Abstract

Diagnosis of articular cartilage pathology in the early disease stages using current clinical diagnostic imaging modalities is challenging, particularly because there is often no visible change in the tissue surface and matrix content, such as proteoglycans (PG). In this study, we propose the use of near infrared (NIR) spectroscopy to spatially map PG content in articular cartilage. The relationship between NIR spectra and reference data (PG content) obtained from histology of normal and artificially induced PG-depleted cartilage samples was investigated using principal component (PC) and partial least squares (PLS) regression analyses. Significant correlation was obtained between both data (R2 = 91.40%, p<0.0001). The resulting correlation was used to predict PG content from spectra acquired from whole joint sample, this was then employed to spatially map this component of cartilage across the intact sample. We conclude that NIR spectroscopy is a feasible tool for evaluating cartilage contents and mapping their distribution across mammalian joint.

© 2014 Optical Society of America

Full Article  |  PDF Article
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2014 (1)

I. O. Afara, I. Prasadam, H. Moody, R. Crawford, Y. Xiao, and A. Oloyede, “Near infrared spectroscopy for rapid determination of Mankin score components: a potential tool for quantitative characterization of articular cartilage at surgery,” Arthroscopy 30(9), 1146–1155 (2014).
[Crossref] [PubMed]

2013 (4)

I. Afara, S. Singh, and A. Oloyede, “Application of near infrared (NIR) spectroscopy for determining the thickness of articular cartilage,” Med. Eng. Phys. 35(1), 88–95 (2013).
[Crossref] [PubMed]

I. O. Afara, I. Prasadam, R. Crawford, Y. Xiao, and A. Oloyede, “Near infrared (NIR) absorption spectra correlates with subchondral bone micro-CT parameters in osteoarthritic rat models,” Bone 53(2), 350–357 (2013).
[Crossref] [PubMed]

I. Afara, S. Singh, H. Moody, and A. Oloyede, “A comparison of the histochemical and image-derived proteoglycan content of articular cartilage,” Anat. Physiol. 3, 1000120 (2013).

I. O. Afara, S. Singh, and A. Oloyede, “Load-unloading response of intact and artificially degraded articular cartilage correlated with near infrared (NIR) absorption spectra,” J. Mech. Behav. Biomed. Mater. 20, 249–258 (2013).
[Crossref] [PubMed]

2012 (3)

M. A. Khalil, H. K. Kim, I. K. Kim, M. Flexman, R. Dayal, G. Shrikhande, and A. H. Hielscher, “Dynamic diffuse optical tomography imaging of peripheral arterial disease,” Biomed. Opt. Express 3(9), 2288–2298 (2012).
[Crossref] [PubMed]

I. Afara, I. Prasadam, R. Crawford, Y. Xiao, and A. Oloyede, “Non-destructive evaluation of articular cartilage defects using near-infrared (NIR) spectroscopy in osteoarthritic rat models and its direct relation to Mankin score,” Osteoarthritis Cartilage 20(11), 1367–1373 (2012).
[Crossref] [PubMed]

J. van Tiel, E. E. Bron, P. K. Bos, S. Klein, M. Reijman, J. A. Verhaar, G. P. Krestin, H. Weinans, G. Kotek, and E. H. Oei, “Reproducibility of 3D delayed gadolinium enhanced MRI of cartilage (DGEMRIC) of the knee at 3.0 Tesla in patients with early-stage osteoarthritis,” Osteoarthritis Cartilage 20, S230–S231 (2012).
[Crossref]

2011 (2)

I. O. Afara, Z. Pawlak, and A. Oloyede, “Current State of the Application of Infrared Optical Methods for Assessing Articular Cartilage,” J. Mater. Sci. Eng. A 1, 1–7 (2011).

G. Spahn, H. M. Klinger, M. Baums, U. Pinkepank, and G. O. Hofmann, “Reliability in arthroscopic grading of cartilage lesions: results of a prospective blinded study for evaluation of inter-observer reliability,” Arch. Orthop. Trauma Surg. 131(3), 377–381 (2011).
[Crossref] [PubMed]

2010 (4)

S. Saarakkala, P. Julkunen, P. Kiviranta, J. Mäkitalo, J. S. Jurvelin, and R. K. Korhonen, “Depth-wise progression of osteoarthritis in human articular cartilage: investigation of composition, structure and biomechanics,” Osteoarthritis Cartilage 18(1), 73–81 (2010).
[Crossref] [PubMed]

L. Rieppo, S. Saarakkala, T. Närhi, J. Holopainen, M. Lammi, H. J. Helminen, J. S. Jurvelin, and J. Rieppo, “Quantitative analysis of spatial proteoglycan content in articular cartilage with Fourier transform infrared imaging spectroscopy: Critical evaluation of analysis methods and specificity of the parameters,” Microsc. Res. Tech. 73(5), 503–512 (2010).
[PubMed]

J. K. Marticke, A. Hösselbarth, K. L. Hoffmeier, I. Marintschev, S. Otto, M. Lange, H. K. W. Plettenberg, G. Spahn, and G. O. Hofmann, “How do visual, spectroscopic and biomechanical changes of cartilage correlate in osteoarthritic knee joints?” Clin. Biomech. (Bristol, Avon) 25(4), 332–340 (2010).
[Crossref] [PubMed]

G. Spahn, H. M. Klinger, M. Baums, M. Hoffmann, H. Plettenberg, A. Kroker, and G. O. Hofmann, “Near-Infrared Spectroscopy for Arthroscopic Evaluation of Cartilage Lesions: Results of a Blinded, Prospective, Interobserver Study,” Am. J. Sports Med. 38(12), 2516–2521 (2010).
[Crossref] [PubMed]

2008 (1)

G. Spahn, H. Plettenberg, H. Nagel, E. Kahl, H. M. Klinger, T. Mückley, M. Günther, G. O. Hofmann, and J. A. Mollenhauer, “Evaluation of cartilage defects with near-infrared spectroscopy (NIR): an ex vivo study,” Med. Eng. Phys. 30(3), 285–292 (2008).
[Crossref] [PubMed]

2007 (2)

G. Spahn, H. Plettenberg, E. Kahl, H. M. Klinger, T. Mückley, and G. O. Hofmann, “Near-infrared (NIR) spectroscopy. A new method for arthroscopic evaluation of low grade degenerated cartilage lesions. Results of a pilot study,” BMC Musculoskelet. Disord. 8(1), 47 (2007).
[Crossref] [PubMed]

C. P. Brown, R. W. Crawford, and A. Oloyede, “Indentation stiffness does not discriminate between normal and degraded articular cartilage,” Clin. Biomech. (Bristol, Avon) 22(7), 843–848 (2007).
[Crossref] [PubMed]

2006 (2)

H. R. Moody, C. P. Brown, J. C. Bowden, R. W. Crawford, D. L. S. McElwain, and A. O. Oloyede, “In vitro degradation of articular cartilage: does trypsin treatment produce consistent results?” J. Anat. 209(2), 259–267 (2006).
[Crossref] [PubMed]

X. Bi, X. Yang, M. P. G. Bostrom, and N. P. Camacho, “Fourier transform infrared imaging spectroscopy investigations in the pathogenesis and repair of cartilage,” Biochim. Biophys. Acta 1758(7), 934–941 (2006).
[Crossref] [PubMed]

2003 (1)

C. J. Tiderius, L. E. Olsson, P. Leander, O. Ekberg, and L. Dahlberg, “Delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) in early knee osteoarthritis,” Magn. Reson. Med. 49(3), 488–492 (2003).
[Crossref] [PubMed]

2002 (2)

E. B. Hunziker, “Articular cartilage repair: basic science and clinical progress. A review of the current status and prospects,” Osteoarthritis Cartilage 10(6), 432–463 (2002).
[Crossref] [PubMed]

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]

2000 (1)

A. Borthakur, E. M. Shapiro, J. Beers, S. Kudchodkar, J. B. Kneeland, and R. Reddy, “Sensitivity of MRI to proteoglycan depletion in cartilage: comparison of sodium and proton MRI,” Osteoarthritis Cartilage 8(4), 288–293 (2000).
[Crossref] [PubMed]

1998 (1)

J. A. Buckwalter and H. J. Mankin, “Articular Cartilage: Degeneration and Osteoarthrosis, Repair, Regeneration, and Transplantation,” J. Bone Jt. Surg. 47, 612–632 (1998).

1996 (1)

K. Király, T. Lapveteläinen, J. Arokoski, K. Törrönen, L. Módis, I. Kiviranta, and H. J. Helminen, “Application of selected cationic dyes for the semiquantitative estimation of glycosaminoglycans in histological sections of articular cartilage by microspectrophotometry,” Histochem. J. 28(8), 577–590 (1996).
[Crossref] [PubMed]

1994 (1)

F. Guilak, A. Ratcliffe, N. Lane, M. P. Rosenwasser, and V. C. Mow, “Mechanical and biochemical changes in the superficial zone of articular cartilage in canine experimental osteoarthritis,” J. Orthop. Res. 12(4), 474–484 (1994).
[Crossref] [PubMed]

1991 (1)

F. Faris, M. Thorniley, Y. Wickramasinghe, R. Houston, P. Rolfe, N. Livera, and A. Spencer, “Non-invasive Invivo near-Infrared Optical Measurement of the Penetration Depth in the Neonatal Head,” Clin. Phys. Physiol. Meas. 12(4), 353–358 (1991).
[Crossref] [PubMed]

1988 (1)

1985 (2)

P. Geladi, D. MacDougall, and H. Martens, “Linearization and Scatter-Correction for Near-Infrared Reflectance Spectra of Meat,” Appl. Spectrosc. 39(3), 491–500 (1985).
[Crossref]

I. Kiviranta, J. Jurvelin, M. Tammi, A. M. Säämänen, and H. J. Helminen, “Microspectrophotometric quantitation of glycosaminoglycans in articular cartilage sections stained with Safranin O,” Histochemistry 82(3), 249–255 (1985).
[Crossref] [PubMed]

1971 (1)

L. Rosenberg, “Chemical basis for the histological use of safranin O in the study of articular cartilage,” J. Bone Joint Surg. Am. 53(1), 69–82 (1971).
[PubMed]

Afara, I.

I. Afara, S. Singh, and A. Oloyede, “Application of near infrared (NIR) spectroscopy for determining the thickness of articular cartilage,” Med. Eng. Phys. 35(1), 88–95 (2013).
[Crossref] [PubMed]

I. Afara, S. Singh, H. Moody, and A. Oloyede, “A comparison of the histochemical and image-derived proteoglycan content of articular cartilage,” Anat. Physiol. 3, 1000120 (2013).

I. Afara, I. Prasadam, R. Crawford, Y. Xiao, and A. Oloyede, “Non-destructive evaluation of articular cartilage defects using near-infrared (NIR) spectroscopy in osteoarthritic rat models and its direct relation to Mankin score,” Osteoarthritis Cartilage 20(11), 1367–1373 (2012).
[Crossref] [PubMed]

Afara, I. O.

I. O. Afara, I. Prasadam, H. Moody, R. Crawford, Y. Xiao, and A. Oloyede, “Near infrared spectroscopy for rapid determination of Mankin score components: a potential tool for quantitative characterization of articular cartilage at surgery,” Arthroscopy 30(9), 1146–1155 (2014).
[Crossref] [PubMed]

I. O. Afara, S. Singh, and A. Oloyede, “Load-unloading response of intact and artificially degraded articular cartilage correlated with near infrared (NIR) absorption spectra,” J. Mech. Behav. Biomed. Mater. 20, 249–258 (2013).
[Crossref] [PubMed]

I. O. Afara, I. Prasadam, R. Crawford, Y. Xiao, and A. Oloyede, “Near infrared (NIR) absorption spectra correlates with subchondral bone micro-CT parameters in osteoarthritic rat models,” Bone 53(2), 350–357 (2013).
[Crossref] [PubMed]

I. O. Afara, Z. Pawlak, and A. Oloyede, “Current State of the Application of Infrared Optical Methods for Assessing Articular Cartilage,” J. Mater. Sci. Eng. A 1, 1–7 (2011).

Arokoski, J.

K. Király, T. Lapveteläinen, J. Arokoski, K. Törrönen, L. Módis, I. Kiviranta, and H. J. Helminen, “Application of selected cationic dyes for the semiquantitative estimation of glycosaminoglycans in histological sections of articular cartilage by microspectrophotometry,” Histochem. J. 28(8), 577–590 (1996).
[Crossref] [PubMed]

Baums, M.

G. Spahn, H. M. Klinger, M. Baums, U. Pinkepank, and G. O. Hofmann, “Reliability in arthroscopic grading of cartilage lesions: results of a prospective blinded study for evaluation of inter-observer reliability,” Arch. Orthop. Trauma Surg. 131(3), 377–381 (2011).
[Crossref] [PubMed]

G. Spahn, H. M. Klinger, M. Baums, M. Hoffmann, H. Plettenberg, A. Kroker, and G. O. Hofmann, “Near-Infrared Spectroscopy for Arthroscopic Evaluation of Cartilage Lesions: Results of a Blinded, Prospective, Interobserver Study,” Am. J. Sports Med. 38(12), 2516–2521 (2010).
[Crossref] [PubMed]

Beers, J.

A. Borthakur, E. M. Shapiro, J. Beers, S. Kudchodkar, J. B. Kneeland, and R. Reddy, “Sensitivity of MRI to proteoglycan depletion in cartilage: comparison of sodium and proton MRI,” Osteoarthritis Cartilage 8(4), 288–293 (2000).
[Crossref] [PubMed]

Bertrand, D.

Bi, X.

X. Bi, X. Yang, M. P. G. Bostrom, and N. P. Camacho, “Fourier transform infrared imaging spectroscopy investigations in the pathogenesis and repair of cartilage,” Biochim. Biophys. Acta 1758(7), 934–941 (2006).
[Crossref] [PubMed]

Borthakur, A.

A. Borthakur, E. M. Shapiro, J. Beers, S. Kudchodkar, J. B. Kneeland, and R. Reddy, “Sensitivity of MRI to proteoglycan depletion in cartilage: comparison of sodium and proton MRI,” Osteoarthritis Cartilage 8(4), 288–293 (2000).
[Crossref] [PubMed]

Bos, P. K.

J. van Tiel, E. E. Bron, P. K. Bos, S. Klein, M. Reijman, J. A. Verhaar, G. P. Krestin, H. Weinans, G. Kotek, and E. H. Oei, “Reproducibility of 3D delayed gadolinium enhanced MRI of cartilage (DGEMRIC) of the knee at 3.0 Tesla in patients with early-stage osteoarthritis,” Osteoarthritis Cartilage 20, S230–S231 (2012).
[Crossref]

Bostrom, M. P. G.

X. Bi, X. Yang, M. P. G. Bostrom, and N. P. Camacho, “Fourier transform infrared imaging spectroscopy investigations in the pathogenesis and repair of cartilage,” Biochim. Biophys. Acta 1758(7), 934–941 (2006).
[Crossref] [PubMed]

Bowden, J. C.

H. R. Moody, C. P. Brown, J. C. Bowden, R. W. Crawford, D. L. S. McElwain, and A. O. Oloyede, “In vitro degradation of articular cartilage: does trypsin treatment produce consistent results?” J. Anat. 209(2), 259–267 (2006).
[Crossref] [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]

Bron, E. E.

J. van Tiel, E. E. Bron, P. K. Bos, S. Klein, M. Reijman, J. A. Verhaar, G. P. Krestin, H. Weinans, G. Kotek, and E. H. Oei, “Reproducibility of 3D delayed gadolinium enhanced MRI of cartilage (DGEMRIC) of the knee at 3.0 Tesla in patients with early-stage osteoarthritis,” Osteoarthritis Cartilage 20, S230–S231 (2012).
[Crossref]

Brown, C. P.

C. P. Brown, R. W. Crawford, and A. Oloyede, “Indentation stiffness does not discriminate between normal and degraded articular cartilage,” Clin. Biomech. (Bristol, Avon) 22(7), 843–848 (2007).
[Crossref] [PubMed]

H. R. Moody, C. P. Brown, J. C. Bowden, R. W. Crawford, D. L. S. McElwain, and A. O. Oloyede, “In vitro degradation of articular cartilage: does trypsin treatment produce consistent results?” J. Anat. 209(2), 259–267 (2006).
[Crossref] [PubMed]

Buckwalter, J. A.

J. A. Buckwalter and H. J. Mankin, “Articular Cartilage: Degeneration and Osteoarthrosis, Repair, Regeneration, and Transplantation,” J. Bone Jt. Surg. 47, 612–632 (1998).

Camacho, N. P.

X. Bi, X. Yang, M. P. G. Bostrom, and N. P. Camacho, “Fourier transform infrared imaging spectroscopy investigations in the pathogenesis and repair of cartilage,” Biochim. Biophys. Acta 1758(7), 934–941 (2006).
[Crossref] [PubMed]

Crawford, R.

I. O. Afara, I. Prasadam, H. Moody, R. Crawford, Y. Xiao, and A. Oloyede, “Near infrared spectroscopy for rapid determination of Mankin score components: a potential tool for quantitative characterization of articular cartilage at surgery,” Arthroscopy 30(9), 1146–1155 (2014).
[Crossref] [PubMed]

I. O. Afara, I. Prasadam, R. Crawford, Y. Xiao, and A. Oloyede, “Near infrared (NIR) absorption spectra correlates with subchondral bone micro-CT parameters in osteoarthritic rat models,” Bone 53(2), 350–357 (2013).
[Crossref] [PubMed]

I. Afara, I. Prasadam, R. Crawford, Y. Xiao, and A. Oloyede, “Non-destructive evaluation of articular cartilage defects using near-infrared (NIR) spectroscopy in osteoarthritic rat models and its direct relation to Mankin score,” Osteoarthritis Cartilage 20(11), 1367–1373 (2012).
[Crossref] [PubMed]

Crawford, R. W.

C. P. Brown, R. W. Crawford, and A. Oloyede, “Indentation stiffness does not discriminate between normal and degraded articular cartilage,” Clin. Biomech. (Bristol, Avon) 22(7), 843–848 (2007).
[Crossref] [PubMed]

H. R. Moody, C. P. Brown, J. C. Bowden, R. W. Crawford, D. L. S. McElwain, and A. O. Oloyede, “In vitro degradation of articular cartilage: does trypsin treatment produce consistent results?” J. Anat. 209(2), 259–267 (2006).
[Crossref] [PubMed]

Dahlberg, L.

C. J. Tiderius, L. E. Olsson, P. Leander, O. Ekberg, and L. Dahlberg, “Delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) in early knee osteoarthritis,” Magn. Reson. Med. 49(3), 488–492 (2003).
[Crossref] [PubMed]

Dayal, R.

Devaux, M. F.

Ekberg, O.

C. J. Tiderius, L. E. Olsson, P. Leander, O. Ekberg, and L. Dahlberg, “Delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) in early knee osteoarthritis,” Magn. Reson. Med. 49(3), 488–492 (2003).
[Crossref] [PubMed]

Faris, F.

F. Faris, M. Thorniley, Y. Wickramasinghe, R. Houston, P. Rolfe, N. Livera, and A. Spencer, “Non-invasive Invivo near-Infrared Optical Measurement of the Penetration Depth in the Neonatal Head,” Clin. Phys. Physiol. Meas. 12(4), 353–358 (1991).
[Crossref] [PubMed]

Flexman, M.

Geladi, P.

Guilak, F.

F. Guilak, A. Ratcliffe, N. Lane, M. P. Rosenwasser, and V. C. Mow, “Mechanical and biochemical changes in the superficial zone of articular cartilage in canine experimental osteoarthritis,” J. Orthop. Res. 12(4), 474–484 (1994).
[Crossref] [PubMed]

Günther, M.

G. Spahn, H. Plettenberg, H. Nagel, E. Kahl, H. M. Klinger, T. Mückley, M. Günther, G. O. Hofmann, and J. A. Mollenhauer, “Evaluation of cartilage defects with near-infrared spectroscopy (NIR): an ex vivo study,” Med. Eng. Phys. 30(3), 285–292 (2008).
[Crossref] [PubMed]

Helminen, H. J.

L. Rieppo, S. Saarakkala, T. Närhi, J. Holopainen, M. Lammi, H. J. Helminen, J. S. Jurvelin, and J. Rieppo, “Quantitative analysis of spatial proteoglycan content in articular cartilage with Fourier transform infrared imaging spectroscopy: Critical evaluation of analysis methods and specificity of the parameters,” Microsc. Res. Tech. 73(5), 503–512 (2010).
[PubMed]

K. Király, T. Lapveteläinen, J. Arokoski, K. Törrönen, L. Módis, I. Kiviranta, and H. J. Helminen, “Application of selected cationic dyes for the semiquantitative estimation of glycosaminoglycans in histological sections of articular cartilage by microspectrophotometry,” Histochem. J. 28(8), 577–590 (1996).
[Crossref] [PubMed]

I. Kiviranta, J. Jurvelin, M. Tammi, A. M. Säämänen, and H. J. Helminen, “Microspectrophotometric quantitation of glycosaminoglycans in articular cartilage sections stained with Safranin O,” Histochemistry 82(3), 249–255 (1985).
[Crossref] [PubMed]

Hielscher, A. H.

Hoffmann, M.

G. Spahn, H. M. Klinger, M. Baums, M. Hoffmann, H. Plettenberg, A. Kroker, and G. O. Hofmann, “Near-Infrared Spectroscopy for Arthroscopic Evaluation of Cartilage Lesions: Results of a Blinded, Prospective, Interobserver Study,” Am. J. Sports Med. 38(12), 2516–2521 (2010).
[Crossref] [PubMed]

Hoffmeier, K. L.

J. K. Marticke, A. Hösselbarth, K. L. Hoffmeier, I. Marintschev, S. Otto, M. Lange, H. K. W. Plettenberg, G. Spahn, and G. O. Hofmann, “How do visual, spectroscopic and biomechanical changes of cartilage correlate in osteoarthritic knee joints?” Clin. Biomech. (Bristol, Avon) 25(4), 332–340 (2010).
[Crossref] [PubMed]

Hofmann, G. O.

G. Spahn, H. M. Klinger, M. Baums, U. Pinkepank, and G. O. Hofmann, “Reliability in arthroscopic grading of cartilage lesions: results of a prospective blinded study for evaluation of inter-observer reliability,” Arch. Orthop. Trauma Surg. 131(3), 377–381 (2011).
[Crossref] [PubMed]

J. K. Marticke, A. Hösselbarth, K. L. Hoffmeier, I. Marintschev, S. Otto, M. Lange, H. K. W. Plettenberg, G. Spahn, and G. O. Hofmann, “How do visual, spectroscopic and biomechanical changes of cartilage correlate in osteoarthritic knee joints?” Clin. Biomech. (Bristol, Avon) 25(4), 332–340 (2010).
[Crossref] [PubMed]

G. Spahn, H. M. Klinger, M. Baums, M. Hoffmann, H. Plettenberg, A. Kroker, and G. O. Hofmann, “Near-Infrared Spectroscopy for Arthroscopic Evaluation of Cartilage Lesions: Results of a Blinded, Prospective, Interobserver Study,” Am. J. Sports Med. 38(12), 2516–2521 (2010).
[Crossref] [PubMed]

G. Spahn, H. Plettenberg, H. Nagel, E. Kahl, H. M. Klinger, T. Mückley, M. Günther, G. O. Hofmann, and J. A. Mollenhauer, “Evaluation of cartilage defects with near-infrared spectroscopy (NIR): an ex vivo study,” Med. Eng. Phys. 30(3), 285–292 (2008).
[Crossref] [PubMed]

G. Spahn, H. Plettenberg, E. Kahl, H. M. Klinger, T. Mückley, and G. O. Hofmann, “Near-infrared (NIR) spectroscopy. A new method for arthroscopic evaluation of low grade degenerated cartilage lesions. Results of a pilot study,” BMC Musculoskelet. Disord. 8(1), 47 (2007).
[Crossref] [PubMed]

Holopainen, J.

L. Rieppo, S. Saarakkala, T. Närhi, J. Holopainen, M. Lammi, H. J. Helminen, J. S. Jurvelin, and J. Rieppo, “Quantitative analysis of spatial proteoglycan content in articular cartilage with Fourier transform infrared imaging spectroscopy: Critical evaluation of analysis methods and specificity of the parameters,” Microsc. Res. Tech. 73(5), 503–512 (2010).
[PubMed]

Hösselbarth, A.

J. K. Marticke, A. Hösselbarth, K. L. Hoffmeier, I. Marintschev, S. Otto, M. Lange, H. K. W. Plettenberg, G. Spahn, and G. O. Hofmann, “How do visual, spectroscopic and biomechanical changes of cartilage correlate in osteoarthritic knee joints?” Clin. Biomech. (Bristol, Avon) 25(4), 332–340 (2010).
[Crossref] [PubMed]

Houston, R.

F. Faris, M. Thorniley, Y. Wickramasinghe, R. Houston, P. Rolfe, N. Livera, and A. Spencer, “Non-invasive Invivo near-Infrared Optical Measurement of the Penetration Depth in the Neonatal Head,” Clin. Phys. Physiol. Meas. 12(4), 353–358 (1991).
[Crossref] [PubMed]

Hunziker, E. B.

E. B. Hunziker, “Articular cartilage repair: basic science and clinical progress. A review of the current status and prospects,” Osteoarthritis Cartilage 10(6), 432–463 (2002).
[Crossref] [PubMed]

Julkunen, P.

S. Saarakkala, P. Julkunen, P. Kiviranta, J. Mäkitalo, J. S. Jurvelin, and R. K. Korhonen, “Depth-wise progression of osteoarthritis in human articular cartilage: investigation of composition, structure and biomechanics,” Osteoarthritis Cartilage 18(1), 73–81 (2010).
[Crossref] [PubMed]

Jurvelin, J.

I. Kiviranta, J. Jurvelin, M. Tammi, A. M. Säämänen, and H. J. Helminen, “Microspectrophotometric quantitation of glycosaminoglycans in articular cartilage sections stained with Safranin O,” Histochemistry 82(3), 249–255 (1985).
[Crossref] [PubMed]

Jurvelin, J. S.

S. Saarakkala, P. Julkunen, P. Kiviranta, J. Mäkitalo, J. S. Jurvelin, and R. K. Korhonen, “Depth-wise progression of osteoarthritis in human articular cartilage: investigation of composition, structure and biomechanics,” Osteoarthritis Cartilage 18(1), 73–81 (2010).
[Crossref] [PubMed]

L. Rieppo, S. Saarakkala, T. Närhi, J. Holopainen, M. Lammi, H. J. Helminen, J. S. Jurvelin, and J. Rieppo, “Quantitative analysis of spatial proteoglycan content in articular cartilage with Fourier transform infrared imaging spectroscopy: Critical evaluation of analysis methods and specificity of the parameters,” Microsc. Res. Tech. 73(5), 503–512 (2010).
[PubMed]

Kahl, E.

G. Spahn, H. Plettenberg, H. Nagel, E. Kahl, H. M. Klinger, T. Mückley, M. Günther, G. O. Hofmann, and J. A. Mollenhauer, “Evaluation of cartilage defects with near-infrared spectroscopy (NIR): an ex vivo study,” Med. Eng. Phys. 30(3), 285–292 (2008).
[Crossref] [PubMed]

G. Spahn, H. Plettenberg, E. Kahl, H. M. Klinger, T. Mückley, and G. O. Hofmann, “Near-infrared (NIR) spectroscopy. A new method for arthroscopic evaluation of low grade degenerated cartilage lesions. Results of a pilot study,” BMC Musculoskelet. Disord. 8(1), 47 (2007).
[Crossref] [PubMed]

Khalil, M. A.

Kim, H. K.

Kim, I. K.

Király, K.

K. Király, T. Lapveteläinen, J. Arokoski, K. Törrönen, L. Módis, I. Kiviranta, and H. J. Helminen, “Application of selected cationic dyes for the semiquantitative estimation of glycosaminoglycans in histological sections of articular cartilage by microspectrophotometry,” Histochem. J. 28(8), 577–590 (1996).
[Crossref] [PubMed]

Kiviranta, I.

K. Király, T. Lapveteläinen, J. Arokoski, K. Törrönen, L. Módis, I. Kiviranta, and H. J. Helminen, “Application of selected cationic dyes for the semiquantitative estimation of glycosaminoglycans in histological sections of articular cartilage by microspectrophotometry,” Histochem. J. 28(8), 577–590 (1996).
[Crossref] [PubMed]

I. Kiviranta, J. Jurvelin, M. Tammi, A. M. Säämänen, and H. J. Helminen, “Microspectrophotometric quantitation of glycosaminoglycans in articular cartilage sections stained with Safranin O,” Histochemistry 82(3), 249–255 (1985).
[Crossref] [PubMed]

Kiviranta, P.

S. Saarakkala, P. Julkunen, P. Kiviranta, J. Mäkitalo, J. S. Jurvelin, and R. K. Korhonen, “Depth-wise progression of osteoarthritis in human articular cartilage: investigation of composition, structure and biomechanics,” Osteoarthritis Cartilage 18(1), 73–81 (2010).
[Crossref] [PubMed]

Klein, S.

J. van Tiel, E. E. Bron, P. K. Bos, S. Klein, M. Reijman, J. A. Verhaar, G. P. Krestin, H. Weinans, G. Kotek, and E. H. Oei, “Reproducibility of 3D delayed gadolinium enhanced MRI of cartilage (DGEMRIC) of the knee at 3.0 Tesla in patients with early-stage osteoarthritis,” Osteoarthritis Cartilage 20, S230–S231 (2012).
[Crossref]

Klinger, H. M.

G. Spahn, H. M. Klinger, M. Baums, U. Pinkepank, and G. O. Hofmann, “Reliability in arthroscopic grading of cartilage lesions: results of a prospective blinded study for evaluation of inter-observer reliability,” Arch. Orthop. Trauma Surg. 131(3), 377–381 (2011).
[Crossref] [PubMed]

G. Spahn, H. M. Klinger, M. Baums, M. Hoffmann, H. Plettenberg, A. Kroker, and G. O. Hofmann, “Near-Infrared Spectroscopy for Arthroscopic Evaluation of Cartilage Lesions: Results of a Blinded, Prospective, Interobserver Study,” Am. J. Sports Med. 38(12), 2516–2521 (2010).
[Crossref] [PubMed]

G. Spahn, H. Plettenberg, H. Nagel, E. Kahl, H. M. Klinger, T. Mückley, M. Günther, G. O. Hofmann, and J. A. Mollenhauer, “Evaluation of cartilage defects with near-infrared spectroscopy (NIR): an ex vivo study,” Med. Eng. Phys. 30(3), 285–292 (2008).
[Crossref] [PubMed]

G. Spahn, H. Plettenberg, E. Kahl, H. M. Klinger, T. Mückley, and G. O. Hofmann, “Near-infrared (NIR) spectroscopy. A new method for arthroscopic evaluation of low grade degenerated cartilage lesions. Results of a pilot study,” BMC Musculoskelet. Disord. 8(1), 47 (2007).
[Crossref] [PubMed]

Kneeland, J. B.

A. Borthakur, E. M. Shapiro, J. Beers, S. Kudchodkar, J. B. Kneeland, and R. Reddy, “Sensitivity of MRI to proteoglycan depletion in cartilage: comparison of sodium and proton MRI,” Osteoarthritis Cartilage 8(4), 288–293 (2000).
[Crossref] [PubMed]

Korhonen, R. K.

S. Saarakkala, P. Julkunen, P. Kiviranta, J. Mäkitalo, J. S. Jurvelin, and R. K. Korhonen, “Depth-wise progression of osteoarthritis in human articular cartilage: investigation of composition, structure and biomechanics,” Osteoarthritis Cartilage 18(1), 73–81 (2010).
[Crossref] [PubMed]

Kotek, G.

J. van Tiel, E. E. Bron, P. K. Bos, S. Klein, M. Reijman, J. A. Verhaar, G. P. Krestin, H. Weinans, G. Kotek, and E. H. Oei, “Reproducibility of 3D delayed gadolinium enhanced MRI of cartilage (DGEMRIC) of the knee at 3.0 Tesla in patients with early-stage osteoarthritis,” Osteoarthritis Cartilage 20, S230–S231 (2012).
[Crossref]

Krestin, G. P.

J. van Tiel, E. E. Bron, P. K. Bos, S. Klein, M. Reijman, J. A. Verhaar, G. P. Krestin, H. Weinans, G. Kotek, and E. H. Oei, “Reproducibility of 3D delayed gadolinium enhanced MRI of cartilage (DGEMRIC) of the knee at 3.0 Tesla in patients with early-stage osteoarthritis,” Osteoarthritis Cartilage 20, S230–S231 (2012).
[Crossref]

Kroker, A.

G. Spahn, H. M. Klinger, M. Baums, M. Hoffmann, H. Plettenberg, A. Kroker, and G. O. Hofmann, “Near-Infrared Spectroscopy for Arthroscopic Evaluation of Cartilage Lesions: Results of a Blinded, Prospective, Interobserver Study,” Am. J. Sports Med. 38(12), 2516–2521 (2010).
[Crossref] [PubMed]

Kudchodkar, S.

A. Borthakur, E. M. Shapiro, J. Beers, S. Kudchodkar, J. B. Kneeland, and R. Reddy, “Sensitivity of MRI to proteoglycan depletion in cartilage: comparison of sodium and proton MRI,” Osteoarthritis Cartilage 8(4), 288–293 (2000).
[Crossref] [PubMed]

Lammi, M.

L. Rieppo, S. Saarakkala, T. Närhi, J. Holopainen, M. Lammi, H. J. Helminen, J. S. Jurvelin, and J. Rieppo, “Quantitative analysis of spatial proteoglycan content in articular cartilage with Fourier transform infrared imaging spectroscopy: Critical evaluation of analysis methods and specificity of the parameters,” Microsc. Res. Tech. 73(5), 503–512 (2010).
[PubMed]

Lane, N.

F. Guilak, A. Ratcliffe, N. Lane, M. P. Rosenwasser, and V. C. Mow, “Mechanical and biochemical changes in the superficial zone of articular cartilage in canine experimental osteoarthritis,” J. Orthop. Res. 12(4), 474–484 (1994).
[Crossref] [PubMed]

Lange, M.

J. K. Marticke, A. Hösselbarth, K. L. Hoffmeier, I. Marintschev, S. Otto, M. Lange, H. K. W. Plettenberg, G. Spahn, and G. O. Hofmann, “How do visual, spectroscopic and biomechanical changes of cartilage correlate in osteoarthritic knee joints?” Clin. Biomech. (Bristol, Avon) 25(4), 332–340 (2010).
[Crossref] [PubMed]

Lapveteläinen, T.

K. Király, T. Lapveteläinen, J. Arokoski, K. Törrönen, L. Módis, I. Kiviranta, and H. J. Helminen, “Application of selected cationic dyes for the semiquantitative estimation of glycosaminoglycans in histological sections of articular cartilage by microspectrophotometry,” Histochem. J. 28(8), 577–590 (1996).
[Crossref] [PubMed]

Leander, P.

C. J. Tiderius, L. E. Olsson, P. Leander, O. Ekberg, and L. Dahlberg, “Delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) in early knee osteoarthritis,” Magn. Reson. Med. 49(3), 488–492 (2003).
[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]

Livera, N.

F. Faris, M. Thorniley, Y. Wickramasinghe, R. Houston, P. Rolfe, N. Livera, and A. Spencer, “Non-invasive Invivo near-Infrared Optical Measurement of the Penetration Depth in the Neonatal Head,” Clin. Phys. Physiol. Meas. 12(4), 353–358 (1991).
[Crossref] [PubMed]

MacDougall, D.

Mäkitalo, J.

S. Saarakkala, P. Julkunen, P. Kiviranta, J. Mäkitalo, J. S. Jurvelin, and R. K. Korhonen, “Depth-wise progression of osteoarthritis in human articular cartilage: investigation of composition, structure and biomechanics,” Osteoarthritis Cartilage 18(1), 73–81 (2010).
[Crossref] [PubMed]

Mankin, H. J.

J. A. Buckwalter and H. J. Mankin, “Articular Cartilage: Degeneration and Osteoarthrosis, Repair, Regeneration, and Transplantation,” J. Bone Jt. Surg. 47, 612–632 (1998).

Marintschev, I.

J. K. Marticke, A. Hösselbarth, K. L. Hoffmeier, I. Marintschev, S. Otto, M. Lange, H. K. W. Plettenberg, G. Spahn, and G. O. Hofmann, “How do visual, spectroscopic and biomechanical changes of cartilage correlate in osteoarthritic knee joints?” Clin. Biomech. (Bristol, Avon) 25(4), 332–340 (2010).
[Crossref] [PubMed]

Martens, H.

Marticke, J. K.

J. K. Marticke, A. Hösselbarth, K. L. Hoffmeier, I. Marintschev, S. Otto, M. Lange, H. K. W. Plettenberg, G. Spahn, and G. O. Hofmann, “How do visual, spectroscopic and biomechanical changes of cartilage correlate in osteoarthritic knee joints?” Clin. Biomech. (Bristol, Avon) 25(4), 332–340 (2010).
[Crossref] [PubMed]

McElwain, D. L. S.

H. R. Moody, C. P. Brown, J. C. Bowden, R. W. Crawford, D. L. S. McElwain, and A. O. Oloyede, “In vitro degradation of articular cartilage: does trypsin treatment produce consistent results?” J. Anat. 209(2), 259–267 (2006).
[Crossref] [PubMed]

Módis, L.

K. Király, T. Lapveteläinen, J. Arokoski, K. Törrönen, L. Módis, I. Kiviranta, and H. J. Helminen, “Application of selected cationic dyes for the semiquantitative estimation of glycosaminoglycans in histological sections of articular cartilage by microspectrophotometry,” Histochem. J. 28(8), 577–590 (1996).
[Crossref] [PubMed]

Mollenhauer, J. A.

G. Spahn, H. Plettenberg, H. Nagel, E. Kahl, H. M. Klinger, T. Mückley, M. Günther, G. O. Hofmann, and J. A. Mollenhauer, “Evaluation of cartilage defects with near-infrared spectroscopy (NIR): an ex vivo study,” Med. Eng. Phys. 30(3), 285–292 (2008).
[Crossref] [PubMed]

Moody, H.

I. O. Afara, I. Prasadam, H. Moody, R. Crawford, Y. Xiao, and A. Oloyede, “Near infrared spectroscopy for rapid determination of Mankin score components: a potential tool for quantitative characterization of articular cartilage at surgery,” Arthroscopy 30(9), 1146–1155 (2014).
[Crossref] [PubMed]

I. Afara, S. Singh, H. Moody, and A. Oloyede, “A comparison of the histochemical and image-derived proteoglycan content of articular cartilage,” Anat. Physiol. 3, 1000120 (2013).

Moody, H. R.

H. R. Moody, C. P. Brown, J. C. Bowden, R. W. Crawford, D. L. S. McElwain, and A. O. Oloyede, “In vitro degradation of articular cartilage: does trypsin treatment produce consistent results?” J. Anat. 209(2), 259–267 (2006).
[Crossref] [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]

Mow, V. C.

F. Guilak, A. Ratcliffe, N. Lane, M. P. Rosenwasser, and V. C. Mow, “Mechanical and biochemical changes in the superficial zone of articular cartilage in canine experimental osteoarthritis,” J. Orthop. Res. 12(4), 474–484 (1994).
[Crossref] [PubMed]

Mückley, T.

G. Spahn, H. Plettenberg, H. Nagel, E. Kahl, H. M. Klinger, T. Mückley, M. Günther, G. O. Hofmann, and J. A. Mollenhauer, “Evaluation of cartilage defects with near-infrared spectroscopy (NIR): an ex vivo study,” Med. Eng. Phys. 30(3), 285–292 (2008).
[Crossref] [PubMed]

G. Spahn, H. Plettenberg, E. Kahl, H. M. Klinger, T. Mückley, and G. O. Hofmann, “Near-infrared (NIR) spectroscopy. A new method for arthroscopic evaluation of low grade degenerated cartilage lesions. Results of a pilot study,” BMC Musculoskelet. Disord. 8(1), 47 (2007).
[Crossref] [PubMed]

Nagel, H.

G. Spahn, H. Plettenberg, H. Nagel, E. Kahl, H. M. Klinger, T. Mückley, M. Günther, G. O. Hofmann, and J. A. Mollenhauer, “Evaluation of cartilage defects with near-infrared spectroscopy (NIR): an ex vivo study,” Med. Eng. Phys. 30(3), 285–292 (2008).
[Crossref] [PubMed]

Närhi, T.

L. Rieppo, S. Saarakkala, T. Närhi, J. Holopainen, M. Lammi, H. J. Helminen, J. S. Jurvelin, and J. Rieppo, “Quantitative analysis of spatial proteoglycan content in articular cartilage with Fourier transform infrared imaging spectroscopy: Critical evaluation of analysis methods and specificity of the parameters,” Microsc. Res. Tech. 73(5), 503–512 (2010).
[PubMed]

Oei, E. H.

J. van Tiel, E. E. Bron, P. K. Bos, S. Klein, M. Reijman, J. A. Verhaar, G. P. Krestin, H. Weinans, G. Kotek, and E. H. Oei, “Reproducibility of 3D delayed gadolinium enhanced MRI of cartilage (DGEMRIC) of the knee at 3.0 Tesla in patients with early-stage osteoarthritis,” Osteoarthritis Cartilage 20, S230–S231 (2012).
[Crossref]

Oloyede, A.

I. O. Afara, I. Prasadam, H. Moody, R. Crawford, Y. Xiao, and A. Oloyede, “Near infrared spectroscopy for rapid determination of Mankin score components: a potential tool for quantitative characterization of articular cartilage at surgery,” Arthroscopy 30(9), 1146–1155 (2014).
[Crossref] [PubMed]

I. O. Afara, S. Singh, and A. Oloyede, “Load-unloading response of intact and artificially degraded articular cartilage correlated with near infrared (NIR) absorption spectra,” J. Mech. Behav. Biomed. Mater. 20, 249–258 (2013).
[Crossref] [PubMed]

I. Afara, S. Singh, and A. Oloyede, “Application of near infrared (NIR) spectroscopy for determining the thickness of articular cartilage,” Med. Eng. Phys. 35(1), 88–95 (2013).
[Crossref] [PubMed]

I. O. Afara, I. Prasadam, R. Crawford, Y. Xiao, and A. Oloyede, “Near infrared (NIR) absorption spectra correlates with subchondral bone micro-CT parameters in osteoarthritic rat models,” Bone 53(2), 350–357 (2013).
[Crossref] [PubMed]

I. Afara, S. Singh, H. Moody, and A. Oloyede, “A comparison of the histochemical and image-derived proteoglycan content of articular cartilage,” Anat. Physiol. 3, 1000120 (2013).

I. Afara, I. Prasadam, R. Crawford, Y. Xiao, and A. Oloyede, “Non-destructive evaluation of articular cartilage defects using near-infrared (NIR) spectroscopy in osteoarthritic rat models and its direct relation to Mankin score,” Osteoarthritis Cartilage 20(11), 1367–1373 (2012).
[Crossref] [PubMed]

I. O. Afara, Z. Pawlak, and A. Oloyede, “Current State of the Application of Infrared Optical Methods for Assessing Articular Cartilage,” J. Mater. Sci. Eng. A 1, 1–7 (2011).

C. P. Brown, R. W. Crawford, and A. Oloyede, “Indentation stiffness does not discriminate between normal and degraded articular cartilage,” Clin. Biomech. (Bristol, Avon) 22(7), 843–848 (2007).
[Crossref] [PubMed]

Oloyede, A. O.

H. R. Moody, C. P. Brown, J. C. Bowden, R. W. Crawford, D. L. S. McElwain, and A. O. Oloyede, “In vitro degradation of articular cartilage: does trypsin treatment produce consistent results?” J. Anat. 209(2), 259–267 (2006).
[Crossref] [PubMed]

Olsson, L. E.

C. J. Tiderius, L. E. Olsson, P. Leander, O. Ekberg, and L. Dahlberg, “Delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) in early knee osteoarthritis,” Magn. Reson. Med. 49(3), 488–492 (2003).
[Crossref] [PubMed]

Otto, S.

J. K. Marticke, A. Hösselbarth, K. L. Hoffmeier, I. Marintschev, S. Otto, M. Lange, H. K. W. Plettenberg, G. Spahn, and G. O. Hofmann, “How do visual, spectroscopic and biomechanical changes of cartilage correlate in osteoarthritic knee joints?” Clin. Biomech. (Bristol, Avon) 25(4), 332–340 (2010).
[Crossref] [PubMed]

Pawlak, Z.

I. O. Afara, Z. Pawlak, and A. Oloyede, “Current State of the Application of Infrared Optical Methods for Assessing Articular Cartilage,” J. Mater. Sci. Eng. A 1, 1–7 (2011).

Pinkepank, U.

G. Spahn, H. M. Klinger, M. Baums, U. Pinkepank, and G. O. Hofmann, “Reliability in arthroscopic grading of cartilage lesions: results of a prospective blinded study for evaluation of inter-observer reliability,” Arch. Orthop. Trauma Surg. 131(3), 377–381 (2011).
[Crossref] [PubMed]

Plettenberg, H.

G. Spahn, H. M. Klinger, M. Baums, M. Hoffmann, H. Plettenberg, A. Kroker, and G. O. Hofmann, “Near-Infrared Spectroscopy for Arthroscopic Evaluation of Cartilage Lesions: Results of a Blinded, Prospective, Interobserver Study,” Am. J. Sports Med. 38(12), 2516–2521 (2010).
[Crossref] [PubMed]

G. Spahn, H. Plettenberg, H. Nagel, E. Kahl, H. M. Klinger, T. Mückley, M. Günther, G. O. Hofmann, and J. A. Mollenhauer, “Evaluation of cartilage defects with near-infrared spectroscopy (NIR): an ex vivo study,” Med. Eng. Phys. 30(3), 285–292 (2008).
[Crossref] [PubMed]

G. Spahn, H. Plettenberg, E. Kahl, H. M. Klinger, T. Mückley, and G. O. Hofmann, “Near-infrared (NIR) spectroscopy. A new method for arthroscopic evaluation of low grade degenerated cartilage lesions. Results of a pilot study,” BMC Musculoskelet. Disord. 8(1), 47 (2007).
[Crossref] [PubMed]

Plettenberg, H. K. W.

J. K. Marticke, A. Hösselbarth, K. L. Hoffmeier, I. Marintschev, S. Otto, M. Lange, H. K. W. Plettenberg, G. Spahn, and G. O. Hofmann, “How do visual, spectroscopic and biomechanical changes of cartilage correlate in osteoarthritic knee joints?” Clin. Biomech. (Bristol, Avon) 25(4), 332–340 (2010).
[Crossref] [PubMed]

Prasadam, I.

I. O. Afara, I. Prasadam, H. Moody, R. Crawford, Y. Xiao, and A. Oloyede, “Near infrared spectroscopy for rapid determination of Mankin score components: a potential tool for quantitative characterization of articular cartilage at surgery,” Arthroscopy 30(9), 1146–1155 (2014).
[Crossref] [PubMed]

I. O. Afara, I. Prasadam, R. Crawford, Y. Xiao, and A. Oloyede, “Near infrared (NIR) absorption spectra correlates with subchondral bone micro-CT parameters in osteoarthritic rat models,” Bone 53(2), 350–357 (2013).
[Crossref] [PubMed]

I. Afara, I. Prasadam, R. Crawford, Y. Xiao, and A. Oloyede, “Non-destructive evaluation of articular cartilage defects using near-infrared (NIR) spectroscopy in osteoarthritic rat models and its direct relation to Mankin score,” Osteoarthritis Cartilage 20(11), 1367–1373 (2012).
[Crossref] [PubMed]

Qannari, M.

Ratcliffe, A.

F. Guilak, A. Ratcliffe, N. Lane, M. P. Rosenwasser, and V. C. Mow, “Mechanical and biochemical changes in the superficial zone of articular cartilage in canine experimental osteoarthritis,” J. Orthop. Res. 12(4), 474–484 (1994).
[Crossref] [PubMed]

Reddy, R.

A. Borthakur, E. M. Shapiro, J. Beers, S. Kudchodkar, J. B. Kneeland, and R. Reddy, “Sensitivity of MRI to proteoglycan depletion in cartilage: comparison of sodium and proton MRI,” Osteoarthritis Cartilage 8(4), 288–293 (2000).
[Crossref] [PubMed]

Reijman, M.

J. van Tiel, E. E. Bron, P. K. Bos, S. Klein, M. Reijman, J. A. Verhaar, G. P. Krestin, H. Weinans, G. Kotek, and E. H. Oei, “Reproducibility of 3D delayed gadolinium enhanced MRI of cartilage (DGEMRIC) of the knee at 3.0 Tesla in patients with early-stage osteoarthritis,” Osteoarthritis Cartilage 20, S230–S231 (2012).
[Crossref]

Rieppo, J.

L. Rieppo, S. Saarakkala, T. Närhi, J. Holopainen, M. Lammi, H. J. Helminen, J. S. Jurvelin, and J. Rieppo, “Quantitative analysis of spatial proteoglycan content in articular cartilage with Fourier transform infrared imaging spectroscopy: Critical evaluation of analysis methods and specificity of the parameters,” Microsc. Res. Tech. 73(5), 503–512 (2010).
[PubMed]

Rieppo, L.

L. Rieppo, S. Saarakkala, T. Närhi, J. Holopainen, M. Lammi, H. J. Helminen, J. S. Jurvelin, and J. Rieppo, “Quantitative analysis of spatial proteoglycan content in articular cartilage with Fourier transform infrared imaging spectroscopy: Critical evaluation of analysis methods and specificity of the parameters,” Microsc. Res. Tech. 73(5), 503–512 (2010).
[PubMed]

Robert, P.

Rolfe, P.

F. Faris, M. Thorniley, Y. Wickramasinghe, R. Houston, P. Rolfe, N. Livera, and A. Spencer, “Non-invasive Invivo near-Infrared Optical Measurement of the Penetration Depth in the Neonatal Head,” Clin. Phys. Physiol. Meas. 12(4), 353–358 (1991).
[Crossref] [PubMed]

Rosenberg, L.

L. Rosenberg, “Chemical basis for the histological use of safranin O in the study of articular cartilage,” J. Bone Joint Surg. Am. 53(1), 69–82 (1971).
[PubMed]

Rosenwasser, M. P.

F. Guilak, A. Ratcliffe, N. Lane, M. P. Rosenwasser, and V. C. Mow, “Mechanical and biochemical changes in the superficial zone of articular cartilage in canine experimental osteoarthritis,” J. Orthop. Res. 12(4), 474–484 (1994).
[Crossref] [PubMed]

Säämänen, A. M.

I. Kiviranta, J. Jurvelin, M. Tammi, A. M. Säämänen, and H. J. Helminen, “Microspectrophotometric quantitation of glycosaminoglycans in articular cartilage sections stained with Safranin O,” Histochemistry 82(3), 249–255 (1985).
[Crossref] [PubMed]

Saarakkala, S.

S. Saarakkala, P. Julkunen, P. Kiviranta, J. Mäkitalo, J. S. Jurvelin, and R. K. Korhonen, “Depth-wise progression of osteoarthritis in human articular cartilage: investigation of composition, structure and biomechanics,” Osteoarthritis Cartilage 18(1), 73–81 (2010).
[Crossref] [PubMed]

L. Rieppo, S. Saarakkala, T. Närhi, J. Holopainen, M. Lammi, H. J. Helminen, J. S. Jurvelin, and J. Rieppo, “Quantitative analysis of spatial proteoglycan content in articular cartilage with Fourier transform infrared imaging spectroscopy: Critical evaluation of analysis methods and specificity of the parameters,” Microsc. Res. Tech. 73(5), 503–512 (2010).
[PubMed]

Shapiro, E. M.

A. Borthakur, E. M. Shapiro, J. Beers, S. Kudchodkar, J. B. Kneeland, and R. Reddy, “Sensitivity of MRI to proteoglycan depletion in cartilage: comparison of sodium and proton MRI,” Osteoarthritis Cartilage 8(4), 288–293 (2000).
[Crossref] [PubMed]

Shrikhande, G.

Singh, S.

I. Afara, S. Singh, and A. Oloyede, “Application of near infrared (NIR) spectroscopy for determining the thickness of articular cartilage,” Med. Eng. Phys. 35(1), 88–95 (2013).
[Crossref] [PubMed]

I. Afara, S. Singh, H. Moody, and A. Oloyede, “A comparison of the histochemical and image-derived proteoglycan content of articular cartilage,” Anat. Physiol. 3, 1000120 (2013).

I. O. Afara, S. Singh, and A. Oloyede, “Load-unloading response of intact and artificially degraded articular cartilage correlated with near infrared (NIR) absorption spectra,” J. Mech. Behav. Biomed. Mater. 20, 249–258 (2013).
[Crossref] [PubMed]

Spahn, G.

G. Spahn, H. M. Klinger, M. Baums, U. Pinkepank, and G. O. Hofmann, “Reliability in arthroscopic grading of cartilage lesions: results of a prospective blinded study for evaluation of inter-observer reliability,” Arch. Orthop. Trauma Surg. 131(3), 377–381 (2011).
[Crossref] [PubMed]

J. K. Marticke, A. Hösselbarth, K. L. Hoffmeier, I. Marintschev, S. Otto, M. Lange, H. K. W. Plettenberg, G. Spahn, and G. O. Hofmann, “How do visual, spectroscopic and biomechanical changes of cartilage correlate in osteoarthritic knee joints?” Clin. Biomech. (Bristol, Avon) 25(4), 332–340 (2010).
[Crossref] [PubMed]

G. Spahn, H. M. Klinger, M. Baums, M. Hoffmann, H. Plettenberg, A. Kroker, and G. O. Hofmann, “Near-Infrared Spectroscopy for Arthroscopic Evaluation of Cartilage Lesions: Results of a Blinded, Prospective, Interobserver Study,” Am. J. Sports Med. 38(12), 2516–2521 (2010).
[Crossref] [PubMed]

G. Spahn, H. Plettenberg, H. Nagel, E. Kahl, H. M. Klinger, T. Mückley, M. Günther, G. O. Hofmann, and J. A. Mollenhauer, “Evaluation of cartilage defects with near-infrared spectroscopy (NIR): an ex vivo study,” Med. Eng. Phys. 30(3), 285–292 (2008).
[Crossref] [PubMed]

G. Spahn, H. Plettenberg, E. Kahl, H. M. Klinger, T. Mückley, and G. O. Hofmann, “Near-infrared (NIR) spectroscopy. A new method for arthroscopic evaluation of low grade degenerated cartilage lesions. Results of a pilot study,” BMC Musculoskelet. Disord. 8(1), 47 (2007).
[Crossref] [PubMed]

Spencer, A.

F. Faris, M. Thorniley, Y. Wickramasinghe, R. Houston, P. Rolfe, N. Livera, and A. Spencer, “Non-invasive Invivo near-Infrared Optical Measurement of the Penetration Depth in the Neonatal Head,” Clin. Phys. Physiol. Meas. 12(4), 353–358 (1991).
[Crossref] [PubMed]

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]

Tammi, M.

I. Kiviranta, J. Jurvelin, M. Tammi, A. M. Säämänen, and H. J. Helminen, “Microspectrophotometric quantitation of glycosaminoglycans in articular cartilage sections stained with Safranin O,” Histochemistry 82(3), 249–255 (1985).
[Crossref] [PubMed]

Thorniley, M.

F. Faris, M. Thorniley, Y. Wickramasinghe, R. Houston, P. Rolfe, N. Livera, and A. Spencer, “Non-invasive Invivo near-Infrared Optical Measurement of the Penetration Depth in the Neonatal Head,” Clin. Phys. Physiol. Meas. 12(4), 353–358 (1991).
[Crossref] [PubMed]

Tiderius, C. J.

C. J. Tiderius, L. E. Olsson, P. Leander, O. Ekberg, and L. Dahlberg, “Delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) in early knee osteoarthritis,” Magn. Reson. Med. 49(3), 488–492 (2003).
[Crossref] [PubMed]

Törrönen, K.

K. Király, T. Lapveteläinen, J. Arokoski, K. Törrönen, L. Módis, I. Kiviranta, and H. J. Helminen, “Application of selected cationic dyes for the semiquantitative estimation of glycosaminoglycans in histological sections of articular cartilage by microspectrophotometry,” Histochem. J. 28(8), 577–590 (1996).
[Crossref] [PubMed]

van Tiel, J.

J. van Tiel, E. E. Bron, P. K. Bos, S. Klein, M. Reijman, J. A. Verhaar, G. P. Krestin, H. Weinans, G. Kotek, and E. H. Oei, “Reproducibility of 3D delayed gadolinium enhanced MRI of cartilage (DGEMRIC) of the knee at 3.0 Tesla in patients with early-stage osteoarthritis,” Osteoarthritis Cartilage 20, S230–S231 (2012).
[Crossref]

Verhaar, J. A.

J. van Tiel, E. E. Bron, P. K. Bos, S. Klein, M. Reijman, J. A. Verhaar, G. P. Krestin, H. Weinans, G. Kotek, and E. H. Oei, “Reproducibility of 3D delayed gadolinium enhanced MRI of cartilage (DGEMRIC) of the knee at 3.0 Tesla in patients with early-stage osteoarthritis,” Osteoarthritis Cartilage 20, S230–S231 (2012).
[Crossref]

Weinans, H.

J. van Tiel, E. E. Bron, P. K. Bos, S. Klein, M. Reijman, J. A. Verhaar, G. P. Krestin, H. Weinans, G. Kotek, and E. H. Oei, “Reproducibility of 3D delayed gadolinium enhanced MRI of cartilage (DGEMRIC) of the knee at 3.0 Tesla in patients with early-stage osteoarthritis,” Osteoarthritis Cartilage 20, S230–S231 (2012).
[Crossref]

Wickramasinghe, Y.

F. Faris, M. Thorniley, Y. Wickramasinghe, R. Houston, P. Rolfe, N. Livera, and A. Spencer, “Non-invasive Invivo near-Infrared Optical Measurement of the Penetration Depth in the Neonatal Head,” Clin. Phys. Physiol. Meas. 12(4), 353–358 (1991).
[Crossref] [PubMed]

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]

Xiao, Y.

I. O. Afara, I. Prasadam, H. Moody, R. Crawford, Y. Xiao, and A. Oloyede, “Near infrared spectroscopy for rapid determination of Mankin score components: a potential tool for quantitative characterization of articular cartilage at surgery,” Arthroscopy 30(9), 1146–1155 (2014).
[Crossref] [PubMed]

I. O. Afara, I. Prasadam, R. Crawford, Y. Xiao, and A. Oloyede, “Near infrared (NIR) absorption spectra correlates with subchondral bone micro-CT parameters in osteoarthritic rat models,” Bone 53(2), 350–357 (2013).
[Crossref] [PubMed]

I. Afara, I. Prasadam, R. Crawford, Y. Xiao, and A. Oloyede, “Non-destructive evaluation of articular cartilage defects using near-infrared (NIR) spectroscopy in osteoarthritic rat models and its direct relation to Mankin score,” Osteoarthritis Cartilage 20(11), 1367–1373 (2012).
[Crossref] [PubMed]

Yang, X.

X. Bi, X. Yang, M. P. G. Bostrom, and N. P. Camacho, “Fourier transform infrared imaging spectroscopy investigations in the pathogenesis and repair of cartilage,” Biochim. Biophys. Acta 1758(7), 934–941 (2006).
[Crossref] [PubMed]

Am. J. Sports Med. (1)

G. Spahn, H. M. Klinger, M. Baums, M. Hoffmann, H. Plettenberg, A. Kroker, and G. O. Hofmann, “Near-Infrared Spectroscopy for Arthroscopic Evaluation of Cartilage Lesions: Results of a Blinded, Prospective, Interobserver Study,” Am. J. Sports Med. 38(12), 2516–2521 (2010).
[Crossref] [PubMed]

Anat. Physiol. (1)

I. Afara, S. Singh, H. Moody, and A. Oloyede, “A comparison of the histochemical and image-derived proteoglycan content of articular cartilage,” Anat. Physiol. 3, 1000120 (2013).

Appl. Spectrosc. (2)

Arch. Orthop. Trauma Surg. (1)

G. Spahn, H. M. Klinger, M. Baums, U. Pinkepank, and G. O. Hofmann, “Reliability in arthroscopic grading of cartilage lesions: results of a prospective blinded study for evaluation of inter-observer reliability,” Arch. Orthop. Trauma Surg. 131(3), 377–381 (2011).
[Crossref] [PubMed]

Arthroscopy (1)

I. O. Afara, I. Prasadam, H. Moody, R. Crawford, Y. Xiao, and A. Oloyede, “Near infrared spectroscopy for rapid determination of Mankin score components: a potential tool for quantitative characterization of articular cartilage at surgery,” Arthroscopy 30(9), 1146–1155 (2014).
[Crossref] [PubMed]

Biochim. Biophys. Acta (1)

X. Bi, X. Yang, M. P. G. Bostrom, and N. P. Camacho, “Fourier transform infrared imaging spectroscopy investigations in the pathogenesis and repair of cartilage,” Biochim. Biophys. Acta 1758(7), 934–941 (2006).
[Crossref] [PubMed]

Biomed. Opt. Express (1)

BMC Musculoskelet. Disord. (1)

G. Spahn, H. Plettenberg, E. Kahl, H. M. Klinger, T. Mückley, and G. O. Hofmann, “Near-infrared (NIR) spectroscopy. A new method for arthroscopic evaluation of low grade degenerated cartilage lesions. Results of a pilot study,” BMC Musculoskelet. Disord. 8(1), 47 (2007).
[Crossref] [PubMed]

Bone (1)

I. O. Afara, I. Prasadam, R. Crawford, Y. Xiao, and A. Oloyede, “Near infrared (NIR) absorption spectra correlates with subchondral bone micro-CT parameters in osteoarthritic rat models,” Bone 53(2), 350–357 (2013).
[Crossref] [PubMed]

Clin. Biomech. (Bristol, Avon) (2)

J. K. Marticke, A. Hösselbarth, K. L. Hoffmeier, I. Marintschev, S. Otto, M. Lange, H. K. W. Plettenberg, G. Spahn, and G. O. Hofmann, “How do visual, spectroscopic and biomechanical changes of cartilage correlate in osteoarthritic knee joints?” Clin. Biomech. (Bristol, Avon) 25(4), 332–340 (2010).
[Crossref] [PubMed]

C. P. Brown, R. W. Crawford, and A. Oloyede, “Indentation stiffness does not discriminate between normal and degraded articular cartilage,” Clin. Biomech. (Bristol, Avon) 22(7), 843–848 (2007).
[Crossref] [PubMed]

Clin. Phys. Physiol. Meas. (1)

F. Faris, M. Thorniley, Y. Wickramasinghe, R. Houston, P. Rolfe, N. Livera, and A. Spencer, “Non-invasive Invivo near-Infrared Optical Measurement of the Penetration Depth in the Neonatal Head,” Clin. Phys. Physiol. Meas. 12(4), 353–358 (1991).
[Crossref] [PubMed]

Histochem. J. (1)

K. Király, T. Lapveteläinen, J. Arokoski, K. Törrönen, L. Módis, I. Kiviranta, and H. J. Helminen, “Application of selected cationic dyes for the semiquantitative estimation of glycosaminoglycans in histological sections of articular cartilage by microspectrophotometry,” Histochem. J. 28(8), 577–590 (1996).
[Crossref] [PubMed]

Histochemistry (1)

I. Kiviranta, J. Jurvelin, M. Tammi, A. M. Säämänen, and H. J. Helminen, “Microspectrophotometric quantitation of glycosaminoglycans in articular cartilage sections stained with Safranin O,” Histochemistry 82(3), 249–255 (1985).
[Crossref] [PubMed]

J. Anat. (1)

H. R. Moody, C. P. Brown, J. C. Bowden, R. W. Crawford, D. L. S. McElwain, and A. O. Oloyede, “In vitro degradation of articular cartilage: does trypsin treatment produce consistent results?” J. Anat. 209(2), 259–267 (2006).
[Crossref] [PubMed]

J. Bone Joint Surg. Am. (1)

L. Rosenberg, “Chemical basis for the histological use of safranin O in the study of articular cartilage,” J. Bone Joint Surg. Am. 53(1), 69–82 (1971).
[PubMed]

J. Bone Joint Surg. Br. (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]

J. Bone Jt. Surg. (1)

J. A. Buckwalter and H. J. Mankin, “Articular Cartilage: Degeneration and Osteoarthrosis, Repair, Regeneration, and Transplantation,” J. Bone Jt. Surg. 47, 612–632 (1998).

J. Mater. Sci. Eng. A (1)

I. O. Afara, Z. Pawlak, and A. Oloyede, “Current State of the Application of Infrared Optical Methods for Assessing Articular Cartilage,” J. Mater. Sci. Eng. A 1, 1–7 (2011).

J. Mech. Behav. Biomed. Mater. (1)

I. O. Afara, S. Singh, and A. Oloyede, “Load-unloading response of intact and artificially degraded articular cartilage correlated with near infrared (NIR) absorption spectra,” J. Mech. Behav. Biomed. Mater. 20, 249–258 (2013).
[Crossref] [PubMed]

J. Orthop. Res. (1)

F. Guilak, A. Ratcliffe, N. Lane, M. P. Rosenwasser, and V. C. Mow, “Mechanical and biochemical changes in the superficial zone of articular cartilage in canine experimental osteoarthritis,” J. Orthop. Res. 12(4), 474–484 (1994).
[Crossref] [PubMed]

Magn. Reson. Med. (1)

C. J. Tiderius, L. E. Olsson, P. Leander, O. Ekberg, and L. Dahlberg, “Delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) in early knee osteoarthritis,” Magn. Reson. Med. 49(3), 488–492 (2003).
[Crossref] [PubMed]

Med. Eng. Phys. (2)

I. Afara, S. Singh, and A. Oloyede, “Application of near infrared (NIR) spectroscopy for determining the thickness of articular cartilage,” Med. Eng. Phys. 35(1), 88–95 (2013).
[Crossref] [PubMed]

G. Spahn, H. Plettenberg, H. Nagel, E. Kahl, H. M. Klinger, T. Mückley, M. Günther, G. O. Hofmann, and J. A. Mollenhauer, “Evaluation of cartilage defects with near-infrared spectroscopy (NIR): an ex vivo study,” Med. Eng. Phys. 30(3), 285–292 (2008).
[Crossref] [PubMed]

Microsc. Res. Tech. (1)

L. Rieppo, S. Saarakkala, T. Närhi, J. Holopainen, M. Lammi, H. J. Helminen, J. S. Jurvelin, and J. Rieppo, “Quantitative analysis of spatial proteoglycan content in articular cartilage with Fourier transform infrared imaging spectroscopy: Critical evaluation of analysis methods and specificity of the parameters,” Microsc. Res. Tech. 73(5), 503–512 (2010).
[PubMed]

Osteoarthritis Cartilage (5)

I. Afara, I. Prasadam, R. Crawford, Y. Xiao, and A. Oloyede, “Non-destructive evaluation of articular cartilage defects using near-infrared (NIR) spectroscopy in osteoarthritic rat models and its direct relation to Mankin score,” Osteoarthritis Cartilage 20(11), 1367–1373 (2012).
[Crossref] [PubMed]

J. van Tiel, E. E. Bron, P. K. Bos, S. Klein, M. Reijman, J. A. Verhaar, G. P. Krestin, H. Weinans, G. Kotek, and E. H. Oei, “Reproducibility of 3D delayed gadolinium enhanced MRI of cartilage (DGEMRIC) of the knee at 3.0 Tesla in patients with early-stage osteoarthritis,” Osteoarthritis Cartilage 20, S230–S231 (2012).
[Crossref]

A. Borthakur, E. M. Shapiro, J. Beers, S. Kudchodkar, J. B. Kneeland, and R. Reddy, “Sensitivity of MRI to proteoglycan depletion in cartilage: comparison of sodium and proton MRI,” Osteoarthritis Cartilage 8(4), 288–293 (2000).
[Crossref] [PubMed]

E. B. Hunziker, “Articular cartilage repair: basic science and clinical progress. A review of the current status and prospects,” Osteoarthritis Cartilage 10(6), 432–463 (2002).
[Crossref] [PubMed]

S. Saarakkala, P. Julkunen, P. Kiviranta, J. Mäkitalo, J. S. Jurvelin, and R. K. Korhonen, “Depth-wise progression of osteoarthritis in human articular cartilage: investigation of composition, structure and biomechanics,” Osteoarthritis Cartilage 18(1), 73–81 (2010).
[Crossref] [PubMed]

Other (2)

H.-R. Bjørsvik and H. Martens, “Data analysis: Calibration of NIR instruments by PLS regression,” in Handbook of Near Infrared Analysis, A. D. Burns and E. W. Ciurczak, eds., 2nd ed. (Marcell Dekker, Inc., 2001).

C. Kradjel, “NIR analysis of polymers,” in Handbook of Near Infrared Analysis, A. D. Burns and E. W. Ciurczak, eds., 2nd ed. (Marcel Dekker, Inc., 2001).

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Figures (5)

Fig. 1
Fig. 1 Study protocol flow diagram
Fig. 2
Fig. 2 (A) Typical absorbance-depth profiles of safranin-O stained cartilage sections showing proteoglycan loss in cartilage samples, and (B) representative near infrared absorption spectra (offset corrected) for (a) group 0, (b) group 1, (c) group 2, (d) group 3, and (e) group 4.
Fig. 3
Fig. 3 Scores plot of the 1st and 2nd principal components of near infrared (NIR) spectral data showing classification of articular cartilage samples into distinct groups based on their PG content grade. Ellipse shows sub-group within class 2.
Fig. 4
Fig. 4 Partial least squares calibration (a) and validation (b) plots for correlation between near infrared (NIR) spectral data and PG content for normal and artificially degraded cartilage samples. Agreement between AS1 and AS2 grading results (c), and validation of NIR-predicted PG content data against results of AS2 (d).
Fig. 5
Fig. 5 (a) Image of bovine patella with focal defect. (b) Raw (low-resolution) image of PG distribution across sample. (c) Smoothed (bilinear interpolated) image showing distribution of percentage PG loss across sample.

Tables (2)

Tables Icon

Table 1 PG content based on depth loss of Safranin-O stain on histological sections

Tables Icon

Table 2 Assessment statistics of articular cartilage NIR to PG content grade correlation based on specific regions of the spectrum with and without pre-processing. RMSECV = root mean square error of cross-validation [† indicates the region comprising the water peak of articular cartilage]

Metrics