Abstract

Neovascularity also known as angiogenesis is an early feature of inflammatory arthritis disease. Therefore, identifying the development of neovascularity is one way to potentially detect and characterize arthritis. Laser-based photoacoustic imaging (PAI) is an emerging biomedical imaging modality which may aid in the detection of both early and continued development of neovascularity. In this work, we investigated the feasibility of PAI to measure angiogenesis, for the purpose of evaluating and monitoring inflammatory arthritis and responses to treatment. The imaging results on an arthritis rat model demonstrate that 1) there is noticeable enhancement in image intensities in the arthritic ankle joints when compared to the normal joints, and 2) there is noticeable decrease in image intensities in the arthritic ankle joints after treatment when compared to the untreated arthritic joints. In order to validate the findings from PAI, we performed positron emission tomography (PET) and histology on the same joints. The diameters of the ankle joints, as a clinical score of the arthritis, were also measured at each time point.

© 2013 OSA

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  1. Centers for Disease Control and Prevention (CDC), “Racial/ethnic differences in the prevalence and impact of doctor-diagnosed arthritis—United States, 2002,” MMWR Morb. Mortal. Wkly. Rep.54(5), 119–123 (2005).
    [PubMed]
  2. O. Fitzgerald and B. Bresnihan, “Synovial vascularity is increased in rheumatoid arthritis: comment on the article by Stevens et al,” Arthritis Rheum.35(12), 1540–1541 (1992).
    [CrossRef] [PubMed]
  3. A. E. Koch, “Review: angiogenesis: implications for rheumatoid arthritis,” Arthritis Rheum.41(6), 951–962 (1998).
    [CrossRef] [PubMed]
  4. A. J. Hayes, “Angioneogenesis in rheumatoid arthritis,” Lancet354(9176), 423–424 (1999).
    [CrossRef] [PubMed]
  5. E. M. Paleolog and J. M. Miotla, “Angiogenesis in arthritis: role in disease pathogenesis and as a potential therapeutic target,” Angiogenesis2(4), 295–307 (1998).
    [CrossRef] [PubMed]
  6. D. A. Walsh, “Angiogenesis and arthritis,” Rheumatology (Oxford)38(2), 103–112 (1999).
    [CrossRef] [PubMed]
  7. A. E. Koch, “Angiogenesis as a target in rheumatoid arthritis,” Ann. Rheum. Dis.62(90002Suppl 2), ii60–ii67 (2003).
    [CrossRef] [PubMed]
  8. P. H. Wooley, “Animal models of rheumatoid arthritis,” Curr. Opin. Rheumatol.3(3), 407–420 (1991).
    [CrossRef] [PubMed]
  9. M. M. Halloran, J. M. Woods, R. M. Strieter, Z. Szekanecz, M. V. Volin, S. Hosaka, G. K. Haines, S. L. Kunkel, M. D. Burdick, A. Walz, and A. E. Koch, “The role of an epithelial neutrophil-activating peptide-78-like protein in rat adjuvant-induced arthritis,” J. Immunol.162(12), 7492–7500 (1999).
    [PubMed]
  10. S. Shahrara, A. E. I. Proudfoot, J. M. Woods, J. H. Ruth, M. A. Amin, C. C. Park, C. S. Haas, R. M. Pope, G. K. Haines, Y. Y. Zha, and A. E. Koch, “Amelioration of rat adjuvant-induced arthritis by Met-RANTES,” Arthritis Rheum.52(6), 1907–1919 (2005).
    [CrossRef] [PubMed]
  11. M. M. Halloran, Z. Szekanecz, N. Barquin, G. K. Haines, and A. E. Koch, “Cellular adhesion molecules in rat adjuvant arthritis,” Arthritis Rheum.39(5), 810–819 (1996).
    [CrossRef] [PubMed]
  12. J. D. Taurog, D. C. Argentieri, and R. A. McReynolds, “Adjuvant arthritis,” Methods Enzymol.162, 339–355 (1988).
    [CrossRef] [PubMed]
  13. D. A. Barnes, J. Tse, M. Kaufhold, M. Owen, J. Hesselgesser, R. Strieter, R. Horuk, and H. D. Perez, “Polyclonal antibody directed against human RANTES ameliorates disease in the Lewis rat adjuvant-induced arthritis model,” J. Clin. Invest.101(12), 2910–2919 (1998).
    [CrossRef] [PubMed]
  14. X. Wang, J. B. Fowlkes, J. M. Cannata, C. Hu, and P. L. Carson, “Photoacoustic imaging with a commercial ultrasound system and a custom probe,” Ultrasound Med. Biol.37(3), 484–492 (2011).
    [CrossRef] [PubMed]
  15. M. K. Chen and T. R. Guilarte, “Translocator protein 18 kDa (TSPO): molecular sensor of brain injury and repair,” Pharmacol. Ther.118(1), 1–17 (2008).
    [CrossRef] [PubMed]
  16. V. Papadopoulos and L. Lecanu, “Translocator protein (18 kDa) TSPO: an emerging therapeutic target in neurotrauma,” Exp. Neurol.219(1), 53–57 (2009).
    [CrossRef] [PubMed]

2011 (1)

X. Wang, J. B. Fowlkes, J. M. Cannata, C. Hu, and P. L. Carson, “Photoacoustic imaging with a commercial ultrasound system and a custom probe,” Ultrasound Med. Biol.37(3), 484–492 (2011).
[CrossRef] [PubMed]

2009 (1)

V. Papadopoulos and L. Lecanu, “Translocator protein (18 kDa) TSPO: an emerging therapeutic target in neurotrauma,” Exp. Neurol.219(1), 53–57 (2009).
[CrossRef] [PubMed]

2008 (1)

M. K. Chen and T. R. Guilarte, “Translocator protein 18 kDa (TSPO): molecular sensor of brain injury and repair,” Pharmacol. Ther.118(1), 1–17 (2008).
[CrossRef] [PubMed]

2005 (2)

S. Shahrara, A. E. I. Proudfoot, J. M. Woods, J. H. Ruth, M. A. Amin, C. C. Park, C. S. Haas, R. M. Pope, G. K. Haines, Y. Y. Zha, and A. E. Koch, “Amelioration of rat adjuvant-induced arthritis by Met-RANTES,” Arthritis Rheum.52(6), 1907–1919 (2005).
[CrossRef] [PubMed]

Centers for Disease Control and Prevention (CDC), “Racial/ethnic differences in the prevalence and impact of doctor-diagnosed arthritis—United States, 2002,” MMWR Morb. Mortal. Wkly. Rep.54(5), 119–123 (2005).
[PubMed]

2003 (1)

A. E. Koch, “Angiogenesis as a target in rheumatoid arthritis,” Ann. Rheum. Dis.62(90002Suppl 2), ii60–ii67 (2003).
[CrossRef] [PubMed]

1999 (3)

D. A. Walsh, “Angiogenesis and arthritis,” Rheumatology (Oxford)38(2), 103–112 (1999).
[CrossRef] [PubMed]

A. J. Hayes, “Angioneogenesis in rheumatoid arthritis,” Lancet354(9176), 423–424 (1999).
[CrossRef] [PubMed]

M. M. Halloran, J. M. Woods, R. M. Strieter, Z. Szekanecz, M. V. Volin, S. Hosaka, G. K. Haines, S. L. Kunkel, M. D. Burdick, A. Walz, and A. E. Koch, “The role of an epithelial neutrophil-activating peptide-78-like protein in rat adjuvant-induced arthritis,” J. Immunol.162(12), 7492–7500 (1999).
[PubMed]

1998 (3)

D. A. Barnes, J. Tse, M. Kaufhold, M. Owen, J. Hesselgesser, R. Strieter, R. Horuk, and H. D. Perez, “Polyclonal antibody directed against human RANTES ameliorates disease in the Lewis rat adjuvant-induced arthritis model,” J. Clin. Invest.101(12), 2910–2919 (1998).
[CrossRef] [PubMed]

E. M. Paleolog and J. M. Miotla, “Angiogenesis in arthritis: role in disease pathogenesis and as a potential therapeutic target,” Angiogenesis2(4), 295–307 (1998).
[CrossRef] [PubMed]

A. E. Koch, “Review: angiogenesis: implications for rheumatoid arthritis,” Arthritis Rheum.41(6), 951–962 (1998).
[CrossRef] [PubMed]

1996 (1)

M. M. Halloran, Z. Szekanecz, N. Barquin, G. K. Haines, and A. E. Koch, “Cellular adhesion molecules in rat adjuvant arthritis,” Arthritis Rheum.39(5), 810–819 (1996).
[CrossRef] [PubMed]

1992 (1)

O. Fitzgerald and B. Bresnihan, “Synovial vascularity is increased in rheumatoid arthritis: comment on the article by Stevens et al,” Arthritis Rheum.35(12), 1540–1541 (1992).
[CrossRef] [PubMed]

1991 (1)

P. H. Wooley, “Animal models of rheumatoid arthritis,” Curr. Opin. Rheumatol.3(3), 407–420 (1991).
[CrossRef] [PubMed]

1988 (1)

J. D. Taurog, D. C. Argentieri, and R. A. McReynolds, “Adjuvant arthritis,” Methods Enzymol.162, 339–355 (1988).
[CrossRef] [PubMed]

Amin, M. A.

S. Shahrara, A. E. I. Proudfoot, J. M. Woods, J. H. Ruth, M. A. Amin, C. C. Park, C. S. Haas, R. M. Pope, G. K. Haines, Y. Y. Zha, and A. E. Koch, “Amelioration of rat adjuvant-induced arthritis by Met-RANTES,” Arthritis Rheum.52(6), 1907–1919 (2005).
[CrossRef] [PubMed]

Argentieri, D. C.

J. D. Taurog, D. C. Argentieri, and R. A. McReynolds, “Adjuvant arthritis,” Methods Enzymol.162, 339–355 (1988).
[CrossRef] [PubMed]

Barnes, D. A.

D. A. Barnes, J. Tse, M. Kaufhold, M. Owen, J. Hesselgesser, R. Strieter, R. Horuk, and H. D. Perez, “Polyclonal antibody directed against human RANTES ameliorates disease in the Lewis rat adjuvant-induced arthritis model,” J. Clin. Invest.101(12), 2910–2919 (1998).
[CrossRef] [PubMed]

Barquin, N.

M. M. Halloran, Z. Szekanecz, N. Barquin, G. K. Haines, and A. E. Koch, “Cellular adhesion molecules in rat adjuvant arthritis,” Arthritis Rheum.39(5), 810–819 (1996).
[CrossRef] [PubMed]

Bresnihan, B.

O. Fitzgerald and B. Bresnihan, “Synovial vascularity is increased in rheumatoid arthritis: comment on the article by Stevens et al,” Arthritis Rheum.35(12), 1540–1541 (1992).
[CrossRef] [PubMed]

Burdick, M. D.

M. M. Halloran, J. M. Woods, R. M. Strieter, Z. Szekanecz, M. V. Volin, S. Hosaka, G. K. Haines, S. L. Kunkel, M. D. Burdick, A. Walz, and A. E. Koch, “The role of an epithelial neutrophil-activating peptide-78-like protein in rat adjuvant-induced arthritis,” J. Immunol.162(12), 7492–7500 (1999).
[PubMed]

Cannata, J. M.

X. Wang, J. B. Fowlkes, J. M. Cannata, C. Hu, and P. L. Carson, “Photoacoustic imaging with a commercial ultrasound system and a custom probe,” Ultrasound Med. Biol.37(3), 484–492 (2011).
[CrossRef] [PubMed]

Carson, P. L.

X. Wang, J. B. Fowlkes, J. M. Cannata, C. Hu, and P. L. Carson, “Photoacoustic imaging with a commercial ultrasound system and a custom probe,” Ultrasound Med. Biol.37(3), 484–492 (2011).
[CrossRef] [PubMed]

Chen, M. K.

M. K. Chen and T. R. Guilarte, “Translocator protein 18 kDa (TSPO): molecular sensor of brain injury and repair,” Pharmacol. Ther.118(1), 1–17 (2008).
[CrossRef] [PubMed]

Fitzgerald, O.

O. Fitzgerald and B. Bresnihan, “Synovial vascularity is increased in rheumatoid arthritis: comment on the article by Stevens et al,” Arthritis Rheum.35(12), 1540–1541 (1992).
[CrossRef] [PubMed]

Fowlkes, J. B.

X. Wang, J. B. Fowlkes, J. M. Cannata, C. Hu, and P. L. Carson, “Photoacoustic imaging with a commercial ultrasound system and a custom probe,” Ultrasound Med. Biol.37(3), 484–492 (2011).
[CrossRef] [PubMed]

Guilarte, T. R.

M. K. Chen and T. R. Guilarte, “Translocator protein 18 kDa (TSPO): molecular sensor of brain injury and repair,” Pharmacol. Ther.118(1), 1–17 (2008).
[CrossRef] [PubMed]

Haas, C. S.

S. Shahrara, A. E. I. Proudfoot, J. M. Woods, J. H. Ruth, M. A. Amin, C. C. Park, C. S. Haas, R. M. Pope, G. K. Haines, Y. Y. Zha, and A. E. Koch, “Amelioration of rat adjuvant-induced arthritis by Met-RANTES,” Arthritis Rheum.52(6), 1907–1919 (2005).
[CrossRef] [PubMed]

Haines, G. K.

S. Shahrara, A. E. I. Proudfoot, J. M. Woods, J. H. Ruth, M. A. Amin, C. C. Park, C. S. Haas, R. M. Pope, G. K. Haines, Y. Y. Zha, and A. E. Koch, “Amelioration of rat adjuvant-induced arthritis by Met-RANTES,” Arthritis Rheum.52(6), 1907–1919 (2005).
[CrossRef] [PubMed]

M. M. Halloran, J. M. Woods, R. M. Strieter, Z. Szekanecz, M. V. Volin, S. Hosaka, G. K. Haines, S. L. Kunkel, M. D. Burdick, A. Walz, and A. E. Koch, “The role of an epithelial neutrophil-activating peptide-78-like protein in rat adjuvant-induced arthritis,” J. Immunol.162(12), 7492–7500 (1999).
[PubMed]

M. M. Halloran, Z. Szekanecz, N. Barquin, G. K. Haines, and A. E. Koch, “Cellular adhesion molecules in rat adjuvant arthritis,” Arthritis Rheum.39(5), 810–819 (1996).
[CrossRef] [PubMed]

Halloran, M. M.

M. M. Halloran, J. M. Woods, R. M. Strieter, Z. Szekanecz, M. V. Volin, S. Hosaka, G. K. Haines, S. L. Kunkel, M. D. Burdick, A. Walz, and A. E. Koch, “The role of an epithelial neutrophil-activating peptide-78-like protein in rat adjuvant-induced arthritis,” J. Immunol.162(12), 7492–7500 (1999).
[PubMed]

M. M. Halloran, Z. Szekanecz, N. Barquin, G. K. Haines, and A. E. Koch, “Cellular adhesion molecules in rat adjuvant arthritis,” Arthritis Rheum.39(5), 810–819 (1996).
[CrossRef] [PubMed]

Hayes, A. J.

A. J. Hayes, “Angioneogenesis in rheumatoid arthritis,” Lancet354(9176), 423–424 (1999).
[CrossRef] [PubMed]

Hesselgesser, J.

D. A. Barnes, J. Tse, M. Kaufhold, M. Owen, J. Hesselgesser, R. Strieter, R. Horuk, and H. D. Perez, “Polyclonal antibody directed against human RANTES ameliorates disease in the Lewis rat adjuvant-induced arthritis model,” J. Clin. Invest.101(12), 2910–2919 (1998).
[CrossRef] [PubMed]

Horuk, R.

D. A. Barnes, J. Tse, M. Kaufhold, M. Owen, J. Hesselgesser, R. Strieter, R. Horuk, and H. D. Perez, “Polyclonal antibody directed against human RANTES ameliorates disease in the Lewis rat adjuvant-induced arthritis model,” J. Clin. Invest.101(12), 2910–2919 (1998).
[CrossRef] [PubMed]

Hosaka, S.

M. M. Halloran, J. M. Woods, R. M. Strieter, Z. Szekanecz, M. V. Volin, S. Hosaka, G. K. Haines, S. L. Kunkel, M. D. Burdick, A. Walz, and A. E. Koch, “The role of an epithelial neutrophil-activating peptide-78-like protein in rat adjuvant-induced arthritis,” J. Immunol.162(12), 7492–7500 (1999).
[PubMed]

Hu, C.

X. Wang, J. B. Fowlkes, J. M. Cannata, C. Hu, and P. L. Carson, “Photoacoustic imaging with a commercial ultrasound system and a custom probe,” Ultrasound Med. Biol.37(3), 484–492 (2011).
[CrossRef] [PubMed]

Kaufhold, M.

D. A. Barnes, J. Tse, M. Kaufhold, M. Owen, J. Hesselgesser, R. Strieter, R. Horuk, and H. D. Perez, “Polyclonal antibody directed against human RANTES ameliorates disease in the Lewis rat adjuvant-induced arthritis model,” J. Clin. Invest.101(12), 2910–2919 (1998).
[CrossRef] [PubMed]

Koch, A. E.

S. Shahrara, A. E. I. Proudfoot, J. M. Woods, J. H. Ruth, M. A. Amin, C. C. Park, C. S. Haas, R. M. Pope, G. K. Haines, Y. Y. Zha, and A. E. Koch, “Amelioration of rat adjuvant-induced arthritis by Met-RANTES,” Arthritis Rheum.52(6), 1907–1919 (2005).
[CrossRef] [PubMed]

A. E. Koch, “Angiogenesis as a target in rheumatoid arthritis,” Ann. Rheum. Dis.62(90002Suppl 2), ii60–ii67 (2003).
[CrossRef] [PubMed]

M. M. Halloran, J. M. Woods, R. M. Strieter, Z. Szekanecz, M. V. Volin, S. Hosaka, G. K. Haines, S. L. Kunkel, M. D. Burdick, A. Walz, and A. E. Koch, “The role of an epithelial neutrophil-activating peptide-78-like protein in rat adjuvant-induced arthritis,” J. Immunol.162(12), 7492–7500 (1999).
[PubMed]

A. E. Koch, “Review: angiogenesis: implications for rheumatoid arthritis,” Arthritis Rheum.41(6), 951–962 (1998).
[CrossRef] [PubMed]

M. M. Halloran, Z. Szekanecz, N. Barquin, G. K. Haines, and A. E. Koch, “Cellular adhesion molecules in rat adjuvant arthritis,” Arthritis Rheum.39(5), 810–819 (1996).
[CrossRef] [PubMed]

Kunkel, S. L.

M. M. Halloran, J. M. Woods, R. M. Strieter, Z. Szekanecz, M. V. Volin, S. Hosaka, G. K. Haines, S. L. Kunkel, M. D. Burdick, A. Walz, and A. E. Koch, “The role of an epithelial neutrophil-activating peptide-78-like protein in rat adjuvant-induced arthritis,” J. Immunol.162(12), 7492–7500 (1999).
[PubMed]

Lecanu, L.

V. Papadopoulos and L. Lecanu, “Translocator protein (18 kDa) TSPO: an emerging therapeutic target in neurotrauma,” Exp. Neurol.219(1), 53–57 (2009).
[CrossRef] [PubMed]

McReynolds, R. A.

J. D. Taurog, D. C. Argentieri, and R. A. McReynolds, “Adjuvant arthritis,” Methods Enzymol.162, 339–355 (1988).
[CrossRef] [PubMed]

Miotla, J. M.

E. M. Paleolog and J. M. Miotla, “Angiogenesis in arthritis: role in disease pathogenesis and as a potential therapeutic target,” Angiogenesis2(4), 295–307 (1998).
[CrossRef] [PubMed]

Owen, M.

D. A. Barnes, J. Tse, M. Kaufhold, M. Owen, J. Hesselgesser, R. Strieter, R. Horuk, and H. D. Perez, “Polyclonal antibody directed against human RANTES ameliorates disease in the Lewis rat adjuvant-induced arthritis model,” J. Clin. Invest.101(12), 2910–2919 (1998).
[CrossRef] [PubMed]

Paleolog, E. M.

E. M. Paleolog and J. M. Miotla, “Angiogenesis in arthritis: role in disease pathogenesis and as a potential therapeutic target,” Angiogenesis2(4), 295–307 (1998).
[CrossRef] [PubMed]

Papadopoulos, V.

V. Papadopoulos and L. Lecanu, “Translocator protein (18 kDa) TSPO: an emerging therapeutic target in neurotrauma,” Exp. Neurol.219(1), 53–57 (2009).
[CrossRef] [PubMed]

Park, C. C.

S. Shahrara, A. E. I. Proudfoot, J. M. Woods, J. H. Ruth, M. A. Amin, C. C. Park, C. S. Haas, R. M. Pope, G. K. Haines, Y. Y. Zha, and A. E. Koch, “Amelioration of rat adjuvant-induced arthritis by Met-RANTES,” Arthritis Rheum.52(6), 1907–1919 (2005).
[CrossRef] [PubMed]

Perez, H. D.

D. A. Barnes, J. Tse, M. Kaufhold, M. Owen, J. Hesselgesser, R. Strieter, R. Horuk, and H. D. Perez, “Polyclonal antibody directed against human RANTES ameliorates disease in the Lewis rat adjuvant-induced arthritis model,” J. Clin. Invest.101(12), 2910–2919 (1998).
[CrossRef] [PubMed]

Pope, R. M.

S. Shahrara, A. E. I. Proudfoot, J. M. Woods, J. H. Ruth, M. A. Amin, C. C. Park, C. S. Haas, R. M. Pope, G. K. Haines, Y. Y. Zha, and A. E. Koch, “Amelioration of rat adjuvant-induced arthritis by Met-RANTES,” Arthritis Rheum.52(6), 1907–1919 (2005).
[CrossRef] [PubMed]

Proudfoot, A. E. I.

S. Shahrara, A. E. I. Proudfoot, J. M. Woods, J. H. Ruth, M. A. Amin, C. C. Park, C. S. Haas, R. M. Pope, G. K. Haines, Y. Y. Zha, and A. E. Koch, “Amelioration of rat adjuvant-induced arthritis by Met-RANTES,” Arthritis Rheum.52(6), 1907–1919 (2005).
[CrossRef] [PubMed]

Ruth, J. H.

S. Shahrara, A. E. I. Proudfoot, J. M. Woods, J. H. Ruth, M. A. Amin, C. C. Park, C. S. Haas, R. M. Pope, G. K. Haines, Y. Y. Zha, and A. E. Koch, “Amelioration of rat adjuvant-induced arthritis by Met-RANTES,” Arthritis Rheum.52(6), 1907–1919 (2005).
[CrossRef] [PubMed]

Shahrara, S.

S. Shahrara, A. E. I. Proudfoot, J. M. Woods, J. H. Ruth, M. A. Amin, C. C. Park, C. S. Haas, R. M. Pope, G. K. Haines, Y. Y. Zha, and A. E. Koch, “Amelioration of rat adjuvant-induced arthritis by Met-RANTES,” Arthritis Rheum.52(6), 1907–1919 (2005).
[CrossRef] [PubMed]

Strieter, R.

D. A. Barnes, J. Tse, M. Kaufhold, M. Owen, J. Hesselgesser, R. Strieter, R. Horuk, and H. D. Perez, “Polyclonal antibody directed against human RANTES ameliorates disease in the Lewis rat adjuvant-induced arthritis model,” J. Clin. Invest.101(12), 2910–2919 (1998).
[CrossRef] [PubMed]

Strieter, R. M.

M. M. Halloran, J. M. Woods, R. M. Strieter, Z. Szekanecz, M. V. Volin, S. Hosaka, G. K. Haines, S. L. Kunkel, M. D. Burdick, A. Walz, and A. E. Koch, “The role of an epithelial neutrophil-activating peptide-78-like protein in rat adjuvant-induced arthritis,” J. Immunol.162(12), 7492–7500 (1999).
[PubMed]

Szekanecz, Z.

M. M. Halloran, J. M. Woods, R. M. Strieter, Z. Szekanecz, M. V. Volin, S. Hosaka, G. K. Haines, S. L. Kunkel, M. D. Burdick, A. Walz, and A. E. Koch, “The role of an epithelial neutrophil-activating peptide-78-like protein in rat adjuvant-induced arthritis,” J. Immunol.162(12), 7492–7500 (1999).
[PubMed]

M. M. Halloran, Z. Szekanecz, N. Barquin, G. K. Haines, and A. E. Koch, “Cellular adhesion molecules in rat adjuvant arthritis,” Arthritis Rheum.39(5), 810–819 (1996).
[CrossRef] [PubMed]

Taurog, J. D.

J. D. Taurog, D. C. Argentieri, and R. A. McReynolds, “Adjuvant arthritis,” Methods Enzymol.162, 339–355 (1988).
[CrossRef] [PubMed]

Tse, J.

D. A. Barnes, J. Tse, M. Kaufhold, M. Owen, J. Hesselgesser, R. Strieter, R. Horuk, and H. D. Perez, “Polyclonal antibody directed against human RANTES ameliorates disease in the Lewis rat adjuvant-induced arthritis model,” J. Clin. Invest.101(12), 2910–2919 (1998).
[CrossRef] [PubMed]

Volin, M. V.

M. M. Halloran, J. M. Woods, R. M. Strieter, Z. Szekanecz, M. V. Volin, S. Hosaka, G. K. Haines, S. L. Kunkel, M. D. Burdick, A. Walz, and A. E. Koch, “The role of an epithelial neutrophil-activating peptide-78-like protein in rat adjuvant-induced arthritis,” J. Immunol.162(12), 7492–7500 (1999).
[PubMed]

Walsh, D. A.

D. A. Walsh, “Angiogenesis and arthritis,” Rheumatology (Oxford)38(2), 103–112 (1999).
[CrossRef] [PubMed]

Walz, A.

M. M. Halloran, J. M. Woods, R. M. Strieter, Z. Szekanecz, M. V. Volin, S. Hosaka, G. K. Haines, S. L. Kunkel, M. D. Burdick, A. Walz, and A. E. Koch, “The role of an epithelial neutrophil-activating peptide-78-like protein in rat adjuvant-induced arthritis,” J. Immunol.162(12), 7492–7500 (1999).
[PubMed]

Wang, X.

X. Wang, J. B. Fowlkes, J. M. Cannata, C. Hu, and P. L. Carson, “Photoacoustic imaging with a commercial ultrasound system and a custom probe,” Ultrasound Med. Biol.37(3), 484–492 (2011).
[CrossRef] [PubMed]

Woods, J. M.

S. Shahrara, A. E. I. Proudfoot, J. M. Woods, J. H. Ruth, M. A. Amin, C. C. Park, C. S. Haas, R. M. Pope, G. K. Haines, Y. Y. Zha, and A. E. Koch, “Amelioration of rat adjuvant-induced arthritis by Met-RANTES,” Arthritis Rheum.52(6), 1907–1919 (2005).
[CrossRef] [PubMed]

M. M. Halloran, J. M. Woods, R. M. Strieter, Z. Szekanecz, M. V. Volin, S. Hosaka, G. K. Haines, S. L. Kunkel, M. D. Burdick, A. Walz, and A. E. Koch, “The role of an epithelial neutrophil-activating peptide-78-like protein in rat adjuvant-induced arthritis,” J. Immunol.162(12), 7492–7500 (1999).
[PubMed]

Wooley, P. H.

P. H. Wooley, “Animal models of rheumatoid arthritis,” Curr. Opin. Rheumatol.3(3), 407–420 (1991).
[CrossRef] [PubMed]

Zha, Y. Y.

S. Shahrara, A. E. I. Proudfoot, J. M. Woods, J. H. Ruth, M. A. Amin, C. C. Park, C. S. Haas, R. M. Pope, G. K. Haines, Y. Y. Zha, and A. E. Koch, “Amelioration of rat adjuvant-induced arthritis by Met-RANTES,” Arthritis Rheum.52(6), 1907–1919 (2005).
[CrossRef] [PubMed]

Angiogenesis (1)

E. M. Paleolog and J. M. Miotla, “Angiogenesis in arthritis: role in disease pathogenesis and as a potential therapeutic target,” Angiogenesis2(4), 295–307 (1998).
[CrossRef] [PubMed]

Ann. Rheum. Dis. (1)

A. E. Koch, “Angiogenesis as a target in rheumatoid arthritis,” Ann. Rheum. Dis.62(90002Suppl 2), ii60–ii67 (2003).
[CrossRef] [PubMed]

Arthritis Rheum. (4)

S. Shahrara, A. E. I. Proudfoot, J. M. Woods, J. H. Ruth, M. A. Amin, C. C. Park, C. S. Haas, R. M. Pope, G. K. Haines, Y. Y. Zha, and A. E. Koch, “Amelioration of rat adjuvant-induced arthritis by Met-RANTES,” Arthritis Rheum.52(6), 1907–1919 (2005).
[CrossRef] [PubMed]

M. M. Halloran, Z. Szekanecz, N. Barquin, G. K. Haines, and A. E. Koch, “Cellular adhesion molecules in rat adjuvant arthritis,” Arthritis Rheum.39(5), 810–819 (1996).
[CrossRef] [PubMed]

O. Fitzgerald and B. Bresnihan, “Synovial vascularity is increased in rheumatoid arthritis: comment on the article by Stevens et al,” Arthritis Rheum.35(12), 1540–1541 (1992).
[CrossRef] [PubMed]

A. E. Koch, “Review: angiogenesis: implications for rheumatoid arthritis,” Arthritis Rheum.41(6), 951–962 (1998).
[CrossRef] [PubMed]

Curr. Opin. Rheumatol. (1)

P. H. Wooley, “Animal models of rheumatoid arthritis,” Curr. Opin. Rheumatol.3(3), 407–420 (1991).
[CrossRef] [PubMed]

Exp. Neurol. (1)

V. Papadopoulos and L. Lecanu, “Translocator protein (18 kDa) TSPO: an emerging therapeutic target in neurotrauma,” Exp. Neurol.219(1), 53–57 (2009).
[CrossRef] [PubMed]

J. Clin. Invest. (1)

D. A. Barnes, J. Tse, M. Kaufhold, M. Owen, J. Hesselgesser, R. Strieter, R. Horuk, and H. D. Perez, “Polyclonal antibody directed against human RANTES ameliorates disease in the Lewis rat adjuvant-induced arthritis model,” J. Clin. Invest.101(12), 2910–2919 (1998).
[CrossRef] [PubMed]

J. Immunol. (1)

M. M. Halloran, J. M. Woods, R. M. Strieter, Z. Szekanecz, M. V. Volin, S. Hosaka, G. K. Haines, S. L. Kunkel, M. D. Burdick, A. Walz, and A. E. Koch, “The role of an epithelial neutrophil-activating peptide-78-like protein in rat adjuvant-induced arthritis,” J. Immunol.162(12), 7492–7500 (1999).
[PubMed]

Lancet (1)

A. J. Hayes, “Angioneogenesis in rheumatoid arthritis,” Lancet354(9176), 423–424 (1999).
[CrossRef] [PubMed]

Methods Enzymol. (1)

J. D. Taurog, D. C. Argentieri, and R. A. McReynolds, “Adjuvant arthritis,” Methods Enzymol.162, 339–355 (1988).
[CrossRef] [PubMed]

MMWR Morb. Mortal. Wkly. Rep. (1)

Centers for Disease Control and Prevention (CDC), “Racial/ethnic differences in the prevalence and impact of doctor-diagnosed arthritis—United States, 2002,” MMWR Morb. Mortal. Wkly. Rep.54(5), 119–123 (2005).
[PubMed]

Pharmacol. Ther. (1)

M. K. Chen and T. R. Guilarte, “Translocator protein 18 kDa (TSPO): molecular sensor of brain injury and repair,” Pharmacol. Ther.118(1), 1–17 (2008).
[CrossRef] [PubMed]

Rheumatology (Oxford) (1)

D. A. Walsh, “Angiogenesis and arthritis,” Rheumatology (Oxford)38(2), 103–112 (1999).
[CrossRef] [PubMed]

Ultrasound Med. Biol. (1)

X. Wang, J. B. Fowlkes, J. M. Cannata, C. Hu, and P. L. Carson, “Photoacoustic imaging with a commercial ultrasound system and a custom probe,” Ultrasound Med. Biol.37(3), 484–492 (2011).
[CrossRef] [PubMed]

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Figures (7)

Fig. 1
Fig. 1

Schematic of the experimental setup for PAI and US dual-modality imaging of a rat ankle joint.

Fig. 2
Fig. 2

PAI and US dual-modality imaging of a rat ankle joint affected by AIA. (A) Gray-scale PAI image. (B) Gray-scale US image. (C) Pseudo-color PAI image superimposed on the gray-scale US image.

Fig. 3
Fig. 3

(A) Average photoacoustic image intensities in the normal vs. the arthritic ankle joints. (B) Average diameters of the normal vs. the arthritic ankle joints.

Fig. 4
Fig. 4

Photomicrographs of a normal (A) and an arthritic (B and C) rat tarsal (ankle) joints. A and B: original magnification × 40, bar = 500 μm. C: original magnification × 400, bar = 50μm.

Fig. 5
Fig. 5

Pseudo-color PA image superimposed on the gray-scale US image. (A) Image of an arthritic joint of a rat from the non-treatment control group, (B) image of an arthritic joint of a rat from the treatment group.

Fig. 6
Fig. 6

(A) Average photoacoustic image intensities in the treated vs. the untreated arthritic ankle joints. (B) Average diameters of the treated vs. the untreated arthritic ankle joints.

Fig. 7
Fig. 7

MicroPET images covering the rear part of the rat body, including the ankle joints that were the targets for imaging. A, B and C are images of a rat from the treatment group taken on day 0 (normal), day 20 (arthritic) and day 35 (treated), respectively. D, E and F are images of a rat from the non-treatment group taken on day 0 (normal), day 20 (arthritic) and day 35 (untreated), respectively.

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