Capacity for sliding between tendon fascicles decreases with ageing in injury prone equine tendons: A possible mechanism for age-related tendinopathy?

European Cells and Materials

Volumn 25, Issue , 2012, Pages 48-60

  Thorpe, Chavaunne T ^a,b   Udeze, Chineye P ^a   Birch, Helen L ^c   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 COLLEGE LONDON   (United Kingdom)

Author keywords

Ageing; Equine; Injury; Interfascicular matrix; Mechanics; Superficial digital flexor tendon; Tendon

Indexed keywords

AGE; AGING; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; COMMON DIGITAL EXTENSOR; CONTROLLED STUDY; DISEASE PREDISPOSITION; HORSE; MECHANICAL STRESS; MUSCULOSKELETAL FUNCTION; MUSCULOSKELETAL STIFFNESS; NONHUMAN; SUPERFICIAL DIGITAL FLEXOR; TENDINITIS; TENDON; TENDON FASCICLE SLIDING; ANIMAL; ANIMAL DISEASE; EXTRACELLULAR MATRIX; HORSE DISEASE; PATHOLOGY; PATHOPHYSIOLOGY; YOUNG MODULUS;

AGE FACTORS; AGING; ANIMALS; ELASTIC MODULUS; EXTRACELLULAR MATRIX; HORSE DISEASES; HORSES; TENDINOPATHY; TENDONS;

MLCS; MLOWN;

EID: 84878423070     PISSN: 14732262     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (57)

1. Alexander RM (1991) Energy-saving mechanisms in walking and running. J Exp Biol 160: 55-69.
2. Ãstrand H, Stalhand J, Karlsson J, Karlsson M, Sonesson B, Lanne T (2011) In vivo estimation of the contribution of elastin and collagen to the mechanical properties in the human abdominal aorta: effect of age and sex. J Appl Physiol 110: 176-187.
3. Avery NC, Bailey AJ (2005) Enzymic and non-enzymic cross-linking mechanisms in relation to turnover of collagen: relevance to aging and exercise. Scand J Med Sci Sports 15: 231-240.
4. Bank RA, Te Koppele JM, Oostingh G, Hazleman BL, Riley GP (1999) Lysylhydroxylation and non-reducible crosslinking of human supraspinatus tendon collagen: changes with age and in chronic rotator cuff tendinitis. Ann Rheum Dis 58: 35-41.
5. 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.
6. 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.
7. Birch HL (2007) Tendon matrix composition and turnover in relation to functional requirements. Int J Exp Pathol 88: 241-248.
8. Birch HL, Bailey JV, Bailey AJ, Goodship AE (1999) Age-related changes to the molecular and cellular components of equine flexor tendons. Equine Vet J 31: 391-396.
9. Birch HL, Smith TJ, Poulton C, Peiffer D, Goodship AE (2002) Do regional variations in flexor tendons predispose to site-specific injuries? Equine Vet J Suppl 34: 288-292.
10. Birch HL, Wilson AM, Goodship AE (2008) Physical activity: does long-term, high-intensity exercise in horses result in tendon degeneration? J Appl Physiol 105: 1927-1933.
11. 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.
12. Clayton RAE, Court-Brown CM (2008) The epidemiology of musculoskeletal tendinous and ligamentous injuries. Injury 39: 1338-1344.
13. Dahlgren LA, Brower-Toland BD, Nixon AJ (2005) Cloning and expression of type III collagen in normal and injured tendons of horses. Am J Vet Res 66: 266-270.
14. Dudhia J, Scott CM, Draper ERC, Heinegård D, Pitsillides AA, Smith RK (2007) Aging enhances a mechanically-induced reduction in tendon strength by an active process involving matrix metalloproteinase activity. Aging Cell 6: 547-556.
15. Elliott DM, Robinson PS, Gimbel JA, Sarver JJ, Abboud JA, Iozzo RV, Soslowsky LJ (2003) Effect of altered matrix proteins on quasilinear viscoelastic properties in transgenic mouse tail tendons. Ann Biomed Eng 31: 599-605.
16. Fallon J, Blevins FT, Vogel K, Trotter J (2002) Functional morphology of the supraspinatus tendon. J Orthop Res 20: 920-926.
17. 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.
18. Funakoshi T, Schmid T, Hsu H, Spector M (2008) Lubricin Distribution in the Goat Infraspinatus Tendon: A Basis for Interfascicular Lubrication. J Bone Joint Surg Am. 90: 803-814.
19. Gillis C, Sharkey N, Stover SM, Pool RR, Meagher DM, Willits N (1995) Effect of maturation and aging on material and ultrasonographic properties of equine superficial digital flexor tendon. Am J Vet Res 56: 1345-1350.
20. Gillis C, Pool RR, Meagher DM, Stover SM, Reiser K, Willits N (1997) Effect of maturation and aging on the histomorphometric and biochemical characteristics of equine superficial digital flexor tendon. Am J Vet Res 58: 425-430.
21. Goodship AE, Birch HL (2005) Cross sectional area measurement of tendon and ligament in vitro: a simple, rapid, non-destructive technique. J Biomech 38: 605-608.
22. Gupta HS, Seto J, Krauss S, Boesecke P, Screen HRC (2010) In situ multi-level analysis of viscoelastic deformation mechanisms in tendon collagen. J Struct Biol 169: 183-191.
23. Hess GW (2010) Achilles tendon rupture: a review of etiology, population, anatomy, risk factors, and injury prevention. Foot Ankle Spec 3: 29-32.
24. Hills BA (2000) Boundary lubrication in vivo. Proc Inst Mech Eng H 214: 83-94.
25. Innes JF, Clegg P (2010) Comparative rheumatology: what can be learnt from naturally occurring musculoskeletal disorders in domestic animals? Rheumatol 49: 1030-1039.
26. Ireland JL, Clegg PD, McGowan CM, McKane SA, Chandler KJ, Pinchbeck GL (2012) Disease prevalence in geriatric horses in the United Kingdom: veterinary clinical assessment of 200 cases. Equine Vet J 44: 101-106.
27. Kannus P (2000) Structure of the tendon connective tissue. Scand J Med Sci Sports 10: 312-320.
28. 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.
29. Kastelic J, Galeski A, Baer E (1978) The multicomposite structure of tendon. Connect Tissue Res 6: 11-23.
30. 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.
31. Kohrs RT, Zhao C, Sun Y-L, Jay GD, Zhang L, Warman ML, An K-N, Amadio PC (2011) Tendon fascicle gliding in wild type, heterozygous, and lubricin knockout mice. J Orthop Res 29: 384-389.
32. 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.
33. Legerlotz K, Riley GP, Screen HR (2010) Specimen dimensions influence the measurement of material properties in tendon fascicles. J Biomech 43: 2274-2280.
34. Legerlotz K, Jones GC, Screen HR, Riley GP (2011) Cyclic loading of tendon fascicles using a novel fatigue loading system increases interleukin-6 expression by tenocytes. Scand J Med Sci Sports DOI: 10.1111/j.1600-0838.2011.01410.x.
35. Lichtwark GA, Wilson AM (2005) In vivo mechanical properties of the human Achilles tendon during one-legged hopping. J Exp Biol 208: 4715-4725.
36. 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.
37. Maganaris CN, Paul JP (1999) In vivo human tendon mechanical properties. J Physiol 521: 307-313.
38. Patterson-Kane JC, Firth EC, Goodship AE, Parry DA (1997) Age-related differences in collagen crimp patterns in the superficial digital flexor tendon core region of untrained horses. Aust Vet J 75: 39-44.
39. Perkins NR, Reid SWJ, Morris RS (2005) Risk factors for injury to the superficial digital flexor tendon and suspensory apparatus in Thoroughbred racehorses in New Zealand. N Z Vet J 53: 184-192.
40. Reeves ND, Maganaris CN, Narici MV (2003) Effect of strength training on human patella tendon mechanical properties of older individuals. J Physiol 548: 971-981.
41. Reuvers J, Thoreson AR, Zhao C, Zhang L, Jay GD, An KN, Warman ML, Amadio PC (2011) The mechanical properties of tail tendon fascicles from lubricin knockout, wild type and heterozygous mice. J Struct Biol 176: 41-45.
42. Riemersa DJ, Schamhardt HC (1982) The cryo-jaw, a clamp designed for in vitro rheology studies of horse digital flexor tendons. J Biomech 15: 619-620.
43. Riley G (2008) Tendinopathy: from basic science to treatment. Nat Clin Pract Rheum 4: 82-89.
44. Riley GP, Harrall RL, Constant CR, Chard MD, Cawston TE, Hazleman BL (1994) Glycosaminoglycans of human rotator cuff tendons: changes with age and in chronic rotator cuff tendinitis. Ann Rheum Dis 53: 367-376.
45. Robinson PS, Lin TW, Reynolds PR, Derwin KA, Iozzo RV, Soslowsky LJ (2004) Strain-rate sensitive mechanical properties of tendon fascicles from mice with genetically engineered alterations in collagen and decorin. J Biomech Eng 126: 252-257.
46. Robinson PS, Huang TF, Kazam E, Iozzo RV, Birk DE, Soslowsky LJ (2005) Influence of decorin and biglycan on mechanical properties of multiple tendons in knockout mice. J Biomech Eng 127:181-185.
47. Screen HRC (2008) Investigating load relaxation mechanics in tendon. J Mech Behav Biomed Mater 1:51-58.
48. Smith RK, Birch HL, Goodman S, Heinegard D, Goodship AE (2002) The influence of ageing and exercise on tendon growth and degeneration--hypotheses for the initiation and prevention of strain-induced tendinopathies. Comp Biochem Physiol A Mol Integr Physiol 133: 1039-1050.
49. Smith KD, Vaughan-Thomas A, Spiller DG, Innes JF, Clegg PD, Comerford EJ (2011) The organisation of elastin and fibrillins 1 and 2 in the cruciate ligament complex. J Anat 218: 600-607.
50. 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.
51. Thorpe CT (2010) Extracellular matrix synthesis and degradation in functionally distinct tendons. PhD Thesis, University College London.
52. Thorpe CT, Clegg PD, Birch HL (2010a) A review of tendon injury: why is the equine superficial digital flexor tendon most at risk? Equine Vet J 42: 174-180.
53. Thorpe CT, Streeter I, Pinchbeck GL, Goodship AE, Clegg PD, Birch HL (2010b) Aspartic acid racemization and collagen degradation markers reveal an accumulation of damage in tendon collagen that is enhanced with aging. J Biol Chem 285: 15674-15681.
54. Thorpe CT, Udeze CP, Birch HL, Clegg PD, Screen HRC (2012) Specialisation of tendon mechanical properties results from inter-fascicular differences. J R Soc Interface 9: 3108-3117.
55. Wood LK, Arruda EM, Brooks SV (2011) Regional stiffening with aging in tibialis anterior tendons of mice occurs independent of changes in collagen fibril morphology. J Appl Physiol 111: 999-1006.
56. Wren TAL, Yerby SA, Beaupré GS, Carter DR (2001) Mechanical properties of the human achilles tendon. Clin Biomech 16: 245-251.
57. Yamamoto E, Iwanaga W, Yamamoto N, Hayashi K (2004) Growth-related changes in the mechanical properties of collagen fascicles from rabbit patellar tendons. Biorheology 41: 1-11.