Applications of 3D printing on craniofacial bone repair: A systematic review.

OBJECTIVES Three-dimensional (3D) bioprinting, a method derived from additive manufacturing technology, is a recent and ongoing trend for the construction of 3D volumetric structures. The purpose of this systematic review is to summarize evidence from existing human and animal studies assessing the application of 3D printing on bone repair and regeneration in the craniofacial region. DATA & SOURCES A rigorous search of all relevant clinical trials and case series was performed, based on specific inclusion and exclusion criteria. The search was conducted in all available electronic databases and sources, supplemented by a manual search, in December 2017. STUDY SELECTION 43 articles (6 human and 37 animal studies) fulfilled the criteria. The human studies included totally 81 patients with craniofacial bone defects. Titanium or hydroxylapatite scaffolds were most commonly implanted. The follow-up period ranged between 6 and 24 months. Bone repair was reported successful in nearly every case, with minimal complications. Also, animal intervention studies used biomaterials and cells in various combination, offering insights into the techniques, through histological, biochemical, histomorphometric and microcomputed tomographic findings. The results in both humans and animals, though promising, are yet to be verified for clinical impact. CONCLUSIONS Future research should be focused on well-designed clinical trials to confirm the short- and long- term efficacy of 3D printing strategies for craniofacial bone repair. CLINICAL SIGNIFICANCE Emerging 3D printing technology opens a new era for tissue engineering. Humans and animals on application of 3D printing for craniofacial bone repair showed promising results which will lead clinicians to investigate more thoroughly alternative therapeutic methods for craniofacial bone defects.

[1]  Nils-Claudius Gellrich,et al.  Bone repair by cell-seeded 3D-bioplotted composite scaffolds made of collagen treated tricalciumphosphate or tricalciumphosphate-chitosan-collagen hydrogel or PLGA in ovine critical-sized calvarial defects. , 2010, Journal of biomedical materials research. Part B, Applied biomaterials.

[2]  E. D. Rekow,et al.  In vivo bone response to 3D periodic hydroxyapatite scaffolds assembled by direct ink writing. , 2007, Journal of biomedical materials research. Part A.

[3]  John L Ricci,et al.  Three-Dimensional Printing of Bone Repair and Replacement Materials: Impact on Craniofacial Surgery , 2012, The Journal of craniofacial surgery.

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

[5]  Anthony Atala,et al.  3D bioprinting of tissues and organs , 2014, Nature Biotechnology.

[6]  Zhijian Shen,et al.  Inorganic polymers: morphogenic inorganic biopolymers for rapid prototyping chain. , 2013, Progress in molecular and subcellular biology.

[7]  Joseph C Wenke,et al.  Effect of calcium phosphate coating and rhBMP-2 on bone regeneration in rabbit calvaria using poly(propylene fumarate) scaffolds. , 2015, Acta biomaterialia.

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

[9]  P. Alam ‘A’ , 2021, Composites Engineering: An A–Z Guide.

[10]  Wei Sun,et al.  Biopolymer deposition for freeform fabrication of hydrogel tissue constructs , 2007 .

[11]  C. V. van Blitterswijk,et al.  Porous Ti6Al4V scaffold directly fabricating by rapid prototyping: preparation and in vitro experiment. , 2006, Biomaterials.

[12]  Dong-Woo Cho,et al.  Development of a bone reconstruction technique using a solid free-form fabrication (SFF)-based drug releasing scaffold and adipose-derived stem cells. , 2013, Journal of biomedical materials research. Part A.

[13]  R. Maciel Filho,et al.  Improvement in Cranioplasty: Advanced Prosthesis Biomanufacturing☆ , 2016 .

[14]  Ibrahim T. Ozbolat,et al.  Current advances and future perspectives in extrusion-based bioprinting. , 2016, Biomaterials.

[15]  John L Ricci,et al.  Bone regeneration in critical bone defects using three-dimensionally printed β-tricalcium phosphate/hydroxyapatite scaffolds is enhanced by coating scaffolds with either dipyridamole or BMP-2. , 2017, Journal of biomedical materials research. Part B, Applied biomaterials.

[16]  Muhanad M Hatamleh,et al.  Simultaneous Computer-Aided Design/Computer-Aided Manufacture Bimaxillary Orthognathic Surgery and Mandibular Reconstruction Using Selective-Laser Sintered Titanium Implant. , 2016, The Journal of craniofacial surgery.

[17]  H. Lysdahl,et al.  Dental pulp-derived stromal cells exhibit a higher osteogenic potency than bone marrow-derived stromal cells in vitro and in a porcine critical-size bone defect model , 2016, SICOT-J.

[18]  C K Chua,et al.  Development of tissue scaffolds using selective laser sintering of polyvinyl alcohol/hydroxyapatite biocomposite for craniofacial and joint defects , 2004, Journal of materials science. Materials in medicine.

[19]  Eui Kyun Park,et al.  Effect of the biodegradation rate controlled by pore structures in magnesium phosphate ceramic scaffolds on bone tissue regeneration in vivo. , 2016, Acta biomaterialia.

[20]  Wei Zheng,et al.  Investigation of angiogenesis in bioactive 3-dimensional poly(d,l-lactide-co-glycolide)/nano-hydroxyapatite scaffolds by in vivo multiphoton microscopy in murine calvarial critical bone defect. , 2016, Acta biomaterialia.

[21]  S. Hollister Porous scaffold design for tissue engineering , 2005, Nature materials.

[22]  Minna Kellomäki,et al.  A review of rapid prototyping techniques for tissue engineering purposes , 2008, Annals of medicine.

[23]  B. Derby,et al.  Delivery of human fibroblast cells by piezoelectric drop-on-demand inkjet printing. , 2008, Biomaterials.

[24]  Miqin Zhang,et al.  Chitosan-alginate hybrid scaffolds for bone tissue engineering. , 2005, Biomaterials.

[25]  Lars Sennerby,et al.  A clinical and histologic evaluation of implant integration in the posterior maxilla after sinus floor augmentation with autogenous bone, bovine hydroxyapatite, or a 20:80 mixture. , 2002, The International journal of oral & maxillofacial implants.

[26]  S. Durual,et al.  Large Bone Vertical Augmentation Using a Three-Dimensional Printed TCP/HA Bone Graft: A Pilot Study in Dog Mandible. , 2016, Clinical implant dentistry and related research.

[27]  Jinming Wang,et al.  Evaluation of 3D-Printed Polycaprolactone Scaffolds Coated with Freeze-Dried Platelet-Rich Plasma for Bone Regeneration , 2017, Materials.

[28]  Su-Heon Woo,et al.  Cranioplasty Enhanced by Three-Dimensional Printing: Custom-Made Three-Dimensional-Printed Titanium Implants for Skull Defects , 2016, The Journal of craniofacial surgery.

[29]  J. Shim,et al.  Comparative Efficacies of Collagen-Based 3D Printed PCL/PLGA/β-TCP Composite Block Bone Grafts and Biphasic Calcium Phosphate Bone Substitute for Bone Regeneration , 2017, Materials.

[30]  P. Alam ‘L’ , 2021, Composites Engineering: An A–Z Guide.

[31]  I. Cuthill,et al.  Survey of the Quality of Experimental Design, Statistical Analysis and Reporting of Research Using Animals , 2009, PloS one.

[32]  Pierre Hardouin,et al.  Biomaterial challenges and approaches to stem cell use in bone reconstructive surgery. , 2004, Drug discovery today.

[33]  J. Hollinger,et al.  Evaluation of particulate Bioglass in a rabbit radius ostectomy model. , 1997, Journal of biomedical materials research.

[34]  S. Koka,et al.  [Osseointegrated dental implants]. , 1990, Les Cahiers de prothese.

[35]  J. Fisher,et al.  Tissue engineering solutions for cleft palates. , 2007, Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons.

[36]  E. D. Rekow,et al.  MicroCT analysis of hydroxyapatite bone repair scaffolds created via three-dimensional printing for evaluating the effects of scaffold architecture on bone ingrowth. , 2008, Journal of Biomedical Materials Research. Part A.

[37]  D W Hutmacher,et al.  [Calvarial reconstruction by customized bioactive implant]. , 2010, Handchirurgie, Mikrochirurgie, plastische Chirurgie : Organ der Deutschsprachigen Arbeitsgemeinschaft fur Handchirurgie : Organ der Deutschsprachigen Arbeitsgemeinschaft fur Mikrochirurgie der Peripheren Nerven und Gefasse : Organ der V....

[38]  H Oonishi,et al.  Orthopaedic applications of hydroxyapatite. , 1991, Biomaterials.

[39]  S. Takayama,et al.  Rapid generation of multiplexed cell cocultures using acoustic droplet ejection followed by aqueous two-phase exclusion patterning. , 2012, Tissue engineering. Part C, Methods.

[40]  M. D. Vlad,et al.  Design and properties of 3D scaffolds for bone tissue engineering. , 2016, Acta biomaterialia.

[41]  N. Lang,et al.  Healing at mandibular block-grafted sites. An experimental study in dogs. , 2015, Clinical oral implants research.

[42]  Jan Wolff,et al.  Application of Additive Manufacturing in Oral and Maxillofacial Surgery. , 2015, Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons.

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

[44]  M. Hernán,et al.  ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions , 2016, British Medical Journal.

[45]  Boon Chin Heng,et al.  Histological evaluation of osteogenesis of 3D-printed poly-lactic-co-glycolic acid (PLGA) scaffolds in a rabbit model , 2009, Biomedical materials.

[46]  M Nakamura,et al.  Biomatrices and biomaterials for future developments of bioprinting and biofabrication , 2010, Biofabrication.

[47]  Faleh Tamimi,et al.  Vertical bone augmentation with 3D-synthetic monetite blocks in the rabbit calvaria. , 2011, Journal of clinical periodontology.

[48]  H. Abukawa,et al.  Tissue-engineered bone with 3-dimensionally printed β-tricalcium phosphate and polycaprolactone scaffolds and early implantation: an in vivo pilot study in a porcine mandible model. , 2015, Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons.

[49]  I. Cuthill,et al.  Reporting : The ARRIVE Guidelines for Reporting Animal Research , 2010 .

[50]  S. Milz,et al.  Hydroxyapatite scaffolds for bone tissue engineering made by 3D printing , 2005, Journal of materials science. Materials in medicine.

[51]  I. Zein,et al.  Fused deposition modeling of novel scaffold architectures for tissue engineering applications. , 2002, Biomaterials.

[52]  Changqing Zhang,et al.  Three-dimensional printed strontium-containing mesoporous bioactive glass scaffolds for repairing rat critical-sized calvarial defects. , 2015, Acta biomaterialia.

[53]  M. Heiland,et al.  Selective laser-melted fully biodegradable scaffold composed of poly(d,l-lactide) and β-tricalcium phosphate with potential as a biodegradable implant for complex maxillofacial reconstruction: In vitro and in vivo results. , 2017, Journal of biomedical materials research. Part B, Applied biomaterials.

[54]  Faleh Tamimi,et al.  Craniofacial vertical bone augmentation: a comparison between 3D printed monolithic monetite blocks and autologous onlay grafts in the rabbit. , 2009, Biomaterials.

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

[56]  Faleh Tamimi,et al.  Osseointegration of dental implants in 3D-printed synthetic onlay grafts customized according to bone metabolic activity in recipient site. , 2014, Biomaterials.

[57]  L. Ciocca,et al.  Customized hybrid biomimetic hydroxyapatite scaffold for bone tissue regeneration. , 2017, Journal of biomedical materials research. Part B, Applied biomaterials.

[58]  Joachim Aigner,et al.  Alginate as a chondrocyte-delivery substance in combination with a non-woven scaffold for cartilage tissue engineering. , 2002, Biomaterials.

[59]  Lobat Tayebi,et al.  Three-Dimensional Bioprinting Materials with Potential Application in Preprosthetic Surgery. , 2016, Journal of prosthodontics : official journal of the American College of Prosthodontists.

[60]  Wei Sun,et al.  Effects of dispensing pressure and nozzle diameter on cell survival from solid freeform fabrication-based direct cell writing. , 2008, Tissue engineering. Part A.

[61]  Timothy J Horn,et al.  Overview of Current Additive Manufacturing Technologies and Selected Applications , 2012, Science progress.

[62]  P. Alam ‘W’ , 2021, Composites Engineering.

[63]  F. Hölzle,et al.  Bone tissue engineering using polyetherketoneketone scaffolds combined with autologous mesenchymal stem cells in a sheep calvarial defect model. , 2016, Journal of cranio-maxillo-facial surgery : official publication of the European Association for Cranio-Maxillo-Facial Surgery.

[64]  Yuki Kanno,et al.  Maxillofacial reconstruction using custom-made artificial bones fabricated by inkjet printing technology , 2009, Journal of Artificial Organs.

[65]  I. Smirnov,et al.  3D Printing of Octacalcium Phosphate Bone Substitutes , 2015, Front. Bioeng. Biotechnol..

[66]  Z. Gou,et al.  Custom Repair of Mandibular Bone Defects with 3D Printed Bioceramic Scaffolds , 2018, Journal of dental research.

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

[68]  Jianzhong Fu,et al.  Bone regeneration in 3D printing bioactive ceramic scaffolds with improved tissue/material interface pore architecture in thin-wall bone defect , 2017, Biofabrication.

[69]  Phil Campbell,et al.  Inkjet-based biopatterning of SDF-1β augments BMP-2-induced repair of critical size calvarial bone defects in mice. , 2014, Bone.

[70]  Joseph E Losee,et al.  Precise Control of Osteogenesis for Craniofacial Defect Repair: The Role of Direct Osteoprogenitor Contact in BMP-2-Based Bioprinting , 2012, Annals of plastic surgery.

[71]  L. Hench Bioceramics and the origin of life. , 1989, Journal of biomedical materials research.

[72]  Dong-Woo Cho,et al.  Ornamenting 3D printed scaffolds with cell-laid extracellular matrix for bone tissue regeneration. , 2015, Biomaterials.

[73]  Ana Civantos,et al.  Biological Properties of Solid Free Form Designed Ceramic Scaffolds with BMP-2: In Vitro and In Vivo Evaluation , 2012, PloS one.

[74]  Yijin Ren,et al.  Surgically facilitated experimental movement of teeth: systematic review. , 2015, The British journal of oral & maxillofacial surgery.

[75]  Ethan L Nyberg,et al.  3D-Printing Technologies for Craniofacial Rehabilitation, Reconstruction, and Regeneration , 2016, Annals of Biomedical Engineering.

[76]  T. Sohmura,et al.  Custom-made titanium devices as membranes for bone augmentation in implant treatment: Clinical application and the comparison with conventional titanium mesh. , 2015, Journal of cranio-maxillo-facial surgery : official publication of the European Association for Cranio-Maxillo-Facial Surgery.

[77]  Abhay S Pandit,et al.  Porous titanium scaffolds fabricated using a rapid prototyping and powder metallurgy technique. , 2008, Biomaterials.

[78]  Ali Khademhosseini,et al.  3D biofabrication strategies for tissue engineering and regenerative medicine. , 2014, Annual review of biomedical engineering.

[79]  Dong-Woo Cho,et al.  Efficacy of rhBMP-2 loaded PCL/PLGA/β-TCP guided bone regeneration membrane fabricated by 3D printing technology for reconstruction of calvaria defects in rabbit , 2014, Biomedical materials.

[80]  Dong-Woo Cho,et al.  Effects of 3D-Printed Polycaprolactone/β-Tricalcium Phosphate Membranes on Guided Bone Regeneration , 2017, International journal of molecular sciences.

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

[82]  M. Larosa,et al.  Cranial reconstruction: 3D biomodel and custom-built implant created using additive manufacturing. , 2014, Journal of cranio-maxillo-facial surgery : official publication of the European Association for Cranio-Maxillo-Facial Surgery.

[83]  F. Guillemot,et al.  Laser assisted bioprinting of engineered tissue with high cell density and microscale organization. , 2010, Biomaterials.

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

[85]  Xiaofeng Cui,et al.  Thermal inkjet printing in tissue engineering and regenerative medicine. , 2012, Recent patents on drug delivery & formulation.

[86]  M. Hier,et al.  Three‐dimensionally printed polyetherketoneketone scaffolds with mesenchymal stem cells for the reconstruction of critical‐sized mandibular defects , 2017, The Laryngoscope.

[87]  Thierry Chartier,et al.  A new custom made bioceramic implant for the repair of large and complex craniofacial bone defects. , 2013, Journal of cranio-maxillo-facial surgery : official publication of the European Association for Cranio-Maxillo-Facial Surgery.

[88]  J. Sterne,et al.  The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials , 2011, BMJ : British Medical Journal.

[89]  Jean-Pierre Kruth,et al.  Material incress manufacturing by rapid prototyping techniques , 1991 .

[90]  K. Lee,et al.  Cartilage regeneration using biodegradable oxidized alginate/hyaluronate hydrogels. , 2014, Journal of biomedical materials research. Part A.

[91]  Eric D. Miller,et al.  Inkjet-based biopatterning of bone morphogenetic protein-2 to spatially control calvarial bone formation. , 2010, Tissue engineering. Part A.

[92]  Yi Zuo,et al.  Biocompatibility and osteogenesis of biomimetic nano-hydroxyapatite/polyamide composite scaffolds for bone tissue engineering. , 2007, Biomaterials.

[93]  T. Boland,et al.  Inkjet printing of viable mammalian cells. , 2005, Biomaterials.

[94]  Sung Soo Chung,et al.  An improvement in sintering property of beta-tricalcium phosphate by addition of calcium pyrophosphate. , 2002, Biomaterials.

[95]  S. Nair,et al.  Novel chitin/nanosilica composite scaffolds for bone tissue engineering applications. , 2009, International journal of biological macromolecules.

[96]  Fabien Guillemot,et al.  In vivo bioprinting for computer- and robotic-assisted medical intervention: preliminary study in mice , 2010, Biofabrication.

[97]  Moustapha Kassem,et al.  Surface-modified functionalized polycaprolactone scaffolds for bone repair: in vitro and in vivo experiments. , 2014, Journal of biomedical materials research. Part A.

[98]  D. Moher,et al.  Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. , 2009, Journal of clinical epidemiology.

[99]  Ji Hoon Park,et al.  Bone regeneration by means of a three‐dimensional printed scaffold in a rat cranial defect , 2018, Journal of tissue engineering and regenerative medicine.

[100]  P. Alam ‘T’ , 2021, Composites Engineering: An A–Z Guide.

[101]  D. Cho,et al.  Effects of 3 D-Printed Polycaprolactone / β-Tricalcium Phosphate Membranes on Guided Bone Regeneration , 2018 .

[102]  R. Kandel,et al.  Porous calcium polyphosphate scaffolds for bone substitute applications in vivo studies. , 2002, Biomaterials.

[103]  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.