A novel bidirectional continuous perfusion bioreactor for the culture of large-sized bone tissue-engineered constructs

Journal of Biomedical Materials Research - Part B Applied Biomaterials

Volumn 101, Issue 8, 2013, Pages 1377-1386

  Gardel, Leandro S ^a,b   Correia Gomes, Carla ^b   Serra, Luís A ^c   Gomes, Manuela E ^a   Reis, Rui L ^a  

^a UNIVERSITY OF MINHO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c HOSPITAL DE SANTO ANTÓNIO   (Portugal)

Author keywords

bone; flow perfusion system; goat bone marrow stromal cells; osteogenic differentiation; starch polycaprolactone scaffolds

Indexed keywords

BIOCONVERSION; BIOREACTORS; BONE; CELL PROLIFERATION; CELLS; CYTOLOGY; METABOLISM; PHOSPHATASES; SCANNING ELECTRON MICROSCOPY; SHEAR FLOW; STARCH; TISSUE;

BONE MARROW STROMAL CELLS; BONE TISSUE ENGINEERING; CELLULAR PROLIFERATIONS; CRITICAL SIZED DEFECTS; FLOW PERFUSION; OSTEOGENIC DIFFERENTIATION; POLYCAPROLACTONE SCAFFOLDS; PRELIMINARY ASSESSMENT;

SCAFFOLDS (BIOLOGY);

ALKALINE PHOSPHATASE; DNA; POLYCAPROLACTONE; STARCH; POLYESTER; STARCH POLYCAPROLACTONE;

ANIMAL CELL; ARTICLE; BIOREACTOR; BONE; BONE MARROW; BONE MARROW STROMAL CELL; BONE REGENERATION; BONE TISSUE ENGINEERING; CELL DIFFERENTIATION; CONTROLLED STUDY; FLOW PERFUSION SYSTEM; GOAT; NONHUMAN; PERFUSION; SCANNING ELECTRON MICROSCOPY; TISSUE ENGINEERING; ANIMAL; BONE DEVELOPMENT; CELL ADHESION; CELL MOTION; CELL PROLIFERATION; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; EQUIPMENT DESIGN; MESENCHYMAL STROMA CELL; PHENOTYPE; PROCEDURES; TISSUE SCAFFOLD;

ANIMALS; BIOREACTORS; BONE AND BONES; CELL ADHESION; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; EQUIPMENT DESIGN; GOATS; MESENCHYMAL STROMAL CELLS; OSTEOGENESIS; PERFUSION; PHENOTYPE; POLYESTERS; STARCH; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84886591731     PISSN: 15524973     EISSN: 15524981     Source Type: Journal    
DOI: 10.1002/jbm.b.32955     Document Type: Article

References (45)

1. van den Dolder J, Bancroft GN, Sikavitsas VI, Spauwen PH, Jansen JA, Mikos AG,. Flow perfusion culture of marrow stromal osteoblasts in titanium fiber mesh. J Biomed Mater Res Part A 2003; 64 (2): 235-241.
2. Grayson WL, Marolt D, Bhumiratana S, Frohlich M, Guo XE, Vunjak-Novakovic G,. Optimizing the medium perfusion rate in bone tissue engineering bioreactors. Biotechnol Bioeng 2011; 108 (5): 1159-1170.
3. Grayson WL, Bhumiratana S, Cannizzaro C, Chao PHG, Lennon DP, Caplan AI, Vunjak-Novakovic G,. Effects of initial seeding density and fluid perfusion rate on formation of tissue-engineered bone. Tissue Eng Part A 2008; 14 (11): 1809-1820.
4. Marolt D, Augst A, Freed LE,. Bone and cartilage tissue constructs grown using human bone marrow stromal cells, silk scaffolds and rotating bioreactors. Biomaterials 2006; 27 (36): 6138-6149.
5. Gomes ME, Bossano CM, Johnston CM, Reis RL, Mikos AG,. In vitro localization of bone growth factors in constructs of biodegradable scaffolds seeded with marrow stromal cells and cultured in a flow perfusion bioreactor. Tissue Eng 2006; 12 (1): 177-188.
6. Gomes ME, Holtorf HL, Reis RL, Mikos AG,. Influence of the porosity of starch-based fiber mesh scaffolds on the proliferation and osteogenic differentiation of bone marrow stromal cells cultured in a flow perfusion bioreactor. Tissue Eng 2006; 12 (4): 801-809.
7. Reichert JC, Saifzadeh S, Wullschleger ME, Epari DR, Schutz MA, Duda GN, Schell H, van Griensven M, Redl H, Hutmacher DW,. The challenge of establishing preclinical models for segmental bone defect research. Biomaterials 2009; 30 (12): 2149-2163.
8. Lindsey RW, Gugala Z, Milne E, Sun M, Gannon FH, Latta LL,. The efficacy of cylindrical titanium mesh cage for the reconstruction of a critical-size canine segmental femoral diaphyseal defect. J Orthop Res 2006; 24 (7): 1438-1453.
9. Gugala Z, Gogolewski S,. Regeneration of segmental diaphyseal defects in sheep tibiae using resorbable polymeric membranes: A preliminary study. J Orthop Trauma 1999; 13 (3): 187-195.
10. Pashkuleva I, Azevedo HS, Reis RL,. Surface structural investigation of starch-based biomaterials. Macromol Biosci 2008; 8 (2): 210-219.
11. Rodrigues MT, Gomes ME, Viegas CA, Azevedo JT, Dias IR, Guzon FM, Reis RL,. Tissue-engineered constructs based on SPCL scaffolds cultured with goat marrow cells: functionality in femoral defects. J Tissue Eng Regen Med 2011; 5 (1): 41-49.
12. 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 Part A 2003; 67A (1): 87-95.
13. Gomes ME, Azevedo HS, Moreira AR, Ella V, Kellomaki M, Reis RL,. Starch-poly(epsilon-caprolactone) and starch-poly(lactic acid) fibre-mesh scaffolds for bone tissue engineering applications: structure, mechanical properties and degradation behaviour. J Tissue Eng Regen Med 2008; 2 (5): 243-252.
14. Marques AP, Cruz HR, Coutinho OP, Reis RL,. Effect of starch-based biomaterials on the in vitro proliferation and viability of osteoblast-like cells. J Mater Sci Mater Med 2005; 16 (9): 833-842.
15. Gomes ME, Ribeiro AS, Malafaya PB, Reis RL, Cunha AM,. A new approach based on injection moulding to produce biodegradable starch-based polymeric scaffolds: morphology, mechanical and degradation behaviour. Biomaterials 2001; 22 (9): 883-889.
16. Santos MI, Tuzlakoglu K, Fuchs S, Gomes ME, Peters K, Unger RE, Piskin E, Reis RL, Kirkpatrick CJ,. Endothelial cell colonization and angiogenic potential of combined nano- and micro-fibrous scaffolds for bone tissue engineering. Biomaterials 2008; 29 (32): 4306-4313.
17. Martins AM, Pham QP, Malafaya PB, Sousa RA, Gomes ME, Raphael RM, Kasper FK, Reis RL, Mikos AG,. The role of lipase and alpha-amylase in the degradation of starch/poly(epsilon-caprolactone) fiber meshes and the osteogenic differentiation of cultured marrow stromal cells. Tissue Eng Part A 2009; 15 (2): 295-305.
18. Santos TC, Marques AP, Horing B, Martins AR, Tuzlakoglu K, Castro AG, van Griensven M, Reis RL,. In vivo short-term and long-term host reaction to starch-based scaffolds. Acta Biomater 2010; 6 (11): 4314-4326.
19. Rodrigues MT, Martins A, Dias IR, Viegas CA, Neves NM, Gomes ME, Reis RL,. Synergistic effect of scaffold composition and dynamic culturing environment in multilayered systems for bone tissue engineering. J Tissue Eng Regen Med 2012; 6 (10): e24-e30.
20. Bancroft GN, Sikavitsas VI, van den Dolder J, Sheffield TL, Ambrose CG, Jansen JA, Mikos AG,. Fluid flow increases mineralized matrix deposition in 3D perfusion culture of marrow stromal osteoblasts in a dose-dependent manner. Proc Natl Acad Sci USA 2002; 99 (20): 12600-12605.
21. Martin Y, Vermette P,. Bioreactors for tissue mass culture: design, characterization, and recent advances. Biomaterials 2005; 26 (35): 7481-75503.
22. Martin I, Wendet D, Heberer M,. The roles of bioreactor in tissue engineering. Trends Biotechnol 2004; 22 (2): 80-86.
23. Stiehler M, Bunger 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 Part A 2009; 89 (1): 96-107.
24. 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 Part A 2008; 86 (2): 323-332.
25. Mygind T, Stiehler M, Baatrup A, Li H, Zoua X, Flyvbjerg A, Kassem M, Bunger C,. Mesenchymal stem cell ingrowth and differentiation on coralline hydroxyapatite scaffolds. Biomaterials 2007; 28 (6): 1036-1047.
26. Chen HC, Hu YC,. Bioreactors for tissue engineering. Biotechnol Lett 2006; 28 (18): 1415-1423.
27. 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 (1): 136-148.
28. Yu XJ, 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 USA 2004; 101 (31): 11203-11208.
29. 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 (4): 513-519.
30. Molnar G, Schroedl NA, Gonda SR, Hartzell CR,. Skeletal muscle satellite cells cultured in simulated microgravity. In Vitro Cell Dev Biol Anim 1997; 33 (5): 386-391.
31. 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 USA 2003; 100 (25): 14683-14688.
32. 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 (11): 1279-1288.
33. Keogh MB, Partap S, Daly JS, O'Brien FJ,. Three hours of perfusion culture prior to 28 days of static culture, enhances osteogenesis by human cells in a collagen GAG scaffold. Biotechnol Bioeng 2011; 108 (5): 1203-1210.
34. Du DJ, Furukawa KS, Ushida T,. 3D culture of osteoblast-like cells by unidirectional or oscillatory flow for bone tissue engineering. Biotechnol Bioeng 2009; 102 (6): 1670-1678.
35. Schliephake H, Zghoul N, Jager V, van Griensven M, Zeichen J, Gelinsky M, Szubtarsky N,. Bone formation in trabecular bone cell seeded scaffolds used for reconstruction of the rat mandible. Int J Oral Maxillofac Surg 2009; 38 (2): 166-172.
36. Zhang ZY, Teoh SH, Chong WS, Foo TT, Chng YC, Choolani M, Chan J,. A biaxial rotating bioreactor for the culture of fetal mesenchymal stem cells for bone tissue engineering. Biomaterials 2009; 30 (14): 2694-2704.
37. Sailon AM, Allori AC, Davidson EH, Reformat DD, Allen RJ, Warren SM,. A novel flow-perfusion bioreactor supports 3D dynamic cell culture. J Biomed Biotechnol 2009; 2009: 1-7.
38. Bjerre L, Bunger CE, Kassem M, Mygind T,. Flow perfusion culture of human mesenchymal stem cells on silicate-substituted tricalcium phosphate scaffolds. Biomaterials 2008; 29 (17): 2616-2627.
39. 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 Part A 2008; 86 (3): 796-803.
40. Kavlock KD, Goldstein AS,. Effect of pulsatile flow on the osteogenic differentiation of bone marrow stromal cells in porous scaffolds. Biomed Sci Instrum 2008; 44: 471-476.
41. Holtorf HL, Jansen JA, Mikos AG,. Flow perfusion culture induces the osteoblastic differentiation of marrow stromal cell-scaffold constructs in the absence of dexamethasone. J Biomed Mater Res Part A 2005; 72A (3): 326-334.
42. 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 (9): 1238-1248.
43. Xie YZ, Hardouin P, Zhu ZN, Tang TT, Dai KR, Lu JX,. Three-dimensional flow perfusion culture system for stem cell proliferation inside the critical-size beta-tricalcium phosphate scaffold. Tissue Eng 2006; 12 (12): 3535-3543.
44. Olivier V, Hivart PH, Descamps M, Hardouin P,. In vitro culture of large bone substitutes in a new bioreactor: importance of the flow direction. Biomed Mater 2007 (2): 174-180.
45. Zhang ZY, Teoh SH, Teo EY, Chong MSK, Shin CW, Tien FT, Choolani MA, Chan JKY,. A comparison of bioreactors for culture of fetal mesenchymal stem cells for bone tissue engineering. Biomaterials 2010; 31 (33): 8684-8695.