Skip to main content
Top
Published in: European Archives of Oto-Rhino-Laryngology 6/2013

01-05-2013 | Laryngology

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

Authors: Anna-Katharina Rohlfs, Eric Goodyer, Till Clauditz, Markus Hess, Malte Kob, Susan Koops, Klaus Püschel, Frank W. Roemer, Frank Müller

Published in: European Archives of Oto-Rhino-Laryngology | Issue 6/2013

Login to get access

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.
Literature
1.
go back to reference Mallur PS, Rosen CA (2010) Vocal fold injection: review of indications, techniques, and materials for augmentation. Clin Exp Otorhinolaryngol 3(4):177–182PubMedCrossRef Mallur PS, Rosen CA (2010) Vocal fold injection: review of indications, techniques, and materials for augmentation. Clin Exp Otorhinolaryngol 3(4):177–182PubMedCrossRef
2.
go back to reference 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):646–650PubMedCrossRef 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):646–650PubMedCrossRef
3.
go back to reference 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):1033–1041PubMedCrossRef 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):1033–1041PubMedCrossRef
6.
go back to reference 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):3201–3207PubMedCrossRef 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):3201–3207PubMedCrossRef
9.
go back to reference 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 271–297 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 271–297
10.
go back to reference Perlman AL, Titze IR, Cooper DS (1984) Elasticity of canine vocal fold tissue. J Speech Hear Res 27(2):212–219PubMed Perlman AL, Titze IR, Cooper DS (1984) Elasticity of canine vocal fold tissue. J Speech Hear Res 27(2):212–219PubMed
11.
go back to reference 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 291–303 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 291–303
12.
go back to reference Alipour-Haghighi F, Titze IR (1991) Elastic models of vocal fold tissues. J Acoust Soc Am 90(3):1326–1331PubMedCrossRef Alipour-Haghighi F, Titze IR (1991) Elastic models of vocal fold tissues. J Acoust Soc Am 90(3):1326–1331PubMedCrossRef
13.
go back to reference Berke GS (1992) Intraoperative measurement of the elastic modulus of the vocal fold. Part 1. Device development. Laryngoscope 102(7):760–769PubMedCrossRef Berke GS (1992) Intraoperative measurement of the elastic modulus of the vocal fold. Part 1. Device development. Laryngoscope 102(7):760–769PubMedCrossRef
14.
go back to reference Berke GS, Smith ME (1992) Intraoperative measurement of the elastic modulus of the vocal fold. Part 2. Preliminary results. Laryngoscope 102:770–778PubMedCrossRef Berke GS, Smith ME (1992) Intraoperative measurement of the elastic modulus of the vocal fold. Part 2. Preliminary results. Laryngoscope 102:770–778PubMedCrossRef
15.
go back to reference 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 102:584–591PubMed 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 102:584–591PubMed
16.
go back to reference Min YB, Titze IR, Alipour-Haghighi F (1995) Stress–strain response of the human vocal ligament. Ann Otol Rhinol Laryngol 104(7):563–569PubMed Min YB, Titze IR, Alipour-Haghighi F (1995) Stress–strain response of the human vocal ligament. Ann Otol Rhinol Laryngol 104(7):563–569PubMed
17.
go back to reference Chan RW, Titze IR (1999) Viscoelastic shear properties of human vocal fold mucosa: measurement methodology and empirical results. J Acoust Soc Am 106:2008–2021PubMedCrossRef Chan RW, Titze IR (1999) Viscoelastic shear properties of human vocal fold mucosa: measurement methodology and empirical results. J Acoust Soc Am 106:2008–2021PubMedCrossRef
18.
go back to reference 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):1145–1152PubMedCrossRef 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):1145–1152PubMedCrossRef
19.
go back to reference 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)PubMedCrossRef 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)PubMedCrossRef
20.
go back to reference 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):565–580PubMedCrossRef 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):565–580PubMedCrossRef
21.
go back to reference 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 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
23.
go back to reference Matts P, Goodyer E (1988) A new instrument to measure the mechanical properties of the human stratum corneum. J Cosmet Sci 49:321–323 Matts P, Goodyer E (1988) A new instrument to measure the mechanical properties of the human stratum corneum. J Cosmet Sci 49:321–323
24.
go back to reference 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):758–763PubMedCrossRef 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):758–763PubMedCrossRef
25.
go back to reference 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):45–50PubMedCrossRef 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):45–50PubMedCrossRef
26.
go back to reference 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):143–150PubMedCrossRef 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):143–150PubMedCrossRef
27.
go back to reference 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):631–635PubMedCrossRef 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):631–635PubMedCrossRef
28.
go back to reference Dr Askeland, Fulay PP (2006) The science and engineering of material, 5th edn. Cengage Learning Emea, Stamford, p 198 Dr Askeland, Fulay PP (2006) The science and engineering of material, 5th edn. Cengage Learning Emea, Stamford, p 198
30.
go back to reference 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 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.
go back to reference 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 22–43 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 22–43
32.
go back to reference 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 244–309 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 244–309
33.
go back to reference Chan RW, Titze IR (2003) Effect of postmortem changes and freezing on the viscoelastic properties of vocal fold tissues. Ann Biomed Eng 31(4):482–491PubMedCrossRef Chan RW, Titze IR (2003) Effect of postmortem changes and freezing on the viscoelastic properties of vocal fold tissues. Ann Biomed Eng 31(4):482–491PubMedCrossRef
34.
go back to reference 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):207–216PubMedCrossRef 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):207–216PubMedCrossRef
35.
go back to reference Chan RW, Tayama N (2002) Biomechanical effects of hydration in vocal fold tissues. Otolaryngol Head Neck Surg 126(5):528–537PubMedCrossRef Chan RW, Tayama N (2002) Biomechanical effects of hydration in vocal fold tissues. Otolaryngol Head Neck Surg 126(5):528–537PubMedCrossRef
36.
go back to reference 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):125–129PubMedCrossRef 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):125–129PubMedCrossRef
37.
go back to reference 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):1207–1219PubMedCrossRef 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):1207–1219PubMedCrossRef
38.
go back to reference Branski RC, Verdolini K, Sandulache V, Rosen CA, Hebda PA (2006) Vocal fold wound healing: a review for clinicians. J Voice 20(3):432–442PubMedCrossRef Branski RC, Verdolini K, Sandulache V, Rosen CA, Hebda PA (2006) Vocal fold wound healing: a review for clinicians. J Voice 20(3):432–442PubMedCrossRef
39.
go back to reference 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):1035–1040PubMedCrossRef 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):1035–1040PubMedCrossRef
40.
go back to reference 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), Amsterdam 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), Amsterdam
41.
go back to reference 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):15–20PubMed 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):15–20PubMed
42.
go back to reference 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):44–48PubMed 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):44–48PubMed
43.
go back to reference 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):2248–2256PubMedCrossRef 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):2248–2256PubMedCrossRef
44.
go back to reference 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 265–266 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 265–266
Metadata
Title
The anisotropic nature of the human vocal fold: an ex vivo study
Authors
Anna-Katharina Rohlfs
Eric Goodyer
Till Clauditz
Markus Hess
Malte Kob
Susan Koops
Klaus Püschel
Frank W. Roemer
Frank Müller
Publication date
01-05-2013
Publisher
Springer-Verlag
Published in
European Archives of Oto-Rhino-Laryngology / Issue 6/2013
Print ISSN: 0937-4477
Electronic ISSN: 1434-4726
DOI
https://doi.org/10.1007/s00405-013-2428-x

Other articles of this Issue 6/2013

European Archives of Oto-Rhino-Laryngology 6/2013 Go to the issue