Biocompatible nanostructured solid adhesives for biological soft tissues (original) (raw)

Abstract

Over the past few years, the development of novel adhesives for biological soft tissue adhesion has gained significant interest. Such adhesives should be non-toxic and biocompatible. In this study, we synthesized a novel solid adhesive using nanostructured hydroxyapatite (HAp) and evaluated its physical adhesion properties through in vitro testing with synthetic hydrogels and mouse soft tissues. The results revealed that HAp-nanoparticle dispersions and HAp-nanoparticle-assembled nanoporous plates showed efficient adhesion to hydrogels. Interestingly, the HAp plates showed different adhesive properties depending upon the shape of their nanoparticles. The HAp plate made up of 17nm-sized nanoparticles showed an adhesive strength 2.2times higher than that of the conventional fibrin glue for mouse skin tissues. The present study indicates a new application of inorganic biomaterials (bioceramics) as a soft tissue adhesive. Organic adhesives such as fibrin glues or cyanoacrylate derivativ...

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References (55)

  1. M. Matsuda, M. Inoue, T. Taguchi, Adhesive properties and biocompatibility of tissue adhesives composed of various hydrophobically modified gelatins and disuccinimidyl tartrate, J. Bioact. Compat. Polym. 27 (2012) 481-498. doi:10.1177/0883911512455116.
  2. Y.-C. Tseng, H. Suong-Hyu, Y. Ikada, Y. Shimizu, K. Tamura, S. Hitomi, In vivo evaluation of 2-cyanoacrylates as surgical adhesives, J. Appl. Biomater. 1 (1990) 111-119.
  3. S. Fukunaga, M. Karck, W. Harringer, J. Cremer, C. Rhein, A. Haverich, The use of gelatin-resorcin-formalin glue in acute aortic dissection type A, Eur. J. Cardio-Thoracic Surg. 15 (1999) 564-570. doi:10.1016/S1010-7940(99)00084-6.
  4. E. V Dare, M. Griffith, P. Poitras, T. Wang, G.F. Dervin, A. Giulivi, M.T. Hincke, Fibrin sealants from fresh or fresh/frozen plasma as scaffolds for in vitro articular cartilage regeneration., Tissue Eng. Part A. 15 (2009) 2285-97. doi:10.1089/ten.tea.2008.0228.
  5. S. Venkatraman, R. Gale, Skin adhesives and skin adhesion. 1. Transdermal drug delivery systems., Biomaterials. 19 (1998) 1119-36. http://www.ncbi.nlm.nih.gov/pubmed/9720896 (accessed May 4, 2016).
  6. K. Jin, Y. Tian, J.S. Erickson, J. Puthoff, K. Autumn, N.S. Pesika, Design and fabrication of Gecko-inspired adhesives, Langmuir. 28 (2012) 5737-5742. doi:10.1021/la204040p.
  7. A.K. Geim, S. V Dubonos, I. V Grigorieva, K.S. Novoselov, a a Zhukov, S.Y. Shapoval, Microfabricated adhesive mimicking gecko foot-hair., Nat. Mater. 2 (2003) 461-463. doi:10.1038/nmat917.
  8. M.P. Murphy, B. Aksak, M. Sitti, Gecko-Inspired Directional and Controllable Adhesion, Small. 5 (2008) 170-175. doi:10.1002/smll.200801161.
  9. B. Aksak, M.P. Murphy, M. Sitti, Adhesion of Biologically Inspired Vertical and Angled Polymer Microfiber Arrays, Langmuir. 23 (2007) 3322-3332. doi:10.1021/la062697t.
  10. H.E. Jeong, J.-K. Lee, H.N. Kim, S.H. Moon, K.Y. Suh, A nontransferring dry adhesive with hierarchical polymer nanohairs, Proc. Natl. Acad. Sci. 106 (2009) 5639-5644. doi:10.1073/pnas.0900323106.
  11. J. Lee, R.S. Fearing, K. Komvopoulos, Directional adhesion of gecko-inspired angled microfiber arrays, Appl. Phys. Lett. 93 (2008) 2006-2009. doi:10.1063/1.3006334.
  12. C. Greiner, E. Arzt, A. del Campo, Hierarchical Gecko-Like Adhesives, Adv. Mater. 21 (2009) 479-482. doi:10.1002/adma.200801548.
  13. D. Sameoto, C. Menon, Direct molding of dry adhesives with anisotropic peel strength using an offset lift-off photoresist mold, J. Micromechanics Microengineering. 19 (2009) 115026. doi:10.1088/0960-1317/19/11/115026.
  14. J. Yu, S. Chary, S. Das, J. Tamelier, N.S. Pesika, K.L. Turner, J.N. Israelachvili, Gecko-Inspired Dry Adhesive for Robotic Applications, Adv. Funct. Mater. 21 (2011) 3010-3018. doi:10.1002/adfm.201100493.
  15. B. Yurdumakan, N.R. Raravikar, P.M. Ajayan, A. Dhinojwala, Synthetic gecko foot-hairs from multiwalled carbon nanotubes., Chem. Commun. (Camb). 405 (2005) 3799-3801. doi:10.1039/b506047h.
  16. S. Rose, A. Prevoteau, P. Elzière, D. Hourdet, A. Marcellan, L. Leibler, Nanoparticle solutions as adhesives for gels and biological tissues., Nature. 505 (2014) 382-5. doi:10.1038/nature12806.
  17. E.I. Abdel-Gawad, S.A. Awwad, Biocompatibility of Intravenous Nano Hydroxyapatite in Male Rats, Nat. Sci. 8 (2010). http://www.sciencepub.net/nature (accessed May 9, 2016).
  18. D.M. Lawton, M.D.J. Lamaletie, D.L. Gardner, Biocompatibility of hydroxyapatite ceramic: response of chondrocytes in a test system using low temperature scanning electron microscopy, J. Dent. 17 (1989) 21-27. doi:10.1016/0300-5712(89)90003-1.
  19. S. V Dorozhkin, Nanosized and nanocrystalline calcium orthophosphates., Acta Biomater. 6 (2010) 715-34. doi:10.1016/j.actbio.2009.10.031.
  20. M. Honda, T.J. Fujimi, S. Izumi, K. Izawa, M. Aizawa, H. Morisue, T. Tsuchiya, N. Kanzawa, Topographical analyses of proliferation and differentiation of osteoblasts in micro-and macropores of apatite-fiber scaffold., J. Biomed. Mater. Res. A. 94 (2010) 937-44. doi:10.1002/jbm.a.32779.
  21. S.-W. Choi, Y. Zhang, S. Thomopoulos, Y. Xia, In vitro mineralization by preosteoblasts in poly(DL-lactide-co-glycolide) inverse opal scaffolds reinforced with hydroxyapatite nanoparticles., Langmuir. 26 (2010) 12126-31. doi:10.1021/la101519b.
  22. M. Okada, T. Matsumoto, Synthesis and modification of apatite nanoparticles for use in dental and medical applications, Jpn. Dent. Sci. Rev. 51 (2015) 85-95. doi:10.1016/j.jdsr.2015.03.004.
  23. K. Tomoda, H. Ariizumi, T. Nakaji, K. Makino, Hydroxyapatite particles as drug carriers for proteins, Colloids Surfaces B Biointerfaces. 76 (2010) 226-235. doi:10.1016/j.colsurfb.2009.10.039.
  24. A. Bouladjine, A. Al-Kattan, P. Dufour, C. Drouet, New advances in nanocrystalline apatite colloids intended for cellular drug delivery., Langmuir. 25 (2009) 12256-65. doi:10.1021/la901671j.
  25. T. Matsumoto, M. Okazaki, M. Inoue, S. Yamaguchi, T. Kusunose, T. Toyonaga, Y. Hamada, J. Takahashi, Hydroxyapatite particles as a controlled release carrier of protein, Biomaterials. 25 (2004) 3807-3812. doi:10.1016/j.biomaterials.2003.10.081.
  26. T. Kawasaki, Hydroxyapatite as a liquid chromatographic packing, J. Chromatogr. 544 (1991) 147-184.
  27. K.L. Kilpadi, P.L. Chang, S.L. Bellis, Hydroxylapatite binds more serum proteins, purified integrins, and osteoblast precursor cells than titanium or steel., J. Biomed. Mater. Res. 57 (2001) 258-67. http://www.ncbi.nlm.nih.gov/pubmed/11484189 (accessed May 9, 2016).
  28. J.S. Lee, A.J. Wagoner Johnson, W.L. Murphy, A modular, hydroxyapatite-binding version of vascular endothelial growth factor, Adv. Mater. 22 (2010) 5494-5498. doi:10.1002/adma.201002970.
  29. M. Tagaya, T. Ikoma, T. Takemura, N. Hanagata, T. Yoshioka, J. Tanaka, Effect of interfacial proteins on osteoblast-like cell adhesion to hydroxyapatite nanocrystals., Langmuir. 27 (2011) 7645-53. doi:10.1021/la200621p.
  30. H. Fujita, T. Kudo, H. Kanetaka, T. Miyazaki, M. Hashimoto, M. Kawashita, Adsorption of Laminin on Hydroxyapatite and Alumina and the MC3T3-E1 Cell Response, ACS Biomater. Sci. Eng. 2 (2016) 1162-1168. doi:10.1021/acsbiomaterials.6b00190.
  31. F. Wu, D.D.W. Lin, J.H. Chang, C. Fischbach, L.A. Estroff, D. Gourdon, Effect of the materials properties of hydroxyapatite nanoparticles on fibronectin deposition and conformation, Cryst. Growth Des. 15 (2015) 2452-2460. doi:10.1021/acs.cgd.5b00231.
  32. M. Uehira, M. Okada, S. Takeda, N. Matsumoto, Preparation and characterization of low-crystallized hydroxyapatite nanoporous plates and granules, Appl. Surf. Sci. 287 (2013) 195-202. doi:10.1016/j.apsusc.2013.09.117.
  33. M. Okada, T. Furuzono, Low-temperature synthesis of nanoparticle-assembled, transparent, and low-crystallized hydroxyapatite blocks, J. Colloid Interface Sci. 360 (2011) 457-462. doi:10.1016/j.jcis.2011.04.068.
  34. M. Okada, D. Hiramatsu, T. Okihara, T. Matsumoto, Adsorption and desorption behaviors of cetylpyridinium chloride on hydroxyapatite nanoparticles with different morphologies, Dent. Mater. J. 35 (2016) 651-658. doi:10.4012/dmj.2015-420.
  35. L. Carlsson, S. Rose, D. Hourdet, A. Marcellan, Nano-hybrid self-crosslinked PDMA/silica hydrogels, Soft Matter. 6 (2010) 3619. doi:10.1039/c0sm00009d.
  36. R.C. Team, R: A Language and Environment for Statistical Computing, (2016).
  37. T. Kawamoto, M. Shimizu, A method for preparing 2-to 50-micron-thick fresh-frozen sections of large samples and undecalcified hard tissues., Histochem. Cell Biol. 113 (2000) 331-9. http://www.ncbi.nlm.nih.gov/pubmed/10883392 (accessed September 7, 2016).
  38. M. Descamps, L. Boilet, G. Moreau, A. Tricoteaux, J. Lu, A. Leriche, V. Lardot, F. Cambier, Processing and properties of biphasic calcium phosphates bioceramics obtained by pressureless sintering and hot isostatic pressing, J. Eur. Ceram. Soc. 33 (2013) 1263-1270. doi:10.1016/j.jeurceramsoc.2012.12.020.
  39. J. Sun, F. Wang, Y. Sui, Z. She, W. Zhai, C. Wang, Y. Deng, Effect of particle size on solubility, dissolution rate, and oral bioavailability: evaluation using coenzyme Q as naked nanocrystals., Int. J. Nanomedicine. 7 (2012) 5733-44. doi:10.2147/IJN.S34365.
  40. H. Takashima, K. Iwaki, R. Furukuwa, K. Takishita, H. Sawada, Preparation and applications of a variety of fluoroalkyl end-capped oligomer/hydroxyapatite composites, J. Colloid Interface Sci. 320 (2008) 436-444. doi:10.1016/j.jcis.2007.12.029.
  41. M. Okada, K. Furukawa, T. Serizawa, Y. Yanagisawa, H. Tanaka, T. Kawai, T. Furuzono, Interfacial Interactions between Calcined Hydroxyapatite Nanocrystals and Substrates, Langmuir. 25 (2009) 6300-6306. doi:10.1021/la804274q.
  42. M.A. Lopes, F.J. Monteiro, J.D. Santos, A.P. Serro, B. Saramago, Hydrophobicity , surface tension , and zeta potential measurements of glass-reinforced hydroxyapatite composites, J Biomed Mater Res. 45 (1999) 370-5.
  43. P.J. van Zwol, G. Palasantzas, J.M. Th De Hosson, Influence of roughness on capillary forces between hydrophilic surfaces, Pysical Rev. E. 78 (2008) 31606. doi:10.1103/PhysRevE.78.031606.
  44. M. Fuji, K. Machida, T. Takei, T. Watanabe, M. Chikazawa, Effect of Surface Geometric Structure on the Adhesion Force between Silica Particles, J. Phys. Chem. B. 102 (1998) 8782-8787. doi:10.1021/jp981978+.
  45. S. Kull, I. Martinelli, E. Briganti, P. Losi, D. Spiller, S. Tonlorenzi, G. Soldani, Glubran2 Surgical Glue: In Vitro Evaluation of Adhesive and Mechanical Properties, J. Surg. Res. 157 (2009) e15-e21. doi:10.1016/j.jss.2009.01.034.
  46. N. V Shah, R. Meislin, Current state and use of biological adhesives in orthopedic surgery., Orthopedics. 36 (2013) 945-56. http://www.ncbi.nlm.nih.gov/pubmed/24579215 (accessed March 29, 2017).
  47. E. Fujii, M. Ohkubo, K. Tsuru, S. Hayakawa, A. Osaka, K. Kawabata, C. Bonhomme, F. Babonneau, Selective protein adsorption property and characterization of nano-crystalline zinc-containing hydroxyapatite, Acta Biomater. 2 (2006) 69-74. doi:10.1016/j.actbio.2005.09.002.
  48. K. Kandori, S. Toshima, M. Wakamura, M. Fukusumi, Y. Morisada, Effects of Modification of Calcium Hydroxyapatites by Trivalent Metal Ions on the Protein Adsorption Behavior, J. Phys. Chem. B. 114 (2010) 2399-2404. doi:10.1021/jp911783r.
  49. T. Matsumoto, M. Okazaki, M. Inoue, Y. Hamada, M. Taira, J. Takahashi, Crystallinity and solubility characteristics of hydroxyapatite adsorbed amino acid, Biomaterials. 23 (2002) 2241-2247. doi:10.1016/S0142-9612(01)00358-1.
  50. J.-H. Lin, H.-Y. Chang, W.-L. Kao, K.-Y. Lin, H.-Y. Liao, Y.-W. You, Y.-T. Kuo, D.-Y. Kuo, K.-J. Chu, Y.-H. Chu, J.-J. Shyue, Effect of Surface Potential on Extracellular Matrix Protein Adsorption, Langmuir. 30 (2014) 10328-10335. doi:10.1021/la5020362.
  51. D. Smoleń, T. Chudoba, S. Gierlotka, A. Kedzierska, W. Łojkowski, K. Sobczak, W. Świȩszkowski, K.J. Kurzydłowski, Hydroxyapatite nanopowder synthesis with a programmed resorption rate, J. Nanomater. 2012 (2012). doi:10.1155/2012/841971.
  52. I.W. Bauer, S.-P. Li, Y.-C. Han, L. Yuan, M.-Z. Yin, Internalization of hydroxyapatite nanoparticles in liver cancer cells, J. Mater. Sci. Mater. Med. 19 (2008) 1091-1095. doi:10.1007/s10856-007-3124-4.
  53. Y. Han, S. Li, X. Cao, L. Yuan, Y. Wang, Y. Yin, T. Qiu, H. Dai, X. Wang, Different Inhibitory Effect and Mechanism of Hydroxyapatite Nanoparticles on Normal Cells and Cancer Cells In Vitro and In Vivo, Sci. Rep. 4 (2014) 7134. doi:10.1038/srep07134.
  54. J. Solon, I. Levental, K. Sengupta, P.C. Georges, P.A. Janmey, F.C. MacKintosh, D. Stamenovic, F. Gallet, A. Bershadsky, L. Addadi, B. Geiger, V.M. Weaver, Fibroblast adaptation and stiffness matching to soft elastic substrates., Biophys. J. 93 (2007) 4453-61. doi:10.1529/biophysj.106.101386.
  55. C. Branco, D.D. Klumpers, W.A. Li, S.T. Koshy, J.C. Weaver, O. Chaudhuri, P.L. Granja, D.J. Mooney, Influence of the stiffness of three-dimensional alginate/collagen-I interpenetrating networks on fibroblast biology, Biomaterials. 35 (2014) 8927-8936. doi:10.1016/j.biomaterials.2014.06.047.