Acta Oto-Laryngologica

ISSN: 0001-6489 (Print) 1651-2251 (Online) Journal homepage: http://www.tandfonline.com/loi/ioto20

Mechanical Properties of the Vocal Fold Tomoyuki Haji, Kazunori Mori, Koichi Omori & Nobuhiko Isshiki To cite this article: Tomoyuki Haji, Kazunori Mori, Koichi Omori & Nobuhiko Isshiki (1992) Mechanical Properties of the Vocal Fold, Acta Oto-Laryngologica, 112:3, 559-565 To link to this article: http://dx.doi.org/10.3109/00016489209137440

Published online: 08 Jul 2009.

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Date: 25 April 2016, At: 16:16

Acta Otolaryngol (Stockh) 1992; 112: 559-565

Mechanical Properties of the Vocal Fold Stress-Strain Studies TOMOYUKI HAJI,’ KAZUNORI MORI? KOICHI OMORI’ and NOBUHIKO ISSHIK13

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From the ‘Department of Otolaryngology, Kochi Medical School, Nankoku. Kochi, ’Department of Otolaryngology and ’Department of Plastic Surgety. Faculty of Medicine, Kyoto University, Kyoto. Japan

Haji T. Mori K, Omori K, Isshiki N. Mechanical properties of the vocal fold. Str-train studies. Acta Otolaryngol (Stockh) 1992; 1 1 2 559-565. The viscoelasticity of the vocal and ventricular folds was experimentally assessed by analyzing the stress-strain relationships obtained using a newly developed measuring system. The degree of stiffness of the mid-membranous portion of the vocal fold was 1- than that near the anterior commissure or the vocal process. The ventricular fold was much less stiff and significantlymore viscous than the vocal fold. At the membranous portion of the vocal fold, the degree of stiffness was less and that of viscosity greater at 2 mm above and below the free margin than at the free margin itself. Key words: stress-strain relation, viscoelasticity, vocalfold.

INTRODUCTION It is well known that the viscoelastic properties or “stiffness” of the vocal folds greatly affects their vibratory movements during phonation. On the basis of experiments using excised larynges, van den Berg (1) has proposed the “myoelastic aerodynamic theory”, while Hiroto (2) has emphasized the importance of viscoelasticity of the vocal fold mucosa and proposed the “mucoviscoelastic aerodynamic theory”. A variety of lesions such as carcinoma, scamng, atrophy, or edema can affect the viscoelasticity or the stiffness of the vocal folds, producing various degrees of dysphonia (3). Vocal fold viscoelasticity can be estimated clinically by stroboscopy under magnification as well as by high-speed filming, but these techniques are sometimes not accurate enough to allow a quantitative assessment. Quantitative evaluation of the mechanical properties of the vocal folds has been reported with the use of several methods. Kaneko et al. (4) and Tanabe et al. (5) measured the damping ratio of vocal fold vibration in hemilaryngectomized human larynges. The damping ratio is known to be one of the most important viscoelastic parameters, but the necessity of using high-speed filming or other equivalent techniques to determine this ratio has precluded its clinical application. Kaneko et al. (6) assessed the overall stiffness of the vocal folds by measuring stress-strain relations at the mid-portion, when the vocal fold was pulled medially by a string. Using square-pillar frontal sections of human and canine vocal folds, Yokoyama et al. (7)have also measured stress-strain relations of vocal fold tissue. They reported that the strain on the “cover” of the vocal fold is much greater than that on the “body”. Kakita et al. (8) measured the viscoelastic characteristics of each layer of excised vocal fold tissue, including Young’s modulus, differential Young’s modulus, the shear modulus, and the shear viscosity. These studies revealed some important features of the mechanical properties of the vocal fold. However, the layer by layer connection of the block-sectioned vocal folds used in some of these experiments may possibly have created significantly different conditions from those normally applying in the larynx. Kaneko et al. (9-13) have studied the mechanical properties of the vocal folds, including their resonance characteristics, equivalent mass, equivalent stiffness, and damping ratio in a

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noninvasive manner using ultrasound. Although these methods certainly represent a valuable approach to the in vivo study of the human vocal folds, the expenses and the technical problems assoCiated with ultrasound hinder its wider application. We recently developed a simple suction method for measuring the mobility of the vocal fold mucOSa objectively. The mobility of the vocal fold muand the ventricular fold mucosa has been assessed at several points along the free margin, and changes of the mobility of the vocal fold muwere also assessed under some experimental conditions (14). In the current study,,we developed a new stress-strain method and applied it to the objective assessment of the viscoelasticity of the vocal fold and the ventricular fold.

MATERIAL AND METHODS

To determine some of the rheological properties of the vocal folds, stress-strain relationships were assessed using freshly excised human larynges. The anatomical relations of the vocal folds to the other hyngeal structures were left unchanged. A simple and objective measurement system was specifically developed for this purpose, consisting of an accurate potentiometer and a force detector with a needle probe which can be moved up and down by a DC smo-motor. The probe was 5 cm in length and had an orthogonal tip with a diameter of 1

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Fig. 2. Assessment of vocal fold viscoelasticity. A stress-strain diagram was obtained by moving the probe downwards to stress the specimen, and then moving it upwards again. The inclination of the stressstrain curve represents the stiffness of the specimen, while the hysteresis represents mainly the viscosity of the specimen. F: stress, d: displacement (strain). Fig. 3. Parameters used for assessing viscoelasticity.

mm. By moving the probe downwards at a speed of 0.2 mmls to stress the specimen, and then moving it upwards at the same speed, a stress-strain diagram was obtained on an X-Y recorder (Fig. 1 a, b). The viscoelasticity or stiffness of the vocal fold specimen was evaluated by analyzing these stress-strain relationships. The inclination of a stress-strain curve represents the stiffness of a specimen, while the hysteresis, or the difference in the stress-strain curves produced when stress is increasing or decreasing, represents mainly the viscosity of a specimen. This means that the stiffer the specimen, the steeper the inclination of the curve. Furthermore, the more viscous the specimen, the larger the hysteresis of the curve (Fig. 2). To evaluate viscoelasticity quantitatively, two parameters (W,.oand RC%) were introduced. The index, Wl.ois a parameter of the stiffness, which means the work done by an external force until the strain reaches 1.0 mm. It is deduced from the measured area which is enclosed by the stress-strain curve, the horizontal line which crosses the point of F=O g and the vertical line which crosses the point of D = 1.O mm. Compression resilience (RC %) is a parameter of the viscoelasticity. If the specimen is more viscous and less elastic, more internal energy is lost due to internal friction, producing a larger hysteresis or lower RC% (Fig. 3). Using the above-mentioned method, the stiffness of the vocal fold was evaluated at the following three points along the free margin: near the anterior commissure, at the middle of the membranous portion, and near the vocal process. Evaluation was also made at the middle of the ventricular fold margin. Seven vocal folds and seven ventricular folds with no pathological changes were obtained from 4 excised human larynges (4 to 6 hours postmortem; 3 males and 1 female; age range: 38 to 78 years) and used in this experiment. To investigate whether or not vocal fold stiffness differed at a distance from the free margin, the following experiment was performed. In this experiment, we used excised canine larynges because of the ease of obtaining fresh specimens. Stressstrain curve tests were performed for three different sites at the middle of the membranous portion (at the free margin itself and 2

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Fig. 1. Stress-strain curves obtained at different points on the vocal and ventricular folds of a &yearold male.

mm above and below the margin) using three vocal folds obtained from two canine larynges. The larynges were transected vertically at the middle of the interarytenoid portion and extended bilaterally. The needle probe was applied perpendicularly to the mucosal surface.

RESULTS The stressstrain curves for various sites of the vocal and ventricular folds of a 44-year-old male are presented in Fig. 4. At the mid-membranous portion, the stress increment was rather gentle in comparison to the increase in strain until the strain reached about 1 mm. When the strain exceeded this level, the stress showed a steep increase. At the anterior commissure and at the vocal process, the degree of stiffness was found to be greater than in the midmembranous region, as demonstrated by differences in the inclination of the stress-strain curve. The degree of stiffness of the ventricular fold was much less than that of the vocal fold, while that of hysteresis was much greater. Fig. 5 shows W,,values (one of the parameters of stiffness described) at 4 different sites on the vocal fold and the ventricular fold, and clearly demonstrates that the local differences in stiffness were quite consistent among the seven different specimens tested. Significant sex- or age-related differences in rheological features were not found in this experiment. Compression resilience (RC%) was significantly lower at the middle of the ventricular fold margin than at the middle of the membranous part of the vocal fold (Fig. 6). In the frontal plane of the canine vocal fold, the degree of stiffness was less and that of hysteresis greater at the points above or below the free margin than at the margin itself (Fig. 7).

DISCUSSION The present method offers several new possibilities in the assessment of viscoelasticity: 1) It allows estimation of the viscoelastic properties of the intact vocal fold at various sites without block-sectioning or layer-by-layer procedures being needed; 2) It permits continuous recording of the changes in stiffness as the vocal fold tissue is displaced laterally, a movement that also occursduring physiological vocal fold vibration; 3) It allows evaluation of the changes of vocal fold viscosity by analyzing the hysteresis; and 4) It can be performed rapidly without deforming the main laryngeal structure.

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In a histological study of the vocal folds, Kurita (15) reported that the loose and pliable cover (epithelium and superficial layer of the lamina propria) was thickest at the midmembranous portion, becoming thinner both anteriorly and posteriorly from there, while the intermediate layer of the lamina propria (consisting primarily of elastic fibers) was thinnest at the midpoint and became thicker towards both ends. These findings are quite consistent with the results of our experiment, since the degree of stiffness was the least at the mid-membranous portion and higher at the anterior and posterior ends of the vocal fold. Wave-like movements are considered to occur mainly in the superficial layer of the lamina propria during vocal fold vibration (16). From the results of our experiments, the mid-membranous portion may be optimal for allowing vocal fold vibration because of its mechanical and histological features. On the other hand, the anterior commissure and the vocal process have a structure suitable for fixing the membranous portion to the laryngeal framework. From the clinical viewpoint, these findings are probably associated with the fact that vocal fold nodules or polyps usually form in the middle of the membranous portion. Since there are sex- and age-related differences in the histological features of the voca1 folds (17), their mechanical properties may well be affected by both age and sex. However, no significant difference was found in this study, probably because of the insufficient number of specimens tested and the differences of the individual postmortem intervals. Of great interest is the finding that viscosity was higher at planes above and below the free margin of the vocal fold than at the free margin itself in the dog. Though it is still unknown how differences in the mechanical properties across the frontal section affect vocal fold

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larynx at various distances from the free margin of the vocal fold in the frontal plane.

vibration, the above findings could be interpreted as improving the on-and-off switching or transient characteristics of the vocal folds. It is known that the canine vocal fold differs from the human vocal fold in some histological features (3, 18). For example, the canine vocal fold has a wider stratified squamous epithelium and lacks the intermediate layer of the lamina propria. However, the canine vocal fold has the same “body and cover” structure as the human vocal fold, so the above-mentioned findings obtained with canine larynges probably also apply to humans. The ventricular fold was found to be much less stiff and more viscous than the vocal fold. These rheological findings coincide well with the histological findings that the ventricular fold has a poorly developed layer structure and loose submucosal tissue. This means that the ventricular fold is more likely to vibrate in an irregular fashion than the vocal fold. This deduction seems to be justified by clinical experience that phonation with the ventricular folds tends to produce a rough voice. One of the greatest advantages of the present stress-strain method is that it allows the use of an intact excised larynx. Viscoelasticity can thus be assessed easily under various physiological and pathological conditions, which cannot be done when using methods like the block-section and layer-by-layer techniques. This method will certainly facilitate further investigation on the viscwlasticity of the vocal folds, which may give us a better understanding of the mechanism of vocal fold vibration and the factors causing various voice disorders.

CONCLUSION The viscoelasticity of the vocal and ventricular folds was assessed experimentally in en bloc excised human and canine larynges, through analysis of stressstrain relationships using data obtained with a newly developed measurement system. The degree of stiffness of the mid-membranous portion of the vocal fold was less than that of the fold near the anterior commissure and the vocal process. The ventricular fold was far less stiff and significantly more viscous than the vocal fold. In the frontal plane at the membranous portion of the canine vocal fold, the degree of stiffness was less and the viscosity greater at the points beneath or on top of the free margin than at the free margin itself.

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REFERENCES 1. Berg J van den. Myoelastic-aerodynamic theory of voice production. J Speech Hear Res 1958; 1: 227-44. 2. Hiroto I. Pathophysiologyof the larynx on phonatory mechanism (in Japanese). Practica Otol (Kyoto) 1966; 5 9 229-91. 3. Hirano M. Structure of the vocal fold in normal and disease states: Anatomical and physical studies. In: Ludlow CL, Hart MOC, eds. Proceedings of the Conference on the Assessment of Vocal Pathology. ASHAreport 11, 1981; 11-30. 4. Kaneko T, Asano H, Naitoh J et al. Biomechanics of the vocal cord: Damping ratio. J Jpn Bronchoescphagol Soc 1974; 2 5 133-78. 5. Tanabe M, Isshiki N, Sawada M. Damping ratio of the vocal cord. Folia Phoniatr 1979; 31: 27-34. 6. Kaneko T, Asano H, Miura T et al. Biomechanics of the vocal c o r d Stiffness (in Japanese). Practica Otol (Kyoto) 1971; 6 4 1229-35. 7. Yokoyama T, Furukawa M, Hirano M. Structure and stiffness of the human and canine vocal cords. Res Rep Faculty Techno1 Nagasaki Univ 1977; 1 0 75-82. 8. Kakita Y, Hirano M, Ohmaru K. Physical properties ofthe vocal fold tissue; Measurements on excised larynges. In: Stevens KN, Hirano M, eds. Vocal fold physiology. Tokyo: Univ of Tokyo Press, 1981: 377-96. 9. Kaneko T, Uchida I, Suzuki H et al. Mechanical properties of the vocal fold measurement in vivo. In: Stevens KN, Hirano M, eds. Vocal fold physiology. Tokyo: Univ of Tokyo Press, 1981: 365-76. 10. Uchida K.Mechanical properties of the normal vocal fold in vivo. J OtolaryngolJpn 1982; 85: 161-74. 11. Kaneko T, Komatsu K, Suzuki H et al. Mechanical properties of the human vocal fold-resonance characteristics in living humans and in excised larynges. In: Titze IR, Scherer RC, eds. Vocal fold physiology, biomechanics, acoustics and phonatory control. Denver: Denver Center for Performing Arts, 1983: 304-17. 12. Komatsu K. Mechanical properties of the vocal folds of fresh excised human larynxes. J Otolaryngol Jpn 1985; 8 8 148-60. 13. Shimada A. Mechanical properties of the human vocal fold elicited by a single rectangular pulse: Damping ratio. J Otolaryngol Jpn 1987; 90:1992-2003. 14. Haji T, lsshiki N, Mori K et al. Experimental study of the mobility of the vocal fold mucosa. Folia Phoniatr 1991; 43: 21-8. 15. Kurita S. Layer structure of the human vocal fold morphological investigation. Otologica Fukuoka 1980; 26: 973-97. 16. Hirano M.Phonosurgery: Basic and clinical investigations. Otologica Fukuoka 1975; 21: 239-440. 17. Hirano M, Kurita S, Nakashima T. Growth, development, and aging of human vocal folds. In: Bless DM, Abbs JH, eds. Vocal fold physiology. San Diego: College-Hill Press, 1983: 22-43. 18. Kurita S,Nagata K,Hirano M. A comparative study of the layer structure of the vocal fold. In: Bless DM, Abbs JH, eds. Vocal fold physiology. San Diego: College-Hill Press, 1983: 3-21.

Manuscript received April 8, 1991; accepted September 10, 1991 Address for correspondence: Tomoyuki Haji, Department of Otolaryngology, Kochi Medical School, Kohasu, Oko-cho, Nankoku, Kochi 783, Japan

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Mechanical properties of the vocal fold. Stress-strain studies.

The viscoelasticity of the vocal and ventricular folds was experimentally assessed by analyzing the stress-strain relationships obtained using a newly...
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