Remodelling of collagen fibre transition stretch and angular distribution in soft biological tissues and cell-seeded hydrogels

Biomechanics and Modeling in Mechanobiology

Volumn 11, Issue 3-4, 2012, Pages 325-339

  Nagel, Thomas ^a   Kelly, Daniel J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Anisotropy; Fibre remodeling; Multiplicative; Natural configuration; Reorientation; Transition stretch

Indexed keywords

BIOLOGICAL TISSUES; COLLAGEN FIBRES; COLLAGEN GELS; CONNECTIVE TISSUES; DEFORMATION GRADIENTS; EXPERIMENTAL STUDIES; EXTRACELLULAR MATRICES; FIBRE REINFORCEMENTS; FIBRIN GELS; HELMHOLTZ ENERGY; IN-VITRO; MECHANICAL ENVIRONMENT; MULTIPLICATIVE; MULTIPLICATIVE DECOMPOSITION; NATURAL CONFIGURATIONS; PHENOMENOLOGICAL MODELS; REORIENTATION; SOFT BIOLOGICAL TISSUE; STRUCTURAL ANISOTROPY; STRUCTURE TENSORS; STRUCTURE-FUNCTION RELATIONSHIP; TRANSITION STRETCH;

ANGULAR DISTRIBUTION; ANISOTROPY; COMPACTION; COMPUTER SIMULATION; DEFORMATION; FIBERS; LOADING; MUSCULOSKELETAL SYSTEM; STRESS ANALYSIS; TISSUE;

COLLAGEN;

SANDER;

COLLAGEN; FIBRIN;

ANIMAL; ANISOTROPY; ARTICLE; BIOMECHANICS; CHEMISTRY; COMPRESSIVE STRENGTH; EXTRACELLULAR MATRIX; GEL; HUMAN; HYDROGEL; MECHANICAL STRESS; METHODOLOGY; STATISTICAL MODEL; TENSILE STRENGTH; TISSUE ENGINEERING;

ANIMALS; ANISOTROPY; BIOMECHANICS; COLLAGEN; COMPRESSIVE STRENGTH; EXTRACELLULAR MATRIX; FIBRIN; GELS; HUMANS; HYDROGELS; MODELS, STATISTICAL; STRESS, MECHANICAL; TENSILE STRENGTH; TISSUE ENGINEERING;

EID: 84861101130     PISSN: 16177959     EISSN: 16177940     Source Type: Journal    
DOI: 10.1007/s10237-011-0313-3     Document Type: Article

References (59)

1. Ateshian GA, Ricken T (2010) Multigenerational interstitial growth of biological tissues. Biomech Model Mechanobiol 9(6):689-702. doi:10.1007/s10237- 010-0205-y
2. Ateshian GA, Rajan V, Chahine NO, Canal CE, Hung CT(2009) Modeling the matrix of articular cartilage using a continuous fiber angular distribution predicts many observed phenomena. J Biomech Eng 131(6):061003. doi:10.1115/1.3118773. http://link.aip.org/link/? JBY/131/061003/1
3. Baaijens F, Bouten C, Driessen N (2010) Modeling collagen remodeling. J Biomech 43(1):166-175. doi:10.1016/j.jbiomech.2009.09. 022
4. Benninghoff A (1925) Form und Bau der Gelenkknorpel in ihren Beziehungen zur Funktion. Zweiter Teil: Der Aufbau des Gelenkknorpels in seinen Beziehungen zur Funktion. Zeit Zellforsch und Mikroskop Anat 2:783-862
5. Cacho F, Elbischger P, Rodrguez J, Doblar M, Holzapfel G (2007) A constitutive model for fibrous tissues considering collagen fiber crimp. Int J Non Linear Mech 42(2): 391-402. doi:10.1016/j. ijnonlinmec.2007.02.002. http://www.sciencedirect.com/science/article/B6TJ2-4N43RYF-1/2/ d8e154070b355511b3a03df9576b2. 6ca, special Issue in Honour of Dr Ronald S. Rivlin (Pubitemid 46654001)
6. Calve S, Dennis RG, Kosnik PE, Baar K, Grosh K, Arruda EM (2004) Engineering of functional tendon. Tissue Eng 10(5-6):755-761. doi:10.1089/1076327041348464 (Pubitemid 38880393)
7. Chandran PL, Barocas VH (2006) Affine versus non-affine fibril kinematics in collagen networks: theoretical studies of network behavior. J Biomech Eng 128(2):259-270. doi:10.1115/1.2165699
8. Cullinane DM, Fredrick A, Eisenberg SR, Pacicca D, Elman MV, Lee C, Salisbury K, Gerstenfeld LC, Einhorn TA (2002) Induction of a neoarthrosis by precisely controlled motion in an experimental mid-femoral defect. J Orthop Res 20(3):579-586. doi:10.1016/S0736-0266(01)00131-0 (Pubitemid 34461018)
9. Davol A, Bingham MS, Sah RL, Klisch SM (2008) A nonlinear finite element model of cartilage growth. Biomech Model Mechanobiol 7(4):295-307. doi:10.1007/s10237-007-0098-6 (Pubitemid 352039638)
10. Donkelaar Cv, Wilson W (2006) Chondrocyte hypertrophy requires matrix turnover. In: Proceedings of 2006 summer bioengineering conference, June 21-25, Amelia Island Plantation, Amelia Island, Florida, USA
11. Driessen NJB, Boerboom RA, Huyghe JM, Bouten CVC, Baaijens FPT (2003a) Computational analyses of mechanically induced collagen fiber remodeling in the aortic heart valve. J Biomech Eng 125(4):549-557. doi:10.1115/1.1590361. http://link.aip.org/link/?JBY/125/549/1 (Pubitemid 37012215)
12. Driessen NJB, Peters GWM, Huyghe JM, Bouten CVC, Baaijens FPT (2003b) Remodelling of continuously distributed collagen fibres in soft connective tissues. J Biomech 36(8):1151-1158 (Pubitemid 36794112)
13. Driessen NJB, Cox MAJ, Bouten CVC, Baaijens FPT (2008) Remodelling of the angular collagen fiber distribution in cardiovascular tissues. Biomech Model Mechanobiol 7(2):93-103. doi:10.1007/s10237-007-0078-x (Pubitemid 351438181)
14. Eastwood M, Mudera VC, McGrouther DA, Brown RA (1998) Effect of precise mechanical loading on fibroblast populated collagen lattices: morphological changes. Cell Motil Cytoskeleton 40(1): 13-21. doi:10.1002/(SICI)1097-0169(1998) 40:1?13::AIDCM2? 3.0.CO;2-G (Pubitemid 28225538)
15. Farahani RM, Kloth LC (2008) The hypothesis of biophysical matrix contraction : wound contraction revisited. Int Wound J 5(3): 477-482. doi:10.1111/j.1742-481X.2007.00402.x (Pubitemid 351877043)
16. Foolen J, van Donkelaar C, Nowlan N, Murphy P, Huiskes R, Ito K (2008) Collagen orientation in periosteum and perichondrium is aligned with preferential directions of tissue growth. J Orthop Res 26(9):1263-1268. doi:10.1002/jor.20586
17. Foolen J, van Donkelaar CC, Soekhradj-Soechit S, Ito K (2010) European society of biomechanics s.m. perren award 2010: an adaptation mechanism for fibrous tissue to sustained shortening. J Biomech 43(16):3168-3176. doi:10.1016/j.jbiomech.2010.07. 040. http://www.sciencedirect.com/science/ article/B6T82-50XJ C0S-1/2/47b646146d92bb178404711cc88ec093
18. Garikipati K, Olberding J, Narayanan H, Arruda E, Grosh K, Calve S (2006) Biological remodelling: stationary energy, configurational change, internal variables and dissipation. J Mech Phys Solids 54(7):1493-1515. doi:10.1016/j.jmps.2005.11.011. http://www.sciencedirect.com/science/article/ B6TXB-4J9MV5T-1/2/b3086bfcb28b11b9b94379805b44cc0e
19. GörkeUJ, GüntherH, Nagel T, WimmerMA(2010)Alarge strain material model for soft tissues with functionally graded properties. J Biomech Eng 132(7):074502. doi:10.1115/1.4001312. http://link. aip.org/link/?JBY/132/ 074502/1
20. Grassl ED, Oegema TR, Tranquillo RT (2003) A fibrin-based arterial media equivalent. J Biomed Mater Res 66A(3):550-561. doi:10. 1002/jbm.a.10589 (Pubitemid 37517200)
21. Guterl CC, Hung CT, Ateshian GA (2010) Electrostatic and nonelectrostatic contributions of proteoglycans to the compressive equilibrium modulus of bovine articular cartilage. J Biomech, http://linkinghub.elsevier.com/retrieve/pii/ S0021929010000552
22. Hariton I, de Botton G, Gasser TC, Holzapfel GA (2007) Stress-driven collagen fiber remodeling in arterial walls. Biomech Model Mechanobiol 6(3):163-175. doi:10.1007/s10237-006-0049-7 (Pubitemid 46450733)
23. Holzapfel G, Gasser T, Ogden R (2000) A new constitutive framework for arterial wall mechanics and a comparative study of material models. J Elast 61:1-48. doi:10.1023/A:1010835316564 (Pubitemid 32732278)
24. Huang C, Yannas IV (1977) Mechanochemical studies of enzymatic degradation of insoluble collagen fibers. J Biomed Mater Res 11(1):137-154. doi:10.1002/jbm.820110113 (Pubitemid 8059844)
25. Humphrey JD (1999) Remodeling of a collagenous tissue at fixed lengths. J Biomech Eng 121(6):591-597 (Pubitemid 30010723)
26. Humphrey JD (2001) Stress, strain, and mechanotransduction in cells. J Biomech Eng 123(6):638-641 (Pubitemid 34016558)
27. Humphrey JD (2008) Vascular adaptation and mechanical homeostasis at tissue, cellular, and sub-cellular levels. Cell Biochem Biophys 50(2):53-78. doi:10.1007/s12013-007-9002-3
28. KjaerM(2004) Role of extracellularmatrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev 84(2):649-698. doi:10.1152/physrev.00031.2003 (Pubitemid 38365495)
29. Lanir Y (1979) A structural theory for the homogeneous biaxial stress-strain relationships in flat collagenous tissues. J Biomech 12(6):423-436. doi:10.1016/0021-9290(79)90027-7. http://www.sciencedirect.com/ science/article/B6T82-4BYSH9M-RY/2/274635ab97b0102537fa5fb3fba2584d (Pubitemid 9191484)
30. Lanir Y (1983) Constitutive equations for fibrous connective tissues. J Biomech 16(1):1-12. doi:10.1016/0021-9290(83)90041-6. http://www.sciencedirect. com/science/article/B6T82-4BYSGW3-K2/2/53454c63da65efe4ec62db52e1936e80 (Pubitemid 13125809)
31. Lubarda VA (2004) Constitutive theories based on the multiplicative decomposition of deformation gradient: thermoelasticity, elastoplasticity, and biomechanics. Appl Mech Rev 57(2):95-108. doi:10.1115/1.1591000. http://link.aip.org/link/?AMR/57/95/1 (Pubitemid 40748663)
32. Magnusson SP, Narici MV, Maganaris CN, Kjaer M (2008) Human tendon behaviour and adaptation, in vivo. J Physiol 586(1):71-81. doi:10.1113/jphysiol. 2007.139105
33. MenzelA(2007)Afibre reorientationmodel for orthotropicmultiplicative growth. Biomech Model Mechanobiol 6(5):303-320, doi:10. 1007/s10237-006-0061-y
34. Nabeshima Y, Grood ES, Sakurai A, Herman JH (1996) Uniaxial tension inhibits tendon collagen degradation by collagenase in vitro. J Orthop Res 14(1):123-130, doi:10.1002/jor.1100140120 (Pubitemid 26091612)
35. Nagel T, Kelly D (2010) Mechano-regulation of mesenchymal stem cell differentiation and collagen organisation during skeletal tissue regeneration. In: The 16th annual conference of the section of bioengineering, Royal Academy of Medicine in Ireland
36. Nguyen T, Jones R, Boyce B (2007) Modeling the anisotropic finite-deformation viscoelastic behavior of soft fiber-reinforced composites. Int J Solids Struct 44(25-26):8366-8389. doi:10.1016/j.ijsolstr.2007.06.020. http://www.sciencedirect.com/science/article/B6VJS-4P192N5-5/2/ ca27874f7c8846e0bd3e3e2.712b5f06e (Pubitemid 47632568)
37. Ohsumi T, Flaherty J, Evans M, Barocas V (2008) Three-dimensional simulation of anisotropic cell-driven collagen gel compaction. Biomech ModelMechanobiol 7:53-62. doi:10.1007/s10237-007- 0075-0
38. Ramasubramanian A, Taber LA (2008) Computational modeling of morphogenesis regulated by mechanical feedback. Biomech Model Mechanobiol 7(2):77-91. doi:10.1007/s10237-007-0077-y (Pubitemid 351438180)
39. Raykin J, Rachev AI, Rudolph L Gleason J (2009) A phenomenological model for mechanically mediated growth, remodeling, damage, and plasticity of gel-derived tissue engineered blood vessels. J Biomech Eng 131(10):101016. doi:10.1115/1.4000124. http://link.aip.org/link/?JBY/131/101016/1
40. Reese S (2003) Meso-macro modelling of fibre-reinforced rubber-like composites exhibiting large elastoplastic deformation. Int J Solids Struct 40(4):951-980, doi:10.1016/S0020-7683(02)00602-9. http://www.sciencedirect.com/ science/article/B6VJS-47G3NBTD/2/e0e715844c81b2b8fad2d92c0892712c (Pubitemid 36211452)
41. Rodriguez EK, Hoger A, McCulloch AD (1994) Stress-dependent finite growth in soft elastic tissues. J Biomech 27(4):455-467. doi:10.1016/0021-9290(94) 90021-3. http://www.sciencedirect. com/science/article/B6T82-4BYSHS4-XN/2/ b43d9a5da6237fbfc b6091da32bd04cc (Pubitemid 24102058)
42. Roeder BA, Kokini K, Sturgis JE, Robinson JP, Voytik-Harbin SL (2002) Tensile mechanical properties of three-dimensional type i collagen extracellular matrices with varied microstructure. J Biomech Eng 124(2):214-222 (Pubitemid 34407065)
43. Ruberti JW, Hallab NJ (2005) Strain-controlled enzymatic cleavage of collagen in loaded matrix. Biochem Biophys Res Commun 336(2):483-489. doi:10.1016/j.bbrc.2005.08.128. http://www.sciencedirect.com/science/article/ B6WBK-4GYH6J8-3/2/2591795f10a92b5dcbf6a0edbb81c53f (Pubitemid 41267255)
44. Sacks MS, Smith DB, Hiester ED (1998) The aortic valve microstructure: effects of transvalvular pressure. J Biomed Mater Res 41(1):131-141. doi:10.1002/(SICI)1097-4636(199807)41: 1131::AID-JBM163.0.CO;2-Q (Pubitemid 28255903)
45. Sander E, Barocas V, Tranquillo R (2010) Initial fiber alignment pattern alters extracellular matrix synthesis in fibroblast-populated fibrin gel cruciforms and correlates with predicted tension. Ann Biomed Eng 1-16. doi:10.1007/s10439-010-0192-2
46. Silver FH, Siperko LM, Seehra GP (2003) Mechanobiology of force transduction in dermal tissue. Skin Res Technol 9(1):3-23 (Pubitemid 36621682)
47. Spurrier R (1978) Comment on singularity-free extraction of a quaternion from a direction-cosine matrix. J Spacecr Rockets 15(4): 255-255
48. Taber LA (1995) Biomechanics of growth, remodeling, and morphogenesis. Appl Mech Rev 48(8):487-545. doi:10.1115/1.3005109. http://link.aip.org/link/? AMR/48/487/1
49. Tegmark M (1996) An icosahedron-based method for pixelizing the celestial sphere. Astrophys J Lett 470(2):L81. http://stacks.iop. org/1538-4357/470/i=2/ a=L81
50. Thomas GC, AsanbaevaA, Vena P, Sah RL, KlischSM(2009)Anonlinear constituent based viscoelastic model for articular cartilage and analysis of tissue remodeling due to altered glycosaminoglycancollagen interactions. J Biomech Eng 131(10):101, 002. doi:10. 1115/1.3192139
51. Thomopoulos S, Fomovsky GM, Holmes JW (2005) The development of structural and mechanical anisotropy in fibroblast populated collagen gels. J Biomech Eng 127(5):742-750 (Pubitemid 41374633)
52. Thomopoulos S, Fomovsky GM, Chandran PL, Holmes JW (2007) Collagen fiber alignment does not explain mechanical anisotropy in fibroblast populated collagen gels. J Biomech Eng 129(5): 642-650. doi:10.1115/1.2768104 (Pubitemid 350005825)
53. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA (2002) Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 3(5):349-363. doi:10.1038/nrm809 (Pubitemid 34619269)
54. Vaishnav RN, Vossoughi J (1987) Residual stress and strain in aortic segments. J Biomech 20(3):235-237, 239. doi:10.1016/0021- 9290(87)90290-9, http://www.sciencedirect.com/science/article/B6T82-4C35T63-BV/2/ 1b7eab5cf251e4d17410 b80da91c7608
55. Watton PN, Hill NA, Heil M (2004) A mathematical model for the growth of the abdominal aortic aneurysm. Biomech Model Mechanobiol 3(2):98-113. doi:10.1007/s10237-004-0052-9 (Pubitemid 40265574)
56. Wilson W, Driessen NJB, van Donkelaar CC, Ito K (2006) Prediction of collagen orientation in articular cartilage by a collagen remodeling algorithm. Osteoarthritis Cartilage 14(11):1196-1202. doi:10. 1016/j.joca.2006.05.006 (Pubitemid 44490317)
57. Wood TO, Cooke PH, Goodship AE (1988) The effect of exercise and anabolic steroids on themechanical properties and crimpmorphology of the rat tendon. Am J Sports Med 16(2):153-158
58. Wrobel LK, Fray TR, Molloy JE, Adams JJ, Armitage MP, Sparrow JC (2002) Contractility of single human dermal myofibroblasts and fibroblasts.Cell Motil Cytoskeleton 52(2):82-90. doi:10.1002/cm. 10034
59. Zulliger MA, Fridez P, Hayashi K, Stergiopulos N (2004) A strain energy function for arteries accounting for wall composition and structure. J Biomech 37(7):989-1000. doi:10.1016/j.jbiomech. 2003.11.026 (Pubitemid 38686323)