Skip to main content

Advertisement

Log in

Empirical measurements of biomechanical anisotropy of the human vocal fold lamina propria

  • Original Paper
  • Published:
Biomechanics and Modeling in Mechanobiology Aims and scope Submit manuscript

Abstract

The vocal folds are known to be mechanically anisotropic due to the microstructural arrangement of fibrous proteins such as collagen and elastin in the lamina propria. Even though this has been known for many years, the biomechanical anisotropic properties have rarely been experimentally studied. We propose that an indentation procedure can be used with uniaxial tension in order to obtain an estimate of the biomechanical anisotropy within a single specimen. Experiments were performed on the lamina propria of three male and three female human vocal folds dissected from excised larynges. Two experiments were conducted: each specimen was subjected to cyclic uniaxial tensile loading in the longitudinal (i.e., anterior–posterior) direction, and then to cyclic indentation loading in the transverse (i.e., medial–lateral) direction. The indentation experiment was modeled as contact on a transversely isotropic half-space using the Barnett–Lothe tensors. The longitudinal elastic modulus E L was computed from the tensile test, and the transverse elastic modulus E T and longitudinal shear modulus G L were obtained by inverse analysis of the indentation force-displacement response. It was discovered that the average of E L /E T was 14 for the vocal ligament and 39 for the vocal fold cover specimens. Also, the average of E L /G L , a parameter important for models of phonation, was 28 for the vocal ligament and 54 for the vocal fold cover specimens. These measurements of anisotropy could contribute to more accurate models of fundamental frequency regulation and provide potentially better insights into the mechanics of vocal fold vibration.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alipour F, Berry D, Titze I (2000) A finite-element model of vocal-fold vibration. J Acoust Soc Am 108: 3003–3012

    Article  Google Scholar 

  • Barnett D, Lothe J (1975) Line force loadings on anisotropic half-spaces and wedges. Phys Norv 8: 13–22

    Google Scholar 

  • Berry D, Titze I (1996) Normal modes in a continuum model of vocal fold tissues. J Acoust Soc Am 100: 3345–3354

    Article  Google Scholar 

  • Bühler R, Sennes L, Tsuji D, Mauad T, da Silva L, Saldiva P (2011) Collagen type I, collagen type III, and versican in vocal fold lamina propria. Arch Otolaryngol Head Neck Surg 137: 604–608

    Article  Google Scholar 

  • Butler J, Hammond T, SD G (2001) Gender-related differences of hyaluronic acid distribution in the human vocal fold. Laryngoscope 111: 907–911

    Article  Google Scholar 

  • Chan R, Rodriguez M (2008) A simple-shear rheometer for linear viscoelastic characterization of vocal fold tissues at phonatory frequencies. J Acoust Soc Am 124: 1207–1219

    Article  Google Scholar 

  • Chan R, Titze I (2003) Effect of postmortem changes and freezing on the viscoelastic properties of vocal fold tissues. Ann Biomed Eng 31: 482–491

    Article  Google Scholar 

  • Chan R, Fu M, Young L, Tirunagari N (2007) Relative contributions of collagen and elastin to elasticity of the vocal fold under tension. Ann Biomed Eng 35: 1471–1483

    Article  Google Scholar 

  • Chan R, Siegmund T, Zhang K (2009) Biomechanics of fundamental frequency regulation: constitutive modeling of the vocal fold lamina propria. Logop Phoniatr Voco 34: 181–189

    Article  Google Scholar 

  • Chhetri D, Zhang Z, Neubauer J (2011) Measurement of young’s modulus of vocal folds by indentation. J Voice 25: 1–7

    Article  Google Scholar 

  • Cook D, Nauman E, Mongeau L (2009) Ranking vocal fold model parameters by their influence on modal frequencies. J Acoust Soc Am 126: 2002–2010

    Article  Google Scholar 

  • Cox M, Driessen N, Boerboom R, Bouten C, Baaijens F (2008) Mechanical characterization of anisotropic planar biological soft tissues using finite indentation: experimental feasibility. J Biomech 41: 422–429

    Article  Google Scholar 

  • Dahan M, Zarka J (1977) Elastic contact between a sphere and a semi infinite transversely isotropic body. Int J Solids Struct 13: 229–238

    Article  MATH  Google Scholar 

  • de Vries M, Schutte H, Verkerke G (1999) Determination of parameters for lumped parameter models of the vocal folds using a finite element method approach. J Acoust Soc Am 106: 3620–3628

    Article  Google Scholar 

  • Dong X, Guo X (2004) The dependence of transversely isotropic elasticity of human femoral cortical bone on porosity. J Biomech 37: 1281–1287

    Article  Google Scholar 

  • Fan Z, Swadener J, Rho J, Roy M, Pharr G (2002) Anisotropic properties of human tibial cortical bone as measured by nanoindentation. J Orthop Res 20: 806–810

    Article  Google Scholar 

  • Gefen A, Margulies S (2004) Are in vivo and in situ brain tissues mechanically similar. J Biomech 37: 1339–1352

    Article  Google Scholar 

  • Gray S (2000) Cellular physiology of the vocal folds. Otolaryng Clin N Am 33: 679–697

    Article  Google Scholar 

  • Gray S, Titze I, Alipour F, Hammond T (2000) Biomechanical and histological observations of vocal fold fibrous proteins. Ann Otol Rhinol Laryngol 109: 77–85

    Google Scholar 

  • Haji T, Mori K, Omori K, Isshiki N (1992) Mechanical properties of the vocal fold. stress-strain studies. Acta Otolaryngol (Stockh) 112: 559–565

    Article  Google Scholar 

  • Hammond T, Gray S, Butler J (2000) Age- and gender-related collagen distribution in human vocal folds. Ann Otol Rhinol Laryngol 109: 913–920

    Google Scholar 

  • Hirano M, Kakita Y, Ohmaru K, Kurita S (1982) Structure and mechanical properties of the vocal fold. In: Lass N (ed) Speech and language: advances in basic research and practice, vol 7, Academic Press, New York, pp 271–297

  • Ishii K, Zhai W, Akita M, Hirose H (1996) Ultrastructure of the lamina propria of the human vocal fold. Acta Otolaryngol (Stockh) 116: 778–782

    Article  Google Scholar 

  • Kelleher J, Zhang K, Siegmund T, Chan R (2010) Spatially varying properties of the vocal ligament contribute to its eigenfrequency response. J Mech Behav Biomed 3: 600–609

    Article  Google Scholar 

  • Kelleher J, Siegmund T, Chan R, Henslee E (2011) Optical measurements of vocal fold tensile properties: implications for phonatory mechanics. J Biomech 44: 1729–1734

    Article  Google Scholar 

  • Kelleher J, Siegmund T, Chan R (2012) Could spatial heterogeneity in human vocal fold elastic properties improve the quality of phonation? Ann Biomed Eng. doi:10.1007/s10439-012-0609-1

  • Lothe J, Barnett D (1976) On the existence of surface-wave solutions for anisotropic elastic half-spaces with free surface. J Appl Phys 47: 428–433

    Article  Google Scholar 

  • Lotz J, Gerhart T, Hayes W (1991) Mechanical properties of metaphyseal bone in the proximal femur. J Biomech 24: 317–329

    Article  Google Scholar 

  • Mattice J, Lau A, Oyena M, Kent R (2006) Spherical indentation load-relaxation of soft biological tissues. J Mater Res 21: 2003–2010

    Article  Google Scholar 

  • Madruga de Melo E, Lemos M, Aragao Ximenes Filho J, Sennes L, Nascimento Saldiva P, Tsuji D (2003) Distribution of collagen in the lamina propria of the human vocal fold. Laryngoscope 113: 2187–2191

    Article  Google Scholar 

  • Min Y, Titze I, Alipour-Haghighi F (1995) Stress-strain response of the human vocal ligament. Ann Otol Rhinol Laryngol 104: 563–569

    Google Scholar 

  • Miri A, Tripathy U, Mongeau L, Wiseman P (2012) Nonlinear laser scanning microscopy of human vocal folds. Laryngoscope 122: 356–363

    Article  Google Scholar 

  • Monniere V, Sell D (1994) Collagen as a biomarker of aging. In: Balin A (eds) Practical handbook of human biological age determination. CRC Press, Boca Raton

    Google Scholar 

  • Moore S, McMahon P, Debski R (2004) Bi-directional mechanical properties of the axillary pouch of the glenohumeral capsule: implications for modeling and surgical repair. J Biomech Eng 126: 284–288

    Article  Google Scholar 

  • Moore S, McMahon P, Azemi E, Debski R (2005) Bi-directional mechanical properties of the posterior region of the glenohumeral capsule. J Biomech 38: 1365–1369

    Article  Google Scholar 

  • Popov V (2010) Contact mechanics and friction. Springer, Berlin

    Book  MATH  Google Scholar 

  • Quapp K, Weiss J (1998) Material characterization of human medial collateral ligament. J Biomech Eng 120: 757–763

    Article  Google Scholar 

  • Sato K, Hirano M (1997) Age-related changes of elastic fibers in the superficial layer of the lamina propria of vocal folds. Ann Otol Rhinol Laryngol 106: 44–48

    Google Scholar 

  • Swadener J, Pharr G (2001) Indentation of elastically anisotropic half-spaces by cones and parabolae of revolution. Philos Mag A 81: 447–466

    Article  Google Scholar 

  • Swanson S (2004) Hertzian contact of orthotropic materials. Int J Solids Struct 41: 1945–1959

    Article  MATH  Google Scholar 

  • Tateya T, Tateya I, Bless D (2006) Collagen subtypes in human vocal folds. Ann Otol Rhinol Laryngol 115: 469–476

    Google Scholar 

  • Thibeault S, Gray S, Bless D, Chan R, Ford C (2002) Histologic and rheologic characterization of vocal fold scarring. J Voice 16: 96–104

    Article  Google Scholar 

  • Ting T (1996) Anisotropic elasticity. Oxford University Press, New York

    MATH  Google Scholar 

  • Titze I (1976) On the mechanics of vocal-fold vibration. J Acoust Soc Am 60: 1366–1380

    Article  Google Scholar 

  • Titze I (2000) Principles of voice production, 2nd edn. National Center for Voice and Speech, Denver

    Google Scholar 

  • Titze I (2006) The myoelastic aerodynamic theory of phonation. National Center for Voice and Speech, Iowa City

    Google Scholar 

  • Tran Q, Berke G, Gerratt B, Kreiman J (1993) Measurement of young’s modulus in the in vivo human vocal folds. Ann Otol Rhinol Laryngol 102: 584–591

    Google Scholar 

  • Turner J (1980) Contact on a transversely isotropic half-space, or between two transversely isotropic bodies. Int J Solids Struct 16: 409–419

    Article  MATH  Google Scholar 

  • Vlassak J, Ciavarella M, Barber J, Wang X (2003) The indentation modulus of elastically anisotropic materials for indenters of arbitrary shape. J Mech Phys Solids 51: 1701–1721

    Article  MATH  Google Scholar 

  • Willis J (1966) Hertzian contact of anisotropic bodies. J Mech Phys Solids 14: 163–176

    Article  MathSciNet  MATH  Google Scholar 

  • Yoo L, Reed J, Shin A, Kung J, Gimzewski J, Poukens V, Goldberg R, Mancini R, Taban M, Moy R, Demer J (2011) Characterization of ocular tissues using microindentation and hertzian viscoelastic models. Invest Ophthalmol Vis Sci 52: 3475–3482

    Article  Google Scholar 

  • Yu H (2001) A concise treatment of indentation problems in transversely isotropic half-spaces. Int J Solids Struct 38: 2213–2232

    Article  MATH  Google Scholar 

  • Zhang K, Siegmund T, Chan R (2007) A two-layer composite model of the vocal fold lamina propria for fundamental frequency regulation. J Acoust Soc Am 122: 1090–1101

    Article  Google Scholar 

  • Zhang K, Siegmund T, Chan R (2009) Modeling of the transient responses of the vocal fold lamina propria. J Mech Behav Biomed 2: 93–104

    Article  Google Scholar 

  • Zhupanska O (2010) Indentation of a rigid sphere into an elastic half-space in the direction orthogonal to the axis of material symmetry. J Elast 99: 147–161

    Article  MathSciNet  MATH  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thomas Siegmund.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kelleher, J.E., Siegmund, T., Du, M. et al. Empirical measurements of biomechanical anisotropy of the human vocal fold lamina propria. Biomech Model Mechanobiol 12, 555–567 (2013). https://doi.org/10.1007/s10237-012-0425-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10237-012-0425-4

Keywords

Navigation