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Advances in Antimicrobial and Osteoinductive Biomaterials

  • Samson Afewerki
  • Nicole Bassous
  • Samarah Harb
  • Carlos Palo-Nieto
  • Guillermo U. Ruiz-Esparza
  • Fernanda R. Marciano
  • Thomas Webster
  • Anderson Oliveira LoboEmail author
Chapter
  • 123 Downloads

Abstract

The enormous growing problem with antibiotic resistance in pathogenic microbes is one of the greatest threats we are facing today. In the context of orthopedic applications, infections also lead to the limited healing ability of infected and defected bone. Generally, these problems are treated with a load of antibiotics or surgical intervention. Therefore, having antibacterial properties integrated with a biomaterial would reduce the time of healing and treatment, amount of antibiotic needed, and total cost. Currently, there exists several strategies and materials with the potential of tackling these challenges. Some materials with antibacterial properties currently employed are silver nanoparticles (AgNPs), cerium oxide nanoparticles (CeO2NPs), selenium nanoparticles (SeNPs), copper nanoparticles (CuNPs), antimicrobial peptides (AMPs), biopolymers (such as chitosan), and carbon nanostructures. On the other hand, osteoinductive and osteoconductive materials are important to promote bone healing and regeneration. Within this framework, materials which have been employed widely are bioactive glasses (BG), calcium phosphates (CaPs) (e.g., hydroxyapatite (HA), tricalcium β-phosphate (β-TCP), and biphasic calcium phosphate (BCP)), peptides, growth factors, and other elements (e.g., magnesium (Mg), zinc (Zn), strontium (Sr), silicon (Si), selenium (Se), and Cu, to name a few). Some of the current technological solutions that have been employed are, for instance, the use of a co-delivery system, where both the antibacterial and the osteoinducing agents are delivered from the same delivery system. However, this approach requires overcoming challenges with local delivery in a sustained and prolonged way, thus avoiding tissue toxicity. To address these challenges and promote novel biomaterials with dual action, sophisticated thinking and approaches have to be employed. For this, it is of the utmost importance to have a solid fundamental understanding of current technologies, bacteria behavior and response to treatments, and also a correlation between the material of use, the host tissue and bacteria. We hope by highlighting these aspects, we will promote the invention of the next generation of smart biomaterials with dual action ability to both inhibit infection and promote tissue growth.

Keywords

Antibacterial Osteoinduction Osteoconduction Biomaterials Orthopedic treatment Tissue engineering Defect Infection Antibiotic resistant Dentistry 

Notes

Acknowledgements

Dr. Afewerki gratefully acknowledges the financial support from the Sweden-America Foundation (The Family Mix Entrepreneur Foundation) and the Olle Engkvist Byggmästare Foundation. Professor Lobo and Professor Marciano acknowledge the National Council for Scientific and Technological Development for support (CNPq, #303752/2017-3 to AOL and #304133/2017-5 to FRM).

References

  1. 1.
    Thomas MV, Puleo DA (2011) Infection, inflammation, and bone regeneration: a paradoxical relationship. J Dent Res 90(9):1052–1061PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Moriarty TF, Kuehl R, Coenye T, Metsemakers W-J, Morgenstern M, Schwarz EM et al (2016) Orthopaedic device-related infection: current and future interventions for improved prevention and treatment. EFORT Open Rev 1(4):89–99PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Winkler H (2017) Treatment of chronic orthopaedic infection. EFORT Open Rev 2(5):110–116PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Ribeiro M, Monteiro FJ, Ferraz MP (2012) Infection of orthopedic implants with emphasis on bacterial adhesion process and techniques used in studying bacterial-material interactions. Biomatter 2(4):176–194PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Zhang K, Wang S, Zhou C, Cheng L, Gao X, Xie X et al (2018) Advanced smart biomaterials and constructs for hard tissue engineering and regeneration. Bone Res 6(1):31PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Lu H, Liu Y, Guo J, Wu H, Wang J, Wu G (2016) Biomaterials with antibacterial and osteoinductive properties to repair infected bone defects. Int J Mol Sci 17(3):334PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Raphel J, Holodniy M, Goodman SB, Heilshorn SC (2016) Multifunctional coatings to simultaneously promote osseointegration and prevent infection of orthopaedic implants. Biomaterials 84:301–314PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Franci G, Falanga A, Galdiero S, Palomba L, Rai M, Morelli G et al (2015) Silver nanoparticles as potential antibacterial agents. Molecules 20(5):8856–8874PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Pelletier DA, Suresh AK, Holton GA, McKeown CK, Wang W, Gu B et al (2010) Effects of engineered cerium oxide nanoparticles on bacterial growth and viability. Appl Environ Microbiol 76(24):7981–7989PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Guisbiers G, Wang Q, Khachatryan E, Mimun L, Mendoza-Cruz R, Larese-Casanova P et al (2016) Inhibition of E. coli and S. aureus with selenium nanoparticles synthesized by pulsed laser ablation in deionized water. Int J Nanomedicine 11:3731–3736PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Al-Jumaili A, Alancherry S, Bazaka K, Jacob MV (2017) Review on the antimicrobial properties of carbon nanostructures. Materials 10(9):1066PubMedCentralCrossRefPubMedGoogle Scholar
  12. 12.
    Tan H, Ma R, Lin C, Liu Z, Tang T (2013) Quaternized chitosan as an antimicrobial agent: antimicrobial activity, mechanism of action and biomedical applications in orthopedics. Int J Mol Sci 14(1):1854–1869PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Coppo E, Marchese A (2014) Antibacterial activity of polyphenols. Curr Pharm Biotechnol 15(4):380–390PubMedCrossRefGoogle Scholar
  14. 14.
    Lee E, Song Y, Lee S (2014) Antimicrobial property and biodegradability of lignin nanofibers. Master’s thesis, Yonsei University, Republic of KoreaGoogle Scholar
  15. 15.
    Scalbert A (1991) Antimicrobial properties of tannins. Phytochemistry 30(12):3875–3883CrossRefGoogle Scholar
  16. 16.
    Reddy K, Yedery R, Aranha C (2004) Antimicrobial peptides: premises and promises. Int J Antimicrob Agents 24(6):536–547PubMedCrossRefGoogle Scholar
  17. 17.
    Habibovic P, Barralet J (2011) Bioinorganics and biomaterials: bone repair. Acta Biomater 7(8):3013–3026PubMedCrossRefGoogle Scholar
  18. 18.
    Zhang W, Zhu C, Wu Y, Ye D, Wang S, Zou D et al (2014) VEGF and BMP-2 promote bone regeneration by facilitating bone marrow stem cell homing and differentiation. Eur Cell Mater 27(12):1–11PubMedGoogle Scholar
  19. 19.
    Hench LL, Splinter RJ, Allen W, Greenlee T (1971) Bonding mechanisms at the interface of ceramic prosthetic materials. J Biomed Mater Res 5(6):117–141CrossRefGoogle Scholar
  20. 20.
    Tomás H, Alves CS, Rodrigues J (2018) Laponite®: a key nanoplatform for biomedical applications? Nanomedicine 14(7):2407–2420PubMedCrossRefGoogle Scholar
  21. 21.
    Pountos I, Panteli M, Lampropoulos A, Jones E, Calori GM, Giannoudis PV (2016) The role of peptides in bone healing and regeneration: a systematic review. BMC Med 14(1):103PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Ratner BD, Hoffman AS, Schoen FJ, Lemons JE (2004) Biomaterials science—an introduction to materials in medicine, 2nd edn. Elsevier, New YorkGoogle Scholar
  23. 23.
    Hench LL, Thompson I (2010) Twenty-first century challenges for biomaterials. J R Soc Interface 7(Suppl 4):S379–SS91PubMedPubMedCentralGoogle Scholar
  24. 24.
    Campana V, Milano G, Pagano E, Barba M, Cicione C, Salonna G et al (2014) Bone substitutes in orthopaedic surgery: from basic science to clinical practice. J Mater Sci Mater Med 25(10):2445–2461PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Hench LL (1998) Bioceram J Am Ceram Soc 81(7):1705–1728CrossRefGoogle Scholar
  26. 26.
    Rea S, Bonfield W (2004) Biocomposites for medical applications. J Australas Ceram Soc 40(1):43–57Google Scholar
  27. 27.
    Hench L (1980) Biomaterials. Science 208(4446):826–831PubMedCrossRefGoogle Scholar
  28. 28.
    Ratner BD, Hoffman AS, Yaszemski MJ, Lemons JE, Schoen FJ (2012) Biomaterials science : an introduction to materials in medicine. Elsevier Science & Technology, San DiegoGoogle Scholar
  29. 29.
    Uludağ H (2014) Grand challenges in biomaterials. Front Bioeng Biotechnol 2:43PubMedPubMedCentralGoogle Scholar
  30. 30.
    Muschler GF, Nakamoto C, Griffith LG (2004) Engineering principles of clinical cell-based tissue engineering. J Bone Joint Surg Am 86(7):1541–1558PubMedCrossRefGoogle Scholar
  31. 31.
    Kowalski PS, Bhattacharya C, Afewerki S, Langer R (2018) Smart biomaterials: recent advances and future directions. ACS Biomater Sci Eng 4(11):3809–3817CrossRefGoogle Scholar
  32. 32.
    Novosel EC, Kleinhans C, Kluger PJ (2011) Vascularization is the key challenge in tissue engineering. Adv Drug Deliv Rev 63(4):300–311PubMedCrossRefGoogle Scholar
  33. 33.
    Soker S, Machado M, Atala A (2000) Systems for therapeutic angiogenesis in tissue engineering. World J Urol 18(1):10–18PubMedCrossRefGoogle Scholar
  34. 34.
    Rouwkema J, Rivron NC, van Blitterswijk CA (2008) Vascularization in tissue engineering. Trends Biotechnol 26(8):434–441PubMedCrossRefGoogle Scholar
  35. 35.
    Mikos AG, Sarakinos G, Lyman MD, Ingber DE, Vacanti JP, Langer R (1993) Prevascularization of porous biodegradable polymers. Biotechnol Bioeng 42(6):716–723PubMedCrossRefGoogle Scholar
  36. 36.
    Patel ZS, Young S, Tabata Y, Jansen JA, Wong ME, Mikos AG (2008) Dual delivery of an angiogenic and an osteogenic growth factor for bone regeneration in a critical size defect model. Bone 43(5):931–940PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Whang K, Healy K, Elenz D, Nam E, Tsai D, Thomas C et al (1999) Engineering bone regeneration with bioabsorbable scaffolds with novel microarchitecture. Tissue Eng 5(1):35–51PubMedCrossRefGoogle Scholar
  38. 38.
    Petite H, Viateau V, Bensaid W, Meunier A, de Pollak C, Bourguignon M et al (2000) Tissue-engineered bone regeneration. Nat Biotechnol 18(9):959–963PubMedCrossRefGoogle Scholar
  39. 39.
    García JR, García AJ (2016) Biomaterial-mediated strategies targeting vascularization for bone repair. Drug Delivery Transl Res 6(2):77–95CrossRefGoogle Scholar
  40. 40.
    Bielby RC, Christodoulou IS, Pryce RS, Radford WJ, Hench LL, Polak JM (2004) Time- and concentration-dependent effects of dissolution products of 58S Sol–gel bioactive glass on proliferation and differentiation of murine and human osteoblasts. Tissue Eng 10:1018–1026PubMedCrossRefGoogle Scholar
  41. 41.
    Bielby RC, Pryce RS, Hench LL, Polak JM (2005) Enhanced derivation of osteogenic cells from murine embryonic stem cells after treatment with ionic dissolution products of 58S bioactive sol–gel glass. Tissue Eng 11(3–4):479–488PubMedCrossRefGoogle Scholar
  42. 42.
    Gao J, Dennis JE, Solchaga LA, Awadallah AS, Goldberg VM, Caplan AI (2001) Tissue-engineered fabrication of an osteochondral composite graft using rat bone marrow-derived mesenchymal stem cells. Tissue Eng 7(4):363–371PubMedCrossRefGoogle Scholar
  43. 43.
    Karp JM, Shoichet MS, Davies JE (2003) Bone formation on two-dimensional poly (DL-lactide-co-glycolide)(PLGA) films and three-dimensional PLGA tissue engineering scaffolds in vitro. J Biomed Mater Res A 64(2):388–396PubMedCrossRefGoogle Scholar
  44. 44.
    Grande DA, Breitbart AS, Mason J, Paulino C, Laser J, Schwartz RE (1999) Cartilage tissue engineering: current limitations and solutions. Clin Orthop Relat Res 367:S176–SS85CrossRefGoogle Scholar
  45. 45.
    Hutmacher DW, Sittinger M (2003) Periosteal cells in bone tissue engineering. Tissue Eng 9(Suppl 1):S45–S64PubMedCrossRefGoogle Scholar
  46. 46.
    De Miguel MP, Fuentes-Julián S, Alcaina Y (2010) Pluripotent stem cells: origin, maintenance and induction. Stem Cell Rev 6(4):633–649CrossRefGoogle Scholar
  47. 47.
    Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS et al (1998) Embryonic stem cell lines derived from human blastocysts. Science 282(5391):1145–1147PubMedCrossRefGoogle Scholar
  48. 48.
    Hubbell JA, Thomas SN, Swartz MA (2009) Materials engineering for immunomodulation. Nature 462(7272):449–460PubMedCrossRefGoogle Scholar
  49. 49.
    Quaile A (2012) Infections associated with spinal implants. Int Orthop 36(2):451–456PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Arciola CR, Campoccia D, Montanaro L (2018) Implant infections: adhesion, biofilm formation and immune evasion. Nat Rev Microbiol 16(7):397–409PubMedCrossRefGoogle Scholar
  51. 51.
    Bose S, Bandyopadhyay A (2017) Materials and devices for bone disorders, 1st edn. Elsevier, Amsterdam, pp 1–560CrossRefGoogle Scholar
  52. 52.
    Romanò CL, Scarponi S, Gallazzi E, Romanò D, Drago L (2015) Antibacterial coating of implants in orthopaedics and trauma: a classification proposal in an evolving panorama. J Orthop Surg Res 10(1):157PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Aranya AK, Pushalkar S, Zhao M, LeGeros RZ, Zhang Y, Saxena D (2017) Antibacterial and bioactive coatings on titanium implant surfaces. J Biomed Mater Res A 105(8):2218–2227PubMedCentralCrossRefPubMedGoogle Scholar
  54. 54.
    Orapiriyakul W, Young PS, Damiati L, Tsimbouri PM (2018) Antibacterial surface modification of titanium implants in orthopaedics. J Tissue Eng 9:2041731418789838PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Kim JS, Kuk E, Yu KN, Kim J-H, Park SJ, Lee HJ et al (2007) Antimicrobial effects of silver nanoparticles. Nanomedicine 3(1):95–101PubMedCrossRefGoogle Scholar
  56. 56.
    Rahman S, Carter P, Bhattarai N (2017) Aloe vera for tissue engineering applications. J Funct Biomater 8(1):6PubMedCentralCrossRefPubMedGoogle Scholar
  57. 57.
    Bansal SS, Kausar H, Vadhanam MV, Ravoori S, Pan J, Rai SN et al (2014) Curcumin implants, not curcumin diet, inhibit estrogen-induced mammary carcinogenesis in ACI rats. Cancer Prev Res (Phila) 7(4):456–465CrossRefGoogle Scholar
  58. 58.
    Pakdel F, Ghasemi S, Babaloo A, Javadzadeh Y, Momeni R, Ghanizadeh M et al (2017) Antibacterial effects of garlic extracts and ziziphora essential oil on bacteria associated with peri-implantitis. J Clin Diagn Res 11(4):ZC16–ZC19PubMedPubMedCentralGoogle Scholar
  59. 59.
    Nichols SP, Schoenfisch MH (2013) Nitric oxide flux-dependent bacterial adhesion and viability at fibrinogen-coated surfaces. Biomater Sci 1(11):1151–1159CrossRefGoogle Scholar
  60. 60.
    Freitas SC, Correa-Uribe A, Cristina L, Martins M, Pelaez-Vargas A (2018) Self-assembled monolayers for dental implants. Int J Dent 2018:4395460PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Bessa PC, Casal M, Reis RL (2008) Bone morphogenetic proteins in tissue engineering: the road from laboratory to clinic, part II (BMP delivery). J Tissue Eng Regen Med 2(2–3):81–96PubMedCrossRefGoogle Scholar
  62. 62.
    Simmons CA, Alsberg E, Hsiong S, Kim WJ, Mooney DJ (2004) Dual growth factor delivery and controlled scaffold degradation enhance in vivo bone formation by transplanted bone marrow stromal cells. Bone 35(2):562–569PubMedCrossRefGoogle Scholar
  63. 63.
    Zhao L, Chu PK, Zhang Y, Wu Z (2009) Antibacterial coatings on titanium implants. J Biomed Mater Res B Appl Biomater 91(1):470–480PubMedCrossRefGoogle Scholar
  64. 64.
    Modjarrad K, Ebnesajjad S (2013) Handbook of polymer applications in medicine and medical devices. Elsevier, Amsterdam, pp 1–354Google Scholar
  65. 65.
    Bohner M (2010) Resorbable biomaterials as bone graft substitutes. Mater Today 13(1):24–30CrossRefGoogle Scholar
  66. 66.
    Wilhelmi M, Haverich A (2013) Functionalized medical implants in the era of personalized medicine. Clin Pract 10(2):119–121CrossRefGoogle Scholar
  67. 67.
    Qin M, Liu Y, Wang L, Li D, Jin Z, Liu Y et al (2017) Laser metal direct forming of the customized titanium implants. Rare Metal Mater Eng 46(2017):1924–1928Google Scholar
  68. 68.
    Bosetti M, Fusaro L, Nicolì E, Borrone A, Aprile S, Cannas M (2014) Poly-L-lactide acid-modified scaffolds for osteoinduction and osteoconduction. J Biomed Mater Res Part A 102(10):3531–3539CrossRefGoogle Scholar
  69. 69.
    Goonoo N, Bhaw-Luximon A (2018) Regenerative medicine: induced pluripotent stem cells and their benefits on accelerated bone tissue reconstruction using scaffolds. J Mater Res 33(11):1573–1591CrossRefGoogle Scholar
  70. 70.
    Algburi A, Comito N, Kashtanov D, Dicks LMT, Chikindas ML (2017) Control of biofilm formation: antibiotics and beyond. Appl Environ Microbiol 83(3):e02508–e02516PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Albrektsson T, Johansson C (2001) Osteoinduction, osteoconduction and osseointegration. Eur Spine J 10(Suppl 2):S96–S101PubMedPubMedCentralGoogle Scholar
  72. 72.
    Jäger M, Jennissen HP, Dittrich F, Fischer A, Köhling HL (2017) Antimicrobial and osseointegration properties of nanostructured titanium orthopaedic implants. Materials (Basel) 10(11):1302PubMedCentralCrossRefPubMedGoogle Scholar
  73. 73.
    Hatton BD (2015) Antimicrobial coatings for metallic biomaterials. In: Wen C (ed) Surface coating and modification of metallic biomaterials. Woodhead Publishing, Sawston, pp 379–391CrossRefGoogle Scholar
  74. 74.
    Betancourt T, Brannon-Peppas L (2006) Micro- and nanofabrication methods in nanotechnological medical and pharmaceutical devices. Int J Nanomed 1(4):483–495CrossRefGoogle Scholar
  75. 75.
    Besinis A, Hadi SD, Le HR, Tredwin C, Handy RD (2017) Antibacterial activity and biofilm inhibition by surface modified titanium alloy medical implants following application of silver, titanium dioxide and hydroxyapatite nanocoatings. Nanotoxicology 11(3):327–338PubMedCrossRefGoogle Scholar
  76. 76.
    Tripathy A, Pahal S, Mudakavi RJ, Raichur AM, Varma MM, Sen P (2018) Impact of bioinspired nanotopography on the antibacterial and antibiofilm efficacy of chitosan. Biomacromolecules 19(4):1340–1346PubMedCrossRefGoogle Scholar
  77. 77.
    Ercan B, Khang D, Carpenter J, Webster TJ (2013) Using mathematical models to understand the effect of nanoscale roughness on protein adsorption for improving medical devices. Int J Nanomedicine 8(Suppl 1):75–81PubMedPubMedCentralGoogle Scholar
  78. 78.
    Slavin YN, Asnis J, Häfeli UO, Bach H (2017) Metal nanoparticles: understanding the mechanisms behind antibacterial activity. J Nanobiotechnol 15(1):65CrossRefGoogle Scholar
  79. 79.
    Pandey JK, Swarnkar R, Soumya K, Dwivedi P, Singh MK, Sundaram S et al (2014) Silver nanoparticles synthesized by pulsed laser ablation: as a potent antibacterial agent for human enteropathogenic gram-positive and gram-negative bacterial strains. Appl Biochem Biotechnol 174(3):1021–1031PubMedCrossRefGoogle Scholar
  80. 80.
    O’Neill J (2016) The review on antimicrobial resistance. Tackling drug-resistant infections globally: final report and recommendationsGoogle Scholar
  81. 81.
    Gupta A, Mumtaz S, Li C-H, Hussain I, Rotello VM (2019) Combatting antibiotic-resistant bacteria using nanomaterials. Chem Soc Rev 48(2):415–427PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Kumar M, Curtis A, Hoskins C (2018) Application of nanoparticle technologies in the combat against anti-microbial resistance. Pharmaceutics 10(1):11PubMedCentralCrossRefPubMedGoogle Scholar
  83. 83.
    Alpaslan E, Geilich BM, Yazici H, Webster TJ (2017) pH-controlled cerium oxide nanoparticle inhibition of both gram-positive and gram-negative bacteria growth. Sci Rep 7:45859PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Zhang BG, Myers DE, Wallace GG, Brandt M, Choong PF (2014) Bioactive coatings for orthopaedic implants-recent trends in development of implant coatings. Int J Mol Sci 15(7):11878–11921PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Gupta A, Landis RF, Li C-H, Schnurr M, Das R, Lee Y-W et al (2018) Engineered polymer nanoparticles with unprecedented antimicrobial efficacy and therapeutic indices against multidrug-resistant bacteria and biofilms. J Am Chem Soc 140(38):12137–12143PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Rai M, Yadav A, Gade A (2009) Silver nanoparticles as a new generation of antimicrobials. Biotechnol Adv 27(1):76–83CrossRefGoogle Scholar
  87. 87.
    Le Ouay B, Stellacci F (2015) Antibacterial activity of silver nanoparticles: a surface science insight. Nano Today 10(3):339–354CrossRefGoogle Scholar
  88. 88.
    Chaloupka K, Malam Y, Seifalian AM (2010) Nanosilver as a new generation of nanoproduct in biomedical applications. Trends Biotechnol 28(11):580–588PubMedCrossRefGoogle Scholar
  89. 89.
    Qin H, Zhu C, An Z, Jiang Y, Zhao Y, Wang J et al (2014) Silver nanoparticles promote osteogenic differentiation of human urine-derived stem cells at noncytotoxic concentrations. Int J Nanomedicine 9:2469–2478PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Mahmood M, Li Z, Casciano D, Khodakovskaya MV, Chen T, Karmakar A et al (2011) Nanostructural materials increase mineralization in bone cells and affect gene expression through miRNA regulation. J Cell Mol Med 15(11):2297–2306PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Sportelli MC, Izzi M, Volpe A, Clemente M, Picca RA, Ancona A et al (2018) The pros and cons of the use of laser ablation synthesis for the production of silver nano-antimicrobials. Antibiotics (Basel) 7(3):67CrossRefGoogle Scholar
  92. 92.
    Loo YY, Rukayadi Y, Nor-Khaizura M-A-R, Kuan CH, Chieng BW, Nishibuchi M, Radu S (2018) In vitro antimicrobial activity of green synthesized silver nanoparticles against selected gram-negative foodborne pathogens. Front Microbiol 9:1555PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Huma Z-e, Gupta A, Javed I, Das R, Hussain SZ, Mumtaz S et al (2018) Cationic silver nanoclusters as potent antimicrobials against multidrug-resistant bacteria. ACS Omega 3(12):16721–16727PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Panáček A, Kvítek L, Smékalová M, Večeřová R, Kolář M, Röderová M et al (2018) Bacterial resistance to silver nanoparticles and how to overcome it. Nat Nanotechnol 13(1):65–71PubMedCrossRefGoogle Scholar
  95. 95.
    Pareek V, Gupta R, Panwar J (2018) Do physico-chemical properties of silver nanoparticles decide their interaction with biological media and bactericidal action? A review. Mater Sci Eng C 90(11):739–749CrossRefGoogle Scholar
  96. 96.
    Patil MP, Kim G-D (2017) Eco-friendly approach for nanoparticles synthesis and mechanism behind antibacterial activity of silver and anticancer activity of gold nanoparticles. Appl Microbiol Biotechnol 101(1):79–92PubMedCrossRefGoogle Scholar
  97. 97.
    Hosnedlova B, Kepinska M, Skalickova S, Fernandez C, Ruttkay-Nedecky B, Peng Q et al (2018) Nano-selenium and its nanomedicine applications: a critical review. Int J Nanomedicine 13:2107–2128PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Stolzoff M, Wang S, Webster T (eds) (2016) Efficacy and mechanism of selenium nanoparticles as antibacterial agents. In: Front. bioeng. biotechnol. conference abstract: 10th world biomaterials congress.  https://doi.org/10.3389/conf.FBIOE.2016.01.01826
  99. 99.
    Srivastava N, Mukhopadhyay M (2015) Green synthesis and structural characterization of selenium nanoparticles and assessment of their antimicrobial property. Bioprocess Biosyst Eng 38(9):1723–1730PubMedCrossRefGoogle Scholar
  100. 100.
    Shoeibi S, Mashreghi M (2017) Biosynthesis of selenium nanoparticles using Enterococcus faecalis and evaluation of their antibacterial activities. J Trace Elem Med Biol 39:135–139PubMedCrossRefGoogle Scholar
  101. 101.
    Huang X, Chen X, Chen Q, Yu Q, Sun D, Liu J (2016) Investigation of functional selenium nanoparticles as potent antimicrobial agents against superbugs. Acta Biomater 30:397–407PubMedCrossRefGoogle Scholar
  102. 102.
    Wang Q, Webster TJ (2012) Nanostructured selenium for preventing biofilm formation on polycarbonate medical devices. J Biomed Mater Res Part A 100(12):3205–3210CrossRefGoogle Scholar
  103. 103.
    Farias IAP, dos Santos CCL, Sampaio FC (2018) Antimicrobial activity of cerium oxide nanoparticles on opportunistic microorganisms: a systematic review. Biomed Res Int 2018:1CrossRefGoogle Scholar
  104. 104.
    Li S, Dong S, Xu W, Tu S, Yan L, Zhao C et al (2018) Antibacterial hydrogels. Adv Sci 5(5):1700527CrossRefGoogle Scholar
  105. 105.
    Jain A, Duvvuri LS, Farah S, Beyth N, Domb AJ, Khan W (2014) Antimicrobial polymers. Adv Healthc Mater 3(12):1969–1985PubMedCrossRefGoogle Scholar
  106. 106.
    Yang Y, Cai Z, Huang Z, Tang X, Zhang X (2018) Antimicrobial cationic polymers: from structural design to functional control. Polym J 50(1):33–44CrossRefGoogle Scholar
  107. 107.
    Du H, Wang Y, Yao X, Luo Q, Zhu W, Li X et al (2016) Injectable cationic hydrogels with high antibacterial activity and low toxicity. Polym Chem 7(36):5620–5624CrossRefGoogle Scholar
  108. 108.
    Hosseinnejad M, Jafari SM (2016) Evaluation of different factors affecting antimicrobial properties of chitosan. Int J Biol Macromol 85:467–475PubMedCrossRefGoogle Scholar
  109. 109.
    Rinaudo M (2006) Chitin and chitosan: properties and applications. Prog Polym Sci 31(7):603–632CrossRefGoogle Scholar
  110. 110.
    Muñoz-Bonilla A, Fernández-García M (2012) Polymeric materials with antimicrobial activity. Prog Polym Sci 37(2):281–339CrossRefGoogle Scholar
  111. 111.
    Cheah WY, Show P-L, Ng IS, Lin G-Y, Chiu C-Y, Chang Y-K (2019) Antibacterial activity of quaternized chitosan modified nanofiber membrane. Int J Biol Macromol 126:569–577PubMedCrossRefGoogle Scholar
  112. 112.
    Ignatova M, Starbova K, Markova N, Manolova N, Rashkov I (2006) Electrospun nano-fibre mats with antibacterial properties from quaternised chitosan and poly(vinyl alcohol). Carbohydr Res 341(12):2098–2107PubMedCrossRefGoogle Scholar
  113. 113.
    Sajomsang W, Gonil P, Tantayanon S (2009) Antibacterial activity of quaternary ammonium chitosan containing mono or disaccharide moieties: preparation and characterization. Int J Biol Macromol 44(5):419–427PubMedCrossRefGoogle Scholar
  114. 114.
    Wang D (2016) Osteoinductive and antibacterial biomaterials for bone tissue engineering. Dissertation, Vrije Universiteit AmsterdamGoogle Scholar
  115. 115.
    Goy RC, Britto D, Assis OBG (2009) A review of the antimicrobial activity of chitosan. Polímeros 19(3):241–247CrossRefGoogle Scholar
  116. 116.
    Rabea EI, Badawy MET, Stevens CV, Smagghe G, Steurbaut W (2003) Chitosan as antimicrobial agent: applications and mode of action. Biomacromolecules 4(6):1457–1465PubMedCrossRefGoogle Scholar
  117. 117.
    Raafat D, Sahl HG (2009) Chitosan and its antimicrobial potential—a critical literature survey. Microb Biotechnol 2(2):186–201PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Eckhard LH, Sol A, Abtew E, Shai Y, Domb AJ, Bachrach G et al (2014) Biohybrid polymer-antimicrobial peptide medium against Enterococcus faecalis. PLoS One 9(10):e109413PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Chen Q, Ma Z, Liu G, Wei H, Xie X (2016) Antibacterial activity of cationic cyclen-functionalized fullerene derivatives: membrane stress. Dig J Nanomater Bios 11:753–761Google Scholar
  120. 120.
    Medeiros SJ, Oliveira AM, de Carvalho JO, Ricci R, Martins MCC, Rodrigues BV et al (2018) Nanohydroxyapatite/graphene nanoribbons nanocomposites induce in vitro osteogenesis and promote in vivo bone neoformation. ACS Biomater Sci Eng 4(5):1580–1590Google Scholar
  121. 121.
    Siqueira IA, Corat MAF, Cavalcanti BN, Neto WAR, Martin AA, Bretas RES et al (2015) In vitro and in vivo studies of novel poly (D, L-lactic acid), superhydrophilic carbon nanotubes, and nanohydroxyapatite scaffolds for bone regeneration. ACS Appl Mater Interfaces 7(18):9385–9398PubMedCrossRefGoogle Scholar
  122. 122.
    Van Noorden R (2011) Chemistry: the trials of new carbon. Nature 469(7328):14–16PubMedCrossRefGoogle Scholar
  123. 123.
    Mocan T, Matea CT, Pop T, Mosteanu O, Buzoianu AD, Suciu S et al (2017) Carbon nanotubes as anti-bacterial agents. Cell Mol Life Sci 74(19):3467–3479PubMedCrossRefGoogle Scholar
  124. 124.
    Aslan S, Loebick CZ, Kang S, Elimelech M, Pfefferle LD, Van Tassel PR (2010) Antimicrobial biomaterials based on carbon nanotubes dispersed in poly (lactic-co-glycolic acid). Nanoscale 2(9):1789–1794PubMedCrossRefGoogle Scholar
  125. 125.
    Dizaj SM, Mennati A, Jafari S, Khezri K, Adibkia K (2015) Antimicrobial activity of carbon-based nanoparticles. Adv Pharm Bull 5(1):19–23Google Scholar
  126. 126.
    Gurunathan S, Han JW, Dayem AA, Eppakayala V, Kim J-H (2012) Oxidative stress-mediated antibacterial activity of graphene oxide and reduced graphene oxide in Pseudomonas aeruginosa. Int J Nanomed 7:5901–5914CrossRefGoogle Scholar
  127. 127.
    Ricci R, Leite N, Da-Silva N, Pacheco-Soares C, Canevari R, Marciano F et al (2017) Graphene oxide nanoribbons as nanomaterial for bone regeneration: effects on cytotoxicity, gene expression and bactericidal effect. Mater Sci Eng C 78:341–348CrossRefGoogle Scholar
  128. 128.
    Zhao C, Deng B, Chen G, Lei B, Hua H, Peng H et al (2016) Large-area chemical vapor deposition-grown monolayer graphene-wrapped silver nanowires for broad-spectrum and robust antimicrobial coating. Nano Res 9(4):963–973CrossRefGoogle Scholar
  129. 129.
    Rodrigues BV, Leite NC, das Neves Cavalcanti B, da Silva NS, Marciano FR, Corat EJ et al (2016) Graphene oxide/multi-walled carbon nanotubes as nanofeatured scaffolds for the assisted deposition of nanohydroxyapatite: characterization and biological evaluation. Int J Nanomedicine 11:2569–2585PubMedPubMedCentralGoogle Scholar
  130. 130.
    Lochab B, Shukla S, Varma IK (2014) Naturally occurring phenolic sources: monomers and polymers. RSC Adv 4(42):21712–21752CrossRefGoogle Scholar
  131. 131.
    Upton BM, Kasko AM (2016) Strategies for the conversion of lignin to high-value polymeric materials: review and perspective. Chem Rev 116(4):2275–2306PubMedCrossRefGoogle Scholar
  132. 132.
    Dong X, Dong M, Lu Y, Turley A, Jin T, Wu C (2011) Antimicrobial and antioxidant activities of lignin from residue of corn stover to ethanol production. Ind Crop Prod 34(3):1629–1634CrossRefGoogle Scholar
  133. 133.
    Erakovic S, Jankovic A, Tsui GCP, Tang C-Y, Miskovic-Stankovic V, Stevanovic T (2014) Novel bioactive antimicrobial lignin containing coatings on titanium obtained by electrophoretic deposition. Int J Mol Sci 15(7):12294–12322PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Chung K-T, Wong TY, Wei C-I, Huang Y-W, Lin Y (1998) Tannins and human health: a review. Crit Rev Food Sci Nutr 38(6):421–464PubMedCrossRefGoogle Scholar
  135. 135.
    Park JH, Choi S, Moon HC, Seo H, Kim JY, Hong S-P et al (2017) Antimicrobial spray nanocoating of supramolecular Fe(III)-tannic acid metal-organic coordination complex: applications to shoe insoles and fruits. Sci Rep 7(1):6980PubMedPubMedCentralCrossRefGoogle Scholar
  136. 136.
    Sarjit A, Wang Y, Dykes GA (2015) Antimicrobial activity of gallic acid against thermophilic campylobacter is strain specific and associated with a loss of calcium ions. Food Microbiol 46:227–233PubMedCrossRefGoogle Scholar
  137. 137.
    Arbenz A, Averous L (2015) Chemical modification of tannins to elaborate aromatic biobased macromolecular architectures. Green Chem 17(5):2626–2646CrossRefGoogle Scholar
  138. 138.
    Redondo LM, Chacana PA, Dominguez JE, Fernandez Miyakawa ME (2014) Perspectives in the use of tannins as alternative to antimicrobial growth promoter factors in poultry. Front Microbiol 5:118PubMedPubMedCentralCrossRefGoogle Scholar
  139. 139.
    Daglia M (2012) Polyphenols as antimicrobial agents. Curr Opin Biotechnol 23(2):174–181PubMedCrossRefGoogle Scholar
  140. 140.
    Papuc C, Goran GV, Predescu CN, Nicorescu V, Stefan G (2017) Plant polyphenols as antioxidant and antibacterial agents for shelf-life extension of meat and meat products: classification, structures, sources, and action mechanisms. Compr Rev Food Sci Food Saf 16(6):1243–1268CrossRefGoogle Scholar
  141. 141.
    Ahn BK (2017) Perspectives on mussel-inspired wet adhesion. J Am Chem Soc 139(30):10166–10171PubMedCrossRefGoogle Scholar
  142. 142.
    Habibovic P, de Groot K (2007) Osteoinductive biomaterials—properties and relevance in bone repair. J Tissue Eng Regen Med 1(1):25–32PubMedCrossRefGoogle Scholar
  143. 143.
    Zhu Y, Zhang K, Zhao R, Ye X, Chen X, Xiao Z et al (2017) Bone regeneration with micro/nano hybrid-structured biphasic calcium phosphate bioceramics at segmental bone defect and the induced immunoregulation of MSCs. Biomaterials 147:133–144PubMedCrossRefGoogle Scholar
  144. 144.
    Barradas A, Yuan H, van Blitterswijk CA, Habibovic P (2011) Osteoinductive biomaterials: current knowledge of properties, experimental models and biological mechanisms. Eur Cell Mater 21:407–429PubMedCrossRefGoogle Scholar
  145. 145.
    Holzwarth JM, Ma PX (2011) Biomimetic nanofibrous scaffolds for bone tissue engineering. Biomaterials 32(36):9622–9629PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    Webster TJ, Massa-Schlueter EA, Smith JL, Slamovich EB (2004) Osteoblast response to hydroxyapatite doped with divalent and trivalent cations. Biomaterials 25(11):2111–2121PubMedCrossRefGoogle Scholar
  147. 147.
    LeGeros RZ (2008) Calcium phosphate-based osteoinductive materials. Chem Rev 108(11):4742–4753PubMedPubMedCentralCrossRefGoogle Scholar
  148. 148.
    Rahaman MN, Day DE, Bal BS, Fu Q, Jung SB, Bonewald LF et al (2011) Bioactive glass in tissue engineering. Acta Biomater 7(6):2355–2373PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    Roseti L, Parisi V, Petretta M, Cavallo C, Desando G, Bartolotti I et al (2017) Scaffolds for bone tissue engineering: state of the art and new perspectives. Mater Sci Eng C 78:1246–1262CrossRefGoogle Scholar
  150. 150.
    Caballero SSR, Saiz E, Montembault A, Tadier S, Maire E, David L et al (2019) 3-D printing of chitosan-calcium phosphate inks: rheology, interactions and characterization. J Mater Sci Mater Med 30(1):6CrossRefGoogle Scholar
  151. 151.
    Iviglia G, Morra M, Cassinelli C, Torre E, Rodriguez Y, Baena R (2018) New collagen-coated calcium phosphate synthetic bone filler (Synergoss®): a comparative surface analysis. Int J Appl Ceram Technol 15(4):910–920CrossRefGoogle Scholar
  152. 152.
    Inzana JA, Olvera D, Fuller SM, Kelly JP, Graeve OA, Schwarz EM et al (2014) 3D printing of composite calcium phosphate and collagen scaffolds for bone regeneration. Biomaterials 35(13):4026–4034PubMedPubMedCentralCrossRefGoogle Scholar
  153. 153.
    Gao X, Song J, Ji P, Zhang X, Li X, Xu X et al (2016) Polydopamine-templated hydroxyapatite reinforced polycaprolactone composite nanofibers with enhanced cytocompatibility and osteogenesis for bone tissue engineering. ACS Appl Mater Interfaces 8(5):3499–3515PubMedCrossRefPubMedCentralGoogle Scholar
  154. 154.
    Li H, Chang J (2005) pH-compensation effect of bioactive inorganic fillers on the degradation of PLGA. Compos Sci Technol 65(14):2226–2232CrossRefGoogle Scholar
  155. 155.
    Stevanović M, Filipović N, Djurdjević J, Lukić M, Milenković M, Boccaccini A (2015) 45S5Bioglass®-based scaffolds coated with selenium nanoparticles or with poly (lactide-co-glycolide)/selenium particles: processing, evaluation and antibacterial activity. Colloids Surf B Biointerfaces 132:208–215PubMedCrossRefPubMedCentralGoogle Scholar
  156. 156.
    Li A, Ren H, Cui Y, Wang C, Zhou X, Lin H et al (2017) Detailed structure of a new bioactive glass composition for the design of bone repair materials. J Non-Cryst Solids 475:10–14CrossRefGoogle Scholar
  157. 157.
    Sarin S, Rekhi A (2016) Bioactive glass: a potential next generation biomaterial. SRM J Res Dent Sci 7(1):27–32CrossRefGoogle Scholar
  158. 158.
    El-Rashidy AA, Roether JA, Harhaus L, Kneser U, Boccaccini AR (2017) Regenerating bone with bioactive glass scaffolds: a review of in vivo studies in bone defect models. Acta Biomater 62:1–28PubMedCrossRefPubMedCentralGoogle Scholar
  159. 159.
    Jones JR (2013) Review of bioactive glass: from Hench to hybrids. Acta Biomater 9(1):4457–4486PubMedCrossRefPubMedCentralGoogle Scholar
  160. 160.
    Chen QZ, Thompson ID, Boccaccini AR (2006) 45S5 Bioglass®-derived glass–ceramic scaffolds for bone tissue engineering. Biomaterials 27(11):2414–2425PubMedCrossRefPubMedCentralGoogle Scholar
  161. 161.
    Kargozar S, Baino F, Hamzehlou S, Hill RG, Mozafari M (2018) Bioactive glasses: sprouting angiogenesis in tissue engineering. Trends Biotechnol 36(4):430–444PubMedCrossRefPubMedCentralGoogle Scholar
  162. 162.
    Jones JR, Brauer DS, Hupa L, Greenspan DC (2016) Bioglass and bioactive glasses and their impact on healthcare. Int J Appl Glas Sci 7(4):423–434CrossRefGoogle Scholar
  163. 163.
    Sheikhi A, Afewerki S, Oklu R, Gaharwar AK, Khademhosseini A (2018) Effect of ionic strength on shear-thinning nanoclay–polymer composite hydrogels. Biomater Sci 6:2073–2083PubMedPubMedCentralCrossRefGoogle Scholar
  164. 164.
    Hoppe A, Güldal NS, Boccaccini AR (2011) A review of the biological response to ionic dissolution products from bioactive glasses and glass-ceramics. Biomaterials 32(11):2757–2774PubMedCrossRefGoogle Scholar
  165. 165.
    Valliant EM, Romer F, Wang D, McPhail DS, Smith ME, Hanna JV et al (2013) Bioactivity in silica/poly (γ-glutamic acid) sol–gel hybrids through calcium chelation. Acta Biomater 9(8):7662–7671PubMedCrossRefGoogle Scholar
  166. 166.
    Catauro M, Bollino F, Papale F (2018) Surface modifications of titanium implants by coating with bioactive and biocompatible poly (ε-caprolactone)/SiO2 hybrids synthesized via sol–gel. Arab J Chem 11(7):1126–1133CrossRefGoogle Scholar
  167. 167.
    Hickey DJ, Ercan B, Sun L, Webster TJ (2015) Adding MgO nanoparticles to hydroxyapatite–PLLA nanocomposites for improved bone tissue engineering applications. Acta Biomater 14:175–184PubMedCrossRefGoogle Scholar
  168. 168.
    Webster TJ, Ergun C, Doremus RH, Bizios R (2002) Hydroxylapatite with substituted magnesium, zinc, cadmium, and yttrium. II. Mechanisms of osteoblast adhesion. J Biomed Mater Res 59(2):312–317PubMedCrossRefGoogle Scholar
  169. 169.
    Querido W, Rossi AL, Farina M (2016) The effects of strontium on bone mineral: a review on current knowledge and microanalytical approaches. Micron 80:122–134CrossRefGoogle Scholar
  170. 170.
    Yang F, Yang D, Tu J, Zheng Q, Cai L, Wang L (2011) Strontium enhances osteogenic differentiation of mesenchymal stem cells and in vivo bone formation by activating Wnt/catenin signaling. Stem Cells 29(6):981–991CrossRefGoogle Scholar
  171. 171.
    Lemaire-Hurtel A-S, Mentaverri R, Caudrillier A, Cournarie F, Wattel A, Kamel S et al (2009) The calcium-sensing receptor is involved in strontium ranelate-induced osteoclast apoptosis. New insights into the associated signaling pathways. J Biol Chem 284(1):575–584CrossRefGoogle Scholar
  172. 172.
    Fiorilli S, Molino G, Pontremoli C, Iviglia G, Torre E, Cassinelli C et al (2018) The incorporation of strontium to improve bone-regeneration ability of mesoporous bioactive glasses. Materials 11(5):678PubMedCentralCrossRefPubMedGoogle Scholar
  173. 173.
    Kannan S, Pina S, Ferreira JMF (2006) Formation of strontium-stabilized β-tricalcium phosphate from calcium-deficient apatite. J Am Ceram Soc 89(10):3277–3280CrossRefGoogle Scholar
  174. 174.
    Oryan A, Baghaban Eslaminejad M, Kamali A, Hosseini S, Sayahpour FA, Baharvand H (2019) Synergistic effect of strontium, bioactive glass and nano-hydroxyapatite promotes bone regeneration of critical-sized radial bone defects. J Biomed Mater Res B Appl Biomater 107(1):50–64PubMedCrossRefGoogle Scholar
  175. 175.
    Zeng H, Cao J (2013) Selenium in bone health: roles in antioxidant protection and cell proliferation. Nutrients 5:97–110PubMedPubMedCentralCrossRefGoogle Scholar
  176. 176.
    Ebert R, Ulmer M, Zeck S, Meissner-Weigl J, Schneider D, Stopper H et al (2006) Selenium supplementation restores the antioxidative capacity and prevents cell damage in bone marrow stromal cells in vitro. Stem Cells 24(5):1226–1235PubMedCrossRefGoogle Scholar
  177. 177.
    Liu H, Bian W, Liu S, Huang K (2012) Selenium protects bone marrow stromal cells against hydrogen peroxide-induced inhibition of osteoblastic differentiation by suppressing oxidative stress and ERK signaling pathway. Biol Trace Elem Res 150(1):441–450PubMedCrossRefGoogle Scholar
  178. 178.
    Dollwet HHA, Sorenson JRJ (1988) Roles of copper in bone maintenance and healing. Biol Trace Elem Res 18(1):39–48PubMedCrossRefGoogle Scholar
  179. 179.
    Shi M, Chen Z, Farnaghi S, Friis T, Mao X, Xiao Y et al (2016) Copper-doped mesoporous silica nanospheres, a promising immunomodulatory agent for inducing osteogenesis. Acta Biomater 30:334–344PubMedCrossRefGoogle Scholar
  180. 180.
    Li X, He Q, Shi J (2014) Global gene expression analysis of cellular death mechanisms induced by mesoporous silica nanoparticle-based drug delivery system. ACS Nano 8(2):1309–1320PubMedCrossRefGoogle Scholar
  181. 181.
    Vukicevic S, Sampath KT (2002) Bone morphogenetic proteins: from laboratory to clinical practice, 1st edn. Birkhäuser, BaselCrossRefGoogle Scholar
  182. 182.
    Ho-Shui-Ling A, Bolander J, Rustom LE, Johnson AW, Luyten FP, Picart C (2018) Bone regeneration strategies: engineered scaffolds, bioactive molecules and stem cells current stage and future perspectives. Biomaterials 180:143–162PubMedPubMedCentralCrossRefGoogle Scholar
  183. 183.
    Lombardi G, Di CS, Rubino M, Faggiano A, Vuolo L, Guerra E et al (2011) The roles of parathyroid hormone in bone remodeling: prospects for novel therapeutics. J Endocrinol Investig 34(7 Suppl):18–22Google Scholar
  184. 184.
    Jung RE, Hämmerle CH, Kokovic V, Weber FE (2007) Bone regeneration using a synthetic matrix containing a parathyroid hormone peptide combined with a grafting material. Int J Oral Maxillofac Implants 22(2):258–266Google Scholar
  185. 185.
    Johnson CT, García AJ (2015) Scaffold-based anti-infection strategies in bone repair. Ann Biomed Eng 43(3):515–528PubMedCrossRefGoogle Scholar
  186. 186.
    Salles GN, Calió ML, Afewerki S, Pacheco-Soares C, Porcionatto M, Hölscher C et al (2018) Prolonged drug-releasing fibers attenuate Alzheimer’s disease-like pathogenesis. ACS Appl Mater Interfaces 10(43):36693–36702PubMedCrossRefGoogle Scholar
  187. 187.
    Lobo AO, Afewerki S, de Paula MMM, Ghannadian P, Marciano FR, Zhang YS et al (2018) Electrospun nanofiber blend with improved mechanical and biological performance. Int J Nanomedicine 13:7891–7903PubMedPubMedCentralCrossRefGoogle Scholar
  188. 188.
    De Paula MMM, Bassous NJ, Afewerki S, Harb SV, Ghannadian P, Marciano FR et al (2018) Understanding the impact of crosslinked PCL/PEG/GelMA electrospun nanofibers on bactericidal activity. PLoS One 13(12):e0209386PubMedPubMedCentralCrossRefGoogle Scholar
  189. 189.
    Wang Y, Jiang Y, Zhang Y, Wen S, Wang Y, Zhang H (2019) Dual functional electrospun core-shell nanofibers for anti-infective guided bone regeneration membranes. Mater Sci Eng C 98:134–139CrossRefGoogle Scholar
  190. 190.
    Shi L, Zhang W, Yang K, Shi H, Li D, Liu J et al (2015) Antibacterial and osteoinductive capability of orthopedic materials via cation–π interaction mediated positive charge. J Mater Chem B 3(5):733–737CrossRefGoogle Scholar
  191. 191.
    Yang G, Yang H, Shi L, Wang T, Zhou W, Zhou T et al (2018) Enhancing corrosion resistance, osteoinduction, and antibacterial properties by Zn/Sr additional surface modification of magnesium alloy. ACS Biomater Sci Eng 4(12):4289–4298CrossRefGoogle Scholar
  192. 192.
    Kumar S, Bose S, Chatterjee K (2014) Amine-functionalized multiwall carbon nanotubes impart osteoinductive and bactericidal properties in poly(ε-caprolactone) composites. RSC Adv 4(37):19086–19098CrossRefGoogle Scholar
  193. 193.
    Zhang Y, Dong C, Yang S, Chiu T-W, Wu J, Xiao K et al (2018) Enhanced silver loaded antibacterial titanium implant coating with novel hierarchical effect. J Biomater Appl 32(9):1289–1299PubMedCrossRefGoogle Scholar
  194. 194.
    Qian X, Qing F, Jun O, Hong S (2014) Construction of drug-loaded titanium implants via layer-by-layer electrostatic self-assembly. West China J Stomatol 32:537–541Google Scholar
  195. 195.
    Xu C, Lei C, Meng L, Wang C, Song Y (2012) Chitosan as a barrier membrane material in periodontal tissue regeneration. J Biomed Mater Res B Appl Biomater 100(5):1435–1443PubMedCrossRefGoogle Scholar
  196. 196.
    Li W, Ding Y, Yu S, Yao Q, Boccaccini AR (2015) Multifunctional chitosan-45S5 bioactive glass-poly(3-hydroxybutyrate-co-3-hydroxyvalerate) microsphere composite membranes for guided tissue/bone regeneration. ACS Appl Mater Interfaces 7(37):20845–20854PubMedCrossRefGoogle Scholar
  197. 197.
    Zhou P, Xia Y, Cheng X, Wang P, Xie Y, Xu S (2014) Enhanced bone tissue regeneration by antibacterial and osteoinductive silica-HACC-zein composite scaffolds loaded with rhBMP-2. Biomaterials 35(38):10033–10045PubMedPubMedCentralCrossRefGoogle Scholar
  198. 198.
    Nasajpour A, Ansari S, Rinoldi C, Shahrokhi Rad A, Aghaloo T, Ryon Shin S et al (2018) A multifunctional polymeric periodontal membrane with osteogenic and antibacterial characteristics. Adv Funct Mater 28:1703437CrossRefGoogle Scholar
  199. 199.
    Wei C-K, Ding S-J (2017) Dual-functional bone implants with antibacterial ability and osteogenic activity. J Mater Chem B 5(10):1943–1953CrossRefGoogle Scholar
  200. 200.
    Bergemann C, Zaatreh S, Wegner K, Arndt K, Podbielski A, Bader R et al (2017) Copper as an alternative antimicrobial coating for implants—an in vitro study. World J Transplant 7(3):193–202PubMedPubMedCentralCrossRefGoogle Scholar
  201. 201.
    Lemire JA, Harrison JJ, Turner RJ (2013) Antimicrobial activity of metals: mechanisms, molecular targets and applications. Nat Rev Microbiol 11(6):371–384PubMedCrossRefGoogle Scholar
  202. 202.
    Zheng Z, Yin W, Zara JN, Li W, Kwak J, Mamidi R et al (2010) The use of BMP-2 coupled—nanosilver-PLGA composite grafts to induce bone repair in grossly infected segmental defects. Biomaterials 31(35):9293–9300PubMedPubMedCentralCrossRefGoogle Scholar
  203. 203.
    Liu Y, Zheng Z, Zara JN, Hsu C, Soofer DE, Lee KS et al (2012) The antimicrobial and osteoinductive properties of silver nanoparticle/poly (DL-lactic-co-glycolic acid)-coated stainless steel. Biomaterials 33(34):8745–8756CrossRefGoogle Scholar
  204. 204.
    Stevanović M, Uskoković V, Filipović M, Škapin SD, Uskoković D (2013) Composite PLGA/AgNpPGA/AscH nanospheres with combined osteoinductive, antioxidative, and antimicrobial activities. ACS Appl Mater Interfaces 5(18):9034–9042PubMedPubMedCentralCrossRefGoogle Scholar
  205. 205.
    Sun CY, Che YJ, Lu SJ (2015) Preparation and application of collagen scaffold-encapsulated silver nanoparticles and bone morphogenetic protein 2 for enhancing the repair of infected bone. Biotechnol Lett 37(2):467–473PubMedPubMedCentralCrossRefGoogle Scholar
  206. 206.
    Pacheco H, Vedantham K, Aniket, Young A, Marriott I, El-Ghannam A (2014) Tissue engineering scaffold for sequential release of vancomycin and rhBMP2 to treat bone infections. J Biomed Mater Res A 102(12):4213–4223PubMedGoogle Scholar
  207. 207.
    Wang Y, Wang X, Li H, Xue D, Shi Z, Qi Y et al (2011) Assessing the character of the rhBMP-2- and vancomycin-loaded calcium sulphate composites in vitro and in vivo. Arch Orthop Trauma Surg 131(7):991–1001CrossRefGoogle Scholar
  208. 208.
    Li X, Xu J, Filion TM, Ayers DC, Song J (2013) pHEMA-nHA encapsulation and delivery of vancomycin and rhBMP-2 enhances its role as a bone graft substitute. Clin Orthop Relat Res 471(8):2540–2547PubMedCrossRefGoogle Scholar
  209. 209.
    Guelcher SA, Brown KV, Li B, Guda T, Lee B-H, Wenke JC (2011) Dual-purpose bone grafts improve healing and reduce infection. J Orthop Trauma 25(8):477–482PubMedCrossRefGoogle Scholar
  210. 210.
    Neoh KG, Hu X, Zheng D, Kang ET (2012) Balancing osteoblast functions and bacterial adhesion on functionalized titanium surfaces. Biomaterials 33(10):2813–2822PubMedCrossRefGoogle Scholar
  211. 211.
    Cheng H, Xiong W, Fang Z, Guan H, Wu W, Li Y et al (2016) Strontium (Sr) and silver (Ag) loaded nanotubular structures with combined osteoinductive and antimicrobial activities. Acta Biomater 31:388–400CrossRefGoogle Scholar
  212. 212.
    Bose S, Banerjee D, Bandyopadhyay A (2017) Chapter 1—Introduction to biomaterials and devices for bone disorders. In: Bose S, Bandyopadhyay A (eds) Materials for bone disorders. Academic, New York, pp 1–27Google Scholar
  213. 213.
    Anastas PT, Warner JC (1998) Green chemistry: theory and practice. Oxford University Press, OxfordGoogle Scholar
  214. 214.
    Anastas P, Eghbali N (2010) Green chemistry: principles and practice. Chem Soc Rev 39(1):301–312PubMedCrossRefGoogle Scholar
  215. 215.
    Kiran A, Kumar T, Sanghavi R, Doble M, Ramakrishna S (2018) Antibacterial and bioactive surface modifications of titanium implants by PCL/TiO2 nanocomposite coatings. Nanomaterials. 8(10):860PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Samson Afewerki
    • 1
    • 2
  • Nicole Bassous
    • 3
  • Samarah Harb
    • 4
  • Carlos Palo-Nieto
    • 5
  • Guillermo U. Ruiz-Esparza
    • 1
    • 2
  • Fernanda R. Marciano
    • 6
  • Thomas Webster
    • 3
  • Anderson Oliveira Lobo
    • 7
    Email author
  1. 1.Division of Engineering in Medicine, Department of MedicineHarvard Medical School, Brigham & Women’s HospitalCambridgeUSA
  2. 2.Harvard-MIT Division of Health Science and Technology, Massachusetts Institute of Technology, MITCambridgeUSA
  3. 3.Nanomedicine Laboratory, Department of Chemical EngineeringNortheastern UniversityBostonUSA
  4. 4.Institute of ChemistrySão Paulo State UniversityAraraquaraBrazil
  5. 5.Department of Medicinal Chemistry, BMCUppsala UniversityUppsalaSweden
  6. 6.Department of PhysicsUFPI—Federal University of PiauíTeresinaBrazil
  7. 7.LIMAV—Interdisciplinary Laboratory for Advanced Materials, Department of Materials EngineeringUFPI—Federal University of PiauíTeresinaBrazil

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