Tensile properties, collagen content, and crosslinks in connective tissues of the immature knee joint

Eleswarapu, Sriram V.<sup>1,2</sup>; Responte, Donald J.<sup>1</sup>; Athanasiou, Kyriacos A.<sup>3</sup>

Affiliations

¹Department of Bioengineering, Rice University, Houston, Texas, United States of America

²Medical Scientist Training Program, Baylor College of Medicine, Houston, Texas, United States of America

³Department of Biomedical Engineering, University of California, Davis, California, United States of America

Abstract

Background: The major connective tissues of the knee joint act in concert during locomotion to provide joint stability, smooth articulation, shock absorption, and distribution of mechanical stresses. These functions are largely conferred by the intrinsic material properties of the tissues, which are in turn determined by biochemical composition. A thorough understanding of the structure-function relationships of the connective tissues of the knee joint is needed to provide design parameters for efforts in tissue engineering.

Methodology/Principal Findings: The objective of this study was to perform a comprehensive characterization of the tensile properties, collagen content, and pyridinoline crosslink abundance of condylar cartilage, patellar cartilage, medial and lateral menisci, cranial and caudal cruciate ligaments (analogous to anterior and posterior cruciate ligaments in humans, respectively), medial and lateral collateral ligaments, and patellar ligament from immature bovine calves. Tensile stiffness and strength were greatest in the menisci and patellar ligament, and lowest in the hyaline cartilages and cruciate ligaments; these tensile results reflected trends in collagen content. Pyridinoline crosslinks were found in every tissue despite the relative immaturity of the joints, and significant differences were observed among tissues. Notably, for the cruciate ligaments and patellar ligament, crosslink density appeared more important in determining tensile stiffness than collagen content.

Conclusions/Significance: To our knowledge, this study is the first to examine tensile properties, collagen content, and pyridinoline crosslink abundance in a direct head-to-head comparison among all of the major connective tissues of the knee. This is also the first study to report results for pyridinoline crosslink density that suggest its preferential role over collagen in determining tensile stiffness for certain tissues.

Links

DOI: 10.1371/journal.pone.0026178

PubMed: 22022553

WoS: 000295978600042

History

Received: 2011-08-01

Accepted: 2011-09-21

Online: 2011-10-13

Cited Works (13)

Year	Entry
2004	Almarza AJ, Athanasiou KA. Design characteristics for the tissue engineering of cartilaginous tissues. Ann Biomed Eng. January 2004;32(1):2-17.
1996	Sah RL, Trippel SB, Grodzinsky AJ. Differential effects of serum, insulin-like growth factor-I, and fibroblast growth factor-2 on the maintenance of cartilage physical properties during long-term culture. J Orthop Res. January 1996;14(1):44-52.
2007	Moutos FT, Freed LE, Guilak F. A biomimetic three-dimensional woven composite scaffold for functional tissue engineering of cartilage. Nat Mater. February 2007;6(2):162-167.
2006	Hu JC, Athanasiou KA. A self-assembling process in articular cartilage tissue engineering. Tissue Eng. April 2006;12(4):969-979.
2007	Lohmander LS, Englund PM, Dahl LL, Roos EM. The long-term consequence of anterior cruciate ligament and meniscus injuries: osteoarthritis. Am J Sports Med. October 2007;35(10):1756-1769.
2000	Mauck RL, Soltz MA, Wang CCB, Wong DD, Chao P-HG, Valhmu WB, Hung CT, Ateshian GA. Functional tissue engineering of articular cartilage through dynamic loading of chondrocyte-seeded agarose gels. J Biomech Eng. June 2000;122(3):252-260.
1980	Kurosawa H, Fukubayashi T, Nakajima H. Load-bearing mode of the knee joint: physical behavior of the knee joint with or without menisci. Clin Orthop Relat Res. June 1980;149:283-290.
2000	Woo SL-Y, Debski RE, Zeminski J, Abramowitch SD, Chan Saw SS, Fenwick JA. Injury and repair of ligaments and tendons. Annu Rev Biomed Eng. 2000;2:83-118.
2004	Almarza AJ, Athanasiou KA. Seeding techniques and scaffolding choice for tissue engineering of the temporomandibular joint disk. Tissue Eng. November 2004;10(11-12):1787-1795.
2003	Williamson AK, Chen AC, Masuda K, Thonar EJ, Sah RL. Tensile mechanical properties of bovine articular cartilage: variations with growth and relationships to collagen network components. J Orthop Res. September 2003;21(5):872-880.
2006	Aufderheide AC, Athanasiou KA. A direct compression stimulator for articular cartilage and meniscal explants. Ann Biomed Eng. September 2006;34(9):1463-1474.
2006	Hootman JM, Helmick CG. Projections of US prevalence of arthritis and associated activity limitations. Arthritis Rheum. January 2006;54(1):226-229.
1997	Bank RA, Beekman B, Verzijl N, de Roos JADM, Nico Sakkee A, TeKoppele JM. Sensitive fluorimetric quantitation of pyridinium and pentosidine crosslinks in biological samples in a single high-performance liquid chromatographic run. J Chromatogr B Biomed Sci Appl. December 5, 1997;703:37.

Cited By (16)

Year	Entry
2014	Makris EA, Responte DJ, Paschos NK, Hu JC, Athanasiou KA. Developing functional musculoskeletal tissues through hypoxia and lysyl oxidase-induced collagen cross-linking. Proc Natl Acad Sci USA. November 11, 2014;111(45):E4832-E4841.
2016	Yoshida K. Characterizing the Structure-Function Relationships of the Mouse Cervix in Pregnancy: Towards the Development of a Hormone-Mediated Material Model for Cervical Remodeling [PhD thesis]. Columbia University; 2016.
2018	Durney KM. Investigations of Articular Cartilage Delamination Wear and a Novel Laser Treatment Strategy to Increase Wear Resistance [PhD thesis]. Columbia University; 2018.
2014	Puetzer JL. Development of Engineered Menisci With Native-Like Organization Using High Density Collagen Gels and Mechanical Stimulation [PhD thesis]. Ithaca, NY: Cornell University; August 2014.
2020	Han B. Decorin Regulates the Structure and Biomechanical Functions of Articular Cartilage Extracellular Matrix in Health and Disease [PhD thesis]. Drexel University; October 2020.
2021	Conway CK. Biaxial Contractility, Passive Biomechanics, and Murine Cervical Modeling [PhD thesis]. Tulane University; April 2021.
2014	MacBarb RF. A Scaffold-Free Approach to Optimizing a Biomimetic TMJ Disc [PhD thesis]. Davis, University of California; 2014.
2014	Murphy MK. Engineering Functional Cartilage for the Temporomandibular Joint [PhD thesis]. Davis, University of California; 2014.
2015	Lee JK. Bioactive and Mechanical Stimuli for Engineering Neocartilage With Native Tissue-Like Tensile Properties [PhD thesis]. Davis, University of California; 2015.
2016	Cissell DD. Toward Detection of Early Degeneration, Restoration of Function, and Evaluation of Regeneration in Cartilage [PhD thesis]. Davis, University of California; 2016.
2016	Huang BJ. Scale-Up of Engineered, Large, Anatomically Shaped Neocartilage With Robust Biomechanical Properties [PhD thesis]. Davis, University of California; 2016.
2017	Brown WEHP. Engineering Osteochondral Constructs to Treat Articular Cartilage Defects [PhD thesis]. Davis, University of California; 2017.
2017	Huwe LW. Functional Articular Cartilage Engineering for Regenerating the Patellofemoral and Temporomandibular Joints [PhD thesis]. Davis, University of California; 2017.
2020	Link JM. Toward Enhancing the Durability and Integration of Engineered Articular Cartilage [PhD thesis]. Irvine, CA: Irvine, University of California; 2020.
2016	Qu F. Biomaterial-Mediated Reprogramming of the Wound Interface to Enhance Meniscal Repair [PhD thesis]. Philadelphia, PA: University of Pennsylvania; 2016.
2017	Fang F. Composition-Dependent Mechanisms of Multiscale Tendon Mechanics [PhD thesis]. St. Louis, MO: Washington University in St. Louis; August 2017.