Hydroxyapatite Thin Films of Marine Origin as Sustainable Candidates for Dental Implants

Novel biomaterials with promising bone regeneration potential, derived from rich, renewable, and cheap sources, are reported. Thus, thin films were synthesized from marine-derived (i.e., from fish bones and seashells) hydroxyapatite (MdHA) by pulsed laser deposition (PLD) technique. Besides the physical–chemical and mechanical investigations, the deposited thin films were also evaluated in vitro using dedicated cytocompatibility and antimicrobial assays. The morphological examination of MdHA films revealed the fabrication of rough surfaces, which were shown to favor good cell adhesion, and furthermore could foster the in-situ anchorage of implants. The strong hydrophilic behavior of the thin films was evidenced by contact angle (CA) measurements, with values in the range of 15–18°. The inferred bonding strength adherence values were superior (i.e., ~49 MPa) to the threshold established by ISO regulation for high-load implant coatings. After immersion in biological fluids, the growth of an apatite-based layer was noted, which indicated the good mineralization capacity of the MdHA films. All PLD films exhibited low cytotoxicity on osteoblast, fibroblast, and epithelial cells. Moreover, a persistent protective effect against bacterial and fungal colonization (i.e., 1- to 3-log reduction of E. coli, E. faecalis, and C. albicans growth) was demonstrated after 48 h of incubation, with respect to the Ti control. The good cytocompatibility and effective antimicrobial activity, along with the reduced fabrication costs from sustainable sources (available in large quantities), should, therefore, recommend the MdHA materials proposed herein as innovative and viable solutions for the development of novel coatings for metallic dental implants.

[1]  N. Ekren,et al.  Marine-derived bioceramics for orthopedic, reconstructive and dental surgery applications , 2022, Journal of the Australian Ceramic Society.

[2]  A. Scribante,et al.  Customized Minimally Invasive Protocols for the Clinical and Microbiological Management of the Oral Microbiota , 2022, Microorganisms.

[3]  Jianzhang Liu,et al.  Microbiological and clinical evaluation of ultrasonic debridement with/without erythritol air polishing during supportive periodontal therapy in arches with full-arch fixed implant-supported prostheses: protocol for a randomised controlled trial , 2021, BMJ Open.

[4]  L. Duta,et al.  A Review on Biphasic Calcium Phosphate Materials Derived from Fish Discards , 2021, Nanomaterials.

[5]  A. Scribante,et al.  SEM/EDS Evaluation of the Mineral Deposition on a Polymeric Composite Resin of a Toothpaste Containing Biomimetic Zn-Carbonate Hydroxyapatite (microRepair®) in Oral Environment: A Randomized Clinical Trial , 2021, Polymers.

[6]  R. Teghil,et al.  Substituted Hydroxyapatite, Glass, and Glass-Ceramic Thin Films Deposited by Nanosecond Pulsed Laser Deposition (PLD) for Biomedical Applications: A Systematic Review , 2021, Coatings.

[7]  I. Mihailescu,et al.  Fish Bone Derived Bi-Phasic Calcium Phosphate Coatings Fabricated by Pulsed Laser Deposition for Biomedical Applications , 2020, Marine drugs.

[8]  L. Wolff,et al.  Peri-Implant Diseases: Diagnosis, Clinical, Histological, Microbiological Characteristics and Treatment Strategies. A Narrative Review , 2020, Antibiotics.

[9]  D. Chioibasu,et al.  In Vivo Assessment of Bone Enhancement in the Case of 3D-Printed Implants Functionalized with Lithium-Doped Biological-Derived Hydroxyapatite Coatings: A Preliminary Study on Rabbits , 2020, Coatings.

[10]  D. Vranceanu,et al.  Magnesium Doped Hydroxyapatite-Based Coatings Obtained by Pulsed Galvanostatic Electrochemical Deposition with Adjustable Electrochemical Behavior , 2020, Coatings.

[11]  L. Figueiredo,et al.  Fish Processing Industry Residues: A Review of Valuable Products Extraction and Characterization Methods , 2020, Waste and Biomass Valorization.

[12]  A. Bakulin,et al.  Radio frequency magnetron sputtering of Sr- and Mg-substituted β-tricalcium phosphate: Analysis of the physicochemical properties and deposition rate of coatings , 2020 .

[13]  A. Scribante,et al.  Biomimetic Effect of Nano-Hydroxyapatite in Demineralized Enamel before Orthodontic Bonding of Brackets and Attachments: Visual, Adhesion Strength, and Hardness in In Vitro Tests , 2020, BioMed research international.

[14]  D. Chioibasu,et al.  Animal Origin Bioactive Hydroxyapatite Thin Films Synthesized by RF-Magnetron Sputtering on 3D Printed Cranial Implants , 2019, Metals.

[15]  L. Duta,et al.  Lithium-Doped Biological-Derived Hydroxyapatite Coatings Sustain In Vitro Differentiation of Human Primary Mesenchymal Stem Cells to Osteoblasts , 2019, Coatings.

[16]  A. Rafiee,et al.  Effect of hydroxyapatite nanoparticles on enamel remineralization and estimation of fissure sealant bond strength to remineralized tooth surfaces: an in vitro study , 2019, BMC oral health.

[17]  L. Duta,et al.  Current Status on Pulsed Laser Deposition of Coatings from Animal-Origin Calcium Phosphate Sources , 2019, Coatings.

[18]  Teddy Tite,et al.  Cationic Substitutions in Hydroxyapatite: Current Status of the Derived Biofunctional Effects and Their In Vitro Interrogation Methods , 2018, Materials.

[19]  Pınar Terzioğlu,et al.  Natural calcium phosphates from fish bones and their potential biomedical applications. , 2018, Materials science & engineering. C, Materials for biological applications.

[20]  G. Graziani,et al.  A Review on Ionic Substitutions in Hydroxyapatite Thin Films: Towards Complete Biomimetism , 2018, Coatings.

[21]  L. Duta,et al.  Physical-chemical characterization and biological assessment of simple and lithium-doped biological-derived hydroxyapatite thin films for a new generation of metallic implants , 2018 .

[22]  Luyuan Chen,et al.  In Vitro and In Vivo Osteogenic Activity of Titanium Implants Coated by Pulsed Laser Deposition with a Thin Film of Fluoridated Hydroxyapatite , 2018, International journal of molecular sciences.

[23]  I. Oladele,et al.  Non-synthetic sources for the development of hydroxyapatite , 2018 .

[24]  Kezheng Chen,et al.  Physicochemical and biological properties of bovine-derived porous hydroxyapatite/collagen composite and its hydroxyapatite powders , 2017 .

[25]  V. Thakur,et al.  Facile synthesis and characterization of hydroxyapatite particles for high value nanocomposites and biomaterials , 2017 .

[26]  Á. F. González,et al.  Approach to reduce the zoonotic parasite load in fish stocks: When science meets technology , 2017, Fisheries Research.

[27]  I. Mihailescu,et al.  Comparative physical, chemical and biological assessment of simple and titanium-doped ovine dentine-derived hydroxyapatite coatings fabricated by pulsed laser deposition , 2017 .

[28]  M. Fathi,et al.  A comparative study on physicochemical properties of hydroxyapatite powders derived from natural and synthetic sources , 2017, Russian Journal of Non-Ferrous Metals.

[29]  M. Marcacci,et al.  Ion-substituted calcium phosphate coatings deposited by plasma-assisted techniques: A review. , 2017, Materials science & engineering. C, Materials for biological applications.

[30]  Noam Eliaz,et al.  Calcium Phosphate Bioceramics: A Review of Their History, Structure, Properties, Coating Technologies and Biomedical Applications , 2017, Materials.

[31]  D. Flanagan Enterococcus faecalis and Dental Implants , 2017, The Journal of oral implantology.

[32]  I. Mercioniu,et al.  Bioglass implant-coating interactions in synthetic physiological fluids with varying degrees of biomimicry , 2017, International journal of nanomedicine.

[33]  G. Stan,et al.  Submicrometer Hollow Bioglass Cones Deposited by Radio Frequency Magnetron Sputtering: Formation Mechanism, Properties, and Prospective Biomedical Applications. , 2016, ACS applied materials & interfaces.

[34]  I. Mihailescu,et al.  Structural, compositional, mechanical characterization and biological assessment of bovine-derived hydroxyapatite coatings reinforced with MgF2 or MgO for implants functionalization. , 2016, Materials science & engineering. C, Materials for biological applications.

[35]  H. Birkedal,et al.  Environmentally benign fabrication of calcium hydroxyapatite using seashells collected in Baltic Sea countries: A comparative study , 2016 .

[36]  G. Stan,et al.  Superior biofunctionality of dental implant fixtures uniformly coated with durable bioglass films by magnetron sputtering. , 2015, Journal of the mechanical behavior of biomedical materials.

[37]  Monika Šupová,et al.  Substituted hydroxyapatites for biomedical applications: A review , 2015 .

[38]  L. Zudaire,et al.  Conversion of waste animal bones into porous hydroxyapatite by alkaline treatment: effect of the impregnation ratio and investigation of the activation mechanism , 2015, Journal of Materials Science.

[39]  L. López-Cerero,et al.  Assessment of periodontal and opportunistic flora in patients with peri-implantitis. , 2015, Clinical oral implants research.

[40]  J. Venkatesan,et al.  Isolation and Characterization of Nano-Hydroxyapatite from Salmon Fish Bone , 2015, Materials.

[41]  K. Pfeffer,et al.  Real-time PCR analysis of fungal organisms and bacterial species at peri-implantitis sites , 2015, International journal of implant dentistry.

[42]  Chikara Ohtsuki,et al.  A unified in vitro evaluation for apatite-forming ability of bioactive glasses and their variants , 2015, Journal of Materials Science: Materials in Medicine.

[43]  V. Vishwakarma,et al.  Antibacterial effects of silver–zirconia composite coatings using pulsed laser deposition onto 316L SS for bio implants , 2014, Progress in Biomaterials.

[44]  M. Heiland,et al.  Definition, etiology, prevention and treatment of peri-implantitis – a review , 2014, Head & Face Medicine.

[45]  N. Roveri,et al.  Remineralization and repair of enamel surface by biomimetic Zn-carbonate hydroxyapatite containing toothpaste: a comparative in vivo study , 2014, Front. Physiol..

[46]  R. Prasad,et al.  Alkaline Phosphatase: An Overview , 2014, Indian Journal of Clinical Biochemistry.

[47]  Jong-Ho Lee,et al.  Clinical outcomes of magnesium-incorporated oxidised implants: a randomised double-blind clinical trial. , 2014, Clinical oral implants research.

[48]  I. Mihailescu,et al.  Antifungal activity of Ag:hydroxyapatite thin films synthesized by pulsed laser deposition on Ti and Ti modified by TiO2 nanotubes substrates , 2014 .

[49]  I. Mihailescu,et al.  Biomimetic nanocrystalline apatite coatings synthesized by Matrix Assisted Pulsed Laser Evaporation for medical applications , 2014 .

[50]  I. Shakir,et al.  Extracting hydroxyapatite and its precursors from natural resources , 2014, Journal of Materials Science.

[51]  S. Samavedi,et al.  Calcium phosphate ceramics in bone tissue engineering: a review of properties and their influence on cell behavior. , 2013, Acta biomaterialia.

[52]  M. Otto,et al.  Molecular basis of in vivo biofilm formation by bacterial pathogens. , 2012, Chemistry & biology.

[53]  G. Charalampakis,et al.  Clinical and microbiological characteristics of peri-implantitis cases: a retrospective multicentre study. , 2012, Clinical oral implants research.

[54]  F. Oktar,et al.  Attachment and Proliferation of Osteoblasts on Lithium-Hydroxyapatite Composites , 2012 .

[55]  S. K. Fokter Recent Advances in Arthroplasty , 2012 .

[56]  C. Oldani,et al.  Titanium as a Biomaterial for Implants , 2012 .

[57]  J. Ulrichová,et al.  Osteoblast and gingival fibroblast markers in dental implant studies. , 2011, Biomedical papers of the Medical Faculty of the University Palacky, Olomouc, Czechoslovakia.

[58]  G. Stan,et al.  Differentiation of mesenchymal stem cells onto highly adherent radio frequency-sputtered carbonated hydroxylapatite thin films. , 2010, Journal of biomedical materials research. Part A.

[59]  A. Boccaccini,et al.  Characterisation of the bioactive behaviour of sol–gel hydroxyapatite–CaO and hydroxyapatite–CaO–bioactive glass composites , 2010 .

[60]  G. Stan,et al.  Effect of annealing upon the structure and adhesion properties of sputtered bio-glass/titanium coatings , 2009 .

[61]  J. Jansen,et al.  Thin Calcium Phosphate Coatings for Medical Implants , 2009 .

[62]  M. Bohner,et al.  Can bioactivity be tested in vitro with SBF solution? , 2009, Biomaterials.

[63]  N. Lang,et al.  One-year bacterial colonization patterns of Staphylococcus aureus and other bacteria at implants and adjacent teeth. , 2008, Clinical oral implants research.

[64]  K. Asokan,et al.  High energy irradiation : a tool for enhancing the bioactivity of Hydroxyapatite , 2008 .

[65]  L. Rimondini,et al.  The Remineralizing Effect of Carbonate-Hydroxyapatite Nanocrystals on Dentine , 2007 .

[66]  A. Piattelli,et al.  The effect of material characteristics, of surface topography and of implant components and connections on soft tissue integration: a literature review. , 2006, Clinical oral implants research.

[67]  Th Leventouri,et al.  Synthetic and biological hydroxyapatites: crystal structure questions. , 2006, Biomaterials.

[68]  Tadashi Kokubo,et al.  How useful is SBF in predicting in vivo bone bioactivity? , 2006, Biomaterials.

[69]  V. Nelea,et al.  Biomaterials: New Issues and Breakthroughs for Biomedical Applications , 2006 .

[70]  F. Oktar,et al.  Effect of sintering temperature on mechanical and microstructural properties of bovine hydroxyapatite (BHA) , 2006 .

[71]  Chuanzhong Chen,et al.  Pulsed laser deposition and its current research status in preparing hydroxyapatite thin films , 2005 .

[72]  M. A. Respaldiza,et al.  Study of the stoichiometry transfer in pulsed laser deposition of bioactive silica-based glasses , 2004 .

[73]  T. Webster,et al.  Enhanced functions of osteoblasts on nanophase ceramics. , 2000, Biomaterials.

[74]  R. A. Condrate,et al.  The Infrared and Raman Spectra of β-and α-Tricalcium Phosphate (Ca3(Po4)2) , 1998 .

[75]  G. H. Nancollas,et al.  The effect of lithium on the precipitation of hydroxyapatite from aqueous solutions , 1986 .

[76]  D. K. Owens,et al.  Estimation of the surface free energy of polymers , 1969 .

[77]  Eric Gilman,et al.  A third assessment of global marine fisheries discards , 2019 .

[78]  A. Adeogun,et al.  Synthesis of organic derived hydroxyapatite scaffold from pig bone waste for tissue engineering applications , 2018 .

[79]  Paolo M. Ossi,et al.  Laser-Surface Interactions for New Materials Production , 2010 .

[80]  G. Stan,et al.  POLYMER-LIKE AND DIAMOND-LIKE CARBON COATINGS PREPARED BY RF-PECVD FOR BIOMEDICAL APPLICATIONS , 2010 .

[81]  I. Mihailescu,et al.  Advanced Biomimetic Implants Based on Nanostructured Coatings Synthesized by Pulsed Laser Technologies , 2010 .

[82]  B. Léon Pulsed Laser Deposition of Thin Calcium Phosphate Coatings , 2009 .

[83]  Serena M. Best,et al.  Bioceramics: Past, present and for the future , 2008 .

[84]  T. Moriguchi,et al.  REACTION OF Ca-DEFICIENT HYDROXYAPATITE WITH HEAVY METAL IONS ALONG WITH METAL SUBSTITUTION , 2008 .