Neuromuscular Function After Exercise-Induced Muscle Damage

Sports Med 2004; 34 (1): 49-69 0112-1642/04/0001-0049/$31.00/0

REVIEW ARTICLE

 2004 Adis Data Information BV. All rights reserved.

Neuromuscular Function After Exercise-Induced Muscle Damage Theoretical and Applied Implications Christopher Byrne,1 Craig Twist2,3 and Roger Eston3 1 2 3

Centre for Human Performance, Defence Medical and Environmental Research Institute, DSO National Laboratories, Republic of Singapore Department of Sport & Exercise Sciences, North East Wales Institute of Higher Education, Wrexham, UK School of Sport Health and Exercise Sciences, University of Wales, Bangor, UK

Contents Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49 1. Effects of Exercise-Induced Muscle Damage on Muscle Function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52 1.1 Effects on the Joint Angle-Torque Relationship . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52 1.2 Effects on the Torque-Angular Velocity Relationship . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53 1.3 Effects on Athletic Performance Measures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56 1.3.1 Power-Generating Ability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56 1.3.2 Vertical Jump Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57 1.3.3 Sprinting Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57 1.3.4 Endurance Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58 1.4 Effects on Neuromuscular Control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58 2. Theoretical Implications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59 2.1 Central Fatigue . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59 2.2 Excitation-Contraction Coupling Impairment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 60 2.3 Redistribution of Sarcomere Lengths . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 60 2.4 Selective Fibre Type Damage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61 2.5 Impaired Metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62 3. Applied Implications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63 3.1 Strength and Power Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63 3.2 Endurance Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63 3.3 Intermittent High-Intensity Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63 4. Future Directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64 5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64

Abstract

Exercise-induced muscle damage is a well documented phenomenon particularly resulting from eccentric exercise. When eccentric exercise is unaccustomed or is performed with an increased intensity or duration, the symptoms associated with muscle damage are a common outcome and are particularly associated with participation in athletic activity. Muscle damage results in an immediate and prolonged reduction in muscle function, most notably a reduction in force-generating capacity, which has been quantified in human studies through isometric and dynamic isokinetic testing modalities. Investigations of the torque-angular velocity relationship have failed to reveal a consistent pattern of change, with inconsistent reports of functional change being dependent on the muscle action and/or angular velocity of movement. The consequences of damage on dynamic, mul-

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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 Sports Med 2004; 34 (1)

Neuromuscular Function After Exercise-Induced Muscle Damage

with exercise-induced muscle damage, relate these decrements to theoretical views regarding underlying mechanisms, and finally to discuss the potential impact of muscle damage on athletic performance. Eccentric muscle actions possess several unique features,[112] which potentially explain why performance of these actions often results in damage to the muscle. The classic in vitro force-velocity relationship of maximally activated muscle indicates that force generated during an eccentric action is 1.5–1.9 times greater than isometric force.[113-117] Although the in vivo torque-velocity relationship of human muscle differs due to neural inhibition of maximal eccentric actions,[115,116] well motivated individuals can achieve greater torques during a maximal voluntary eccentric versus an isometric or concentric action.[112] Furthermore, motor unit activation (as assessed by electromyography) is lower for maximal eccentric versus isometric or concentric actions and less motor unit activation is required for a given force under eccentric conditions.[112,116,118,119] This combination of high force and low fibre recruitment places a high mechanical stress on the involved structures and has been implicated as a causative factor in muscle damage.[112] Enoka[112] suggested that such a loading profile might take the form of a lower level of activation distributed across the entire population of motoneurons or the activation of only a subset of the entire population (e.g. type II fibres, see section 2.4). Although differences in the recruitment order of motor units between concentric and eccentric actions have been observed,[120,121] an alteration in the recruitment order of motor units does not appear to be a general control strategy for eccentric actions.[122] The mechanism of force generation during an eccentric action also differs, whereby the cross-bridges are detached mechanically rather than undergoing a detachment that involves adenosine triphosphate (ATP) splitting, as with concentric actions.[122,123] The compliant portion of individual cross-bridges is also stretched further during an eccentric versus an isometric action.[122,123] There also seems to be a length-dependent factor involved in the damaging process, since eccentric actions performed at long muscle length result in greater evidence of damage than those performed at short muscle length.[17,49]  2004 Adis Data Information BV. All rights reserved.

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It is widely believed that eccentric exercise-induced muscle damage is initiated by mechanical factors.[6,9,10,18,124-126] Force produced during eccentric actions and magnitude of strain (i.e. change in length as a function of initial length [%]) appear important mechanical factors determining muscle damage. This concept is straightforward when considering the loading profile and range of motion associated with high force eccentric actions, such as those used in plyometrics and resistance training. However, other factors (e.g. metabolic depletion, calcium influx, generation of reactive oxygen species, musculo-tendonous stiffness regulation) may initiate or contribute to the damaging process,[99,127,128] particularly when considering damage resulting from prolonged low force eccentric actions, such as with distance running. Initial manifestations of damage are disrupted sarcomeres and damage to components of the excitation-contraction (E-C) coupling system.[125,126,129] After these initial events there follows a process of muscle fibre degeneration and regeneration, which has been described in detail elsewhere.[3,91-95,97,124,128] During these stages, the transient symptoms of DOMS, muscle stiffness, and muscle swelling appear and subside. These symptoms are mediated by the inflammatory response that accompanies muscle fibre damage and causes a transfer of fluid and cells to the affected muscles for the removal of damaged contractile proteins and cellular debris, before regeneration begins.[36,94,130] Muscle soreness is the most commonly used marker of exercise-induced muscle damage in human studies,[131] is probably the most well recognised indicator of damage among athletic populations, and yet shares a poor temporal relationship with histological evidence of muscle damage[3] and measures of muscle function.[13,30,83] Objective measures of soreness have been gained by using a ‘myometer’ to measure the applied force to a muscle group at the pain threshold[13,17,18,22,51,90] and subjective measures of soreness have been gained by numerical scales, questionnaires and visual analogue scales.[21,25,28,30,82] Both forms of measurement have demonstrated that muscle soreness following eccentric exercise has a characteristic time course. Exercised muscles are pain-free for approximately 8 hours and then soreness increases and peaks over the Sports Med 2004; 34 (1)

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next 24–48 hours.[13,17,18,21,22,90] Jones and Round[123] observed that after intense eccentric exercise, a person will go to bed with only minor discomfort but will wake the next morning with severe, and in some cases almost disabling pain, first appreciated when trying to get out of bed. All discomfort usually subsides within 96 hours.[90,93] Thus, the term ‘DOMS’ is appropriate in describing the typical time course of the sensation but conveys little about the nature of the sensation.[90] The sensation of soreness comprises muscle tenderness, pain on palpation, and also mechanical stiffness in the muscle that results in pain when the muscle is passively stretched or activated.[21,90,93] DOMS should not be used as an indicator of the magnitude of muscle damage or functional impairment, since function is impaired before soreness arises and damage becomes worse when soreness has dissipated.[3,30,83] Muscle function can also remain impaired when soreness has dissipated and this could lead to practical problems if the dissipation of DOMS is used as a signal to resume normal training when the muscle is in a weakened state. DOMS is believed to arise from damage and inflammation of non-contractile connective tissue,[18,90] which gives rise to painful sensations when the muscle is palpated, stretched or activated. 1. Effects of Exercise-Induced Muscle Damage on Muscle Function In a recent review of the measurement tools used in the study of eccentric exercise-induced muscle damage, Warren et al.[131] suggested that measures of muscle function provide the most effective means of evaluating the magnitude and time course of damage resulting from eccentric muscle actions. Functional impairments (e.g. reductions in strength and power) are immediate, prolonged, and perhaps the most important symptom of damage when considering athletic performance in the presence of muscle damage. 1.1 Effects on the Joint Angle-Torque Relationship

Measures of isometric strength have been the most widely used method of determining muscle function after eccentric exercise.[131] The method  2004 Adis Data Information BV. All rights reserved.

involves the study participant performing a maximal voluntary contraction (MVC) of a muscle group at a fixed joint angle for 2–5 seconds to determine muscle strength. In general, isometric strength is reduced immediately post-eccentric exercise and recovery is gradual and prolonged. The magnitude and time course of strength loss appear dependent on the training history of the muscle group, with the greatest and longest lasting strength loss consistently observed in the relatively inactive elbow flexors[22,28,76] versus the locomotory muscles of the lower limbs.[11,12,49] Clarkson et al.[21] reported that a typical response to maximal eccentric exercise of the elbow flexors was an immediate 50–60% reduction in strength followed by a linear recovery to baseline by 2 weeks post-exercise. However, further studies have reported much longer time courses of recovery. Howell et al.[28] reported an immediate 35% loss of strength following submaximal eccentric exercise of the elbow flexors and suggested that the half-time of recovery may be as long as 5–6 weeks. More recently, Sayers and Clarkson[76] measured strength loss and recovery of the elbow flexors in 192 volunteers (98 males, 94 females) after 50 maximal voluntary eccentric muscle actions of the non-dominant arm. On average, strength was reduced by 57% immediately post-exercise and remained 33% lower at 5.5 days. No differences were apparent between males and females. Approximately 20% (n = 32) of the sample demonstrated strength loss exceeding 70%, with the majority of these study participants demonstrating some recovery by 5.5 days, but not fully recovering strength by 26 days post-exercise. Interestingly, 24 out of the 32 study participants were female, suggesting that some females may be more susceptible to greater initial reductions in strength than males. However, these same females recovered strength more rapidly than males with an equivalent strength deficit. A minority of the sample (n = 9) demonstrated severe strength loss (>70%) and little recovery by 5.5 days. When these study participants were monitored until full recovery, the time course varied between 33 and 89 days. Of note, two male study participants recorded the longest recovery of strength (61 and 89 days). These results demonstrate that for relatively inactive muscle groups, such as the elbow flexors, the magnitude of strength loss Sports Med 2004; 34 (1)


following eccentric exercise-induced muscle damage can be dramatic and recovery can take up to 12 weeks. Sayers and Clarkson[76] suggested that some individuals displaying protracted recovery periods may be predisposed to a prolonged inflammatory response that may contribute directly to the prolonged impairment of muscle function. The knee and ankle extensors also demonstrate immediate and prolonged reductions in isometric strength following exercise-induced muscle damage, although the magnitude of strength loss is usually less than that observed for the elbow flexors. Early work by Komi and Viitasalo[11] demonstrated a 35% reduction in knee extensor strength and a decrease in the rate of force development, which had not recovered 2 days after 40 maximal eccentric actions performed on a leg press apparatus. Recent work by Byrne and Eston[79] demonstrated a 30–40% reductions in knee extensor strength with recovery incomplete (approximately 95%) 7 days after 100 repetitions of the eccentric phase of the barbell squat exercise performed with a load of 80% of concentric one repetition maximum. Following marathon running, Avela et al.[53] reported a 30% reduction in ankle extensor strength and rate of force development with full recovery by 2 and 4 days post-race, respectively. Other studies have documented the acute fatigue effects of long-distance endurance exercise on isometric strength but have not monitored recovery.[132-137] For example, reductions of 10%, 26% and 30% have been reported in the knee extensors immediately following an 85km cross-country ski race,[132] a 42.2km marathon,[134] and a 65km ultramarathon race,[137] respectively. The consistent findings from research investigating the effects of eccentric exercise or prolonged SSC exercise on locomotory muscle groups are an immediate and prolonged reduction in strength and a decreased rate of force development. The apparent inconsistencies in the magnitude of strength loss and length of recovery between the elbow flexor and knee extensor muscle groups is possibly due to the severity of the initial damage, as a result of more severe damage-inducing exercise (maximal versus submaximal eccentric), and less natural activation of the elbow flexors during everyday activity. Examination of isometric strength as a function of joint angle has revealed that relative strength loss  2004 Adis Data Information BV. All rights reserved.

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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)

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Table I. Studies investigating dynamic muscle function by isokinetic dynamometry after exercise-induced muscle damage Study

Muscle group

Study participants

Activity

Muscle action

Angular velocity (rad/sec)

Recovery

Comments

Friden et al.[1]

Knee extensors

12M

30 min eccentric cycle ergometer

Isometric, concentric

1.57, 3.14, 5.24

Isometric and concentric 1.57 and 3.14 rad/sec recovered by D6. Strength at 5.24 rad/sec not recovered by D6

Slower recovery at higher angular velocity. Biopsy evidence of selective type II fibre damage

Sherman et al.[14]

Knee extensors

10M runners

42.2km marathon 175.7 ± 20.4 min

Concentric

1.1, 3.2, 5.3

Greater than 7 days for all velocities

Recovery more rapid with rest vs exercise in week after marathon

Golden and Dudley[24]

Knee extensors

8M

100 eccentric actions at 85% of eccentric 1RM (10 sets × 10 reps)

Isometric, concentric, eccentric

1.05, 3.14

Isometric and eccentric at 1.05 and 3.14 rad/ sec by D7. Concentric 1.05 rad/sec by D10, concentric 3.14 rad/sec not recovered by D10

Slower recovery for concentric actions particularly at high angular velocity

Gibala et al.[7]

Elbow flexors

8M untrained

64 eccentric actions at 80% of concentric 1RM (8 sets × 8 reps)


0.52, 3.14

By D4 for 3.14 but not 0.52 rad/sec

Slower recovery at lower angular velocity

Knee extensors

10M

40 min downhill (–10% gradient) running (5 × 8 min) at 80% HRmax

Concentric, eccentric

0.52, 2.83

By D4 for eccentric 0.52 rad/sec. By D7 for eccentric 2.83 rad/sec

Slower recovery of eccentric strength at higher angular velocity

Hortobagyi et al.[8]

Knee extensors

12 (6M, 6F) moderately active

100 eccentric actions at 80% of eccentric 1RM (10 sets × 10 reps)

Isometric, concentric, eccentric

1.04

No difference in rate of recovery. Greatest deficit at D2, complete recovery by D7

Greater decline in isotonic eccentric versus concentric (58% vs 39%) 1RM at D2 post-exercise

Deschnes et al.[60]

Knee extensors

9M untrained

100 maximal isokinetic concentric/eccentric actions at 0.53 rad/sec (4 sets × 25 reps)


1.09, 3.14

Concentric 3.14 rad/sec not affected. Isometric by D7, concentric 1.09 rad/sec by D2

Muscle function preserved at high angular velocity

Byrne et al.[66]

Knee extensors


100 maximal isokinetic eccentric actions at 1.57 rad/ sec (10 sets × 10 reps)


0.52, 3.14

No differences in recovery. Approx. 90% for isometric, 0.52 and 3.14 at D7

No muscle action- or velocity-dependent effect observed

Eston et al.

[35]

Byrne et al.

Sports Med 2004; 34 (1)

Continued next page

Immediate postexercise measurements only (–22.3 ± 8.1%)


D = day post-eccentric exercise; F = females; HRmax = maximum heart rate; M = males; reps = repetitions; RM = repetition maximum.

Muscle function preserved at high angular velocity Concentric 4.19 rad/sec reduced to a lesser extent (–12.5 ± 8.9%) vs concentric 1.05 rad/ sec (–18.5 ± 6.1%), isometric (–20.8 ± 11.2%), and eccentric 1.05 rad/sec Concentric 1.05, 4.19. Eccentric 1.05 Isometric, concentric, eccentric 50 maximal isokinetic eccentric actions at 1.05 rad/sec (5 sets × 10 reps) 10M active Michaut et al.[80] Elbow flexors

No muscle actiondependent effect observed No differences in recovery. Complete by D7 1.57 Isometric, concentric, eccentric 100 eccentric actions at 70% body mass load (10 sets × 10 reps) Knee extensors Byrne and Eston[78]


Muscle group Study

Table I. Contd

Study participants

Activity

Muscle action

Angular velocity (rad/sec)

Recovery

Comments


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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)

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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

The ability to generate power is an aspect of human muscle function that has received limited attention after exercise-induced muscle damage. The major concern for the athlete is if a selective loss of concentric and eccentric strength at high angular velocities of movement occurs, as reported by some studies of the torque-velocity relationship.[1,24,35] This would render the affected muscle(s) markedly less powerful at the velocities of movement associated with athletic events. Sherman et al.[14] were perhaps the first to measure maximal dynamic exercise performance after a bout of damage-inducing exercise. These authors employed a maximal work capacity test consisting  2004 Adis Data Information BV. All rights reserved.

of 50 maximal leg extensions at 3.2 rad/sec and reported a 47% reduction in work capacity immediately after a marathon race in ten trained male runners. Interestingly, five study participants who performed daily ‘recovery’ exercise in the week post-marathon, consisting of 20–45 minutes of running per day at 50–60% maximal oxygen uptake ˙ 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 15–20% were apparent immediately after eccentric exercise and remained for 2 days at 80 rpm and for over 4 days at 110 rpm. The longer recovery period at the higher movement velocity would seem to suggest a selective loss of performance at high angular velocities of movement. More recently, Byrne and Eston[79] reported immediate and prolonged reductions in peak power during a 30-second Wingate cycle test. The reductions in power output were the direct result of an inability to achieve a high pedal frequency since the external load remained constant before and after eccentric exercise. Moreover, the recovery pattern of peak power was different to that of isometric strength. Whereas isometric strength demonstrated a linear recovery, peak power demonstrated further decrements at days 1 and 2 post-exercise before recovering linearly (figure 1). These results suggest that muscle power, unlike strength, may be affected by DOMS and the inflammatory response to exercise-induced muscle damage. In contrast, Malm et al.[139] reported no significant change in Wingate 30-second cycle test performance and an unexpected improvement in intermittent maximal intensity cycle performance (10 × 10 seconds of all-out cycling interspersed with 50-second rest periods) folSports Med 2004; 34 (1)

Strength/power (% of pre-exercise values)


100 90

Strength Power

* **

*

Post

D1

*

*

D2

D3

80 70 60 50 D7

Time after exercise Fig. 1. Loss and recovery of isometric knee extensor strength and Wingate peak power after eccentric exercise-induced muscle damage. Values are means (± standard error) expressed as a percentage of pre-exercise values (reproduced from Byrne and Eston,[79] with permission). D = day post-eccentric exercise; Post = 1h post muscle-damaging exercise; * indicates a significant difference for both strength and power from pre-exercise values, p < 0.05; ** indicates a significant difference between the loss of strength and power, p < 0.05.

lowing eccentric exercise of the knee extensors. However, the eccentric exercise protocol employed in this study may not have been sufficiently intense to produce functional changes, judging by the absence of an increase in creatine kinase and only moderate muscle soreness. Miles et al.[44] reported an immediate and prolonged impairment of the ability of damaged muscle to generate rapid force. During unloaded maximal velocity concentric movements of the elbow flexors in response to a light stimulus, increases were observed for movement time and the time to reach peak velocity, with a gradual slowing of peak velocity. Peak velocity slowed by approximately 3.5 rad/ sec (25%) at 4 days post-exercise. Interestingly, premotor time, representing central processing time, was unchanged. Such findings are consistent with a change in the force-velocity relationship towards slower muscle and the notion of selective type II fibre damage. 1.3.2 Vertical Jump Performance

Komi and colleagues[37,53,57,99,132,134,135,140,141] have extensively studied the effect of short- and long-lasting SSC exercise on neuromuscular performance during a drop jump from approximately  2004 Adis Data Information BV. All rights reserved.

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50cm height (for review see Komi[99]). When muscle damage was induced through intense plyometric exercise or through marathon running, prolonged reductions in maximal force and electromyographic activity, ground reaction forces, stretch-reflex sensitivity, muscle and joint stiffness regulation and drop jump performance were observed.[53,57,134,135] The recovery process was shown to occur in a bimodal pattern with an initial dramatic reduction in performance followed by an early recovery before secondary reductions in performance at 2–3 days postexercise.[53,57] The secondary decline in performance observed in these studies was suggested as being associated with the well documented inflammatory response to muscle damage. These studies have demonstrated that damaged muscle has a reduced tolerance to impact forces during an SSC movement.[97] During a drop jump, there is an increased contact time during breaking and push-off phases due to decreased strength, reflex activity and initial stiffness. Work is increased during the push-off phase resulting in reduced efficiency and the potential to accelerate fatigue during repeated SSC actions.[53,57,134,135] Byrne and Eston[79] recently investigated the effect of exercise-induced muscle damage on vertical jumping performance with and without use of the SSC. Reductions in vertical jumping performance were immediate, long lasting (up to 4 days), and dependent on the type of jump performed (see figure 2). Interestingly, jump performance was affected to a greater extent under squat jump conditions (no SSC) than in the countermovement or drop jump (with SSC). Similar results have been observed after intensive plyometric exercise[142] and after an ultramarathon foot race.[48] These results suggest that the SSC possibly attenuates the detrimental performance effects associated with exercise-induced muscle damage. 1.3.3 Sprinting Performance

Semark et al.[51] studied the effects of exerciseinduced muscle damage on sprint performance. Using a single sprint effort, assessed at 5, 10, 20 and 30m from a standing start, there was no evidence to suggest that muscle damage had a detrimental effect on sprint time or acceleration. Although muscle soreness was evident, serum creatine kinase meaSports Med 2004; 34 (1)

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Byrne et al.

Height (% of pre-exercise values)

100

*

*

CMJ

DJ

95

90

85 SJ

Fig. 2. Average reduction in squat jump (SJ), countermovement jump (CMJ), and drop jump (DJ) performance (% of pre-exercise values) over a 7-day period following eccentric exercise-induced muscle damage. Vertical jumping performance was assessed with (CMJ, DJ) and without (SJ) use of the stretch-shortening cycle. Values are means (± standard error) [reproduced from Byrne and Eston,[78] with permission] . * indicates a significantly greater preservation of CMJ and DJ than SJ performance.

surements demonstrated no significant change over the assessed time period. It is therefore possible that the protocol may not have induced sufficient muscle damage to influence performance. 1.3.4 Endurance Performance

An elevated physiological response to endurance exercise has been reported after muscle damaging exercise.[143,144] When six untrained male study participants performed 15 minutes of sub-maximal ˙ 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  2004 Adis Data Information BV. All rights reserved.

results demonstrate that most, but not all, physiological responses to endurance exercise were amplified when muscle damage was present. The loss of muscle function and SSC efficiency through repetitive SSC actions, as occurs in the quadriceps and calf muscles during running (see section 1.3.2), may directly contribute to fatigue during prolonged exercise.[99,145] Muscle damage has also been shown to alter thermoregulation during exercise in the heat.[146] In comparison to pre-exercise values, core temperature was elevated by 0.2–0.3°C and heart rate by 12 beats/min during 50 minutes of treadmill walking at ˙ 2max and in environmenan intensity of 45–50% VO tal conditions of 40°C and 20% relative humidity, performed 2 and 6–7 hours after lower body eccentric exercise. Exercise was also associated with greater heat storage and energy expenditure, suggesting a decreased economy of walking. These changes had subsided at 26 hours post-eccentric exercise, although the elevated heart rate response still remained. The authors suggested that the altered thermoregulatory and cardiovascular responses were modest and highlighted that the largest individual increase in core temperature (0.4°C) was equivalent to what would be expected from an individual hypohydrated by 2–3% (bodyweight loss). However, the attainment of a critical core temperature may be the rate-limiting factor when endurance exercise is performed in an uncompensable hot environment,[147,148] and thus even a modest elevation of core temperature would reduce the capacity for heat storage and be a potential disadvantage to the athlete. 1.4 Effects on Neuromuscular Control

A reduction in neuromuscular efficiency of the knee extensors has been observed after eccentric exercise.[11,60] This is reflected as a decrease in the force : integrated electromyographic (iEMG) activity ratio, resulting in a greater central activation (nervous stimulation) being required for the achievement of a sub-maximal or maximal force. Deschenes et al.[60] recently reported that the increased iEMG was localised to the rectus femoris where soreness was focussed. Furthermore, the impairment in neuromuscular efficiency was demonstrated to outlast other symptoms of damage such as Sports Med 2004; 34 (1)


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.

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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 (