3,864
Views
113
CrossRef citations to date
0
Altmetric
Review

The role of perfusion bioreactors in bone tissue engineering

, &
Pages 167-175 | Published online: 01 Oct 2012

References

  • Yeatts AB, Fisher JP. Bone tissue engineering bioreactors: dynamic culture and the influence of shear stress. Bone 2011; 48:171 - 81; http://dx.doi.org/10.1016/j.bone.2010.09.138; PMID: 20932947
  • Yu X, Botchwey EA, Levine EM, Pollack SR, Laurencin CT. Bioreactor-based bone tissue engineering: the influence of dynamic flow on osteoblast phenotypic expression and matrix mineralization. Proc Natl Acad Sci U S A 2004; 101:11203 - 8; http://dx.doi.org/10.1073/pnas.0402532101; PMID: 15277663
  • Hill NM, Horne JG, Devane PA. Donor site morbidity in the iliac crest bone graft. Aust N Z J Surg 1999; 69:726 - 8; http://dx.doi.org/10.1046/j.1440-1622.1999.01674.x; PMID: 10527350
  • Seiler JG 3rd, Johnson J. Iliac crest autogenous bone grafting: donor site complications. J South Orthop Assoc 2000; 9:91 - 7; PMID: 10901646
  • Cypher TJ, Grossman JP. Biological principles of bone graft healing. J Foot Ankle Surg 1996; 35:413 - 7; http://dx.doi.org/10.1016/S1067-2516(96)80061-5; PMID: 8915864
  • Sikavitsas VI, Bancroft GN, Mikos AG. Formation of three-dimensional cell/polymer constructs for bone tissue engineering in a spinner flask and a rotating wall vessel bioreactor. J Biomed Mater Res 2002; 62:136 - 48; http://dx.doi.org/10.1002/jbm.10150; PMID: 12124795
  • Gao H, Ayyaswamy PS, Ducheyne P. Dynamics of a microcarrier particle in the simulated microgravity environment of a rotating-wall vessel. Microgravity Sci Technol 1997; 10:154 - 65; PMID: 11543416
  • Moore WR, Graves SE, Bain GI. Synthetic bone graft substitutes. ANZ J Surg 2001; 71:354 - 61; http://dx.doi.org/10.1046/j.1440-1622.2001.02128.x; PMID: 11409021
  • Bongio M, van den Beucken JJJP, Leeuwenburgh SCG, Jansen JA. Development of bone substitute materials: from ‘biocompatible’to ‘instructive’. J Mater Chem 2010; 20:8747 - 59; http://dx.doi.org/10.1039/c0jm00795a
  • Calori GM, Mazza E, Colombo M, Ripamonti C. The use of bone-graft substitutes in large bone defects: any specific needs?. Injury 2011; 42:Suppl 2 S56 - 63; http://dx.doi.org/10.1016/j.injury.2011.06.011; PMID: 21752369
  • Wendt D, Marsano A, Jakob M, Heberer M, Martin I. Oscillating perfusion of cell suspensions through three-dimensional scaffolds enhances cell seeding efficiency and uniformity. Biotechnol Bioeng 2003; 84:205 - 14; http://dx.doi.org/10.1002/bit.10759; PMID: 12966577
  • Griffith LG, Naughton G. Tissue engineering--current challenges and expanding opportunities. Science 2002; 295:1009 - 14; http://dx.doi.org/10.1126/science.1069210; PMID: 11834815
  • Langer R. Tissue engineering. Mol Ther 2000; 1:12 - 5; http://dx.doi.org/10.1006/mthe.1999.0003; PMID: 10933907
  • Godara P, McFarland CD, Nordon RE. Design of bioreactors for mesenchymal stem cell tissue engineering. J Chem Technol Biotechnol 2008; 83:408 - 20; http://dx.doi.org/10.1002/jctb.1918
  • Bernhardt A, Lode A, Peters F, Gelinsky M. Optimization of culture conditions for osteogenically-induced mesenchymal stem cells in β-tricalcium phosphate ceramics with large interconnected channels. J Tissue Eng Regen Med 2010; 5:444 - 53; PMID: 20848550
  • Martin I, Wendt D, Heberer M. The role of bioreactors in tissue engineering. Trends Biotechnol 2004; 22:80 - 6; http://dx.doi.org/10.1016/j.tibtech.2003.12.001; PMID: 14757042
  • Meinel L, Karageorgiou V, Fajardo R, Snyder B, Shinde-Patil V, Zichner L, et al. Bone tissue engineering using human mesenchymal stem cells: effects of scaffold material and medium flow. Ann Biomed Eng 2004; 32:112 - 22; http://dx.doi.org/10.1023/B:ABME.0000007796.48329.b4; PMID: 14964727
  • Botchwey E. A., Dupree MA, Pollack SR, Levine EM, Laurencin CT. Tissue engineered bone: Measurement of nutrient transport in three-dimensional matrices. J Biomed Mater Res A 2003; 67A:357 - 67; http://dx.doi.org/10.1002/jbm.a.10111
  • Stiehler M, Bünger C, Baatrup A, Lind M, Kassem M, Mygind T. Effect of dynamic 3-D culture on proliferation, distribution, and osteogenic differentiation of human mesenchymal stem cells. J Biomed Mater Res A 2009; 89:96 - 107; PMID: 18431785
  • Sailon AM, Allori AC, Davidson EH, Reformat DD, Allen RJ Jr., Warren SM. A novel flow-perfusion bioreactor supports 3D dynamic cell culture. J Biomed Biotechnol 2009; 2009:873816; http://dx.doi.org/10.1155/2009/873816; PMID: 20037739
  • Carpentier B, Layrolle P, Legallais C. Bioreactors for bone tissue engineering. Int J Artif Organs 2011; 34:259 - 70; http://dx.doi.org/10.5301/IJAO.2011.6333; PMID: 21374561
  • Kim HJ, Kim UJ, Leisk GG, Bayan C, Georgakoudi I, Kaplan DL. Bone regeneration on macroporous aqueous-derived silk 3-D scaffolds. Macromol Biosci 2007; 7:643 - 55; http://dx.doi.org/10.1002/mabi.200700030; PMID: 17477447
  • Sikavitsas VI, Bancroft GN, Holtorf HL, Jansen JA, Mikos AG. Mineralized matrix deposition by marrow stromal osteoblasts in 3D perfusion culture increases with increasing fluid shear forces. Proc Natl Acad Sci U S A 2003; 100:14683 - 8; http://dx.doi.org/10.1073/pnas.2434367100; PMID: 14657343
  • Sikavitsas VI, Temenoff JS, Mikos AG. Biomaterials and bone mechanotransduction. Biomaterials 2001; 22:2581 - 93; http://dx.doi.org/10.1016/S0142-9612(01)00002-3; PMID: 11519777
  • Burdick JA, Vunjak-Novakovic G. Engineered microenvironments for controlled stem cell differentiation. Tissue Eng Part A 2009; 15:205 - 19; http://dx.doi.org/10.1089/ten.tea.2008.0131; PMID: 18694293
  • Wang T-W, Wu H-C, Wang H-Y, Lin F-H, Sun J-S. Regulation fo adult human mesenchymal stem cells into osteogenic and chondrogenic lineages by different bioreactor systems. J Biomed Mater Res A 2007; 88A:935 - 46; http://dx.doi.org/10.1002/jbm.a.31914
  • Goldstein AS, Juarez TM, Helmke CD, Gustin MC, Mikos AG. Effect of convection on osteoblastic cell growth and function in biodegradable polymer foam scaffolds. Biomaterials 2001; 22:1279 - 88; http://dx.doi.org/10.1016/S0142-9612(00)00280-5; PMID: 11336300
  • Alvarez-Barreto JF, Linehan SM, Shambaugh RL, Sikavitsas VI. Flow perfusion improves seeding of tissue engineering scaffolds with different architectures. Ann Biomed Eng 2007; 35:429 - 42; http://dx.doi.org/10.1007/s10439-006-9244-z; PMID: 17216348
  • Bancroft GN, Sikavitsas VI, Mikos AG. Design of a flow perfusion bioreactor system for bone tissue-engineering applications. Tissue Eng 2003; 9:549 - 54; http://dx.doi.org/10.1089/107632703322066723; PMID: 12857422
  • Janssen FW, Oostra J, Oorschot A, van Blitterswijk CA. A perfusion bioreactor system capable of producing clinically relevant volumes of tissue-engineered bone: in vivo bone formation showing proof of concept. Biomaterials 2006; 27:315 - 23; http://dx.doi.org/10.1016/j.biomaterials.2005.07.044; PMID: 16125223
  • Bjerre L, Bünger CE, Kassem M, Mygind T. Flow perfusion culture of human mesenchymal stem cells on silicate-substituted tricalcium phosphate scaffolds. Biomaterials 2008; 29:2616 - 27; http://dx.doi.org/10.1016/j.biomaterials.2008.03.003; PMID: 18374976
  • Grayson WL, Bhumiratana S, Cannizzaro C, Chao PHG, Lennon DP, Caplan AI, et al. Effects of initial seeding density and fluid perfusion rate on formation of tissue-engineered bone. Tissue Eng Part A 2008; 14:1809 - 20; http://dx.doi.org/10.1089/ten.tea.2007.0255; PMID: 18620487
  • Sucosky P, Osorio DF, Brown JB, Neitzel GP. Fluid mechanics of a spinner-flask bioreactor. Biotechnol Bioeng 2004; 85:34 - 46; http://dx.doi.org/10.1002/bit.10788; PMID: 14705010
  • Vunjak Novakovic G, Freed LE, Biron RJ, Langer R. Effects of mixing on the composition and morphology of tissue engineered cartilage. AIChE J 1996; 42:850 - 60; http://dx.doi.org/10.1002/aic.690420323
  • Datta N, Pham QP, Sharma U, Sikavitsas VI, Jansen JA, Mikos AG. In vitro generated extracellular matrix and fluid shear stress synergistically enhance 3D osteoblastic differentiation. Proc Natl Acad Sci U S A 2006; 103:2488 - 93; http://dx.doi.org/10.1073/pnas.0505661103; PMID: 16477044
  • Bjerre L, Bünger C, Baatrup A, Kassem M, Mygind T. Flow perfusion culture of human mesenchymal stem cells on coralline hydroxyapatite scaffolds with various pore sizes. J Biomed Mater Res A 2011; 97:251 - 63; http://dx.doi.org/10.1002/jbm.a.33051; PMID: 21442726
  • Mygind T, Stiehler M, Baatrup A, Li H, Zou X, Flyvbjerg A, et al. Mesenchymal stem cell ingrowth and differentiation on coralline hydroxyapatite scaffolds. Biomaterials 2007; 28:1036 - 47; http://dx.doi.org/10.1016/j.biomaterials.2006.10.003; PMID: 17081601
  • Granet C, Laroche N, Vico L, Alexandre C, Lafage-Proust MH. Rotating-wall vessels, promising bioreactors for osteoblastic cell culture: comparison with other 3D conditions. Med Biol Eng Comput 1998; 36:513 - 9; http://dx.doi.org/10.1007/BF02523224; PMID: 10198539
  • Qiu Q-Q, Ducheyne P, Ayyaswamy PS, Fabrication S. Fabrication, characterization and evaluation of bioceramic hollow microspheres used as microcarriers for 3-D bone tissue formation in rotating bioreactors. Biomaterials 1999; 20:989 - 1001; http://dx.doi.org/10.1016/S0142-9612(98)00183-5; PMID: 10378799
  • Botchwey EA, Pollack SR, Levine EM, Johnston ED, Laurencin CT. Quantitative analysis of three-dimensional fluid flow in rotating bioreactors for tissue engineering. J Biomed Mater Res A 2004; 69:205 - 15; http://dx.doi.org/10.1002/jbm.a.10163; PMID: 15057993
  • Botchwey EA, Pollack SR, Levine EM, Laurencin CT. Bone tissue engineering in a rotating bioreactor using a microcarrier matrix system. J Biomed Mater Res 2001; 55:242 - 53; http://dx.doi.org/10.1002/1097-4636(200105)55:2<242::AID-JBM1011>3.0.CO;2-D; PMID: 11255176
  • Botchwey EA, Pollack SR, El-Amin S, Levine EM, Tuan RS, Laurencin CT. Human osteoblast-like cells in three-dimensional culture with fluid flow. Biorheology 2003; 40:299 - 306; PMID: 12454419
  • Weinbaum S, Cowin SC, Zeng Y. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech 1994; 27:339 - 60; http://dx.doi.org/10.1016/0021-9290(94)90010-8; PMID: 8051194
  • Marolt D, Augst A, Freed LE, Vepari C, Fajardo R, Patel N, et al. Bone and cartilage tissue constructs grown using human bone marrow stromal cells, silk scaffolds and rotating bioreactors. Biomaterials 2006; 27:6138 - 49; http://dx.doi.org/10.1016/j.biomaterials.2006.07.015; PMID: 16895736
  • Qiu Q-Q, Ducheyne P, Ayyaswamy PS. 3D bone tissue engineered with bioactive microspheres in simulated microgravity. In Vitro Cell Dev Biol Anim 2001; 37:157 - 65; http://dx.doi.org/10.1290/1071-2690(2001)037<0157:BTEWBM>2.0.CO;2; PMID: 11370806
  • Terai H, Hannouche D, Ochoa E, Yamano Y, Vacanti JP. In vitro engineering of bone using a rotational oxygen-permeable bioreactor system. Mater Sci Eng C 2002; 20:3 - 8; http://dx.doi.org/10.1016/S0928-4931(02)00006-1
  • Yoshimoto H, Shin YM, Terai H, Vacanti JP. A biodegradable nanofiber scaffold by electrospinning and its potential for bone tissue engineering. Biomaterials 2003; 24:2077 - 82; http://dx.doi.org/10.1016/S0142-9612(02)00635-X; PMID: 12628828
  • Song K, Liu T, Cui Z, Li X, Ma X. Three-dimensional fabrication of engineered bone with human bio-derived bone scaffolds in a rotating wall vessel bioreactor. J Biomed Mater Res A 2008; 86:323 - 32; http://dx.doi.org/10.1002/jbm.a.31624; PMID: 17969035
  • Grayson WL, Fröhlich M, Yeager K, Bhumiratana S, Chan ME, Cannizzaro C, et al. Engineering anatomically shaped human bone grafts. Proc Natl Acad Sci U S A 2010; 107:3299 - 304; http://dx.doi.org/10.1073/pnas.0905439106; PMID: 19820164
  • Chen H-C, Hu Y-C. Bioreactors for tisue engineering. Biotechnol Lett 2006; 28:1215 - 9; http://dx.doi.org/10.1007/s10529-006-9111-x; PMID: 16799759
  • Bancroft GN, Sikavitsas VI, van den Dolder J, Sheffield TL, Ambrose CG, Jansen JA, et al. Fluid flow increases mineralized matrix deposition in 3D perfusion culture of marrow stromal osteoblasts in a dose-dependent manner. Proc Natl Acad Sci U S A 2002; 99:12600 - 5; http://dx.doi.org/10.1073/pnas.202296599; PMID: 12242339
  • Holtorf HL, Datta N, Jansen JA, Mikos AG. Scaffold mesh size affects the osteoblastic differentiation of seeded marrow stromal cells cultured in a flow perfusion bioreactor. J Biomed Mater Res A 2005; 74:171 - 80; http://dx.doi.org/10.1002/jbm.a.30330; PMID: 15965910
  • Gomes ME, Sikavitsas VI, Behravesh E, Reis RL, Mikos AG. Effect of flow perfusion on the osteogenic differentiation of bone marrow stromal cells cultured on starch-based three-dimensional scaffolds. J Biomed Mater Res A 2003; 67:87 - 95; http://dx.doi.org/10.1002/jbm.a.10075; PMID: 14517865
  • Wang Y, Uemura T, Dong J, Kojima H, Tanaka J, Tateishi T. Application of perfusion culture system improves in vitro and in vivo osteogenesis of bone marrow-derived osteoblastic cells in porous ceramic materials. Tissue Eng 2003; 9:1205 - 14; http://dx.doi.org/10.1089/10763270360728116; PMID: 14670108
  • Holtorf HL, Sheffield TL, Ambrose CG, Jansen JA, Mikos AG. Flow perfusion culture of marrow stromal cells seeded on porous biphasic calcium phosphate ceramics. Ann Biomed Eng 2005; 33:1238 - 48; http://dx.doi.org/10.1007/s10439-005-5536-y; PMID: 16133930
  • Porter BD, Lin ASP, Peister A, Hutmacher D, Guldberg RE. Noninvasive image analysis of 3D construct mineralization in a perfusion bioreactor. Biomaterials 2007; 28:2525 - 33; http://dx.doi.org/10.1016/j.biomaterials.2007.01.013; PMID: 17258311
  • Sikavitsas VI, Bancroft GN, Lemoine JJ, Liebschner MA, Dauner M, Mikos AG. Flow perfusion enhances the calcified matrix deposition of marrow stromal cells in biodegradable nonwoven fiber mesh scaffolds. Ann Biomed Eng 2005; 33:63 - 70; http://dx.doi.org/10.1007/s10439-005-8963-x; PMID: 15709706
  • Gomes ME, Reis RL, Mikos AG. Bone tissue engineering constructs based on starch scaffolds and bone marrow cells cultured in a flow perfusion bioreactor. Trans Tech Publ 2006; 2006:980 - 4
  • Sikavitsas VI, Bancroft GN, Lemoine JJ, Liebschner MA, Dauner M, Mikos AG. Flow perfusion enhances the calcified matrix deposition of marrow stromal cells in biodegradable nonwoven fiber mesh scaffolds. Ann Biomed Eng 2005; 33:63 - 70; http://dx.doi.org/10.1007/s10439-005-8963-x; PMID: 15709706
  • Alvarez-Barreto JF, Sikavitsas VI. Improved mesenchymal stem cell seeding on RGD-modified poly(L-lactic acid) scaffolds using flow perfusion. Macromol Biosci 2007; 7:579 - 88; http://dx.doi.org/10.1002/mabi.200600280; PMID: 17457938
  • Janssen FW, Hofland I, van Oorschot A, Oostra J, Peters H, van Blitterswijk CA. Online measurement of oxygen consumption by goat bone marrow stromal cells in a combined cell-seeding and proliferation perfusion bioreactor. J Biomed Mater Res A 2006; 79:338 - 48; http://dx.doi.org/10.1002/jbm.a.30794; PMID: 16878315
  • Cartmell SH, Porter BD, Garciáa AJ, Guldberg RE. Effects of medium perfusion rate on cell-seeded three-dimensional bone constructs in vitro. Tissue Eng 2003; 9:1197 - 203; http://dx.doi.org/10.1089/10763270360728107; PMID: 14670107
  • Jaasma MJ, Plunkett NA, O’Brien FJ. Design and validation of a dynamic flow perfusion bioreactor for use with compliant tissue engineering scaffolds. J Biotechnol 2008; 133:490 - 6; http://dx.doi.org/10.1016/j.jbiotec.2007.11.010; PMID: 18221813
  • Cioffi M, Boschetti F, Raimondi MT, Dubini G. Modeling evaluation of the fluid-dynamic microenvironment in tissue-engineered constructs: a micro-CT based model. Biotechnol Bioeng 2006; 93:500 - 10; http://dx.doi.org/10.1002/bit.20740; PMID: 16224789
  • Grayson WL, Marolt D, Bhumiratana S, Fröhlich M, Guo XE, Vunjak-Novakovic G. Optimizing the medium perfusion rate in bone tissue engineering bioreactors. Biotechnol Bioeng 2011; 108:1159 - 70; http://dx.doi.org/10.1002/bit.23024; PMID: 21449028
  • Hidalgo-Bastida LA, Thirunavukkarasu S, Griffiths S, Cartmell SH, Naire S. Modeling and design of optimal flow perfusion bioreactors for tissue engineering applications. Biotechnol Bioeng 2012; 109:1095 - 9; http://dx.doi.org/10.1002/bit.24368; PMID: 22068720
  • White FM. Viscous fluid flow. McGraw-Hill New York, 1991.
  • van den Dolder J, Bancroft GN, Sikavitsas VI, Spauwen PHM, Jansen JA, Mikos AG. Flow perfusion culture of marrow stromal osteoblasts in titanium fiber mesh. J Biomed Mater Res A 2003; 64:235 - 41; http://dx.doi.org/10.1002/jbm.a.10365; PMID: 12522809
  • Du D, Furukawa K, Ushida T. Oscillatory perfusion seeding and culturing of osteoblast-like cells on porous beta-tricalcium phosphate scaffolds. J Biomed Mater Res A 2008; 86:796 - 803; http://dx.doi.org/10.1002/jbm.a.31641; PMID: 18041721
  • Du D, Furukawa KS, Ushida T. 3D culture of osteoblast-like cells by unidirectional or oscillatory flow for bone tissue engineering. Biotechnol Bioeng 2009; 102:1670 - 8; http://dx.doi.org/10.1002/bit.22214; PMID: 19160373
  • Jagodzinski M, Breitbart A, Wehmeier M, Hesse E, Haasper C, Krettek C, et al. Influence of perfusion and cyclic compression on proliferation and differentiation of bone marrow stromal cells in 3-dimensional culture. J Biomech 2008; 41:1885 - 91; http://dx.doi.org/10.1016/j.jbiomech.2008.04.001; PMID: 18495131
  • Kavlock KD, Goldstein AS. Effect of pulse frequency on the osteogenic differentiation of mesenchymal stem cells in a pulsatile perfusion bioreactor. J Biomech Eng 2011; 133:091005; http://dx.doi.org/10.1115/1.4004919; PMID: 22010740
  • Sharp LA, Lee YW, Goldstein AS. Effect of low-frequency pulsatile flow on expression of osteoblastic genes by bone marrow stromal cells. Ann Biomed Eng 2009; 37:445 - 53; http://dx.doi.org/10.1007/s10439-008-9632-7; PMID: 19130228
  • Jaasma MJ, O’Brien FJ. Mechanical stimulation of osteoblasts using steady and dynamic fluid flow. Tissue Eng Part A 2008; 14:1213 - 23; http://dx.doi.org/10.1089/ten.tea.2007.0321; PMID: 18433309