Journal of Applied Physiology
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

J Appl Physiol 100: 1489-1498, 2006. First published January 5, 2006; doi:10.1152/japplphysiol.00524.2005
8750-7587/06 $8.00
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow All Versions of this Article:
100/5/1489    most recent
00524.2005v1
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (3)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Butterfield, T. A.
Right arrow Articles by Herzog, W.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Butterfield, T. A.
Right arrow Articles by Herzog, W.

Effect of altering starting length and activation timing of muscle on fiber strain and muscle damage

Timothy A. Butterfield and Walter Herzog

Faculty of Kinesiology, University of Calgary, Calgary, Alberta, Canada

Submitted 3 May 2005 ; accepted in final form 1 January 2006


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Muscle strain injuries are some of the most frequent injuries in sports and command a great deal of attention in an effort to understand their etiology. These injuries may be the culmination of a series of subcellular events accumulated through repetitive lengthening (eccentric) contractions during exercise, and they may be influenced by a variety of variables including fiber strain magnitude, peak joint torque, and starting muscle length. To assess the influence of these variables on muscle injury magnitude in vivo, we measured fiber dynamics and joint torque production during repeated stretch-shortening cycles in the rabbit tibialis anterior muscle, at short and long muscle lengths, while varying the timing of activation before muscle stretch. We found that a muscle subjected to repeated stretch-shortening cycles of constant muscle-tendon unit excursion exhibits significantly different joint torque and fiber strains when the timing of activation or starting muscle length is changed. In particular, measures of fiber strain and muscle injury were significantly increased by altering activation timing and increasing the starting length of the muscle. However, we observed differential effects on peak joint torque during the cyclic stretch-shortening exercise, as increasing the starting length of the muscle did not increase torque production. We conclude that altering activation timing and muscle length before stretch may influence muscle injury by significantly increasing fiber strain magnitude and that fiber dynamics is a more important variable than muscle-tendon unit dynamics and torque production in influencing the magnitude of muscle injury.

skeletal muscle; muscle mechanics; lengthening contractions

MUSCLE STRAIN INJURIES ARE the most frequent injuries in sports (20). As a result, they have commanded a great deal of attention in an effort to understand their etiology. Over the years, several risk factors have been proposed, including muscle weakness and fatigue (20, 21), malfunctioning neuromuscular coordination pattern (1, 21), inadequate flexibility (29, 53), improper warm-up (10, 48), and inadequate strength or endurance (15, 29), among others. However, the relationship between these proposed strain injury etiologies and the muscle injury mechanisms gleaned from in situ and in vitro experiments in the past has not been firmly established.

Historically, experimental protocols used to elucidate the mechanisms of severe disruptive muscle injury have focused on high magnitudes of force and strain. To assess the function of muscle after severe disruptive muscle strain injuries, isolated muscles (37, 50, 54) or fibers (4, 5, 59, 60) are preactivated and subjected to a minimal number of stretches beyond physiological range to produce a severe, disruptive strain injury. These protocols have been instrumental in elucidating relationships between mechanical factors, muscle strain injury, and the subsequent physiological response. Although such studies have been essential to our understanding of severe muscle strain injuries, the fact that these are produced utilizing a nonphysiological range of motion makes application to in vivo muscle function difficult.

Conversely, strain-induced subcellular damage results in delayed onset muscle soreness, does not result in immediate pain and disability, and appears to limit the subsequent fibrosis, allowing regeneration and repair that may improve the function of the muscle. Most in vivo muscle injury protocols have resulted in nondisruptive, subcellular damage after eccentric exercise in either human (38–40) or animal models (3, 16, 28, 32). When using in vivo protocols within a physiological range of motion, more than one repetition is required to produce muscle injury (16, 23, 57). This may be due to the disassociation between fiber dynamics and muscle-tendon unit (MTU) dynamics that have been observed during locomotion (24, 26). Muscles acting as compliant actuators (61) tend to store and release energy during locomotion, which serves to increase the efficiency of the musculoskeletal system (25). This type of behavior is not represented well during in vitro and in situ eccentric contraction protocols and may be a key feature in the difference between disruptive strain injury and subcellular damage in vivo. Recently, it has been proposed that the accumulation of subcellular damage through repetitive fiber strain may lead to progressive MTU injury, culminating in an acute, observable muscle strain injury in athletes (9).

It is well accepted that muscle strain injuries occur while the muscle is activated and lengthening (13, 17–19, 21, 31, 34, 36, 62). Utilizing lengthening contractions (eccentric contractions), animal models have provided great insight into the cellular mechanisms of muscle strain injury. Traditionally, two unique mechanical properties of lengthening contractions have been associated with strain induced muscle injury: high peak force production (30, 37, 54) and fiber strain magnitude (34, 35). With the use of these ideas, subcellular damage has been proposed to result from a sequence of events that may begin with either cytoskeletal disruption (6, 34) or unstable sarcomeres (42, 51). The loss of structural integrity of the fibers, in combination with subsequent active lengthening contractions, may result in increasing injury with time (22). In this fashion, microscopic subcellular damage may ultimately present clinically as muscle pain and weakness, as fiber necrosis progresses to inflammation and impairment (8, 9, 45).

Starting muscle length before stretch has been shown to influence muscle injury, with a longer starting length resulting in a greater magnitude of muscle injury in in vitro (23, 52, 58), in situ (55), and in vivo (16, 39) protocols. This may be due to several factors: first, stretch at longer muscle lengths may produce greater peak force compared with stretch at shorter muscle lengths, and this has been associated with increases in strain injury (37); and, second, at very long muscle lengths the overextension of sarcomeres within fibers may result in contractile element injury, propagating to fiber necrosis and weakness (9, 45, 58), indirectly implicating fiber length in muscle strain injury.

The association between activation timing and muscle strain injury has also been proposed as an etiology for muscle strain injury (7), but the exact mechanisms are unknown. Although there is a dearth of evidence supporting this hypothesis, an in situ approach by Stevens (50) showed that altering the timing of activation during stretch-shortening cycles influenced the magnitude of muscle injury in rat hindlimb muscles. In addition, activation timing has been shown to influence peak force production during lengthening contractions (34), which potentially provides a link between activation timing and muscle fiber injury due to high peak force production during lengthening contractions.

Ultimately, the effects of activation timing and starting muscle length on peak force and fiber dynamics during stretch-shortening cycles remain unknown. Therefore, the purpose of this paper was threefold: first, to determine the effects of small changes in the timing of activation on fiber dynamics and joint torque production during in vivo stretch-shortening cycles at short muscle lengths; second, to compare the fiber dynamics and joint torque during stretch-shortening cycles at short muscle length with those measured during an identical stretch-shortening protocol at long muscle length; and lastly, to elucidate the potential relationship between peak force, fiber strain, and muscle injury.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Surgical procedure.   Muscle and fiber strain was determined from both hindlimbs of 18 skeletally mature female New Zealand White rabbits (5.5 ± 0.2 kg, Riemens, St. Agatha, ON, Canada). Rabbits were obtained and studied with the approval of the Animal Care Committee of the University of Calgary and were housed locally in accordance with Canadian Council on Animal Care Guidelines. Rabbits were tranquilized with 0.18 ml (10 mg/ml) acepro-25 (MTC Pharmaceuticals, Cambridge, ON, Canada) and held under anesthesia with 1.5% isoflurane, 0.6 l/min N2O, and 0.8 l/min O2. Incisions were made on the posterior aspect of the hindlimbs, anterior to the sciatic vein, and the biceps femoris and semimembranosus were separated exposing the peroneal nerve. Nerve cuff stimulating electrodes were secured over the right and left common peroneal nerves, superior to the gastrocnemius and distal to the branching of the sciatic nerve. In this manner, all dorsiflexors of the tibiotarsal joints were stimulated effectively.

To measure fascicle lengths, an incision was made over the anterior aspect of the shank, exposing the tibialis anterior and extensor digitorum longus. The fascia was removed from the anterior aspect of the tibialis anterior (TA), and a superficial fascicle was isolated by microstimulation (12). Piezoelectric crystals (Sonometric, London, ON, Canada), 2 mm in diameter, were sutured to the proximal and distal ends of the fascicle in the central, superficial region. After implantation, the skin was stapled closed.

Fiber strain measurements.   Rabbits were divided into three groups, based on starting muscle length and timing of muscle activation. Group one (SOS, n = 11 TA) consisted of stimulation at the onset of stretch (plantar flexion), with lengthening contractions starting at a short muscle length (70° tibiotarsal joint angle). Group two (SPS, n = 7 TA) consisted of stimulation preceding stretch by 100 ms, with lengthening contractions starting at a short muscle length (70° tibiotarsal joint angle). Group three (SPL, n = 6 TA) consisted of stimulation preceding stretch by 100 ms, with lengthening contractions starting at a longer muscle length (95° tibiotarsal joint angle). Lengthening contractions in all three groups were performed through a range of motion that resulted in a ~5% strain to the MTU, or 35° range of motion in the SOS and SPS groups. Because the TA moment arm decreases as the tibiotarsal joint is plantar flexed, the tibiotarsal joint angle change needed to produce a ~5% MTU strain in the SPL group was 50°.

Setup and experimental protocols.   For all three groups, rabbits were first placed supine in a stereotaxic frame with the knee joint at 90°. The left foot was strapped to a servo-motor foot plate (Parker Hannifin, Irwin, PA) that was controlled via computer (Motion Planner, Rohnert Park, CA). The tibiotarsal angle was set at 90° (increased tibiotarsal joint angle = increased plantar flexion), which served as the reference angle for the remainder of the experiment. The peroneal nerve cuff leads were attached to a stimulator (Grass S8800, Astro-Med, Longueil, QC, Canada), and the {alpha}-motoneuron threshold was determined (pulse duration = 0.1 ms, frequency = 150 Hz, train duration = 500 ms).

First, preexercise isometric ankle torque was measured by supramaximally stimulating (3 x {alpha}-motoneuron threshold voltage, pulse duration = 0.1 ms, frequency = 150 Hz, train duration = 2,000 ms) the dorsiflexor muscles, beginning at a tibiotarsal angle of 55° and progressing in 5° increments to 155°. The foot was returned to a dorsiflexed position (55° tibiotarsal angle) for 2 min of rest between contractions. Then, cyclic lengthening contractions were performed from a tibiotarsal angle of 70 to 105° of plantar flexion at 70°/s for the SOS and SPS groups and from 95 to 145° of plantar flexion at 100°/s for the SPL group. Tibiotarsal torque was measured from strain gauges placed on the cam between the servo-motor and foot plate. The protocol consisted of five sets of ten cyclic lengthening contractions, with 2 min of rest between sets.

Afterward, isometric joint torque was once again measured for the 21 tibiotarsal joint angles (55–155° in 5° increments) for direct comparison to the preexercise values. To calculate the angle of peak joint torque for each rabbit, all values >75% of the absolute peak joint torque were normalized and fit with a second order polynomial, and peak joint torque was calculated as the peak value of the polynomial approximation (11). Individual shifts in the torque-joint angle relationships were calculated by comparing the angle of peak isometric joint torque postexercise to the angle of peak isometric joint torque production preexercise. The mean shift in peak joint torque production was calculated for each exercise group (SOS, SPS, SPL).

Data collection.   All data were collected via Sonosoft data-acquisition systems (Sonometrics, London, ON, Canada) at 498 samples per second. In addition, strain gauge signals were also recorded using WinDaq data-acquisition software (Dataq instruments, Akron, OH). Torque signals were low-pass filtered at 20 Hz through a second order recursive Butterworth filter (Intertechnology, Don Mills, ON, Canada). Fiber lengths during the entire protocol were measured using sonomicrometry with the two piezoelectric crystals inserted in a central, superficial fascicle (14, 24). Because fibers of the TA do not run the entire length of the muscle (33), we measured fascicle length. Thus the term "fiber" in this paper refers to fascicles that span the entire length of the TA from the distal to proximal aponeurosis. Percent fiber strain was calculated using Eq. 1.

Formula 1(1)
Briefly, the piezoelectric crystals can transmit and receive sound waves, allowing a measurement of the time interval between sound wave propagation from one crystal and reception by the other crystal. Because sound travels at a constant velocity (V) in both passive and contracting mammalian skeletal muscle (14), the distance between the two crystals (L), or the fascicle length, is simply a function of time, based on Eq. 2.

Formula 2(2)
Thus the difference ({Delta}T) between the instantaneous ultrasound transmission time (T) and the transmission time at the muscle fiber reference length just before starting the MTU activation and stretch (To) provides the change in fiber length during contraction. MTU length change was determined by using a tendon travel approach (2) after animals were killed.

Because of the complex fiber dynamics during eccentric contractions, we defined the stretch and shortening cycles of the fibers in all three groups with respect to Fig. 1 : active shortening, period of fiber shortening at the onset of MTU stretch as force is increasing (Br – Ar); active strain, period of fiber stretch during the eccentric MTU phase (Cr – Br); relaxation strain, period of fiber stretch at the beginning of passive MTU shortening, when muscle force is decreasing (Dr – Cr); passive shortening, period of fiber shortening during passive MTU shortening (Ar+1 – Dr). Lastly, maximum strain was calculated as the shortest fiber length subtracted from the longest fiber length during each repetition (Fig. 1, Dr – Br) and included both active and relaxation strains. Because of the change in activation timing for the SPS and SPL groups, active shortening of the fibers occurred during an isometric contraction of the MTU and preceded plantar flexion of the tibiotarsal joint by 100 ms. In addition, we kept activation duration constant at 500 ms between all three groups to minimize the confounding effects of fatigue between protocols. Thus the alteration of timing activation used in this study is associated with a complete shift of activation duration with respect to joint motion. Therefore, although active shortening occurs as a 100-ms isometric contraction in the SPS and SPL groups, the relaxation strain occurs during 100 ms of passive plantar flexion in these groups, whereas relaxation strain occurs during passive dorsiflexion in the SOS group.


Figure 1
View larger version (8K):
[in this window]
[in a new window]
  		Fig. 1. Top: representative raw data trace of repetition 1 showing fiber strain during one MTU stretch-shorten cycle for the SOS group (solid lines), SPS group (dashed line), and SPL group (dotted line). Subscript r represents eccentric-concentric repetition number. Ar, starting length of the fibers before each lengthening contraction. Br, shortest length of the fiber after the active shortening (Ar to Br) during the eccentric contraction. Active strain is defined as the change of fiber length during the eccentric phase from Br to Cr (Cr – Br). During the concentric, deactivated phase, the relaxation strain occurs from point Cr to point Dr, and the corresponding length change is calculated by Dr – Cr. After the relaxation strain, the fibers shorten as the MTU continues to shorten during the return of the foot to the initial, dorsiflexed position, and to point Ar of the next repetition, point Ar+1. Down arrows indicate start of activation. Middle: corresponding raw data trace of repetition 1 showing joint-torque during 1 muscle-tendon unit (MTU) stretch-shorten cycle for the SOS group (stimulation at onset of stretch, with lengthening contractions starting at a short muscle length; solid lines), SPS group (stimulation preceding stretch by 100 ms, with lengthening contractions starting at a short muscle length; dashed line), and SPL group (stimulation preceding stretch by 100 ms, with lengthening contractions starting at a longer muscle length; dotted line). Bottom: illustration of MTU length change for SOS group (solid line) and SPS and SPL groups (dashed line).

 
Statistics.   All statistical analyses were performed using SPSS version 12.0 (SPSS, Chicago, IL). For all parameters measured, means and SE are reported. A two-way analysis of variance was used to assess the effects of both activation timing and set on fiber strain magnitude. Significant interaction effects were analyzed by using a multivariate analysis of variance with a least squared differences post hoc analysis. To measure the difference in torque production and torque decrement between groups, a Kruskal-Wallis {chi}2 test was used. After the exercise protocol, MTU injury was measured using three different techniques: 1) by quantifying the rightward shift in the ankle torque joint-angle relationship, 2) by measuring the isometric joint torque decrement at 21 distinct tibiotarsal joint angles, and 3) by measuring the reduction in isometric joint torque production at optimal muscle length. Statistical significance was set at P < 0.05.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
During the stretch-shortening cycles the mechanical strains experienced by the MTU were similar between all three groups (P = 0.973). Mean MTU strains were 5.0 ± 0.2% for the SOS group, 5.0 ± 0.5% for the SPS group, and 5.2 ± 0.7% for the SPL group. Although activation timing and muscle length were altered, fiber dynamics were qualitatively similar between all three protocols, as fibers from all groups underwent a four-phase length change during one complete stretch-shortening cycle (Fig. 1), regardless of activation timing and starting muscle length. In addition, we observed that active fiber shortening diminished with each repetition in each set and recovered at the start of the following set. Comparison of joint torque and fiber length changes in these groups (data not shown) was consistent with our previous findings of an increasing compliance within the contractile element during repeated stretch-shortening cycles between sets for all groups (12).

Initially, fibers shortened upon activation and force production for all groups. Active fiber shortening occurred while the MTU was lengthening in the SOS group but occurred while the MTU length was constant in the SPS and SPL groups (Fig. 1, Br-Ar). Mean active fiber shortening was not significantly different between the three exercise groups (P = 0.081); however, active fiber shortening did vary significantly within groups, among sets (P < 0.001). Preactivation at long muscle lengths (SPL) resulted in significantly less active shortening compared with preactivation at short muscle lengths (SPS) in sets 1, 2, and 3 (P < 0.05, Fig. 2). A significant interaction of activation timing and set (P = 0.038) indicated that preactivation before stretch (SPS and SPL groups) resulted in a greater reduction in active shortening over time compared with the SOS group (Fig. 2).


Figure 2
View larger version (22K):
[in this window]
[in a new window]
  		Fig. 2. Mean active fiber shortening (defined as Br – Ar, Fig. 1) for all 50 repetitions in the SOS group ({circ}), the SPS group ({blacksquare}), and the SPL groups ({blacktriangleup}). Overall, altering the starting length of the muscle before stretch after preactivation had no effect on active fiber shortening, because the SPS and SPL groups were not significantly different. However, preactivation at short muscle length resulted in greater active shortening of the fibers compared with the SOS group in sets 1 and 2 ({ddagger}) and compared with the SPL group in sets 1, 2, and 4 ({dagger}).

 
Active fiber strain (Fig. 1, Cr – Br) was calculated during activation and lengthening of the MTU (lengthening contraction). Therefore, active strain in the SOS group ceased at the end of plantar flexion, or at a tibiotarsal joint angle of 105° (Fig. 1). Because of the offset of activation in the SPS and SPL groups, active strain ceased 100 ms before the end of plantar flexion. This occurred at a tibiotarsal joint angle of 98° for the SPS group and at a tibiotarsal joint angle of 135° for the SPL group. Simply altering the timing of activation at short muscle lengths did not significantly increase active fiber strain between the SOS and SPS groups (P = 0.065), but increasing starting length increased active fiber strain (SPL) compared with both SOS (P < 0.001) and SPS (P = 0.002) groups. Within groups, active fiber strains differed among sets (P < 0.001); however, there were no interaction effects between group and set (P = 0.625, Fig. 3).


Figure 3
View larger version (26K):
[in this window]
[in a new window]
  		Fig. 3. Mean active fiber strain (defined as Cr – Br, Fig. 1) for all 50 repetitions in the SOS ({circ}), SPS ({blacksquare}), and SPL ({blacktriangleup}) groups. Between groups, preactivation of the muscle before stretch at long muscle lengths resulted in significantly greater active fiber strains for all 50 repetitions compared with both exercise groups beginning at short muscle lengths. However, preactivation at short lengths did not significantly alter mean active strain values. Within sets, all active strain values obtained by exercise at long lengths (SPL group) were greater than those of the SOS (+) and SPS ({dagger}) groups. *Differences between groups.

 
Relaxation strain occurred at the cessation of activation in all three protocols. In the SOS group, relaxation strain occurred while the MTU was shortening, but in the SPS and SPL groups relaxation strain occurred while the MTU was lengthening for an additional 100 ms (Dr-Cr, Fig. 1). Relaxation strains differed significantly between the groups (P = 0.001) as well as within groups (P < 0.001), although the relaxation strains of both preactivation groups (SPS and SPL) were nearly identical (Fig. 4). Thus mean relaxation strains in both preactivation groups (SPS and SPL) were significantly greater than the SOS group (P < 0.001) but not significantly different from each other (P = 0.884, Fig. 4). The significant interaction effect (P < 0.001) indicated that relaxation strains significantly diminished over time but to a greater extent in the preactivation groups.


Figure 4
View larger version (21K):
[in this window]
[in a new window]
  		Fig. 4. Mean relaxation fiber strain (defined as Dr – Cr, Fig. 1) for all 50 repetitions in the SOS ({circ}), SPS ({blacksquare}), and SPL ({blacktriangleup}) groups. Between groups, preactivation of the muscle before stretch (SPS and SPL groups) resulted in significantly greater relaxation fiber strains for all 50 repetitions compared with exercise beginning at short muscle without preactivation (SOS group). Within sets, preactivating the muscle before stretch (SPS, SPL) resulted in significantly greater relaxation fiber strains compared with the SOS group (+, {ddagger}) for every set. However, there was no significant difference in relaxation fiber strains in the preactivation groups in any set, regardless of starting muscle length (SPL compared with SPS). *Differences between groups.

 
Maximum fiber strain [the sum of active and relaxation fiber strains (Dr – Br, Fig. 1)] was significantly altered by preactivation. Preactivating the muscle before stretch at short lengths (SPS) significantly increased maximum strain compared with the SOS group (P < 0.001), whereas increasing starting muscle length also resulted in significantly greater maximum fiber strain compared with both the SOS (P < 0.001) and SPS groups (P = 0.036). There was a significant interaction of exercise group and set (P < 0.001), indicating that although maximum fiber strains in the preactivation groups (SPS and SPL) differed from the maximum fiber strains in the SOS group, these differences varied between sets for the duration of the exercise (Fig. 5).


Figure 5
View larger version (23K):
[in this window]
[in a new window]
  		Fig. 5. Mean maximum fiber strain (defined as Dr – Br, Fig. 1) for all 50 repetitions in the SOS ({circ}), SPS ({blacksquare}), and SPL ({blacktriangleup}) groups. Maximum strain is the sum of active strain and relaxation strain. Maximum strain was significantly different between all 3 groups and within all 5 sets. Preactivation before stretch at short muscle lengths significantly increased maximum strain compared with the values obtained from stretch without preactivation at the short muscle length ({ddagger}). However, preactivation at the long muscle length resulted in significantly greater maximum strains compared with exercise at short length, both with ({dagger}) and without (+) preactivation. *Differences between groups.

 
Torque joint-angle relationship.   Peak isometric joint torque was reduced at all tibiotarsal joint angles in all three groups, and the shape of the torque-angle curve was altered after the exercise protocols (Figs. 6–8). After the exercise bouts, peak joint torque was produced at a greater tibiotarsal joint angle (corresponding to a longer muscle length) within each group compared with preexercise values in the SOS group (+7.7 ± 1.9°, P = 0.028, Fig. 6), the SPS group (+7.9 ± 1.8°, P = 0.01, Fig. 7), and the SPL group (+10.9 ± 1.0°, P < 0.001, Fig. 8). However, these rightward shifts were not significantly different between the three groups (P = 0.122).


Figure 6
View larger version (18K):
[in this window]
[in a new window]
  		Fig. 6. Preexercise ({circ}) and postexercise (bullet) torque-joint angle relationship for the SOS group. Note the shift of peak joint torque production to a greater joint angle and a change in the shape of the relationship after the exercise bouts. Inset: normalized values >75% peak torque for pre- ({circ}) and postexercise (bullet) values in each group were fitted with a second order polynomial, depicting the rightward shift in peak joint torque production after exercise (+7.7 ± 1.9°).

 

Figure 8
View larger version (18K):
[in this window]
[in a new window]
  		Fig. 8. Preexercise ({triangleup}) and postexercise ({blacktriangleup}) torque-joint angle relationship for the SPL group. Note the significant shift of peak joint torque production to a greater joint angle and a change in the shape of the relationship after the exercise bout. Inset: normalized values >75% peak torque for preexercise ({triangleup}) and postexercise ({blacktriangleup}) values in each group were fitted with a second order polynomial, depicting the rightward shift in peak joint torque production after exercise (+10.9 ± 1.0°).

 

Figure 7
View larger version (17K):
[in this window]
[in a new window]
  		Fig. 7. Preexercise ({square}) and postexercise ({blacksquare}) torque-joint angle relationship for the SPS group. Note the significant shift of peak joint torque production to a greater joint angle and a change in the shape of the relationship after the exercise bout. Inset: normalized values >75% peak torque for comparing preexercise ({square}) and postexercise ({blacksquare}) values in each group were fitted with a second order polynomial, depicting the rightward shift in peak joint torque production after exercise (+7.9 ± 1.8°).

 
Isometric joint torque decrement at various tibiotarsal joint angles.   After the eccentric exercise protocol, the reduction in mean isometric joint torque was not significantly different between any of the three groups at the shortest muscle length, which corresponded to a tibiotarsal joint angle of 55° (P = 0.334, Fig. 9). However, applying a preactivation before stretch at short muscle lengths (SPS) and long muscle lengths (SPL) significantly reduced postexercise isometric joint torque at tibiotarsal joint angles of 60° and greater compared with the SOS group. Exercise at long lengths (SPL) resulted in the greatest reduction in postexercise isometric joint torque at all tibiotarsal joint angles >60° (Fig. 9).


Figure 9
View larger version (18K):
[in this window]
[in a new window]
  		Fig. 9. Reduction in peak joint torque at all 21 tibiotarsal joint angles for the SOS ({circ}), SPS ({blacksquare}), and SPL ({blacktriangleup}) groups. Values are expressed as a percentage reduction from the preexercise joint-torque at the corresponding angle. Preactivation at short muscle length before stretch as well as increasing starting muscle length before stretch both resulted in significantly greater reduction in peak joint torque production at all tibiotarsal joint angles >55°. *Significantly different reduction in postexercise isometric joint torque between all 3 groups at the joint angle indicated.

 
Reduction in isometric joint torque at optimal length.   The tibiotarsal joint angle at which the peak joint torque was produced shifted rightward after the exercise protocol in all three groups (Figs. 6–8). Therefore, we identified this new optimum muscle length after exercise and selected the corresponding peak isometric joint torque for comparison to the preexercise values. The mean reduction in peak joint torque after the lengthening contraction bouts was significantly different between groups (P = 0.003). The values were 26.9 ± 1.8% for the SOS group, 37.3 ± 2.7% for the SPS group, and 50.2 ± 3.8% for the SPL group. At short muscle lengths, a small alteration in the timing of muscle activation (SPS group) resulted in a significantly greater reduction in peak isometric joint torque compared with exercise at short muscle lengths without preactivation (SOS group). Additionally, increasing the starting length of the muscle before the cyclic stretch-shortening protocol also resulted in a significantly greater reduction in peak isometric joint torque production compared with both short muscle length groups, with (SPS) and without (SOS) preactivation.

Peak joint torque during stretch-shortening cycles.   Peak joint torque produced during the cyclic stretch-shortening cycles was produced at the longest fiber length magnitudes during activation, corresponding to the end of active fiber strain (point C, Fig. 1). Preactivating the muscle before stretch at short muscle lengths (SPS group) resulted in a significant increase in joint torque for all repetitions of the first three sets (Fig. 10, P < 0.05). In sets 4 and 5, preactivation resulted in significantly greater joint torque for only the last five and six repetitions, respectively (Fig. 10). Increasing the starting muscle length before stretch (SPL) resulted in greater joint torque production in sets 2 and 3 compared with the SOS group (P < 0.05). However, comparing the preactivation groups (SPS, SPL), increasing starting length (SPL) did not result in greater joint torque. Surprisingly, the SPL group produced torque values that were not different than the SOS group in the last two sets, illustrating that preactivation at longer muscle lengths does not significantly increase peak torque production for the majority of the stretch-shortening cycle (Fig. 10).


Figure 10
View larger version (20K):
[in this window]
[in a new window]
  		Fig. 10. Mean peak joint torque produced during the lengthening contractions for all 50 repetitions in the SOS ({circ}), SPS ({blacksquare}), and SPL ({blacktriangleup}) groups. Preactivation at short and long lengths resulted in a significantly greater torque production compared with exercise without preactivation. However, increasing muscle length before exercise (SPL) never increased joint torque compared with preactivation at short lengths (SPS). *SPS torque significantly greater than SOS torque; +SPL torque significantly greater than SOS torque; #SPS and SPL torque greater than SOS torque.

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
ACKNOWLEDGMENTS
 REFERENCES
 
The purpose of this study was to alter the timing of activation and starting muscle length before repetitive stretch-shortening cycles in an in vivo rabbit model and to measure the subsequent effects on fiber strain, peak force and muscle injury (7, 16, 22, 50). Traditionally, variables that influence muscle strain injuries have been measured in in vitro or in situ single-stretch protocols, whereby peak force and fiber strain have been studied as potential contributors to the muscle strain injury etiology. In an effort to keep our protocol as physiologically representative as possible (22), we used a physiological range of motion in this study (~5% MTU strain) and therefore needed to subject the muscles to a greater number of repetitive stretch-shortening cycles to induce injury (16, 23, 56, 57). Here, after repetitive lengthening contractions in vivo, muscle injury, as assessed by three different means, was significantly increased by altering activation timing at short lengths or increasing the starting length before the cycles.

Peak torque in the angle-torque relationship was produced at longer muscle lengths after all three exercise protocols (Fig. 6–8); however, the difference in the magnitude of the rightward shift was relatively small after exercise at short muscle lengths (7.7 ± 1.9° in the SOS group, and 7.9 ± 1.8° in the SPS group) and was not significantly increased after exercise at long lengths (10.9 ± 1.0° in the SPL group). Traditionally, the rightward shift in the FLR has been used as an indicator of muscle injury magnitude, with a greater injury resulting in a greater rightward shift (55). Recently, we showed that the shift in the FLR after lengthening contractions may not be sensitive enough to determine injury at short muscle lengths, where fatigue effects may confound the shift (11). Therefore we also quantified muscle injury by the difference in the reduction in joint torque between the three exercise groups.

To maintain a consistent metabolic cost during exercise bouts, activation duration was kept at 500 ms for all three protocols. Although there is evidence of a length dependence for fatigue in mammalian skeletal muscle, whereby exercise at long muscle lengths exhibits less fatigue compared with short lengths, there is some dispute as to whether isometric contractions at short muscle lengths (46, 47) exhibit greater fatigue than corresponding isometric contractions at optimal lengths (41). Here, the two groups used at the short muscle lengths exhibited significantly different torque decrement based on timing of activation, indicating a disparate effect of the activation timing on muscle damage, as fatigue is assumed to be similar in these two groups at identical exercise lengths. In addition, the dynamic, active lengthening contractions performed in the present study included the optimal tibiotarsal joint angle in the exercise range of motion in all groups. Also, if the two groups that were exercised at short muscle lengths exhibited greater fatigue compared with the groups exercised at long lengths, that would only exacerbate the difference in injury measured between the short and long length groups. Furthermore, the trend toward peak force production at longer muscle lengths, as well as a narrowing of the torque-joint angle relationship after exercise, further confirms that exercise at longer lengths resulted in greater subcellular damage compared with exercise at short lengths (45). Therefore, we surmised that the significant differences in peak isometric torque values postexercise were due to injury and not fatigue (34).

We observed a significant difference in the reduction of isometric joint torque at all joint angles >55° between the three groups (Fig. 9), indicating that force production was affected at nearly all muscle and sarcomere lengths within the physiological range. The greatest reduction in peak joint torque observed was at short muscle lengths. Similar results have been reported previously after lengthening contraction induced injury and may be explained by damage to calcium handling structures (11, 16). Previously, we have measured a progressive increase in compliance of the contractile element during repeated stretch-shortening cycles (12), which may also contribute to the greater loss of force at short compared with long muscle lengths (42).

The reduction in peak isometric joint torque after lengthening contractions has been proposed to be the most sensitive means of quantifying muscle injury (44). Peak joint torque at optimal muscle length was decreased by 27% in the SOS group. This value increased to 37% by simply altering activation timing in the SPS group, while maintaining a consistent 5% muscle strain. In a previous study, it had been reported that the alteration of activation timing changed muscle injury magnitudes after three stretch-shortening cycles of 30% muscle strain in vitro (50). Here, we were able to produce muscle injury through repetitive stretch-shortening cycles using small magnitude muscle strains, within the physiological capabilities.

By increasing the length of the muscle before contraction (SPL), peak joint torque was reduced to a greater extent (50% of the preexercise value) after the stretch-shortening cycles, compared with those using short muscle lengths (SOS, SPS). Although muscle length has been proposed as a key variable in strain induced muscle injury, much of this work has been performed in vitro (23, 52, 58) or in situ (27, 55) by single or multiple stretch protocols, often utilizing large magnitudes of muscle stretch beyond the physiological range (27). Few studies have assessed the influence of starting muscle length on muscle injury in vivo (16, 39, 43), and only one has utilized a similar approach to the one used here (16). Using in vivo rat dorsiflexors, Cutlip et al. (16) found significantly greater muscle injury after 70 stretch-shortening contractions at long compared with short muscle lengths. Because this study focused on the time-dependent effects of muscle injury, no attempt was made to explain why exercise at longer muscle lengths resulted in greater injury. Recently, muscle injury after repetitive lengthening contractions within a physiological range has been associated with the peak forces produced (23). However, as we have shown here, peak joint torque was significantly less for the majority of the stretch-shortening cycles at long muscle lengths compared with the corresponding peak torque at short muscle lengths. It is notable, however, that the rate of decay of joint torque appears to be greatest during exercise at long muscle lengths (Fig. 10), possibly indicating an increased rate of damage as exercise progressed.

In this study, preactivation of the muscle before stretch at short muscle lengths resulted in significantly greater peak joint torque production during the majority of the 50 stretch-shortening cycles compared with the SOS group (Fig. 10). This is in agreement with others who have preactivated the muscle in an effort to increase force production before stretch (34), but the first to show the difference across repetitions. Here, preactivating the muscle at short lengths resulted in both greater peak joint torque production and subsequently greater muscle injury, as defined by the decrease in isometric torque production at optimal length. In contrast, increasing the starting length of the muscle before stretch resulted in greater muscle injury, but it did not result in greater peak joint torque being produced during exercise, implying either that the mechanism of injury is different between the groups or that another variable may have a greater influence.

Fiber strains have never been directly measured during in vivo, controlled cyclic stretch-shortening cycles before. Although Lieber and Fridén (34) found fiber strain to be the best predictor of the observed muscle injury after repetitive lengthening contractions, fiber strains were estimated and assumed to be constant throughout 900 stretch-shortening cycles. However, in their study, increased fiber strain was achieved by a greater magnitude and rate of muscle stretch. Although greater muscle excursion has been shown to result in greater muscle injury (49), the direct association between injury, fiber dynamics and muscle dynamics can be tenuous, as we have shown here. In this study, we maintained an identical mechanical strain to the MTU during all three exercise protocols. By applying a preactivation before stretch at short muscle lengths, fiber shortening and joint torque were significantly increased (Fig. 2). However, at long muscle length, active strain was significantly increased compared with active strain during exercise at short muscle lengths (Fig. 3), but torque values remained unaffected by increasing muscle length. Therefore, although active strain has been proposed to be the best predictor of muscle strain injury (34), it may not hold true for exercise at all muscle lengths, because peak torque was significantly increased only at short lengths, but active fiber strains were only greater at the long muscle length.

Although Lieber and Fridén measured muscle strain and estimated fiber length (34), we measured fiber length directly. By defining active strain as the magnitude of fiber stretch during the application of stimulation, active strain did not include the greatest fiber length change, as this occurred at the cessation of muscle stimulation. The significant increase in fiber strains observed at short muscle lengths using preactivation occurred at the cessation of external activation of the muscle. Although activation ceased before the end of muscle stretch, force was still produced by the muscle, albeit decreasing rapidly. This drop in force as the muscle approached the end range of stretch resulted in relaxation strains that were over 100% greater than those obtained without preactivation (Fig. 4).

Together, active strain and relaxation strain add up to what we have defined as maximum fiber strain (Fig. 1). At short muscle lengths active strain was not significantly increased with preactivation, although relaxation strain was. This may be due to the compliance at short muscle lengths, which allowed for greater active fiber shortening in the preactivated (SPS) compared with the normal (SOS) group. At the long length, the increased stiffness of the MTU prohibited great active shortening and therefore limited the amount of energy that could be stored and released within the MTU. Overall, maximum fiber strain was significantly increased with preactivation as well as increased starting muscle length, coincident with muscle injury. However, the manner in which maximum strain increased was different between the groups: first, at the short length, preactivation allowed for greater active shortening, no change in active strain, and greater relaxation strain; and, second, at the long muscle length, active shortening was limited, resulting in greater active strain and no change in relaxation strain. Together these active and relaxation strains result in a significantly greater maximum strain at the short muscle length owing to changes in the relaxation strain with preactivation and a greater maximum strain at the long muscle length owing to changes in active strain magnitude.

One limitation to this study was the method used to alter the timing of activation. To effectively limit the effects of fatigue across groups, we chose to use an activation of identical duration (500 ms) for all three groups. Therefore the timing of activation during the stretch-shortening cycles resulted in a shift of activation by 100 ms, causing relaxation strains to occur during passive plantar flexion in two of the three groups studied (SPS and SPL). It is possible that the duration of the activation period relative to the stretch duration may produce the differences observed between the groups and that the timing of activation cessation may be another important variable that must be considered in muscle injury research.

In summary, muscle strain injuries can be insidious, and the culmination of small mechanical alterations within the muscle may result in sudden pain and loss of function. This is the first study to show that a muscle subjected to repeated stretch-shortening cycles of constant MTU excursion exhibits significantly different joint torque and fiber strains when the timing of activation or starting muscle length are changed. These results lend support to a mechanism of strain induced muscle injury as proposed by Best and Garrett (7), whereby a "poorly understood neuromuscular coordination pattern" may contribute to muscle strain injuries. Therefore, we conclude that activation timing and muscle length before stretch may influence muscle injury by significantly increasing fiber strain magnitude and that fiber dynamics are more important variables than MTU dynamics or muscle force in influencing the magnitude of muscle damage.


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
REFERENCES
 
We thank Tim Leonard and Hoa Nguyen for technical assistance, the Canadian Institutes of Health Research (CIHR) Training Program in Bone and Joint Health, National Sciences and Engineering Research Council of Canada, and the CIHR Research Chair Program.


   FOOTNOTES
 

Address for reprint requests and other correspondence: W. Herzog, Faculty of Kinesiology, Univ. of Calgary, Calgary, Alberta, Canada T2N 1N4 (e-mail: walter{at}kin.ucalgary.ca)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 

  1. Agre JC. Hamstring injuries. Proposed aetiological factors, prevention, and treatment. Sports Med 2: 21–33, 1985.[ISI][Medline]
  2. An KN, Takahashi K, Harrigan TP, and Chao EY. Determination of muscle orientations and moment arms. J Biomech Eng 106: 280–282, 1984.[ISI][Medline]
  3. Armstrong RB, Ogilvie RW, and Schwane JA. Eccentric exercise-induced injury to rat skeletal muscle. J Appl Physiol 54: 80–93, 1983.[Abstract/Free Full Text]
  4. Balnave CD and Allen DG. Intracellular calcium and force in single mouse muscle fibres following repeated contractions with stretch. J Physiol 488: 25–36, 1995.[ISI][Medline]
  5. Balnave CD, Davey DF, and Allen DG. Distribution of sarcomere length and intracellular calcium in mouse skeletal muscle following stretch-induced injury. J Physiol 502: 649–659, 1997.[CrossRef][ISI][Medline]
  6. Barash IA, Peters D, Fridén J, Lutz GJ, and Lieber RL. Desmin cytoskeletal modifications after a bout of eccentric exercise in the rat. Am J Physiol Regul Integr Comp Physiol 283: R958–R963, 2002.[Abstract/Free Full Text]
  7. Best TM and Garrett WE. Hamstring strains: expediting return to pay. Physician Sportsmed 24: 37–44, 1996.
  8. Brockett CL, Morgan DL, and Proske U. Human hamstring muscles adapt to eccentric exercise by changing optimum length. Med Sci Sports Exerc 33: 783–790, 2001.[CrossRef][ISI][Medline]
  9. Brockett CL, Morgan DL, and Proske U. Predicting hamstring strain injury in elite athletes. Med Sci Sports Exerc 36: 379–387, 2004.[CrossRef][ISI][Medline]
  10. Burkett LN. Causative factors in hamstring strains. Med Sci Sports 2: 39–42, 1970.[Medline]
  11. Butterfield TA and Herzog W. Is the force-length relationship a useful indicator of contractile element damage following eccentric exercise? J Biomech 38: 1932–1937, 2005.[CrossRef][ISI][Medline]
  12. Butterfield TA and Herzog W. Quantification of muscle fiber strain during in vivo repetitive stretch-shortening cycles. J Appl Physiol 99: 593–602, 2005.[Abstract/Free Full Text]
  13. Caiozzo VJ and Green S. Breakout session 2: muscle injury. Clin Orthop 403, Suppl: S120–S125, 2002.
  14. Caputi AA, Hoffer JA, and Pose IE. Velocity of ultrasound in active and passive cat medial gastrocnemius muscle. J Biomech 25: 1067–1074, 1992.[CrossRef][ISI][Medline]
  15. Croisier JL, Forthomme B, Namurois MH, Vanderthommen M, and Crielaard JM. Hamstring muscle strain recurrence and strength performance disorders. Am J Sports Med 30: 199–203, 2002.[Abstract/Free Full Text]
  16. Cutlip RG, Geronilla KB, Baker BA, Kashon ML, Miller GR, and Schopper AW. Impact of muscle length during stretch-shortening contractions on real-time and temporal muscle performance measures in rats in vivo. J Appl Physiol 96: 507–516, 2004.[Abstract/Free Full Text]
  17. Fridén J. Changes in human skeletal muscle induced by long-term eccentric exercise. Cell Tissue Res 236: 365–372, 1984.[ISI][Medline]
  18. Fridén J and Lieber RL. Segmental muscle fiber lesions after repetitive eccentric contractions. Cell Tissue Res 293: 165–171, 1998.[CrossRef][ISI][Medline]
  19. Fridén J, Sjostrom M, and Ekblom B. Myofibrillar damage following intense eccentric exercise in man. Int J Sports Med 4: 170–176, 1983.[ISI][Medline]
  20. Garrett WE Jr. Muscle strain injuries: clinical and basic aspects. Med Sci Sports Exerc 22: 436–443, 1990.[ISI][Medline]
  21. Garrett WE Jr. Muscle strain injuries. Am J Sports Med 24: S2–S8, 1996.[ISI][Medline]
  22. Geronilla KB, Miller GR, Mowrey KF, Wu JZ, Kashon ML, Brumbaugh K, Reynolds J, Hubbs A, and Cutlip RG. Dynamic force responses of skeletal muscle during stretch-shortening cycles. Eur J Appl Physiol 90: 144–153, 2003.[CrossRef][ISI][Medline]
  23. Gosselin LE and Burton H. Impact of initial muscle length on force deficit following lengthening contractions in mammalian skeletal muscle. Muscle Nerve 25: 822–827, 2002.[CrossRef][ISI][Medline]
  24. Griffiths RI. Shortening of muscle fibres during stretch of the active cat medial gastrocnemius muscle: the role of tendon compliance. J Physiol 436: 219–236, 1991.[Abstract/Free Full Text]
  25. Hof AL, Geelen BA, and Van den Berg J. Calf muscle moment, work and efficiency in level walking; role of series elasticity. J Biomech 16: 523–537, 1983.[CrossRef][ISI][Medline]
  26. Hoffer JA, Caputi AA, Pose IE, and Griffiths RI. Roles of muscle activity and load on the relationship between muscle spindle length and whole muscle length in the freely walking cat. Prog Brain Res 80: 75–85, 1989.[ISI][Medline]
  27. Hunter KD and Faulkner JA. Pliometric contraction-induced injury of mouse skeletal muscle: effect of initial length. J Appl Physiol 82: 278–283, 1997.[Abstract/Free Full Text]
  28. Ingalls CP, Wenke JC, Nofal T, and Armstrong RB. Adaptation to lengthening contraction-induced injury in mouse muscle. J Appl Physiol 97: 1067–1076, 2004.[Abstract/Free Full Text]
  29. Jonhagen S, Nemeth G, and Eriksson E. Hamstring injuries in sprinters. The role of concentric and eccentric hamstring muscle strength and flexibility. Am J Sports Med 22: 262–266, 1994.[Abstract/Free Full Text]
  30. Katz B. The relation between force and speed in muscular contraction. J Physiol 96: 45–64, 1939.
  31. Kirkendall DT and Garrett WE Jr. Clinical perspectives regarding eccentric muscle injury. Clin Orthop S81–S89, 2002.
  32. Koh TJ and Herzog W. Eccentric training does not increase sarcomere number in rabbit dorsiflexor muscles. J Biomech 31: 499–501, 1998.[CrossRef][ISI][Medline]
  33. Lieber RL and Blevins FT. Skeletal muscle architecture of the rabbit hindlimb: functional implications of muscle design. J Morphol 199: 93–101, 1989.[CrossRef][ISI][Medline]
  34. Lieber RL and Fridén J. Muscle damage is not a function of muscle force but active muscle strain. J Appl Physiol 74: 520–526, 1993.[Abstract/Free Full Text]
  35. Lieber RL and Fridén J. Mechanisms of muscle injury gleaned from animal models. Am J Phys Med Rehabil 81: S70–S79, 2002.[CrossRef][ISI][Medline]
  36. Lieber RL, Shah S, and Fridén J. Cytoskeletal disruption after eccentric contraction-induced muscle injury. Clin Orthop 403, Suppl: S90–S99, 2002.
  37. McCully KK and Faulkner JA. Injury to skeletal muscle fibers of mice following lengthening contractions. J Appl Physiol 59: 119–126, 1985.[Abstract/Free Full Text]
  38. McHugh MP, Connolly DA, Eston RG, Gartman EJ, and Gleim GW. Electromyographic analysis of repeated bouts of eccentric exercise. J Sports Sci 19: 163–170, 2001.[CrossRef][ISI][Medline]
  39. McHugh MP and Pasiakos S. The role of exercising muscle length in the protective adaptation to a single bout of eccentric exercise. Eur J Appl Physiol 93: 286–293, 2004.[CrossRef][ISI][Medline]
  40. McHugh MP and Tetro DT. Changes in the relationship between joint angle and torque production associated with the repeated bout effect. J Sports Sci 21: 927–932, 2003.[CrossRef][ISI][Medline]
  41. McKenzie DK and Gandevia SC. Influence of muscle length on human inspiratory and limb muscle endurance. Respir Physiol 67: 171–182, 1987.[CrossRef][ISI][Medline]
  42. Morgan DL. New insights into the behavior of muscle during active lengthening. Biophys J 57: 209–221, 1990.[Abstract/Free Full Text]
  43. Newham DJ, Jones DA, Ghosh G, and Aurora P. Muscle fatigue and pain after eccentric contractions at long and short length. Clin Sci (Lond) 74: 553–557, 1988.[Medline]
  44. Noonan TJ, Best TM, Seaber AV, and Garrett WE Jr. Identification of a threshold for skeletal muscle injury. Am J Sports Med 22: 257–261, 1994.[Abstract/Free Full Text]
  45. Proske U and Morgan DL. Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. J Physiol 537: 333–345, 2001.[Abstract/Free Full Text]
  46. Rassier DE. The effects of length on fatigue and twitch potentiation in human skeletal muscle. Clin Physiol 20: 474–482, 2000.[CrossRef][ISI][Medline]
  47. Sacco P, McIntyre DB, and Jones DA. Effects of length and stimulation frequency on fatigue of the human tibialis anterior muscle. J Appl Physiol 77: 1148–1154, 1994.[Abstract/Free Full Text]
  48. Safran MR, Garrett WE Jr, Seaber AV, Glisson RR and Ribbeck BM. The role of warmup in muscular injury prevention. Am J Sports Med 16: 123–129, 1988.[Abstract/Free Full Text]
  49. Song H, Nakazato K, and Nakajima H. Effect of increased excursion of the ankle on the severity of acute eccentric contraction-induced strain injury in the gastrocnemius: an in vivo rat study. Am J Sports Med 32: 1263–1269, 2004.[Abstract/Free Full Text]
  50. Stevens ED. Effect of phase of stimulation on acute damage caused by eccentric contractions in mouse soleus muscle. J Appl Physiol 80: 1958–1962, 1996.[Abstract/Free Full Text]
  51. Talbot JA and Morgan DL. Quantitative analysis of sarcomere non-uniformities in active muscle following a stretch. J Muscle Res Cell Motil 17: 261–268, 1996.[CrossRef][ISI][Medline]
  52. Talbot JA and Morgan DL. The effects of stretch parameters on eccentric exercise-induced damage to toad skeletal muscle. J Muscle Res Cell Motil 19: 237–245, 1998.[CrossRef][ISI][Medline]
  53. Taylor DC, Dalton JD Jr, Seaber AV and Garrett WE Jr. Viscoelastic properties of muscle-tendon units. The biomechanical effects of stretching. Am J Sports Med 18: 300–309, 1990.[Abstract/Free Full Text]
  54. Warren GL, Hayes DA, Lowe DA, and Armstrong RB. Mechanical factors in the initiation of eccentric contraction-induced injury in rat soleus muscle. J Physiol 464: 457–475, 1993.[Abstract/Free Full Text]
  55. Whitehead NP, Morgan DL, Gregory JE, and Proske U. Rises in whole muscle passive tension of mammalian muscle after eccentric contractions at different lengths. J Appl Physiol 95: 1224–1234, 2003.[Abstract/Free Full Text]
  56. Willems ME and Stauber WT. Changes in force by repeated stretches of skeletal muscle in young and old female Sprague Dawley rats. Aging (Milano) 12: 478–481, 2000.[Medline]
  57. Willems ME and Stauber WT. Force deficits after repeated stretches of activated skeletal muscles in female and male rats. Acta Physiol Scand 172: 63–67, 2001.[CrossRef][ISI][Medline]
  58. Wood SA, Morgan DL, and Proske U. Effects of repeated eccentric contractions on structure and mechanical properties of toad sartorius muscle. Am J Physiol Cell Physiol 265: C792–C800, 1993.[Abstract/Free Full Text]
  59. Yeung EW, Balnave CD, Ballard HJ, Bourreau JP, and Allen DG. Development of T-tubular vacuoles in eccentrically damaged mouse muscle fibres. J Physiol 540: 581–592, 2002.[Abstract/Free Full Text]
  60. Yeung EW, Bourreau JP, Allen DG, and Ballard HJ. Effect of eccentric contraction-induced injury on force and intracellular pH in rat skeletal muscles. J Appl Physiol 92: 93–99, 2002.[Abstract/Free Full Text]
  61. Zajac FE. Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. Crit Rev Biomed Eng 17: 359–411, 1989.[ISI][Medline]
  62. Zarins B and Ciullo JV. Acute muscle and tendon injuries in athletes. Clin Sports Med 2: 167–182, 1983.[Medline]



This article has been cited by other articles:


Home page
 Biophys. JHome page
A. Panchangam, D. R. Claflin, M. L. Palmer, and J. A. Faulkner
Magnitude of Sarcomere Extension Correlates with Initial Sarcomere Length during Lengthening of Activated Single Fibers from Soleus Muscle of Rats
Biophys. J., August 15, 2008; 95(4): 1890 - 1901.
[Abstract] [Full Text] [PDF]

Home page
 J. Appl. Physiol.Home page
A. J. Blazevich, D. Cannavan, D. R. Coleman, and S. Horne
Influence of concentric and eccentric resistance training on architectural adaptation in human quadriceps muscles
J Appl Physiol, November 1, 2007; 103(5): 1565 -