Preparation and characterization of biodegradable nano hydroxyapatite–bacterial cellulose composites with well-defined honeycomb pore arrays for bone tissue engineering applications

Cellulose

Volumn 23, Issue 2, 2016, Pages 1263-1282

  Favi, Pelagie Marlene ^a   Ospina, Sandra Patricia ^b   Kachole, Mukta ^c   Gao, Ming ^c   Atehortua, Lucia ^b   Webster, Thomas Jay ^a,d  

^a Northeastern University   (United States)

^b UNIVERSIDAD DE ANTIOQUIA   (Colombia)

^c NORTHEASTERN UNIVERSITY   (United States)

^d KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

2,3 Dialdehyde bacterial cellulose; Biodegradable; Biomimetic hydroxyapatite; Bone tissue regeneration; Laser perforation; Microporous scaffold; Nanotechnology

Indexed keywords

BACTERIA; BIOCOMPATIBILITY; BIODEGRADATION; BIOMECHANICS; BIOMIMETICS; BONE; CELL CULTURE; CELL ENGINEERING; CELLULOSE; HONEYCOMB STRUCTURES; HYDROGELS; HYDROXYAPATITE; MECHANICAL PROPERTIES; MICROPOROSITY; NANOCOMPOSITES; NANOTECHNOLOGY; OXIDATION; PORE SIZE; SODIUM COMPOUNDS; STEM CELLS; TISSUE; TISSUE REGENERATION;

BACTERIAL CELLULOSE; BIODEGRADABLE; BIOMIMETIC HYDROXYAPATITES; BONE TISSUE REGENERATION; LASER PERFORATION; MICROPOROUS;

SCAFFOLDS (BIOLOGY);

EID: 84957033476     PISSN: 09690239     EISSN: 1572882X     Source Type: Journal    
DOI: 10.1007/s10570-016-0867-4     Document Type: Article

References (67)

1. Ahrem H et al (2014) Laser-structured bacterial nanocellulose hydrogels support ingrowth and differentiation of chondrocytes and show potential as cartilage implants. Acta Biomater 10:1341–1353. doi:10.1016/j.actbio.2013.12.004
2. Akkouch A, Zhang Z, Rouabhia M (2014) Engineering bone tissue using human dental pulp stem cells and an osteogenic collagen–hydroxyapatite-poly(L-lactide-co-ε-caprolactone) scaffold. J Biomater Appl 28(6):922–936. doi:10.1177/0885328213486705
3. American Society for Testing and Materials (2010) Standard test method for tensile properties of plastics. ASTM International, West Conshohocken, PA
4. Backdahl H, Esguerra M, Delbro D, Risberg B, Gatenholm P (2008) Engineering microporosity in bacterial cellulose scaffolds. J Tissue Eng Regen Med 2:320–330. doi:10.1002/term.97
5. Bäckdahl H, Helenius G, Bodin A, Nannmark U, Johansson BR, Risberg B, Gatenholm P (2006) Mechanical properties of bacterial cellulose and interactions with smooth muscle cells. Biomaterials 27:2141–2149. doi:10.1016/j.biomaterials.2005.10.026
6. Bansal M, Kaushik M, Khattak BBP, Sharma A (2014) Comparison of nanocrystalline hydroxyapatite and synthetic resorbable hydroxyapatite graft in the treatment of intrabony defects: a clinical and radiographic study. J Indian Soc Periodontol 18:213–219. doi:10.4103/0972-124X.131329
7. Berner A et al (2012) Biomimetic tubular nanofiber mesh and platelet rich plasma-mediated delivery of BMP-7 for large bone defect regeneration. Cell Tissue Res 347:603–612. doi:10.1007/s00441-011-1298-z
8. Bhardwaj N, Kundu SC (2010) Electrospinning: a fascinating fiber fabrication technique. Biotechnol Adv 28:325–347. doi:10.1016/j.biotechadv.2010.01.004
9. Bielecki S, Krystoynowicz A, Turkiewicz M, Kalinowska H (2001) Bacterial cellulose. In: Vandamme EJ, De Baets S, Steinb A (eds) Biopolymers. Polysaccharides I, polysaccharides from prokaryotes, vol 5. Wiley, Weinham, pp 37–46
10. Bose S, Vahabzadeh S, Bandyopadhyay A (2013) Bone tissue engineering using 3D printing. Mater Today 16:496–504. doi:10.1016/j.mattod.2013.11.017
11. Croisier F, Jérôme C (2013) Chitosan-based biomaterials for tissue engineering. Eur Polym J 49:780–792. doi:10.1016/j.eurpolymj.2012.12.009
12. Cui D, Daley W, Naftel JP, Lynch JC, Haines DE, Yang G, Fratkin JD (2011) Atlas of histology: with functional and clinical correlations, 1st edn. Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia
13. El-Ayoubi R, Degrandpre C, DiRaddo R, Yousefi A-M, Lavigne P (2011) Design and dynamic culture of 3D-scaffolds for cartilage tissue engineering. J Biomater Appl 25:429–444. doi:10.1177/0885328209355332
14. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677–689. doi:10.1016/j.cell.2006.06.044
15. Evans FG (1976) Mechanical properties and histology of cortical bone from younger and older men. Anat Rec 185:1–11. doi:10.1002/ar.1091850102
16. Favi PM, Benson RS, Neilsen NR, Hammonds RL, Bates CC, Stephens CP, Dhar MS (2013) Cell proliferation, viability, and in vitro differentiation of equine mesenchymal stem cells seeded on bacterial cellulose hydrogel scaffolds. Mater Sci Eng C 33:1935–1944. doi:10.1016/j.msec.2012.12.100
17. Favi PM, Dhar MS, Neilsen NR, Benson RS (2014) Proliferation and osteogenic differentiation of mesenchymal stem cells on biodegradable calcium-deficient hydroxyapatite tubular bacterial cellulose composites. MRS Proc. doi:10.1557/opl.2014.287
18. Fontana J et al (1990) Acetobacter cellulose pellicle as a temporary skin substitute. Appl Biochem Biotechnol 24–25:253–264. doi:10.1007/bf02920250
19. Harley BA, Lynn AK, Wissner-Gross Z, Bonfield W, Yannas IV, Gibson LJ (2010) Design of a multiphase osteochondral scaffold. II. Fabrication of a mineralized collagen–glycosaminoglycan scaffold. J Biomed Mater Res A 92A:1066–1077. doi:10.1002/jbm.a.32361
20. Helenius G, Bäckdahl H, Bodin A, Nannmark U, Gatenholm P, Risberg B (2006) In vivo biocompatibility of bacterial cellulose. J Biomed Mater Res A 76A:431–438. doi:10.1002/jbm.a.30570
21. Hersel U, Dahmen C, Kessler H (2003) RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials 24:4385–4415. doi:10.1016/S0142-9612(03)00343-0
22. Hu J, Zhou Y, Huang L, Liu J, Lu H (2014) Effect of nano-hydroxyapatite coating on the osteoinductivity of porous biphasic calcium phosphate ceramics. BMC Musculoskelet Disord 15:114. doi:10.1186/1471-2474-15-114
23. Hu J et al (2011) J Biomed Mater Res B, 2011, 97B and US Patent No. 20100172889
24. Hutchens SA, Benson RS, Evans BR, O’Neill HM, Rawn CJ (2006) Biomimetic synthesis of calcium-deficient hydroxyapatite in a natural hydrogel. Biomaterials 27:4661–4670. doi:10.1016/j.biomaterials.2006.04.032
25. Hutchens S, Benson R, Evans B, Rawn C, O’Neill H (2009) A resorbable calcium-deficient hydroxyapatite hydrogel composite for osseous regeneration. Cellulose 16:887–898. doi:10.1007/s10570-009-9300-6
26. Jalota S, Bhaduri SB, Tas AC (2008) Using a synthetic body fluid (SBF) solution of 27 mM HCO3− to make bone substitutes more osteointegrative. Mater Sci Eng C 28:129–140. doi:10.1016/j.msec.2007.10.058
27. Karageorgiou V, Kaplan D (2005) Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 26:5474–5491. doi:10.1016/j.biomaterials.2005.02.002
28. Kim B-S, Kang HJ, Lee J (2013) Improvement of the compressive strength of a cuttlefish bone-derived porous hydroxyapatite scaffold via polycaprolactone coating. J Biomed Mater Res B 101:1302–1309. doi:10.1002/jbm.b.32943
29. Kirkham KD, Roundy CB (2014) Current technology of beam profile measurement. In: Dickey FM (ed) Laser beam shaping: theory and techniques, 2nd edn. CRC Press, Taylor & Francis Group, Boca Raton, FL, pp 463–524
30. Klemm D, Schumann D, Udhardt U, Marsch S (2001) Bacterial synthesized cellulose—artificial blood vessels for microsurgery. Prog Polym Sci 26:1561–1603. doi:10.1016/s0079-6700(01)00021-1
31. Kondo T (1998) Hydrogen bonds in cellulose and cellulose derivatives. In: Dumitriu S (ed) Polysaccharides: structural diversity and functional versatility. vol Dumitriu S. Marcel Dekker Inc, New York, NY, pp 131–172
32. Kuboki Y, Jin Q, Takita H (2001) Geometry of carriers controlling phenotypic expression in BMP-induced osteogenesis and chondrogenesis. J Bone Joint Surg Am 83-A(Suppl 1 (Pt 2)):S105–S115
33. Kubota T, Sato K, Yamamoto S, Hirano A (1984) Ultrastructural study of the formation of psammoma bodies in fibroblastic meningioma. J Neurosurg 60:512–517. doi:10.3171/jns.1984.60.3.0512
34. Kucharzewski M, Slezak A, Franek A (2003) Topical treatment of non-healing venous leg ulcers by cellulose membrane. Phlebologie 32:138–169
35. Lee YM et al (2000) Tissue engineered bone formation using chitosan/tricalcium phosphate sponges. J Periodontol 71:410–417. doi:10.1902/jop.2000.71.3.410
36. Li J, Wan Y, Li L, Liang H, Wang J (2009) Preparation and characterization of 2,3-dialdehyde bacterial cellulose for potential biodegradable tissue engineering scaffolds. Mater Sci Eng C 29:1635–1642. doi:10.1016/j.msec.2009.01.006
37. Li K, Wang J, Liu X, Xiong X, Liu H (2012) Biomimetic growth of hydroxyapatite on phosphorylated electrospun cellulose nanofibers. Carbohydr Polym 90:1573–1581. doi:10.1016/j.carbpol.2012.07.033
38. Liu H, Webster TJ (2011) Enhanced biological and mechanical properties of well-dispersed nanophase ceramics in polymer composites: from 2D to 3D printed structures. Mater Sci Eng C 31:77–89. doi:10.1016/j.msec.2010.07.013
39. Lynn AK, Best SM, Cameron RE, Harley BA, Yannas IV, Gibson LJ, Bonfield W (2010) Design of a multiphase osteochondral scaffold. I. Control of chemical composition. J Biomed Mater Res A 92A:1057–1065. doi:10.1002/jbm.a.32415
40. Ma J et al (2014) Concise review: cell-based strategies in bone tissue engineering and regenerative medicine. Stem Cells Transl Med 3:98–107. doi:10.5966/sctm.2013-0126
41. Marolt D, Knezevic M, Novakovic GV (2010) Bone tissue engineering with human stem cells. Stem Cell Res Ther 1:10–20
42. Murphy CM, Haugh MG, O’Brien FJ (2010) The effect of mean pore size on cell attachment, proliferation and migration in collagen–glycosaminoglycan scaffolds for bone tissue engineering. Biomaterials 31:461–466. doi:10.1016/j.biomaterials.2009.09.063
43. Nguyen DT, Burg KJL (2015) Bone tissue engineering and regenerative medicine: targeting pathological fractures. J Biomed Mater Res A 103:420–429. doi:10.1002/jbm.a.35139
44. Okita Y, Saito T, Isogai A (2010) Entire surface oxidation of various cellulose microfibrils by TEMPO-mediated oxidation. Biomacromolecules 11:1696–1700. doi:10.1021/bm100214b
45. Painter TJ (1988) Control of depolymerisation during the preparation of reduced dialdehyde cellulose. Carbohydr Res 179:259–268. doi:10.1016/0008-6215(88)84123-5
46. Parenteau-Bareil R, Gauvin R, Berthod F (2010) Collagen-based biomaterials for tissue engineering applications. Materials 3:1863–1887
47. Pina S, Oliveira JM, Reis RL (2015) Natural-based nanocomposites for bone tissue engineering and regenerative medicine: a review. Adv Mater. doi:10.1002/adma.201403354
48. Pommerening K, Rein H, Betram D, Muller R (1992) Estimation of dialdehyde groups in 2,3-dialdehyde bead cellulose. Carboohydr Res 233:219–223
49. Rambo CR, Recouvreux DOS, Carminatti CA, Pitlovanciv AK, Antônio RV, Porto LM (2008) Template assisted synthesis of porous nanofibrous cellulose membranes for tissue engineering. Mater Sci Eng C 28:549–554. doi:10.1016/j.msec.2007.11.011
50. Roy-Chowdhury P, Kumar V (2006) Fabrication and evaluation of porous 2,3-dialdehydecellulose membrane as a potential biodegradable tissue-engineering scaffold. J Biomed Mater Res A 76A:300–309. doi:10.1002/jbm.a.30503
51. Salmen L, Akerholm M, Hinterstoisser B (2005) Two-dimensional Fourier transform infrared spectroscopy applied to cellulose and paper. In: Dumitriu S (ed) Polysaccharides: structural diversity and functional versatility, 2nd edn. CRC Press, Taylor & Francis Group, Boca Raton, FL, pp 159–187
52. Sanchavanakit N, Sangrungraungroj W, Kaomongkolgit R, Banaprasert T, Pavasant P, Phisalaphong M (2006) Growth of human keratinocytes and fibroblasts on bacterial cellulose film. Biotechnol Prog 22:1194–1199. doi:10.1021/bp060035o
53. Schrarnrn M, Hestrin S (1954) Factors affecting production of cellulose at the air/liquid interface of a culture of Acetobacter xylinum. J Gen Microbiol 11:123–129
54. Smith EL et al (2014) Evaluation of skeletal tissue repair, part 1: assessment of novel growth-factor-releasing hydrogels in an ex vivo chick femur defect model. Acta Biomater 10:4186–4196. doi:10.1016/j.actbio.2014.06.011
55. Suárez-González D et al (2013) Controlled multiple growth factor delivery from bone tissue engineering scaffolds via designed affinity. Tissue Eng A 20:2077–2087. doi:10.1089/ten.tea.2013.0358
56. Svensson A, Nicklasson E, Harrah T, Panilaitis B, Kaplan DL, Brittberg M, Gatenholm P (2005) Bacterial cellulose as a potential scaffold for tissue engineering of cartilage. Biomaterials 26:419–431. doi:10.1016/j.biomaterials.2004.02.049
57. Torabinejad B, Mohammadi-Rovshandeh J, Davachi SM, Zamanian A (2014) Synthesis and characterization of nanocomposite scaffolds based on triblock copolymer of l-lactide, ε-caprolactone and nano-hydroxyapatite for bone tissue engineering. Mater Sci Eng C 42:199–210. doi:10.1016/j.msec.2014.05.003
58. Tracy BM, Doremus RH (1984) Direct electron microscopy studies of the bone–hydroxylapatite interface. J Biomed Mater Res 18:719–726. doi:10.1002/jbm.820180702
59. Tsuruga E, Takita H, Itoh H, Wakisaka Y, Kuboki Y (1997) Pore size of porous hydroxyapatite as the cell-substratum controls BMP-induced osteogenesis. J Biochem 121:317–324
60. Ustundag CB, Kaya F, Kamitakahara M, Kaya C, Ioku K (2012) Production of tubular porous hydroxyapatite using electrophoretic deposition. J Ceram Soc Jpn 120:569–573
61. Varma AJ, Kulkarni MP (2002) Oxidation of cellulose under controlled conditions. Polym Degrad Stabil 77:25–27
62. Wan YZ et al (2007) Biomimetic synthesis of hydroxyapatite/bacterial cellulose nanocomposites for biomedical applications. Mater Sci Eng C 27:855–864. doi:10.1016/j.msec.2006.10.002
63. Wang J, Chunxi Y, Yizao W, Honglin L, Fang H, Kerong D, Yuan H (2011) Laser patterning of bacterial cellulose hydrogel and its modification with gelatin and hydroxyapatite for bone tissue engineering. Soft Mater 11:173–180. doi:10.1080/1539445X.2011.611204
64. Webster TJ, Ergun C, Doremus RH, Siegel RW, Bizios R (2000a) Enhanced functions of osteoblasts on nanophase ceramics. Biomaterials 21:1803–1810. doi:10.1016/S0142-9612(00)00075-2
65. Webster TJ, Ergun C, Doremus RH, Siegel RW, Bizios R (2000b) Specific proteins mediate enhanced osteoblast adhesion on nanophase ceramics. J Biomed Mater Res 51:475–483. doi:10.1002/1097-4636(20000905)51:3<475:aid-jbm23>3.0.co;2-9
66. Wegman F, Geuze RE, van der Helm YJ, Cumhur Öner F, Dhert WJA, Alblas J (2014) Gene delivery of bone morphogenetic protein-2 plasmid DNA promotes bone formation in a large animal model. J Tissue Eng Regen Med 8:763–770. doi:10.1002/term.1571
67. Wu J, Zheng Y, Yang Z, Lin Q, Qiao K, Chen X, Peng Y (2014) Influence of dialdehyde bacterial cellulose with the nonlinear elasticity and topology structure of ECM on cell adhesion and proliferation. RSC Adv 4:3998–4009. doi:10.1039/C3RA45407J