High-Bandwidth AFM-Based Rheology Reveals that Cartilage is Most Sensitive to High Loading Rates at Early Stages of Impairment

Utilizing a newly developed atomic-force-microscopy-based wide-frequency rheology system, we measured the dynamic nanomechanical behavior of normal and glycosaminoglycan (GAG)-depleted cartilage, the latter representing matrix degradation that occurs at the earliest stages of osteoarthritis. We obse...

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Bibliographic Details
Main Authors: Tavakoli Nia, Hadi, Soltani Bozchalooi, Iman, Li, Yang, Han, Lin, Hung, Han-Hwa K., Frank, Eliot, Youcef-Toumi, Kamal, Ortiz, Christine, Grodzinsky, Alan J.
Other Authors: Massachusetts Institute of Technology. Center for Biomedical Engineering
Format: Article
Language:en_US
Published: Elsevier B.V. 2014
Online Access:http://hdl.handle.net/1721.1/92000
https://orcid.org/0000-0003-3511-5679
https://orcid.org/0000-0003-1970-9901
https://orcid.org/0000-0002-4942-3456
Description
Summary:Utilizing a newly developed atomic-force-microscopy-based wide-frequency rheology system, we measured the dynamic nanomechanical behavior of normal and glycosaminoglycan (GAG)-depleted cartilage, the latter representing matrix degradation that occurs at the earliest stages of osteoarthritis. We observed unique variations in the frequency-dependent stiffness and hydraulic permeability of cartilage in the 1 Hz-to-10 kHz range, a frequency range that is relevant to joint motions from normal ambulation to high-frequency impact loading. Measurement in this frequency range is well beyond the capabilities of typical commercial atomic force microscopes. We showed that the dynamic modulus of cartilage undergoes a dramatic alteration after GAG loss, even with the collagen network still intact: whereas the magnitude of the dynamic modulus decreased two- to threefold at higher frequencies, the peak frequency of the phase angle of the modulus (representing fluid-solid frictional dissipation) increased 15-fold from 55 Hz in normal cartilage to 800 Hz after GAG depletion. These results, based on a fibril-reinforced poroelastic finite-element model, demonstrated that GAG loss caused a dramatic increase in cartilage hydraulic permeability (up to 25-fold), suggesting that early osteoarthritic cartilage is more vulnerable to higher loading rates than to the conventionally studied “loading magnitude”. Thus, over the wide frequency range of joint motion during daily activities, hydraulic permeability appears the most sensitive marker of early tissue degradation.