Light reading

http://www.springerlink.com/content/rdxtk6nf3gq7hjcc/fulltext.pdf

All the best with the up and coming season :slight_smile:

I have no permission to access it… would you be so kind and send me to mail: duxx82@gmail.com? Thanks in advance

same here mate … no can do … no23@hotmail.com please

Optimization models for the force and energy in
competitive running
Horst Behncke
Fachbereich Mathematik/Informatik, Universita¬ t Osnabru¬ ck, Germany
Fax (0541) 969-2770
Received 19 July 1995; received in revised form

27 February 1996

Abstract. In [2] the author has developed an optimization model for the force
and energy in competitive running. In this paper the energy processes in the
muscle were described by a three-compartment hydraulic model. Here this is
reviewed brießy and applied to the current world records in order to determine
the key parameters, maximal force, energy reserves and oxygen uptake.
These values agree well with those given in the literature and those obtained
by other means. The velocity proÞles for 100 m sprints are described equally
well. The model is then applied to older world records to deduce a relation
between the force and energy by linear regression. Finally the fully parameterized
model is used to compute the e¤ects of adverse wind and altitude.
Inasmuch as there are data available, there is a good agreement.
Key words: Competitive running Ð Force Ð Energy

Sorry everyone I will send to those who posted their email and/or try to upload it to the sight…if that’s okay and possible :frowning:

Let me know if I’m not allowed to post the article as it’s been a while since I have.

How Upper Neck Muscles Influence Hamstring Length

Below are the abstracts of an interesting research study. The researchers used PNF (or active resistance) stretching to examine the effect of upper neck muscles on hip joint range of motion.
Stretching the hamstrings caused 9% increase in hip extension range of motion as measured with the passive ‘straight leg raise’ (SLR) manouver. Yet stretching the small suboccipital muscles(which connect the occiput with the upper two vertebrae) resulted in almost twice as much (13%) increase of hamstring length as measured with the same SLR test.
The explanation for this extraordinary finding has probably more to do with the neurological importance of the suboccipital muscles. These small muscles have the highest density of muscles spindles in the whole body (and apparently on the whole planet!) and have a major sensory function for antigravity organization. Via the so called ‘Tonic Neck Reflex’ (which we share with most other mammals) an extension of these muscles tends to trigger a tonus decrease of the hipjoint extensors.
My suggested conclusion for bodyworkers & movem. therapists: if a client shortens the upper neck, his hamstrings will stay short no matter how much he wants to stretch or lengthen them. Whereas if he lowers the tonus of these upper neck muscles (either passively via myofascial manipulation or via active ideokinetic movement facilitation) lengthening the hamstrings and increasing hip flexion range of motion will be much easier.
This fits also with a verbal report I heard from Hubert Godard about an interesting research in Italy: runners on a treadmill would unconsciously increase their running speed when a bioelectrical device on their neck lowered the tonus of the upper neck muscles. Whereas increasing the tonus of these muscles made them slow down their speed, although they were not aware of this and perceived their speed as constant. So a stiff occiput-neck connection will tend to ‘put a break’ into the legs via shortening of the hamstrings, and a long and loose occiput-neck connection will take ‘the break out’ by lengthening the midrange of hamstring length and will make the legs swing much faster and easier.
Robert Schleip
P.S.: For more info on the suboccipital muscles see: McPartland J M, Brodeur R R, Rectus capitis posterior minor: a small but important suboccipital muscle, Journal of Bodywork and Movement Therapies, January 1996


Hormones in Short-Term Exercises: Anaerobic Events


Strength and Conditioning Journal: Vol. 25, No. 4, pp. 31–37.

Hormones in Short-Term Exercises: Anaerobic Events
Atko Viru and Mehis Viru

Institute of Exercise Biology, University of Tartu, Estonia

Key Words: hormones, anaerobic, epinephrine, glycogenolysis

PAST REVIEWS HAVE INDICATED hormonal metabolic control as an essential mechanism for metabolic adjustments during exercise and performance (19, 20, 32, 58). Most studies have considered prolonged exercises (19, 58). However, in short-term anaerobic exercise, the actual performance may take less time compared with the triggering of the hormonal response. Therefore, a hormonal response would occur after the sprint, acyclic power, or high-resistance activity was completed because a time delay is unavoidable. However, hormonal responses such as increases of blood concentration of catecholamines, cortisol, and testosteron are evoked by sprint (15, 39), short-term power (3, 36), and strength (16, 24) exercises. A question arises whether these rapid hormonal responses influence the metabolic processes and have significance during these anaerobic exercises. This brief review explores the possibilities for hormonal metabolic control in short-term anaerobic exercises, and the following topics are discussed:

The possibility for fast-rate hormonal changes.

The time characteristics of metabolic effects of fast-rate hormones.

The exercise intensities and the hormonal response.

Fast-Rate Hormonal Responses

Exercise-induced hormonal changes are classified as fast-, moderate-, and slow-rate responses (56). The fast-rate responses are characterized by significant hormonal changes appearing within the first minute after the onset of exercise. These responses are common for activation of the sympathoadrenal system (rapid increase of blood levels of epinephrine and norepinephrine) as well as the pituitary-adrenocortical system (rapid increase of corticotropin concentration, followed by a less rapid but longer lasting cortisol response) (30, 57). Fast-rate hormonal responses are related to the effect of the central motor command. Impulsation from cortical pyramidal neurons communicates directly with the spinal motoneurons. At the same time, a collateral charge reaches the hypothalamic center and activates the sympathoadrenal system as well as neurosecretory neurons (32). The activating messages are sent to the adrenal medulla by sympathetic nerves. The pituitary hypothalamic liberins (releasing neurohormones) activate the adenohypophysis. Furthermore, hormones released from the adenohypophysis travel through circulation and act on peripherial endocrine glands. This way, highly intensive supramaximal exercises and very short muscle efforts of explosive or high resistance types are capable of triggering increased activity of several endocrine systems.

Epinephrine and norepinephrine are fast-rate response hormones that are stored in endoplasmic granules of the cells of the adrenal medulla in the definite form. Sympathetic nerve impulses from the splanchnic nerve to the adrenomedullary cells cause liberation of acetylcholine from nerve endings. Under the action of acetylcholine, epinephrine and norepinephrine release from the granules and flow into the circulating blood. As a result, epinephrine and norepinephrine levels in blood increase rapidly at the beginning of exercise. Triggering of other hormonal responses requires more time because it depends on the secretion time of neurohormones from the hypothalamus, activation of secretion of trophic hormones in the pituitary, and activation of peripheral endocrine gland.

Significance of Exercise Intensity for Hormone Responses

Exercise intensity is one of the main determinants of hormonal changes during the exercise (59). Epinephrine and norepinephrine responses are modest or nonexistent at low or moderate intensities of exercise. When a critical intensity, called intensity threshold, is surpassed, a sharp rise appears in concentrations of both epinephrine and norepinephrine (21, 38, 55). Several studies provided evidence that the threshold intensity for catecholamine response is close to the anaerobic threshold (8, 38, 40, 53).

Corticotropin (13, 48, 50), cortisol (11, 25, 46), ß-endorphin (14, 48, 50), and growth hormone (8, 44, 52) also exhibit intensity thresholds during an exercise response. Similarly to catecholamines, threshold intensities for corticotropin, ß-endorphin (48), and cortisol (46) are close to the anaerobic threshold as indicated by lactate dynamics. Results of Gabriel et al. (18) confirmed that exercise until volitional exhaustion increased blood levels of epinephrine, norepinephrine, cortisol, corticotropin, and ß-endorphin when the intensity corresponded to 100% of the individual’s anaerobic threshold. However, hormonal responses were not significant at intensities corresponding to 85% of the anaerobic threshold. Chwalbinska-Moneta et al. (8) reported a close relationship between triggering growth hormone response and the anaerobic threshold. However, others have reported that the growth hormone threshold is lower than the anaerobic threshold (25, 52). Glucagon levels appeared to increase in exercises at 100% of O2max but did not increase at lower intensities during short-term exercises (21, 45). The testosteron response to exercise for men was significant at 4.0 W•kg−1 but not at 1.5–2.5 W•kg−1 (28). Galbo et al. (22) reported a modest increase in testosteron level in their subjects after maximal, but not submaximal, treadmill exercises. Exercise intensities between 40 and 70% of O2max (21, 25, 47) were associated with a decline in the insulin concentration. Furthermore, a decrease in insulin levels appeared at very low (10% O2max) exercise intensity while consuming a high-fat diet (47). However, near- or supramaximal exercise intensities may lead to an increase in the insulin levels instead of the usual decrease (1, 27).

Unlike catecholamine responses, at overthreshold intensities the magnitude of cortisol response does not exhibit a strict dependence on futher increase of exercise intensity (46). Various studies have indicated that cortisol responses are more related to exercise duration than to the level of power output or running velocity (25, 26, 51). Supramaximal exercises may even attenuate cortisol response (2, 30, 46). It has been suggested that increased H+ ion concentration in anaerobic exercises might inhibit the cortisol response (2). The contribution of exercise intensity and duration for formation of the cortisol response is rather complicated: In some cases, the effect of the intensity may be stronger than the effect of the duration (37).

Exercise duration appears to have a strong effect on growth hormone. In fact, the exercise duration may overshadow the significance of exercise intensity (32, 51). Unlike growth hormone, exercise duration does not increase the testosteron response. As exercise duration increases, the testosteron levels decline (22) to values below the initial level (31). Wilkerson et al. (61) reported increased testosteron levels in their subjects during 20 minutes of exercise with an exercise intensity between 60 and 80% O2max. However, further increases of exercise intensity were not associated with more pronounced increases in testosteron concentrations. In women, testosteron responses are related to steroidogenesis in the adrenal cortex. Therefore, there are gender differences in testosteron patterns during exercise. In women, testosteron concentration was the highest at the end of 2 hours of exercise (60).

The determination of plasma volume showed that the increased testosteron concentrations depended on reduction of plasma volume. Thus, the actual increase in testosteron secretion was not found (61).

Effect of Anaerobic Exercise on Blood Hormone Levels

Taking into account the significance of exercise intensity for hormonal responses, there should be little doubt that anaerobic exercises activate endocrine functions. The questions remaining are what is the minimum duration of highly intensive exercise to trigger hormonal responses, and do these responses appear during or after “pure” anaerobic exercises?

Fentem et al. (15) reported increased blood epinephrine and norepinephrine concentrations during 6 seconds of cycling at maximal power output. Thus, we can conclude that anaerobic exercises lasting only a few seconds are capable of activating the sympathoadrenal system. However, blood sampling in this study took place 3 minutes after the exercise, and we cannot conclude that these hormones were released during the 6 seconds of exercise. Furthermore, a 4- to 7-fold increase in norepinephrine and epinephrine has been reported immediately after 30 seconds of maximal pedalling rate (39) or within 30–90 seconds after a 30-second dash (4). The high hormone concentrations are evidence of a high-rate catecholamine response. Consequently, it can be assumed that rapidly secreted catecholamines may contribute to the metabolic control during sprint exercises, at least during the second half of these very short-term exercises.

Fast responses have also been found in corticotropin (6, 13, 14, 17, 30), ß-endorphin (4, 14, 17), and cortisol (13, 30) levels. Because corticotropin activates the secretion of cortisol, the corticotropin response is faster than that of cortisol (6, 30). Although growth hormone and glucagon responses usually appear in aerobic exercises after a lag period of 10 minutes or more (57), these responses are detectable in anaerobic exercises immediately after the end of exercise and last 1–2 minutes or even less (43, 45).

Repeated short-interval, short-term anaerobic exercise (similar to the interval training) leads to pronounced lactate accumulations in the blood and is associated with high catecholamines (45), growth hormone (1, 23, 29, 54), and testosteron (23, 28) levels. Adlercreutz et al. (1) reported that the high rate of testosteron response was associated with a parallel increase of lutropin concentration in blood. Lutropin is the endogenous stimulus for testosteron secretion.

Although short-term high-intensity exercises trigger the hormonal responses, their maximum hormonal response may not appear immediately after the end of exercise but rather 5–15 (in some cases even 30) minutes later. Obviously, the stimulus for activation of endocrine function was so strong that it created a prolonged readiness for intensive muscular activity (for fighting in phylogenetic past).

In submaximal exercise, the typical training effect is a reduced response to several hormones because of an increase of the intensity threshold measured in terms of power output (19, 58). At the same time, training increases the capacities of the endocrine system (58), leading to an exaggerated hormonal response in trained organism during supramaximal exercises. The improved functional capacities of the endocrine system are apparent by the increased concentration of blood catecholamines (5, 33, 34, 55), ß-endorphine (5, 7, 14), cortisol (5, 51), and growth hormone (5, 51) responses to supramaximal exercise in a trained organism. Particularly important are exaggerated catecholamine responses after sprint training (42) and corticotropin, cortisol, and ß-endorphin responses after sprint-interval training (35). In the sprint-trained person, the immediate increase of growth hormone as well as increases of cortisol and insulin concentration are, after 30 seconds of sprint, more pronounced than in endurance-trained persons (43).

Hormones in Metabolic Control During Anaerobic Exercises

Metabolic effects of hormones are based on the binding of a hormone to its specific cellular receptor. The hormone-receptor complex initiates a further chain of intracellular events, leading to a certain alteration in enzyme activity that may increase or decrease due to changes in molecules of enzyme proteins. Another possibility is induction of synthesis of an enzyme protein. Hormone receptors are located either on the cellular membrane (e.g., catecholamines), in the cytoplasm (e.g., steroid hormones), or in the cellular nucleus (e.g., thyroid hormones). Alterations in enzyme molecules are introduced by means of receptors on cellular membranes, which allow for rapid metabolic effects. Also rapid are the metabolic effects that result from hormone interference to the postreceptory processes, evoked by another hormone through its specific cellular hormone receptor. Receptors in cytoplasm or nucleus initiate protein synthesis. The cascade of these processes requires time up to a couple of hours.

The most rapid hormonal metabolic effect is that of epinephrine on glycogenolysis. In skeletal muscles, glycogen degradation is triggered by intracellular metabolic alterations associated with the initiation of the contraction of myofibrils (appearance of acetylcholine inside the cell, increased concentration of Ca2+ in sarcoplasma). However, the effects of these metabolic alterations are short-term. Epinephrine ensures prolonged and pronounced degradation of glycogen in muscle tissue (49). Because training—particularly sprint training—increases epinephrine responses, it is possible that the amount of epinephrine rapidly reaching the muscle tissue and binding with adrenoreceptors of the sarcolemma has an essential role for achieving the maximal rate of glycogenolysis. In this way, an extensive mobilization of the anaerobic working capacity is achieved.

The specific receptor for cortisol is located in the cytoplasm. Therefore, several metabolic effects of cortisol (e.g., control of glucose-alanine cycle, stimulation of gluconeogenesis and of catabolic processes) appear after an hour or more has elapsed. However, cortisol can promote processes following the binding of epinephrine to the receptor without a substantial time lag. In this case the cortisol binding by its specific cytoplasmic receptor is not necessary. Hence, cortisol is essential in creating intracellular conditions for increased action of epinephrine.

The metabolic effects of other hormones are too slow for evoking changes in cellular metabolism during short-term anaerobic exercises. However, rapid recovery of anaerobic working capacity, muscle strength, and power depends on influences of insulin, cortisol, and testosteron on glycogen resynthesis (58).

Normal intra- and extracellular balance of sodium and potassium ions must be restored with each contraction-relaxation cycle. This balance influences intracellular shifts of calcium. The relaxation process depends directly on reabsorption of cytoplasmic calcium by the sarcoplasmic reticulum. In very intensive exercises, the restoration of ionic balances between intra- and extracellular sodium and potassium contents is not complete, and this becomes a factor decreasing the performance (10, 12). Therefore, after each strong contraction, ionic shifts must happen at a high rate to restore the initial conditions. This depends on the function of the Na+/K±pump on the cellular membrane and the Ca2±pump in the membrane of sarcoplasmatic reticulum. The function of ionic pumps is an energy-consuming process dependent upon adenosine triphosphate by enzymes Na+, K±ATPase, and Ca2±ATPase. The main activator of the Na+/K+ pump is epinephrine, whereas the long-term adaptations of the pump (increased number of related molecules, particularly molecules of Na+/K±ATPase) depend on insulin and thyroid hormones (9). Sprint training increases human skeletal muscle Na+/K+ATPase concentration and improves K+ regulation (41).

Conclusion

High intensities of anaerobic exercises elicit pronounced hormonal responses. However, most of these hormonal responses appear or reach their maximum after short-term exercises. Therefore, the existence of a certain hormonal response does not indicate that the hormone contributes to metabolic control. The rapid action of epinephrine on muscle glycogenolysis makes it essential in triggering and maintaining muscle glycogen breakdown during anaerobic exercise, mainly in those anaerobic exercises in which duration is more than 20–30 seconds. It is possible that cortisol influences the epinephrine hormone response. Contribution of other hormones in metabolic control during short-term anaerobic exercises does not seem plausible. However, the exercise-induced hormonal responses may have significance during the recovery period as well as during the preparation of the athlete for subsequent efforts, with short rest intervals. The role of hormones in long-term adaptation for anaerobic performance has not been demonstrated.

References

  1. Adlercreutz, H., M. Härkönen, K. Kuoppasalmi, K. Kosunen, H. Näveri, and S. Rehunen. Physical activity and hormones. Adv. Cardiol. 18:144–157. 1976.

  2. Barwich, D., A. Rettenmeier, and H. Weicker. Serum levels of so-called “stress-hormones” in athletes after short-term consecutive exercises. Int. J. Sports Med. 3: (Suppl.). 8 1982.

  3. Bosco, C., J. Tihanyi, L. Rivalta, G. Parlato, C. Tranquilli, G. Pulvirenti, C. Foti, and A. Viru. Hormonal responses in strenuous jumping effort. Jpn. J. Physiol. 46:93–98. 1996.

  4. Brooks, S., J. Burrin, M.E. Cheetham, G.M. Hall, T. Yeo, and C. Williams. The response of the catecholamines and ß-endorphin to brief maximal exercise in man. Eur. J. Appl. Physiol. 57:230–234. 1988. [

  5. Bullen, B.A., S. Skrinar, J.Z. Beitins, D.B. Carr, S.M. Repport, C.O. Dotson, M. de Fencl, E.V. Gervine, and J.W. McArthur. Endurance training effects on plasma hormonal responsiveness and sex hormone secretion. J. Appl. Physiol. 56:1453–1463. 1984. [

  6. Buono, M.J., J.E. Yeager, and J.A. Hodgdon. Plasma adrenocorticotropin and cortisol responses to brief high-intensity exercise in humans. J. Appl. Physiol. 61:1337–1339. 1986.

  7. Carr, D.B., B.A. Bullen, S. Skriner, M.A. Arnold, M. Rosenblatt, and J.Z. Beitins. Physical conditioning facilitates the exercise-induced secretion of beta-endorphin and beta-lipotropin in women. N. Engl. J. Med. 305:560–563. 1981.

  8. Chwalbinska-Moneta, J., H. Krysztofiak, A. Ziemba, K. Nazar, and H. Kaciuba-Uscilko. Threshold increases in plasma growth hormone in relation to plasma catecholamine and blood lactate concentrations during progressive exercise in endurance-trained athletes. Eur. J. Appl. Physiol. 73:117–120. 1996.

  9. Clausen, T. Regulation of active Na±K+ transport in skeletal muscle. Physiol. Rev. 66:542–580. 1986

  10. Clausen, T., and M.E. Everts. K+ induced inhibition of contractile force in rat skeletal muscle—Role of active Na+, K±transport. Am. J. Physiol. 252:E492–E499. 1991. 2

  11. Davies, C.T.M., and J.D. Few. Effect of exercise on adrenocortical function. J. Appl. Physiol. 35:887–891. 1973.

  12. Everts, M.E., T. Lomo, and T. Clausen. Changes in K+, Na+ and calcium contents during in vivo stimulation of rat skeletal muscle. Acta Physiol. Scand. 47:357–368. 1993.

  13. Farrell, P.A., T.L. Garthwaite, and A.B. Gustafson. Plasma adrenocorticotropin and cortisol responses to submaximal and exhaustive exercise. J. Appl. Physiol. 55:1441–1444. 1983.

  14. Farrell, P.A., M. Kjaer, F.W. Bach, and H. Galbo. Beta-endorphin and adrenocorticotropin response to supramaximal treadmill exercise in trained and untrained males. Acta Physiol. Scand. 130:619–625. 1987.

  15. Fentem, P.H., I.A. Macdonald, B. Munoz, and S.A. Watson. Catecholamine responses to brief maximum exercise in man. J. Physiol. 361:89 1985.

  16. Few, J.D., F.J. Imms, and J.C. Weiner. Pituitary-adrenal response to static exercise in men. Clin. Sci. 49:201–206. 1975.

  17. Fraioli, F., C. Moretti, D. Paolucci, E. Alicicco, F. Cresconzi, and G. Fortunio. Physical exercise stimulates marked concomitant release of ß-endorphin and adrenocorticotropin (ACTH) in peripheral blood. Experientia. 36:987–989. 1980.

  18. Gabriel, H., L. Schwarz, G. Steffens, and W. Kindermann. Immunoregulatory hormones, circulating leucocyte and lymphocyte subpopulations before and after endurance exercise of different intensities. Int. J. Sports Med. 13:359–366. 1992.

  19. Galbo, H. Hormonal and Metabolis Adaptations to Exercise. Stuttgart, Germany: Thieme Verlag. 1983.

  20. Galbo, H. Exercise physiology : Humoral function. Sports Sci. Rev. 1:65–93. 1992.

  21. Galbo, H., J.J. Holst, and N.J. Christensen. Glucagon and plasma catecholamine response to graded and prolonged exercise in man. J. Appl. Physiol. 38:70–76. 1975. [

  22. Galbo, H., L. Hummer, I.S. Petersen, N.J. Christensen, and W. Bie. Thyroid and testicular hormonal responses to graded and prolonged exercise in man. Eur. J. Appl. Physiol. 36:101–106. 1977.

  23. Gray, A.B., R.D. Telford, and M.J. Weidemann. Endocrine response to intense interval exercise. Eur. J. Appl. Physiol. 66:366–371. 1993. [

  24. Grucza, K., J.F. Kahn, G. Cybulski, W. Niewiadomski, E. Stupnicka, and K. Nazar. Cardiovascular and sympatho-adrenal responses to static handcrip performed with one and two hands. Eur. J. Appl. Physiol. 59:184–188. 1989.

  25. Hartley, L.H., J.W. Mason, R.P. Hogan, L.G. Jones, T.A. Kotchen, E.H. Mougey, F.E. Wherry, L.L. Pennington, and P.T. Rickets. Multiple hormonal responses to graded exercise in relation to physical training. J. Appl. Physiol. 33:602–606. 1972.

  26. Hartley, L.H., J.W. Mason, R.P. Hogan, L.G. Jones, T.A. Kotchen, E.H. Mougey, F.E. Wherry, L.L. Pennington, and P.T. Rickets. Multiple hormonal responses to prolonged exercise in relation to physical training. J. Appl. Physiol. 33:607–610. 1972. [

  27. Hermansen, L., E.D.R. Pruett, J.B. Osnes, and F.A. Giere. Blood glucose and plasma insulin response to maximal exercise and glucose infusion. J. Appl. Physiol. 29:13–16. 1970.

  28. Jezova, D., M. Vigas, P. Tatar, R. Kvetnansky, K. Nazar, H. Kaciuba-Uscilko, and S. Kozlowski. Plasma testosteron and catecholamine responses to physical exercise of different intensity in men. Eur. J. Appl. Physiol. 54:62–66. 1985. [

  29. Karagiorgos, A., J.F. Garcia, and G.A. Brooks. Growth hormone response to continuous and intermittent exercise. Med. Sci. Sports. Exerc. 11:302–307. 1970.

  30. Karelson, K., T. Smirnova, and A. Viru. Interrelations between plasma ACTH and cortisol levels during exercise in men. Biol. Sport. 11:75–82. 1994.

  31. Kindermann, W., and W.M. Schmitt. Verhalten von testosteron in Blutserum bei Körperarbeit unterschiedlicher Dauer und Intensität. Dtsch. Z. Sportmed. 36:99–104. 1985.

  32. Kjaer, M. Regulation of hormonal and metabolic responses during exercise in humans. Exerc. Sport. Sci. Rev. 20:161–184. 1992.

  33. Kjaer, M., and H. Galbo. Effect of physical training on capacity to secrete epinephrine. J. Appl. Physiol. 64:11–16. 1988.

  34. Kjaer, M., P.A. Farrell, N.J. Christensen, and H. Galbo. Increased epinephrine response and inaccurate glucoregulation in exercising athletes. J. Appl. Physiol. 61:1693–1700. 1986.

  35. Kraemer, W.J., S.J. Fleck, R. Callister, M. Shealy, G.A. Dudley, C.M. Maresh, L. Marchietelli, C. Curthirds, T. Murray, and J.E. Falkel. Training responses of plasma beta-endorphin, adrenocorticotropin, and cortisol. Med. Sci. Sports Exerc. 21:146–153. 1989.

  36. Kraemer, W.J., J.F. Patton, H.G. Knuttgen, C.J. Hannon, T. Kettler, E.G. Scott, J.E. Dziados, A.C. Fry, P.N. Frykman, and E.A. Harman. Effects of high-intensity cycle exercise on sympathoadrenal-medullary response pattern. J. Appl. Physiol. 70:8–14. 1991.

  37. Kuoppasalmi, K., H. Näveri, M. Härkönen, and H. Adlercreutz. Plasma cortisol, androstenedione, testosteron and luteinizing hormone in running exercise of different intensity. Scand. J. Clin. Lab. Invest. 40:403–409. 1980.

  38. Lehmann, M., J. Keul, and M. DaPrada. Plasma catecholamines in trained and untrained volunteers during graduated exercise. Int. J. Sports Med. 2:143–147. 1981.

  39. Macdonald, I.A., S.A. Wootton, B. Munroe, P.H. Fentem, and C. Williams. Catecholamine response to maximal anaerobic exercise. In: Biochemistry of Exercise. H.G. Knuttgen, J.A.Vogel, and J. Poortmans, eds Champaign, IL: Human Kinetics. 1983. pp. 749–754.

  40. Mazzeo, R.S., and J. Marshall. Influence of plasma catecholamines on the lactate threshold during graded exercise. J. Appl. Physiol. 67:1319–1322. 1989.

  41. McKenna, M.J., T.A. Schmidt, H. Hagriaves, L. Cameron, S.L. Skinner, and K. Kjeldsen. Sprint training increases human skeletal muscle Na+,K±ATPase concentration and improves K+ regulation. J. Appl. Physiol. 75:173–180. 1993.

  42. Nevill, M.E., L.H. Boobis, S. Brooks, and C. Williams. Effect of training on muscle metabolism during treadmill sprinting in man. J. Appl. Physiol. 67:2376–2382. 1989. [

  43. Nevill, M.E., D.J. Holmyard, G.M. Hale, P. Allsop, A. von Oosterhout, J.M. Burrin, and A.M. Nevill. Growth hormone response to treadmill sprinting in sprint and endurance-trained athletes. Eur. J. Appl. Physiol. 72:460–467. 1996.

  44. Näveri, H. Blood hormone and metabolite levels during graded cycle ergometer exercise. Scand. J. Clin. Lab. Invest. 45:1319–1322. 1986.

  45. Näveri, H., K. Kuoppasalmi, and M. Härkönen. Plasma glucogen and catecholamines during exhaustive short-term exercise. Eur. J. Appl. Physiol. 33:308–311. 1985.

  46. Port, K. Serum and saliva cortisol responses and blood lactate accumulation during incremental exercise testing. Int. J. Sports Med. 12:490–494. 1991.

  47. Pruett, E.D.R. Glucose and insulin during prolonged work stress in men living on different diets. J. Appl. Physiol. 28:199–208. 1970.

  48. Rahkila, P., E. Hakala, M. Alen, K. Salminen, and T. Laatikainen. ß-endorphin and corticotropin release is dependent on a threshold intensity of running exercise in male endurance athletes. Life Sci. 43:551–558. 1988. [

  49. Richter, E.A., N.B. Ruderman, H. Couras, E. Selur, and H. Galbo. Muscle glycogenolysis during exercise. Dual control by epinephrine and contraction. Am. J. Physiol. 242:E25–E32. 1982. .

  50. Schwarz, L., and W. Kindermann. ß-endorphin, adrenocorticotropic hormone, cortisol and catecholamines during aerobic and anaerobic exercise. Eur. J. Appl. Physiol. 61:165–171. 1990. [

  51. Snegovskaya, V., and A. Viru. Steroid and pituitary hormone responses to rowing exercises: Relative significance of exercise intensity and duration and performance level. Eur. J. Appl. Physiol. 67:59–65. 1993.

  52. Sutton, J.R., and L. Lazarus. Growth hormone in exercise: Comparison of physiologic and pharmacologic stimuli. J. Appl. Physiol. 41:523–527. 1976.

  53. Urhausen, A., B. Weiler, B. Coen, and W. Kindermann. Plasma catecholamines during endurance exercise of different intensities as related to the individual anaerobic threshold. Eur. J. Appl. Physiol. 69:16–20. 1994.

  54. Vanhelder, W.P., M.W. Radomski, R.C. Goode, and K. Casey. Hormonal and metabolic responses to three types of exercise of equal duration and external work output. Eur. J. Appl. Physiol. 54:337–342. 1985.

  55. Vendsalu, A. Studies on adrenaline and noradrenaline in human plasma. Acta Physiol. Scand. 173 Suppl.49) 1–123. 1960.

  56. Viru, A. Exercise metabolism and endocrine function. In: Biochemistry of Exercise. H.G. Knuttgen, J.A. Vogel, and J. Poortmans, eds. Champaign, IL: Human Kinetics. 1983. pp. 83–86.

  57. Viru, A. Plasma hormones and physical exercise. Int. J. Sports Med. 13:201–209. 1992.

  58. Viru, A. Adaptation in Sports Training. Boca Raton, Ann Arbor, London, Tokyo: CRC Press. 1995.

  59. Viru, A., T. Smirnova, K. Karelson, V. Snegovskaya, and M. Viru. Determinants and modulators of hormonal responses to exercise. Biol. Sport. 13:169–187. 1996. 2

  60. Webb, M.L., J.P. Wallace, C. Hamill, J.L. Hodgson, and M.M. Mashaldi. Serum testosteron concentration during two hours of moderate intensity treadmill running in trained men and women. Endocr. Res. 10:27–38. 1984. [

  61. Wilkerson, J.E., S.M. Horvath, and B. Gutin. Plasma testosteron during treadmill exercise. J. Appl. Physiol. 49:249–253. 1980.

Atko-Meeme Viru is a professor emeritus specializing in exercise physiology at the University of Tartu, Estonia. He earned a Ph.D. from the University of Tartu, and D.Sc. from the Academy of Sciences of Estonia. His investigations examine endocrine functions in muscular activity and adaptation mechanisms in training.
Mehis Viru is a senior researcher at the Institute of Exercise Biology, University of Tartu. He earned a Ph.D. from the University of Tartu. His research work is focused on specificity of training effects on skeletal muscles and endocrine functions, as well as on biochemical monitoring of training.

Is anyone familiar with the work of Serge Gracovetsky?

Influence of static stretching on viscoelastic properties of human tendon structures in vivo
Keitaro Kubo, Hiroaki Kanehisa, Yasuo Kawakami, and Tetsuo Fukunaga
Department of Life Science (Sports Sciences), University of Tokyo, Komaba 3-8-1, Meguro, Tokyo 153-8902, Japan

ABSTRACT

The purpose of this study was to investigate the influences of static stretching on the viscoelastic properties of human tendon structures in vivo. Seven male subjects performed static stretching in which the ankle was passively flexed to 35° of dorsiflexion and remained stationary for 10 min. Before and after the stretching, the elongation of the tendon and aponeurosis of medial gastrocnemius muscle (MG) was directly measured by ultrasonography while the subjects performed ramp isometric plantar flexion up to the maximum voluntary contraction (MVC), followed by a ramp relaxation. The relationship between the estimated muscle force (Fm) of MG and tendon elongation (L) during the ascending phase was fitted to a linear regression, the slope of which was defined as stiffness of the tendon structures. The percentage of the area within the Fm-L loop to the area beneath the curve during the ascending phase was calculated as an index representing hysteresis. Stretching produced no significant change in MVC but significantly decreased stiffness and hysteresis from 22.9 ± 5.8 to 20.6 ± 4.6 N/mm and from 20.6 ± 8.8 to 13.5 ± 7.6%, respectively. The present results suggest that stretching decreased the viscosity of tendon structures but increased the elasticity.
medial gastrocnemius muscle; stiffness; hysteresis; flexibility

INTRODUCTION

STRETCHING HAS BEEN RECOMMENDED to prevent injury and to improve performance by regaining joint range of motion, i.e., increasing flexibility (8, 25, 31). It has been documented that the potential mechanism for reduced risk of injury with increasing flexibility is the change in the viscoelastic properties of muscle-tendon units (31). Magnusson et al. (17), who determined the stiffness of muscle-tendon units as a result of observations on the ratio of the change in passive muscle moment to that in joint angle, suggested that repetitive stretches made hamstrings more compliant. In addition, Wilson et al. (32), who applied a damped oscillation technique to determine the stiffness of the upper limbs, showed that the enhancement in rebound bench press performance observed consequent to flexibility training was caused by a reduction in stiffness of muscle-tendon units, increasing the utilization of elastic strain energy during the rebound bench press lift. It is well known that if an activated muscle is stretched before shortening, its performance is enhanced during the concentric phase. Many previous studies have indicated that this phenomenon is purported to be the result of strain energy stored in the tendon structures (e.g., Refs. 12, 28). Taken together, these previous results would indicate that the stretching training had made the viscoelastic properties of tendon structures compliant, and thus the stored elastic energy during stretch-shortening cycle increased. However, no attempt has been made to investigate the influences of stretching on the properties of human tendon structures in vivo.
Because most biological tissues act viscoelastically, if the muscle-tendon unit is stretched and then held at a constant length, the passive force at that length gradually declines, a phenomenon known as stress relaxation (17, 25). It has been demonstrated both in vitro (25) and in vivo (17) that repeated stretching of muscle-tendon units to a constant length significantly reduces peak passive tension. These findings suggest that stretching reduces the viscosity and/or stiffness of the muscle-tendon unit, which would be a factor to increase the joint range of motion. In addition, the viscoelastic materials of the muscle-tendon unit produce a variation in the load-deformation relationship that takes place between the loading and unloading curves during a cyclic tensile test (1). This is called hysteresis. For viscoelastic materials, greater energy is absorbed during loading than is dissipated during unloading (25). The hysteresis, i.e., the area within the loop, represents the energy loss as heat due to internal damping, and the area under the unload curve is the energy recovered in the elastic recoil (1). Wilson et al. (32) reported that flexibility training for the upper limbs induced a significant increase in work during the initial concentric portion of the rebound bench press lift. This led us to speculate that stretching may be an effective way to increase reused energy during exercise involving a stretch-shortening cycle, by reducing the hysteresis. However, only few studies have ever tried to quantify the hysteresis of the human muscle-tendon unit in vivo and to investigate the effects of stretching on it (16).
Recent reports have shown that ultrasonography can be used to determine the stiffness and Young’s modulus of human tendon structures in vivo (10, 12, 14, 15). Hence, we applied this technique to determine the magnitude of elongation in the tendon structure of human medial gastrocnemius (MG) muscle before and after static stretching and examine the changes in the stiffness and hysteresis. The purpose of the present study was to investigate the effects of static stretching on the viscoelastic properties of human tendon structures in vivo.

METHODS

Subjects
Seven healthy men (age 25.3 ± 1.4 yr, height 172.6 ± 4.9 cm, weight 70.8 ± 7.9 kg; means ± SD) voluntarily participated in the present study as subjects. When the data were collected, the subjects were participating in recreational sports but had experienced neither strength training nor flexibility training programs. The subjects were fully informed of the procedures to be utilized as well as the purpose of this study. Written, informed consent was obtained from all subjects.
Measurement of Viscoelastic Properties of Tendon Structures
Before and after stretching, torque produced during isometric planar flexion and elongation in the tendon structures of MG was determined by a dynamometer (Myoret, Asics) and ultrasonography, respectively.
Measurement of torque. The experimental setup is schematically shown in Fig. 1A. The subject lay prone on a test bench, and the waist and shoulders were secured by adjustable lap belts and held in position. The right ankle joint was set at 0° (anatomic position) with the knee joint at full extension, and the foot was securely strapped to a foot plate connected to the lever arm of the dynamometer. Before the test, the subject performed a standardized warm-up and submaximal contractions to become accustomed to the test procedure. The subject was instructed to develop a gradually increasing force from relax to maximal voluntary contraction (MVC) within 5 s, followed by a gradual relaxation within 5 s. The task was repeated two times per subject with at least 3 min between trials. Torque signals were analog-to-digital converted at a sampling rate of 1 kHz (MacLab/8, type ML780, AD Instrument) and analyzed by a personal computer (Performa 630, Macintosh). The measured values that are shown below are the means of two trials.

View larger version (26K):
[in this window]
[in a new window]
Fig. 1. A: schematic representation of experimental setup. PC, personal computer; VTR, videotape recorder; TQ, torque; MG, medial gastrocnemius muscle; Sol, soleus muscle. B: platform was moved to 35° of dorsiflexion and held for 10 min.

Measurement of elongation of tendon structures. A real-time ultrasonic apparatus (SSD-2000, Aloka) was used to obtain a longitudinal ultrasonic image of MG at the level of 30% of the lower leg length, i.e., from the popliteal crease to the center of the lateral malleolus. The ultrasonic images were recorded on videotape at 30 Hz, synchronized with recordings of a clock timer for subsequent analyses. The tester visually confirmed the echoes from the aponeurosis and MG fascicles. The point at which one fascicle was attached to the aponeurosis § was visualized on the ultrasonic image. P moved proximally during isometric torque development up to maximum (Fig. 2). A marker was placed between the skin and the ultrasonic probe as the landmark to confirm that the probe did not move during measurements. The cross-point between superficial aponeurosis and fascicles did not move. Therefore, the displacement of P (L) is considered to indicate the lengthening of the deep aponeurosis and the distal tendon (10, 12).

View larger version (64K):
[in this window]
[in a new window]
Fig. 2. Ultrasonic images of longitudinal sections of MG muscle during isometric contraction. A marker (X) was placed between the skin and the ultrasonic probe as the landmark to confirm that the probe did not move during measurements. The cross-point § between superficial aponeurosis and fascicles did not move. P was determined from the echoes of the deep aponeurosis and fascicles. P moved proximally during isometric torque development from rest (P1) to 50% of maximal voluntary contraction (50%MVC; P2). The distance traveled by P (L) was defined as the length change of tendon and aponeurosis during contraction.

Calculations of strain, stiffness, and hysteresis. The L value at MVC was converted to the strain by the following equation

where TL is the length of the tendon structure, i.e., the distance between the measurement site for L and the estimated insertion of the muscle.
To calculate the stiffness, first, the measured torque (TQ) during isometric plantar flexion was converted to muscle force (Fm) by the following equation

where k is the relative contribution of the physiological cross- sectional area of MG within plantar flexor muscles (6) and MA is the moment arm length of triceps surae muscles at 0° of ankle joint, which was estimated from the lower leg length of each subject as described by Visser et al. (27).
As reported in previous studies using animal and human cadavers (e.g., Ref. 11), the Fm-L relation in the tendon structure was curvilinear consisting of an initial region (toe region) characterized by a large increase in L with increasing force and a linear region immediately after the toe region. The ratio of change in L to that in Fm at every 10% of MVC increased linearly with increasing force production levels from 10-50% of MVC and became almost constant in the range of 50-100% of MVC (12). In the present study, therefore, the Fm and L values above 50% of MVC were fitted to a linear regression equation, the slope of which was adopted as an index of stiffness (12).
The Fm-L curves during the ascending and descending phases of force development produced a loop. In the present study, the area of each of the curves under both the ascending and descending phases was calculated. Then the ratio of the area within the Fm-L loop (elastic energy dissipated) to the area beneath the curve during ascending phase (elastic energy input) was calculated as an index of hysteresis.
The repeatability for the stiffness and hysteresis measurements were investigated on two separate days in a preliminary study with 19 young men (22.6 ± 2.8 yr, 171.5 ± 6.1 cm, 69.2 ± 5.8 kg). The average values of stiffness and hysteresis obtained in the two tests were 23.2 ± 5.3 N/mm and 22.2 ± 8.8%, respectively. Both the measured stiffness and the hysteresis had considerable interindividual variations: 13.8-34.3 N/mm in stiffness and 9.7-37.2% in hysteresis. However, there were no significant differences between test and retest values of stiffness and hysteresis. The test-retest correlation coefficient ® was 0.90 for stiffness and 0.86 for hysteresis. The coefficient of variation was 5% for stiffness and 11% for hysteresis.
Static Stretching
Static stretching was administered to the right lower leg of the subject. The posture of the subject and setup were similar to those for the measurement of viscoelastic properties of tendon structures as mentioned above. The platform of the dynamometer, which was attached to the sole of the subject’s foot, was moved to 35° of dorsiflexion with a constant velocity of 5°/s (Fig. 1B) and held at this position for 10 min. The passive torque (Nm) during the stretching was detected by the dynamometer. Throughout the stretching, the subjects were requested to relax completely and not offer any voluntary resistance. To confirm the potential contribution of the contractile component during the stretching, we recorded electromyographic (EMG) activities from MG, lateral gastrocnemius, soleus, and tibial anterior muscles with Ag/AgCl surface electrodes (5 mm in diameter) placed on the belly of each muscle with a 25-mm interelectrode distance. The passive torque and EMG signals were transmitted to a computer (Performa 630, Macintosh) at a sampling rate of 1 kHz. The EMG was full-wave rectified and integrated for every 1 min of the stretching to give integrated EMG.
Statistics
Descriptive data included means ± SD. The significance of difference between before and after the static stretching was analyzed by a paired Student’s t-test. The level of significance was set at P < 0.05.

RESULTS

Before the stretching, the Fm-L relationship was nonlinear in form, as previously reported for animal and human tendons in vitro (Fig. 3A). The initial region of the ascending curve (toe region) was characterized by a large increase in L with increasing Fm. Moreover, the Fm-L curves during ascending and descending phases produced a loop (Fig. 3B). The strain, stiffness, and hysteresis ranged from 6.6 to 10.4% (8.1 ± 1.6%), from 15.8 to 34.3 N/mm (22.9 ± 5.8 N/mm) and from 9.7 to 33.7% (20.6 ± 8.8%), respectively.

View larger version (13K):
[in this window]
[in a new window]
Fig. 3. Data from 7 subjects before stretching. A: the initial region of the curve was characterized by a large increase in L with increasing muscle force (Fm). Mean stiffness was 22.9 ± 5.8 N/mm. B: the Fm-L curves during ascending and descending phase produced a loop. The hysteresis value was 20.6 ± 8.8%.

The passive torque during stretching showed a peak at an initial phase (36.1 ± 7.0 Nm), after which torque decayed to a plateau with lengthening time (Fig. 4). The mean rate of decline in passive torque was 23.6 ± 8.5%. During the stretching, EMG activities of all the muscles tested were very small and did not change significantly, whereas the passive torque declined (Table 1).

View larger version (15K):
[in this window]
[in a new window]
Fig. 4. Passive torque during stretching showed an initial peak, after which torque decayed to a plateau.

View this table:
[in this window]
[in a new window]
Table 1. Initial and final 1-min iEMG responses during 10-min stretching

There was no significant difference in MVC values between those before and after stretching. However, the L values at near MVC became significantly greater after stretching (Fig. 5). The Fm-L loop, on the other hand, became significantly smaller after stretching (Fig. 6). The measured viscoelastic parameters are shown in Table 2. The stretching induced significant decreases in stiffness and hysteresis and increases in the areas under both loading and unloading curves.

View larger version (16K):
[in this window]
[in a new window]
Fig. 5. Data from 7 subjects. L tended to be greater after stretching than before. L above 300 N was significantly greater after the stretching than before. *Significant difference between before and after stretching.

View larger version (13K):
[in this window]
[in a new window]
Fig. 6. Data from 7 subjects. Fm-L curves during ascending and descending phase produced a loop (hysteresis). The hysteresis was significantly smaller after (A; 13.5 ± 7.6%) than before stretching (B; 20.6 ± 8.8%).

View this table:
[in this window]
[in a new window]
Table 2. Measured parameters before and after stretching

DISCUSSION

The average stiffness before static stretching was 23 N/mm. To make a comparison with prior findings on the stiffness of tendon structures without the influences of dimensional differences, we tried to convert the Fm-L curve to a stress-strain curve and then calculate the Young’s modulus, i.e., the slope of the stress-strain curve, using the procedure described by Ito et al. (10) and Kubo et al. (12). For this purpose, cross-sectional area and length of the tendon were obtained from a previous report (50 mm2 for the Achilles tendon; Ref. 33) and from the distance between the measurement site and estimated insertion of the muscle. The obtained Young’s modulus with an average of 280 MPa agreed with our recent observations on that of tendon structures in knee extensors (250 MPa; Ref. 12), but it was considerably lower than those previously reported for animal and human cadaver tendons, 0.6-1.8 GPa (1, 11). This discrepancy can be attributed to the fact that the stiffness value determined in the present study represents the elasticities of both outer tendon and aponeurosis, whereas the above-quoted research on Young’s modulus investigated the outer tendon only (1, 11). Few studies have ever tried to investigate the elastic properties of aponeurosis of animals (3, 13, 23). Scott and Loeb (23) stated that the elastic properties of aponeurosis were similar to those of tendon. On the other hand, Ettema and Huijing (3) and Lieber (13) showed that the aponeurosis strain was greater than that of tendon. We are unable to offer reasons for the discrepancy. Anyway, the strain of tendon structures obtained in the present study, 8.1%, lies within the range of aponeurosis strain values, 8-10%, which were directly determined using animal materials (3, 13). This supports that the lower Young’s modulus obtained in the present study is attributable largely to the elasticity of the aponeurosis. Recently, Maganaris and Paul (15) demonstrated that the aponeurosis strain values were significantly greater than those of tendon in tibial anterior muscle. Furthermore, Roberts et al. (21) stated that most of energy storage in running turkeys must have occurred in the aponeurosis, thus suggesting that the large extensibility of the aponeurosis has been shown to make muscle contractions more efficient during movement. Namely, the present results on stiffness suggest that the human tendon structures in vivo are quite compliant, and therefore care must be taken when estimating the dynamics of the muscle-tendon unit during human movements using data on tendon elasticity that have been obtained from experiments using human cadavers and/or animals.
In the present study, the loading and unloading curves during a cyclic force development test produced a loop (i.e., hysteresis) as observed in vitro (e.g., Ref. 25). In addition to evidence that passive torque during stretching gradually decreased without any changes in EMG, the appearance of hysteresis suggests that the human tendon structures in vivo have viscoelastic profiles. The area surrounded by the loop represents the energy loss as heat due to internal damping, whereas the area under the unloading curve is the energy recovered in elastic recoil (1). Hence, the hysteresis of tendon structures should be taken into account when estimating the dynamics of the muscle-tendon unit during human movements (28). However, no study has ever tried to quantify the hysteresis of human tendon structures in vivo. The hysteresis determined in the present study averaged 21%. This ranks high within the range of the values reported for 18 species of adult quadrupedal mammals, 3-20% (19). However, the hysteresis value obtained in the present study is comparable to that of human tendons at various strain rates in vitro, ~25% (9).
To calculate the Fm, we estimated moment arm length and relative contribution of MG to the triceps surae muscles in terms of physiological cross-sectional areas. The variation in moment arm length and relative contribution of MG among subjects might have caused the large variability in the measured parameters. The moment arm length and physiological cross-sectional areas of respective muscles of each subject would be necessary for an accurate absolute Fm determination. In the present study, we aimed to study whether the tendon properties changed after static stretching. In addition, there were no significant differences in the activation levels (integrated EMG) of each triceps surae muscles before and after stretching (data not shown). Therefore, we considered that this Fm calculation based on these assumptions would be valid to study the changes of the tendon properties after static stretching.
The stretching technique used in this study made the tendon structures more compliant by decreasing stiffness from 22.9 ± 5.8 to 20.6 ± 4.6 N/mm. Furthermore, the areas under both the loading and unloading curves increased and hysteresis decreased significantly after stretching. The hysteresis is considered an indication of the viscosity of the tissue (1). Therefore, the observed lower hysteresis after stretching can be interpreted as a decline of viscosity within tendon structures. The in vivo data of the present study are consistent with previous findings regarding the influences of stretching on the viscoelasticity of tendons, obtained through observations in vitro. For example, Viidik (26) reported that stretching the tail tendon of rat increased its compliance. Similarly, Wang et al. (29) observed an elongation in wallaby tail tendon on cyclic stretching. In addition to these findings on the elasticity, Frisen et al. (5) and Viidik (26) showed that repeated cyclic stretches of rat tendons decreased hysteresis, suggesting a reduction of energy dissipation in the tissues after stretching.
With regard to the acute influences of stretching on the viscoelasticity of human in vivo, however, the only information available from previous studies is data on the length changes in the muscle-tendon unit, estimated from the relation between passive torque and joint angle. Magnusson et al. (17, 18) observed a reduction of passive torque at a constant joint angle after repetitive stretches, suggesting that stretching makes the muscle-tendon unit more compliant. Despite similarities in the muscle group subjected to stretching and the test protocol used for determination of stiffness, however, others failed to find any changes in the joint angle-passive torque relation after stretching (7, 30). One reason for the discrepancy might involve the difference between the stretch maneuvers used in each study. Taylor et al. (25) have documented in vitro that repeated stretching of muscle-tendon units to a constant length significantly reduces peak passive tension. In their results, after four stretches there was little alteration of the muscle-tendon unit, implying that a minimum number of stretches is required for most of the elongation in repetitive stretching (25). For human muscle-tendon units in vivo, however, treatment programs that consisted of 3-10 sets of 15- to 30-s stretching for hamstrings followed by a 20- to 30-s period of relaxation did not induce a significant change in the joint angle-passive torque relation after the stretching (7, 30). On the other hand, Magnusson et al. (17, 18), who administered five repetitions of 90-s static stretching with an interval of 30 s for hamstrings in vivo, observed that passive resistance in both the initial and final phases during stretch to a constant joint angle diminished with subsequent stretch. In the results of Magnusson et al. (17, 18), however, no significant decline in passive resistance was found after 40-45 s of the 90-s stretch for hamstrings. In addition, five repetitions of the 90-s stretch decreased the relative difference between passive resistances in the initial and final phases in every trial with each subsequent stretch (17, 18). These findings suggest that the existence of changes in the viscoelasticity of muscle-tendon units will depend on the duration rather than the number of stretches, and, if they occur, they should not be rapidly reversible. Although the stretch maneuver used in the present study was not repetitive, it induced a reduction of passive torque by 24% over 10 min, characterized by less change in the latter phase of the stretching (Fig. 4). Taking the above-mentioned point into account, the prescribed duration of stretch in this study may be assumed to be enough to change the viscoelasticity of the stressed tendon structures and to prevent them from returning rapidly.
The mechanisms that resulted in the decreases of stiffness and hysteresis after stretching are unknown. At least for the lowered stiffness observed in the present study, however, an acute change in the structure of the tendons might be involved. In a prior study using dogs (4), it has been documented that continual tensile stress applied during tibial lengthening apparently leads to an alteration in the biomechanical properties of the tendons that can result in a marked decrease of the elastic modulus, which is probably caused by strain-induced damage of the tendons and their repair processes. Stretch maneuvers for the human muscle-tendon unit in vivo can place stress on both the parallel and series elastic components (18). As a result of observations on human in vivo, Magnusson et al. (18) suggested that the observed decline in the stiffness of muscle-tendon units after stretching would be an immediate adaptation of the parallel elastic component to a lower imposed load. However, the present result that the stiffness of the tendon structures decreased after stretch provides for the possibility that stretching induces change in the material function of the series elastic component, too. From the findings of Stromberg and Wiederhielm (24), the collagen fibers follow a wavelike course in the unstressed tendons, but they become aligned or parallel with increasing stress. If a similar phenomenon occurs in the tendon structures on completion of the stretch maneuver used in the present study, the observed reduction in the stiffness might be attributed to an acute change in the arrangement of collagen fibers.
The present results provide a physiological background to increases in the joint range of motion after stretching. Furthermore, the observed changes in the viscoelasticity of the tendon structures may be a reason for the delay in intrinsic muscle contraction after stretching that has been reported in previous studies (2, 22). The chief function of tendon structures is to transfer force produced by the contractile component to the joint and/or bone connected in series. A stiff tendon will be advantageous for performing brisk, accurate movements because it affects rapid tension changes (20). Inversely, if stretching has the effect of changing tendon structures to be more compliant, it will lead to a lower rate of force production and/or a delay of muscle activation. In fact, Rosenbaum and Henning (22) observed reductions of the rate of force development and EMG amplitudes and an increase in EMG latencies after static stretching of the triceps surae. From the standpoint of preventing athletic injuries, however, we can say that stretching and the subsequent decrease in stiffness diminish the imposed load across the muscle-tendon junction during rapid movements.
In conclusion, the present study showed that, using ultrasonography, it was possible to quantify the viscoelastic properties (stiffness and hysteresis) of human tendon structures in vivo. Furthermore, static stretching decreases the viscosity of tendon structures as well as increases the elasticity. This provides a physiological background for reducing passive resistance and improving joint range of motion after stretching.

FOOTNOTES
Address for reprint requests and other correspondence: Keitaro Kubo, Dept. of Life Science (Sports Sciences), Univ. of Tokyo, Komaba 3-8-1, Meguro-ku, Tokyo 153-8902, Japan (E-mail: kubo@idaten.c.u-tokyo.ac.jp ).
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.
Received 30 May 2000; accepted in final form 5 September 2000.

REFERENCES

  1. Butler, DL, Grood ES, Noyes FK, and Zernicke RF. Biomechanics of ligaments and tendons. Exerc Sport Sci Rev 6: 125-181, 1978[Medline].

  2. Cook, CS, and McDonagh MJN Force responses to controlled stretches of electrically stimulated human muscle-tendon complex. Exp Physiol 80: 477-490, 1995[Abstract].

  3. Ettema, GJC, and Huijing PA. Properties of the tendinous structures and series elastic component of the EDL muscle-tendon complex of the rat. J Biomech 22: 1209-1215, 1989[ISI][Medline].

  4. Fink, B, Schwinger G, Singer J, Schmielau G, and Ruther W. Biomechanical properties of tendons during lower-leg lengthening in dogs using the Ilizarov method. J Biomech 32: 763-768, 1999[ISI][Medline].

  5. Frisen, M, Magi M, Sonnerup L, and Viidik A. Rheological analysis of soft collagenous tissue. Part I. Theoretical consideration. J Biomech 2: 13-20, 1969[ISI].

  6. Fukunaga, T, Roy RR, Shellock FG, Hodgson JA, and Edgerton VR. Specific tension of human plantar flexors and dorsiflexors. J Appl Physiol 80: 158-165, 1996[Abstract/Free Full Text].

  7. Halbertsma, JP, van Bolhuis AI, and Goeken LN. Sport stretching: effect on passive muscle stiffness of short hamstrings. Arch Phys Med Rehabil 77: 688-692, 1996[ISI][Medline].

  8. Hortobagyi, T, Faludi J, Tihanyi J, and Merkely B. Effects of intense stretching flexibility training on the mechanical profile of the knee extensors and on the range of motion of the hip joint. Int J Sports Med 6: 317-321, 1985[ISI][Medline].

  9. Hubbard, RP, and Soutas-Little RW. Mechanical properties of human tendon and their age dependence. J Biomech Eng 106: 144-150, 1984[ISI][Medline].

  10. Ito, M, Kawakami Y, Ichinose Y, Fukashiro S, and Fukunaga T. Nonisometric behavior of fascicles during isometric contractions of a human muscle. J Appl Physiol 85: 1230-1235, 1998[Abstract/Free Full Text].

  11. Ker, RF. Dynamic tensile properties of the plantaris tendon of sheep. J Exp Biol 93: 283-302, 1981[Abstract].

  12. Kubo, K, Kawakami Y, and Fukunaga T. Influence of elastic properties of tendon structures on jump performance in humans. J Appl Physiol 87: 2090-2096, 1999[Abstract/Free Full Text].

  13. Lieber, RI. Frog semitendinosus tendon load-strain and stress-strain properties during passive loading. Am J Physiol Cell Physiol 261: C86-C92, 1991.

  14. Maganaris, CN, and Paul JP. In vivo human tendon mechanical properties. J Physiol (Lond) 521: 307-313, 1999[Abstract/Free Full Text].

  15. Maganaris, CN, and Paul JP. Load-elongation characteristics of in vivo human tendon and aponeurosis. J Exp Biol 203: 751-756, 2000[Abstract/Free Full Text].

  16. Magnusson, SP, Aagaard P, Simonsen EB, and Bojsen-Moller F. A biomechanical evaluation of cyclic and static stretch in human skeletal muscle. Int J Sports Med 19: 310-316, 1998[ISI][Medline].

  17. Magnusson, SP, Simonsen EB, Aagaard P, Gleim GW, McHugh MP, and Kjaer M. Viscoelastic response to repeated static stretching in human skeletal muscle. Scand J Med Sci Sports 5: 342-347, 1995[Medline].

  18. Magnusson, SP, Simonsen EB, Aagaard P, and Kjaer M. Biomechanical responses to repeated stretches in human hamstring muscle in vivo. Am J Sports Med 24: 622-628, 1996[Abstract].

  19. Pollock, CM, and Shadwick RE. Relationship between body mass and biomechanical properties of limb tendons in adult mammals. J Appl Physiol 35: 1016-1021, 1994.

  20. Proske, V, and Morgan DL. Tendon stiffness: methods of measurement and significance for the control of movement. A review. J Biomech 20: 75-82, 1987[ISI][Medline].

  21. Roberts, TJ, Marsh RL, Weyand PG, and Taylor CR. Muscular force in running turkeys: the economy of minimizing work. Science 275: 1113-1115, 1997[Abstract/Free Full Text].

  22. Rosenbaum, D, and Henning EM. The influence of stretching and warm-up exercises on Achilles tendon reflex activity. J Sports Sci 13: 481-490, 1995[Medline].

  23. Scott, SH, and Loeb GE. Mechanical properties of aponeurosis and tendon of the cat soleus muscle during whole-muscle isometric contractions. J Morphol 224: 73-86, 1995[ISI][Medline].

  24. Stromberg, DD, and Wiederhielm CA. Viscoelastic description of a collagenous tissue in simple elongation. J Appl Physiol 26: 857-862, 1969[Free Full Text].

  25. Taylor, DC, Dalton JD, Seaber AV, and Garrett WE. Viscoelastic properties of muscle-tendon units. The biomechanical effects of stretching. Am J Sports Med 18: 300-309, 1990[Abstract].

  26. Viidik, A. Simultaneous mechanical and light microscopic studies of collagen fibers. Z Anat Entwicklungsgesch 136: 204-212, 1972[ISI][Medline].

  27. Visser, JJ, Hoogkamer JE, Bobbert MF, and Huijing PA. Length and moment arm of human leg muscles as a function of knee and hip-joint angles. Eur J Appl Physiol 61: 453-460, 1990.

  28. Voigt, M, Moller FB, Simonsen EB, and Poulsen PD. The influence of tendon Young’ modulus, dimensions and instanta-neous moment arms on the efficiency of human movement. J Biomech 28: 281-291, 1995[ISI][Medline].

  29. Wang, XT, Ker R, and Alexander RM. Fatigue rupture of wallaby tail tendons. J Exp Biol 198: 847-852, 1995[Abstract/Free Full Text].

  30. Wiemann, K, and Hahn K. Influences of strength, stretching and circulatory exercises on flexibility parameters of the human hamstrings. Int J Sports Med 18: 340-346, 1997[ISI][Medline].

  31. Willson, GJ, Wood GA, and Elliot BC. The relationship between stiffness of the musculature and static flexibility: an alternative explanation for the occurrence of muscular injury. Int J Sports Med 12: 403-407, 1991[ISI][Medline].

  32. Wilson, GJ, Elliott BC, and Wood GA. Stretch shorten cycle performance enhancement through flexibility training. Med Sci Sports Exerc 24: 116-123, 1992[ISI][Medline].

  33. Yamaguchi, GT, Sawa AGU, Moran DW, Fessler MJ, and Winters JM. A survey of human musculotendon actuator parameters. In: Multiple Muscle Systems: Biomechanics and Movement Organization, edited by Winters JM, and Woo SL-Y… New York: Springer-Verlag, 1990, p. 717-773

Influences of repetitive muscle contractions with
different modes on tendon elasticity in vivo
KEITARO KUBO, HIROAKI KANEHISA, YASUO KAWAKAMI, AND TETSUO FUKUNAGA
Department of Life Science (Sports Sciences), University of Tokyo,
Komaba 3-8-1, Meguro, Tokyo, Japan
Received 28 November 2000; accepted in final form 27 February 2001
Kubo, Keitaro, Hiroaki Kanehisa, Yasuo Kawakami,
and Tetsuo Fukunaga. Influences of repetitive muscle contractions
with different modes on tendon elasticity in vivo. J
Appl Physiol 91: 277–282, 2001.—The present study aimed
to investigate the effects of repetitive muscle contractions on
the elasticity of human tendon structures in vivo. Before and
after each endurance test, the elongation of the tendon and
aponeurosis of vastus lateralis muscle (L) was directly measured
by ultrasonography while the subjects performed ramp
isometric knee extension up to maximal voluntary isometric
contraction (MVC). Six male subjects performed muscle endurance
tests that consisted of knee extension tasks with
four different contraction modes: 1) 50 repetitions of maximal
voluntary eccentric action for 3 s with 3 s of relaxation (ET1),
2) three sets of 50 repetitions of MVC for 1 s with 3 s of
relaxation (ET2), 3) 50 repetitions of MVC for 3 s with 3 s of
relaxation (ET3), and 4) 50 repetitions of 50% MVC for 6 s
with 6 s of relaxation (ET4). In ET1 and ET2, there were no
significant differences in L values at any force production
levels between before and after endurance tests. In the cases
of ET3 and ET4, however, the extent of elongation after the
completion of the tests tended to be greater. The L values
above 330 N in ET3 and 440 N in ET4, respectively, were
significantly greater after endurance tests than before. These
results suggested that the repeated longer duration contractions
would make the tendon structures more compliant and
that the changes in the elasticity might be not be affected by
either muscle action mode or force production level but by the
duration of action.
stiffness; damage; vastus lateralis muscle; ultrasonography
REPEATED MUSCLE CONTRACTIONS result in a reduction of
peak contraction force. Some previous studies demonstrated
that this result is accompanied by the lengthening
in electromechanical delay and the reduction in
rate of force development (e.g., Ref. 27). The mechanisms
underlying these phenomena have not been elucidated.
Vigreux et al. (21) have found that compliance
in the fatigued muscle is significantly higher than that
in the nonfatigued muscle. On the other hand, the
tendon structures have been assumed to be the major
source of series elastic component (16). Therefore,
there is a possibility that the changes in the elasticity
of tendon structures could be a factor leading to the
above-mentioned degradation in muscle contractility.
Previous findings obtained from animal experiments
have shown that the elasticity of tendons is changeable
through physical training (15, 25). However, the adaptations
of tendon structures to training vary with the
mode of exercise performed. For example, Woo et al.
(25) indicated that the ultimate strength and stiffness
of tendon in pigs increased through 12 mo of endurance
training. However, Pousson et al. (15) observed a decrease
in the stiffness of rat soleus muscle after 11 wk
of vertical jumping training. These differences tempt
us to assume that, if the elasticity of tendon structures
changes by repeated muscle actions, its magnitude will
be influenced by the type of muscle action. Furthermore,
it is necessary to grasp the effects of acute
exercises on the tendon properties for the understanding
of the effects of different training regimes.
It is well known that exercises involving high-force
eccentric muscle actions induce temporary muscle pain
and damage (e.g., Ref. 14). Evidence of damage includes
disruption of muscle fibers (2) and changes in
voluntary strength and contractile properties in the
immediate postexercise period (1). Komi (5) has shown
that eccentric stresses exceed conventional concentric
and isometric force by threefold. Therefore, it may be
assumed that the eccentric contraction will induce
greater change in the elasticity of tendon structures
than other muscle action modes.
Real-time ultrasonography allows in vivo recording
of human tendon structures movement during isometric
muscle action (3, 6–11). The present study aimed to
examine the changes in the elastic properties of human
tendon structures caused by repeated maximal voluntary
muscle actions with different modes, force production
levels, and durations.
METHODS
Subjects
Six men [age 24.9 6 0.8 (SD) yr, height 172.5 6 10.0 cm,
weight 71.3 6 10.9 kg] voluntarily participated in this study.
The subjects were fully informed of the procedures to be
Address for reprint requests and other correspondence: K. Kubo,
Dept. of Life Science (Sports Sciences), Univ. of Tokyo, Komaba 3-8-1,
Meguro-ku, Tokyo 153-8902, Japan (E-mail: kubo@idaten.c.u-tokyo.
ac.jp).
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.
J Appl Physiol
91: 277–282, 2001.
8750-7587/01 $5.00 Copyright © 2001 the American Physiological Society http://www.jap.org 277
on November 16, 2006 jap.physiology.org Downloaded from
utilized as well as the purpose of this study. Written informed
consent was obtained from all subjects. None of the
subjects was engaged in any sort of competitive exercise, and
each took part in sports occasionally, at a recreational level.
This study was approved by the office of Department of
Sports Sciences, University of Tokyo, and complied with their
requirements for human experimentation.
Muscle Endurance Test
After a standardized warm-up, the subjects performed
muscle endurance tests that consisted of knee extension
tasks with four different action modes: 1) 50 repetitions of
maximum voluntary eccentric action for 3 s with 3 s of
relaxation (ET1), 2) three times 50 repetitions of maximum
voluntary isometric action (MVC) for 1 s with 3 s of relaxation
(ET2), 3) 50 repetitions of MVC for 3 s with 3 s of relaxation
(ET3), and 4) 50 repetitions of 50% MVC for 6 s with 6 s of
relaxation (ET4). The four muscle endurance tests are summarized
in Fig. 1. Tests were performed by each subject on 4
separate days, with at least 2 wk between sessions, but no
longer than 4 wk were allowed to separate the four sessions.
The exerted torque (TQ) signal was recorded for each action
during the muscle endurance test and then was integrated
with respect to time. The obtained integrated TQ was referred
to as iTQ.
Measurement of Elastic Properties of Tendon Structures
Before and after each endurance task, the elongation of the
tendon and apponeurosis of the vastus lateralis (VL) muscle
as well as TQ was recorded continuously while the subjects
performed ramp isometric knee extension up to MVC. For
ET2, measurements of tendon elongation were performed
after each 50 repetitions.
Measurement of TQ. Each subject was seated on the test
bench of a dynamometer (Myolet, Asics) at a hip joint angle of
80° flexed (full extension 5 0°). The axis of the lever arm of
the dynamometer was visually aligned with the center of
rotation of the knee joint. The right foot was firmly attached
to the lever arm of the dynamometer with a strap and fixed at
a knee joint angle of 80° flexed (full extension 5 0°). The
subjects were asked to exert isometric knee extension TQ
increasingly from zero (relax) to MVC within 5 s. TQ signals
were analog-to-digital converted at a sampling rate of 1 kHz
(MacLab/8, type ML780, AD Instrument) and analyzed by a
computer (Macintosh Performa 630, Apple). The task was
repeated two times per subject with at least 3 min between
trials. The measured values that are shown below are the
means of two trials.
Measurement of elongation of tendon structures. A realtime
ultrasonic apparatus (SSD-2000, Aloka) was used to
obtain a longitudinal ultrasonic image of VL at the level of
50% of the thigh length. The ultrasonic images were recorded
on videotape at 30 Hz, synchronized with recordings of a
clock timer for subsequent analyses. The tester visually con-
firmed the echoes from the aponeurosis and VL fascicles. The
point at which one fascicle was attached to the aponeurosis
§ was visualized on the ultrasonic image. The P moved
proximally during isometric TQ development up to maximum
(Fig. 2). A marker (X) was placed between the skin and the
ultrasonic probe as the landmark to confirm that the probe
did not move during measurements. The cross-point between
superficial aponeurosis and fascicles did not move. Therefore,
the displacement of P (L) is considered to indicate the lengthening
of the deep aponeurosis and the distal tendon (9). The
reliability of the ultrasound measurement of L has been
established elsewhere (6–9).
Fig. 1. Four muscle endurance tests protocols: 1) 50 repetitions (rep)
of maximum voluntary eccentric action for 3 s with 3 s of relaxation
(ET1), 2) three sets of 50 repetitions of maximal voluntary isometric
contraction (MVC) for 1 s with 3 s of relaxation (ET2), 3) 50 repetitions
of MVC for 3 s with 3 s of relaxation (ET3), and 4) 50 repetitions
of 50% MVC for 6 s with 6 s of relaxation (ET4).
Fig. 2. Ultrasonic images of longitudinal sections of vastus lateralis
(VL) muscle at rest (A) and during 50% MVC contraction (B). Point
at which 1 fascicle was attached to deep aponeurosis was determined
as P. The distance traveled by P was defined as the length change of
tendon and aponeurosis during contraction. VI, vastus intermedius;
P1, P at 0% MVC; P2, P at 50% MVC.
278 CHANGE OF TENDON ELASTICITY AFTER MUSCLE CONTRACTIONS
on November 16, 2006 jap.physiology.org Downloaded from
Calculation of the elastic properties. The TQ measured by
the dynamometer was converted to muscle force (Fm) by the
equation
Fm 5 k z TQ z MA2 1
where k is the relative contribution of VL to the quadriceps
femoris muscle in terms of physiological cross-sectional area
(13), and MA is the moment arm length of quadriceps femoris
muscle at 80° of knee flexion, which was estimated from the
thigh length of each subject as described by Visser et al. (22).
In the present study, the Fm and L values above 50% of
MVC were fitted to a linear regression equation, the slope of
which was adopted as an index of stiffness (6–9). Comparison
of stiffness values among four tests (before endurance test)
revealed no significant difference and a coefficient of variance
of 3.5–9.8% (mean 6.2%).
Measurement of Electromyogram
Bipolar surface electrodes (5 mm in diameter) were placed
over the bellies of VL, rectus femoris (RF), vastus medialis
(VM) and biceps femoris (BF) muscles with a constant interelectrode
distance of 25 mm. The electromyographic (EMG)
signals were transmitted to a computer (Macintosh Performa
630, Apple) at a sampling rate of 1 kHz. The EMG was
full-wave rectified and integrated for the duration of the
contraction to give integrated EMG (iEMG).
Measurement of Muscle Architecture
The ultrasonic apparatus was also used to determine the
thickness (MT) and pennation angle (PA) of VL. For MT, the
cross-sectional image was obtained at a site of the middle of
the thigh length. From the ultrasonic image, the interface
between the subcutaneous adipose tissue and VL and interface
between the muscle [vastus intermedius (VI) muscle]
and bone were identified from the ultrasonic image. The
distance from the adipose tissue-L interface to the VL-VI
interface was defined as MT. Also, at this position, the longitudinal
image was obtained for PA. PA was defined as the
angle between the fascicle and the deep aponeurosis.
Statistics
Descriptive data included means 6 SD. The significance of
difference between values before and after endurance test
was analyzed by Student’s t-test. One-way ANOVA was used
for the comparison among four conditions. If the F statistic of
the analysis of variance was significant, differences among
four conditions were assessed by a Scheffe´’s test. The level of
significance was set at P , 0.05.
RESULTS
Figure 3 shows the changes in TQ values during
muscle endurance tests, expressed as absolute values
for the mean of five consecutive trials. In ET4, all the
subjects almost completed the task with their own
prescribed force production levels. The rates of decline
in TQ in ET1, ET2, and ET3 were 41.5 6 15.2, 36.0 6
18.7, and 44.2 6 18.1%, respectively. No significant
differences in the rate of decline in TQ were found
among the three endurance tests. The iTQ value was
significantly lower in ET1 than in the other three
endurance tests (Fig. 4). Among ET2, ET3, and ET4,
however, there were no significant differences in iTQ.
Table 1 shows the iEMG values of RF, VL, VM, and
BF during the measurement of elongation of tendon
structures (i.e., ramp isometric contractions) before
and after ET3. The EMG activities of each quadriceps
femoris muscles (RF, VL, VM) did not differ signifi-
Fig. 3. The changes in torque during the 4 endurance tests expressed
as absolute values for the mean of 5 consecutive trials [ET1
(n), ET2 ({, E, ‚), ET3 (closed cross), ET4 (hatched square)]. Values
are means 6 SD. There was no significant difference in the rate of
decline of force among 3 tests (ET1, ET2, ET3). In ET4, all subjects
almost completed the prescribed test.
Fig. 4. The integrated torque values during the 4 tasks. Values are
means 6 SD. The integrated torque value was significantly lower in
ET1 than the other 3 ETs, whereas there were no significant differences
among the other three tests. Significantly greater than ET1,
P , 0.05.
Table 1. iEMG values during ramp isometric
contraction before and after ET3
RF VL VM BF
Before 1.2160.53 1.4660.37 1.4360.32 0.1060.03
After 1.1760.44 1.4260.30 1.4060.44 0.1060.04
Values are means 6 SD given in mV. iEMG, integrated electromyogram;
ET3, 50 repetitions of maximal voluntary isometric contraction
(MVC) for 1 s with 3 s of relaxation. RF, rectus femoris; VL,
vastus lateralis; VM, vastus medius; BF, biceps femoris. There were
no significant differences.
279 CHANGE OF TENDON ELASTICITY AFTER MUSCLE CONTRACTIONS
on November 16, 2006 jap.physiology.org Downloaded from
cantly before and after ET3. The iEMG of BF were very
small and did not change significantly after ET3. Similar
results were obtained in the other three tests (ET1,
ET2, ET4), too.
Figure 5 shows the relationship between Fm and L
before and after each endurance test. There were no
significant differences in the rate of decline in MVC
value among the four endurance tests (Table 2). Similarly,
there were no significant differences in the rate
of increment in MT and PA among the four endurance
tests (Table 2). In ET1 and ET2, there were no significant
differences in L values at any force production
levels between before and after endurance tests. No
significant changes in stiffness values were found after
ET1 (P 5 0.119) and ET2 (P 5 0.156) (Table 2). In the
cases of ET3 and ET4, however, the extent of elongation
after the completion of the tests tended to be
greater. The L values above 330 N in ET3 and 440 N in
ET4, respectively, were significantly greater after endurance
tests than before. The stiffness decreased significantly
after ET3 (P 5 0.016) and ET4 (P 5 0.012)
(Table 2).
DISCUSSION
The major finding of the present study was that the
repeated longer duration contractions made the tendon
structures more compliant and that the changes in the
elasticity were affected by the duration of action but
not by force production level. Before interpreting the
results obtained, however, we must draw the attention
to the limitations and assumptions of the methodology
followed. To calculate the muscle force, we estimated
moment arm length and relative contribution of VL to
the knee extensor muscles in terms of physiological
cross-sectional areas. The variation in moment arm
length and relative contribution of VL among subjects
might have caused the large variability in the mea-
Fig. 5. The relationship between muscle force
(Fm) and the displacement of P (L) before (h)
and after (l) endurance test. Values are
means 6 SD. In ET1 (A) and ET2 ©, there
were no significant differences in L values
between before and after. In ET3 (B) and ET4
(D), the extent of elongation before tended to
be greater than that after. Significantly
greater than before, P , 0.05.
Table 2. Measured variables before and after endurance tests
MVC, Nm Muscle Thickness, mm Pennation Angle, ° Stiffness, N/mm
Before After Before After Before After Before After
ET1 246651 174650
31.164.3 32.864.5
18.261.2 19.261.1* 58.965.0 55.1610.3
ET2 240642 184638* 31.664.1 33.064.1* 18.461.0 19.561.6* 63.467.7 58.2611.4
ET3 236635 173644* 31.963.5 33.163.2* 18.261.4 19.361.5* 62.668.3 45.165.8*
ET4 244644 171636* 31.363.2 32.963.8* 18.661.2 19.761.1* 64.266.8 47.366.5*
Values are means 6 SD. ET1, 50 repetitions of maximal voluntary eccentric action for 3 s with 3 s of relaxation; ET2, 3 sets of 50 repetitions
of MVC for 3 s with 3 s of relaxation; ET4, 50 repetitions of 50% MVC for 6 s with 6 s of relaxation. *Significantly different from before, P ,
0.05.
280 CHANGE OF TENDON ELASTICITY AFTER MUSCLE CONTRACTIONS
on November 16, 2006 jap.physiology.org Downloaded from
sured parameters. The moment arm length and physiological
cross-sectional areas of respective muscles of
each subject would be necessary for an “accurate” absolute
muscle force determination. In the present
study, however, we aimed to study whether the tendon
properties changed after the repeated muscle contractions.
In addition, there were no significant differences
in the activation levels (iEMG) of knee extensor muscles
before and after the endurance tests (Table 1).
Therefore, we considered that this muscle force calculation
based on these assumptions would be valid to
study the changes of the tendon properties after the
endurance tests. The present results demonstrated
that the repeated longer duration contractions made
the human tendon structures more compliant in vivo.
This agrees with the findings of Vigreux et al. (21),
suggesting that the fatigued muscle is more compliant
than the nonfatigued muscle. However, the extent of
changes observed in the elasticity depended on the
exercise modes performed. Namely, endurance tests
involving either eccentric or rapid isometric muscle
actions with high force production did not induce significant
changes in the elasticity of tendon structures.
Previous studies have shown that exercise involving
high-force eccentric muscle actions can produce temporary
muscle pain and damage (e.g., Ref. 14). In addition,
force production in an explosive exercise such as
jumping can yield the lengthening of tendon structures
in the lower limb (10). At the beginning of the study,
therefore, it was expected that the endurance tests
involving either eccentric actions (ET1) or rapid force
production (ET2) would induce greater changes in the
elasticity compared with the other test conditions.
However, no significant changes in stiffness values
were found after the ET1 and ET2 (Table 2; P . 0.05).
Certainly, the TQ values that developed in the ET1
were significantly greater than those in the other test
conditions. However, the duration in which TQ values
in ET1 were higher than the level achieved in the other
test conditions was relatively short. Similarly, for ET2,
the duration in which the peak value of TQ could be
maintained was very short. On the other hand, the
elongation of tendon structures increased after ET3
and ET4, as characterized by the higher force production-
longer duration and the lower force productionlonger
duration, respectively, compared with ET1 and
ET2. Therefore, it may be assumed that the elasticity
of tendon structures is influenced not by muscle action
mode or force production level but by the duration of
force production.
The mechanisms that change the elasticity of tendon
structures after the repeated longer duration contractions
are unknown. At least for the increased elasticity
observed in the present study, however, an acute
change in the structure of the tendons might be involved.
From the findings of Stromberg and Wiederhielm
(19), the collagen fibers follow a wavelike
course in the unstressed tendons, but they become
aligned or parallel with increasing stress. If a similar
phenomenon occurs in the tendon structures on completion
of the endurance tests used in the present
study, the observed increment in the tendon elongation
might be attributed to an acute change in the arrangement
of collagen fibers. Recently, we showed that the
static stretching of plantar flexors for 10 min made the
tendon structures in the medial gastrocnemius muscle
more compliant (8). Therefore, we considered that the
stretched tendon structures for a given duration (muscle
contraction and/or stretching) would lead to an
acute change in the structure of the tendons. In addition,
these changes might have occurred in the aponeurosis,
because the most elasticity was in the aponeurosis
(4). In any case, further investigations are needed to
clear up this point.
Another possible explanation is the alteration of the
viscoelastic properties of the intramuscular connective
tissue as a result of an actual muscle temperature
increase with contractions. Certainly, it has been
shown in a number of studies that dense connective
tissue, composed primarily of collagen fibers, becomes
more extensible as its temperature is increased within
normal physiological limits (18, 24). Warren et al. (24)
studied the effects of temperature on rat tail tendon
extensibility and concluded that the viscoelastic response
of this tissue increases with temperature increase.
In contrast, Magnusson et al. (12) demonstrated
that 30 min of continuous running elevated
intramuscular temperature significantly but did not
measurably affect the viscoelastic properties of the
hamstring muscle-tendon complex. In the present
study, although no attempts were made to monitor the
temperatures of muscle and tendon, there were no
significant differences in the percent decline of MVC
and increments of MT and PA among the four endurance
tests (Table 2). Therefore, it is likely that the
different changes in tendon structures after four endurance
tests would not be caused by muscle temperature
increases.
Fatigue leads to failure after repeated applications of
stress, which may be much lower than the ultimate
stress. The phenomenon is well known in man-made
materials such as metals and polymers (e.g., Ref. 20).
Recent studies showed that mean extension of wallaby
tail tendons increased slowly during the fatigue test
but much faster just before rupture (17, 23). Wang et
al. (23) implied that this failure would result from
cumulative damage. Some of the changes in tendon
cells (fibroblasts), collagen fibers, and ultrastructure
associated with a response to excessive loading have
recently been documented in various animal models
(e.g., Ref. 26). For example, Zamora and Marini (26)
reported that collagen bundles in the tendon were
disrupted and that empty longitudinal spaces were
observed. They have suggested that the tendon undergoes
a process similar to muscle hypertrophy but that
“remodeling of the tendon architecture may involve a
transient period of mechanical weakness” because of
the observed ultrastructural changes. Therefore, it
seems that the observed increase in L values after
repeated contractions is a phenomenon corresponding
to “a transient period of mechanical weakness” in tendon
structures. If so, the stiffer tendon in endurance
281 CHANGE OF TENDON ELASTICITY AFTER MUSCLE CONTRACTIONS
on November 16, 2006 jap.physiology.org Downloaded from
runners, which was reported in a prior study (6), may
be a result of remodeling of the tendon architecture to
compensate for mechanical weakness. In any case,
longitudinal observations need to clear up this point.
In conclusion, these results suggested that repeated
longer duration contractions would make the tendon
structures more compliant and that the changes in the
elasticity might be affected not by either muscle action
mode or force production level but by the duration of
actions.
REFERENCES

  1. Davies CTM and White MJ. Muscle weakness following eccentric
    work in man. Pflu¨ gers Arch 392: 168–171, 1981.
  2. Friden J, Sjostrom M, and Ekblom B. Myofibrillar damage
    following intense eccentric exercise in man. Int J Sports Med 4:
    170–176, 1983.
  3. Ito M, Kawakami Y, Ichinose Y, Fukashiro S, and Fukunaga
    T. Nonisometric behavior of fascicles during isometric
    contractions of a human muscle. J Appl Physiol 85: 1230–1235,
  4. Kawakami Y and Lieber RL. Interaction between series compliance
    and sarcomere kinetics determines internal sarcomere
    shortening during fixed-end contraction. J Biomech 33: 1249–
    1255, 2000.
  5. Komi PV. Relevance of in vivo force measurements to human
    biomechanics. J Biomech 23, Suppl 1: 23–34, 1990.
  6. Kubo K, Kanehisa H, Kawakami Y, and Fukunaga T. Elastic
    properties of muscle-tendon complex in long distance runners.
    Eur J Appl Physiol 81: 181–187, 2000.
  7. Kubo K, Kanehisa H, Kawakami Y, and Fukunaga T. Elastic
    properties of tendon structures of lower limbs in sprinters.
    Acta Physiol Scand 168: 327–335, 2000.
  8. Kubo K, Kanehisa H, Kawakami Y, and Fukunaga T. Influence
    of static stretching on viscoelastic properties of human
    tendon structures in vivo. J Appl Physiol 90: 520–527, 2001.
  9. Kubo K, Kawakami Y, and Fukunaga T. The influence of
    elastic properties of tendon structures on jump performance in
    humans. J Appl Physiol 87: 2090–2096, 1999.
  10. Kurokawa S, Honglinang Y, Nagareda H, Funato K, and
    Fukunaga T. Muscle fiber behavior of gastrocnemius during
    vertical jumping (Abstract). Proceedings of the XVIth Congress of
    the International Society of Biomechanics Tokyo Japan 1997.
    Tokoyo: Univ of Tokyo, 1997, p. 233.
  11. Maganaris CN and Paul JP. In vivo human tendon mechanical
    properties. J Physiol (Lond) 521: 307–313, 1999.
  12. Magnusson SP, Aagaard P, Larsson B, and Kjaer M. Passive
    energy absorption by human muscle-tendon unit is unaffected
    by increase in intramuscular temperature. J Appl Physiol
    88: 1215–1220, 2000.
  13. Narici MV, Roi GC, Landoni L, Minetti AE, and Cerretelli
    P. Assessment of human knee extensor muscles stress from in
    vivo physiological cross-sectional area and strength measurements.
    Eur J Appl Physiol 65: 438–444, 1992.
  14. Nosaka K and Clarkson PM. Changes in indicators of inflammation
    after eccentric exercise of the elbow flexors. Med Sci
    Sports Exerc 28: 953–961, 1996.
  15. Pousson M, Perot C, and Goubel F. Stiffness changes and
    fibre type transitions in rat soleus muscle produced by jumping
    training. Pflugers Arch 419, 127–130, 1991.
  16. Proske V and Morgan DL. Tendon stiffness: methods of measurement
    and significance for the control of movement. A review.
    J Biomech 20: 75–82, 1987.
  17. Schechtman H and Bader DL. In vitro fatigue of human
    tendons. J Biomech 30: 829–835, 1997.
  18. Strickler T, Malone T, and Garrett WE. The effects of passive
    warming on muscle injury. Am J Sports Med 18: 141–145, 1990.
  19. Stromberg DD and Wiederhielm CA. Viscoelastic description
    of a collagenous tissue in simple elongation. J Appl Physiol 26:
    857–862, 1969.
  20. Takemori MT. Polymer fatigue. Annu Rev Mater Sci 14: 171–
    204, 1984.
  21. Vigreux B, Cnockaert JC, and Pertuzon E. Effects of fatigue
    on the series elastic component of human muscle. Eur J Appl
    Physiol 45: 11–17, 1980.
  22. Visser JJ, Hoogkamer JE, Bobbert MF, and Huijing PA.
    Length and moment arm of human leg muscles as a function of
    knee and hip-joint angles. Eur J Appl Physiol 61: 453–460, 1990.
  23. Wang XT, Ker R, and Alexander RM. Fatigue rupture of
    wallaby tail tendons. J Exp Biol 198: 847–852, 1995.
  24. Warren CG, Lehmann JF, and Koblanski HN. Elongation of
    rat tail tendon: effects of load and temperature. Arch Phys Med
    Rehabil 51: 465–474, 1971.
  25. Woo SL, Gomez MA, Amiel D, Ritter MA, Gelberman RH,
    and Akeson WH. The effects of exercise on the biomechanical
    and biochemical properties of swine digital flexor tendons. J Biomech
    Eng 103: 51–56, 1981.
  26. Zamora AJ and Marini JF. Tendon and myo-tendinous junction
    in an overloaded skeletal muscle of the rat. Anat Embryol
    (Berl) 179: 89–96, 1988.
  27. Zhou SM, McKenna J, Lawson DL, Morrison WE, and
    Fairweather I. Effects of fatigue and sprint training on electromechanical
    delay of knee

Effect of stretching training on the viscoelastic properties of human tendon structures in vivo
Keitaro Kubo, Hiroaki Kanehisa, and Tetsuo Fukunaga
Department of Life Science (Sports Sciences), University of Tokyo, Komaba 3-8-1, Meguro, Tokyo 153-8902, Japan

ABSTRACT 

TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The purpose of this study was to examine whether stretching training altered the viscoelastic properties of human tendon structures in vivo. Eight men performed the stretching training for 3 wk. Before and after the stretching training, the elongation of the tendon and aponeurosis of medial gastrocnemius muscle was directly measured by ultrasonography while the subjects performed ramp isometric plantar flexion up to the voluntary maximum, followed by a ramp relaxation. The relationship between the estimated muscle force (Fm) and tendon elongation (L) during the ascending phase was fitted to a linear regression, the slope of which was defined as stiffness of tendon structures. The percentage of the area within the Fm-L loop to the area beneath the curve during ascending phase was calculated as an index representing hysteresis. To assess the flexibility, the passive torque of the plantar flexor muscles was measured during the passive stretch from 0° (anatomic position) to 25° of dorsiflexion with a constant velocity of 5°/s. The slope of the linear portion of the passive torque-angle curve during stretching was defined as flexibility index. Flexibility index decreased significantly after stretching training (13.4 ± 4.6%). On the other hand, the stretching training produced no significant change in stiffness but significantly decreased hysteresis from 19.9 ± 11.7 to 12.5 ± 9.5%. The present results suggested that stretching training affected the viscosity of tendon structures but not the elasticity.

passive torque-angle curve; stiffness; hysteresis; ultrasonography; stretch

INTRODUCTION 

TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
THE USE OF STRETCHING EXERCISES to improve flexibility is a widespread practice among competitive and recreational athletes. Numerous stretching studies employing this test have documented increases in the maximal joint range of motion after stretching exercises (5, 14, 26). However, the findings obtained by the technique could be affected by factors such as a raised muscle pain threshold. Alternatively, Toft et al. (20) pointed out that the passive tension measurements would be more objective than the range of motion measurements, because psychological factors did not interfere with results. They found a 36% decrease in passive tension of plantar flexors after a 3-wk stretching program. However, the mechanisms for the acute and chronic changes in joint range of motion and/or passive tension remain ambiguous.

It is widely conjectured that increasing flexibility will promote better performances during various movements (1, 26). For example, Wilson et al. (26), who applied a damped oscillation technique to determine the stiffness of the upper limbs, showed that the rebound bench press performance enhancement observed consequent to flexibility training was caused by a reduction in stiffness of muscle-tendon units, increasing the utilization of elastic strain energy during the rebound bench press lift. Inversely, Rosenbaum and Henning (17) observed reductions of the rate of force development and electromyograph (EMG) amplitudes, and an increase in EMG latencies, after static stretching of the triceps surae. Taken together, these previous results would indicate that the stretching training made the viscoelastic properties of tendon structures change. However, no attempt has been made to investigate the influences of stretching on the properties of human tendon structures in vivo.

Recent reports have shown that ultrasonography can be used to determine the stiffness and hysteresis of human tendon structures in vivo (10, 11, 13). Furthermore, our laboratory showed that the static stretching of plantar flexors for 10 min significantly decreased the stiffness and hysteresis of tendon structures in medial gastrocnemius (MG) muscle (10). Hence, we applied this technique to determine the magnitude of elongation in the tendon structure of human MG muscle before and after static stretching training for 3 wk. The purpose of the present study was to investigate the effects of static stretching training for 3 wk on the viscoelastic properties (stiffness and hysteresis) of human tendon structures in vivo. A brief account of this work has been presented previously in abstract form (8).

METHODS 

TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
Subjects. Eight healthy men [age 24.6 ± 1.8 (SD) yr, height 173.0 ± 7.1 cm, weight 75.4 ± 14.6 kg] participated as subjects. When the data were collected, the subjects had been participating in recreational sports but did not have any experience in strength training or flexibility training programs. The subjects were fully informed of the procedures to be utilized as well as the purpose of this study. Written informed consent was obtained from all subjects. This study was approved by the office of Department of Sports Sciences, University of Tokyo, and complied with their requirements for human experimentation.

Measurement of EMG. EMG activity was recorded during the ramp isometric contraction (measurement of tendon properties) and passive stretch (measurement of flexibility). Bipolar surface electrodes (5 mm in diameter) were placed over the bellies of MG, lateral gastrocnemius, soleus, and tibial anterior (TA) with a constant interelectrode distance of 25 mm. The positions of the electrodes were marked on the skin by small ink dots. These stained dots ensured the same electrode positioning in each test during the experimental period. EMG signals were transmitted to a computer (Macintosh Performa 630, Apple) at a sampling rate of 1 kHz. EMG was full-wave rectified and integrated for the duration of the contraction and passive stretch to give integrated EMG (iEMG).

Measurement of flexibility. To assess flexibility, the joint angle and the passive torque were measured during a passive stretch of the triceps surae muscles. The subject lay prone on a test bench, and the waist and shoulders were secured by adjustable lap belts and held in position. The subjects did not warm up before the stretch maneuver. The right ankle joint was set at 0° (anatomic position) with the knee joint at full extension, and the foot was securely strapped to a footplate connected to the lever arm of the dynamometer (Myoret, Asics). The platform of the dynamometer, which was attached to the sole of the subject’s foot, was moved to 25° of dorsiflexion with a constant velocity of 5°/s. The passive torque (Nm) during the stretching was detected by the dynamometer. Throughout the stretching, the subjects were requested to relax completely and not offer any voluntary resistance. The passive torque, joint angle, and EMG of triceps surae muscles were continuously recorded over the entire range of stretch maneuvers. The slope of the portion of the passive torque-angle curve from 15 to 25° was defined as flexibility index.

Measurement of viscoelastic properties of tendon structures. Tendon structures behave as a nonlinear viscoelastic structure. The constant slope is supposed to represent stiffness of the collagenous material from which the tendon is constructed. In this study, “elasticity” is defined as the stiffness (see below). On the other hand, the loading and unloading curves during cyclic tensile test produce a loop (hysteresis). In this study, we will use the term “viscosity” to refer to the hysteresis.

The posture of the subject and setup were similar to that for the measurement of flexibility as described above. The right ankle joint was set at 0° anatomic position. Before the test, the subject performed a standardized warm-up and submaximal contractions to become accustomed to the test procedure. The subject was instructed to develop a gradually increasing force from relaxation to maximal voluntary contraction (MVC) within 5 s, followed by a gradual relaxation within 5 s. The task was repeated two times per subject with at least 3 min between trials. Torque signals were analog-to-digital converted at a sampling rate of 1 kHz (MacLab/8, type ML780, AD Instrument) and analyzed by a personal computer (Performa 630, Macintosh). The measured values that are shown below are the means of two trials.

A real-time ultrasonic apparatus (SSD-2000, Aloka) was used to obtain a longitudinal ultrasonic image of MG at the level of 30% of the lower leg length, i.e., from the popliteal crease to the center of the lateral malleolus. The ultrasonic images were recorded on videotape at 30 Hz, synchronized with recordings of a clock timer for subsequent analyses. The tester visually confirmed the echoes from the aponeurosis and MG fascicles. The point at which one fascicle was attached to the aponeurosis § was visualized on the ultrasonic image. P moved proximally during isometric torque development up to maximum (Fig. 1). A marker (X) was placed between the skin and the ultrasonic probe as the landmark to confirm that the probe did not move during measurements. The cross-point § between superficial aponeurosis and fascicles did not move. Therefore, the displacement of P (L) is considered to indicate the lengthening of the deep aponeurosis and the distal tendon (10, 11).

View larger version (64K):
[in this window]
[in a new window]
Fig. 1. Ultrasonic images of longitudinal sections of medial gastrocnemius (MG) muscle isometric contraction. A marker (X) was placed between the skin and the ultrasonic probe as the landmark to confirm that the probe did not move during measurements. The cross-point § between superficial aponeurosis and fascicles did not move. P was determined from the echoes of the deep aponeurosis and fascicles. P moved proximally during isometric torque development from rest (P1; A) to 50% maximal voluntary contraction (MVC) (P2; B). The distance traveled by P (L) was defined as the length change of tendon and aponeurosis during contraction. Sol, soleus.

The measured torque (TQ) during isometric plantar flexion was converted to muscle force (Fm) by the following equation

where k is the relative contribution of the physiological cross-sectional area of MG within plantar flexor muscles (3) and MA is the moment arm length of triceps surae muscles at 0° of ankle joint, which was estimated from the lower leg length of each subject as described by Visser et al. (22).

As reported in previous studies using animal and human cadavers (e.g., Ref. 27), the Fm-L relation in the tendon structure was curvilinear, consisting of an initial region (toe region) characterized by a large increase in L with increasing force and a linear region immediately after the toe region. In the present study, therefore, the Fm and L values above 50% of MVC were fitted to a linear regression equation, the slope of which was adopted as stiffness (10, 11).

The Fm-L curves during the ascending and descending phases of force development produced a loop. In the present study, the area of each of the curves under both the ascending and descending phases was calculated. Then, the ratio of the area within the Fm-L loop (elastic energy dissipated) to the area beneath the curve during ascending phase (elastic energy input) was calculated as hysteresis (10).

The test-retest correlation coefficient was 0.90 for stiffness and 0.86 for hysteresis. The coefficient of variation was 5% for stiffness and 11% for hysteresis.

Static stretching training. The subjects were randomly assigned to stretch the plantar flexor muscles on one leg while the opposite side served as a control. Two sessions, one in the morning and one in the afternoon, were performed on a daily basis for 20 consecutive days. This duration was chosen because previous research had demonstrated significant flexibility improvements within this training period (6, 23). Each session consisted of five stretches for 45 s with a 15-s rest in between. The stretch maneuver was performed at 35° of dorsiflexion with the ankle joint in the standing position with the stretch leg in a straight position and hip in neutral rotation (Fig. 2). The subjects filled out a form on a daily basis to register compliance. They were instructed not to initiate any new forms of training. The subjects did not perform any stretch training on the day of test.

View larger version (19K):
[in this window]
[in a new window]
Fig. 2. Schematic representation of setup of static stretching training. The stretch maneuver was performed at 35° of dorsiflexion with the ankle joint in the standing position. Two sessions, one in the morning and one in the afternoon, were performed on a daily basis for 20 consecutive days.

Statistics. Descriptive data included means ± SD. A two-way ANOVA [2 (groups) × 2 (test times)] was used to analyze the data. The F ratio for main effects and interactions was considered significant at P < 0.05. Significant differences among means at P < 0.05 were detected by using post hoc test.

RESULTS 

TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
During the stretching, EMG activities of all the muscles tested were very small (<1% of MVC), which confirmed the lack of contribution from the contractile component to the measured resistance to stretch. The relationship between passive torque and ankle joint angle during the passive stretch is shown in Fig. 3. In the control side, there were no significant differences in the passive torque values at any ankle angles. For the trained side, the passive torque values at all ankle angles decreased significantly after the stretching training. The flexibility index value decreased significantly from 1.43 ± 0.33 to 1.24 ± 0.30 Nm/° (13.4 ± 4.6%; P = 0.007).

View larger version (12K):
[in this window]
[in a new window]
Fig. 3. Relationship between passive torque and ankle joint angle during the passive stretch of the triceps surae muscle in the trained (A) and control (B) side. Values are means ± SD. Passive torque values at all ankle angles decreased significantly after the stretching training. Furthermore, flexibility index decreased significantly after training. *Significantly lower than before, P < 0.05.

Figure 4 shows the relationships between Fm and L. In the control and trained sides, there were no significant differences in L values at any force levels, and no significant changes in MVC and stiffness were found. For the trained side, on the other hand, the %MVC-L loop became significantly smaller after stretching training (Fig. 5). The measured viscoelastic parameters are shown in Table 1. The stretching training produced no significant change in stiffness (P = 0.621) but significantly decreased hysteresis (37.2 ± 22.2%, P = 0.009). In addition, there were no significant differences in the activation levels (iEMG) of each plantar flexor muscle before and after training (Table 2). Furthermore, we also confirmed that little cocontraction of the dorsiflexor muscle (TA) occurred during plantar flexion.

View larger version (13K):
[in this window]
[in a new window]
Fig. 4. Relationships between muscle force (Fm) and L in the trained (A) and control (B) side. Values are means ± SD. For both sides, there were no significant differences in L values at any force levels.

View larger version (13K):
[in this window]
[in a new window]
Fig. 5. %MVC-L curves during ascending and descending phase produced a loop (hysteresis). Values are means ± SD. In the trained side, the hysteresis was significantly smaller after (B) than before (A). Data for the control side are not shown.

View this table:
[in this window]
[in a new window]
Table 1. Measured variables before and after stretching training

View this table:
[in this window]
[in a new window]
Table 2. iEMG values during ramp isometric contraction

DISCUSSION 

TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
Before interpreting the results obtained, however, we must draw attention to the limitations and assumptions of the methodology followed. To calculate Fm, we estimated moment arm length and relative contribution of MG to the plantar flexor muscles in terms of physiological cross-sectional areas. The variation in moment arm length and relative contribution of MG among subjects might have caused the large variability in the measured parameters. Moment arm length and physiological cross-sectional areas of respective muscles of each subject would be necessary for an “accurate” absolute muscle force determination. In the present study, however, we aimed to study whether the tendon properties changed after the stretching training. In addition, there were no significant differences in the activation levels (iEMG) of each triceps surae muscles before and after stretching training (Table 2). We also confirmed that little cocontraction of dorsiflexor muscle (TA) occurred during plantar flexion (Table 2). Therefore, we considered that this muscle force calculation, based on these assumptions, would be valid to study the changes of the tendon properties after the stretching training.

In any human isometric tests, the joint angle has been assumed to be constant without the joint angle being directly monitored. Thus, because isometric contraction of muscle about a joint will produce more or less angular joint rotation in the direction of the intended movement, the resulting tendon and aponeurosis displacement is the result of displacement attributed to both joint angular rotation and contractile tensile loading. Magnusson et al. (13) demonstrated the importance of accounting for even small amounts of joint motion: despite a rigid frame that was adjusted separately for each subject, the average plantar flexion motion was 3.6°, which resulted in an overestimation of the displacement by up to ~30%. However, it seems reasonable to suppose that there was no difference in this kind of error between before and after stretching training. In the present study, therefore, we may say that a little overestimation of the displacement in the ankle joint would not affect the present result.

Many previous studies have demonstrated that the maximum range of motion, i.e., flexibility, increased after the stretching training (5, 14, 26). Alternatively, Toft et al. (20) reported that the passive torque of ankle joint decreased after the stretching training for 3 wk. They suggested that the passive torque measurements would be more objective than the range of motion measurements, because psychological factors did not interfere with results. In the present study, therefore, we adopted the passive torque measurements for assessing the flexibility, instead of the measurements of maximum range of motion. The present result showed that flexibility index value decreased significantly after the stretching training (13.4%). Similarly, the flexibility increase observed in response to the stretching program was within the 11.1-24.6% increase in flexibility of a number of lower body muscle groups, as reported by Wallin et al. (23). Furthermore, in the present study, because during passive dorsiflexion the EMG amplitude was below 1% of MVC (data not shown), it is unlikely that muscle activity contributed significantly to passive torque. Therefore, it is obvious that the static stretching training of ankle joint for 3 wk increases the flexibility of plantar flexor muscles.

There are many sources of the passive torque during passive stretch test: the joint capsule, movement and extension of ligament, synovial fluid movement, and elongation of the connective tissue within the muscle belly. Several researchers have suggested that the major contributors to passive tension are the extensibility of the connective tissue elements in parallel with the muscle fibers, i.e., parallel elastic component (7, 12, 15). The passive tension is influenced by a lengthening deformation of the connective tissues of the endomysium, perimysium, and epimysium of the muscle belly (4). Although all three components of the connective tissues that package the muscle belly contribute to the resistance when a muscle is passively stretched, the relatively large amount of perimysium is considered the tissue that is the major contributor to extracellular passive resistance to stretch (16). From the findings of Purslow (16), the perimysial collagen network, referring to as the parallel elastic component, played a role to prevent overstretching of the muscle fiber bundles. Therefore, the present result implies that the stretching training does not affect the elasticity of tendon structures, i.e., series elastic component, but does affect that of the connective tissue elements in parallel with the muscle fibers, i.e., parallel elastic component.

Recently, our laboratory showed that the static stretching of plantar flexors for 10 min made the tendon structures in the MG muscle more compliant (10). Therefore, it is possible to substantiate the hypothesis that the stretching training alters the stiffness of tendon structures. In the present study, however, no significant change in stiffness of tendon structures was found after the stretching training. Magnusson et al. (13) demonstrated that repetitive static stretches in human skeletal muscle, each lasting 90 s, yielded an immediate decrease in passive tension but that the tension returned to baseline within 1 h. Our laboratory also reported the acute change in stiffness after the static stretching, but this change was relatively small (8.9%; Ref. 10). Furthermore, we observed that flexibility index was unrelated to the stiffness of tendon structures (9). Considering these findings, it seems reasonable to suppose that the stretching training increases the flexibility but not the elasticity of tendon structures.

Many previous studies on the effect of stretching exercise on the properties of muscle and tendon have been limited to animal studies (18, 19, 21, 24). For example, Viidik (21) reported that stretching the tail tendon of the rat increased its compliance. Recent studies showed that mean extension of wallaby tail tendons increased slowly during the fatigue test but much faster just before rupture (24). The force-length relation in the tendon structure is curvilinear, consisting of an initial region (toe region) characterized by a large increase in the length with increasing force and a linear region immediately after the toe region (27). The toe region has been assumed to be due to a structural change in collagen fiber organization from a crimpy or wavy pattern to a more straightened, parallel arrangement (21). The crimp gives rise to the toe region of the length-tension relation of tendons (21). From the findings of Stromberg and Wiederhielm (18), the collagen fibers follow a wavelike course in the unstressed tendons, but they become aligned or parallel with increasing stress. These studies, which have attempted to establish the influence of stretching on the tendon properties, have mainly investigated the effects of “acute” stretching programs rather than “long-term or chronic” stretching.

In the present study, the hysteresis of tendon structures decreased significantly after the stretching training. Also, we observed an acute decrease in the hysteresis of tendon structures after 10 min of static stretching (10). Frisen et al. (2) and Viidik (21) also showed that repeated cyclic stretches of rat tendons decreased hysteresis, suggesting a reduction of energy dissipation in the tissues after stretching. The mechanisms, which resulted in the decreases of hysteresis after acute and long-term stretching, are unknown. At least for the lowered hysteresis observed in the present study, a change in the structure of the tendons might be involved. However, future work is needed to clarify this phenomenon.

The hysteresis, i.e., the area within the loop, represents the energy loss as heat due to internal damping, whereas the area under the unloaded curve is the energy recovered in the elastic recoil. Hence, the hysteresis of tendon structures should be taken into account when estimating the dynamics of the muscle-tendon complex during human movements. For example, the value of 20% obtained in our measurements (before stretching training) would be representative of the percent energy dissipated as heat in loading-unloading cycles of the tendon during several everyday-life activities. As a result of observations on human in vivo, Wilson et al. (26) reported that flexibility training for the upper limbs induced a significant increase in work during the initial concentric portion of the rebound bench press lift. Also, Dintiman (1) found that the sprint performance was improved when a stretching regimen was included with regular sprint training. These led us to speculate that stretching may be an effective way to increase reused energy during exercise involving a stretch-shortening cycle, by reducing the hysteresis.

In conclusion, the stretching training produced no significant change in stiffness of tendon structures, but it significantly decreased hysteresis. The present results suggested that the static stretching training affected the viscosity of tendon structures but not the elasticity. However, we have no definite information on how the changes induced by stretching training in tendon properties are correlated to performances during stretch-shortening cycle exercises. Further investigations are needed to clear up this point.

FOOTNOTES 

Address for reprint requests and other correspondence: K. Kubo, Dept. of Life Science (Sports Sciences), Univ. of Tokyo, Komaba 3-8-1, Meguro-ku, Tokyo 153-8902, Japan (E-mail: kubo@idaten.c.u-tokyo.ac.jp).

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.

10.1152/japplphysiol.00658.2001

Received 26 June 2001; accepted in final form 25 September 2001.

REFERENCES 

TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

  1. Dintiman, GB. Effects of various training programs on running speed. Res Q 35: 456-463, 1964[ISI][Medline].

  2. Frisen, M, Magi M, Sonnerup L, and Viidik A. Rheological analysis of soft collagenous tissue. Part I. Theoretical consideration. J Biomech 2: 13-20, 1969[ISI].

  3. Fukunaga, T, Roy RR, Shellock FG, Hodgson JA, and Edgerton VR. Specific tension of human plantar flexors and dorsiflexors. J Appl Physiol 80: 158-165, 1996[Abstract/Free Full Text].

  4. Gajdosik, RL. Passive extensibility of skeletal muscle: review of the literature with clinical implications. Clin Biomech (Bristol, Avon) 16: 87-101, 2001[Medline].

  5. Halbertsma, JP, and Goeken LN. Stretching exercises: effect on passive extensibility and stiffness in short hamstrings on healthy subjects. Arch Phys Med Rehabil 75: 976-981, 1994[ISI][Medline].

  6. Hortobagyi, T, Faludi J, Tihanyi J, and Merkely B. Effects of intense stretching flexibility training on the mechanical profile of the knee extensors and on the range of motion of the hip joint. Int J Sports Med 6: 317-321, 1985[ISI][Medline].

  7. Jewell, BR, and Wilkie DR. An analysis of the mechanical components in frog’s striated muscle. J Physiol (Lond) 143: 515-540, 1958[ISI].

  8. Kubo, K, Kanehisa H, and Fukunaga T. Effect of stretching training on the viscoelastic properties of human tendon structures in vivo (Abstract). J Ultrasound Med 20: 128, 2001.

  9. Kubo, K, Kanehisa H, and Fukunaga T. Is passive stiffness related to the elasticity of tendon structures? Eur J Appl Physiol 85: 226-232, 2001[ISI][Medline].

  10. Kubo, K, Kanehisa H, Kawakami Y, and Fukunaga T. Influence of static stretching on viscoelastic properties of human tendon structures in vivo. J Appl Physiol 90: 511-519, 2001[Abstract/Free Full Text].

  11. Kubo, K, Kawakami Y, and Fukunaga T. Influence of elastic properties of tendon structures on jump performance in humans. J Appl Physiol 87: 2090-2096, 1999[Abstract/Free Full Text].

  12. Latash, ML, and Zatsiorsky VM. Joint stiffness: myth or reality? Hum Mov Sci 12: 653-692, 1993[ISI].

  13. Magnusson, SP, Aagaard P, Rosager S, Dyhre-Poulsen P, and Kjaer M. Load-displacement properties of human triceps surae aponeurosis in vivo. J Physiol (Lond) 531: 277-288, 2001[Abstract/Free Full Text].

  14. Magnusson, SP, Simonsen EB, Aagaard P, Sorensen H, and Kjaer M. A mechanism for altered flexibility in human skeletal muscle. J Physiol (Lond) 497: 291-298, 1996[Abstract].

  15. McHugh, MP, Kremenic IJ, Fox MB, and Glem GW. The role of mechanical and neural restraints to joint range of motion during passive stretch. Med Sci Sports Exerc 30: 928-932, 1998[ISI][Medline].

  16. Purslow, PP. Strain-induced reorientation of an intramuscular connective tissue network: implications for passive muscle elasticity. J Biomech 22: 21-31, 1989[ISI][Medline].

  17. Rosenbaum, D, and Henning EM. The influence of stretching and warm-up exercises on Achilles tendon reflex activity. J Sports Sci 13: 481-490, 1995[Medline].

  18. Stromberg, DD, and Wiederhielm CA. Viscoelastic description of a collagenous tissue in simple elongation. J Appl Physiol 26: 857-862, 1969[Free Full Text].

  19. Taylor, DC, Dalton JD, Seaber AV, and Garrett WE. Viscoelastic properties of muscle-tendon units. The biomechanical effects of stretching. Am J Sports Med 18: 300-309, 1990[Abstract].

  20. Toft, E, Espersn GT, Kalund S, Sinkjaer T, and Hornemann BC. Passive tension of the ankle before and after stretching. Am J Sports Med 17: 489-494, 1989[Abstract].

  21. Viidik, A. Simultaneous mechanical and light microscopic studies of collagen fibers. Z Anat Entwicklungsgesch 136: 204-212, 1972[ISI][Medline].

  22. Visser, JJ, Hoogkamer JE, Bobbert MF, and Huijing PA. Length and moment arm of human leg muscles as a function of knee and hip-joint angles. Eur J Appl Physiol 61: 453-460, 1990.

  23. Wallin, D, Ekblom B, Grahn R, and Nordenborg T. Improvement of muscle flexibility: a comparison between two techniques. Am J Sports Med 13: 263-268, 1985[Abstract].

  24. Wang, XT, Ker R, and Alexander RM. Fatigue rupture of wallaby tail tendons. J Exp Biol 198: 847-852, 1995[Abstract/Free Full Text].

  25. Wiemann, K, and Hahn K. Influences of strength, stretching, and circulatory exercises on flexibility parameters of human hamstrings. Int J Sports Med 18: 340-346, 1996[ISI].

  26. Wilson, GJ, Elliott BC, and Wood GA. Stretch shorten cycle performance enhancement through flexibility training. Med Sci Sports Exerc 24: 116-123, 1992[ISI][Medline].

  27. Woo, SL, Gomez MA, Amiel D, Ritter MA, Gelberman RH, and Akeson WH. The effects of exercise on the biomechanical and biochemical properties of swine digital flexor tendons. J Biomech Eng 103: 51-56, 1981[ISI][Medline].