Neuromuscular Function After Exercise Induced.5

REVIEW ARTICLE
Sports Med 2004; 34 (1): 49-69 0112-1642/04/0001-0049/$31.00/0 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-
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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
2004 Adis Data Information BV. All rights reserved.
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
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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 1.51.9 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]
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
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next 2448 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
involves the study participant performing a maximal voluntary contraction (MVC) of a muscle group at a fixed joint angle for 25 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 5060% 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 56 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)
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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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 3040% 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
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)
2004 Adis Data Information BV. All rights reserved. Sports Med 2004; 34 (1)
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Table I. Studies investigating dynamic muscle function by isokinetic dynamometry after exercise-induced muscle damage Study Friden et al.[1] Muscle group Knee extensors Study participants 12M Activity 30 min eccentric cycle ergometer Muscle action Isometric, concentric Angular velocity (rad/sec) 1.57, 3.14, 5.24 Recovery Isometric and concentric 1.57 and 3.14 rad/sec recovered by D6. Strength at 5.24 rad/sec not recovered by D6 Greater than 7 days for all velocities 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 By D4 for 3.14 but not 0.52 rad/sec By D4 for eccentric 0.52 rad/sec. By D7 for eccentric 2.83 rad/sec No difference in rate of recovery. Greatest deficit at D2, complete recovery by D7 Concentric 3.14 rad/sec not affected. Isometric by D7, concentric 1.09 rad/sec by D2 No differences in recovery. Approx. 90% for isometric, 0.52 and 3.14 at D7 Comments Slower recovery at higher angular velocity. Biopsy evidence of selective type II fibre damage Recovery more rapid with rest vs exercise in week after marathon Slower recovery for concentric actions particularly at high angular velocity
Sherman et al.[14] Golden and Dudley[24]
Knee extensors
10M runners
42.2km marathon 175.7 20.4 min 100 eccentric actions at 85% of eccentric 1RM (10 sets 10 reps)
Concentric
1.1, 3.2, 5.3
Knee extensors
8M
Isometric, concentric, eccentric
1.05, 3.14
Gibala et al.[7]
Elbow flexors
8M untrained
64 eccentric actions at 80% of concentric 1RM (8 sets 8 reps) 40 min downhill (10% gradient) running (5 8 min) at 80% HRmax 100 eccentric actions at 80% of eccentric 1RM (10 sets 10 reps)
Isometric, concentric Concentric, eccentric Isometric, concentric, eccentric
0.52, 3.14
Slower recovery at lower angular velocity Slower recovery of eccentric strength at higher angular velocity Greater decline in isotonic eccentric versus concentric (58% vs 39%) 1RM at D2 post-exercise Muscle function preserved at high angular velocity No muscle action- or velocity-dependent effect observed
Eston et al.
[35]
Knee extensors
10M
0.52, 2.83
Hortobagyi et al.[8]
Knee extensors
12 (6M, 6F) moderately active
1.04
Deschnes et al.[60]
Knee extensors
9M untrained
100 maximal isokinetic concentric/eccentric actions at 0.53 rad/sec (4 sets 25 reps) 100 maximal isokinetic eccentric actions at 1.57 rad/ sec (10 sets 10 reps)
Isometric, concentric
1.09, 3.14
Byrne et al.[66]
Knee extensors
8 (5M, 3F) moderately active
Isometric, concentric
0.52, 3.14
Byrne et al.
Continued next page
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Immediate postexercise measurements only
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)
No muscle actiondependent effect observed No differences in recovery. Complete by D7
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
Muscle function preserved at high angular velocity
Comments
(22.3 8.1%)
Michaut et al.[80] Elbow flexors
D = day post-eccentric exercise; F = females; HRmax = maximum heart rate; M = males; reps = repetitions; RM = repetition maximum.
Angular velocity (rad/sec)
Recovery
Muscle action
Isometric, concentric, eccentric 8 (5M, 3F) moderately active Byrne and Eston[78] Knee extensors 100 eccentric actions at 70% body mass load (10 sets 10 reps)
1.57
Study participants
Activity
Table I. Contd
Study
Muscle group
10M active
50 maximal isokinetic eccentric actions at 1.05 rad/sec (5 sets 10 reps)
Isometric, concentric, eccentric
Concentric 1.05, 4.19. Eccentric 1.05
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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
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 2045 minutes of running per day at 5060% maximal oxygen uptake 2max), did not achieve full recovery of maximal (VO 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 1520% 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)
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
57
Strength/power (% of pre-exercise values)
100 90 80 70 60 50
Strength Power
* **
Post
D1
D2 Time after exercise
D3
D7
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
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 23 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
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
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)
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100 Height (% of pre-exercise values)
*
95
90
85 SJ CMJ DJ 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 2max, exercise cycle ergometer exercise at 80% VO 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] 2max however, no differences were observed for VO or endurance time. In both of these studies, no difference in sub-maximal oxygen consumption 2) was observed after eccentric exercise, sug(VO gesting that exercise efficiency was unaltered. These
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 0.20.3C and heart rate by 12 beats/min during 50 minutes of treadmill walking at 2max and in environmenan intensity of 4550% VO tal conditions of 40C and 20% relative humidity, performed 2 and 67 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 (0.4C) was equivalent to what would be expected from an individual hypohydrated by 23% (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
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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.
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,
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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 (1020Hz) compared with high frequencies (50100Hz) 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)
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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]
2.4 Selective Fibre Type Damage
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 reSlow Before After
1.0 0.8 0.6 0.4 0.2 0.0
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 2004 Adis Data Information BV. All rights reserved.
2.0 1.5 1.0 0.5 0.0
Fast
Tension (N)
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.
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600 500
Pre DI
Torque (N
. m)
400 300 200 100 0 0 10 20 30 Time (sec) 40 50 60
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.
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
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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 estrogens 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
3.1 Strength and Power Exercise
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
Selective alterations to the torque angular-velocity relationship would have serious implications for
Thompson et al.[180] examined the impact of prolonged intermittent high-intensity shuttle running on muscle soreness and markers of muscle damage
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with study participants unaccustomed to such activity. Results indicated significant increases in creatine kinase and aspartate aminotransferase, which peaked at 2448 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 2448 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)
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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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Neuromuscular Function After Exercise-Induced Muscle Damage

Neuromuscular Function After Exercise-Induced Muscle Damage

Neuromuscular Function After Exercise-Induced Muscle Damage

Sherman et al.[14] Golden and Dudley[24]

1.1, 3.2, 5.3

Isometric, concentric, eccentric

Isometric, concentric Concentric, eccentric Isometric, concentric, eccentric

12 (6M, 6F) moderately active

8 (5M, 3F) moderately active

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Neuromuscular Function After Exercise-Induced Muscle Damage

Immediate postexercise measurements only

No muscle actiondependent effect observed No differences in recovery. Complete by D7

Muscle function preserved at high angular velocity

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Michaut et al.[80] Elbow flexors

Angular velocity (rad/sec)

50 maximal isokinetic eccentric actions at 1.05 rad/sec (5 sets 10 reps)

Isometric, concentric, eccentric

Concentric 1.05, 4.19. Eccentric 1.05

Neuromuscular Function After Exercise-Induced Muscle Damage

Strength/power (% of pre-exercise values)

D2 Time after exercise

100 Height (% of pre-exercise values)

Neuromuscular Function After Exercise-Induced Muscle Damage

Neuromuscular Function After Exercise-Induced Muscle Damage

1.0 0.8 0.6 0.4 0.2 0.0

2.0 1.5 1.0 0.5 0.0

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Neuromuscular Function After Exercise-Induced Muscle Damage

Neuromuscular Function After Exercise-Induced Muscle Damage

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Sports Med 2004; 34 (1)

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Sports Med 2004; 34 (1)

Neuromuscular Function After Exercise-Induced Muscle Damage

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Sports Med 2004; 34 (1)

147. 148. 149.

150. 151. 152. 153. 154. 155. 156.

157. 158. 159. 160. 161. 162. 163. 164.

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