0
Technical Brief

Effect of Strain, Region, and Tissue Composition on Glucose Partitioning in Meniscus Fibrocartilage

[+] Author and Article Information
Kelsey L. Kleinhans

Orthopaedic Biomechanics Laboratory,
Department of Biomedical Engineering,
University of Miami,
1251 Memorial Drive, MEA 219,
Coral Gables, FL 33124-0621
e-mail: k.kleinhans@umiami.edu

Alicia R. Jackson

Orthopaedic Biomechanics Laboratory,
Department of Biomedical Engineering,
University of Miami,
1251 Memorial Drive, MEA 207,
Coral Gables, FL 33124-0621
e-mail: a.jackson2@miami.edu

1Corresponding author.

Manuscript received August 18, 2016; final manuscript received December 12, 2016; published online January 23, 2017. Assoc. Editor: James C. Iatridis.

J Biomech Eng 139(3), 034502 (Jan 23, 2017) (6 pages) Paper No: BIO-16-1345; doi: 10.1115/1.4035537 History: Received August 18, 2016; Revised December 12, 2016

A nearly avascular tissue, the knee meniscus relies on diffusive transport for nutritional supply to cells. Nutrient transport depends on solute partitioning in the tissue, which governs the amount of nutrients that can enter a tissue. The purpose of the present study was to investigate the effects of mechanical strain, tissue region, and tissue composition on the partition coefficient of glucose in meniscus fibrocartilage. A simple partitioning experiment was employed to measure glucose partitioning in porcine meniscus tissues from two regions (horn and central), from both meniscal components (medial and lateral), and at three levels of compression (0%, 10%, and 20%). Partition coefficient values were correlated to strain level, water volume fraction, and glycosaminoglycan (GAG) content of tissue specimens. Partition coefficient values ranged from 0.47 to 0.91 (n = 48). Results show that glucose partition coefficient is significantly (p < 0.001) affected by compression, decreasing with increasing strain. Furthermore, we did not find a statistically significant effect of tissue when comparing medial versus lateral (p = 0.181) or when comparing central and horn regions (p = 0.837). There were significant positive correlations between tissue water volume fraction and glucose partitioning for all groups. However, the correlation between GAG content and partitioning was only significant in the lateral horn group. Determining how glucose partitioning is affected by tissue composition and loading is necessary for understanding nutrient availability and related tissue health and/or degeneration. Therefore, this study is important for better understanding the transport and nutrition-related mechanisms of meniscal degeneration.

FIGURES IN THIS ARTICLE
<>
Copyright © 2017 by ASME
Your Session has timed out. Please sign back in to continue.

References

Englund, M. , Haugen, I. K. , Guermazi, A. , Roemer, F. W. , Niu, J. , Neogi, T. , Aliabadi, P. , and Felson, D. T. , 2016, “ Evidence That Meniscus Damage may be a Component of Osteoarthritis: The Framingham Study,” Osteoarthritis Cartilage, 24(2), pp. 270–273. [CrossRef] [PubMed]
Murphy, L. , and Helmick, C. G. , 2012, “ The Impact of Osteoarthritis in the United States: A Population-Health Perspective,” Am. J. Nurs., 112(3 Suppl 1), pp. S13–S19. [CrossRef] [PubMed]
Sweigart, M. A. , and Athanasiou, K. A. , 2001, “ Toward Tissue Engineering of the Knee Meniscus,” Tissue Eng., 7(2), pp. 111–129. [CrossRef] [PubMed]
McDevitt, C. A. , and Webber, R. J. , 1990, “ The Ultrastructure and Biochemistry of Meniscal Cartilage,” Clin. Orthop. Relat. Res., 252, pp. 8–18.
Danzig, L. A. , Hargens, A. R. , Gershuni, D. H. , Skyhar, M. J. , Sfakianos, P. N. , and Akeson, W. H. , 1987, “ Increased Transsynovial Transport With Continuous Passive Motion,” J. Orthop. Res., 5(3), pp. 409–413. [CrossRef] [PubMed]
Makris, E. A. , Hadidi, P. , and Athanasiou, K. A. , 2011, “ The Knee Meniscus: Structure-Function, Pathophysiology, Current Repair Techniques, and Prospects for Regeneration,” Biomaterials, 32(30), pp. 7411–7431. [CrossRef] [PubMed]
Heywood, H. K. , Bader, D. L. , and Lee, D. A. , 2006, “ Rate of Oxygen Consumption by Isolated Articular Chondrocytes is Sensitive to Medium Glucose Concentration,” J. Cell. Physiol., 206(2), pp. 402–410. [CrossRef] [PubMed]
Bibby, S. R. , and Urban, J. P. , 2004, “ Effect of Nutrient Deprivation on the Viability of Intervertebral Disc Cells,” Eur. Spine J., 13(8), pp. 695–701. [CrossRef] [PubMed]
Holm, S. , Maroudas, A. , Urban, J. P. , Selstam, G. , and Nachemson, A. , 1981, “ Nutrition of the Intervertebral Disc: Solute Transport and Metabolism,” Connect. Tissue Res., 8(2), pp. 101–119. [CrossRef] [PubMed]
Cisewski, S. E. , Zhang, L. , Kuo, J. , Wright, G. J. , Wu, Y. , Kern, M. J. , and Yao, H. , 2015, “ The Effects of Oxygen Level and Glucose Concentration on the Metabolism of Porcine TMJ Disc Cells,” Osteoarthritis Cartilage, 23(10), pp. 1790–1796. [CrossRef] [PubMed]
Richardson, S. , Neama, G. , Phillips, T. , Bell, S. , Carter, S. D. , Moley, K. H. , Moley, J. F. , Vannucci, S. J. , and Mobasheri, A. , 2003, “ Molecular Characterization and Partial cDNA Cloning of Facilitative Glucose Transporters Expressed in Human Articular Chondrocytes; Stimulation of 2-Deoxyglucose Uptake by IGF-I and Elevated MMP-2 Secretion by Glucose Deprivation,” Osteoarthritis Cartilage, 11(2), pp. 92–101. [CrossRef] [PubMed]
Heywood, H. K. , Bader, D. L. , and Lee, D. A. , 2006, “ Glucose Concentration and Medium Volume Influence Cell Viability and Glycosaminoglycan Synthesis in Chondrocyte-Seeded Alginate Constructs,” Tissue Eng., 12(12), pp. 3487–3496. [CrossRef] [PubMed]
Fetter, N. L. , Leddy, H. A. , Guilak, F. , and Nunley, J. A. , 2006, “ Composition and Transport Properties of Human Ankle and Knee Cartilage,” J. Orthop. Res., 24(2), pp. 211–219. [CrossRef] [PubMed]
Maroudas, A. , 1968, “ Physicochemical Properties of Cartilage in the Light of Ion Exchange Theory,” Biophys. J., 8(5), pp. 575–595. [CrossRef] [PubMed]
Maroudas, A. , Stockwell, R. A. , Nachemson, A. , and Urban, J. , 1975, “ Factors Involved in the Nutrition of the Human Lumbar Intervertebral Disc: Cellularity and Diffusion of Glucose In Vitro,” J. Anat., 120(1), pp. 113–130. [PubMed]
Maroudas, A. , 1976, “ Transport of Solutes Through Cartilage: Permeability to Large Molecules,” J. Anat., 122(2), pp. 335–347. [PubMed]
Torzilli, P. A. , Grande, D. A. , and Arduino, J. M. , 1998, “ Diffusive Properties of Immature Articular Cartilage,” J. Biomed. Mater. Res., 40(1), pp. 132–138. [CrossRef] [PubMed]
Quinn, T. M. , Morel, V. , and Meister, J. J. , 2001, “ Static Compression of Articular Cartilage can Reduce Solute Diffusivity and Partitioning: Implications for the Chondrocyte Biological Response,” J. Biomech., 34(11), pp. 1463–1469. [CrossRef] [PubMed]
Quinn, T. M. , Kocian, P. , and Meister, J. J. , 2000, “ Static Compression is Associated With Decreased Diffusivity of Dextrans in Cartilage Explants,” Arch. Biochem. Biophys., 384(2), pp. 327–334. [CrossRef] [PubMed]
Nimer, E. , Schneiderman, R. , and Maroudas, A. , 2003, “ Diffusion and Partition of Solutes in Cartilage Under Static Load,” Biophys. Chem., 106(2), pp. 125–146. [CrossRef] [PubMed]
Garcia, A. M. , Szasz, N. , Trippel, S. B. , Morales, T. I. , Grodzinsky, A. J. , and Frank, E. H. , 2003, “ Transport and Binding of Insulin-Like Growth Factor I Through Articular Cartilage,” Arch. Biochem. Biophys., 415(1), pp. 69–79. [CrossRef] [PubMed]
Roberts, S. , Urban, J. P. , Evans, H. , and Eisenstein, S. M. , 1996, “ Transport Properties of the Human Cartilage Endplate in Relation to Its Composition and Calcification,” Spine, 21(4), pp. 415–420. [CrossRef] [PubMed]
Schneiderman, R. , Snir, E. , Popper, O. , Hiss, J. , Stein, H. , and Maroudas, A. , 1995, “ Insulin-Like Growth Factor-I and Its Complexes in Normal Human Articular Cartilage: Studies of Partition and Diffusion,” Arch. Biochem. Biophys., 324(1), pp. 159–172. [CrossRef] [PubMed]
Torzilli, P. A. , 1993, “ Effects of Temperature, Concentration and Articular Surface Removal on Transient Solute Diffusion in Articular Cartilage,” Med. Biol. Comput. Eng., 31(Suppl. 1), pp. S93–S98. [CrossRef]
Jackson, A. R. , Yuan, T. Y. , Huang, C. Y. , Brown, M. D. , and Gu, W. Y. , 2012, “ Nutrient Transport in Human Annulus Fibrosus is Affected by Compressive Strain and Anisotropy,” Ann. Biomed. Eng., 40(12), pp. 2551–2558. [CrossRef] [PubMed]
Changoor, A. , Fereydoonzad, L. , Yaroshinsky, A. , and Buschmann, M. D. , 2010, “ Effects of Refrigeration and Freezing on the Electromechanical and Biomechanical Properties of Articular Cartilage,” ASME J. Biomech. Eng., 132(6), p. 064502. [CrossRef]
Gu, W. Y. , Lewis, B. , Lai, W. M. , Ratcliffe, A. , and Mow, V. C. , 1996, “ A Technique for Measuring Volume and True Density of the Solid Matrix of Cartilaginous Tissues,” J. Biomech., 33, pp. 89–90.
Jackson, A. R. , Yuan, T. Y. , Huang, C. Y. , Travascio, F. , and Gu, W. Y. , 2008, “ Effect of Compression and Anisotropy on the Diffusion of Glucose in Annulus Fibrosus,” Spine, 33(1), pp. 1–7. [CrossRef] [PubMed]
Farndale, R. W. , Sayers, C. A. , and Barrett, A. J. , 1982, “ A Direct Spectrophotometric Microassay for Sulfated Glycosaminoglycans in Cartilage Cultures,” Connect. Tissue Res., 9(4), pp. 247–248. [CrossRef] [PubMed]
Jackson, A. R. , and Gu, W. Y. , 2009, “ Transport Properties of Cartilaginous Tissues,” Curr. Rheumatol. Rev., 5(1), pp. 40–50. [CrossRef] [PubMed]
Travascio, F. , Jackson, A. R. , Brown, M. D. , and Gu, W. Y. , 2009, “ Relationship Between Solute Transport Properties and Tissue Morphology in Human Annulus Fibrosus,” J. Orthop. Res., 27(12), pp. 1625–1630. [CrossRef] [PubMed]
Martin Seitz, A. , Galbusera, F. , Krais, C. , Ignatius, A. , and Durselen, L. , 2013, “ Stress-Relaxation Response of Human Menisci Under Confined Compression Conditions,” J. Mech. Behav. Biomed. Mater., 26, pp. 68–80. [CrossRef] [PubMed]
Eckstein, F. , Lemberger, B. , Stammberger, T. , Englmeier, K. H. , and Reiser, M. , 2000, “ Patellar Cartilage Deformation In Vivo After Static Versus Dynamic Loading,” J. Biomech., 33(7), pp. 819–825. [CrossRef] [PubMed]
Chia, H. N. , and Hull, M. L. , 2008, “ Compressive Moduli of the Human Medial Meniscus in the Axial and Radial Directions at Equilibrium and at a Physiological Strain Rate,” J. Orthop. Res., 26(7), pp. 951–956. [CrossRef] [PubMed]
Yang, N. H. , Canavan, P. K. , Nayeb-Hashemi, H. , Najafi, B. , and Vaziri, A. , 2010, “ Protocol for Constructing Subject-Specific Biomechanical Models of Knee Joint,” Comput. Methods Biomech. Biomed. Eng., 13(5), pp. 589–603. [CrossRef]
O'Hara, B. P. , Urban, J. P. , and Maroudas, A. , 1990, “ Influence of Cyclic Loading on the Nutrition of Articular Cartilage,” Ann. Rheum. Dis., 49(7), pp. 536–539. [CrossRef] [PubMed]
Katz, M. M. , Hargens, A. R. , and Garfin, S. R. , 1986, “ Intervertebral Disc Nutrition. Diffusion Versus Convection,” Clin. Orthop., 210, pp. 243–245.
Urban, J. P. , Holm, S. , Maroudas, A. , and Nachemson, A. , 1982, “ Nutrition of the Intervertebral Disc: Effect of Fluid Flow on Solute Transport,” Clin. Orthop., 170, pp. 296–302.
Upton, M. L. , Chen, J. , Guilak, F. , and Setton, L. A. , 2003, “ Differential Effects of Static and Dynamic Compression on Meniscal Cell Gene Expression,” J. Orthop. Res., 21(6), pp. 963–969. [CrossRef] [PubMed]
Imler, S. M. , Doshi, A. N. , and Levenston, M. E. , 2004, “ Combined Effects of Growth Factors and Static Mechanical Compression on Meniscus Explant Biosynthesis,” Osteoarthritis Cartilage, 12(9), pp. 736–744. [CrossRef] [PubMed]
Kleinhans, K. L. , Jaworski, L. M. , Schneiderbauer, M. M. , and Jackson, A. R. , 2015, “ Effect of Static Compressive Strain, Anisotropy, and Tissue Region on the Diffusion of Glucose in Meniscus Fibrocartilage,” ASME J. Biomech. Eng., 137(10), p. 101004. [CrossRef]
Kleinhans, K. L. , McMahan, J. B. , and Jackson, A. R. , 2016, “ Electrical Conductivity and Ion Diffusion in Porcine Meniscus: Effects of Strain, Anisotropy, and Tissue Region,” J. Biomech., 49(13), pp. 3041–3046. [CrossRef] [PubMed]
Sweigart, M. A. , Zhu, C. F. , Burt, D. M. , DeHoll, P. D. , Agrawal, C. M. , Clanton, T. O. , and Athanasiou, K. A. , 2004, “ Intraspecies and Interspecies Comparison of the Compressive Properties of the Medial Meniscus,” Ann. Biomed. Eng., 32(11), pp. 1569–1579. [CrossRef] [PubMed]
Burstein, D. , Gray, M. L. , Hartman, A. L. , Gipe, R. , and Foy, B. D. , 1993, “ Diffusion of Small Solutes in Cartilage as Measured by Nuclear Magnetic Resonance (NMR) Spectroscopy and Imaging,” J. Orthop. Res., 11(4), pp. 465–478. [CrossRef] [PubMed]
Maroudas, A. , 1970, “ Distribution and Diffusion of Solutes in Articular Cartilage,” Biophys. J., 10(5), pp. 365–379. [CrossRef] [PubMed]
Torzilli, P. A. , Arduino, J. M. , Gregory, J. D. , and Bansal, M. , 1997, “ Effect of Proteoglycan Removal on Solute Mobility in Articular Cartilage,” J. Biomech., 30(9), pp. 895–902. [CrossRef] [PubMed]
Almarza, A. J. , and Athanasiou, K. A. , 2004, “ Design Characteristics for the Tissue Engineering of Cartilaginous Tissues,” Ann. Biomed. Eng., 32(1), pp. 2–17. [CrossRef] [PubMed]
Killian, M. L. , Lepinski, N. M. , Haut, R. C. , and Haut Donahue, T. L. , 2010, “ Regional and Zonal Histo-Morphological Characteristics of the Lapine Menisci,” Anat. Rec., 293(12), pp. 1991–2000. [CrossRef]
Sanchez-Adams, J. , Willard, V. P. , and Athanasiou, K. A. , 2011, “ Regional Variation in the Mechanical Role of Knee Meniscus Glycosaminoglycans,” J. Appl. Physiol., 111(6), pp. 1590–1596. [CrossRef] [PubMed]
Sweigart, M. A. , and Athanasiou, K. A. , 2005, “ Biomechanical Characteristics of the Normal Medial and Lateral Porcine Knee Menisci,” Proc. Inst. Mech. Eng., Part H, 219(1), pp. 53–62. [CrossRef]
Joshi, M. D. , Suh, J. K. , Marui, T. , and Woo, S. L. , 1995, “ Interspecies Variation of Compressive Biomechanical Properties of the Meniscus,” J. Biomed. Mater. Res., 29(7), pp. 823–828. [CrossRef] [PubMed]
Chu, C. R. , Szczodry, M. , and Bruno, S. , 2010, “ Animal Models for Cartilage Regeneration and Repair,” Tissue Eng., Part B, 16(1), pp. 105–115. [CrossRef]
Di Giancamillo, A. , Deponti, D. , Addis, A. , Domeneghini, C. , and Peretti, G. M. , 2014, “ Meniscus Maturation in the Swine Model: Changes Occurring Along With Anterior to Posterior and Medial to Lateral Aspect During Growth,” J. Cell. Mol. Med., 18(10), pp. 1964–1974. [CrossRef] [PubMed]

Figures

Grahic Jump Location
Fig. 1

(a) Schematic showing the location and size of specimens obtained from the porcine knee meniscus, along with the lateral and medial menisci; (b) Schematic drawing of the partition coefficient chamber including the solution chamber, o-ring, tissue sample, porous filter, bolts, and cap; and (c) flow chart showing the sequence of baths used to calculate the partition coefficient

Grahic Jump Location
Fig. 2

Correlation between glucose partition coefficient and (a) static compressive strain; (b) tissue water volume fraction, ϕw ; and (c) GAG content. Note for all figures, n = 48; regression analysis shown is for pooled data, although individual groups are shown. Correlation coefficients and p-values for all groups are shown in Table 2.

Tables

Errata

Some tools below are only available to our subscribers or users with an online account.

Related Content

Customize your page view by dragging and repositioning the boxes below.

Related Journal Articles
Related eBook Content
Topic Collections

Sorry! You do not have access to this content. For assistance or to subscribe, please contact us:

  • TELEPHONE: 1-800-843-2763 (Toll-free in the USA)
  • EMAIL: asmedigitalcollection@asme.org
Sign In