Skip to main content
SpringerLink
Log in

In Vivo Mechanical Characterization of the Distraction Callus During Bone Consolidation

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

Understanding the evolution of callus mechanical properties over time provides insights in the mechanobiology of fracture healing and tissue differentiation, can be used to validate numerical models, and informs clinical practice. Bone transport experiments were performed in sheep, in which a distractor type Ilizarov was implanted. The forces through the fixator evolution were measured and the callus stiffness was estimated from these forces. Computerized tomography images were taken and bone volume of the callus at different stages was obtained. The results showed that the maximum bone tissue production rate (0.146 cm3/day) was achieved 20 days after the end of the distraction phase. 50 days after the end of the distraction phase, the callus was ossified completely and had its maximum volume, 6–10 cm3. In addition, 80–90% of the load sustained by the operated limb was recovered and the callus stiffness increased exponentially until 5.4–11.4 kN/mm, still below 10% of the healthy level of callus stiffness. The effects of the bony bridging of the callus and the time of the fixator removal on callus force, stiffness and volume were analyzed. These outcomes allowed relating quantifiable biological aspects (callus volume and tissue production rate) with mechanical parameters (callus force and stiffness) using data from the same experiment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  1. Aarnes, G. T., H. Steen, L. P. Kristiansen, E. Festø, and P. Ludvigsen. Optimum loading mode for axial stiffness testing in limb lengthening. J. Orthop. Res. 24:348–354, 2006.

    Article  PubMed  Google Scholar 

  2. Aarnes, G. T., H. Steen, P. Ludvigsen, N. A. Waanders, R. Huiskes, and S. A. Goldstein. In vivo assessment of regenerate axial stiffness in distraction osteogenesis. J. Orthop. Res. 23:494–498, 2005.

    Article  PubMed  Google Scholar 

  3. Aronson, J. Temporal and spatial increases in blood flow during distraction osteogenesis. Clin. Orthop. Relat. Res. 301:124–131, 1994.

    PubMed  Google Scholar 

  4. Aronson, J., and J. H. Harp. Mechanical forces as predictors of healing during tibial lengthening by distraction osteogenesis. Clin. Orthop. Relat. Res. 301:73–79, 1994.

    PubMed  Google Scholar 

  5. Aronson, J., B. H. Harrison, C. L. Stewart, and J. H. Harp, Jr. The histology of distraction osteogenesis using different external fixators. Clin. Orthop. Relat. Res. 241:106–116, 1989.

    PubMed  Google Scholar 

  6. Aronson, J., X. C. Shen, R. A. Skinner, W. R. Hogue, T. M. Badger, and C. K. Lumpkin, Jr. Rat model of distraction osteogenesis. J. Orthop. Res. 15:221–226, 1997.

    Article  CAS  PubMed  Google Scholar 

  7. Brunner, U. H., J. Cordey, L. Schweiberer, and S. M. Perren. Force required for bone segment transport in the treatment of large bone defects using medullary nail fixation. Clin. Orthop. Relat. Res. 301:147–155, 1994.

    PubMed  Google Scholar 

  8. Claes, L. E., and J. L. Cunningham. Monitoring the mechanical properties of healing bone. Clin. Orthop. Relat. Res. 467:1964–1971, 2009.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. Claes, L., R. Grass, T. Schmickal, B. Kisse, C. Eggers, H. Gerngross, W. Mutschler, M. Arand, T. Wintermeyer, and A. Wentzensen. Monitoring and healing analysis of 100 tibial shaft fractures. Langenbecks. Arch. Surg. 387:146–152, 2002.

    Article  CAS  PubMed  Google Scholar 

  10. Claes, L., J. Laule, K. Wenger, G. Suger, U. Liener, and L. Kinzl. The influence of stiffness of the fixator on maturation of callus after segmental transport. J. Bone Jt. Surg. Br. 82:142–148, 2000.

    Article  CAS  Google Scholar 

  11. Claes, L. E., H.-J. Wilke, P. Augat, S. Rübenacker, and K. J. Margevicius. Effect of dynamization on gap healing of diaphyseal fractures under external fixation. Clin. Biomech. (Bristol, Avon). 10:227–234, 1995.

    Article  PubMed  Google Scholar 

  12. Cunningham, J. L., J. Kenwright, and C. J. Kershaw. Biomechanical measurement of fracture healing. J. Med. Eng. Technol. 14:92–101, 1990.

    Article  CAS  PubMed  Google Scholar 

  13. De Pablos Jr, J., and J. Canadell. Experimental physeal distraction in immature sheep. Clin. Orthop. Relat. Res. 250:73–80, 1990.

    PubMed  Google Scholar 

  14. Delloye, C., G. Delefortrie, L. Coutelier, and A. Vincent. Bone regenerate formation in cortical bone during distraction lengthening. An experimental study. Clin. Orthop. Relat. Res. 250:34–42, 1990.

    PubMed  Google Scholar 

  15. Duda, G. N., K. Eckert-Hubner, R. Sokiranski, A. Kreutner, R. Miller, and L. Claes. Analysis of inter-fragmentary movement as a function of musculoskeletal loading conditions in sheep. J. Biomech. 31:201–210, 1998.

    Article  CAS  PubMed  Google Scholar 

  16. Dwyer, J. S., P. J. Owen, G. A. Evans, J. H. Kuiper, and J. B. Richardson. Stiffness measurements to assess healing during leg lengthening. A preliminary report. J. Bone. Jt. Surg. Br. 78:286–289, 1996.

    CAS  Google Scholar 

  17. Evans, F. G. Mechanical Properties of Bone. Springfield: Charles C. Thomas Publisher, 1973.

    Google Scholar 

  18. Floerkemeier, T., W. Aljuneidi, J. Reifenrath, N. Angrisani, D. Rittershaus, D. Gottschalk, S. Besdo, A. Meyer-Lindenberg, H. Windhagen, and F. Thorey. Telemetric in vivo measurement of compressive forces during consolidation in a rabbit model. Technol. Health Care 19:173–183, 2011.

    PubMed  Google Scholar 

  19. Floerkemeier, T., F. Thorey, C. Hurschler, M. Wellmann, F. Witte, and H. Windhagen. Stiffness of callus tissue during distraction osteogenesis. Orthop. Traumatol. Surg. Res. 96:155–160, 2010.

    Article  CAS  PubMed  Google Scholar 

  20. Forriol, F., L. Denaro, U. G. Longo, H. Taira, N. Maffulli, and V. Denaro. Bone lengthening osteogenesis, a combination of intramembranous and endochondral ossification: an experimental study in sheep. Strateg. Trauma Limb Reconstr. 5:71–78, 2010.

    Article  Google Scholar 

  21. Gardner, T. N., M. Evans, H. Simpson, and J. Kenwright. Force-displacement behaviour of biological tissue during distraction osteogenesis. Med. Eng. Phys. 20:708–715, 1998.

    Article  CAS  PubMed  Google Scholar 

  22. Grasa, J., M. J. Gomez-Benito, L. A. Gonzalez-Torres, D. Asiain, F. Quero, and J. M. Garcia-Aznar. Monitoring in vivo load transmission through an external fixator. Ann. Biomed. Eng. 38:605–612, 2010.

    Article  CAS  PubMed  Google Scholar 

  23. Hente, R., J. Cordey, and S. M. Perren. In vivo measurement of bending stiffness in fracture healing. Biomed. Eng. Online 2:8, 2003.

    Article  PubMed Central  PubMed  Google Scholar 

  24. Ilizarov, G. A. The tension-stress effect on the genesis and growth of tissues. Part I. The influence of stability of fixation and soft-tissue preservation. Clin. Orthop. Relat. Res. 238:249–281, 1989.

    PubMed  Google Scholar 

  25. Ilizarov, G. A. The tension-stress effect on the genesis and growth of tissues: Part II. The influence of the rate and frequency of distraction. Clin. Orthop. Relat. Res. 239:263–285, 1989.

    PubMed  Google Scholar 

  26. Isaksson, H., O. Comas, C. C. van Donkelaar, J. Mediavilla, W. Wilson, R. Huiskes, and K. Ito. Bone regeneration during distraction osteogenesis: mechano-regulation by shear strain and fluid velocity. J. Biomech. 40:2002–2011, 2007.

    Article  PubMed  Google Scholar 

  27. Kojimoto, H., N. Yasui, T. Goto, S. Matsuda, and Y. Shimomura. Bone lengthening in rabbits by callus distraction. The role of periosteum and endosteum. J. Bone Jt. Surg. Br. 70:543–549, 1988.

    CAS  Google Scholar 

  28. Leong, P. L., and E. F. Morgan. Measurement of fracture callus material properties via nanoindentation. Acta Biomater. 4:1569–1575, 2008.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Leong, P. L., and E. F. Morgan. Correlations between indentation modulus and mineral density in bone-fracture calluses. Integr. Comp. Biol. 49:59–68, 2009.

    Article  PubMed Central  PubMed  Google Scholar 

  30. Manjubala, I., Y. Liu, D. R. Epari, P. Roschger, H. Schell, P. Fratzl, and G. N. Duda. Spatial and temporal variations of mechanical properties and mineral content of the external callus during bone healing. Bone 45:185–192, 2009.

    Article  CAS  PubMed  Google Scholar 

  31. Mora-Macías, J., E. Reina-Romo, and J. Domínguez. Distraction device to estimate the axial stiffness of the callus in vivo. Med. Eng. Phys., 2015 (Under review).

  32. Mora-Macías, J., E. Reina-Romo, J. Morgaz, and J. Domínguez. In vivo gait analysis during bone transport. Ann. Biomed. Eng. 2015. doi:10.1007/s10439-015-1262-2.

    Google Scholar 

  33. Ohyama, M., Y. Miyasaka, M. Sakurai, A. T. Yokobori, Jr., and S. Sasaki. The mechanical behavior and morphological structure of callus in experimental callotasis. Biomed. Mater. Eng. 4:273–281, 1994.

    CAS  PubMed  Google Scholar 

  34. Okazaki, H., T. Kurokawa, K. Nakamura, T. Matsushita, K. Mamada, and H. Kawaguchi. Stimulation of bone formation by recombinant fibroblast growth factor-2 in callotasis bone lengthening of rabbits. Calcif. Tissue Int. 64:542–546, 1999.

    Article  CAS  PubMed  Google Scholar 

  35. Panjabi, M. M., R. W. Lindsey, S. D. Walter, and A. A. White, 3rd. The clinician’s ability to evaluate the strength of healing fractures from plain radiographs. J. Orthop. Trauma 3:29–32, 1989.

    Article  CAS  PubMed  Google Scholar 

  36. Panjabi, M. M., S. D. Walter, M. Karuda, A. A. White, and J. P. Lawson. Correlations of radiographic analysis of healing fractures with strength: a statistical analysis of experimental osteotomies. J. Orthop. Res. 3:212–218, 1985.

    Article  CAS  PubMed  Google Scholar 

  37. Preininger, B., S. Checa, F. L. Molnar, P. Fratzl, G. N. Duda, and K. Raum. Spatial-temporal mapping of bone structural and elastic properties in a sheep model following osteotomy. Ultrasound Med. Biol. 37:474–483, 2011.

    Article  PubMed  Google Scholar 

  38. Reina-Romo, E., M. J. Gomez-Benito, J. Dominguez, and J. M. Garcia-Aznar. A lattice-based approach to model distraction osteogenesis. J. Biomech. 45:2736–2742, 2012.

    Article  CAS  PubMed  Google Scholar 

  39. Reina-Romo, E., M. J. Gomez-Benito, J. Dominguez, F. Niemeyer, T. Wehner, U. Simon, and L. E. Claes. Effect of the fixator stiffness on the young regenerate bone after bone transport: computational approach. J. Biomech. 44:917–923, 2011.

    Article  CAS  PubMed  Google Scholar 

  40. Reina-Romo, E., M. J. Gomez-Benito, J. M. Garcia-Aznar, J. Dominguez, and M. Doblare. Modeling distraction osteogenesis: analysis of the distraction rate. Biomech. Model. Mechanobiol. 8:323–335, 2009.

    Article  CAS  PubMed  Google Scholar 

  41. Reina-Romo, E., M. J. Gomez-Benito, J. M. Garcia-Aznar, J. Dominguez, and M. Doblare. Growth mixture model of distraction osteogenesis: effect of pre-traction stresses. Biomech. Model. Mechanobiol. 9:103–115, 2010.

    Article  PubMed  Google Scholar 

  42. Reina-Romo, E., M. J. Gomez-Benito, J. M. Garcia-Aznar, J. Dominguez, and M. Doblare. An interspecies computational study on limb lengthening. Proc. Inst. Mech. Eng. H 224:1245–1256, 2010.

    Article  CAS  PubMed  Google Scholar 

  43. Reina-Romo, E., M. J. Gomez-Benito, A. Sampietro-Fuentes, J. Dominguez, and J. M. Garcia-Aznar. Three-dimensional simulation of mandibular distraction osteogenesis: mechanobiological analysis. Ann. Biomed. Eng. 39:35–43, 2011.

    Article  CAS  PubMed  Google Scholar 

  44. Richards, M., J. A. Goulet, M. B. Schaffler, and S. A. Goldstein. Temporal and spatial characterization of regenerate bone in the lengthened rabbit tibia. J. Bone Miner. Res. 14:1978–1986, 1999.

    Article  CAS  PubMed  Google Scholar 

  45. Richardson, J. B., J. L. Cunningham, A. E. Goodship, B. T. O’Connor, and J. Kenwright. Measuring stiffness can define healing of tibial fractures. J. Bone Jt. Surg. Br. 76:389–394, 1994.

    CAS  Google Scholar 

  46. Rodriguez-Florez, N., M. L. Oyen, and S. J. Shefelbine. Insight into differences in nanoindentation properties of bone. J. Mech. Behav. Biomed. Mater. 18:90–99, 2013.

    Article  PubMed  Google Scholar 

  47. Ryan, T. P. Modern Regression Methods. Hoboken, NJ: Wiley, 2009.

    Google Scholar 

  48. Simon, U., P. Augat, A. Ignatius, and L. Claes. Influence of the stiffness of bone defect implants on the mechanical conditions at the interface–a finite element analysis with contact. J. Biomech. 36:1079–1086, 2003.

    Article  CAS  PubMed  Google Scholar 

  49. Waanders, N. A., M. Richards, H. Steen, J. L. Kuhn, S. A. Goldstein, and J. A. Goulet. Evaluation of the mechanical environment during distraction osteogenesis. Clin. Orthop. Relat. Res. 349:225–234, 1998.

    Article  PubMed  Google Scholar 

  50. Webb, J., G. Herling, T. Gardner, J. Kenwright, and A. H. Simpson. Manual assessment of fracture stiffness. Injury 27:319–320, 1996.

    Article  CAS  PubMed  Google Scholar 

  51. Windhagen, H., S. Kolbeck, H. Bail, A. Schmeling, and M. Raschke. Quantitative assessment of in vivo bone regeneration consolidation in distraction osteogenesis. J. Orthop. Res. 18:912–919, 2000.

    Article  CAS  PubMed  Google Scholar 

  52. Yasui, N., H. Kojimoto, H. Shimizu, and Y. Shimomura. The effect of distraction upon bone, muscle, and periosteum. Orthop. Clin. North Am. 22:563–567, 1991.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge the research support of the Consejería de Innovacion, Ciencia y Empleo de la Junta de Andalucía (P09-TEP-5195) and the FPU grant of the Ministerio de Educación del Gobierno de España (AP2010-5061). The authors are also grateful to the University of Zaragoza for its collaboration.

Conflict of interest

The authors have no financial or personal relationships that could inappropriately influence the contents of this paper.

Author information

Authors and Affiliations

  1. Department of Mechanical Engineering, Escuela Técnica Superior de Ingeniería, University of Seville, Camino de los Descubrimientos s/n, 41092, Seville, Spain

    J. Mora-Macías, E. Reina-Romo & J. Domínguez

  2. Department of Orthopedics, Virgen del Rocío Hospital, 41013, Seville, Spain

    M. López-Pliego & M. A. Giráldez-Sánchez

Authors
  1. J. Mora-Macías
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. Reina-Romo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. López-Pliego
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. A. Giráldez-Sánchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. Domínguez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. Mora-Macías.

Additional information

Associate Editor Peter E. McHugh oversaw the review of this article.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mora-Macías, J., Reina-Romo, E., López-Pliego, M. et al. In Vivo Mechanical Characterization of the Distraction Callus During Bone Consolidation. Ann Biomed Eng 43, 2663–2674 (2015). https://doi.org/10.1007/s10439-015-1330-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-015-1330-7

Keywords

Search

Navigation