Abstract
As a bone scaffold, meeting all basic requirements besides dealing with other bone-related issues—bone cancer and accelerated regeneration—is not expected from traditional scaffolds, but a newer class of scaffolds called multifunctional. From a clinical point of view, being a multifunctional scaffold means reducing in healing time, direct costs—medicine, surgery, and hospitalization—and indirect costs—loss of mobility, losing job, and pain. The main aim of the present review is following the multifunctional bone scaffolds trend to deal with both bone regeneration and cancer therapy. Special consideration is given to different fabrication techniques which have been applied to yield these materials spanning from traditional to modern ones. Moreover, the hierarchical structure of bone plus bone cancers and available medicines to them are introduced to familiarize the potential reader of review with the pluri-disciplinary essence of the field. Eventually, a brief discussion relating to the future trend of these materials is provided.
Similar content being viewed by others
References
Pérez-Amodio S, Engel E (2014) Bone biology and regeneration. Bio-Ceram Clin Appl. https://doi.org/10.1002/9781118406748.ch11
Reznikov N, Shahar R, Weiner S (2014) Bone hierarchical structure in three dimensions. Acta Biomater 10:3815–3826. https://doi.org/10.1016/j.actbio.2014.05.024
Lohkamp M, Kromer TO, Schmitt H (2017) Osteoarthritis and joint replacements of the lower limb and spine in ex-professional soccer players: a systematic review. Scand J Med Sci Sports 27:1038–1049. https://doi.org/10.1111/sms.12846
Salmon JH, Rat AC, Sellam J, Michel M, Eschard JP, Guillemin F, Jolly D, Fautrel B (2016) Economic impact of lower-limb osteoarthritis worldwide: a systematic review of cost-of-illness studies. Osteoarthr Cartil 24:1500–1508. https://doi.org/10.1016/j.joca.2016.03.012
Pawelec KM (2019) Introduction to the challenges of bone repair. In: Pawelec KM, Planell E (eds) Woodhead publishing series in biomaterials, 2nd edn. Woodhead Publishing, Sawston, pp 1–13. https://doi.org/10.1016/B978-0-08-102451-5.00001-9
Fraumeni JF Jr (1967) Stature and malignant tumors of bone in childhood and adolescence. Cancer 20:967–973. https://doi.org/10.1002/1097-0142(196706)20:6%3c967:AID-CNCR2820200606%3e3.0.CO;2-P
Purushotham S, Ramanujan RV (2010) Thermoresponsive magnetic composite nanomaterials for multimodal cancer therapy. Acta Biomater 6:502–510. https://doi.org/10.1016/j.actbio.2009.07.004
Gupta R, Bajpai AK (2011) Magnetically guided release of ciprofloxacin from superparamagnetic polymer nanocomposites. J Biomater Sci Polym Ed 22:893–918. https://doi.org/10.1163/092050610X496387
Xu R, Ma J, Sun X, Chen Z, Jiang X, Guo Z, Huang L, Li Y, Wang M, Wang C, Liu J, Fan X, Gu J, Chen X, Zhang Y, Gu N (2009) Ag nanoparticles sensitize IR-induced killing of cancer cells. Cell Res 19:1031–1034. https://doi.org/10.1038/cr.2009.89
Gallego Ó, Puntes V (2006) What can nanotechnology do to fight cancer? Clin Transl Oncol 8:788–795. https://doi.org/10.1007/s12094-006-0133-6
Vallet-Regí M, Ruiz-Hernández E (2011) Bioceramics: from bone regeneration to cancer nanomedicine. Adv Mater 23:5177–5218. https://doi.org/10.1002/adma.201101586
Gu W, Wu C, Chen J, Xiao Y (2013) Nanotechnology in the targeted drug delivery for bone diseases and bone regeneration. Int J Nanomed 8:2305–2317. https://doi.org/10.2147/IJN.S44393
Qu H, Fu H, Han Z, Sun Y (2019) Biomaterials for bone tissue engineering scaffolds: a review. RSC Adv 9:26252–26262. https://doi.org/10.1039/C9RA05214C
Vallet-Regí M, Lozano D, González B, Izquierdo-Barba I (2020) Biomaterials against bone infection. Adv Healthc Mater. https://doi.org/10.1002/adhm.202000310
Hutmacher DW (2000) Scaffolds in tissue engineering bone and cartilage. Biomater Silver Jubil Compend. https://doi.org/10.1016/B978-008045154-1.50021-6
Bigham A, Kermani S, Saudi A, Aghajanian A, Rafienia M (2020) On the bioactivity and mechanical properties of gehlenite nanobioceramic: a comparative study YR—2020/4/1. J Med Signals Sens 10:105–112. https://doi.org/10.4103/jmss.JMSS_41_19
Rafienia M, Bigham A, Saudi A, Rahmati S (2018) Gehlenite nanobioceramic: sol–gel synthesis, characterization, and in vitro assessment of its bioactivity. Mater Lett. https://doi.org/10.1016/j.matlet.2018.04.094
Bigham A, Hassanzadeh-Tabrizi SA, Rafienia M, Salehi H (2016) Ordered mesoporous magnesium silicate with uniform nanochannels as a drug delivery system: the effect of calcination temperature on drug delivery rate. Ceram Int. https://doi.org/10.1016/j.ceramint.2016.08.009
Marques C, Ferreira JMF, Andronescu E, Ficai D, Sonmez M, Ficai A (2014) Multifunctional materials for bone cancer treatment. Int J Nanomed 9:2713–2725. https://doi.org/10.2147/IJN.S55943
Bigham A, Aghajanian AH, Behzadzadeh S, Sokhani Z, Shojaei S, Kaviani Y, Hassanzadeh-Tabrizi SA (2019) Nanostructured magnetic Mg2SiO4–CoFe2O4 composite scaffold with multiple capabilities for bone tissue regeneration. Mater Sci Eng, C 99:83–95. https://doi.org/10.1016/j.msec.2019.01.096
Lu Y, Li L, Zhu Y, Wang X, Li M, Lin Z, Hu X, Zhang Y, Yin Q, Xia H, Mao C (2018) Multifunctional copper-containing carboxymethyl chitosan/alginate scaffolds for eradicating clinical bacterial infection and promoting bone formation. ACS Appl Mater Interfaces 10:127–138. https://doi.org/10.1021/acsami.7b13750
Zhang Q, Mochalin VN, Neitzel I, Hazeli K, Niu J, Kontsos A, Zhou JG, Lelkes PI, Gogotsi Y (2012) Mechanical properties and biomineralization of multifunctional nanodiamond-PLLA composites for bone tissue engineering. Biomaterials 33:5067–5075. https://doi.org/10.1016/j.biomaterials.2012.03.063
Tamay DG, Dursun Usal T, Alagoz AS, Yucel D, Hasirci N, Hasirci V (2019) 3D and 4D printing of polymers for tissue engineering applications. Front Bioeng Biotechnol 7:164. https://doi.org/10.3389/fbioe.2019.00164
Ma H, Feng C, Chang J, Wu C (2018) 3D-printed bioceramic scaffolds: from bone tissue engineering to tumor therapy. Acta Biomater 79:37–59. https://doi.org/10.1016/j.actbio.2018.08.026
Fuchs RK, Thompson WR, Warden SJ (2019) Bone biology. In: Pawelec KM, Planell E (eds) Woodhead publishing series in biomaterials, 2nd edn. Woodhead Publishing, Sawston, pp 15–52
Wegst UGK, Bai H, Saiz E, Tomsia AP, Ritchie RO (2015) Bioinspired structural materials. Nat Mater 14:23–36. https://doi.org/10.1038/nmat4089
Koester KJ, Ager JW, Ritchie RO (2008) The true toughness of human cortical bone measured with realistically short cracks. Nat Mater 7:672–677. https://doi.org/10.1038/nmat2221
Rho J-Y, Kuhn-Spearing L, Zioupos P (1998) Mechanical properties and the hierarchical structure of bone. Med Eng Phys 20:92–102. https://doi.org/10.1016/S1350-4533(98)00007-1
Eliaz N, Metoki N (2017) Calcium phosphate bioceramics: a review of their history, structure, properties, coating technologies and biomedical applications. Materials. https://doi.org/10.3390/ma10040334
Dang W, Li T, Li B, Ma H, Zhai D, Wang X, Chang J, Xiao Y, Wang J, Wu C (2018) A bifunctional scaffold with CuFeSe2 nanocrystals for tumor therapy and bone reconstruction. Biomaterials 160:92–106. https://doi.org/10.1016/j.biomaterials.2017.11.020
Samavedi S, Joy N (2017) 3D printing for the development of in vitro cancer models. Curr Opin Biomed Eng 2:35–42. https://doi.org/10.1016/j.cobme.2017.06.003
Mouriño V, Boccaccini AR (2010) Bone tissue engineering therapeutics: controlled drug delivery in three-dimensional scaffolds. J R Soc Interface 7:209–227. https://doi.org/10.1098/rsif.2009.0379
Wadajkar AS, Bhavsar Z, Ko C-Y, Koppolu B, Cui W, Tang L, Nguyen KT (2012) Multifunctional particles for melanoma-targeted drug delivery. Acta Biomater 8:2996–3004. https://doi.org/10.1016/j.actbio.2012.04.042
Ruel-Gariépy E, Shive M, Bichara A, Berrada M, Le Garrec D, Chenite A, Leroux J-C (2004) A thermosensitive chitosan-based hydrogel for the local delivery of paclitaxel. Eur J Pharm Biopharm 57:53–63. https://doi.org/10.1016/S0939-6411(03)00095-X
Nagarajan S, Reddy BSR, Tsibouklis J (2011) In vitro effect on cancer cells: synthesis and preparation of polyurethane membranes for controlled delivery of curcumin. J Biomed Mater Res, Part A 99A:410–417. https://doi.org/10.1002/jbm.a.33203
Fan H, Dash AK (2001) Effect of cross-linking on the in vitro release kinetics of doxorubicin from gelatin implants. Int J Pharm 213:103–116. https://doi.org/10.1016/S0378-5173(00)00651-7
Andronescu E, Ficai A, Albu MG, Mitran V, Sonmez M, Ficai D, Ion R, Cimpean A (2013) Collagen-hydroxyapatite/cisplatin drug delivery systems for locoregional treatment of bone cancer. Technol Cancer Res Treat 12:275–284. https://doi.org/10.7785/tcrt.2012.500331
Mann S, Khawar S, Moran C, Kalhor N (2019) Revisiting localized malignant mesothelioma. Ann Diagn Pathol 39:74–77. https://doi.org/10.1016/j.anndiagpath.2019.02.014
Sabino MAC, Luger NM, Mach DB, Rogers SD, Schwei MJ, Mantyh PW (2003) Different tumors in bone each give rise to a distinct pattern of skeletal destruction, bone cancer-related pain behaviors and neurochemical changes in the central nervous system. Int J Cancer 104:550–558. https://doi.org/10.1002/ijc.10999
Kaliki S, Rathi SG, Palkonda VAR (2018) Primary orbital Ewing sarcoma family of tumors: a study of 12 cases. Eye 32:615–621. https://doi.org/10.1038/eye.2017.278
Goyal S, Roscoe J, Ryder WDJ, Gattamaneni HR, Eden TOB (2004) Symptom interval in young people with bone cancer. Eur J Cancer 40:2280–2286. https://doi.org/10.1016/j.ejca.2004.05.017
Corre I, Verrecchia F, Crenn V, Redini F, Trichet V (2020) The osteosarcoma microenvironment: a complex but targetable ecosystem. Cells. https://doi.org/10.3390/cells9040976
Glass AG, Fraumeni JF Jr (1970) Epidemiology of bone cancer in children. JNCI J Natl Cancer Inst 44:187–199. https://doi.org/10.1093/jnci/44.1.187
Atallah JP, Elshenawy MA, Ali Badran A, Alata MK, Gad A, Alharbi AH, Alquaydheb HN, Alshamsan BI (2020) The outcome of vincristine, dactinomycin D, ifosfamide and doxorubicin (VAIA) as first-line therapy for adult-patients with metastatic ewing sarcoma; a single-center experience. J Clin Oncol 38:e23501–e23501. https://doi.org/10.1200/JCO.2020.38.15_suppl.e23501
Scarborough JA, McClure E, Anderson P, Dhawan A, Durmaz A, Lessnick SL, Hitomi M, Scott JG (2020) Identifying states of collateral sensitivity during the evolution of therapeutic resistance in Ewing’s sarcoma. BioRxiv. https://doi.org/10.1101/2020.02.11.943936
Miles DT, Voskuil RT, Dale W, Mayerson JL, Scharschmidt TJ (2020) Integration of denosumab therapy in the management of giant cell tumors of bone. J Orthop 22:38–47. https://doi.org/10.1016/j.jor.2020.03.020
Sun J, Wei Q, Zhou Y, Wang J, Liu Q, Xu H (2017) A systematic analysis of FDA-approved anticancer drugs. BMC Syst Biol 11:87. https://doi.org/10.1186/s12918-017-0464-7
Prasad SR, Jayakrishnan A, Kumar TSS (2020) Combinational delivery of anticancer drugs for osteosarcoma treatment using electrosprayed core shell nanocarriers. J Mater Sci Mater Med 31:44. https://doi.org/10.1007/s10856-020-06379-5
Plichta Z, Horák D, Mareková D, Turnovcová K, Kaiser R, Jendelová P (2020) Poly[N-(2-hydroxypropyl)methacrylamide]-modified magnetic γ-F2O3 nanoparticles conjugated with doxorubicin for glioblastoma treatment. ChemMedChem 15:96–104. https://doi.org/10.1002/cmdc.201900564
Ahmadi D, Zarei M, Rahimi M, Khazaie M, Asemi Z, Mir SM, Sadeghpour A, Karimian A, Alemi F, Rahmati-Yamchi M, Salehi R, Jadidi-Niaragh F, Yousefi M, Khelgati N, Majidinia M, Safa A, Yousefi B (2020) Preparation and in vitro evaluation of pH-responsive cationic cyclodextrin coated magnetic nanoparticles for delivery of methotrexate to the Saos-2 bone cancer cells. J Drug Deliv Sci Technol 57:101584. https://doi.org/10.1016/j.jddst.2020.101584
Kinch MS, Hoyer D, Patridge E, Plummer M (2015) Target selection for FDA-approved medicines. Drug Discov Today 20:784–789. https://doi.org/10.1016/j.drudis.2014.11.001
Bao Y, Kong X, Yang L, Liu R, Shi Z, Li W, Hua B, Hou W (2014) Complementary and alternative medicine for cancer pain: an overview of systematic reviews, evidence-based complement. Altern Med 2014:170396. https://doi.org/10.1155/2014/170396
Hutmacher DW (2000) Scaffolds in tissue engineering bone and cartilage. In: Williams JC (ed) Biomaterials. Elsevier Science, Oxford, pp 175–189. https://doi.org/10.1016/B978-008045154-1.50021-6
Bigham A, Saudi A, Rafienia M, Rahmati S, Bakhtiyari H, Salahshouri F, Sattary M, Hassanzadeh-Tabrizi SA (2019) Electrophoretically deposited mesoporous magnesium silicate with ordered nanopores as an antibiotic-loaded coating on surface-modified titanium. Mater Sci Eng, C 96:765–775. https://doi.org/10.1016/j.msec.2018.12.013
R. Langer, J.P. Vacanti, Tissue engineering, Science (80-.). 260 (1993) 920 LP – 926. https://doi.org/10.1126/science.8493529
Hollister SJ (2005) Porous scaffold design for tissue engineering. Nat Mater 4:518–524. https://doi.org/10.1038/nmat1421
Hollister SJ (2009) Scaffold design and manufacturing: from concept to clinic. Adv Mater 21:3330–3342. https://doi.org/10.1002/adma.200802977
Vallet-Regí M, González-Calbet JM (2004) Calcium phosphates as substitution of bone tissues. Prog Solid State Chem 32:1–31. https://doi.org/10.1016/j.progsolidstchem.2004.07.001
Izquierdo-Barba I (2014) Scaffold designing. Bio-Ceram Clin Appl. https://doi.org/10.1002/9781118406748.ch10
Bigham A, Aghajanian AH, Saudi A, Rafienia M (2020) Hierarchical porous Mg2SiO4–CoFe2O4 nanomagnetic scaffold for bone cancer therapy and regeneration: surface modification and in vitro studies. Mater Sci Eng, C 109:110579. https://doi.org/10.1016/j.msec.2019.110579
Ansari M, Bigham A, Hassanzadeh Tabrizi SA, Abbastabar Ahangar H (2018) Copper-substituted spinel Zn–Mg ferrite nanoparticles as potential heating agents for hyperthermia. J Am Ceram Soc. https://doi.org/10.1111/jace.15510
Farzin A, Fathi M, Emadi R (2017) Multifunctional magnetic nanostructured hardystonite scaffold for hyperthermia, drug delivery and tissue engineering applications. Mater Sci Eng, C 70:21–31. https://doi.org/10.1016/j.msec.2016.08.060
Iqbal Y, Bae H, Rhee I, Hong S (2016) Control of the saturation temperature in magnetic heating by using polyethylene-glycol-coated rod-shaped nickel-ferrite (NiFe2O4) nanoparticles. J Korean Phys Soc 68:587–592. https://doi.org/10.3938/jkps.68.587
Sun C, Lee JSH, Zhang M (2008) Magnetic nanoparticles in MR imaging and drug delivery. Adv Drug Deliv Rev 60:1252–1265. https://doi.org/10.1016/j.addr.2008.03.018
Ansari M, Bigham A, Ahangar HA (2019) Super-paramagnetic nanostructured CuZnMg mixed spinel ferrite for bone tissue regeneration. Mater Sci Eng, C 105:110084. https://doi.org/10.1016/j.msec.2019.110084
Bigham A, Aghajanian AH, Allahdaneh S, Hassanzadeh-Tabrizi SA (2019) Multifunctional mesoporous magnetic Mg2SiO4–CuFe2O4 core-shell nanocomposite for simultaneous bone cancer therapy and regeneration. Ceram Int 45:19481–19488. https://doi.org/10.1016/j.ceramint.2019.06.205
Bigham A, Foroughi F, Motamedi M, Rafienia M (2018) Multifunctional nanoporous magnetic zinc silicate-ZnFe2O4 core-shell composite for bone tissue engineering applications. Ceram Int. https://doi.org/10.1016/j.ceramint.2018.03.264
Hsiao C-W, Chuang E-Y, Chen H-L, Wan D, Korupalli C, Liao Z-X, Chiu Y-L, Chia W-T, Lin K-J, Sung H-W (2015) Photothermal tumor ablation in mice with repeated therapy sessions using NIR-absorbing micellar hydrogels formed in situ. Biomaterials 56:26–35. https://doi.org/10.1016/j.biomaterials.2015.03.060
Chen Q, Xu L, Liang C, Wang C, Peng R, Liu Z (2016) Photothermal therapy with immune-adjuvant nanoparticles together with checkpoint blockade for effective cancer immunotherapy. Nat Commun 7:13193. https://doi.org/10.1038/ncomms13193
Zhang C, Bu W, Ni D, Zuo C, Cheng C, Li Q, Zhang L, Wang Z, Shi J (2016) A polyoxometalate cluster paradigm with self-adaptive electronic structure for acidity/reducibility-specific photothermal conversion. J Am Chem Soc 138:8156–8164. https://doi.org/10.1021/jacs.6b03375
Zhou F, Li X, Naylor MF, Hode T, Nordquist RE, Alleruzzo L, Raker J, Lam SSK, Du N, Shi L, Wang X, Chen WR (2015) InCVAX—a novel strategy for treatment of late-stage, metastatic cancers through photoimmunotherapy induced tumor-specific immunity. Cancer Lett 359:169–177. https://doi.org/10.1016/j.canlet.2015.01.029
Dang W, Ma B, Huan Z, Lin R, Wang X, Li T, Wu J, Ma N, Zhu H, Chang J, Wu C (2019) LaB6 surface chemistry-reinforced scaffolds for treating bone tumors and bone defects. Appl Mater Today 16:42–55. https://doi.org/10.1016/j.apmt.2019.04.015
Mehrafzoon S, Hassanzadeh-Tabrizi SA, Bigham A (2018) Synthesis of nanoporous Baghdadite by a modified sol-gel method and its structural and controlled release properties. Ceram Int. https://doi.org/10.1016/j.ceramint.2018.04.244
Wang L, Cao J, Lei DL, Cheng XB, Zhou HZ, Hou R, Zhao YH, Cui FZ (2010) Application of nerve growth factor by gel increases formation of bone in mandibular distraction osteogenesis in rabbits. Br J Oral Maxillofac Surg 48:515–519. https://doi.org/10.1016/j.bjoms.2009.08.042
Bigham A, Hassanzadeh-Tabrizi SA, Khamsehashari A, Chami A (2018) Surfactant-assisted sol–gel synthesis and characterization of hierarchical nanoporous merwinite with controllable drug release. J Sol–Gel Sci Technol 87:618–625. https://doi.org/10.1007/s10971-018-4777-9
Foroughi F, Hassanzadeh-Tabrizi SA, Bigham A (2016) In situ microemulsion synthesis of hydroxyapatite-MgFe2O4 nanocomposite as a magnetic drug delivery system. Mater Sci Eng, C. https://doi.org/10.1016/j.msec.2016.07.028
Ansari M, Bigham A, Hassanzadeh-Tabrizi SA, Abbastabar Ahangar H (2017) Synthesis and characterization of Cu0.3Zn0.5Mg0.2Fe2O4 nanoparticles as a magnetic drug delivery system. J Magn Magn Mater 439:67–75. https://doi.org/10.1016/j.jmmm.2017.04.084
Abdal-hay A, Sheikh FA, Lim JK (2013) Air jet spinning of hydroxyapatite/poly(lactic acid) hybrid nanocomposite membrane mats for bone tissue engineering. Colloids Surf B Biointerfaces 102:635–643. https://doi.org/10.1016/j.colsurfb.2012.09.017
Izquierdo-Barba I, Colilla M, Vallet-Regí M (2008) Nanostructured mesoporous silicas for bone tissue regeneration. J Nanomater 2008:106970. https://doi.org/10.1155/2008/106970
Roy TD, Simon JL, Ricci JL, Rekow ED, Thompson VP, Parsons JR (2003) Performance of degradable composite bone repair products made via three-dimensional fabrication techniques. J Biomed Mater Res, Part A 66A:283–291. https://doi.org/10.1002/jbm.a.10582
Deville S, Saiz E, Nalla RK, Tomsia AP (2006) Freezing as a path to build complex composites. Science 311:515–518. https://doi.org/10.1126/science.1120937
Aghajanian AH, Bigham A, Khodaei M, Hossein Kelishadi S (2019) Porous titanium scaffold coated using forsterite/poly-3-hydroxybutyrate composite for bone tissue engineering. Surf Coat Technol 378:124942. https://doi.org/10.1016/j.surfcoat.2019.124942
Almirall A, Larrecq G, Delgado JA, Martı́nez S, Planell JA, Ginebra MP (2004) Fabrication of low temperature macroporous hydroxyapatite scaffolds by foaming and hydrolysis of an α-TCP paste. Biomaterials 25:3671–3680. https://doi.org/10.1016/j.biomaterials.2003.10.066
Yeong W-Y, Chua C-K, Leong K-F, Chandrasekaran M (2004) Rapid prototyping in tissue engineering: challenges and potential. Trends Biotechnol 22:643–652. https://doi.org/10.1016/j.tibtech.2004.10.004
Huang Z-M, Zhang Y-Z, Kotaki M, Ramakrishna S (2003) A review on polymer nanofibers by electrospinning and their applications in nanocomposites. Compos Sci Technol 63:2223–2253. https://doi.org/10.1016/S0266-3538(03)00178-7
Yoon JJ, Kim JH, Park TG (2003) Dexamethasone-releasing biodegradable polymer scaffolds fabricated by a gas-foaming/salt-leaching method. Biomaterials 24:2323–2329. https://doi.org/10.1016/S0142-9612(03)00024-3
Baino F, Novajra G, Vitale-Brovarone C (2015) Bioceramics and scaffolds: a winning combination for tissue engineering. Front Bioeng Biotechnol 3:202. https://doi.org/10.3389/fbioe.2015.00202
Abdellahi M, Najafinezhad A, Ghayour H, Saber-Samandari S, Khandan A (2017) Preparing diopside nanoparticle scaffolds via space holder method: simulation of the compressive strength and porosity. J Mech Behav Biomed Mater 72:171–181. https://doi.org/10.1016/j.jmbbm.2017.05.004
Najafinezhad A, Abdellahi M, Nasiri-Harchegani S, Soheily A, Khezri M, Ghayour H (2017) On the synthesis of nanostructured akermanite scaffolds via space holder method: the effect of the spacer size on the porosity and mechanical properties. J Mech Behav Biomed Mater 69:242–248. https://doi.org/10.1016/j.jmbbm.2017.01.002
Miao X, Lim W-K, Huang X, Chen Y (2005) Preparation and characterization of interpenetrating phased TCP/HA/PLGA composites. Mater Lett 59:4000–4005. https://doi.org/10.1016/j.matlet.2005.07.062
Wu C, Fan W, Zhu Y, Gelinsky M, Chang J, Cuniberti G, Albrecht V, Friis T, Xiao Y (2011) Multifunctional magnetic mesoporous bioactive glass scaffolds with a hierarchical pore structure. Acta Biomater 7:3563–3572. https://doi.org/10.1016/j.actbio.2011.06.028
Aghajanian AH, Khazaei BA, Khodaei M, Rafienia M (2018) Fabrication of porous Mg–Zn scaffold through modified replica method for bone tissue engineering. J Bionic Eng 15:907–913. https://doi.org/10.1007/s42235-018-0077-x
Fukasawa T, Ando M, Ohji T, Kanzaki S (2001) Synthesis of porous ceramics with complex pore structure by freeze-dry processing. J Am Ceram Soc 84:230–232. https://doi.org/10.1111/j.1151-2916.2001.tb00638.x
Fukasawa T, Deng Z-Y, Ando M, Ohji T, Kanzaki S (2002) Synthesis of porous silicon nitride with unidirectionally aligned channels using freeze-drying process. J Am Ceram Soc 85:2151–2155. https://doi.org/10.1111/j.1151-2916.2002.tb00426.x
Rezwan K, Chen QZ, Blaker JJ, Boccaccini AR (2006) Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. Biomaterials 27:3413–3431. https://doi.org/10.1016/j.biomaterials.2006.01.039
Niu Y, Guo L, Liu J, Shen H, Su J, An X, Yu B, Wei J, Shin J-W, Guo H, Ji F, He D (2015) Bioactive and degradable scaffolds of the mesoporous bioglass and poly(l-lactide) composite for bone tissue regeneration. J Mater Chem B 3:2962–2970. https://doi.org/10.1039/C4TB01796J
Ma Z, Kotaki M, Inai R, Ramakrishna S (2005) Potential of nanofiber matrix as tissue-engineering scaffolds. Tissue Eng 11:101–109. https://doi.org/10.1089/ten.2005.11.101
Enayati MS, Behzad T, Sajkiewicz P, Rafienia M, Bagheri R, Ghasemi-Mobarakeh L, Kolbuk D, Pahlevanneshan Z, Bonakdar SH (2018) Development of electrospun poly (vinyl alcohol)-based bionanocomposite scaffolds for bone tissue engineering. J Biomed Mater Res, Part A 106:1111–1120. https://doi.org/10.1002/jbm.a.36309
Yin Z, Chen X, Chen JL, Shen WL, Hieu Nguyen TM, Gao L, Ouyang HW (2010) The regulation of tendon stem cell differentiation by the alignment of nanofibers. Biomaterials 31:2163–2175. https://doi.org/10.1016/j.biomaterials.2009.11.083
Li D, Xia Y (2004) Electrospinning of nanofibers: reinventing the wheel? Adv Mater 16:1151–1170. https://doi.org/10.1002/adma.200400719
Agarwal S, Wendorff JH, Greiner A (2009) Progress in the field of electrospinning for tissue engineering applications. Adv Mater 21:3343–3351. https://doi.org/10.1002/adma.200803092
Leong KF, Cheah CM, Chua CK (2003) Solid freeform fabrication of three-dimensional scaffolds for engineering replacement tissues and organs. Biomaterials 24:2363–2378. https://doi.org/10.1016/S0142-9612(03)00030-9
Butscher A, Bohner M, Hofmann S, Gauckler L, Müller R (2011) Structural and material approaches to bone tissue engineering in powder-based three-dimensional printing. Acta Biomater 7:907–920. https://doi.org/10.1016/j.actbio.2010.09.039
Ghomi H, Jaberzadeh M, Fathi MH (2011) Novel fabrication of forsterite scaffold with improved mechanical properties. J Alloys Compd 509:L63–L68. https://doi.org/10.1016/j.jallcom.2010.10.106
Abdellahi M, Karamian E, Najafinezhad A, Ranjabar F, Chami A, Khandan A (2018) Diopside-magnetite; a novel nanocomposite for hyperthermia applications. J Mech Behav Biomed Mater 77:534–538. https://doi.org/10.1016/j.jmbbm.2017.10.015
Naeimi M, Rafienia M, Fathi M, Janmaleki M, Bonakdar S, Ebrahimian-Hosseinabadi M (2016) Incorporation of chitosan nanoparticles into silk fibroin-based porous scaffolds: chondrogenic differentiation of stem cells. Int J Polym Mater Polym Biomater 65:202–209. https://doi.org/10.1080/00914037.2015.1099103
Toloue EB, Karbasi S, Salehi H, Rafienia M (2019) Potential of an electrospun composite scaffold of poly (3-hydroxybutyrate)-chitosan/alumina nanowires in bone tissue engineering applications. Mater Sci Eng, C 99:1075–1091. https://doi.org/10.1016/j.msec.2019.02.062
Fu S, Hu H, Chen J, Zhu Y, Zhao S (2020) Silicone resin derived larnite/C scaffolds via 3D printing for potential tumor therapy and bone regeneration. Chem Eng J 382:122928. https://doi.org/10.1016/j.cej.2019.122928
Schwartzalder K, Somers AV (1963) Method of making a porous shape of sintered refractory ceramic articles. https://patents.google.com/patent/US3090094A/en
Bartonickova E, Ptacek P, Opravil T, Soukal F, Masilko J, Novotny R, Svec J, Havlica J (2015) Mullite-based refractories fabricated by foam casting. Ceram Int 41:14116–14123. https://doi.org/10.1016/j.ceramint.2015.07.032
Deng X, Wang J, Huang Z, Zhao W, Li F, Zhang H (2015) Research progress in preparation of porous ceramics. Interceram Int Ceram Rev 64:100–103. https://doi.org/10.1007/BF03401108
Bretcanu O, Misra S, Roy I, Renghini C, Fiori F, Boccaccini AR, Salih V (2009) In vitro biocompatibility of 45S5 Bioglass®-derived glass–ceramic scaffolds coated with poly(3-hydroxybutyrate). J Tissue Eng Regen Med 3:139–148. https://doi.org/10.1002/term.150
Khamsehashari N, Hassanzadeh-Tabrizi SA, Bigham A (2018) Effects of strontium adding on the drug delivery behavior of silica nanoparticles synthesized by P123-assisted sol-gel method. Mater Chem Phys 205:283–291. https://doi.org/10.1016/j.matchemphys.2017.11.034
Zhu Y, Shang F, Li B, Dong Y, Liu Y, Lohe MR, Hanagata N, Kaskel S (2013) Magnetic mesoporous bioactive glass scaffolds: preparation, physicochemistry and biological properties. J Mater Chem B 1:1279–1288. https://doi.org/10.1039/C2TB00262K
Güden M, Çelik E, Hızal A, Altındiş M, Çetiner S (2008) Effects of compaction pressure and particle shape on the porosity and compression mechanical properties of sintered Ti6Al4V powder compacts for hard tissue implantation. J Biomed Mater Res Part B Appl Biomater 85B:547–555. https://doi.org/10.1002/jbm.b.30978
Oh I-H, Nomura N, Masahashi N, Hanada S (2003) Mechanical properties of porous titanium compacts prepared by powder sintering. Scr Mater 49:1197–1202. https://doi.org/10.1016/j.scriptamat.2003.08.018
Niu W, Bai C, Qiu G, Wang Q (2009) Processing and properties of porous titanium using space holder technique. Mater Sci Eng, A 506:148–151. https://doi.org/10.1016/j.msea.2008.11.022
Dunand DC (2004) Processing of titanium foams. Adv Eng Mater 6:369–376. https://doi.org/10.1002/adem.200405576
Arifvianto B, Zhou J (2014) Fabrication of metallic biomedical scaffolds with the space holder method: a review. Materials (Basel) 7:3588–3622. https://doi.org/10.3390/ma7053588
Singh R, Lee PD, Dashwood RJ, Lindley TC (2010) Titanium foams for biomedical applications: a review. Mater Technol 25:127–136. https://doi.org/10.1179/175355510X12744412709403
Wen CE, Mabuchi M, Yamada Y, Shimojima K, Chino Y, Asahina T (2001) Processing of biocompatible porous Ti and Mg. Scr Mater 45:1147–1153. https://doi.org/10.1016/S1359-6462(01)01132-0
Torres Y, Pavón JJ, Rodríguez JA (2012) Processing and characterization of porous titanium for implants by using NaCl as space holder. J Mater Process Technol 212:1061–1069. https://doi.org/10.1016/j.jmatprotec.2011.12.015
Laptev A, Bram M, Buchkremer HP, Stöver D (2004) Study of production route for titanium parts combining very high porosity and complex shape. Powder Metall 47:85–92. https://doi.org/10.1179/003258904225015536
Gligor I, Soritau O, Todea M, Berce C, Vulpoi A, Marcu T, Cernea V, Simon S, Popa C (2013) Porous c.p. titanium using dextrin as space holder for endosseous implants. Part Sci Technol 31:357–365. https://doi.org/10.1080/02726351.2012.749556
Zhao X, Sun H, Lan L, Huang J, Zhang H, Wang Y (2009) Pore structures of high-porosity NiTi alloys made from elemental powders with NaCl temporary space-holders. Mater Lett 63:2402–2404. https://doi.org/10.1016/j.matlet.2009.07.069
Jakubowicz J, Adamek G, Dewidar M (2013) Titanium foam made with saccharose as a space holder. J Porous Mater 20:1137–1141. https://doi.org/10.1007/s10934-013-9696-0
Najafinezhad A, Abdellahi M, Saber-Samandari S, Ghayour H, Khandan A (2018) Hydroxyapatite-M-type strontium hexaferrite: a new composite for hyperthermia applications. J Alloys Compd 734:290–300. https://doi.org/10.1016/j.jallcom.2017.10.138
Sahmani S, Khandan A, Saber-Samandari S, Mohammadi Aghdam M (2020) Effect of magnetite nanoparticles on the biological and mechanical properties of hydroxyapatite porous scaffolds coated with ibuprofen drug. Mater Sci Eng, C 111:110835. https://doi.org/10.1016/j.msec.2020.110835
Sill TJ, von Recum HA (2008) Electrospinning: applications in drug delivery and tissue engineering. Biomaterials 29:1989–2006. https://doi.org/10.1016/j.biomaterials.2008.01.011
Rezvani Ghomi E, Khalili S, Nouri Khorasani S, Esmaeely Neisiany R, Ramakrishna S (2019) Wound dressings: current advances and future directions. J Appl Polym Sci 136:47738. https://doi.org/10.1002/app.47738
Ramakrishna S, Fujihara K, Teo W-E, Yong T, Ma Z, Ramaseshan R (2006) Electrospun nanofibers: solving global issues. Mater Today 9:40–50. https://doi.org/10.1016/S1369-7021(06)71389-X
Teo W-E, Ramakrishna S (2006) A review on electrospinning design and nanofibre assemblies. Nanotechnology 17:R89. https://doi.org/10.1088/0957-4484/17/14/R01
Kim TG, Park S-H, Chung HJ, Yang D-Y, Park TG (2010) Microstructured scaffold coated with hydroxyapatite/collagen nanocomposite multilayer for enhanced osteogenic induction of human mesenchymal stem cells. J Mater Chem 20:8927–8933. https://doi.org/10.1039/C0JM01062F
Dalby MJ, Gadegaard N, Tare R, Andar A, Riehle MO, Herzyk P, Wilkinson CDW, Oreffo ROC (2007) The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat Mater 6:997–1003. https://doi.org/10.1038/nmat2013
Pramanik S, Pingguan-Murphy B, Abu Osman NA (2012) Progress of key strategies in development of electrospun scaffolds: bone tissue. Sci Technol Adv Mater 13:43002. https://doi.org/10.1088/1468-6996/13/4/043002
Neisiany RE, Enayati MS, Kazemi-Beydokhti A, Das O, Ramakrishna S (2020) Multilayered bio-based electrospun membranes: a potential porous media for filtration applications. Front Mater 7:67. https://doi.org/10.3389/fmats.2020.00067
Khosravi F, Nouri Khorasani S, Rezvani Ghomi E, Kichi MK, Zilouei H, Farhadian M, Esmaeely Neisiany R (2019) A bilayer GO/nanofibrous biocomposite coating to enhance 316L stainless steel corrosion performance. Mater Res Express 6:086470. https://doi.org/10.1088/2053-1591/ab26d5
Kim H-W, Song J-H, Kim H-E (2005) Nanofiber generation of gelatin-hydroxyapatite biomimetics for guided tissue regeneration. Adv Funct Mater 15:1988–1994. https://doi.org/10.1002/adfm.200500116
Stanishevsky A, Chowdhury S, Chinoda P, Thomas V (2008) Hydroxyapatite nanoparticle loaded collagen fiber composites: microarchitecture and nanoindentation study. J Biomed Mater Res, Part A 86A:873–882. https://doi.org/10.1002/jbm.a.31657
Fu S, Wang X, Guo G, Shi S, Liang H, Luo F, Wei Y, Qian Z (2010) Preparation and characterization of nano-hydroxyapatite/poly(ε-caprolactone) − poly(ethylene glycol) − poly(ε-caprolactone) composite fibers for tissue engineering. J Phys Chem C 114:18372–18378. https://doi.org/10.1021/jp106488t
Khosravi F, Nouri Khorasani S, Khalili S, Esmaeely Neisiany R, Rezvani Ghomi E, Ejeian F, Das O, Nasr-Esfahani HM (2020) Development of a highly proliferated bilayer coating on 316L stainless steel implants. Polymers 12:1022. https://doi.org/10.3390/polym12051022
Gloria A, Russo T, D’Amora U, Zeppetelli S, D’Alessandro T, Sandri M, Bañobre-López M, Piñeiro-Redondo Y, Uhlarz M, Tampieri A, Rivas J, Herrmannsdörfer T, Dediu VA, Ambrosio L, De Santis R (2013) Magnetic poly(ε-caprolactone)/iron-doped hydroxyapatite nanocomposite substrates for advanced bone tissue engineering. J R Soc Interface 10:20120833. https://doi.org/10.1098/rsif.2012.0833
Amarjargal A, Tijing LD, Park C-H, Im I-T, Kim CS (2013) Controlled assembly of superparamagnetic iron oxide nanoparticles on electrospun PU nanofibrous membrane: a novel heat-generating substrate for magnetic hyperthermia application. Eur Polym J 49:3796–3805. https://doi.org/10.1016/j.eurpolymj.2013.08.026
Meng J, Xiao B, Zhang Y, Liu J, Xue H, Lei J, Kong H, Huang Y, Jin Z, Gu N, Xu H (2013) Super-paramagnetic responsive nanofibrous scaffolds under static magnetic field enhance osteogenesis for bone repair in vivo. Sci Rep 3:2655. https://doi.org/10.1038/srep02655
Radmansouri M, Bahmani E, Sarikhani E, Rahmani K, Sharifianjazi F, Irani M (2018) Doxorubicin hydrochloride—loaded electrospun chitosan/cobalt ferrite/titanium oxide nanofibers for hyperthermic tumor cell treatment and controlled drug release. Int J Biol Macromol 116:378–384. https://doi.org/10.1016/j.ijbiomac.2018.04.161
Mishra R, Bishop T, Valerio IL, Fisher JP, Dean D (2016) The potential impact of bone tissue engineering in the clinic. Regen Med 11:571–587. https://doi.org/10.2217/rme-2016-0042
Lu Y, Chen G, Long Z, Li M, Ji C, Wang F, Li H, Lu J, Wang Z, Li J (2019) Novel 3D-printed prosthetic composite for reconstruction of massive bone defects in lower extremities after malignant tumor resection. J Bone Oncol 16:100220. https://doi.org/10.1016/j.jbo.2019.100220
Ke X, Qiu J, Wang X, Yang X, Shen J, Ye S, Yang G, Xu S, Bi Q, Gou Z, Jia X, Zhang L (2020) Modification of pore-wall in direct ink writing wollastonite scaffolds favorable for tuning biodegradation and mechanical stability and enhancing osteogenic capability. FASEB J 34:5673–5687. https://doi.org/10.1096/fj.201903044R
Chen Y, Han P, Vandi L-J, Dehghan-Manshadi A, Humphry J, Kent D, Stefani I, Lee P, Heitzmann M, Cooper-White J, Dargusch M (2019) A biocompatible thermoset polymer binder for Direct Ink Writing of porous titanium scaffolds for bone tissue engineering. Mater Sci Eng, C 95:160–165. https://doi.org/10.1016/j.msec.2018.10.033
Kanczler JM, Wells JA, Gibbs DMR, Marshall KM, Tang DKO, Oreffo ROC (2020) Chapter 50—Bone tissue engineering and bone regeneration. In: Lanza R, Langer R, Vacanti JP, Atala E (eds) Principles of tissue engineering, 5th edn. Academic Press, Cambridge, pp 917–935. https://doi.org/10.1016/B978-0-12-818422-6.00052-6
Kondiah PPD, Choonara YE, Kondiah PJ, Marimuthu T, du Toit LC, Kumar P, Pillay V (2020) Recent progress in 3D-printed polymeric scaffolds for bone tissue engineering. In: du Toit LC, Kumar P, Choonara YE, Pillay TE (eds) Woodhead publishing series in biomaterials. Elsevier, Amsterdam, pp 59–81. https://doi.org/10.1016/B978-0-12-818471-4.00003-0
MorenoMadrid AP, Vrech SM, Sanchez MA, Rodriguez AP (2019) Advances in additive manufacturing for bone tissue engineering scaffolds. Mater Sci Eng, C 100:631–644. https://doi.org/10.1016/j.msec.2019.03.037
Emre Ö, Mirigul A (2019) Effect of structural hybrid design on mechanical and biological properties of CoCr scaffolds fabricated by selective laser melting. Rapid Prototyp J 26:615–624. https://doi.org/10.1108/RPJ-07-2019-0186
Qu H (2020) Additive manufacturing for bone tissue engineering scaffolds. Mater Today Commun 24:101024. https://doi.org/10.1016/j.mtcomm.2020.101024
Esslinger S, Gadow R (2020) Additive manufacturing of bioceramic scaffolds by combination of FDM and slip casting. J Eur Ceram Soc 40:3707–3713. https://doi.org/10.1016/j.jeurceramsoc.2019.10.029
Choi WJ, Hwang KS, Kwon HJ, Lee C, Kim CH, Kim TH, Heo SW, Kim J-H, Lee J-Y (2020) Rapid development of dual porous poly(lactic acid) foam using fused deposition modeling (FDM) 3D printing for medical scaffold application. Mater Sci Eng, C 110:110693. https://doi.org/10.1016/j.msec.2020.110693
Kholgh Eshkalak S, Rezvani Ghomi E, Dai Y, Choudhury D, Ramakrishna S (2020) The role of three-dimensional printing in healthcare and medicine. Mater Des 194:108940. https://doi.org/10.1016/j.matdes.2020.108940
Ji K, Wang Y, Wei Q, Zhang K, Jiang A, Rao Y, Cai X (2018) Application of 3D printing technology in bone tissue engineering. Bio-Des Manuf 1:203–210. https://doi.org/10.1007/s42242-018-0021-2
Ma H, Jiang C, Zhai D, Luo Y, Chen Y, Lv F, Yi Z, Deng Y, Wang J, Chang J, Wu C (2016) A bifunctional biomaterial with photothermal effect for tumor therapy and bone regeneration. Adv Funct Mater 26:1197–1208. https://doi.org/10.1002/adfm.201504142
Ma H, Luo J, Sun Z, Xia L, Shi M, Liu M, Chang J, Wu C (2016) 3D printing of biomaterials with mussel-inspired nanostructures for tumor therapy and tissue regeneration. Biomaterials 111:138–148. https://doi.org/10.1016/j.biomaterials.2016.10.005
Khandan A, Ozada N, Saber-Samandari S, Ghadiri Nejad M (2018) On the mechanical and biological properties of bredigite-magnetite (Ca7MgSi4O16–Fe3O4) nanocomposite scaffolds. Ceram Int 44:3141–3148. https://doi.org/10.1016/j.ceramint.2017.11.082
Lu J-W, Yang F, Ke Q-F, Xie X-T, Guo Y-P (2018) Magnetic nanoparticles modified-porous scaffolds for bone regeneration and photothermal therapy against tumors. Nanomed Nanotechnol Biol Med 14:811–822. https://doi.org/10.1016/j.nano.2017.12.025
Wang H, Zeng X, Pang L, Wang H, Lin B, Deng Z, Qi ELX, Miao N, Wang D, Huang P, Hu H, Li J (2020) Integrative treatment of anti-tumor/bone repair by combination of MoS2 nanosheets with 3D printed bioactive borosilicate glass scaffolds. Chem Eng J 396:125081. https://doi.org/10.1016/j.cej.2020.125081
Liu Y, Lin R, Ma L, Zhuang H, Feng C, Chang J, Wu C (2020) Mesoporous bioactive glass for synergistic therapy of tumor and regeneration of bone tissue. Appl Mater Today 19:100578. https://doi.org/10.1016/j.apmt.2020.100578
Liu Y, Li T, Ma H, Zhai D, Deng C, Wang J, Zhuo S, Chang J, Wu C (2018) 3D-printed scaffolds with bioactive elements-induced photothermal effect for bone tumor therapy. Acta Biomater 73:531–546. https://doi.org/10.1016/j.actbio.2018.04.014
Wu C, Zhou Y, Xu M, Han P, Chen L, Chang J, Xiao Y (2013) Copper-containing mesoporous bioactive glass scaffolds with multifunctional properties of angiogenesis capacity, osteostimulation and antibacterial activity. Biomaterials 34:422–433. https://doi.org/10.1016/j.biomaterials.2012.09.066
Wu C, Zhou Y, Fan W, Han P, Chang J, Yuen J, Zhang M, Xiao Y (2012) Hypoxia-mimicking mesoporous bioactive glass scaffolds with controllable cobalt ion release for bone tissue engineering. Biomaterials 33:2076–2085. https://doi.org/10.1016/j.biomaterials.2011.11.042
Hadidi M, Bigham A, Saebnoori E, Hassanzadeh-Tabrizi SA, Rahmati S, Alizadeh ZM, Nasirian V, Rafienia M (2017) Electrophoretic-deposited hydroxyapatite-copper nanocomposite as an antibacterial coating for biomedical applications. Surf Coat Technol. https://doi.org/10.1016/j.surfcoat.2017.04.055
Author information
Authors and Affiliations
Contributions
AB, FF, and ERG summarized the literature and wrote a major part of the manuscript. MR, REN, and SR conducted the deep review, editing, guidance, and supervision. All authors have read and approved the article for publication.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Human and animal rights
This article does not contain any studies with human or animal subjects performed by any of the authors.
Rights and permissions
About this article
Cite this article
Bigham, A., Foroughi, F., Rezvani Ghomi, E. et al. The journey of multifunctional bone scaffolds fabricated from traditional toward modern techniques. Bio-des. Manuf. 3, 281–306 (2020). https://doi.org/10.1007/s42242-020-00094-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42242-020-00094-4