Eccentric Training Improves Tendon Biomechanical Properties: A Rat Model Jean-Franc¸ois Kaux,1 Pierre Drion,2 Vincent Libertiaux,3 Alain Colige,4 Audrey Hoffmann,4 Betty Nusgens,4 Benoıˆt Besanc¸on,1 Be´ne´dicte Forthomme,1 Caroline Le Goff,5 Rachel Franzen,6 Jean-Olivier Defraigne,7 Serge Cescotto,3 Markus Rickert,8 Jean-Michel Crielaard,1 Jean-Louis Croisier1 1
Physical Medicine Service and Department of Motility Sciences, University Hospital of Lie`ge, University of Lie`ge, Avenue de 1’Hoˆpital, B35, B-4000 Liege, Belgium, 2Animal Facility of University Hospital of Lie`ge, ULg-GIGA-R, University of Lie`ge, Belgium, 3Department Argenco, University of Lie`ge, Belgium, 4Laboratory of Connective Tissues Biology, GIGA-R, University of Lie`ge, Belgium, 5Department of Clinical Biology, University Hospital of Lie`ge, University of Lie`ge, Belgium, 6Department of Biomedical and Preclinic Sciences, GIGA-R, University of Lie`ge, Belgium, 7CREDEC, Laboratory of Experimental Surgery, University of Lie`ge, Belgium, 8Department of Orthopaedic Surgery, University of Heidelberg, Germany Received 7 December 2011; accepted 9 July 2012 Published online 30 July 2012 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/jor.22202
ABSTRACT: The treatment of choice for tendinopathies is eccentric reeducation. Although the clinical results appear favorable, the biomechanical changes to the tissue are not yet clear. Even if the mechanotransduction theory is commonly accepted, the physiology of tendons is not clearly understood. We aimed to better define the biomechanical and histological changes that affect healthy tendon after eccentric and concentric training. This study compared the effects of two methods of training (eccentric [E] training and concentric [C] training) with untrained (U) rats. The animals were trained over a period of 5 weeks. The tricipital, patellar, and Achilles tendons were removed, measured and a tensile test until failure was performed. A histological analysis (hematoxylin and eosin and Masson’s trichrome stains) was also realized. There was a significant increase in the rupture force of the patellar and tricipital tendons between the U and E groups. The tricipital tendons in the control group presented a significantly smaller cross-sectional area than the E- and C-trained groups, but none was constated between E and C groups. No significant difference was observed for the mechanical stress between the three groups for all three tendons. Histological studies demonstrated the development of a greater number of blood vessels and a larger quantity of collagen in the E group. The mechanical properties of tendons in rats improve after specific training, especially following eccentric training. Our results partly explained how mechanical loading, especially in eccentric mode, could improve the healing of tendon. ß 2012 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 31:119–124, 2013 Keywords: tendon; eccentric; concentric; rat
Tendinopathies affect the upper and lower limbs and occur frequently in subjects who are physically active and play sports.1 They represent the most commonly diagnosed musculoskeletal disorders (around 20%) by a general practitioner.1 Once chronic, these pathologies no longer respond to classical treatments and are difficult to address, in part because their physiopathology remains partially unknown.1 The current treatment of choice for tendinopathies is eccentric physical therapy.1 In the 1980s, Stanish proposed the basic rules for an eccentric training programme.2 Subsequently, numerous clinical studies have shown that a prolonged program of sub-maximal eccentric contractions, performed for 6 weeks to 1 year, significantly reduced all symptoms of tendinopathy for a period of several months to several years, depending on the gravity of the condition.3–5 A There is no conflict of interest. The abstract was presented by Dr. Jean-Franc¸ois Kaux at the Second Congress of the European College of Sport and Exercise Physicians (ECOSEP) held in London, UK, September 9–11, 2010. And at the 17th Annual Congress of the European College of Sports Sciences (ECSS) held in Bruges, Belgium, July 4–7, 2012. Grant sponsor: Fonds Le´on Fre´de´ricq; Grant sponsor: Fondation Lejeune-Lechien. Correspondence to: Jean-Franc¸ois Kaux (T: þ32-4-366-84-73; F: þ32-4-366-72-30; E-mail:
[email protected]) ß 2012 Orthopaedic Research Society. Published by Wiley Periodicals, Inc.
minimum of 20 training sessions appears to be necessary to ensure that the treatment is effective. Although the clinical results appear favorable, the morphological and biochemical changes in the tissue are not yet clear. The aim of this study was to better define the biomechanical changes that affect healthy tendinous tissue after eccentric and concentric training. To our knowledge, this type of biomechanical analysis of healthy tendons in rats following specific and repetitive effort has not been reported previously. Before analyzing the pathological modifications of tendons due to eccentric exercises, we determined how a healthy tendon adapts to different types of training. Indeed, the physiology of tendons and, above all, the physiopathology of tendinopathy are not clearly understood. Even if the mechanotransduction theory is commonly accepted to explain the transformation of mechanical loads to a cellular response, and to promote to an adaptation of the tendon to this stress, biomechanical and histological characteristics remain still unclear and not determined in the healthy tendon submitted to an eccentric or concentric exercise. This study provides an interesting basis for further analyses and characterizations of pathological tendons.
MATERIALS AND METHODS The Institutional Animal Care and Use Ethics Committee of the University of Lie`ge approved the protocol used in this JOURNAL OF ORTHOPAEDIC RESEARCH JANUARY 2013
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study. The ‘‘Guide for the Care and Use of Laboratory Animals,’’ prepared by the Institute of Laboratory Animal Resources, National Research Council and published by the National Academy Press, was followed carefully throughout the experiments. The rats were weighed on a weekly basis, and daily examinations were performed to ensure that the rats were in good health throughout the experiment.
fields by counting nuclei and blood vessels. Fibrillar collagen accumulation was visualized in green but not quantified. In the H&E stained cross-sections, the cell nuclei are a bluepurple color. The extracellular matrix and the proteins in the fibroblast cytoplasm are pink. On the cross-sections stained using the TRI technique, the bright green colored collagen is particularly obvious.
Population Sprague–Dawley rats of 2 months (18 in total, each weighing 300 g) were divided into three groups: U for untrained (controls), C for concentric, and E for eccentric groups.
Statistical Analysis The mean and standard deviation (SD) were calculated for each data set. The aberrant values obtained after the determination of quartiles Q1 and Q3 were eliminated from the analysis if they were outside the limits [Q11.5 (Q3Q1)] and [Q3 þ 1.5 (Q3Q1)]. The normality of distribution has been tested and confirmed to allow the use of an ANOVA. The values of the force at rupture, the cross-sectional area of tendons and the ratio between the force and the section of the three groups were compared using an ANOVA combined with a post-hoc Scheffe´ test where necessary. The values were considered significant when the p-value was C), and were particularly visible in the tricipital tendons from the group E. Eccentric exercise has been shown to lead to an increase in the synthesis of collagen fibres.12 Moreover, the tendons from the group E seemed to present a transitory increase in the number of peripheral blood vessels without any increase in inflammatory cell infiltration or the pathological morphology. These visible tissue modifications appear to correspond to the normal physiological process of the tendon adapting to the external stress. Indeed, Nakamura et al.14 demonstrated that eccentric exercise in rats contributes to stabilized angiogenesis during the early phases of tendon injury and may help to improve the healing of tendons.
CONCLUSION This study demonstrates that the mechanical properties of healthy tendons in rats improve after specific training and that an eccentric training program is
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more beneficial than a concentric program. The higher resistance of trained tendons mostly results from an increase of the cross-sectional area although small modifications of the tissue architecture may also play a role. A better understanding of the biochemical processes regulating mechanotransduction would allow improvement in the treatment of tendinopathies and other pathologies that are sensitive to variations in local tissue strength.
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