Journal of the Korean institute of surface engineering (한국표면공학회지)

The Korean Institute of Surface Engineering (한국표면공학회)
권호 표지
DOI QR코드

DOI QR Code

Research trends and Efficacy Analysis of Surface Characteristics of Bone Grafts

골이식재의 표면 특성 연구 동향과 유효성 분석

  • Yong-Hoon Jeong (Department of Medical Device Development Center, Osong Medical Innovation Foundation (KBIOHealth)) ;
  • Gye-Wook Lee (Department of Medical Device Development Center, Osong Medical Innovation Foundation (KBIOHealth)) ;
  • Tae-Gon Jung (Department of Medical Device Development Center, Osong Medical Innovation Foundation (KBIOHealth))
  • 정용훈 (오송첨단의료산업진흥재단 첨단의료기기개발지원센터) ;
  • 이계욱 (오송첨단의료산업진흥재단 첨단의료기기개발지원센터) ;
  • 정태곤 (오송첨단의료산업진흥재단 첨단의료기기개발지원센터)
  • Received : 2024.07.04
  • Accepted : 2024.07.23
  • Published : 2024.08.31
Download PDF
⟨ Previous Next ⟩

Abstract

As the population ages, the importance of effective bone disease treatments is increasing, highlighting the role of bone grafts. Bone grafts are categorized into natural (autografts, allografts, xenografts) and synthetic (ceramics, polymers). Natural grafts have excellent regenerative abilities but pose biological risks, while synthetic grafts are biocompatible but less effective in regeneration. Various studies aim to enhance the safety and efficacy of bone grafts, significantly altering their surface properties. This review examines these studies and the resulting surface changes, aiming to guide future research and clinical applications.

Keywords

References

  1. J.M. Lane, H.S. Sandhu, Current approaches to experimental bone grafting, Orthopedic Clinics of North America, 18 (1987) 213-225.
  2. S.D. Boden, D.R. Sumner, Biologic factors affecting spinal fusion and bone regeneration, Spine, 20 (1995) 113S.
  3. S.N. Khan, F. Cammisa, H.S. Sandhu, D.P. Diwan, K.L. Girardi, D.R. Lane, K.S. Khan, The biology of bone grafting, JAAOS-Journal of the American Academy of Orthopaedic Surgeons, 13 (2005) 77-86.
  4. M.A. Velasco, C.A. Narvaez-Tovar, D.A. Garzon-Alvarado, Design, materials, and mechanobiology of biodegradable scaffolds for bone tissue engineering, Biomedical Research International, (2015) 729076.
  5. J.J. Klawitter, J.G. Bagwell, A.M. Weinstein, B.W. Sauer, J.R. Pruitt, An evaluation of bone growth into porous high density polyethylene, Journal of Biomedical Materials Research, (1976) 311-323.
  6. A.H. Schmidt, Autologous bone graft: is it still the gold standard?, Injury, 52 (2021) S18-S22.
  7. G.F. Rogers, A.K. Greene, Autogenous bone graft: basic science and clinical implications, Journal of Craniofacial Surgery, 23 (2012) 323-327.
  8. H.Y. Park, S.I. Kim, Y.H. Kim, Biomaterials and futures for bone regeneration, Journal of the Korean Orthopaedic Association, 57 (2022) 447-456.
  9. J. Jeong, J.H. Kim, J.H. Shim, J.H. Hwang, W.H. Heo, Bioactive calcium phosphate materials and applications in bone regeneration, Biomaterials Research, 23 (2019) 4.
  10. Y. Fillingham, J. Jacobs, Bone grafts and their substitutes, The Bone & Joint Journal, 98 (2016) 6-9.
  11. E.M. Younger, M.W. Chapman, Morbidity at bone graft donor sites, Journal of Orthopaedic Trauma, 3 (1989) 192-195.
  12. B. Mahardawi, S.H. Kim, C.H. Kim, H.S. Kim, Autogenous tooth bone graft material prepared chairside and its clinical applications: a systematic review, International Journal of Oral and Maxillofacial Surgery, 52 (2023) 132-141.
  13. G.W. Kim, S.K. Lee, J.Y. Kim, J.Y. Seo, S.I. Park, Analysis of crystalline structure of autogenous tooth bone graft material: X-ray diffraction analysis, Journal of the Korean Association of Oral and Maxillofacial Surgeons, 37 (2011) 225-228.
  14. S.H. Lee, Low crystalline hydroxyl carbonate apatite, The Journal of the Korean Dental Association, 44 (2006) 524-533.
  15. Y.K. Kim, J.Y. Lee, Y.S. Kim, J.W. Yun, Analysis of the inorganic component of autogenous tooth bone graft material, Journal of Nanoscience and Nanotechnology, 11 (2011) 7442-7445.
  16. Centers for Disease Control (CDC), Transmission of HIV through bone transplantation: case report and public health recommendations, MMWR. Morbidity and Mortality Weekly Report, 37 (1988) 597-599.
  17. R. Murugan, K.P. Rao, T.S. Sampath Kumar, Heat-deproteinated xenogeneic bone from slaughterhouse waste: physico-chemical properties, Bulletin of Materials Science, 26 (2003) 523- 528.
  18. A. Figueiredo, M.S. Brito, J.A. Carvalho, R.L. Resende, F.M. Passos, A.C. Borges, Comparison of a xenogeneic and an alloplastic material used in dental implants in terms of physicochemical characteristics and in vivo inflammatory response, Materials Science and Engineering: C, 33 (2013) 3506-3518.
  19. C. Delloye, M. Cornu, D. Druez, O. Barbier, Bone allografts: what they can offer and what they cannot, The Journal of Bone & Joint Surgery British Volume, 89 (2007) 574-580.
  20. J.F. Trotter, Transmission of hepatitis C by implantation of a processed bone graft: a case report, The Journal of Bone and Joint Surgery, 85 (2003) 2215-2217.
  21. A. Pruss, R. Ottinger, M. Keler, J. Maier, R. Hepner, Effect of gamma irradiation on human cortical bone transplants contaminated with enveloped and non-enveloped viruses, Biologicals, 30 (2002) 125-133.
  22. T. Boyce, J. Edwards, N. Scarborough, Allograft bone: the influence of processing on safety and performance, Orthopedic Clinics, 30 (1999) 571-581.
  23. C.A. DePaula, R.J. Phipps, A.W. Goldenberg, R.G. Tamer, Effects of hydrogen peroxide cleaning procedures on bone graft osteoinductivity and mechanical properties, Cell and Tissue Banking, 6 (2005) 287-298.
  24. M.W. Wolfe, S.L. Salkeld, S.D. Cook, Bone morphogenetic proteins in the treatment of non-unions and bone defects: historical perspective and current knowledge, The University of Pennsylvania Orthopaedic Journal, 12 (1999) 1-6.
  25. G. Villatte, P. Bassel, B. Nguyen, Evaluation of the biomechanical and structural properties of bone allografts treated with a new cleaning process, World Journal of Advanced Research and Reviews, 14 (2022) 608-616.
  26. A. Rasch, K. Wolf, C. Krause, U. Nolte, F. Langer, Evaluation of bone allograft processing methods: impact on decellularization efficacy, biocompatibility and mesenchymal stem cell functionality, PLoS One, 14 (2019) e0218404.
  27. D.K. Kim, H.J. Jeong, J.Y. Park, J.H. Lee, Y.J. Kim, Comparison of a synthetic bone substitute composed of carbonated apatite with an anorganic bovine xenograft in particulate forms in a canine maxillary augmentation model, Clinical Oral Implants Research, 21 (2010) 1334-1344.
  28. I.A. Karampas, C.G. Kontoyannis, Characterization of calcium phosphates mixtures, Vibrational Spectroscopy, 64 (2013) 126-133.
  29. S.T. Kao, D.D. Scott, A review of bone substitutes, Oral and Maxillofacial Surgery Clinics of North America, 19 (2007) 513-521.
  30. B. Long, S. Liu, X. Zhang, L. Wang, Evaluation of a novel reconstituted bone xenograft using processed bovine cancellous bone in combination with purified bovine bone morphogenetic protein, Xenotransplantation, 19 (2012) 122-132.
  31. N.N. Pathak, D.K. Pathak, P.D. Sharma, Mineral composition of antlers of three deer species reared in captivity, Small Ruminant Research, 42 (2001) 61-65.
  32. B.T. Bezerra, J.C. de Almeida, R.C. Lopes, R.J.L. Lima, Autogenous bone graft versus bovine bone graft in association with platelet-rich plasma for the reconstruction of alveolar clefts: a pilot study, International Journal of Oral and Maxillofacial Surgery, 52 (2023) 132-141.
  33. A. A. Qabbani, H.G. Wang, J.B. Lin, Evaluation of decellularization process for developing osteogenic bovine cancellous bone scaffolds in-vitro, PLoS One, 18 (2023) e0283922.
  34. M.L. Wong, L.G. Griffiths, Immunogenicity in xenogeneic scaffold generation: antigen removal vs. decellularization, Acta Biomaterialia, 10 (2014) 1806-1816.
  35. D.W. Hutmacher, M. Sittinger, M.V. Risbud, State of the art and future directions of scaffold-based bone engineering from a biomaterials perspective, Journal of Tissue Engineering and Regenerative Medicine, 1 (2007) 245-260.
  36. T. Jensen, L. Schou, L. Svendsen, H. Forman, Maxillary sinus floor augmentation with Bio-Oss or Bio-Oss mixed with autogenous bone as graft in animals: a systematic review, International Journal of Oral and Maxillofacial Surgery, 41 (2012) 114-120.
  37. R. Manfro, M.J. Conz, G.T. Moura, F.A. Ponzoni, R.P. Santos, A.A. Gruber, Comparative, histological and histomorphometric analysis of three anorganic bovine xenogenous bone substitutes: Bio-Oss, Bone-Fill and Gen-Ox anorganic, Journal of Maxillofacial and Oral Surgery, 13 (2014) 464-470.
  38. Y. Gao, X. Deng, W. Lin, H. Zhong, Characterization and osteoblast-like cell compatibility of porous scaffolds: bovine hydroxyapatite and novel hydroxyapatite artificial bone, Journal of Materials Science: Materials in Medicine, 17 (2006) 815-823.
  39. M.P. Ramirez Fernandez, M.A. de Souza, F.J. Montoya, C.H.L. de Vasconcelos, SEM-EDX study of the degradation process of two xenograft materials used in sinus lift procedures, Materials, 10 (2017) 542.
  40. P. Habibovic, M. C. Kruyt, M. V. Juhl, S. Clyens, R. Martinetti, L. Dolcini, N. Theilgaard, C. A. van Blitterswijk, Comparative in vivo study of six hydroxyapatite-based bone graft substitutes, Journal of Orthopaedic Research, 26 (2008) 1363-1370.
  41. H.Y. Chang, W.H. Tuan, P.L. Lai, Biphasic ceramic bone graft with biphasic degradation rates, Materials Science and Engineering: C, 118 (2021) 111421.
  42. R.Z. LeGeros, Properties of osteoconductive biomaterials: calcium phosphates, Clinical Orthopaedics and Related Research, 395 (2002) 81-98.
  43. R. Detsch, U. Mayr, B. Ziegler, F. Moser, D. Hofmann, K. Schaefer, The resorption of nanocrystalline calcium phosphates by osteoclast-like cells, Acta Biomaterialia, 6 (2010) 3223-3233.
  44. A. Ogose, K. Hotta, H. Kawashima, T. Tokunaga, T. Endo, H. Umezu, H. Ito, Comparison of hydroxyapatite and beta tricalcium phosphate as bone substitutes after excision of bone tumors, Journal of Biomedical Materials Research Part B: Applied Biomaterials, 72 (2005) 94-101.
  45. J. Kim, S. Kim, I. Song, Biomimetic octacalcium phosphate bone has superior bone regeneration ability compared to xenogeneic or synthetic bone, Materials, 14 (2021) 5300.
  46. R.C. Lopes, R.S. Silva, G.R. Pereira, F.A. Almeida, Bone-bioglass graft-an alternative to improve the osseointegration, Processing and Application of Ceramics, 16 (2022) 230-236.
  47. Y. Ling, H.J. Wang, S.P. Zhang, Improved the biocompatibility of cancellous bone with compound physicochemical decellularization process, Regenerative Biomaterials, 7 (2020) 443-451.
  48. R.E. Unger, A. Sartoris, F. Boschetti, M. Steimberg, M.V. de Cilla, C. Colombo, M. Santin, In vivo biocompatibility investigation of an injectable calcium carbonate (vaterite) as a bone substitute including compositional analysis via SEM-EDX technology, International Journal of Molecular Sciences, 23 (2022) 1196.
  49. V.S. Komlev, E.V. Sergeeva, O.M. Barinov, Bioactivity and effect of bone formation for octacalcium phosphate ceramics, Octacalcium Phosphate Biomaterials, Woodhead Publishing (2020) 85-119.
  50. E. Oprita, G.D. Perlea, A.L. Antonov, In vitro behaviour of osteoblast cells seeded into a COL/β-TCP composite scaffold, Open Life Sciences, 3 (2008) 31-37.
  51. X. Zhang, H. Li, J. Liu, X. Zhu, Restoration of critical-sized defects in the rabbit mandible using autologous bone marrow stromal cells hybridized with nano-β-tricalcium phosphate/collagen scaffolds, Journal of Nanomaterials, 2013 (2013) 913438.
  52. J.E. Mate-Sanchez de Val, F. Monje, J.M.C. Sola-Ruiz, A. Balara, F.G. Giner-Tarrida, Comparison of three hydroxyapatite/β-tricalcium phosphate/collagen ceramic scaffolds: an in vivo study, Journal of Biomedical Materials Research Part A, 102 (2014) 1037-1046.
  53. M. Ebrahimi, M. Kazemzadeh-Narbat, S. Paul, K. Roy, R. Ghavami, H. Zhang, A.S. Khademhosseini, Fabrication and characterization of novel nano hydroxyapatite/β-tricalcium phosphate scaffolds in three different composition ratios, Journal of Biomedical Materials Research Part A, 100 (2012) 2260-2268.
  54. G. Jain, D. Blaauw, S. Chang, A comparative study of two bone graft substitutes-InterOss® Collagen and OCS-B Collagen®, Journal of Functional Biomaterials, 13 (2022) 28.
  55. E. Solheim, Growth factors in bone, International Orthopaedics, 22 (1998) 410-416.
  56. I. E. Bialy, W. Jiskoot, M.R. Nejadnik, Formulation, delivery and stability of bone morphogenetic proteins for effective bone regeneration, Pharmaceutical Research, 34 (2017) 1152-1170.
  57. W. Wang, K.W.K. Yeung, Bone grafts and biomaterials substitutes for bone defect repair: a review, Bioactive Materials, 2 (2017) 224-247.
  58. M. Pfeiffenberger, J. Schroter, M. Liedert, F. Jakob, T. Bruckner, M. Amling, F. Jakob, Fracture healing research-shift towards in vitro modeling?, Biomedicines, 9 (2021) 748.
  59. K.L. Ong, K.K. Villarraga, J.P. Lau, C.L. Carreon, M. Kurtz, Off-label use of bone morphogenetic proteins in the United States using administrative data, Spine, 35 (2010) 1794-1800.
  60. V. Sreekumar, A. Kumar, M.J. Rosa, BMP9 a possible alternative drug for the recently withdrawn BMP7? New perspectives for (re-)implementation by personalized medicine, Archives of Toxicology, 91 (2017) 1353-1366.
  61. Y. Zhang, J. Li, S. Wang, B. Liu, Addition of a synthetically fabricated osteoinductive biphasic calcium phosphate bone graft to BMP2 improves new bone formation, Clinical Implant Dentistry and Related Research, 18 (2016) 1238-1247.
  62. M.A. Miranda, M.S. Moon, Treatment strategy for nonunions and malunions, Surgical Treatment of Orthopaedic Trauma, 1 (2007) 77-100.
  63. B. M. Wheatley, S. J. Yang, J. E. Urban, C. B. Hsu, J. C. Jacobs, J. E. Nerlich, Effect of NSAIDs on bone healing rates: a meta-analysis, JAAOS-Journal of the American Academy of Orthopaedic Surgeons, 27 (2019) e330-e336.
  64. L. C. Gerstenfeld, W. J. Sarada, J. V. Charles, M. P. Stephen, R. T. William, Impaired fracture healing in the absence of TNF-α signaling: the role of TNF-α in endochondral cartilage resorption, Journal of Bone and Mineral Research, 18 (2003) 1584-1592.
  65. S. Recknagel, A. Bindl, K. Kurz, D. Wehner, D. Ehrnthaller, R. J. Claes, M. R. Schuetz, Systemic inflammation induced by a thoracic trauma alters the cellular composition of the early fracture callus, Journal of Trauma and Acute Care Surgery, 74 (2013) 531-537.
  66. F. Batool, I. Struillou, F. Petit, B. Bugueno, P. Richard, C. Bruneau, Modulation of immune-inflammatory responses through surface modifications of biomaterials to promote bone healing and regeneration, Journal of Tissue Engineering, 12 (2021) 20417314211041428.
  67. G. Zhou, B. Zhu, F. Jing, Y. Qiu, Y. Weng, Reducing the inflammatory responses of biomaterials by surface modification with glycosaminoglycan multilayers, Journal of Biomedical Materials Research Part A, 104 (2016) 493-502.
  68. H. Al-Khoury, M. T. Geoghegan, J. T. El-Sayed, M. A. Desmond, T. K. Thomas, Anti-inflammatory surface coatings based on polyelectrolyte multilayers of heparin and polycationic nanoparticles of naproxen-bearing polymeric drugs, Biomacromolecules, 20 (2019) 4015-4025.
  69. T. Xu, K. Zhao, B. Cheng, Development of the biomaterials technology for the infection resistance, Current Pharmaceutical Design, 24 (2018) 886-895.
  70. C. Gao, Z. Feng, L. Zhao, Q. Chen, X. Qiu, Enhancement mechanisms of graphene in nano-58S bioactive glass scaffold: mechanical and biological performance, Scientific Reports, 4 (2014) 4712.
  71. S. Y. Park, J. Park, S. H. Sim, M. G. Sung, K. S. Kim, B. H. Hong, J. S. Nam, Enhanced differentiation of human neural stem cells into neurons on graphene, Advanced Materials, 23 (2011) H263.
  72. X. Shi, Y. Tian, Y. Wang, Z. Wang, Regulating cellular behavior on few-layer reduced graphene oxide films with well-controlled reduction states, Advanced Functional Materials, 22 (2012) 751-759.
  73. S. Kim, H. Kuang, A. Muller, L. Senyo, Graphene-biomineral hybrid materials, Advanced Materials, 23 (2011) 2009-2014.
  74. P. G. Coelho, J. T. Granjeiro, S. J. Larsson, H. O. Hayashi, Argon-based atmospheric pressure plasma enhances early bone response to rough titanium surfaces, Journal of Biomedical Materials Research Part A, 100 (2012) 1901-1906.
  75. K. Duske, S. Koban, J. F. Kindel, W. Schroder, N. Nebe, Atmospheric plasma enhances wettability and cell spreading on dental implant metals, Journal of Clinical Periodontology, 39 (2012) 400-407.
  76. B. D. Boyan, E. M. Lotz, Z. Schwartz, Roughness and hydrophilicity as osteogenic biomimetic surface properties, Tissue Engineering Part A, 23 (2017) 1479-1489.
  77. L. Canullo, F. Menini, G. Schwarz, M. Tobar, M. P. Heinemann, Effects of argon plasma treatment on the osteoconductivity of bone grafting materials, Clinical Oral Investigations, 24 (2020) 2611-2623.
  78. P. T. Vu, J. P. Conroy, A. M. Yousefi, The effect of argon plasma surface treatment on poly (lactic-co-glycolic acid)/collagen-based biomaterials for bone tissue engineering, Biomimetics, 7 (2022) 218.
  79. G. Daculsi, A. Passuti, J. Martin, J. L. Deudon, M. Legeros, A. Raher, Transformation of biphasic calcium phosphate ceramics invivo : ultrastructural and physicochemical characterization, Journal of Biomedical Materials Research, 23 (1989) 883-894.
  80. G. Daculsi, J. M. Bouler, A. LeGeros, M. A. LeGeros, B. Weiss, Formation of carbonate-apatite crystals after implantation of calcium phosphate ceramics, Calcified Tissue International, 46 (1990) 20-27.
  81. S. Bose, S. Roy, A. Bandyopadhyay, Understanding of dopant-induced osteogenesis and angiogenesis in calcium phosphate ceramics, Trends in Biotechnology, 31 (2013) 594-605.
  82. S. Minardi, G. Corradetti, S. Taraballi, A. P. Overby, G. V. Messina, R. Tasciotti, Evaluation of the osteoinductive potential of a bio-inspired scaffold mimicking the osteogenic niche for bone augmentation, Biomaterials, 62 (2015) 128-137.
  83. L. Stipniece, R. Salma-Ancane, M. Berzina-Cimdina, Strontium substituted hydroxyapatite promotes direct primary human osteoblast maturation, Ceramics International, 47 (2021) 3368-3379.
  84. Z. Geng, Y. Wang, Y. Zhang, J. Qi, Nanosized strontium substituted hydroxyapatite prepared from egg shell for enhanced biological properties, Journal of Biomaterials Applications, 32 (2018) 896-905.
  85. S. Chen, H. S. Guo, J. M. S. Lee, S. W. Tsai, Biomimetic synthesis of Mg-substituted hydroxyapatite nanocomposites and three-dimensional printing of composite scaffolds for bone regeneration, Journal of Biomedical Materials Research Part A, 107 (2019) 2512-2521.
  86. L. Bauer, G. Zlotnikov, J. A. Ziegelmeier, A. Muller, Bone-mimetic porous hydroxyapatite/whitlockite scaffolds: preparation, characterization and interactions with human mesenchymal stem cells, Journal of Materials Science, 56 (2021) 3947-3969.
  87. K. H. Park, Y. K. Jang, K. J. Jang, J. J. Kim, S. H. Lee, Zinc promotes osteoblast differentiation in human mesenchymal stem cells via activation of the cAMP-PKA-CREB signaling pathway, Stem Cells and Development, 27 (2018) 1125-1135.
  88. E. A. Ofudje, O. A. Akinbile, B. O. Olanrewaju, Synthesis and characterization of Zn-Doped hydroxyapatite: scaffold application, antibacterial and bioactivity studies, Heliyon, 5 (2019).
  89. K. Matsunaga, H. Murata, Formation energies of substitutional sodium and potassium in hydroxyapatite, Materials Transactions, 50 (2009) 1041-1045.
  90. Y. Sugiura, Y. Makita, Sodium induces octacalcium phosphate formation and enhances its layer structure by affecting the hydrous layer phosphate, Crystal Growth & Design, 18 (2018) 6165-6171.
  91. A. Fakharzadeh, F. Mohammadi, M. Rahimzadeh, K. Javad, Effect of dopant loading on the structural features of silver-doped hydroxyapatite obtained by mechanochemical method, Ceramics International, 43 (2017) 12588-12598.
  92. C. Shi, Y. L. Zhang, W. P. Xiao, G. Zhang, X. Y. Liu, Ultra-trace silver-doped hydroxyapatite with non-cytotoxicity and effective antibacterial activity, Materials Science and Engineering: C, 55 (2015) 497-505.
  93. M. Germaini, J. C. Orsola, G. H. Pineda, Osteoblast and osteoclast responses to A/B type carbonate-substituted hydroxyapatite ceramics for bone regeneration, Biomedical Materials, 12 (2017) 035008.
  94. T. Kasai, R. Sekine, K. Kawai, S. Okada, S. Mizuno, Bone tissue engineering using porous carbonate apatite and bone marrow cells, Journal of Craniofacial Surgery, 21 (2010) 473-478.
  95. S. Hesaraki, A. Sharifi, M. Zamanian, S. B. Salahshoor, Comparative study of mesenchymal stem cells osteogenic differentiation on low-temperature biomineralized nanocrystalline carbonated hydroxyapatite and sintered hydroxyapatite, Journal of Biomedical Materials Research Part B: Applied Biomaterials, 102 (2014) 108-118.
  96. K. Pajor, L. Pajchel, J. Kolmas, Hydroxyapatite and fluorapatite in conservative dentistry and oral implantology-a review, Materials, 12 (2019) 2683.
  97. V. Uskokovic, M. A. Iyer, V. M. Wu, One ion to rule them all: the combined antibacterial, osteoinductive and anticancer properties of selenite-incorporated hydroxyapatite, Journal of Materials Chemistry B, 5 (2017) 1430-1445.
  98. K.L. Pang, K.Y. Chin, Emerging anticancer potentials of selenium on osteosarcoma, International Journal of Molecular Sciences, 20 (2019) 5318.
  99. A. Ressler, Z. Manic, I. Lukic, B. Petrovic, V. Panic, M. Jovanovic, Ionic substituted hydroxyapatite for bone regeneration applications: A review, Open Ceramics, 6 (2021) 100122.
  100. H. S. Kim, S. G. Kumbar, S. P. Nukavarapu, Biomaterial-directed cell behavior for tissue engineering, Current Opinion in Biomedical Engineering, 17 (2021) 100260.
  101. C. J. Wilson, R. E. Clegg, M. T. Leavesley, M. J. Pearcy, Mediation of biomaterial-cell interactions by adsorbed proteins: a review, Tissue Engineering, 11 (2005) 1-18.
  102. B. Geiger, A. Bershadsky, R. Pankov, K. M. Yamada, Transmembrane crosstalk between the extracellular matrix and the cytoskeleton, Nature Reviews Molecular Cell Biology, 2 (2001) 793-805.
  103. T. J. Webster, R. W. Siegel, R. Bizios, Specific proteins mediate enhanced osteoblast adhesion on nanophase ceramics, Journal of Biomedical Materials Research, 51 (2000) 475-483.
  104. Y. Tian, B. Zhou, L. M. Park, C. F. Sun, Z. Wang, Surface energy-mediated fibronectin adsorption and osteoblast responses on nanostructured diamond, Journal of Materials Science & Technology, 35 (2019) 817-823.
  105. A. B. Faia-Torres, M. M. Charnley, D. Goren, R. G. Darga, G. M. Neff, Differential regulation of osteogenic differentiation of stem cells on surface roughness gradients, Biomaterials, 35 (2014) 9023-9032.
  106. M. M. Ouberai, K. Xu, M. E. Welland, Effect of the interplay between protein and surface on the properties of adsorbed protein layers, Biomaterials, 35 (2014) 6157-6163.
  107. R. M. Visalakshan, A. Pham, S. Jin, M. T. Clark, M. S. Ranganathan, A. L. Wood, Biomaterial surface hydrophobicity-mediated serum protein adsorption and immune responses, ACS Applied Materials & Interfaces, 11 (2019) 27615-27623.
  108. K. M. Hotchkiss, N. M. Clark, R. Olivares-Navarrete, Macrophage response to hydrophilic biomaterials regulates MSC recruitment and T-helper cell populations, Biomaterials, 182 (2018) 202-215.
  109. P. Cernochova, D. Tomankova, T. Hradilova, A. Nebesarova, R. Peterkova, A. Martynkova, Cell type specific adhesion to surfaces functionalised by amine plasma polymers, Scientific Reports, 10 (2020) 1-14.
  110. S. Guo, K. Liang, S. Hong, Tailoring polyelectrolyte architecture to promote cell growth and inhibit bacterial adhesion, ACS Applied Materials & Interfaces, 10 (2018) 7882-7891.
  111. E. Mariani, A. Lisignoli, R. Borzi, B. Pulsatelli, Biomaterials: foreign bodies or tuners for the immune response?, International Journal of Molecular Sciences, 20 (2019) 636.
  112. J. N. Barbosa, A. C. Martins, R. F. Gadelha, The influence of functional groups of self-assembled monolayers on fibrous capsule formation and cell recruitment, Journal of Biomedical Materials Research Part A, 76 (2006) 737-743.
  113. S. Kamath, H. Bhushan, A. Chakrabarti, S. R. Murthy, S. Basu, Surface chemistry influences implant-mediated host tissue responses, Journal of Biomedical Materials Research Part A, 86 (2008) 617-626.
  114. L. R. Jaidev, K. Chatterjee, Surface functionalization of 3D printed polymer scaffolds to augment stem cell response, Materials & Design, 161 (2019) 44-54.
  115. I. Beitlitum, H. Magdassi, T. George, E. Gazit, A. T. Hoffman, A novel micro-CT analysis for evaluating the regenerative potential of bone augmentation xenografts in rabbit calvarias, Scientific Reports, 14 (2024) 4321.
  116. S. J. Schambach, J. H. Bag, J. C. Lutz, M. Stark, C. G. Persing, Application of micro-CT in small animal imaging, Methods, 50 (2010) 2-13.
  117. H. M. Jo, D. J. Kim, H. T. Seo, Application of modified porcine xenograft by collagen coating in the veterinary field: pre-clinical and clinical evaluations, Frontiers in Veterinary Science, 11 (2024) 1373099.
  118. M. M. Figueiredo, J. A. F. Gamelas, A. G. Martins, Characterization of bone and bone-based graft materials using FTIR spectroscopy, Infrared Spectroscopy-Life and Biomedical Sciences, (2012) 315-338.
  119. H. Liu, C. Wei, X. Wu, An in vitro evaluation of the Ca/P ratio for the cytocompatibility of nano-to-micron particulate calcium phosphates for bone regeneration, Acta Biomaterialia, 4 (2008) 1472-1479.
  120. K.F. Tseng, H.L. Huang, W.J. Lin, H.Y. Chang, W.S. Lin, H.Y. Chen, Osseointegration potential assessment of bone graft materials loaded with mesenchymal stem cells in peri-implant bone defects, International Journal of Molecular Sciences, 25 (2024) 862.
  121. I. Beitlitum, H. Magdassi, T. George, E. Gazit, A. T. Hoffman, A novel micro-CT analysis for evaluating the regenerative potential of bone augmentation xenografts in rabbit calvarias, Scientific Reports, 14 (2024) 4321.
  122. Y. K. Lee, J. H. Choi, K. W. Park, H. Y. Cho, Micro-CT and histomorphometric study of bone regeneration effect with autogenous tooth biomaterial enriched with platelet-rich fibrin in an animal model, Scanning, 2021 (2021) 6656791.
  123. E. Mazzoni, P. Muraro, A. Coviello, F. Mastracci, D. M. Baldini, Enhanced osteogenic differentiation of human bone marrow-derived mesenchymal stem cells by a hybrid hydroxylapatite/collagen scaffold, Frontiers in Cell and Developmental Biology, 8 (2021) 610570.
  124. A. A. Vu, B. J. Clark, S. J. Kennedy, Effects of surface area and topography on 3D printed tricalcium phosphate scaffolds for bone grafting applications, Additive Manufacturing, 39 (2021) 101870.
  125. D. Boyd, J. R. Li, S. H. Thomas, Analysis of γ-irradiated synthetic bone grafts by 29Si MAS-NMR spectroscopy, calorimetry and XRD, Journal of Non-Crystalline Solids, 355 (2009) 2285-2288.
  126. B. H. Gowda, K. Srikari, K. Ravishankar, Assessment of inorg-anic and organic components in demineralized tooth graft material, AIP Conference Proceedings, 2274 (2020) 1-4.
  127. Z. Mladenovic, M. Maletic, T. Schlegel, U. Stern, B. Z. Markovic, Surface characterization of bone graft substitute materials conditioned in cell culture medium, Surface and Interface Analysis, 42 (2010) 452-456.
  128. K. Hong, Analysis of crystal structure of bone graft material using analyses of X-ray diffraction and scanning electron microscope image, Korean Academy of Preventive Dentistry, 15 (2019) 215-219.
  129. D. Bizari, K. G. Bogdanov, M. L. Almeida, Development of biphasic hydroxyapatite/dicalcium phosphate dihydrate (DCPD) bone graft using polyurethane foam template: in vitro and in vivo study, Advances in Applied Ceramics, 110 (2011) 417-425.
  130. J. Zhang, Z. X. Zhao, H. Huang, C. F. Liu, Improving osteogenesis of PLGA/HA porous scaffolds based on dual delivery of BMP-2 and IGF-1 via a polydopamine coating, RSC Advances, 7 (2017) 56732-56742.
  131. A. N. Koo, K. H. Kim, H. S. Lee, C. B. Park, Enhanced bone regeneration by porous poly (L-lactide) scaffolds with surface-immobilized nanohydroxyapatite, Macromolecular Research, 18 (2010) 1030-1036.
  132. P. Danilevicius, K. K. Kucuk, B. T. Uz, The effect of porosity on cell ingrowth in 3D laser-fabricated biodegradable scaffolds for bone regeneration, The European Conference on Lasers and Electro-Optics, Optica Publishing Group (2013).
  133. M. R. Shah, P. M. Patel, S. K. Bhatt, N. V. Patel, Estimation of drug absorption in antibiotic soaked bone grafts, Indian Journal of Orthopaedics, 50 (2016) 669-676.
  134. P. Mazon, A. Marquina, E. Martinez, R. Garcia, M. J. Esbrit, Enhancing bone tissue regeneration with rGO-coated Si-Ca-P bioceramic scaffold, Boletin de la Sociedad Espanola de Ceramica y Vidrio, 63 (2024) 59-71.
  135. S. Bottcher, B. Ganss, H. Neuhoff, T. Kaltenbach, An HPLC assay and a microbiological assay to determine levofloxacin in soft tissue, bone, bile and serum, Journal of Pharmaceutical and Biomedical Analysis, 25 (2001) 197-203.
  136. E. Verne, M. Bonini, G. Trossarelli, A. Piovani, Early stage reactivity and in vitro behavior of silica-based bioactive glasses and glass-ceramics, Journal of Materials Science: Materials in Medicine, 20 (2009) 75-86.