Influence of different stretching rates on the viscoelastic behaviour of the relaxed human hamstrings

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1 Prof. Dr. Klaus Wiemann, Dr. Andreas Klee, Robert Raser Bergische Universität Gesamthochschule Wuppertal, 1998 Lit: Bundesinstitut für Sportwissenschaft, Köln: Sportwissenschaftliche Forschungsprojekte, Erhebung 1998, Proj. Nr.: DE D 6129 Influence of different stretching rates on the viscoelastic behaviour of the relaxed human hamstrings Abstract The purpose of the study was to investigate the viscoelastic responses of the human hamstrings on different stretching rates. In 12 male subjects lying on the left side, the right leg knee extension test was performed by stretching the absolutely relaxed hamstrings (EMG control) up to a submaximal extent (dynamic period, DP), and by holding this position for 10 s (static period, SP). In the DP of the stretch procedures, 2 different stretching rates were used, 6 /s (slow stretch, SS) and 60 /s (rapid stretch, SR). The subjects had to undergo 4 stretch procedures (SS SR SS SR or SR SS SR SS, respectively). The passive muscle resistance torque was recorded during DP and SP. In general, the passive stretching tension of SP after SS was significantly higher than after SR. Especially, the passive stretch tension after that SS procedures performed at the beginning of the sequence was significantly higher than after the remaining procedures. We suppose that the rapid stretch procedure decreased the passive stretch tension by a thixotropic response of the muscle s tissue and that the decrease continued in the remaining procedures. This observation may be important in planing therapeutic methods and exercises in sports.

2 Introduction The mechanical behaviour of the passive muscle-tendon unit in stretching has been characterized as viscoelastic, and has been compared with the mechanical behaviour of a shock absorber or a dash pot (22), respectively. Viscoelastic behaviour as a response to deformation combines an elastic component with a viscous component (Fig. 1). In respect to the elastic component, the deformation is load dependent, i.e. the amount of deformation increases with the amount of force (4, 5, 24). Transferred to stretched muscle-tendon units, the amount of muscle lengthening increases with the stretching force. This behaviour of stretched muscles has been corroborated by numerous investigations, in vitro (e.g. 2, 8, 23, 25, 26), as well as in vivo (e.g. 7, 10, 14, 16, 20, 29, 31). In respect to the viscous properties of viscoelastic material, it must be expected (Fig. 1) that the resistance of the material against the deformation increases with increasing deformation rate (4, 5, 24). Therefore, it should be suspected that a high stretching rate generates a higher passive resistance of the stretched muscle than a low stretching rate. This resistive torque-velocity relationship of muscles has been demonstrated in vitro (1, 23, 27) as well as in vivo (16). Fig. 1 Hypothetical stress response of viscoelastic material (below) on two different deformation rates (above). e: Mainly elastic component of stress response. v: Mainly viscous component of stress response. If viscoelastic material will be deformed into a new position, and this new position will be held constant, the resistance against the deformation will decline over time. This viscoelastic stress relaxation has been characterized as having three components, an initial fast declining component, a subsequent slow declining component, and a final constant component. The fast and slow declining components must be ascribed to the viscous properties of the material, the constant component elucidates the elastic properties of the material (Fig. 1). The viscoelastic stress relaxation of stretched muscles has been demonstrated in vitro (23) as well as in vivo (3, 17, 18, 20, 21): A muscle stretched to a new constant length will show a decrease of stretching tension over time. However, it must be suspected that, in the static period after a rapid stretch, the declining amount of the passive muscle stretch tension will be higher than after a slow stretch (1) as Fig. 1 elucidates. The final constant component of the

3 stress relaxation must be expected as being identical after rapid stretch and slow stretch, respectively (23). It seems to be unknown if human muscles in vivo respond differently to different stretching rates when they are maintained at a fixed length after the stretch. Therefore, the purpose of the present study was to investigate the viscoelastic behaviour of relaxed human hamstrings in vivo during a static period immediately after stretches with different stretching rates. Materials and methods Mechanical set-up A table-like experimental station (Fig. 2) was constructed to measure the passive resistance of the relaxed hamstrings during a knee extension as knee flexion torque (Nm). Lying on the left side on the table board of the experimental station the subject s right hip joint was flexed up to 60 (extended hip joint = 180 ). The right knee joint flexed up to 60 (extended knee joint = 180 ) was positioned on a rotation disc (diameter = 0.6m). By shifting the rotation disc the axis of the knee joint could be aligned with the axis of the rotation disc. The subject s pelvis was strapped to a back-rest, the left thigh resting on the table board of the experimental station was strapped there, and the right shank was fixed to the rotation disc. By means of a traction wire, in which a load cell (DIGIMAX, Mechatronic) was integrated, the rotation disc could be manually rotated in the horizontal plane so that the knee joint was extended, and the hamstrings were stretched. The load cell picked up the rotation force (Nm) which was necessary to extend the knee joint and to hold the knee joint in the extended position. This rotation force can be defined as the resistance (= passive stretch tension) of the hamstrings against the stretch manoeuvre. The load cell was calibrated by using loads of 25 and 50 N. A calibration over a time span of 30 s was carried out to ensure that stress relaxation of the load cell did not occur. To quantify the angle of knee extension a goniometer (Dinopot HQ5) was fixed at the axis of the rotation disc and calibrated in a 60 and 180 angle. The measurement error of the goniometer received less than The measurement error of the load cell amounted to 0.02 Nm. In a parallel study involving 12 subjects quantification of the stretching tension produced a retest correlation coefficient of rtt = on condition that two knee extension procedures up to an knee joint angle of 115 were carried out within a 3 min interval. However, rtt attained on condition that the subject left the experimental station after the pretest and was replaced on it 5 min later to carry out the retest.

4 Fig. 2 Experimental station (simplified presentation). a: Axis of rotation. b1 - b4: Fastening belts. br: Back rest. et: Table board of the experimental station. lc: Load cell. rd: Rotation disc. tw. Traction wire. EMG recording Surface electrodes (sinter electrodes, pick-up area 6 mm, interelectrode distance 20 mm, ground electrode at the left shank) were attached to the subject s hamstrings muscle group and knee extensor muscle group to pick up their electrical activity. This was done to ensure that - during the stretch maneuver and the following static period - the stretch procedure was not restrained by involuntary activity of the hamstrings or supported by the knee extensors, respectively. Subjects Twelve male subjects (students of physical education or junior assistants) aged 22 to 31 volunteered to participate in the study. All subjects were free from any lower extremity pathology. Experimental protocol The subject was prepared for bipolar surface electromyography in the usual way. The electrodes were attached to the right leg midway between the gluteal fold and the distal end of the muscle belly of the hamstrings and to the right leg knee extensors one and a half handbreadth above the patella. The interelectrode resistance was tested to be less than 5000 ohm. Afterwards, the subject was placed on the experimental station and fixed as described above. When the subject was asked to relax his right leg muscles the knee joint automatically moved into a position of muscular balance between 60 and 70 and remained there. Starting from this position the knee joint was stretched up to a final position of a knee joint angle of 115 (= dynamic period, DP), held in this final position for a time span of 10 s (= static period, SP), and released to the starting position.

5 Two different stretching rates were chosen: i) rapid stretch (SR): the final position had to be achieved within a time span of s in a ballistic manner, i.e. a stretching rate of more than 60 /s in the middle of the DP, ii) slow stretch (SS): the knee joint had to be turned into the final position within a time span of 10 s by using a relatively constant moving rate, i.e. a stretching rate of nearly 6 /s. Two experimental groups were constituted, to which subjects were randomly assigned: i) group beginning with rapid stretch (rs-group), ii) group beginning with slow stretch (ss-group). The subjects had to undergo two slow stretches and two rapid stretches, by turns, with a rest of three minutes between the single stretch procedures. The sequences and the nomenclatures of the 4 stretch procedure modes per experimental group are illustrated in Table 1. Data analysis Passive hamstring torque and knee joint angle were continuously recorded from the beginning of the dynamic period up to the end of static period. The signals were A/D converted at 100 Hz and stored on a PC. After each stretch procedure, the EMG records were visually controlled on the monitor to ensure that EMG activity of both, the knee extensors and the knee flexors were not different from the basic noise (i.e. values of nearly mv). Otherwise, the stretch procedure was repeated. In the dynamic period of the stretch procedure, the torque picked up by the load cell was caused by the viscoelastic resistance of the stretched muscle as well as by the angular acceleration of the mass of both, the rotation disc and the subject s shank fixed on it, respectively. Since - in the dynamic period - the angular acceleration varied from test to test affected by the manually performed stretch procedure, only the tension torque picked up in the static period of the stretch procedure was used for data analysis: In each 1s lasting time span of the 10 s lasting static period, the mean torque was calculated and used for data analysis. Statistics Repeated measurement Anova followed by paired t-tests was used to examine whether the stretch tension torque varied from one 1s-time span of SP to another. One factor Anova (subgroup) for repeated measurement following by t-tests for dependent and independent samples was employed to examine the differences between the subgroups and between the stretch procedure modes. An alpha level of 0.05 was accepted as statistically significant.

6 Fig. 3 Typical record of the knee joint angle (above) and the stretch tension torque of the hamstrings (below) in the dynamic and static period of one subject's stretch procedures. Dotted line: Slow stretch. Solid line: Rapid stretch. Results Fig. 3 shows a typical response of one subject s hamstring stretch tension on a slow stretch and a rapid stretch procedure. Fig. 4 demonstrates the mean viscoelastic behaviour of the hamstrings (i.e. the history of the passive stretch tension) in the static period of the stretch procedure within the test groups and the subgroups. The descriptive statistics of the hamstrings stretch tension during the static period are summarised in Tab. 2. Fig 4 Stretch tension torque of the hamstrings during the passive period of the stretch manoeuvre. a) Comparison between slow stretch (SS) and rapid stretch (SR). b) Comparison between the experimental group beginning with slow stretch (ss) and the group beginning with rapid stretch (rs). c) Comparison between different stretching modes (Nomenclature see Table 1!). In the static period following slow stretch, the stretch tension decreased significantly from one 1s-time span to another (p < 0.01), beginning with the first 1s-time span (Fig. 4a, Table 2). In the static period following rapid stretch, the stretch tension decreased in the same way

7 (Fig. 4a). However, the difference between stretch tension of the first and the second 1s-time span did not attain a significant value (Table 2). Table 1: Experimental groups, treatment modes, sequences and nomenclature of the hamstring stretch procedures. rs: experimental group beginning with rapid stretch. ss: experimental group beginning with slow stretch. SR: rapid stretch procedure. SS: slow stretch procedure. Table 2: Mean torque of stretch tension (Nm) of the hamstrings in the first ten 1s-time spans of the static period after slow stretch (SS) and after rapid stretch (SR), and in the experimental groups (ss and rs, nomenclature see Table 1). Means ± SD. Difference to the following second: #: p < 0.05; ##: p < 0.01 (paired t-test) Difference between SS and SR: : p < 0.05; : p < 0.01 (paired t-test) Difference between ss and rs: &: p < 0.05 (t-test for independent samples) Paired t-tests following repeated measurement Anova showed a significant difference between static period stretch tension of the slow stretch group (SS) and the rapid stretch group (SR) (Fig. 4a, Table 2), in general, and, in particular, that the mean static stretch tension after the initially performed slow stretch (SS1) was significantly higher (19.04 Nm) than in the remaining groups (SS2: Nm, SR1: Nm, and SR2: Nm). A t-test for independent samples following one-factor Anova elucidated a significant difference between the experimental group beginning with rapid stretch (rs) und the experimental group

8 beginning with slow stretch (ss) (Fig. 4b, Table 2), and, in particular, that the stretch tension in sss was significantly higher than in rss, ssr, and rsr, respectively (Fig. 4c). Finally, the sss1 stretch manoeuvre produced a significantly higher static stretch tension during the static period than the other seven stretch manoeuvres (Fig. 5). Fig. 5 Mean passive tension torque of the 8 different hamstring testing modes within the 10s lasting static period (Nomenclature see Table 1!). Differences to sss1: : p < 0.05 (paired t test, 2 tail Sig.) (&): p < 0.1 (t test for independent samples, 1 tail Sig.) &: p < 0.05 (t test for independent samples, 1 tail Sig.) Discussion Experimental procedure Usually, hamstring stretch tests are carried out in sitting subjects (knee extension test; 17-21) or in subjects lying in supine position (straight leg raising test; 7, 22, 31), respectively. In those tests, the straight leg or the shank, respectively, are elevated from a lower position to a higher located final position and fixed in the final position for a certain time to examine the passive stretch relaxation of the hamstrings. In this final position, the decrease of the picked up tension torque will not only be influenced by the viscoelastic properties of the stretched hamstrings but also by the gravitational force which leads to a displacement of tissue and body fluid to an unknown proportion. Therefore in the present study, we decided to test the subjects lying on the left side and to perform the stretch procedure in the horizontal plane - like Gajdosik (6) - in order to eliminate the displacing influence of gravity. In former investigations, the stretch procedure had been carried out manually (22). Recently, commercial instruments (e.g. isokinetic dynamometers) were used, to perform the stretch manoeuvre by means of a servo motor (17-21). In studies using these motor driven

9 instruments, the angular rate of the stretch procedure had been held quite low (approx. 5 /s). In the course of human ballistic movements in sports and exercises( e.g. sprinting and throwing), however, angular velocities can be observed which are higher than 100 /s. These high angular velocities bring about high stretching rates for the antagonistic muscles. If the rapidly stretched muscles responded like viscoelastic material, in the stretching period as well as in a following period of holding the stretched position, a high stretch tension torque would have to be expected (see Fig. 1), which would restrain the ballistic movements. Therefore, we have decided to compare the viscoelastic behaviour of slowly stretched and rapidly stretched hamstrings. Rapid hamstring stretches, however, can be performed more effectively in knee extension tests than in straight leg raising tests. Therefore, we preferred the knee extension test. In experiments using isokinetic dynamometers, stretches are usually performed in a ramp like manner (Fig. 1). In human movements, however, rapid muscle stretches occur in a ballistic way. Therefore, we preferred manually performed stretches to simulate the physiological properties as closely as possible. In recent stress relaxation studies, final stretched position periods of s have been used. However, skilled ballistic movements in sports and exercises do not contain static periods of such enlarged duration. Therefore, we confined with a static period of 10 s which seems to be sufficient to answer the present questions. Passive static stretch tension If the muscle-tendon unit is classified as viscoelastic material, a decrease of stretch tension must be expected during the static period after a stretch procedure. The course of the decreasing period should show an initial fast component (i.e. high relative decrease), a subsequent slow component (i.e. small relative decrease) and a final stable component (see Fig. 1). In the present study, this viscoelastic behaviour with fast, slow, and stable components could not be observed during the 10s lasting static period. Obviously, in the present study, the static period has been too short for discriminating these components. Especially, the findings of several investigators (17, 20-22, 27) suggest that the shift from the fast component to the slow component will become observable still after s of the static period, and the stable component will even establish after s. Nevertheless, a viscoelastic stress relaxation during the static period could be demonstrated by the present investigations. Because the subjects were lying on one side and the stretch procedure was carried out in the horizontal plane, the observed tension torque decline could not be caused by gravitationally conditioned displacements of tissue and body fluid. Instead, the decline of the tension torque was probably due to changes in viscous elements of the muscle-tendon unit. Viscoelastic material is expected to generate a higher tension in the static period after a rapid deformation than in the static period after a slow deformation (Fig. 1). In respect to the

10 muscle-tendon unit, a higher initial stretch tension must be expected in the static period after rapid stretch than after slow stretch. Subsequently, an approximation of the stretch tension after rapid stretch and slow stretch by a faster decline of the stretch tension after rapid stretch must be supposed. Just after a certain time span, the final stable stretch tension after rapid stretch and slow stretch will attain an identical value (Fig. 1). In the present investigation, the supposed high initial stretch tension could not be detected. In contrast to the assumption, the stretch tension in the static period after rapid stretch was significantly lower than in static period after slow stretch. This result was in contrast to the theoretically calculated behaviour of viscoelastic material as well as in contrast to findings of Bagni et al. (1), Mutungi and Ranatunga (23) and Taylor et al. (27), which investigated animal models in vitro. Additionally, Lamontagne et al. (16) found a higher passive resistive torque associated with a higher stretching velocity of human plantar flexor muscles. We suppose the sources of our findings to lie in the dynamic period of the stretch procedure. However, the nature of these sources remain unclear, because no mechanical properties could be detected which might be responsible for the reduced viscoelastic resistance at the end of the dynamic phase of rapid stretch or at the beginning of the static phase after rapid stretch, respectively. Additionally, no neuronal sources could be seen. Since reflexive responses of both, the hamstrings and the knee extensor muscles, on the stretching procedure in slow stretch as well as in rapid stretch were excluded by a visual control of the EMG-records, stretch and tension reflex responses mediated over the group Ia, Ib and II receptors could by no means have led to changes in the picked up torque. Presumably, the existence of an intrinsic mechanism in human muscle has been responsible for the present results. Hagbarth et al. (9), Wiegner (30) and Lakie and Robson (15) reported about a change in the viscosity of muscle-tendon units: A passive disturbance of the muscle-tendon unit seemed to reduce the viscous resistance to stretch. An explanation for this so called thixotropic behaviour can be seen in a loosening of (thixotropic) molecular bonds (e.g. stable cross-bridges between actin and myosin) by passive disturbances like rapid stretching procedures. However, the presence of attached crossbridges in relaxed muscles has been discussed contrarily (1, 12, 13). It therefore appears that further sources of thixotropic behaviour must be taken into consideration, e.g. changes in the molecular conformation of diverse intra- and extrasarcomeric filaments (e.g. titin filaments, intermediate filaments et al.) presumably mediated by a rate triggered molekular switch. A corroboration of the hypotheses about the thixotropic sources of the observed reduced passive tension may be seen in the findings that slow stretch performed at first in the stretch procedure sequence (sss1) produced higher passive stretch tension than the remaining stretching modes (Fig. 5). Presumably, the rate of the first slow stretch was not intensive enough to initiate a thixotropic change of the molecular structures. Therefore, the passive tension during the static phase following sss1 was still quite high. Only after the first rapid stretches (rsr1, ssr1), the muscle-tendon unit presented the tension decrease - probably mediated by means of thixotropy - and retained this status for the following tests (rss1, sss2, ssr2, rss2, ssr2).

11 In conclusion, the low passive tension in rapidly stretched muscles seems physiologically valuable, because, in explosive ballistic movements, the thixotropic response of the rapidly stretched antagonistic muscle ensure that it will not generate a high stretch resistance restraining the intended movement rate. Furthermore, based upon the present findings, it must be supposed that initial rapid stretches may reduce the passive muscle tension more effectively than smooth or slow stretches. This assumption will be important in planning physiotherapeutic measures and warming-up methods in sports to lower muscle stiffness. However, the stretch conditions that tend to reduce the passive muscular tension are still unclear and need further investigations. References 1 Bagni, M.A., Cecchi, G., Colomo, F., Garzella, P.: Are weakly binding bridges present in resting intact muscle fibers? Biophys J 54: , Cavagna, G.A., Citterio, G.: Effect of stretching on the elastic characteristics and the contractile component of frog striated muscle. J Physiol 239: 1-14, Esteki, A., Mansour, J.M.: An experimental based nonlinear viscoelastic model of joint passiv moment. J Biomechanics 29: , Fung, Y.C.: A first course in continuum mechanics. Englewood Cliffs, Fung, Y.C.: Biomechanics. New York, Heidelberg, Berlin, Gajdosik, R.L.: Effects of static stretching on the maximal length and resistance to passive stretch of short hamstrings muscles. JOSPT 14, 6: , Göeken, L.N., Hof, L.: Instrumental straight-leg raising: Results in healthy subjects. Arch Phys Med Rehabil 74, 2: , Goldspink, G., Tabary, C., Tabary, J.C., Tardieu, C., Tardieu, G.: Effect of denervation on the adaptation of sarcomere number and muscle extensibility to the functional length of the muscle. J Physiol 236: , Hagbarth, K.E., Hägglund, J.V., Nordin, M., Wallin, E.U.: Thixotropic behaviour of human finger flexor muscles with accompanying changes in spindle and reflex responses to stretch. J Physiol 368: , Halar, E.M., Stolov, W.C., Venkatesh, B., Brozovich, F.V., Harley, J.D. : Gastrocnemius muscle belly and tendon length in stroke patients and able-bodied persons. Arch Phys Med Rehabil 59: , Heslinga, J.W., Huijing, P.A.: Effects of short length immobilization of medial gastrocnemius muscle of growing young adult rats. Eur J Morph 30, 4: , Hufschmidt, A., Schwaller, I.: Short-range elasticity and resting tension of relaxed human lower leg muscles. J Physiol 391: , Hutton, R.S.: Neuromuscular basis of stretching exercises. Komi, P.V. (Ed.): Strength and power in sport. Oxford: 29-38, 1993.

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