Effect of fatigue loading on structure and functional behaviour of fascicles from energy-storing tendons

Acta Biomaterialia

Volumn 10, Issue 7, 2014, Pages 3217-3224

  Thorpe, Chavaunne T ^a,b   Riley, Graham P ^c   Birch, Helen L ^d   Clegg, Peter D ^b   Screen, Hazel R C ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Confocal microscopy; Fatigue damage; Hysteresis; Mechanical testing; Micromechanics

Indexed keywords

HYSTERESIS; MECHANICAL TESTING; RECOVERY; STIFFNESS; TENDONS;

'CURRENT; APPLIED STRAIN; ENERGY; EXTENSION MECHANISMS; FATIGUE LOADINGS; FUNCTIONAL BEHAVIORS; LARGER DEFORMATIONS; MICROSTRUCTURAL STRAINS; STRAIN RESPONSE; STRUCTURE BEHAVIOR;

FATIGUE DAMAGE;

ANIMAL EXPERIMENT; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELASTICITY; FATIGUE; FATIGUE LOADING; FLEXOR TENDON; FORELIMB; HYSTERESIS; LOCOMOTION; MUSCLE FUNCTION; MUSCLE INJURY; MUSCULOSKELETAL SYSTEM PARAMETERS; NONHUMAN; PRIORITY JOURNAL; RISK FACTOR; SCANNING ELECTRON MICROSCOPY; ANATOMY AND HISTOLOGY; ANIMAL; BIOMECHANICS; HORSE; MECHANICAL STRESS; PHYSIOLOGY; TENDON;

EQUIDAE;

ANIMALS; BIOMECHANICAL PHENOMENA; HORSES; STRESS, MECHANICAL; TENDONS;

EID: 84901806280     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.04.008     Document Type: Article

References (55)

1. R.M. Alexander Energy-saving mechanisms in walking and running J Exp Biol 160 1991 55 69
2. P.R. Stephens, D.M. Nunamaker, and D.M. Butterweck Application of a Hall-effect transducer for measurement of tendon strains in horses Am J Vet Res 50 1989 1089 1095
3. G.A. Lichtwark, and A.M. Wilson Is Achilles tendon compliance optimised for maximum muscle efficiency during locomotion? J Biomech 40 2007 1768 1775
4. E.L. Batson, R.J. Paramour, T.J. Smith, H.L. Birch, J.C. Patterson-Kane, and A.E. Goodship Are the material properties and matrix composition of equine flexor and extensor tendons determined by their functions? Equine Vet J 35 2003 314 318
5. J. Kastelic, A. Galeski, and E. Baer The multicomposite structure of tendon Connect Tissue Res 6 1978 11 23
6. P. Kannus Structure of the tendon connective tissue Scand J Med Sci Sports 10 2000 312 320
7. H.L. Birch, S. Worboys, S. Eissa, B. Jackson, S. Strassburg, and P.D. Clegg Matrix metabolism rate differs in functionally distinct tendons Matrix Biol 27 2008 182 189
8. H.L. Birch Tendon matrix composition and turnover in relation to functional requirements Int J Exp Pathol 88 2007 241 248
9. C.T. Thorpe, C. Klemt, G.P. Riley, H.L. Birch, P.D. Clegg, and H.R. Screen Helical sub-structures in energy-storing tendons provide a possible mechanism for efficient energy storage and return Acta Biomater 9 2013 7948 7956
10. C.T. Thorpe, C.P. Udeze, H.L. Birch, P.D. Clegg, and H.R.C. Screen Specialization of tendon mechanical properties results from interfascicular differences J R Soc Interface 9 2012 3108 3117
11. C.T. Thorpe, I. Streeter, G.L. Pinchbeck, A.E. Goodship, P.D. Clegg, and H.L. Birch Aspartic acid racemization and collagen degradation markers reveal an accumulation of damage in tendon collagen that is enhanced with aging J Biol Chem 285 2010 15674 15681
12. M. Franchi, M. Quaranta, M. Macciocca, V. De Pasquale, V. Ottani, and A. Ruggeri Structure relates to elastic recoil and functional role in quadriceps tendon and patellar ligament Micron 40 2009 370 377
13. E.R. Ely, C.S. Avella, J.S. Price, R.K. Smith, J.L. Wood, and K.L. Verheyen Descriptive epidemiology of fracture, tendon and suspensory ligament injuries in National Hunt racehorses in training Equine Vet J 41 2009 372 378
14. Y. Kasashima, T. Takahashi, R.K. Smith, A.E. Goodship, A. Kuwano, and T. Ueno et al. Prevalence of superficial digital flexor tendonitis and suspensory desmitis in Japanese Thoroughbred flat racehorses in 1999 Equine Vet J 36 2004 346 350
15. K. Knobloch, U. Yoon, and P.M. Vogt Acute and overuse injuries correlated to hours of training in master running athletes Foot Ankle Int 29 2008 671 676
16. P. Kannus, and A. Natri Etiology and pathophysiology of tendon ruptures in sports Scand J Med Sci Sports 7 1997 107 112
17. G. Riley Tendinopathy: from basic science to treatment Nat Clin Pract Rheum 4 2008 82 89
18. C.T. Thorpe, G.P. Riley, H.L. Birch, P.D. Clegg, and H.R. Screen Fascicles from energy-storing tendons show an age-specific response to cyclic fatigue loading J R Soc Interface 11 2014 20131058
19. V.W.T. Cheng, and H.R.C. Screen The micro-structural strain response of tendon J Mater Sci 42 2007 8957 8965
20. K.P. Quinn, and B.A. Winkelstein Preconditioning is correlated with altered collagen fiber alignment in ligament J Biomech Eng 133 2011 064506
21. S.L. Woo Mechanical properties of tendons and ligaments. I. Quasi-static and nonlinear viscoelastic properties Biorheology 19 1982 385 396
22. Y.C. Fung Biomechanics: mechanical properties of living tissues 2nd ed. 1993 Springer New York
23. N. Conza Part 3: tissue preconditioning Exp Tech 29 2005 43 46
24. K.S. Miller, L. Edelstein, B.K. Connizzo, and L.J. Soslowsky Effect of preconditioning and stress relaxation on local collagen fiber re-alignment: inhomogeneous properties of rat supraspinatus tendon J Biomech Eng 134 2012 031007
25. K.S. Miller, B.K. Connizzo, E. Feeney, and L.J. Soslowsky Characterizing local collagen fiber re-alignment and crimp behavior throughout mechanical testing in a mature mouse supraspinatus tendon model J Biomech 45 2012 2061 2065
26. J.F. Innes, and P. Clegg Comparative rheumatology: what can be learnt from naturally occurring musculoskeletal disorders in domestic animals? Rheumatol (Oxford) 49 2010 1030 1039
27. P.P.Y. Lui, N. Maffulli, C. Rolf, and R.K.W. Smith What are the validated animal models for tendinopathy? Scand J Med Sci Sports 21 2010 3 17
28. H. Huang, J. Zhang, K. Sun, X. Zhang, and S. Tian Effects of repetitive multiple freeze-thaw cycles on the biomechanical properties of human flexor digitorum superficialis and flexor pollicis longus tendons Clin Biomech 26 2011 419 423
29. A. Meghoufel, G. Cloutier, N. Crevier-Denoix, and J.A. de Guise Ultrasound B-scan image simulation, segmentation, and analysis of the equine tendon Med Phys 37 2010 1038 1046
30. K. Legerlotz, G.C. Jones, H.R.C. Screen, and G.P. Riley Cyclic loading of tendon fascicles using a novel fatigue loading system increases interleukin-6 expression by tenocytes Scand J Med Sci Sports 23 2013 31 37
31. H.R.C. Screen, D.A. Lee, D.L. Bader, and J.C. Shelton An investigation into the effects of the hierarchical structure of tendon fascicles on micromechanical properties Proc Inst Mech Eng H J Eng Med 218 2004 109 119
32. S. Cheng, E.C. Clarke, and L.E. Bilston The effects of preconditioning strain on measured tissue properties J Biomech 42 2009 1360 1362
33. H. Eshel, and Y. Lanir Effects of strain level and proteoglycan depletion on preconditioning and viscoelastic responses of rat dorsal skin Ann Biomed Eng 29 2001 164 172
34. L. Schatzmann, P. Brunner, and H.U. Staubli Effect of cyclic preconditioning on the tensile properties of human quadriceps tendons and patellar ligaments Knee Surg Sports Traumatol Arthrosc 6 Suppl. 1 1998 S56 S61
35. B.K. Graf, R. Vanderby Jr., M.J. Ulm, R.P. Rogalski, and R.J. Thielke Effect of preconditioning on the viscoelastic response of primate patellar tendon Arthroscopy 10 1994 90 96
36. Y. Lanir, and Y.C. Fung Two-dimensional mechanical properties of rabbit skin - II. Experimental results J Biomech 7 1974 171 182
37. A. Sverdlik, and Y. Lanir Time-dependent mechanical behavior of sheep digital tendons, including the effects of preconditioning J Biomech Eng 124 2002 78 84
38. Y. Goulam Houssen, I. Gusachenko, M.C. Schanne-Klein, and J.M. Allain Monitoring micrometer-scale collagen organization in rat-tail tendon upon mechanical strain using second harmonic microscopy J Biomech 44 2011 2047 2052
39. H.R.C. Screen, S. Toorani, and J.C. Shelton Microstructural stress relaxation mechanics in functionally different tendons Med Eng Phys 35 2012 96 102
40. H.R.C. Screen, J. Seto, S. Krauss, P. Boesecke, and H.S. Gupta Extrafibrillar diffusion and intrafibrillar swelling at the nanoscale are associated with stress relaxation in the soft collagenous matrix tissue of tendons Soft Matter 7 2011 11243 11251
41. S.P. Reese, and J.A. Weiss Tendon fascicles exhibit a linear correlation between Poisson's ratio and force during uniaxial stress relaxation J Biomech Eng 135 2013 034501
42. K.G. Helmer, J. Wellen, P. Grigg, and C.H. Sotak Measurement of the spatial redistribution of water in rabbit Achilles tendon in response to static tensile loading J Biomech Eng 126 2004 651 656
43. S. Han, S.J. Gemmell, K.G. Helmer, P. Grigg, J.W. Wellen, and A.H. Hoffman et al. Changes in ADC caused by tensile loading of rabbit Achilles tendon: evidence for water transport J Magn Reson 144 2000 217 227
44. J.A. Hannafin, and S.P. Arnoczky Effect of cyclic and static tensile loading on water content and solute diffusion in canine flexor tendons: an in vitro study J Orthop Res 12 1994 350 356
45. P. Ciarletta, and M. Ben Amar A finite dissipative theory of temporary interfibrillar bridges in the extracellular matrix of ligaments and tendons J R Soc Interface 6 2009 909 924
46. G. Khodabakhshi, D. Walker, A. Scutt, L. Way, R.M. Cowie, and D.R. Hose Measuring three-dimensional strain distribution in tendon J Microsc 249 2013 195 205
47. A. Neviaser, N. Andarawis-Puri, and E. Flatow Basic mechanisms of tendon fatigue damage J Shoulder Elbow Surg 21 2012 158 163
48. D. Fung, J. Sereysky, J. Basta-Pljakic, D. Laudier, R. Huq, and K. Jepsen et al. Second harmonic generation imaging and Fourier transform spectral analysis reveal damage in fatigue-loaded tendons Ann Biomed Eng 38 2010 1741 1751
49. D.T. Fung, V.M. Wang, D.M. Laudier, J.H. Shine, J. Basta-Pljakic, and K.J. Jepsen et al. Subrupture tendon fatigue damage J Orthop Res 27 2009 264 273
50. J.H. Shepherd, K. Legerlotz, T. Demirci, C. Klemt, G.P. Riley, and H.R. Screen Functionally distinct tendon fascicles exhibit different creep and stress relaxation behaviour Proc Inst Mech Eng H 2013
51. D.T. Fung, V.M. Wang, N. Andarawis-Puri, J. Basta-Pljakic, Y. Li, and D.M. Laudier et al. Early response to tendon fatigue damage accumulation in a novel in vivo model J Biomech 43 2010 274 279
52. C.T. Thorpe, G.P. Riley, H.L. Birch, P.D. Clegg, and H.R. Screen Fascicles from energy-storing tendons show an age-specific response to cyclic fatigue loading J R Soc Interface 11 2014 20131058
53. R.F. Ker, X.T. Wang, and A.V. Pike Fatigue quality of mammalian tendons J Exp Biol 203 2000 1317 1327
54. G.A. Lichtwark, A.G. Cresswell, and R.J. Newsham-West Effects of running on human Achilles tendon length-tension properties in the free and gastrocnemius components J Exp Biol 216 2013 4388 4394
55. J.H. Shepherd, and H.R.C. Screen Fatigue loading of tendon Int J Exp Pathol 94 2013 260 270