Abstract

Osteoporosis is a progressive bone disease that is characterized by a decrease in bone mass and the deterioration in bone microarchitecture. This study investigates the feasibility of characterizing bone microstructure by analyzing the frequency spectrum of the photoacoustic (PA) signal from the bone. Modeling and numerical simulation of PA signal were performed on trabecular bone simulations and CT scans with different trabecular thicknesses. The resulting quasi-linear photoacoustic spectra were fittted by linear regression, from which the spectral parameter slope was quantified. The simulation based on two different models both demonstrate that bone specimens with thinner trabecular thicknesses have higher slope. Experiment on osteoporotic rat femoral heads with different mineral content was conducted. The finding from the experiment was in good agreement with the simulation, demonstrating that the frequency-domain analysis of PA signals can provide an objective assessment of bone microstructure and deterioration. Considering that PA measurement is non-ionizing, non-invasive, and has sufficient penetration in both calcified and non-calcified tissues, this new bone evaluation method based on photoacoustic spectral analysis holds potential for clinical management of osteoporosis and other bone diseases.

© 2015 Optical Society of America

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References

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  1. P. Pisani, M. D. Renna, F. Conversano, E. Casciaro, M. Muratore, E. Quarta, M. D. Paola, and S. Casciaro, “Screening and early diagnosis of osteoporosis through X-ray and ultrasound based techniques,” World J. Radiol. 5(11), 398–410 (2013).
    [Crossref] [PubMed]
  2. C. V. Albanese, F. De Terlizzi, and R. Passariello, “Quantitative ultrasound of the phalanges and DXA of the lumbar spine and proximal femur in evaluating the risk of osteoporotic vertebral fracture in postmenopausal women,” Radiol. Med. (Torino) 116(1), 92–101 (2011).
    [Crossref] [PubMed]
  3. W. C. Hayes, S. J. Piazza, and P. K. Zysset, “Biomechanics of fracture risk prediction of the hip and spine by quantitative computed tomography,” Radiol. Clin. North Am. 29(1), 1–18 (1991).
    [PubMed]
  4. C. C. Glüer, C. Y. Wu, M. Jergas, S. A. Goldstein, and H. K. Genant, “Three quantitative ultrasound parameters reflect bone structure,” Calcif. Tissue Int. 55(1), 46–52 (1994).
    [Crossref] [PubMed]
  5. J. Töyräs, M. T. Nieminen, H. Kröger, and J. S. Jurvelin, “Bone mineral density, ultrasound velocity, and broadband attenuation predict mechanical properties of trabecular bone differently,” Bone 31(4), 503–507 (2002).
    [Crossref] [PubMed]
  6. C. Liu, D. Ta, F. Fujita, T. Hachiken, M. Matsukawa, K. Mizuno, and W. Wang, “The relationship between ultrasonic backscatter and trabecular anisotropic microstructure in cancellous bone,” J. Appl. Phys. 115(6), 064906 (2014).
    [Crossref]
  7. C. F. Njeh, C. M. Boivin, and C. M. Langton, “The role of ultrasound in the assessment of osteoporosis: a review,” Osteoporos. Int. 7(1), 7–22 (1997).
    [Crossref] [PubMed]
  8. B. Lashkari and A. Mandelis, “Coregistered photoacoustic and ultrasonic signatures of early bone density variations,” J. Biomed. Opt. 19(3), 036015 (2014).
    [Crossref] [PubMed]
  9. B. Lashkari, L. Yang, and A. Mandelis, “The application of backscattered ultrasound and photoacoustic signals for assessment of bone collagen and mineral contents,” Quant. Imaging Med. Surg. 5(1), 46–56 (2015).
    [PubMed]
  10. L. Yang, B. Lashkari, J. W. Tan, and A. Mandelis, “Photoacoustic and ultrasound imaging of cancellous bone tissue,” J. Biomed. Opt. 20(7), 076016 (2015).
    [Crossref] [PubMed]
  11. T. Feng, K. M. Kozloff, C. Tian, J. E. Perosky, Y.-S. Hsiao, S. Du, J. Yuan, C. X. Deng, and X. Wang, “Bone assessment via thermal photo-acoustic measurements,” Opt. Lett. 40(8), 1721–1724 (2015).
    [Crossref] [PubMed]
  12. I. Steinberg, A. Eyal, and I. Gannot, “Multispectral photoacoustic method for the early detection and diagnosis of osteoporosis,” in SPIE BiOS(International Society for Optics and Photonics, 2013), pp. 85656G–85656G–85659.
  13. I. Steinberg, I. Gannot, and A. Eyal, “Investigation of a dual modal method for bone pathologies using quantitative ultrasound and photoacoustics,” in SPIE BiOS(International Society for Optics and Photonics, 2015), pp. 93230R–93230R–93236.
  14. A. Pifferi, A. Torricelli, P. Taroni, A. Bassi, E. Chikoidze, E. Giambattistelli, and R. Cubeddu, “Optical biopsy of bone tissue: a step toward the diagnosis of bone pathologies,” J. Biomed. Opt. 9(3), 474–480 (2004).
    [Crossref] [PubMed]
  15. P. Moilanen, Z. Zhao, P. Karppinen, T. Karppinen, V. Kilappa, J. Pirhonen, R. Myllylä, E. Haeggström, and J. Timonen, “Photo-acoustic excitation and optical detection of fundamental flexural guided wave in coated bone phantoms,” Ultrasound Med. Biol. 40(3), 521–531 (2014).
    [Crossref] [PubMed]
  16. Y. Yang, S. Wang, C. Tao, X. Wang, and X. Liu, “Photoacoustic tomography of tissue subwavelength microstructure with a narrowband and low frequency system,” Appl. Phys. Lett. 101(3), 034105 (2012).
    [Crossref]
  17. G. Xu, I. A. Dar, C. Tao, X. Liu, C. X. Deng, and X. Wang, “Photoacoustic spectrum analysis for microstructure characterization in biological tissue: A feasibility study,” Appl. Phys. Lett. 101(22), 221102 (2012).
    [Crossref] [PubMed]
  18. S. Wang, C. Tao, X. Wang, and X. Liu, “Quantitative detection of stochastic microstructure in turbid media by photoacoustic spectral matching,” Appl. Phys. Lett. 102(11), 114102 (2013).
    [Crossref]
  19. E. M. Strohm, I. Gorelikov, N. Matsuura, and M. C. Kolios, “Modeling photoacoustic spectral features of micron-sized particles,” Phys. Med. Biol. 59(19), 5795–5810 (2014).
    [Crossref] [PubMed]
  20. R. E. Kumon, C. X. Deng, and X. Wang, “Frequency-domain analysis of photoacoustic imaging data from prostate adenocarcinoma tumors in a murine model,” Ultrasound Med. Biol. 37(5), 834–839 (2011).
    [Crossref] [PubMed]
  21. G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The Functional Pitch of An Organ: Quantification of Tissue Texture with Photoacoustic Spectrum Analysis,” Radiology 271(1), 248–254 (2014).
    [Crossref] [PubMed]
  22. A. M. Parfitt, C. H. Mathews, A. R. Villanueva, M. Kleerekoper, B. Frame, and D. S. Rao, “Relationships between surface, volume, and thickness of iliac trabecular bone in aging and in osteoporosis. Implications for the microanatomic and cellular mechanisms of bone loss,” J. Clin. Invest. 72(4), 1396–1409 (1983).
    [Crossref] [PubMed]
  23. B. T. Cox, S. Kara, S. R. Arridge, and P. C. Beard, “k-space propagation models for acoustically heterogeneous media: Application to biomedical photoacoustics,” J. Acoust. Soc. Am. 121(6), 3453–3464 (2007).
    [Crossref] [PubMed]
  24. M. Glatt, A. Pataki, G. P. Evans, S. B. Hornby, and J. R. Green, “Loss of vertebral bone and mechanical strength in estrogen-deficient rats is prevented by long-term administration of zoledronic acid,” Osteoporos. Int. 15(9), 707–715 (2004).
    [Crossref] [PubMed]
  25. C. Chappard, E. Camus, F. Lefebvre, G. Guillot, J. Bittoun, G. Berger, and P. Laugier, “Evaluation of error bounds on calcaneal speed of sound caused by surrounding soft tissue,” J. Clin. Densitom. 3(2), 121–131 (2000).
    [Crossref] [PubMed]
  26. M. O. Culjat, D. Goldenberg, P. Tewari, and R. S. Singh, “A review of tissue substitutes for ultrasound imaging,” Ultrasound Med. Biol. 36(6), 861–873 (2010).
    [Crossref] [PubMed]
  27. M. L. Oelze and W. D. O’Brien., “Frequency-dependent attenuation-compensation functions for ultrasonic signals backscattered from random media,” J. Acoust. Soc. Am. 111(5), 2308–2319 (2002).
    [Crossref] [PubMed]
  28. T. J. Allen, B. T. Cox, and P. C. Beard, “Generating photoacoustic signals using high-peak power pulsed laser diodes,” in Photons Plus Ultrasound: Imaging and Sensing 2005, A. A. Oraevsky, and L. V. Wang, eds. (Spie-Int Soc Optical Engineering, Bellingham, 2005), pp. 233–242.
  29. P. Karppinen, A. Salmi, P. Moilanen, T. Karppinen, Z. M. Zhao, R. Myllyla, J. Timonen, and E. Haeggstrom, “Phase-delayed laser diode array allows ultrasonic guided wave mode selection and tuning,” J. Appl. Phys. 113(14), 144904 (2013).
    [Crossref]

2015 (3)

B. Lashkari, L. Yang, and A. Mandelis, “The application of backscattered ultrasound and photoacoustic signals for assessment of bone collagen and mineral contents,” Quant. Imaging Med. Surg. 5(1), 46–56 (2015).
[PubMed]

L. Yang, B. Lashkari, J. W. Tan, and A. Mandelis, “Photoacoustic and ultrasound imaging of cancellous bone tissue,” J. Biomed. Opt. 20(7), 076016 (2015).
[Crossref] [PubMed]

T. Feng, K. M. Kozloff, C. Tian, J. E. Perosky, Y.-S. Hsiao, S. Du, J. Yuan, C. X. Deng, and X. Wang, “Bone assessment via thermal photo-acoustic measurements,” Opt. Lett. 40(8), 1721–1724 (2015).
[Crossref] [PubMed]

2014 (5)

C. Liu, D. Ta, F. Fujita, T. Hachiken, M. Matsukawa, K. Mizuno, and W. Wang, “The relationship between ultrasonic backscatter and trabecular anisotropic microstructure in cancellous bone,” J. Appl. Phys. 115(6), 064906 (2014).
[Crossref]

P. Moilanen, Z. Zhao, P. Karppinen, T. Karppinen, V. Kilappa, J. Pirhonen, R. Myllylä, E. Haeggström, and J. Timonen, “Photo-acoustic excitation and optical detection of fundamental flexural guided wave in coated bone phantoms,” Ultrasound Med. Biol. 40(3), 521–531 (2014).
[Crossref] [PubMed]

B. Lashkari and A. Mandelis, “Coregistered photoacoustic and ultrasonic signatures of early bone density variations,” J. Biomed. Opt. 19(3), 036015 (2014).
[Crossref] [PubMed]

E. M. Strohm, I. Gorelikov, N. Matsuura, and M. C. Kolios, “Modeling photoacoustic spectral features of micron-sized particles,” Phys. Med. Biol. 59(19), 5795–5810 (2014).
[Crossref] [PubMed]

G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The Functional Pitch of An Organ: Quantification of Tissue Texture with Photoacoustic Spectrum Analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

2013 (3)

P. Karppinen, A. Salmi, P. Moilanen, T. Karppinen, Z. M. Zhao, R. Myllyla, J. Timonen, and E. Haeggstrom, “Phase-delayed laser diode array allows ultrasonic guided wave mode selection and tuning,” J. Appl. Phys. 113(14), 144904 (2013).
[Crossref]

S. Wang, C. Tao, X. Wang, and X. Liu, “Quantitative detection of stochastic microstructure in turbid media by photoacoustic spectral matching,” Appl. Phys. Lett. 102(11), 114102 (2013).
[Crossref]

P. Pisani, M. D. Renna, F. Conversano, E. Casciaro, M. Muratore, E. Quarta, M. D. Paola, and S. Casciaro, “Screening and early diagnosis of osteoporosis through X-ray and ultrasound based techniques,” World J. Radiol. 5(11), 398–410 (2013).
[Crossref] [PubMed]

2012 (2)

Y. Yang, S. Wang, C. Tao, X. Wang, and X. Liu, “Photoacoustic tomography of tissue subwavelength microstructure with a narrowband and low frequency system,” Appl. Phys. Lett. 101(3), 034105 (2012).
[Crossref]

G. Xu, I. A. Dar, C. Tao, X. Liu, C. X. Deng, and X. Wang, “Photoacoustic spectrum analysis for microstructure characterization in biological tissue: A feasibility study,” Appl. Phys. Lett. 101(22), 221102 (2012).
[Crossref] [PubMed]

2011 (2)

R. E. Kumon, C. X. Deng, and X. Wang, “Frequency-domain analysis of photoacoustic imaging data from prostate adenocarcinoma tumors in a murine model,” Ultrasound Med. Biol. 37(5), 834–839 (2011).
[Crossref] [PubMed]

C. V. Albanese, F. De Terlizzi, and R. Passariello, “Quantitative ultrasound of the phalanges and DXA of the lumbar spine and proximal femur in evaluating the risk of osteoporotic vertebral fracture in postmenopausal women,” Radiol. Med. (Torino) 116(1), 92–101 (2011).
[Crossref] [PubMed]

2010 (1)

M. O. Culjat, D. Goldenberg, P. Tewari, and R. S. Singh, “A review of tissue substitutes for ultrasound imaging,” Ultrasound Med. Biol. 36(6), 861–873 (2010).
[Crossref] [PubMed]

2007 (1)

B. T. Cox, S. Kara, S. R. Arridge, and P. C. Beard, “k-space propagation models for acoustically heterogeneous media: Application to biomedical photoacoustics,” J. Acoust. Soc. Am. 121(6), 3453–3464 (2007).
[Crossref] [PubMed]

2004 (2)

M. Glatt, A. Pataki, G. P. Evans, S. B. Hornby, and J. R. Green, “Loss of vertebral bone and mechanical strength in estrogen-deficient rats is prevented by long-term administration of zoledronic acid,” Osteoporos. Int. 15(9), 707–715 (2004).
[Crossref] [PubMed]

A. Pifferi, A. Torricelli, P. Taroni, A. Bassi, E. Chikoidze, E. Giambattistelli, and R. Cubeddu, “Optical biopsy of bone tissue: a step toward the diagnosis of bone pathologies,” J. Biomed. Opt. 9(3), 474–480 (2004).
[Crossref] [PubMed]

2002 (2)

J. Töyräs, M. T. Nieminen, H. Kröger, and J. S. Jurvelin, “Bone mineral density, ultrasound velocity, and broadband attenuation predict mechanical properties of trabecular bone differently,” Bone 31(4), 503–507 (2002).
[Crossref] [PubMed]

M. L. Oelze and W. D. O’Brien., “Frequency-dependent attenuation-compensation functions for ultrasonic signals backscattered from random media,” J. Acoust. Soc. Am. 111(5), 2308–2319 (2002).
[Crossref] [PubMed]

2000 (1)

C. Chappard, E. Camus, F. Lefebvre, G. Guillot, J. Bittoun, G. Berger, and P. Laugier, “Evaluation of error bounds on calcaneal speed of sound caused by surrounding soft tissue,” J. Clin. Densitom. 3(2), 121–131 (2000).
[Crossref] [PubMed]

1997 (1)

C. F. Njeh, C. M. Boivin, and C. M. Langton, “The role of ultrasound in the assessment of osteoporosis: a review,” Osteoporos. Int. 7(1), 7–22 (1997).
[Crossref] [PubMed]

1994 (1)

C. C. Glüer, C. Y. Wu, M. Jergas, S. A. Goldstein, and H. K. Genant, “Three quantitative ultrasound parameters reflect bone structure,” Calcif. Tissue Int. 55(1), 46–52 (1994).
[Crossref] [PubMed]

1991 (1)

W. C. Hayes, S. J. Piazza, and P. K. Zysset, “Biomechanics of fracture risk prediction of the hip and spine by quantitative computed tomography,” Radiol. Clin. North Am. 29(1), 1–18 (1991).
[PubMed]

1983 (1)

A. M. Parfitt, C. H. Mathews, A. R. Villanueva, M. Kleerekoper, B. Frame, and D. S. Rao, “Relationships between surface, volume, and thickness of iliac trabecular bone in aging and in osteoporosis. Implications for the microanatomic and cellular mechanisms of bone loss,” J. Clin. Invest. 72(4), 1396–1409 (1983).
[Crossref] [PubMed]

Albanese, C. V.

C. V. Albanese, F. De Terlizzi, and R. Passariello, “Quantitative ultrasound of the phalanges and DXA of the lumbar spine and proximal femur in evaluating the risk of osteoporotic vertebral fracture in postmenopausal women,” Radiol. Med. (Torino) 116(1), 92–101 (2011).
[Crossref] [PubMed]

Arridge, S. R.

B. T. Cox, S. Kara, S. R. Arridge, and P. C. Beard, “k-space propagation models for acoustically heterogeneous media: Application to biomedical photoacoustics,” J. Acoust. Soc. Am. 121(6), 3453–3464 (2007).
[Crossref] [PubMed]

Bassi, A.

A. Pifferi, A. Torricelli, P. Taroni, A. Bassi, E. Chikoidze, E. Giambattistelli, and R. Cubeddu, “Optical biopsy of bone tissue: a step toward the diagnosis of bone pathologies,” J. Biomed. Opt. 9(3), 474–480 (2004).
[Crossref] [PubMed]

Beard, P. C.

B. T. Cox, S. Kara, S. R. Arridge, and P. C. Beard, “k-space propagation models for acoustically heterogeneous media: Application to biomedical photoacoustics,” J. Acoust. Soc. Am. 121(6), 3453–3464 (2007).
[Crossref] [PubMed]

Berger, G.

C. Chappard, E. Camus, F. Lefebvre, G. Guillot, J. Bittoun, G. Berger, and P. Laugier, “Evaluation of error bounds on calcaneal speed of sound caused by surrounding soft tissue,” J. Clin. Densitom. 3(2), 121–131 (2000).
[Crossref] [PubMed]

Bittoun, J.

C. Chappard, E. Camus, F. Lefebvre, G. Guillot, J. Bittoun, G. Berger, and P. Laugier, “Evaluation of error bounds on calcaneal speed of sound caused by surrounding soft tissue,” J. Clin. Densitom. 3(2), 121–131 (2000).
[Crossref] [PubMed]

Boivin, C. M.

C. F. Njeh, C. M. Boivin, and C. M. Langton, “The role of ultrasound in the assessment of osteoporosis: a review,” Osteoporos. Int. 7(1), 7–22 (1997).
[Crossref] [PubMed]

Camus, E.

C. Chappard, E. Camus, F. Lefebvre, G. Guillot, J. Bittoun, G. Berger, and P. Laugier, “Evaluation of error bounds on calcaneal speed of sound caused by surrounding soft tissue,” J. Clin. Densitom. 3(2), 121–131 (2000).
[Crossref] [PubMed]

Carson, P. L.

G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The Functional Pitch of An Organ: Quantification of Tissue Texture with Photoacoustic Spectrum Analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Casciaro, E.

P. Pisani, M. D. Renna, F. Conversano, E. Casciaro, M. Muratore, E. Quarta, M. D. Paola, and S. Casciaro, “Screening and early diagnosis of osteoporosis through X-ray and ultrasound based techniques,” World J. Radiol. 5(11), 398–410 (2013).
[Crossref] [PubMed]

Casciaro, S.

P. Pisani, M. D. Renna, F. Conversano, E. Casciaro, M. Muratore, E. Quarta, M. D. Paola, and S. Casciaro, “Screening and early diagnosis of osteoporosis through X-ray and ultrasound based techniques,” World J. Radiol. 5(11), 398–410 (2013).
[Crossref] [PubMed]

Chappard, C.

C. Chappard, E. Camus, F. Lefebvre, G. Guillot, J. Bittoun, G. Berger, and P. Laugier, “Evaluation of error bounds on calcaneal speed of sound caused by surrounding soft tissue,” J. Clin. Densitom. 3(2), 121–131 (2000).
[Crossref] [PubMed]

Chikoidze, E.

A. Pifferi, A. Torricelli, P. Taroni, A. Bassi, E. Chikoidze, E. Giambattistelli, and R. Cubeddu, “Optical biopsy of bone tissue: a step toward the diagnosis of bone pathologies,” J. Biomed. Opt. 9(3), 474–480 (2004).
[Crossref] [PubMed]

Conversano, F.

P. Pisani, M. D. Renna, F. Conversano, E. Casciaro, M. Muratore, E. Quarta, M. D. Paola, and S. Casciaro, “Screening and early diagnosis of osteoporosis through X-ray and ultrasound based techniques,” World J. Radiol. 5(11), 398–410 (2013).
[Crossref] [PubMed]

Cox, B. T.

B. T. Cox, S. Kara, S. R. Arridge, and P. C. Beard, “k-space propagation models for acoustically heterogeneous media: Application to biomedical photoacoustics,” J. Acoust. Soc. Am. 121(6), 3453–3464 (2007).
[Crossref] [PubMed]

Cubeddu, R.

A. Pifferi, A. Torricelli, P. Taroni, A. Bassi, E. Chikoidze, E. Giambattistelli, and R. Cubeddu, “Optical biopsy of bone tissue: a step toward the diagnosis of bone pathologies,” J. Biomed. Opt. 9(3), 474–480 (2004).
[Crossref] [PubMed]

Culjat, M. O.

M. O. Culjat, D. Goldenberg, P. Tewari, and R. S. Singh, “A review of tissue substitutes for ultrasound imaging,” Ultrasound Med. Biol. 36(6), 861–873 (2010).
[Crossref] [PubMed]

Dar, I. A.

G. Xu, I. A. Dar, C. Tao, X. Liu, C. X. Deng, and X. Wang, “Photoacoustic spectrum analysis for microstructure characterization in biological tissue: A feasibility study,” Appl. Phys. Lett. 101(22), 221102 (2012).
[Crossref] [PubMed]

De Terlizzi, F.

C. V. Albanese, F. De Terlizzi, and R. Passariello, “Quantitative ultrasound of the phalanges and DXA of the lumbar spine and proximal femur in evaluating the risk of osteoporotic vertebral fracture in postmenopausal women,” Radiol. Med. (Torino) 116(1), 92–101 (2011).
[Crossref] [PubMed]

Deng, C. X.

T. Feng, K. M. Kozloff, C. Tian, J. E. Perosky, Y.-S. Hsiao, S. Du, J. Yuan, C. X. Deng, and X. Wang, “Bone assessment via thermal photo-acoustic measurements,” Opt. Lett. 40(8), 1721–1724 (2015).
[Crossref] [PubMed]

G. Xu, I. A. Dar, C. Tao, X. Liu, C. X. Deng, and X. Wang, “Photoacoustic spectrum analysis for microstructure characterization in biological tissue: A feasibility study,” Appl. Phys. Lett. 101(22), 221102 (2012).
[Crossref] [PubMed]

R. E. Kumon, C. X. Deng, and X. Wang, “Frequency-domain analysis of photoacoustic imaging data from prostate adenocarcinoma tumors in a murine model,” Ultrasound Med. Biol. 37(5), 834–839 (2011).
[Crossref] [PubMed]

Du, S.

Evans, G. P.

M. Glatt, A. Pataki, G. P. Evans, S. B. Hornby, and J. R. Green, “Loss of vertebral bone and mechanical strength in estrogen-deficient rats is prevented by long-term administration of zoledronic acid,” Osteoporos. Int. 15(9), 707–715 (2004).
[Crossref] [PubMed]

Feng, T.

Frame, B.

A. M. Parfitt, C. H. Mathews, A. R. Villanueva, M. Kleerekoper, B. Frame, and D. S. Rao, “Relationships between surface, volume, and thickness of iliac trabecular bone in aging and in osteoporosis. Implications for the microanatomic and cellular mechanisms of bone loss,” J. Clin. Invest. 72(4), 1396–1409 (1983).
[Crossref] [PubMed]

Fujita, F.

C. Liu, D. Ta, F. Fujita, T. Hachiken, M. Matsukawa, K. Mizuno, and W. Wang, “The relationship between ultrasonic backscatter and trabecular anisotropic microstructure in cancellous bone,” J. Appl. Phys. 115(6), 064906 (2014).
[Crossref]

Genant, H. K.

C. C. Glüer, C. Y. Wu, M. Jergas, S. A. Goldstein, and H. K. Genant, “Three quantitative ultrasound parameters reflect bone structure,” Calcif. Tissue Int. 55(1), 46–52 (1994).
[Crossref] [PubMed]

Giambattistelli, E.

A. Pifferi, A. Torricelli, P. Taroni, A. Bassi, E. Chikoidze, E. Giambattistelli, and R. Cubeddu, “Optical biopsy of bone tissue: a step toward the diagnosis of bone pathologies,” J. Biomed. Opt. 9(3), 474–480 (2004).
[Crossref] [PubMed]

Glatt, M.

M. Glatt, A. Pataki, G. P. Evans, S. B. Hornby, and J. R. Green, “Loss of vertebral bone and mechanical strength in estrogen-deficient rats is prevented by long-term administration of zoledronic acid,” Osteoporos. Int. 15(9), 707–715 (2004).
[Crossref] [PubMed]

Glüer, C. C.

C. C. Glüer, C. Y. Wu, M. Jergas, S. A. Goldstein, and H. K. Genant, “Three quantitative ultrasound parameters reflect bone structure,” Calcif. Tissue Int. 55(1), 46–52 (1994).
[Crossref] [PubMed]

Goldenberg, D.

M. O. Culjat, D. Goldenberg, P. Tewari, and R. S. Singh, “A review of tissue substitutes for ultrasound imaging,” Ultrasound Med. Biol. 36(6), 861–873 (2010).
[Crossref] [PubMed]

Goldstein, S. A.

C. C. Glüer, C. Y. Wu, M. Jergas, S. A. Goldstein, and H. K. Genant, “Three quantitative ultrasound parameters reflect bone structure,” Calcif. Tissue Int. 55(1), 46–52 (1994).
[Crossref] [PubMed]

Gorelikov, I.

E. M. Strohm, I. Gorelikov, N. Matsuura, and M. C. Kolios, “Modeling photoacoustic spectral features of micron-sized particles,” Phys. Med. Biol. 59(19), 5795–5810 (2014).
[Crossref] [PubMed]

Green, J. R.

M. Glatt, A. Pataki, G. P. Evans, S. B. Hornby, and J. R. Green, “Loss of vertebral bone and mechanical strength in estrogen-deficient rats is prevented by long-term administration of zoledronic acid,” Osteoporos. Int. 15(9), 707–715 (2004).
[Crossref] [PubMed]

Guillot, G.

C. Chappard, E. Camus, F. Lefebvre, G. Guillot, J. Bittoun, G. Berger, and P. Laugier, “Evaluation of error bounds on calcaneal speed of sound caused by surrounding soft tissue,” J. Clin. Densitom. 3(2), 121–131 (2000).
[Crossref] [PubMed]

Hachiken, T.

C. Liu, D. Ta, F. Fujita, T. Hachiken, M. Matsukawa, K. Mizuno, and W. Wang, “The relationship between ultrasonic backscatter and trabecular anisotropic microstructure in cancellous bone,” J. Appl. Phys. 115(6), 064906 (2014).
[Crossref]

Haeggstrom, E.

P. Karppinen, A. Salmi, P. Moilanen, T. Karppinen, Z. M. Zhao, R. Myllyla, J. Timonen, and E. Haeggstrom, “Phase-delayed laser diode array allows ultrasonic guided wave mode selection and tuning,” J. Appl. Phys. 113(14), 144904 (2013).
[Crossref]

Haeggström, E.

P. Moilanen, Z. Zhao, P. Karppinen, T. Karppinen, V. Kilappa, J. Pirhonen, R. Myllylä, E. Haeggström, and J. Timonen, “Photo-acoustic excitation and optical detection of fundamental flexural guided wave in coated bone phantoms,” Ultrasound Med. Biol. 40(3), 521–531 (2014).
[Crossref] [PubMed]

Hayes, W. C.

W. C. Hayes, S. J. Piazza, and P. K. Zysset, “Biomechanics of fracture risk prediction of the hip and spine by quantitative computed tomography,” Radiol. Clin. North Am. 29(1), 1–18 (1991).
[PubMed]

Hornby, S. B.

M. Glatt, A. Pataki, G. P. Evans, S. B. Hornby, and J. R. Green, “Loss of vertebral bone and mechanical strength in estrogen-deficient rats is prevented by long-term administration of zoledronic acid,” Osteoporos. Int. 15(9), 707–715 (2004).
[Crossref] [PubMed]

Hsiao, Y.-S.

Jergas, M.

C. C. Glüer, C. Y. Wu, M. Jergas, S. A. Goldstein, and H. K. Genant, “Three quantitative ultrasound parameters reflect bone structure,” Calcif. Tissue Int. 55(1), 46–52 (1994).
[Crossref] [PubMed]

Joshi, B.

G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The Functional Pitch of An Organ: Quantification of Tissue Texture with Photoacoustic Spectrum Analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Jurvelin, J. S.

J. Töyräs, M. T. Nieminen, H. Kröger, and J. S. Jurvelin, “Bone mineral density, ultrasound velocity, and broadband attenuation predict mechanical properties of trabecular bone differently,” Bone 31(4), 503–507 (2002).
[Crossref] [PubMed]

Kara, S.

B. T. Cox, S. Kara, S. R. Arridge, and P. C. Beard, “k-space propagation models for acoustically heterogeneous media: Application to biomedical photoacoustics,” J. Acoust. Soc. Am. 121(6), 3453–3464 (2007).
[Crossref] [PubMed]

Karppinen, P.

P. Moilanen, Z. Zhao, P. Karppinen, T. Karppinen, V. Kilappa, J. Pirhonen, R. Myllylä, E. Haeggström, and J. Timonen, “Photo-acoustic excitation and optical detection of fundamental flexural guided wave in coated bone phantoms,” Ultrasound Med. Biol. 40(3), 521–531 (2014).
[Crossref] [PubMed]

P. Karppinen, A. Salmi, P. Moilanen, T. Karppinen, Z. M. Zhao, R. Myllyla, J. Timonen, and E. Haeggstrom, “Phase-delayed laser diode array allows ultrasonic guided wave mode selection and tuning,” J. Appl. Phys. 113(14), 144904 (2013).
[Crossref]

Karppinen, T.

P. Moilanen, Z. Zhao, P. Karppinen, T. Karppinen, V. Kilappa, J. Pirhonen, R. Myllylä, E. Haeggström, and J. Timonen, “Photo-acoustic excitation and optical detection of fundamental flexural guided wave in coated bone phantoms,” Ultrasound Med. Biol. 40(3), 521–531 (2014).
[Crossref] [PubMed]

P. Karppinen, A. Salmi, P. Moilanen, T. Karppinen, Z. M. Zhao, R. Myllyla, J. Timonen, and E. Haeggstrom, “Phase-delayed laser diode array allows ultrasonic guided wave mode selection and tuning,” J. Appl. Phys. 113(14), 144904 (2013).
[Crossref]

Kilappa, V.

P. Moilanen, Z. Zhao, P. Karppinen, T. Karppinen, V. Kilappa, J. Pirhonen, R. Myllylä, E. Haeggström, and J. Timonen, “Photo-acoustic excitation and optical detection of fundamental flexural guided wave in coated bone phantoms,” Ultrasound Med. Biol. 40(3), 521–531 (2014).
[Crossref] [PubMed]

Kleerekoper, M.

A. M. Parfitt, C. H. Mathews, A. R. Villanueva, M. Kleerekoper, B. Frame, and D. S. Rao, “Relationships between surface, volume, and thickness of iliac trabecular bone in aging and in osteoporosis. Implications for the microanatomic and cellular mechanisms of bone loss,” J. Clin. Invest. 72(4), 1396–1409 (1983).
[Crossref] [PubMed]

Kolios, M. C.

E. M. Strohm, I. Gorelikov, N. Matsuura, and M. C. Kolios, “Modeling photoacoustic spectral features of micron-sized particles,” Phys. Med. Biol. 59(19), 5795–5810 (2014).
[Crossref] [PubMed]

Kozloff, K. M.

Kröger, H.

J. Töyräs, M. T. Nieminen, H. Kröger, and J. S. Jurvelin, “Bone mineral density, ultrasound velocity, and broadband attenuation predict mechanical properties of trabecular bone differently,” Bone 31(4), 503–507 (2002).
[Crossref] [PubMed]

Kumon, R. E.

R. E. Kumon, C. X. Deng, and X. Wang, “Frequency-domain analysis of photoacoustic imaging data from prostate adenocarcinoma tumors in a murine model,” Ultrasound Med. Biol. 37(5), 834–839 (2011).
[Crossref] [PubMed]

Langton, C. M.

C. F. Njeh, C. M. Boivin, and C. M. Langton, “The role of ultrasound in the assessment of osteoporosis: a review,” Osteoporos. Int. 7(1), 7–22 (1997).
[Crossref] [PubMed]

Lashkari, B.

L. Yang, B. Lashkari, J. W. Tan, and A. Mandelis, “Photoacoustic and ultrasound imaging of cancellous bone tissue,” J. Biomed. Opt. 20(7), 076016 (2015).
[Crossref] [PubMed]

B. Lashkari, L. Yang, and A. Mandelis, “The application of backscattered ultrasound and photoacoustic signals for assessment of bone collagen and mineral contents,” Quant. Imaging Med. Surg. 5(1), 46–56 (2015).
[PubMed]

B. Lashkari and A. Mandelis, “Coregistered photoacoustic and ultrasonic signatures of early bone density variations,” J. Biomed. Opt. 19(3), 036015 (2014).
[Crossref] [PubMed]

Laugier, P.

C. Chappard, E. Camus, F. Lefebvre, G. Guillot, J. Bittoun, G. Berger, and P. Laugier, “Evaluation of error bounds on calcaneal speed of sound caused by surrounding soft tissue,” J. Clin. Densitom. 3(2), 121–131 (2000).
[Crossref] [PubMed]

Lefebvre, F.

C. Chappard, E. Camus, F. Lefebvre, G. Guillot, J. Bittoun, G. Berger, and P. Laugier, “Evaluation of error bounds on calcaneal speed of sound caused by surrounding soft tissue,” J. Clin. Densitom. 3(2), 121–131 (2000).
[Crossref] [PubMed]

Lin, J. D.

G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The Functional Pitch of An Organ: Quantification of Tissue Texture with Photoacoustic Spectrum Analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Liu, C.

C. Liu, D. Ta, F. Fujita, T. Hachiken, M. Matsukawa, K. Mizuno, and W. Wang, “The relationship between ultrasonic backscatter and trabecular anisotropic microstructure in cancellous bone,” J. Appl. Phys. 115(6), 064906 (2014).
[Crossref]

Liu, X.

S. Wang, C. Tao, X. Wang, and X. Liu, “Quantitative detection of stochastic microstructure in turbid media by photoacoustic spectral matching,” Appl. Phys. Lett. 102(11), 114102 (2013).
[Crossref]

G. Xu, I. A. Dar, C. Tao, X. Liu, C. X. Deng, and X. Wang, “Photoacoustic spectrum analysis for microstructure characterization in biological tissue: A feasibility study,” Appl. Phys. Lett. 101(22), 221102 (2012).
[Crossref] [PubMed]

Y. Yang, S. Wang, C. Tao, X. Wang, and X. Liu, “Photoacoustic tomography of tissue subwavelength microstructure with a narrowband and low frequency system,” Appl. Phys. Lett. 101(3), 034105 (2012).
[Crossref]

Mandelis, A.

B. Lashkari, L. Yang, and A. Mandelis, “The application of backscattered ultrasound and photoacoustic signals for assessment of bone collagen and mineral contents,” Quant. Imaging Med. Surg. 5(1), 46–56 (2015).
[PubMed]

L. Yang, B. Lashkari, J. W. Tan, and A. Mandelis, “Photoacoustic and ultrasound imaging of cancellous bone tissue,” J. Biomed. Opt. 20(7), 076016 (2015).
[Crossref] [PubMed]

B. Lashkari and A. Mandelis, “Coregistered photoacoustic and ultrasonic signatures of early bone density variations,” J. Biomed. Opt. 19(3), 036015 (2014).
[Crossref] [PubMed]

Mathews, C. H.

A. M. Parfitt, C. H. Mathews, A. R. Villanueva, M. Kleerekoper, B. Frame, and D. S. Rao, “Relationships between surface, volume, and thickness of iliac trabecular bone in aging and in osteoporosis. Implications for the microanatomic and cellular mechanisms of bone loss,” J. Clin. Invest. 72(4), 1396–1409 (1983).
[Crossref] [PubMed]

Matsukawa, M.

C. Liu, D. Ta, F. Fujita, T. Hachiken, M. Matsukawa, K. Mizuno, and W. Wang, “The relationship between ultrasonic backscatter and trabecular anisotropic microstructure in cancellous bone,” J. Appl. Phys. 115(6), 064906 (2014).
[Crossref]

Matsuura, N.

E. M. Strohm, I. Gorelikov, N. Matsuura, and M. C. Kolios, “Modeling photoacoustic spectral features of micron-sized particles,” Phys. Med. Biol. 59(19), 5795–5810 (2014).
[Crossref] [PubMed]

Meng, Z.-X.

G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The Functional Pitch of An Organ: Quantification of Tissue Texture with Photoacoustic Spectrum Analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Mizuno, K.

C. Liu, D. Ta, F. Fujita, T. Hachiken, M. Matsukawa, K. Mizuno, and W. Wang, “The relationship between ultrasonic backscatter and trabecular anisotropic microstructure in cancellous bone,” J. Appl. Phys. 115(6), 064906 (2014).
[Crossref]

Moilanen, P.

P. Moilanen, Z. Zhao, P. Karppinen, T. Karppinen, V. Kilappa, J. Pirhonen, R. Myllylä, E. Haeggström, and J. Timonen, “Photo-acoustic excitation and optical detection of fundamental flexural guided wave in coated bone phantoms,” Ultrasound Med. Biol. 40(3), 521–531 (2014).
[Crossref] [PubMed]

P. Karppinen, A. Salmi, P. Moilanen, T. Karppinen, Z. M. Zhao, R. Myllyla, J. Timonen, and E. Haeggstrom, “Phase-delayed laser diode array allows ultrasonic guided wave mode selection and tuning,” J. Appl. Phys. 113(14), 144904 (2013).
[Crossref]

Muratore, M.

P. Pisani, M. D. Renna, F. Conversano, E. Casciaro, M. Muratore, E. Quarta, M. D. Paola, and S. Casciaro, “Screening and early diagnosis of osteoporosis through X-ray and ultrasound based techniques,” World J. Radiol. 5(11), 398–410 (2013).
[Crossref] [PubMed]

Myllyla, R.

P. Karppinen, A. Salmi, P. Moilanen, T. Karppinen, Z. M. Zhao, R. Myllyla, J. Timonen, and E. Haeggstrom, “Phase-delayed laser diode array allows ultrasonic guided wave mode selection and tuning,” J. Appl. Phys. 113(14), 144904 (2013).
[Crossref]

Myllylä, R.

P. Moilanen, Z. Zhao, P. Karppinen, T. Karppinen, V. Kilappa, J. Pirhonen, R. Myllylä, E. Haeggström, and J. Timonen, “Photo-acoustic excitation and optical detection of fundamental flexural guided wave in coated bone phantoms,” Ultrasound Med. Biol. 40(3), 521–531 (2014).
[Crossref] [PubMed]

Nieminen, M. T.

J. Töyräs, M. T. Nieminen, H. Kröger, and J. S. Jurvelin, “Bone mineral density, ultrasound velocity, and broadband attenuation predict mechanical properties of trabecular bone differently,” Bone 31(4), 503–507 (2002).
[Crossref] [PubMed]

Njeh, C. F.

C. F. Njeh, C. M. Boivin, and C. M. Langton, “The role of ultrasound in the assessment of osteoporosis: a review,” Osteoporos. Int. 7(1), 7–22 (1997).
[Crossref] [PubMed]

O’Brien, W. D.

M. L. Oelze and W. D. O’Brien., “Frequency-dependent attenuation-compensation functions for ultrasonic signals backscattered from random media,” J. Acoust. Soc. Am. 111(5), 2308–2319 (2002).
[Crossref] [PubMed]

Oelze, M. L.

M. L. Oelze and W. D. O’Brien., “Frequency-dependent attenuation-compensation functions for ultrasonic signals backscattered from random media,” J. Acoust. Soc. Am. 111(5), 2308–2319 (2002).
[Crossref] [PubMed]

Paola, M. D.

P. Pisani, M. D. Renna, F. Conversano, E. Casciaro, M. Muratore, E. Quarta, M. D. Paola, and S. Casciaro, “Screening and early diagnosis of osteoporosis through X-ray and ultrasound based techniques,” World J. Radiol. 5(11), 398–410 (2013).
[Crossref] [PubMed]

Parfitt, A. M.

A. M. Parfitt, C. H. Mathews, A. R. Villanueva, M. Kleerekoper, B. Frame, and D. S. Rao, “Relationships between surface, volume, and thickness of iliac trabecular bone in aging and in osteoporosis. Implications for the microanatomic and cellular mechanisms of bone loss,” J. Clin. Invest. 72(4), 1396–1409 (1983).
[Crossref] [PubMed]

Passariello, R.

C. V. Albanese, F. De Terlizzi, and R. Passariello, “Quantitative ultrasound of the phalanges and DXA of the lumbar spine and proximal femur in evaluating the risk of osteoporotic vertebral fracture in postmenopausal women,” Radiol. Med. (Torino) 116(1), 92–101 (2011).
[Crossref] [PubMed]

Pataki, A.

M. Glatt, A. Pataki, G. P. Evans, S. B. Hornby, and J. R. Green, “Loss of vertebral bone and mechanical strength in estrogen-deficient rats is prevented by long-term administration of zoledronic acid,” Osteoporos. Int. 15(9), 707–715 (2004).
[Crossref] [PubMed]

Perosky, J. E.

Piazza, S. J.

W. C. Hayes, S. J. Piazza, and P. K. Zysset, “Biomechanics of fracture risk prediction of the hip and spine by quantitative computed tomography,” Radiol. Clin. North Am. 29(1), 1–18 (1991).
[PubMed]

Pifferi, A.

A. Pifferi, A. Torricelli, P. Taroni, A. Bassi, E. Chikoidze, E. Giambattistelli, and R. Cubeddu, “Optical biopsy of bone tissue: a step toward the diagnosis of bone pathologies,” J. Biomed. Opt. 9(3), 474–480 (2004).
[Crossref] [PubMed]

Pirhonen, J.

P. Moilanen, Z. Zhao, P. Karppinen, T. Karppinen, V. Kilappa, J. Pirhonen, R. Myllylä, E. Haeggström, and J. Timonen, “Photo-acoustic excitation and optical detection of fundamental flexural guided wave in coated bone phantoms,” Ultrasound Med. Biol. 40(3), 521–531 (2014).
[Crossref] [PubMed]

Pisani, P.

P. Pisani, M. D. Renna, F. Conversano, E. Casciaro, M. Muratore, E. Quarta, M. D. Paola, and S. Casciaro, “Screening and early diagnosis of osteoporosis through X-ray and ultrasound based techniques,” World J. Radiol. 5(11), 398–410 (2013).
[Crossref] [PubMed]

Quarta, E.

P. Pisani, M. D. Renna, F. Conversano, E. Casciaro, M. Muratore, E. Quarta, M. D. Paola, and S. Casciaro, “Screening and early diagnosis of osteoporosis through X-ray and ultrasound based techniques,” World J. Radiol. 5(11), 398–410 (2013).
[Crossref] [PubMed]

Rao, D. S.

A. M. Parfitt, C. H. Mathews, A. R. Villanueva, M. Kleerekoper, B. Frame, and D. S. Rao, “Relationships between surface, volume, and thickness of iliac trabecular bone in aging and in osteoporosis. Implications for the microanatomic and cellular mechanisms of bone loss,” J. Clin. Invest. 72(4), 1396–1409 (1983).
[Crossref] [PubMed]

Renna, M. D.

P. Pisani, M. D. Renna, F. Conversano, E. Casciaro, M. Muratore, E. Quarta, M. D. Paola, and S. Casciaro, “Screening and early diagnosis of osteoporosis through X-ray and ultrasound based techniques,” World J. Radiol. 5(11), 398–410 (2013).
[Crossref] [PubMed]

Salmi, A.

P. Karppinen, A. Salmi, P. Moilanen, T. Karppinen, Z. M. Zhao, R. Myllyla, J. Timonen, and E. Haeggstrom, “Phase-delayed laser diode array allows ultrasonic guided wave mode selection and tuning,” J. Appl. Phys. 113(14), 144904 (2013).
[Crossref]

Singh, R. S.

M. O. Culjat, D. Goldenberg, P. Tewari, and R. S. Singh, “A review of tissue substitutes for ultrasound imaging,” Ultrasound Med. Biol. 36(6), 861–873 (2010).
[Crossref] [PubMed]

Strohm, E. M.

E. M. Strohm, I. Gorelikov, N. Matsuura, and M. C. Kolios, “Modeling photoacoustic spectral features of micron-sized particles,” Phys. Med. Biol. 59(19), 5795–5810 (2014).
[Crossref] [PubMed]

Ta, D.

C. Liu, D. Ta, F. Fujita, T. Hachiken, M. Matsukawa, K. Mizuno, and W. Wang, “The relationship between ultrasonic backscatter and trabecular anisotropic microstructure in cancellous bone,” J. Appl. Phys. 115(6), 064906 (2014).
[Crossref]

Tan, J. W.

L. Yang, B. Lashkari, J. W. Tan, and A. Mandelis, “Photoacoustic and ultrasound imaging of cancellous bone tissue,” J. Biomed. Opt. 20(7), 076016 (2015).
[Crossref] [PubMed]

Tao, C.

S. Wang, C. Tao, X. Wang, and X. Liu, “Quantitative detection of stochastic microstructure in turbid media by photoacoustic spectral matching,” Appl. Phys. Lett. 102(11), 114102 (2013).
[Crossref]

G. Xu, I. A. Dar, C. Tao, X. Liu, C. X. Deng, and X. Wang, “Photoacoustic spectrum analysis for microstructure characterization in biological tissue: A feasibility study,” Appl. Phys. Lett. 101(22), 221102 (2012).
[Crossref] [PubMed]

Y. Yang, S. Wang, C. Tao, X. Wang, and X. Liu, “Photoacoustic tomography of tissue subwavelength microstructure with a narrowband and low frequency system,” Appl. Phys. Lett. 101(3), 034105 (2012).
[Crossref]

Taroni, P.

A. Pifferi, A. Torricelli, P. Taroni, A. Bassi, E. Chikoidze, E. Giambattistelli, and R. Cubeddu, “Optical biopsy of bone tissue: a step toward the diagnosis of bone pathologies,” J. Biomed. Opt. 9(3), 474–480 (2004).
[Crossref] [PubMed]

Tewari, P.

M. O. Culjat, D. Goldenberg, P. Tewari, and R. S. Singh, “A review of tissue substitutes for ultrasound imaging,” Ultrasound Med. Biol. 36(6), 861–873 (2010).
[Crossref] [PubMed]

Tian, C.

Timonen, J.

P. Moilanen, Z. Zhao, P. Karppinen, T. Karppinen, V. Kilappa, J. Pirhonen, R. Myllylä, E. Haeggström, and J. Timonen, “Photo-acoustic excitation and optical detection of fundamental flexural guided wave in coated bone phantoms,” Ultrasound Med. Biol. 40(3), 521–531 (2014).
[Crossref] [PubMed]

P. Karppinen, A. Salmi, P. Moilanen, T. Karppinen, Z. M. Zhao, R. Myllyla, J. Timonen, and E. Haeggstrom, “Phase-delayed laser diode array allows ultrasonic guided wave mode selection and tuning,” J. Appl. Phys. 113(14), 144904 (2013).
[Crossref]

Torricelli, A.

A. Pifferi, A. Torricelli, P. Taroni, A. Bassi, E. Chikoidze, E. Giambattistelli, and R. Cubeddu, “Optical biopsy of bone tissue: a step toward the diagnosis of bone pathologies,” J. Biomed. Opt. 9(3), 474–480 (2004).
[Crossref] [PubMed]

Töyräs, J.

J. Töyräs, M. T. Nieminen, H. Kröger, and J. S. Jurvelin, “Bone mineral density, ultrasound velocity, and broadband attenuation predict mechanical properties of trabecular bone differently,” Bone 31(4), 503–507 (2002).
[Crossref] [PubMed]

Villanueva, A. R.

A. M. Parfitt, C. H. Mathews, A. R. Villanueva, M. Kleerekoper, B. Frame, and D. S. Rao, “Relationships between surface, volume, and thickness of iliac trabecular bone in aging and in osteoporosis. Implications for the microanatomic and cellular mechanisms of bone loss,” J. Clin. Invest. 72(4), 1396–1409 (1983).
[Crossref] [PubMed]

Wang, S.

S. Wang, C. Tao, X. Wang, and X. Liu, “Quantitative detection of stochastic microstructure in turbid media by photoacoustic spectral matching,” Appl. Phys. Lett. 102(11), 114102 (2013).
[Crossref]

Y. Yang, S. Wang, C. Tao, X. Wang, and X. Liu, “Photoacoustic tomography of tissue subwavelength microstructure with a narrowband and low frequency system,” Appl. Phys. Lett. 101(3), 034105 (2012).
[Crossref]

Wang, W.

C. Liu, D. Ta, F. Fujita, T. Hachiken, M. Matsukawa, K. Mizuno, and W. Wang, “The relationship between ultrasonic backscatter and trabecular anisotropic microstructure in cancellous bone,” J. Appl. Phys. 115(6), 064906 (2014).
[Crossref]

Wang, X.

T. Feng, K. M. Kozloff, C. Tian, J. E. Perosky, Y.-S. Hsiao, S. Du, J. Yuan, C. X. Deng, and X. Wang, “Bone assessment via thermal photo-acoustic measurements,” Opt. Lett. 40(8), 1721–1724 (2015).
[Crossref] [PubMed]

G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The Functional Pitch of An Organ: Quantification of Tissue Texture with Photoacoustic Spectrum Analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

S. Wang, C. Tao, X. Wang, and X. Liu, “Quantitative detection of stochastic microstructure in turbid media by photoacoustic spectral matching,” Appl. Phys. Lett. 102(11), 114102 (2013).
[Crossref]

G. Xu, I. A. Dar, C. Tao, X. Liu, C. X. Deng, and X. Wang, “Photoacoustic spectrum analysis for microstructure characterization in biological tissue: A feasibility study,” Appl. Phys. Lett. 101(22), 221102 (2012).
[Crossref] [PubMed]

Y. Yang, S. Wang, C. Tao, X. Wang, and X. Liu, “Photoacoustic tomography of tissue subwavelength microstructure with a narrowband and low frequency system,” Appl. Phys. Lett. 101(3), 034105 (2012).
[Crossref]

R. E. Kumon, C. X. Deng, and X. Wang, “Frequency-domain analysis of photoacoustic imaging data from prostate adenocarcinoma tumors in a murine model,” Ultrasound Med. Biol. 37(5), 834–839 (2011).
[Crossref] [PubMed]

Wu, C. Y.

C. C. Glüer, C. Y. Wu, M. Jergas, S. A. Goldstein, and H. K. Genant, “Three quantitative ultrasound parameters reflect bone structure,” Calcif. Tissue Int. 55(1), 46–52 (1994).
[Crossref] [PubMed]

Xu, G.

G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The Functional Pitch of An Organ: Quantification of Tissue Texture with Photoacoustic Spectrum Analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

G. Xu, I. A. Dar, C. Tao, X. Liu, C. X. Deng, and X. Wang, “Photoacoustic spectrum analysis for microstructure characterization in biological tissue: A feasibility study,” Appl. Phys. Lett. 101(22), 221102 (2012).
[Crossref] [PubMed]

Yang, L.

L. Yang, B. Lashkari, J. W. Tan, and A. Mandelis, “Photoacoustic and ultrasound imaging of cancellous bone tissue,” J. Biomed. Opt. 20(7), 076016 (2015).
[Crossref] [PubMed]

B. Lashkari, L. Yang, and A. Mandelis, “The application of backscattered ultrasound and photoacoustic signals for assessment of bone collagen and mineral contents,” Quant. Imaging Med. Surg. 5(1), 46–56 (2015).
[PubMed]

Yang, Y.

Y. Yang, S. Wang, C. Tao, X. Wang, and X. Liu, “Photoacoustic tomography of tissue subwavelength microstructure with a narrowband and low frequency system,” Appl. Phys. Lett. 101(3), 034105 (2012).
[Crossref]

Yuan, J.

T. Feng, K. M. Kozloff, C. Tian, J. E. Perosky, Y.-S. Hsiao, S. Du, J. Yuan, C. X. Deng, and X. Wang, “Bone assessment via thermal photo-acoustic measurements,” Opt. Lett. 40(8), 1721–1724 (2015).
[Crossref] [PubMed]

G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The Functional Pitch of An Organ: Quantification of Tissue Texture with Photoacoustic Spectrum Analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Zhao, Z.

P. Moilanen, Z. Zhao, P. Karppinen, T. Karppinen, V. Kilappa, J. Pirhonen, R. Myllylä, E. Haeggström, and J. Timonen, “Photo-acoustic excitation and optical detection of fundamental flexural guided wave in coated bone phantoms,” Ultrasound Med. Biol. 40(3), 521–531 (2014).
[Crossref] [PubMed]

Zhao, Z. M.

P. Karppinen, A. Salmi, P. Moilanen, T. Karppinen, Z. M. Zhao, R. Myllyla, J. Timonen, and E. Haeggstrom, “Phase-delayed laser diode array allows ultrasonic guided wave mode selection and tuning,” J. Appl. Phys. 113(14), 144904 (2013).
[Crossref]

Zysset, P. K.

W. C. Hayes, S. J. Piazza, and P. K. Zysset, “Biomechanics of fracture risk prediction of the hip and spine by quantitative computed tomography,” Radiol. Clin. North Am. 29(1), 1–18 (1991).
[PubMed]

Appl. Phys. Lett. (3)

Y. Yang, S. Wang, C. Tao, X. Wang, and X. Liu, “Photoacoustic tomography of tissue subwavelength microstructure with a narrowband and low frequency system,” Appl. Phys. Lett. 101(3), 034105 (2012).
[Crossref]

G. Xu, I. A. Dar, C. Tao, X. Liu, C. X. Deng, and X. Wang, “Photoacoustic spectrum analysis for microstructure characterization in biological tissue: A feasibility study,” Appl. Phys. Lett. 101(22), 221102 (2012).
[Crossref] [PubMed]

S. Wang, C. Tao, X. Wang, and X. Liu, “Quantitative detection of stochastic microstructure in turbid media by photoacoustic spectral matching,” Appl. Phys. Lett. 102(11), 114102 (2013).
[Crossref]

Bone (1)

J. Töyräs, M. T. Nieminen, H. Kröger, and J. S. Jurvelin, “Bone mineral density, ultrasound velocity, and broadband attenuation predict mechanical properties of trabecular bone differently,” Bone 31(4), 503–507 (2002).
[Crossref] [PubMed]

Calcif. Tissue Int. (1)

C. C. Glüer, C. Y. Wu, M. Jergas, S. A. Goldstein, and H. K. Genant, “Three quantitative ultrasound parameters reflect bone structure,” Calcif. Tissue Int. 55(1), 46–52 (1994).
[Crossref] [PubMed]

J. Acoust. Soc. Am. (2)

B. T. Cox, S. Kara, S. R. Arridge, and P. C. Beard, “k-space propagation models for acoustically heterogeneous media: Application to biomedical photoacoustics,” J. Acoust. Soc. Am. 121(6), 3453–3464 (2007).
[Crossref] [PubMed]

M. L. Oelze and W. D. O’Brien., “Frequency-dependent attenuation-compensation functions for ultrasonic signals backscattered from random media,” J. Acoust. Soc. Am. 111(5), 2308–2319 (2002).
[Crossref] [PubMed]

J. Appl. Phys. (2)

P. Karppinen, A. Salmi, P. Moilanen, T. Karppinen, Z. M. Zhao, R. Myllyla, J. Timonen, and E. Haeggstrom, “Phase-delayed laser diode array allows ultrasonic guided wave mode selection and tuning,” J. Appl. Phys. 113(14), 144904 (2013).
[Crossref]

C. Liu, D. Ta, F. Fujita, T. Hachiken, M. Matsukawa, K. Mizuno, and W. Wang, “The relationship between ultrasonic backscatter and trabecular anisotropic microstructure in cancellous bone,” J. Appl. Phys. 115(6), 064906 (2014).
[Crossref]

J. Biomed. Opt. (3)

B. Lashkari and A. Mandelis, “Coregistered photoacoustic and ultrasonic signatures of early bone density variations,” J. Biomed. Opt. 19(3), 036015 (2014).
[Crossref] [PubMed]

L. Yang, B. Lashkari, J. W. Tan, and A. Mandelis, “Photoacoustic and ultrasound imaging of cancellous bone tissue,” J. Biomed. Opt. 20(7), 076016 (2015).
[Crossref] [PubMed]

A. Pifferi, A. Torricelli, P. Taroni, A. Bassi, E. Chikoidze, E. Giambattistelli, and R. Cubeddu, “Optical biopsy of bone tissue: a step toward the diagnosis of bone pathologies,” J. Biomed. Opt. 9(3), 474–480 (2004).
[Crossref] [PubMed]

J. Clin. Densitom. (1)

C. Chappard, E. Camus, F. Lefebvre, G. Guillot, J. Bittoun, G. Berger, and P. Laugier, “Evaluation of error bounds on calcaneal speed of sound caused by surrounding soft tissue,” J. Clin. Densitom. 3(2), 121–131 (2000).
[Crossref] [PubMed]

J. Clin. Invest. (1)

A. M. Parfitt, C. H. Mathews, A. R. Villanueva, M. Kleerekoper, B. Frame, and D. S. Rao, “Relationships between surface, volume, and thickness of iliac trabecular bone in aging and in osteoporosis. Implications for the microanatomic and cellular mechanisms of bone loss,” J. Clin. Invest. 72(4), 1396–1409 (1983).
[Crossref] [PubMed]

Opt. Lett. (1)

Osteoporos. Int. (2)

C. F. Njeh, C. M. Boivin, and C. M. Langton, “The role of ultrasound in the assessment of osteoporosis: a review,” Osteoporos. Int. 7(1), 7–22 (1997).
[Crossref] [PubMed]

M. Glatt, A. Pataki, G. P. Evans, S. B. Hornby, and J. R. Green, “Loss of vertebral bone and mechanical strength in estrogen-deficient rats is prevented by long-term administration of zoledronic acid,” Osteoporos. Int. 15(9), 707–715 (2004).
[Crossref] [PubMed]

Phys. Med. Biol. (1)

E. M. Strohm, I. Gorelikov, N. Matsuura, and M. C. Kolios, “Modeling photoacoustic spectral features of micron-sized particles,” Phys. Med. Biol. 59(19), 5795–5810 (2014).
[Crossref] [PubMed]

Quant. Imaging Med. Surg. (1)

B. Lashkari, L. Yang, and A. Mandelis, “The application of backscattered ultrasound and photoacoustic signals for assessment of bone collagen and mineral contents,” Quant. Imaging Med. Surg. 5(1), 46–56 (2015).
[PubMed]

Radiol. Clin. North Am. (1)

W. C. Hayes, S. J. Piazza, and P. K. Zysset, “Biomechanics of fracture risk prediction of the hip and spine by quantitative computed tomography,” Radiol. Clin. North Am. 29(1), 1–18 (1991).
[PubMed]

Radiol. Med. (Torino) (1)

C. V. Albanese, F. De Terlizzi, and R. Passariello, “Quantitative ultrasound of the phalanges and DXA of the lumbar spine and proximal femur in evaluating the risk of osteoporotic vertebral fracture in postmenopausal women,” Radiol. Med. (Torino) 116(1), 92–101 (2011).
[Crossref] [PubMed]

Radiology (1)

G. Xu, Z.-X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The Functional Pitch of An Organ: Quantification of Tissue Texture with Photoacoustic Spectrum Analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Ultrasound Med. Biol. (3)

P. Moilanen, Z. Zhao, P. Karppinen, T. Karppinen, V. Kilappa, J. Pirhonen, R. Myllylä, E. Haeggström, and J. Timonen, “Photo-acoustic excitation and optical detection of fundamental flexural guided wave in coated bone phantoms,” Ultrasound Med. Biol. 40(3), 521–531 (2014).
[Crossref] [PubMed]

M. O. Culjat, D. Goldenberg, P. Tewari, and R. S. Singh, “A review of tissue substitutes for ultrasound imaging,” Ultrasound Med. Biol. 36(6), 861–873 (2010).
[Crossref] [PubMed]

R. E. Kumon, C. X. Deng, and X. Wang, “Frequency-domain analysis of photoacoustic imaging data from prostate adenocarcinoma tumors in a murine model,” Ultrasound Med. Biol. 37(5), 834–839 (2011).
[Crossref] [PubMed]

World J. Radiol. (1)

P. Pisani, M. D. Renna, F. Conversano, E. Casciaro, M. Muratore, E. Quarta, M. D. Paola, and S. Casciaro, “Screening and early diagnosis of osteoporosis through X-ray and ultrasound based techniques,” World J. Radiol. 5(11), 398–410 (2013).
[Crossref] [PubMed]

Other (3)

I. Steinberg, A. Eyal, and I. Gannot, “Multispectral photoacoustic method for the early detection and diagnosis of osteoporosis,” in SPIE BiOS(International Society for Optics and Photonics, 2013), pp. 85656G–85656G–85659.

I. Steinberg, I. Gannot, and A. Eyal, “Investigation of a dual modal method for bone pathologies using quantitative ultrasound and photoacoustics,” in SPIE BiOS(International Society for Optics and Photonics, 2015), pp. 93230R–93230R–93236.

T. J. Allen, B. T. Cox, and P. C. Beard, “Generating photoacoustic signals using high-peak power pulsed laser diodes,” in Photons Plus Ultrasound: Imaging and Sensing 2005, A. A. Oraevsky, and L. V. Wang, eds. (Spie-Int Soc Optical Engineering, Bellingham, 2005), pp. 233–242.

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Figures (5)

Fig. 1
Fig. 1 (A) Six artificial trabecular bone samples showing different levels of bone loss. (B) Normalized power spectral density (PSD) and linear fit (R2 = 0.90, 0.90, 0.92, 0.92, 0.94, 0.96, respectively, for samples 1-6) of each bone sample. (C) The spectral parameter slope quantified from the power spectrum of each bone sample presented as a function of the mean trabecular thickness (MTT).
Fig. 2
Fig. 2 (A) Micro-CT images of three rat tibia bones (OVX, Sham, and OVX + ZOL) with different trabecular microstructures, i.e. different mean trabecular thickness (MTTs). (B) Binarized micro-CT images of the three rat tibia bones. Their qualified MTTs were 0.050, 0.053, 0.061 mm respectivly. (C) Normalized power spectral density (PSD) and linear fit (R2 = 0.95, 0.86, 0.85, respectively, for OVX, Sham, and OVX + ZOL) of each bone sample. The leads to quantified spectral parameter slope. (D) The spectral parameter slope quantified from the power spectrum of each bone sample.
Fig. 3
Fig. 3 Experimental setup for PA measurement of bone. (B) Typical RF PA signals from a rat femur. Trabecular signal and cortical signal was distinguished base on the time flight. (C) Geometry for measuring the RF PA signal from a thin hair fiber (i.e. a point source) to be used for calibration. (D) The power specrum of the PA signal from the point source that was used later in calibrating the PA measurement from each bone specimen. (E) Power spectra density (PSD) of the trabecular signal in (B) before and after calibration.
Fig. 4
Fig. 4 Example micro-CT images of femur bones of female rats subject to (A) OVX, (B) Sham, and (C) OVX + ZOL with mean trabecular thickness (MTT) 0.10, 0.22 and 0.26 mm, demonstrating the decrease and increase in MTT for the bones in the OVX and OVX + ZOL groups, respectively, in comparion to the normal controls.
Fig. 5
Fig. 5 PASA of rat femur bone specimens. (A) Examples of power spectral density (PSD) of the RF PA signal of three groups (OVX, Sham, OVX + ZOL) after calibration by removing the system response. The corresponding linear fit (R2 = 0.24, 0.78, 0.68, respectively, for OVX, Sham, and OVX + ZOL) in the spectral range of 2.8-31.5 MHz leads to quantified spectral parameter slope. (B) The quantified spectral parameter slope of the three groups of bones.

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