Bone grafts: which is the ideal biomaterial?

Bovine xenograft materials, followed by synthetic biomaterials, which unfortunately still lack documented predictability and clinical performance, dominate the market for the cranio-maxillofacial area. In Europe, new stringent regulations are expected to further limit the allograft market in the future. AIM Within this narrative review, we discuss possible future biomaterials for bone replacement. SCIENTIFIC RATIONALE FOR STUDY Although the bone graft (BG) literature is overflooded, only a handful of new BG substitutes are clinically available. Laboratory studies tend to focus on advanced production methods and novel biomaterial features, which can be costly to produce. PRACTICAL IMPLICATIONS In this review, we ask why such a limited number of BGs are clinically available when compared to extensive laboratory studies. We also discuss what features are needed for an ideal BG. RESULTS We have identified the key properties of current bone substitutes and have provided important information to guide clinical decision-making and generate new perspectives on bone substitutes. Our results indicated that different mechanical and biological properties are needed despite each having a broad spectrum of variations. CONCLUSIONS We foresee bone replacement composite materials with higher levels of bioactivity, providing an appropriate balance between bioabsorption and volume maintenance for achieving ideal bone remodelling.

[1]  J. Vahle,et al.  Skeletal Changes in Rats Given Daily Subcutaneous Injections of Recombinant Human Parathyroid Hormone (1-34) for 2 Years and Relevance to Human Safety , 2002, Toxicologic pathology.

[2]  T. Damron,et al.  Ultraporous β-tricalcium phosphate alone or combined with bone marrow aspirate for benign cavitary lesions: comparison in a prospective randomized clinical trial. , 2013, The Journal of bone and joint surgery. American volume.

[3]  Danielle S W Benoit,et al.  Controlled and sustained delivery of siRNA/NPs from hydrogels expedites bone fracture healing. , 2017, Biomaterials.

[4]  W. Grayson,et al.  Stromal cells and stem cells in clinical bone regeneration , 2015, Nature Reviews Endocrinology.

[5]  N. Mardas,et al.  Radiographic alveolar bone changes following ridge preservation with two different biomaterials. , 2011, Clinical oral implants research.

[6]  Dietmar W. Hutmacher,et al.  Design and Fabrication of Tubular Scaffolds via Direct Writing in a Melt Electrospinning Mode , 2012, Biointerphases.

[7]  G. Georgiou,et al.  Glass reinforced hydroxyapatite for hard tissue surgery--part 1: Mechanical properties. , 2001, Biomaterials.

[8]  Aldo R Boccaccini,et al.  Regenerating bone with bioactive glass scaffolds: A review of in vivo studies in bone defect models. , 2017, Acta biomaterialia.

[9]  J. Jansen,et al.  Synthesis and application of nanostructured calcium phosphate ceramics for bone regeneration. , 2012, Journal of biomedical materials research. Part B, Applied biomaterials.

[10]  C. Deng,et al.  TGF-β and BMP Signaling in Osteoblast Differentiation and Bone Formation , 2012, International journal of biological sciences.

[11]  Rami Mosheiff,et al.  Tissue engineering approaches for bone repair: concepts and evidence. , 2011, Injury.

[12]  Ahmed K. Emara,et al.  Recent biological trends in management of fracture non-union. , 2015, World journal of orthopedics.

[13]  D. Kaplan,et al.  Porosity of 3D biomaterial scaffolds and osteogenesis. , 2005, Biomaterials.

[14]  David F. Williams On the mechanisms of biocompatibility. , 2008, Biomaterials.

[15]  J. Lindhe,et al.  Effect of a xenograft on early bone formation in extraction sockets: an experimental study in dog. , 2009, Clinical oral implants research.

[16]  V. Goldberg,et al.  The biology of bone grafts. , 1993, Seminars in arthroplasty.

[17]  D. Lorich,et al.  SYMPOSIUM: TRIBUTE TO DR. MARSHALL URIST: MUSCULOSKELETAL GROWTH FACTORS Complications of Recombinant Human BMP-2 for Treating Complex Tibial Plateau Fractures , 2009 .

[18]  H. Nowzari,et al.  Risk of prion disease transmission through bovine-derived bone substitutes: a systematic review. , 2013, Clinical implant dentistry and related research.

[19]  Fergal J O'Brien,et al.  The effect of mean pore size on cell attachment, proliferation and migration in collagen-glycosaminoglycan scaffolds for bone tissue engineering. , 2010, Biomaterials.

[20]  Amit Bandyopadhyay,et al.  Recent advances in bone tissue engineering scaffolds. , 2012, Trends in biotechnology.

[21]  H. Egusa,et al.  Current bone substitutes for implant dentistry. , 2017, Journal of prosthodontic research.

[22]  J. Chevalier,et al.  Crack growth resistance of alumina, zirconia and zirconia toughened alumina ceramics for joint prostheses. , 2002, Biomaterials.

[23]  F. Benazzo,et al.  Biodegradable Scaffolds for Bone Regeneration Combined with Drug-Delivery Systems in Osteomyelitis Therapy , 2017, Pharmaceuticals.

[24]  Cato T Laurencin,et al.  Bone tissue engineering: recent advances and challenges. , 2012, Critical reviews in biomedical engineering.

[25]  O. Barbier,et al.  Bone allografts: What they can offer and what they cannot. , 2007, The Journal of bone and joint surgery. British volume.

[26]  Lei Zhang,et al.  Progress of Calcium Sulfate and Inorganic Composites for Bone Defect Repair: Progress of Calcium Sulfate and Inorganic Composites for Bone Defect Repair , 2013 .

[27]  Julian R Jones,et al.  Optimising bioactive glass scaffolds for bone tissue engineering. , 2006, Biomaterials.

[28]  G. Logroscino,et al.  Bone substitutes in orthopaedic surgery: from basic science to clinical practice , 2014, Journal of Materials Science: Materials in Medicine.

[29]  H. Pape,et al.  Tissue Engineering von Knochengewebe , 2009, Der Unfallchirurg.

[30]  A. Rosenbaum,et al.  Bone grafts, bone substitutes and orthobiologics , 2012, Organogenesis.

[31]  J. Reseland,et al.  Proline-Rich Peptide Mimics Effects of Enamel Matrix Derivative on Rat Oral Mucosa Incisional Wound Healing. , 2015, Journal of periodontology.

[32]  W. Mackenzie,et al.  Development of Bone Targeting Drugs , 2017, International journal of molecular sciences.

[33]  Jason A Inzana,et al.  3D printing of composite calcium phosphate and collagen scaffolds for bone regeneration. , 2014, Biomaterials.

[34]  T. Damron,et al.  Use of 3D β-tricalcium phosphate (Vitoss®) scaffolds in repairing bone defects , 2007 .

[35]  R Sinha,et al.  Vitoss Synthetic Cancellous Bone (Void Filler). , 2009, Medical journal, Armed Forces India.

[36]  P. Giannoudis,et al.  What should be the characteristics of the ideal bone graft substitute? , 2011, Injury.

[37]  B. Pippenger,et al.  Osteoinductive potential of 4 commonly employed bone grafts , 2016, Clinical Oral Investigations.

[38]  S. Taschieri,et al.  Histomorphometric outcomes after lateral sinus floor elevation procedure: a systematic review of the literature and meta-analysis. , 2016, Clinical oral implants research.

[39]  Manish K Jaiswal,et al.  Bioactive nanoengineered hydrogels for bone tissue engineering: a growth-factor-free approach. , 2015, ACS nano.

[40]  M. G. Cusella De Angelis,et al.  Emerging Perspectives in Scaffold for Tissue Engineering in Oral Surgery , 2017, Stem cells international.

[41]  B. Schmidt-Rohlfing,et al.  [Tissue engineering of bone tissue. Principles and clinical applications]. , 2009, Der Unfallchirurg.

[42]  T. Barth,et al.  Retrospective analysis of 10,000 implants from insertion up to 20 years—analysis of implantations using augmentative procedures , 2016, International Journal of Implant Dentistry.

[43]  E. Marcantonio,et al.  Comparison of biomaterial implants in the dental socket: histological analysis in dogs. , 2010, Clinical implant dentistry and related research.

[44]  G. Hannink,et al.  Injectable bone-graft substitutes: current products, their characteristics and indications, and new developments. , 2011, Injury.

[45]  J. Wohlfahrt,et al.  Bone formation in TiO2 bone scaffolds in extraction sockets of minipigs. , 2012, Acta biomaterialia.

[46]  J. Vacanti,et al.  Tissue engineering: a 21st century solution to surgical reconstruction. , 2001, The Annals of thoracic surgery.

[47]  N. Epstein,et al.  Complications due to the use of BMP/INFUSE in spine surgery: The evidence continues to mount , 2013, Surgical neurology international.

[48]  M. Bohner,et al.  Resorbable biomaterials as bone graft substitutes , 2010 .

[49]  C. Stefanini,et al.  Bovine bone matrix/poly(l-lactic-co-ε-caprolactone)/gelatin hybrid scaffold (SmartBone®) for maxillary sinus augmentation: A histologic study on bone regeneration. , 2017, International journal of pharmaceutics.

[50]  N. Mardas,et al.  Radiographic and clinical outcomes of implants placed in ridge preserved sites: a 12-month post-loading follow-up. , 2013, Clinical oral implants research.

[51]  D. Benoit,et al.  Agonism of Wnt–β‐catenin signalling promotes mesenchymal stem cell (MSC) expansion , 2015, Journal of tissue engineering and regenerative medicine.

[52]  C. Finkemeier,et al.  Bone-grafting and bone-graft substitutes. , 2002, The Journal of bone and joint surgery. American volume.

[53]  J. Reseland,et al.  Enhanced Osteoblast Differentiation on Scaffolds Coated with TiO2 Compared to SiO2 and CaP Coatings , 2012, Biointerphases.

[54]  A. Boccaccini,et al.  TiO2 foams with poly-(d,l-lactic acid) (PDLLA) and PDLLA/Bioglass® coatings for bone tissue engineering scaffolds , 2009 .

[55]  M Pei,et al.  A review of decellularized stem cell matrix: a novel cell expansion system for cartilage tissue engineering. , 2011, European cells & materials.

[56]  T. Albert,et al.  Physical and monetary costs associated with autogenous bone graft harvesting. , 2003, American journal of orthopedics.

[57]  Elena García-Gareta,et al.  Osteoinduction of bone grafting materials for bone repair and regeneration. , 2015, Bone.

[58]  S. Matsuda,et al.  Inhibition of miR‐92a Enhances Fracture Healing via Promoting Angiogenesis in a Model of Stabilized Fracture in Young Mice , 2014, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[59]  Yang Guo Progress of Calcium Sulfate and Inorganic Composites for Bone Defect Repair , 2013 .

[60]  H. Haugen,et al.  Processing of highly porous TiO2 bone scaffolds with improved compressive strength , 2013 .

[61]  K. Anseth,et al.  Synthesis and characterization of a fluvastatin-releasing hydrogel delivery system to modulate hMSC differentiation and function for bone regeneration. , 2006, Biomaterials.

[62]  N. Mardas,et al.  Alveolar ridge preservation with guided bone regeneration and a synthetic bone substitute or a bovine-derived xenograft: a randomized, controlled clinical trial. , 2010, Clinical oral implants research.

[63]  Daniel A. Seigerman,et al.  The Clinical Use of Allografts, Demineralized Bone Matrices, Synthetic Bone Graft Substitutes and Osteoinductive Growth Factors: A Survey Study , 2005, HSS Journal.

[64]  G. Duda,et al.  A review of biomaterials in bone defect healing, remaining shortcomings and future opportunities for bone tissue engineering , 2018, Bone & joint research.

[65]  Francesco Baino,et al.  Bioceramics and Scaffolds: A Winning Combination for Tissue Engineering , 2015, Front. Bioeng. Biotechnol..

[66]  J. Pilitsis,et al.  Bone healing and spinal fusion. , 2002, Neurosurgical focus.

[67]  A. Khademhosseini,et al.  Bioactive Silicate Nanoplatelets for Osteogenic Differentiation of Human Mesenchymal Stem Cells , 2013, Advanced materials.

[68]  Murugan Ramalingam,et al.  Stem cell biology and tissue engineering in dental sciences , 2015 .

[69]  P. Moy,et al.  Which hard tissue augmentation techniques are the most successful in furnishing bony support for implant placement? , 2007, The International journal of oral & maxillofacial implants.

[70]  J. Elliott Calcium Phosphate Biominerals , 2002 .

[71]  Karin A. Hing,et al.  Bioceramic Bone Graft Substitutes: Influence of Porosity and Chemistry , 2005 .

[72]  D. Belisario,et al.  Adipose-Derived Stromal Vascular Fraction/Xenohybrid Bone Scaffold: An Alternative Source for Bone Regeneration , 2018, Stem cells international.

[73]  S. Jo,et al.  Histological Evaluation of the Healing Process of Various Bone Graft Materials after Engraftment into the Human Body , 2018, Materials.

[74]  S. Scarfì Use of bone morphogenetic proteins in mesenchymal stem cell stimulation of cartilage and bone repair. , 2016, World journal of stem cells.

[75]  W. Enneking,et al.  Allograft Bone Decreases in Strength In Vivo over Time , 2005, Clinical orthopaedics and related research.

[76]  M. Monjo,et al.  Porous ceramic titanium dioxide scaffolds promote bone formation in rabbit peri-implant cortical defect model. , 2013, Acta biomaterialia.

[77]  D. Hutmacher,et al.  Scaffolds in tissue engineering bone and cartilage. , 2000, Biomaterials.

[78]  Rik Huiskes,et al.  Effects of mechanical forces on maintenance and adaptation of form in trabecular bone , 2000, Nature.

[79]  M. Sanz,et al.  Effectiveness of Lateral Bone Augmentation on the Alveolar Crest Dimension , 2015, Journal of dental research.

[80]  J. Burdick,et al.  Influence of three-dimensional hyaluronic acid microenvironments on mesenchymal stem cell chondrogenesis. , 2009, Tissue engineering. Part A.

[81]  C. Scopa,et al.  Histological comparison of autograft, allograft-DBM, xenograft, and synthetic grafts in a trabecular bone defect: an experimental study in rabbits. , 2009, Medical science monitor : international medical journal of experimental and clinical research.

[82]  G. Muschler,et al.  Significance of the Porosity and Physical Chemistry of Calcium Phosphate Ceramics , 1988, Annals of the New York Academy of Sciences.

[83]  Antonios G Mikos,et al.  Review: mineralization of synthetic polymer scaffolds for bone tissue engineering. , 2007, Tissue engineering.

[84]  Joon B. Park Bioceramics: Properties, Characterizations, and Applications , 2008 .

[85]  P. Kasten,et al.  Porosity and pore size of beta-tricalcium phosphate scaffold can influence protein production and osteogenic differentiation of human mesenchymal stem cells: an in vitro and in vivo study. , 2008, Acta biomaterialia.

[86]  P. Dileo,et al.  What is the role of routine follow-up for localised limb soft tissue sarcomas? A retrospective analysis of 174 patients , 2014, British Journal of Cancer.

[87]  S. Gheduzzi,et al.  A comparison of the viscoelastic properties of bone grafts. , 2006, Clinical biomechanics.

[88]  M. Monjo,et al.  TiO 2 Scaffolds Sustain Differentiation of MC3T3-E1 Cells , 2012 .

[89]  M. Ebrahimzadeh,et al.  Current Concepts in Scaffolding for Bone Tissue Engineering. , 2018, The archives of bone and joint surgery.

[90]  G. Zimmermann,et al.  Allograft bone matrix versus synthetic bone graft substitutes. , 2011, Injury.

[91]  Jin-Ye Wang,et al.  Mechanical properties of artificial materials for bone repair , 2014 .

[92]  A. L. Oliveira,et al.  Sodium silicate gel as a precursor for the in vitro nucleation and growth of a bone-like apatite coating in compact and porous polymeric structures. , 2003, Biomaterials.

[93]  Aldo R Boccaccini,et al.  45S5 Bioglass-derived glass-ceramic scaffolds for bone tissue engineering. , 2006, Biomaterials.

[94]  J. Reseland,et al.  Impact of trace elements on biocompatibility of titanium scaffolds , 2010, Biomedical materials.

[95]  S. Bose,et al.  Calcium phosphate ceramic systems in growth factor and drug delivery for bone tissue engineering: a review. , 2012, Acta biomaterialia.

[96]  M. Santoro,et al.  Polymeric scaffolds as stem cell carriers in bone repair , 2015, Journal of tissue engineering and regenerative medicine.

[97]  G. Hannink,et al.  Bioresorbability, porosity and mechanical strength of bone substitutes: what is optimal for bone regeneration? , 2011, Injury.

[98]  A. Tencer,et al.  Significance of the Porosity and Physical Chemistry of Calcium Phosphate Ceramics , 1988, Annals of the New York Academy of Sciences.

[99]  G. Perale,et al.  Composite polymer-coated mineral grafts for bone regeneration: material characterisation and model study , 2014 .

[100]  Ralph Müller,et al.  In vivo behavior of calcium phosphate scaffolds with four different pore sizes. , 2006, Biomaterials.

[101]  Qingshan Chen,et al.  Cross-linking Characteristics and Mechanical Properties of an Injectable Biomaterial Composed of Polypropylene Fumarate and Polycaprolactone Co-polymer , 2011, Journal of biomaterials science. Polymer edition.

[102]  B. Baroli From natural bone grafts to tissue engineering therapeutics: Brainstorming on pharmaceutical formulative requirements and challenges. , 2009, Journal of pharmaceutical sciences.

[103]  Gianaurelio Cuniberti,et al.  Three-dimensional printing of hierarchical and tough mesoporous bioactive glass scaffolds with a controllable pore architecture, excellent mechanical strength and mineralization ability. , 2011, Acta biomaterialia.

[104]  Sophia P Pilipchuk,et al.  Tissue engineering for bone regeneration and osseointegration in the oral cavity. , 2015, Dental materials : official publication of the Academy of Dental Materials.

[105]  M. Sanz,et al.  Simultaneous lateral bone augmentation and implant placement using a particulated synthetic bone substitute around chronic peri‐implant dehiscence defects in dogs , 2017, Journal of clinical periodontology.

[106]  A. Musset,et al.  Bone substitutes: a review of their characteristics, clinical use, and perspectives for large bone defects management , 2018, Journal of tissue engineering.

[107]  M. Monjo,et al.  Effect of TiO2 scaffolds coated with alginate hydrogel containing a proline-rich peptide on osteoblast growth and differentiation in vitro. , 2013, Journal of biomedical materials research. Part A.

[108]  J. Jansen,et al.  In vivo degradation of porous poly(propylene fumarate)/poly(DL-lactic-co-glycolic acid) composite scaffolds. , 2005, Biomaterials.

[109]  G. Benic,et al.  Guided bone regeneration with particulate vs. block xenogenic bone substitutes: a pilot cone beam computed tomographic investigation , 2017, Clinical oral implants research.

[110]  C. Laurencin,et al.  The role of small molecules in musculoskeletal regeneration. , 2012, Regenerative medicine.

[111]  Jian Li,et al.  Mechanical and Biological Properties of Hydroxyapatite/tricalcium Phosphate Scaffolds Coated with Poly(lactic-co-glycolic Acid) , 2007 .

[112]  H. S. Azevedo,et al.  Natural origin biodegradable systems in tissue engineering and regenerative medicine: present status and some moving trends , 2007, Journal of The Royal Society Interface.

[113]  M. Bengisu Borate glasses for scientific and industrial applications: a review , 2016, Journal of Materials Science.

[114]  N. A. Abu Osman,et al.  Polycaprolactone/starch composite: Fabrication, structure, properties, and applications. , 2015, Journal of biomedical materials research. Part A.

[115]  Ung-Jin Kim,et al.  In vitro cartilage tissue engineering with 3D porous aqueous-derived silk scaffolds and mesenchymal stem cells. , 2005, Biomaterials.

[116]  N. Ebraheim,et al.  Bone‐Graft Harvesting From Iliac and Fibular Donor Sites: Techniques and Complications , 2001, The Journal of the American Academy of Orthopaedic Surgeons.

[117]  M. Kawanami,et al.  Periodontal repair following implantation of beta-tricalcium phosphate with different pore structures in Class III furcation defects in dogs. , 2012, Dental materials journal.

[118]  Amit Bandyopadhyay,et al.  Effects of silica and zinc oxide doping on mechanical and biological properties of 3D printed tricalcium phosphate tissue engineering scaffolds. , 2012, Dental materials : official publication of the Academy of Dental Materials.

[119]  G. Perinetti,et al.  New bone formation after transcrestal sinus floor elevation was influenced by sinus cavity dimensions: A prospective histologic and histomorphometric study , 2018, Clinical oral implants research.

[120]  P. Layrolle,et al.  Impact of biomaterial microtopography on bone regeneration: comparison of three hydroxyapatites , 2017, Clinical oral implants research.