Abstract

The alignment of deposited minerals in tissues such as bone and teeth plays a critical role in the mechanical properties of these tissues. Therefore, assessment of features that are characteristic of aligned biominerals could aid in the development of novel biomaterials and engineered tissues that can be used to replace damaged or defective human tissues. In this study, we demonstrate that light scattering spectroscopy can serve as a useful tool for the noninvasive characterization of mineralization on aligned organic substrates. Specifically, we used silk films with oriented and nonoriented secondary structures as a protein matrix for control of mineralization. The mineral deposits displayed self-affine fractal morphologies with the oriented films yielding a significantly higher Hurst parameter, which in turn suggests higher levels of fractal organization. In addition, the value of the upper bound of fractal correlation lengths was significantly smaller for the oriented than for the nonoriented films and correlated well with the size of the corresponding nanocrystalline mineral beads identified by scanning electron microscope imaging.

© 2009 Optical Society of America

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  1. S. Mann, Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry, (Oxford U. Press, 2001).
  2. G. He, T. Dahl, A. Veis, and A. George, “Nucleation of apatite crystals in vitroby self-assembled dentin matrix protein 1,” Nature Mater. 2, 552-558 (2003).
    [CrossRef]
  3. J. Venugopal, P. Vadgama, T. S. Sampath Kumar, and S. Ramakrishna, “Biocomposite nanofibers and osteoblasts for bone tissue engineering,” Nanotechnology 18, 55101-55109 (2007).
    [CrossRef]
  4. S. S. Liao, F. Z. Cui, and Y. Zhu, “Osteoblasts adherence and migration through three dimensional porous mineralized collagen based composite: nHAC/PLA,” J. Bioactive Comp. Polymers 19, 117-130 (2004).
    [CrossRef]
  5. R. Z. Wang, F. Z. Cui, H. B. Lu, H. B. Wen, C. L. Ma, and H. D. Li, “Synthesis of nanophase hydroxyapatite/collagen composite,” J. Mater. Sci. Lett. 14, 490-492 (1995).
    [CrossRef]
  6. C. Du, F. Z. Cui, X. D. Zhu, and K. de Groot, “Three dimensional nano-HAp/collagen matrix loading with osteogenic cells in organ culture,” J. Biomed. Mater. Res. 44, 407-415 (1999).
    [CrossRef] [PubMed]
  7. M. C. Chang, C. C. Ko, and W. H. Douglas, “Preparation of hydroxyapatite-gelatin nanocomposite,” Biomaterials 24, 2853-2862 (2003).
    [CrossRef] [PubMed]
  8. X. D. Kong, F. Z. Cui, X. M. Wang, M. Zhang, and W. Zhang, “Silk fibroin regulated mineralization of hydroxyapatite nanocrystals,” J. Cryst. Growth 270, 197-202 (2004).
    [CrossRef]
  9. G. H. Altman, F. Diaz, C. Jakuba, T. Calabro, R. L. Horan, J. Chen, H. Lu, J. Richmond, and D. L. Kaplan, “Silk based biomaterials,” Biomaterials 24, 401-416 (2003).
    [CrossRef]
  10. S. Gupta, M. Hunter, P. Cebe, J. M. Levitt, D. L. Kaplan, and I. Georgakoudi, “Non-invasive optical characterization of biomaterial mineralization,” Biomaterials 29, 2359-2369 (2008).
    [CrossRef] [PubMed]
  11. W. L. Rice, S. Firdous, Sharad Gupta, M. Hunter, C. W. P. Foo, Y. Wang, H. J. Kim, D. L. Kaplan, and I. Georgakoudi, “Non invasive characterization of structure and morphology of silk fibroin biomaterials using non-linear microscopy,” Biomaterials 29, 2015-2024 (2008).
    [CrossRef] [PubMed]
  12. C. Li, H. J. Jin, G. D. Botsaris, and D. L. Kaplan, “Silk apatite composites from electrospun fibers,” J. Mater. Res. 20, 3374-3384 (2005).
    [CrossRef]
  13. Y. L. Kim, Y. Liu, R. K. Wali, H. K. Roy, M. J. Goldberg, A. K. Kromin, K. Chen, and V. Backman, “Simultaneous measurement of angular and spectral properties of light scattering for characterization of tissue microarchitecture and its alteration in early precancer,” IEEE J Sel. Top. Quantum Electron. 9, 243-257 (2003).
    [CrossRef]
  14. M. Hunter, V. Backman, G. Popescu, M. Kalashnikov, C. W. Boone, A. Wax, G. Venkatesh, K. Badizadegan, G. D. Stoner, and M. S. Feld, “Tissue self-affinity and polarized light scattering in the born approximation: A new model for precancer detection,” Phys. Rev. Lett. 97, 138102 (2006).
    [CrossRef] [PubMed]
  15. B. B. Mandelbrot, The Fractal Geometry of Nature, revised ed., 19th printing (Freeman, 2000).
  16. G. Dougherty and G. M. Henebry, “Fractal signature and lacunarity in the measurement of the texture of trabecular bone in clinical CT images,” Med. Eng. Phys. 23, 369-380 (2001).
    [CrossRef] [PubMed]
  17. S. Simukanga and W. C. Lombe, “Electrochemical properties of apatite and other minerals of Zambian phosphate ores in aqueous solution,” Fertilizer Res. 41, 159-166 (1995).
    [CrossRef]

2008 (2)

S. Gupta, M. Hunter, P. Cebe, J. M. Levitt, D. L. Kaplan, and I. Georgakoudi, “Non-invasive optical characterization of biomaterial mineralization,” Biomaterials 29, 2359-2369 (2008).
[CrossRef] [PubMed]

W. L. Rice, S. Firdous, Sharad Gupta, M. Hunter, C. W. P. Foo, Y. Wang, H. J. Kim, D. L. Kaplan, and I. Georgakoudi, “Non invasive characterization of structure and morphology of silk fibroin biomaterials using non-linear microscopy,” Biomaterials 29, 2015-2024 (2008).
[CrossRef] [PubMed]

2007 (1)

J. Venugopal, P. Vadgama, T. S. Sampath Kumar, and S. Ramakrishna, “Biocomposite nanofibers and osteoblasts for bone tissue engineering,” Nanotechnology 18, 55101-55109 (2007).
[CrossRef]

2006 (1)

M. Hunter, V. Backman, G. Popescu, M. Kalashnikov, C. W. Boone, A. Wax, G. Venkatesh, K. Badizadegan, G. D. Stoner, and M. S. Feld, “Tissue self-affinity and polarized light scattering in the born approximation: A new model for precancer detection,” Phys. Rev. Lett. 97, 138102 (2006).
[CrossRef] [PubMed]

2005 (1)

C. Li, H. J. Jin, G. D. Botsaris, and D. L. Kaplan, “Silk apatite composites from electrospun fibers,” J. Mater. Res. 20, 3374-3384 (2005).
[CrossRef]

2004 (2)

S. S. Liao, F. Z. Cui, and Y. Zhu, “Osteoblasts adherence and migration through three dimensional porous mineralized collagen based composite: nHAC/PLA,” J. Bioactive Comp. Polymers 19, 117-130 (2004).
[CrossRef]

X. D. Kong, F. Z. Cui, X. M. Wang, M. Zhang, and W. Zhang, “Silk fibroin regulated mineralization of hydroxyapatite nanocrystals,” J. Cryst. Growth 270, 197-202 (2004).
[CrossRef]

2003 (4)

G. H. Altman, F. Diaz, C. Jakuba, T. Calabro, R. L. Horan, J. Chen, H. Lu, J. Richmond, and D. L. Kaplan, “Silk based biomaterials,” Biomaterials 24, 401-416 (2003).
[CrossRef]

M. C. Chang, C. C. Ko, and W. H. Douglas, “Preparation of hydroxyapatite-gelatin nanocomposite,” Biomaterials 24, 2853-2862 (2003).
[CrossRef] [PubMed]

G. He, T. Dahl, A. Veis, and A. George, “Nucleation of apatite crystals in vitroby self-assembled dentin matrix protein 1,” Nature Mater. 2, 552-558 (2003).
[CrossRef]

Y. L. Kim, Y. Liu, R. K. Wali, H. K. Roy, M. J. Goldberg, A. K. Kromin, K. Chen, and V. Backman, “Simultaneous measurement of angular and spectral properties of light scattering for characterization of tissue microarchitecture and its alteration in early precancer,” IEEE J Sel. Top. Quantum Electron. 9, 243-257 (2003).
[CrossRef]

2001 (2)

G. Dougherty and G. M. Henebry, “Fractal signature and lacunarity in the measurement of the texture of trabecular bone in clinical CT images,” Med. Eng. Phys. 23, 369-380 (2001).
[CrossRef] [PubMed]

S. Mann, Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry, (Oxford U. Press, 2001).

2000 (1)

B. B. Mandelbrot, The Fractal Geometry of Nature, revised ed., 19th printing (Freeman, 2000).

1999 (1)

C. Du, F. Z. Cui, X. D. Zhu, and K. de Groot, “Three dimensional nano-HAp/collagen matrix loading with osteogenic cells in organ culture,” J. Biomed. Mater. Res. 44, 407-415 (1999).
[CrossRef] [PubMed]

1995 (2)

R. Z. Wang, F. Z. Cui, H. B. Lu, H. B. Wen, C. L. Ma, and H. D. Li, “Synthesis of nanophase hydroxyapatite/collagen composite,” J. Mater. Sci. Lett. 14, 490-492 (1995).
[CrossRef]

S. Simukanga and W. C. Lombe, “Electrochemical properties of apatite and other minerals of Zambian phosphate ores in aqueous solution,” Fertilizer Res. 41, 159-166 (1995).
[CrossRef]

Altman, G. H.

G. H. Altman, F. Diaz, C. Jakuba, T. Calabro, R. L. Horan, J. Chen, H. Lu, J. Richmond, and D. L. Kaplan, “Silk based biomaterials,” Biomaterials 24, 401-416 (2003).
[CrossRef]

Backman, V.

M. Hunter, V. Backman, G. Popescu, M. Kalashnikov, C. W. Boone, A. Wax, G. Venkatesh, K. Badizadegan, G. D. Stoner, and M. S. Feld, “Tissue self-affinity and polarized light scattering in the born approximation: A new model for precancer detection,” Phys. Rev. Lett. 97, 138102 (2006).
[CrossRef] [PubMed]

Y. L. Kim, Y. Liu, R. K. Wali, H. K. Roy, M. J. Goldberg, A. K. Kromin, K. Chen, and V. Backman, “Simultaneous measurement of angular and spectral properties of light scattering for characterization of tissue microarchitecture and its alteration in early precancer,” IEEE J Sel. Top. Quantum Electron. 9, 243-257 (2003).
[CrossRef]

Badizadegan, K.

M. Hunter, V. Backman, G. Popescu, M. Kalashnikov, C. W. Boone, A. Wax, G. Venkatesh, K. Badizadegan, G. D. Stoner, and M. S. Feld, “Tissue self-affinity and polarized light scattering in the born approximation: A new model for precancer detection,” Phys. Rev. Lett. 97, 138102 (2006).
[CrossRef] [PubMed]

Boone, C. W.

M. Hunter, V. Backman, G. Popescu, M. Kalashnikov, C. W. Boone, A. Wax, G. Venkatesh, K. Badizadegan, G. D. Stoner, and M. S. Feld, “Tissue self-affinity and polarized light scattering in the born approximation: A new model for precancer detection,” Phys. Rev. Lett. 97, 138102 (2006).
[CrossRef] [PubMed]

Botsaris, G. D.

C. Li, H. J. Jin, G. D. Botsaris, and D. L. Kaplan, “Silk apatite composites from electrospun fibers,” J. Mater. Res. 20, 3374-3384 (2005).
[CrossRef]

Calabro, T.

G. H. Altman, F. Diaz, C. Jakuba, T. Calabro, R. L. Horan, J. Chen, H. Lu, J. Richmond, and D. L. Kaplan, “Silk based biomaterials,” Biomaterials 24, 401-416 (2003).
[CrossRef]

Cebe, P.

S. Gupta, M. Hunter, P. Cebe, J. M. Levitt, D. L. Kaplan, and I. Georgakoudi, “Non-invasive optical characterization of biomaterial mineralization,” Biomaterials 29, 2359-2369 (2008).
[CrossRef] [PubMed]

Chang, M. C.

M. C. Chang, C. C. Ko, and W. H. Douglas, “Preparation of hydroxyapatite-gelatin nanocomposite,” Biomaterials 24, 2853-2862 (2003).
[CrossRef] [PubMed]

Chen, J.

G. H. Altman, F. Diaz, C. Jakuba, T. Calabro, R. L. Horan, J. Chen, H. Lu, J. Richmond, and D. L. Kaplan, “Silk based biomaterials,” Biomaterials 24, 401-416 (2003).
[CrossRef]

Chen, K.

Y. L. Kim, Y. Liu, R. K. Wali, H. K. Roy, M. J. Goldberg, A. K. Kromin, K. Chen, and V. Backman, “Simultaneous measurement of angular and spectral properties of light scattering for characterization of tissue microarchitecture and its alteration in early precancer,” IEEE J Sel. Top. Quantum Electron. 9, 243-257 (2003).
[CrossRef]

Cui, F. Z.

S. S. Liao, F. Z. Cui, and Y. Zhu, “Osteoblasts adherence and migration through three dimensional porous mineralized collagen based composite: nHAC/PLA,” J. Bioactive Comp. Polymers 19, 117-130 (2004).
[CrossRef]

X. D. Kong, F. Z. Cui, X. M. Wang, M. Zhang, and W. Zhang, “Silk fibroin regulated mineralization of hydroxyapatite nanocrystals,” J. Cryst. Growth 270, 197-202 (2004).
[CrossRef]

C. Du, F. Z. Cui, X. D. Zhu, and K. de Groot, “Three dimensional nano-HAp/collagen matrix loading with osteogenic cells in organ culture,” J. Biomed. Mater. Res. 44, 407-415 (1999).
[CrossRef] [PubMed]

R. Z. Wang, F. Z. Cui, H. B. Lu, H. B. Wen, C. L. Ma, and H. D. Li, “Synthesis of nanophase hydroxyapatite/collagen composite,” J. Mater. Sci. Lett. 14, 490-492 (1995).
[CrossRef]

Dahl, T.

G. He, T. Dahl, A. Veis, and A. George, “Nucleation of apatite crystals in vitroby self-assembled dentin matrix protein 1,” Nature Mater. 2, 552-558 (2003).
[CrossRef]

de Groot, K.

C. Du, F. Z. Cui, X. D. Zhu, and K. de Groot, “Three dimensional nano-HAp/collagen matrix loading with osteogenic cells in organ culture,” J. Biomed. Mater. Res. 44, 407-415 (1999).
[CrossRef] [PubMed]

Diaz, F.

G. H. Altman, F. Diaz, C. Jakuba, T. Calabro, R. L. Horan, J. Chen, H. Lu, J. Richmond, and D. L. Kaplan, “Silk based biomaterials,” Biomaterials 24, 401-416 (2003).
[CrossRef]

Dougherty, G.

G. Dougherty and G. M. Henebry, “Fractal signature and lacunarity in the measurement of the texture of trabecular bone in clinical CT images,” Med. Eng. Phys. 23, 369-380 (2001).
[CrossRef] [PubMed]

Douglas, W. H.

M. C. Chang, C. C. Ko, and W. H. Douglas, “Preparation of hydroxyapatite-gelatin nanocomposite,” Biomaterials 24, 2853-2862 (2003).
[CrossRef] [PubMed]

Du, C.

C. Du, F. Z. Cui, X. D. Zhu, and K. de Groot, “Three dimensional nano-HAp/collagen matrix loading with osteogenic cells in organ culture,” J. Biomed. Mater. Res. 44, 407-415 (1999).
[CrossRef] [PubMed]

Feld, M. S.

M. Hunter, V. Backman, G. Popescu, M. Kalashnikov, C. W. Boone, A. Wax, G. Venkatesh, K. Badizadegan, G. D. Stoner, and M. S. Feld, “Tissue self-affinity and polarized light scattering in the born approximation: A new model for precancer detection,” Phys. Rev. Lett. 97, 138102 (2006).
[CrossRef] [PubMed]

Firdous, S.

W. L. Rice, S. Firdous, Sharad Gupta, M. Hunter, C. W. P. Foo, Y. Wang, H. J. Kim, D. L. Kaplan, and I. Georgakoudi, “Non invasive characterization of structure and morphology of silk fibroin biomaterials using non-linear microscopy,” Biomaterials 29, 2015-2024 (2008).
[CrossRef] [PubMed]

Foo, C. W. P.

W. L. Rice, S. Firdous, Sharad Gupta, M. Hunter, C. W. P. Foo, Y. Wang, H. J. Kim, D. L. Kaplan, and I. Georgakoudi, “Non invasive characterization of structure and morphology of silk fibroin biomaterials using non-linear microscopy,” Biomaterials 29, 2015-2024 (2008).
[CrossRef] [PubMed]

Georgakoudi, I.

W. L. Rice, S. Firdous, Sharad Gupta, M. Hunter, C. W. P. Foo, Y. Wang, H. J. Kim, D. L. Kaplan, and I. Georgakoudi, “Non invasive characterization of structure and morphology of silk fibroin biomaterials using non-linear microscopy,” Biomaterials 29, 2015-2024 (2008).
[CrossRef] [PubMed]

S. Gupta, M. Hunter, P. Cebe, J. M. Levitt, D. L. Kaplan, and I. Georgakoudi, “Non-invasive optical characterization of biomaterial mineralization,” Biomaterials 29, 2359-2369 (2008).
[CrossRef] [PubMed]

George, A.

G. He, T. Dahl, A. Veis, and A. George, “Nucleation of apatite crystals in vitroby self-assembled dentin matrix protein 1,” Nature Mater. 2, 552-558 (2003).
[CrossRef]

Goldberg, M. J.

Y. L. Kim, Y. Liu, R. K. Wali, H. K. Roy, M. J. Goldberg, A. K. Kromin, K. Chen, and V. Backman, “Simultaneous measurement of angular and spectral properties of light scattering for characterization of tissue microarchitecture and its alteration in early precancer,” IEEE J Sel. Top. Quantum Electron. 9, 243-257 (2003).
[CrossRef]

Gupta, S.

S. Gupta, M. Hunter, P. Cebe, J. M. Levitt, D. L. Kaplan, and I. Georgakoudi, “Non-invasive optical characterization of biomaterial mineralization,” Biomaterials 29, 2359-2369 (2008).
[CrossRef] [PubMed]

Gupta, Sharad

W. L. Rice, S. Firdous, Sharad Gupta, M. Hunter, C. W. P. Foo, Y. Wang, H. J. Kim, D. L. Kaplan, and I. Georgakoudi, “Non invasive characterization of structure and morphology of silk fibroin biomaterials using non-linear microscopy,” Biomaterials 29, 2015-2024 (2008).
[CrossRef] [PubMed]

He, G.

G. He, T. Dahl, A. Veis, and A. George, “Nucleation of apatite crystals in vitroby self-assembled dentin matrix protein 1,” Nature Mater. 2, 552-558 (2003).
[CrossRef]

Henebry, G. M.

G. Dougherty and G. M. Henebry, “Fractal signature and lacunarity in the measurement of the texture of trabecular bone in clinical CT images,” Med. Eng. Phys. 23, 369-380 (2001).
[CrossRef] [PubMed]

Horan, R. L.

G. H. Altman, F. Diaz, C. Jakuba, T. Calabro, R. L. Horan, J. Chen, H. Lu, J. Richmond, and D. L. Kaplan, “Silk based biomaterials,” Biomaterials 24, 401-416 (2003).
[CrossRef]

Hunter, M.

W. L. Rice, S. Firdous, Sharad Gupta, M. Hunter, C. W. P. Foo, Y. Wang, H. J. Kim, D. L. Kaplan, and I. Georgakoudi, “Non invasive characterization of structure and morphology of silk fibroin biomaterials using non-linear microscopy,” Biomaterials 29, 2015-2024 (2008).
[CrossRef] [PubMed]

S. Gupta, M. Hunter, P. Cebe, J. M. Levitt, D. L. Kaplan, and I. Georgakoudi, “Non-invasive optical characterization of biomaterial mineralization,” Biomaterials 29, 2359-2369 (2008).
[CrossRef] [PubMed]

M. Hunter, V. Backman, G. Popescu, M. Kalashnikov, C. W. Boone, A. Wax, G. Venkatesh, K. Badizadegan, G. D. Stoner, and M. S. Feld, “Tissue self-affinity and polarized light scattering in the born approximation: A new model for precancer detection,” Phys. Rev. Lett. 97, 138102 (2006).
[CrossRef] [PubMed]

Jakuba, C.

G. H. Altman, F. Diaz, C. Jakuba, T. Calabro, R. L. Horan, J. Chen, H. Lu, J. Richmond, and D. L. Kaplan, “Silk based biomaterials,” Biomaterials 24, 401-416 (2003).
[CrossRef]

Jin, H. J.

C. Li, H. J. Jin, G. D. Botsaris, and D. L. Kaplan, “Silk apatite composites from electrospun fibers,” J. Mater. Res. 20, 3374-3384 (2005).
[CrossRef]

Kalashnikov, M.

M. Hunter, V. Backman, G. Popescu, M. Kalashnikov, C. W. Boone, A. Wax, G. Venkatesh, K. Badizadegan, G. D. Stoner, and M. S. Feld, “Tissue self-affinity and polarized light scattering in the born approximation: A new model for precancer detection,” Phys. Rev. Lett. 97, 138102 (2006).
[CrossRef] [PubMed]

Kaplan, D. L.

S. Gupta, M. Hunter, P. Cebe, J. M. Levitt, D. L. Kaplan, and I. Georgakoudi, “Non-invasive optical characterization of biomaterial mineralization,” Biomaterials 29, 2359-2369 (2008).
[CrossRef] [PubMed]

W. L. Rice, S. Firdous, Sharad Gupta, M. Hunter, C. W. P. Foo, Y. Wang, H. J. Kim, D. L. Kaplan, and I. Georgakoudi, “Non invasive characterization of structure and morphology of silk fibroin biomaterials using non-linear microscopy,” Biomaterials 29, 2015-2024 (2008).
[CrossRef] [PubMed]

C. Li, H. J. Jin, G. D. Botsaris, and D. L. Kaplan, “Silk apatite composites from electrospun fibers,” J. Mater. Res. 20, 3374-3384 (2005).
[CrossRef]

G. H. Altman, F. Diaz, C. Jakuba, T. Calabro, R. L. Horan, J. Chen, H. Lu, J. Richmond, and D. L. Kaplan, “Silk based biomaterials,” Biomaterials 24, 401-416 (2003).
[CrossRef]

Kim, H. J.

W. L. Rice, S. Firdous, Sharad Gupta, M. Hunter, C. W. P. Foo, Y. Wang, H. J. Kim, D. L. Kaplan, and I. Georgakoudi, “Non invasive characterization of structure and morphology of silk fibroin biomaterials using non-linear microscopy,” Biomaterials 29, 2015-2024 (2008).
[CrossRef] [PubMed]

Kim, Y. L.

Y. L. Kim, Y. Liu, R. K. Wali, H. K. Roy, M. J. Goldberg, A. K. Kromin, K. Chen, and V. Backman, “Simultaneous measurement of angular and spectral properties of light scattering for characterization of tissue microarchitecture and its alteration in early precancer,” IEEE J Sel. Top. Quantum Electron. 9, 243-257 (2003).
[CrossRef]

Ko, C. C.

M. C. Chang, C. C. Ko, and W. H. Douglas, “Preparation of hydroxyapatite-gelatin nanocomposite,” Biomaterials 24, 2853-2862 (2003).
[CrossRef] [PubMed]

Kong, X. D.

X. D. Kong, F. Z. Cui, X. M. Wang, M. Zhang, and W. Zhang, “Silk fibroin regulated mineralization of hydroxyapatite nanocrystals,” J. Cryst. Growth 270, 197-202 (2004).
[CrossRef]

Kromin, A. K.

Y. L. Kim, Y. Liu, R. K. Wali, H. K. Roy, M. J. Goldberg, A. K. Kromin, K. Chen, and V. Backman, “Simultaneous measurement of angular and spectral properties of light scattering for characterization of tissue microarchitecture and its alteration in early precancer,” IEEE J Sel. Top. Quantum Electron. 9, 243-257 (2003).
[CrossRef]

Levitt, J. M.

S. Gupta, M. Hunter, P. Cebe, J. M. Levitt, D. L. Kaplan, and I. Georgakoudi, “Non-invasive optical characterization of biomaterial mineralization,” Biomaterials 29, 2359-2369 (2008).
[CrossRef] [PubMed]

Li, C.

C. Li, H. J. Jin, G. D. Botsaris, and D. L. Kaplan, “Silk apatite composites from electrospun fibers,” J. Mater. Res. 20, 3374-3384 (2005).
[CrossRef]

Li, H. D.

R. Z. Wang, F. Z. Cui, H. B. Lu, H. B. Wen, C. L. Ma, and H. D. Li, “Synthesis of nanophase hydroxyapatite/collagen composite,” J. Mater. Sci. Lett. 14, 490-492 (1995).
[CrossRef]

Liao, S. S.

S. S. Liao, F. Z. Cui, and Y. Zhu, “Osteoblasts adherence and migration through three dimensional porous mineralized collagen based composite: nHAC/PLA,” J. Bioactive Comp. Polymers 19, 117-130 (2004).
[CrossRef]

Liu, Y.

Y. L. Kim, Y. Liu, R. K. Wali, H. K. Roy, M. J. Goldberg, A. K. Kromin, K. Chen, and V. Backman, “Simultaneous measurement of angular and spectral properties of light scattering for characterization of tissue microarchitecture and its alteration in early precancer,” IEEE J Sel. Top. Quantum Electron. 9, 243-257 (2003).
[CrossRef]

Lombe, W. C.

S. Simukanga and W. C. Lombe, “Electrochemical properties of apatite and other minerals of Zambian phosphate ores in aqueous solution,” Fertilizer Res. 41, 159-166 (1995).
[CrossRef]

Lu, H.

G. H. Altman, F. Diaz, C. Jakuba, T. Calabro, R. L. Horan, J. Chen, H. Lu, J. Richmond, and D. L. Kaplan, “Silk based biomaterials,” Biomaterials 24, 401-416 (2003).
[CrossRef]

Lu, H. B.

R. Z. Wang, F. Z. Cui, H. B. Lu, H. B. Wen, C. L. Ma, and H. D. Li, “Synthesis of nanophase hydroxyapatite/collagen composite,” J. Mater. Sci. Lett. 14, 490-492 (1995).
[CrossRef]

Ma, C. L.

R. Z. Wang, F. Z. Cui, H. B. Lu, H. B. Wen, C. L. Ma, and H. D. Li, “Synthesis of nanophase hydroxyapatite/collagen composite,” J. Mater. Sci. Lett. 14, 490-492 (1995).
[CrossRef]

Mandelbrot, B. B.

B. B. Mandelbrot, The Fractal Geometry of Nature, revised ed., 19th printing (Freeman, 2000).

Mann, S.

S. Mann, Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry, (Oxford U. Press, 2001).

Popescu, G.

M. Hunter, V. Backman, G. Popescu, M. Kalashnikov, C. W. Boone, A. Wax, G. Venkatesh, K. Badizadegan, G. D. Stoner, and M. S. Feld, “Tissue self-affinity and polarized light scattering in the born approximation: A new model for precancer detection,” Phys. Rev. Lett. 97, 138102 (2006).
[CrossRef] [PubMed]

Ramakrishna, S.

J. Venugopal, P. Vadgama, T. S. Sampath Kumar, and S. Ramakrishna, “Biocomposite nanofibers and osteoblasts for bone tissue engineering,” Nanotechnology 18, 55101-55109 (2007).
[CrossRef]

Rice, W. L.

W. L. Rice, S. Firdous, Sharad Gupta, M. Hunter, C. W. P. Foo, Y. Wang, H. J. Kim, D. L. Kaplan, and I. Georgakoudi, “Non invasive characterization of structure and morphology of silk fibroin biomaterials using non-linear microscopy,” Biomaterials 29, 2015-2024 (2008).
[CrossRef] [PubMed]

Richmond, J.

G. H. Altman, F. Diaz, C. Jakuba, T. Calabro, R. L. Horan, J. Chen, H. Lu, J. Richmond, and D. L. Kaplan, “Silk based biomaterials,” Biomaterials 24, 401-416 (2003).
[CrossRef]

Roy, H. K.

Y. L. Kim, Y. Liu, R. K. Wali, H. K. Roy, M. J. Goldberg, A. K. Kromin, K. Chen, and V. Backman, “Simultaneous measurement of angular and spectral properties of light scattering for characterization of tissue microarchitecture and its alteration in early precancer,” IEEE J Sel. Top. Quantum Electron. 9, 243-257 (2003).
[CrossRef]

Sampath Kumar, T. S.

J. Venugopal, P. Vadgama, T. S. Sampath Kumar, and S. Ramakrishna, “Biocomposite nanofibers and osteoblasts for bone tissue engineering,” Nanotechnology 18, 55101-55109 (2007).
[CrossRef]

Simukanga, S.

S. Simukanga and W. C. Lombe, “Electrochemical properties of apatite and other minerals of Zambian phosphate ores in aqueous solution,” Fertilizer Res. 41, 159-166 (1995).
[CrossRef]

Stoner, G. D.

M. Hunter, V. Backman, G. Popescu, M. Kalashnikov, C. W. Boone, A. Wax, G. Venkatesh, K. Badizadegan, G. D. Stoner, and M. S. Feld, “Tissue self-affinity and polarized light scattering in the born approximation: A new model for precancer detection,” Phys. Rev. Lett. 97, 138102 (2006).
[CrossRef] [PubMed]

Vadgama, P.

J. Venugopal, P. Vadgama, T. S. Sampath Kumar, and S. Ramakrishna, “Biocomposite nanofibers and osteoblasts for bone tissue engineering,” Nanotechnology 18, 55101-55109 (2007).
[CrossRef]

Veis, A.

G. He, T. Dahl, A. Veis, and A. George, “Nucleation of apatite crystals in vitroby self-assembled dentin matrix protein 1,” Nature Mater. 2, 552-558 (2003).
[CrossRef]

Venkatesh, G.

M. Hunter, V. Backman, G. Popescu, M. Kalashnikov, C. W. Boone, A. Wax, G. Venkatesh, K. Badizadegan, G. D. Stoner, and M. S. Feld, “Tissue self-affinity and polarized light scattering in the born approximation: A new model for precancer detection,” Phys. Rev. Lett. 97, 138102 (2006).
[CrossRef] [PubMed]

Venugopal, J.

J. Venugopal, P. Vadgama, T. S. Sampath Kumar, and S. Ramakrishna, “Biocomposite nanofibers and osteoblasts for bone tissue engineering,” Nanotechnology 18, 55101-55109 (2007).
[CrossRef]

Wali, R. K.

Y. L. Kim, Y. Liu, R. K. Wali, H. K. Roy, M. J. Goldberg, A. K. Kromin, K. Chen, and V. Backman, “Simultaneous measurement of angular and spectral properties of light scattering for characterization of tissue microarchitecture and its alteration in early precancer,” IEEE J Sel. Top. Quantum Electron. 9, 243-257 (2003).
[CrossRef]

Wang, R. Z.

R. Z. Wang, F. Z. Cui, H. B. Lu, H. B. Wen, C. L. Ma, and H. D. Li, “Synthesis of nanophase hydroxyapatite/collagen composite,” J. Mater. Sci. Lett. 14, 490-492 (1995).
[CrossRef]

Wang, X. M.

X. D. Kong, F. Z. Cui, X. M. Wang, M. Zhang, and W. Zhang, “Silk fibroin regulated mineralization of hydroxyapatite nanocrystals,” J. Cryst. Growth 270, 197-202 (2004).
[CrossRef]

Wang, Y.

W. L. Rice, S. Firdous, Sharad Gupta, M. Hunter, C. W. P. Foo, Y. Wang, H. J. Kim, D. L. Kaplan, and I. Georgakoudi, “Non invasive characterization of structure and morphology of silk fibroin biomaterials using non-linear microscopy,” Biomaterials 29, 2015-2024 (2008).
[CrossRef] [PubMed]

Wax, A.

M. Hunter, V. Backman, G. Popescu, M. Kalashnikov, C. W. Boone, A. Wax, G. Venkatesh, K. Badizadegan, G. D. Stoner, and M. S. Feld, “Tissue self-affinity and polarized light scattering in the born approximation: A new model for precancer detection,” Phys. Rev. Lett. 97, 138102 (2006).
[CrossRef] [PubMed]

Wen, H. B.

R. Z. Wang, F. Z. Cui, H. B. Lu, H. B. Wen, C. L. Ma, and H. D. Li, “Synthesis of nanophase hydroxyapatite/collagen composite,” J. Mater. Sci. Lett. 14, 490-492 (1995).
[CrossRef]

Zhang, M.

X. D. Kong, F. Z. Cui, X. M. Wang, M. Zhang, and W. Zhang, “Silk fibroin regulated mineralization of hydroxyapatite nanocrystals,” J. Cryst. Growth 270, 197-202 (2004).
[CrossRef]

Zhang, W.

X. D. Kong, F. Z. Cui, X. M. Wang, M. Zhang, and W. Zhang, “Silk fibroin regulated mineralization of hydroxyapatite nanocrystals,” J. Cryst. Growth 270, 197-202 (2004).
[CrossRef]

Zhu, X. D.

C. Du, F. Z. Cui, X. D. Zhu, and K. de Groot, “Three dimensional nano-HAp/collagen matrix loading with osteogenic cells in organ culture,” J. Biomed. Mater. Res. 44, 407-415 (1999).
[CrossRef] [PubMed]

Zhu, Y.

S. S. Liao, F. Z. Cui, and Y. Zhu, “Osteoblasts adherence and migration through three dimensional porous mineralized collagen based composite: nHAC/PLA,” J. Bioactive Comp. Polymers 19, 117-130 (2004).
[CrossRef]

Biomaterials (4)

M. C. Chang, C. C. Ko, and W. H. Douglas, “Preparation of hydroxyapatite-gelatin nanocomposite,” Biomaterials 24, 2853-2862 (2003).
[CrossRef] [PubMed]

G. H. Altman, F. Diaz, C. Jakuba, T. Calabro, R. L. Horan, J. Chen, H. Lu, J. Richmond, and D. L. Kaplan, “Silk based biomaterials,” Biomaterials 24, 401-416 (2003).
[CrossRef]

S. Gupta, M. Hunter, P. Cebe, J. M. Levitt, D. L. Kaplan, and I. Georgakoudi, “Non-invasive optical characterization of biomaterial mineralization,” Biomaterials 29, 2359-2369 (2008).
[CrossRef] [PubMed]

W. L. Rice, S. Firdous, Sharad Gupta, M. Hunter, C. W. P. Foo, Y. Wang, H. J. Kim, D. L. Kaplan, and I. Georgakoudi, “Non invasive characterization of structure and morphology of silk fibroin biomaterials using non-linear microscopy,” Biomaterials 29, 2015-2024 (2008).
[CrossRef] [PubMed]

Fertilizer Res. (1)

S. Simukanga and W. C. Lombe, “Electrochemical properties of apatite and other minerals of Zambian phosphate ores in aqueous solution,” Fertilizer Res. 41, 159-166 (1995).
[CrossRef]

IEEE J Sel. Top. Quantum Electron. (1)

Y. L. Kim, Y. Liu, R. K. Wali, H. K. Roy, M. J. Goldberg, A. K. Kromin, K. Chen, and V. Backman, “Simultaneous measurement of angular and spectral properties of light scattering for characterization of tissue microarchitecture and its alteration in early precancer,” IEEE J Sel. Top. Quantum Electron. 9, 243-257 (2003).
[CrossRef]

J. Bioactive Comp. Polymers (1)

S. S. Liao, F. Z. Cui, and Y. Zhu, “Osteoblasts adherence and migration through three dimensional porous mineralized collagen based composite: nHAC/PLA,” J. Bioactive Comp. Polymers 19, 117-130 (2004).
[CrossRef]

J. Biomed. Mater. Res. (1)

C. Du, F. Z. Cui, X. D. Zhu, and K. de Groot, “Three dimensional nano-HAp/collagen matrix loading with osteogenic cells in organ culture,” J. Biomed. Mater. Res. 44, 407-415 (1999).
[CrossRef] [PubMed]

J. Cryst. Growth (1)

X. D. Kong, F. Z. Cui, X. M. Wang, M. Zhang, and W. Zhang, “Silk fibroin regulated mineralization of hydroxyapatite nanocrystals,” J. Cryst. Growth 270, 197-202 (2004).
[CrossRef]

J. Mater. Res. (1)

C. Li, H. J. Jin, G. D. Botsaris, and D. L. Kaplan, “Silk apatite composites from electrospun fibers,” J. Mater. Res. 20, 3374-3384 (2005).
[CrossRef]

J. Mater. Sci. Lett. (1)

R. Z. Wang, F. Z. Cui, H. B. Lu, H. B. Wen, C. L. Ma, and H. D. Li, “Synthesis of nanophase hydroxyapatite/collagen composite,” J. Mater. Sci. Lett. 14, 490-492 (1995).
[CrossRef]

Med. Eng. Phys. (1)

G. Dougherty and G. M. Henebry, “Fractal signature and lacunarity in the measurement of the texture of trabecular bone in clinical CT images,” Med. Eng. Phys. 23, 369-380 (2001).
[CrossRef] [PubMed]

Nanotechnology (1)

J. Venugopal, P. Vadgama, T. S. Sampath Kumar, and S. Ramakrishna, “Biocomposite nanofibers and osteoblasts for bone tissue engineering,” Nanotechnology 18, 55101-55109 (2007).
[CrossRef]

Nature Mater. (1)

G. He, T. Dahl, A. Veis, and A. George, “Nucleation of apatite crystals in vitroby self-assembled dentin matrix protein 1,” Nature Mater. 2, 552-558 (2003).
[CrossRef]

Phys. Rev. Lett. (1)

M. Hunter, V. Backman, G. Popescu, M. Kalashnikov, C. W. Boone, A. Wax, G. Venkatesh, K. Badizadegan, G. D. Stoner, and M. S. Feld, “Tissue self-affinity and polarized light scattering in the born approximation: A new model for precancer detection,” Phys. Rev. Lett. 97, 138102 (2006).
[CrossRef] [PubMed]

Other (2)

B. B. Mandelbrot, The Fractal Geometry of Nature, revised ed., 19th printing (Freeman, 2000).

S. Mann, Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry, (Oxford U. Press, 2001).

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Figures (4)

Fig. 1
Fig. 1

(a) SHG microscopic images of oriented water annealed film acquired with 800 nm excitation through 20 × objective. (b) SHG microscopic images of nonoriented water annealed film acquired with 800 nm excitation through 20 × objective. Images were acquired with the same laser excitation power and PMT gain settings.

Fig. 2
Fig. 2

(a) Differential light scattering map of mineralized oriented water annealed film, (b) differential light scattering map of mineralized nonoriented water annealed film. LSS spectra of (c) oriented mineralized film and (d) nonoriented mineralized silk film (open circles), with corresponding self-affine fractal model fits (solid lines) achieved using Eq. (1).

Fig. 3
Fig. 3

Plot of fractal parameters (a) power law exponent α and (b) upper scale L for oriented and nonoriented films.

Fig. 4
Fig. 4

SEM images of mineralized (a) oriented and (b) nonoriented films at 10 , 000 × magnification after the first cycle of mineralization. (c)  30 , 000 × resolution SEM image of oriented film and (d)  30 , 000 × resolution SEM image of nonoriented film. (e) Inverse power law fitted PSD profile of 10 , 000 × oriented film shown in (a). (f) Inverse power law fitted PSD profile of 10 , 000 × nonoriented film shown in (b).

Equations (1)

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Δ I ( λ ) λ 4 1 [ 1 + ( 4 π L / λ ) 2 ] α ,

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