Skip to main content Accessibility help
×
Home
Hostname: page-component-544b6db54f-lmg95 Total loading time: 0.206 Render date: 2021-10-24T02:43:39.316Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": true, "newCiteModal": false, "newCitedByModal": true, "newEcommerce": true, "newUsageEvents": true }

Design and Demonstration of a Microbiaxial Optomechanical Device for Multiscale Characterization of Soft Biological Tissues with Two-Photon Microscopy

Published online by Cambridge University Press:  13 January 2011

Joseph T. Keyes
Affiliation:
Graduate Interdisciplinary Program in Biomedical Engineering, The University of Arizona, Tucson, AZ 85721, USA
Stacy M. Borowicz
Affiliation:
Department of Aerospace and Mechanical Engineering, The University of Arizona, Tucson, AZ 85721, USA
Jacob H. Rader
Affiliation:
Department of Aerospace and Mechanical Engineering, The University of Arizona, Tucson, AZ 85721, USA
Urs Utzinger
Affiliation:
Graduate Interdisciplinary Program in Biomedical Engineering, The University of Arizona, Tucson, AZ 85721, USA BIO5 Institute for Biocollaborative Research, The University of Arizona, Tucson, AZ 85721, USA Department of Biomedical Engineering, The University of Arizona, Tucson, AZ 85721, USA
Mohamad Azhar
Affiliation:
BIO5 Institute for Biocollaborative Research, The University of Arizona, Tucson, AZ 85721, USA Department of Cell Biology and Anatomy, The University of Arizona, Tucson, AZ 85721, USA
Jonathan P. Vande Geest*
Affiliation:
Graduate Interdisciplinary Program in Biomedical Engineering, The University of Arizona, Tucson, AZ 85721, USA Department of Aerospace and Mechanical Engineering, The University of Arizona, Tucson, AZ 85721, USA BIO5 Institute for Biocollaborative Research, The University of Arizona, Tucson, AZ 85721, USA Department of Biomedical Engineering, The University of Arizona, Tucson, AZ 85721, USA
*
Corresponding author. E-mail: jpv1@email.arizona.edu

Abstract

The biomechanical response of tissues serves as a valuable marker in the prediction of disease and in understanding the related behavior of the body under various disease and age states. Alterations in the macroscopic biomechanical response of diseased tissues are well documented; however, a thorough understanding of the microstructural events that lead to these changes is poorly understood. In this article we introduce a novel microbiaxial optomechanical device that allows two-photon imaging techniques to be coupled with macromechanical stimulation in hydrated planar tissue specimens. This allows that the mechanical response of the microstructure can be quantified and related to the macroscopic response of the same tissue sample. This occurs without the need to fix tissue in strain states that could introduce a change in the microstructural configuration. We demonstrate the passive realignment of fibrous proteins under various types of loading, which demonstrates the ability of tissue microstructure to reinforce itself in periods of high stress. In addition, the collagen and elastin response of tissue during viscoelastic behavior is reported showing interstitial fluid movement and fiber realignment potentially responsible for the temporal behavior. We also demonstrate that nonhomogeneities in fiber strain exist over biaxial regions of assumed homogeneity.

Type
Biological Applications
Copyright
Copyright © Microscopy Society of America 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Azhar, M., Yin, M., Bommireddy, R., Duffy, J.J., Yang, J., Pawlowski, S.A., Boivin, G.P., Engle, S.J., Sanford, L.P., Grisham, C., Singh, R.R., Babcock, G.F. & Doetschman, T. (2009). Generation of mice with a conditional allele for transforming growth factor beta 1 gene. Genesis 47(6), 423431.CrossRefGoogle ScholarPubMed
Bell, J.P.-P.a.P.D. (2008). Confocal and two-photon microscopy. In Methods in Molecular Medicine, vol. 86: Renal Disease: Techniques and Protocols, I, Humana Press (Ed.), pp. 129138. Berlin, New York: Springer.Google Scholar
Bhatia, A. & Vesely, I. (2005). The effect of glycosaminoglycans and hydration on the viscoelastic properties of aortic valve cusps. Conf Proc IEEE Eng Med Biol Soc 3, 29792980.Google ScholarPubMed
Billiar, K.L. & Sacks, M.S. (1997). A method to quantify the fiber kinematics of planar tissues under biaxial stretch. J Biomech 30(7), 753756.CrossRefGoogle ScholarPubMed
Boulesteix, T., Pena, A.M., Pages, N., Godeau, G., Sauviat, M.P., Beaurepaire, E. & Schanne-Klein, M.C. (2006). Micrometer scale ex vivo multiphoton imaging of unstained arterial wall structure. Cytometry A 69(1), 2026.CrossRefGoogle ScholarPubMed
Cox, G., Kable, E., Jones, A., Fraser, I., Manconi, F. & Gorrell, M.D. (2003). 3-dimensional imaging of collagen using second harmonic generation. J Struct Biol 141(1), 5362.CrossRefGoogle ScholarPubMed
Debes, J.C. & Fung, Y.C. (1995). Biaxial mechanics of excised canine pulmonary arteries. Am J Physiol 269(2 Pt 2), H433H442.Google ScholarPubMed
DiSilvestro, M.R. & Suh, J.K. (2002). Biphasic poroviscoelastic characteristics of proteoglycan-depleted articular cartilage: Simulation of degeneration. Ann Biomed Eng 30(6), 792800.CrossRefGoogle ScholarPubMed
Driessen, N.J., Boerboom, R.A., Huyghe, J.M., Bouten, C.V. & Baaijens, F.P. (2003). Computational analyses of mechanically induced collagen fiber remodeling in the aortic heart valve. J Biomech Eng 125(4), 549557.CrossRefGoogle ScholarPubMed
Eberl, C., Gianola, D.S. & Thompson, R. (2006). Matlab central. In File ID: 12413, I. Natick, MA: The Mathworks, Inc.Google Scholar
Eshel, H. & Lanir, Y. (2001). Effects of strain level and proteoglycan depletion on preconditioning and viscoelastic responses of rat dorsal skin. Ann Biomed Eng 29(2), 164172.CrossRefGoogle ScholarPubMed
Fung, Y. (1993). Biomechanics: Mechanical Properties of Living Tissues. New York: Springer.CrossRefGoogle Scholar
Fung, Y.C. & Liu, S.Q. (1995). Determination of the mechanical properties of the different layers of blood vessels in vivo. Proc Natl Acad Sci USA 92(6), 21692173.CrossRefGoogle ScholarPubMed
Gianola, D.S. & Eberl, C. (2009). Micro- and nanoscale tensile testing of materials. JOM—J Min Met Mat Soc 61(3), 2435.CrossRefGoogle Scholar
Gleason, R.L., Gray, S.P., Wilson, E. & Humphrey, J.D. (2004). A multiaxial computer-controlled organ culture and biomechanical device for mouse carotid arteries. J Biomech Eng 126(6), 787795.CrossRefGoogle ScholarPubMed
Halloran, B.G., Davis, V.A., McManus, B.M., Lynch, T.G. & Baxter, B.T. (1995). Localization of aortic disease is associated with intrinsic differences in aortic structure. J Surg Res 59(1), 1722.CrossRefGoogle ScholarPubMed
Hariton, I., de Botton, G., Gasser, T.C. & Holzapfel, G.A. (2007a). Stress-driven collagen fiber remodeling in arterial walls. Biomech Model Mechanobiol 6(3), 163175.CrossRefGoogle ScholarPubMed
Hariton, I., de Botton, G., Gasser, T.C. & Holzapfel, G.A. (2007b). Stress-modulated collagen fiber remodeling in a human carotid bifurcation. J Theor Biol 248(3), 460470.CrossRefGoogle Scholar
Haskett, D., Johnson, G., Zhou, A., Utzinger, U. & Vande Geest, J. (2010). Microstructural and biomechanical alterations of the human aorta as a function of age and location. Biomech Model Mechanobiol 9(6), 725736.CrossRefGoogle ScholarPubMed
Hepworth, D.G., Steven-Fountain, A., Bruce, D.M. & Vincent, J.F. (2001). Affine versus non-affine deformation in soft biological tissues, measured by the reorientation and stretching of collagen fibres through the thickness of compressed porcine skin. J Biomech 34(3), 341346.CrossRefGoogle ScholarPubMed
Hu, J.J., Humphrey, J.D. & Yeh, A.T. (2009). Characterization of engineered tissue development under biaxial stretch using nonlinear optical microscopy. Tissue Eng Part A 15(7), 15531564.CrossRefGoogle ScholarPubMed
Humphrey, J.D. (2001). Cardiovascular Solid Mechanics: Cells, Tissues, and Organs. New York: Springer.Google Scholar
Humphrey, J.D., Vawter, D.L. & Vito, R.P. (1987). Quantification of strains in biaxially tested soft tissues. J Biomech 20(1), 5965.CrossRefGoogle ScholarPubMed
Humphrey, J.D., Wells, P.B., Baek, S., Hu, J.J., McLeroy, K. & Yeh, A.T. (2008). A theoretically-motivated biaxial tissue culture system with intravital microscopy. Biomech Model Mechanobiol 7(4), 323334.CrossRefGoogle ScholarPubMed
Jani, B. & Rajkumar, C. (2006). Ageing and vascular ageing. Postgrad Med J 82(968), 357362.CrossRefGoogle ScholarPubMed
Kirkpatrick, N.D., Andreou, S., Hoying, J.B. & Utzinger, U. (2007). Live imaging of collagen remodeling during angiogenesis. Am J Physiol Heart Circ Physiol 292(6), H3198H3206.CrossRefGoogle ScholarPubMed
Labropoulos, N., Ashraf Mansour, M., Kang, S.S., Oh, D.S., Buckman, J. & Baker, W.H. (2000). Viscoelastic properties of normal and atherosclerotic carotid arteries. Eur J Vasc Endovasc Surg 19(3), 221225.CrossRefGoogle ScholarPubMed
Lillie, M.A. & Gosline, J.M. (2007). Limits to the durability of arterial elastic tissue. Biomaterials 28(11), 20212031.CrossRefGoogle ScholarPubMed
Lipman, R.D., Grossman, P., Bridges, S.E., Hamner, J.W. & Taylor, J.A. (2002). Mental stress response, arterial stiffness, and baroreflex sensitivity in healthy aging. J Gerontol A Biol Sci Med Sci 57(7), B279B284.CrossRefGoogle ScholarPubMed
Mase, G.T. & Mase, G.E. (1999). Continuum Mechanics for Engineers, Second Edition. Boca Raton, FL: CRC Press.CrossRefGoogle Scholar
Nishijo, N., Sugiyama, F., Kimoto, K., Taniguchi, K., Murakami, K., Suzuki, S., Fukamizu, A. & Yagami, K. (1998). Salt-sensitive aortic aneurysm and rupture in hypertensive transgenic mice that overproduce angiotensin II. Lab Invest 78(9), 10591066.Google ScholarPubMed
Okamoto, R.J., Wagenseil, J.E., DeLong, W.R., Peterson, S.J., Kouchoukos, N.T. & Sundt, T.M. 3rd. (2002). Mechanical properties of dilated human ascending aorta. Ann Biomed Eng 30(5), 624635.CrossRefGoogle ScholarPubMed
Roeder, B.A., Kokini, K., Sturgis, J.E., Robinson, J.P. & Voytik-Harbin, S.L. (2002). Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure. J Biomech Eng 124(2), 214222.CrossRefGoogle ScholarPubMed
Sacks, M.S., Merryman, W.D. & Schmidt, D.E. (2009). On the biomechanics of heart valve function. J Biomech 42(12), 18041824.CrossRefGoogle ScholarPubMed
Safar, M.E., Blacher, J., Mourad, J.J. & London, G.M. (2000). Stiffness of carotid artery wall material and blood pressure in humans: Application to antihypertensive therapy and stroke prevention. Stroke 31(3), 782790.CrossRefGoogle ScholarPubMed
Sokolis, D.P. (2008). Passive mechanical properties and constitutive modeling of blood vessels in relation to microstructure. Med Biol Eng Comput 46(12), 11871199.CrossRefGoogle ScholarPubMed
Stella, J.A., Liao, J., Hong, Y., Merryman, W.D., Wagner, W.R. & Sacks, M.S. (2008). Tissue-to-cellular level deformation coupling in cell micro-integrated elastomeric scaffolds. Biomaterials 29(22), 32283236.CrossRefGoogle ScholarPubMed
Timmins, L.H., Wu, Q., Yeh, A.T., Moore, J.E. Jr. & Greenwald, S.E. (2010). Structural inhomogeneity and fiber orientation in the inner arterial media. Am J Physiol Heart Circ Physiol 298(5), H1537H1545.CrossRefGoogle ScholarPubMed
Vande Geest, J.P., Sacks, M.S. & Vorp, D.A. (2004). Age dependency of the biaxial biomechanical behavior of human abdominal aorta. J Biomech Eng 126(6), 815822.CrossRefGoogle ScholarPubMed
Vande Geest, J.P., Sacks, M.S. & Vorp, D.A. (2006). The effects of aneurysm on the biaxial mechanical behavior of human abdominal aorta. J Biomech 39(7), 13241334.CrossRefGoogle ScholarPubMed
Voytik-Harbin, S.L., Roeder, B.A., Sturgis, J.E., Kokini, K. & Robinson, J.P. (2003). Simultaneous mechanical loading and confocal reflection microscopy for three-dimensional microbiomechanical analysis of biomaterials and tissue constructs. Microsc Microanal 9(1), 7485.CrossRefGoogle ScholarPubMed
Zhang, W., Liu, Y. & Kassab, G.S. (2007). Viscoelasticity reduces the dynamic stresses and strains in the vessel wall: Implications for vessel fatigue. Am J Physiol Heart Circ Physiol 293(4), H2355H2360.CrossRefGoogle ScholarPubMed
Zoumi, A., Lu, X., Kassab, G.S. & Tromberg, B.J. (2004). Imaging coronary artery microstructure using second-harmonic and two-photon fluorescence microscopy. Biophys J 87(4), 27782786.CrossRefGoogle ScholarPubMed
Zoumi, A., Yeh, A. & Tromberg, B.J. (2002). Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon exrefd fluorescence. Proc Natl Acad Sci USA 99(17), 1101411019.CrossRefGoogle ScholarPubMed
22
Cited by

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Design and Demonstration of a Microbiaxial Optomechanical Device for Multiscale Characterization of Soft Biological Tissues with Two-Photon Microscopy
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Design and Demonstration of a Microbiaxial Optomechanical Device for Multiscale Characterization of Soft Biological Tissues with Two-Photon Microscopy
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Design and Demonstration of a Microbiaxial Optomechanical Device for Multiscale Characterization of Soft Biological Tissues with Two-Photon Microscopy
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *