European Journal of Applied Physiology

, Volume 99, Issue 4, pp 449–454

A stretching program increases the dynamic passive length and passive resistive properties of the calf muscle-tendon unit of unconditioned younger women

Authors

    • Clinical Kinesiology Research Laboratory, The School of Physical Therapy and Rehabilitation ScienceThe University of Montana
  • Jennifer D. Allred
    • Clinical Kinesiology Research Laboratory, The School of Physical Therapy and Rehabilitation ScienceThe University of Montana
  • Holly L. Gabbert
    • Clinical Kinesiology Research Laboratory, The School of Physical Therapy and Rehabilitation ScienceThe University of Montana
  • Beth A. Sonsteng
    • Clinical Kinesiology Research Laboratory, The School of Physical Therapy and Rehabilitation ScienceThe University of Montana
Short Communication

DOI: 10.1007/s00421-006-0366-7

Cite this article as:
Gajdosik, R.L., Allred, J.D., Gabbert, H.L. et al. Eur J Appl Physiol (2007) 99: 449. doi:10.1007/s00421-006-0366-7

Abstract

This study examined the effects of a 6-week stretching program on the dynamic passive elastic properties of the calf muscle-tendon unit (MTU) of unconditioned younger women. After random assignment of 12 women (age 18–31 years) to a stretching group (SG) or to a control group (CG), six subjects in the SG and four subjects in the CG completed the study. For the initial tests, a Kin-Com®dynamometer moved the ankle from plantarflexion to maximal dorsiflexion (DF) with negligible surface EMG activity in the soleus, gastrocnemius and tibialis anterior muscles. Angular displacement, passive resistive torque, area under the curve (passive elastic energy) and stiffness variables were reduced from the passive DF torque curves. The SG then completed ten static wall stretches held 15 s each, five times a week for 6 weeks, the CG did not. The tests were repeated and the changes between the tests and retests were examined for group differences (Mann–Whitney U). The SG had significant increases in the maximal passive DF angle (7° ± 4°), maximal passive DF torque (11.2 ± 8.3 N m), full stretch range of motion (23° ± 24°), full stretch mean torque (3.4 ± 2.1 N m), and area under the full stretch curve (22.7 ± 23.5° N m) compared to the CG (P ≤ 0.019). The passive stiffness did not change significantly. The results showed that a stretching program for unconditioned calf MTUs increased the maximal DF angle and length extensibility, as well as the passive resistive properties throughout the full stretch range of motion. The adaptations within the calf MTU provide evidence that stretching enhances the dynamic passive length and passive resistive properties in unconditioned younger women.

Keywords

Calf muscle-tendon unitDynamic passive elastic propertiesStretchingWomen

Introduction

The calf muscle-tendon unit (MTU) plays an important role in the effectiveness and efficiency of walking and running, and calf MTU stretching programs are used routinely to increase dorsiflexion (DF) range of motion (ROM). Although stretching programs are common, little is known about how stretching programs influence the dynamic passive elastic properties of the calf MTU. Studies with animal models have indicated that the soleus muscles of endurance-trained rats adapt with increased tensile strength and stiffness compared to controls (Kovanen and Suominen 1988; Kovanen et al. 1984). Kovanen et al. (1984) reported that the endurance-trained muscles had greater concentrations of connective tissues and possibly increased collagen fiber cross-linking, which would contribute to greater resistance to passive stretch. In another study, eccentric training, which includes stretching, resulted in greater active and passive stiffness of rat muscles, explained primarily by adaptive changes in the sarcomeric cytoskeletal protein titin (Reich et al. 2000) and not by adaptations in the connective tissues. Changes in the protein titin, that anchors the myosin filament to the Z-disc and serves as an adaptable molecular spring (Lindstedt et al. 2002; Prado et al. 2005) were implicated because the increased stiffness resulted from increased passive resistance throughout the full passive length extensibility. In contrast, the connective tissues of the MTU are thought to offer their greatest passive resistance near the maximal stretch length (Lindstedt et al. 2001; Reich et al. 2000).

One recent study showed that the calf MTUs of long distance runners have greater passive resistive torque when compared to untrained men after controlling for body mass (Gajdosik and Riggin 2005). Although speculative, the increased passive resistive properties may have been influenced by exercise adaptations in the connective tissues and in the cytoskeletal protein titin as a result of eccentric training and therapeutic stretching (Gajdosik and Riggin 2005). A study with untrained older women (age 65–89 years), indicated that an 8-week stretching program for the calf MTUs increased the passive resistive properties through the full stretch ROM (Gajdosik et al 2005b). At the start of the study none of the women was in an exercise program designed to lengthen or strengthen the calf MTU, so the adaptive response may have resulted from stretching unconditioned calf MTUs and not necessarily because the women were older. Moreover, the stretching exercises completed by the older women may have included some low level muscle activation, which would simulate a low level eccentric activation, as some older people have difficulty relaxing sufficiently to achieve a completely passive stretch (Gajdosik 2006). Taken together, the studies cited above suggest that greater passive resistive properties are associated with endurance training and eccentrically conditioned muscles, and that a stretching program, which could include very low level of eccentric activations, may increase the passive resistive properties of unconditioned MTUs. Accordingly, the purpose of this study was to examine the influence of a stretching program on the dynamic passive elastic properties of the calf MTU of younger women who were not engaged in an exercise program and who were considered unconditioned. The women represented the physical condition of people before starting an exercise program or during a rehabilitation program in which impaired de-conditioned calf MTUs may develop secondary to injury or disease. Women were selected because studies have suggested that men and women may respond differently to therapeutic stretching (Gajdosik et al. 2006).

Methods

Subjects

Twelve unconditioned women (age 18–31 years) not participating in an exercise program volunteered for this study. After randomly assigning the women to either a stretching group (SG) or to a control group (CG), six subjects in the SG and four subjects in the CG completed the study. The age, height, and mass of the women in the SG (n = 6) were 23 years (SD 4 years, 18–31 years), 165 cm (SD 8 cm, 158–176 cm), and 67 kg (SD 10 kg, 54–78 kg), respectively. The age, height, and mass for the women in the CG (n = 4) were 21 years (SD 1 year, 20–23 years), 169 cm (SD 4 cm, 163–172 cm), and 70 kg (SD 18 kg, 52–95 kg), respectively. The women were minimally active as determined by self-report of habitual activities (Gajdosik et al. 2005b), they did not participate in a stretching or strengthening calf MTU exercise program and they were free of neurological or orthopedic disorders that could confound the results. The study was approved by the Institutional Review Board for the Use of Human Subjects in Research at the University of Montana.

Instrumentation

A Kin-Com® isokinetic dynamometer (KINETIC COMMUNICATOR II 500H, Software Version 4.03, Chattecx Corp., Chattanooga, TN, 37405, USA) and ankle–foot apparatus were used to stretch the calf MTU by moving the ankle from plantar flexion (PF) into DF at 5° s−1 (0.087 rad s−1) and back into PF at 5° s−1. A 90° angle between the foot and the leg was defined as 0°, DF degrees were positive and PF degrees were negative. The lever arm was held constant at 20 cm to express the passive resistance in torque (N m).

Surface electromyography (SEMG) (GCS 67, Therapeutics Unlimited, 2835 Friendship St, Iowa City, IA, 52245, USA) was used to monitor the activity of the soleus, the medial head of the gastrocnemius and the tibialis anterior muscles during the tests. The specifications of the EMG system, the electrodes, skin preparation and electrode placements were in accordance with the SENIAM guidelines (Hermens et al. 2000) and reported in detail previously (Gajdosik et al. 2005a). The angle (°), velocity (°s−1) and torque (N m) signals from the Kin-Com® (sampled at 500 Hz) were simultaneously synchronized with the SEMG tracings from the three leg muscles. The root mean square (RMS) of the SEMG signal was expressed as a percentage of maximal isometric voluntary contraction (MVC) SEMG of the three leg muscles to ensure that the stretches were passive, operationally defined as <5% of the MVC SEMG.

Procedures and measurements

The testing procedures and measurements were in accordance with previous established methods (Gajdosik et al. 2005a). The subjects first assumed a supine position on an examination table, the axis of the right ankle was estimated and the leg was marked for proper positioning. The subjects then completed a pre-testing calf-muscle-stretching exercise of ten static wall stretches held for 15 s each. To stretch the right calf MTU while standing, the left foot was placed on the floor in front of the body with the knee slightly bent, and the right foot was placed behind the body. The women kept the right knee straight and the heel on the floor. They then stretched the right calf MTU by bending the left knee and moving the right ankle into DF until they felt a maximal stretch, as tolerated. After stretching, the SEMG electrodes were attached over the appropriate muscle bellies, and the subjects assumed a supine, relaxed position on the Kin-Com® table to test the right calf MTU with the knee extended. After repeated manual passive stretch trials to encourage relaxation, the maximal DF angle was identified just prior to pain or increased SEMG activity from the calf muscles. The ankle–foot apparatus was then placed at 45° of PF and using the Kin-Com® motor, the ankle was stretched passively to the maximal DF angle and immediately returned back into PF. Three stretch and return trials were performed at 5° s−1. After the passive tests, the subjects completed three PF MVCs to record the maximal SEMG activity of the two calf muscles and three trials of DF MVCs to record the maximal SEMG activity of the TA muscle.

Group assignments

After the initial test session, the women were randomly assigned to the SC or to the CG. The SG stretched the calf MTUs bilaterally using the same pre-testing stretching exercise, which was ten static wall stretches held for 15 s each. This typical calf MTU stretching exercise was completed five times each week for 6 weeks for a total of 30 exercise sessions. The subjects were contacted routinely and monitored closely throughout the 6 weeks to encourage exercise compliance. The women in the control group did not stretch, but they were contacted throughout the period to ensure their enthusiasm for the project. After the 6-week intervention period, the subjects were retested as in the original tests. One researcher (RLG) identified the maximal angle of the passive DF stretch and remained blinded to subject group assignment.

Statistics

The three passive stretch trials from the tests and the retests were averaged and the mean, standard deviation, and range were tabulated for the maximal DF angle, which represented the maximal MTU length, and for the maximal passive DF torque. An initial DF angle was identified at the angle of initial passive resistive torque, and the difference between the initial DF angle and the maximal DF angle defined the full stretch ROM, which represented the length extensibility. The mean passive torque was measured through this full stretch ROM. Because the full stretch curves were non-linear, a third order polynomial function was fitted to the passive curves (mean coefficient of determination of R2 = 0.998), and the fitted curves were used to calculate the area under the full stretch curve (absorbed passive elastic energy) and the average passive elastic stiffness as the slope (ΔN m/Δ°). The passive curves were linear through the latter part of the rise in the curve, so a linear regression line of best fit through the last 10° of the DF stretch was used to determine the passive elastic stiffness as the slope in this part of the curve (Gajdosik and Riggin 2005). See Fig. 1 for a representative example of the passive torque curve and the variables reduced from the torque and angle data. A Mann–Whitney U Test was used to examine if changes between the tests and retests differed between the groups. The statistical significance was set at P ≤0.05.
https://static-content.springer.com/image/art%3A10.1007%2Fs00421-006-0366-7/MediaObjects/421_2006_366_Fig1_HTML.gif
Fig. 1

Representative example of the passive dorsiflexion (DF) stretch curve showing the maximal DF angle, maximal DF torque, length extensibility (full stretch range of motion), absorbed passive elastic energy (area under the curve), A mean torque through full stretch, B passive elastic stiffness as the curvilinear slope through the full stretch, and C passive elastic stiffness as the linear slope through the last 10° of stretch

Results

The mean RMS SEMG activity during the dynamic stretches was <1% of that recorded during the MVCs for all three muscles for both groups, which ensured that the stretches were passive as operationally defined. The full stretch passive curves for the tests and the retests for the SG and CG are depicted in Fig. 2a and b, respectively. The maximal DF angle, maximal passive DF torque, full stretch ROM and full stretch mean torque increased significantly for the SG compared to the CG (P ≤ 0.019) (Table 1). The area under the full stretch curve also increased for the SG compared to the CG (P = 0.011), but the change in the full stretch passive elastic stiffness and the passive elastic stiffness for the last 10° of the stretch ROM did not differ between groups (Table 2).
https://static-content.springer.com/image/art%3A10.1007%2Fs00421-006-0366-7/MediaObjects/421_2006_366_Fig2_HTML.gif
Fig. 2

Passive stretch curves for the tests and for the retests after the 6-week stretching program for a stretching group (n = 6), and b control group (n = 4). The curves for the stretching group showed and increase in the maximal DF angle, maximal passive DF torque, length extensibility (full stretch range of motion), full stretch mean torque, and the absorbed passive elastic energy (area under the full stretch curves) (P ≤ 0.019)

Table 1

Mean (±SD) and range for the maximal dorsiflexion (DF) angle, maximal DF torque, full stretch range of motion (ROM) and full stretch mean torque for the stretching group (n = 6) and the control group (n = 4)

Measurements

Mean ± SD and range

P value

 Maximal DF angle (°)

  Stretching group

 0.017

   Test

21.3 ± 6.6, 9–28

   Retest

28.7 ± 9.2, 14–40

   Difference

7.4 ± 4.3, 2–13

  Control group

   Test

19.8 ± 10.7, 11–35

   Retest

20.3 ± 9.4, 11–33

   Difference

0.5 ± 1.9, −2–2

 Maximal DF torque (N m)

  Stretching group

 0.019

   Test

14.6 ± 5.0, 9–22

   Retest

25.8 ± 5.2, 19–33

   Difference

11.2 ± 8.3, 4–24

  Control group

   Test

18.4 ± 4.0, 16–24

   Retest

20.0 ± 4.8, 15–26

   Difference

1.6 ± 2.7, −1–5

   Full stretch ROM (°)

  Stretching group

 0.014

   Test

44.2 ± 13.4, 28–65

   Retest

66.8 ± 15.0, 46–81

   Difference

22.6 ± 23.5, 1–53

  Control group

   Test

56.0 ± 16.4, 41–79

   Retest

54.8 ± 15.1, 39–75

   Difference

−1.2 ± 2.2, −4–1

   Full stretch mean torque (N m)

  Stretching group

 0.011

   Test

4.6 ± 1.1, 3–6

   Retest

8.0 ± 1.2, 7–10

   Difference

3.4 ± 2.1, 2–7

  Control group

   Test

5.9 ± 1.3, 4–8

   Retest

6.1 ± 1.3, 5–8

   Difference

0.2 ± 0.8, −1–1

The differences between the tests and the retests after the 6-week stretching program were significantly greater for the Stretching Group (P ≤ 0.019)

Table 2

Mean (±SD) and range for the absorbed passive elastic energy (area under the full stretch curve), the full stretch passive elastic stiffness, and the passive elastic stiffness in the last 10° of the stretch for the stretching group (n = 6) and the control group (n = 4)

Measurements

Mean ± SD

Range

P value

 Area under passive curve (°N m)

  Stretching group

P = 0.011

   Test

215 ± 108

85–386

   Retest

534 ± 180

334–765

   Difference

318 ± 251

92–680

  Control group

   Test

338 ± 171

210–589

   Retest

338 ± 157

244–572

   Difference

−0.5 ± 41

−38–57

Full stretch passive elastic stiffness (N m deg−1)

  Stretching group

P = 0.831 (NS)

   Test

0.29 ± 0.18

0.11–0.58

   Retest

0.35 ± 0.12

0.23–0.57

   Difference

0.06 ± 0.10

−0.03–0.20

  Control group

   Test

0.37 ± 0.12

0.25–0.49

   Retest

0.38 ± 0.10

0.26–0.47

   Difference

0.01 ± 0.04

−0.02–0.06

Last 10° passive elastic stiffness (N m deg−1)

  Stretching group

P= 0.136 (NS)

   Test

0.65 ± 0.17

0.44–0.88

   Retest

0.87 ± 0.08

0.72–0.97

   Difference

0.22 ± 0.15

0.00–0.44

  Control group

   Test

0.71 ± 0.08

0.62–0.81

   Retest

0.81 ± 0.15

0.66–1.01

   Difference

0.10 ± 0.10

−0.03–0.20

The difference for the area under the curve between the tests and the retests was significantly greater for the stretching group (P = 0.011), but the passive elastic stiffness measurements did not change significantly

Discussion

The length and passive resistive torque properties for the SG showed significant adaptations in response to the stretching program. The increased maximal DF angle and the increased maximal passive resistive torque indicated that the stretching program increased the maximal calf MTU length and their ability to withstand a maximal passive load. These adaptations are in line with the results of the recent study with unconditioned older women that reported an increased DF angle and greater maximal passive DF torque after stretching three times a week for 8 weeks (Gajdosik et al. 2005b). The increased mean passive resistive torque through the full ROM appeared to shift the initial angle of the full passive stretch curves to the left, which contributed to the greater full stretch ROM, or greater length extensibility of the calf MTU.

The 6-week program of stretching unconditioned calf MTUs to their maximal tolerated length apparently stimulated passive resistive force adaptations throughout the full-length extensibility of the MTU, similar to what was reported previously for the older women (Gajdosik et al. 2005b). Although speculative, the passive adaptations may have been influenced by remodeling of the connective tissues of the muscle belly (endomysium, perimysium, epimysium) and tendon. Studies with immobilized animal muscles have shown that the connective tissues of skeletal muscles readily adapt to changes in muscle lengths by changes in their amount (Tabary et al. 1972) and organization (Williams and Goldspink 1984). Thus, the stretching program could have stimulated changes in these connective tissues in relation to the increased muscle lengths, which would enhance the muscles’ ability to withstand a greater passive resistive torque, especially near their maximal tolerated stretch lengths (Lindstedt et al. 2001; Reich et al. 2000). The passive adaptations also may have been influenced by adaptations in the noncontractile proteins of the sarcomeric cytoskeleton, particularly the protein titin. Reports have suggested that adaptable titin isoforms are specific for slow twitch and fast twitch dominated muscles (Prado et al. 2005), titin isoforms are species-specific related to function (Lindstedt et al. 2002) and that eccentric endurance exercise, which includes muscle stretching, may promote the formation of different titin isoforms that serve as adaptable molecular springs within the muscle tissue (Lindstedt et al. 2001; Reich et al. 2000). The muscles of rats that underwent chronic eccentric training for 8 weeks on a motorized treadmill had increased passive resistive forces through the full passive stretch curve (Reich et al. 2000), very similar to the results of the current study. Thus, the calf MTU stretching program may have stimulated increased passive resistive adaptations in the unconditioned muscle tissue directly, and not only in the connective tissues. The adaptations also may have been influenced by very low level eccentric activation during the stretch, as the stretching exercises may not have been completely passive. Additional research is needed to examine the mechanisms underlying the adaptive passive elastic properties in unconditioned muscles, but it seems plausible that adaptations in the connective tissues and in the titin protein could both account for the increased passive elastic resistive properties that we measured.

Our results indicated that passive elastic stiffness as an important property might be overstated. Although there appeared to be a trend for increased passive elastic stiffness in the SG (see Table 2), the change was not significantly greater than for the CG, perhaps influenced by the small sample size. The increased passive resistive torque, however, was also apparently offset by the increased muscle length, which resulted in no significant change in the slopes of the curves. The significant changes in the MTUs’ length and passive resistive torque were best appreciated by the increased absorbed passive elastic energy as represented by the area under the curve (°N m), because the areas were calculated based on changes in the length (°) and the passive resistive torque (N m). From a perspective of function, the significant increase in the absorbed passive elastic energy from a stretching program may be important, as this increase could enhance the passive elastic recoil of the muscles and increase the effectiveness and efficiency of ambulatory activities (Gajdosik et al. 2005b).

Conclusions

A 6-week static stretching program for the calf MTU of unconditioned younger women increased the maximal DF angle (maximal length), maximal DF passive resistive torque, full stretch ROM (length extensibility), the full stretch mean passive torque, and area under the full stretch curve (absorbed passive elastic energy). The full stretch passive elastic stiffness and the passive elastic stiffness in the last 10° of the stretch did not change significantly. The length and passive resistive adaptations indicated that the unconditioned calf MTUs showed a remarkable ability to respond to a stretching program by increasing physical stress tolerance, perhaps influenced by changes in the connective tissues and the non-contractile protein titin of the sarcomeric cytoskeleton.

Aknowledgments

This study was funded by The Clinical Kinesiology Student Research Fund and by grants from The MJ Murdock Charitable Trust Foundation and The University of Montana (USA).

The experiments in this study complied with the current laws of the United States of America.

Copyright information

© Springer-Verlag 2006