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Journal of Orthopaedic Surgery and Research Biomed Central Journal of Orthopaedic Surgery and Research BioMed Central Research article Open Access Isokinetic eccentric exercise can induce skeletal muscle injury within the physiologic excursion of muscle-tendon unit: a rabbit model Yang-Hwei Tsuang1, Shui-Ling Lam2, Lien-Chen Wu1, Chang-Jung Chiang1, Li-Ting Chen3, Pei-Yu Chen1, Jui-Sheng Sun*4,5 and Chien-Che Wang6 Address: 1Department of Orthopedic Surgery, Taipei City Hospital, Taipei, Taiwan, 2Department of Physical Medicine & Rehabilitation, Cardinal Tien Hospital, Taipei, Taiwan, 3Department of Research and Development, Healthbanks Biotechnology Corporation Ltd, Taipei, Taiwan, 4Department of Orthopedic Surgery, National Taiwan University Hospital, Taipei, Taiwan, 5Institute of Biomedical Engineering, National Yang- Ming University, Taipei, Taiwan and 6Department of Orthopedic Surgery, PoJen General Hospital, Taipei, Taiwan Email: Yang-Hwei Tsuang - [email protected]; Shui-Ling Lam - [email protected]; Lien-Chen Wu - [email protected]; Chang- Jung Chiang - [email protected]; Li-Ting Chen - [email protected]; Pei-Yu Chen - [email protected]; Jui- Sheng Sun* - [email protected]; Chien-Che Wang - [email protected] * Corresponding author Published: 21 August 2007 Received: 18 February 2007 Accepted: 21 August 2007 Journal of Orthopaedic Surgery and Research 2007, 2:13 doi:10.1186/1749-799X-2-13 This article is available from: http://www.josr-online.com/content/2/1/13 © 2007 Tsuang et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background and Purpose: Intensive eccentric exercise can cause muscle damage. We simulated an animal model of isokinetic eccentric exercise by repetitively stretching stimulated triceps surae muscle-tendon units to determine if such exercise affects the mechanical properties of the unit within its physiologic excursion. Methods: Biomechanical parameters of the muscle-tendon unit were monitored during isokinetic eccentric loading in 12 rabbits. In each animal, one limb (control group) was stretched until failure. The other limb (study group) was first subjected to isokinetic and eccentric cyclic loading at the rate of 10.0 cm/min to 112% (group I) or 120% (group II) of its initial length for 1 hour and then stretched to failure. Load-deformation curves and biomechanical parameters were compared between the study and control groups. Results: When the muscle-tendon unit received eccentric cyclic loading to 112%, changes in all biomechanical parameters – except for the slope of the load-deformation curve – were not significant. In contrast, most parameters, including the slope of the load-deformation curve, peak load, deformation at peak load, total energy absorption, and energy absorption before peak load, significantly decreased after isokinetic eccentric cyclic loading to 120%. Conclusion: We found a threshold for eccentrically induced injury of the rabbit triceps surae muscle at between 12% and 20% strain, which is within the physiologic excursion of the muscle- tendon units. Our study provided evidence that eccentric exercise may induce changes in the biomechanical properties of skeletal muscles, even within the physiologic range of the excursion of the muscle-tendon unit. Page 1 of 7 (page number not for citation purposes) Journal of Orthopaedic Surgery and Research 2007, 2:13 http://www.josr-online.com/content/2/1/13 Background induced by tetanic stimulation, and this kind of distur- In the musculoskeletal system, muscle is the only tissue bances could result in structural changes in the muscle- that can actively develop tension. When skeletal muscle is tendon unit [20]. In the present study, we used low-fre- stimulated, it rapidly changes from passive tissue to active quency nerve stimulation (10 Hz) to prevent the possible tissue. This change can cause muscular injuries, primarily confounding effect of tetanic-nerve stimulation on the strains or tears, which are extremely common in profes- muscle during the experiment. sional and amateur athletes [1,2]. In sports medicine, stretching exercises are often recommended to prevent Cyclic stretching of the triceps surae muscle-tendon unit injury and to improve performance [3,4]. However, inten- can substantially affect its tensile properties [21]. How- sive exercise training can result in muscular damage and ever, the effect of cyclic loading on the skeletal muscle- soreness, especially when the exercise involves eccentric tendon unit during an eccentric model is still unclear. A contraction [5,6]. threshold for stretch-induced injury can be reproduced at 25% strain of the triceps surae muscle-tendon unit [18]. Researchers have demonstrated that eccentric contrac- In this study, the muscle eccentric contraction was simu- tions create more force than either isometric or concentric lated by repetitively stretching stimulated muscle-tendon contractions [7,8]. McCully and Faulkner reported that units. We hypothesized that eccentric cyclic loading could the extent of injury was related to the peak force devel- produce a deleterious effect on the unit at relatively low oped during a lengthening contraction [8]. The increased strain level and that isokinetic eccentric exercise affected development of force may be responsible for muscular the mechanical properties of the unit, even within its injury in eccentric contraction [7]. Later, Jones et al stud- physiologic excursion. ied the influence of mechanical factors (ie, force on long- lasting changes in voluntary force occurrence) and found Methods that the generation of low-frequency fatigue and muscular Animal preparation injury is length dependent rather than force dependent This study was approved by the National Taiwan Univer- [9]. sity Medical College's Animal Research Committee. Twelve New Zealand White rabbits (4 months old, mean To investigate the deleterious effects of eccentric exercise weight 2.5 kg, SD 0.2 kg) were equally divided into two on humans, scientists usually use biochemical and elec- groups. In group I, the triceps muscle-tendon unit was trophysiologic parameters to indirectly monitor the passively stretched to 112% of its resting length, and in degrees of muscular injury [10-14]. An evaluation of the group II, it was stretched to 120%. The leg in each tested biomechanical properties of skeletal muscle includes an rabbit chosen to be the study or control leg was randomly assessment for macroscopic tears. However, this method assigned. does not apply to evaluate the potential deleterious effect of eccentric exercise on the biomechanical properties of Preparation of the animals was the same as previously human skeletal muscles. reported [16]. After the animals were anesthetized with ketamine 50 mg/kg given subcutaneously, an incision was In a rabbit model, Lieber and Frieden demonstrated that made from the midcalf to the plantar surface of the foot high force per se does not cause muscular damage after on the lateral aspect of each hind limb. The Achilles ten- eccentric contraction, but rather the magnitude of the don was isolated with special care to maintain the integ- active strain does [15]. It has been demonstrated that the rity of the neurovascular bundle and tendon insertion. triceps surae muscle-tendon unit behaved viscoelastically and the extent of muscle injuries was closely related with Biomechanical test the stretch rate. The muscle-tendon unit tolerated great During the test procedure, the sedated rabbits were put on tensile force and endured high energy at fast stretch status supine position with the hip fixed in 90 degrees of flexion. [16]. The extent of muscular injuries were closely related To determine the in situ length of the muscle-tendon unit, to the stretch rate; with fast stretch rates, an increased peak a dial calipers accurate to 0.05 mm was used to measure tensile force was required, and energy absorption the distance between the origin of the triceps surae at the increased [16]. In later studies of eccentric contraction, we distal femur and the insertion site at calcaneus with the found that when the stimulated muscle failed, the passive knee while the ankle was flexed 90° [16]. The anesthe- muscle force was dominant and closely related to the tized rabbit was then placed in a frame attached to a test- extent of stretch [17]. In these studies, a single stretch to ing machine (MTS Bionix 858, Minneapolis, MN, USA). failure produced injury. The hind limbs were immobilized with K-wire transfixa- tion through the proximal tibia. The distal tendinous In previous reports on injuries induced by eccentric con- insertion was freed by means of osteotomy at the calca- traction [18,19] activation of muscle tissue was usually neal tuberosity and then clamped to the load cell of the Page 2 of 7 (page number not for citation purposes) Journal of Orthopaedic Surgery and Research 2007, 2:13 http://www.josr-online.com/content/2/1/13 test system. The muscle was passively extended to its orig- Statistical analysis inal length before osteotomy. A 3-N preload was applied Differences in the energy that the muscle-tendon unit on the muscle, and its length was measured again [16]. absorbed before peak load and at full separation of the ruptured fragments were analyzed by using the paired t Before the experiment, a skin incision was made over test. Because of the great individual variation in the bilateral buttock region to expose the sciatic nerve. The strength of the triceps surae muscle, the paired t test was nerve was isolated and clamped with a nerve stimulator also used to evaluate differences between limbs of the rab- (TENS SkylarkTM transcutaneous electrical nerve stimula- bits in each group. The level of statistical significance was tor; Skylark Device Co., Ltd., ROC). set at P < 0.05. For the study group, the muscle-tendon unit of one hind Results limb was cyclically loaded for 1 hour at a rate of 10.0 cm/ After isokinetic eccentric loading, all muscle-tendon units min to a strain amplitude of 12% or 20%.
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