Skip Navigation LinksHome > November 2004 - Volume 36 - Issue 11 > Passive Force, Angle, and Stiffness Changes after Stretching...
Medicine & Science in Sports & Exercise:
Applied Sciences: Biodynamics

Passive Force, Angle, and Stiffness Changes after Stretching of Hamstring Muscles

REID, DUNCAN A.; MCNAIR, PETER J.

Free Access
Article Outline
Collapse Box

Author Information

Physical Rehabilitation Research Centre, School of Physiotherapy, Auckland University of Technology, Auckland, NEW ZEALAND

Address for correspondence: Duncan Reid, School of Physiotherapy, Auckland University of Technology, Private Bag 92006, Auckland, New Zealand; E-mail: duncan.reid@aut.ac.nz.

Submitted for publication December 2003.

Accepted for publication June 2004.

The New Zealand Society of Physiotherapists Scholarship Trust Fund provided financial assistance for this research.

Collapse Box

Abstract

Periodic or long-term stretching programs have demonstrated changes in joint range of motion. The suggested mechanisms for these increases in range of motion are changes in the tissue properties of the muscle and more recently stretch tolerance. However, few studies have examined changes in passive resistive forces and related these changes to increases in range of motion.

Purpose: The purpose of this study was to investigate the influence of a 6-wk hamstring-stretching program on knee extension range of motion, passive resistive forces, and muscle stiffness.

Methods: A randomized control trial with repeated measures was undertaken with 43 school-age subjects. Hamstring extensibility was assessed by a passive knee extension test using a Kincom® isokinetic dynamometer. The intervention group participated in a 6-wk hamstring-stretching program. Stretches were performed 5 d·wk−1, once per day, held for 30 s, and for 3 repetitions. The control group did not stretch over the 6-wk intervention period. Measurements of hamstring extensibility were repeated at the end of the 6-wk intervention.

Results: After the intervention period, significant (P < 0.05) increases in knee extension range of motion, passive resistive force, and stiffness were observed in the experimental group. No significant differences were observed in the control group’s findings for the same variables.

Conclusions: The findings of this study are consistent with other literature that shows periodic stretching programs over a 6-wk time frame produce significant changes in knee extension range of motion. The finding of increased stiffness in the new range of motion, gained as a result of the stretching program, provides some evidence that structural changes had occurred in the stretched muscles.

Stretching exercises have long been considered an essential part of preexercise warm-up procedures (23), a method of improving the efficiency of movement (7), improving muscle performance (22,28), altering posture (24), and reducing muscle strain and injury (11). The extensibility of soft tissues is related to the resistance of the tissue as it lengthens (18). During a static stretching procedure, one aim may be to overcome the passive resistance of the soft tissues and by doing so increase the range of motion in the joints. A number of studies have demonstrated that stretching muscle tissue can increase joint range of motion (1–4,15,20).

Few studies have examined changes in passive resistive forces associated with these increases in range of motion. Those that have (10,15) have noted that passive resistive forces increase after the training programs. Some researchers have interpreted this finding as a change in stretch tolerance as compared with a change in the structural components of the muscle (10,15). Stretch tolerance can be defined as the ability of a subject to tolerate an increase in the discomfort of the stretching procedure at the terminal range of motion. To better appreciate whether structural changes are occurring with changes in range of motion, an examination of muscle stiffness (the ratio of change in force to change in angle) is required. To date, no researchers have examined stiffness in the new range of motion after a stretching program. If muscle stiffness changed with increased range of motion, then this would provide evidence for changes in the muscle structure. Conversely, if no changes occurred, then increases in range of motion could be due to both structural changes and stretch tolerance. Therefore, the purpose of this study was to investigate the effect of a 6-wk hamstring-stretching program on knee extension range of motion, passive resistive forces, and muscle stiffness.

Back to Top | Article Outline

METHODS

Subjects.

In accordance with the requirements of the Auckland University of Technology (AUT) ethics committee, 43 male subjects (mean age, 15.8 ± 1.0 yr; height, 182 ± 5.3 cm; mass, 76 ± 8.5 kg; see Table 1) from two Auckland secondary schools were invited to participate on a voluntary basis. Written consent was gained before testing. With respect to the selection criteria, all subjects had to be free of injuries in the lower limb and have no current history of low-back pain. The schools were randomly assigned by a coin toss to either the control group or the intervention group. The schools, rather than individual subjects, were randomly assigned, to avoid the possible interaction between subjects during the intervention period. Such interaction was likely due to the small class sizes within a single participating school. The subjects in the control group were unaware of the purpose of the study. That is, they did not know that an experimental group was undertaking a stretching study. The principal investigator was blinded to the allocation of the schools and was not involved in the supervision of the stretching program. Data collection was performed at the Physical Rehabilitation Research Centre of the Auckland University of Technology.

Table 1
Table 1
Image Tools
Back to Top | Article Outline
Hamstring extensibility.

A passive knee extension test using the Kincom® dynamometer (Kinetic Communicator, II 500H, Chattex Corp., Chattanooga, TN) was utilized to measure hamstring extensibility. These methods were similar to that used by other investigators (13–17). In accordance with the manufacturer’s instructions, the limb weight of subjects was gravity corrected with subjects in a supine position. This procedure was carried out before and after the intervention period. After the measurement of limb weight, subjects were seated in the Kincom® and a firm lumbar roll was placed in the low lumbar spine (L2–L4 level) to maintain the lumbar lordosis and reduce the likelihood of the pelvis rotating posteriorly during the stretch procedure. The thigh to be tested was placed on a specially constructed pad that created an angle of 25° to the horizontal. The height of the pad was adjustable so that during the stretch procedure the lower leg was unable to reach full knee joint extension. The thigh was secured with a Velcro strap onto the pad. The subject was secured in the sitting position with a Velcro strap across the chest and a seat belt over the anterior aspect of the pelvis. The knee joint was positioned with the axis of rotation in line with the axle of the lever arm of the Kincom®. Once the subjects were ready, the limb to be tested was moved to the starting position at 80° of knee flexion. A blindfold was placed over the subjects’ eyes, and they were asked to relax the muscles about the knee joint throughout the motion and to concentrate on the sensation of the stretch. Surface electromyographic (EMG) activity from the rectus femoris and the lateral hamstring muscles (Delsys 2.01 electrodes, 5 dB down at 20 and 450 Hz) was monitored to ensure that subjects complied with this request. The root mean square of muscle activity was normalized to a maximum voluntary isometric contraction recorded at the completion of each test. The EMG activity could then be expressed as a percentage of the activity recorded during their maximum isometric voluntary contraction. If a subject’s EMG data was >1% of a maximum voluntary contraction, then that subject’s data were discarded. The Kincom® dynamometer extended the knee passively at 10°·s−1. The EMG data were recorded simultaneously with signals from the Kincom®’s load cell and potentiometer at a sampling frequency of 500 Hz and relayed to a computerized data acquisition system for subsequent processing. Subjects used an emergency stop switch to halt knee extension at the point when they perceived the maximum tolerable stretch on the hamstring muscles. This terminal position was then designated as the point of maximal passive knee extension.

Four trials were undertaken. The first trial was used to familiarize the subjects with the procedure. Three further trials were undertaken, and the average of these trials was used for data analyses. The reliability of these procedures was determined during pilot testing. Based on 10 subjects’ data, the reliability was high (intraclass coefficient = 0.97, with a lower confidence interval of 0.93).

The variables of interest were the maximal passive resistive force, the maximum range of motion, and stiffness. Stiffness was calculated using a computer-based program that differentiated the force and angle data, and subsequently provided the mean stiffness for the final 10% of the range of motion. The final 10% of range of motion was determined at baseline and then again after the intervention period.

Back to Top | Article Outline
Stretching program.

Subjects in the intervention group were instructed to stretch their hamstrings using the Stance Phase Stretch method (20). This method required the subject to be in a standing position with the right leg forward as if they were about to start a running race. The right thigh was stretched first by placing it in front of the left leg. Both knees were slightly flexed. Both hands were placed on the right knee. Subjects then tilted the pelvis forward to create a lordosis in the lumbar spine. Once in this position, subjects were asked to bend forward from the waist until they felt a stretching sensation in the right hamstring. The stretch was accentuated if required, by straightening the right knee using pressure downward from both hands, without changing the posture of the upper body. Thus, the stretch was passively induced. Subjects were instructed to hold the stretch for 30 s and then repeat the procedure on the left leg. Three repetitions were performed on each leg. The stretches were performed once a day on five consecutive days of the week, for 6 wk. An independent research assistant supervised the subjects in the stretching program throughout the intervention period.

The subjects kept a diary of the stretches and other physical activity. Type, duration, and intensity of exercise over the 6-wk intervention period were recorded. Qualitative analysis of the diaries after the intervention period provided evidence that the subjects had been consistent with the stretching protocol and in their level of daily physical activity. The control group was instructed not to stretch their hamstrings over the 6 wk of the trial. They also kept a diary of other physical activities they did, noting type, duration, and intensity of exercise. Qualitative analysis of the diaries after the intervention period provided evidence that the subjects had been consistent with their level of daily physical activity and had not engaged in any stretching exercises with the lower-limb muscle groups.

Back to Top | Article Outline
Statistical analysis.

Descriptive statistics were analyzed to determine the appropriateness of utilizing parametric analyses. A two-factor ANOVA was utilized for this study. The two factors were time (pre- and postintervention), which was the repeated measure, and group (experimental and control), the between-subject factor. Thereafter, comparisons within groups across the factor time were made using paired t-tests. The statistical analysis was undertaken using Statistical Package for Social Sciences Version 10.0 (Chicago, IL). The alpha level was set at 0.05.

Back to Top | Article Outline

RESULTS

Subjects.

All subjects in the control group and the intervention group completed the program. The subjects’ compliance to stretching the hamstrings in the intervention group was 100%.

Back to Top | Article Outline
Knee extension range of motion.

Figure 1 displays the mean knee extension range of movement for the stretch group and the control group. There was a significant interaction effect (P = 0.001). Although no change occurred in the control group, subjects in the stretch group were a mean 16.1° ± 7.1° short of full knee extension at the start of the intervention, and improved significantly to 6.0° ± 6.8° after the intervention (P = 0.000).

Figure 1
Figure 1
Image Tools
Back to Top | Article Outline
Force measurements.

Figure 2 displays the maximal passive resistive force during the passive knee extension test of the stretch group and the control group. There was a significant interaction effect (P = 0.000). Although there was no change in the control group, subjects in the stretch group had a mean of 72.7 ± 34.3 N at baseline, and this level increased significantly to 114.4 ± 30.6 N after the intervention (P = 0.000).

Figure 2
Figure 2
Image Tools
Back to Top | Article Outline
Stiffness.

Figure 3 displays the mean data for stiffness (N·deg−1) over the final 10% of the knee extension range of motion for subjects in the stretch group and control groups at baseline and after the intervention. There was a significant interaction effect (P = 0.001). Although there was no change in the control group, the stretch group had a mean of 3.31 ± 1.49 N·deg−1 at baseline, and this increased significantly to a mean of 4.18 ± 0.96 N·deg−1 after the intervention (P = 0.001).

Figure 3
Figure 3
Image Tools
Back to Top | Article Outline

DISCUSSION

The results of the current study demonstrated that 6 wk of static stretches to the hamstring muscles resulted in a 10° increase in knee extension range of movement. Only one other study by Magnusson and coworkers (15) has examined changes in range of motion using procedures similar to the current study. Whereas Magnusson et al. (15) also observed a 10° increase in knee extension, the stretching duration and the type of stretch differed from the current study. Subjects in the Magnusson et al. study (15) stretched twice a day, holding each stretch for 45 s over a 3-wk period for a total stretch duration of 9000 s (150 min). This was significantly greater than the stretch duration of the current study, which was 2700 s (45 min). The stretch duration in the current study was similar to a number of other studies (1–3) that have used a clinical test, the passive knee extension test (4,11,19) to measure changes in range of motion. The increases in range of motion reported in the current study were similar to the findings of these latter researchers (1,3,6).

With respect to changes in passive resistive force, the results of the current study were also consistent with Magnusson et al. (15). An increase in joint angle was accompanied by an increase in force (see Fig. 2). Other researchers (4,9,10) have also noted increases in forces with increases in range of motion. In the current study the changes in force increased to a greater magnitude compared with the increase in range of motion and hence muscle stiffness was also increased. This was in contrast to the findings of Magnusson et al. (15). An examination the force-angle curves in the Magnusson et al. study ((15), Fig. 7) indicated there was an increase in terminal angle, peak torque, and energy but no change in the shape of the curve. In the current study, the stiffness over the final 10% of the knee extension range of motion for the intervention group was significantly greater (see Figs. 3 and 4). As Magnusson et al. (15) and other researchers (9,10) found no change had occurred in the force-angle curves after stretching interventions, they argued that the structural parameters of the muscle had not been altered and concluded that the increased maximal range of motion was achieved as a consequence of stretch tolerance. One possible reason for the difference could be related to the age differences in the current study and that of Magnusson et al. (15). Subjects in the Magnusson et al. study (15) had a mean age of 26 ± 6 yr, compared with a mean age of 15.8 ± 1.0 yr in the current study. Animal studies (21) have demonstrated that structural parameters are different in maturing tissue as compared with adult soft tissues, but comparative stretching programs between young subjects and mature subjects have not been undertaken. The results of the current study, however, did show that in the new range of motion, an increase in the stiffness had occurred, therefore, providing evidence that there were changes to the structural characteristics of the tissue.

Figure 4
Figure 4
Image Tools

The mechanism associated with these changes can only be speculated upon from studies involving animals that have been immobilized. Evidence from animal studies and experimental protocols that involve immobilization of the muscle in a lengthened position have shown that increases in muscle fiber lengths do occur as a result of the lengthening procedures (12,25). Williams and Goldspink (25) demonstrated that a muscle immobilized in a lengthened position had increased mass and added sarcomeres in series, and that this event occurred primarily at the distal end of the contractile elements. Goldspink et al. (8) suggested that such changes were a local response to increased tension in the muscle. Whether the changes in mass observed after a lengthening regimen also show a hypertrophy effect has not been documented. Such an effect would explain the increased stiffness observed in the current study. Other studies using animals investigated the effects of progressive bone lengthening on muscle stiffness (26,27) and demonstrated that sarcomeres are added in series during the procedure, but if the rate of lengthening is too fast, there is a detrimental effect with a significant increase in muscle stiffness. The researchers commented that significant increases in muscle stiffness were due to an increased lying down in the amount of connective tissue in the muscle as a result of damage to the tissue caused by the rapid stretching regimen. It would seem that the results of these studies suggest there is an optimal force required for appropriate sarcomere growth and adaptation of the connective tissue within the muscle. Animal studies such as these may add support to the hypothesis of Gajdosik (4,5), who suggested that the increases in hamstring length in human tissue may be due to the possible increases in the number of sarcomeres in series, and this may explain the increase in the passive length of the muscles after a stretching regimen. However, for confirmation of this view, a study involving animals that examines the effects of a stretching program without an immobilization procedure is needed to appreciate the changes in both contractile and connective tissue elements.

Back to Top | Article Outline

SUMMARY AND CONCLUSIONS

After a 6-wk periodic hamstring-stretching program, subjects’ knee extension range of motion increased. The increase in the knee joint angle was accompanied by an increase in passive resistive forces, and that was greater than that observed for range of motion. Hence, stiffness was increased in the new range of motion gained after stretching. These findings provided evidence to support the suggestion that structural changes occurred in the muscles.

Back to Top | Article Outline

REFERENCES

1. Bandy, W., and J. Irion. The effect of time on static stretch on the flexibility of the hamstring muscles. Phys. Ther. 74:845–850, 1994.

2. Bandy, W., J. Irion, and M. Briggler. The effect of static stretch and dynamic range of motion training on the flexibility of the hamstring muscles. J. Orthop. Sports Phys. Ther. 27:295–300, 1998.

3. Bandy, W., J. Irion, and M. Briggler. The effect of time and frequency of static stretching on flexibility of the hamstring muscles. Phys. Ther. 77:1090–1096, 1997.

4. Gajdosik, R. Effects of static stretching on the maximal length and resistance to passive stretch of short hamstrings muscles. J. Orthop. Sports Phys. Ther. 14:250–255, 1991.

5. Gajdosik, R. Passive extensibility of skeletal muscle: review of the literature with clinical implications. Clin. Biomech. 16:87–101, 2001.

6. Girouard, C., and B. Hurley. Does strength training inhibit gains in range of motion from flexibility training in older adults? Med. Sci. Sports Exerc. 27:1444–1449, 1995.

7. Godges, J., H. MacRae, C. Longdon, C. Tinberg, and P. MacRae. The effects of two stretching procedures on hip range of motion and gait economy. JOSPT 10:350–357, 1989.

8. Goldspink, G., C. Tabary, J. Tabary, C. Tardieu, and G. Tardieu. Effect of denervation on the adaptation of sarcomere number and muscle extensibility to the functional length of muscle. J. Physiol. 236:733–742, 1974.

9. Halbertsma, J., A. Bolhuis, and L. Goeken. Sport stretching: effect on passive stiffness of short hamstrings. Arch. Phys. Med. Rehabil. 77:688–692, 1996.

10. Halbertsam, J., N. Ludwig, and M. Goeken. Stretching exercises: effect on passive extensibility and stiffness in short hamstrings of healthy subjects. Arch. Phys. Med. Rehabil. 75:976–981, 1994.

11. Hartig, D., and J. Henderson. Increasing hamstring flexibility decreases lower extremity overuse injuries in military basic trainees. Am. J. Sports Med. 27:173–176, 1999.

12. Herbert, R., and R. Balnave. The effect of position of immobilization on resting length, resting stiffness, and weight of the soleus muscle of the rabbit. J. Orthop. Res. 11:358–366, 1993.

13. Klinge, K., P. Magnusson, E. Simonson, M. Per Aagaard, K. Klausen, and M. Kjaer. Effect of strength and flexibility training on skeletal muscle electromyographic activity, stiffness, and viscoelastic stress relaxation response. Am. J. Sports Med. 25:710–716, 1997.

14. Magnusson, P., E. Simonsen, P. Aagaard, and M. Kjaer. Biomechanical responses to repeated stretches in human hamstring muscle in vivo. Am. J. Sports Med. 24:622–628, 1996.

15. Magnusson, P., E. Simonsen, P. Aagaard, H. Sorenson, and M. Kjaer. A mechanism for altered flexibility in human skeletal muscle. J. Physiol. 497:291–298, 1996.

16. Magnusson, S. Passive properties of human skeletal muscle during stretch maneuvers. Scand. J. Med. Sci. Sports 8:65–77, 1998.

17. Magnusson, S., E. Simonsen, P. Aagaard, G. Gleim, M. McHugh, and M. Kjaer. Viscoelastic response to repeated static stretching in the human hamstring muscle. Scand. J. Med. Sci. Sports 5:342–347, 1995.

18. McNair, P., and S. Stanley. Effect of passive stretching and jogging on the series elastic muscle stiffness and the range of motion of the ankle joint. Br. J. Sports Med. 30:313–318, 1996.

19. Roberts, J., and K. Wilson. Effect of stretching duration on active and passive range of motion in the lower extremity. Br. J. Sports Med. 33:259–263, 1999.

20. Ross, M. Effect of Lower extremity position and stretching on hamstring muscle flexibility. J. Strength Cond. Res. 13:124–129, 1999.

21. Shadwick, R. Elastic energy storage in tendons: mechanical differences related to function and age. J. Appl. Physiol. 68:1033–1040, 1990.

22. Shellock, F., and W. Prentice. Warming up and stretching for improved physical performance and prevention of sports related injuries. Sports Med. 2:267–278, 1985.

23. Smith, C. The warm up procedure: to stretch or not to stretch: a brief review. J. Orthop. Sports Phys. Ther. 19:12–17, 1994.

24. White, S., and S. Sahrmann. A movement systems balance approach to the management of musculoskeletal pain. In: Physical Therapy of the Cervical and Thoracic Spine, R. Grant (Ed.). Edinburgh: Churchill Livingstone, 1994, pp. 339–378.

25. Williams, P., and G. Goldspink. The effect of immobilisation on the longitudinal growth of straited muscle fibres. J. Anat. 116:45–55, 1973.

26. Williams, P., P. Kyberd, H. Simpson, J. Kenwright, and G. Goldspink. The morphological basis of increased stiffness of rabbit tibialis anterior muscles during surgical limb lengthening. J. Anat. 193:131–138, 1998.

27. Williams, P., H. Simpson, P. Kyberd, J. Kenwright, and G. Goldspink. Effect of rate of distraction on loss of range of joint movement, muscle stiffness, and intramuscular connective tissue content during surgical limb lengthening: a study in the rabbit. Anat. Rec. 255:78–83, 1999.

28. Worrell, T., T. Smith, and J. Winegardner. Effect of hamstring stretching on hamstring muscle performance. JOSPT 20:154–159, 1994.

Keywords:

HAMSTRING STRETCHING; VISCOELASTICITY; FLEXIBILITY; TRAINING; CHILDREN

©2004The American College of Sports Medicine

Login

Article Tools

Images

Share

Search for Similar Articles
You may search for similar articles that contain these same keywords or you may modify the keyword list to augment your search.

Connect With Us