Examining Differences in Local Collagen Fiber Crimp Frequency Throughout Mechanical Testing in a Developmental Mouse Supraspinatus Tendon Model

Journal of Biomechanical Engineering - Tập 134 Số 4 - 2012
Kristin S. Miller1, Brianne K. Connizzo1, Elizabeth Feeney1, Jennica J. Tucker1, Louis J. Soslowsky1
1McKay Orthopaedic Research Laboratory, University of Pennsylvania, 424 Stemmler Hall, 36th and Hamilton Walk, Philadelphia, PA, 19104-6081

Tóm tắt

Crimp morphology is believed to be related to tendon mechanical behavior. While crimp has been extensively studied at slack or nondescript load conditions in tendon, few studies have examined crimp at specific, quantifiable loading conditions. Additionally, the effect of the number of cycles of preconditioning on collagen fiber crimp behavior has not been examined. Further, the dependence of collagen fiber crimp behavior on location and developmental age has not been examined in the supraspinatus tendon. Local collagen fiber crimp frequency is quantified throughout tensile mechanical testing using a flash freezing method immediately following the designated loading protocol. Samples are analyzed quantitatively using custom software and semi-quantitatively using a previously established method to validate the quantitative software. Local collagen fiber crimp frequency values are compared throughout the mechanical test to determine where collagen fiber frequency changed. Additionally, the effect of the number of preconditioning cycles is examined compared to the preload and toe-region frequencies to determine if increasing the number of preconditioning cycles affects crimp behavior. Changes in crimp frequency with age and location are also examined. Decreases in collagen fiber crimp frequency were found at the toe-region at all ages. Significant differences in collagen fiber crimp frequency were found between the preload and after preconditioning points at 28 days. No changes in collagen fiber crimp frequency were found between locations or between 10 and 28 days old. Local collagen fiber crimp frequency throughout mechanical testing in a postnatal developmental mouse SST model was measured. Results confirmed that the uncrimping of collagen fibers occurs primarily in the toe-region and may contribute to the tendon’s nonlinear behavior. Additionally, results identified changes in collagen fiber crimp frequency with an increasing number of preconditioning cycles at 28 days, which may have implications on the measurement of mechanical properties and identifying a proper reference configuration.

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Tài liệu tham khảo

Cheng, The Effects of Preconditioning Strain on Measured Tissue Properties, J. Biomech., 42, 1360, 10.1016/j.jbiomech.2009.03.023

Woo, Mechanical Properties of Tendons and Ligaments. I. Quasi-Static and Nonlinear Viscoelastic Properties, Biorheology, 19, 385, 10.3233/BIR-1982-19301

Miller, K. S., Edelstein, L., Connizzo, B. K., and Soslowsky, L. J., 2012, “Effect of Preconditioning and Stress Relaxation on Local Collagen Fiber Re-Alignment: Inhomogeneous Properties of Rat Supraspinatus Tendon,” J. Biomech. Eng., in press.

Quinn, Preconditioning is Correlated With Altered Collagen Fiber Alignment in Ligament, J. Biomech. Eng., 133, 064506, 10.1115/1.4004205

Houssen, Monitoring Micrometer-Scale Collagen Organization in Rat-Tail Tendon Upon Mechanical Strain Using Second Harmonic Microscopy, J. Biomech., 44, 2047, 10.1016/j.jbiomech.2011.05.009

Franchi, Different Crimp Patterns in Collagen Fibrils Relate to the Subfibrillar Arrangement, Connect. Tissue Res., 49, 85, 10.1080/03008200801913635

Franchi, Crimp Morphology in Relaxed and Stretched Rat Achilles Tendon, J. Anat., 210, 1, 10.1111/j.1469-7580.2006.00666.x

Franchi, Tendon and Ligament Fibrillar Crimps Give Rise to Left-Handed Helices of Collagen Fibrils in Both Planar and Helical Crimps, J. Anat., 216, 301, 10.1111/j.1469-7580.2009.01188.x

Franchi, Collagen Fibre Arrangement and Functional Crimping Pattern of the Medial Collateral Ligament in the Rat Knee, Knee Surg. Sports Traumatol. Arthrosc., 18, 1671, 10.1007/s00167-010-1084-6

Hurschler, Scanning Electron Microscopic Characterization of Healing and Normal Rat Ligament Microstructure Under Slack and Loaded Conditions, Connect. Tissue Res., 44, 59, 10.1080/03008200390200193

Miller, K. S., Connizzo, B. K., and Soslowsky, L. J., 2011, “Collagen Fiber Re-Alignment in a Neonatal Developmental Mouse Supraspinatus Tendon Model,” Ann. Biomed. Eng., in press.10.1007/s10439-011-0490-3

Diamant, Collagen; Ultrastructure and its Relation to Mechanical Properties as a Function of Ageing, Proc. R. Soc. London, Ser. B, 180, 293, 10.1098/rspb.1972.0019

Gathercole, Crimp Morphology in the Fibre-Forming Collagens, Matrix, 11, 214, 10.1016/S0934-8832(11)80161-7

Shah, Development of Crimp Morphology and Cellular Changes in Chick Tendons, Dev. Biol., 94, 499, 10.1016/0012-1606(82)90366-9

Ansorge, Mechanical, Compositional, and Structural Properties of the Post-Natal Mouse Achilles Tendon, Ann. Biomed. Eng., 39, 1904, 10.1007/s10439-011-0299-0

Boorman, Using a Freeze Substitution Fixation Technique and Histological Crimp Analysis for Characterizing Regions of Strain in Ligaments Loaded in Situ, J. Orthop. Res., 24, 793, 10.1002/jor.20081

Stouffer, The Relationship Between Crimp Pattern and Mechanical Response of Human Patellar Tendon-Bone Units, J. Biomech. Eng., 107, 158, 10.1115/1.3138536

Lake, Effect of Fiber Distribution and Realignment on the Nonlinear and Inhomogeneous Mechanical Properties of Human Supraspinatus Tendon Under Longitudinal Tensile Loading, J. Orthop. Res., 27, 1596, 10.1002/jor.20938

Thomopoulos, Variation of Biomechanical, Structural, and Compositional Properties Along the Tendon to Bone Insertion Site, J. Orthop. Res., 21, 413, 10.1016/S0736-0266(03)0057-3

Festing, Design and Statistical Methods in Studies Using Animal Models of Development, ILAR J., 47, 5, 10.1093/ilar.47.1.5

Peltz, Exercise Following a Short Immobilization Period is Detrimental to Tendon Properties and Joint Mechanics in a Rat Rotator Cuff Injury Model, J. Orthop. Res., 28, 841, 10.1002/jor.21059

Thornton, Ligament Creep Recruits Fibres at Low Stresses and can Lead to Modulus-Reducing Fibre Damage at Higher Creep Stresses: A Study in Rabbit Medial Collateral Ligament Model, J. Orthop. Res., 20, 967, 10.1016/S0736-0266(02)00028-1

Landerman, An Empirical Evaluation of the Predictive Mean Matching Method for Imputing Missing Values, Sociolog. Methods Res., 26, 3, 10.1177/0049124197026001001

Little, Missing-Data Adjustments in Large Surveys, J. Bus. Econ. Stat., 6, 287, 10.2307/1391878

Yuan, Multiple Imputation Using SAS Software, J. Stat. Software, 45, 1

Birk, Collagen Fibrillogenesis in Situ: Fibril Segments Undergo Post-Depositional Modifications Resulting in Linear and Lateral Growth During Matrix Development, Dev. Dyn., 202, 229, 10.1002/aja.1002020303

Birk, Collagen Fibrillogenesis in Situ: Fibril Segments Become Long Fibrils as the Developing Tendon Matures, Dev. Dyn., 208, 291, 10.1002/(SICI)1097-0177(199703)208:3<291::AID-AJA1>3.0.CO;2-D

Zhang, Development of Tendon Structure and Function: Regulation of Collagen Fibrillogenesis, J. Musculoskeletal and Neuronal Interact., 5, 5

Provenzano, Collagen Fibril Morphology and Organization: Implications for Force Transmission in Ligament and Tendon, Matrix Biol., 25, 71, 10.1016/j.matbio.2005.09.005

Hansen, Recruitment of Tendon Crimp With Applied Tensile Strain, J. Biomech. Eng., 124, 72, 10.1115/1.1427698

Woo, Injury and Repair of Ligaments and Tendons, Annu. Rev. Biomed. Eng., 2, 83, 10.1146/annurev.bioeng.2.1.83

Rigby, Effect of Cyclic Extension on the Physical Properties of Tendon Collagen and Its Possible Relation to Biological Ageing of Collagen, Nature, 202, 1072, 10.1038/2021072a0

Rigby, The Mechanical Properties of Rat Tail Tendon, J. Gen. Physiol., 43, 265, 10.1085/jgp.43.2.265

Screen, An Investigation Into the Effects of the Hierarchical Structure of Tendon Fascicles on Micromechanical Properties, Proc. Inst. Mech. Eng., Part H: J. Eng. Med., 218, 109, 10.1243/095441104322984004

Viidik, Simultaneous Mechanical and Light Microscopic Studies of Collagen Fibers, Z. Anat. Entwicklungsgesch, 136, 204, 10.1007/BF00519178

Duenwald, Stress Relaxation and Recovery in Tendon and Ligament: Experiment and Modeling, Biorheology, 47, 1, 10.3233/BIR-2010-0559

Lokshin, Viscoelasticity and Preconditioning of Rat Skin Under Uniaxial Stretch: Microstructural Constitutive Characterization, J. Biomech. Eng., 131, 031009, 10.1115/1.3049479

Sellaro, Effects of Collagen Fiber Orientation on the Response of Biologically Derived Soft Tissue Biomaterials to Cyclic Loading, J. Biomed. Mater. Res. Part A, 80, 194, 10.1002/jbm.a.30871