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Ultra-high field diffusion tensor imaging of articular cartilage correlated with histology and scanning electron microscopy

  • José G. Raya
  • Andreas P. Arnoldi
  • Daniel L. Weber
  • Lucianna Filidoro
  • Olaf Dietrich
  • Silvia Adam-Neumair
  • Elisabeth Mützel
  • Gerd Melkus
  • Reinhard Putz
  • Maximilian F. Reiser
  • Peter M. Jakob
  • Christian Glaser
Research Article

Abstract

Object

To investigate the relationship of the different diffusion tensor imaging (DTI) parameters (ADC, FA, and first eigenvector (EV)) to the constituents (proteoglycans and collagen), the zonal arrangement of the collagen network, and mechanical loading of articular cartilage.

Material and methods

DTI of eight cartilage-on-bone samples of healthy human patellar cartilage was performed at 17.6 T. Three samples were additionally imaged under indentation loading. After DTI, samples underwent biomechanical testing, safranin-O staining for semiquantitative proteoglycan estimation, and scanning electron microscopy (SEM) for depicting collagen architecture.

Results

From the articular surface to the bone–cartilage interface, ADC continuously decreased and FA increased. Cartilage zonal heights calculated from EVs strongly correlated with SEM-derived zonal heights (P < 0.01, r 2=0.87). Compression reduced ADC in the superficial 30% of cartilage and increased FA in the superficial 5% of cartilage. Reorientation of the EVs indicative of collagen fiber reorientation under the indenter was observed. No significant correlation was found between ADC, FA, and compressive stiffness.

Conclusions

Correlating ADC and FA with proteoglycan and collagen content suggests that diffusion is dominated by different depth-dependent mechanisms within cartilage. Knowledge of the spatial distribution of the DTI parameters and their variation contributes to form a database for future analysis of defective cartilage.

Keywords

Cartilage DTI Histology SEM Biomechanics Safranin-O 

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References

  1. 1.
    Buckwalter JA, Mankin HJ (1997) Articular cartilage, part II. J Bone Joint Surg Am 79(5): 612–632Google Scholar
  2. 2.
    Burstein D, Gray ML, Hartman AL, Gipe R, Foy BD (1993) Diffusion of small solutes in cartilage as measured by nuclear magnetic resonance (NMR) spectroscopy and imaging. J Orthop Res 11(4): 465–478PubMedCrossRefGoogle Scholar
  3. 3.
    Xia Y (2000) Magic-angle effect in magnetic resonance imaging of articular cartilage: a review. Invest Radiol 35(10): 602–621PubMedCrossRefGoogle Scholar
  4. 4.
    Borthakur A, Mellon E, Niyogi S, Witschey W, Kneeland JB, Reddy R (2006) Sodium and T1rho MRI for molecular and diagnostic imaging of articular cartilage. NMR Biomed 19(7): 781–821PubMedCrossRefGoogle Scholar
  5. 5.
    Gray ML, Burstein D, Kim YJ, Maroudas A (2007) 2007 Elizabeth Winston Lanier award winner. Magnetic resonance imaging of cartilage glycosaminoglycan: basic principles, imaging technique, and clinical applications. J Orthop Res 26(3): 281–291CrossRefGoogle Scholar
  6. 6.
    Filidoro L, Dietrich O, Weber J, Rauch E, Filidoro L, Dietrich O, Oerther T, Wick M, Reiser MF, Glaser C (2005) High-resolution diffusion tensor imaging of human patellar cartilage: feasibility and preliminary findings. Magn Reson Med 53(5): 993–998PubMedCrossRefGoogle Scholar
  7. 7.
    de Visser SK, Bowden JC, Wentrup-Byrne E, Rintoul L, Bostrom T, Pope JM, Momot KI (2008) Anisotropy of collagen fibre alignment in bovine cartilage: comparison of polarised light microscopy and spatially resolved diffusion-tensor measurements. Osteoarthritis Cartilage 16(6): 689–697PubMedCrossRefGoogle Scholar
  8. 8.
    Xia Y, Farquhar T, Burton-Wurster N, Vernier-Singer M, Lust G, Jelinski LW (1995) Self-diffusion monitors degraded cartilage. Arch Biochem Biophys 323(2): 323–328PubMedCrossRefGoogle Scholar
  9. 9.
    Knauss R, Schiller J, Fleischer G, Karger JKnauss R, Schiller J, Fleischer G, Karger J, Arnold K (1999) Self-diffusion of water in cartilage and cartilage components as studied by pulsed field gradient NMR . Magn Reson Med 41(2): 285–292PubMedCrossRefGoogle Scholar
  10. 10.
    Meder R, de Visser SK, Bowden JC, Bostrom T, Pope JM (2006) Diffusion tensor imaging of articular cartilage as a measure of tissue microstructure. Osteoarthritis Cartilage 14(9): 875–881PubMedCrossRefGoogle Scholar
  11. 11.
    Deng X, Farley M, Nieminen MT, Gray M, Burstein D (2007) Diffusion tensor imaging of native and degenerated human articular cartilage. Magn Reson Imaging 25(2): 168–171PubMedCrossRefGoogle Scholar
  12. 12.
    Raya GJ, Melkus G, Adam-Neumair S, Dietrich O, Mützel E, Kahr B, Reiser MF, Jakob PM, Putz R, Glaser C (2011) Invest Radiol 46(6):401–409Google Scholar
  13. 13.
    de Visser SK, Crawford RW, Pope JM (2008) Structural adaptations in compressed articular cartilage measured by diffusion tensor imaging. Osteoarthritis Cartilage 16(1): 83–89PubMedCrossRefGoogle Scholar
  14. 14.
    Raya JG, Melkus G, Dietrich O, Mützel E, Reiser MF, Jackob PM, Glaser C (2010) In: Proceedings of the meeting of the international society of magnetic resonance in the medicine, Montréal, CanadaGoogle Scholar
  15. 15.
    Conturo TE, McKinstry RC, Akbudak E, Robinson BH (1996) Encoding of anisotropic diffusion with tetrahedral gradients: a general mathematical diffusion formalism and experimental results. Magn Reson Med 35(3): 399–412PubMedCrossRefGoogle Scholar
  16. 16.
    Glaser C, Putz R (2002) Functional anatomy of articular cartilage under compressive loading: Quantitative aspects of global, local and zonal reactions of the collagenous network with respect to the surface integrity. Osteoarthritis Cartilage 10(2): 83–99PubMedCrossRefGoogle Scholar
  17. 17.
    Damon BM (2008) Effects of image noise in muscle diffusion tensor (DT)-MRI assessed using numerical simulations. Magn Reon Med 60(4): 934–944CrossRefGoogle Scholar
  18. 18.
    Hayes WC, Keer LM, Herrmann G, Mockros LF (1972) A mathematical analysis for indentation tests of articular cartilage. J Biomech 5(5): 541–551PubMedCrossRefGoogle Scholar
  19. 19.
    Korhonen RK, Laasanen MS, Toyras J, Rieppo J, Hirvonen J, Helminen HJ, Jurvelin JS (2002) Comparison of the equilibrium response of articular cartilage in unconfined compression, confined compression and indentation. J Biomech 35(7): 903–909PubMedCrossRefGoogle Scholar
  20. 20.
    Shimizu C, Coutts RD, Healey RM, Kubo T, Hirasawa Y, Amiel D (1997) Method of histomorphometric assessment of glycosaminoglycans in articular cartilage. J Orthop Res 15(5): 670–674PubMedCrossRefGoogle Scholar
  21. 21.
    Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1(8476): 307–310PubMedCrossRefGoogle Scholar
  22. 22.
    Maroudas A, Venn M (1977) Chemical composition and swelling of normal and osteoarthrotic femoral head cartilage. II. Swelling. Ann Rheum Dis 36(5): 399–406PubMedCrossRefGoogle Scholar
  23. 23.
    Henkelman RM, Stanisz GJ, Kim JK, Bronskill MJ (1994) Anisotropy of NMR properties of tissues. Magn Reson Med 32(5): 592–601PubMedCrossRefGoogle Scholar
  24. 24.
    Kääb MJ, Ito K, Clark JM, Nötzli HP (2000) The acute structural changes of loaded articular cartilage following meniscectomy or ACL-transection. Osteoarthritis Cartilage 8(6): 464–473PubMedCrossRefGoogle Scholar
  25. 25.
    Clark JM, Norman A, Noetzli H (1997) Postnatal development of the collagen matrix in rabbit tibial plateau cartilage. J Anat 191(4): 215–227PubMedCrossRefGoogle Scholar
  26. 26.
    Keinan-Adamsky K, Shinar H, Navon G (2006) Multinuclear NMR and MRI studies of the maturation of pig articular cartilage. Magn Reson Med 55(3): 532–540PubMedCrossRefGoogle Scholar
  27. 27.
    Kiviranta I, Jurvelin J, Tammi M, Saamanen AM, Helminen HJ (1985) Microspectrophotometric quantitation of glycosaminoglycans in articular cartilage sections stained with Safranin O . Histochemistry 82(3): 249–255PubMedCrossRefGoogle Scholar
  28. 28.
    Venn MF (1978) Variation of chemical composition with age in human femoral head cartilage. Ann Rheum Dis 37(2): 168– 174PubMedCrossRefGoogle Scholar
  29. 29.
    Bayliss MT, Venn M, Maroudas A, Ali SY (1983) Structure of proteoglycans from different layers of human articular cartilage. Biochem J 209(2): 387–400PubMedGoogle Scholar
  30. 30.
    Wayne JS, Kraft KA, Shields KJ, Yin C, Owen JR, Disler DG (2003) MR imaging of normal and matrix-depleted cartilage: correlation with biomechanical function and biochemical composition. Radiology 228(2): 493–499PubMedCrossRefGoogle Scholar
  31. 31.
    Nissi MJ, Rieppo J, Töyräs J, Laasanen MS, Kiviranta I, Nieminen MT, Jurvelin JS (2007) Estimation of mechanical properties of articular cartilage with MRI - dGEMRIC, T2 and T1 imaging in different species with variable stages of maturation. Osteoarthritis Cartilage 15(10): 1141–1148PubMedCrossRefGoogle Scholar
  32. 32.
    Lammentausta E, Kiviranta P, Nissi MJ, Laasanen MS, Kiviranta I, Nieminen MT, Jurvelin JS (2006) T2 relaxation time and delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) of human patellar cartilage at 1.5 T and 9.4 T: Relationships with tissue mechanical properties. J Orthop Res 24(3): 366–374PubMedCrossRefGoogle Scholar
  33. 33.
    Kurkijärvi JE, Nissi MJ, Rieppo J, Töyräs J, Kiviranta I, Nieminen MT, Jurvelin JS (2008) The zonal architecture of human articular cartilage described by T2 relaxation time in the presence of Gd-DTPA2-. Magn Reson Imaging 26(5): 602–607PubMedCrossRefGoogle Scholar
  34. 34.
    Baldassarri M, Goodwin JS, Farley ML, Bierbaum BE, Goldring SR, Goldring MB, Burstein D, Gray ML (2007) Relationship between cartilage stiffness and dGEMRIC index: correlation and prediction. J Orthop Res 25(7): 904–912PubMedCrossRefGoogle Scholar
  35. 35.
    Muir H, Bullough P, Maroudas A (1970) The distribution of collagen in human articular cartilage with some of its physiological implications. J Bone Joint Surg Br 52: 554–563PubMedGoogle Scholar
  36. 36.
    Venn MF, Maroudas A (1977) Chemical composition and swelling of normal and osteoarthrotic femoral head cartilage. I. Chemical composition. Ann Rheum Dis 36(2): 121–129PubMedCrossRefGoogle Scholar
  37. 37.
    Maroudas A, Bayliss MT, Venn MF (1980) Further studies on the composition of human femoral head cartilage. Ann Rheum Dis 39(5): 514–523PubMedCrossRefGoogle Scholar
  38. 38.
    Shinar H, Navon G (2006) Multinuclear NMR and microscopic MRI studies of the articular cartilage nanostructure. NMR Biomed 19(7): 877–893PubMedCrossRefGoogle Scholar
  39. 39.
    Azuma T, Nakai R, Takizawa O, Tsutsumi S (2009) In vivo structural analysis of articular cartilage using diffusion tensor magnetic resonance imaging. Magn Reson Imaging 27(9): 1242–1248PubMedCrossRefGoogle Scholar
  40. 40.
    Raya JG, Horng A, Dietrich O, Krasnokutsky S, Beltran LS, Reiser M, Recht M, Glaser C (2010) In vivo DTI of articular cartilage: a new set of biomarkers for the early diagnosis of osteoarthritis in vivo. In: Proceedings of the meeting of the international society of magnetic resonance in the medicine, Montréal, Canada, Abstract no. 501Google Scholar

Copyright information

© ESMRMB 2011

Authors and Affiliations

  • José G. Raya
    • 1
  • Andreas P. Arnoldi
    • 2
  • Daniel L. Weber
    • 3
  • Lucianna Filidoro
    • 4
  • Olaf Dietrich
    • 4
  • Silvia Adam-Neumair
    • 2
  • Elisabeth Mützel
    • 5
  • Gerd Melkus
    • 3
  • Reinhard Putz
    • 6
  • Maximilian F. Reiser
    • 2
    • 4
  • Peter M. Jakob
    • 3
  • Christian Glaser
    • 1
    • 2
  1. 1.Department of RadiologyNew York University Langone Medical Center, Center of Biomedical ImagingNew YorkUSA
  2. 2.Department of Clinical Radiology—GroßhadernLudwig Maximilian University of MunichMunichGermany
  3. 3.Department of Experimental Physics VUniversity of WürzburgWürzburgGermany
  4. 4.Josef Lissner Laboratory for Biomedical Imaging, Department of Clinical Radiology—GroßhadernLudwig Maximilian University of MunichMunichGermany
  5. 5.Department of Forensic MedicineLudwig Maximilian University of MunichMunichGermany
  6. 6.Department of AnatomyLudwig Maximilian University of MunichMunichGermany

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