3D-Printed Scaffolds and Biomaterials: Review of Alveolar Bone Augmentation and Periodontal Regeneration Applications

To ensure a successful dental implant therapy, the presence of adequate vertical and horizontal alveolar bone is fundamental. However, an insufficient amount of alveolar ridge in both dimensions is often encountered in dental practice due to the consequences of oral diseases and tooth loss. Although postextraction socket preservation has been adopted to lessen the need for such invasive approaches, it utilizes bone grafting materials, which have limitations that could negatively affect the quality of bone formation. To overcome the drawbacks of routinely employed grafting materials, bone graft substitutes such as 3D scaffolds have been recently investigated in the dental field. In this review, we highlight different biomaterials suitable for 3D scaffold fabrication, with a focus on “3D-printed” ones as bone graft substitutes that might be convenient for various applications related to implant therapy. We also briefly discuss their possible adoption for periodontal regeneration.

[1]  W. Lu,et al.  A biomimetic hierarchical scaffold: natural growth of nanotitanates on three-dimensional microporous Ti-based metals. , 2008, Nano letters.

[2]  Jiang Chang,et al.  Fabrication and characterization of bioactive wollastonite/PHBV composite scaffolds. , 2004, Biomaterials.

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

[4]  S. Teoh,et al.  Novel 3D polycaprolactone scaffold for ridge preservation--a pilot randomised controlled clinical trial. , 2015, Clinical oral implants research.

[5]  D. Hutmacher,et al.  Multiphasic Scaffolds for Periodontal Tissue Engineering , 2014, Journal of dental research.

[6]  Huaping Tan,et al.  Alginate-Based Biomaterials for Regenerative Medicine Applications , 2013, Materials.

[7]  M. Longaker,et al.  Biomaterials for Craniofacial Bone Engineering , 2014, Journal of dental research.

[8]  P. Berardinelli,et al.  In Vivo Behavior of a Custom-Made 3D Synthetic Bone Substitute in Sinus Augmentation Procedures in Sheep. , 2015, The Journal of oral implantology.

[9]  Wenhai Huang,et al.  Kinetics and mechanisms of the conversion of silicate (45S5), borate, and borosilicate glasses to hydroxyapatite in dilute phosphate solutions , 2006, Journal of materials science. Materials in medicine.

[10]  L. Cheung,et al.  Biodegradable polycaprolactone-chitosan three-dimensional scaffolds fabricated by melt stretching and multilayer deposition for bone tissue engineering: assessment of the physical properties and cellular response , 2011, Biomedical materials.

[11]  I. A. Jones,et al.  Craniofacial osteoblast responses to polycaprolactone produced using a novel boron polymerisation technique and potassium fluoride post-treatment. , 2003, Biomaterials.

[12]  S. Bryant,et al.  Cell encapsulation in biodegradable hydrogels for tissue engineering applications. , 2008, Tissue engineering. Part B, Reviews.

[13]  Ke Yang,et al.  Formation by ion plating of Ti-coating on pure Mg for biomedical applications , 2005 .

[14]  S. Hofmann,et al.  Initial cell pre-cultivation can maximize ECM mineralization by human mesenchymal stem cells on silk fibroin scaffolds. , 2011, Acta biomaterialia.

[15]  Antonios G Mikos,et al.  Biomimetic materials for tissue engineering. , 2003, Biomaterials.

[16]  T. Arinzeh,et al.  Biphasic Calcium Phosphate Ceramics for Bone Regeneration and Tissue Engineering Applications , 2010, Materials.

[17]  J. Fisher,et al.  Functional Tissue Engineering of Bone: Signals and Scaffolds , 2003 .

[18]  C. Laurencin,et al.  Biodegradable polymers as biomaterials , 2007 .

[19]  G. Thouas,et al.  Progress and challenges in biomaterials used for bone tissue engineering: bioactive glasses and elastomeric composites , 2012, Progress in Biomaterials.

[20]  C. Laurencin,et al.  Cellulose and collagen derived micro-nano structured scaffolds for bone tissue engineering. , 2013, Journal of biomedical nanotechnology.

[21]  Larry L. Hench,et al.  Bioceramics: From Concept to Clinic , 1991 .

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

[23]  I. Vroman,et al.  Biodegradable Polymers , 2009, Materials.

[24]  B. Griffith,et al.  Application of Materials in Medicine, Biology, and Artificial Organs , 1996 .

[25]  Horst Kessler,et al.  RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. , 2003, Biomaterials.

[26]  Miqin Zhang,et al.  Biphasic calcium phosphate nanocomposite porous scaffolds for load-bearing bone tissue engineering. , 2004, Biomaterials.

[27]  A. Piattelli,et al.  Custom-Made Computer-Aided-Design/Computer-Aided-Manufacturing Biphasic Calcium-Phosphate Scaffold for Augmentation of an Atrophic Mandibular Anterior Ridge , 2015, Case reports in dentistry.

[28]  C. G. Pitt Poly-ε-caprolactone and its copolymers , 1990 .

[29]  D. Kaigler,et al.  Bone repair cells for craniofacial regeneration. , 2012, Advanced drug delivery reviews.

[30]  Hsin-I Chang,et al.  Cell Responses to Surface and Architecture of Tissue Engineering Scaffolds , 2011 .

[31]  A. Göpferich,et al.  Why degradable polymers undergo surface erosion or bulk erosion. , 2002, Biomaterials.

[32]  C A van Blitterswijk,et al.  3D fiber-deposited scaffolds for tissue engineering: influence of pores geometry and architecture on dynamic mechanical properties. , 2006, Biomaterials.

[33]  A Haverich,et al.  Left main coronary artery fistula exiting into the right atrium , 2003, Heart.

[34]  Li Li,et al.  A review on biodegradable polymeric materials for bone tissue engineering applications , 2009 .

[35]  Ke Yang,et al.  In vivo evaluation of biodegradable magnesium alloy bone implant in the first 6 months implantation. , 2009, Journal of biomedical materials research. Part A.

[36]  Bo Mi Moon,et al.  3D silk fibroin scaffold incorporating titanium dioxide (TiO2) nanoparticle (NPs) for tissue engineering. , 2014, International journal of biological macromolecules.

[37]  H. Rios,et al.  Pre-augmentation soft tissue expansion: an overview. , 2016, Clinical oral implants research.

[38]  Suming Li,et al.  Hydrolytic degradation characteristics of aliphatic polyesters derived from lactic and glycolic acids. , 1999 .

[39]  R. Legeros,et al.  Properties of osteoconductive biomaterials: calcium phosphates. , 2002, Clinical orthopaedics and related research.

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

[41]  Masayuki Yamato,et al.  Application of periodontal ligament cell sheet for periodontal regeneration: a pilot study in beagle dogs. , 2005, Journal of periodontal research.

[42]  G. Romanos,et al.  Role of primary stability for successful osseointegration of dental implants: Factors of influence and evaluation. , 2013, Interventional medicine & applied science.

[43]  B. McAllister,et al.  Bone augmentation techniques. , 2007, Journal of periodontology.

[44]  D. Day,et al.  Mechanisms for converting bioactive silicate, borate, and borosilicate glasses to hydroxyapatite in dilute phosphate solution , 2006 .

[45]  N. Dewitt bone and cartilage , 2003, Nature.

[46]  Lorenzo Moroni,et al.  Combining technologies to create bioactive hybrid scaffolds for bone tissue engineering , 2013, Biomatter.

[47]  Colleen L Flanagan,et al.  Bone tissue engineering using polycaprolactone scaffolds fabricated via selective laser sintering. , 2005, Biomaterials.

[48]  Alexis M Pietak,et al.  Magnesium and its alloys as orthopedic biomaterials: a review. , 2006, Biomaterials.

[49]  D. Mooney,et al.  Hydrogels for tissue engineering. , 2001, Chemical Reviews.

[50]  C. Doillon,et al.  Denatured collagen as support for a FGF-2 delivery system: physicochemical characterizations and in vitro release kinetics and bioactivity. , 2004, Biomaterials.

[51]  V. Petrovic,et al.  Craniofacial bone tissue engineering. , 2012, Oral surgery, oral medicine, oral pathology and oral radiology.

[52]  Saso Ivanovski,et al.  Advanced tissue engineering scaffold design for regeneration of the complex hierarchical periodontal structure. , 2014, Journal of clinical periodontology.

[53]  Anselm Wiskott,et al.  A 3D printed TCP/HA structure as a new osteoconductive scaffold for vertical bone augmentation. , 2016, Clinical oral implants research.

[54]  Margam Chandrasekaran,et al.  Rapid prototyping in tissue engineering: challenges and potential. , 2004, Trends in biotechnology.

[55]  Larry L. Hench,et al.  The story of Bioglass® , 2006, Journal of materials science. Materials in medicine.

[56]  Daniel Torres-Lagares,et al.  Importance of Poly(lactic-co-glycolic acid) in Scaffolds for Guided Bone Regeneration: A Focused Review. , 2015, The Journal of oral implantology.

[57]  Wei Fan,et al.  A biphasic scaffold design combined with cell sheet technology for simultaneous regeneration of alveolar bone/periodontal ligament complex. , 2012, Biomaterials.

[58]  V. Guarino,et al.  Biomimetic Strategies for Bone Repair and Regeneration , 2012, Journal of functional biomaterials.

[59]  A. Göpferich,et al.  Mechanisms of polymer degradation and erosion. , 1996, Biomaterials.

[60]  Larry L. Hench,et al.  Bonding mechanisms at the interface of ceramic prosthetic materials , 1971 .

[61]  I. Aranaz,et al.  Functional Characterization of Chitin and Chitosan , 2009 .

[62]  Y. Seol,et al.  Spatiotemporally Controlled Microchannels of Periodontal Mimic Scaffolds , 2014, Journal of dental research.

[63]  H. Terheyden,et al.  Bone augmentation procedures in localized defects in the alveolar ridge: clinical results with different bone grafts and bone-substitute materials. , 2009, The International journal of oral & maxillofacial implants.

[64]  Magdi H. Yacoub,et al.  Hydrogel scaffolds for tissue engineering: Progress and challenges , 2013, Global cardiology science & practice.

[65]  S N Jayasinghe,et al.  In vitro assessment of the biological response to nano-sized hydroxyapatite , 2004, Journal of materials science. Materials in medicine.

[66]  F. Fontana,et al.  Clinical outcomes of vertical bone augmentation to enable dental implant placement: a systematic review. , 2008, Journal of clinical periodontology.

[67]  J. Zerwekh,et al.  Porous ceramics as bone graft substitutes in long bone defects: A biomechanical, histological, and radiographic analysis , 1996, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[68]  E. Díaz,et al.  In vitro degradation of Poly(caprolactone)/nHA composites , 2014 .

[69]  Miqin Zhang,et al.  Influence of processing parameters on pore structure of 3D porous chitosan-alginate polyelectrolyte complex scaffolds. , 2011, Journal of biomedical materials research. Part A.

[70]  G. Ciardelli,et al.  Bioartificial polymeric materials based on polysaccharides , 2001, Journal of biomaterials science. Polymer edition.

[71]  Hector F Rios,et al.  Biomimetic hybrid scaffolds for engineering human tooth-ligament interfaces. , 2010, Biomaterials.

[72]  P. Coulthard,et al.  Interventions for replacing missing teeth: horizontal and vertical bone augmentation techniques for dental implant treatment. , 2009, The Cochrane database of systematic reviews.

[73]  A. Piattelli,et al.  Vertical Ridge Augmentation of the Atrophic Posterior Mandible With Custom-Made, Computer-Aided Design/Computer-Aided Manufacturing Porous Hydroxyapatite Scaffolds , 2013, The Journal of craniofacial surgery.

[74]  Chengtie Wu,et al.  Bioactive Inorganic and Organic Composite Materials for Bone Regeneration and Gene Delivery , 2013 .

[75]  B. Luan,et al.  Protective coatings on magnesium and its alloys — a critical review , 2002 .

[76]  W. Thein-Han,et al.  Collagen-calcium phosphate cement scaffolds seeded with umbilical cord stem cells for bone tissue engineering. , 2011, Tissue engineering. Part A.

[77]  A. Boccaccini,et al.  Copper-releasing, boron-containing bioactive glass-based scaffolds coated with alginate for bone tissue engineering. , 2012, Acta biomaterialia.

[78]  F. O'Brien Biomaterials & scaffolds for tissue engineering , 2011 .

[79]  Amy J Wagoner Johnson,et al.  The mechanical properties and osteoconductivity of hydroxyapatite bone scaffolds with multi-scale porosity. , 2007, Biomaterials.

[80]  Changyou Gao,et al.  Surface modification of polycaprolactone with poly(methacrylic acid) and gelatin covalent immobilization for promoting its cytocompatibility. , 2002, Biomaterials.

[81]  Patrik Schmuki,et al.  Nanosize and vitality: TiO2 nanotube diameter directs cell fate. , 2007, Nano letters.

[82]  J. Arts,et al.  Bioactive and osteoinductive bone graft substitutes: definitions, facts and myths. , 2011, Injury.

[83]  S. Dong,et al.  Scaffolding biomaterials for cartilage regeneration , 2014 .

[84]  A. McGoron,et al.  Biodegradable Magnesium Alloys: A Review of Material Development and Applications , 2012, Journal of biomimetics, biomaterials, and tissue engineering.

[85]  Thomas J Webster,et al.  Increased osteoblast function on PLGA composites containing nanophase titania. , 2005, Journal of biomedical materials research. Part A.

[86]  Benjamin M Wu,et al.  Recent advances in 3D printing of biomaterials , 2015, Journal of Biological Engineering.

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

[88]  C. Sfeir,et al.  Magnesium ion stimulation of bone marrow stromal cells enhances osteogenic activity, simulating the effect of magnesium alloy degradation. , 2014, Acta biomaterialia.

[89]  Sophia P Pilipchuk,et al.  3D-printed Bioresorbable Scaffold for Periodontal Repair , 2015, Journal of dental research.

[90]  S. Hollister,et al.  Tissue engineering bone-ligament complexes using fiber-guiding scaffolds. , 2012, Biomaterials.

[91]  C Perka,et al.  Matrix-mixed culture: new methodology for chondrocyte culture and preparation of cartilage transplants. , 2000, Journal of biomedical materials research.

[92]  E. Nery,et al.  A Veterans Administration Cooperative Study of biphasic calcium phosphate ceramic in periodontal osseous defects. , 1990, Journal of periodontology.

[93]  F. Sbrana,et al.  Oriented collagen nanocoatings for tissue engineering. , 2014, Colloids and surfaces. B, Biointerfaces.

[94]  Lara Yildirimer,et al.  Three-dimensional biomaterial degradation - Material choice, design and extrinsic factor considerations. , 2014, Biotechnology advances.

[95]  Peter Fratzl,et al.  Tissue growth into three-dimensional composite scaffolds with controlled micro-features and nanotopographical surfaces. , 2013, Journal of biomedical materials research. Part A.

[96]  Yoshito Ikada,et al.  Challenges in tissue engineering , 2006, Journal of The Royal Society Interface.

[97]  G. Rasperini,et al.  Surgical Approaches Based on Biological Objectives: GTR versus GBR Techniques , 2013, International journal of dentistry.

[98]  Nan Ma,et al.  Laser printing of skin cells and human stem cells. , 2010, Tissue engineering. Part C, Methods.

[99]  C. Sfeir,et al.  Porous magnesium/PLGA composite scaffolds for enhanced bone regeneration following tooth extraction. , 2015, Acta biomaterialia.

[100]  Jeremy Mao,et al.  Bone tissue engineering and regeneration: from discovery to the clinic--an overview. , 2011, Tissue engineering. Part B, Reviews.

[101]  Huipin Yuan,et al.  BIOMATERIALS : CURRENT KNOWLEDGE OF PROPERTIES , EXPERIMENTAL MODELS AND BIOLOGICAL MECHANISMS , 2011 .

[102]  A. Mikos,et al.  Mini‐review: Islet transplantation to create a bioartificial pancreas , 1994, Biotechnology and bioengineering.

[103]  Chan Ho Park,et al.  Image-based, fiber guiding scaffolds: a platform for regenerating tissue interfaces. , 2014, Tissue engineering. Part C, Methods.

[104]  S. Hollister,et al.  Optimal design and fabrication of scaffolds to mimic tissue properties and satisfy biological constraints. , 2002, Biomaterials.

[105]  Jie Zhao,et al.  Amorphous calcium phosphate and its application in dentistry , 2011, Chemistry Central journal.

[106]  Y. Fung,et al.  Bone and Cartilage , 1993 .

[107]  Y. Kinoshita,et al.  Recent Developments of Functional Scaffolds for Craniomaxillofacial Bone Tissue Engineering Applications , 2013, TheScientificWorldJournal.

[108]  G. Williamson,et al.  ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY ORAL Radiology , 2014 .

[109]  C J Damien,et al.  Bone graft and bone graft substitutes: a review of current technology and applications. , 1991, Journal of applied biomaterials : an official journal of the Society for Biomaterials.

[110]  R. Kaushik,et al.  Poly-ϵ-caprolactone microspheres and nanospheres: an overview , 2004 .

[111]  C H Lee,et al.  Anatomically Shaped Tooth and Periodontal Regeneration by Cell Homing , 2010, Journal of dental research.

[112]  Stephanie J Bryant,et al.  Controlling the spatial distribution of ECM components in degradable PEG hydrogels for tissue engineering cartilage. , 2003, Journal of biomedical materials research. Part A.

[113]  Dietmar Werner Hutmacher,et al.  How smart do biomaterials need to be? A translational science and clinical point of view. , 2013, Advanced drug delivery reviews.

[114]  M. Esposito,et al.  A 3-year post-loading report of a randomised controlled trial on the rehabilitation of posterior atrophic mandibles: short implants or longer implants in vertically augmented bone? , 2011, European journal of oral implantology.

[115]  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.

[116]  G. Khang Evolution of gradient concept for the application of regenerative medicine , 2015 .

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

[118]  D. Wendt,et al.  Rapid prototyped porous nickel–titanium scaffolds as bone substitutes , 2014, Journal of tissue engineering.

[119]  N. Gadegaard,et al.  3D polymer scaffolds for tissue engineering. , 2006, Nanomedicine.

[120]  Yilin Cao,et al.  Comparative study of the use of poly(glycolic acid), calcium alginate and pluronics in the engineering of autologous porcine cartilage. , 1998, Journal of biomaterials science. Polymer edition.

[121]  D. Hutmacher,et al.  The return of a forgotten polymer : Polycaprolactone in the 21st century , 2009 .

[122]  Robert J. Kane,et al.  Hydroxyapatite reinforced collagen scaffolds with improved architecture and mechanical properties. , 2015, Acta biomaterialia.

[123]  J T Czernuszka,et al.  Collagen-hydroxyapatite composites for hard tissue repair. , 2006, European cells & materials.

[124]  D W Hutmacher,et al.  Three-Dimensional Bioprinting for Regenerative Dentistry and Craniofacial Tissue Engineering , 2015, Journal of dental research.

[125]  J. Ramirez-Vick,et al.  Scaffold design for bone regeneration. , 2014, Journal of nanoscience and nanotechnology.

[126]  Linda G Griffith,et al.  Engineering principles of clinical cell-based tissue engineering. , 2004, The Journal of bone and joint surgery. American volume.

[127]  T. Maekawa,et al.  POLYMERIC SCAFFOLDS IN TISSUE ENGINEERING APPLICATION: A REVIEW , 2011 .

[128]  J. Goddard,et al.  Polymer surface modification for the attachment of bioactive compounds , 2007 .

[129]  Hans Peter Wiesmann,et al.  Bone and Cartilage Engineering , 2006 .

[130]  Hyoun‐Ee Kim,et al.  Degradation and drug release of phosphate glass/polycaprolactone biological composites for hard-tissue regeneration. , 2005, Journal of biomedical materials research. Part B, Applied biomaterials.

[131]  P. Jeleń,et al.  Spectroscopic studies of electrophoretically deposited hybrid HAp/CNT coatings on titanium. , 2014, Spectrochimica acta. Part A, Molecular and biomolecular spectroscopy.

[132]  K. Jandt,et al.  Growth of osteoblast-like cells on biomimetic apatite-coated chitosan scaffolds. , 2008, Journal of biomedical materials research. Part B, Applied biomaterials.

[133]  L. Tan,et al.  The preparation, cytocompatibility, and in vitro biodegradation study of pure β-TCP on magnesium , 2009, Journal of materials science. Materials in medicine.

[134]  Peng Shang,et al.  Three-dimensional printed multiphase scaffolds for regeneration of periodontium complex. , 2014, Tissue engineering. Part A.

[135]  M. Lim,et al.  In vitro biological evaluation of electrospun Polycaprolactone/gelatine nanofibrous scaffold for tissue engineering , 2015 .

[136]  Nicola Maffulli,et al.  Bone regenerative medicine: classic options, novel strategies, and future directions , 2014, Journal of Orthopaedic Surgery and Research.

[137]  Gorka Orive,et al.  Cell microencapsulation technology: towards clinical application. , 2008, Journal of controlled release : official journal of the Controlled Release Society.

[138]  Tao Zhang,et al.  Nanomaterials and bone regeneration , 2015, Bone Research.

[139]  W. Kisaalita,et al.  Exploring cellular adhesion and differentiation in a micro‐/nano‐hybrid polymer scaffold , 2010, Biotechnology progress.

[140]  Mark A. Randolph,et al.  Tissue Engineered Neocartilage Using Plasma Derived Polymer Substrates and Chondrocytes , 1998, Plastic and reconstructive surgery.

[141]  Scott J Hollister,et al.  Effect of polycaprolactone scaffold permeability on bone regeneration in vivo. , 2011, Tissue engineering. Part A.

[142]  S. Teoh,et al.  The degradation profile of novel, bioresorbable PCL-TCP scaffolds: an in vitro and in vivo study. , 2008, Journal of biomedical materials research. Part A.

[143]  Hideo Nakajima,et al.  Metallic Scaffolds for Bone Regeneration , 2009, Materials.

[144]  A. Piattelli,et al.  Maxillary ridge augmentation with custom-made CAD/CAM scaffolds. A 1-year prospective study on 10 patients. , 2014, The Journal of oral implantology.