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Passive stretching is commonly used to increase limb range of movement prior to athletic performance but it is unclear which component of the muscle–tendon unit (MTU) is affected by this procedure. Movement of the myotendinous junction (MTJ) of the gastrocnemius medialis muscle was measured by ultrasonography in eight male participants (20.5 ± 0.9 years) during a standard stretch in which the ankle was passively dorsiflexed at 1 deg s−1 from 0 deg (the foot at right angles to the tibia) to the participants' volitional end range of motion (ROM). Passive torque, muscle fascicle length and pennation angle were also measured. Standard stretch measurements were made before (pre-) and after (post-) five passive conditioning stretches. During each conditioning stretch the MTU was taken to the end ROM and held for 1 min. Pre-conditioning the extension of the MTU during stretch was taken up almost equally by muscle and tendon. Following conditioning, ROM increased by 4.6 ± 1.5 deg (17%) and the passive stiffness of the MTU was reduced (between 20 and 25 deg) by 47% from 16.0 ± 3.6 to 10.2 ± 2.0 Nm deg−1. Distal MTJ displacement (between 0 and 25 deg) increased from 0.92 ± 0.06 to 1.16 ± 0.05 cm, accounting for all the additional MTU elongation and indicating that there was no change in tendon properties. Muscle extension pre-conditioning was explicable by change in length and pennation angle of the fascicles but post-conditioning this was not the case suggesting that at least part of the change in muscle with conditioning stretches was due to altered properties of connective tissue.
Pre-exercise stretching is an integral part of many athletes' warm-up routines (Dadebo et al. 2004) and may be performed for many reasons but, probably, the most common is to increase flexibility. It is often assumed that these procedures change the physical properties of tendons (Witvrouw et al. 2004) but there is little objective evidence to support this view. Flexibility is usually quantified by measuring the maximum range of motion about a joint (ROM), such as in the sit and reach test (Pollock & Wenger, 1998). However, in this type of test a number of limitations have been reported; for example, the only measure is the end point of the movement which can be influenced by factors such as pain, stretch tolerance and reflex activation of the agonist muscle (Magnusson et al. 1996a; McHugh et al. 1998); nor does it give any information about the elastic properties of the muscle or tendon. An alternative approach is to determine the joint torque during a passive stretch (Sale et al. 1982) and the relationship between joint angle and torque is a measure of the overall stiffness of the muscle–tendon unit (MTU).
The stretching used by athletes usually involves taking the MTU to the end of the range of motion and holding it there for up to 1 min before relaxing and then repeating the procedure several times. There have been several reports that stretching of this nature reduces the slope of the relationship between joint angle and passive torque of the muscle–tendon unit, and consistently leads to an increase in the end range of motion (Wilson et al. 1992; Halbertsma et al. 1996; Evetovich et al. 2003; Witvrouw et al. 2004; Reisman et al. 2005). In none of these cases, however, was it possible to determine whether the change in MTU stiffness was due to alterations in the properties of the muscle or the tendon or some combination of the two.
Magnusson et al. (1997) proposed that the material properties of the muscle contribute to passive torque and Gajdosik (2001) suggested, more specifically, that the cytoskeleton of the sarcomere and intramuscular connective tissue constitute parallel elastic components that contribute to passive tension, modification of which could lead to a change in overall stiffness of the MTU. However, muscle fibres themselves are known to exhibit thixotropic properties although whether this short range elastic component resides in a small population of attached crossbridges or is a property of titin remains a matter of debate (Proske & Morgan, 1984; Rassier et al. 2005). Nevertheless changing the thixotropic state of the muscle fibres could account for the change in stiffness with stretching.
It was previously thought that the Achilles tendon contributed little to the increase in length of the MTU during stretch (Halar et al. 1978) but this now seems unlikely given the demonstration of the compliant nature of tendons in vivo (Fukunaga et al. 1996). Indeed, Herbert et al. (2002) report that during passive dorsiflexion and stretching of the gastrocnemius muscle only 27% of the overall length change was ‘seen’ as an increase in the muscle fascicle length and consequently the tendon, or other structures, must make the major contribution to the passive extension of the MTU.
The stiffness of the tendon can be estimated by ultrasonography, following the movement of the myotendinous junction during a ramped isometric contraction (Maganaris & Paul, 1999). Kubo et al. (2001) measured tendon stiffness in this manner before and after 5 min of passive stretching and reported an 8% decrease in stiffness and changes in the tendon hysteresis. However, the length–tension relationship of tendon is non-linear and the stiffness measured under the high forces generated during isometric contractions is unlikely to represent the stiffness of the tendon when subject to the relatively low forces involved in passive movement of the MTU (Ettema & Huijing, 1989; Lieber & Friden, 2000). It remains an open question therefore as to whether the changes in MTU properties as a result of stretching during warm-up are due to changes in the muscle or tendon.
There were three objectives of the work described here; the first was to make direct observations of the myotendinous junction to further the work of Herbert et al. (2002) and determine to what degree the muscle fascicles, distal tendon and aponeurosis contribute to the change in length of the MTU during passive stretching of the gastrocnemius medialis (GM). The second objective was to see if the conditioning achieved by passive stretch during warm-up could be replicated by a series of rapid short stretches that are known to reset the thixotropic properties of muscle. The third objective was to determine the extent to which muscle conditioning changes the properties of the tendon, muscle fascicles or other structures, to produce the change in overall stiffness of the MTU and increased flexibility sought after by many athletes.
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The findings reported here have confirmed the suggestion of Herbert et al. (2002) that in a resting pre- or non-conditioned MTU, such as the gastrocnemius medialis, a large proportion of the movement during passive stretch is taken up by the tendon. We have expanded these observations and those of others who have demonstrated a lower passive torque–angle relationship following stretching (Wilson et al. 1992; Halbertsma et al. 1996), by showing that the decrease in MTU stiffness following repeated stretches, such as those used by athletes during warm-up, is not due to a change in the tendon but rather to an increased compliance of the proximal, muscular, portion of the MTU. This increased compliance of the muscle is not, however, fully explained by a change in the extensibility of the muscle fascicles and we propose that connective tissue elements within the muscle change their elastic properties when subject to repeated stretches.
Stretch such as used during a warm-up is known to cause an acute increase in ROM which may in part be due to an increase in the subjects' tolerance of stretch (Magnusson et al. 2000) and also a decrease in the stiffness of the whole MTU, changing the passive torque–angle relationship of the hamstrings and gastrocnemius (Wilson et al. 1992; Evetovich et al. 2003). The changes we report in passive torque as a result of the conditioning stretches are very similar to these previous observations. However, the MTU is a complex structure consisting of tendon, muscle fibres and connective tissue and it is of interest to see how the different components respond following conditioning by repeated stretches. Ultrasound techniques allow measurements to be made of changes in fascicle length from which Herbert et al. (2002) made inferences about changes in tendon length. Here we have expanded these observations to include measurements of the displacement of the MTJ which allows a more direct estimation of changes in length of the tendon and other structures both before and after conditioning.
The movement of the MTJ of little more than a centimetre during the standard stretches is relatively small. To obtain an estimate of changes in tendon length the displacement of the MTJ has to be subtracted from the change in length of the whole MTU which in turn is estimated from the change in angle at the ankle joint. It is important therefore to assess the possibility of systematic errors in the measurements we have made. Observing markers placed on the skin it was found that there was a distal movement of the skin as the MTU was stretched, leading to a probable under-estimation of the displacement of MTJ and consequent over-estimation of the elongation of the tendon. The measurements were made pre-conditioning over four repeated stretches, but we have no reason to think that the movement of the skin would be any different after the five conditioning stretches. These observations were made in only one subject and so a correction has not been applied to the data presented here. However, the subject was typical in every respect so we assume that all MTJ movements may have been under-estimated by about 15%. This systematic error makes little or no difference to the conclusions related to our first and second objectives. Thus, we can confirm that during a standard passive stretch to 25 deg a substantial component of the MTU extension is taken up by the muscle and it makes very little difference whether this constitutes 46% or, after correction, 53% of the total movement. Likewise it does not affect our conclusions regarding the role of thixotropy (see below). In respect of the changes occurring as a result of the conditioning stretches, the error does not affect the qualitative observation that it is the muscle and not the tendon that is most affected. However, when it comes to quantitative assessments of the contribution of changes in fascicle length to the changes in stiffness of the distal, muscular, portion of the MTU it then becomes necessary to take into account the possible measurement errors.
The extension of the muscle fascicles during a standard stretch was slightly less than that of the MTJ (Table 1) and so accounted for a little less than 50% of the total MTU extension prior to conditioning stretches. This is considerably more than the 27% reported by Herbert et al. (2002) but is similar to values of 43–46% reported in the GM muscle by others (Kawakami et al. 1998; Maganaris, 2003). The most likely explanation is that in the study of Herbert et al. (2002) the subjects were tested with a flexed knee which would have shortened the gastrocnemius introducing some slack into the system which would be taken up before any extension of the fascicles occurred. In our experiments the knee was always fully extended. Nevertheless, the qualitative observation of the importance of tendon extensibility during passive movement is the same.
Our main concern was what would happen to the muscle when conditioned by repeated passive stretches, a type of warm-up that results in greater flexibility (ROM) and reduced overall MTU stiffness. Resting muscle fibres have thixotropic properties (Hill, 1968) and it is well known that muscle stiffness of this nature can be reduced by relatively small amounts of movement (Campbell & Lakie, 1998). Consequently we subjected the muscle to a number of quick stretches that would be expected to abolish the short range elastic component, or possibly change the conformation of titin, but this had no effect on the overall stiffness of the MTU (Fig. 5) or movement of the MTJ. We conclude that reducing the contribution of short-range elastic component of the muscle fibres is unlikely to be the mechanism leading to increased flexibility as a result of static stretching.
In contrast to the pre-conditioning state where the increase in total MTU length during a standard stretch was taken up almost equally between muscle and tendon, the proportion of the increase in MTU length due to changes in muscle length post-conditioning was increased while there was a decreased contribution from tendon elongation. It is tempting to calculate the stiffness of the various components of the MTU from data such as those illustrated in Fig. 4. The problem, however, is that the measured torque probably contains an appreciable component derived from frictional forces within the joint capsule making it impossible to know the actual torque experienced by the tendon and muscle and it is possible that compressing the ankle joint during the conditioning stretches may have altered its properties. Nevertheless, if it is assumed that the proportion of the measured torque contributed by the different elements remains the same pre- and post-conditioning then it is evident that the effect of the conditioning is to reduce the stiffness of the muscle by about half while the tendon shows no significant change following the conditioning stretches. Our conclusions contradict those of a number of authors who suggest that stretching primarily affects the stiffness of tendons (Wilson et al. 1992; Witvrouw et al. 2004). However, these latter observations were based on the reduction in the joint angle–torque relationships from which no direct conclusions could be made regarding the contribution of different components of the muscle–tendon unit.
Whilst the additional movement that occurred following the conditioning stretches was localized to the muscle it was surprising that this was not reflected in a change in the extension of the muscle fascicles during the standard stretch (Fig. 6; Table 2). In trying to account for changes in MTJ in terms of fascicle length it is necessary to take into account the angle of pennation with the relevant measurement being the fascicle length resolved along the axis of the MTU. Table 3 shows the change in the resolved length of the fascicles and these have been compared with the change in MTJ after it has been adjusted for the likely error arising from movement of the ultrasound markers on the skin. The effect of conditioning was to increase the angle of pennation with the ankle at 0 deg and the change in pennation angle during stretch to 25 deg was somewhat greater than in the initial pre-conditioning state. Pre-conditioning, the change in MTJ and resolved fascicle length were virtually identical while post-conditioning the movement of the MTJ was 0.19 cm greater than the change in resolved fascicle length. This suggests that the additional extension of the components of the MTU proximal to the MTJ was, at least in part, the result of changes in structures other than the muscle fibres. Muscle fibres are surrounded by a complex connective tissue network to which they are attached along the length of the fibre and not only at the ends. This connective tissue, particularly the perimysium, is considered to be a major extracellular contributor to passive stiffness (Purslow, 1989). Likewise, Gajdosik (2001) suggested that lengthening deformation of the connective tissues within the muscle belly (endomysium, perimysium and epimysium) could influence passive stiffness.
The increased ROM and flexibility resulting from the decreased stiffness of the muscle following conditioning stretches would clearly be beneficial to athletes competing in events where flexibility is essential. There is, however, evidence suggesting that static stretching could reduce muscle force and power output, with detrimental consequences to sporting performance (Gleim & McHugh, 1997). In the present investigation fascicle length was unchanged by stretching, which was probably the result of an increase in the aponeurosis compliance. More compliant connective tissue may reduce the sensitivity of muscle spindles (Avela et al. 1999), possibly reducing the speed of muscle activation and this may account for the reported reductions in power output during sprinting after stretching exercise (Nelson et al. 2005). Consequently in events such as gymnastics, high jumping and hurdling where both flexibility and high power are required, there may be a trade-off between the two effects of stretching during warm-up. However, as discussed by Magnusson et al. (2000) the time course of the in vivo physiological adaptations associated with static stretching remains unresolved.
The results presented here provide information about the behaviour of three components of the muscle–tendon complex when it is stretched and how these are affected by a series of conditioning stretches such as are commonly used during athletic warm-up. The conclusions are that pre-conditioning the MTU extension is taken up in nearly equal parts by the tendon and muscle fascicles but, post-conditioning, the anatomical muscle becomes less stiff and accounts for the decrease in overall stiffness of the MTU and the increased ROM. There are suggestions from our results that the changes within the muscle may be due, in part, to altered properties of connective tissue elements. The nature of these elements and how they are affected by conditioning stretches is largely unknown and clearly a topic of considerable future interest.