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...
| Main Authors: | , , , , , , , , |
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| Other Authors: | |
| Format: | Article |
| Language: | en_US |
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Elsevier B.V.
2014
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| 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 |
| _version_ | 1811076079430926336 |
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| author | Tavakoli Nia, Hadi Soltani Bozchalooi, Iman Li, Yang Han, Lin Hung, Han-Hwa K. Frank, Eliot Youcef-Toumi, Kamal Ortiz, Christine Grodzinsky, Alan J. |
| author2 | Massachusetts Institute of Technology. Center for Biomedical Engineering |
| author_facet | Massachusetts Institute of Technology. Center for Biomedical Engineering Tavakoli Nia, Hadi Soltani Bozchalooi, Iman Li, Yang Han, Lin Hung, Han-Hwa K. Frank, Eliot Youcef-Toumi, Kamal Ortiz, Christine Grodzinsky, Alan J. |
| author_sort | Tavakoli Nia, Hadi |
| collection | MIT |
| description | 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. |
| first_indexed | 2024-09-23T10:15:51Z |
| format | Article |
| id | mit-1721.1/92000 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T10:15:51Z |
| publishDate | 2014 |
| publisher | Elsevier B.V. |
| record_format | dspace |
| spelling | mit-1721.1/920002022-09-26T16:50:47Z High-Bandwidth AFM-Based Rheology Reveals that Cartilage is Most Sensitive to High Loading Rates at Early Stages of Impairment Tavakoli Nia, Hadi Soltani Bozchalooi, Iman Li, Yang Han, Lin Hung, Han-Hwa K. Frank, Eliot Youcef-Toumi, Kamal Ortiz, Christine Grodzinsky, Alan J. Massachusetts Institute of Technology. Center for Biomedical Engineering Massachusetts Institute of Technology. Department of Biological Engineering Massachusetts Institute of Technology. Department of Electrical Engineering and Computer Science Massachusetts Institute of Technology. Department of Materials Science and Engineering Massachusetts Institute of Technology. Department of Mechanical Engineering Tavakoli Nia, Hadi Soltani Bozchalooi, Iman Li, Yang Han, Lin Hung, Han-Hwa K. Frank, Eliot Youcef-Toumi, Kamal Ortiz, Christine Grodzinsky, Alan J. 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. Whitaker Foundation (Fellowship) National Science Foundation (U.S.) (grant CMMI- 0758651) National Institutes of Health (U.S.) (grant AR060331) 2014-12-02T21:58:12Z 2014-12-02T21:58:12Z 2013-04 2012-12 Article http://purl.org/eprint/type/JournalArticle 00063495 http://hdl.handle.net/1721.1/92000 Nia, Hadi Tavakoli, Iman S. Bozchalooi, Yang Li, Lin Han, Han-Hwa Hung, Eliot Frank, Kamal Youcef-Toumi, Christine Ortiz, and Alan Grodzinsky. “High-Bandwidth AFM-Based Rheology Reveals That Cartilage Is Most Sensitive to High Loading Rates at Early Stages of Impairment.” Biophysical Journal 104, no. 7 (April 2013): 1529–1537. https://orcid.org/0000-0003-3511-5679 https://orcid.org/0000-0003-1970-9901 https://orcid.org/0000-0002-4942-3456 en_US http://dx.doi.org/10.1016/j.bpj.2013.02.048 Biophysical Journal Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf Elsevier B.V. Elsevier Open Archive |
| spellingShingle | Tavakoli Nia, Hadi Soltani Bozchalooi, Iman Li, Yang Han, Lin Hung, Han-Hwa K. Frank, Eliot Youcef-Toumi, Kamal Ortiz, Christine Grodzinsky, Alan J. High-Bandwidth AFM-Based Rheology Reveals that Cartilage is Most Sensitive to High Loading Rates at Early Stages of Impairment |
| title | High-Bandwidth AFM-Based Rheology Reveals that Cartilage is Most Sensitive to High Loading Rates at Early Stages of Impairment |
| title_full | High-Bandwidth AFM-Based Rheology Reveals that Cartilage is Most Sensitive to High Loading Rates at Early Stages of Impairment |
| title_fullStr | High-Bandwidth AFM-Based Rheology Reveals that Cartilage is Most Sensitive to High Loading Rates at Early Stages of Impairment |
| title_full_unstemmed | High-Bandwidth AFM-Based Rheology Reveals that Cartilage is Most Sensitive to High Loading Rates at Early Stages of Impairment |
| title_short | High-Bandwidth AFM-Based Rheology Reveals that Cartilage is Most Sensitive to High Loading Rates at Early Stages of Impairment |
| title_sort | high bandwidth afm based rheology reveals that cartilage is most sensitive to high loading rates at early stages of impairment |
| url | 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 |
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