min downhill running bout (DRB) with
−15% slope at 73.5% of maximal heart rate. Indirect markers
of muscle damage (SOR and CK), RE (80% VO2max), and
kinematic parameters were measured before and 2 and 5 days
after the DRB. SOR and CK levels increased 2 days after the
DRB, returning to baseline values 5 days after the exercise.
Although kinematic parameters were modified, the DRB did
not alter RE. The authors proposed that changes in kinematics
might be due to increases in SOR, which compromises the
range of motion, and thus alters the movement patterns.
In another model to investigate the influence of downhill
running-induced muscle damage on RE, Braun and Dutto
[93] conducted a study in which 9 endurance-trained subjects
underwent a DRB (30 minutes at 70% VO2peak with a
−10% slope). Assessments of SOR, RE (65%, 75% and 85%
VO2max), and stride length were performed before and 48
hours after the DRB. SOR was increased and RE was impaired
48 hours after the DRB, suggesting that muscle damage might
have increased the energy cost of running. The authors stated
that the muscle damage decreased the range of motion and
strength, thus compromising running kinematics, which is
known to be related to RE.
To better describe the time course of changes in RE,
Chen et al. [94] subjected 10 soccer-trained volunteers to a
downhill running protocol similar to that proposed by Braun
and Dutto [93]. Muscle damage (MVC, SOR, CK and MB)
and RE (65%, 75%,d and 85% VO2max) were assessed before
and 1 hour and 1–5 days after the DRB. Alterations in muscle
damage markers were consistent with those found in the
literature, including increases in CK, MB, and SOR, with peak
values attained 48 hours after the DRB. Strength loss was
also maximal immediately after the DRB. All muscle damage
markers returned to baseline values 5 days after the DRB.
The magnitude of change was smaller, and the time course
recovery was faster for RE (4–7% and 4 days, resp.) than
for the indirect markers (i.e., isometric peak torque (IPT))
of muscle damage (7–21% and 4 days, resp.). The authors
suggested that the alterations in running kinematics, the need
to recruit more muscle fibres, the impairment in the stretch-
shortening cycle, and the reduced levels of muscle glycogen
might impair RE following a DRB.
Because alterations in the muscular tissue due to EIMD
have been shown to affect RE because of differences in muscle
fibre recruitment and other neuromuscular properties, Chen
et al. [11] assessed RE at 3 different intensities (70, 80, and
90%VO2peak) after a DRB. Muscle damage markers showed
the expected alterations, peaking 2 days after DRB. The
The Scientific World Journal
7
alteration in RE measured at 90% VO2peak was significantly
higher than at 80% VO2peak. No significant change in RE
was found at 70% VO2peak. Previous studies have indicated
that fast-twitch motor units are progressively recruited with
increased levels of exercise intensity [102]. Because several
investigations have reported selective damage to type II
muscle fibres after eccentric muscle actions in humans [40,
103], there appears to be a relationship between the motor
unit recruitment pattern and impairment in RE.
Therefore, the effects of strength exercises and down-
hill running on RE seem to be different. While strength
exercises seem to affect RE only during high intensity sub-
maximal exercises (∼90% VO2max), downhill running also
increases the energetic cost during moderate exercises (>65%
VO2max). It is important to note that during running
exercise, the VO2SC is attenuated (heavy intensity) and/or
nonexistent (moderate). Thus, the effect of strength exercises
on RE seems to occur only at running intensities at which the
VO2SC is present. Greater muscle mass and/or the magnitude
or specificity of muscle damage induced by downhill running
may partially explain these results.
A variety of interventions have been proposed to enhance
recovery from EIMD, that is, to reduce the severity and
duration of injury and SOR. It is a common belief that low-
intensity training (i.e., active recovery) enhances the recovery
process by accelerating the return to homeostasis after EIMD.
To investigate whether submaximal running would influence
the recovery from DRB, Chen et al. [98] analysed the effect
of 30-minute daily running exercises performed at different
intensities (40%, 50%, 60%, and 70% VO2peak) by different
groups on the recovery of muscle damage and RE. Muscle
damage was induced by a DRB (30 minutes at 70% VO2peak
with −10% slope). The authors found that the time-course
recovery of muscle damage markers and RE was similar for
all groups, regardless of whether submaximal running was
performed. Thus, low-to-moderate-intensity running seems
not to improve the recovery from muscle damage and/or RE
impairment.
Performing a similar subsequent bout of eccentric exer-
cise results in significantly less change in the markers of
muscle damage. This phenomenon is known as the RBE [104].
In fact, Byrnes et al. [105] and Chen et al. [66] demonstrated
that when a DRB was repeated 1–6 weeks after the first
bout, the indirect markers of muscle damage (isometric peak
torque, CK, SOR, and range of motion) were significantly
reduced. Moreover, Chen et al. [106] verified that the RBE
was also observed in RE and running kinematics parameters.
In this study, 12 male subjects underwent the same downhill
running protocol adopted by Chen et al. [11] except the
interval allowed between bouts that was twice as long, to
allow full recovery from the first bout. The authors found
significant changes in all markers of muscle damage after both
protocols. However, the RE, kinematics parameters, and SOR
were less affected after the second DRB. Therefore, one bout
of DRB might induce a protective effect, leading to reduced
levels of SOR and blunted changes in RE and biomechanical
parameters.
In another study, Burt et al. [12] subjected 9 subjects to
repeated bouts of 100 squats and measured muscle damage
markers (isometric peak torque, vertical jump height, CK,
and SOR) and RE before, immediately after the bouts, and 1-2
days after the bouts. The bouts were separated by enough time
to recover from the EIMD symptoms. All muscle damage
and RE markers were significantly affected by the first bout.
However, no alterations in some muscle damage markers and
RE were observed after the second bout. Thus, a previous
damaging activity leads to blunted or nonexistent alterations
in muscle damage markers and RE.
6. Supplementation and Muscle
Damage Recovery
A series of recent studies has investigated the influence of
different types of supplementation on recovery from and
prevention of muscle damage. The main supplements that
seem to protect against muscle damage are the flavonoids,
which are known for their efficient anti-inflammatory and
antioxidant properties. Studies investigating supplementa-
tion with flavonoid rich substances and their influence on
muscle damage will be discussed.
Howatson et al. [107] conducted a study in which muscle
damage, inflammatory response, and oxidative stress were
measured before, immediately after, and 24 and 48 hours
after a marathon. The purpose of this study was to inves-
tigate whether a tart cherry juice supplement would affect
recovery from muscle damage after marathon running in 20
recreational marathon runners, using a double-blind placebo
intervention. Muscle damage markers determined in this
study were CK, LDH, DOMS, and IPT. Other parameters
(total antioxidant status, thiobarbituric acid reactive species,d
and protein carbonyls) were measured to identify inflam-
matory response, and oxidative stress. Both groups (control
versus supplemented) demonstrated similar decreases in IPT.
However, IPT was higher for the supplementation group
at all time points, showing faster recovery. Moreover, the
authors found that the supplementation enhanced the anti-
inflammatory response as well as reduced the oxidative stress.
Kuehl et al. [108] investigated the effects of tart cherry
juice supplementation on SOR immediately after a long-
distance running (∼26 km) bout. The study was performed
in a randomised, double-blind placebo fashion in 54 experi-
enced runners. The subjects were separated in two groups:
placebo and tart cherry supplement. Both groups started
ingesting their supplements 7 days prior to the running
bout. The increase in SOR was significantly greater for the
placebo group when compared to the tart cherry group.
These findings are similar to those of Howatson et al. [107]
and indicate that the anti-inflammatory and antioxidant
properties of the tart cherry supplement might reduce SOR
after EIMD.
Supplements containing flavonoid compounds have been
shown to confer a protective effect against muscle damage
either by attenuating a vast number of markers or by accel-
erating their recovery after the EIMD. This type of protection
has been hypothesised to be due to the anti-inflammatory and
antioxidant properties present in these types of compounds
[107]. A number of studies have shown a direct relationship
between flavonoid supplementation and protection against
8
The Scientific World Journal
muscle damage. Because muscle damage may affect RE, it
would be interesting to analyse if this type of supplementation
can protect against RE impairment after EIMD.
7. Conclusion
Despite the systematic implications of RE on aerobic running
performance, only a few experiments have specifically stud-
ied the response of this index after EIMD. Recent studies have
analysed RE after strength exercises (i.e., jumps, isoinertial
and isokinetic eccentric exercises) and downhill running.
These studies have found that the magnitude of reduction in
muscle function (MVC) after EIMD is greater than the RE
and kinematic parameters. Moreover, the time course for the
changes in muscle function, RE, and kinematic parameters
are not similar. As a whole, these data suggest that the putative
mechanisms underlying muscle function and RE during the
recovery from EIMD are not completely shared. The effects
of muscle damage on RE seem to depend of the interaction
between the type of eccentric exercise and the intensity
at which the RE is measured. Strength exercises seem to
modify RE preferentially during high-intensity exercise (∼
90% VO2max). However, the effects of downhill running can
also be observed at moderate intensities (>65% VO2max).
Finally, a single session of strength exercise or downhill
running attenuates changes in indirect markers of muscle
damage and blunts changes in RE.
Acknowledgments
This research was supported by grants from Conselho
Nacional de Desenvolvimento Cient´ıfico e Tecnol´ogico and
Fundac¸˜ao de Amparo a Pesquisa do Estado de S˜ao Paulo, and
the authors declar that they have no conflict of interests.
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Exercise-induced muscle damage and running economy in humans.
Assumpção, Cláudio de Oliveira,Lima, Leonardo Coelho Rabello,Oliveira, Felipe Bruno Dias,Greco, Camila Coelho,Denadai, Benedito Sérgio