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Multiscaling for Molecular Models to Predict Lab Scale Sample Properties: A Review of Phenomenological Models

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Abstract

One of the defining features of biological materials is that they are highly hierarchical with different structures at different length scales. Often they are complex nanocomposites of soft fibrous polymeric phase and hard mineral phase. For instance, bone has up to seven levels of hierarchy and nacre shows up to six levels of hierarchal structure. In spite of complex hierarchical structures, the smallest building blocks in such biological materials are at the nanometer length scale. The extent of interfacial interaction and the interfacial arrangement are important determinants of the structure–function property relationship of biomaterials and influence the mechanical strength substantially. Challenges lie in identifying nature’s mechanisms behind imparting such properties and its pathways in fabricating and optimizing these composites. The key here is the formation of large amount of precisely and carefully designed organic–inorganic interfaces and synergy of mechanisms acting over multiple scales to distribute loads and damage, dissipate energy, and resist change in properties owing to damages such as cracking. This chapter presents a brief overview of the role of interfacial structural design and interfacial forces in imparting superior mechanical performance to hard biological materials. Focus is on understanding the underlying engineering principles of nature’s materials for use in biomedical engineering and biomaterial development.

Keywords

Phenomenological models Biological materials Effect of interfaces Hierarchical modeling Multiscale modeling 

References

  1. 1.
  2. 2.
    G.E. Fantner et al., Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nat. Mater. 4, 612–616 (2005)CrossRefPubMedGoogle Scholar
  3. 3.
    J.D. Currey, Mechanical-properties of mother of pearl in tension. Proc. R. Soc. Lond. B Biol. Sci. 196, 443–463 (1977)CrossRefGoogle Scholar
  4. 4.
    F. Barthelat, Biomimetics for next generation materials. Philos. Trans. R. Soc. A Math. Phys. Eng. Sci. 365, 2907–2919 (2007). doi: 10.1098/rsta.2007.0006 CrossRefGoogle Scholar
  5. 5.
    J.Y. Rho, L. Kuhn-Spearing, P. Zioupos, Mechanical properties and the hierarchical structure of bone. Med. Eng. Phys. 20, 92–102 (1998)CrossRefPubMedGoogle Scholar
  6. 6.
    S. Weiner, H.D. Wagner, The material bone: structure mechanical function relations. Annu. Rev. Mater. Sci. 28, 271–298 (1998)CrossRefGoogle Scholar
  7. 7.
    H.J. Gao, B.H. Ji, I.L. Jager, E. Arzt, P. Fratzl, Materials become insensitive to flaws at nanoscale: lessons from nature. Proc. Natl. Acad. Sci. U. S. A. 100, 5597–5600 (2003). doi: 10.1073/pnas.0631609100 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    R. Vaia, Polymer nanocomposites: status and opportunities. MRS Bull. (USA) 26, 394–401 (2001)CrossRefGoogle Scholar
  9. 9.
    D.K. Dubey, V. Tomar, Role of the nanoscale interfacial arrangement in mechanical strength of tropocollagen-hydroxyapatite based hard biomaterials. Acta Biomater. 5, 2704–2716 (2009). doi: 10.1016/j.actbio.2009.02.035 CrossRefPubMedGoogle Scholar
  10. 10.
    W.J. Landis, K.J. Hodgens, J. Arena, M.J. Song, B.F. McEwen, Structural relations between collagen and mineral in bone as determined by high voltage electron microscopic tomography. Microsc. Res. Tech. 33, 192–202 (1996)CrossRefPubMedGoogle Scholar
  11. 11.
    W.J. Landis et al., Mineralization of collagen may occur on fibril surfaces: evidence from conventional and high-voltage electron microscopy and three-dimensional imaging. J. Struct. Biol. 117, 24–35 (1996)CrossRefPubMedGoogle Scholar
  12. 12.
    P. Fratzl, N. Fratzlzelman, K. Klaushofer, G. Vogl, K. Koller, Nucleation and growth of mineral crystals in bone studied by small-angle X-ray scattering. Calcif. Tissue Int. 48, 407–413 (1991)CrossRefPubMedGoogle Scholar
  13. 13.
    D.K. Dubey, V. Tomar, Role of the nanoscale interfacial arrangement in mechanical strength of tropocollagen-hydroxyapatite based hard biomaterials. Acta Biomater. 5, 2704–2716 (2009). doi: 10.1016/j.actbio.2009.02.035 CrossRefPubMedGoogle Scholar
  14. 14.
    D.K. Dubey, V. Tomar, Understanding the influence of structural hierarchy and its coupling with chemical environment on the strength of idealized tropocollagen-hydroxyapatite biomaterials. J. Mech. Phys. Solid 57, 1702–1717 (2009)CrossRefGoogle Scholar
  15. 15.
    D.K. Dubey, V. Tomar, Effect of tensile and compressive loading on hierarchical strength of idealized tropocollagen-hydroxyapatite biomaterials as a function of chemical environment. J. Phys. Condens. Matter 21, 205103 (2009)CrossRefPubMedGoogle Scholar
  16. 16.
    P. Fratzl, R. Weinkamer, Nature’s hierarchical materials. Prog. Mater. Sci. 52, 1263–1334 (2007)CrossRefGoogle Scholar
  17. 17.
    M.A. Meyers, P.Y. Chen, A.Y.M. Lin, Y. Seki, Biological materials: structure and mechanical properties. Prog. Mater. Sci. 53, 1–206 (2008). doi: 10.1016/j.pmatsci.2007.05.002 CrossRefGoogle Scholar
  18. 18.
    M.E. Launey, R.O. Ritchie, On the fracture toughness of advanced materials. Adv. Mater. 21, 2103–2110 (2009). doi: 10.1002/adma.200803322 CrossRefGoogle Scholar
  19. 19.
    D.K. Dubey, V. Tomar, Understanding the influence of structural hierarchy and its coupling with chemical environment on the strength of idealized tropocollagen–hydroxyapatite biomaterials. J. Mech. Phys. Solid 57, 1702–1717 (2009). doi: 10.1016/j.jmps.2009.07.002 CrossRefGoogle Scholar
  20. 20.
    D.K. Dubey, V. Tomar, The effect of tensile and compressive loading on the hierarchical strength of idealized tropocollagen-hydroxyapatite biomaterials as a function of the chemical environment. J. Phys. Condens. Matter 21, 205103 (2009). doi: 10.1088/0953-8984/21/20/205103 CrossRefPubMedGoogle Scholar
  21. 21.
    M.J. Buehler, Nanomechanics of collagen fibrils under varying cross-link densities: atomistic and continuum studies. J. Mech. Behav. Biomed. Mater. 1, 59–67 (2008)CrossRefPubMedGoogle Scholar
  22. 22.
    A.D. Simone, L. Vitaglaino, R. Berisio, Role of hydration in collagen triple helix stabilization. Biochem. Biophys. Res. Commun. 372, 121–125 (2008)CrossRefPubMedGoogle Scholar
  23. 23.
    R. Bhowmik, K.S. Katti, D.R. Katti, Influence of mineral-polymer interactions on molecular mechanics of polymer in composite bone biomaterials. Mater. Res. Soc. Symp. Proc. 978, 6 (2007). Paper #: 0978-GG0914-0905-FF0909-0905Google Scholar
  24. 24.
    D. Zhang, U. Chippada, K. Jordan, Effect of the structural water on the mechanical properties of collagen-like microfibrils: a molecular dynamics study. Ann. Biomed. Eng. 35, 1216–1230 (2007)CrossRefPubMedGoogle Scholar
  25. 25.
    N.M. Neves, J.F. Mano, Structure/mechanical behavior relationships in crossed-lamellar sea shells. Mater. Sci. Eng. C Biomim. Supramol. Syst. 25, 113–118 (2005). doi: 10.1016/j.msec.2005.01.004 CrossRefGoogle Scholar
  26. 26.
    G.M. Luz, J.F. Mano, Biomimetic design of materials and biomaterials inspired by the structure of nacre. Philos. Trans. R. Soc. A Math. Phys. Eng. Sci. 367, 1587–1605 (2009). doi: 10.1098/rsta.2009.0007 CrossRefGoogle Scholar
  27. 27.
    M. Sarikaya, C. Tamerler, A.K.Y. Jen, K. Schulten, F. Baneyx, Molecular biomimetics: nanotechnology through biology. Nat. Mater. 2, 577–585 (2003)CrossRefPubMedGoogle Scholar
  28. 28.
    B.D. Ratner, S.J. Bryant, Biomaterials: where we have been and where we are going. Annu. Rev. Biomed. Eng. 6, 41–75 (2004). doi: 10.1146/annurev.bioeng.6.040803.140027 CrossRefPubMedGoogle Scholar
  29. 29.
    C. Sanchez, H. Arribart, M.M.G. Guille, Biomimetism and bioinspiration as tools for the design of innovative materials and systems. Nat. Mater. 4, 277–288 (2005). doi: 10.1038/nmat1339 CrossRefPubMedGoogle Scholar
  30. 30.
    P. Fratzl, Biomimetic materials research: what can we really learn from nature’s structural materials? J. R. Soc. Interface 4, 637–642 (2007). doi: 10.1098/rsif.2007.0218 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    B. Bhushan, Biomimetics: lessons from nature—an overview. Philos. Trans. R. Soc. A Math. Phys. Eng. Sci. 367, 1445–1486 (2009). doi: 10.1098/rsta.2009.0011 CrossRefGoogle Scholar
  32. 32.
    M.E. Launey et al., Designing highly toughened hybrid composites through nature-inspired hierarchical complexity. Acta Mater. 57, 2919–2932 (2009). doi: 10.1016/j.actamat.2009.03.003 CrossRefGoogle Scholar
  33. 33.
    E. Munch et al., Tough, bio-inspired hybrid materials. Science 322, 1516–1520 (2008). doi: 10.1126/science.1164865 CrossRefPubMedGoogle Scholar
  34. 34.
    L.C. Palmer, C.J. Newcomb, S.R. Kaltz, E.D. Spoerke, S.I. Stupp, Biomimetic systems for hydroxyapatite mineralization inspired by bone and enamel. Chem. Rev. 108, 4754–4783 (2008). doi: 10.1021/cr8004422 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    T. Leventouri, Synthetic and biological hydroxyapatites: crystal structure questions. Biomaterials 27, 3339–3342 (2006)CrossRefPubMedGoogle Scholar
  36. 36.
    S.C. Cowin, Bone Mechanics Handbook (CRC Press, Boca Raton, FL, 2001)Google Scholar
  37. 37.
    B. Ji, H. Gao, Mechanical properties of nanostructure of biological materials. J. Mech. Phys. Solid 52, 1963–2000 (2004)CrossRefGoogle Scholar
  38. 38.
    I. Jager, P. Fratzl, Mineralized collagen fibrils: a mechanical model with a staggered arrangement of mineral particles. Biophys. J. 79, 1737–1746 (2000)CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    P. Fratzl, H.S. Gupta, E.P. Paschalis, P. Roschger, Structure and mechanical quality of the collagen-mineral nano-composite in bone. J. Mater. Chem. 14, 2115–2123 (2004)CrossRefGoogle Scholar
  40. 40.
    H.S. Gupta et al., Cooperative deformation of mineral and collagen in bone at the nanoscale. Proc. Natl. Acad. Sci. U. S. A. 103, 17741–17746 (2006). doi: 10.1073/pnas.0604237103 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    H.S. Gupta et al., Nanoscale deformation mechanisms in bone. Nano Lett. 5, 2108–2111 (2005)CrossRefPubMedGoogle Scholar
  42. 42.
    B.H. Ji, A study of the interface strength between protein and mineral in biological materials. J. Biomech. 41, 259–266 (2008)CrossRefPubMedGoogle Scholar
  43. 43.
    H.R. Wenk, F. Heidelbach, Crystal alignment of carbonated apatite in bone and calcified tendon: results from quantitative texture analysis. Bone 24, 361–369 (1999)CrossRefPubMedGoogle Scholar
  44. 44.
    J.D. Currey, J.D. Taylor, The mechanical behaviour of some molluscan hard tissues. J. Zool. 173, 395–406 (1974)CrossRefGoogle Scholar
  45. 45.
    M. Sarikaya, I.A. Aksay, Biomimetic, Design and Processing of Materials. Polymers and Complex Materials (American Institute of Physics, Woodbury, NY, 1995)Google Scholar
  46. 46.
    R.Z. Wang, Z. Suo, A.G. Evans, N. Yao, I.A. Aksay, Deformation mechanisms in nacre. J. Mater. Res. 16, 2485–2493 (2001)CrossRefGoogle Scholar
  47. 47.
    M. Sarikaya, An introduction to biomimetics—a structural viewpoint. Microsc. Res. Tech. 27, 360–375 (1994)CrossRefPubMedGoogle Scholar
  48. 48.
    T.E. Schaffer et al., Does abalone nacre form by heteroepitaxial nucleation or by growth through mineral bridges? Chem. Mater. 9, 1731–1740 (1997)CrossRefGoogle Scholar
  49. 49.
    F. Song, X.H. Zhang, Y.L. Bai, Microstructure and characteristics in the organic matrix layers of nacre. J. Mater. Res. 17, 1567–1570 (2002)CrossRefGoogle Scholar
  50. 50.
    F. Song, X.H. Zhang, Y.L. Bai, Microstructure in a biointerface. J. Mater. Sci. Lett. 21, 639–641 (2002)CrossRefGoogle Scholar
  51. 51.
    X.D. Li, W.C. Chang, Y.J. Chao, R.Z. Wang, M. Chang, Nanoscale structural and mechanical characterization of a natural nanocomposite material: the shell of red abalone. Nano Lett. 4, 613–617 (2004). doi: 10.1021/nl049962k CrossRefGoogle Scholar
  52. 52.
    M. Rousseau et al., Multiscale structure of sheet nacre. Biomaterials 26, 6254–6262 (2005). doi: 10.1016/j.biomaterials.2005.03.028 CrossRefPubMedGoogle Scholar
  53. 53.
    H. Peterlik, P. Roschger, K. Klaushofer, P. Fratzl, From brittle to ductile fracture of bone. Nat. Mater. 5, 52–55 (2006)CrossRefPubMedGoogle Scholar
  54. 54.
    H.S. Gupta et al., Nanoscale deformation mechanisms in bone. Nano Lett. 5, 2108–2111 (2005)CrossRefPubMedGoogle Scholar
  55. 55.
    A.P. Jackson, J.F.V. Vincent, R.M. Turner, The mechanical design of nacre. Proc. R. Soc. Lond. B Biol. Sci. 234, 415–440 (1988)CrossRefGoogle Scholar
  56. 56.
    B.L. Smith et al., Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites. Nature 399, 761–763 (1999)CrossRefGoogle Scholar
  57. 57.
    T. Sumitomo, H. Kakisawa, Y. Owaki, Y. Kagawa, In situ transmission electron microscopy observation of reversible deformation in nacre organic matrix. J. Mater. Res. 23, 1466–1471 (2008). doi: 10.1557/jmr.2008.0184 CrossRefGoogle Scholar
  58. 58.
    F. Barthelat, H. Tang, P.D. Zavattieri, C.M. Li, H.D. Espinosa, On the mechanics of mother-of-pearl: a key feature in the material hierarchical structure. J. Mech. Phys. Solid 55, 306–337 (2007). doi: 10.1016/j.jmps.2006.07.007 CrossRefGoogle Scholar
  59. 59.
    F. Barthelat, C.M. Li, C. Comi, H.D. Espinosa, Mechanical properties of nacre constituents and their impact on mechanical performance. J. Mater. Res. 21, 1977–1986 (2006). doi: 10.1557/jmr.2006.0239 CrossRefGoogle Scholar
  60. 60.
    R. Menig, M.H. Meyers, M.A. Meyers, K.S. Vecchio, Quasi-static and dynamic mechanical response of Haliotis rufescens (abalone) shells. Acta Mater. 48, 2383–2398 (2000)CrossRefGoogle Scholar
  61. 61.
    B.J.F. Bruet et al., Nanoscale morphology and indentation of individual nacre tablets from the gastropod mollusc Trochus niloticus. J. Mater. Res. 20, 2400–2419 (2005). doi: 10.1557/jmr.2005.0273 CrossRefGoogle Scholar
  62. 62.
    J.B. Thompson et al., Bone indentation recovery time correlates with bond reforming time. Nature 414, 773–776 (2001)CrossRefPubMedGoogle Scholar
  63. 63.
    K.S. Katti, D.R. Katti, S.M. Pradhan, A. Bhosle, Platelet interlocks are the key to toughness and strength in nacre. J. Mater. Res. 20, 1097–1100 (2005). doi: 10.1557/jmr.2005.0171 CrossRefGoogle Scholar
  64. 64.
    K.S. Katti, D.R. Katti, Why is nacre so tough and strong? Mater. Sci. Eng. C Biomim. Supramol. Syst. 26, 1317–1324 (2006). doi: 10.1016/j.msec.2005.08.013 CrossRefGoogle Scholar
  65. 65.
    N. Sasaki, S. Odajima, Stress-strain curve and Young’s modulus of a collagen molecule as determined by the X-ray diffraction technique. J. Biomech. 29, 655–658 (1996)CrossRefPubMedGoogle Scholar
  66. 66.
    S.J. Eppell, B.N. Smith, H. Kahn, R. Ballarini, Nano measurements with micro-devices: mechanical properties of hydrated collagen fibrils. J. R. Soc. Interface 3, 117–121 (2005)CrossRefPubMedCentralGoogle Scholar
  67. 67.
    A.J. Hodge, J.A. Petruska, in Aspects of Protein Structure. Proceedings of a Symposium, ed. by G.N. Ramachandran (1963), pp. 289–300Google Scholar
  68. 68.
    P.J. Thurner et al., High-speed photography of compressed human trabecular bone correlates whitening to microscopic damage. Eng. Fract. Mech. 74, 1928–1941 (2007)CrossRefGoogle Scholar
  69. 69.
    H. Gao, Application of fracture mechanics concepts to hierarchical biomechanics of bone and bone-like materials. Int. J. Fract. 138, 101–137 (2006)CrossRefGoogle Scholar
  70. 70.
    M.J. Buehler, Atomistic and continuum modeling of mechanical properties of collagen: elasticity, fracture, and self-assembly. J. Mater. Res. 21, 1947–1962 (2006)CrossRefGoogle Scholar
  71. 71.
    M.J. Buehler, Molecular nanomechanics of nascent bone: fibrillar toughening by mineralization. Nanotechnology 18, 295102–295110 (2007)CrossRefGoogle Scholar
  72. 72.
    A.C. Lorenzo, E.R. Caffarena, Elastic properties, Young’s modulus determination and structural stability of the tropocollagen molecule: a computational study by steered molecular dynamics. J. Biomech. 38, 1527–1533 (2005)CrossRefPubMedGoogle Scholar
  73. 73.
    M. Israelowitz, S.W.H. Rizvi, J. Kramer, H.P. von Schroeder, Computational modeling of type I collagen fibers to determine the extracellular matrix structure of connective tissues. Protein Eng. Des. Sel. 18, 329–335 (2005)CrossRefPubMedGoogle Scholar
  74. 74.
    M.J. Buehler, Nanomechanics of collagen fibrils under varying cross-link densities: atomistic and continuum studies. J. Mech. Behav. Biomed. Mater. 1, 59–67 (2008)CrossRefPubMedGoogle Scholar
  75. 75.
    J.W. Handgraaf, F. Zerbetto, Molecular dynamics study of onset of water gelation around the collagen triple helix. Proteins Struct. Funct. Bioinform. 64, 711–718 (2006)CrossRefGoogle Scholar
  76. 76.
    R.J. Radmer, T.E. Klein, Triple helical structure and stabilization of collagen-like molecules with 4(R)-hydroxyproline in the Xaa position. Biophys. J. 90, 578–588 (2006)CrossRefPubMedGoogle Scholar
  77. 77.
    T. Hassenkam et al., High-resolution AFM imaging of intact and fractured trabecular bone. Bone 35, 4–10 (2004)CrossRefPubMedGoogle Scholar
  78. 78.
    S. Weiner, Y. Talmon, W. Traub, Electron diffraction of mollusc shell organic matrices and their relationship to the mineral phase. Int. J. Biol. Macromol. 5, 325–328 (1983)CrossRefGoogle Scholar
  79. 79.
    W.J. Landis, M.J. Song, A. Leith, L. McEwen, B.F. McEwen, Mineral and organic matrix interaction in normally calcifying tendon visualized in 3 dimensions by high-voltage electron-microscopic tomography and graphic image-reconstruction. J. Struct. Biol. 110, 39–54 (1993)CrossRefPubMedGoogle Scholar
  80. 80.
    D.K. Dubey, V. Tomar, Role of hydroxyapatite crystal shape in nanoscale mechanical behavior of model tropocollagen-hydroxyapatite hard biomaterials. Mater. Sci. Eng. C Mater. Biol. Appl. 29, 2133–2140 (2009). doi: 10.1016/j.msec.2009.04.015 CrossRefGoogle Scholar
  81. 81.
    D.K. Dubey, V. Tomar, Effect of osteogenesis imperfecta mutations in tropocollagen molecule on strength of biomimetic tropocollagen-hydroxyapatite nanocomposites. Appl. Phys. Lett. 96, 023701–023703 (2010)CrossRefGoogle Scholar
  82. 82.
    A.S. Posner, R.A. Beebe, The surface chemistry of bone mineral and related calcium phosphates. Semin. Arthritis Rheum. 4, 267–291 (1975)CrossRefPubMedGoogle Scholar
  83. 83.
    R. Bhowmik, K.S. Katti, D.R. Katti, Influence of mineral-polymer interactions on molecular mechanics of polymer in composite bone biomaterials. Mater. Res. Soc. Symp. Proc. 978, 6 (2007)Google Scholar
  84. 84.
    F. Barthelat, H.D. Espinosa, An experimental investigation of deformation and fracture of nacre-mother of pearl. Exp. Mech. 47, 311–324 (2007). doi: 10.1007/s11340-007-9040-1 CrossRefGoogle Scholar
  85. 85.
    P. Ghosh, D.R. Katti, K.S. Katti, Mineral proximity influences mechanical response of proteins in biological mineral-protein hybrid systems. Biomacromolecules 8, 851–856 (2007)CrossRefPubMedGoogle Scholar
  86. 86.
    D.K. Dubey, V. Tomar, Effect of changes in tropocollagen residue sequence and hydroxyapatite mineral texture on the strength of ideal nanoscale tropocollagen-hydroxyapatite biomaterials. J. Mater. Sci. Mater. Med. 21, 161–171 (2010). doi: 10.1007/s10856-009-3837-7 CrossRefPubMedGoogle Scholar
  87. 87.
    Z.Y. Tang, N.A. Kotov, S. Magonov, B. Ozturk, Nanostructured artificial nacre. Nat. Mater. 2, 413–418 (2003). doi: 10.1038/nmat906 CrossRefPubMedGoogle Scholar
  88. 88.
    P. Podsiadlo et al., Layer-by-layer assembly of nacre-like nanostructured composites with antimicrobial properties. Langmuir 21, 11915–11921 (2005). doi: 10.1021/la051284+ CrossRefPubMedGoogle Scholar
  89. 89.
    J. Benesch, J. Mano, R. Reis, Proteins and their peptide motifs in acellular apatite mineralization of scaffolds for tissue engineering. Tissue Eng. Part B Rev. 14, 433–445 (2008)CrossRefPubMedGoogle Scholar
  90. 90.
    D. Verma, K. Katti, D. Katti, Nature of water in nacre: a 2D Fourier transform infrared spectroscopic study. Spectrochim. Acta Part A Mol. Biomol. Spectrosc. 67, 784–788 (2007)CrossRefGoogle Scholar
  91. 91.
    B.A. Wustman, J.C. Weaver, D.E. Morse, J.S. Evans, Structure–function studies of the Lustrin a polyelectrolyte domains, RKSY and D4. Connect. Tissue Res. 44(Suppl. 1), 10–15 (2003)CrossRefPubMedGoogle Scholar
  92. 92.
    G.M. Luz, J.F. Mano, Biomimetic design of materials and biomaterials inspired by the structure of nacre. Philos. Trans. R. Soc. A 28(367), 1587–1605 (2009)CrossRefGoogle Scholar
  93. 93.
    D.R. Katti, P. Ghosh, S. Schmidt, K.S. Katti, Mechanical properties of the sodium montmorillonite interlayer intercalated with amino acids. Biomacromolecules 6, 3267–3282 (2005)CrossRefGoogle Scholar
  94. 94.
    P. Fratzl, R. Weinkamer, Nature’s hierarchical materials. Prog. Mater. Sci. 52, 1263–1334 (2007)CrossRefGoogle Scholar
  95. 95.
    X. Li, Z.-H. Xu, R. Wang, In situ observation of nanograin rotation and deformation in nacre. Nano Lett. 6, 2301–2304 (2006)CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Purdue UniversityWest LafayetteUSA
  2. 2.Indian Institute of Technology DelhiNew DelhiIndia

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