Viscoelastic modeling of canine vocalis muscle in relaxation

Analysis of vocal fold vibration requires information on the viscoelastic properties of the vocalis muscle. The force response of two canine vocalis muscles was measured in one-dimensional, stepwise elongation of the tissue as a function of time with a computer-controlled ergometer. The viscoelastic behavior of the muscle in its passive state was demonstrated through the relaxation test. A quasilinear viscoelastic model was used to parametrize the relaxation function, and results are reported for various levels of strain. Furthermore, a model was used to obtain theoretical time-dependent stress-strain curves to compare with experimental data.     

A three-dimensional model of vocal fold abduction/adduction

A three-dimensional biomechanical model of tissue deformation was developed to simulate dynamic vocal fold abduction and adduction. The model was made of 1721 nearly incompressible finite elements. The cricoarytenoid joint was modeled as a rocking-sliding motion, similar to two concentric cylinders. The vocal ligament and the thyroarytenoid muscle's fiber characteristics were implemented as a fiber-gel composite made of an isotropic ground substance imbedded with fibers. These fibers had contractile and/or passive nonlinear stress-strain characteristics. The verification of the model was made by comparing the range and speed of motion to published vocal fold kinematic data. The model simulated abduction to a maximum glottal angle of about 31 degrees. Using the posterior-cricoarytenoid muscle, the model produced an angular abduction speed of 405 degrees per second. The system mechanics seemed to favor abduction over adduction in both peak speed and response time, even when all intrinsic muscle properties were kept identical. The model also verified the notion that the vocalis and muscularis portions of the thyroarytenoid muscle play significantly different roles in posturing, with the muscularis portion having the larger effect on arytenoid movement. Other insights into the mechanisms of abduction/adduction were given.     

Characterization of chronic vocal fold scarring in a rabbit model

The purpose of the current study was to assess the histologic and rheologic properties of the scarred vocal fold lamina propria during a chronic phase of wound repair in a rabbit model. Eighteen rabbit larynges were scarred using a procedure that involved stripping the vocal fold lamina propria down to the thyroarytenoid muscle, using 3-mm microforceps. The approximate dimension of injury to the vocal fold was 3 x 1.5 x 0.5 mm [length x width x depth]. At 6 months postoperatively, histologic analysis of the scarred and control lamina propria in eight of these rabbits was completed for collagen, procollagen, elastin, and hyaluronic acid. Compared with control samples, scarred tissue samples revealed fragmented and disorganized elastin fibers. Additionally, collagen was significantly increased, organized, and formed thick bundles in the scarred vocal fold lamina propria. Measurements of the viscoelastic shear properties of the scarred and control lamina propria in the remaining 10 rabbits revealed increased elastic shear modulus (G') in 8 of 10 scarred samples and increased dynamic viscosity (eta') in 9 of 10 scarred samples. Although rheologic differences were not statistically significant, they revealed that on average, scarred samples were stiffer and more viscous than the normal controls. Histologic data are interpreted as indicating that by 6 months postinjury, the scarred rabbit vocal fold has reached a mature phase of wound repair, characterized by an increased, organized, and thick bundle collagen matrix. Rheologic data are interpreted as providing support for the potential role of increased, thick bundle collagen, and a disorganized elastin network on shear stiffness and dynamic viscosity in the chronic vocal fold scar. Based on these results, a 6-month postoperative time frame is proposed for future studies of chronic vocal fold scarring using the rabbit animal model.     

Measurements of vocal fold tissue viscoelasticity: approaching the male phonatory frequency range

Viscoelastic shear properties of human vocal fold tissues have been reported previously. However, data have only been obtained at very low frequencies (< or = 15 Hz). This necessitates data extrapolation to the frequency range of phonation based on constitutive modeling and time-temperature superposition. This study attempted to obtain empirical measurements at higher frequencies with the use of a controlled strain torsional rheometer, with a design of directly controlling input strain that introduced significantly smaller system inertial errors compared to controlled stress rheometry. Linear viscoelastic shear properties of the vocal fold mucosa (cover) from 17 canine larynges were quantified at frequencies of up to 50 Hz. Consistent with previous data, results showed that the elastic shear modulus (G'), viscous shear modulus (G"), and damping ratio (zeta) of the vocal fold mucosa were relatively constant across 0.016-50 Hz, whereas the dynamic viscosity (eta') decreased monotonically with frequency. Constitutive characterization of the empirical data by a quasilinear viscoelastic model and a statistical network model demonstrated trends of viscoelastic behavior at higher frequencies generally following those observed at lower frequencies. These findings supported the use of controlled strain rheometry for future investigations of the viscoelasticity of vocal fold tissues and phonosurgical biomaterials at phonatory frequencies.     

Assessment of local vocal fold deformation characteristics in an in vitro static tensile test

Voice quality is strongly dependent on vocal fold dynamics, which in turn are dependent on lung pressure and vocal fold biomechanics. Numerical and physical models are often used to investigate the interactions of these different subsystems. However, the utility of numerical and physical models is limited unless appropriately validated with data from physiological models. Hence a method that enables analysis of local vocal fold deformations along the entire surface is presented. In static tensile tests, forces are applied to distinctive working points being located in cover and muscle, respectively, so that specific layer properties can be investigated. The forces are directed vertically upward and are applied along or above the vocal fold edge. The resulting deformations are analyzed using multiple perspectives and three-dimensional reconstruction. Deformation characteristics of four human vocal folds were investigated. Preliminary results showed two phases of deformation: a range with a small slope for small deformations fading into a significant nonlinear deformation trend with a high slope. An increase of tissue stiffness from posterior to anterior was detected. This trend is more significant for muscle and in the mid-anterior half of the vocal fold.     

A theoretical study of the effects of various laryngeal configurations on the acoustics of phonation.

Simulation of glottal volume flow and vocal fold tissue movement was accomplished by numerical solution of a time-dependent boundary value problem, in which nonuniform, orthotropic, linear, incompressible vocal fold tissue media were surrounded by irregularly shaped boundaries, which were either fixed or subject to aerodynamic stresses. Spatial nonuniformity of the tissues was of the layered type, including a mucosal layer, a ligamental layer, and muscular layers. Orthotropy was required to stabilized the vocal folds longitudinally and to accomodate large variations in muscular stress. Incompressibility and vertical motions at the golttis played an important role in producing and sustaining phonation. A nominal configuration for male fundamental speaking pitches was selected, and the regulation of fundamental frequency, intensity, average volume flow, and vocal efficiency was investigated in terms of variations around this nominal configuration. Parameters which were varied consisted of geometrical factors such as length, thickness, and depth, factors for shaping the glottis, as well as tissue elasticities, tissue viscosities, and subglottal pressure. Since nonlinear stress-strain properties were not included, subglottal pressure did not produce a pronounced effect upon fundamental frequency under these somewhat edealized conditions F0 rasing correlated strongly with increased tension in the ligament, and somewhat with increasing tension in the vocalis. F0 lowering correlated with increase in vocal fold length when the tensions were held constant, but not with increase in vocal fold thickness. Vocal intensity and efficiency are shown to have local maxima as the configurational parameters are varied one at a time. It appears that oral acoustic power output and vocal efficiency can be maximized by proper adjustments of longitudinal tension of nonmuscular (mucosal and ligamental) tissue layers in relation to muscular layers. Quantitative verification of the "body-cover" theory is therefore suggested, and several further implications with regard to control of the human larynx are considered.     

Three-dimensional biomechanical properties of human vocal folds: parameter optimization of a numerical model to match in vitro dynamics

The human voice signal originates from the vibrations of the two vocal folds within the larynx. The interactions of several intrinsic laryngeal muscles adduct and shape the vocal folds to facilitate vibration in response to airflow. Three-dimensional vocal fold dynamics are extracted from in vitro hemilarynx experiments and fitted by a numerical three-dimensional-multi-mass-model (3DM) using an optimization procedure. In this work, the 3DM dynamics are optimized over 24 experimental data sets to estimate biomechanical vocal fold properties during phonation. Accuracy of the optimization is verified by low normalized error (0.13 ± 0.02), high correlation (83% ± 2%), and reproducible subglottal pressure values. The optimized, 3DM parameters yielded biomechanical variations in tissue properties along the vocal fold surface, including variations in both the local mass and stiffness of vocal folds. That is, both mass and stiffness increased along the superior-to-inferior direction. These variations were statistically analyzed under different experimental conditions (e.g., an increase in tension as a function of vocal fold elongation and an increase in stiffness and a decrease in mass as a function of glottal airflow). The study showed that physiologically relevant vocal fold tissue properties, which cannot be directly measured during in vivo human phonation, can be captured using this 3D-modeling technique.     

Effects of long-term intubation on vocal fold mucosa in dogs

A canine model was used to study effects of long-term intubation on vocal fold mucosa. Dogs' larynges were removed 5 weeks after a 7-day intubation period and were compared with control tissue. Intubation effects on vocal fold mucosa were highly variable. Most severe damage was observed posteriorly, at the presumed location of direct tube-mucosa contact. Effects judged to be less severe but still significant were noted in tissue anterior to this site. Morphometric analysis of the layers of the intubated mucosa revealed significant differences in epithelium, connective tissue, and glands, as compared with control tissue. Differences were also observed for blood vessels and nerves. Of particular clinical importance was evidence of damage along membranous, as well as cartilaginous, portions of the true vocal fold, and of damaged connective tissue and cartilage underlying epithelium which appeared normal. Implications of the findings for recovery from intubation, and for voice, are discussed.     

A simple-shear rheometer for linear viscoelastic characterization of vocal fold tissues at phonatory frequencies

Previous studies reporting the linear viscoelastic shear properties of the human vocal fold cover or mucosa have been based on torsional rheometry, with measurements limited to low audio frequencies, up to around 80 Hz. This paper describes the design and validation of a custom-built, controlled-strain, linear, simple-shear rheometer system capable of direct empirical measurements of viscoelastic shear properties at phonatory frequencies. A tissue specimen was subjected to simple shear between two parallel, rigid acrylic plates, with a linear motor creating a translational sinusoidal displacement of the specimen via the upper plate, and the lower plate transmitting the harmonic shear force resulting from the viscoelastic response of the specimen. The displacement of the specimen was measured by a linear variable differential transformer whereas the shear force was detected by a piezoelectric transducer. The frequency response characteristics of these system components were assessed by vibration experiments with accelerometers. Measurements of the viscoelastic shear moduli (G' and G") of a standard ANSI S2.21 polyurethane material and those of human vocal fold cover specimens were made, along with estimation of the system signal and noise levels. Preliminary results showed that the rheometer can provide valid and reliable rheometric data of vocal fold lamina propria specimens at frequencies of up to around 250 Hz, well into the phonatory range.     

Experimental study of the effects of surface mucus viscosity on the glottic cycle

Numerous clinical findings indicate that viscosity of laryngeal mucosa is a crucial factor in glottal perfomance. Experience using experimental test benches has shown the importance of humidifying air stream used to induce vibration in excised larynges. Nevertheless, there is a lack of knowledge particularly regarding the physicochemical properties of laryngeal mucus. The purpose of this study was to research vocal fold vibration in excised larynges using artificial mucus of precisely known viscosity. Eight freshly harvested porcine larynges were examined. Parameters measured were Fo and vocal fold contact time. Measurements were performed under three conditions: basal (no fluid application on vocal cord surface), after application of a fluid of 60cP viscosity (Visc60), and after application of a fluid of 100cP viscosity (Visc100). Electroglottographic measurements were performed at two different times for each condition: 1 s after airflow onset (T1) and 6 seconds after airflow onset (T2). Statistical analysis consisted of comparing data obtained under each condition at T1 and T2. The results showed a significant decrease in Fo after application of Visc60 and Visc100 fluids and a decrease in Fo at T2. Closure time was significantly higher under Visc60 conditions and under Visc100 conditions than under basal conditions. Application of artificial mucus to the mucosa of the vocal folds lowered vibratory frequency and prolonged the contact phase. Our interpretation of this data is that the presence of mucus on the surface of the vocal folds generated superficial tension and caused adhesion, which is a source of nonlinearity in vocal vibration.     

Interstitial protein alterations in rabbit vocal fold with scar

Fibrous and interstitial proteins compose the extracellular matrix of the vocal fold lamina propria and account for its biomechanic properties. Vocal fold scarring is characterized by altered biomechanical properties, which create dysphonia. Although alterations of the fibrous proteins have been confirmed in the rabbit vocal fold scar, interstitial proteins, which are known to be important in wound repair, have not been investigated to date. Using a rabbit model, interstitial proteins decorin, fibromodulin, and fibronectin were examined immunohistologically, two months postinduction of vocal fold scar by means of forcep biopsy. Significantly decreased decorin and fibromodulin with significantly increased fibronectin characterized scarred vocal fold tissue. The implications of altered interstitial proteins levels and their affect on the fibrous proteins will be discussed in relation to increased vocal fold stiffness and viscosity, which characterizes vocal fold scar.     

Simulated effects of cricothyroid and thyroarytenoid muscle activation on adult-male vocal fold vibration

Adjustments to cricothyroid and thyroarytenoid muscle activation are critical to the control of fundamental frequency and aerodynamic aspects of vocal fold vibration in humans. The aerodynamic and physical effects of these muscles are not well understood and are difficult to study in vivo. Knowledge of the contributions of these two muscles is essential to understanding both normal and disordered voice physiology. In this study, a three-mass model for voice simulation in adult males was used to produce systematic changes to cricothyroid and thyroarytenoid muscle activation levels. Predicted effects on fundamental frequency, aerodynamic quantities, and physical quantities of vocal fold vibration were assessed. Certain combinations of these muscle activations resulted in aerodynamic and physical characteristics of vibration that might increase the mechanical stress placed on the vocal fold tissue.     

Cooperative Regulation of Vocal Fold Morphology and Stress by the Cricothyroid and Thyroarytenoid Muscles

Voice is produced by vibrations of vocal folds that consist of multiple layers. The portion of the vocal fold tissue that vibrates varies depending primarily on laryngeal muscle activity. The effective depth of tissue vibration should significantly influence the vibrational behavior of the tissue and resulting voice quality. However, thus far, the effect of the activation of individual muscles on the effective depth is not well understood. In this study, a three-dimensional finite element analysis is performed to investigate the effect of the activation of two major laryngeal muscles, the cricothyroid (CT) and thyroarytenoid (TA) muscles, on vocal fold morphology and stress distribution in the tissue. Because structures that bear less stress can easily be deformed and involved in vibration, information on the morphology and stress distribution may provide a useful estimate of the effective depth. The results of the analyses indicate that the two muscles perform distinct roles, which allow cooperative control of the morphology and stress. When the CT muscle is activated, the tip region of the vocal folds becomes thinner and curves upward, resulting in the elevation of the stress magnitude all over the tissue to a certain degree that depends on the stiffness of each layer. On the other hand, the TA muscle acts to suppress the morphological change and controls the stress magnitude in a position-dependent manner. Thus, the present analyses demonstrate quantitative relationships between the two muscles in their cooperative regulation of vocal fold morphology and stress.     

Optoreflectometry Determination of the Resonance Properties of a Vocal Fold

A new method of measuring the resonance properties of a vocal fold using electromagnetic excitation and laser optoreflectometry for response monitoring is described. Two resonance peaks were experimentally identified with one magnet stuck on the vocal fold at frequencies F0(1m)=54.7 Hz and F0'(1m)=35.8 Hz. The addition of a second magnet allowed calculation of the actual viscoelastic properties of the vocal fold: F0=71.8 Hz; quality factor Q=8.03; mass m=0.057 g; stiffness k=11.6 Nm; and damping zeta=0.0032 Nm(-1). A numerical simulation of a two-layered model verified the experimental data.     

High frequency ultrasonic characterization of human vocal fold tissue

Recently, endolaryngeal sonography at frequencies ranging from 10 to 30 MHz has been found to be useful in diagnosing diseases of the vocal folds (VFs). However, image resolution can be further improved by ultrasound at higher frequencies, necessitating the measurement of high-frequency acoustic properties of VF tissue. The ultrasonic parameters of integrated backscatter, sound velocity, and frequency-dependent attenuation coefficient were measured in both the lamina propria (LP) and vocalis muscle (VM) of human VFs using a 47 MHz high-frequency ultrasonic transducer. The integrated backscatter was -173.44+/-6.14 (mean+/-s.d.) and -195.13+/-3.58 dB in the LP and VM, respectively, the sound velocity was 1667.68+/-44.9 and 1595.07+/-39.33 ms, and the attenuation coefficient at 47 MHz was 8.28+/-1.72 and 7.17+/-1.30 dBmm. The difference between these ultrasonic parameters may be attributed to variations in the structure and fiber concentrations in VF tissue. These results could serve as a useful clinical reference for the further development of high-frequency ultrasound devices for endolarynx sonography applications.     

Dependence of phonation threshold pressure on vocal tract acoustics and vocal fold tissue mechanics

Analytical and computer simulation studies have shown that the acoustic impedance of the vocal tract as well as the viscoelastic properties of vocal fold tissues are critical for determining the dynamics and the energy transfer mechanism of vocal fold oscillation. In the present study, a linear, small-amplitude oscillation theory was revised by taking into account the propagation of a mucosal wave and the inertive reactance (inertance) of the supraglottal vocal tract as the major energy transfer mechanisms for flow-induced self-oscillation of the vocal fold. Specifically, analytical results predicted that phonation threshold pressure (Pth) increases with the viscous shear properties of the vocal fold, but decreases with vocal tract inertance. This theory was empirically tested using a physical model of the larynx, where biological materials (fat, hyaluronic acid, and fibronectin) were implanted into the vocal fold cover to investigate the effect of vocal fold tissue viscoelasticity on Pth. A uniform-tube supraglottal vocal tract was also introduced to examine the effect of vocal tract inertance on Pth. Results showed that Pth decreased with the inertive impedance of the vocal tract and increased with the viscous shear modulus (G") or dynamic viscosity (eta') of the vocal fold cover, consistent with theoretical predictions. These findings supported the potential biomechanical benefits of hyaluronic acid as a surgical bioimplant for repairing voice disorders involving the superficial layer of the lamina propria, such as scarring, sulcus vocalis, atrophy, and Reinke's edema.     

A virtual trajectory model predicts differences in vocal fold kinematics in individuals with vocal hyperfunction

A simple, one degree of freedom virtual trajectory model of vocal fold kinematics was developed to investigate whether kinematic features of vocal fold movement confirm increased muscle stiffness. Model simulations verified that increases in stiffness were associated with changes in kinematic parameters, suggesting that increases in gesture rate would affect kinematic features to a lesser degree in vocal hyperfunction patients given the increased levels of muscle tension they typically employ to phonate. This hypothesis was tested experimentally in individuals with muscle tension dysphonia (MTD; N = 10) and vocal nodules (N = 10) relative to controls with healthy normal voice (N = 10) who were examined with trans-nasal endoscopy during a simple vocal fold abductory-adductory task. Kinematic measures in MTD patients were less affected by increased gesture rate, consistent with the hypothesis that these individuals have elevated typical laryngeal muscle tension. Group comparisons of the difference between medium and fast gesture rates (Mann-Whitney, one-tailed) showed statistically significant differences between the control and MTD individuals on the two kinematic features examined (p<0.05). Results in nodules participants were mixed and are discussed independently. The findings support the potential use of vocal fold kinematics as an objective clinical assay of vocal hyperfunction.     

Spatial arrangement of the structural elements ofvocal fold layers: An adjustment to the vibration process

It is well established that the multilayered structure of the vocal fold is highly adjusted to the requirements of the vibration process during phonation. There is also some partial data indicating that the spatial arrangement of each vocal fold layer corresponds to the functional requirements, and thus facilitate the phonation process. Nevertheless, all reports on the spatial arrangement of the vocal fold structures deal only with an individual element of the vocal fold histologic structure. The present study encompasses the spatial histologic analysis of all major elements of the vocal fold layers. It was demonstrated that the vocal fold epithelial cells, the connective and muscle fibers, and even the blood vessels run parallel to the vocal fold free edge, which indicates a high adjustment to the phonation requirements and the vibration process.