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A Materials Perspective on the Design of Damage-Resilient Bone Implants Through Additive/Advanced Manufacturing

  • Hortense Le FerrandEmail author
  • Christos E. Athanasiou
Advanced Manufacturing for Biomaterials and Biological Materials

Abstract

After more than 5 decades of research, the failure of bone implants is still poorly understood. The aging population makes it increasingly urgent to solve this issue. Among the reasons for failure, catastrophic brittle fracture can be directly related to the implant material and fabrication and deserves more attention. Indeed, clinically available implants do not sufficiently reproduce the hierarchical and heterogeneous microstructural organization of our natural bones, ultimately failing at replicating their mechanical strength and toughness. Nevertheless, recent advances in additive and advanced manufacturing have opened new horizons for the fabrication of biomimetic bone implants, challenging at the same time their characterization, testing, and modeling. This critical review covers selected recent achievements in bone implant research from a materials standpoint and aims at deciphering some of the most urgent issues in this multidisciplinary field.

Notes

Acknowledgements

H. L. F. acknowledges financial support from Nanyang Technological University with the Start-Up grant M4082382.050 and discussions with Dr. F. Bouville and Prof. S.-H. Teoh. C. E. A. acknowledges valuable discussions with Mr. X. Liu and Mr. T. Cai concerning the proofreading the manuscript.

Supplementary material

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Supplementary material 1 (PDF 109 kb)

References

  1. 1.
    H.M. Kremers, D.R. Larson, C.S. Crowson, W.K. Kremers, R.E. Washington, C.A. Steiner, W.A. Jiranek, and D.J. Berry, J. Bone Joint Surg. 97, 1386 (2015).CrossRefGoogle Scholar
  2. 2.
    C. Cheung, S. Bin, M. Chadha, E.S. Chow, Y. Chung, F. Lee, U. Jaisamrarn, H. Ng, Y. Takeuchi, C. Wu, W. Xia, J. Yu, and S. Fujiwara, Osteoporos. Sarcopenia 4, 16 (2018).CrossRefGoogle Scholar
  3. 3.
    K.L. Corbett, E. Losina, A.A. Nti, J.J.Z. Prokopetz, and J.N. Katz, PLoS ONE 5, e13520 (2010).CrossRefGoogle Scholar
  4. 4.
    L.E. Bayliss, D. Culliford, A.P. Monk, S. Glyn-jones, D. Prieto-alhambra, A. Judge, C. Cooper, A.J. Carr, N.K. Arden, D.J. Beard, and A.J. Price, Lancet 389, 1424 (2017).CrossRefGoogle Scholar
  5. 5.
    A.M. Elbuluk, A.B. Old, J.A. Bosco, R. Schwarzkopf, and R. Iorio, Arthroplast. Today 3, 286 (2017).CrossRefGoogle Scholar
  6. 6.
    M. Weber, T. Renkawitz, F. Voellner, B. Craiovan, F. Greimel, M. Worlicek, J. Grifka, and A. Benditz, Biomed. Res. Int. 2018, 8987104 (2018).Google Scholar
  7. 7.
    M. Dhima, V. Paulusova, A.B. Carr, K.L. Rieck, C. Lohse, and T.J. Salinas, J. Prosthet. Dent. 111, 124 (2014).CrossRefGoogle Scholar
  8. 8.
    A. Marshall, M.D. Ries, and W. Paprosky, J. Am. Acad. Orthop. Surg. 16, 1 (2008).CrossRefGoogle Scholar
  9. 9.
    S.H. Teoh, Int. J. Fatigue 22, 825 (2000).CrossRefGoogle Scholar
  10. 10.
    L. Ewart and S. Suresh, J. Mater. Sci. 22, 1173 (1987).CrossRefGoogle Scholar
  11. 11.
    K. Man, L. Jiang, R. Foster, and X.B. Yang, J. Funct. Biomater. 8, 33 (2017).CrossRefGoogle Scholar
  12. 12.
    E. Gibon, L. Lu, T. Lin, Z. Yao, S.B. Goodman, H. Cochin, and M. Surgery, J. Biomed. Mater. Res. B Appl. Biomater. 105, 1685 (2017).CrossRefGoogle Scholar
  13. 13.
    A.J.S. Fox, A. Bedi, and S.A. Rodeo, Sports Health 1, 461 (2009).CrossRefGoogle Scholar
  14. 14.
    A.J. Kerin, M.R. Wisnom, and M.A. Adams, Proc. Inst. Mech. Eng. Part H J. Eng. Med. 212, 273 (1998).CrossRefGoogle Scholar
  15. 15.
    Y. Xiao, D.A. Rennerfeldt, E.A. Friis, S.H. Gehrke, and M.S. Detamore, J. Tissue Eng. Regen. Med. 11, 121 (2017).CrossRefGoogle Scholar
  16. 16.
    A.J. Teichtahl, A.E. Wluka, P. Wijethilake, Y. Wang, A. Ghasem-zadeh, and F.M. Cicuttini, Arthritis Res. Ther. 17, 207 (2015).CrossRefGoogle Scholar
  17. 17.
    R.J. Mogil, S.C. Kaste, R.J. Ferry, M.M. Hudson, D.A. Mulrooney, C.R. Howell, R.E. Partin, D.K. Srivastava, L.L. Robison, and K.K. Ness, JAMA Oncol. 2, 908 (2016).CrossRefGoogle Scholar
  18. 18.
    V. Ruprecht, P. Monzo, A. Ravasio, Z. Yue, E. Makhija, P.O. Strale, N. Gauthier, G.V. Shivashankar, V. Studer, C. Albiges-rizo, and V. Viasnoff, J. Cell Sci. 130, 51 (2017).CrossRefGoogle Scholar
  19. 19.
    M. Sobieraj and C. Rimnac, J. Mech. Behav. Biomed. Mater. 2, 433 (2009).CrossRefGoogle Scholar
  20. 20.
    B. Weightman, S.A. Swanson, G.H. Isaac, and B.M. Wroblewski, J. Bone Joint Surg. 73, 806 (1991).CrossRefGoogle Scholar
  21. 21.
    V. Ooij, S.M. Kurtz, F. Stessels, H. Noten, and L. Van Rhijn, Spine (Phila. Pa. 1976) 32, 223 (2007).CrossRefGoogle Scholar
  22. 22.
    B.M.E. Launey and R.O. Ritchie, Adv. Mater. 21, 2103 (2009).CrossRefGoogle Scholar
  23. 23.
    W. Huang, D. Restrepo, J.Y. Jung, F.Y. Su, Z. Liu, R.O. Ritchie, J. McKittrick, P. Zavattieri, and D. Kisailus, Adv. Mater. 1901561, 1 (2019).Google Scholar
  24. 24.
    K.J. Koester, J.W. Ager, and R.O. Ritchie, Nat. Mater. 7, 672 (2008).CrossRefGoogle Scholar
  25. 25.
    M.E. Launey, P.Y. Chen, J. McKittrick, and R.O. Ritchie, Acta Biomater. 6, 1505 (2010).CrossRefGoogle Scholar
  26. 26.
    D.R. Pedersen, R.D. Crowninshield, R.A. Brand, and R.C. Johnston, J. Biomech. 15, 305 (1982).CrossRefGoogle Scholar
  27. 27.
    J.A. Rodriguez and H.J. Cooper, Bone Joint J. 95-B, 63 (2013).CrossRefGoogle Scholar
  28. 28.
    L.C. Zhang, E.C.S. Kiat, and A. Pramanik, Adv. Mater. Res. 78, 212 (2009).CrossRefGoogle Scholar
  29. 29.
    K. Colic, A. Sedmak, A. Grbovic, U. Tatic, and S. Sedmak, Procedia Eng. 149, 257 (2016).CrossRefGoogle Scholar
  30. 30.
    J.C. Koch, Am. J. Anat. 21, 177 (1917).CrossRefGoogle Scholar
  31. 31.
    T. Macirowsk, S. Topic, and R.W. Mann, J. Biomech. Eng. 116, 10 (1994).CrossRefGoogle Scholar
  32. 32.
    G.A.P. Renders, L. Mulder, L.J. Van Ruijven, and T.M.G.J. Van Eijden, J. Anat. 210, 239 (2007).CrossRefGoogle Scholar
  33. 33.
    G. Osterhoff, E.F. Morgan, S.J. Shefelbine, L. Karim, L.M. McNamara, and P. Augat, Injury 47, 11 (2016).CrossRefGoogle Scholar
  34. 34.
    R. Müller, Nat. Rev. Rheumatol. 5, 373 (2009).CrossRefGoogle Scholar
  35. 35.
    J. Mckittrick, P. Chen, L. Tombolato, E.E. Novitskaya, M.W. Trim, G.A. Hirata, E.A. Olevsky, M.F. Horstemeyer, and M.A. Meyers, Mater. Sci. Eng. C 30, 331 (2010).CrossRefGoogle Scholar
  36. 36.
    E. Novitskaya, P.-Y. Chen, E. Hamed, J. Li, V.A. Lubarda, I. Jasiuk, and J. McKittrick, Theor. Appl. Mech. 38, 209 (2011).MathSciNetCrossRefGoogle Scholar
  37. 37.
    F.A. Shah, Bone Res. 7, 1 (2019).CrossRefGoogle Scholar
  38. 38.
    A.G. Reisinger, D.H. Pahr, and P.K. Zysset, J. Mech. Behav. Biomed. Mater. 4, 2113 (2011).CrossRefGoogle Scholar
  39. 39.
    J.G. Kennedy and D.R. Carter, J. Biomech. Eng. 107, 183 (1985).CrossRefGoogle Scholar
  40. 40.
    A. Gustafsson, M. Wallin, H. Khayyeri, and H. Isaksson, Biomech. Model. Mechanobiol. 18, 1247 (2019).CrossRefGoogle Scholar
  41. 41.
    S.J. Eppell, W. Tong, J.L. Katz, L. Kuhn, and M.J. Glimcher, J. Orthop. Res. 19, 1027 (2001).CrossRefGoogle Scholar
  42. 42.
    D.S. Bocciarelli, Calcif. Tissue Res. 5, 261 (1970).CrossRefGoogle Scholar
  43. 43.
    M.P.E. Wenger, L. Bozec, M.A. Horton, and P. Mesquida, Biophys. J. 93, 1255 (2007).CrossRefGoogle Scholar
  44. 44.
    W.S. William and L. Breger, J. Biomech. 8, 407 (1975).CrossRefGoogle Scholar
  45. 45.
    M.H. Shamos, Nature 4, 1963 (1963).Google Scholar
  46. 46.
    U.G.K. Wegst, H. Bai, E. Saiz, A.P. Tomsia, and R.O. Ritchie, Nat. Mater. 14, 23 (2015).CrossRefGoogle Scholar
  47. 47.
    V. Imbeni, J.J. Kruzic, G.W. Marshall, S.J. Marshall, and R.O. Ritchie, Nat. Mater. 4, 229 (2005).CrossRefGoogle Scholar
  48. 48.
    S.R. Oungoulian, K.M. Durney, B.K. Jones, C.S. Ahmad, T. Clark, and G.A. Ateshian, J. Biomech. 2015 Jul 16;48(10) 48, 1957 (2016).Google Scholar
  49. 49.
    O. Franke, K. Durst, V. Maier, M. Göken, T. Birkholz, H. Schneider, F. Hennig, and K. Gelse, Acta Biomater. 3, 873 (2007).CrossRefGoogle Scholar
  50. 50.
    M. Canillas, P. Pena, A.H. De Aza, and M.A. Rodríguez, Boletín La Soc. Española Cerámica y Vidr. 56, 91 (2017).CrossRefGoogle Scholar
  51. 51.
    C.-H. Liu, C.-J. Lin, Y.-H. Hu, and Z.-H. You, Appl. Sci. 8, 698 (2018).CrossRefGoogle Scholar
  52. 52.
    C.T. Chen and G.X. Gu, MRS Commun. 9, 556 (2019).CrossRefGoogle Scholar
  53. 53.
    K.G. Reyes and B. Maruyama, MRS Bull. 44, 530 (2019).CrossRefGoogle Scholar
  54. 54.
    S.J. Mary and S. Rajendran, Zast. Mater. 53, 181 (2012).Google Scholar
  55. 55.
    J. Jeong, J.H. Kim, J.H. Shim, N.S. Hwang, and C.Y. Heo, Biomater. Res. 23, 1 (2019).CrossRefGoogle Scholar
  56. 56.
    A. Abdel-Wahab, N. Nordin, and V. Silberschmidt, J. Phys. Conf. Ser. 382, 0 (2012).Google Scholar
  57. 57.
    M.E. Launey, M.J. Buehler, and R.O. Ritchie, Annu. Rev. Mater. Res. 40, 25 (2010).CrossRefGoogle Scholar
  58. 58.
    R.O. Ritchie, J.H. Kinney, J.J. Kruzic, and R.K. Nalla, Fatigue Fract. Eng. Mater. Struct. 28, 345 (2005).CrossRefGoogle Scholar
  59. 59.
    E.N. Brown, S.R. White, and N.R. Sottos, J. Mater. Sci. 41, 6266 (2006).CrossRefGoogle Scholar
  60. 60.
    R.R. Adharapurapu, K.S. Vecchio, F. Jiang, and A. Rohatgi, Metall. Mater. Trans. A Phys. Metall. Mater. Sci. 36, 1595 (2005).CrossRefGoogle Scholar
  61. 61.
    R.O. Ritchie, Nat. Mater. 10, 817 (2011).CrossRefGoogle Scholar
  62. 62.
    B. Lawn, Fracture of Brittle Solids, 2nd ed. (Cambridge: Cambridge University Press, 1993).CrossRefGoogle Scholar
  63. 63.
    A.G. Evans, J. Am. Ceram. Soc. 73, 187 (1990).CrossRefGoogle Scholar
  64. 64.
    N. Padture, J. Am. Ceram. Soc. 77, 519 (1994).CrossRefGoogle Scholar
  65. 65.
    Y. Yang, C. Ramirez, X. Wang, Z. Guo, A. Tokranov, R. Zhao, I. Szlufarska, J. Lou, and B.W. Sheldon, Carbon N. Y. 115, 402 (2017).CrossRefGoogle Scholar
  66. 66.
    B.W. Sheldon, E.Y. Sun, S.R. Nutt, and J.J. Brennan, J. Am. Ceram. Soc. 79, 539 (1996).CrossRefGoogle Scholar
  67. 67.
    S. Mohammad, M. Valashani, and F. Barthelat, Bioinspir. Biomim. 10, 26005 (2015).CrossRefGoogle Scholar
  68. 68.
    M. Mirkhalaf, T. Zhou, and F. Barthelat, PNAS 115, 9128 (2018).CrossRefGoogle Scholar
  69. 69.
    F. Lee, M.S. Sandlin, and K.J. Bowman, J. Am. Ceram. Soc. 76, 1793 (1993).CrossRefGoogle Scholar
  70. 70.
    X. Zhu and Y. Sakka, Sci. Technol. Adv. Mater. 9, 1 (2008).CrossRefGoogle Scholar
  71. 71.
    F. Barthelat, H. Tang, P.D. Zavattieri, and H.D. Espinosa, J. Mech. Phys. Solids 55, 306 (2007).CrossRefGoogle Scholar
  72. 72.
    J. Sun and B. Bhushan, RSC Adv. 2, 7617 (2012).CrossRefGoogle Scholar
  73. 73.
    U. Pasqualini and M.E. Pasqualini, Ariesdue 4, 1 (2009).Google Scholar
  74. 74.
    G. Atlan, O. Delattre, S. Berland, A. Lefaou, G. Nabias, D. Cot, and E. Lopez, Biomaterials 20, 1017 (1999).CrossRefGoogle Scholar
  75. 75.
    S. Berland, O. Delattre, S. Borzeix, Y. Catonné, and E. Lopez, Biomaterials 26, 2767 (2005).CrossRefGoogle Scholar
  76. 76.
    V. Moby, G. Zhang, A. Brion, A. Willemin, A. Bianchi, D. Mainard, L. Galois, P. Gillet, and M. Rousseau, J. Biomed. Mater. Res. A 105A, 662 (2017).Google Scholar
  77. 77.
    H. Le Ferrand, F. Bouville, T.P. Niebel, and A.R. Studart, Nat. Mater. 14, 1172 (2015).CrossRefGoogle Scholar
  78. 78.
    T.P. Niebel, F. Bouville, D. Kokkinis, and A.R. Studart, J. Mech. Phys. Solids 96, 133 (2016).CrossRefGoogle Scholar
  79. 79.
    Y. Yang, X. Li, M. Chu, H. Sun, J. Jin, K. Yu, Q. Wang, Q. Zhou, and Y. Chen, Sci. Adv. 5, 1 (2019).Google Scholar
  80. 80.
    C. Huang, J. Peng, Y. Cheng, Q. Zhao, Y. Du, S. Dou, A.P. Tomsia, H.D. Wagner, L. Jiang, and Q. Cheng, J. Mater. Chem. A 7, 2787 (2019).CrossRefGoogle Scholar
  81. 81.
    M.E. Launey, E. Munch, D.H. Alsem, E. Saiz, A.P. Tomsia, and R.O. Ritchie, J. R. Soc. Interface 7, 741 (2010).CrossRefGoogle Scholar
  82. 82.
    A. Wat, J.I. Lee, C.W. Ryu, B. Gludovatz, J. Kim, A.P. Tomsia, T. Ishikawa, J. Schmitz, A. Meyer, M. Alfreider, D. Kiener, E.S. Park, and R.O. Ritchie, Nat. Commun. 10, 1 (2019).CrossRefGoogle Scholar
  83. 83.
    U.G.K. Wegst, M. Schecter, A.E. Donius, and P.M. Hunger, Philos. Trans. R. Soc. A Math. Phys. Eng. Sci. 368, 2099 (2010).CrossRefGoogle Scholar
  84. 84.
    S. Deville, E. Saiz, and A.P. Tomsia, Biomaterials 27, 5480 (2006).CrossRefGoogle Scholar
  85. 85.
    J. Ni, H. Ling, S. Zhang, Z. Wang, and Z. Peng, Materials Today Bio. 3, 24 (2019).CrossRefGoogle Scholar
  86. 86.
    R. Masaeli, K. Zandsalimi, M. Rasoulianboroujeni, and L. Tayebi, Tissue Eng. Part B Rev. 25, 387 (2019).CrossRefGoogle Scholar
  87. 87.
    U. Heise, J.F. Osborn, and F. Duwe, Int. Orthop. 14, 329 (1990).CrossRefGoogle Scholar
  88. 88.
    H.N.W. Lekkerkerker and G.J. Vroege, Philos. Trans. R Soc. A 371, 263 (2013).CrossRefGoogle Scholar
  89. 89.
    K. Thorkelsson, P. Bai, and T. Xu, Nano Today 10, 48 (2015).CrossRefGoogle Scholar
  90. 90.
    L. Onsager, Ann. N. Y. Acad. Sci. 51, 627 (1949).CrossRefGoogle Scholar
  91. 91.
    H.N.W. Lekkerkerker and G.J. Vroege, Philos. Trans. R. Soc. A Math. Phys. Eng. Sci. 371, 263 (2013).CrossRefGoogle Scholar
  92. 92.
    W. Xue and G.S. Grest, Phys. Rev. Lett. 64, 419 (1990).CrossRefGoogle Scholar
  93. 93.
    D. Yunus, Y. Shi, S. Sohrabi, and Y. Liu, Nanotechnology 27, 0 (2016).CrossRefGoogle Scholar
  94. 94.
    I. Nelson and S.E. Naleway, Integr. Med. Res. 8, 2372 (2019).Google Scholar
  95. 95.
    H. Watanabe, T. Kimura, and T. Yamaguchi, J. Am. Ceram. Soc. 72, 189 (1989).Google Scholar
  96. 96.
    A. Garbin, I. Leibacher, P. Hahn, H. Le Ferrand, A. Studart, and J. Dual, J. Acoust. Soc. Am. 138, 2759 (2015).CrossRefGoogle Scholar
  97. 97.
    H. Le Ferrand, F. Bouville, and A.R. Studart, Soft Matter 15, 3886 (2019).CrossRefGoogle Scholar
  98. 98.
    S. Wu, S. Peng, and C.H. Wang, Polymers (Basel) 10, 542 (2018).CrossRefGoogle Scholar
  99. 99.
    D. Velegol, A. Garg, R. Guha, A. Kar, and M. Kumar, Soft Matter 12, 4686 (2016).CrossRefGoogle Scholar
  100. 100.
    P. Warren, Nature 429, 822 (2004).CrossRefGoogle Scholar
  101. 101.
    A.F. Demirörs, P.P. Pillai, B. Kowalczyk, and B.A. Grzybowski, Nature 503, 99 (2013).CrossRefGoogle Scholar
  102. 102.
    D. Kokkinis, M. Schaffner, and A.R. Studart, Nat. Commun. 45, 333 (2015).Google Scholar
  103. 103.
    R. Libanori, R.M. Erb, A. Reiser, H. Le Ferrand, M.J. Süess, R. Spolenak, and A.R. Studart, Nat. Commun. 3, 1 (2012).CrossRefGoogle Scholar
  104. 104.
    F.L. Bargardi, H. Le Ferrand, R. Libanori, and A.R. Studart, Nat. Commun. 7, 1 (2016).CrossRefGoogle Scholar
  105. 105.
    L. Bracaglia, B.T. Smith, E. Watson, N. Arumugasaamy, A.G. Mikos, and J.P. Fisher, Acta Biomater. 25, 289 (2016).Google Scholar
  106. 106.
    S.M. Bittner, B.T. Smith, L. Diaz-Gomez, C.D. Hudgins, A.J. Melchiorri, D.W. Scott, J.P. Fisher, and A.G. Mikos, Acta Biomater. 90, 37 (2019).CrossRefGoogle Scholar
  107. 107.
    B.P. Greil, Adv. Eng. Mater. 2, 339 (2000).CrossRefGoogle Scholar
  108. 108.
    J.J. Martin, B.E. Fiore, and R.M. Erb, Nat. Commun. 6, 1 (2015).Google Scholar
  109. 109.
    E. Munch, M.E. Launey, D.H. Alsem, E. Saiz, A.P. Tomsia, and R.O. Ritchie, Science (80-) 322, 1516 (2008).CrossRefGoogle Scholar
  110. 110.
    F. Bouville, E. Maire, S. Meille, B. Van De Moortèle, and A.J. Stevenson, Nat. Mater. 13, 508 (2014).CrossRefGoogle Scholar
  111. 111.
    H. Le Ferrand, J. Mater. Res. 34, 169 (2019).CrossRefGoogle Scholar
  112. 112.
    P. Niksiar, F.Y. Su, M.B. Frank, T.A. Ogden, S.E. Naleway, M.A. Meyers, J. Mckittrick, and M.M. Porter, Ceramics 2, 1 (2019).CrossRefGoogle Scholar
  113. 113.
    Z. Hu, X. Shen, S. Geng, P. Shen, and Q. Jiang, Ceram. Int. 44, 5803 (2018).CrossRefGoogle Scholar
  114. 114.
    C. Wang, X. Chen, B. Wang, M. Huang, B. Wang, Y. Jiang, and R.S. Ruo, ACS Nano 12, 5816 (2018).CrossRefGoogle Scholar
  115. 115.
    H. Bai, F. Walsh, B. Gludovatz, B. Delattre, C. Huang, Y. Chen, A.P. Tomsia, and R.O. Ritchie, Adv. Mater. 2, 50 (2016).CrossRefGoogle Scholar
  116. 116.
    K.L. Scotti and D.C. Dunand, Prog. Mater Sci. 94, 243 (2018).CrossRefGoogle Scholar
  117. 117.
    H. Le Ferrand and F. Bouville, J. Am. Ceram. Soc. 102, 7253 (2019).CrossRefGoogle Scholar
  118. 118.
    B.R. Marple and S. Tuffe, in Functionally Graded Materials, edited by I. Shiota and M. Miyamoto, pp. 159–166 (1997).Google Scholar
  119. 119.
    S. Gantenbein, K. Masania, W. Woigk, J.P.W. Sesseg, T.A. Tervoort, and A.R. Studart, Nature 561, 226 (2018).CrossRefGoogle Scholar
  120. 120.
    E. Feilden, C. Ferraro, Q. Zhang, E. García-Tuñón, E. D’Elia, F. Giuliani, L. Vandeperre, and E. Saiz, Sci. Rep. 7, 1 (2017).CrossRefGoogle Scholar
  121. 121.
    S. Deville, E. Saiz, R.K. Nalla, and A.P. Tomsia, Science (80-) 311, 1 (2006).CrossRefGoogle Scholar
  122. 122.
    Y. Tang, Q. Miao, S. Qiu, K. Zhao, and L. Hu, J. Eur. Ceram. Soc. 34, 4077 (2014).CrossRefGoogle Scholar
  123. 123.
    S. Amini, A. Masic, L. Bertinetti, J.S. Teguh, J.S. Herrin, X. Zhu, H. Su, and A. Miserez, Nat. Commun. 5, 1 (2014).CrossRefGoogle Scholar
  124. 124.
    M. Sebastiani, K.E. Johanns, E.G. Herbert, and G.M. Pharr, Curr. Opin. Solid State Mater. Sci. 19, 324 (2015).CrossRefGoogle Scholar
  125. 125.
    M. Grossman, F. Bouville, F. Erni, K. Masania, R. Libanori, and A.R. Studart, Adv. Mater. 29, 1 (2017).CrossRefGoogle Scholar
  126. 126.
    B. Lawn, A.G. Evans, and D. Marshall, J. Am. Ceram. Soc. 63, 574 (1980).CrossRefGoogle Scholar
  127. 127.
    B.W. Sheldon and W.A. Curtin, Nat. Mater. 3, 505 (2004).CrossRefGoogle Scholar
  128. 128.
    J. Rice, J. Appl. Mech. 35, 379 (1968).CrossRefGoogle Scholar
  129. 129.
    C.E. Athanasiou, M.O. Hongler, and Y. Bellouard, Phys. Rev. Appl. 8, 1 (2017).CrossRefGoogle Scholar
  130. 130.
    C.E. Athanasiou and Y. Bellouard, Micromachines 6, 1365 (2015).CrossRefGoogle Scholar
  131. 131.
    Z. Jia and L. Wang, Acta Mater. 173, 61 (2019).CrossRefGoogle Scholar
  132. 132.
    ASTM C1421-18, Standard Test Methods for Determination of Fracture Toughness of Advanced Ceramics at Ambient Temperature (ASTM International, West Conshohocken, PA, 2018).Google Scholar
  133. 133.
    P.Y. Chen, A.G. Stokes, and J. McKittrick, Acta Biomater. 5, 693 (2009).CrossRefGoogle Scholar
  134. 134.
    T. Nose and T. Fujii, J. Am. Ceram. Soc. 71, 328 (1988).CrossRefGoogle Scholar
  135. 135.
    F. Bouville, E. Maire, S. Meille, B. Van de Moortèle, A.J. Stevenson, and S. Deville, arXiv 1707.09528, 2 (2017).Google Scholar
  136. 136.
    J.Y. Buffiere, E. Maire, J. Adrien, J.P. Masse, and E. Boller, Proc. Soc. Exp. Mech. 67, 289 (2010).CrossRefGoogle Scholar
  137. 137.
    J. Réthoré, N. Limodin, J.Y. Buffière, S. Roux, and F.Ç. Hild, Procedia IUTAM 4, 151 (2012).CrossRefGoogle Scholar
  138. 138.
    S.C. Wu, T.Q. Xiao, and P.J. Withers, Eng. Fract. Mech. 182, 127 (2017).CrossRefGoogle Scholar
  139. 139.
    H. Le Ferrand, F. Bouville, T.P. Niebel, and A.R. Studart, Nat. Mater. 16, 1272 (2017).CrossRefGoogle Scholar
  140. 140.
    J. Ast, M. Ghidelli, K. Durst, M. Göken, M. Sebastiani, and A.M. Korsunsky, Mater. Des. 173, 107762 (2019).CrossRefGoogle Scholar
  141. 141.
    R.O. Ritchie, K.J. Koester, S. Ionova, W. Yao, N.E. Lane, and J.W. Ager III, Bone 23, 1 (2008).Google Scholar
  142. 142.
    F. Barthelat, A.K. Dastjerdi, and R. Rabiei, J. R. Soc. Interface 10, 849 (2013).Google Scholar
  143. 143.
    D.M. Ebenstein and L.A. Pruitt, Nano Today 1, 26 (2006).CrossRefGoogle Scholar
  144. 144.
    F. Haque, Surf. Eng. 19, 255 (2003).CrossRefGoogle Scholar
  145. 145.
    L.V. Coutts, T. Jenkins, T. Li, D.G. Dunlop, R.O.C. Oreffo, C. Cooper, N.C. Harvey, P.J. Thurner, N.K. Arden, J.M. Latham, P. Taylor, M. Baxter, N. Moss, C. Ball, and K. Chan, J. Mech. Behav. Biomed. Mater. 46, 292 (2015).CrossRefGoogle Scholar
  146. 146.
    R. Sonntag, S. Braun, L. Al-Salehi, J. Reinders, U. Mueller, and J.P. Kretzer, PLoS ONE 12, 1 (2017).Google Scholar
  147. 147.
    A. Ravichandran, F. Wen, J. Lim, M.S.K. Chong, J.K.Y. Chan, and S.H. Teoh, J. Tissue Eng. Regen. Med. 12, e2039 (2018).CrossRefGoogle Scholar
  148. 148.
    E.A. Zimmermann, E. Schaible, H. Bale, H.D. Barth, S.Y. Tang, P. Reichert, B. Busse, T. Alliston, J.W. Ager, and R.O. Ritchie, Proc. Natl. Acad. Sci. USA 109, 11890 (2012).CrossRefGoogle Scholar
  149. 149.
    J.J. Kruzic, D.K. Kim, K.J. Koester, and R.O. Ritchie, J. Mech. Behav. Biomed. Mater. 2, 384 (2009).CrossRefGoogle Scholar
  150. 150.
    M. Zalaznik, S. Novak, M. Huskić, and M. Kalin, Lubr. Sci. 28, 27 (2016).CrossRefGoogle Scholar
  151. 151.
    M.Z. Hossain, C.J. Hsueh, B. Bourdin, and K. Bhattacharya, J. Mech. Phys. Solids 71, 15 (2014).MathSciNetCrossRefGoogle Scholar
  152. 152.
    C.J. Hsueh and K. Bhattacharya, J. Appl. Mech. Trans. ASME 83, 1 (2016).CrossRefGoogle Scholar
  153. 153.
    R. Liu, A. Kumar, Z. Chen, A. Agrawal, V. Sundararaghavan, and A. Choudhary, Sci. Rep. 5, 1 (2015).Google Scholar
  154. 154.
    G.X. Gu, C.T. Chen, D.J. Richmond, and M.J. Buehler, Mater. Horiz. 5, 939 (2018).CrossRefGoogle Scholar

Copyright information

© The Minerals, Metals & Materials Society 2020

Authors and Affiliations

  1. 1.School of Mechanical and Aerospace Engineering, School of Materials Science and EngineeringNanyang Technological UniversitySingaporeSingapore
  2. 2.School of EngineeringBrown UniversityProvidenceUSA

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