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Cyclic Deformation-Induced Solute Transport in Tissue Scaffolds with Computer Designed, Interconnected, Pore Networks: Experiments and Simulations

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Abstract

Nutrient supply and waste removal in porous tissue engineering scaffolds decrease from the periphery to the center, leading to limited depth of ingrowth of new tissue into the scaffold. However, as many tissues experience cyclic physiological strains, this may provide a mechanism to enhance solute transport in vivo before vascularization of the scaffold. The hypothesis of this study was that pore cross-sectional geometry and interconnectivity are of major importance for the effectiveness of cyclic deformation-induced solute transport. Transparent elastic polyurethane scaffolds, with computer-programmed design of pore networks in the form of interconnected channels, were fabricated using a 3D printing and injection molding technique. The scaffold pores were loaded with a colored tracer for optical contrast, cyclically compressed with deformations of 10 and 15% of the original undeformed height at 1.0 Hz. Digital imaging was used to quantify the spatial distribution of the tracer concentration within the pores. Numerical simulations of a fluid–structure interaction model of deformation-induced solute transport were compared to the experimental data. The results of experiments and modeling agreed well and showed that pore interconnectivity heavily influences deformation-induced solute transport. Pore cross-sectional geometry appears to be of less relative importance in interconnected pore networks. Validated computer models of solute transport can be used to design optimal scaffold pore geometries that will enhance the convective transport of nutrients inside the scaffold and the removal of waste, thus improving the cell survivability deep inside the scaffold.

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References

  1. Bingham, J. T., R. Papannagari, S. K. Van de Velde, C. Gross, T. J. Gill, D. T. Felson, H. E. Rubash, and G. Li. In vivo cartilage contact deformation in the healthy human tibiofemoral joint. Rheumatology (Oxford) 47:1622–1627, 2008.

    Google Scholar 

  2. Bowman, R. S., J. L. Wilson, and P. Hu. Diffusion coefficients of hydrologic tracers measured by a Taylor dispersion technique. In: Proceedings of the Geological Society of America, 2001, paper 116-0.

  3. Brown, D. A., W. R. MacLellan, H. Laks, J. C. Dunn, B. M. Wu, and R. E. Beygui. Analysis of oxygen transport in a diffusion-limited model of engineered heart tissue. Biotechnol. Bioeng., 97:962-975, 2007. doi:10.1002/bit.21295.

    Article  PubMed  CAS  Google Scholar 

  4. Brown, D. A., W. R. Maclellan, B. M. Wu, and R. E. Beygui. Analysis of pH gradients resulting from mass transport limitations in engineered heart tissue. Ann. Biomed. Eng., 35:1885-1897, 2007. doi:10.1007/s10439-007-9360-4.

    Article  PubMed  Google Scholar 

  5. Depprich, R., J. Handschel, H. P. Wiesmann. J. Jasche-Meyer, and U. Meyer, Use of bioreactors in maxillofacial tissue engineering. Br. J. Oral Maxillofac. Surg., 46:349-354, 2008. doi:10.1016/j.bjoms.2008.01.012.

    Article  PubMed  Google Scholar 

  6. Evans, R. C., and T. M. Quinn. Solute convection in dynamically compressed cartilage. J. Biomech., 39:1048-1055, 2006. doi:10.1016/j.jbiomech.2005.02.017.

    Article  PubMed  Google Scholar 

  7. Gardiner, B., D. Smith, P. Pivonka, A. Grodzinsky, E. Frank, and L. Zhang. Solute transport in cartilage undergoing cyclic deformation. Comput. Methods Biomech. Biomed. Engin., 10:265-278, 2007. doi:10.1080/10255840701309163.

    Article  Google Scholar 

  8. Hollister, S. J. Porous scaffold design for tissue engineering. Nat. Mater., 4:518-524, 2005. doi:10.1038/nmat1421.

    Article  PubMed  CAS  Google Scholar 

  9. Huang, C. Y., K. L. Hagar, L. E. Frost, Y. Sun, and H. S. Cheung. Effects of cyclic compressive loading on chondrogenesis of rabbit bone-marrow derived mesenchymal stem cells. Stem Cells, 22:313-323, 2004. doi:10.1634/stemcells.22-3-313.

    Article  PubMed  CAS  Google Scholar 

  10. Hung, C. T., R. L. Mauck, C. C. Wang, E. G. Lima, and G. A. Ateshian. A paradigm for functional tissue engineering of articular cartilage via applied physiologic deformational loading. Ann. Biomed. Eng., 32:35-49, 2004. doi:10.1023/B:ABME.0000007789.99565.42.

    Article  PubMed  Google Scholar 

  11. Ikada, Y. Challenges in tissue engineering. J. R. Soc. Interface, 3:589-601, 2006. doi:10.1098/rsif.2006.0124.

    Article  PubMed  CAS  Google Scholar 

  12. Jorgensen, S. M., O. Demirkaya, and E. L. Ritman. Three-dimensional imaging of vasculature and parenchyma in intact rodent organs with X-ray micro-CT. Am. J. Physiol., 275:H1103-1114, 1998.

    PubMed  CAS  Google Scholar 

  13. Kantor, B., S. M. Jorgensen, P. E. Lund, M. S. Chmelik, D. A. Reyes, and E. L. Ritman. Cryostatic micro-computed tomography imaging of arterial wall perfusion. Scanning, 24:186-190, 2002.

    PubMed  Google Scholar 

  14. Kim, B. S., J. Nikolovski, J. Bonadio, and D. J. Mooney. Cyclic mechanical strain regulates the development of engineered smooth muscle tissue. Nat. Biotechnol., 17:979-983, 1999. doi:10.1038/13671.

    Article  PubMed  CAS  Google Scholar 

  15. Kubelka, P., and F. Munk. Ein Beitrag zur Optik der Farbanstriche. Z. Techn. Physik, 12:593-601, 1931.

    Google Scholar 

  16. Lee, K. W., S. Wang, L. Lu, E. Jabbari, B. L. Currier, and M. J. Yaszemski. Fabrication and characterization of poly(propylene fumarate) scaffolds with controlled pore structures using 3-dimensional printing and injection molding. Tissue Eng., 12:2801-2811, 2006. doi:10.1089/ten.2006.12.2801.

    Article  PubMed  CAS  Google Scholar 

  17. Leyton, L. Fluid behaviour in biological systems. Oxford: Clarendon Press, 1975.

    Google Scholar 

  18. Liang, Y., H. Zhu, T. Gehrig, and M. H. Friedman. Measurement of the transverse strain tensor in the coronary arterial wall from clinical intravascular ultrasound images. J. Biomech. 41:2906–2911, 2008.

    Google Scholar 

  19. Lu, L., and A. G. Mikos. The importance of new processing techniques in tissue engineering. MRS Bull., 21:28-32, 1996.

    PubMed  CAS  Google Scholar 

  20. Malda, J., T. J. Klein, and Z. Upton. The roles of hypoxia in the in vitro engineering of tissues. Tissue Eng., 13:2153-2162, 2007. doi:10.1089/ten.2006.0417.

    Article  PubMed  CAS  Google Scholar 

  21. Mansbridge, J. Commercial considerations in tissue engineering. J. Anat., 209:527-532, 2006. doi:10.1111/j.1469-7580.2006.00631.x.

    Article  PubMed  CAS  Google Scholar 

  22. Mansbridge, J., K. Liu, R. Patch, K. Symons, and E. Pinney. Three-dimensional fibroblast culture implant for the treatment of diabetic foot ulcers: metabolic activity and therapeutic range. Tissue Eng., 4:403-414, 1998. doi:10.1089/ten.1998.4.403.

    Article  PubMed  CAS  Google Scholar 

  23. Mauck, R. L., C. T. Hung, and G. A. Ateshian. Modeling of neutral solute transport in a dynamically loaded porous permeable gel: implications for articular cartilage biosynthesis and tissue engineering. J. Biomech. Eng., 125:602-614, 2003. doi:10.1115/1.1611512.

    Article  PubMed  Google Scholar 

  24. Olson, R. M. Human carotid artery wall thickness, diameter, and blood flow by a noninvasive technique. J. Appl. Physiol., 37:955-960, 1974.

    PubMed  CAS  Google Scholar 

  25. Op Den Buijs, J., K. W. Lee, S. M. Jorgensen, S. Wang, M. J. Yaszemski, and E. L. Ritman. High resolution X-ray imaging of dynamic solute transport in cyclically deformed porous tissue scaffolds. Proc. SPIE, 69161A:1-10, 2008.

    Google Scholar 

  26. Persson, M. Accurate dye tracer concentration estimations using image analysis. Soil Sci. Soc. Am. J., 69:967-975, 2005.

    Article  CAS  Google Scholar 

  27. Petit, C., F. Pietri-Rouxel, A. Lesne, T. Leste-Lasserre, D. Mathez, R. K. Naviaux, P. Sonigo, F. Bouillaud, and J. Leibowitch. Oxygen consumption by cultured human cells is impaired by a nucleoside analogue cocktail that inhibits mitochondrial DNA synthesis. Mitochondrion, 5:154-161, 2005. doi:10.1016/j.mito.2004.09.004.

    Article  PubMed  CAS  Google Scholar 

  28. Portner, R., S. Nagel-Heyer, C. Goepfert, P. Adamietz, and N. M. Meenen. Bioreactor design for tissue engineering. J. Biosci. Bioeng., 100:235-245, 2005. doi:10.1263/jbb.100.235.

    Article  PubMed  CAS  Google Scholar 

  29. Radisic, M., J. Malda, E. Epping, W. Geng, R. Langer, and G. Vunjak-Novakovic. Oxygen gradients correlate with cell density and cell viability in engineered cardiac tissue. Biotechnol. Bioeng., 93:332-343, 2006. doi:10.1002/bit.20722.

    Article  PubMed  CAS  Google Scholar 

  30. Rich, D. Methods for Measurement and Control of Ink Concentration and Film Thickness, US Patent 7,077,064 B1, 2006.

  31. Sengers, B. G., C. W. Oomens, and F. P. Baaijens. An integrated finite-element approach to mechanics, transport and biosynthesis in tissue engineering. J. Biomech. Eng., 126:82-91, 2004. doi:10.1115/1.1645526.

    Article  PubMed  Google Scholar 

  32. Sharma, G., and H. J. Trussell. Digital color imaging. IEEE Trans. Image Process., 6:901-932, 1997. doi:10.1109/83.597268.

    Article  PubMed  CAS  Google Scholar 

  33. Stafilidis, S., K. Karamanidis, G. Morey-Klapsing, G. Demonte, G. P. Bruggemann, and A. Arampatzis. Strain and elongation of the vastus lateralis aponeurosis and tendon in vivo during maximal isometric contraction. Eur. J. Appl. Physiol., 94:317-322, 2005. doi:10.1007/s00421-004-1301-4.

    Article  PubMed  Google Scholar 

  34. Teske, A. J., B. W. De Boeck, P. G. Melman, G. T. Sieswerda, P. A. Doevendans, and M. J. Cramer. Echocardiographic quantification of myocardial function using tissue deformation imaging, a guide to image acquisition and analysis using tissue Doppler and speckle tracking. Cardiovasc. Ultrasound, 5:27, 2007. doi:10.1186/1476-7120-5-27.

    Article  PubMed  Google Scholar 

  35. Traill, T. A., D. G. Gibson, and D. J. Brown. Study of left ventricular wall thickness and dimension changes using echocardiography. Br. Heart J., 40:162-169, 1978. doi:10.1136/hrt.40.2.162.

    Article  PubMed  CAS  Google Scholar 

  36. Volkmer, E., I. Drosse, S. Otto, A. Stangelmayer, M. Stengele, B. C. Kallukalam, W. Mutschler, and M. Schieker. Hypoxia in Static and Dynamic 3D Culture Systems for Tissue Engineering of Bone. Tissue Eng. Part A, 14:1331-1340, 2008.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported in part by the Mayo Graduate School and NIH grant EB000305. The authors thank the Division of Engineering of Mayo Clinic for hardware and software support to run the numerical simulations, and Ms. Geraldine K. Bernard for help with injection mold printing.

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Authors and Affiliations

  1. Physiological Imaging Research Laboratory, Department of Physiology and Biomedical Engineering, Alfred 2-409, Mayo Clinic College of Medicine, 200 First Street SW, Rochester, MN, 55905, USA

    Jorn Op Den Buijs & Erik L. Ritman

  2. Department of Physiology and Biomedical Engineering & Division of Engineering, Mayo Clinic College of Medicine, 200 First Street SW, Rochester, MN, 55905, USA

    Dan Dragomir-Daescu

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  1. Jorn Op Den Buijs
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  3. Erik L. Ritman
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Correspondence to Erik L. Ritman.

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Op Den Buijs, J., Dragomir-Daescu, D. & Ritman, E.L. Cyclic Deformation-Induced Solute Transport in Tissue Scaffolds with Computer Designed, Interconnected, Pore Networks: Experiments and Simulations. Ann Biomed Eng 37, 1601–1612 (2009). https://doi.org/10.1007/s10439-009-9712-3

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