Abstract
Composition and structural organization of tendon changes during aging and these alterations affect the mechanical behaviors of this structure. Therefore, this experiment was designed to study the biomechanical properties together with changes in dry weight content of normal superficial digital flexor tendon of rabbits from pre-natal stage to 112 days post-natally. Forty-two White New Zealand rabbits were assigned to seven different age groups (from 5–7 days before birth to 112 days after birth), each consisting of six animals. The right superficial digital flexor tendons were used for biomechanical studies and the left ones for percentage dry weight investigation. Ultimate tensile strength, stiffness, maximum energy, and percentage dry weight values significantly increased in each higher age group compared to those of the younger group and the yield strain and maximum strain decreased comparatively as a function of age. This improvement in the mechanical behavior of tendons during aging could be correlated with increase in collagen content, alteration in the collagen fibril differentiation and distribution from small-sized unimodal fibrils to trimodally distributed collagen fibrils, improvement in quantity and quality of the cross-linking, fibril continuity, type of collagen, development and maturation of crimp pattern, tissue alignment and organization. Therefore, characterization of mechanical behavior and tissue dry weight, as an index of collagen content, from fetal stage to skeletally mature animals is essential in better understanding the tissue structural development and hierarchical organization coincidental with the material properties of this organ.
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References
Allard P, Thiery PS, Bourgault A, Drouin G (1979) Pressure dependence of the area micrometer’ method in evaluation of cruciate ligament cross-section. J Biomed Eng 1:265–267, doi:10.1016/0141-5425(79)90163-8
Becker CK, Savelberg HH, Barneveld A (1994) In vitro mechanical properties of the accessory ligament of the deep digital flexor tendon in horses in relation to age. Equine Vet J 26:454–459
Beredjiklian PK, Favata M, Cartmell JS, Flanagan CL, Crombleholme TM, Soslowsky LJ (2003) Regenerative versus reparative healing in tendon: a study of biomechanical and histological properties in fetal sheep. Am Biomed Eng 31:1143–1152, doi:10.1114/1.1616931
Birk DE, Mayne R (1997) Localization of collagen types I, III and during tendon development. Changes in collagen types I and III are correlated with changes in fibril diameter. Eur J Cell Biol 72(4):352–361
Butler DL, Grood ES, Noyes FR (1978) Biomechanics of ligaments and tendons. Exerc Sport Sci Rev 6:125–181
Cribb AM, Scott JE (1995) Tendon response to tensile stress: an ultrastructural investigation of collagen: proteoglycan interactions in stressed tendon. J Anat 187:423–428
Flint MH, Craig AS, Reily HC, Gillard GC, Parry DAD (1984) Collagen fibril diameters and glycosaminoglycan content of skin-indices of tissue maturity and function. Connect Tissue Res 13:69–81, doi:10.3109/03008208409152144
Frank C, McDonald D, Bray D, Bray R, Rangayyan R, Chimich D et al (1992) Collagen fibril diameters in the healing adult rabbit medial collateral ligament. Connect Tissue Res 27:251–263, doi:10.3109/03008209209007000
Goodship AE, Cooke PH (1987) Biocompatibility of tendon and ligaments. Crit Rev Biocomp 2(2):303–334
Graham HK, Holmes DF, Watson RB, Kadler KE (2000) Identification of collagen fibril fusion during vertebrate tendon morphogenesis. The process relies on unipolar fibrils and is regulated by collagen-proteoglycan interaction. J Mol Biol 28:891–902, doi:10.1006/jmbi.1999.3384
Greiling H, Gressner AM, Stuhlsatz HW (1979) Effects of agents interacting with connective tissues. Agents Act Suppl 5:99–109
Hashemi J, Chandrashekar N, Slauterbeck J (2005) The mechanical properties of the human patellar tendon are correlated to its mass density and are independent of sex. Clin Biomech (Bristol, Avon) 20(6):645–652, doi:10.1016/j.clinbiomech.2005.02.008
Haut RC, Lancaster RL, Charles ED (1992) Mechanical properties of the canine patellar tendon: Some correlation with age and the content of collagen. J Biomech 25:163–173, doi:10.1016/0021-9290(92)90273-4
Ippolito E, Natali PG, Postacchini F, Accinni L, De Martino C (1980) Morphological, immunochemical and biochemical study of rabbit Achilles tendon at various ages. J Bone Joint Surg 62-A(4):583–598
Karpakka J, Vannannen K, Virtanen P, Savolainen J, Orava S, Takala TE (1990) The effects of remobilization and exercise on collagen biosynthesis in rat tendon. Acta Physiol Scand 139:139–145
McBride DJ, Hahn RA, Silver FH (1985) Morphological characterization of tendon development during chick embryogenesis: measurement of birefringence retardation. Int J Biol Macromol 7:71–76, doi:10.1016/0141-8130(85)90034-0
McPherson JM, Piez KA (1988) The molecular and cellular biology of wound repair. Plenum, New York, pp 471–496
Mitchell TW, Rigby BJ (1975) In vivo and in vitro ageing of collagen examined using isometric melting technique. Biochim Biophys Acta 393:531–541
Nordin M, Frankel VH (1980) Biomechanics of collagenous tissues. In: Frankel VH, Nordin M (eds) Basic biomechanics of the skeletal system. Lea and Febiger, Philadelphia, pp 87–110
Noyes FR, Butler DL, Grood ES, Zernicke RF, Hefzy MS (1984) Biomechanical analysis of human ligament grafts used in knee-ligament repairs and reconstructions. J Bone Joint Surg Am 66:344–352
Oryan A (1995) Role of collagen in soft connective tissue wound healing. Transplant Proc 27(5):2759–2761
Oryan A, Peyghan R (1996) Morphology and biomechanical properties of tendons and ligaments. J Fac Vet Med Tehran Univ 50(2):13–38
Oryan A, Shoushtari AH (2007) Histology and ultrastructure of the developing superficial digital flexor tendon in rabbits. Anat Histol Embryol 37:134–140, doi:10.1111/j.1439-0264.2007.00811.x
Oryan A, Peyghan R, Emami MJ (1993) The effects of physical activity on tendon healing. Iranian J Med Sci 18(2):13–20
Parry DAD, Barnes GRG, Craig AS (1978) A comparison of the size distribution of collagen fibrils in connective tissues as a function of age and a possible relation between fibril size distribution and mechanical properties. Proc R Soc London (Biol) 203:305–321
Parry DAD, Craig AS (1984) Growth and development of collagen fibrils. In: Ruggeri A, Motta PM (eds) Ultrastructure of the connective tissue matrix. Nijhoff, Boston, pp 34–64
Parry DAD, Flint MH, Gillard GC, Craig AS (1982) A role for glycosaminoglycan in the development of collagen. FEBS Lett 149(1):1–7, doi:10.1016/0014-5793(82)81060-0
Provenzano PP, Vanderby R Jr (2006) Collagen fibril morphology and organization: Implication for force transmission in ligament and tendon. Matrix Biol 25(2):71–84, doi:10.1016/j.matbio.2005.09.005
Provenzano PP, Alejandro-Osorio AL, Valhmu WB, Vandery R Jr (2005) Intrinsic fibroblast mediated remodeling of damaged collagenous matrices in vivo. Matrix Biol 23:543–555, doi:10.1016/j.matbio.2004.09.008
Raspanti M, Ottani V, Ruggeri A (1990) Subfibrillar architecture and functional properties of collagen: A comparative study in rat tendons. J Anat 172:157–164
Scott JE (1992) Supramolecular organization of extra-cellular matrix glycosaminoglycans, in vitro and in the tissues. Federat Am Scient Exp Biol J 6(9):2639–2645
Scott JE (1993) The nomenclature of the glycosaminoglycans and proteoglycans. Glycoconj J 10:2639–2645, doi:10.1007/BF00737960
Scott JE, Orford CR (1981) Dermatan sulphate proteoglycan associated with rat tail tendon collagen at the “d” band in the gap region. Biochem J 197:213–216
Shadwick ER (1990) Elastic energy storage in tendons: Mechanical differences related to function and age. J Appl Physiol 68:1033–1040, doi:10.1063/1.346741
Silver IA, Brown PN, Goodship AE, Lanyon LE, McCullagh KG, Perry GC et al (1985) A clinical and experimental study of tendon injury, healing and treatment in the horse. Equine Vet J Suppl 1:1–43
Silver FH, Freeman JW, Seehra GP (2003) Collagen self assembly and the development of tendon mechanical properties. J Biomech 36(10):1529–1553, doi:10.1016/S0021-9290(03)00135-0
Viidik A (1980) Interdependence between structure and function in collagenous tissues. In: Viddik A, Vuust J (eds) Biology of collagen. Academic, London, pp 257–280
Williams IF, McCullagh KG, Silver IA (1984) The distribution of types I and III collagen and fibronectin in the healing equine tendon. Connect Tissue Res 12:211–227, doi:10.3109/03008208409013684
Williams IF, Craig AS, Parry DAD, Goodship AE, Shah J, Silver IA (1985) Development of collagen fibril organization and collagen crimp pattern during tendon healing. Int J Biol Macromol 7:275–282, doi:10.1016/0141-8130(85)90025-X
Woo SL-Y, Ritter MA, Amiel D, Sanders TM, Gomez MA, Kuei SC et al (1980) The biomechanical and biochemical properties of swine tendons—long term effects of exercise on the digital extensors. Connect Tissue Res 7:177–183, doi:10.3109/03008208009152109
Woo SL-Y, Gomez MA, Akeson WH (1985) Mechanical behaviour of soft connective tissues: Measurements modification, injuries and treatment. In: Naham AM, Melvin J (eds) The biomechanics of trauma. Appleton-Century-Crofts, Norwalk, pp 109–133
Woo SL-Y, Inoue M, McGurk-Burleson E, Gomez MA (1987) Treatment of the medial collateral ligament injury II: Structure and function of canine knees response to differing treatment regimens. Am J Sports Med 15:22–29, doi:10.1177/036354658701500104
Zhang G, Young BB, Ezura Y, Favata M, Soslowsky LJ, Chakravarti S et al (2005) Development of tendon structure and function: regulation of collagen fibrillogenesis. J Musculoskelet Neuronal Interact 5(1):5–21
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Oryan, A., Shoushtari, A.H. Biomechanical properties and dry weight content of the developing superficial digital flexor tendon in rabbit. Comp Clin Pathol 18, 131–137 (2009). https://doi.org/10.1007/s00580-008-0764-9
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DOI: https://doi.org/10.1007/s00580-008-0764-9