Advertisement

Journal of Bionic Engineering

, Volume 9, Issue 3, pp 367–376 | Cite as

Cuttlebone: Characterisation, application and development of biomimetic materials

  • Joseph Cadman
  • Shiwei Zhou
  • Yuhang Chen
  • Qing LiEmail author
Article

Abstract

Cuttlebone signifies a special class of ultra-lightweight cellular natural material possessing unique chemical, mechanical and structural properties, which have drawn considerable attention in the literature. The aim of this paper is to better understand the mechanical and biological roles of cuttlebone. First, the existing literature concerning the characterisation and potential applications inspired by this remarkable biomaterial is critiqued. Second, the finite element-based homogenisation method is used to verify that morphological variations within individual cuttlebone samples have minimal impact on the effective mechanical properties. This finding agrees with existing literature, which suggests that cuttlebone strength is dictated by the cuttlefish habitation depth. Subsequently, this homogenisation approach is further developed to characterise the effective mechanical bulk modulus and biofluidic permeability that cuttlebone provides, thereby quantifying its mechanical and transporting functionalities to inspire bionic design of structures and materials for more extensive applications. Finally, a brief rationale for the need to design a biomimetic material inspired by the cuttlebone microstructure is provided, based on the preceding investigation.

Keywords

cuttlebone characterisation biomimetic homogenisation 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. [1]
    Birchall J D, Thomas N L. On the architecture and function of cuttlefish bone. Journal of Materials Science, 1983, 18, 2081–2086.CrossRefGoogle Scholar
  2. [2]
    Gower D, Vincent J F V. The mechanical design of the cuttlebone and its bathymetric implications. Biomimetics, 1996, 4, 37–57.Google Scholar
  3. [3]
    Vogel S. Living in a physical world VIII. Gravity and life in water. Journal of Biosciences, 2006, 31, 309–322.CrossRefGoogle Scholar
  4. [4]
    Sherrard K M. Cuttlebone morphology limits habitat depth in eleven species of Sepia (Cephalopoda: Sepiidae). The Biological Bulletin, 2000, 198, 404–414.CrossRefGoogle Scholar
  5. [5]
    Falini G, Fermani S. Chitin mineralization. Tissue Engineering, 2004, 10, 1–6.CrossRefGoogle Scholar
  6. [6]
    Vincent J F V. Ceramics from invertebrate animals, in Levy M B (Ed.), Handbook of Elastic Properties of Solids, Liquids and Gases, Academic Press, New York, USA, 2001, 213–226.Google Scholar
  7. [7]
    Liang Y, Zhao J, Wang L, Li F M. The relationship between mechanical properties and crossed-lamellar structure of mollusk shells. Materials Science and Engineering a-Structural Materials Properties Microstructure and Processing, 2008, 483–484, 309-312.Google Scholar
  8. [8]
    Jackson A P, Vincent J F V, Turner R M. Comparison of nacre with other ceramic composites. Journal of Materials Science, 1990, 25, 3173–3178.CrossRefGoogle Scholar
  9. [9]
    Mayer G. New classes of tough composite materials- Lessons from natural rigid biological systems. Materials Science and Engineering: C, 2006, 26, 1261–1268.CrossRefGoogle Scholar
  10. [10]
    Mayer G. Rigid biological systems as models for synthetic composites. Science, 2005, 310, 1144–1147.CrossRefGoogle Scholar
  11. [11]
    Mayer G, Sarikaya M. Rigid biological composite materials: Structural examples for biomimetic design. Experimental Mechanics, 2002, 42, 395–403.CrossRefGoogle Scholar
  12. [12]
    Boletzky S V. Sepia officinalis, in: Boyle P R (Ed.), Cephalopod Life Cycles, Academic Press, London, UK, 1983, 31–52.Google Scholar
  13. [13]
    Gutowska M A, Melzner F, Portner H O, Meier S. Cuttlebone calcification increases during exposure to elevated seawater pCO2 in the cephalopod Sepia officinalis. Marine Biology, 2010, 157, 1653–1663.CrossRefGoogle Scholar
  14. [14]
    Ward P D, Boletzky S V. Shell implosion depth and implosion morphologies in three species of Sepia (Cephalopoda) from the Mediterranean Sea. Journal of the Marine Biological Association of the United Kingdom, 1984, 64, 955–966.CrossRefGoogle Scholar
  15. [15]
    Denton E J, Gilpinbrown J B, Howarth J V. The osmotic mechanism of cuttlebone. Journal of the Marine Biological Association of the United Kingdom, 1961, 41, 351–363.CrossRefGoogle Scholar
  16. [16]
    Poompradub S, Ikeda Y, Kokubo Y, Shiono T. Cuttlebone as reinforcing filler for natural rubber. European Polymer Journal, 2008, 44, 4157–4164.CrossRefGoogle Scholar
  17. [17]
    Yildirim O S, Okumus Z, Kizilkaya M, Ozdemir Y, Durak R, Okur A. Comparative quantative analysis of sodium, magnesium, potassium and calcium in healthy cuttlefish backbone and non-pathological human elbow bone. Canadian Journal of Analytical Sciences and Spectroscopy, 2007, 52, 270–275.Google Scholar
  18. [18]
    Garcia-Enriquez S, Guadarrama H E, Reyes-Gonzalez I, Mendizabal E, Jasso-Gastinel C F, Garcia-Enriquez B, Rembao-Boiorquez D, Pane-Pianese C. Mechanical performance and in vivo tests of an acrylic bone cement filled with bioactive sepia officinalis cuttlebone. Journal of Biomaterials Science-Polymer Edition, 2010, 21, 113–125.CrossRefGoogle Scholar
  19. [19]
    Jasso-Gastinel C F, Enriquez S G, Flores J, Reyes-Gonzalez I, Mijares E M. Acrylic bone cements modified with bioactive filler. Macromolecular Symposia, 2009, 283–284, 159-166.Google Scholar
  20. [20]
    Ivankovic H, Ferrer G G, Tkalcec E, Orlic S, Ivankovic M. Preparation of highly porous hydroxyapatite from cuttlefish bone. Journal of Materials Science: Materials in Medicine, 2009, 20, 1039–1046.Google Scholar
  21. [21]
    Ivankovic H, Tkalcec E, Orlic S, Ferrer G G, Schauperl Z. Hydroxyapatite formation from cuttlefish bones: kinetics. Journal of Materials Science-Materials in Medicine, 2010, 21, 2711–2722.CrossRefGoogle Scholar
  22. [22]
    Kasioptas A, Geisler T, Putnis C V, Perdikouri C, Putnis A. Crystal growth of apatite by replacement of an aragonite precursor. Journal of Crystal Growth, 2010, 312, 2431–2440.CrossRefGoogle Scholar
  23. [23]
    Rocha J H, Lemos A F, Agathopoulos S, Kannan S, Valério P, Ferreira J M. Hydrothermal growth of hydroxyapatite scaffolds from aragonitic cuttlefish bones. Journal of Biomedical Materials Research - Part A, 2006, 77, 160–168.CrossRefGoogle Scholar
  24. [24]
    Rocha J H G, Lemos A F, Agathopoulos S, Valerio P, Kannan S, Oktar F N, Ferreira J M F. Scaffolds for bone restoration from cuttlefish. Bone, 2005, 37, 850–857.CrossRefGoogle Scholar
  25. [25]
    Rocha J H G, Lemos A F, Kannan S, Agathopoulos S, Ferreira J M F. Hydroxyapatite scaffolds hydrothermally grown from aragonitic cuttlefish bones. Journal of Materials Chemistry, 2005, 15, 5007–5011.CrossRefGoogle Scholar
  26. [26]
    Kannan S, Rocha J H G, Agathopoulos S, Ferreira J M F. Fluorine-substituted hydroxyapatite scaffolds hydrothermally grown from aragonitic cuttlefish bones. Acta Biomaterialia, 2007, 3, 243–249.CrossRefGoogle Scholar
  27. [27]
    Zaremba C M, Morse D E, Mann S, Hansma P K, Stucky G D. Aragonite-hydroxyapatite conversion in gastropod (abalone) nacre. Chemistry of Materials, 1998, 10, 3813–3824.CrossRefGoogle Scholar
  28. [28]
    Cadman J, Chen Y, Zhou S, Li Q. Bioinspired lightweight cellular materials - understanding effects of natural variation on mechanical properties. Mater. Sci. Eng. C-Biomimetic Supramol. Syst. 2012, Submitted.Google Scholar
  29. [29]
    Culverwell E, Wimbush S C, Hall S R. Biotemplated synthesis of an ordered macroporous superconductor with high critical current density using a cuttlebone template. Chemical Communications, 2008, 1055–1057.Google Scholar
  30. [30]
    Lee S J, Lee Y C, Yoon Y S. Characteristics of calcium phosphate powders synthesized from cuttlefish bone and phosphoric acid. Journal of Ceramic Processing Research, 2007, 8, 427–430.Google Scholar
  31. [31]
    Lee S J, Yoon Y S, Lee M H, Oh N S. Highly sinterable beta-tricalcium phosphate synthesized from eggshells. Materials Letters, 2007, 61, 1279–1282.CrossRefGoogle Scholar
  32. [32]
    Jia X, Ma X, Wei D, Dong J, Qian W. Direct formation of silver nanoparticles in cuttlebone-derived organic matrix for catalytic applications. Colloids and Surfaces A: Physicochemical and Engineering Aspects, 2008, 330, 234–240.CrossRefGoogle Scholar
  33. [33]
    Xu G L, Li H, Ma X Y, Jia X P, Dong J, Qian W P. A cuttlebone- derived matrix substrate for hydrogen peroxide/ glucose detection. Biosensors and Bioelectronics, 2009, 25, 362–367.CrossRefGoogle Scholar
  34. [34]
    Jia X P, Qian W P, Wu D J, Wei D W, Xu G L, Liu X J. Cuttlebone-derived organic matrix as a scaffold for assembly of silver nanoparticles and application of the composite films in surface-enhanced raman scattering. Colloid and Surfaces B: Biointerfaces, 2009, 68, 231–237.CrossRefGoogle Scholar
  35. [35]
    Ogasawara W, Shenton W, Davis S A, Mann S. Template mineralization of ordered macroporous chitin-silica composites using a cuttlebone-derived organic matrix. Chemistry of Materials, 2000, 12, 2835–2837.CrossRefGoogle Scholar
  36. [36]
    Prasitsilp M, Jenwithisuk R, Kongsuwan K, Damrongchai N, Watts P. Cellular responses to chitosan in vitro: The importance of deacetylation. Journal of Materials Science: Materials in Medicine, 2000, 11, 773–778.Google Scholar
  37. [37]
    Cadman J, Zhou S, Chen Y, Li Q. Topology optimization of cellular structures, learnt from cuttlefish. in Rodrigues H, Guedes J M, Fernandes P, Folgado J, Neves M M (Eds.), Eighth World Congress on Structural and Multidisciplinary Optimization, ISSMO, Lisboa, Portugal, 2009.Google Scholar
  38. [38]
    Cadman J, Zhou S, Chen Y, Li W, Appleyard R, Li Q. Characterization of cuttlebone for a biomimetic design of cellular structures. Acta Mechanica Sinica, 2010, 26, 27–35.CrossRefzbMATHGoogle Scholar
  39. [39]
    Bendsoe M P, Kikuchi N. Generating optimal topologies in structural design using a homogenization method. Computer Methods in Applied Mechanics and Engineering, 1988, 197–224.Google Scholar
  40. [40]
    Song Y S, Youn J R. Evaluation of effective thermal conductivity for carbon nanotube/polymer composites using control volume finite element method. Carbon, 2006, 44, 710–717.CrossRefGoogle Scholar
  41. [41]
    Cadman J, Chen Y, Zhou S, Li Q. Creating biomaterials inspired by the microstructure of cuttlebone. Materials Science Forum, 2010, 654–656, 2229-2232.Google Scholar
  42. [42]
    Cadman J, Chen Y, Zhou S, Li Q. Assessing the effects of natural variations in microstructure for the biomimetic modeling of cuttlebone. Advanced Materials Research, 2010, 123–125, 295-298.Google Scholar
  43. [43]
    Bensoussan A, Papanicolaou G, Lions J L. Asymptotic Analysis for Periodic Structures, North Holland Pub Co, Amsterdam, Holland, 1978.zbMATHGoogle Scholar
  44. [44]
    Torquato S, Hyun S, Donev A. Multifunctional composites: optimizing microstructures for simultaneous transport of heat and electricity. Physical Review Letters, 2002, 89, 266601.Google Scholar
  45. [45]
    Gibiansky L V, Sigmund O. Multiphase composites with extremal bulk modulus. Journal of the Mechanics and Physics of Solids, 2000, 48, 461–498.MathSciNetCrossRefzbMATHGoogle Scholar
  46. [46]
    Zhou S, Li Q. Design of graded two-phase microstructures for tailored elasticity gradients. Journal of Materials Science, 2008d, 43, 5157–5167.CrossRefGoogle Scholar
  47. [47]
    De Kruijf N, Zhou S W, Li Q, Mai Y W. Topological design of structures and composite materials with multiobjectives. International Journal of Solids and Structures, 2007, 44, 7092–7109.CrossRefzbMATHGoogle Scholar
  48. [48]
    Chen Y H, Zhou S W, Li Q. Computational design for multifunctional microstructural composites. International Journal of Modern Physics B, 2009, 23, 1345–1351.CrossRefGoogle Scholar
  49. [49]
    Zhou S W, Li Q. A variational level set method for the topology optimization of steady-state Navier-Stokes flow. Journal of Computational Physics, 2008g, In Press.Google Scholar
  50. [50]
    Jung Y, Torquato S. Fluid permeabilities of triply periodic minimal surfaces. Physical Review E, 2005, 72, 056319.Google Scholar
  51. [51]
    Zhou S W, Li Q. A microstructure diagram for known bounds in conductivity. Journal of Materials Research, 2008a, 23, 798–811.MathSciNetCrossRefGoogle Scholar
  52. [52]
    Hashin Z, Shtrikman S. A variational appraoch to the theory of elastic behaviour of multiphase materials. Journal of the Mechanics and Physics of Solids, 1963a, 11, 127–140.MathSciNetCrossRefzbMATHGoogle Scholar
  53. [53]
    Milton G W, Kohn R V. Variational bounds on the effective moduli of anisotropic composites. Journal of the Mechanics and Physics of Solids 1988, 36, 597–629.MathSciNetCrossRefzbMATHGoogle Scholar
  54. [54]
    Hutmacher D W, Sittinger M, Risbud M V. Scaffold-based tissue engineering: rationale for computer-aided design and solid free-form fabrication systems. Trends in Biotechnology, 2004, 22, 354–362.CrossRefGoogle Scholar
  55. [55]
    Liu C Z, Czernuszka J T. Development of biodegradable scaffolds for tissue engineering: a perspective on emerging technology. Materials Science and Technology, 2007, 23, 379–391.CrossRefGoogle Scholar

Copyright information

© Jilin University 2012

Authors and Affiliations

  • Joseph Cadman
    • 1
  • Shiwei Zhou
    • 2
  • Yuhang Chen
    • 3
  • Qing Li
    • 1
    Email author
  1. 1.School of Aerospace, Mechanical and Mechatronic EngineeringThe University of SydneyAustralia
  2. 2.Innovative Structures Group, School of Civil, Environmental and Chemical EngineeringRMIT UniversityMelbourneAustralia
  3. 3.School of Engineering and Physical SciencesHeriot-Watt UniversityEdinburghUK

Personalised recommendations