Viscoelastic measurements of vocal folds using the linear skin rheometer

Abstract

As the number of interventions for vocal fold scar grows and with the advancement of mathematical modeling, greater accuracy and precision in the measurement of vocal fold pliability will become essential. Although indirect pliability measures have been used successfully, direct measurement of tissue pliability is essential. Indirect measurement with parallel plate technology has limitations; it requires the tissue to be removed from the surrounding framework, allows no site specificity, and offers no future for in vivo use in animals or humans. We tested the linear skin rheometer (LSR) in the evaluation of vocal fold pliability. We measured site-specific rheology of vocal folds thereby creating "pliability maps" in human, dog, and rat cadaveric larynges under conditions of altered stiffness; the canine vocal folds possessed sulci, the rat vocal fold was stiff secondary to controlled biopsy, and the human vocal fold was injected with trichloroacetic acid. Histology was performed to confirm the site and type of canine sulci. We found that the LSR reliably detected stiffness in the vocal folds of all species and created "pliability maps" consistent with previous data and clinical observations. The LSR should prove useful in the evaluation of vocal fold pliability for ex vivo and ultimately for in vivo applications.

FIGURE 1.

Schematic of the LSR device.

FIGURE 2.

The LSR device as used for DSR measurements on hemilarynges.

FIGURE 3.

The DSR measurement setup. A custom needle probe (100 mm length, 1 mm diameter, 5 mm tapered tip) was inserted into each vocal fold region of interest, perpendicular to the plane of the vocal fold medial edge and at a depth of 1 mm. Data were collected across a matrix of 30 (6×5) measurement points to map variations in DSR as a function of vocal fold region. The dimension with six points was in the anterior-posterior plane: the most anterior point was placed 2 mm from the attachment of the vocal fold to the thyroid cartilage and the most posterior point was placed at the vocal process. The dimension with five points was in the inferior-superior plane: Hemilarynges were marked at the superior, mid, and inferior third positions of the vocal fold lumen surface in addition to the marking at the superior vocal fold surface and in the subglottal region.

FIGURE 4.

A representative 2D map of variations in DSR by vocal fold region in a normal canine vocal fold. Y-axis values 1, 2, and 3 correspond to measurement points on the inferior, middle, and superior third of the medial surface of the vocal fold, respectively. X-axis values (1–6) correspond to measurement points progressing from the anterior to posterior end of the membranous vocal fold, respectively. DSR values are consistently higher in the anterior and posterior vocal fold regions compared with the midmembranous region. In the midmembranous region, DSR values are highest near the free edge. DSR units are g/mm.

FIGURE 5.

A representative 2D map of variations in DSR by vocal fold region in a normal human vocal fold. Y-axis values 1, 2, 3, 4, and 5 correspond to measurement points on the subglottis, inferior, middle, and superior third of the medial surface, and superior surface of the vocal fold, respectively. X-axis values (1–6) correspond to measurement points progressing from the anterior to posterior end of the membranous vocal fold, respectively. DSR values in the posterior vocal fold region are higher than all other vocal fold regions. DSR is highest at the vocal process, with a value of 2.78 g/mm. DSR values in the subglottal region are greater than those observed in the vocal fold proper. DSR units are g/mm.

FIGURE 6.

Mean DSR values of normal and scarred rat vocal folds (1.35 [±0.20] and 2.37 [±0.23] g/mm, respectively).

FIGURE 7.

Gross appearance (upper row), EVG stain (middle row), and 2D map of DSR value by vocal fold region (lower row), in canine vocal folds with bilateral sulcus vocalis. Gross appearance and 2D DSR map of the left vocal fold are flipped horizontally. Y-axis values 1, 2, 3, 4, and 5 of the left vocal fold correspond to measurement points on the subglottis, inferior, middle, and superior third of the medial surface, and superior surface of the vocal fold, respectively. Y-axis values 1, 2, and 3 of the right vocal fold correspond to measurement points on the inferior, middle, and superior third of the medial surface, respectively. X-axis values (1–6) correspond to measurement points progressing from the anterior to posterior end of the membranous vocal fold, respectively. The upper and lower white lines indicate the free edge and lower margin of the vocal fold. DSR units are g/mm. (Left) Localized type 3 sulcus in the superior third of the left midmembranous vocal fold. DSR values in the sulcus region (white dashed line) are relatively higher than in the surrounding area. DSR values in the anterior and posterior vocal fold regions are higher than those in the midmembranous region. (Right) Localized shallow type 2 sulcus in the superior third of the right midmembranous vocal fold. DSR values in the sulcus region (white dashed line) appear consistent with those in the surrounding area. DSR values in the anterior and posterior vocal fold regions are higher than those in the midmembranous region.

FIGURE 8.

Effect of TCA application on DSR values in the human vocal fold. A. Pliability map before treatment with TCA. B. Pliability map after the treatment with topical TCA. C. Pliability map after the treatment with topical and injected TCA. Y-axis values 1, 2, 3, 4, and 5 correspond to measurement points on the subglottis, inferior, middle, and superior third of the medial surface, and superior surface of the vocal fold, respectively. X-axis values (1–6) correspond to measurement points progressing from the anterior to posterior end of the membranous vocal fold, respectively. DSR units are g/mm.

FIGURE 9.

Plots of the differences in DSR values between normal and topical TCA injection (blue diamonds) and normal and topical + injected TCA vocal folds (yellow diamonds). Areas with higher pretest DSR rates (ie, stiff tissues such as cartilage) experience less alteration than areas with low pretest DSR rates (eg, midmembranous vocal fold). Values of DSR are measured in g/mm. X-axis is pretest elasticity. Y-axis is the difference in g/mm between pre- and posttest.

FIGURE 10.

Graph of a fitted linear plot derived from measuring the loss rate of fluids of known viscosity. X-axis is loss rate measured in g/mm. Y-axis is viscosity measured in cP.