Abstract

In a synovial joint, the articular cartilage is directly affected during the progression of Osteoarthritis (OA). The characterization of early stage modification in extra-cellular matrix of cartilage is essential for detection as well as understanding the progression of disease. The objective of this study is to demonstrate the potential and capability of nonlinear optical microscopy for the morphological investigation of early stage osteoarthritic cartilage. ICRS Grade-I cartilage sections were obtained from the femoral condyle of the human knee. The surface of articular cartilage was imaged by second harmonic generation and two-photon excited fluorescence microscopy. Novel morphological features like microsplits and wrinkles were observed, which would otherwise not be visible in other clinical imaging modalities (e.g., CT, MRI, ultrasound and arthroscope. The presence of superficial layer with distinct collagen fibrils parallel to the articular surface in 4 specimens out of 14 specimens, indicates that different phases of OA within ICRS Grade-I can be detected by SHG microscopy. All together, the observed novel morphologies in early stage osteoarthritic cartilage indicates that SHG microscopy might be a significant tool for the assessment of cartilage disorder.

© 2015 Optical Society of America

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References

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2015 (1)

2014 (4)

D. J. Hunter, D. Schofield, and E. Callander, “The individual and socioeconomic impact of osteoarthritis,” Nat. Rev. Rheumatol. 10(7), 437–441 (2014).
[PubMed]

C. P. Brown, M. A. Houle, K. Popov, M. Nicklaus, C. A. Couture, M. Laliberté, T. Brabec, A. Ruediger, A. J. Carr, A. J. Price, H. S. Gill, L. Ramunno, and F. Légaré, “Imaging and modeling collagen architecture from the nano to micro scale,” Biomed. Opt. Express 5(1), 233–243 (2014).
[Crossref] [PubMed]

R. Kumar, K. M. Grønhaug, E. I. Romijn, A. Finnøy, C. L. Davies, J. O. Drogset, and M. B. Lilledahl, “Analysis of human knee osteoarthritic cartilage using polarization sensitive second harmonic generation microscopy,” Proc. SPIE 9129, 91292Z (2014).
[Crossref]

B. He, J. P. Wu, T. B. Kirk, J. A. Carrino, C. Xiang, and J. Xu, “High-resolution measurements of the multilayer ultra-structure of articular cartilage and their translational potential,” Arthritis Res. Ther. 16(2), 205 (2014).
[PubMed]

2012 (1)

C. P. Brown, M. A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater. 5(1), 62–70 (2012).
[Crossref] [PubMed]

2011 (1)

A. Steward, Y. Liu, and D. Wagner, “Engineering cell attachments to scaffolds in cartilage tissue engineering,” JOM 63(4), 74–82 (2011).
[Crossref]

2009 (4)

A. J. Sophia Fox, A. Bedi, and S. A. Rodeo, “The basic science of articular cartilage: structure, composition, and function,” Sports Health 1(6), 461–468 (2009).
[Crossref] [PubMed]

M. R. Tsai, C. H. Chen, and C. K. Sun, “Third and second harmonic generation imaging of human articular cartilage,” Proc. SPIE 7183, 71831V (2009).
[Crossref]

S. Tang, W. Jung, D. McCormick, T. Xie, J. Su, Y. C. Ahn, B. J. Tromberg, and Z. Chen, “Design and implementation of fiber-based multiphoton endoscopy with microelectromechanical systems scanning,” J. Biomed. Opt. 14(3), 034005 (2009).
[Crossref] [PubMed]

H. Bao and M. Gu, “A 0.4-mm-diameter probe for nonlinear optical imaging,” Opt. Express 17(12), 10098–10104 (2009).
[Crossref] [PubMed]

2008 (3)

W. Jung, S. Tang, D. T. McCormic, T. Xie, Y. C. Ahn, J. Su, I. V. Tomov, T. B. Krasieva, B. J. Tromberg, and Z. Chen, “Miniaturized probe based on a microelectromechanical system mirror for multiphoton microscopy,” Opt. Lett. 33(12), 1324–1326 (2008).
[Crossref] [PubMed]

J. C. Mansfield, C. P. Winlove, J. Moger, and S. J. Matcher, “Collagen fiber arrangement in normal and diseased cartilage studied by polarization sensitive nonlinear microscopy,” J. Biomed. Opt. 13(4), 044020 (2008).
[Crossref] [PubMed]

J. Martel-Pelletier, C. Boileau, J. P. Pelletier, and P. J. Roughley, “Cartilage in normal and osteoarthritis conditions,” Best Pract. Res. Clin. Rheumatol. 22(2), 351–384 (2008).
[Crossref] [PubMed]

2007 (1)

A. Fioravanti, E. Moretti, G. Scapigliati, R. Cervone, M. Galeazzi, and G. Collodel, “Morphological, immunocytochemical and biochemical studies in human osteoarthritic chondrocytes exposed to IL-1b and cyclical hydrostatic pressure,” Clin. Exp. Rheumatol. 25(5), 690–695 (2007).
[PubMed]

2006 (2)

J. C. Mansfield, C. P. Winlove, K. Knapp, and S. J. Matcher, “Imaging articular cartilage using second harmonic generation microscopy,” Proc. SPIE 6089, 60891O (2006).
[Crossref]

W. E. Horton, P. Bennion, and L. Yang, “Cellular, molecular, and matrix changes in cartilage during aging and osteoarthritis,” J. Musculoskelet. Neuronal Interact. 6(4), 379–381 (2006).
[PubMed]

2005 (2)

J. A. Buckwalter, H. J. Mankin, and A. J. Grodzinsky, “Articular cartilage and osteoarthritis,” Instr. Course Lect. 54(54), 465–480 (2005).
[PubMed]

A. T. Yeh, M. J. Hammer-Wilson, D. C. Van Sickle, H. P. Benton, A. Zoumi, B. J. Tromberg, and G. M. Peavy, “Nonlinear optical microscopy of articular cartilage,” Osteoarthritis Cartilage 13(4), 345–352 (2005).
[Crossref] [PubMed]

2003 (1)

W. Mohler, A. C. Millard, and P. J. Campagnola, “Second harmonic generation imaging of endogenous structural proteins,” Methods 29(1), 97–109 (2003).
[Crossref] [PubMed]

2002 (1)

B. H. Brismar, T. Wredmark, T. Movin, J. Leandersson, and O. Svensson, “Observer reliability in the arthroscopic classification of osteoarthritis of the knee,” J. Bone Joint Surg. Br. 84(1), 42–47 (2002).
[Crossref] [PubMed]

2001 (2)

A. M. Bendele, “Animal models of osteoarthritis,” J. Musculoskelet. Neuronal Interact. 1(4), 363–376 (2001).
[PubMed]

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, “Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis,” J. Rheumatol. 28(6), 1311–1318 (2001).
[PubMed]

1999 (1)

K. Ostergaard, C. B. Andersen, J. Petersen, K. Bendtzen, and D. M. Salter, “Validity of histopathological grading of articular cartilage from osteoarthritic knee joints,” Ann. Rheum. Dis. 58(4), 208–213 (1999).
[Crossref] [PubMed]

1997 (2)

K. Ostergaard, J. Petersen, C. B. Andersen, K. Bendtzen, and D. M. Salter, “Histologic/histochemical grading system for osteoarthritic articular cartilage: reproducibility and validity,” Arthritis Rheum. 40(10), 1766–1771 (1997).
[Crossref] [PubMed]

A. Saïed, E. Chérin, H. Gaucher, P. Laugier, P. Gillet, J. Floquet, P. Netter, and G. Berger, “Assessment of articular cartilage and subchondral bone: subtle and progressive changes in experimental osteoarthritis using 50 MHz echography in vitro,” J. Bone Miner. Res. 12(9), 1378–1386 (1997).
[Crossref] [PubMed]

1991 (1)

D. D. Dean, “Proteinase-mediated cartilage degradation in osteoarthritis,” Semin. Arthritis Rheum. 20(6Suppl 2), 2–11 (1991).
[Crossref] [PubMed]

1984 (1)

T. D. Brown and D. T. Shaw, “In vitro contact stress distribution on the femoral condyles,” J. Orthop. Res. 2(2), 190–199 (1984).
[Crossref] [PubMed]

1964 (1)

D. G. Murray, “Experimentally induced arthritis using intra-articular papain,” Arthritis Rheum. 7(3), 211–219 (1964).
[Crossref] [PubMed]

Ahn, Y. C.

S. Tang, W. Jung, D. McCormick, T. Xie, J. Su, Y. C. Ahn, B. J. Tromberg, and Z. Chen, “Design and implementation of fiber-based multiphoton endoscopy with microelectromechanical systems scanning,” J. Biomed. Opt. 14(3), 034005 (2009).
[Crossref] [PubMed]

W. Jung, S. Tang, D. T. McCormic, T. Xie, Y. C. Ahn, J. Su, I. V. Tomov, T. B. Krasieva, B. J. Tromberg, and Z. Chen, “Miniaturized probe based on a microelectromechanical system mirror for multiphoton microscopy,” Opt. Lett. 33(12), 1324–1326 (2008).
[Crossref] [PubMed]

Andersen, C. B.

K. Ostergaard, C. B. Andersen, J. Petersen, K. Bendtzen, and D. M. Salter, “Validity of histopathological grading of articular cartilage from osteoarthritic knee joints,” Ann. Rheum. Dis. 58(4), 208–213 (1999).
[Crossref] [PubMed]

K. Ostergaard, J. Petersen, C. B. Andersen, K. Bendtzen, and D. M. Salter, “Histologic/histochemical grading system for osteoarthritic articular cartilage: reproducibility and validity,” Arthritis Rheum. 40(10), 1766–1771 (1997).
[Crossref] [PubMed]

Bao, H.

Bedi, A.

A. J. Sophia Fox, A. Bedi, and S. A. Rodeo, “The basic science of articular cartilage: structure, composition, and function,” Sports Health 1(6), 461–468 (2009).
[Crossref] [PubMed]

Bendele, A. M.

A. M. Bendele, “Animal models of osteoarthritis,” J. Musculoskelet. Neuronal Interact. 1(4), 363–376 (2001).
[PubMed]

Bendtzen, K.

K. Ostergaard, C. B. Andersen, J. Petersen, K. Bendtzen, and D. M. Salter, “Validity of histopathological grading of articular cartilage from osteoarthritic knee joints,” Ann. Rheum. Dis. 58(4), 208–213 (1999).
[Crossref] [PubMed]

K. Ostergaard, J. Petersen, C. B. Andersen, K. Bendtzen, and D. M. Salter, “Histologic/histochemical grading system for osteoarthritic articular cartilage: reproducibility and validity,” Arthritis Rheum. 40(10), 1766–1771 (1997).
[Crossref] [PubMed]

Bennion, P.

W. E. Horton, P. Bennion, and L. Yang, “Cellular, molecular, and matrix changes in cartilage during aging and osteoarthritis,” J. Musculoskelet. Neuronal Interact. 6(4), 379–381 (2006).
[PubMed]

Benton, H. P.

A. T. Yeh, M. J. Hammer-Wilson, D. C. Van Sickle, H. P. Benton, A. Zoumi, B. J. Tromberg, and G. M. Peavy, “Nonlinear optical microscopy of articular cartilage,” Osteoarthritis Cartilage 13(4), 345–352 (2005).
[Crossref] [PubMed]

Berger, G.

A. Saïed, E. Chérin, H. Gaucher, P. Laugier, P. Gillet, J. Floquet, P. Netter, and G. Berger, “Assessment of articular cartilage and subchondral bone: subtle and progressive changes in experimental osteoarthritis using 50 MHz echography in vitro,” J. Bone Miner. Res. 12(9), 1378–1386 (1997).
[Crossref] [PubMed]

Boileau, C.

J. Martel-Pelletier, C. Boileau, J. P. Pelletier, and P. J. Roughley, “Cartilage in normal and osteoarthritis conditions,” Best Pract. Res. Clin. Rheumatol. 22(2), 351–384 (2008).
[Crossref] [PubMed]

Brabec, T.

Brezinski, M. E.

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, “Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis,” J. Rheumatol. 28(6), 1311–1318 (2001).
[PubMed]

Brismar, B. H.

B. H. Brismar, T. Wredmark, T. Movin, J. Leandersson, and O. Svensson, “Observer reliability in the arthroscopic classification of osteoarthritis of the knee,” J. Bone Joint Surg. Br. 84(1), 42–47 (2002).
[Crossref] [PubMed]

Brown, C. P.

C. P. Brown, M. A. Houle, K. Popov, M. Nicklaus, C. A. Couture, M. Laliberté, T. Brabec, A. Ruediger, A. J. Carr, A. J. Price, H. S. Gill, L. Ramunno, and F. Légaré, “Imaging and modeling collagen architecture from the nano to micro scale,” Biomed. Opt. Express 5(1), 233–243 (2014).
[Crossref] [PubMed]

C. P. Brown, M. A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater. 5(1), 62–70 (2012).
[Crossref] [PubMed]

Brown, T. D.

T. D. Brown and D. T. Shaw, “In vitro contact stress distribution on the femoral condyles,” J. Orthop. Res. 2(2), 190–199 (1984).
[Crossref] [PubMed]

Buckwalter, J. A.

J. A. Buckwalter, H. J. Mankin, and A. J. Grodzinsky, “Articular cartilage and osteoarthritis,” Instr. Course Lect. 54(54), 465–480 (2005).
[PubMed]

Callander, E.

D. J. Hunter, D. Schofield, and E. Callander, “The individual and socioeconomic impact of osteoarthritis,” Nat. Rev. Rheumatol. 10(7), 437–441 (2014).
[PubMed]

Campagnola, P. J.

W. Mohler, A. C. Millard, and P. J. Campagnola, “Second harmonic generation imaging of endogenous structural proteins,” Methods 29(1), 97–109 (2003).
[Crossref] [PubMed]

Carr, A. J.

Carrino, J. A.

B. He, J. P. Wu, T. B. Kirk, J. A. Carrino, C. Xiang, and J. Xu, “High-resolution measurements of the multilayer ultra-structure of articular cartilage and their translational potential,” Arthritis Res. Ther. 16(2), 205 (2014).
[PubMed]

Cervone, R.

A. Fioravanti, E. Moretti, G. Scapigliati, R. Cervone, M. Galeazzi, and G. Collodel, “Morphological, immunocytochemical and biochemical studies in human osteoarthritic chondrocytes exposed to IL-1b and cyclical hydrostatic pressure,” Clin. Exp. Rheumatol. 25(5), 690–695 (2007).
[PubMed]

Chen, C. H.

M. R. Tsai, C. H. Chen, and C. K. Sun, “Third and second harmonic generation imaging of human articular cartilage,” Proc. SPIE 7183, 71831V (2009).
[Crossref]

Chen, M.

C. P. Brown, M. A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater. 5(1), 62–70 (2012).
[Crossref] [PubMed]

Chen, Z.

S. Tang, W. Jung, D. McCormick, T. Xie, J. Su, Y. C. Ahn, B. J. Tromberg, and Z. Chen, “Design and implementation of fiber-based multiphoton endoscopy with microelectromechanical systems scanning,” J. Biomed. Opt. 14(3), 034005 (2009).
[Crossref] [PubMed]

W. Jung, S. Tang, D. T. McCormic, T. Xie, Y. C. Ahn, J. Su, I. V. Tomov, T. B. Krasieva, B. J. Tromberg, and Z. Chen, “Miniaturized probe based on a microelectromechanical system mirror for multiphoton microscopy,” Opt. Lett. 33(12), 1324–1326 (2008).
[Crossref] [PubMed]

Chérin, E.

A. Saïed, E. Chérin, H. Gaucher, P. Laugier, P. Gillet, J. Floquet, P. Netter, and G. Berger, “Assessment of articular cartilage and subchondral bone: subtle and progressive changes in experimental osteoarthritis using 50 MHz echography in vitro,” J. Bone Miner. Res. 12(9), 1378–1386 (1997).
[Crossref] [PubMed]

Collodel, G.

A. Fioravanti, E. Moretti, G. Scapigliati, R. Cervone, M. Galeazzi, and G. Collodel, “Morphological, immunocytochemical and biochemical studies in human osteoarthritic chondrocytes exposed to IL-1b and cyclical hydrostatic pressure,” Clin. Exp. Rheumatol. 25(5), 690–695 (2007).
[PubMed]

Couture, C. A.

Davies, C. L.

R. Kumar, K. M. Grønhaug, E. I. Romijn, A. Finnøy, C. L. Davies, J. O. Drogset, and M. B. Lilledahl, “Analysis of human knee osteoarthritic cartilage using polarization sensitive second harmonic generation microscopy,” Proc. SPIE 9129, 91292Z (2014).
[Crossref]

Dean, D. D.

D. D. Dean, “Proteinase-mediated cartilage degradation in osteoarthritis,” Semin. Arthritis Rheum. 20(6Suppl 2), 2–11 (1991).
[Crossref] [PubMed]

Drexler, W.

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, “Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis,” J. Rheumatol. 28(6), 1311–1318 (2001).
[PubMed]

Drogset, J. O.

R. Kumar, K. M. Grønhaug, E. I. Romijn, A. Finnøy, C. L. Davies, J. O. Drogset, and M. B. Lilledahl, “Analysis of human knee osteoarthritic cartilage using polarization sensitive second harmonic generation microscopy,” Proc. SPIE 9129, 91292Z (2014).
[Crossref]

Finnøy, A.

R. Kumar, K. M. Grønhaug, E. I. Romijn, A. Finnøy, C. L. Davies, J. O. Drogset, and M. B. Lilledahl, “Analysis of human knee osteoarthritic cartilage using polarization sensitive second harmonic generation microscopy,” Proc. SPIE 9129, 91292Z (2014).
[Crossref]

Fioravanti, A.

A. Fioravanti, E. Moretti, G. Scapigliati, R. Cervone, M. Galeazzi, and G. Collodel, “Morphological, immunocytochemical and biochemical studies in human osteoarthritic chondrocytes exposed to IL-1b and cyclical hydrostatic pressure,” Clin. Exp. Rheumatol. 25(5), 690–695 (2007).
[PubMed]

Floquet, J.

A. Saïed, E. Chérin, H. Gaucher, P. Laugier, P. Gillet, J. Floquet, P. Netter, and G. Berger, “Assessment of articular cartilage and subchondral bone: subtle and progressive changes in experimental osteoarthritis using 50 MHz echography in vitro,” J. Bone Miner. Res. 12(9), 1378–1386 (1997).
[Crossref] [PubMed]

Fujimoto, J. G.

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, “Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis,” J. Rheumatol. 28(6), 1311–1318 (2001).
[PubMed]

Galeazzi, M.

A. Fioravanti, E. Moretti, G. Scapigliati, R. Cervone, M. Galeazzi, and G. Collodel, “Morphological, immunocytochemical and biochemical studies in human osteoarthritic chondrocytes exposed to IL-1b and cyclical hydrostatic pressure,” Clin. Exp. Rheumatol. 25(5), 690–695 (2007).
[PubMed]

Gaucher, H.

A. Saïed, E. Chérin, H. Gaucher, P. Laugier, P. Gillet, J. Floquet, P. Netter, and G. Berger, “Assessment of articular cartilage and subchondral bone: subtle and progressive changes in experimental osteoarthritis using 50 MHz echography in vitro,” J. Bone Miner. Res. 12(9), 1378–1386 (1997).
[Crossref] [PubMed]

Gill, H. S.

C. P. Brown, M. A. Houle, K. Popov, M. Nicklaus, C. A. Couture, M. Laliberté, T. Brabec, A. Ruediger, A. J. Carr, A. J. Price, H. S. Gill, L. Ramunno, and F. Légaré, “Imaging and modeling collagen architecture from the nano to micro scale,” Biomed. Opt. Express 5(1), 233–243 (2014).
[Crossref] [PubMed]

C. P. Brown, M. A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater. 5(1), 62–70 (2012).
[Crossref] [PubMed]

Gillet, P.

A. Saïed, E. Chérin, H. Gaucher, P. Laugier, P. Gillet, J. Floquet, P. Netter, and G. Berger, “Assessment of articular cartilage and subchondral bone: subtle and progressive changes in experimental osteoarthritis using 50 MHz echography in vitro,” J. Bone Miner. Res. 12(9), 1378–1386 (1997).
[Crossref] [PubMed]

Grodzinsky, A. J.

J. A. Buckwalter, H. J. Mankin, and A. J. Grodzinsky, “Articular cartilage and osteoarthritis,” Instr. Course Lect. 54(54), 465–480 (2005).
[PubMed]

Grønhaug, K. M.

R. Kumar, K. M. Grønhaug, E. I. Romijn, A. Finnøy, C. L. Davies, J. O. Drogset, and M. B. Lilledahl, “Analysis of human knee osteoarthritic cartilage using polarization sensitive second harmonic generation microscopy,” Proc. SPIE 9129, 91292Z (2014).
[Crossref]

Gu, M.

Hammer-Wilson, M. J.

A. T. Yeh, M. J. Hammer-Wilson, D. C. Van Sickle, H. P. Benton, A. Zoumi, B. J. Tromberg, and G. M. Peavy, “Nonlinear optical microscopy of articular cartilage,” Osteoarthritis Cartilage 13(4), 345–352 (2005).
[Crossref] [PubMed]

He, B.

B. He, J. P. Wu, T. B. Kirk, J. A. Carrino, C. Xiang, and J. Xu, “High-resolution measurements of the multilayer ultra-structure of articular cartilage and their translational potential,” Arthritis Res. Ther. 16(2), 205 (2014).
[PubMed]

Hikita, A.

Horton, W. E.

W. E. Horton, P. Bennion, and L. Yang, “Cellular, molecular, and matrix changes in cartilage during aging and osteoarthritis,” J. Musculoskelet. Neuronal Interact. 6(4), 379–381 (2006).
[PubMed]

Houle, M. A.

C. P. Brown, M. A. Houle, K. Popov, M. Nicklaus, C. A. Couture, M. Laliberté, T. Brabec, A. Ruediger, A. J. Carr, A. J. Price, H. S. Gill, L. Ramunno, and F. Légaré, “Imaging and modeling collagen architecture from the nano to micro scale,” Biomed. Opt. Express 5(1), 233–243 (2014).
[Crossref] [PubMed]

C. P. Brown, M. A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater. 5(1), 62–70 (2012).
[Crossref] [PubMed]

Hunter, D. J.

D. J. Hunter, D. Schofield, and E. Callander, “The individual and socioeconomic impact of osteoarthritis,” Nat. Rev. Rheumatol. 10(7), 437–441 (2014).
[PubMed]

Iimura, T.

Imamura, T.

Jesser, C.

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, “Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis,” J. Rheumatol. 28(6), 1311–1318 (2001).
[PubMed]

Jung, W.

S. Tang, W. Jung, D. McCormick, T. Xie, J. Su, Y. C. Ahn, B. J. Tromberg, and Z. Chen, “Design and implementation of fiber-based multiphoton endoscopy with microelectromechanical systems scanning,” J. Biomed. Opt. 14(3), 034005 (2009).
[Crossref] [PubMed]

W. Jung, S. Tang, D. T. McCormic, T. Xie, Y. C. Ahn, J. Su, I. V. Tomov, T. B. Krasieva, B. J. Tromberg, and Z. Chen, “Miniaturized probe based on a microelectromechanical system mirror for multiphoton microscopy,” Opt. Lett. 33(12), 1324–1326 (2008).
[Crossref] [PubMed]

Kirk, T. B.

B. He, J. P. Wu, T. B. Kirk, J. A. Carrino, C. Xiang, and J. Xu, “High-resolution measurements of the multilayer ultra-structure of articular cartilage and their translational potential,” Arthritis Res. Ther. 16(2), 205 (2014).
[PubMed]

Kiyomatsu, H.

Knapp, K.

J. C. Mansfield, C. P. Winlove, K. Knapp, and S. J. Matcher, “Imaging articular cartilage using second harmonic generation microscopy,” Proc. SPIE 6089, 60891O (2006).
[Crossref]

Krasieva, T. B.

Kumar, R.

R. Kumar, K. M. Grønhaug, E. I. Romijn, A. Finnøy, C. L. Davies, J. O. Drogset, and M. B. Lilledahl, “Analysis of human knee osteoarthritic cartilage using polarization sensitive second harmonic generation microscopy,” Proc. SPIE 9129, 91292Z (2014).
[Crossref]

Laliberté, M.

Laugier, P.

A. Saïed, E. Chérin, H. Gaucher, P. Laugier, P. Gillet, J. Floquet, P. Netter, and G. Berger, “Assessment of articular cartilage and subchondral bone: subtle and progressive changes in experimental osteoarthritis using 50 MHz echography in vitro,” J. Bone Miner. Res. 12(9), 1378–1386 (1997).
[Crossref] [PubMed]

Leandersson, J.

B. H. Brismar, T. Wredmark, T. Movin, J. Leandersson, and O. Svensson, “Observer reliability in the arthroscopic classification of osteoarthritis of the knee,” J. Bone Joint Surg. Br. 84(1), 42–47 (2002).
[Crossref] [PubMed]

Légaré, F.

C. P. Brown, M. A. Houle, K. Popov, M. Nicklaus, C. A. Couture, M. Laliberté, T. Brabec, A. Ruediger, A. J. Carr, A. J. Price, H. S. Gill, L. Ramunno, and F. Légaré, “Imaging and modeling collagen architecture from the nano to micro scale,” Biomed. Opt. Express 5(1), 233–243 (2014).
[Crossref] [PubMed]

C. P. Brown, M. A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater. 5(1), 62–70 (2012).
[Crossref] [PubMed]

Li, X.

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, “Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis,” J. Rheumatol. 28(6), 1311–1318 (2001).
[PubMed]

Lilledahl, M. B.

R. Kumar, K. M. Grønhaug, E. I. Romijn, A. Finnøy, C. L. Davies, J. O. Drogset, and M. B. Lilledahl, “Analysis of human knee osteoarthritic cartilage using polarization sensitive second harmonic generation microscopy,” Proc. SPIE 9129, 91292Z (2014).
[Crossref]

Liu, Y.

A. Steward, Y. Liu, and D. Wagner, “Engineering cell attachments to scaffolds in cartilage tissue engineering,” JOM 63(4), 74–82 (2011).
[Crossref]

Lodge, M. B.

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, “Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis,” J. Rheumatol. 28(6), 1311–1318 (2001).
[PubMed]

Mankin, H. J.

J. A. Buckwalter, H. J. Mankin, and A. J. Grodzinsky, “Articular cartilage and osteoarthritis,” Instr. Course Lect. 54(54), 465–480 (2005).
[PubMed]

Mansfield, J. C.

J. C. Mansfield, C. P. Winlove, J. Moger, and S. J. Matcher, “Collagen fiber arrangement in normal and diseased cartilage studied by polarization sensitive nonlinear microscopy,” J. Biomed. Opt. 13(4), 044020 (2008).
[Crossref] [PubMed]

J. C. Mansfield, C. P. Winlove, K. Knapp, and S. J. Matcher, “Imaging articular cartilage using second harmonic generation microscopy,” Proc. SPIE 6089, 60891O (2006).
[Crossref]

Martel-Pelletier, J.

J. Martel-Pelletier, C. Boileau, J. P. Pelletier, and P. J. Roughley, “Cartilage in normal and osteoarthritis conditions,” Best Pract. Res. Clin. Rheumatol. 22(2), 351–384 (2008).
[Crossref] [PubMed]

Martin, S.

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, “Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis,” J. Rheumatol. 28(6), 1311–1318 (2001).
[PubMed]

Matcher, S. J.

J. C. Mansfield, C. P. Winlove, J. Moger, and S. J. Matcher, “Collagen fiber arrangement in normal and diseased cartilage studied by polarization sensitive nonlinear microscopy,” J. Biomed. Opt. 13(4), 044020 (2008).
[Crossref] [PubMed]

J. C. Mansfield, C. P. Winlove, K. Knapp, and S. J. Matcher, “Imaging articular cartilage using second harmonic generation microscopy,” Proc. SPIE 6089, 60891O (2006).
[Crossref]

McCormic, D. T.

McCormick, D.

S. Tang, W. Jung, D. McCormick, T. Xie, J. Su, Y. C. Ahn, B. J. Tromberg, and Z. Chen, “Design and implementation of fiber-based multiphoton endoscopy with microelectromechanical systems scanning,” J. Biomed. Opt. 14(3), 034005 (2009).
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Millard, A. C.

W. Mohler, A. C. Millard, and P. J. Campagnola, “Second harmonic generation imaging of endogenous structural proteins,” Methods 29(1), 97–109 (2003).
[Crossref] [PubMed]

Miura, H.

Miyazaki, T.

Moger, J.

J. C. Mansfield, C. P. Winlove, J. Moger, and S. J. Matcher, “Collagen fiber arrangement in normal and diseased cartilage studied by polarization sensitive nonlinear microscopy,” J. Biomed. Opt. 13(4), 044020 (2008).
[Crossref] [PubMed]

Mohler, W.

W. Mohler, A. C. Millard, and P. J. Campagnola, “Second harmonic generation imaging of endogenous structural proteins,” Methods 29(1), 97–109 (2003).
[Crossref] [PubMed]

Moretti, E.

A. Fioravanti, E. Moretti, G. Scapigliati, R. Cervone, M. Galeazzi, and G. Collodel, “Morphological, immunocytochemical and biochemical studies in human osteoarthritic chondrocytes exposed to IL-1b and cyclical hydrostatic pressure,” Clin. Exp. Rheumatol. 25(5), 690–695 (2007).
[PubMed]

Movin, T.

B. H. Brismar, T. Wredmark, T. Movin, J. Leandersson, and O. Svensson, “Observer reliability in the arthroscopic classification of osteoarthritis of the knee,” J. Bone Joint Surg. Br. 84(1), 42–47 (2002).
[Crossref] [PubMed]

Murray, D. G.

D. G. Murray, “Experimentally induced arthritis using intra-articular papain,” Arthritis Rheum. 7(3), 211–219 (1964).
[Crossref] [PubMed]

Netter, P.

A. Saïed, E. Chérin, H. Gaucher, P. Laugier, P. Gillet, J. Floquet, P. Netter, and G. Berger, “Assessment of articular cartilage and subchondral bone: subtle and progressive changes in experimental osteoarthritis using 50 MHz echography in vitro,” J. Bone Miner. Res. 12(9), 1378–1386 (1997).
[Crossref] [PubMed]

Nicklaus, M.

Oshima, Y.

Ostergaard, K.

K. Ostergaard, C. B. Andersen, J. Petersen, K. Bendtzen, and D. M. Salter, “Validity of histopathological grading of articular cartilage from osteoarthritic knee joints,” Ann. Rheum. Dis. 58(4), 208–213 (1999).
[Crossref] [PubMed]

K. Ostergaard, J. Petersen, C. B. Andersen, K. Bendtzen, and D. M. Salter, “Histologic/histochemical grading system for osteoarthritic articular cartilage: reproducibility and validity,” Arthritis Rheum. 40(10), 1766–1771 (1997).
[Crossref] [PubMed]

Peavy, G. M.

A. T. Yeh, M. J. Hammer-Wilson, D. C. Van Sickle, H. P. Benton, A. Zoumi, B. J. Tromberg, and G. M. Peavy, “Nonlinear optical microscopy of articular cartilage,” Osteoarthritis Cartilage 13(4), 345–352 (2005).
[Crossref] [PubMed]

Pelletier, J. P.

J. Martel-Pelletier, C. Boileau, J. P. Pelletier, and P. J. Roughley, “Cartilage in normal and osteoarthritis conditions,” Best Pract. Res. Clin. Rheumatol. 22(2), 351–384 (2008).
[Crossref] [PubMed]

Petersen, J.

K. Ostergaard, C. B. Andersen, J. Petersen, K. Bendtzen, and D. M. Salter, “Validity of histopathological grading of articular cartilage from osteoarthritic knee joints,” Ann. Rheum. Dis. 58(4), 208–213 (1999).
[Crossref] [PubMed]

K. Ostergaard, J. Petersen, C. B. Andersen, K. Bendtzen, and D. M. Salter, “Histologic/histochemical grading system for osteoarthritic articular cartilage: reproducibility and validity,” Arthritis Rheum. 40(10), 1766–1771 (1997).
[Crossref] [PubMed]

Pitris, C.

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, “Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis,” J. Rheumatol. 28(6), 1311–1318 (2001).
[PubMed]

Popov, K.

Price, A. J.

C. P. Brown, M. A. Houle, K. Popov, M. Nicklaus, C. A. Couture, M. Laliberté, T. Brabec, A. Ruediger, A. J. Carr, A. J. Price, H. S. Gill, L. Ramunno, and F. Légaré, “Imaging and modeling collagen architecture from the nano to micro scale,” Biomed. Opt. Express 5(1), 233–243 (2014).
[Crossref] [PubMed]

C. P. Brown, M. A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater. 5(1), 62–70 (2012).
[Crossref] [PubMed]

Ramunno, L.

Rodeo, S. A.

A. J. Sophia Fox, A. Bedi, and S. A. Rodeo, “The basic science of articular cartilage: structure, composition, and function,” Sports Health 1(6), 461–468 (2009).
[Crossref] [PubMed]

Romijn, E. I.

R. Kumar, K. M. Grønhaug, E. I. Romijn, A. Finnøy, C. L. Davies, J. O. Drogset, and M. B. Lilledahl, “Analysis of human knee osteoarthritic cartilage using polarization sensitive second harmonic generation microscopy,” Proc. SPIE 9129, 91292Z (2014).
[Crossref]

Roughley, P. J.

J. Martel-Pelletier, C. Boileau, J. P. Pelletier, and P. J. Roughley, “Cartilage in normal and osteoarthritis conditions,” Best Pract. Res. Clin. Rheumatol. 22(2), 351–384 (2008).
[Crossref] [PubMed]

Ruediger, A.

Saïed, A.

A. Saïed, E. Chérin, H. Gaucher, P. Laugier, P. Gillet, J. Floquet, P. Netter, and G. Berger, “Assessment of articular cartilage and subchondral bone: subtle and progressive changes in experimental osteoarthritis using 50 MHz echography in vitro,” J. Bone Miner. Res. 12(9), 1378–1386 (1997).
[Crossref] [PubMed]

Saitou, T.

Salter, D. M.

K. Ostergaard, C. B. Andersen, J. Petersen, K. Bendtzen, and D. M. Salter, “Validity of histopathological grading of articular cartilage from osteoarthritic knee joints,” Ann. Rheum. Dis. 58(4), 208–213 (1999).
[Crossref] [PubMed]

K. Ostergaard, J. Petersen, C. B. Andersen, K. Bendtzen, and D. M. Salter, “Histologic/histochemical grading system for osteoarthritic articular cartilage: reproducibility and validity,” Arthritis Rheum. 40(10), 1766–1771 (1997).
[Crossref] [PubMed]

Saunders, K.

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, “Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis,” J. Rheumatol. 28(6), 1311–1318 (2001).
[PubMed]

Scapigliati, G.

A. Fioravanti, E. Moretti, G. Scapigliati, R. Cervone, M. Galeazzi, and G. Collodel, “Morphological, immunocytochemical and biochemical studies in human osteoarthritic chondrocytes exposed to IL-1b and cyclical hydrostatic pressure,” Clin. Exp. Rheumatol. 25(5), 690–695 (2007).
[PubMed]

Schofield, D.

D. J. Hunter, D. Schofield, and E. Callander, “The individual and socioeconomic impact of osteoarthritis,” Nat. Rev. Rheumatol. 10(7), 437–441 (2014).
[PubMed]

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T. D. Brown and D. T. Shaw, “In vitro contact stress distribution on the femoral condyles,” J. Orthop. Res. 2(2), 190–199 (1984).
[Crossref] [PubMed]

Sophia Fox, A. J.

A. J. Sophia Fox, A. Bedi, and S. A. Rodeo, “The basic science of articular cartilage: structure, composition, and function,” Sports Health 1(6), 461–468 (2009).
[Crossref] [PubMed]

Stamper, D.

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, “Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis,” J. Rheumatol. 28(6), 1311–1318 (2001).
[PubMed]

Steward, A.

A. Steward, Y. Liu, and D. Wagner, “Engineering cell attachments to scaffolds in cartilage tissue engineering,” JOM 63(4), 74–82 (2011).
[Crossref]

Su, J.

S. Tang, W. Jung, D. McCormick, T. Xie, J. Su, Y. C. Ahn, B. J. Tromberg, and Z. Chen, “Design and implementation of fiber-based multiphoton endoscopy with microelectromechanical systems scanning,” J. Biomed. Opt. 14(3), 034005 (2009).
[Crossref] [PubMed]

W. Jung, S. Tang, D. T. McCormic, T. Xie, Y. C. Ahn, J. Su, I. V. Tomov, T. B. Krasieva, B. J. Tromberg, and Z. Chen, “Miniaturized probe based on a microelectromechanical system mirror for multiphoton microscopy,” Opt. Lett. 33(12), 1324–1326 (2008).
[Crossref] [PubMed]

Sun, C. K.

M. R. Tsai, C. H. Chen, and C. K. Sun, “Third and second harmonic generation imaging of human articular cartilage,” Proc. SPIE 7183, 71831V (2009).
[Crossref]

Svensson, O.

B. H. Brismar, T. Wredmark, T. Movin, J. Leandersson, and O. Svensson, “Observer reliability in the arthroscopic classification of osteoarthritis of the knee,” J. Bone Joint Surg. Br. 84(1), 42–47 (2002).
[Crossref] [PubMed]

Tang, S.

S. Tang, W. Jung, D. McCormick, T. Xie, J. Su, Y. C. Ahn, B. J. Tromberg, and Z. Chen, “Design and implementation of fiber-based multiphoton endoscopy with microelectromechanical systems scanning,” J. Biomed. Opt. 14(3), 034005 (2009).
[Crossref] [PubMed]

W. Jung, S. Tang, D. T. McCormic, T. Xie, Y. C. Ahn, J. Su, I. V. Tomov, T. B. Krasieva, B. J. Tromberg, and Z. Chen, “Miniaturized probe based on a microelectromechanical system mirror for multiphoton microscopy,” Opt. Lett. 33(12), 1324–1326 (2008).
[Crossref] [PubMed]

Tomov, I. V.

Tromberg, B. J.

S. Tang, W. Jung, D. McCormick, T. Xie, J. Su, Y. C. Ahn, B. J. Tromberg, and Z. Chen, “Design and implementation of fiber-based multiphoton endoscopy with microelectromechanical systems scanning,” J. Biomed. Opt. 14(3), 034005 (2009).
[Crossref] [PubMed]

W. Jung, S. Tang, D. T. McCormic, T. Xie, Y. C. Ahn, J. Su, I. V. Tomov, T. B. Krasieva, B. J. Tromberg, and Z. Chen, “Miniaturized probe based on a microelectromechanical system mirror for multiphoton microscopy,” Opt. Lett. 33(12), 1324–1326 (2008).
[Crossref] [PubMed]

A. T. Yeh, M. J. Hammer-Wilson, D. C. Van Sickle, H. P. Benton, A. Zoumi, B. J. Tromberg, and G. M. Peavy, “Nonlinear optical microscopy of articular cartilage,” Osteoarthritis Cartilage 13(4), 345–352 (2005).
[Crossref] [PubMed]

Tsai, M. R.

M. R. Tsai, C. H. Chen, and C. K. Sun, “Third and second harmonic generation imaging of human articular cartilage,” Proc. SPIE 7183, 71831V (2009).
[Crossref]

Van Sickle, D. C.

A. T. Yeh, M. J. Hammer-Wilson, D. C. Van Sickle, H. P. Benton, A. Zoumi, B. J. Tromberg, and G. M. Peavy, “Nonlinear optical microscopy of articular cartilage,” Osteoarthritis Cartilage 13(4), 345–352 (2005).
[Crossref] [PubMed]

Wagner, D.

A. Steward, Y. Liu, and D. Wagner, “Engineering cell attachments to scaffolds in cartilage tissue engineering,” JOM 63(4), 74–82 (2011).
[Crossref]

Winlove, C. P.

J. C. Mansfield, C. P. Winlove, J. Moger, and S. J. Matcher, “Collagen fiber arrangement in normal and diseased cartilage studied by polarization sensitive nonlinear microscopy,” J. Biomed. Opt. 13(4), 044020 (2008).
[Crossref] [PubMed]

J. C. Mansfield, C. P. Winlove, K. Knapp, and S. J. Matcher, “Imaging articular cartilage using second harmonic generation microscopy,” Proc. SPIE 6089, 60891O (2006).
[Crossref]

Wredmark, T.

B. H. Brismar, T. Wredmark, T. Movin, J. Leandersson, and O. Svensson, “Observer reliability in the arthroscopic classification of osteoarthritis of the knee,” J. Bone Joint Surg. Br. 84(1), 42–47 (2002).
[Crossref] [PubMed]

Wu, J. P.

B. He, J. P. Wu, T. B. Kirk, J. A. Carrino, C. Xiang, and J. Xu, “High-resolution measurements of the multilayer ultra-structure of articular cartilage and their translational potential,” Arthritis Res. Ther. 16(2), 205 (2014).
[PubMed]

Xiang, C.

B. He, J. P. Wu, T. B. Kirk, J. A. Carrino, C. Xiang, and J. Xu, “High-resolution measurements of the multilayer ultra-structure of articular cartilage and their translational potential,” Arthritis Res. Ther. 16(2), 205 (2014).
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Supplementary Material (3)

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Figures (5)

Fig. 1
Fig. 1 A schematic diagram showing the optical module inserted in the excitation beam path to achieve CPL for uniform illumination of cartilage. It also shows the orientation of cartilage during acquisition of NLOM image.
Fig. 2
Fig. 2 Histology (H&E stain) and arthroscopy image of a typical ICRS Grade-I osteoarthritic cartilage.
Fig. 3
Fig. 3 SHG images of ICRS Grade-I osteoarthritic cartilage that shows microsplits at depth (a) 5µm (b) 15µm and (c) 30µm from the articular surface of cartilage. (d) TPEF image of the section 3(c). The TPEF image does not show microsplits as clear as in SHG image.
Fig. 4
Fig. 4 SHG images of ICRS Grade-I osteoarthritic cartilage that shows superficial layer at depth (a) 5µm (b) 15µm.
Fig. 5
Fig. 5 SHG images of ICRS Grade-I osteoarthritic cartilage that shows ripples/wrinkles at the depth (a) 5µm (b) 15µm. (c) SHG-3D perspective view of rippling. (d) TPEF image of the section 5(c). The feature of rippling is not observed clearly in TPEF image.

Tables (1)

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Table 1 Morphological features that were observed in ICRS Grade-I osteoarthritic human cartilage

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