Abstract

Since neovascularization has been reported that it is associated with tendinopathy, assessments of vascularity are important for both diagnosis and treatment estimation. Photoacoustic imaging, taking the advantages of good ultrasonic resolution and high optical absorption contrast, has been shown a promising tool for vascular imaging. In this study, we explore the feasibility of photoacoustic micro-imaging in noninvasive monitoring of microvascular changes in Achilles tendon injuries on a mouse model in vivo. During collagenase-induced tendinitis, a 25-MHz photoacoustic microscope was used to image microvascular changes in Achilles tendons of mice longitudinally up to 23 days. In addition, complementary tissue structural information was revealed by collateral 25-MHz ultrasound microscopy. Morphological changes and proliferation of new blood vessels in Achilles tendons were observed during and after the acute inflammation. Observed microvascular changes during tendinitis were similar to the findings in the literatures. This study demonstrates that photoacoustic imaging can potentially be a complementary tool for high sensitive diagnosis and assessment of treatment performance in tendinopathy.

© 2011 OSA

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  1. N. Maffulli, P. Sharma, and K. L. Luscombe, “Achilles tendinopathy: aetiology and management,” J. R. Soc. Med. 97(10), 472–476 (2004).
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  3. C. A. Harris and A. J. Peduto, “Achilles tendon imaging,” Australas. Radiol. 50(6), 513–525 (2006).
    [CrossRef] [PubMed]
  4. W. Grassi, E. Filippucci, A. Farina, and C. Cervini, “Sonographic imaging of tendons,” Arthritis Rheum. 43(5), 969–976 (2000).
    [CrossRef] [PubMed]
  5. M. Zanetti, A. Metzdorf, H. P. Kundert, H. Zollinger, P. Vienne, B. Seifert, and J. Hodler, “Achilles tendons: clinical relevance of neovascularization diagnosed with power Doppler US,” Radiology 227(2), 556–560 (2003).
    [CrossRef] [PubMed]
  6. L. Öhberg, R. Lorentzon, and H. Alfredson, “Neovascularisation in Achilles tendons with painful tendinosis but not in normal tendons: an ultrasonographic investigation,” Knee Surg. Sports Traumatol. Arthrosc. 9(4), 233–238 (2001).
    [CrossRef] [PubMed]
  7. M. Kristoffersen, L. Öhberg, C. Johnston, and H. Alfredson, “Neovascularisation in chronic tendon injuries detected with colour Doppler ultrasound in horse and man: implications for research and treatment,” Knee Surg. Sports Traumatol. Arthrosc. 13(6), 505–508 (2005).
    [CrossRef] [PubMed]
  8. S. A. Fenwick, B. L. Hazleman, and G. P. Riley, “The vasculature and its role in the damaged and healing tendon,” Arthritis Res. 4(4), 252–260 (2002).
    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
  10. W. van Snellenberg, J. P. Wiley, and G. Brunet, “Achilles tendon pain intensity and level of neovascularization in athletes as determined by color Doppler ultrasound,” Scand. J. Med. Sci. Sports 17(5), 530–534 (2007).
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  11. M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
    [CrossRef]
  12. D. L. Chamberland, X. Wang, and B. J. Roessler, “Photoacoustic tomography of carrageenan-induced arthritis in a rat model,” J. Biomed. Opt. 13(1), 011005 (2008).
    [CrossRef] [PubMed]
  13. H. F. Zhang, K. Maslov, M. L. Li, G. Stoica, and L. V. Wang, “In vivo volumetric imaging of subcutaneous microvasculature by photoacoustic microscopy,” Opt. Express 14(20), 9317–9323 (2006).
    [CrossRef] [PubMed]
  14. L. V. Wang, “Tutorial on Photoacoustic Microscopy and Computed Tomography,” IEEE J. Sel. Top. Quantum Electron. 14(1), 171–179 (2008).
    [CrossRef]
  15. K. Maslov, G. Stoica, and L. V. Wang, “In vivo dark-field reflection-mode photoacoustic microscopy,” Opt. Lett. 30(6), 625–627 (2005).
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  16. H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
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    [CrossRef] [PubMed]
  18. Y. J. Chen, C. J. Wang, K. D. Yang, Y. R. Kuo, H. C. Huang, Y. T. Huang, Y. C. Sun, and F. S. Wang, “Extracorporeal shock waves promote healing of collagenase-induced Achilles tendinitis and increase TGF-β1 and IGF-I expression,” J. Orthop. Res. 22(4), 854–861 (2004).
    [CrossRef] [PubMed]
  19. M. L. Li, W. J. Guan, and P. C. Li, “Improved synthetic aperture focusing technique with applications in high-frequency ultrasound imaging,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 51(1), 63–70 (2004).
    [CrossRef] [PubMed]
  20. M. L. Li, H. E. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Improved in vivo photoacoustic microscopy based on a virtual-detector concept,” Opt. Lett. 31(4), 474–476 (2006).
    [CrossRef] [PubMed]
  21. K. A. Piróg, O. Jaka, Y. Katakura, R. S. Meadows, K. E. Kadler, R. P. Boot-Handford, and M. D. Briggs, “A mouse model offers novel insights into the myopathy and tendinopathy often associated with pseudoachondroplasia and multiple epiphyseal dysplasia,” Hum. Mol. Genet. 19(1), 52–64 (2010).
    [CrossRef] [PubMed]
  22. S. J. Warden, “Animal models for the study of tendinopathy,” Br. J. Sports Med. 41(4), 232–240 (2007).
    [CrossRef] [PubMed]
  23. Y. Jiang, T. Harrison, J. Ranasinghesagara, and R. J. Zemp, “Photoacoustic and high-frequency power Doppler ultrasound biomicroscopy: a comparative study,” J. Biomed. Opt. 15(5), 056008 (2010).
    [CrossRef] [PubMed]
  24. A. G. Naccarato, P. Viacava, G. Bocci, G. Fanelli, P. Aretini, A. Lonobile, G. Montruccoli, and G. Bevilacqua, “Definition of the microvascular pattern of the normal human adult mammary gland,” J. Anat. 203(6), 599–603 (2003).
    [CrossRef] [PubMed]

2010 (2)

K. A. Piróg, O. Jaka, Y. Katakura, R. S. Meadows, K. E. Kadler, R. P. Boot-Handford, and M. D. Briggs, “A mouse model offers novel insights into the myopathy and tendinopathy often associated with pseudoachondroplasia and multiple epiphyseal dysplasia,” Hum. Mol. Genet. 19(1), 52–64 (2010).
[CrossRef] [PubMed]

Y. Jiang, T. Harrison, J. Ranasinghesagara, and R. J. Zemp, “Photoacoustic and high-frequency power Doppler ultrasound biomicroscopy: a comparative study,” J. Biomed. Opt. 15(5), 056008 (2010).
[CrossRef] [PubMed]

2009 (1)

C. K. Yeh, J. J. Chen, M. L. Li, J. J. Luh, and J. J. J. Chen, “In vivo imaging of blood flow in the mouse Achilles tendon using high-frequency ultrasound,” Ultrasonics 49(2), 226–230 (2009).
[CrossRef] [PubMed]

2008 (2)

D. L. Chamberland, X. Wang, and B. J. Roessler, “Photoacoustic tomography of carrageenan-induced arthritis in a rat model,” J. Biomed. Opt. 13(1), 011005 (2008).
[CrossRef] [PubMed]

L. V. Wang, “Tutorial on Photoacoustic Microscopy and Computed Tomography,” IEEE J. Sel. Top. Quantum Electron. 14(1), 171–179 (2008).
[CrossRef]

2007 (2)

W. van Snellenberg, J. P. Wiley, and G. Brunet, “Achilles tendon pain intensity and level of neovascularization in athletes as determined by color Doppler ultrasound,” Scand. J. Med. Sci. Sports 17(5), 530–534 (2007).
[PubMed]

S. J. Warden, “Animal models for the study of tendinopathy,” Br. J. Sports Med. 41(4), 232–240 (2007).
[CrossRef] [PubMed]

2006 (5)

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
[CrossRef]

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[CrossRef] [PubMed]

C. A. Harris and A. J. Peduto, “Achilles tendon imaging,” Australas. Radiol. 50(6), 513–525 (2006).
[CrossRef] [PubMed]

M. L. Li, H. E. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Improved in vivo photoacoustic microscopy based on a virtual-detector concept,” Opt. Lett. 31(4), 474–476 (2006).
[CrossRef] [PubMed]

H. F. Zhang, K. Maslov, M. L. Li, G. Stoica, and L. V. Wang, “In vivo volumetric imaging of subcutaneous microvasculature by photoacoustic microscopy,” Opt. Express 14(20), 9317–9323 (2006).
[CrossRef] [PubMed]

2005 (2)

K. Maslov, G. Stoica, and L. V. Wang, “In vivo dark-field reflection-mode photoacoustic microscopy,” Opt. Lett. 30(6), 625–627 (2005).
[CrossRef] [PubMed]

M. Kristoffersen, L. Öhberg, C. Johnston, and H. Alfredson, “Neovascularisation in chronic tendon injuries detected with colour Doppler ultrasound in horse and man: implications for research and treatment,” Knee Surg. Sports Traumatol. Arthrosc. 13(6), 505–508 (2005).
[CrossRef] [PubMed]

2004 (4)

N. Maffulli, P. Sharma, and K. L. Luscombe, “Achilles tendinopathy: aetiology and management,” J. R. Soc. Med. 97(10), 472–476 (2004).
[CrossRef] [PubMed]

Y. J. Chen, C. J. Wang, K. D. Yang, Y. R. Kuo, H. C. Huang, Y. T. Huang, Y. C. Sun, and F. S. Wang, “Extracorporeal shock waves promote healing of collagenase-induced Achilles tendinitis and increase TGF-β1 and IGF-I expression,” J. Orthop. Res. 22(4), 854–861 (2004).
[CrossRef] [PubMed]

M. L. Li, W. J. Guan, and P. C. Li, “Improved synthetic aperture focusing technique with applications in high-frequency ultrasound imaging,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 51(1), 63–70 (2004).
[CrossRef] [PubMed]

L. Öhberg and H. Alfredson, “Effects on neovascularisation behind the good results with eccentric training in chronic mid-portion Achilles tendinosis?” Knee Surg. Sports Traumatol. Arthrosc. 12(5), 465–470 (2004).
[CrossRef] [PubMed]

2003 (2)

A. G. Naccarato, P. Viacava, G. Bocci, G. Fanelli, P. Aretini, A. Lonobile, G. Montruccoli, and G. Bevilacqua, “Definition of the microvascular pattern of the normal human adult mammary gland,” J. Anat. 203(6), 599–603 (2003).
[CrossRef] [PubMed]

M. Zanetti, A. Metzdorf, H. P. Kundert, H. Zollinger, P. Vienne, B. Seifert, and J. Hodler, “Achilles tendons: clinical relevance of neovascularization diagnosed with power Doppler US,” Radiology 227(2), 556–560 (2003).
[CrossRef] [PubMed]

2002 (1)

S. A. Fenwick, B. L. Hazleman, and G. P. Riley, “The vasculature and its role in the damaged and healing tendon,” Arthritis Res. 4(4), 252–260 (2002).
[CrossRef] [PubMed]

2001 (2)

L. Öhberg, R. Lorentzon, and H. Alfredson, “Neovascularisation in Achilles tendons with painful tendinosis but not in normal tendons: an ultrasonographic investigation,” Knee Surg. Sports Traumatol. Arthrosc. 9(4), 233–238 (2001).
[CrossRef] [PubMed]

R. S. D. Campbell and A. J. Grainger, “Current concepts in imaging of tendinopathy,” Clin. Radiol. 56(4), 253–267 (2001).
[CrossRef] [PubMed]

2000 (1)

W. Grassi, E. Filippucci, A. Farina, and C. Cervini, “Sonographic imaging of tendons,” Arthritis Rheum. 43(5), 969–976 (2000).
[CrossRef] [PubMed]

Alfredson, H.

M. Kristoffersen, L. Öhberg, C. Johnston, and H. Alfredson, “Neovascularisation in chronic tendon injuries detected with colour Doppler ultrasound in horse and man: implications for research and treatment,” Knee Surg. Sports Traumatol. Arthrosc. 13(6), 505–508 (2005).
[CrossRef] [PubMed]

L. Öhberg and H. Alfredson, “Effects on neovascularisation behind the good results with eccentric training in chronic mid-portion Achilles tendinosis?” Knee Surg. Sports Traumatol. Arthrosc. 12(5), 465–470 (2004).
[CrossRef] [PubMed]

L. Öhberg, R. Lorentzon, and H. Alfredson, “Neovascularisation in Achilles tendons with painful tendinosis but not in normal tendons: an ultrasonographic investigation,” Knee Surg. Sports Traumatol. Arthrosc. 9(4), 233–238 (2001).
[CrossRef] [PubMed]

Aretini, P.

A. G. Naccarato, P. Viacava, G. Bocci, G. Fanelli, P. Aretini, A. Lonobile, G. Montruccoli, and G. Bevilacqua, “Definition of the microvascular pattern of the normal human adult mammary gland,” J. Anat. 203(6), 599–603 (2003).
[CrossRef] [PubMed]

Bevilacqua, G.

A. G. Naccarato, P. Viacava, G. Bocci, G. Fanelli, P. Aretini, A. Lonobile, G. Montruccoli, and G. Bevilacqua, “Definition of the microvascular pattern of the normal human adult mammary gland,” J. Anat. 203(6), 599–603 (2003).
[CrossRef] [PubMed]

Bocci, G.

A. G. Naccarato, P. Viacava, G. Bocci, G. Fanelli, P. Aretini, A. Lonobile, G. Montruccoli, and G. Bevilacqua, “Definition of the microvascular pattern of the normal human adult mammary gland,” J. Anat. 203(6), 599–603 (2003).
[CrossRef] [PubMed]

Boot-Handford, R. P.

K. A. Piróg, O. Jaka, Y. Katakura, R. S. Meadows, K. E. Kadler, R. P. Boot-Handford, and M. D. Briggs, “A mouse model offers novel insights into the myopathy and tendinopathy often associated with pseudoachondroplasia and multiple epiphyseal dysplasia,” Hum. Mol. Genet. 19(1), 52–64 (2010).
[CrossRef] [PubMed]

Briggs, M. D.

K. A. Piróg, O. Jaka, Y. Katakura, R. S. Meadows, K. E. Kadler, R. P. Boot-Handford, and M. D. Briggs, “A mouse model offers novel insights into the myopathy and tendinopathy often associated with pseudoachondroplasia and multiple epiphyseal dysplasia,” Hum. Mol. Genet. 19(1), 52–64 (2010).
[CrossRef] [PubMed]

Brunet, G.

W. van Snellenberg, J. P. Wiley, and G. Brunet, “Achilles tendon pain intensity and level of neovascularization in athletes as determined by color Doppler ultrasound,” Scand. J. Med. Sci. Sports 17(5), 530–534 (2007).
[PubMed]

Campbell, R. S. D.

R. S. D. Campbell and A. J. Grainger, “Current concepts in imaging of tendinopathy,” Clin. Radiol. 56(4), 253–267 (2001).
[CrossRef] [PubMed]

Cervini, C.

W. Grassi, E. Filippucci, A. Farina, and C. Cervini, “Sonographic imaging of tendons,” Arthritis Rheum. 43(5), 969–976 (2000).
[CrossRef] [PubMed]

Chamberland, D. L.

D. L. Chamberland, X. Wang, and B. J. Roessler, “Photoacoustic tomography of carrageenan-induced arthritis in a rat model,” J. Biomed. Opt. 13(1), 011005 (2008).
[CrossRef] [PubMed]

Chen, J. J.

C. K. Yeh, J. J. Chen, M. L. Li, J. J. Luh, and J. J. J. Chen, “In vivo imaging of blood flow in the mouse Achilles tendon using high-frequency ultrasound,” Ultrasonics 49(2), 226–230 (2009).
[CrossRef] [PubMed]

Chen, J. J. J.

C. K. Yeh, J. J. Chen, M. L. Li, J. J. Luh, and J. J. J. Chen, “In vivo imaging of blood flow in the mouse Achilles tendon using high-frequency ultrasound,” Ultrasonics 49(2), 226–230 (2009).
[CrossRef] [PubMed]

Chen, Y. J.

Y. J. Chen, C. J. Wang, K. D. Yang, Y. R. Kuo, H. C. Huang, Y. T. Huang, Y. C. Sun, and F. S. Wang, “Extracorporeal shock waves promote healing of collagenase-induced Achilles tendinitis and increase TGF-β1 and IGF-I expression,” J. Orthop. Res. 22(4), 854–861 (2004).
[CrossRef] [PubMed]

Fanelli, G.

A. G. Naccarato, P. Viacava, G. Bocci, G. Fanelli, P. Aretini, A. Lonobile, G. Montruccoli, and G. Bevilacqua, “Definition of the microvascular pattern of the normal human adult mammary gland,” J. Anat. 203(6), 599–603 (2003).
[CrossRef] [PubMed]

Farina, A.

W. Grassi, E. Filippucci, A. Farina, and C. Cervini, “Sonographic imaging of tendons,” Arthritis Rheum. 43(5), 969–976 (2000).
[CrossRef] [PubMed]

Fenwick, S. A.

S. A. Fenwick, B. L. Hazleman, and G. P. Riley, “The vasculature and its role in the damaged and healing tendon,” Arthritis Res. 4(4), 252–260 (2002).
[CrossRef] [PubMed]

Filippucci, E.

W. Grassi, E. Filippucci, A. Farina, and C. Cervini, “Sonographic imaging of tendons,” Arthritis Rheum. 43(5), 969–976 (2000).
[CrossRef] [PubMed]

Grainger, A. J.

R. S. D. Campbell and A. J. Grainger, “Current concepts in imaging of tendinopathy,” Clin. Radiol. 56(4), 253–267 (2001).
[CrossRef] [PubMed]

Grassi, W.

W. Grassi, E. Filippucci, A. Farina, and C. Cervini, “Sonographic imaging of tendons,” Arthritis Rheum. 43(5), 969–976 (2000).
[CrossRef] [PubMed]

Guan, W. J.

M. L. Li, W. J. Guan, and P. C. Li, “Improved synthetic aperture focusing technique with applications in high-frequency ultrasound imaging,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 51(1), 63–70 (2004).
[CrossRef] [PubMed]

Harris, C. A.

C. A. Harris and A. J. Peduto, “Achilles tendon imaging,” Australas. Radiol. 50(6), 513–525 (2006).
[CrossRef] [PubMed]

Harrison, T.

Y. Jiang, T. Harrison, J. Ranasinghesagara, and R. J. Zemp, “Photoacoustic and high-frequency power Doppler ultrasound biomicroscopy: a comparative study,” J. Biomed. Opt. 15(5), 056008 (2010).
[CrossRef] [PubMed]

Hazleman, B. L.

S. A. Fenwick, B. L. Hazleman, and G. P. Riley, “The vasculature and its role in the damaged and healing tendon,” Arthritis Res. 4(4), 252–260 (2002).
[CrossRef] [PubMed]

Hodler, J.

M. Zanetti, A. Metzdorf, H. P. Kundert, H. Zollinger, P. Vienne, B. Seifert, and J. Hodler, “Achilles tendons: clinical relevance of neovascularization diagnosed with power Doppler US,” Radiology 227(2), 556–560 (2003).
[CrossRef] [PubMed]

Huang, H. C.

Y. J. Chen, C. J. Wang, K. D. Yang, Y. R. Kuo, H. C. Huang, Y. T. Huang, Y. C. Sun, and F. S. Wang, “Extracorporeal shock waves promote healing of collagenase-induced Achilles tendinitis and increase TGF-β1 and IGF-I expression,” J. Orthop. Res. 22(4), 854–861 (2004).
[CrossRef] [PubMed]

Huang, Y. T.

Y. J. Chen, C. J. Wang, K. D. Yang, Y. R. Kuo, H. C. Huang, Y. T. Huang, Y. C. Sun, and F. S. Wang, “Extracorporeal shock waves promote healing of collagenase-induced Achilles tendinitis and increase TGF-β1 and IGF-I expression,” J. Orthop. Res. 22(4), 854–861 (2004).
[CrossRef] [PubMed]

Jaka, O.

K. A. Piróg, O. Jaka, Y. Katakura, R. S. Meadows, K. E. Kadler, R. P. Boot-Handford, and M. D. Briggs, “A mouse model offers novel insights into the myopathy and tendinopathy often associated with pseudoachondroplasia and multiple epiphyseal dysplasia,” Hum. Mol. Genet. 19(1), 52–64 (2010).
[CrossRef] [PubMed]

Jiang, Y.

Y. Jiang, T. Harrison, J. Ranasinghesagara, and R. J. Zemp, “Photoacoustic and high-frequency power Doppler ultrasound biomicroscopy: a comparative study,” J. Biomed. Opt. 15(5), 056008 (2010).
[CrossRef] [PubMed]

Johnston, C.

M. Kristoffersen, L. Öhberg, C. Johnston, and H. Alfredson, “Neovascularisation in chronic tendon injuries detected with colour Doppler ultrasound in horse and man: implications for research and treatment,” Knee Surg. Sports Traumatol. Arthrosc. 13(6), 505–508 (2005).
[CrossRef] [PubMed]

Kadler, K. E.

K. A. Piróg, O. Jaka, Y. Katakura, R. S. Meadows, K. E. Kadler, R. P. Boot-Handford, and M. D. Briggs, “A mouse model offers novel insights into the myopathy and tendinopathy often associated with pseudoachondroplasia and multiple epiphyseal dysplasia,” Hum. Mol. Genet. 19(1), 52–64 (2010).
[CrossRef] [PubMed]

Katakura, Y.

K. A. Piróg, O. Jaka, Y. Katakura, R. S. Meadows, K. E. Kadler, R. P. Boot-Handford, and M. D. Briggs, “A mouse model offers novel insights into the myopathy and tendinopathy often associated with pseudoachondroplasia and multiple epiphyseal dysplasia,” Hum. Mol. Genet. 19(1), 52–64 (2010).
[CrossRef] [PubMed]

Kristoffersen, M.

M. Kristoffersen, L. Öhberg, C. Johnston, and H. Alfredson, “Neovascularisation in chronic tendon injuries detected with colour Doppler ultrasound in horse and man: implications for research and treatment,” Knee Surg. Sports Traumatol. Arthrosc. 13(6), 505–508 (2005).
[CrossRef] [PubMed]

Kundert, H. P.

M. Zanetti, A. Metzdorf, H. P. Kundert, H. Zollinger, P. Vienne, B. Seifert, and J. Hodler, “Achilles tendons: clinical relevance of neovascularization diagnosed with power Doppler US,” Radiology 227(2), 556–560 (2003).
[CrossRef] [PubMed]

Kuo, Y. R.

Y. J. Chen, C. J. Wang, K. D. Yang, Y. R. Kuo, H. C. Huang, Y. T. Huang, Y. C. Sun, and F. S. Wang, “Extracorporeal shock waves promote healing of collagenase-induced Achilles tendinitis and increase TGF-β1 and IGF-I expression,” J. Orthop. Res. 22(4), 854–861 (2004).
[CrossRef] [PubMed]

Li, M. L.

C. K. Yeh, J. J. Chen, M. L. Li, J. J. Luh, and J. J. J. Chen, “In vivo imaging of blood flow in the mouse Achilles tendon using high-frequency ultrasound,” Ultrasonics 49(2), 226–230 (2009).
[CrossRef] [PubMed]

H. F. Zhang, K. Maslov, M. L. Li, G. Stoica, and L. V. Wang, “In vivo volumetric imaging of subcutaneous microvasculature by photoacoustic microscopy,” Opt. Express 14(20), 9317–9323 (2006).
[CrossRef] [PubMed]

M. L. Li, H. E. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Improved in vivo photoacoustic microscopy based on a virtual-detector concept,” Opt. Lett. 31(4), 474–476 (2006).
[CrossRef] [PubMed]

M. L. Li, W. J. Guan, and P. C. Li, “Improved synthetic aperture focusing technique with applications in high-frequency ultrasound imaging,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 51(1), 63–70 (2004).
[CrossRef] [PubMed]

Li, P. C.

M. L. Li, W. J. Guan, and P. C. Li, “Improved synthetic aperture focusing technique with applications in high-frequency ultrasound imaging,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 51(1), 63–70 (2004).
[CrossRef] [PubMed]

Lonobile, A.

A. G. Naccarato, P. Viacava, G. Bocci, G. Fanelli, P. Aretini, A. Lonobile, G. Montruccoli, and G. Bevilacqua, “Definition of the microvascular pattern of the normal human adult mammary gland,” J. Anat. 203(6), 599–603 (2003).
[CrossRef] [PubMed]

Lorentzon, R.

L. Öhberg, R. Lorentzon, and H. Alfredson, “Neovascularisation in Achilles tendons with painful tendinosis but not in normal tendons: an ultrasonographic investigation,” Knee Surg. Sports Traumatol. Arthrosc. 9(4), 233–238 (2001).
[CrossRef] [PubMed]

Luh, J. J.

C. K. Yeh, J. J. Chen, M. L. Li, J. J. Luh, and J. J. J. Chen, “In vivo imaging of blood flow in the mouse Achilles tendon using high-frequency ultrasound,” Ultrasonics 49(2), 226–230 (2009).
[CrossRef] [PubMed]

Luscombe, K. L.

N. Maffulli, P. Sharma, and K. L. Luscombe, “Achilles tendinopathy: aetiology and management,” J. R. Soc. Med. 97(10), 472–476 (2004).
[CrossRef] [PubMed]

Maffulli, N.

N. Maffulli, P. Sharma, and K. L. Luscombe, “Achilles tendinopathy: aetiology and management,” J. R. Soc. Med. 97(10), 472–476 (2004).
[CrossRef] [PubMed]

Maslov, K.

Meadows, R. S.

K. A. Piróg, O. Jaka, Y. Katakura, R. S. Meadows, K. E. Kadler, R. P. Boot-Handford, and M. D. Briggs, “A mouse model offers novel insights into the myopathy and tendinopathy often associated with pseudoachondroplasia and multiple epiphyseal dysplasia,” Hum. Mol. Genet. 19(1), 52–64 (2010).
[CrossRef] [PubMed]

Metzdorf, A.

M. Zanetti, A. Metzdorf, H. P. Kundert, H. Zollinger, P. Vienne, B. Seifert, and J. Hodler, “Achilles tendons: clinical relevance of neovascularization diagnosed with power Doppler US,” Radiology 227(2), 556–560 (2003).
[CrossRef] [PubMed]

Montruccoli, G.

A. G. Naccarato, P. Viacava, G. Bocci, G. Fanelli, P. Aretini, A. Lonobile, G. Montruccoli, and G. Bevilacqua, “Definition of the microvascular pattern of the normal human adult mammary gland,” J. Anat. 203(6), 599–603 (2003).
[CrossRef] [PubMed]

Naccarato, A. G.

A. G. Naccarato, P. Viacava, G. Bocci, G. Fanelli, P. Aretini, A. Lonobile, G. Montruccoli, and G. Bevilacqua, “Definition of the microvascular pattern of the normal human adult mammary gland,” J. Anat. 203(6), 599–603 (2003).
[CrossRef] [PubMed]

Öhberg, L.

M. Kristoffersen, L. Öhberg, C. Johnston, and H. Alfredson, “Neovascularisation in chronic tendon injuries detected with colour Doppler ultrasound in horse and man: implications for research and treatment,” Knee Surg. Sports Traumatol. Arthrosc. 13(6), 505–508 (2005).
[CrossRef] [PubMed]

L. Öhberg and H. Alfredson, “Effects on neovascularisation behind the good results with eccentric training in chronic mid-portion Achilles tendinosis?” Knee Surg. Sports Traumatol. Arthrosc. 12(5), 465–470 (2004).
[CrossRef] [PubMed]

L. Öhberg, R. Lorentzon, and H. Alfredson, “Neovascularisation in Achilles tendons with painful tendinosis but not in normal tendons: an ultrasonographic investigation,” Knee Surg. Sports Traumatol. Arthrosc. 9(4), 233–238 (2001).
[CrossRef] [PubMed]

Peduto, A. J.

C. A. Harris and A. J. Peduto, “Achilles tendon imaging,” Australas. Radiol. 50(6), 513–525 (2006).
[CrossRef] [PubMed]

Piróg, K. A.

K. A. Piróg, O. Jaka, Y. Katakura, R. S. Meadows, K. E. Kadler, R. P. Boot-Handford, and M. D. Briggs, “A mouse model offers novel insights into the myopathy and tendinopathy often associated with pseudoachondroplasia and multiple epiphyseal dysplasia,” Hum. Mol. Genet. 19(1), 52–64 (2010).
[CrossRef] [PubMed]

Ranasinghesagara, J.

Y. Jiang, T. Harrison, J. Ranasinghesagara, and R. J. Zemp, “Photoacoustic and high-frequency power Doppler ultrasound biomicroscopy: a comparative study,” J. Biomed. Opt. 15(5), 056008 (2010).
[CrossRef] [PubMed]

Riley, G. P.

S. A. Fenwick, B. L. Hazleman, and G. P. Riley, “The vasculature and its role in the damaged and healing tendon,” Arthritis Res. 4(4), 252–260 (2002).
[CrossRef] [PubMed]

Roessler, B. J.

D. L. Chamberland, X. Wang, and B. J. Roessler, “Photoacoustic tomography of carrageenan-induced arthritis in a rat model,” J. Biomed. Opt. 13(1), 011005 (2008).
[CrossRef] [PubMed]

Seifert, B.

M. Zanetti, A. Metzdorf, H. P. Kundert, H. Zollinger, P. Vienne, B. Seifert, and J. Hodler, “Achilles tendons: clinical relevance of neovascularization diagnosed with power Doppler US,” Radiology 227(2), 556–560 (2003).
[CrossRef] [PubMed]

Sharma, P.

N. Maffulli, P. Sharma, and K. L. Luscombe, “Achilles tendinopathy: aetiology and management,” J. R. Soc. Med. 97(10), 472–476 (2004).
[CrossRef] [PubMed]

Stoica, G.

Sun, Y. C.

Y. J. Chen, C. J. Wang, K. D. Yang, Y. R. Kuo, H. C. Huang, Y. T. Huang, Y. C. Sun, and F. S. Wang, “Extracorporeal shock waves promote healing of collagenase-induced Achilles tendinitis and increase TGF-β1 and IGF-I expression,” J. Orthop. Res. 22(4), 854–861 (2004).
[CrossRef] [PubMed]

van Snellenberg, W.

W. van Snellenberg, J. P. Wiley, and G. Brunet, “Achilles tendon pain intensity and level of neovascularization in athletes as determined by color Doppler ultrasound,” Scand. J. Med. Sci. Sports 17(5), 530–534 (2007).
[PubMed]

Viacava, P.

A. G. Naccarato, P. Viacava, G. Bocci, G. Fanelli, P. Aretini, A. Lonobile, G. Montruccoli, and G. Bevilacqua, “Definition of the microvascular pattern of the normal human adult mammary gland,” J. Anat. 203(6), 599–603 (2003).
[CrossRef] [PubMed]

Vienne, P.

M. Zanetti, A. Metzdorf, H. P. Kundert, H. Zollinger, P. Vienne, B. Seifert, and J. Hodler, “Achilles tendons: clinical relevance of neovascularization diagnosed with power Doppler US,” Radiology 227(2), 556–560 (2003).
[CrossRef] [PubMed]

Wang, C. J.

Y. J. Chen, C. J. Wang, K. D. Yang, Y. R. Kuo, H. C. Huang, Y. T. Huang, Y. C. Sun, and F. S. Wang, “Extracorporeal shock waves promote healing of collagenase-induced Achilles tendinitis and increase TGF-β1 and IGF-I expression,” J. Orthop. Res. 22(4), 854–861 (2004).
[CrossRef] [PubMed]

Wang, F. S.

Y. J. Chen, C. J. Wang, K. D. Yang, Y. R. Kuo, H. C. Huang, Y. T. Huang, Y. C. Sun, and F. S. Wang, “Extracorporeal shock waves promote healing of collagenase-induced Achilles tendinitis and increase TGF-β1 and IGF-I expression,” J. Orthop. Res. 22(4), 854–861 (2004).
[CrossRef] [PubMed]

Wang, L. V.

L. V. Wang, “Tutorial on Photoacoustic Microscopy and Computed Tomography,” IEEE J. Sel. Top. Quantum Electron. 14(1), 171–179 (2008).
[CrossRef]

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[CrossRef] [PubMed]

M. L. Li, H. E. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Improved in vivo photoacoustic microscopy based on a virtual-detector concept,” Opt. Lett. 31(4), 474–476 (2006).
[CrossRef] [PubMed]

H. F. Zhang, K. Maslov, M. L. Li, G. Stoica, and L. V. Wang, “In vivo volumetric imaging of subcutaneous microvasculature by photoacoustic microscopy,” Opt. Express 14(20), 9317–9323 (2006).
[CrossRef] [PubMed]

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
[CrossRef]

K. Maslov, G. Stoica, and L. V. Wang, “In vivo dark-field reflection-mode photoacoustic microscopy,” Opt. Lett. 30(6), 625–627 (2005).
[CrossRef] [PubMed]

Wang, X.

D. L. Chamberland, X. Wang, and B. J. Roessler, “Photoacoustic tomography of carrageenan-induced arthritis in a rat model,” J. Biomed. Opt. 13(1), 011005 (2008).
[CrossRef] [PubMed]

Warden, S. J.

S. J. Warden, “Animal models for the study of tendinopathy,” Br. J. Sports Med. 41(4), 232–240 (2007).
[CrossRef] [PubMed]

Wiley, J. P.

W. van Snellenberg, J. P. Wiley, and G. Brunet, “Achilles tendon pain intensity and level of neovascularization in athletes as determined by color Doppler ultrasound,” Scand. J. Med. Sci. Sports 17(5), 530–534 (2007).
[PubMed]

Xu, M.

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
[CrossRef]

Yang, K. D.

Y. J. Chen, C. J. Wang, K. D. Yang, Y. R. Kuo, H. C. Huang, Y. T. Huang, Y. C. Sun, and F. S. Wang, “Extracorporeal shock waves promote healing of collagenase-induced Achilles tendinitis and increase TGF-β1 and IGF-I expression,” J. Orthop. Res. 22(4), 854–861 (2004).
[CrossRef] [PubMed]

Yeh, C. K.

C. K. Yeh, J. J. Chen, M. L. Li, J. J. Luh, and J. J. J. Chen, “In vivo imaging of blood flow in the mouse Achilles tendon using high-frequency ultrasound,” Ultrasonics 49(2), 226–230 (2009).
[CrossRef] [PubMed]

Zanetti, M.

M. Zanetti, A. Metzdorf, H. P. Kundert, H. Zollinger, P. Vienne, B. Seifert, and J. Hodler, “Achilles tendons: clinical relevance of neovascularization diagnosed with power Doppler US,” Radiology 227(2), 556–560 (2003).
[CrossRef] [PubMed]

Zemp, R. J.

Y. Jiang, T. Harrison, J. Ranasinghesagara, and R. J. Zemp, “Photoacoustic and high-frequency power Doppler ultrasound biomicroscopy: a comparative study,” J. Biomed. Opt. 15(5), 056008 (2010).
[CrossRef] [PubMed]

Zhang, H. E.

Zhang, H. F.

H. F. Zhang, K. Maslov, M. L. Li, G. Stoica, and L. V. Wang, “In vivo volumetric imaging of subcutaneous microvasculature by photoacoustic microscopy,” Opt. Express 14(20), 9317–9323 (2006).
[CrossRef] [PubMed]

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[CrossRef] [PubMed]

Zollinger, H.

M. Zanetti, A. Metzdorf, H. P. Kundert, H. Zollinger, P. Vienne, B. Seifert, and J. Hodler, “Achilles tendons: clinical relevance of neovascularization diagnosed with power Doppler US,” Radiology 227(2), 556–560 (2003).
[CrossRef] [PubMed]

Arthritis Res. (1)

S. A. Fenwick, B. L. Hazleman, and G. P. Riley, “The vasculature and its role in the damaged and healing tendon,” Arthritis Res. 4(4), 252–260 (2002).
[CrossRef] [PubMed]

Arthritis Rheum. (1)

W. Grassi, E. Filippucci, A. Farina, and C. Cervini, “Sonographic imaging of tendons,” Arthritis Rheum. 43(5), 969–976 (2000).
[CrossRef] [PubMed]

Australas. Radiol. (1)

C. A. Harris and A. J. Peduto, “Achilles tendon imaging,” Australas. Radiol. 50(6), 513–525 (2006).
[CrossRef] [PubMed]

Br. J. Sports Med. (1)

S. J. Warden, “Animal models for the study of tendinopathy,” Br. J. Sports Med. 41(4), 232–240 (2007).
[CrossRef] [PubMed]

Clin. Radiol. (1)

R. S. D. Campbell and A. J. Grainger, “Current concepts in imaging of tendinopathy,” Clin. Radiol. 56(4), 253–267 (2001).
[CrossRef] [PubMed]

Hum. Mol. Genet. (1)

K. A. Piróg, O. Jaka, Y. Katakura, R. S. Meadows, K. E. Kadler, R. P. Boot-Handford, and M. D. Briggs, “A mouse model offers novel insights into the myopathy and tendinopathy often associated with pseudoachondroplasia and multiple epiphyseal dysplasia,” Hum. Mol. Genet. 19(1), 52–64 (2010).
[CrossRef] [PubMed]

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

L. V. Wang, “Tutorial on Photoacoustic Microscopy and Computed Tomography,” IEEE J. Sel. Top. Quantum Electron. 14(1), 171–179 (2008).
[CrossRef]

IEEE Trans. Ultrason. Ferroelectr. Freq. Control (1)

M. L. Li, W. J. Guan, and P. C. Li, “Improved synthetic aperture focusing technique with applications in high-frequency ultrasound imaging,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 51(1), 63–70 (2004).
[CrossRef] [PubMed]

J. Anat. (1)

A. G. Naccarato, P. Viacava, G. Bocci, G. Fanelli, P. Aretini, A. Lonobile, G. Montruccoli, and G. Bevilacqua, “Definition of the microvascular pattern of the normal human adult mammary gland,” J. Anat. 203(6), 599–603 (2003).
[CrossRef] [PubMed]

J. Biomed. Opt. (2)

Y. Jiang, T. Harrison, J. Ranasinghesagara, and R. J. Zemp, “Photoacoustic and high-frequency power Doppler ultrasound biomicroscopy: a comparative study,” J. Biomed. Opt. 15(5), 056008 (2010).
[CrossRef] [PubMed]

D. L. Chamberland, X. Wang, and B. J. Roessler, “Photoacoustic tomography of carrageenan-induced arthritis in a rat model,” J. Biomed. Opt. 13(1), 011005 (2008).
[CrossRef] [PubMed]

J. Orthop. Res. (1)

Y. J. Chen, C. J. Wang, K. D. Yang, Y. R. Kuo, H. C. Huang, Y. T. Huang, Y. C. Sun, and F. S. Wang, “Extracorporeal shock waves promote healing of collagenase-induced Achilles tendinitis and increase TGF-β1 and IGF-I expression,” J. Orthop. Res. 22(4), 854–861 (2004).
[CrossRef] [PubMed]

J. R. Soc. Med. (1)

N. Maffulli, P. Sharma, and K. L. Luscombe, “Achilles tendinopathy: aetiology and management,” J. R. Soc. Med. 97(10), 472–476 (2004).
[CrossRef] [PubMed]

Knee Surg. Sports Traumatol. Arthrosc. (3)

L. Öhberg and H. Alfredson, “Effects on neovascularisation behind the good results with eccentric training in chronic mid-portion Achilles tendinosis?” Knee Surg. Sports Traumatol. Arthrosc. 12(5), 465–470 (2004).
[CrossRef] [PubMed]

L. Öhberg, R. Lorentzon, and H. Alfredson, “Neovascularisation in Achilles tendons with painful tendinosis but not in normal tendons: an ultrasonographic investigation,” Knee Surg. Sports Traumatol. Arthrosc. 9(4), 233–238 (2001).
[CrossRef] [PubMed]

M. Kristoffersen, L. Öhberg, C. Johnston, and H. Alfredson, “Neovascularisation in chronic tendon injuries detected with colour Doppler ultrasound in horse and man: implications for research and treatment,” Knee Surg. Sports Traumatol. Arthrosc. 13(6), 505–508 (2005).
[CrossRef] [PubMed]

Nat. Biotechnol. (1)

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[CrossRef] [PubMed]

Opt. Express (1)

Opt. Lett. (2)

Radiology (1)

M. Zanetti, A. Metzdorf, H. P. Kundert, H. Zollinger, P. Vienne, B. Seifert, and J. Hodler, “Achilles tendons: clinical relevance of neovascularization diagnosed with power Doppler US,” Radiology 227(2), 556–560 (2003).
[CrossRef] [PubMed]

Rev. Sci. Instrum. (1)

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
[CrossRef]

Scand. J. Med. Sci. Sports (1)

W. van Snellenberg, J. P. Wiley, and G. Brunet, “Achilles tendon pain intensity and level of neovascularization in athletes as determined by color Doppler ultrasound,” Scand. J. Med. Sci. Sports 17(5), 530–534 (2007).
[PubMed]

Ultrasonics (1)

C. K. Yeh, J. J. Chen, M. L. Li, J. J. Luh, and J. J. J. Chen, “In vivo imaging of blood flow in the mouse Achilles tendon using high-frequency ultrasound,” Ultrasonics 49(2), 226–230 (2009).
[CrossRef] [PubMed]

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Figures (4)

Fig. 1
Fig. 1

(A) System block diagram. (B) Illustration of longitudinal view where the scanning along the longitudinal direction of the Achilles tendon is performed. (C) Photograph of mouse Achilles tendon being imaged with a scanning region of 6 mm by 2mm.

Fig. 2
Fig. 2

Images of the Achilles tendons acquired on the 12th day after the injection of saline and collagenase. Left panels are images of the controlled Achilles tendon and right panels are images of the injured Achilles tendon. (A) and (B): ultrasound images; (C) and (D): photoacoustic images; (E) and (F): combined photoaoucstic and ultrasound images where pseudo-color represents photoacoustic signals. The ultrasound images are displayed in a 40-dB dynamic range, and the photoaocustic images are shown in a linear scale. The terms C, D, M, and AT in (A) represent calcaneus, dermis, muscle, and Achilles tendon, respectively. The terms SV and TV in (E) represent subcutaneous vessels and tendon vessels respectively.

Fig. 3
Fig. 3

Images of the Achilles tendons acquired on the 23rd day post injection. Left panels are images of the controlled tendon and right panels are images of the injured tendon. (A) and (B): ultrasound images; (C) and (D): photoacoustic images; (E) and (F): combined photoacoustic and ultrasound images; (G) and (H): H&E stained histological sections. The terms C, AT, and V in (G and (H) represent calcaneus, Achilles tendon, vessels around the tendon, respectively.

Fig. 4
Fig. 4

Vascular area ratio of the controlled and injured Achilles tendons before the injection of saline and collagenase and on the 12th and 23rd days post injection.

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