Extraordinary biological properties of a new calcium hydroxyapatite/poly(lactide-co-glycolide)-based scaffold confirmed by in vivo investigation
-
Vukoman Jokanović
, Božana Čolović
, Dejan Marković , Milan Petrović , Ivan Soldatović , Djordje Antonijević , Petar Milosavljević , Nikola Sjerobabin und Jelena Sopta
Abstract
This study examined the potential of a new porous calcium hydroxyapatite scaffold covered with poly (lactide-co-glycolide) (PLGA) as a bone substitute, identifying its advantages over Geistlich Bio-Oss®, considered the gold standard, in in vivo biofunctionality investigations. Structural and morphological properties of the new scaffold were analyzed by scanning electron and atomic force microscopy. The biofunctionality assays were performed on New Zealand white rabbits using new scaffold for filling full-thickness defects of critical size. The evaluated parameters were: the presence of macrophages, giant cells, monoocytes, plasma cells, granulocytes, neoangiogenesis, fibroplasia, and the percentage of mineralization. Parallel biofunctionality assays were performed using Geistlich Bio-Oss®. The appearance of bone defects 12 weeks after the new scaffold implantation showed the presence of a small number of typical immune response cells. Furthermore, significantly reduced number of capillary buds, low intensity of fibroplasia and high degree of mineralization in a lamellar pattern indicated that the inflammation process has been almost completely overcome and that the new bone formed was in the final phase of remodeling. All biofunctionality assays proved the new scaffold’s suitability as a bone substitute for applications in maxillofacial surgery. It showed numerous biological advantages over Geistlich Bio-Oss® which was reflected mainly as a lower number of giant cells surrounding implanted material and higher degree of mineralization in new formed bone.
Funding source: Ministry of Education
Award Identifier / Grant number: 172026
Funding statement: This study was supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia (Project No. 172026).
Acknowledgments:
This study was supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia (Project No. 172026).
References
[1] Amini AR, Laurencin CT, Nukavarapu SP. Bone tissue engineering: recent advances and challenges. Crit Rev Biomed Eng. 2012; 40: 363–408.10.1615/CritRevBiomedEng.v40.i5.10Suche in Google Scholar
[2] Anderson JM, Rodriguez A, Chang DT. Foreign body reaction to biomaterials. Semin Immunol 2008; 20: 86–100.10.1016/j.smim.2007.11.004Suche in Google Scholar
[3] Bonadio J, Smiley JE, Patil P, Goldstein S. Localized, direct plasmid gene delivery in vivo: prolonged therapy results in reproducible tissue regeneration. Nat Med 1999; 5: 753–759.10.1038/10473Suche in Google Scholar
[4] Bose S, Roy M, Bandyopadhyay A. Recent advances in bone tissue engineering scaffolds. Trends Biotechnol 2012; 30: 547–564.10.1016/j.tibtech.2012.07.005Suche in Google Scholar
[5] Brodbeck WG, Macewan M, Colton E, Meyerson H, Anderson JM. Lymphocytes and the foreign body response: lymphocyte enhancement of macrophage adhesion and fusion. J Biomed Mater Res A 2005; 74: 222–229.10.1002/jbm.a.30313Suche in Google Scholar
[6] Brown LF, Lanir N, McDonagh J, Tognazzi K, Dvorak AM, Dvorak HF. Fibroblast migration in fibrin gel matrices. Am J Pathol 1993; 142: 273–283.Suche in Google Scholar
[7] Carmagnola D, Adriaens P, Berglundh T. Healing of human extraction sockets filled with Bio-Oss®. Clin Oral Impl Res 2003; 14: 137–143.10.1034/j.1600-0501.2003.140201.xSuche in Google Scholar
[8] Cestari TM, de Oliveira RC, Sanada JT, Garlet GP, Taga R, Granjeiro JM. Biocompatibility evaluation of a new bioresorbable pin for membrane fixation. Braz Dent J 2010; 21: 482–490.10.1590/S0103-64402010000600002Suche in Google Scholar
[9] Chapekar MS. Tissue engineering: challenges and opportunities. J Biomed Mater Res 2000; 53: 617–620.10.1002/1097-4636(2000)53:6<617::AID-JBM1>3.0.CO;2-CSuche in Google Scholar
[10] Constanz BR, Ison IC, Fulmer MT, et al. Skeletal repair by in situ formation of the mineral phase of bone. Science 1995; 267: 1769–1799.10.1126/science.7892603Suche in Google Scholar
[11] Cunha MJS, Esper LA, Sbrana MC, de Oliveira PGFP, do ValleAL, de Almeida ALPF. Effect of low-Level laser on bone defects treated with bovine or autogenous bone grafts: In vivo study in rat calvaria. BioMed Res Int 2014; 2014; Article ID 104230.10.1155/2014/104230Suche in Google Scholar
[12] Dhandayuthapani B, Yoshida Y, Maekawa T, Kumar DS. Polymeric scaffolds in tissue engineering application: a review. Int J Polymer Sci 2011; Article ID 290602, 1–19.10.1155/2011/290602Suche in Google Scholar
[13] Dimar JR, Glassman SD. The art of bone grafting. Curr Opin Orthopaed 2007; 18: 226–233.10.1097/BCO.0b013e328112f35dSuche in Google Scholar
[14] Durucan C, Brown PW. Calcium-deficient hydroxyapatite-PLGA composites: mechanical and microstructural investigation. J Biomed Mater Res 2000; 51: 726–734.10.1002/1097-4636(20000915)51:4<726::AID-JBM22>3.0.CO;2-LSuche in Google Scholar
[15] Frankenburg EP, Goldstein SA, Bauer TW, Harris SA, Poser RD. Biomechanical and histological evaluation of a calcium phosphate cement. J Bone Joint Surg Am 1998; 80: 1112–1124.10.2106/00004623-199808000-00004Suche in Google Scholar
[16] Furlaneto FAC, Nagata MJH, Fucini SE, Deliberador TM, Okamoto T, Messora MR. Bone healing in critical-size defects treated with bioactive glass/calcium sulfate: a histologic and histometric study in rat calvaria. Clin Oral Implants Res 2007, 18: 311–318.10.1111/j.1600-0501.2006.01331.xSuche in Google Scholar
[17] Ghanaati S, Barbeck M, Willershausen I, et al. Nanocrystalline hydroxyapatite bone substitute leads to sufficient bone tissue formation already after 3 months: histological and histomorphometrical analysis 3 and 6 months following human sinus cavity augmentation. Clin Implant Dent Relat Res 2013; 15: 883–892.10.1111/j.1708-8208.2011.00433.xSuche in Google Scholar
[18] Gil-Albarova J, Vila M, Badiola-Vargas J, Sánchez-Salcedo S, Herrera A, Vallet-Regi M. In vivo osteointegration of three-dimensional crosslinked gelatin-coated hydroxyapatite foams. Acta Biomater 2012; 8: 3777–3783.10.1016/j.actbio.2012.06.019Suche in Google Scholar
[19] Hollinger J. Strategies for regenerating bone of the craniofacial complex. Bone 1993; 14: 575–580.10.1016/8756-3282(93)90196-HSuche in Google Scholar
[20] Hutmacher DW. Scaffolds in tissue engineering bone and cartilage. Biomaterials 2000; 21: 2529–2543.10.1016/S0142-9612(00)00121-6Suche in Google Scholar
[21] Iqbal Sabir M, Xu X, Li L. A review on biodegradable polymeric materials for bone tissue engineering applications. J Mater Sci 2009; 44: 5713–5724.10.1007/s10853-009-3770-7Suche in Google Scholar
[22] Jensen T, Schou S, Stavropoulos A, Terheyden H, Holmstrup P. Maxillary sinus floor augmentation with Bio-Oss or Bio-Oss mixed with autogenous bone as graft: a systematic review. Clin Oral Impl Res 2012; 23: 263–273.10.1016/j.ijom.2011.08.010Suche in Google Scholar
[23] Jokanović V. Nanomedicine, the greatest challenge of the 21th century. Belgrade: Datastatus; 2012.Suche in Google Scholar
[24] Jokanović V, Čolović B, Jokanović B, Rudolf R. Relationship between activity of silica thin films and density of cells occupation. J Biomed Mater Res Part A 2014; 102: 1707–1714.10.1002/jbm.a.34844Suche in Google Scholar
[25] Jokanović V, Jokanović B, Marković D, et al. Kinetics and sintering mechanisms of hydro-thermally obtained hydroxyapatite. Mat Chem Phys 2008; 111: 180–185.10.1016/j.matchemphys.2008.04.005Suche in Google Scholar
[26] Kang Y, Scully A, Young DA, et al. Enhanced mechanical performance and biological evaluation of a PLGA coated β-TCP composite scaffold for load-bearing applications. Eur Polym J 2011; 47: 1569–1577.10.1016/j.eurpolymj.2011.05.004Suche in Google Scholar
[27] Kariem H, Pastrama MI, Roohani-Esfahani SI, Pivonka P, Zreiqat H, Hellmich C. Micro-poro-elasticity of baghdadite-based bone tissue engineering scaffolds: a unifying approach based on ultrasonics, nanoindentation, and homogenization theory. Mater Sci Eng C Mater Biol Appl 2015; 46: 553–564.10.1016/j.msec.2014.10.072Suche in Google Scholar
[28] Keller J, Brink S, Busse B, et al. Divergent resorbability and effects on osteoclast formation of commonly used bone substitutes in a human in vitro-assay. PLoS One 2012; 7: e46757.10.1371/journal.pone.0046757Suche in Google Scholar
[29] Komlev VS, Mastrogiacomo M, Pereira RC, Peyrin F, Rustichelli F, Cancedda R. Biodegradation of porous calcium phosphate scaffolds in an ectopic bone formation model studied by X-ray computed microtomograph. Eur Cell Mater 2010; 19: 136–146.10.22203/eCM.v019a14Suche in Google Scholar
[30] Komlev VS, Popov VK, Mironov AV, et al. 3D printing of octacalcium phosphate bone substitutes. Front Bioeng Biotechnol 2015; 3: 81.10.3389/fbioe.2015.00081Suche in Google Scholar
[31] Leferink AM, Chng YC, van Blitterswijk CA, Moroni L. Distribution and viability of fetal and adult human bone marrow stromal cells in a biaxial rotating vessel bioreactor after seeding on polymeric 3D additive manufactured scaffolds. Front Bioeng Biotechnol 2015; 3: 169.10.3389/fbioe.2015.00169Suche in Google Scholar
[32] LeGeros RZ. Biodegradation and bioresorption of calcium phosphate ceramics. Clin Mater 1993; 14: 65–88.10.1016/0267-6605(93)90049-DSuche in Google Scholar
[33] Leukers B, Gulkan HL, Irsen SH, et al. Hydroxyapatite scaffolds for bone tissue engineering made by 3D printing. J Mater Sci Mater Med 2005; 16: 1121–1124.10.1007/s10856-005-4716-5Suche in Google Scholar PubMed
[34] Li C, Vepari C, Jin HJ, Kim HJ, Kaplan DL. Electrospun silk-BMP-2 scaffolds for bone tissue engineering. Biomaterials 2006; 27: 3115–3124.10.1016/j.biomaterials.2006.01.022Suche in Google Scholar
[35] Li X, Wang L, Fan Y, Feng Q, Cui FY, Watari F. Nanostructured scaffolds for bone tissue engineering. J Biomed Mater Res Part A 2013; 101A: 2424–2435.10.1002/jbm.a.34539Suche in Google Scholar
[36] Liljensten EL, Attaelmanan AG, Larsson C, et al. Hydroxyapatite granule/carrier composites promote new bone formation in cortical defects. Clin Implant Dent Relat Res 2000; 2: 50–59.10.1111/j.1708-8208.2000.tb00106.xSuche in Google Scholar
[37] Liu X, Ma PX. Polymeric Scaffolds for bone tissue engineering. Ann Biomed Eng 2004; 32: 477–486.10.1023/B:ABME.0000017544.36001.8eSuche in Google Scholar
[38] Ma PX. Scaffolds for tissue fabrication. Mater Today 2004; 7: 30–40.10.1016/S1369-7021(04)00233-0Suche in Google Scholar
[39] Ma PX. Tissue Engineering. In: Kroschwitz JI, editor. Encyclopedia of polymer science and technology. Hoboken, NJ: John Wiley & Sons, Inc.; 2005: 261–291.Suche in Google Scholar
[40] Meng D, Dong L, Wen Y, Xie Q. Effects of adding resorbable chitosan microspheres to calcium phosphate cements for bone regeneration. Mater Sci Eng C 2015; 47: 266–272.10.1016/j.msec.2014.11.049Suche in Google Scholar
[41] Miño-Fariña N, Muñoz-Guzón F, López-Peña M, et al. Quantitative analysis of the resorption and osteoconduction of a macroporous calcium phosphate bone cement for the repair of a critical size defect in the femoral condyle. Vet J 2009; 179: 264–272.10.1016/j.tvjl.2007.09.011Suche in Google Scholar
[42] Park JE, Barbul A. Understanding the role of immune regulation in wound healing. Am J Surg 2004; 187: 11S–16S.10.1016/S0002-9610(03)00296-4Suche in Google Scholar
[43] Petrović M, Čolović B, Jokanović V, Marković D. Self assembly of biomimetic hydroxyapatite on the surface of different polymer thin films. J Ceram Process Res 2012; 13: 398–404.Suche in Google Scholar
[44] Piattelli M, Favero GA, Scarano A Orsini G Piattelli A. Bone reactions to anorganic bovine bone (Bio-Oss) used in sinus augmentation procedures: a histologic long-term report of 20 cases in humans. Int J Oral Maxillofac Implants 1999; 14: 835–840.Suche in Google Scholar
[45] Ramay HRR, Zhang M. Biphasic calcium phosphate nanocomposite porous scaffolds for load-bearing bone tissue engineering. Biomaterials 2004; 25: 5171–5180.10.1016/j.biomaterials.2003.12.023Suche in Google Scholar PubMed
[46] Rezwan K, Chen QZ, Blaker JJ, Boccaccini AR. Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. Biomaterials 2006; 27: 3413–3431.10.1016/j.biomaterials.2006.01.039Suche in Google Scholar PubMed
[47] Rose FRAJ, Oreffo ROC. Breakthroughs and views, bone tissue engineering: hope vs hype. Biochem Biophys Res Comm 2002; 292: 1–7.10.1006/bbrc.2002.6519Suche in Google Scholar
[48] Sfeir C, Ho L, Doll BA, Azari K, Hollinger JO. Fracture Repair. In: Lieberman JR, Friedlaender GE, editors. Bone regeneration and repair. New York: Humana Press 2005: 21–44.10.1385/1-59259-863-3:021Suche in Google Scholar
[49] Tovar N, Jimbo R, Gangolli R, et al. Evaluation of bone response to various anorganic bovine bone xenografts: an experimental calvaria defect study. Int J Oral Maxillofac Surg 2014; 43: 251–260.10.1016/j.ijom.2013.07.005Suche in Google Scholar
[50] Zhang RY, Ma PX. Porous poly(L-lactic acid)/apatite composites created by biomimetic process. J Biomed Mater Res 1999; 45: 285–293.10.1002/(SICI)1097-4636(19990615)45:4<285::AID-JBM2>3.0.CO;2-2Suche in Google Scholar
[51] Zhang W, Zhao H, Peng X, Cheng T, Zhang X. Low-dose captopril inhibits wear debrisinduced inflammatory osteolysis. J Int Med Res 2011; 39: 798–804.10.1177/147323001103900312Suche in Google Scholar
Supplemental Material:
The online version of this article (DOI: https://doi.org/10.1515/bmt-2015-0164) offers supplementary material, available to authorized users.
©2017 Walter de Gruyter GmbH, Berlin/Boston
Artikel in diesem Heft
- Frontmatter
- Review
- Bone plates for osteosynthesis – a systematic review of test methods and parameters for biomechanical testing
- Research articles
- Computer assisted evaluation of plate osteosynthesis of diaphyseal femur fracture considering interfragmentary movement: a finite element study
- Larger screw diameter may not guarantee greater pullout strength for headless screws – a biomechanical study
- Design considerations for patient-specific surgical templates for total hip arthroplasty with respect to acetabular cartilage
- Migration measurement of the cemented Lubinus SP II hip stem – a 10-year follow-up using radiostereometric analysis
- Shear stress and von Mises stress distributions in the periphery of an embedded acetabular cup implant during impingement
- Mechanical properties of contemporary orthodontic adhesives used for lingual fixed retention
- Extraordinary biological properties of a new calcium hydroxyapatite/poly(lactide-co-glycolide)-based scaffold confirmed by in vivo investigation
- Feasibility study of using a Microsoft Kinect for virtual coaching of wheelchair transfer techniques
- Accuracy of leg alignment measurements from antero-posterior radiographs
- Holoentropy enabled-decision tree for automatic classification of diabetic retinopathy using retinal fundus images
- Pattern recognition of enrichment levels of SELEX-based candidate aptamers for human C-reactive protein
- Source localization of S-cone and L/M-cone driven signals using silent substitution flash stimulation
Artikel in diesem Heft
- Frontmatter
- Review
- Bone plates for osteosynthesis – a systematic review of test methods and parameters for biomechanical testing
- Research articles
- Computer assisted evaluation of plate osteosynthesis of diaphyseal femur fracture considering interfragmentary movement: a finite element study
- Larger screw diameter may not guarantee greater pullout strength for headless screws – a biomechanical study
- Design considerations for patient-specific surgical templates for total hip arthroplasty with respect to acetabular cartilage
- Migration measurement of the cemented Lubinus SP II hip stem – a 10-year follow-up using radiostereometric analysis
- Shear stress and von Mises stress distributions in the periphery of an embedded acetabular cup implant during impingement
- Mechanical properties of contemporary orthodontic adhesives used for lingual fixed retention
- Extraordinary biological properties of a new calcium hydroxyapatite/poly(lactide-co-glycolide)-based scaffold confirmed by in vivo investigation
- Feasibility study of using a Microsoft Kinect for virtual coaching of wheelchair transfer techniques
- Accuracy of leg alignment measurements from antero-posterior radiographs
- Holoentropy enabled-decision tree for automatic classification of diabetic retinopathy using retinal fundus images
- Pattern recognition of enrichment levels of SELEX-based candidate aptamers for human C-reactive protein
- Source localization of S-cone and L/M-cone driven signals using silent substitution flash stimulation