Skip to main content

Advertisement

Log in

Mechanobiology of Bone Consolidation During Distraction Osteogenesis: Bone Lengthening Vs. Bone Transport

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

Abstract

Bone lengthening and bone transport are regeneration processes that commonly rely on distraction osteogenesis, a widely accepted surgical procedure to deal with numerous bony pathologies. Despite the extensive study in the literature of the influence of biomechanical factors, a lack of knowledge about their mechanobiological differences prevents a clinical particularization. Bone lengthening treatments were performed on sheep metatarsus by reproducing the surgical and biomechanical protocol of previous bone transport experiments. Several in vivo monitoring techniques were employed to build an exhaustive comparison: gait analysis, radiographic and CT assessment, force measures through the fixation, or mechanical characterization of the new tissue. A significant initial loss of the bearing capacity, quantified by the ground reaction forces and the limb contact time with the ground, is suffered by the bone lengthening specimens. The potential effects of this anomaly on the musculoskeletal force distribution and the evolution of the bone callus elastic modulus over time are also analyzed. Imaging techniques also seem to reveal lower bone volume in the bone lengthening callus than in the bone transport one, but an equivalent mineralization rate. The simultaneous quantification of biological and mechanical parameters provides valuable information for the daily clinical routine and numerical tools development.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

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, P. Ludvigsen, L. P. Kristiansen, and O. Reikerås. High frequency distraction improves tissue adaptation during leg lengthening in humans. J Orthop. Res. 20:789–792, 2002.

    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.

    PubMed  Google Scholar 

  3. Augat, P., E. F. Morgan, T. J. Lujan, T. J. MacGillivray, and W. H. Cheung. Imaging techniques for the assessment of fracture repair. Injury. 45(Suppl 2):S16–S22, 2014.

    PubMed  Google Scholar 

  4. Blázquez-Carmona, P., J. Mora-Macías, J. A. Sanz-Herrera, J. Morgaz, R. Navarrete-Calvo, J. Domínguez, and E. Reina-Romo. Mechanical influence of surrounding soft tissue on bone regeneration processes: a bone lengthening study. Ann. Biomed. Eng. 2020. https://doi.org/10.1007/s10439-020-02592-z.

    Article  PubMed  Google Scholar 

  5. Blázquez-Carmona, P., M. Sanchez-Raya, J. Mora-Macías, J. A. Gómez-Galán, J. Domínguez, and E. Reina-Romo. Real-time wireless platform for in vivo monitoring of bone regeneration. Sensors. 20:4591, 2020.

    Google Scholar 

  6. Breik, O., D. Tivey, K. Umapathysivam, and P. Anderson. Does the rate of distraction or type of distractor affect the outcome of mandibular distraction in children with micrognathia? J. Oral Maxillofac. Surg. 74:1441–1453, 2016.

    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.

    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.

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  10. Corrales, L. A., S. Morshed, M. Bhandari, and T. Miclau, III. Variability in the assessment of fracture-healing in orthopaedic trauma studies. J. Bone Joint Surg. Am. 90:1862–1868, 2008.

    PubMed  PubMed Central  Google Scholar 

  11. Duda, G. N., K. Eckert-Hübner, 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.

    CAS  PubMed  Google Scholar 

  12. 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 Joint Surg. Br. 78:286–289, 1996.

    CAS  PubMed  Google Scholar 

  13. Fischer, S., A. Anders, I. Nolte, and N. Schilling. Compensatory load redistribution in walking and trotting dogs with hind limb lameness. Vet. J. 197:746–752, 2013.

    CAS  PubMed  Google Scholar 

  14. Fisher, J. S., J. J. Kazam, D. Fufa, and R. J. Bartolotta. Radiologic evaluation of fracture healing. Skeletal Radiol. 48:349–361, 2019.

    PubMed  Google Scholar 

  15. 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.

    CAS  PubMed  Google Scholar 

  16. 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. Strategies Trauma Limb Reconstr. 5:71–78, 2010.

    PubMed  PubMed Central  Google Scholar 

  17. Fürmetz, J., C. Soo, W. Behrendt, P. H. Thaller, H. Siekmann, J. Böhme, and C. Josten. Bone transport for limb reconstruction following severe tibial fractures. Orthop. Rev. 8:6384, 2016.

    Google Scholar 

  18. Galardi, G., G. Comi, L. Lozza, P. Marchettini, M. Novarina, R. Facchini, and A. Paronzini. Peripheral nerve damage during limb lengthening. Neurophysiology in five cases of bilateral tibial lengthening. J. Bone Jt Surg. Br. 72:121–124, 1990.

    CAS  Google Scholar 

  19. Grasa, J., M. J. Gómez-Benito, L. A. González-Torres, D. Asiaín, F. Quero, and J. M. García-Aznar. Monitoring in vivo load transmission through an external fixator. Ann. Biomed. Eng. 38:605–612, 2010.

    CAS  PubMed  Google Scholar 

  20. Hasler, C. C., and A. H. Krieg. Current concepts of leg lengthening. J. Child. Orthop. 6:89–104, 2012.

    PubMed  PubMed Central  Google Scholar 

  21. Hayashi, K., I. Yoshioka, A. Khanal, N. Furuta, K. Tominaga, and J. Fukuda. Effects of latency on bone formation during consolidation period of rabbit mandibular distraction. Asian J. Oral Maxillofac. Surg. 20:5–11, 2008.

    Google Scholar 

  22. Jacobs, B. Y., H. E. Kloefkorn, and K. D. Allen. Gait analysis methods for rodent models of osteoarthritis. Curr. Pain Headache Rep. 18:456, 2014.

    PubMed  PubMed Central  Google Scholar 

  23. Kessler, P., F. W. Neukam, and J. Wiltfang. Effects of distraction forces and frequency of distraction on bony regeneration. Br. J. Oral. Maxillofac. Surg. 43:392–398, 2005.

    CAS  PubMed  Google Scholar 

  24. Koczewski, P., F. Urban, and M. Józwiak. Analysis of some gait parameters at different stages of leg lengthening using the Ilizarov technique. Chir Narzadow Ruchu Orthop. Pol. 69:393–397, 2004.

    Google Scholar 

  25. Krizsan-Agbas, D., M. K. Winter, L. S. Eggimann, J. Meriwether, N. E. Berman, P. G. Smith, and K. E. McCarson. Gait analysis at multiple speeds reveals differential functional and structural outcomes in response to graded spinal cord injury. J. Neurotrauma. 31:846–856, 2014.

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 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.

    PubMed  PubMed Central  Google Scholar 

  28. 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.

    CAS  PubMed  Google Scholar 

  29. Mattei, L., F. Di Puccio, and S. Marchetti. In vivo impact testing on a lengthened femur with external fixation: a future option for non-invasive monitoring of fracture healing? J. R. Soc. Interface. 15:20180068, 2018.

    PubMed  PubMed Central  Google Scholar 

  30. Mora-Macías, J., P. García-Florencio, A. Pajares, P. Miranda, J. Domínguez, and E. Reina-Romo. Elastic modulus of woven bone: correlation with evolution of porosity and x-ray greyscale. Ann. Biomed. Eng. 2020. https://doi.org/10.1007/s10439-020-02529-6.

    Article  PubMed  Google Scholar 

  31. Mora-Macías, J., M. A. Giráldez-Sánchez, M. López, J. Domínguez, and M. E. Reina-Romo. Comparison of methods for assigning the material properties of distraction callus in computational model. Int. J. Numer. Method. Biomed. Eng. 35:e3227, 2019.

    PubMed  Google Scholar 

  32. Mora-Macías, J., A. Pajares, P. Miranda, J. Domínguez, and E. Reina-Romo. Mechanical characterization via nanoindentation of the woven bone developed during bone transport. J. Mech. Behav. Biomed. Mater. 74:236–244, 2017.

    PubMed  Google Scholar 

  33. Mora-Macías, J., E. Reina-Romo, and J. Domínguez. Distraction osteogenesis device to estimate the axial stiffness of the callus in vivo. Med. Eng. Phys. 37:969–978, 2015.

    PubMed  Google Scholar 

  34. Mora-Macías, J., E. Reina-Romo, and J. Domínguez. Model of the distraction callus tissue behavior during bone transport based in experiments in vivo. J. Mech. Behav. Biomed. Mater. 61:419–430, 2016.

    PubMed  Google Scholar 

  35. Mora-Macías, J., E. Reina-Romo, M. López-Pliego, M. A. Giráldez-Sánchez, and J. Domínguez. In vivo mechanical characterization of the distraction callus during bone consolidation. Ann. Biomed. Eng. 43:2663–2674, 2015.

    PubMed  Google Scholar 

  36. Mora-Macías, J., E. Reina-Romo, J. Morgaz, and J. Domínguez. In vivo gait analysis during bone transport. Ann. Biomed. Eng. 43:2090–2100, 2015.

    PubMed  Google Scholar 

  37. Morasiewicz, M., P. Koprowski, Z. Wrzosek, and S. Dragan. Gait analysis in patients after lengthening and correction of tibia with Ilizarov technique. Physiotherapy. 18:9–18, 2010.

    Google Scholar 

  38. Moseley, C. F. Leg lengthening. A review of 30 years. Clin. Orthop. Relat. Res. 247:38–43, 1989.

    Google Scholar 

  39. Paley, D. Problems, obstacles, and complications of limb lengthening by Ilizarov technique. Clin. Orthop. Relat. Res. 250:81–104, 1990.

    Google Scholar 

  40. 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.

    CAS  PubMed  Google Scholar 

  41. Pardes, A., B. R. Freedman, and L. J. Soslowsky. Ground reaction forces are more sensitive gait measures than temporal parameters in rodents following rotator cuff injury. J. Biomech. 49:376–381, 2016.

    CAS  PubMed  Google Scholar 

  42. Reichel, H., S. Lebek, C. Alter, and W. Hein. Biomechanical and densitometric bone properties after callus distraction in sheep. Clin. Orthop. Relat. Res. 357:237–254, 1998.

    Google Scholar 

  43. Reina-Romo, E., M. J. Gómez-Benito, J. M. García-Aznar, J. Domínguez, and M. Doblaré. Modeling distraction osteogenesis: analysis of the distraction rate. Biomech. Model Mechanobiol. 8:323–335, 2009.

    CAS  PubMed  Google Scholar 

  44. Reina-Romo, E., M. J. Gómez-Benito, J. M. García-Aznar, J. Domínguez, and M. Doblaré. An interspecies computational study on limb lengthening. Proc. Inst. Mech. Eng. 224:1245–1256, 2010.

    CAS  Google Scholar 

  45. Reina-Romo, E., M. J. Gómez-Benito, J. M. García-Aznar, J. Domínguez, and M. Doblaré. Growth mixture model of distraction osteogenesis: effect of pre-traction stresses. Biomech. Model Mechanobiol. 9:103–115, 2010.

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  47. Sailhan, F. Bone lengthening (distraction osteogenesis): a literature review. Osteoporos. Int. 22:2011–2015, 2011.

    CAS  PubMed  Google Scholar 

  48. Seebeck, P., M. S. Thompson, A. Parwani, W. R. Taylor, H. Shell, and G. N. Duda. Gait evaluation: a tool to monitor bone healing? Clin. Biomech. 20:883–891, 2005.

    CAS  Google Scholar 

  49. Singare, S., L. Dichen, Y. Liu, W. Zhongying, and J. Wang. The effect of latency on bone lengthening force and bone mineralization: an investigation using strain gauge mounted on internal distractor device. Biomed. Eng. Online. 5:18, 2006.

    PubMed  PubMed Central  Google Scholar 

  50. Sopakayang, R., and R. De Vita. A mathematical model for creep, relaxation and strain stiffening in parallel-fibered collagen tissues. Med. Eng. Phys. 33:1056–1063, 2011.

    PubMed  Google Scholar 

  51. Svodoba, Z., L. Bizovska, M. Janura, E. Kubonova, K. Janurova, and N. Vuillerme. Variability of spatial temporal gait parameters and the center of pressure displacements during gait in elderly fallers and nonfallers: a 6-month prospective study. PLoS ONE. 12:e0171997, 2017.

    Google Scholar 

  52. Vauhkonen, M., J. Peltonen, E. Karaharju, K. Aalto, and I. Alitalo. Collagen synthesis and mineralization in early phase of distraction bone healing. Bone Miner. 10:171–181, 1990.

    CAS  PubMed  Google Scholar 

  53. 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.

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  55. Wehner, T., M. Steiner, A. Ignatius, and L. Claes. Prediction of the time course of callus stiffness as a function of mechanical parameters in experimental rat fracture healing studies—a numerical study. PLoS ONE. 9:e115695, 2014.

    PubMed  PubMed Central  Google Scholar 

  56. Wen, H., S. Zhus, C. Li, and Y. Xu. Bone transport versus acute shortening for the management of infected tibial bone defects: a meta-analysis. BMC Musculoskelet. Disord. 21:80, 2020.

    PubMed  PubMed Central  Google Scholar 

  57. Yin, Q., Z. Sun, S. Gu, Y. Bao, X. Wei, and S. Song. Effectiveness comparison of using bone transport and bone shortening-lengthening for tibial bone and soft tissue defects. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi. 28:818–822, 2014.

    PubMed  Google Scholar 

  58. Young, N., F. D. Bell, and A. Anthony. Pediatric pain patterns during Ilizarov treatment of limb length discrepancy and angular deformity. J. Pediatr. Orthop. 14:352–357, 1994.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the Junta de Andalucía and the Ministerio de Economía y Competitividad from the Government of Spain for funding this research (US-1261691, DPI2017-82501-P, and PGC2018-097257-B-C31) and the FPU Grant of one of the authors (FPU17/05361).

Conflict of interest

The authors have no financial or personal relationships which could inappropriately influence the contents of this paper. Therefore, no conflict of interest is declared.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pablo Blázquez-Carmona.

Additional information

Associate Editor Michael S. Detamore oversaw the review of this article.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Blázquez-Carmona, P., Mora-Macías, J., Morgaz, J. et al. Mechanobiology of Bone Consolidation During Distraction Osteogenesis: Bone Lengthening Vs. Bone Transport. Ann Biomed Eng 49, 1209–1221 (2021). https://doi.org/10.1007/s10439-020-02665-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-020-02665-z

Keywords

Navigation