Size does matter: an integrative in vivo-in silico approach for the treatment of critical size bone defects

PLoS Comput Biol. 2014 Nov 6;10(11):e1003888. doi: 10.1371/journal.pcbi.1003888. eCollection 2014 Nov.

Abstract

Although bone has a unique restorative capacity, i.e., it has the potential to heal scarlessly, the conditions for spontaneous bone healing are not always present, leading to a delayed union or a non-union. In this work, we use an integrative in vivo-in silico approach to investigate the occurrence of non-unions, as well as to design possible treatment strategies thereof. The gap size of the domain geometry of a previously published mathematical model was enlarged in order to study the complex interplay of blood vessel formation, oxygen supply, growth factors and cell proliferation on the final healing outcome in large bone defects. The multiscale oxygen model was not only able to capture the essential aspects of in vivo non-unions, it also assisted in understanding the underlying mechanisms of action, i.e., the delayed vascularization of the central callus region resulted in harsh hypoxic conditions, cell death and finally disrupted bone healing. Inspired by the importance of a timely vascularization, as well as by the limited biological potential of the fracture hematoma, the influence of the host environment on the bone healing process in critical size defects was explored further. Moreover, dependent on the host environment, several treatment strategies were designed and tested for effectiveness. A qualitative correspondence between the predicted outcomes of certain treatment strategies and experimental observations was obtained, clearly illustrating the model's potential. In conclusion, the results of this study demonstrate that due to the complex non-linear dynamics of blood vessel formation, oxygen supply, growth factor production and cell proliferation and the interactions thereof with the host environment, an integrative in silico-in vivo approach is a crucial tool to further unravel the occurrence and treatments of challenging critical sized bone defects.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cartilage / metabolism
  • Cells, Cultured
  • Computer Simulation
  • Fracture Healing / physiology*
  • Fractures, Bone / physiopathology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Models, Biological*
  • Oxygen / metabolism
  • Periosteum / cytology
  • Tissue Engineering
  • Tissue Scaffolds

Substances

  • Oxygen

Grants and funding

AC is a PhD fellow of the Research Foundation Flanders (FWO-Vlaanderen). The research leading to these results has received funding from the European Research Council under the European Union's Seventh Framework Programme (FP7/2007–2013)/ERC Grant Agreement n° 279100 and 308223). NvG is funded by BOF-KU Leuven GOA project 3M120209 and FWO-project G.0A72.13N. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. This work is part of Prometheus, the KU Leuven R&D Division of Skeletal Tissue Engineering: http://www.mtm.kuleuven.be/prometheus/.