Articular cartilage (AC) is an aneural and avascular tissue that covers the ends of articulating bones in diarthrodial joints, and its main functions are to distribute joint loading and to provide nearly frictionless movement of the articulating bones. The mechanical properties of AC can be attribute to the complex structure of its extracellular matrix (ECM), mainly composed by collagen fibres, proteoglycan (PG) aggregates and interstitial water [1, 2]. Nowadays, the progression of mean expectation of life has highlighted the importance of a correct diagnosis for many age-related diseases. In AC, aging process occur in older age with cellular senescence [3, 4] and ECM modifications [5, 6], frequently involving in Osteoarthritic diseases [7–9]. Osteoarthritis (OA) is the most common degenerative joint disease and represent one of the most common disabilities cause (6,6% of Italian population, actually), posing a high economical burden to society. OA is characterized by the proceeding destruction of AC by uncontrolled proteolysis of ECM and typically leads to a remodeling of affected joints. No treatment neither early diagnosis method currently exist for OA pathologies, and the detection of differences and relations between early OA and aging is still an open field in clinical research [3, 8, 10]. To understand the progression of the disease, the comprehension of mechanisms involving on to ECM components during AC degradation is essential. The reduction of PGs concentration is recognized as the first symptom of degeneration in OA [11–14], while collagen fibers result more resistant from degradation. Using different experimental techniques, it is possible to observe the contribution of degradation of a specific macromolecule to the AC disease progression. Dielectric Spectroscopy (DS) resulted as an indirect indicator of collagen fibrils integrity through observation of intermolecular hydrogen bounds formation between water molecules [15]. Moreover, some water molecules result oriented along collagen fibers and that orientation is well recognized by Magnetic Resonance T2 -weighted imaging (T2w-MRI) contrast variations through intra-molecular dipole interactions of water hydrogen nuclei[16-18]. The study of the dynamic of water molecules in cartilage resulted to provide information on cartilage structure [19-21]. Diffusion Tensor Imaging (DTI) [22-26] is a widely used Magnetic Resonance technique to investigate fiber microstructures in human brain, like in skeletal muscle tissue [27]. Moreover, some authors [20, 28, 29] have demonstrated that DTI technique can recognise collagen fibril orientation and other authors [20, 30, 31] have shown how the reduction of proteoglycan content in cartilage affect water Apparent Diffusion Coefficient (ADC). For all the cartilage futures listed so far, and taking into account the potentiality provided by DTI investigations, here we monitored cartilage aging by means of DTI and T2 -weighted imaging techniques. Specifically, starting to the observation that in cartilage is generally observed a reduction in water content during aging [32], we investigate in vitro cartilage samples during natural dehydration process. Moreover, we combined NMR with DS measurements to deeply investigate structural variation in cartilage matrix. [1] Zernia, G. 2006. Collagen dynamics in articular cartilage under osmotic pressure. NMR Biomed. 19:1010-1019. [2] Newman, A.P. 1998. Articular cartilage repair. Am. J. Sports. Med. 26:309-324. [3] R. F. Loeser. Aging and osteoarthritis. Curr. Op. Rheum.,(23), 492 (2011). [4] H. Muir. The chondrocyte, architect of cartilage. biomechanics,structure, function and molecular biology of cartilage matrix macromolecules. Bioessays, (17), 1039 (1995). [5] E. Wachtel, A. Maroudas and R. Schneiderman. Age-related changes in collagen packing of human articular cartilage. Bioch. Bioph. Acta, (1243), 239 (1995). [6] J. Dudhia. Aggrecan, aging and assembly in articular cartilage.Cellular and Molecular Life Sciences, (62), 2241 (2005). [7] M. B. Goldring and S. R. Goldring. Osteoarthritis. J. Cell. Physiol., (213), 626 (2007). [8] D. Umlauf, S. Frank, T. Pap and J. Bertrand. Cartilage biology, pathology, and repair. Cellular and Molecular Life Sciences,(67), 41974211 (2010). [9] F. Eckstein, M. Kunzy, M. Schutzery, M. Hudelmaier, R. D.Jackson, J. Yu, C. B. Eaton and E. Schneider. Two year longitudinal change and teste-retest-precision of knee cartilage morphology in a pilot study for the osteoarthritis initiative. OsteoArthritis and Cartilage, (15), 1326 (2007). [10] M. Beekhuizen, Y. M. Bastiaansen-Jenniskens, W. Koevoet,D. B. F. Saris, W. J. A. Dhert, L. B. Creemers and G. J. V. M.van Osch. Osteoarthritic synovial tissue inhibition of proteoglycan production in human osteoarthritic knee cartilage. Arth.& Rheum., (63), 1918 (2011). [11] H. J. Mankin, H. Dorfman, L. Lippiello and L. Zarins. Biochemical and metabolic abnormalities in articular cartilage from osteoarthritic human hips. ii: Correlation of morphology with biochemical and metabolic data. J. Bone Joint. Surg. Am., (53), 523 (1971). [12] A. A. V. de Loo, O. Arntz, I. Otterness and W. V. den Berg. Proteoglycan loss and subsequent replenishment in articularcartilage after a mild arthritic insult by il-1 in mice: impaired proteoglycan turnover in the recovery phase. Ag. Act., (41), 200 (1994). [13] G. Grushko, R. Schneiderman and A. Maroudas. Some bichemical and biophysical parameters for the study of the pathogenesis of osteoarthritis: comparison between the processes of aging and degeneration in human hip cartilage. Conn. Tiss. Res., (19), 149 (1989). [14] J. Degroot, N. Verzijl, R. Bank, F. P. J. Lafeber, J. W. J. Bijlsma and J. Tekoppele. Age-related decrease in proteoglycan syntesis of human articular chondrocytes. Arth. Reum., (42), 1003 (1999). [15] J. R. Grigera, F. Vericat, K. Hallenga and H. Berendsen. Dielectric properties of hydrated collagen. Biopol., (18), 35 (1979). [16] Akella, S.V.S., R.R. Regatte, A.J. Wheaton, A. Borthakur, and R. Reddy. 2004. Reduction of Residual Dipolar Interaction in Cartilage by Spin-Lock Technique. Magn. Res. Med. 52:1103-1109. [17] Migchelsen, C. and H.J.C. Berendsen. 1973. Proton exchange and molecular orientation of water in hydrated collagen fibers. J.Chem.Phys. 59(1):296-305. [18] Shinar, H., and G. Navon. 2006. Multinuclear NMR and Microscopic MRI studies of articular cartilage nanostructure. NMR Biomed.19:877-893. [19] Filidoro, L., O. Dietrich, J. Weber, E. Rauch, T. Oerther, M. Wick, M.F. Reiser, and C. Glaser. 2005. High-Resolution DTI of human patellar cartilage: feasibility and preliminary findings. Magn. Res. Med. 53:993-998. [20] Raya, J.G., Melkus, G., Adam-Neumair, S., Dietrich, O., Mutzel, E., Kahr, B., Reiser, M.F., Jakob, P.M., Putz, R. and C. Glaser. 2011. Change of diffusion tensor imaging parameters in articular cartilage with progressive proteoglycan extraction. Invest. Radiol. 46:401-409. [21] Azuma, T., Nakai, R., Takizawa O. and S. Tsutsumi. 2009. In vivo structural analysis of articular cartilage using diffusion tensor magnetic resonance imaging. Magn. Res. Im. 27:1242-1248. [22] Basser, P.J., and C. Pierpaoli. 1996. Microstructural and Physiological Features of Tissues elucidated by Quantitative-Diffusion-Tensor MRI. J.Magn.Res. 111:209-219. [23] Pierpaoli, C., P. Jezzard, P.J. Basser, J. Barnett , and G. Di Chiro. 1996. Diffusion tensor MR imaging of the human brain. Radiol. 201:637-648. [24] Basser, P.J., J. Mattiello, and D. LeBihan. 1994. MR Diffusion Tensor Spectroscopy and Imaging. Bioph. J. 66:259-267. [25] Le Bihan, D. 1991. Molecular diffusion nuclear magnetic resonance imaging. Magn. Res. Quart. 7:1-30. [26] Basser, P.J., and D.K. Jones. 2002. Diffusion-Tensor MRI. NMR Biomed. 15:456 -467. [27] Napadow, V.J., V. Q. Chen, V. Mai, P.T.C. So, and R. J. Gilbert. 2001. Quantitative Analysis of Three-Dimensional-Resolved Fiber Architecture in Heterogeneous Skeletal Muscle Tissue Using NMR and Optical Imaging Methods. Bioph. J. 80:2968-2975. [28] De Visser, S.K., J. C. Bowden, E. Wentrup-Byrne, L. Rintoul, T. Bostrom, J. M. Pope D and K. I. Momot. 2008. Anisotropy of collagen fibre alignment in bovine cartilage: comparison of polarised light microscopy and spatially resolved diffusion-tensor measurements. Ost. and Cart.16: 689-697. [29] Pierce, D.M., Trobin W., Raya J.G., Trattnig S., Bishof H., Glaser C. and G.A. Holzapfeli. 2010. DT-MRI based computation of collagen fiber deformation in human articular cartilage: a feasibility study. Ann. Biom. Eng. 38:2447–2463. [30] Meder, R., S. K. de Visser, J. C. Bowden, T. Bostrom, and J. M. Pope. 2006. Diffusion tensor imaging of articular cartilage as a measure of tissue microstructure Ost. and Cart. 14, 875-881. [31] Othman, S.F., Williams, J.M., Sumner, D.R. and R.L. Magin. 2004. MRI heterogeneity of articular cartilage in strong magnetic field: dependence on proteoglycan content. Magn. Res. Eng. 23B(1):33-43. [32] Venn, M. F. 1978. Variation of chemical composition with age in human femoral head cartilage. Ann. Rheum. Dis. 37:168-174.
Investigation of cartlilage aging by means of MRI, DTI and DS techniques / Gruber, CESARE ERNESTO MARIA. - (2012 Mar 02).
Investigation of cartlilage aging by means of MRI, DTI and DS techniques
GRUBER, CESARE ERNESTO MARIA
02/03/2012
Abstract
Articular cartilage (AC) is an aneural and avascular tissue that covers the ends of articulating bones in diarthrodial joints, and its main functions are to distribute joint loading and to provide nearly frictionless movement of the articulating bones. The mechanical properties of AC can be attribute to the complex structure of its extracellular matrix (ECM), mainly composed by collagen fibres, proteoglycan (PG) aggregates and interstitial water [1, 2]. Nowadays, the progression of mean expectation of life has highlighted the importance of a correct diagnosis for many age-related diseases. In AC, aging process occur in older age with cellular senescence [3, 4] and ECM modifications [5, 6], frequently involving in Osteoarthritic diseases [7–9]. Osteoarthritis (OA) is the most common degenerative joint disease and represent one of the most common disabilities cause (6,6% of Italian population, actually), posing a high economical burden to society. OA is characterized by the proceeding destruction of AC by uncontrolled proteolysis of ECM and typically leads to a remodeling of affected joints. No treatment neither early diagnosis method currently exist for OA pathologies, and the detection of differences and relations between early OA and aging is still an open field in clinical research [3, 8, 10]. To understand the progression of the disease, the comprehension of mechanisms involving on to ECM components during AC degradation is essential. The reduction of PGs concentration is recognized as the first symptom of degeneration in OA [11–14], while collagen fibers result more resistant from degradation. Using different experimental techniques, it is possible to observe the contribution of degradation of a specific macromolecule to the AC disease progression. Dielectric Spectroscopy (DS) resulted as an indirect indicator of collagen fibrils integrity through observation of intermolecular hydrogen bounds formation between water molecules [15]. Moreover, some water molecules result oriented along collagen fibers and that orientation is well recognized by Magnetic Resonance T2 -weighted imaging (T2w-MRI) contrast variations through intra-molecular dipole interactions of water hydrogen nuclei[16-18]. The study of the dynamic of water molecules in cartilage resulted to provide information on cartilage structure [19-21]. Diffusion Tensor Imaging (DTI) [22-26] is a widely used Magnetic Resonance technique to investigate fiber microstructures in human brain, like in skeletal muscle tissue [27]. Moreover, some authors [20, 28, 29] have demonstrated that DTI technique can recognise collagen fibril orientation and other authors [20, 30, 31] have shown how the reduction of proteoglycan content in cartilage affect water Apparent Diffusion Coefficient (ADC). For all the cartilage futures listed so far, and taking into account the potentiality provided by DTI investigations, here we monitored cartilage aging by means of DTI and T2 -weighted imaging techniques. Specifically, starting to the observation that in cartilage is generally observed a reduction in water content during aging [32], we investigate in vitro cartilage samples during natural dehydration process. Moreover, we combined NMR with DS measurements to deeply investigate structural variation in cartilage matrix. [1] Zernia, G. 2006. Collagen dynamics in articular cartilage under osmotic pressure. NMR Biomed. 19:1010-1019. [2] Newman, A.P. 1998. Articular cartilage repair. Am. J. Sports. Med. 26:309-324. [3] R. F. Loeser. Aging and osteoarthritis. Curr. Op. Rheum.,(23), 492 (2011). [4] H. Muir. The chondrocyte, architect of cartilage. biomechanics,structure, function and molecular biology of cartilage matrix macromolecules. Bioessays, (17), 1039 (1995). [5] E. Wachtel, A. Maroudas and R. Schneiderman. Age-related changes in collagen packing of human articular cartilage. Bioch. Bioph. Acta, (1243), 239 (1995). [6] J. Dudhia. Aggrecan, aging and assembly in articular cartilage.Cellular and Molecular Life Sciences, (62), 2241 (2005). [7] M. B. Goldring and S. R. Goldring. Osteoarthritis. J. Cell. Physiol., (213), 626 (2007). [8] D. Umlauf, S. Frank, T. Pap and J. Bertrand. Cartilage biology, pathology, and repair. Cellular and Molecular Life Sciences,(67), 41974211 (2010). [9] F. Eckstein, M. Kunzy, M. Schutzery, M. Hudelmaier, R. D.Jackson, J. Yu, C. B. Eaton and E. Schneider. Two year longitudinal change and teste-retest-precision of knee cartilage morphology in a pilot study for the osteoarthritis initiative. OsteoArthritis and Cartilage, (15), 1326 (2007). [10] M. Beekhuizen, Y. M. Bastiaansen-Jenniskens, W. Koevoet,D. B. F. Saris, W. J. A. Dhert, L. B. Creemers and G. J. V. M.van Osch. Osteoarthritic synovial tissue inhibition of proteoglycan production in human osteoarthritic knee cartilage. Arth.& Rheum., (63), 1918 (2011). [11] H. J. Mankin, H. Dorfman, L. Lippiello and L. Zarins. Biochemical and metabolic abnormalities in articular cartilage from osteoarthritic human hips. ii: Correlation of morphology with biochemical and metabolic data. J. Bone Joint. Surg. Am., (53), 523 (1971). [12] A. A. V. de Loo, O. Arntz, I. Otterness and W. V. den Berg. Proteoglycan loss and subsequent replenishment in articularcartilage after a mild arthritic insult by il-1 in mice: impaired proteoglycan turnover in the recovery phase. Ag. Act., (41), 200 (1994). [13] G. Grushko, R. Schneiderman and A. Maroudas. Some bichemical and biophysical parameters for the study of the pathogenesis of osteoarthritis: comparison between the processes of aging and degeneration in human hip cartilage. Conn. Tiss. Res., (19), 149 (1989). [14] J. Degroot, N. Verzijl, R. Bank, F. P. J. Lafeber, J. W. J. Bijlsma and J. Tekoppele. Age-related decrease in proteoglycan syntesis of human articular chondrocytes. Arth. Reum., (42), 1003 (1999). [15] J. R. Grigera, F. Vericat, K. Hallenga and H. Berendsen. Dielectric properties of hydrated collagen. Biopol., (18), 35 (1979). [16] Akella, S.V.S., R.R. Regatte, A.J. Wheaton, A. Borthakur, and R. Reddy. 2004. Reduction of Residual Dipolar Interaction in Cartilage by Spin-Lock Technique. Magn. Res. Med. 52:1103-1109. [17] Migchelsen, C. and H.J.C. Berendsen. 1973. Proton exchange and molecular orientation of water in hydrated collagen fibers. J.Chem.Phys. 59(1):296-305. [18] Shinar, H., and G. Navon. 2006. Multinuclear NMR and Microscopic MRI studies of articular cartilage nanostructure. NMR Biomed.19:877-893. [19] Filidoro, L., O. Dietrich, J. Weber, E. Rauch, T. Oerther, M. Wick, M.F. Reiser, and C. Glaser. 2005. High-Resolution DTI of human patellar cartilage: feasibility and preliminary findings. Magn. Res. Med. 53:993-998. [20] Raya, J.G., Melkus, G., Adam-Neumair, S., Dietrich, O., Mutzel, E., Kahr, B., Reiser, M.F., Jakob, P.M., Putz, R. and C. Glaser. 2011. Change of diffusion tensor imaging parameters in articular cartilage with progressive proteoglycan extraction. Invest. Radiol. 46:401-409. [21] Azuma, T., Nakai, R., Takizawa O. and S. Tsutsumi. 2009. In vivo structural analysis of articular cartilage using diffusion tensor magnetic resonance imaging. Magn. Res. Im. 27:1242-1248. [22] Basser, P.J., and C. Pierpaoli. 1996. Microstructural and Physiological Features of Tissues elucidated by Quantitative-Diffusion-Tensor MRI. J.Magn.Res. 111:209-219. [23] Pierpaoli, C., P. Jezzard, P.J. Basser, J. Barnett , and G. Di Chiro. 1996. Diffusion tensor MR imaging of the human brain. Radiol. 201:637-648. [24] Basser, P.J., J. Mattiello, and D. LeBihan. 1994. MR Diffusion Tensor Spectroscopy and Imaging. Bioph. J. 66:259-267. [25] Le Bihan, D. 1991. Molecular diffusion nuclear magnetic resonance imaging. Magn. Res. Quart. 7:1-30. [26] Basser, P.J., and D.K. Jones. 2002. Diffusion-Tensor MRI. NMR Biomed. 15:456 -467. [27] Napadow, V.J., V. Q. Chen, V. Mai, P.T.C. So, and R. J. Gilbert. 2001. Quantitative Analysis of Three-Dimensional-Resolved Fiber Architecture in Heterogeneous Skeletal Muscle Tissue Using NMR and Optical Imaging Methods. Bioph. J. 80:2968-2975. [28] De Visser, S.K., J. C. Bowden, E. Wentrup-Byrne, L. Rintoul, T. Bostrom, J. M. Pope D and K. I. Momot. 2008. Anisotropy of collagen fibre alignment in bovine cartilage: comparison of polarised light microscopy and spatially resolved diffusion-tensor measurements. Ost. and Cart.16: 689-697. [29] Pierce, D.M., Trobin W., Raya J.G., Trattnig S., Bishof H., Glaser C. and G.A. Holzapfeli. 2010. DT-MRI based computation of collagen fiber deformation in human articular cartilage: a feasibility study. Ann. Biom. Eng. 38:2447–2463. [30] Meder, R., S. K. de Visser, J. C. Bowden, T. Bostrom, and J. M. Pope. 2006. Diffusion tensor imaging of articular cartilage as a measure of tissue microstructure Ost. and Cart. 14, 875-881. [31] Othman, S.F., Williams, J.M., Sumner, D.R. and R.L. Magin. 2004. MRI heterogeneity of articular cartilage in strong magnetic field: dependence on proteoglycan content. Magn. Res. Eng. 23B(1):33-43. [32] Venn, M. F. 1978. Variation of chemical composition with age in human femoral head cartilage. Ann. Rheum. Dis. 37:168-174.I documenti in IRIS sono protetti da copyright e tutti i diritti sono riservati, salvo diversa indicazione.
