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

Journal of the Royal Society Interface

Volumn 11, Issue 92, 2014, Pages

  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

Ageing; Confocal microscopy; Fascicle; Micromechanics; Structure function

Indexed keywords

CONFOCAL MICROSCOPY; MICROMECHANICS; REPAIR; TENDONS;

AGEING; CYCLIC FATIGUE LOADING; FASCICLE; FATIGUE FAILURES; HELICAL STRUCTURES; HELIX STRUCTURES; MICROSTRUCTURAL STRAINS; STRUCTURE FUNCTIONS;

FATIGUE DAMAGE;

AGE; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FATIGUE; FORELIMB; IMAGE ANALYSIS; IN VIVO STUDY; NONHUMAN; ROTATION; TENDINITIS; TENDON; TENDON STRESS; WRIST; ANALYSIS OF VARIANCE; ANIMAL; ANIMAL DISEASE; BIOMECHANICS; CONFOCAL MICROSCOPY; ENERGY TRANSFER; FASCICLE; HORSE; HORSE DISEASE; IMAGE PROCESSING; MATERIALS TESTING; MICROMECHANICS; MUSCLE FATIGUE; PATHOLOGY; PHYSIOLOGY; STRUCTURE-FUNCTION; YOUNG MODULUS;

AGEING; CONFOCAL MICROSCOPY; FASCICLE; MICROMECHANICS; STRUCTURE-FUNCTION;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; BIOMECHANICAL PHENOMENA; ELASTIC MODULUS; ENERGY TRANSFER; HORSE DISEASES; HORSES; IMAGE PROCESSING, COMPUTER-ASSISTED; MATERIALS TESTING; MICROSCOPY, CONFOCAL; MUSCLE FATIGUE; TENDINOPATHY; TENDONS;

EID: 84893087268     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2013.1058     Document Type: Article

References (56)

1. Kastelic J, Galeski A, Baer E. 1978 The multicomposite structure of tendon. Connect. Tissue Res. 6, 11-23. (doi:10.3109/03008207809152283)
2. Kannus P. 2000 Structure of the tendon connective tissue. Scand. J. Med. Sci. Sports 10, 312-320. (doi:10.1034/j.1600-0838.2000.010006312.x)
3. Batson EL, Paramour RJ, Smith TJ, Birch HL, Patterson-Kane JC, Goodship AE. 2003 Are the material properties and matrix composition of equine flexor and extensor tendons determined by their functions? Equine Vet. J. 35, 314-318. (doi:10.2746/042516403776148327)
4. Birch HL, Worboys S, Eissa S, Jackson B, Strassburg S, Clegg PD. 2008 Matrix metabolism rate differs in functionally distinct tendons. Matrix Biol. 27, 182-189. (Pubitemid 351375387)
5. Thorpe CT, Streeter I, Pinchbeck GL, Goodship AE, Clegg PD, Birch HL. 2010 Aspartic acid racemization and collagen degradation markers reveal an accumulation of damage in tendon collagen that is enhanced with aging. J. Biol. Chem. 285, 15 674-15 681. (doi:10.1074/jbc.M109.077503)
6. Thorpe CT, Udeze CP, Birch HL, Clegg PD, Screen HRC. 2012 Specialization of tendon mechanical properties results from interfascicular differences. J. R. Soc. Interface. 9, 3108-3117. (doi:10.1098/rsif.2012.0362)
7. Thorpe CT, Klemt C, Riley GP, Birch HL, Clegg PD, Screen HR. 2013 Helical sub-structures in energystoring tendons provide a possible mechanism for efficient energy storage and return. Acta Biomater. 9, 7948-7956. (doi:10.1016/j.actbio.2013.05.004)
8. Birch HL. 2007 Tendon matrix composition and turnover in relation to functional requirements. Int. J. Exp. Pathol. 88, 241-248. (doi:10.1111/j.1365- 2613.2007.00552.x)
9. Franchi M, Quaranta M, Macciocca M, De Pasquale V, Ottani V, Ruggeri A. 2009 Structure relates to elastic recoil and functional role in quadriceps tendon and patellar ligament. Micron 40, 370-377. (doi:10.1016/j.micron.2008.10. 004)
10. Alexander RM. 1991 Energy-saving mechanisms in walking and running. J. Exp. Biol. 160, 55-69.
11. Biewener AA. 1998 Muscle-tendon stresses and elastic energy storage during locomotion in the horse. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 120, 73-87. (doi:10.1016/S0305-0491(98)00024-8)
12. Lichtwark GA, Wilson AM. 2007 Is Achilles tendon compliance optimised for maximum muscle efficiency during locomotion? J. Biomech. 40, 1768-1775. (doi:10.1016/j.jbiomech.2006.07.025)
13. Lichtwark GA, Wilson AM. 2005 In vivo mechanical properties of the human Achilles tendon during one-legged hopping. J. Exp. Biol. 208, 4715-4725. (doi:10.1242/jeb.01950)
14. Thorpe CT, Udeze CP, Birch HL, Clegg PD, Screen HRC. 2013 Capacity for sliding between tendon fascicles decreases with ageing in injury prone equine tendons: a possible mechanism for age-related tendinopathy? Eur. Cells Mater. 25, 48-60.
15. Patterson-Kane JC, Becker DL, Rich T. 2012 The pathogenesis of tendon microdamage in athletes: the horse as a natural model for basic cellular research. J. Comp. Pathol. 147, 227-247. (doi:10.1016/j.jcpa.2012.05.010)
16. Stephens PR, Nunamaker DM, Butterweck DM. 1989 Application of a hall-effect transducer for measurement of tendon strains in horses. Am. J. Vet. Res. 50, 1089-1095.
17. Cheng VWT, Screen HRC. 2007 The micro-structural strain response of tendon. J. Mater. Sci. 42, 8957-8965. (doi:10.1007/s10853-007-1653-3)
18. Screen HRC, Bader DL, Lee DA, Shelton JC. 2004 Local strain measurement within tendon. Strain 40, 157-163. (doi:10.1111/j.1475-1305.2004.00164.x)
19. Screen HRC, Evans SL. 2009 Measuring strain distributions in the tendon using confocal microscopy and finite elements. J. Strain Anal. Eng. 44, 327-335. (doi:10.1243/03093247JSA491)
20. Khodabakhshi G, Walker D, Scutt A, Way L, Cowie RM, Hose DR. 2013 Measuring three-dimensional strain distribution in tendon. J. Microsc. 249, 195-205. (doi:10.1111/jmi.12009)
21. Riley G. 2008 Tendinopathy: from basic science to treatment. Nat. Clin. Pract. Rheum. 4, 82-89. (doi:10.1038/ncprheum0700)
22. Kujala UM, Sarna S, Kaprio J. 2005 Cumulative incidence of Achilles tendon rupture and tendinopathy in male former elite athletes. Clin. J. Sport Med. 15, 133-135. (doi:10.1097/01.jsm.0000165347.55638.23)
23. Knobloch K, Yoon U, Vogt PM. 2008 Acute and overuse injuries correlated to hours of training in master running athletes. Foot Ankle Int. 29, 671-676. (doi:10.3113/FAI.2008.0671)
24. Kasashima Y, Takahashi T, Smith RK, Goodship AE, Kuwano A, Ueno T, Hirano S. 2004 Prevalence of superficial digital flexor tendonitis and suspensory desmitis in Japanese thoroughbred flat racehorses in 1999. Equine Vet. J. 36, 346-350. (doi:10.2746/0425164044890580)
25. Avella CS, Ely ER, Verheyen KL, Price JS, Wood JL, Smith RK. 2009 Ultrasonographic assessment of the superficial digital flexor tendons of national hunt racehorses in training over two racing seasons. Equine Vet. J. 41, 449-454. (doi:10.2746/042516409X391042)
26. Lui PPY, Maffulli N, Rolf C, Smith RKW. 2010 What are the validated animal models for tendinopathy? Scand. J. Med. Sci. Sports 21, 3-17. (doi:10.1111/j.1600-0838.2010.01164.x)
27. Innes JF, Clegg P. 2010 Comparative rheumatology: what can be learnt from naturally occurring musculoskeletal disorders in domestic animals? Rheumatology 49, 1030-1039. (doi:10.1093/rheumatology/kep465)
28. Clayton RAE, Court-Brown CM. 2008 The epidemiology of musculoskeletal tendinous and ligamentous injuries. Injury 39, 1338-1344. (doi:10.1016/j.injury. 2008.06.021)
29. Ely ER, Avella CS, Price JS, Smith RK, Wood JL, Verheyen KL. 2009 Descriptive epidemiology of fracture, tendon and suspensory ligament injuries in national hunt racehorses in training. Equine Vet. J. 41, 372-378. (doi:10.2746/042516409X371224)
30. Ely ER, Verheyen KL, Wood JL. 2004 Fractures and tendon injuries in national hunt horses in training in the UK: a pilot study. Equine Vet. J. 36, 365-367. (doi:10.2746/0425164044890607)
31. Ireland JL, Clegg PD, McGowan CM, Platt L, Pinchbeck GL. 2011 Factors associated with mortality of geriatric horses in the United Kingdom. Prev. Vet. Med. 101, 204-218. (doi:10.1016/j.prevetmed.2011.06.002)
32. Huang H, Zhang J, Sun K, Zhang X, Tian S. 2011 Effects of repetitive multiple freeze-thaw cycles on the biomechanical properties of human flexor digitorum superficialis and flexor pollicis longus tendons. Clin. Biomech. 26, 419-423. (doi:10.1016/j.clinbiomech.2010.12.006)
33. Legerlotz K, Riley GP, Screen HR. 2010 Specimen dimensions influence the measurement of material properties in tendon fascicles. J. Biomech. 43, 2274-2280. (doi:10.1016/j.jbiomech.2010.04.040)
34. Legerlotz K, Jones GC, Screen HRC, Riley GP. 2013 Cyclic loading of tendon fascicles using a novel fatigue loading system increases interleukin-6 expression by tenocytes. Scand. J. Med. Sci. Sports 23, 31-37. (doi:10.1111/j.1600-0838.2011.01410.x)
35. Screen HRC, Lee DA, Bader DL, Shelton JC. 2004 An investigation into the effects of the hierarchical structure of tendon fascicles on micromechanical properties. Proc. Inst. Mech. Eng. H J. Eng. Med. 218, 109-119. (doi:10.1243/095441104 322984004)
36. Ker RF, Wang XT, Pike AV. 2000 Fatigue quality of mammalian tendons. J. Exp. Biol. 203, 1317-1327. (Pubitemid 30300962)
37. Neviaser A, Andarawis-Puri N, Flatow E. 2012 Basic mechanisms of tendon fatigue damage. J. Shoulder Elbow Surg. 21, 158-163. (doi:10.1016/j.jse.2011.11. 014)
38. Fung DT et al. 2010 Early response to tendon fatigue damage accumulation in a novel in vivo model. J. Biomech. 43, 274-279. (doi:10.1016/j.jbiomech.2009. 08.039)
39. Fung DT, Wang VM, Laudier DM, Shine JH, Basta-Pljakic J, Jepsen KJ, Schaffler MB, Flatow EL. 2009 Subrupture tendon fatigue damage. J. Orthop. Res. 27, 264-273. (doi:10.1002/jor.20722)
40. Fung D, Sereysky J, Basta-Pljakic J, Laudier D, Huq R, Jepsen K, Schaffler M, Flatow E. 2010 Second harmonic generation imaging and Fourier transform spectral analysis reveal damage in fatigue-loaded tendons. Ann. Biomed. Eng. 38, 1741-1751. (doi:10.1007/s10439-010-9976-7)
41. Sereysky JB, Andarawis-Puri N, Jepsen KJ, Flatow EL. 2012 Structural and mechanical effects of in vivo fatigue damage induction on murine tendon. J. Orthop. Res. 30, 965-972. (doi:10.1002/jor.22012)
42. Parent G, Huppé N, Langelier E. 2011 Low stress tendon fatigue is a relatively rapid process in the context of overuse injuries. Ann. Biomed. Eng. 39, 1535-1545. (doi:10.1007/s10439-011-0254-0)
43. Shepherd JH, Screen HRC. 2013 Fatigue loading of tendon. Int. J. Exp. Path. 94, 260-270. (doi:10. 1111/iep.12037)
44. Sun HB, Li YH, Fung DT, Majeska RJ, Schaffler MB, Flatow EL. 2008 Coordinate regulation of IL-1 beta and MMP-13 in rat tendons following subrupture fatigue damage. Clin. Orthop. Relat. Res. 466, 1555-1561. (doi:10.1007/s11999-008-0278-4)
45. Reese SP, Maas SA, Weiss JA. 2010 Micromechanical models of helical superstructures in ligament and tendon fibers predict large Poisson's ratios. J. Biomech. 43, 1394-1400. (doi:10.1016/j.jbiomech.2010.01.004)
46. Meghoufel A, Cloutier G, Crevier-Denoix N, de Guise JA. 2010 Ultrasound B-scan image simulation, segmentation, and analysis of the equine tendon. Med. Phys. 37, 1038-1046. (doi:10.1118/1.3292633)
47. Ker RF, Alexander RM, Bennett MB. 1988 Why are mammalian tendons so thick? J. Zool. 216, 309-324. (doi:10.1111/j.1469-7998.1988.tb02432.x)
48. Brown NAT, Pandy MG, Kawcak CE, McIlwraith CW. 2003 Force- and moment-generating capacities of muscles in the distal forelimb of the horse. J. Anat. 203, 101-113. (doi:10.1046/j.1469-7580.2003.00206.x)
49. Carroll CC, Dickinson JM, Haus JM, Lee GA, Hollon CJ, Aagaard P, Magnusson SP, Trappe TA. 2008 Influence of aging on the in vivo properties of human patellar tendon. J. Appl. Physiol. 105, 1907-1915. (doi:10.1152/ japplphysiol.00059.2008)
50. Faria A, Gabriel R, Abrantes J, Bras R, Moreira H. 2011 Biomechanical properties of the triceps surae muscle-tendon unit in young and postmenopausal women. Clin. Biomech. 26, 523-528. (doi:10.1016/j.clinbiomech.2010.12.011)
51. Kubo K, Kanehisa H, Miyatani M, Tachi M, Fukunaga T. 2003 Effect of low-load resistance training on the tendon properties in middle-aged and elderly women. Acta Physiol. Scand. 178, 25-32. (doi:10.1046/j.1365-201X.2003.01097.x)
52. Wren TAL, Yerby SA, Beaupré GS, Carter DR. 2001 Mechanical properties of the human Achilles tendon. Clin. Biomech. 16, 245-251. (doi:10.1016/S0268-0033(00)00089-9)
53. Pike AV, Ker RF, Alexander RM. 2000 The development of fatigue quality in high- and low-stressed tendons of sheep (Ovis aries). J. Exp. Biol. 203, 2187-2193. (Pubitemid 30610828)
54. Kietrys DM, Barr-Gillespie AE, Amin M, Wade CK, Popoff SN, Barbe MF. 2012 Aging contributes to inflammation in upper extremity tendons and declines in forelimb agility in a rat model of upper extremity overuse. PLoS ONE 7, e46954. (doi:10.1371/journal.pone.0046954)
55. Devkota AC, Weinhold PS. 2010 Prostaglandin E(2), collagenase, and cell death responses depend on cyclical load magnitude in an explant model of tendinopathy. Connect. Tissue Res. 51, 306-313. (doi:10.3109/03008200903318261)
56. Arnoczky SP, Lavagnino M, Egerbacher M. 2007 The mechanobiological aetiopathogenesis of tendinopathy: is it the over-stimulation or the under-stimulation of tendon cells? Int. J. Exp. Pathol. 88, 217-226. (doi:10.1111/j.1365-2613.2007.00548.x)