Abstract
The objective here was to experimentally characterize the temporal evolution of the structural and mechanical properties of large volume immature regenerated tissues. We studied these evolving tissues from their genesis in controlled mechanical conditions. We developed an animal model based on the periosteal properties leading to unloaded regenerated skeletal tissue. To characterize the temporal evolution of mechanical properties, we carried out indentation tests coupled with macroscopic examinations and histological studies. This combined methodology yielded a range of information on osteogenesis at different scales: macroscopic by simple observation, mesoscopic by indentation test and microscopic by histological study. Results allowed us to identify different periods, providing a link between biological changes and material property evolution in bone tissue regeneration. The regenerated tissue evolves from a viscous, homogeneous, soft material to a heterogeneous stiffer material endowed with a lower viscosity. From a biological point of view, cell organization progresses from a proliferated cell clot to a mature structure closer to that of the bone. During the first 7 days, mechanical and biological results revealed the same evolution: first, the regenerated tissue grew, then, differentiated into an osteochondral tissue and finally calcification began. While our biological results confirm those of other studies, our mechanical results provide the first experimental mechanical characterization by reduced Young’s modulus of such tissue.
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Buckwalter JA, Glimcher MJ, Cooper RR, Recker R (1995) Bone Biology. J Bone Joint Surg 77:1276–1289
Claes LE, Heigele CA (1999) Magnitudes of local stress and strain along bony surfaces predict the course and type of fracture healing. J Biomech 32:255–266
Caplan AI (1994) The mesengenic process. Clin Plast Surg 21:429–435
Carter DR, Blenman PR, Beaupre GS (1988) Correlations between mechanical stress history and tissue differentiation in initial fracture healing. J Orthop Res 6:736–748
Carter DR, Beaupre GS, Giori NJ, Helms JA (1998) Mechanobiology of skeletal regeneration. Clin Orthopaed Relat Res 355S:S41–S55
Cullinane DM, Salisbury KT, Alkhiary Y, Eisenberg S, Gerstenfeld L, Einhorn TA (2003) Effects of the local mechanical environment on vertebrate tissue differentiation during repair: does repair recapitulate development? J Exp Biol 206:2459–2471
Ferguson C, Alpern E, Miclau T, Helms JA (1999) Does adult fracture repair recapitulate embryonic skeletal formation? Mech Dev 87:57–66
Heegaar JH, Beaupre GS, Carter D (1999) Mechanically modulated cartilage growth may regulate joint surface morphogenesis. J Orthop Res 17:509–517
Huiskes R, Driel WD, Prendergast PJ, Soballe K (1997) A biomechanical regulatory model for periprosthetic fibrous-tissue differentiation. J Mater Sci Mater Med 8:785–788
Isaksson H, Comas O, Van Donkelaar CC, Mediavilla J, Wilson W, Huiskes R, Itoa K (2007) Bone regeneration during distraction osteogenesis: Mechano-regulation by shear strain and fluid velocity. J Biomech 40:2002–2011
Lacroix D, Prendergast PJ (2002) A mechano-regulation model for tissue differentiation during fracture healing: analysis of gap size and loading. J Biomech 35:1163–1171
Lacroix D, Prendergast PJ, Li G, Marsh D (2002) Biomechanical model to simulate tissue differentiation and bone regeneration: application to fracture healing. Med Biol Eng Comput 40:14–21
Lau A, Oyen ML, Kent RW, Murakami D, Torigaki T (2008) Indentation stiffness of aging human costal cartilage. Acta Biomater 4(1):97–103
Loboa EG, Wren TA, Beaupre GS, Carter DR (2003) Mechanobiology of soft skeletal tissue differentiation—a computational approach of a fiber-reinforced poroelastic model based on homogeneous and isotropic simplifications. Biomech Model Mechanobiol 2:83–96
Mikic B, Isenstein AL, Chhabra A (2004) Mechanical modulation of cartilage structure and function during embryogenesis in the chick. Ann Biomed Eng 32:18–25
Moukoko D, Pithioux M, Chabrand P (2007) Temporal evolution of mechanical properties of skeletal tissue regeneration in rabbits: an experimental study. Med Biol Eng Comput 45:989–995
O’Driscoll SW, Fitzsimmons JS (2001) The role of periosteum in cartilage repair. Clin Orthopaed Relat Res 391(Suppl):S190–S207
Oliver WC, Pharr GM (1992) An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J Mater Res 7(6):1564–1583
Oliver WC, Pharr GM (2004) Measurement of hardness and elastic modulus by instrumented indentation: advances in understanding and refinements to methodology. J Mater Res 19(1):3–20
Pailler-Mattéi C, Zahouani H (2006) Analysis of adhesive behaviour of human skin in vivo by an indentation test. Tribol Int 39:12–21
Pailler-Mattei C, Bec S, Zahouani H (2008) In vivo measurements of the elastic mechanical properties of human skin by indentation tests. Med Eng Phys 30:599–606
Pharr GM, Oliver WC, Brotzen FR (1992) On the Generality of the Relationship Between Contact Stiffness, Contact Area, and Elastic Moduli During Indentation. J Mater Res 7:613–617
Prendergast PJ, Huiskes R, Soballe K (1997) ESB Research Award 1996, Biophysical stimuli on cells during tissue differentiation at implant interfaces. J Biomech 30:539–548
Räsänen T, Messner K (1996) Regional variations of indentation stiffness and thickness of normal rabbit knee articular cartilage. J Biomed Mater Res 31:519–524
Roemhildt ML, Coughlin KM, Peura GD, Fleming BD, Beynnon BD (2006) Material properties of articular cartilage in the rabbit tibial plateau. J Biomech 39:2331–2337
Simon TM, Van Sickle DC, Kunishima DH, Jackson DW (2003) Cambium cell stimulation from surgical release of the periosteum. J Orthop Res 21:470–480
Soons JAM, Aernouts J, Dirckx JJJ (2010) Elasticity modulus of rabbit middle ear ossicles determined by a novel micro-indentation technique. Hear Res 263:33–37
Zhang J, Niebur GL, Ovaert TC (2008) Mechanical property determination of bone through nano- and micro-indentation testing and finite element simulation. J Biomech 41(2):267–275
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Casanova, R., Moukoko, D., Pithioux, M. et al. Temporal evolution of skeletal regenerated tissue: what can mechanical investigation add to biological?. Med Biol Eng Comput 48, 811–819 (2010). https://doi.org/10.1007/s11517-010-0637-7
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DOI: https://doi.org/10.1007/s11517-010-0637-7