Skip to main content
SpringerLink
Log in

Network Approaches to the Mechanical Failure of Soft Tissues: Implications for Disease and Tissue Engineering

  • Chapter
Structure-Based Mechanics of Tissues and Organs

  • 1519 Accesses

Abstract

Damage and mechanical failure of soft tissues can lead to diseases and even life threatening conditions including the failure of prosthetic heart valves, capillary stress failure, tissue destruction in pulmonary emphysema, and vessel wall aneurysms. Microscale damage occurs when mechanical forces in the tissue are sufficiently high to rupture intercellular connections or enzymatically weakened extracellular matrix (ECM) elements. When the microscale damage reaches a critical amount, tissue or organ failure can happen. In this chapter, we first briefly review the failure of the main constituents of tissues including molecules, cells, elastin, collagen, and proteoglycans. We then discuss failure of tissues modeled as complex networks of these constituents. A key concept here is percolation, a process where network elements reach from one boundary of the network to another. We show that when a certain type of fiber percolates the tissue, the rupture process of the network is primarily governed by the failure properties of the individual fibers. When the main fiber component does not percolate, the failure stress is still dominated by the stiffness of the fiber, but the failure strain emerges as a network phenomenon. Finally, we conclude by proposing some general concepts of how to potentially minimize the risk of failure and best repair a damaged network.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Angele P, Abke J, Kujat R, Faltermeier H, Schumann D, Nerlich M, Kinner B, Englert C, Ruszczak Z, Mehrl R, Mueller R. Influence of different collagen species on physico-chemical properties of crosslinked collagen matrices. Biomaterials. 2004;25(14):2831–41.

    Article  PubMed  CAS  Google Scholar 

  • Araujo AD, Majumdar A, Parameswaran H, Yi E, Spencer JL, Nugent MA, Suki B. Dynamics of enzymatic digestion of elastic fibers and networks under tension. Proc Natl Acad Sci U S A. 2011;108(23):9414–9. doi:10.1073/pnas.1019188108.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Arroyo LH, Lee RT. Mechanisms of plaque rupture: mechanical and biologic interactions. Cardiovasc Res. 1999;41(2):369–75.

    Article  PubMed  CAS  Google Scholar 

  • Barabasi AL, Buldyrev SV, Stanley HE, Suki B. Avalanches in the lung: a statistical mechanical model. Phys Rev Lett. 1996;76(12):2192–5.

    Article  PubMed  CAS  Google Scholar 

  • Bates JH, Davis GS, Majumdar A, Butnor KJ, Suki B. Linking parenchymal disease progression to changes in lung mechanical function by percolation. Am JRespir Crit Care Med. 2007;176(6):617–23.

    Article  PubMed  PubMed Central  Google Scholar 

  • Billiar KL, Throm AM, Frey MT. Biaxial failure properties of planar living tissue equivalents. JBiomed Mater Res A. 2005;73(2):182–91.

    Article  PubMed  CAS  Google Scholar 

  • Black LD, Brewer KK, Morris SM, Schreiber BM, Toselli P, Nugent MA, Suki B, Stone PJ. Effects of elastase on the mechanical and failure properties of engineered elastin-rich matrices. JAppl Physiol. 2005;98(4):1434–41.

    Article  PubMed  CAS  Google Scholar 

  • Black LD, Allen PG, Morris SM, Stone PJ, Suki B. Mechanical and failure properties of extracellular matrix sheets as a function of structural protein composition. Biophys J. 2008;94(5):1916–29.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bland RD, Carlton DP, Scheerer RG, Cummings JJ, Chapman DL. Lung fluid balance in lambs before and after premature birth. JClin Invest. 1989;84(2):568–76. doi:10.1172/JCI114200.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Carey DJ. Biological functions of proteoglycans: use of specific inhibitors of proteoglycan synthesis. Mol Cell Biochem. 1991;104(1–2):21–8.

    PubMed  CAS  Google Scholar 

  • Cavalcante FS, Ito S, Brewer KK, Sakai H, Alencar AM, Almeida MP, Andrade Jr JS, Majumdar A, Ingenito EP, Suki B. Mechanical interactions between collagen and proteoglycans: implications for the stability of lung tissue. JAppl Physiol. 2005;98:672–9.

    Article  PubMed  CAS  Google Scholar 

  • Chen HY, Chu YP. Theoretical determination of the strength of soft noncovalent molecular bonds. Phys Rev E Stat Nonlin Soft Matter Phys. 2005;71(1 Pt 1):010901.

    Article  PubMed  Google Scholar 

  • Christian Gasser T. An irreversible constitutive model for fibrous soft biological tissue: a 3-D microfiber approach with demonstrative application to abdominal aortic aneurysms. Acta Biomater. 2011;7(6):2457–66. doi:10.1016/j.actbio.2011.02.015.

    Article  PubMed  CAS  Google Scholar 

  • Christiansen DL, Huang EK, Silver FH. Assembly of type I collagen: fusion of fibril subunits and the influence of fibril diameter on mechanical properties. Matrix Biol. 2000;19(5):409–20.

    Article  PubMed  CAS  Google Scholar 

  • Dias CL, Dube M, Oliveira FA, Grant M. Scaling in force spectroscopy of macromolecules. Phys Rev E Stat Nonlin Soft Matter Phys. 2005;72(1 Pt 1):011918.

    Article  PubMed  Google Scholar 

  • Dobrin PB, Anidjar S. Pathophysiology of arterial aneurysms. Arch Mal Coeur Vaiss. 1991;84(Spec No 3):57–62.

    PubMed  Google Scholar 

  • Donovan DL, Schmidt SP, Townshend SP, Njus GO, Sharp WV. Material and structural characterization of human saphenous vein. JVasc Surg. 1990;12(5):531–7.

    Article  PubMed  CAS  Google Scholar 

  • Evans E. Probing the relation between force–lifetime–and chemistry in single molecular bonds. Annu Rev Biophys Biomol Struct. 2001;30:105–28. doi:10.1146/annurev.biophys.30.1.105.

    Article  PubMed  CAS  Google Scholar 

  • Fung YC. Biomechanics: mechanical properties of living tissues. 2nd ed. New York: Springer; 1993.

    Book  Google Scholar 

  • Fung YC. Biomechanics: circulation. 2nd ed. New York: Springer; 1997.

    Book  Google Scholar 

  • Goodall S, Crowther M, Bell PR, Thompson MM. The association between venous structural alterations and biomechanical weakness in patients with abdominal aortic aneurysms. JVasc Surg. 2002;35(5):937–42.

    Article  PubMed  Google Scholar 

  • Hamakawa H, Bartolak-Suki E, Parameswaran H, Majumdar A, Lutchen KR, Suki B. Structure-function relations in an elastase-induced mouse model of emphysema. Am JRespir Cell Mol Biol. 2011;45(3):517–24. doi:10.1165/rcmb.2010-0473OC. pii: 2010-0473OC.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Holmes DF, Gilpin CJ, Baldock C, Ziese U, Koster AJ, Kadler KE. Corneal collagen fibril structure in three dimensions: Structural insights into fibril assembly, mechanical properties, and tissue organization. Proc Natl Acad Sci U S A. 2001;98(13):7307–12.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hukins DWL. Connective tissue matrix. Topics in molecular and structural biology, vol. 5. London: Macmillan; 1984.

    Google Scholar 

  • Humphrey JD, Delange SL. An introduction to biomechanics: solids and fluids, analysis and design. New York: Springer; 2004.

    Book  Google Scholar 

  • Ingber DE. Cellular mechanotransduction: putting all the pieces together again. Faseb J. 2006;20(7):811–27.

    Article  PubMed  CAS  Google Scholar 

  • Ito S, Ingenito EP, Brewer KK, Black LD, Parameswaran H, Lutchen KR, Suki B. Mechanics, nonlinearity, and failure strength of lung tissue in a mouse model of emphysema: possible role of collagen remodeling. JAppl Physiol. 2005;98:503–11.

    Article  PubMed  Google Scholar 

  • Ito D, Tanaka E, Yamamoto S. A novel constitutive model of skelet al muscle taking into account anisotropic damage. JMech Behav Biomed Mater. 2010;3(1):85–93. doi:10.1016/j.jmbbm.2009.05.001.

    Article  PubMed  CAS  Google Scholar 

  • Jesudason R, Black L, Majumdar A, Stone P, Suki B. Differential effects of static and cyclic stretching during elastase digestion on the mechanical properties of extracellular matrices. JAppl Physiol. 2007;103(3):803–11.

    Article  PubMed  Google Scholar 

  • Joyce EM, Moore JJ, Sacks MS. Biomechanics of the fet al membrane prior to mechanical failure: review and implications. Eur JObstet Gynecol Reprod Biol. 2009;144 Suppl 1:S121–7. doi:10.1016/j.ejogrb.2009.02.014.

    Article  PubMed  PubMed Central  Google Scholar 

  • Juul SE, Kinsella MG, Wight TN, Hodson WA. Alterations in nonhuman primate (M. nemestrina) lung proteoglycans during normal development and acute hyaline membrane disease. Am JRespir Cell Mol Biol. 1993;8(3):299–310.

    Article  PubMed  CAS  Google Scholar 

  • Kielty CM, Sherratt MJ, Shuttleworth CA. Elastic fibres. JCell Sci. 2002;115(Pt 14):2817–28.

    PubMed  CAS  Google Scholar 

  • Kononov S, Brewer K, Sakai H, Cavalcante FS, Sabayanagam CR, Ingenito EP, Suki B. Roles of mechanical forces and collagen failure in the development of elastase-induced emphysema. Am JRespir Crit Care Med. 2001;164(10 Pt 1):1920–6.

    Article  PubMed  CAS  Google Scholar 

  • Koshiyama K, Wada S. Molecular dynamics simulations of pore formation dynamics during the rupture process of a phospholipid bilayer caused by high-speed equibiaxial stretching. JBiomech. 2011;44(11):2053–8. doi:10.1016/j.jbiomech.2011.05.014.

    Article  Google Scholar 

  • Lanir Y. Constitutive equations for fibrous connective tissues. JBiomech. 1983;16(1):1–12.

    Article  CAS  Google Scholar 

  • Lee TC, Midura RJ, Hascall VC, Vesely I. The effect of elastin damage on the mechanics of the aortic valve. JBiomech. 2001;34(2):203–10.

    Article  CAS  Google Scholar 

  • Lillie MA, Gosline JM. The viscoelastic basis for the tensile strength of elastin. Int JBiol Macromol. 2002;30(2):119–27.

    Article  CAS  Google Scholar 

  • Liu X, Sun JQ, Heggeness MH, Yeh ML, Luo ZP. Direct quantification of the rupture force of single hyaluronan/hyaluronan binding protein bonds. FEBS Lett. 2004;563(1–3):23–7. doi:10.1016/S0014-5793(04)00232-7.

    Article  PubMed  CAS  Google Scholar 

  • Lokshin O, Lanir Y. Viscoelasticity and preconditioning of rat skin under uniaxial stretch: microstructural constitutive characterization. JBiomech Eng. 2009;131(3):031009. doi:10.1115/1.3049479.

    Article  Google Scholar 

  • Marque V, Kieffer P, Gayraud B, Lartaud-Idjouadiene I, Ramirez F, Atkinson J. Aortic wall mechanics and composition in a transgenic mouse model of Marfan syndrome. Arterioscler Thromb Vasc Biol. 2001;21(7):1184–9.

    Article  PubMed  CAS  Google Scholar 

  • McCullagh CM, Jamieson AM, Blackwell J, Gupta R. Viscoelastic properties of human tracheobronchial mucin in aqueous solution. Biopolymers. 1995;35(2):149–59. doi:10.1002/bip.360350203.

    Article  PubMed  CAS  Google Scholar 

  • Nguyen BV, Wang Q, Kuiper NJ, El HaJAJ, Thomas CR, Zhang Z. Strain-dependent viscoelastic behaviour and rupture force of single chondrocytes and chondrons under compression. Biotechnol Lett. 2009;31(6):803–9. doi:10.1007/s10529-009-9939-y.

    Article  PubMed  CAS  Google Scholar 

  • Oroudjev E, Soares J, Arcdiacono S, Thompson JB, Fossey SA, Hansma HG. Segmented nanofibers of spider dragline silk: atomic force microscopy and single-molecule force spectroscopy. Proc Natl Acad Sci U S A. 2002;99 Suppl 2:6460–5. doi:10.1073/pnas.082526499.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Parameswaran H, Majumdar A, Suki B. Linking microscopic spatial patterns of tissue destruction in emphysema to macroscopic decline in stiffness using a 3D computational model. PLoS Comput Biol. 2011;7(4), e1001125. doi:10.1371/journal.pcbi.1001125.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Peeters EA, Oomens CW, Bouten CV, Bader DL, Baaijens FP. Mechanical and failure properties of single attached cells under compression. JBiomech. 2005;38(8):1685–93. doi:10.1016/j.jbiomech.2004.07.018.

    Article  CAS  Google Scholar 

  • Redaelli A, Vesentini S, Soncini M, Vena P, Mantero S, Montevecchi FM. Possible role of decorin glycosaminoglycans in fibril to fibril force transfer in relative mature tendons–a computational study from molecular to microstructural level. JBiomech. 2003;36(10):1555–69.

    Article  CAS  Google Scholar 

  • Ritter MC, Jesudason R, Majumdar A, Stamenovic D, Buczek-Thomas JA, Stone PJ, Nugent MA, Suki B. A zipper network model of the failure mechanics of extracellular matrices. Proc Natl Acad Sci U S A. 2009;106(4):1081–6. doi:10.1073/pnas.0808414106. pii: 0808414106.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sahimi M, Arbabi S. Mechanics of disordered solids. 3. Fracture properties. Phys Rev B. 1993;47(2):713–22.

    Article  Google Scholar 

  • Silver FH, Freeman JW, Seehra GP. Collagen self-assembly and the development of tendon mechanical properties. JBiomech. 2003;36(10):1529–53.

    Article  Google Scholar 

  • Stauffer D, Aharony A. Introduction to percolation theory. 2nd ed. London: Taylor & Francis; 1992.

    Google Scholar 

  • Stenson JD, Hartley P, Wang C, Thomas CR. Determining the mechanical properties of yeast cell walls. Biotechnol Prog. 2011;27(2):505–12. doi:10.1002/btpr.554.

    Article  PubMed  CAS  Google Scholar 

  • Stolz M, Raiteri R, Daniels AU, VanLandingham MR, Baschong W, Aebi U. Dynamic elastic modulus of porcine articular cartilage determined at two different levels of tissue organization by indentation-type atomic force microscopy. Biophys J. 2004;86(5):3269–83. doi:10.1016/S0006-3495(04)74375-1. pii: S0006-3495(04)74375-1.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Suki B, Lutchen KR, Ingenito EP. On the progressive nature of emphysema: roles of proteases, inflammation, and mechanical forces. Am JRespir Crit Care Med. 2003;168(5):516–21.

    Article  Google Scholar 

  • Suki B, Ito S, Stamenovic D, Lutchen KR, Ingenito EP. Biomechanics of the lung parenchyma: critical roles of collagen and mechanical forces. JAppl Physiol. 2005;98(5):1892–9.

    Article  Google Scholar 

  • Suki B, Majumdar A, Nugent MA, Bates JH. In silico modeling of interstitial lung mechanics: implications for disease development and repair. Drug Discov Today Dis Models. 2007;4(3):139–45.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tanaka R, Al-Jamal R, Ludwig MS. Maturational changes in extracellular matrix and lung tissue mechanics. JAppl Physiol. 2001;91(5):2314–21.

    CAS  Google Scholar 

  • Tang Y, Ballarini R, Buehler MJ, Eppell SJ. Deformation micromechanisms of collagen fibrils under uniaxial tension. JR Soc Interface. 2010;7(46):839–50. doi:10.1098/rsif.2009.0390.

    Article  Google Scholar 

  • Urry DW, Parker TM. Mechanics of elastin: molecular mechanism of biological elasticity and its relationship to contraction. JMuscle Res Cell Motil. 2002;23(5–6):543–59.

    Article  CAS  Google Scholar 

  • Volokh KY. Fung’s model of arterial wall enhanced with a failure description. Mol Cell Biomech. 2008;5(3):207–16.

    PubMed  CAS  Google Scholar 

  • Vorp DA. Biomechanics of abdominal aortic aneurysm. JBiomech. 2007;40(9):1887–902.

    Article  Google Scholar 

  • Vorp DA, Schiro BJ, Ehrlich MP, Juvonen TS, Ergin MA, Griffith BP. Effect of aneurysm on the tensile strength and biomechanical behavior of the ascending thoracic aorta. Ann Thorac Surg. 2003;75(4):1210–4.

    Article  PubMed  Google Scholar 

  • West JB. Invited review: pulmonary capillary stress failure. JAppl Physiol. 2000;89(6):2483–9; discussion 2497.

    CAS  Google Scholar 

  • Wilson K, Bradbury A, Whyman M, Hoskins P, Lee A, Fowkes G, McCollum P, Ruckley CV. Relationship between abdominal aortic aneurysm wall compliance and clinical outcome: a preliminary analysis. Eur JVasc Endovasc Surg. 1998;15(6):472–7.

    Article  CAS  Google Scholar 

Download references

Acknowledgement

This work was supported by NIH grants HL090757 and HL-098976.

Author information

Authors and Affiliations

  1. Department of Biomedical Engineering, Boston University, Boston, MA, 02215, USA

    Béla Suki & Arnab Majumdar

Authors
  1. Béla Suki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Arnab Majumdar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Béla Suki .

Editor information

Editors and Affiliations

  1. California Medical Innovations Institute , INDIANAPOLIS, Indiana, USA

    Ghassan S. Kassab

  2. Institute for Computational Engineering, The University of Texas at Austin Institute for Computational Engineering, PITTSBURGH, Pennsylvania, USA

    Michael S. Sacks

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Suki, B., Majumdar, A. (2016). Network Approaches to the Mechanical Failure of Soft Tissues: Implications for Disease and Tissue Engineering. In: Kassab, G., Sacks, M. (eds) Structure-Based Mechanics of Tissues and Organs. Springer, Boston, MA. https://doi.org/10.1007/978-1-4899-7630-7_21

Download citation

Publish with us

Policies and ethics

Search

Navigation