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      Mechanobiology of the Meniscus

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          Abstract

          The meniscus plays a critical biomechanical role in the knee, providing load support, joint stability, and congruity. Importantly, growing evidence indicates that the mechanobiologic response of meniscal cells plays a critical role in the physiologic, pathologic, and repair responses of the meniscus. Here we review experimental and theoretical studies that have begun to directly measure the biomechanical effects of joint loading on the meniscus under physiologic and pathologic conditions, showing that the menisci are exposed to high contact stresses, resulting in a complex and nonuniform stress-strain environment within the tissue. By combining microscale measurements of the mechanical properties of meniscal cells and their pericellular and extracellular matrix regions, theoretical and experimental models indicate that the cells in the meniscus are exposed to a complex and inhomogeneous environment of stress, strain, fluid pressure, fluid flow, and a variety of physicochemical factors. Studies across a range of culture systems from isolated cells to tissues have revealed that the biological response of meniscal cells is directly influenced by physical factors, such as tension, compression, and hydrostatic pressure. In addition, these studies have provided new insights into the mechanotransduction mechanisms by which physical signals are converted into metabolic or pro/anti-inflammatory responses. Taken together, these in vivo and in vitro studies show that mechanical factors play an important role in the health, degeneration, and regeneration of the meniscus. A more thorough understanding of the mechanobiologic responses of the meniscus will hopefully lead to therapeutic approaches to prevent degeneration and enhance repair of the meniscus.

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          Material properties and structure-function relationships in the menisci.

          The menisci serve several important biomechanical functions in the knee. They distribute stresses over a broad area of articular cartilage, absorb shocks during dynamic loading, and probably assist in joint lubrication. These functions enhance the ability of articular cartilage to provide a smooth, near-frictionless articulation and to distribute loads evenly to the underlying bone of the femur and tibia. In addition, the menisci provide stability to the injured knee when the cruciate ligaments or other primary stabilizers are deficient. The ability to perform these mechanical functions is based on the intrinsic material properties of the menisci as well as their gross anatomic structure and attachments. The material properties of the menisci are determined by their biochemical composition and, perhaps more important, by the organization and interactions of the major tissue constituents: water, proteoglycan, and collagen. Interactions among the important constituents of the fibrocartilage matrix cause meniscal tissue to behave as a fiber-reinforced, porous, permeable composite material similar to articular cartilage, in which frictional drag caused by fluid flow governs its response to dynamic loading. The menisci are one-half as stiff in compression and dissipate more energy under dynamic loading than articular cartilage. Energy dissipation, or shock absorption, by the menisci is the result of high frictional drag caused by low permeability of the matrix, which is about one-sixth as permeable as articular cartilage. The dynamic shear modulus of meniscal tissue is only one-fourth to one-sixth as great as that of articular cartilage. The coarse, circumferential Type I collagen fiber bundles of the meniscus give the tissue great tensile stiffness (range, 100-300 megapascals) and strength. The highly oriented collagen ultrastructure of the menisci makes the tissue anisotropic in tension, compression, and shear and appears to dominate its behavior under all loading conditions.
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            The structure and function of the pericellular matrix of articular cartilage.

            Chondrocytes in articular cartilage are surrounded by a narrow pericellular matrix (PCM) that is both biochemically and biomechanically distinct from the extracellular matrix (ECM) of the tissue. While the PCM was first observed nearly a century ago, its role is still under investigation. In support of early hypotheses regarding its function, increasing evidence indicates that the PCM serves as a transducer of biochemical and biomechanical signals to the chondrocyte. Work over the past two decades has established that the PCM in adult tissue is defined biochemically by several molecular components, including type VI collagen and perlecan. On the other hand, the biomechanical properties of this structure have only recently been measured. Techniques such as micropipette aspiration, in situ imaging, computational modeling, and atomic force microscopy have determined that the PCM exhibits distinct mechanical properties as compared to the ECM, and that these properties are influenced by specific PCM components as well as disease state. Importantly, the unique relationships among the mechanical properties of the chondrocyte, PCM, and ECM in different zones of cartilage suggest that this region significantly influences the stress-strain environment of the chondrocyte. In this review, we discuss recent advances in the measurement of PCM mechanical properties and structure that further increase our understanding of PCM function. Taken together, these studies suggest that the PCM plays a critical role in controlling the mechanical environment and mechanobiology of cells in cartilage and other cartilaginous tissues, such as the meniscus or intervertebral disc.
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              Biomechanics and mechanobiology in functional tissue engineering.

              The field of tissue engineering continues to expand and mature, and several products are now in clinical use, with numerous other preclinical and clinical studies underway. However, specific challenges still remain in the repair or regeneration of tissues that serve a predominantly biomechanical function. Furthermore, it is now clear that mechanobiological interactions between cells and scaffolds can critically influence cell behavior, even in tissues and organs that do not serve an overt biomechanical role. Over the past decade, the field of "functional tissue engineering" has grown as a subfield of tissue engineering to address the challenges and questions on the role of biomechanics and mechanobiology in tissue engineering. Originally posed as a set of principles and guidelines for engineering of load-bearing tissues, functional tissue engineering has grown to encompass several related areas that have proven to have important implications for tissue repair and regeneration. These topics include measurement and modeling of the in vivo biomechanical environment; quantitative analysis of the mechanical properties of native tissues, scaffolds, and repair tissues; development of rationale criteria for the design and assessment of engineered tissues; investigation of the effects biomechanical factors on native and repair tissues, in vivo and in vitro; and development and application of computational models of tissue growth and remodeling. Here we further expand this paradigm and provide examples of the numerous advances in the field over the past decade. Consideration of these principles in the design process will hopefully improve the safety, efficacy, and overall success of engineered tissue replacements. Copyright © 2014 Elsevier Ltd. All rights reserved.
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                Author and article information

                Journal
                0157375
                4563
                J Biomech
                J Biomech
                Journal of biomechanics
                0021-9290
                1873-2380
                28 February 2015
                09 February 2015
                1 June 2015
                01 June 2016
                : 48
                : 8
                : 1469-1478
                Affiliations
                Department of Orthopaedic Surgery, Duke University Medical Center, Durham, NC 27710
                Author notes
                Address for Correspondence: Dr. Amy L. McNulty, Duke University Medical Center, Department of Orthopaedic Surgery, DUMC 3093, Durham NC 27710 USA, Phone: (919) 684-6882, Fax: (919) 681-8490, alr@ 123456duke.edu
                Article
                NIHMS662822
                10.1016/j.jbiomech.2015.02.008
                4442061
                25731738
                034c30e8-be95-4fc1-9390-b361d32f603a
                © 2015 Published by Elsevier Ltd.

                This manuscript version is made available under the CC BY-NC-ND 4.0 license.

                History
                Categories
                Article

                Biophysics
                mechanical signal transduction,articular cartilage,collagen,fibrochondrocyte,proteoglycan

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