An ultrasound study of altered hydration behaviour of proteoglycan-degraded articular cartilage

BMC Musculoskeletal Disorders

Wu-Fan Chen²  Qian-Jin Feng²  Wen-Jing Zhang²  Hai-Jun Niu¹  Yi-Yi Yang²  Qing Wang² 

[1] Key Laboratory of the Ministry of Education for Biomechanics and Mechanobiology, School of Biological Science and Medical Engineering, Beihang University, Beijing 100191, China;Institute of Medical Information, School of Biomedical Engineering, Southern Medical University, Guangzhou 510515, China

关键词: Osteoarthritis;    Ultrasound;    Articular cartilage;    Proteoglycans;    Hydration;   

Others  :  1129477
DOI  :  10.1186/1471-2474-14-289

 received in 2013-06-13, accepted in 2013-09-19,  发布年份 2013

【 摘 要 】

Background

Articular cartilage is a solid-fluid biphasic material covering the bony ends of articulating joints. Hydration of articular cartilage is important to joint lubrication and weight-wearing. The aims of this study are to measure the altered hydration behaviour of the proteoglycan-degraded articular cartilage using high-frequency ultrasound and then to investigate the effect of proteoglycan (PG) degradation on cartilage hydration.

Methods

Twelve porcine patellae with smooth cartilage surface were prepared and evenly divided into two groups: normal group without any enzyme treatment and trypsin group treated with 0.25% trypsin solution for 4 h to digest PG in the tissue. After 40-minute exposure to air at room temperature, the specimens were immerged into the physiological saline solution. The dehydration induced hydration behaviour of the specimen was monitored by the high-frequency (25 MHz) ultrasound pulser/receiver (P/R) system. Dynamic strain and equilibrium strain were extracted to quantitatively evaluate the hydration behaviour of the dehydrated cartilage tissues.

Results

The hydration progress of the dehydrated cartilage tissue was observed in M-mode ultrasound image indicating that the hydration behaviour of the PG-degraded specimens decreased. The percentage value of the equilibrium strain (1.84 ± 0.21%) of the PG-degraded cartilage significantly (p < 0.01) decreased in comparison with healthy cartilage (3.46 ± 0.49%). The histological sections demonstrated that almost PG content in the entire cartilage layer was digested by trypsin.

Conclusion

Using high-frequency ultrasound, this study found a reduction in the hydration behaviour of the PG-degraded cartilage. The results indicated that the degradation of PG decreased the hydration capability of the dehydrated tissue. This study may provide useful information for further study on changes in the biomechanical property of articular cartilage in osteoarthritis.

【 授权许可】

   
2013 Wang et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Mankin HJ, Mow VC, Buckwalter JA, Iannotti JP, Ratcliffe A: Articular cartilage structure, composition, and function. In Orthopaedic basic science-. 2nd edition. Edited by Buckwalter JA, Einhoun TA, Simnon SR. Rosemont: American Academy of Orthopaedic Surgeons; 2000:444-470.
• [2]Mow VC, Gu WY, Chen FH: Structure and function of articular cartilage and meniscus,. In Basic Orthopaedic Biomechanics and Mechano-Biology. 3rd edition. Edited by Mow VC, Huiskes R. Philadelphia: Lippincott Williams & Wilkins; 2005:181-258.
• [3]Mow VC, Hung CT: Biomechanics of articular cartilage. In Basic biomechanics of the musculoskeletal system-. 3rd edition. Edited by Nordin M, Frankel VH. London: Lea & Feviger Philadelphia; 2001:60-101.
• [4]Little CB, Ghosh P, Bellenger CR: Topographic variation in biglycan and decorin synthesis by articular cartilage in the early stages of osteoarthritis: an experimental study in sheep. J Orthop Res 1996, 14(3):433-444.
• [5]Lark MW, Bayne EK, Flanagan J, Harper CF, Hoerrner LA, Hutchinson NI, Singer II, Donatelli SA, Weidner JR, Williams HR, Mumford RA, Lohmander LS: Aggrecan degradation in human cartilage. Evidence for both matrix metalloproteinase and aggrecanase activity in normal, osteoarthritic, and rheumatoid joints. J Clin Invest 1997, 100(1):93-106.
• [6]Neame PJ, Sandy JD: Cartilage aggrecan. Biosynthesis, degradation and osteoarthritis. J Fla Med Assoc 1994, 81(3):191-193.
• [7]Fick JM, Espino DM: Articular cartilage surface rupture during compression: investigating the effects of tissue hydration in relation to matrix health. J Mech Behav Biomed Mater 2011, 4(7):1311-1317.
• [8]Hosseininia S, Lindberg LR, Dahlberg LE: Cartilage collagen damage in hip osteoarthritis similar to that seen in knee osteoarthritis; a case-control study of relationship between collagen, glycosaminoglycan and cartilage swelling. BMC Musculoskelet Disord 2013, 14:18. 10.1186/1471-2474-14-18 BioMed Central Full Text
• [9]Lai WM, Hou JS, Mow VC: A triphasic theory for the swelling and deformation behaviors of articular cartilage. J Biomech Eng 1991, 113:245-258.
• [10]Setton LA, Mow VC, Muller FJ, Pita JC, Howell DS: Mechanical properties of canine articular cartilage are significantly altered following transection of the anterior cruciate ligament. J Orthop Res 1994, 12(4):451-463.
• [11]Race A, Broom ND, Robertson P: Effect of loading rate and hydration on the mechanical properties of the discs. Spine 2000, 25(6):662-669.
• [12]Tepic S, Macirowski T, Mann RW: Mechanical properties of articular cartilage elucidated by osmotic loading and ultrasound. Proc Natl Acad Sci U S A 1983, 80:3331-3333.
• [13]Wang Q, Zheng YP: Study on transient osmotic-induced hydration of articular cartilage by high-frequency ultrasound. In Proceedings of Biomedical Engineering Conference on Integrating Science and Technology in the Healthcare Industry. Hong Kong: Biomedical Division, The Hong Kong Institution of Engineers; 2004:135-140.
• [14]Wang Q, Zheng YP, Niu HJ: Changes in triphasic mechanical properties of proteoglycan-depleted articular cartilage extracted from osmotic swelling behavior monitored using high-frequency ultrasound. Mol Cell Biomech 2010, 7(1):45-58.
• [15]Wang Q, Zheng YP: Non-contact evaluation of osmosis-induced shrinkage and swelling behavior of articular cartilage in-situ using real-time high-frequency ultrasound. Instrum Sci Technol 2006, 34:317-334.
• [16]Wang Q, Zheng YP, Huang QH, Leung G, Lam WL, Guo X, Lu HB, Qin L, Mak AFT: Altered osmotic swelling behavior of proteoglycan-depleted bovine articular cartilage using high frequency ultrasound. Phys Med Biol 2008, 53(10):2537-2552.
• [17]Ophir J, Cespedes I, Ponnekanti H, Yazdi Y, Li X: Elastography: a quantitative method for imaging the elasticity of biological tissues. Ultrason Imaging 1991, 13:111-134.
• [18]Zheng YP, Ding CX, Bai J, Mak AFT, Qin L: Measurement of the layered compressive properties of trypsin-treated articular cartilage: an ultrasound investigation. Med Biol Eng Comput 2001, 39:534-541.
• [19]Zheng YP, Patil S, Wang Q: Ultrasound speed in articular cartilage under different bathing saline concentration. Key Eng Mater 2006, 321–323:972-977.
• [20]Gu WY, Lai WM, Mow VC: A mixture theory for charged-hydrated soft tissues containing multi-electrolytes: passive transport and swelling behaviours. J Biomed Eng 1998, 120:169-180.
• [21]Lorenzo P, Bayliss MT, Heinegard D: Altered patterns and synthesis of extracellular matrix macromolecules in early osteoarthritis. Matrix Biol 2004, 23:381-391.
• [22]Torzilli PA, Askari E, Jenkins JT: Water content and solute diffusion properties in articular cartilage. In Biomechanics of diarthrodial joints. Volume 1. Edited by Mow VC, Ratcliffe A, Woo SLY. New York: Springer; 1990::363-390.
• [23]Saarakkala S, Julkunen P, Kiviranta P, Mäkitalo J, Jurvelin JS, Korhonen RK: Depth-wise progression of osteoarthritis in human articular cartilage: investigation of composition, structure and biomechanics. Osteoarthritis Cartilage 2010, 18(1):73-81.
• [24]Chen MH, Broom ND: Concerning the ultrastructural origin of large-scale swelling in articular cartilage. J Anat 1999, 194(Pt 3):445-461.
• [25]Thibault M, Poole AR, Buschmann MD: Cyclic compression of cartilage/bone explants in vitro leads to physical weakening, mechanical breakdown of collagen and release of matrix fragments. J Orthop Res 2002, 20(6):1265-1273.
• [26]Harris ED Jr, Parker HG, Radin EL, Krane SM: Effects of proteolytic enzymes on structural and mechanical properties of cartilage. Arthritis Rheum 1972, 15:497-503.
• [27]Nieminen HJ, Toyras J, Rieppo J, Nieminen MT, Hirvonen J, Korhonen R, Jurvelin JS: Real-time ultrasound analysis of articular cartilage degradation in vitro. Ultrasound Med Biol 2002, 28:519-525.
• [28]Narmoneva DA, Wang JY, Setton LA: A noncontacting method for material property determination for articular cartilage from osmotic loading. Biophys J 2001, 81:3066-3076.
• [29]Hattori K, Uematsu K, Matsumoto T, Ohgushi H: Mechanical effects of surgical procedures on osteochondral grafts elucidated by osmotic loading and real-time ultrasound. Arthritis Res Ther 2009, 11(5):R134. BioMed Central Full Text
• [30]Summers GC, Merrill A, Sharif M, Adams MA: Swelling of articular cartilage depends on the integrity of adjacent cartilage and bone. Biorheology 2008, 45(3–4):365-374.
• [31]Thambyah A, Zhang G, Kim W, Broom ND: Impact induced failure of cartilage-on-bone following creep loading: a microstructural and fracture mechanics study. J Mech Behav Biomed Mater 2012, 14:239-247.
• [32]Wang Q, Zheng YP: Ultrasound Assessment of Boundary Effect on Osmosis-Induced Shrinkage and Swelling of Articular Cartilage in-vitro. Connect Tissue Res 2013, 54(3):153-158.