title: Stretch-induced network reconfiguration of collagen fibres in the human facet capsular ligament.
abstract: Biomaterials can display complex spatial patterns of cellular responses to external forces. Revealing and predicting the role of these patterns in material failure require an understanding of the statistical dependencies between spatially distributed changes in a cell's local biomechanical environment, including altered collagen fibre kinematics in the extracellular matrix. Here, we develop and apply a novel extension of network science methods to investigate how excessive tensile stretch of the human cervical facet capsular ligament (FCL), a common source of chronic neck pain, affects the local reorganization of collagen fibres. We define collagen alignment networks based on similarity in fibre alignment angles measured by quantitative polarized light imaging. We quantify the reorganization of these networks following macroscopic loading by describing the dynamic reconfiguration of network communities, regions of the material that display similar fibre alignment angles. Alterations in community structure occur smoothly over time, indicating coordinated adaptation of fibres to loading. Moreover, flexibility, a measure of network reconfiguration, tracks the loss of FCL's mechanical integrity at the onset of anomalous realignment (AR) and regions of AR display altered community structure. These findings use novel network-based techniques to explain abnormal collagen fibre reorganization, a dynamic and coordinated multivariate process underlying tissue failure.
authors.affiliation: Department of Bioengineering, University of Pennsylvania, Philadelphia, PA 19104, USA.
authors.forename: Sijia
authors.initials: S
authors.lastname: Zhang
authors.affiliation: Department of Bioengineering, University of Pennsylvania, Philadelphia, PA 19104, USA Department of Electrical and Systems Engineering, University of Pennsylvania, Philadelphia, PA 19104, USA.
authors.forename: Danielle S
authors.initials: DS
authors.lastname: Bassett
authors.affiliation: Department of Bioengineering, University of Pennsylvania, Philadelphia, PA 19104, USA Department of Neurosurgery, University of Pennsylvania, Philadelphia, PA 19104, USA winkelst@seas.upenn.edu.
authors.forename: Beth A
authors.initials: BA
authors.lastname: Winkelstein
mesh_terms: D000368:Aged; D003094:Collagen / Q000737:chemistry / Q000502:physiology; D006801:Humans; D008022:Ligaments / Q000737:chemistry / Q000502:physiology; D008297:Male; D008875:Middle Aged; D008954:Models, Biological; D013314:Stress, Mechanical; D016474:Weight-Bearing; D021801:Zygapophyseal Joint / Q000737:chemistry / Q000502:physiology
chemical_list: D003094:Collagen
keywords: collagen; community detection; facet capsular ligament; fibre realignment; time-dependent network
references.citation: Biophys J. 2014 Dec 2;107(11):2592-603
references.pmid: 25468338
references.citation: Science. 2010 May 14;328(5980):876-8
references.pmid: 20466926
references.citation: PLoS One. 2009;4(6):e5902
references.pmid: 19529768
references.citation: PLoS Comput Biol. 2014 Oct;10(10):e1003712
references.pmid: 25275860
references.citation: Matrix Biol. 2006 Mar;25(2):71-84
references.pmid: 16271455
references.citation: Nature. 2007 Apr 5;446(7136):664-7
references.pmid: 17410175
references.citation: J Bone Joint Surg Am. 2006 Aug;88(8):1807-16
references.pmid: 16882906
references.citation: Ann Biomed Eng. 2011 Aug;39(8):2163-73
references.pmid: 21538155
references.citation: Chaos. 2014 Mar;24(1):013112
references.pmid: 24697374
references.citation: Stapp Car Crash J. 2000 Nov;44:171-88
references.pmid: 17458726
references.citation: J Biomed Opt. 2009 Sep-Oct;14(5):054010
references.pmid: 19895112
references.citation: Phys Rev E Stat Nonlin Soft Matter Phys. 2012 Jan;85(1 Pt 1):011304
references.pmid: 22400562
references.citation: J Biomech Eng. 2012 Sep;134(9):091005
references.pmid: 22938372
references.citation: Phys Rev E Stat Nonlin Soft Matter Phys. 2012 Oct;86(4 Pt 1):041306
references.pmid: 23214579
references.citation: Ann Biomed Eng. 2011 Jul;39(7):1891-903
references.pmid: 21416392
references.citation: Phys Rev E Stat Nonlin Soft Matter Phys. 2010 Apr;81(4 Pt 2):046106
references.pmid: 20481785
references.citation: Wound Repair Regen. 2012 Sep-Oct;20(5):658-66
references.pmid: 22882499
references.citation: Chaos. 2009 Dec;19(4):041104
references.pmid: 20059188
references.citation: Dis Model Mech. 2011 Mar;4(2):165-78
references.pmid: 21324931
references.citation: J Musculoskelet Neuronal Interact. 2006 Apr-Jun;6(2):181-90
references.pmid: 16849830
references.citation: Neuroimage. 2011 Aug 1;57(3):892-907
references.pmid: 21605688
references.citation: Nature. 2004 Sep 16;431(7006):308-12
references.pmid: 15372033
references.citation: Vet Surg. 2003 May-Jun;32(3):269-77
references.pmid: 12784204
references.citation: J Orthop Res. 2005 Jul;23(4):779-87
references.pmid: 16022990
references.citation: Genes Dev. 2007 May 1;21(9):1010-24
references.pmid: 17473168
references.citation: Neuroimage. 2010 Sep;52(3):1059-69
references.pmid: 19819337
references.citation: Biomech Model Mechanobiol. 2011 Apr;10(2):269-79
references.pmid: 20526790
references.citation: Phys Rev E Stat Nonlin Soft Matter Phys. 2004 Jun;69(6 Pt 2):066133
references.pmid: 15244693
references.citation: Phys Rev E Stat Nonlin Soft Matter Phys. 2011 Jun;83(6 Pt 1):061303
references.pmid: 21797354
references.citation: J Biomech. 2012 Sep 21;45(14):2325-9
references.pmid: 22840489
references.citation: J Biomech Eng. 2016 Feb 1;138(2). doi: 10.1115/1.4031975
references.pmid: 26549105
references.citation: J Biomech Eng. 2011 Jun;133(6):064506
references.pmid: 21744935
references.citation: Soft Matter. 2014 Nov 28;10(44):8855-63
references.pmid: 25287650
references.citation: Biomech Model Mechanobiol. 2007 Apr;6(3):163-75
references.pmid: 16912884
references.citation: J Orthop Res. 2009 Dec;27(12):1596-602
references.pmid: 19544524
references.citation: Spine (Phila Pa 1976). 1996 Mar 1;21(5):538-43
references.pmid: 8852306
references.citation: Br J Radiol. 2012 Aug;85(1016):1157-72
references.pmid: 22553301
references.citation: PLoS One. 2010;5(10):e13701
references.pmid: 21060892
references.citation: J Neurosci Methods. 2004 Aug 30;137(2):151-9
references.pmid: 15262055
references.citation: World J Orthop. 2012 Feb 18;3(2):10-4
references.pmid: 22470845
references.citation: Soft Matter. 2015 Apr 14;11(14):2731-44
references.pmid: 25703651
references.citation: Phys Rev E Stat Nonlin Soft Matter Phys. 2007 Sep;76(3 Pt 1):031110
references.pmid: 17930202
references.citation: Brain Res. 2012 Jun 21;1461:51-63
references.pmid: 22578356
references.citation: Proc Natl Acad Sci U S A. 2011 May 3;108(18):7641-6
references.pmid: 21502525
references.citation: J Biomech. 2008;41(9):2003-12
references.pmid: 18501912
references.citation: Proc Natl Acad Sci U S A. 2006 Jun 6;103(23):8577-82
references.pmid: 16723398
references.citation: Spine (Phila Pa 1976). 2011 Dec 1;36(25 Suppl):S194-9
references.pmid: 22020612
references.citation: J Appl Physiol (1985). 2008 Dec;105(6):1881-8
references.pmid: 18845780
references.citation: Eur Spine J. 2008 Apr;17(4):556-63
references.pmid: 18080147
references.citation: Proc Natl Acad Sci U S A. 2009 Oct 20;106(42):17675-80
references.pmid: 19805118
references.citation: Phys Rev E Stat Nonlin Soft Matter Phys. 2014 Nov;90(5-1):052203
references.pmid: 25493787
references.citation: J Biomech. 2010 Jul 20;43(10):1870-5
references.pmid: 20381048
references.citation: Biomech Model Mechanobiol. 2012 Mar;11(3-4):325-39
references.pmid: 21611762
references.citation: Chaos. 2013 Mar;23(1):013142
references.pmid: 23556979
references.citation: Neuroimage. 2009 Feb 1;44(3):715-23
references.pmid: 19027073
references.citation: Ann Biomed Eng. 2002 Nov-Dec;30(10):1221-33
references.pmid: 12540198