Fascicles from energy-storing tendons show an age-specific response to cyclic fatigue loading

Some tendons, such as the human Achilles and equine superficial digital flexor tendon (SDFT), act as energy stores, stretching and recoiling to increase efficiency during locomotion. Our previous observations of rotation in response to applied strain in SDFT fascicles suggest a helical structure, which may provide energy-storing tendons with a greater ability to extend and recoil efficiently. Despite this specialization, energy-storing tendons are prone to age-related tendinopathy. The aim of this study was to assess the effect of cyclic fatigue loading (FL) on the microstructural strain response of SDFT fascicles from young and old horses. The data demonstrate two independent age-related mechanisms of fatigue failure; in young horses, FL caused low levels of matrix damage and decreased rotation. This suggests that loading causes alterations to the helix substructure, which may reduce their ability to recoil and recover. By contrast, fascicles from old horses, in which the helix is already compromised, showed greater evidence of matrix damage and suffer increased fibre sliding after FL, which may partially explain the age-related increase in tendinopathy. Elucidation of helix structure and the precise alterations occurring owing to both ageing and FL will help to develop appropriate preventative and repair strategies for tendinopathy.

[1]  Graham P. Riley,et al.  Specimen dimensions influence the measurement of material properties in tendon fascicles , 2010, Journal of biomechanics.

[2]  N. Maffulli,et al.  What are the validated animal models for tendinopathy? , 2011, Scandinavian journal of medicine & science in sports.

[3]  M. Pandy,et al.  Force‐ and moment‐generating capacities of muscles in the distal forelimb of the horse , 2003, Journal of anatomy.

[4]  R. M. Alexander.  Energy-saving mechanisms in walking and running. , 1991, The Journal of experimental biology.

[5]  D. Nunamaker,et al.  Application of a Hall-effect transducer for measurement of tendon strains in horses. , 1989, American journal of veterinary research.

[6]  D. Bader,et al.  An investigation into the effects of the hierarchical structure of tendon fascicles on micromechanical properties , 2004, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[7]  G. Beaupré,et al.  Mechanical properties of the human achilles tendon. , 2001, Clinical biomechanics.

[8]  P. Aagaard,et al.  The influence of aging on the in vivo properties of human patellar tendon , 2008, Journal of applied physiology.

[9]  A. Biewener,et al.  Muscle-tendon stresses and elastic energy storage during locomotion in the horse. , 1998, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[10]  H. Birch,et al.  Matrix metabolism rate differs in functionally distinct tendons. , 2007, Matrix biology : journal of the International Society for Matrix Biology.

[11]  H. Screen,et al.  The micro-structural strain response of tendon , 2007 .

[12]  Eve Langelier,et al.  Low Stress Tendon Fatigue is a Relatively Rapid Process in the Context of Overuse Injuries , 2011, Annals of Biomedical Engineering.

[13]  Helen L Birch,et al.  Tendon matrix composition and turnover in relation to functional requirements , 2007, International journal of experimental pathology.

[14]  C. Court-Brown,et al.  The epidemiology of musculoskeletal tendinous and ligamentous injuries. , 2008, Injury.

[15]  D. Hose,et al.  Measuring three‐dimensional strain distribution in tendon , 2013, Journal of microscopy.

[16]  E. Flatow,et al.  Basic mechanisms of tendon fatigue damage. , 2012, Journal of shoulder and elbow surgery.

[17]  P. Weinhold,et al.  Prostaglandin E2, collagenase, and cell death responses depend on cyclical load magnitude in an explant model of tendinopathy , 2010, Connective tissue research.

[18]  M. Egerbacher,et al.  The mechanobiological aetiopathogenesis of tendinopathy: is it the over‐stimulation or the under‐stimulation of tendon cells? , 2007, International journal of experimental pathology.

[19]  A. Goodship,et al.  Prevalence of superficial digital flexor tendonitis and suspensory desmitis in Japanese Thoroughbred flat racehorses in 1999. , 2010, Equine veterinary journal.

[20]  P. Clegg,et al.  Comparative rheumatology: what can be learnt from naturally occurring musculoskeletal disorders in domestic animals? , 2010, Rheumatology.

[21]  G. Lichtwark,et al.  In vivo mechanical properties of the human Achilles tendon during one-legged hopping , 2005, Journal of Experimental Biology.

[22]  K. Jepsen,et al.  Structural and mechanical effects of in vivo fatigue damage induction on murine tendon , 2012, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[23]  R. F. Ker,et al.  The development of fatigue quality in high- and low-stressed tendons of sheep (Ovis aries). , 2000, The Journal of experimental biology.

[24]  H. Screen,et al.  Cyclic loading of tendon fascicles using a novel fatigue loading system increases interleukin-6 expression by tenocytes , 2011, Scandinavian journal of medicine & science in sports.

[25]  T Fukunaga,et al.  Effect of low-load resistance training on the tendon properties in middle-aged and elderly women. , 2003, Acta physiologica Scandinavica.

[26]  Guy Cloutier,et al.  Ultrasound B-scan image simulation, segmentation, and analysis of the equine tendon. , 2010, Medical physics.

[27]  Evan L. Flatow,et al.  Second Harmonic Generation Imaging and Fourier Transform Spectral Analysis Reveal Damage in Fatigue-Loaded Tendons , 2010, Annals of Biomedical Engineering.

[28]  Ian Streeter,et al.  Aspartic Acid Racemization and Collagen Degradation Markers Reveal an Accumulation of Damage in Tendon Collagen That Is Enhanced with Aging* , 2010, The Journal of Biological Chemistry.

[29]  C. Wade,et al.  Aging Contributes to Inflammation in Upper Extremity Tendons and Declines in Forelimb Agility in a Rat Model of Upper Extremity Overuse , 2012, PloS one.

[30]  S. Evans,et al.  Measuring strain distributions in the tendon using confocal microscopy and finite elements , 2009 .

[31]  E. Baer,et al.  The multicomposite structure of tendon. , 1978, Connective tissue research.

[32]  Natasha Agabalyan,et al.  Tendinopathy – from basic science to treatment. , 2013, International journal of experimental pathology.

[33]  R. F. Ker,et al.  Fatigue quality of mammalian tendons. , 2000, The Journal of experimental biology.

[34]  D. Laudier,et al.  Early response to tendon fatigue damage accumulation in a novel in vivo model. , 2010, Journal of biomechanics.

[35]  R. F. Ker,et al.  Why are mammalian tendons so thick , 1988 .

[36]  D. Bader,et al.  Local Strain Measurement within Tendon , 2004 .

[37]  P. Kannus.  Structure of the tendon connective tissue , 2000, Scandinavian journal of medicine & science in sports.

[38]  H. Sun,et al.  Coordinate Regulation of IL-1β and MMP-13 in Rat Tendons Following Subrupture Fatigue Damage , 2008, Clinical orthopaedics and related research.

[39]  Shawn P. Reese,et al.  Micromechanical models of helical superstructures in ligament and tendon fibers predict large Poisson's ratios. , 2010, Journal of biomechanics.

[40]  H. Birch,et al.  Capacity for sliding between tendon fascicles decreases with ageing in injury prone equine tendons: a possible mechanism for age-related tendinopathy? , 2013, European cells & materials.

[41]  D. Laudier,et al.  Subrupture tendon fatigue damage , 2009, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[42]  D. Becker,et al.  The pathogenesis of tendon microdamage in athletes: the horse as a natural model for basic cellular research. , 2012, Journal of comparative pathology.

[43]  J. Wood,et al.  Descriptive epidemiology of fracture, tendon and suspensory ligament injuries in National Hunt racehorses in training. , 2009, Equine veterinary journal.

[44]  H. Birch,et al.  Specialization of tendon mechanical properties results from interfascicular differences , 2012, Journal of The Royal Society Interface.

[45]  K. Sun,et al.  Effects of repetitive multiple freeze-thaw cycles on the biomechanical properties of human flexor digitorum superficialis and flexor pollicis longus tendons. , 2011, Clinical biomechanics.

[46]  J. Kaprio,et al.  Cumulative Incidence of Achilles Tendon Rupture and Tendinopathy in Male Former Elite Athletes , 2005, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[47]  J. Shepherd,et al.  Fatigue loading of tendon , 2013, International journal of experimental pathology.

[48]  G. Pinchbeck,et al.  Factors associated with mortality of geriatric horses in the United Kingdom. , 2011, Preventive veterinary medicine.

[49]  Peter M. Vogt,et al.  Acute and Overuse Injuries Correlated to Hours of Training in Master Running Athletes , 2008, Foot & ankle international.

[50]  Hazel R C Screen,et al.  Helical sub-structures in energy-storing tendons provide a possible mechanism for efficient energy storage and return. , 2013, Acta biomaterialia.

[51]  J. Wood,et al.  Ultrasonographic assessment of the superficial digital flexor tendons of National Hunt racehorses in training over two racing seasons. , 2009, Equine veterinary journal.

[52]  J. Wood,et al.  Fractures and tendon injuries in National Hunt horses in training in the UK: a pilot study. , 2010, Equine veterinary journal.

[53]  A. Goodship,et al.  Are the material properties and matrix composition of equine flexor and extensor tendons determined by their functions? , 2010, Equine veterinary journal.

[54]  V. Ottani,et al.  Structure relates to elastic recoil and functional role in quadriceps tendon and patellar ligament. , 2009, Micron.

[55]  R. Brás,et al.  Biomechanical properties of the triceps surae muscle-tendon unit in young and postmenopausal women. , 2011, Clinical biomechanics.

[56]  Alan M. Wilson,et al.  Is Achilles tendon compliance optimised for maximum muscle efficiency during locomotion? , 2007, Journal of biomechanics.