Mechanical loading affects angiogenesis and osteogenesis in an in vivo bone chamber: a modeling study.

Animals; Biomechanics/physiology; Bone and Bones/physiology; Computer Simulation; Implants, Experimental; Materials Testing; Models, Biological; Neovascularization, Physiologic; Osteogenesis/physiology; Rabbits; Weight-Bearing/physiology; Wound Healing

Abstract :

[en] Despite a myriad of studies confirming the interaction between biology and mechanics, the exact nature of the main mechanical stimuli and their influence on the bone regeneration processes are still unclear. The hypothesis of this study was that the outcome of peri-implant healing under different implant loading regimens can be explained by the influence of fluid flow on the combination of angiogenesis and osteogenesis through its influence on cell proliferation and differentiation. To investigate this hypothesis a mathematical model of bone regeneration was applied to simulate the peri-implant healing in an in vivo repeated sampling bone chamber for different axial micromechanical implant loading regimes. When mechanical loading was modeled to influence both osteogenic and angiogenic processes, a good agreement was observed between simulations and experiments concerning the amount of bone in the bone chamber, its radial and longitudinal distribution, and the bone-implant contact for different implant displacement magnitudes.

Disciplines :

Engineering, computing & technology: Multidisciplinary, general & others

Author, co-author :

Geris, Liesbet ; Université de Liège - ULiège > Département d'aérospatiale et mécanique > Génie biomécanique

Vandamme, Katleen

Naert, Ignace

Vander Sloten, Jos

Van Oosterwyck, Hans

Duyck, Joke

Language :

English

Title :

Mechanical loading affects angiogenesis and osteogenesis in an in vivo bone chamber: a modeling study.

Publication date :

2010

Journal title :

Tissue Engineering. Part A

ISSN :

1937-3341

eISSN :

1937-335X

Publisher :

Mary Ann Liebert, United States - New York

Volume :

Issue :

Pages :

3353-3361

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 25 January 2012

Statistics

Number of views

45 (3 by ULiège)

Number of downloads

0 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Berglundh, T., Abrahamsson, I., Lang, N.P., and Lindhe, J. De novo alveolar bone formation adjacent to endosseous implants. Clin Oral Implants Res 14, 251, 2003.
Yao, J., Li, X., Bao, C., Fan, H., Zhang, X., and Chen, Z. A novel technique to reconstruct a boxlike bone defect in the mandible and support dental implants with In vivo tissue-engineered bone. J Biomed Mater Res B Appl Biomater 91, 805, 2009.
Al-Khaldi, A., Eliopoulos, N., Martineau, D., Lejeune, L., Lachapelle, K., and Galipeau, J. Postnatal bone marrow stromal cells elicit a potent VEGF-dependent neoangiogenic response in vivo. Gene Ther 10, 621, 2003.
Stevens, M.M., Marini, R.P., Schaefer, D., Aronson, J., Lan-ger, R., and Shastri, V.P. In vivo engineering of organs: the bone bioreactor. Proc Natl Acad Sci USA 102, 11450, 2005.
Bao, C., Zhou, H., Li, W., Li, Y., Fan, H., Yao, J., Liao, Y., and Zhang, X. In: Watanabe, M., and Okuno, O., eds. Interface Oral Health Science 2007. New York, NY: Springer, 2007, pp. 85-94.
Chen, F.M., and Jin, Y. Periodontal tissue engineering and regeneration: current approaches and expanding opportunities. Tissue Eng Part B Rev 16, 219, 2010.
Butler, D.L., Goldstein, S.A., Guldberg, R.E., Guo, X.E., Kamm, R., Laurencin, C.T., McIntire, L.V., Mow, V.C., Nerem, R.M., Sah, R.L., Soslowsky, L.J., Spilker, R.L., and Tranquillo, R.T. The impact of biomechanics in tissue engineering and regenerative medicine. Tissue Eng Part B Rev 15, 477, 2009.
Kasper, G., Dankert, N., Tuischer, J., Hoeft, M., Gaber, T., Glaeser, J.D., Zander, D., Tschirschmann, M., Thompson, M., Matziolis, G., and Duda, G.N. Mesenchymal stem cells regulate angiogenesis according to their mechanical environment. Stem Cells 25, 903, 2007.
Mauney, J.R., Sjostorm, S., Blumberg, J., Horan, R., O'Leary, J.P., Vunjak-Novakovic, G., Volloch, V., and Kaplan, D.L. Mechanical stimulation promotes osteogenic differentiation of human bone marrow stromal cells on 3-D partially demineralized bone scaffolds in vitro. Calcif Tissue Int 74, 458, 2004.
Jagodzinski, M., Breitbart, A., Wehmeier, M., Hesse, E., Haasper, C., Krettek, C., Zeichen, J., and Hankemeier, S. Influence of perfusion and cyclic compression on proliferation and differentiation of bone marrow stromal cells in 3-dimensional culture. J Biomech 41, 1885, 2008.
Weyts, F.A., Bosmans, B., Niesing, R., van Leeuwen, J.P., and Weinans, H. Mechanical control of human osteoblast apoptosis and proliferation in relation to differentiation. Calcif Tissue Int 72, 505, 2003.
Ziros, P.G., Gil, A.P., Georgakopoulos, T., Habeos, I., Kletsas, D., Basdra, E.K., and Papavassiliou, A.G. The bone-specific transcriptional regulator Cbfa1 is a target of mechanical signals in osteoblastic cells. J Biol Chem 277, 23934, 2002.
Mitsui, N., Suzuki, N., Maeno, M., Yanagisawa, M., Koyama, Y., Otsuka, K., and Shimizu, N. Optimal compressive force induces bone formation via increasing bone morphogenetic proteins production and decreasing their antagonists production by Saos-2 cells. Life Sci 78, 2697, 2006.
Holtorf, H.L., Jansen, J.A., and Mikos, A.G. Flow perfusion culture induces the osteoblastic differentiation of marrow stroma cell-scaffold constructs in the absence of dexameth-asone. J Biomed Mater Res A 72, 326, 2005.
van den Dolder, J., Bancroft, G.N., Sikavitsas, V.I., Spauwen, P.H., Jansen, J.A., and Mikos, A.G. Flow perfusion culture of marrow stromal osteoblasts in titanium fiber mesh. J Biomed Mater Res A 64, 235, 2003.
Datta, N., Pham, Q.P., Sharma, U., Sikavitsas, V.I., Jansen, J.A., and Mikos, A.G. In vitro generated extracellular matrix and fluid shear stress synergistically enhance 3D osteoblastic differentiation. Proc Natl Acad Sci USA 103, 2488, 2006.
Knippenberg, M., Helder, M.N., Doulabi, B.Z., Semeins, C.M., Wuisman, P.I., and Klein-Nulend, J. Adipose tissue-derived mesenchymal stem cells acquire bone cell-like responsiveness to fluid shear stress on osteogenic stimulation. Tissue Eng 11, 1780, 2005.
Roelofsen, J., Klein-Nulend, J., and Burger, E.H. Mechanical stimulation by intermittent hydrostatic compression promotes bone-specific gene expression in vitro. J Biomech 28, 1493, 1995.
David, V., Martin, A., Lafage-Prouse, M.H., Malaval, L., Peyroche, S., Jones, D.B., Vico, L., and Guignandon, A. Mechanical loading down-regulates peroxisome pro-liferatoractivated receptor gamma in bone marrow stromal cells and favors osteoblastogenesis at the expense of adipo-gensis. Endocrinology 148, 2553, 2007.
Wang, H., Riha, G.M., Yan, S., Li, M., Chai, H., Yang, H., Yao, Q., and Chen, C. Shear stress induces endothelial differentiation from a murine embryonic mesenchymal progenitor cell line. Arterioscler Thromb Vasc Biol 25, 1817, 2005.
Yamamoto, K., Takahashi, T., Asahara, T., Ohura, N., Sokabe, T., Kamiya, A., and Ando, J. Proliferation, differentiation, and tube formation by endothelial progenitor cells in response to shear stress. J Appl Physiol 95, 2081, 2003.
Hsieh, H.J., Li, N.Q., and Frangos, J.A. Shear stress increases endothelial platelet-derived growth factor mRNA levels. Am J Physiol 260, H642, 1991.
Mitsumata, M., Fishel, R.S., Nerem, R.M., Alexander, R.W., and Berk, B.C. Fluid shear stress stimulates platelet-derived growth factor expression in endothelial cells. Am J Physiol 265, H3, 1993.
Morita, T., Yoshizumi, M., Kurihara, H., Maemura, K., Nagai, R., and Yazaki, Y. Shear stress increases heparin-binding epidermal growth factorlike growth factor mRNA levels in human vascular endothelial cells. Biochem Biophys Res Commun 197, 256, 1993.
Malek, A.M., Gibbons, G.H., Dzau, V.J., and Izumo, S. Fluid shear stress differentially modulates expression of genes encoding basic fibroblast growth factor and platelet-derived growth factor B chain in vascular endothelium. J Clin Invest 92, 2013, 1993.
Ohno, M., Cooke, J.P., Dzau, V.J., and Gibbons, G.H. Fluid shear stress induces endothelial transforming growth factor beta-1 transcription and production: Modulation by potassium channel blockade. J Clin Invest 95, 1363, 1995.
Reijnders, C.M., Bravenboer, N., Tromp, A.M., Blankenstein, M.A., and Lips, P. Effect of mechanical loading on insulinlike growth factor-I gene expression in rat tibia. J Endocrinol 192, 131, 2007.
Bhatt, K.A., Chang, E.I., Warren, S.M., Lin, S., Bastidas, N., Ghali, S., Thibboneir, A., Capla, J.M., McCarthy, J.G., and Gurtner, G.C. Uniaxial mechanical strain: an in vitro correlate to distraction osteogenesis. J Surg Res 143, 329, 2007.
Lau, K.-H.W., Kapur, S., Kesavan, C., and Baylink, D.J. Up-regulation of the Wnt, estrogen receptor, insulin-like growth factor-I, and bone morphogenetic protein pathways in C57BL/6J osteoblasts as opposed to C3H/HeJ osteoblasts in part contributes to the differential anabolic response to fluid shear. J Biol Chem 281, 9576, 2006.
Sakai, K., Mohtai, M., and Iwamoto, Y. Fluid shear stress increases transforming growth factor beta 1 expression in human osteoblast-like cells: modulation by cation channel blockades. Calcif Tissue Int 63, 515, 1998.
Kaspar, D., Seidl, W., Neidlinger-Wilke, C., Ignatius, A., and Claes, L. Dynamic cell stretching increases human osteoblast proliferation and CICP synthesis but decreases osteocalcin synthesis and alkaline phosphatase activity. J Biomech 33, 45, 2000.
Kaspar, D., Seidl, W., Neidlinger-Wilke, C., Beck, A., Claes, L., and Ignatius, A. Proliferation of human-derived osteoblast-like cells depends on the cycle number and frequency of uniaxial strain. J Biomech 35, 873, 2002.
Boutahar, N., Guignandon, A., Vico, L., and Lafage-Proust, M.H. Mechanical strain on osteoblasts activates autopho-sphorylation of focal adhesion kinase and proline-rich tyrosine kinase 2 tyrosine sites involved in ERK activation. J Biol Chem 279, 30588, 2004.
Akimoto, S., Mitsumata, M., Sasaguri, T., and Yoshida, Y. Lamianr shear stress inhibits vascular endothelial cell proliferation by inducing cyclin-dependent kinase inhibitor p21(Sdi1/Cip1/Waf1). Circ Res 86, 185, 2000.
Chen, B.P., Li, Y.S., Zhao, Y., Chen, K.D., Li, S., Lao, J., Yuan, S., Shyy, J.Y., and Chien, S. DNA microarray analysis of gene expression in endothelial cells in response to 24-h shear stress. Physiol Genomics 7, 55, 2001.
Lin, K., Hsu, P.P., Chen, B.P., Yuan, S., Usami, S., Shyy, J.Y., Li, Y.S., and Chien, S. Molecular mechanism of endothelial growth arrest by laminar shear stress. Proc Natl Acad Sci USA 97, 9385, 2000.
Ando, J., and Yamamoto, K. Vascular mechanobiology endo-thelial cell responses to fluid shear stress. Circ J 73, 1983, 2009.
Papachristou, D.J., Papachroni, K.K., Basdra, E.K., and Papavassiliou, A.G. Signaling networks and transcription factors regulating mechanotransduction in bone. Bioessays 31, 794, 2009.
Rubin, J., Rubin, C., and Jacobs, C.R. Molecular pathways mediating mechanical signaling in bone. Gene 15, 367, 2006.
Papachroni, K.K., Karatzas, D.N., Papavassiliou, K.A., Bas-dra, E.K., and Papavassiliou, A.G. Mechanotransduction in osteoblast regulation and bone disease. Trends Mol Med 15, 208, 2009.
Chien, S. Mechanotransduction and endothelial cell ho-meostasis: the wisdom of the cell. Am J Physiol Heart Circ Physiol 292, H1209, 2007.
Anderson, E.J., and Knothe Tate, M.L. Design of tissue engineering scaffolds as delivery devices for mechanical and mechanically modulated signals. Tissue Eng 13, 2525, 2007
Liedert, A., Kaspar, D., Blakytny, R., Claes, L., and Ignatius, A. Signal transduction pathways involved in mechan-otransduction in bone cells. Biochem Biophys Res Commun 349, 1, 2006.
Scott, A., Khan, K.M., Duronio, V., and Hart, D.A. Mechanotransduction in human bone: in vitro cellular physiology that underpins bone changes with exercise. Sports Med 38, 139, 2008.
Allori, A.C., Sailon, A.M., Pan, J.H., and Warren, S.M. Biological basis of bone formation, remodeling, and repair-part III: biomechanical forces. Tissue Eng Part B Rev 14, 285, 2008.
Claes, L., Eckert-Hü bner, K., and Augat, P. The effect of mechanical stability on local vascularization and tissue differentiation in callus healing. J Orthop Res 20, 1099, 2002.
Lienau, J., Schell, H., Duda, G.N., Seebeck, P., Muchow, S., and Bail, H.J. Initial vascularization and tissue differentiation are influenced by fixation stability. J Orthop Res 23, 639, 2005.
Goodship, A.E., Cunningham, J.L., and Kenwright, J. Strain rate and timing of stimulation in mechanical modulation of fracture healing. Clin Orthop Relat Res 355, S105, 1998.
Fang, T.D., Salim, A., Xia, W., Nacamuli, R.P., Guccione, S., Song, H.M., Carano, R.A., Filvaroff, E.H., Bednarski, M.D., Giaccia, A.J., and Longaker, M.T. Angiogenesis is required for successful bone induction during distraction osteogen-esis. J Bone Miner Res 20, 1114, 2005.
Rowe, N.M., Mehrara, B.J., Luchs, J.S., Dudziak, M.E., Steinbrech, D.S., Illei, P.B., Fernandez, G.J., Gittes, G.K., and Longaker, M.T. Angiogenesis during mandibular distraction osteogenesis. Ann Plast Surg 42, 470, 1999.
Warren, S.M., Mehrara, B.J., Steinbrech, D.S., Paccione, M.F., Greenwald, J.A., Spector, J.A., and Longaker, M.T. Rat mandibular distraction osteogenesis: part III. Gradual distraction versus acute lengthening. Plast Reconstr Surg 107, 441, 2001.
Leucht, P., Kim, J.B., Wazen, R., Currey, J.A., Nanci, A., Brunski, J.B., and Helms, J.A. Effect of mechanical stimuli on skeletal regeneration around implants. Bone 40, 919, 2007.
Vandamme, K., Naert, I., Geris, L., Vander Sloten, J., Puers, R., and Duyck, J. The influence of controlled immediate loading and implant design on peri-implant bone formation. J Clin Periodontol 34, 172, 2007.
Vandamme, K., Naert, I., Geris, L., Sloten, J.V., Puers, R., and Duyck, J. Histodynamics of bone tissue formation around immediately loaded cylindrical implants in the rabbit. Clin Oral Implants Res 18, 471, 2007.
Vandamme, K., Naert, I., Geris, L., Vander Sloten, J., Puers, R., and Duyck, J. The effect of micro-motion on the tissue response around immediately loaded roughened titanium implants in the rabbit. Eur J Oral Sci 115, 21, 2007.
Vandamme, K., Naert, I., Vander Sloten, J., Puers, R., and Duyck, J. Effect of implant surface roughness and loading on peri-implant bone formation. J Periodontol 79, 150, 2008.
Geris, L., Vandamme, K., Naert, I., Vander Sloten, J., Duyck, J., and Van Oosterwyck, H. Numerical simulation of bone regeneration in a bone chamber. J Dent Res 88, 158, 2009.
Duyck, J., De Cooman, M., Puers, R., Van Oosterwyck, H., Vander Sloten, J., and Naert, I. A repeated sampling bone chamber methodology for the evaluation of tissue differentiation and bone adaptation around titanium implants under controlled mechanical conditions. J Biomech 37, 1819, 2004.
Duyck, J., Vandamme, K., Geris, L., Van Oosterwyck, H., De Cooman, M., Vander Sloten, J., Puers, R., Naert, I. The influence of micro-motion on the tissue differentiation around immediately loaded cylindrical turned titanium implants. Arch Oral Biol 51, 1, 2006.
Lacroix, D., and Prendergast, P.J. A mechano-regulation model for tissue differentiation during fracture healing: analysis of gap size and loading. J Biomech 35, 1163, 2002.
Geris, L., Vander Sloten, J., and Van Oosterwyck, H. Connecting biology and mechanics in fracture healing: an integrated mathematical modeling framework for the study of nonunions. Biomech Model Mechanobiol, 2010. Doi: 10.1007/s10237-010-0208-8. Epub ahead of print.
Geris, L., Gerisch, A., Vander Sloten, J., Weiner, R., and Van Oosterwyck, H. Angiogenesis in bone fracture healing: a bioregulatory model. J Theor Biol 251, 137, 2008.
Harrison, L.J., Cunningham, J.L., Strömberg, L., and Good-ship, A.E. Controlled induction of a pseudarthrosis: a study using a rodent model. J Orthop Trauma 17, 11, 2003.
Tseng, H., Peterson, T.E., and Berk, B.C. Fluid shear stress stimulates mitogen-activated protein kinase in endothelial cells. Circ Res 77, 869, 1995.
Szmukler-Moncler, S., Salama, H., Reingewirtz, Y., and Dubruille, J.H. Timing of loading and effect of micromotion on bone-dental implant interface: review of experimental literature. J Biomed Mater Res 43, 192, 1998.
Duyck, J., Slaets, E., Sasaguri, K., Vandamme, K., and Naert, I. Effect of intermittent loading and surface roughness on peri-implant bone formation in a bone chamber model. J Clin Periodontol 34, 998, 2007.
Shalabi, M.M., Gortemaker, A., Van't Hof, M.A. Jansen, J.A., and Creugers, N.H. Implant surface roughness and bone healing: a systematic review. J Dent Res 85, 496, 2006.
Schwartz, Z., Nasazky, E., and Boyan, B.D. Surface micro-topography regulates osteointegration: the role of implant surface microtopography in osteointegration. Alpha Ome-gan 98, 9, 2005.
Sammons, R.L., Lumbikanonda, N., Gross, M., and Cantzler, P. Comparison of osteoblast spreading on microstructured dental implant surfaces and cell behaviour in an explant model of osseointegration. A scanning electron microscopic study. Clin Oral Implants Res 16, 657, 2005.
Boyan, B.D., Lossdorfer, S., Wang, L., Zhao, G., Lohmann, C.H., Cochran, D.L., and Schwartz, Z. Osteoblasts generate an osteogenic microenvironment when grown on surfaces with rough microtopographies. Eur Cell Mater 6, 22, 2003.
Geris, L., Vandamme, K., Naert, I., Vander Sloten, J., Duyck, J., and Van Oosterwyck, H. Application of mechan-oregulatory models to simulate the histodynamics of peri-implant bone tissue formation in an in vivo bone chamber. J Biomech 41, 145, 2008.
Wang, J.H.-C., and Thampatty, B.P. An introductory review of cell mechanobiology. Biomech Model Mechanobiol 5, 1, 2006.
Hori, R.Y., and Lewis, J.L. Mechanical properties of the fibrous tissue found at the bone-cement interface following total joint replacement. J Biomed Mat Res 16, 911, 1982.
Claes, L.E., and Heigele, C.A. Magnitudes of local stress and strain along bony surfaces predict the course and type of fracture healing. J Biomech 32, 255, 1999.
Armstrong, C.G., and Mow, V.C. Variations in the intrinsic mechanical properties of human articular cartilage with age, degeneration and water content. J Bone Joint Surg 64A, 88, 1982.
Ochoa, J.A., and Hillberry, B.M. Permeability of bovine cancellous bone. Transactions of the 38th Orthopaedic Research Society 17, 162, 1992.
Jurvelin, J.S., Buschmann, M.D., and Hunziker, E.B. Optical and mechanical determination of poisson's ratio of adult bovine humeral articular cartilage. J Biomech 30, 235, 1997.
Huiskes, R., Van Driel, W.D., Prendergast, P.J., and Søballe, K. A biomechanical regulatory model for periprosthetic fibrous-tissue differentiation. J Mater Sci Mat Med 8, 785, 1997.