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Home / Equine Research Bank / Vet Med Sci / Equine tendon mechanical behaviour: Prospects for repair and...
Veterinary medicine and science2023; doi: 10.1002/vms3.1205

Equine tendon mechanical behaviour: Prospects for repair and regeneration applications.

Abstract: Tendons are dense connective tissues that play an important role in the biomechanical function of the musculoskeletal system. The mechanical forces have been implicated in every aspect of tendon biology. Tendon injuries are frequently occurring and their response to treatments is often unsatisfactory. A better understanding of tendon biomechanics and mechanobiology can help develop treatment options to improve clinical outcomes. Recently, tendon tissue engineering has gained more attention as an alternative treatment due to its potential to overcome the limitations of current treatments. This review first provides a summary of tendon mechanical properties, focusing on recent findings of tendon mechanobiological responses. In the next step, we highlight the biomechanical parameters of equine energy-storing and positional tendons. The final section is devoted to how mechanical loading contributes to tenogenic differentiation using bioreactor systems. This study may help develop novel strategies for tendon injury prevention or accelerate and improve tendon healing.
© 2023 The Authors. Veterinary Medicine and Science published by John Wiley & Sons Ltd.
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Publication Date: 2023-07-20 PubMed ID: 37471573DOI: 10.1002/vms3.1205Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research study explores the mechanical behaviour of equine tendons and the possibilities for their repair, regeneration and treatment of injuries through the application of tendon tissue engineering. The research aims to shed light on how mechanical loading contributes towards tendon regeneration.

Tendon Biomechanics and Mechanobiology

  • This section of the research discusses the mechanical properties of tendons, a dense connective tissue with significant role in musculoskeletal functioning. It elaborates on how mechanical forces are linked with every aspect of tendon biology and how a better comprehension of these factors can aid in finding effective treatments for tendon injuries. Tendon injuries are common and often respond poorly to existing treatments.

Tendon Tissue Engineering

  • The researchers have also examined the possible applications of tendon tissue engineering for the treatment of tendon injuries. Due to the limitations of current treatments for tendon injuries, tendon tissue engineering has emerged as a possible alternative to meet these challenges. It has the potential to augment and expedite the healing process of these injuries.

Biomechanical Parameters of Equine Tendons

  • The study further evaluates the biomechanical parameters of equine energy-storing and positional tendons. Understanding these parameters are critical to the investigation as it forms the basis of the study.

Impact of Mechanical Loading on Tenogenic Differentiation

  • The last section of study examines the effects of mechanical loading on tenogenic differentiation. Specifically, the study looks at using bioreactor systems to understand how mechanical loading supports the differentiation and growth of tenocytes. The findings from this section will offer avenues for implementing new strategies for preventing tendon injuries or improving the speed and quality of tendon healing.

Cite This Article

APA
Shojaee A. (2023). Equine tendon mechanical behaviour: Prospects for repair and regeneration applications. Vet Med Sci. https://doi.org/10.1002/vms3.1205

Publication

Veterinary medicine and science
ISSN: 2053-1095
NlmUniqueID: 101678837
Country: England
Language: English

Researcher Affiliations

Shojaee, Asiyeh
  • Division of Physiology, Department of Basic Sciences, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran.

References

This article includes 122 references
  1. Aeberhard P-A, Grognuz A, Peneveyre C, McCallin S, Hirt-Burri N, Antons J, Pioletti D, Raffoul W, Applegate L A. Efficient decellularization of equine tendon with preserved biomechanical properties and cytocompatibility for human tendon surgery indications. Artificial Organs 2020;44:E161-171.
  2. Agut A, Martínez M L, Sánchez-Valverde M A, Soler M, Rodríguez M J. Ultrasonographic characteristics (cross-sectional area and relative echogenicity) of the digital flexor tendons and ligaments of the metacarpal region in Purebred Spanish horses. The Veterinary Journal 2009;180:377-383.
  3. Altmann B, Grun C, Nies C, Gottwald E. Advanced 3D cell culture techniques in micro-bioreactors, Part II: Systems and applications. Processes 2021;9:21-74.
  4. Arvind V, Huang A H. Mechanobiology of limb musculoskeletal development. Annals of the New York Academy of Sciences 2017;1409:18-32.
  5. Arya S, Kulig K. Tendinopathy alters mechanical and material properties of the Achilles tendon. Journal of Applied Physiology 2010;108:670-675.
  6. Atkinson F, Evans R, Guest J E, Bavin E P, Cacador D, Holland C, Guest D J. Cyclical strain improves artificial equine tendon constructs in vitro. Journal of Tissue Engineering and Regenerative Medicine 2020;14:690-700.
  7. Ault B, Starling G, Parkes R, Pfau T, Pardoe C, Day P, Bettison C, Weller R. The effect of three different shoeing conditions on tendon strain in the thoroughbred forelimb. Equine Veterinary Journal 2015;47:17-17.
  8. Bavin E P, Smith O, Baird A E G, Smith L C, Guest D J. Equine induced pluripotent stem cells have a reduced tendon differentiation capacity compared to embryonic stem cells. Frontiers in Veterinary Science 2015;2:55-67.
  9. Beach Z M, Dekhne M S, Rodriguez A B, Weiss S N, Adams T H, Adams S M, Sun M, Birk D E, Soslowsky L J. Decorin knockdown is beneficial for aged tendons in the presence of biglycan expression. Matrix Biology Plus 2022;15:100114.
  10. Benage L G, Sweeney J D, Giers M B, Balasubramanian R. Dynamic load model systems of tendon inflammation and mechanobiology. Frontiers in Bioengineering and Biotechnology 2022;10:896336.
  11. Birch H L. Tendon matrix composition and turnover in relation to functional requirements. International Journal of Experimental Pathology 2007;88:241-248.
  12. Birch H L, Thorpe C T, Rumian A P. Specialisation of extracellular matrix for function in tendons and ligaments. Muscles, Ligaments and Tendons Journal 2013;3:12-23.
  13. Birch H L, Wilson A M, Goodship A E. Physical activity: Does long-term, high-intensity exercise in horses result in tendon degeneration?. Journal of Applied Physiology 2008;105:1927-1933.
  14. Bolanos R A V, Cokelaere S M, McDermott J M E, Benders K E M, Gbureck U, Plomp S G M, Weinans H, Groll J, van Weeren P R, Malda J. The use of a cartilage decellularized matrix scaffold for the repair of osteochondral defects: The importance of long-term studies in a large animal model. Osteoarthritis Cartilage 2017;25:413-420.
  15. Bosch G, Lameris M C, van Den Belt A J M, Barneveld A, van Weeren P R. The propagation of induced tendon lesions in the equine superficial digital flexor tendon: An ex vivo study. Equine Veterinary Journal 2010;42:407-411.
  16. Burk J, Plenge A, Brehm W, Heller S, Pfeiffer B, Kasper C. Induction of tenogenic differentiation mediated by extracellular tendon matrix and short-term cyclic stretching. Stem Cells International 2016;2016:11.
    doi: 10.1155/2016/7342379google scholar: lookup
  17. Chen K, Hu X, Blemker S S, Holmes J W. Multiscale computational model of Achilles tendon wound healing: Untangling the effects of repair and loading. PLoS Computational Biology 2018;14:e1006652-1006672.
  18. Chen X, Yin Z, Chen J-L, Shen W-L, Liu H-H, Tang Q-M, Fang Z, Lu L-R, Ji J, Ouyang H-W. Force and scleraxis synergistically promote the commitment of human ES cells derived MSCs to tenocytes. Scientific Reports 2015;2:977.
  19. Cherdchutham W, Meershoek L S, van Weeren P R, Barneveld A. Effects of exercise on biomechanical properties of the superficial digital flexor tendon in foals. American Journal of Veterinary Research 2001;62:1859-1864.
  20. Cornelisse C J, Robinson N E. Glucocorticoid therapy and the risk of equine laminitis. Equine Veterinary Education 2013;25:39-46.
  21. Crevier-Denoix N, Collobert C, Pourcelot P, Denoix J M, Sanaa M, Geiger D, Bernard N, Ribot X, Bortolussi C, Bousseau B. Mechanical properties of pathological equine superficial digital flexor tendons. Equine Veterinary Journal 1997;29:23-26.
  22. David F, Cadby J, Bosch G, Brama P, van Weeren R, Van Schie H. Short-term cast immobilisation is effective in reducing lesion propagation in a surgical model of equine superficial digital flexor tendon injury. Equine Veterinary Journal 2012;44:570-575.
  23. De Micheli A J, Swanson J B, Disser N P, Martinez L M, Walker N R, Oliver D J, Cosgrove B D, Mendias C L. Single-cell transcriptomic analysis identifies extensive heterogeneity in the cellular composition of mouse Achilles tendons. American Journal of Physiology-Cell Physiology 2020;319:C885-C894.
  24. Dean B J F, Lostis E, Oakley T, Rombach I, Morrey M E, Carr A J. The risks and benefits of glucocorticoid treatment for tendinopathy: A systematic review of the effects of local glucocorticoid on tendon. Semin arthritis rheum 2014;pp.570-576.
  25. Diloksumpan P, Bolanos R V, Cokelaere S, Pouran B, de Grauw J, van Rijen M, van Weeren R, Levato R, Malda J. Orthotopic bone regeneration within 3D printed bioceramic scaffolds with region-dependent porosity gradients in an equine model. Advanced Healthcare Materials 2020;9:1901807-1901811.
  26. Disser N P, Piacentini A N, De Micheli A J, Schonk M M, Yao V J H, Deng X-H, Oliver D J, Rodeo S A. Achilles tendons display region-specific transcriptomic signatures associated with distinct mechanical properties. The American Journal of Sports Medicine 2022;50:3866-3874.
  27. Docheva D, Müller S A, Majewski M, Evans C H. Biologics for tendon repair. Advanced Drug Delivery Reviews 2015;84:222-239.
  28. Dowling B A, Dart A J. Mechanical and functional properties of the equine superficial digital flexor tendon. The Veterinary Journal 2005;170:184-192.
  29. Dudhia J, Scott C M, Draper E R C, Heinegard D, Pitsillides A A, Smith R K. Aging enhances a mechanically-induced reduction in tendon strength by an active process involving matrix metalloproteinase activity. Aging Cell 2007;6:547-556.
  30. Dyment N A, Barrett J G, Awad H A, Bautista C A, Banes A J, Butler D L. A brief history of tendon and ligament bioreactors: Impact and future prospects. Journal of Orthopaedic Research 2020;38:2318-2330.
  31. Edom-Vovard F D R, Schuler B, Bonnin M-A, Teillet M-A E, Duprez D. Fgf4 positively regulates scleraxis and tenascin expression in chick limb tendons. Developmental Biology 2002;247:351-366.
  32. Edwards L J, Goodship A E, Birch H L, Patterson-Kane J C. Effect of exercise on age-related changes in collagen fibril diameter distributions in the common digital extensor tendons of young horses. American Journal of Veterinary Research 2005;66:564-568.
  33. Ehrle A, Lilge S, Clegg P D, Maddox T W. Equine flexor tendon imaging part 1: Recent developments in ultrasonography, with focus on the superficial digital flexor tendon. The Veterinary Journal 2021;278:105764.
  34. Eisner L E, Rosario R, Andarawis-Puri N, Arruda E M. The role of the non-collagenous extracellular matrix in tendon and ligament mechanical behavior: A review. Journal of Biomechanical Engineering 2022;144:050801.
  35. Engebretson B, Mussett Z R, Sikavitsas V I. The effects of varying frequency and duration of mechanical stimulation on a tissue-engineered tendon construct. Connective Tissue Research 2018;59:167-177.
  36. Fleischhacker V, Klatte-Schulz F, Minkwitz S, Schmock A, Rummler M, Seliger A, Willie B M, Wildemann B. In vivo and in vitro mechanical loading of mouse Achilles tendons and tenocytes-A pilot study. International Journal of Molecular Sciences 2020;21:1313-1328.
  37. Govoni M, Berardi A C, Muscari C, Campardelli R, Bonafe F, Guarnieri C, Reverchon E, Giordano E, Maffulli N, Della Porta G. An engineered multiphase three-dimensional microenvironment to ensure the controlled delivery of cyclic strain and human growth differentiation factor 5 for the tenogenic commitment of human bone marrow mesenchymal stem cells. Tissue Engineering Part A 2017;23:811-822.
  38. Grier W K, Moy A S, Harley B A C. Cyclic tensile strain enhances human mesenchymal stem cell Smad 2/3 activation and tenogenic differentiation in anisotropic collagen-glycosaminoglycan scaffolds. European Cells & Materials 2017;33:227-239.
  39. Groppi L. Stride frequency and stride length in horses performing treadmill endurance exercise. .
  40. Gruyaert M, Pollard D, Dyson S J. An investigation into the occurrence of, and risk factors for, concurrent suspensory ligament injuries in horses with hindlimb proximal suspensory desmopathy. Equine Veterinary Education 2020;32:173-182.
  41. Guney A, Vatansever F, Karaman I, Kafadar I H, Oner M, Turk C Y. Biomechanical properties of Achilles tendon in diabetic vs. non-diabetic patients. Experimental and Clinical Endocrinology & Diabetes 2015;123:428-432.
  42. Heinemeier K M, Kjaer M. In vivo investigation of tendon responses to mechanical loading. Journal of Musculoskeletal & Neuronal Interactions 2011;11:115-123.
  43. Ikeda Y, Ishihara A, Nakajima M, Yamada K. Risk factors for superficial digital flexor tendinopathy in Thoroughbred racing horses in Japan. Journal of Equine Science 2019;30:93-98.
  44. Iozzo R V, Schaefer L. Proteoglycan form and function: A comprehensive nomenclature of proteoglycans. Matrix Biology 2016;42:11-55.
  45. Izu Y, Adams S M, Connizzo B K, Beason D P, Soslowsky L J, Koch M, Birk D E. Collagen XII mediated cellular and extracellular mechanisms regulate establishment of tendon structure and function. Matrix Biology 2021;95:52-67.
  46. Kaya D Ö. Architecture of tendon and ligament and their adaptation to pathological conditions. In Comparative kinesiology of the human body 2020;pp.115-147.
  47. Kayama T, Mori M, Ito Y, Matsushima T, Nakamichi R, Suzuki H, Ichinose S, Saito M, Marumo K, Asahara H. Gtf2ird1-dependent Mohawk expression regulates mechanosensing properties of the tendon. Molecular and Cellular Biology 2016;36:1297-1310.
  48. Kendal A R, Layton T, Al-Mossawi H, Appleton L, Dakin S, Brown R, Loizou C, Rogers M, Sharp R, Carr A. Multi-omic single cell analysis resolves novel stromal cell populations in healthy and diseased human tendon. Scientific Reports 2020;10:1-14.
  49. Kim J J, Musson D S, Matthews B G, Cornish J, Anderson I A, Shim V B. Applying physiologically relevant strains to tenocytes in an in vitro cell device induces in vivo like behaviors. Journal of Bionic Engineering 2016;138:121003-121012.
  50. Kraus A, Luetzenberg R, Abuagela N, Hollenberg S, Infanger M. Spheroid formation and modulation of tenocyte-specific gene expression under simulated microgravity. Muscles, Ligaments and Tendons Journal 2017;7:411-417.
  51. Lee C. Tendon physiology and repair. Orthopaedics and Trauma 2021;35:274-281.
  52. Legerlotz K, Riley G P, Screen H R C. GAG depletion increases the stress-relaxation response of tendon fascicles, but does not influence recovery. Acta Biomaterialia 2013;9:6860-6866.
  53. Lipman K, Wang C, Ting K, Soo C, Zheng Z. Tendinopathy: Injury, repair, and current exploration. Drug Design, Development and Therapy 2018;12:591-603.
  54. Liu H, Zhu S, Zhang C, Lu P, Hu J, Yin Z, Chen X, OuYang H. Crucial transcription factors in tendon development and differentiation: Their potential for tendon regeneration. Cell and Tissue Research 2014;356:287-298.
  55. Liu X, Liu J, Lin S, Zhao X. Hydrogel machines. Materials Today 2020;36:102-124.
  56. Logan A A, Nielsen B D. Training young horses: The science behind the benefits. Animals 2021;11:463-476.
  57. Lozano P F, Scholze M, Babian C, Scheidt H, Vielmuth F, Waschke J, Ondruschka B, Hammer N. Water-content related alterations in macro and micro scale tendon biomechanics. Scientific Reports 2019;9:1-12.
  58. Lui P P Y, Maffulli N, Rolf C, Smith R K W. What are the validated animal models for tendinopathy?. Scandinavian Journal of Medicine & Science in Sports 2011;21:3-17.
  59. Maeda T, Sakabe T, Sunaga A, Sakai K, Rivera A L, Keene D R, Sasaki T, Stavnezer E, Iannotti J, Schweitzer R. Conversion of mechanical force into TGF-B-mediated biochemical signals. Current Biology 2011;21:933-941.
  60. Maredziak M, Marycz K, Lewandowski D, Siudzinska A, Smieszek A. Static magnetic field enhances synthesis and secretion of membrane-derived microvesicles (MVs) rich in VEGF and BMP-2 in equine adipose-derived stromal cells (EqASCs)-a new approach in veterinary regenerative medicine. In vitro Cellular & Developmental Biology Animal 2015;51:230-240.
  61. Moffat P A, Firth E C, Rogers C W, Smith R K W, Barneveld A, Goodship A E, Kawcak C E, McIlwraith C W, van Weeren P R. The influence of exercise during growth on ultrasonographic parameters of the superficial digital flexor tendon of young thoroughbred horses. Equine Veterinary Journal 2008;40:136-140.
  62. Murray R C, Dyson S J, Tranquille C, Adams V. Association of type of sport and performance level with anatomical site of orthopaedic injury diagnosis. Equine Veterinary Journal 2006;38:411-416.
  63. Nirmalanandhan V S, Dressler M R, Shearn J T, Juncosa-Melvin N, Rao M, Gooch C, Bradica G, Butler D L. Mechanical stimulation of tissue engineered tendon constructs: Effect of scaffold materials. Journal of Biomechanical Engineering 2007;129:919-923.
  64. Nourissat G, Berenbaum F, Duprez D. Tendon injury: From biology to tendon repair. Nature Reviews Rheumatology 2015;11:223-233.
  65. O'Brien C, Marr N, Thorpe C. Microdamage in the equine superficial digital flexor tendon. Equine Veterinary Journal 2021;53:417-430.
  66. Oswald I, Rickert M, Bruggemann G-P, Niehoff A, Ulloa C A F, Jahnke A. The influence of cryopreservation and quick-freezing on the mechanical properties of tendons. Journal of Biomechanics 2017;64:226-230.
  67. Pan X S, Li J, Brown E B, Kuo C K. Embryo movements regulate tendon mechanical property development. Philosophical Transactions of the Royal Society B: Biological Sciences 2018;373:20170325.
  68. Patel D, Zamboulis D E, Spiesz E M, Birch H L, Clegg P D, Thorpe C T, Screen H R C. Structure-function specialisation of the interfascicular matrix in the human Achilles tendon. Acta Biomaterialia 2021;131:381-390.
  69. Posey K L, Coustry F, Hecht J T. Cartilage oligomeric matrix protein: COMPopathies and beyond. Matrix Biology 2018;71:161-173.
  70. Raabe O, Shell K, Fietz D, Freitag C, Ohrndorf A, Christ H J, Wenisch S, Arnhold S. Tenogenic differentiation of equine adipose-tissue-derived stem cells under the influence of tensile strain, growth differentiation factors and various oxygen tensions. Cell and Tissue Research 2013;352:509-521.
  71. Revell C K, Jensen O E, Shearer T, Lu Y, Holmes D F, Kadler K E. Collagen fibril assembly: New approaches to unanswered questions. Matrix Biology Plus 2021;12:100079.
  72. Ribitsch I, Gueltekin S, Keith M F, Minichmair K, Peham C, Jenner F, Egerbacher M. Age-related changes of tendon fibril micro-morphology and gene expression. Journal of Anatomy 2020;236:688-700.
  73. Rinoldi C, Costantini M, Kijeńska-Gawrońska E, Testa S, Fornetti E, Heljak M, Ćwiklińska M, Buda R, Baldi J, Cannata S. Tendon tissue engineering: Effects of mechanical and biochemical stimulation on stem cell alignment on cell-laden hydrogel yarns. Advanced Healthcare Materials 2019;8:1801218-1801228.
  74. Salehi-Nik N, Amoabediny G, Pouran B, Tabesh H, Shokrgozar M A, Haghighipour N, Khatibi N, Anisi F, Mottaghy K, Zandieh-Doulabi B. Engineering parameters in bioreactor's design: A critical aspect in tissue engineering. BioMed Research International 2013;2013:15.
    doi: 10.1155/2013/762132google scholar: lookup
  75. Schiele N R, Marturano J E, Kuo C K. Mechanical factors in embryonic tendon development: Potential cues for stem cell tenogenesis. Current Opinion in Biotechnology 2013;24:834-840.
  76. Schneider M, Angele P, Jarvinen T A H, Docheva D. Rescue plan for Achilles: Therapeutics steering the fate and functions of stem cells in tendon wound healing. Advanced Drug Delivery Reviews 2018;129:352-375.
  77. Schwartz M A. Integrins and extracellular matrix in mechanotransduction. Cold Spring Harbor Perspectives in Biology 2010;2:a005066-005080.
  78. Screen H R C, Berk D E, Kadler K E, Ramirez F, Young M F. Tendon functional extracellular matrix. Journal of Orthopaedic Research 2015;33:793-799.
  79. Sheng R, Jiang Y, Backman L J, Zhang W, Chen J. The application of mechanical stimulations in tendon tissue engineering. Stem Cells International 2020;2020:8824783.
  80. Shojaee A, Parham A. Strategies of tenogenic differentiation of equine stem cells for tendon repair: Current status and challenges. Stem Cell Research & Therapy 2019;10:181-194.
  81. Shojaee A, Ejeian F, Parham A, Nasr-Esfahani M H. Optimizing Tenogenic Differentiation of Equine Adipose-Derived Mesenchymal Stem Cells (eq-ASC) Using TGFB3 Along with BMP Antagonists. Cell Journal (Yakhteh) 2022;24:370-379.
  82. Shojaee A, Parham A, Ejeian F, Esfahani M H N. Equine adipose mesenchymal stem cells (eq-ASCs) appear to have higher potential for migration and musculoskeletal differentiation. Research in Veterinary Science 2019;125:235-243.
  83. Subramanian A, Schilling T F. Tendon development and musculoskeletal assembly: Emerging roles for the extracellular matrix. Development 2015;142:4191-4204.
  84. Svard A, Hammerman M, Eliasson P. Elastin levels are higher in healing tendons than in intact tendons and influence tissue compliance. FASEB Journal 2020;34:13409-13418.
  85. Svensson R B, Heinemeier K M, Couppe C, Kjaer M, Magnusson S P. Effect of aging and exercise on the tendon. Journal of Applied Physiology 2016;121:1353-1362.
  86. Takahashi T, Yoshihara E, Mukai K, Ohmura H, Hiraga A. Use of an implantable transducer to measure force in the superficial digital flexor tendon in horses at walk, trot and canter on a treadmill. Equine Veterinary Journal 2010;42:496-501.
  87. Talo G, DArrigo D, Lorenzi S, Moretti M, Lovati A B. Independent, controllable stretch-perfusion bioreactor chambers to functionalize cell-seeded decellularized tendons. Annals of Biomedical Engineering 2020;48:1112-1126.
  88. Theiss F, Mirsaidi A, Mhanna R, Kummerle J, Glanz S, Bahrenberg G, Tiaden A N, Richards P J. Use of biomimetic microtissue spheroids and specific growth factor supplementation to improve tenocyte differentiation and adaptation to a collagen-based scaffold in vitro. Biomaterials 2015;69:99-109.
  89. Thorpe C T, Birch H L, Clegg P D, Screen H R C. The role of the non-collagenous matrix in tendon function. Journal of Experimental Pathology 2013;94:248-259.
  90. Thorpe C T, Chaudhry S, Lei I I, Varone A, Riley G P, Birch H L, Clegg P D, Screen H R C. Tendon overload results in alterations in cell shape and increased markers of inflammation and matrix degradation. Scandinavian Journal of Medicine & Science in Sports 2015;25:e381-e391.
  91. Thorpe C T, Clegg P D, Birch H L. A review of tendon injury: Why is the equine superficial digital flexor tendon most at risk?. Equine Veterinary Journal 2010;42:174-180.
  92. Thorpe C T, Karunaseelan K J, Ng Chieng Hin J, Riley G P, Birch H L, Clegg P D, Screen H R C. Distribution of proteins within different compartments of tendon varies according to tendon type. Journal of Anatomy 2016;229:450-458.
  93. Thorpe C T, Klemt C, Riley G P, Birch H L, Clegg P D, Screen H R C. Helical sub-structures in energy-storing tendons provide a possible mechanism for efficient energy storage and return. Acta Biomaterialia 2013;9:7948-7956.
  94. Thorpe C T, Peffers M J, Simpson D, Halliwell E, Screen H R C, Clegg P D. Anatomical heterogeneity of tendon: Fascicular and interfascicular tendon compartments have distinct proteomic composition. Scientific Reports 2016;6:20455-20467.
  95. Thorpe C T, Riley G P, Birch H L, Clegg P D, Screen H R C. Fascicles and the interfascicular matrix show adaptation for fatigue resistance in energy storing tendons. Acta Biomaterialia 2016;42:308-315.
  96. Thorpe C T, Streeter I, Pinchbeck G L, Goodship A E, Clegg P D, Birch H L. Aspartic acid racemization and collagen degradation markers reveal an accumulation of damage in tendon collagen that is enhanced with aging. The Journal of Biological Chemistry 2010;285:15674-15681.
  97. Thorpe C T, Udeze C P, Birch H L, Clegg P D, Screen H R C. Specialization of tendon mechanical properties results from interfascicular differences. Journal of the Royal Society, Interface 2012;9:3108-3117.
  98. Thorpe C T, Udeze C P, Birch H L, Clegg P D, Screen H R C. Capacity for sliding between tendon fascicles decreases with ageing in injury prone equine tendons: A possible mechanism for age-related tendinopathy. European Cells & Materials 2013;25:48-60.
  99. Tomas A R, Goncalves A I, Paz E, Freitas P, Domingues R M A, Gomes M E. Magneto-mechanical actuation of magnetic responsive fibrous scaffolds boosts tenogenesis of human adipose stem cells. Nanoscale 2019;11:18255-18271.
  100. Tomlinson D J, Erskine R M, Morse C I, Pappachan J M, Sanderson-Gillard E, Onambele-Pearson G L. The combined effects of obesity and ageing on skeletal muscle function and tendon properties in vivo in men. Endocrine 2021;72:411-422.
  101. Verkade M E, Back W, Birch H L. Equine digital tendons show breed-specific differences in their mechanical properties that may relate to athletic ability and predisposition to injury. Equine Veterinary Journal 2019;52:320-325.
  102. Verkade M E, Hazeleger E, van de Lest C H A, Back W. Biochemical differences between distal limb extensor and flexor tendons among equine breeds selected for racing and sport. The Veterinary Journal 2020;262:105515-105521.
  103. Walia B, Huang A H. Tendon stem progenitor cells: Understanding the biology to inform therapeutic strategies for tendon repair. Journal of Orthopaedic Research 2019;37:1270-1280.
  104. Wang H-N, Huang Y-C, Ni G-X. Mechanotransduction of stem cells for tendon repair. Western Journal of Speech Communication 2020;12:952-965.
  105. Wang J H C, Guo Q, Li B. Tendon biomechanics and mechanobiology-a mini-review of basic concepts and recent advancements. Journal of Hand Therapy 2012;25:133-141.
  106. Wang K, Zhao L. The influence of different modes of exercise on healthy and injured tendons. Stem Cells International 2022;2022:3945210.
  107. Wang T, Chen P, Zheng M, Wang A, Lloyd D, Leys T, Zheng Q, Zheng M H. In vitro loading models for tendon mechanobiology. Journal of Orthopedic Research 2018;36:566-575.
  108. Wang T, Gardiner B S, Lin Z, Rubenson J, Kirk T B, Wang A, Xu J, Smith D W, Lloyd D G, Zheng M H. Bioreactor design for tendon/ligament engineering. Tissue Engineering Part B: Reviews 2013;19:133-146.
  109. Wang T, Thien C, Wang C, Ni M, Gao J, Wang A, Jiang Q, Tuan R S, Zheng Q, Zheng M H. 3D uniaxial mechanical stimulation induces tenogenic differentiation of tendon-derived stem cells through a PI3K/AKT signaling pathway. FASEB Journal 2018;32:4804-4814.
  110. Wren T A L, Yerby S A, Beaupre G S, Carter D R. Mechanical properties of the human Achilles tendon. Clinical Biomechanics 2001;16:245-251.
  111. Xu B, Song G, Ju Y, Li X, Song Y, Watanabe S. RhoA/ROCK, cytoskeletal dynamics, and focal adhesion kinase are required for mechanical stretch-induced tenogenic differentiation of human mesenchymal stem cells. Journal of Cellular Physiology 2012;227:2722-2729.
  112. Yang F, Zhang A, Richardson D W. Regulation of the tenogenic gene expression in equine tenocyte-derived induced pluripotent stem cells by mechanical loading and Mohawk. Stem Cell Research 2019;39:101489.
  113. Yang G, Rothrauff B B, Tuan R S. Tendon and ligament regeneration and repair: Clinical relevance and developmental paradigm. Birth Defects Research Part C, Embryo Today: Reviews 2016;99:203-222.
  114. Youngstrom D W, LaDow J E, Barrett J G. Tenogenesis of bone marrow-, adipose-, and tendon-derived stem cells in a dynamic bioreactor. Connective Tissue Research 2016;57:454-465.
  115. Youngstrom D W, Rajpar I, Kaplan D L, Barrett J G. A bioreactor system for in vitro tendon differentiation and tendon tissue engineering. Journal of Orthopedic Research 2015;33:911-918.
  116. Zabrzyński J, Zabrzyńska A, Grzanka D. Tendon-function-related structure, simple healing process and mysterious ageing. Folia Morphologica 2018;77:416-427.
  117. Zamboulis D E, Marr N, Lenzi L, Birch H L, Screen H R C, Clegg P D, Thorpe C T. The interfascicular matrix of energy storing tendons houses heterogenous cell populations disproportionately affected by ageing. Aging and Disease 2023;14(6):16.
    doi: 10.1101/2023.01.04.522701google scholar: lookup
  118. Zamboulis D E, Thorpe C T, Kharaz Y A, Birch H L, Screen H R C, Clegg P D. Postnatal mechanical loading drives adaptation of tissues primarily through modulation of the non-collagenous matrix. Elife 2020;9:e58075.
  119. Zhang G, Zhou X, Hu S, Jin Y, Qiu Z. Large animal models for the study of tendinopathy. Frontiers in Cell and Developmental Biology 2022;10:1031638.
  120. Zhang J, Wang J H-C. Mechanobiological response of tendon stem cells: Implications of tendon homeostasis and pathogenesis of tendinopathy. Journal of Orthopedic Research 2010;28:639-643.
  121. Zhang Q, Adam N C, Nasab S H H, Taylor W R, Smith C R. Techniques for in vivo measurement of ligament and tendon strain: A review. Annals of Biomedical Engineering 2020;49:7-28.
  122. Zhang S, Ju W, Chen X, Zhao Y, Feng L, Yin Z, Chen X. Hierarchical ultrastructure: An overview of what is known about tendons and future perspective for tendon engineering. Bioactive Materials 2022;8:124-139.

Citations

This article has been cited 4 times.
  1. O Kadry M, Abdel-Megeed RM. Autophagy targeted nano-medicine in norphytane atrophic arthritis model: Beclin1/XBP/PTEN/STAT-3A genetic profile. Future Sci OA 2026 Dec;12(1):2580892.
    doi: 10.1080/20565623.2025.2580892pubmed: 41527390google scholar: lookup
  2. Iwasaki N, Llewellyn J, Brown J, Zamboulis DE, Finding EJT, Wheeler-Jones CPD, Thorpe CT. Immunolabelling and Micro-Computed Tomography Revealed Age-Related Alterations in 3D Microvasculature of Tendons. Aging Cell 2026 Jan;25(1):e70293.
    doi: 10.1111/acel.70293pubmed: 41250917google scholar: lookup
  3. Najeb M, Samy A, Rizk A, Mosbah E, Karrouf G. Regenerative biologics modulating inflammation and promoting tenogenesis in equine superficial digital flexor tendonitis: from molecular pathways to clinical translation. Ir Vet J 2025 Sep 17;78(1):21.
    doi: 10.1186/s13620-025-00309-zpubmed: 40963139google scholar: lookup
  4. Milczek-Haduch D, Żmigrodzka M, Witkowska-Piłaszewicz O. Extracellular Vesicles in Sport Horses: Potential Biomarkers and Modulators of Exercise Adaptation and Therapeutics. Int J Mol Sci 2025 May 3;26(9).
    doi: 10.3390/ijms26094359pubmed: 40362597google scholar: lookup
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