Previous investigations have shown that tissue-engineered articular cartilage can be damaged under a combination of compression and sliding shear. In these cases, damage was identified in histological sections after a test was completed. This approach is limited, in that it does not identify when damage occurred. This especially limits the utility of an assay for evaluating damage when comparing modifications to a tissue-engineering protocol. In this investigation, the feasibility of using ultrasound (US) to detect damage as it occurs was investigated. US signals were acquired before, during, and after sliding shear, as were stereomicroscope images of the cartilage surface. Histology was used as the standard for showing if a sample was damaged. We showed that US reflections from the surface of the cartilage were attenuated due to roughening following sliding shear. Furthermore, it was shown that by scanning the transducer across a sample, surface roughness and erosion following sliding shear could be identified. Internal delamination could be identified by the appearance of new echoes between those from the front and back of the sample. Thus, it is feasible to detect damage in engineered cartilage using US.
Get full access to this article
View all access options for this article.
References
1.
GelseK., OlkA., EichhornS., SwobodaB., SchoeneM., and RaumK.Quantitative ultrasound biomicroscopy for the analysis of healthy and repair cartilage tissue. Eur Cells Mater, 19, 58, 2010.
2.
AccardiM.A., McCullenS.D., CallananA., et al. Effects of fiber orientation on the frictional properties and damage of regenerative articular cartilage surfaces. Tissue Eng A, 19, 2300, 2013.
3.
GleghornJ.P., JonesA.R., FlanneryC.R., and BonassarL.J.Boundary mode frictional properties of engineered cartilaginous tissues. Eur Cells Mater, 14, 20, 2007.
4.
WhitneyG.A., JayaramanK., DennisJ., and MansourJ.M.Highly cellular region of scaffold-free engineered cartilage fails under compressive shearing loads. Biomedical Engineering Society Annual Meeting, Austin, TX, 2010.
5.
WhitneyG.A., JayaramanK., DennisJ.E., and MansourJ.M.Scaffold-free cartilage subjected to frictional shear stress demonstrates damage by cracking and surface peeling. J Tissue Eng Regen Med, 11, 412, 2017.
6.
WhitneyG.A., MansourJ.M., and DennisJ.E.Coefficient of friction patterns can identify damage in native and engineered cartilage subjected to frictional-shear stress. Ann Biomed Eng, 43, 2056, 2015.
7.
MotavalliM., WhitneyG.A., DennisJ.E., and MansourJ.M.Investigating a continuous shear strain function for depth-dependent properties of native and tissue engineering cartilage using pixel-size data. J Mech Behav Biomed Mater, 28C, 62, 2013.
8.
ChungC.Y., HeebnerJ., BaskaranH., WelterJ.F., and MansourJ.M.Ultrasound elastography for estimation of regional strain of multilayered hydrogels and tissue-engineered cartilage. Ann Biomed Eng, 43, 2991, 2015.
9.
MansourJ.M., GuD.W., ChungC.Y., et al. Towards the feasibility of using ultrasound to determine mechanical properties of tissues in a bioreactor. Ann Biomed Eng, 42, 2190, 2014.
10.
WalkerJ.M., MyersA.M., SchluchterM.D., et al. Nondestructive evaluation of hydrogel mechanical properties using ultrasound. Ann Biomed Eng, 39, 2521, 2011.
11.
WhitneyG.A., JayaramanK., DennisJ.E., and MansourJ.M.Scaffold-free cartilage subjected to frictional shear stress demonstrates damage by cracking and surface peeling. J Tissue Eng Regen Med, 11, 412, 2017.
12.
KeanT.J., and DennisJ.E.Synoviocyte derived-extracellular matrix enhances human articular chondrocyte proliferation and maintains re-differentiation capacity at both low and atmospheric oxygen tensions. PLoS One, 10, e0129961, 2015.
13.
KeanT.J., MeraH., WhitneyG.A., et al. Disparate response of articular- and auricular-derived chondrocytes to oxygen tension. Connect Tissue Res, 57, 319, 2016.
14.
WhitneyG.A., KeanT.J., FernandesR.J., et al. Thyroxine increases collagen type II expression and accumulation in scaffold-free tissue-engineered articular cartilage. Tissue Eng A, 24, 369, 2018.
15.
SaarakkalaS., TöyräsJ., HirvonenJ., LaasanenM.S., LappalainenR., and JurvelinJ.S.Ultrasonic quantitation of superficial degradation of articular cartilage. Ultrasound Med Biol, 30, 783, 2004.
16.
LaasanenM.S., TöyräsJ., VasaraA., et al. Quantitative ultrasound imaging of spontaneous repair of porcine cartilage. Osteoarthritis Cartilage, 14, 258, 2006.
17.
BergmannG., DeuretzbacherG., HellerM., et al. Hip contact forces and gait patterns from routine activities. J Biomech, 34, 859, 2001.
18.
DavyD.T., KotzarG.M., BrownR.H., et al. Telemetric force measurements across the hip after total arthroplasty. J Bone Joint Surg Am., 70, 45, 1988.
19.
EllisM.I., SeedhomB.B., and WrightV.Forces in the knee joint whilst rising from a seated position. J Biomed Eng, 6, 113, 1984.
20.
LuT.W., O'ConnorJ.J., TaylorS.J., and WalkerP.S.Validation of a lower limb model with in vivo femoral forces telemetered from two subjects. J Biomech, 31, 63, 1998.
21.
SeiregA., and ArvikarR.J.A mathematical model for evaluation of forces in lower extremeties of the musculo-skeletal system. J Biomech, 6, 313, 1973.
22.
SingermanR., BerillaJ., ArchdeaconM., and PeyserA.In vitro forces in the normal and cruciate-deficient knee during simulated squatting motion. J Biomech Eng, 121, 234, 1999.
23.
TaylorW.R., HellerM.O., BergmannG., and DudaG.N.Tibio-femoral loading during human gait and stair climbing. J Orthop Res, 22, 625, 2004.
24.
LinnF.C.Lubrication of animal joints. I. The arthrotripsometer. J Bone Joint Surg Am, 49, 1079, 1967.
25.
LinnF.C., and RadinE.L.Lubrication of animal joints. 3. The effect of certain chemical alterations of the cartilage and lubricant. Arthritis Rheum, 11, 674, 1968.
26.
RadinE.L., and PaulI.L.A consolidated concept of joint lubrication. J Bone Joint Surg Am, 54, 607, 1972.
WhitneyG.A., MeraH., WeidenbecherM., AwadallahA., MansourJ.M., and DennisJ.E.Methods for producing scaffold-free engineered cartilage sheets from auricular and articular chondrocyte cell sources and attachment to porous tantalum. BioRes Open Access, 1, 157, 2012.
29.
NaumannA., DennisJ.E., AwadallahA., et al. Immunochemical and mechanical characterization of cartilage subtypes in rabbit. J Histochem Cytochem, 50, 1049, 2002.
30.
WhitneyG., TraegerG., MansourJ.M., DennisJ.E., and FernandesR.J.Thyroxine improves the tribological performance of scaffold-free engineered cartilage. 2nd International Conference on Bio Tribology, Toronto, Ontario, 2014.
31.
WhitneyG., KeanT., FernandesR.J., WaldmanS., MansourJ.M., and DennisJ.E.Thyroxine significantly increases type II collagen content and functional measures in engineered cartilage. Tissue Eng Part A, 21, S289, 2015.
32.
NieminenH.J., SaarakkalaS., LaasanenM.S., HirvonenJ., JurvelinJ.S., and TöyräsJ.Ultrasound attenuation in normal and spontaneously degenerated articular cartilage. Ultrasound Med Biol, 30, 493, 2004.
33.
JurvelinJ.S., RäsänenT., KolmonenP., and LyyraT.Comparison of optical, needle probe and ultrasonic techniques for the measurement of articular cartilage thickness. J Biomech, 28, 231, 1995.
34.
TöyräsJ., NieminenH.J., LaasanenM.S., et al. Ultrasonic characterization of articular cartilage. Biorheology, 39, 161, 2002.
35.
KalevaE., SaarakkalaS., TöyräsJ., NieminenH.J., and JurvelinJ.S.In-vitro comparison of time-domain, frequency-domain and wavelet ultrasound parameters in diagnostics of cartilage degeneration. Ultrasound Med Biol, 34, 155, 2008.
36.
ChérinE., SaïedA., PellaumailB., et al. Assessment of rat articular cartilage maturation using 50-MHz quantitative ultrasonography. Osteoarthritis Cartilage, 9, 178, 2001.
37.
HattoriK., IkeuchiK., MoritaY., and TakakuraY.Quantitative ultrasonic assessment for detecting microscopic cartilage damage in osteoarthritis. Arthritis Res Ther, 7, R38, 2005.
38.
HattoriK., TakakuraY., MoritaY., TakenakaM., UematsuK., and IkeuchiK.Can ultrasound predict histological findings in regenerated cartilage?. Rheumatology (Oxford), 43, 302, 2004.
39.
KurokiH., NakagawaY., MoriK., et al. Maturation-dependent change and regional variations in acoustic stiffness of rabbit articular cartilage: an examination of the superficial collagen-rich zone of cartilage. Osteoarthritis Cartilage, 14, 784, 2006.
40.
KurokiH., NakagawaY., MoriK., et al. Acoustic stiffness and change in plug cartilage over time after autologous osteochondral grafting: correlation between ultrasound signal intensity and histological score in a rabbit model. Arthrit Res Ther, 6, R492, 2004.
41.
TöyräsJ., RieppoJ., NieminenM.T., HelminenH.J., and JurvelinJ.S.Characterization of enzymatically induced degradation of articular cartilage using high frequency ultrasound. Phys Med Biol, 44, 2723, 1999.
42.
SolchagaL.A., PenickK.J., and WelterJ.F.Chondrogenic differentiation of bone marrow-derived mesenchymal stem cells: tips and tricks. Methods Mol Biol, 698, 253, 2011.
43.
WelterJ., SolchagaL., and BaskaranH.Chondrogenesis from human mesenchymal stem cells: Role of culture conditions. In: HayatE., ed. Stem Cells and Cancer Stem Cells: Therapeutic Applications in Disease and Injury. Berlin: Springer, 2012, pp. 269–281.
44.
NeuC.P., KomvopoulosK., and ReddiA.H.The interface of functional biotribology and regenerative medicine in synovial joints. Tissue Eng B Rev, 14, 235, 2008.
45.
WilliamsG.M., ChanE.F., Temple-WongM.M., et al. Shape, loading, and motion in the bioengineering design, fabrication, and testing of personalized synovial joints. J Biomech, 43, 156, 2010.
46.
LipshitzH., EtheredgeRd., and GlimcherM.J.In vitro studies of the wear of articular cartilage—III. The wear characteristics of chemical modified articular cartilage when worn against a highly polished characterized stainless steel surface. J Biomech, 13, 423, 1980.
47.
VerberneG., MerkherY., HalperinG., MaroudasA., and EtsionI.Techniques for assessment of wear between human cartilage surfaces. Proceedings of the 9th Biennial Conference on Engineering Systems Design and Analysis—20083, 399, 2009.
48.
ForsterH., and FisherJ.The influence of continuous sliding and subsequent surface wear on the friction of articular cartilage. Proc Inst Mech Eng H, 213, 329, 1999.
49.
HuynhR.N., and RaubC.B.Noninvasive surface damage assessment of bovine articular cartilage explants by reflected polarized light microscopy. Conf Proc IEEE Eng Med Biol Soc 2016,2897, 2016.
50.
LötjönenP., JulkunenP., TiituV., JurvelinJ.S., and TöyräsJ.Ultrasound speed varies in articular cartilage under indentation loading. IEEE Trans Ultrason Ferroelectr Freq Contr, 58, 2772, 2011.
51.
LötjönenP., JulkunenP., TöyräsJ., LammiM.J., JurvelinJ.S., and NieminenH.J.Strain-dependent modulation of ultrasound speed in articular cartilage under dynamic compression. Ultrasound Med Biol, 35, 1177, 2009.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
