The effect of eccentric contraction velocity on muscle ... - IOS Press

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Isokinetics and Exercise Science 21 (2013) 1–9 DOI 10.3233/IES-2012-0465 IOS Press

Review Article

The effect of eccentric contraction velocity on muscle damage: A review Felipe Romano Damas Nogueira∗, Miguel Soares Conceic¸a˜ o, Felipe Cassaro Vechin, Edson Manoel Mendes Junior, Guilherme Fernando Couto Rodrigues, Marcio Aparecido Fazolin, Mara Patricia Traina Chacon-Mikahil and Cleiton Augusto Libardi Laboratory of Exercise Physiology, School of Physical Education, University of Campinas, Campinas, Brazil

Abstract. The velocity at which eccentric exercise is performed may be a factor in the extent of muscular damage. However, studies differ regarding the exercise velocity that promotes greater muscle damage. The purpose of this review was to analyze studies that looked into at least two different eccentric exercise velocities and verified markers of muscle damage. Relevant studies for this review were identified and the methodological quality of each study was calculated based on the Physiotherapy Evidence Database (PEDro) scale. Twelve studies were included herein. The mean PEDro rating was 6.67, ranging from 5 to 7. Seven studies reported that the faster eccentric exercise velocity induced greater muscle damage. Four studies showed no differences between velocities and a single study has indicated a greater magnitude of muscle damage after slow eccentric exercise. Therefore, it seems that fast eccentric exercise may indeed be associated with greater muscle damage even though exercise velocity per se is not the main factor involved in eccentric exercise-induced muscle damage in both animal and human models. Keywords: Resistance training, muscle strength, creatine kinase, eccentric exercise

1. Introduction An acute bout of unaccustomed maximal lengthening contractions induces muscle damage [1–3], leading to impaired contractile muscle function and structural muscle injury [4]. Several factors may affect the magnitude of muscle damage, such as age [5,6], muscle strain [7], muscle length [8], number of eccentric actions performed [9,10], daily activities [11], muscle fiber type [12,13] and lengthening contraction velocity [10,14,15], among others. It is hypothesized that muscle damage can be induced both by mechanical and metabolic stress [16]. Moreover, it is possible that the greater the mechanical and metabolic stress, the greater ∗ Corresponding author: Felipe Romano Damas Nogueira, Laboratory of Exercise Physiology, School of Physical Education, Uni´ versity of Campinas, Av. Erico Ver´ıssimo, 701 Zip Code 13083-851, P.O. Box 6134. Campinas, Brazil. Tel.: +55 19 3521 6625; Fax: +55 19 3521 6750; E-mail: [email protected].

the muscle damage. Nevertheless, it seems that mechanical stress is the main factor in muscle damage [13, 17,18]. Velocity interferes in mechanical stress [10] and thus could modulate muscle damage. Controversy exists concerning which eccentric exercise velocity could elicit greater muscle damage, both in animals and humans. The population of muscle fibers affected by eccentric exercise may be velocity dependent [19], since it has been documented that type II fibers seems to be more susceptible to muscle damage than type I fibers [20– 22]. Type II motor fibers (fast-twitch fibers) comprise the fastest type of motor units [23], thus fast eccentric actions should recruit a greater number of fast-twitch muscle fibers than slow eccentric actions. Consequently, considering fiber type susceptibly to injury, velocity of contraction might interfere in the magnitude of muscle damage. In addition, it is possible that velocity could affect the properties of cross-bridges [24, 25], and this might interfere in the susceptibility of

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F.R.D. Nogueira et al. / The effect of eccentric contraction velocity on muscle damage

muscle fibers to damage. Furthermore, Chapman et al. [10] proposed that velocity could influence the number of cross-bridges capable of generating force, and this could induce different mechanical stress per active cross-bridge. In contrast, Paddon-Jones et al. [26] proposed that the velocity of eccentric exercise could interfere in inhibitory/protective neural mechanisms that prevent muscles from damage. Shepstone et al. [19] found through biopsies that fast velocity lengthening contractions resulted in differing disruption of the protein ultrastructure (observed as Z-band streaming). The same study showed greater hypertrophy after fast eccentric exercise than slow eccentric exercise when performed chronically. Thus, it seems reasonable that higher muscle damage may promote greater hypertrophy. In addition, as described above both mechanical tension and metabolic stress can induce muscle damage [16] and hypertrophy [27]. Therefore, velocity could influence the magnitude of muscle damage and hypertrophy. However, muscle damage may produce acute deficits in muscle function [10,15]. In training athletes, for instance, reducing the magnitude of muscle damage might decrease the length of the recovery phase of training, which could improve their performance in the next high-intensity exercise bout [18] and maintain high levels of performance in competitions. Consequently, the magnitude of muscle damage should be considered alongside several variables of interest, for instance training regime or competition. Since velocity may modulate the magnitude of eccentric exercise-induced muscle damage, this review attempted to elucidate which eccentric contraction velocity induces the greatest magnitude of muscle damage. We considered the best studies in literature (both animal and human models) that compared the magnitude of muscle damage induced by different velocities of lengthening contractions. 2. Methodology 2.1. Search strategy Relevant studies for this review were identified by searching PubMed, MEDLINE and ISI Web of Knowledge (1986–February 2011), in addition to a search of reference lists. The databases were searched for the following terms, in various combinations: eccentric, muscle damage, muscle injury, velocity, low-velocity, high-velocity, rapidly, slowly, lengthening contraction,

muscle contraction, repeated bout effect, stretch, recovery and speed. Titles and abstracts were read and those obviously not relevant to the present review issue were eliminated. Remaining studies were selected accordingly to search strategy (inclusion and exclusion criteria) for further analysis. 2.2. Inclusion criteria Studies that utilized at least two defined velocities of eccentric exercise were included in the selection process. Studies should also have analyzed isolated eccentric exercise and made comparisons between velocities of eccentric exercise. For inclusion, studies must have utilized adequate methodology for comparisons between groups for the eccentric-exercise induced muscle damage, i.e., for at least one muscle-damage marker (e.g., isometric strength deficit), and each study must have performed and showed acute comparisons between different velocity groups. 2.3. Exclusion criteria Studies that utilized acceleration, and, therefore, no defined velocity, were excluded. Moreover, studies that utilized any alimentary supplementation or demonstrated different levels of training at pre-exercise analysis were also excluded. 2.4. Quality After applying the inclusion and exclusion criteria, all finally-selected articles were read and the outcomes of each article were recorded. Methodological quality was calculated with the Physiotherapy Evidence Database (PEDro) scale, which is based on the Delphi list [28] as previously used [29,30]. The PEDro scale examines the internal validity and interpretability of experimental trials. The scale has 11 items and is scored to a maximum of 10 points, since, for the first criteria (eligible criteria), no score is attributed [29]. The quality of a study was established and ranked by consensus, since no specific method to perform it is provided by PEDro: high quality – more than 5 points; moderate quality – 4 to 5 points; low quality – 3 or less points. This criteria has been utilized before by Roig et al. [29, 31]. If any study scored 3 or less points, and, therefore, classified as low quality, it was excluded. All studies analyzed for the calculation of the PEDro score were performed by three separate and independent reviewers. All disagreements were resolved in a consensus meeting.


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Fig. 1. Search strategy.

3. Results 3.1. Search results After a first database search, 409 studies were considered and screened. Titles and abstracts were read and those studies that have not met the initial criteria (n = 377) were excluded, resulting in 32 articles. Subsequently, all studies were read and those that did not satisfy the secondary criteria (n = 20) were also eliminated from further analysis, resulting in twelve remaining studies (Fig. 1). The PEDro scale was applied to the final twelve studies selected, and the lowest score was 5. Therefore, all twelve studies reached the accepted quality level and were considered in the present review. 3.2. Methodological quality of studies included The mean PEDro rating was 6.67, ranging from 5 to 7. Eleven studies were classified as “high quality” and just one was classified as of “moderate quality”. The results of the PEDro score are shown in the last column of the Results tables (Tables 1 and 2).

3.3. Effect of eccentric exercise velocity on the magnitude of muscle damage The present review consists of twelve studies that compared at least two eccentric exercise velocities for eccentric exercise-induced muscle damage. Six of these utilized animal models and the other six utilized humans. All studies considered herein showed results for at least one muscle damage marker,such as biopsies, creatine kinase (CK), concentric strength deficit (CSD), eccentric strength deficit (ESD), histological appearance (HIST), isometric strength deficit (ISD), lactate dehydrogenase enzyme (LDH), maximal rate of relaxation deficit (MRRD), maximal rate of tension development deficit (MRTD), muscle soreness (MS), muscle thickness (MT), range of motion (ROM), relaxed elbow joint angle (RANG), shift in optimal length for tension generation (SLopt), total muscle [Ca2+ ] (Ca2+ ) and upper arm circumference (CIR). Tables 1 and 2 show the results of each study. Animal (mice, rat or toad) studies (Table 1). Brooks and Faulkner [7], McCully and Faulkner [9] and Warren et al. [24] performed the eccentric contractions through stimulation with electrodes of mice muscles (in situ extensor digitorum longus muscles [7,9] and in vitro

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F.R.D. Nogueira et al. / The effect of eccentric contraction velocity on muscle damage Table 1 Results of the animal articles included Study

Subjects (muscle accessed)

Velocity of movement

Eccentric exercise

McCully and Faulkner [9]

1360 ± 16 muscle fibers of female albino mice (EDL)

0.2 (Lf/s) 0.5 (Lf/s) 1.0 (Lf/s)

0.5/1.0/2.5/5/900 (s) of eccentric stimulation on each velocity

Warren et al. [24]

180 muscles of untrained female Sprague-Dawley mice (soleus)

0.5 (Lo/s) 1.0 (Lo/s) 1.5 (Lo/s)

5 EA /240 (s) rest between contractions

Lynch and Faulkner [21]

145 fast-twitch fibers of adult male Fischer rats (EDL)

0.5 (Lf/s) 1.0 (Lf/s) 2.0 (Lf/s) 3.0 (Lf/s) 4.0 (Lf/s)

Talbot and Morgan [32]

37 muscles of Cane toads (sartorius)

Willems and Stauber [4] Brooks and Faulkner [7]

Markers of muscle damage results ISD F>S HIST F>S

Conclusion (Velocity effect on muscle damage) F>S

PEDro score

CK activity F>S ISD F>S MRTD F>S MRRD F>S Ca2+ F = S

F>S

7

Single EA

ISD F = S

F=S

6

3.0 (Lo/s) 4.0 (Lo/s)

5 to 60 EA

SLopt F = S ISD F = S

F=S

5

12 caged sedentary female Sprague-Dawley rats (plantar flexors)

50◦ /s 600◦ /s

30 EA

ISD F = S

F=S

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84 CD-1 male healthy mice (EDL)

1.0 (Lf/s) 2.0 (Lf/s) 4.0 (Lf/s) 8.0 (Lf/s) 16.0 (Lf/s)

Single EA

ISD F>S

F>S

7

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Ca2+ , Total muscle [Ca2+ ]; CK, Creatine kinase; EA, Eccentric actions; EDL, Extensor digitorum longus; F, Fast; HIST, Histological appearance; ISD, Isometric strength deficit; Lf/s, Optimal fiber length per second; Lo, Muscle length; Lo/s, Muscle length per second; MRRD, Maximal rate of relaxation deficit; MRTD, Maximal rate of tension development deficit; S, Slow; SLopt, Shift in optimal length for tension generation.

soleus muscle [24]) attached to a lever arm of a servomotor. Willems and Stauber [4] stretched the stimulated plantar flexors muscles of rats in situ by a rotational movement of the ankle; Lynch and Faulkner [21] performed the eccentric contractions utilizing isolated fast-twitch fibers of rats maximally activated (one end of the fiber was fixed to a force transducer and the other end was attached to the lever arm of a servomotor); and Talbot and Morgan [32] used stimulated isolated muscles (sartorius) of toads to perform eccentric contractions through a muscle stretching mechanism (composed by a strain gauge transducer and a linear motor with position feedback control). Brooks and Faulkner [7], McCully and Faulkner [9], and Warren et al. [24], showed that high velocity eccentric contractions induced a higher magnitude of muscle damage than slow eccentric contractions, since fast eccentric exercise resulted in greater ISD [7,9,24] and histological signs of muscle damage [9]. Warren et al. [24], also showed increases in CK activity and greater MRTD and MRRD. However, Ca2+ levels were similar between velocities. Other animal studies, for

example those by Talbot and Morgan [32], Lynch and Faulkner [21], Willems and Stauber [4], indicated similar muscle damage following eccentric exercise velocities, as shown by ISD [4,21,32] and SLopt [32]. Human studies (Table 2). All human studies utilized an isokinetic dynamometer. Four studies indicated greater muscle damage after fast eccentric exercise, compared to slow eccentric exercise [10,15,19,33] whereas one study showed greater muscle damage for the slow velocity group [26] and another showed similar muscle damage between velocities [14]. Chapman et al. [15], reported greater muscle damage after the fast velocity protocol, as demonstrated by all the muscle damage markers utilized by the authors. Fast eccentric exercise elicited greater CK activity, MS, CIR, ISD, ESD and CSD; and lower ROM and RANG than the slow lengthening contractions. These results also showed a slower recovery after a high velocity eccentric protocol. Chapman et al. [33] found similar values between velocities for LDH activity and MS. However, this study showed greater MT, CIR, ISD and CK activity; and lower ROM after high velocity eccen-


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Table 2 Results of the human articles included Study

Subjects (muscle accessed)

Velocity of movement

Eccentric exercise

Markers of muscle damage results

Conclusion (Velocity effect on muscle damage) FS ISD F>S CSD F>S ESD F>S ROM FS

F>S

7

Chapman et al. [10]

16 M young, sedentary (elbow flexors)

30◦ /s 210◦ /s

5 × 6 and 35 × 6 EA for both velocities

CK activity F>S ISD F>S CSD F>S ROM FS

7

Barroso et al. [14]

15 M young, physically active (elbow flexors)

60◦ /s 180◦ /s

30 EA

CK activity F = S ISD F = S ROM F = S MS F = S

F=S

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Chapman et al. [33]

18 M young, recreationally active (elbow flexors)

30◦ /s 210◦ /s

35 × 6 EA/ 90(s)

CK activity F>S LDH activity F=S ISD F>S ROM FS

F>S

6

MT F>S MS F = S

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CIR, Upper arm circumference; CK, Creatine kinase; CSD, Concentric strength deficit; MS, Muscle soreness; EA, Eccentric actions; ESD, Eccentric strength deficit; F, Fast; ISD, Isometric strength deficit; LDH, Lactate dehydrogenase enzyme; M, Men; MT, Muscle thickness; RANG, Relaxed elbow joint angle; ROM, Range of motion; S, Slow; W, Women.

tric exercise. Shepstone et al. [19] performed biopsies and found that fast lengthening contractions resulted in more Z-band streaming per millimeter squared muscle than the slow velocity contractions. Chapman et al. [10] showed greater muscle damage for fast eccentric exercise velocity, as demonstrated by higher values of ISD, CSD and CK activity; and lower ROM. CIR and MS values showed similar changes after fast and slow protocols. Conversely, Paddon-Jones et al. [26] found a greater magnitude of muscle damage after a slow velocity protocol, as shown by greater CIR, ESD and CSD. Nevertheless, similar values between eccentric exercise velocities were found for CK activity and ISD. Interestingly, the fast protocol elicited greater MS. Barroso et al. [14] reported no difference between velocities analyzed for muscle damage markers. This study compared ISD, ROM, MS and CK activity, and found similar values for all these markers for the fast and slow protocols.

4. Discussion In the present review we attempted to elucidate which eccentric exercise velocity would promote greater eccentric exercise-induced muscle damage. Therefore, we searched all studies in the literature, using both animal and human models, which compared at least two eccentric exercise velocities for muscle damage markers. Since we have different models (i.e., animals and humans) and protocols, it became complicated to clarify which eccentric exercise velocity elicits greater muscle damage for all populations. Additionally, in animals, Warren et al. [24] found that the peak total force developed in the protocol is the main factor involved in muscle damage. In contrast, Chapman et al. [34] demonstrated, in humans, that the work and peak torque during eccentric exercise do not predict changes in markers of muscle damage. Yu et al. [35] showed that the sequence of events proposed to lead to muscle damage in an animal model does not apply to

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the muscle damage in human muscle. Consequently, the comparison between exercise-induced muscle damage in humans and animals should be made cautiously. Even between animals, Brooks and Faulkner [7] considered the comparison of results to be difficult, since all animal studies present several differences, such as preparation, number of contractions, fiber types and species utilized. Moreover, some studies work with isolated fibers [21], and others with isolated muscles [24], while others observe the entire animal limb [4]. For humans, the methodologies utilized by the studies comparing different velocities were more similar, making this comparison slightly more solid, since all studies utilized isokinetic equipments and elbow flexors muscles [10,14,15,19,26,33]. However, comparing results for the twelve studies considered in this study, both animal and human models, we found seven studies [7,9,10,15,19,24,33] that considered the fast eccentric exercise velocity to be the greatest inducer of muscle damage. Four studies [4, 14,21,32] showed no difference between eccentric exercise velocities, and just one study showed greater eccentric exercise-induced muscle damage for the slow group [26]. Thus, it seems reasonable to consider that the fast contraction velocity produces more mechanical stress in contractile elements [33]. Hence, higher contraction velocities elicit greater mechanical stress per active muscle fiber [36], while fewer strongly bound cross-bridges are formed during fast-velocity contractions [37]. Chapman et al. [15] reported that the force generated per cross-bridge increases with an increase in the contraction velocity, since a shorter time is available for the formation of active cross-bridges at higher velocities. In addition, increasing the number of forcegenerating cross bridges through increased phosphorylation of myosin regulatory light chain makes fibers more susceptible to muscle damage [38]. Since fast velocities take a shorter time to activate cross-bridges, a greater number of them should be formed in a shorter time for fast contraction compared to slow contraction. Thus, a greater number of force-generating cross bridges are acquired in higher velocities, enhancing susceptibility of muscle fibers to damage [38]. Fast eccentric actions may recruit more type II muscle fibers than slow eccentric actions, since fast-twitch fibers compose the fastest type of motor units [23]. In addition, type II fibers seem to be more susceptible to muscle damage than slow twitch fibers [20–22]. Thus, it seems plausible that greater muscle damage might occur during fast eccentric contractions. Consequent-

ly, the type of fiber susceptibility to muscle damage should explain at least part of the results, demonstrating greater muscle damage after fast eccentric exercise. In contrast, one study found that a slow contraction velocity (30◦/s) showed greater muscle damage than fast velocity eccentric exercise (180◦/s) [26]. Furthermore, Barroso et al. [14] used 60◦ /s and 180◦ /s as slow and fast eccentric exercise velocities, respectively, and found similar changes in indirect markers of muscle damage. However, the velocities analyzed in both studies might not elicit a large discrepancy in the markers of muscle damage. Other studies that have found greater muscle damage after fast lengthening contractions utilized 30◦ /s and 210◦/s [10,15,33]. Paddon-Jones et al. [26] proposed that fast eccentric exercise might be associated with a greater inhibitory/protective neural mechanism that would prevent muscle from damage, thus, rendering slow velocity contractions more threatening in terms of a greater damage to muscle fibers. In addition, the mechanism of differential recruitment in the case of the elbow flexors: biceps brachii which is preferentially recruited during high velocity contractions vs. the brachialis which is preferentially recruited during slow velocity contractions [39] may explain the results. These authors demonstrated that CK plasma activity was similar between fast and slow groups, suggesting that both groups have the same structural damage [26]. However, it has been shown that CK release can be controversial as a muscle damage marker, since the size of the structural damage may not be sufficient for CK release, considering the size of the CK molecule [40,41]. On the other hand, strength deficits might furnish a better marker for muscle damage, since they reflect the capacity of the sarcomeres to produce force [42]. Internal membrane damage could degenerate contractile and structural proteins, impairing excitation-contraction coupling systems [43]. This impairment might reflect in losses of strength produced after eccentric protocols. Paddon-Jones et al. [26] showed greater losses in eccentric and concentric strength for the slow group. However, similar deficits were found in the isometric torque between groups. Analyzing all studies, six studies have shown greater losses in strength for the fast group [7,9,10,15,24,33], and one study [19] showed greater damage for the fast group trough biopsies, a direct marker of muscle damage. Analyzing the effect of velocity on eccentric exercise-induced muscle damage, these results support the conclusion that fast eccentric exercise velocity is associated with greater eccentric exercise-induced muscle damage.


For animal studies, it seems that the strain, defined as the rate of deformation beyond optimum [34], is the main factor involved in eccentric exercise-induced muscle damage [7,21], and velocity should have a secondary importance. Talbot and Morgan [32], Lynch and Faulkner [21], and Willems and Stauber [4], did not find differences in muscle damage between velocities, however they confer importance to a neuromuscular fatigue reflecting on strength deficits. Warren et al. [24] also discuss the importance of fatigue for the understanding of the modification of muscle damage variables. In addition, in studies involving human beings, fatigue should be considered as a confounding factor concerning susceptibility of muscle to damage [10]. In humans, it seems that the number of eccentric actions is the main factor involved in muscle damage [10]. Chapman et al. [15] found greater muscle damage after a fast eccentric exercise protocol. However, the authors equaled the time under tension between velocities. Consequently, the fast group performed 35 sets of 6 repetitions, while the slow group only 5 sets of 6 repetitions, showing a greater number of eccentric contractions for the fast group. Two years later, Chapman et al. [10] compared 5 sets of 6 repetitions and 35 sets of 6 repetitions for both velocities, equaling the number of eccentric actions and time under tension. Indeed, greater muscle damage was identified after fast eccentric exercise, though the difference only became apparent when subjects performed a high number of lengthening contractions (i.e., 35 sets). Moreover, also in animals, Talbot and Morgan [32] related that the number of contractions was one of the main inducers of muscle damage. Consequently, it seems that velocity has a secondary role in modulating the magnitude of muscle damage. It is interesting to note that the human studies considered in the present study performed fast eccentric exercise at a maximum of 210◦ /s. Velocities above 210◦ /s should be further performed and investigated in order to gather additional information and further clarify the effects of eccentric exercise velocity on muscle damage. However, the differences found between velocities in the studies included herein cannot be discarded, i.e., velocity may interfere in the magnitude of eccentric exercise-induced muscle damage, with possible applications in sport and muscular hypertrophy. It is believed that sarcomere disruption could impair the excitation-contraction coupling and calcium signaling, which could activate calcium-sensitive pathways [44]. These events could lead to growth factors liberation and, therefore, muscle hypertrophy [45].

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Furthermore, O’Reilly et al. [46] showed that a single bout of eccentric exercise can induce injury and activate satellite cells, which in turn activates hepatocyte growth factor both locally and systemically. Muscular satellite cells, residing between the basal lamina and the sarcolema, mediate hypertrophy [27,47,48]. Consequently, a protocol that induces greater muscle damage could lead to greater hypertrophy. Shepstone et al. [19] reported greater muscle damage after acute fast lengthening contractions, which could have led to the greater hypertrophy shown for the fast velocity training group. These authors hypothesized that the nature of muscle mechanics on the lengthening portion of forcevelocity curve of higher contraction velocities can promote greater muscle tension, which could stimulate a greater protein synthetic response [19]. In addition, Farthing and Chilibeck [49] showed that fast eccentric exercise promotes greater muscle hypertrophy. These results may not be explained just by the magnitude of muscle damage, since other hypertrophic pathways could be involved in protein synthesis. Additionally, the repeated bout effect, widely described in the literature [50–55], should be present from the second eccentric exercise bout on, attenuating muscle damage. More longitudinal studies relating muscle damage to hypertrophy should be done to clarify this issue. Conversely, muscle damage might produce deficits in muscle function, as shown by strength deficits after eccentric exercise protocols [10,15]. With regard to athletes, individuals should avoid performing an excessive number of high velocity eccentric contractions on the days before competitions, since greater muscle damage may lead to undesirable effects, such as performance deficits. Also, extensive muscle damage might jeopardize their participation in high-intensity exercise bouts throughout their training period [18]. Thus, by reducing the magnitude of muscle damage, the length of the recovery phase of training can be reduced. For individuals just starting a training program, the length of the recovery process and the stress of exercise could be minimized by taking into account these considerations [18]. Therefore, performing a high number of fast eccentric contractions might not be desirable, since reduced injury will reduce the unpleasant effects related to muscle damage. In conclusion, by analyzing the velocity effect on eccentric exercise-induced muscle damage, it seems that fast eccentric exercise velocity induces the greatest magnitude of muscle damage, although it has been shown that the velocity of eccentric exercise is not the main factor involved in eccentric exercise-induced

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muscle damage for both animal and human models. Thus, other variables should be considered concerning the magnitude of damage to muscle fibers, such as strain and number of eccentric contractions. Acknowledgements None of the authors of the present study have any professional relationships with possible companies or manufacturers who would benefit from the results of the present study. References [1]

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