Advertisement

European Archives of Oto-Rhino-Laryngology

, Volume 270, Issue 6, pp 1885–1895 | Cite as

The anisotropic nature of the human vocal fold: an ex vivo study

  • Anna-Katharina RohlfsEmail author
  • Eric Goodyer
  • Till Clauditz
  • Markus Hess
  • Malte Kob
  • Susan Koops
  • Klaus Püschel
  • Frank W. Roemer
  • Frank Müller
Laryngology

Abstract

The purpose of this study was to measure the relationship between the shear elastic properties of vocal fold with respect to the direction of applied stress. There is extensive published material that quantifies the shear viscoelastic properties of the vocal fold, but as much of these data were obtained using rotating parallel plate rheometers, which are unable to resolve out difference of the shear elastic behaviour with respect to direction, there is very little data that indicates anisotropic behaviour. To overcome this gap in knowledge, the team devised an apparatus that is capable of applying a shear stress in a known direction. A series of measurements were taken at the mid-membranous position, in the transverse and longitudinal directions. Point-specific measurements were performed using fourteen human cadaver excised larynges, which were hemi-sectioned to expose the vocal fold. An extremely low sinusoidal shear force of 1 g was applied tangentially to the membrane surface in both the longitudinal and transverse direction, and the resultant shear strain was measured. With the probe applied to the intact vocal fold, the average ratio of the elasticity in the transverse with respect to the longitudinal direction was 0.55. Further investigation using histological staining of collagens in the lamina propria indicates that there is a visible difference in the general alignment of collagen fibres when comparing the coronal and the sagittal sections. Our conclusion is that there is a quantifiable difference between the shear elastic response of the lamina propria in the longitudinal and transverse directions, and that this could be explained by the difference in alignment of collagen fibres within the lamina propria.

Keywords

Ex vivo human larynx Vocal fold layers Linear skin rheometer Biomechanical properties Anisotropy 

References

  1. 1.
    Mallur PS, Rosen CA (2010) Vocal fold injection: review of indications, techniques, and materials for augmentation. Clin Exp Otorhinolaryngol 3(4):177–182PubMedCrossRefGoogle Scholar
  2. 2.
    Sittel C, Thumfart WF, Pototschnig C, Wittekindt C, Eckel HE (2000) Textured polydimethylsiloxane elastomers in the human larynx: safety and efficiency of use. J Biomed Mater Res 53(6):646–650PubMedCrossRefGoogle Scholar
  3. 3.
    Rosen CA, Gartner-Schmidt J, Casiano R, Anderson TD, Johnson F, Remacle M, Sataloff RT, Abitbol J, Shaw G, Archer S, Zraick RI (2009) Vocal fold augmentation with calcium hydroxylapatite: twelve month report. Laryngoscope 119(5):1033–1041PubMedCrossRefGoogle Scholar
  4. 4.
    Carroll TL, Rosen CA (2010) Trial vocal fold injection. J Voice 24(4):494–498PubMedCrossRefGoogle Scholar
  5. 5.
    Chhetri DK, Berke GS (2011) Injection of cultured autologous fibroblasts for human vocal fold scars. Laryngoscope 121(4):785–792. doi: 10.1002/lary.21417 PubMedCrossRefGoogle Scholar
  6. 6.
    Duflo S, Thibeault SL, Li W, Shu XZ, Prestwich G (2006) Effect of a synthetic extracellular matrix on vocal fold lamina propria gene expression in early wound healing. Tissue Eng 12(11):3201–3207PubMedCrossRefGoogle Scholar
  7. 7.
    Titze IR (1973) The human vocal cords: a mathematical model. I. Phonetica 28(3):129–170PubMedCrossRefGoogle Scholar
  8. 8.
    Titze IR (1974) The human vocal cords: a mathematical model. II. Phonetica 29(1):1–21PubMedCrossRefGoogle Scholar
  9. 9.
    Hirano M, Kikita 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 271–297Google Scholar
  10. 10.
    Perlman AL, Titze IR, Cooper DS (1984) Elasticity of canine vocal fold tissue. J Speech Hear Res 27(2):212–219PubMedGoogle Scholar
  11. 11.
    Perlman AL, Durham PL (1987) In-vitro studies of vocal fold mucosa during isometric condition. In: Baer T, Sasaki C, Harris K (eds) Laryngeal function in phonation and respiration. College-Hill Publications, Boston, pp 291–303Google Scholar
  12. 12.
    Alipour-Haghighi F, Titze IR (1991) Elastic models of vocal fold tissues. J Acoust Soc Am 90(3):1326–1331PubMedCrossRefGoogle Scholar
  13. 13.
    Berke GS (1992) Intraoperative measurement of the elastic modulus of the vocal fold. Part 1. Device development. Laryngoscope 102(7):760–769PubMedCrossRefGoogle Scholar
  14. 14.
    Berke GS, Smith ME (1992) Intraoperative measurement of the elastic modulus of the vocal fold. Part 2. Preliminary results. Laryngoscope 102:770–778PubMedCrossRefGoogle Scholar
  15. 15.
    Tran QT, Berke GS, Gerratt BR, Kreiman J (1993) Measurement of Young‘s modulus in the in vivo human vocal folds. Ann Otol Rhinol Laryngol 102:584–591PubMedGoogle Scholar
  16. 16.
    Min YB, Titze IR, Alipour-Haghighi F (1995) Stress–strain response of the human vocal ligament. Ann Otol Rhinol Laryngol 104(7):563–569PubMedGoogle Scholar
  17. 17.
    Chan RW, Titze IR (1999) Viscoelastic shear properties of human vocal fold mucosa: measurement methodology and empirical results. J Acoust Soc Am 106:2008–2021PubMedCrossRefGoogle Scholar
  18. 18.
    Hsiao TY, Wang CL, Chen CN, Hsieh FJ, Shau YW (2002) Elasticity of human vocal folds measured in vivo using color Doppler imaging. Ultrasound Med Biol 28(9):1145–1152PubMedCrossRefGoogle Scholar
  19. 19.
    Klemuk SA, Riede T, Walsh EJ, Titze IR (2011) Adapted to roar: functional morphology of tiger and lion vocal folds. PLoS One 6(11):e27029 (Epub 2011 Nov 2)PubMedCrossRefGoogle Scholar
  20. 20.
    Chan RW, Titze IR (2000) Viscoelastic shear properties of human vocal fold mucosa: theoretical characterization based on constitutive modeling. J Acoust Soc Am 107(1):565–580PubMedCrossRefGoogle Scholar
  21. 21.
    Kelleher JE, Siegmund T, Du M, Naseri E, Chan RW (2012) Empirical measurements of biomechanical anisotropy of the human vocal fold lamina propria. Biomech Model Mechanobiol. doi: 10.1007/s10237-012-0425-4
  22. 22.
    Miri AK, Mongrain R, Chen LX, Mongeau L (2012) Quantitative assessment of the anisotropy of vocal fold tissue using shear rheometry and traction testing. J Biomech Sep 26. doi: 10.1016/j.jbiomech.2012.08.030
  23. 23.
    Matts P, Goodyer E (1988) A new instrument to measure the mechanical properties of the human stratum corneum. J Cosmet Sci 49:321–323Google Scholar
  24. 24.
    Hertegård S, Dahlqvist A, Goodyer E (2006) Viscoelastic measurements after vocal fold scarring in rabbits—short-term results after hyaluronan injection. Acta Otolaryngol 126(7):758–763PubMedCrossRefGoogle Scholar
  25. 25.
    Goodyer E, Hemmerich S, Müller F, Kobler JB, Hess M (2007) The shear modulus of the human vocal fold, preliminary results from 20 larynxes. Eur Arch Otorhinolaryngol 264(1):45–50PubMedCrossRefGoogle Scholar
  26. 26.
    Dailey SH, Tateya I, Montequin D, Welham NV, Goodyer E (2009) Viscoelastic measurements of vocal folds using the linear skin rheometer. J Voice 23(2):143–150PubMedCrossRefGoogle Scholar
  27. 27.
    Goodyer E, Müller F, Licht K, Hess M (2007) In vivo measurement of the shear modulus of the human vocal fold: interim results from eight patients. Eur Arch Otorhinolaryngol 264(6):631–635PubMedCrossRefGoogle Scholar
  28. 28.
    Dr Askeland, Fulay PP (2006) The science and engineering of material, 5th edn. Cengage Learning Emea, Stamford, p 198Google Scholar
  29. 29.
    Nic M, Jirat J, Kosata B (eds) (2006a) “Shear modulus, G”. IUPAC compendium of chemical terminology, online ed. doi: 10.1351/goldbook.S05635. ISBN 0-9678550-9-8
  30. 30.
    Nic M, Jirat J, Kosata B (eds) (2006b) “Modulus of elasticity (Young‘s modulus), E”. IUPAC compendium of chemical terminology, online ed. doi: 10.1351/goldbook.M03966. ISBN 0-9678550-9-8
  31. 31.
    Hirano M, Kurita S, Nakashima T (1983) Growth, development and aging of human vocal folds. In: Bless DM, Abbs JH (eds) Vocal fold physiology. College Hill Press, San Diego, pp 22–43Google Scholar
  32. 32.
    Bendall JR (1973) Postmortem changes in muscle. In: Bourne GH (ed) The structure and function of muscle, vol 2, part II. Academic Press, New York, pp 244–309Google Scholar
  33. 33.
    Chan RW, Titze IR (2003) Effect of postmortem changes and freezing on the viscoelastic properties of vocal fold tissues. Ann Biomed Eng 31(4):482–491PubMedCrossRefGoogle Scholar
  34. 34.
    Hess MM, Mueller F, Kobler JB, Zeitels SM, Goodyer E (2006) Measurements of vocal fold elasticity using the linear skin rheometer. Folia Phoniatr Logop 58(3):207–216PubMedCrossRefGoogle Scholar
  35. 35.
    Chan RW, Tayama N (2002) Biomechanical effects of hydration in vocal fold tissues. Otolaryngol Head Neck Surg 126(5):528–537PubMedCrossRefGoogle Scholar
  36. 36.
    Hemler RJ, Wieneke GH, Lebacq J, Dejonckere PH (2001) Laryngeal mucosa elasticity and viscosity in high and low relative air humidity. Eur Arch Otorhinolaryngol 258(3):125–129PubMedCrossRefGoogle Scholar
  37. 37.
    Chan RW, Rodriguez ML (2008) A simple-shear rheometer for linear viscoelastic characterization of vocal fold tissues at phonatory frequencies. J Acoust Soc Am 124(2):1207–1219PubMedCrossRefGoogle Scholar
  38. 38.
    Branski RC, Verdolini K, Sandulache V, Rosen CA, Hebda PA (2006) Vocal fold wound healing: a review for clinicians. J Voice 20(3):432–442PubMedCrossRefGoogle Scholar
  39. 39.
    Hsiao TY, Wang CL, Chen CN, Hsieh FJ, Shau YW (2001) Noninvasive assessment of laryngeal phonation function using color Doppler ultrasound imaging. Ultrasound Med Biol 27(8):1035–1040PubMedCrossRefGoogle Scholar
  40. 40.
    McGlashan JA, de Cunha DA, Hawkes DJ, Harris TM (1998) Surface mapping of the vibrating vocal folds. In: Proceedings of the 24th world congress of the international association of logopedics and phoniatrics (IALP), AmsterdamGoogle Scholar
  41. 41.
    Sato K, Hirano M, Nakashima T (2002) Age-related changes of collagenous fibers in the human vocal fold mucosa. Ann Otol Rhinol Laryngol 111(1):15–20PubMedGoogle Scholar
  42. 42.
    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(1):44–48PubMedGoogle Scholar
  43. 43.
    Ohashi T, Abe H, Matsumoto T, Sato M (2005) Pipette aspiration technique for the measurement of nonlinear and anisotropic mechanical properties of blood vessel walls under biaxial stretch. J Biomech 38(11):2248–2256PubMedCrossRefGoogle Scholar
  44. 44.
    Otten M, Müller F, Rohlfs AK, Gömmel A, Hess M, Kob M (2010) 3D measurement of vocal fold elasticity using the linear skin rheometer. In: Proceedings of the 36th German annual conference of acoustics (DAGA), Berlin, pp 265–266Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Anna-Katharina Rohlfs
    • 1
    Email author
  • Eric Goodyer
    • 2
  • Till Clauditz
    • 3
  • Markus Hess
    • 1
  • Malte Kob
    • 4
  • Susan Koops
    • 3
  • Klaus Püschel
    • 5
  • Frank W. Roemer
    • 6
  • Frank Müller
    • 1
  1. 1.Department of Voice, Speech and Hearing DisordersUniversity Medical Center Hamburg-EppendorfHamburgGermany
  2. 2.Centre for Computational Intelligence-Bioinformatics GroupFaculty of Technology, DeMontfort UniversityLeicesterUK
  3. 3.Department of PathologyUniversity Medical Center Hamburg-EppendorfHamburgGermany
  4. 4.Erich Thienhaus InstituteUniversity of Music DetmoldDetmoldGermany
  5. 5.Institute for Forensic MedicineUniversity Medical Center Hamburg-EppendorfHamburgGermany
  6. 6.Department of RadiologyKlinikum AugsburgAugsburgGermany

Personalised recommendations