Calcium phosphate combination biomaterials as human mesenchymal stem cell delivery vehicles for bone repair

Journal of Biomedical Materials Research - Part B Applied Biomaterials

Volumn 97 B, Issue 2, 2011, Pages 235-244

  Park, Sang Hyug ^a,b   Tofighi, Aliassghar ^a   Wang, Xiaoqin ^a,b   Strunk, Michael ^a   Ricketts, Thomas ^a   Chang, Jerry ^a   Kaplan, David L ^b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Tufts University   (United States)

Author keywords

alginate; calcium phosphate cement; carboxymethylcelluose; human mesenchymal stem cells; osteogenesis; silk

Indexed keywords

APATITIC CALCIUM PHOSPHATES; BIORESORBABLE; BODY TEMPERATURE; BONE REGENERATION; BONE REPAIR; BONE SUBSTITUTES; CALCIUM PHOSPHATE CEMENT; CARBOXY METHYLCELLULOSE; CARBOXYMETHYLCELLUOSE; CELL DELIVERY; CELL PROTECTION; CELL VIABILITY; DELIVERY VEHICLE; HANDLING CHARACTERISTICS; HIGH QUALITY; HUMAN MESENCHYMAL STEM CELLS; INJECTABILITY; MATRIX; ORTHOPEDIC APPLICATIONS; OSTEOGENESIS; OSTEOGENIC; PHYSIOLOGICAL SALINE; THERAPEUTIC AGENTS; TYPE I COLLAGEN; VISCOSITY MODIFIERS;

ALGINATE; ANIMAL CELL CULTURE; BIOLOGICAL MATERIALS; BIOMIMETICS; BONE; BONE CEMENT; CALCIUM; CELL CULTURE; CELL PROLIFERATION; CEMENTS; COLLAGEN; GENE EXPRESSION; MATERIALS HANDLING; PHOSPHATES; SILK; STEM CELLS;

CALCIUM PHOSPHATE;

ALGINIC ACID; CALCIUM PHOSPHATE CERAMIC; CARBOXYMETHYLCELLULOSE; COLLAGEN;

ADULT; ARTICLE; BONE DEVELOPMENT; BONE REGENERATION; BONE REMODELING; CELL PROLIFERATION; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; MALE; MESENCHYMAL STEM CELL; MORPHOLOGY; NONHUMAN; SILK;

ADULT; BIOCOMPATIBLE MATERIALS; BIOLOGICAL MARKERS; BONE CEMENTS; BONE REGENERATION; BONE SUBSTITUTES; CALCIUM PHOSPHATES; CELLS, CULTURED; HUMANS; MALE; MATERIALS TESTING; MESENCHYMAL STEM CELLS; STRESS, MECHANICAL; TISSUE ENGINEERING;

EID: 79953788932     PISSN: 15524973     EISSN: 15524981     Source Type: Journal    
DOI: 10.1002/jbm.b.31805     Document Type: Article

References (68)

1. Patka P, Haarman HJ, Bakker FC,. Bone transplantation and bone replacement materials. Ned Tijdschr Geneeskd 1998; 142: 893-896.
2. Sandhu HS, Grewal HS, Parvataneni H,. Bone grafting for spinal fusion. Orthop Clin North Am 1999; 30: 685-698. (Pubitemid 29471309)
3. Kwon B, Jenis LG,. Carrier materials for spinal fusion. Spine J 2005; 5: 224S-230S. (Pubitemid 41700065)
4. Lee YM, Seol YJ, Lim YT, Kim S, Han SB, Rhyu IC, Baek SH, Heo SJ, Choi JY, Klokkevold PR, et al. Tissue-engineered growth of bone by marrow cell transplantation using porous calcium metaphosphate matrices. J Biomed Mater Res 2001; 54: 216-223.
5. Petite H, Viateau V, Bensaid W, Meunier A, de Pollak C, Bourguignon M, Oudina K, Sedel L, Guillemin G,. Tissue-engineered bone regeneration. Nat Biotechnol 2000; 18: 959-963. (Pubitemid 32977376)
6. El-Ghannam A,. Bone reconstruction: From bioceramics to tissue engineering. Expert Rev Med Devices 2005; 2: 87-101. (Pubitemid 40124904)
7. Yaszemski MJ, Payne RG, Hayes WC, Langer R, Mikos AG,. Evolution of bone transplantation: Molecular, cellular and tissue strategies to engineer human bone. Biomaterials 1996; 17: 175-185. (Pubitemid 26031373)
8. Yang Z, Yuan H, Tong W, Zou P, Chen W, Zhang X,. Osteogenesis in extraskeletally implanted porous calcium phosphate ceramics: Variability among different kinds of animals. Biomaterials 1996; 17: 2131-2137. (Pubitemid 26364766)
9. Knabe C, Berger G, Gildenhaar R, Meyer J, Howlett CR, Markovic B, Zreiqat H,. Effect of rapidly resorbable calcium phosphates and a calcium phosphate bone cement on the expression of bone-related genes and proteins in vitro. J Biomed Mater Res A 2004; 69: 145-154. (Pubitemid 38364971)
10. Knabe C, Berger G, Gildenhaar R, Howlett CR, Markovic B, Zreiqat H,. The functional expression of human bone-derived cells grown on rapidly resorbable calcium phosphate ceramics. Biomaterials 2004; 25: 335-344. (Pubitemid 37336547)
11. Verret DJ, Ducic Y, Oxford L, Smith J,. Hydroxyapatite cement in craniofacial reconstruction. Otolaryngol Head Neck Surg 2005; 133: 897-899. (Pubitemid 41797242)
12. Xu HH, Simon CG, Jr,. Self-hardening calcium phosphate composite scaffold for bone tissue engineering. J Orthop Res 2004; 22: 535-543. (Pubitemid 38489730)
13. Miyamoto Y, Ishikawa K, Takechi M, Toh T, Yuasa T, Nagayama M, Suzuki K,. Histological and compositional evaluations of three types of calcium phosphate cements when implanted in subcutaneous tissue immediately after mixing. J Biomed Mater Res 1999; 48: 36-42. (Pubitemid 29088486)
14. Lu J, Descamps M, Dejou J, Koubi G, Hardouin P, Lemaitre J, Proust JP,. The biodegradation mechanism of calcium phosphate biomaterials in bone. J Biomed Mater Res 2002; 63: 408-412. (Pubitemid 34791195)
15. Edwards RB, 3rd, Seeherman HJ, Bogdanske JJ, Devitt J, Vanderby R, Jr, Markel MD,. Percutaneous injection of recombinant human bone morphogenetic protein-2 in a calcium phosphate paste accelerates healing of a canine tibial osteotomy. J Bone Joint Surg Am A 2004; 86: 1425-1438. (Pubitemid 38898645)
16. Seeherman HJ, Bouxsein M, Kim H, Li R, Li XJ, Aiolova M, Wozney JM,. Recombinant human bone morphogenetic protein-2 delivered in an injectable calcium phosphate paste accelerates osteotomy-site healing in a nonhuman primate model. J Bone Joint Surg Am A 2004; 86: 1961-1972. (Pubitemid 39232119)
17. Tay BK, Patel VV, Bradford DS,. Calcium sulfate- and calcium phosphate-based bone substitutes. Mimicry of the mineral phase of bone. Orthop Clin North Am 1999; 30: 615-623. (Pubitemid 29471303)
18. Habraken WJ, Wolke JG, Jansen JA,. Ceramic composites as matrices and scaffolds for drug delivery in tissue engineering. Adv Drug Deliv Rev 2007; 59: 234-248. (Pubitemid 46879968)
19. Speirs AD, Oxland TR, Masri BA, Poursartip A, Duncan CP,. Calcium phosphate cement composites in revision hip arthroplasty. Biomaterials 2005; 26: 7310-7318. (Pubitemid 41133582)
20. Lee DD, Tofighi A, Aiolova M, Chakravarthy P, Catalano A, Majahad A, Knaack D,. alpha-BSM: A biomimetic bone substitute and drug delivery vehicle. Clin Orthop Relat Res 1999: S396-405. (Pubitemid 29501518)
21. Knaack D, Goad ME, Aiolova M, Rey C, Tofighi A, Chakravarthy P, Lee DD,. Resorbable calcium phosphate bone substitute. J Biomed Mater Res 1998; 43: 399-409. (Pubitemid 28544099)
22. Larsson S, Bauer TW,. Use of injectable calcium phosphate cement for fracture fixation: A review. Clin Orthop Relat Res 2002: 23-32.
23. LeGeros RZ,. Properties of osteoconductive biomaterials: Calcium phosphates. Clin Orthop Relat Res 2002: 81-98.
24. Vaccaro AR,. The role of the osteoconductive scaffold in synthetic bone graft. Orthopedics 2002; 25: s571-578. (Pubitemid 36401429)
25. Fellah BH, Gauthier O, Weiss P, Chappard D, Layrolle P,. Osteogenicity of biphasic calcium phosphate ceramics and bone autograft in a goat model. Biomaterials 2008; 29: 1177-1188.
26. Habibovic P, Yuan H, van der Valk CM, Meijer G, van Blitterswijk CA, de Groot K,. 3D microenvironment as essential element for osteoinduction by biomaterials. Biomaterials 2005; 26: 3565-3575. (Pubitemid 40038151)
27. Li X, van Blitterswijk CA, Feng Q, Cui F, Watari F,. The effect of calcium phosphate microstructure on bone-related cells in vitro. Biomaterials 2008; 29: 3306-3316.
28. Cho BC, Park JW, Baik BS, Kim IS,. Clinical application of injectable calcium sulfate on early bony consolidation in distraction osteogenesis for the treatment of craniofacial microsomia. J Craniofac Surg 2002; 13: 465-475; discussion 475-467. (Pubitemid 34863627)
29. Tofighi A, Rosenberg A, Sutaris M, Balata SJC,. New generation of synthetic, bioresorbable and injectable calcium phosphate bone substitute matrials: Alpha-bsm, beta-bsm and gamma-bsm. J Biomimetics Biomater Tissue Eng 2009; 2: 39-55.
30. Li RH, Bouxsein ML, Blake CA, D'Augusta D, Kim H, Li XJ, Wozney JM, Seeherman HJ,. rhBMP-2 injected in a calcium phosphate paste (alpha-BSM) accelerates healing in the rabbit ulnar osteotomy model. J Orthop Res 2003; 21: 997-1004. (Pubitemid 37322380)
31. Zegzula HD, Buck DC, Brekke J, Wozney JM, Hollinger JO,. Bone formation with use of rhBMP-2 (recombinant human bone morphogenetic protein-2). J Bone Joint Surg Am 1997; 79: 1778-1790. (Pubitemid 28016582)
32. Schmitt JM, Buck DC, Joh SP, Lynch SE, Hollinger JO,. Comparison of porous bone mineral and biologically active glass in critical-sized defects. J Periodontol 1997; 68: 1043-1053. (Pubitemid 127513670)
33. Linhart W, Briem D, Schmitz ND, Priemel M, Lehmann W, Rueger JM,. Treatment of metaphyseal bone defects after fractures of the distal radius. Medium-term results using a calcium-phosphate cement (BIOBON). Unfallchirurg 2003; 106: 618-624. (Pubitemid 37092759)
34. Kong LB, Zhang TS, Ma J, Boey F,. Progress in synthesis of ferroelectric ceramic materials via high-energy mechanochemical technique. Prog Mater Sci 2008; 53: 207-322. (Pubitemid 351258124)
35. Ambard AJ, Mueninghoff L,. Calcium phosphate cement: Review of mechanical and biological properties. J Prosthodont 2006; 15: 321-328. (Pubitemid 44337428)
36. Weir MD, Xu HH, Simon CG, Jr,. Strong calcium phosphate cement-chitosan-mesh construct containing cell-encapsulating hydrogel beads for bone tissue engineering. J Biomed Mater Res A 2006; 77: 487-496. (Pubitemid 47233572)
37. Simon CG, Jr, Guthrie WF, Wang FW,. Cell seeding into calcium phosphate cement. J Biomed Mater Res A 2004; 68: 628-639. (Pubitemid 38268092)
38. 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: 643-655. (Pubitemid 47264638)
39. Sofia S, McCarthy MB, Gronowicz G, Kaplan DL,. Functionalized silk-based biomaterials for bone formation. J Biomed Mater Res 2001; 54: 139-148.
40. Park SH, Gil ES, Kim HJ, Lee K, Kaplan DL,. Relationships between degradability of silk scaffolds and osteogenesis. Biomaterials 2010; 31: 6162-6172.
41. Park SH, Park SR, Chung SI, Pai KS, Min BH,. Tissue-engineered cartilage using fibrin/hyaluronan composite gel and its in vivo implantation. Artif Organs 2005; 29: 838-845. (Pubitemid 43934125)
42. Jian Pan, Jie Mo Tian, Li Min Dong, Wang C,. Setting behavior of fast-setting calcium phosphate cement with mineral phase of bone. Key Eng Mater 2007; 280-283: 1567-1570.
43. Verfaillie CM,. Adult stem cells: Assessing the case for pluripotency. Trends Cell Biol 2002; 12: 502-508. (Pubitemid 35346700)
44. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR,. Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284: 143-147. (Pubitemid 29282067)
45. Maniatopoulos C, Sodek J, Melcher AH,. Bone formation in vitro by stromal cells obtained from bone marrow of young adult rats. Cell Tissue Res 1988; 254: 317-330.
46. Mankani MH, Kuznetsov SA, Shannon B, Nalla RK, Ritchie RO, Qin Y, Robey PG,. Canine cranial reconstruction using autologous bone marrow stromal cells. Am J Pathol 2006; 168: 542-550. (Pubitemid 43271152)
47. Yuan J, Cui L, Zhang WJ, Liu W, Cao Y,. Repair of canine mandibular bone defects with bone marrow stromal cells and porous beta-tricalcium phosphate. Biomaterials 2007; 28: 1005-1013. (Pubitemid 44809412)
48. Malard O, Guicheux J, Bouler JM, Gauthier O, de Montreuil CB, Aguado E, Pilet P, LeGeros R, Daculsi G,. Calcium phosphate scaffold and bone marrow for bone reconstruction in irradiated area: a dog study. Bone 2005; 36: 323-330. (Pubitemid 40283590)
49. Moreau JL, Xu HH,. Mesenchymal stem cell proliferation and differentiation on an injectable calcium phosphate-chitosan composite scaffold. Biomaterials 2009; 30: 2675-2682.
50. Xu HH, Simon CG, Jr,. Self-hardening calcium phosphate cement-mesh composite: reinforcement, macropores, and cell response. J Biomed Mater Res A 2004; 69: 267-278. (Pubitemid 38478819)
51. Matsuya S, Takagi S, Chow LC,. Effect of mixing ratio and pH on the reaction between Ca4(PO4)2O and CaHPO4. J Mater Sci Mater Med 2000; 11: 305-311.
52. dos Santos LA, Carrodeguas RG, Rogero SO, Higa OZ, Boschi AO, de Arruda AC,. Alpha-tricalcium phosphate cement: "in vitro" cytotoxicity. Biomaterials 2002; 23: 2035-2042. (Pubitemid 34251077)
53. Hsu Feng Ko, Charles Sfeir, Kumta PN,. In situ synthesis and characterization of porous polymer-ceramic composites as scaffolds for gene delivery. Mater Sci Eng C 2007; 27: 479-483. (Pubitemid 46281614)
54. Hutmacher DW, Goh JC, Teoh SH,. An introduction to biodegradable materials for tissue engineering applications. Ann Acad Med Singapore 2001; 30: 183-191. (Pubitemid 33613984)
55. Carrier RL, Papadaki M, Rupnick M, Schoen FJ, Bursac N, Langer R, Freed LE, Vunjak-Novakovic G,. Cardiac tissue engineering: cell seeding, cultivation parameters, and tissue construct characterization. Biotechnol Bioeng 1999; 64: 580-589. (Pubitemid 29359808)
56. Alves HL, Dos Santos LA, Bergmann CP,. Injectability evaluation of tricalcium phosphate bone cement. J Mater Sci Mater Med 2008; 19: 2241-2246.
57. Clarke SA, Hoskins NL, Jordan GR, Henderson SA, Marsh DR,. In vitro testing of Advanced JAX Bone Void Filler System: Species differences in the response of bone marrow stromal cells to beta tri-calcium phosphate and carboxymethylcellulose gel. J Mater Sci Mater Med 2007; 18: 2283-2290. (Pubitemid 350165595)
58. Reynolds MA, Aichelmann-Reidy ME, Kassolis JD, Prasad HS, Rohrer MD,. Calcium sulfate-carboxymethylcellulose bone graft binder: Histologic and morphometric evaluation in a critical size defect. J Biomed Mater Res B Appl Biomater 2007; 83: 451-458. (Pubitemid 350005016)
59. Aspenberg P, Lohmander LS,. Fibroblast growth factor stimulates bone formation. Bone induction studied in rats. Acta Orthop Scand 1989; 60: 473-476. (Pubitemid 19275628)
60. Altman GH, Diaz F, Jakuba C, Calabro T, Horan RL, Chen J, Lu H, Richmond J, Kaplan DL,. Silk-based biomaterials. Biomaterials 2003; 24: 401-416. (Pubitemid 35291198)
61. Wang X, Kluge JA, Leisk GG, Kaplan DL,. Sonication-induced gelation of silk fibroin for cell encapsulation. Biomaterials 2008; 29: 1054-1064. (Pubitemid 350296315)
62. Li Z, Ramay HR, Hauch KD, Xiao D, Zhang M,. Chitosan-alginate hybrid scaffolds for bone tissue engineering. Biomaterials 2005; 26: 3919-3928. (Pubitemid 40038783)
63. Stevens MM, Qanadilo HF, Langer R, Prasad Shastri V,. A rapid-curing alginate gel system: Utility in periosteum-derived cartilage tissue engineering. Biomaterials 2004; 25: 887-894. (Pubitemid 37371996)
64. Lin HR, Yeh YJ,. Porous alginate/hydroxyapatite composite scaffolds for bone tissue engineering: Preparation, characterization, and in vitro studies. J Biomed Mater Res B Appl Biomater 2004; 71: 52-65.
65. Xu HH, Weir MD, Simon CG,. Injectable and strong nano-apatite scaffolds for cell/growth factor delivery and bone regeneration. Dent Mater 2008; 24: 1212-1222.
66. Fukase Y, Eanes ED, Takagi S, Chow LC, Brown WE,. Setting reactions and compressive strengths of calcium phosphate cements. J Dent Res 1990; 69: 1852-1856.
67. Lian JB, Stein GS,. Development of the osteoblast phenotype: Molecular mechanisms mediating osteoblast growth and differentiation. Iowa Orthop J 1995; 15: 118-140.
68. Lian JB, Stein GS, The developmental stages of osteoblast growth and differentiation exhibit selective responses of genes to growth factors (TGF beta 1) and hormones (vitamin D and glucocorticoids). J Oral Implantol 19: 95-105, 1993; discussion 136-107.