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Effects of therapeutic ultrasound associated with static stretching on longitudinal histomorphometric parameters of immobilized soleus of rats

Elisangela Lourdes Artifon Deisi Ferrari Daniela Martins Cunha Cassiane Merigo Nascimento Lucinéia de Fátima Chasko Ribeiro Gladson Ricardo Flor Bertolini About the authors

Abstracts

O músculo é um tecido dotado de plasticidade que se adapta a diferentes estímulos. A imobilização causa danos ao sistema muscular incluindo atrofia, perda da extensibilidade e resistência muscular. O alongamento muscular e o ultrassom terapêutico são modalidades utilizadas para acelerar o processo de reparo muscular, provendo aumento da síntese proteica e melhora da extensibilidade. OBJETIVO: Comparar o uso do ultrassom terapêutico, associado ao alongamento, na remobilização de músculo sóleo, de ratos, submetido ao encurtamento muscular, sobre os aspectos histomorfométricos longitudinais. MATERIAIS E MÉTODOS: Vinte e oito ratos Wistar foram imobilizados por 15 dias e, após liberados do aparato de imobilização, distribuídos em quatro grupos: grupo (GA) apenas remobilizado por alongamento durante 10 dias; e os demais foram submetidos a 10 dias de intervenção terapêutica do ultrassom de 1MHz a 1,0W/cm² (GAUS 1,0); 0,5W/cm² (GAUS 0,5); e 0,2W/cm² (GAUS 0,2), e posterior alongamento dos músculos sóleos. Ao final do tratamento, os animais foram eutanasiados e tiveram seus músculos removidos para posterior análise histológica dos parâmetros longitudinais (contagem de sarcômeros). RESULTADOS: Na análise intragrupo, quanto ao comprimento muscular, apenas o grupo GAUS 0,5 não teve diferença significativa. Quanto à contagem de sarcômeros, os grupos GA e GAUS 0,2 tiveram diferença significativa. Quanto ao tamanho dos sarcômeros, nenhum grupo teve diferença significativa. Na análise intergrupos, nenhum grupo apresentou diferença significativa. CONCLUSÃO: O alongamento foi insuficiente para reverter os efeitos da imobilização. Quando associado ao ultrassom terapêutico, a dose 0,5W/cm² recuperou o comprimento muscular, e as doses 1,0 e 0,5W/cm² contribuíram para o aumento da quantidade dos sarcômeros em série.

imobilização; alongamento passivo; músculo esquelético; sarcômeros


The muscle tissue is endowed with plasticity that adapts to different stimuli. Immobilization causes damage to the musculature including atrophy, loss of muscle strength and extensibility. The stretching and ultrasound treatment modalities are used to speed up muscle repair process as they can increase protein synthesis and improve extensibility. OBJECTIVE: To compare the use of therapeutic thermal and non thermal ultrasound, associated with stretching, in the remobilization of the soleus muscle of rats subjected to position of muscle shortening on aspects histomorphometric longitudinal muscle.} METHODS: 28 rats were immobilized for 15 days, later released from the apparatus and divided into four groups: group AG only remobilized by stretching for 10 days and the others were subjected to 10 days of therapeutic intervention 1MHz of ultrasound at 1.0W/cm² (GAUS 1.0), 0.5W/cm² (GAUS 0.5), and 0.2 W/cm² (GAUS 0.2), and further stretching to the soleus. At the end of treatment, the animals were sacrificed and their soleus muscles were removed for later histological analysis of longitudinal parameters (count of sarcomeres). RESULTS: At intragroup analysis on the muscle length, only the group GAUS 0.5 did not present significant difference. The count of sarcomeres in the groups GA and GAUS 0.2 was statistically different. The size of the sarcomeres in both groups had no statistically significant difference. In inter-group analysis both groups had no statistically significant difference for any of the variables. CONCLUSION: The stretching was insufficient to reverse the effects of immobilization. When associated with therapeutic ultrasound, the dose 0.5 W/cm² recovered muscle length significantly, and the doses 1.0 and 0.5 W/cm² contributed to the significant increase of the number of sarcomeres in immobilized muscles.

immobilization; passive stretching; skeletal muscle; sarcomeres


ORIGINAL ARTICLE

EXERCISE AND SPORTS SCIENCES

Effects of therapeutic ultrasound associated with static stretching on longitudinal histomorphometric parameters of immobilized soleus of rats

Elisangela Lourdes ArtifonI,II; Deisi FerrariI; Daniela Martins CunhaI; Cassiane Merigo NascimentoI; Lucinéia de Fátima Chasko RibeiroIII; Gladson Ricardo Flor BertoliniI

ILaboratory of Studies of Injuries and Physioterapeutic Resources of the State University of Western Paraná (Unioeste) – Cascavel Campus

IIGrant recipiente PIBIC/CNPq/Unioeste

IIICenter of Medical and Pharmaceutical Research – Unioeste – Cascavel Campus

Mailing address

ABSTRACT

The muscle tissue is endowed with plasticity that adapts to different stimuli. Immobilization causes damage to the musculature including atrophy, loss of muscle strength and extensibility. The stretching and ultrasound treatment modalities are used to speed up muscle repair process as they can increase protein synthesis and improve extensibility.

OBJECTIVE: To compare the use of therapeutic thermal and non thermal ultrasound, associated with stretching, in the remobilization of the soleus muscle of rats subjected to position of muscle shortening on aspects histomorphometric longitudinal muscle.

METHODS: 28 rats were immobilized for 15 days, later released from the apparatus and divided into four groups: group AG only remobilized by stretching for 10 days and the others were subjected to 10 days of therapeutic intervention 1MHz of ultrasound at 1.0W/cm² (GAUS 1.0), 0.5W/cm² (GAUS 0.5), and 0.2 W/cm² (GAUS 0.2), and further stretching to the soleus. At the end of treatment, the animals were sacrificed and their soleus muscles were removed for later histological analysis of longitudinal parameters (count of sarcomeres).

RESULTS: At intragroup analysis on the muscle length, only the group GAUS 0.5 did not present significant difference. The count of sarcomeres in the groups GA and GAUS 0.2 was statistically different. The size of the sarcomeres in both groups had no statistically significant difference. In inter-group analysis both groups had no statistically significant difference for any of the variables.

CONCLUSION: The stretching was insufficient to reverse the effects of immobilization. When associated with therapeutic ultrasound, the dose 0.5 W/cm² recovered muscle length significantly, and the doses 1.0 and 0.5 W/cm² contributed to the significant increase of the number of sarcomeres in immobilized muscles.

Keywords: immobilization, passive stretching, skeletal muscle, sarcomeres.

INTRODUCTION

Although immobilization has been a widely used resource for rehabilitation of injuries, it leads to many deleterious consequences to the musculoskeletal system1. A short immobilization period (seven days) is already enough for the muscle to suffer morphometric and mechanical adaptations, such as reduction of muscular mass and length, number of sarcomeres, increase of the conjunctive tissue density and reduction of the maximum resistance of muscular rupture2-4. Increase of conjunctive tissue induces to abnormal crossed ligations of conjunctive tissue fibers, which results in fast muscular stiffness and reduction of range of motion1,5.

Stretching prevents muscular atrophy, proliferation of conjunctive tissue and loss of sarcomeres in series, besides the possibility of activating the protein synthesis and inducing muscular hypertrophy and hyperplasia1. Some authors state that passive stretching with time of 30 seconds is sufficient to obtain greater mobility, while other authors did not find any effect6. Muscular stretching promotes accumulation of slow oxidative RNAm myosin in the fibers termination which help in the synthesis of contractile proteins, in the fast sarcomere union as well as extension of the myofibrils. In special, a large citoplasmatic space containing polysomes opens between the myofibrils and the sarcolema of the myotendineous junction of elongated fibers and many myofibrils are found7.

The therapeutic ultrasound (TUS) is a resource commonly applied in the disorders of the musculoskeletal system, as well as in the speeding of tissue repair of muscular injuries, increase of cellular proliferation and protein synthesis during healing, besides having effect in the blood circulation. This resource makes use of high-frequency sound waves to deeply penetrate soft tissues8-10. The possibility of using different frequencies between 1 and 3MHz is an important measure, since the higher frequencies (3MHz) are more intensely absorbed , becoming more specific for the treatment of superficial tissues, while lower frequencies (1MHz) penetrate more deeply and hence should be used for the deeper tissues10.

The ultrasound effects are classified in termal and non-thermal. Ter Haar11,12 reports that, among the non-thermal effects of ultrasound, as the mechanical waves of the ultrasound go through the tissues, they cause molecules agitation, which provides greater permeability of the tissue membranes, enabling hence better exchange of its nutrients and catabolites removal. Moreover, the ultrasound non-thermal effects (mechanical) improve the cellular metabolism, besides aiding in the release of adherences, by the separation of the collagen fibers13. Concerning the thermal effects, the tissues are warmed up, which provides countless physiological benefits, especially increase in the blood flow in the area to be treated, increase of the collagen extensibility, decrease of articular stiffness, pain relief and decrease of muscular spasms11,12.

In physiotherapeutic clinical practice, ultrasound and stretching are resources widely used; however, many times we do not know the real effects in cellular level of these modalities, in this case, over the muscular fiber. Considering this fact and the deleterious effects of immobilization on the muscular fibers, it is important to understand their implications in the recovery of the shortened muscle, so that this information can be transferred to the clinical practice.

Thus, the aim of this study was to verify and compare the use of stretching, associated or not to use of therapeutic ultrasound, thermal or non-thermal, in the remobilization of the soleus muscle of rats submitted to muscular shortening position, concerning the longitudinal histomorphometric aspects of these muscles.

MATERIALS AND METHODS

28 albine male Wistar rats with 10 ± 2 weeks of age, obtained in the Central Animal Facility of the State University of Western Paraná (Unioeste) were used. The study was conducted according to the International Guidelines of Ethics in Animal Experimentation14 and was approved by the Ethics Committee of Animal Studies of the Unioeste. The animals were sorted and kept in polypropylene cages under controlled environmental conditions, with light/dark cycle of 12 hours, with temperature of 23ºC ± 2ºC and water and food ad libitum.

All animals had the right hinder limb immobilized in maximum plantar flexion, for 15 consecutive days, and were subsequently randomly sorted in four groups with seven animals each for the therapeutic intervention:

GS (Group Stretching): in which, after the immobilization period, the animals were submitted to the static stretching protocol of soleus muscle;

GSUS 1.0 (Group Stretching and TUS of 1.0W/cm2): group in which the animals were submitted to the treatment protocol with TUS and immediately after the static stretching protocol;

GSUS 0.5 (Group Stretching and TUS of 0.5W/cm2): similar to the previous group, but with 0.5W/cm2 dose;

GSUS 0.2 (Group Stretching and TUS of 0.2W/cm2): similar to the previous groups, but with therapeutic dose of 0.2W/cm2.

Immobilization protocol

In this study, the immobilization apparatus chosen was the model developed by Coutinho et al.15, which aims to obtain shortening of the soleus muscle. Therefore, the ankle joint was immobilized at maximal plantar flexion. The shortening position was chosen for causing greater harm to the muscle function16. The animals were daily observed, during the 15 days of immobilization, in order to identify possible damage to the apparatus. After the immobilization removal, the rats were weighed and submitted to cleaning of the right hinder limb on the region of the triceps surae muscle (soleus).

Ultrasound application protocol

Ultrasound therapy used the machine Sonopulse brandname Ibramed®, with frequency of 1.0MHz and 1.0W/cm2 dose, 0.5W/cm2, 0.2W/cm2, respectively to groups GSUS 1.0; GSUS 0.5 and GSUS 0.2, during three minutes on the soleus region of the right hinder limb for a period of 10 days, with two-day interval at the weekends. A handmade restrainer was used in the immobilization to minimize the stress experienced by the animal.

Stretching protocol

In order to apply stretching to the soleus muscle, the ankle joint was manually kept at maximum dorsal flexion during the entire stretching period, at the limit of tissue tension. The intervention consisted of three sets of 30 seconds, with recovery interval of 30 seconds between sets, during 10 days. Likewise, there was a two-day recovery period at the weekends.

Animals' euthanasia

At the end of the experiment, all animals were weighed and euthanized by guillotine decapitation. Immediately after, the right (treated) and left (control) soleus muscles were isolated for cleaning and weighting on analytical scale (Shimadzu®). Subsequently, the muscles were attached to a styrofoam board in their rest length, for length check using an analog pachymeter (Mitutoyo®) and later preparation of the mountings for histological analysis.

Mounting preparation and histological analysis

After having been attached to the styrofoam boards, the muscles were immersed in formaldehyde (10%) during three hours, for tissue attachment. After this period, they were immersed in nitric acid (30%) for 72 hours, in order to break the conjunctive tissue, and later stored in glycerol solution (50%)17.

Subsequently, the muscles were placed on a Petri dish and with the aid of an optical lens (Micronal®), nine muscle fibers were isolated with the help of ultrafine tip tweezers. The isolated fibers were then positioned on waxed histological slides. Out of the nine selected fibers, five were used for counting of the number of sarcomeres in series (the ones with the best visual aspect were selected), during 50µm in six non-consecutive fields, in a total of 300µm of analysis.

An ordinary light microscope (Olympus®), with objective of 40 times, attached to a DCE-s camera was used, with which the images were digitalized. The Image-Pro-Plus 3.0 program was also used to count the sarcomeres in a distance corresponding to 50µm.

Simple rule of three was used for estimation of the total of sarcomeres in series in the analyzed muscle. The considered variables included soleus muscular length, size and number of sarcomeres in series.

STATISTICAL ANALYSIS

The data obtained were analyzed with the Student's t test (for comparison within groups) and ANOVA (for comparison between groups), with Tukey post-test. In all cases, the significance level accepted was of 5%.

RESULTS

Intragroup analysis

Based on the longitudinal histomorphometric parameters of the immobilized soleus muscles of Wistar rats, there was no difference when the left (control) and right (experimental, immobilized and stretched with previous ultrasound 0.5W/cm2 application) muscles were compared (table 1). Concerning muscular length, in the intragroup analysis, only the GSUS 0.5 group did not present significant difference. Concerning the sarcomeres counting, GS and GSUS 0.2 groups presented significant difference between the right (treated) and left (control) muscles. Finally, concerning the sarcomeres size, none group presented significant difference.

Intergroup analysis

The results shown in the analysis between the different treatment groups (GS; GSUS 0.2; GSUS 0.5 and GSUS 1.0) did not present statistically relevant difference for any of the analyzed variables.

DISCUSSION

The functional length of a muscle is important to influence on its contractile properties18-20 and to determine if the muscle adds or loses sarcomeres20,21.

In the present study, only the immobilized and stretched group with previous therapeutic ultrasound with 0.5W/cm2 dose did not present statistically significant difference concerning the quantity of sarcomeres in series and muscular length, when compared with the immobilized and non-immobilized muscles were compared; that is to say, this dose associated with stretching presented positive effects concerning recovery of the deleterious effects caused by immobilization. Costa et al.22 report that the ultrasound produces increase of temperature in the muscular structures, providing muscular relaxation and alteration in viscoelasticity. Such properties may have influenced on the return of the muscular length for this group.

The advantage of the 0.5W/cm2 dose may be linked to the presence of non-thermal effects associated with the thermal effects, which would be responsible for the production of an alteration in the permeability of the membrane and stimulation of the transportation of substances, such as the second messengers. These second messengers stimulate the proliferation of satellite cells, which d could make new fibers in case of death of the cell or would help in the repairing of a focal injury 9. Bertolini et al.23 analyzed the effects of stretching and ultrasound associated or not, and verified that static passive stretching associated with therapeutic ultrasound of 0.5W/cm2 produced alterations only in muscular length at rest, which was increased, corroborating the result of this study.

The application of TUS 1.0W/cm2, associated with stretching, was not sufficient to reestablish muscular length after immobilization. According to Garret et al.24, in order to obtain thermal effect with application of ultrasound, a minimum time of application of five minutes is necessary. Thus, the time of ultrasound application in the present study (three minutes) may have not been sufficient to promote the thermal effects expected with the 1.0W/cm2 dose.

Rantanen et al.8 did not verify regeneration of muscular tissue by application of thermal ultrasound. The same situation was verified in the present study, in which the non-thermal dose of 0.2W/cm2 did not recover the muscular length.

The DNA synthesis of the muscle seems to be controlled by its contractile activity25,26 and mechanical stimuli such as stretching27,28. Immobilization at shortening position induces to atrophy and tissue protein loss29,30. Moreover, growth promoting factors do not act in the immobilized muscle at shortening position, and hence, loses sarcomeres and suffers atrophy21.

The loss of number of sarcomeres in series may be caused by adjustment of the fibers in their extremities, with ideal overlapping of actin and myosin in myofibrils to develop the maximum tension at shortening position20,31. In the present study, it was verified that despite the shortening, there was not reversion of the decrease of quantity of sarcomeres in series derived from the immobilization at shortening position. In previous studies32,33, short-period stretching per se did not normalize the quantity of sarcomeres in series either when compared with the control muscle.

The lack of positive results in the present study concerning stretching may be attributed to the lack of intervals between the interventions and it, considering that other studies34,35 suggested that low frequency of stretching would hamper the degeneration and alterations of the muscle fiber. Thus, the time of stretching application (30 seconds), performed here may have not been sufficient. Moreover, the high frequency of application may have not given time for muscular recovery. A suggestion here hence is an analysis with stretching time longer than 30 seconds, as well as days of interval between applications.

In the groups in which stretching associated with TUS 1.0 and 0.5W/cm2 was used, significant differences were not observed between right and left limbs concerning the quantity of sarcomeres; that is to say, the effect of reduction of sarcomeres in series consequent of the immobilization was reverted. The possible addition of sarcomeres may have been a result of the proliferation of satellite cells, which agglutinate with the cells of the preexisting muscular fibers6.

In the GS and GSUS 0.2W/cm2 groups, there was significant difference between the quantity of sarcomeres in series when the right and left sides are compared; that is to say, there was no recovery of the quantity of sarcomeres. Deyne36 analyzed the effect of stretching and contractile stimulation over the myofibrylogenesis and did not verify stretching as na important factor for the development and maintenance of the muscular sarcomeric structures. When a substance is exposed to a passive force (stretching), it will deform according to the properties of the material, and when a relatively low force is held for a long period of time, the majority of the materials deform in a time-dependent manner. Thus, the duration of the stretching performed in isolation may have been sufficient to promote this deformity6.

Increase in length of sarcomere in shortened muscles is due to stretching of the remaining sarcomeres, allowing hence the development of maximal tension of the muscle despite being shortened31. The GS, GSUS 0.2, GSUS 0.5 and GSUS 1.0 groups did not present significant difference concerning size of sarcomeres between immobilized and non-immobilized limbs, demonstrating the possible return to pre-immobilization size.

CONCLUSIONS

In the present study, stretching alone was not sufficient to revert the deleterious effects of immobilization. When associated with therapeutic ultrasound, only the 0.5W/cm2 dose significantly recovered the muscular length, and the 1.0 and 0.5W/cm2 doses contributed to the significant return of quantity of sarcomeres in series to normal values of the muscles submitted to immobilization.

ACKNOWLEDGEMENTS

To the State University of Western Paraná for the partial grant in the study. To the National Board of Scientific and Technological Development (CNPq) for the support with the scientific initiation scholarship.

REFERENCES

  • 1. Caierão QM, Teodori RM, Minamoto VB. A influência da imobilização sobre o tecido conjuntivo muscular: uma revisão. Fisioter Mov 2007;20:87-92.
  • 2. Silva CA, Guirro RR, Polacow ML, Cancelliero KM, Durigan JL. Rat hindlimb joint immobilization with acrylic resin orthoses. Braz J Med Biol Res 2006;39:979-85.
  • 3. Lima SC, Caierão QM, Durigan JLQ, Schwarzenbeck A, Silva CA, Minamoto VB, et al. Short-term immobilization causes morphometric and mechanical alterations on rat muscles. Rev Bras Fisioter 2007;11:261-6.
  • 4. Natali LH, Silva RS, Ciena AP, Padoin MJ, Alves EPB, Aragão F A, et al. Efeitos da corrida em esteira em músculos sóleos de ratos encurtados por imobilização. Rev Bras Med Esporte 2008;14(6).
  • 5. Williams PE. Effect of intermittent stretch on immobilised muscle. Ann Rheum Dis 1988;47:1014-6.
  • 6. Deyne PG. Application of passive stretch and its implications for muscle fibers. Phys Ther 2001;81819-27
  • 7. Dix DJ, Eisenberg BR. Myosin mRNA accumulation and myofibrillogenesis at the myotendinous junction of stretched muscle fibers. J Cell Biol 1990;111:1885-94.
  • 8. Rantanen JJ, Thorsson O, Wollmer P, Hurme T, Kalimo H. Effects of therapeutic ultrasound on the regeneration of skeletal myofibers after experimental muscle injury. Am J Sports Med 1999;27:54-9.
  • 9. Karnes JL, Burton HW. Continuous therapeutic ultrasound accelerates repair of contraction-induced skeletal muscle damage in rats. Arch Phys Med Rehabil 2002;83:1-4.
  • 10. Matheus JPC, Oliveira FB, Gomide LB, Milani JGPO, Volpon JB, Shimano AC. Efeitos do ultra-som terapêutico nas propriedades mecânicas do músculo esquelético após contusão. Rev Bras Fisioter 2008;12:241-7.
  • 11. Ter Haar G. Therapeutic ultrasound. Eur J Ultrasound 1999;9:3-9.
  • 12. Ter Haar, G. Therapeutic applications of ultrasound. Prog Biophys Mol Biol 2007;93:111-29.
  • 13. Dyson M. Mecanisms involved in therapeutic ultra sound. Physiotherapy 1987;7:116-30.
  • 14. Andersen ML, D'Almeida V, Ko GM, Kawakami, R, Martins PJF, Magalhães LE, et al. Princípios éticos e práticos do uso de animais de experimentação. São Paulo: UNIFESP, 2004.
  • 15. Coutinho EL, Gomes ARS, França CN, Salvini TF. A new model for the immobilization of the rat hind limb. Braz J Med Biol Res 2002;35:1329-32.
  • 16. Williams PE, Goldspink G. Connective tissues changes in immobilized muscle. J Anat 1984;138(pt 2):343-50.
  • 17. Williams PE, Goldspink G. The longitudinal growth of striated muscle fibres. J Cell Sci 1971;9:751-67.
  • 18. Herring SW, Grimm AF, Grim BR. Regulation of sarcomere number in skeletal muscle: a comparison of hypotheses. Muscle Nerve 1984;7:161-73.
  • 19. Fischbach GD, Robbins N. Changes in contractile properties of disused soleus muscles. J Physiol 1969;201:305-20.
  • 20. Tabary JC, Tabary C, Tardieu C, Tardieu G, Goldspink G. Physiological and structural changes in the cat's soleus muscle due to immobilization at different lengths by plaster casts. J Physiol 1972;224:231-44.
  • 21. Goldspink DF. The influence of activity on muscle size and protein turnover. J Physiol 1977;264:283-96.
  • 22. Costa LOP, Costa LCM, Mendes PL, Cancado RL, Lara KL, Lima MD, et al. Efeitos do aquecimento por ultra-som e atividade física aeróbica na flexibilidade do tríceps sural humano: um estudo comparativo. Fisioter Mov 2006;19:19-24.
  • 23. Bertolini GRF, Barbieri CH, Mazzer N. Análise longitudinal de músculos sóleos, de ratos, submetidos ao alongamento passivo com uso prévio de ultra-som terapêutico. Rev Bras Med Esporte 2009;15:115-8.
  • 24. Garret CL, Draper DO, Knight KL. Heat distribution in the lower leg from pulsed short-wave diathermyand ultrasound treatments. J Athl Train 2000;35:50-5.
  • 25. Goldberg AL, Etlinger JD, Goldspink DF, Jablecki C. Mechanism of work-induced hypertrophy of skeletal muscle. Med Sci Sports 1975;7:248-61.
  • 26. Goldspink DF. The effects of denervation on protein turnover of rat skeletal muscle. Biochem J 1976;156:71-80.
  • 27. Kimberg DV, Loeb JN. Differential sensitivity of nuclear and mitochondrial DNA synthesis to suppression by cortisone treatment. Biochim Biophys Acta 1971;246: 412-20.
  • 28. Goldspink DF, Goldberg AL. Influence of pituitary growth hormone on DNA synthesis in rat tissues. Am J Physiol 1975;228:302-9.
  • 29. Goldspink DF. The influence of immobilization and stretch on protein turnover of rat skeletal muscle. J Physiol 1977;264:267-82.
  • 30. Shah SB, Peters D, Jordan KA, Milner DJ, Fridén J, Capetanaki Y, et al. Sarcomere number regulation maintained after immobilization indesmin-null mouse skeletal muscle. J Exp Biol 2001;204(pt 10):1703-10.
  • 31. Williams PE, Goldspink G. Chanfes in sarcomere length and physiological propiertes in immobilized muscle. J Anat 1978;127(pt 3):459-68.
  • 32. Konno EAB, Alves EPB, Bertolini GRF, Barbieri CH, Mazzer N. Remobilização por alongamento estático cíclico em músculo sóleo de ratos imobilizados em encurtamento. Rev Bras Med Esporte 2007;14:122-25.
  • 33. Moseley MM, Herbert RD, Nightingale EJ, Taylor DA, Evans TM, Robertson GJ, et al. Passive stretching does not enhance outcomes in patients with plantarflexion contracture after cast immobilization for ankle fracture: a randomized controlled trial. Arch Phys Med Rehabil 2005;86:1118-26.
  • 34. Vanderburgh HH, Hatfaludy S, Sohar J. Stretch-induced prostaglandins and protein turnover in cultured skeletal muscle. Am J Physiol 1990;259(Cell Physiol 28):C232-C240.
  • 35. Gomes ARS, Cornachione A, Salvini TF, Mattiello-Sverzut AC. Morphological effects of two protocols of passive stretch over the immobilized rat soleus muscle. J Anat 2007;210:328-35.
  • 36. Deyne PG. Formation of sarcomeres in developing myotubes: role of mechanical stretching contractile activation. Am J Physiol Cell Physiol 2000;279:1801-11.

Publication Dates

  • Publication in this collection
    30 Nov 2012
  • Date of issue
    Oct 2012
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