Graphene onto medical grade titanium: an atom-thick multimodal coating that promotes osteoblast maturation and inhibits biofilm formation from distinct species

References

• Aas, J. A., B. J. Paster, L. N. Stokes, I. Olsen, and F. E. Dewhirst. 2005. “Defining the Normal Bacterial Flora of the Oral Cavity.” The Journal of Clinical Microbiology 43 (11): 5721–5732. doi:10.1128/JCM.43.11.5721-5732.2005.
   PubMed Web of Science ®Google Scholar
• ASTM F22-13. 2013. Standard Test Method for Hydrophobic Surface Films by the Water-Break Test. West Conshohocken, PA: ASTM International.
   Google Scholar
• Barao, V. A., M. T. Mathew, W. G. Assuncao, J. C. Yuan, M. A. Wimmer, and C. Sukotjo. 2011. “The Role of Lipopolysaccharide on the Electrochemical Behavior of Titanium.” Journal of Dental Research 90 (5): 613–618. doi:10.1177/0022034510396880.
   PubMed Web of Science ®Google Scholar
• Bornstein, M. M., N. Cionca, and A. Mombelli. 2009. “Systemic Conditions and Treatments as Risks for Implant Therapy.” The International Journal of Oral & Maxillofacial Implants 24: 12–27.
   PubMed Web of Science ®Google Scholar
• Chen, Y., X. L. Gong, and J. G. Gai. 2016. “Progress and Challenges in Transfer of Large-Area Graphene Films.” Advanced Science 3 (8): 1500343. doi:10.1002/advs.201500343.
   Web of Science ®Google Scholar
• Collier, J. P., V. A. Surprenant, M. B. Mayor, M. Wrona, R. E. Jensen, and H. P. Surprenant. 1993. “Loss of Hydroxyapatite Coating on Retrieved, Total Hip Components.” The Journal of Arthroplasty 8 (4): 389–393. doi:10.1016/S0883-5403(06)80037-9.
   PubMedGoogle Scholar
• Daubert, D. M., B. F. Weinstein, S. Bordin, B. G. Leroux, and T. F. Flemmig. 2015. “Prevalence and Predictive Factors for Peri-Implant Disease and Implant Failure: A Cross-Sectional Analysis.” Journal of Periodontology Online 86 (3): 337–347. doi:10.1902/jop.2014.140438.
   PubMed Web of Science ®Google Scholar
• Dellieu, L., E. Lawarée, N. Reckinger, C. Didembourg, J. J. Letesson, M. Sarrazin, O. Deparis, J. Y. Matroule, and J. F. Colomer. 2015. “Do CVD Grown Graphene Films Have Antibacterial Activity on Metallic Substrates?” Carbon 84: 310–316. doi:10.1016/j.carbon.2014.12.025.
   Web of Science ®Google Scholar
• Dubey, N., R. Bentini, I. Islam, T. Cao, A. H. C. Neto, and V. Rosa. 2015. “Graphene: A Versatile Carbon-Based Material for Bone Tissue Engineering.” Stem Cells International 2015: 1. doi:10.1155/2015/804213.
   Web of Science ®Google Scholar
• Ersanli, S., C. Karabuda, F. Beck, and B. Leblebicioglu. 2005. “Resonance Frequency Analysis of One-Stage Dental Implant Stability during the Osseointegration Period.” Journal of Periodontology Online 76 (7): 1066–1071. doi:10.1902/jop.2005.76.7.1066.
   PubMed Web of Science ®Google Scholar
• Faeda, R. S., H. S. Tavares, R. Sartori, A. C. Guastaldi, and E. Marcantonio. 2009. “Biological Performance of Chemical Hydroxyapatite Coating Associated with Implant Surface Modification by Laser Beam: Biomechanical Study in Rabbit Tibias.” Journal of Oral and Maxillofacial Surgery 67 (8): 1706–1715. doi:10.1016/j.joms.2009.03.046.
   PubMed Web of Science ®Google Scholar
• Fechine, G. J. M., I. Martin-Fernandez, G. Yiapanis, R. Bentini, E. S. Kulkarni, R. V. Bof de Oliveira, X. Hu, I. Yarovsky, A. H. Castro Neto, and B. Özyilmaz. 2015. “Direct Dry Transfer of Chemical Vapor Deposition Graphene to Polymeric Substrates.” Carbon 83: 224–231. doi:10.1016/j.carbon.2014.11.038.
   Web of Science ®Google Scholar
• Golub, E. E., and K. Boesze-Battaglia. 2007. “The Role of Alkaline Phosphatase in Mineralization.” Current Opinion in Orthopaedics 18 (5): 444–448. doi:10.1097/BCO.0b013e3282630851.
   Google Scholar
• Gongadze, E., D. Kabaso, S. Bauer, T. Slivnik, P. Schmuki, U. van Rienen, 2011. “Adhesion of Osteoblasts to a Nanorough Titanium Implant Surface.” International Journal of Nanomedicine 6: 1801–1816. doi:10.2147/IJN.S21755.
   PubMed Web of Science ®Google Scholar
• Hadi, S., N. Ashfaq, A. Bey, and S. Khan. 2011. “Biological Factors Responsible for Failure of Osseointegration in Oral Implants.” Biology and Medicine 3: 164–170.
   Google Scholar
• Heitz-Mayfield, L. J., G. E. Salvi, A. Mombelli, M. Faddy, N. P. Lang, and Implant Complication Research Group. 2012. “Anti-Infective Surgical Therapy of Peri-Implantitis. A 12-Month Prospective Clinical Study.” Clinical Oral Implants Research 23: 205–210. doi:10.1111/j.1600-0501.2011.02276.x.
   PubMed Web of Science ®Google Scholar
• Imani, R., D. Kabaso, M. Erdani Kreft, E. Gongadze, S. Penič, K. Eleršič, A. Kos, P. Veranič, R. Zorec, and A. Iglič. 2012. “Morphological Alterations of T24 Cells on Flat and Nanotubular TiO2 Surfaces.” Croatian Medical Journal 53 (6): 577–585. doi:10.3325/cmj.2012.53.577.
   PubMed Web of Science ®Google Scholar
• Jang, B., C. H. Kim, S. T. Choi, K. S. Kim, K. S. Kim, H. J. Lee, S. Cho, J. H. Ahn, and J. H. Kim. 2017. “Damage Mitigation in Roll-to-Roll Transfer of CVD-Graphene to Flexible Substrates.” 2D Materials 4: 024002. doi:10.1088/2053-1583.
   Google Scholar
• Jeffcoat, M. K., E. A. McGlumphy, M. S. Reddy, N. C. Geurs, and H. M. Proskin. 2003. “A Comparison of Hydroxyapatite (HA) -Coated Threaded, HA-Coated Cylindric, and Titanium Threaded Endosseous Dental Implants.” The International Journal of Oral & Maxillofacial Implants 18: 406–410. doi:10.1016/j.prosdent.
   PubMed Web of Science ®Google Scholar
• Johannsen, A., U. Wikesjo, G. Tellefsen, and G. Johannsen. 2012. “Patient Attitudes and Expectations of Dental Implant Treatment–A Questionnaire Study.” Swedish Dental Journal 36: 7–14.
   PubMed Web of Science ®Google Scholar
• Junkar, I., Kulkarni, M. B. Drašler, N. Rugelj, A. Mazare, A. Flašker, D. Drobne, et al. 2016. “Influence of Various Sterilization Procedures on TiO2 Nanotubes Used for Biomedical Devices.” Bioelectrochemistry 109: 79–86. doi:10.1016/j.bioelechem.2016.02.001.
   PubMed Web of Science ®Google Scholar
• Kern, B., J. Shen, M. Starbuck, and G. Karsenty. 2001. “Cbfa1 Contributes to the Osteoblast-Specific Expression of Type I Collagen Genes.” Journal of Biological Chemistry 276 (10): 7101–7107. doi:10.1074/jbc.M006215200.
   PubMed Web of Science ®Google Scholar
• Kim, M. J., C. W. Kim, Y. J. Lim, and S. J. Heo. 2006. “Microrough Titanium Surface Affects Biologic Response in MG63 Osteoblast-like Cells.” Journal of Biomedical Materials Research Part A 79 (4): 1023–1032. doi:10.1002/jbm.a.31040.
   PubMedGoogle Scholar
• Krecisz, M., Kiec-Swierczynska, and K. Bakowicz-Mitura. 2006. “Allergy to Metals as a Cause of Orthopedic Implant Failure.” International Journal of Occupational Medicine and Environmental Health 19: 178–180. doi:10.2478/v10001-006-0025-6.
   PubMedGoogle Scholar
• Kulkarni, M., A. Mazare, E. Gongadze, Š. Perutkova, V. Kralj-Iglič, I. Milošev, P. Schmuki, A. Iglič, and M. Mozetič. 2015. “Titanium Nanostructures for Biomedical Applications.” Nanotechnology 26: 062002. doi:10.1088/0957-4484/26/6/062002.
   PubMed Web of Science ®Google Scholar
• Kulkarni, M., Y. Patil-Sen, I. Junkar, C. V. Kulkarni, M. Lorenzetti, and A. Iglič. 2015. “Wettability Studies of Topologically Distinct Titanium Surfaces.” Colloids Surface B Biointerfaces 129: 47–53. doi:10.1016/j.colsurfb.2015.03.024.
   PubMed Web of Science ®Google Scholar
• Lee, C., X. Wei, J. W. Kysar, and J. Hone. 2008. “Measurement of the Elastic Properties and Intrinsic Strength of Monolayer Graphene.” Science 321 (5887): 385–388. doi:10.1126/science.1157996.
   PubMed Web of Science ®Google Scholar
• Lee, W. C., C. H. Y. X. Lim, H. Shi, L. A. L. Tang, Y. Wang, C. T. Lim, and K. P. Loh. 2011. “Origin of Enhanced Stem Cell Growth and Differentiation on Graphene and Graphene Oxide.” ACS Nano 5 (9): 7334–7341. doi:10.1021/nn202190c.
   PubMed Web of Science ®Google Scholar
• Li, J., G. Wang, H. Zhu, M. Zhang, X. Zheng, Z. Di, X. Liu, and X. Wang. 2015. “Antibacterial Activity of Large-Area Monolayer Graphene Film Manipulated by Charge Transfer.” Scientific Reports 4 (1): 4359. doi:10.1038/srep04359.
   Google Scholar
• Li, X., Y. Zhu, W. Cai, M. Borysiak, B. Han, D. Chen, R. D. Piner, L. Colombo, and R. S. Ruoff. 2009. “Transfer of Large-Area Graphene Films for High-Performance Transparent Conductive Electrodes.” Nano Letters 9 (12): 4359–4363. doi:10.1021/nl902623y.
   PubMed Web of Science ®Google Scholar
• Liang, X., Sperling, B. A. I. Calizo, G. Cheng, C. A. Hacker, Q. Zhang, Y. Obeng, et al. 2011. “Toward Clean and Crackless Transfer of Graphene.” ACS Nano 5 (11): 9144–9153. doi:10.1021/nn203377t.
   PubMed Web of Science ®Google Scholar
• Liao, H., A. S. Andersson, D. Sutherland, S. Petronis, B. Kasemo, and P. Thomsen. 2003. “Response of Rat Osteoblast-like Cells to Microstructured Model Surfaces in Vitro.” Biomaterials 24 (4): 649–654. doi:10.1016/S0142-9612(02)00379-4.
   PubMed Web of Science ®Google Scholar
• Mombelli, A., M. A. van Oosten, E. Schurch, and N. P. Land. 1987. “The Microbiota Associated with Successful or Failing Osseointegrated Titanium Implants.” Oral Microbiology and Immunology 2 (4): 145–151. doi:10.1111/j.1399-302X.1987.tb00298.x.
   PubMedGoogle Scholar
• Mombelli, A., N. Müller, and N. Cionca. 2012. “The Epidemiology of Peri-Implantitis.” Clinical Oral Implants Research 23: 67–76. doi:10.1111/j.1600-0501.2012.02541.x.
   PubMed Web of Science ®Google Scholar
• Morin, J. L. P., N. Dubey, F. E. D. Decroix, E. K. Luong-Van, A. H. Castro Neto, and V. Rosa. 2017. “Graphene Transfer to 3-Dimensional Surfaces: A Vacuum-Assisted Dry Transfer Method.” 2D Materials 4 (2): 025060. doi:10.1088/2053-1583/aa6530.
   Google Scholar
• Narendrakumar, K., M. Kulkarni, O. Addison, A. Mazare, I. Junkar, P. Schmuki, R. Sammons, and A. Iglič. 2015. “Adherence of Oral Streptococci to Nanostructured Titanium Surfaces.” Dental Materials 31 (12): 1460–1468. doi:10.1016/j.dental.2015.09.011.
   PubMed Web of Science ®Google Scholar
• Nayak, T. R., H. Andersen, V. S. Makam, C. Khaw, S. Bae, X. Xu, P. L. R. Ee, et al. 2011. “Graphene for Controlled and Accelerated Osteogenic Differentiation of Human Mesenchymal Stem Cells.” ACS Nano 5 (6): 4670–4678. doi:10.1021/nn200500h.
   PubMed Web of Science ®Google Scholar
• Peng, Z., J. Ni, K. Zheng, Y. Shen, X. Wang, G. He, S. Jin, and T. Tang. 2013. “Dual Effects and Mechanism of TiO2 Nanotube Arrays in Reducing Bacterial Colonization and Enhancing C3H10T1/2 Cell Adhesion.” International Journal of Nanomedicine 8: 3093–3105. doi:10.2147/IJN.S48084.
   PubMed Web of Science ®Google Scholar
• Poser, J. W., F. S. Esch, N. C. Ling, and P. A. Price. 1980. “Isolation and Sequence of the Vitamin K-Dependent Protein from Human Bone. Undercarboxylation of the First Glutamic Acid Residue.” The Journal of Biological Chemistry 255 (18): 8685–8691.
   PubMed Web of Science ®Google Scholar
• Robitaille, N., D. N. Reed, J. D. Walters, and P. S. Kumar. 2016. “Periodontal and Peri-Implant Diseases: Identical or Fraternal Infections?” Molecular Oral Microbiology 31 (4): 285–301. doi:10.1111/omi.12124.
   PubMed Web of Science ®Google Scholar
• Rodriguez, C. L. C., F. Kessler, N. Dubey, V. Rosa, and G. J. M. Fechine. 2017. “CVD Graphene Transfer Procedure to the Surface of Stainless Steel for Stem Cell Proliferation.” Surface and Coatings Technology 311: 10–18. doi:10.1016/j.surfcoat.2016.12.111.
   Web of Science ®Google Scholar
• Rosa, V., A. Della Bona, B. N. Cavalcanti, and J. E. Nör. 2012. “Tissue Engineering: From Research to Dental Clinics.” Dental Materials 28 (4): 341–348. doi:10.1016/j.dental.2011.11.025.
   PubMed Web of Science ®Google Scholar
• Schwartz-Arad, D., O. Mardinger, L. Levin, A. Kozlovsky, and A. Hirshberg. 2005. “Marginal Bone Loss Pattern around Hydroxyapatite-Coated versus Commercially Pure Titanium Implants after up to 12 Years of Follow-up.” The International Journal of Oral & Maxillofacial Implants 20: 238–244.
   PubMed Web of Science ®Google Scholar
• Sojoudi, H., and S. Graham. 2013. “Transfer-Free Selective Area Synthesis of Graphene Using Solid-State Self-Segregation of Carbon in Cu/Ni Bilayers.” ECS Journal of Solid State Science and Technology 2 (6): M17–M21. doi:10.1149/2.016306jss.
   Web of Science ®Google Scholar
• Sun, L., C. C. Berndt, K. A. Gross, and A. Kucuk. 2001. “Material Fundamentals and Clinical Performance of Plasma‐Sprayed Hydroxyapatite Coatings: A Review.” Journal of Biomedical Materials Research 58 (5): 570–592. doi:10.1002/jbm.1056.
   PubMed Web of Science ®Google Scholar
• Tonetto, A., P. W. Lago, M. Borba, and V. Rosa. 2016. “Effects of Chrondro-Osseous Regenerative Compound Associated with Local Treatments in the Regeneration of Bone Defects around Implants: An In Vivo Study.” Clinical Oral Investigations 20 (2): 267–274. doi:10.1007/s00784-015-1509-1.
   PubMed Web of Science ®Google Scholar
• Verdugo, F., T. Laksmana, and A. Uribarri. 2016. “Systemic Antibiotics and the Risk of Superinfection in Peri-Implantitis.” Archives of Oral Biology 64: 39–50. doi:10.1016/j.archoralbio.2015.12.007.
   PubMed Web of Science ®Google Scholar
• Viereck, V., H. Siggelkow, S. Tauber, D. Raddatz, N. Schutze, and M. Hüfner. 2002. “Differential Regulation of Cbfa1/Runx2 and Osteocalcin Gene Expression by Vitamin‐D3, Dexamethasone, and Local Growth Factors in Primary Human Osteoblasts.” Journal of Cellular Biochemistry 86 (2): 348–356. doi:10.1002/jcb.10220.
   PubMed Web of Science ®Google Scholar
• Wang, S., Y. Zhang, N. Abidi, and L. Cabrales. 2009. “Wettability and Surface Free Energy of Graphene Films.” Langmuir: The ACS Journal of Surfaces and Colloids 25 (18): 11078–11081. doi:10.1021/la901402f.
   PubMed Web of Science ®Google Scholar
• Wen, Z., C. J. Seneviratne, K. C. F. Leung, C. H. Wong, S. F. Lee, X. Li, P. C. Leung, C. B. S. Lau, E. Wat, and L. Jin. 2014. “Nanoparticle-Encapsulated Chlorhexidine against Oral Bacterial Biofilms.” PLoS One 9 (8): e103234. doi:10.1371/journal.pone.0103234.
   PubMed Web of Science ®Google Scholar
• Weng, J. J., and Y. Su. 2013. “Nuclear Matrix-Targeting of the Osteogenic Factor Runx2 is Essential for Its Recognition and Activation of the Alkaline Phosphatase Gene.” Biochimica et Biophysica Acta 1830 (3): 2839–2852. doi:10.1016/j.bbagen.2012.12.021.
   PubMed Web of Science ®Google Scholar
• Xie, H., M. Chua, I. Islam, R. Bentini, T. Cao, J. C. Viana-Gomes, A. H. Castro Neto, and V. Rosa. 2016. “CVD-Grown Monolayer Graphene Induces Osteogenic but Not Odontoblastic Differentiation of Dental Pulp Stem Cells.” Dental Materials 33: e13–e21. doi:10.1016/j.dental.2016.09.030.
   PubMed Web of Science ®Google Scholar
• Xie, H., T. Cao, F. J. Rodriguez-Lozano, E. K. Luong-Van, and V. Rosa. 2017. “Graphene for the Development of the Next-Generation of Biocomposites for Dental and Medical Applications.” Dental Materials: Official Publication of the Academy of Dental Materials 33 (7): 765–774. doi:10.1016/j.dental.2017.04.008.
   PubMed Web of Science ®Google Scholar
• Xie, H., T. Cao, J. V. Gomes, A. H. C. Neto, and V. Rosa. 2015. “Two and Three-Dimensional Graphene Substrates to Magnify Osteogenic Differentiation of Periodontal Ligament Stem Cells.” Carbon 93: 266–275. doi:10.1016/j.carbon.2015.05.071.
   Web of Science ®Google Scholar
• Xue, J., J. Sanchez-Yamagishi, D. Bulmash, P. Jacquod, A. Deshpande, K. Watanabe, T. Taniguchi, P. Jarillo-Herrero, and B. J. LeRoy. 2011. “Scanning Tunnelling Microscopy and Spectroscopy of Ultra-Flat Graphene on Hexagonal Boron Nitride.” Nature Materials 10: 282–285. doi:10.1038/nmat2968.
   PubMed Web of Science ®Google Scholar
• Yuan, Y., M. P. Hays, P. R. Hardwidge, and J. Kim. 2017. “Surface Characteristics Influencing Bacterial Adhesion to Polymeric Substrates.” RSC Advances 7 (23): 14254–14261. doi:10.1039/C7RA01571B.
   Web of Science ®Google Scholar
• Zheng, J., Hamlekhan, A. A. Butt, S. Patel, D. Royhman, C. Takoudis, C. Sukotjo, et al. 2014. “Fabrication of Anti-Aging TiO2 Nanotubes on Biomedical Ti Alloys.” PLoS One 9 (5): e96213 doi: 10.1371/journal.pone.0096213.
   PubMed Web of Science ®Google Scholar