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Mucosal Wave Measurement and Visualization

Techniques
Christopher R. Krausert, Aleksandra E. Olszewski, Lindsay N. Taylor, James S. McMurray, Seth H. Dailey,
and Jack J. Jiang, Madison, Wisconsin

Summary: Organized vibration of the vocal folds is critical for high-quality voice production. When the vocal folds
oscillate, the superficial tissue of the vocal fold is displaced in a wave-like fashion, creating the so-called ‘‘mucosal
wave.’’ Because the mucosal wave is dependent on vocal fold structure, physical alterations of that structure cause
mucosal wave abnormalities. Visualization and quantification of mucosal wave properties have become useful param-
eters in diagnosing and managing vocal fold pathology. Mucosal wave measurement provides information about vocal
fold characteristics that cannot be determined with other assessment techniques. Here, we discuss the benefits, disad-
vantages, and clinical applicability of the different mucosal wave measurement techniques, such as electroglottography,
photoglottography, and ultrasound and visualization techniques that include videokymography, stroboscopy, and high-
speed digital imaging. The various techniques and their specific uses are reviewed with the intention of helping
researchers and clinicians choose a method for a given situation and understand its limitations and its potential appli-
cations. Recent applications of these techniques for quantitative assessment demonstrate that additional research must
be conducted to realize the full potential of these tools. Evaluations of existing research and recommendations for future
research are given to promote both the quantitative study of the mucosal wave through accurate and standardized mea-
surement of mucosal wave parameters and the development of reliable methods with which physicians can diagnose
vocal disorders.
Key Words: Mucosal wave–High-speed digital imaging–Stroboscopy–Videokymography–Digital kymography.

INTRODUCTION subglottal space and pulling the lower vocal folds closed, which
Airflow through the trachea and larynx induces vocal fold is exacerbated by Bernoulli’s effect. The upper vocal folds fol-
vibration. This vibration consists of medial and lateral move- low soon after, completing the closing phase of the mucosal
ments that produce the mucosal wave as they travel from the wave.1,4,5 During the closing phase, the elastic properties of
lower to the upper vocal fold lips (Figure 1). The term was the tissue allow the vocal folds to revert to the glottal
coined by Matsushita,1 because the successive movements of midline.3,6 This creates a wave that propagates in the vertical
the vocal folds, either medially or laterally, resemble the waves and medial directions. Mucosal wave measurement captures
in a fluid medium. these movements in both the vertical and lateral planes,
The mucosal wave is initiated by subglottal pressure against providing information about vocal fold characteristics that are
the lower vocal folds. This pressure splits open the lower vocal neglected by other assessment techniques. Vocal tract
fold lips and continues upward until the upper lips separate. The irregularities or vocal fold pathologies, such as vocal fold
structural properties of the vocal folds, namely, the body and nodules, polyps, and paralysis, can cause abnormalities in the
cover relationship, allow the mucosal wave to propagate verti- mucosal wave.7,8 Irregularities in laryngeal resistance lead to
cally. The body consists of the thyroarytenoid muscle and lower abnormal pressure and flow, which may also influence the
lamina propria, whereas the cover consists of the mucosal epi- mucosal wave. Thus, measuring mucosal wave parameters
thelium and the upper lamina propria.2 In the opening phase, the can help diagnose vocal fold pathology and suggest necessary
deformation of the cover by the subglottal pressure allows air to treatments.
pass through the vocal folds and induces the lateral movement Mucosal wave may be measured through indirect imaging
that creates the mucosal wave. Because the lower vocal fold lips techniques, such as electroglottography (EGG), photoglottog-
deform and move laterally before the air reaches the upper raphy (PGG), and ultrasound and visualization techniques
vocal fold lips, a phase difference occurs.1,3 The amplitude, that include videokymography (VKG), stroboscopy, and
phase difference, and velocity of lateral vocal fold lip high-speed digital imaging (HSDI). The advantages and
movement can be measured as mucosal wave parameters. disadvantages of these methods are considered, and the clinical
When the upper vocal folds open, the subglottal air pressure applicability is discussed. Improvements in methods, combina-
is quickly released upward, creating a decreased pressure in the tions of techniques, and the quantification of mucosal wave
parameters in pathological vocal folds are suggested.

Accepted for publication February 4, 2010.


From the Division of Otolaryngology—Head and Neck Surgery, Department of Surgery, MUCOSAL WAVE MEASUREMENT TECHNIQUES
University of Wisconsin-Madison School of Medicine and Public Health, Madison,
Wisconsin. Indirect imaging techniques
Address correspondence and reprint requests to Jack J. Jiang, 1300 University Avenue,
5745 Medical Sciences Center, Madison, WI 53706. E-mail: jjjiang@wisc.edu
PGG is a semi-invasive technique measuring the glottal area.9
Journal of Voice, Vol. 25, No. 4, pp. 395-405 By measuring the transillumination through a vibrating glottal
0892-1997/$36.00
Ó 2011 The Voice Foundation
aperture with a supraglottal (either transnasal or transoral) light
doi:10.1016/j.jvoice.2010.02.001 source and a subglottal photosensor placed on the surface of the
396 Journal of Voice, Vol. 25, No. 4, 2011

FIGURE 1. Diagram of mucosal wave. A. Vocal folds in closed position—top of vocal folds closes, and air pressure column is released through
top; column converts to sound and is released as voice. B. Air pressure column from lungs forces bottom of vibrating vocal folds to open. C. Air
pressure column continues to flow through, opening top of vocal folds. D. ‘‘Bernoulli effect’’ produced by air pressure column leads to closure
of bottom of vocal folds.

skin below the cricoid cartilage, PGG records the change in duration, coordination, and relative contact patterns within
glottal area in real time10 and, thus, can determine glottal open- the glottal cycle (Figure 2). When synchronized with videostro-
ing and closing phases.11 Although transoral light sources may boscopy in normal speakers, EGG can detect the onset of glottal
be relatively comfortable for the patient,12 the use of semi- opening along the inferior surface of the vocal folds, which is
invasive transnasal and pharyngeal light sources limits the otherwise hidden from view, because it is covered by the upper
clinical feasibility of PGG. The waveform measured by PGG vocal fold.14 When used with high-speed imaging and acoustic
cannot be used to describe how the upper and lower vocal analysis, EGG is able to analyze irregular vibratory patterns,
fold lips or the right and left vocal folds are moving relative demonstrating its clinical applicability in analysis of patholog-
to one another. Thus, PGG alone does not provide information ical voice.15 Although EGG waveforms are unaffected by other
about the four vocal fold lips (upper left, upper right, lower left, activity in the vocal tract or environmental noise, they may be
lower right) and cannot determine asymmetries among them, difficult to interpret clinically, because the waveforms are easily
which are common irregularities present in vocal fold patholo- affected by normal variations, such as mucous string across the
gies. It also cannot measure mucosal wave amplitude at a certain glottis.16,17 Like PGG, EGG cannot measure mucosal wave
point along the glottis, because it obtains a glottal area wave- amplitude or anterior-posterior asymmetry, because it is
form of the cumulative total of light passing through the glottis. a cumulative measure of vocal fold contact for all points along
Therefore, it cannot detect anterior-posterior asymmetry in the glottis. Furthermore, EGG and PGG do not have the ability
mucosal wave motion. to distinguish between the left and right vocal folds, rendering
EGG is a noninvasive technique that measures changes in both unable to determine the direct cause of an irregularity.
electrical resistance among electrodes placed on the skin over Color Doppler imaging (CDI) is a noninvasive in vivo
the thyroid cartilage. Electrical impedance decreases as the method used to measure mucosal wave velocity. The noninva-
area of vocal fold contact increases; thus, EGG measures the sive nature of CDI makes it a clinically applicable method for
extent of contact between the vocal folds.9,13 EGG measuring mean mucosal wave velocity and its relationship
waveforms (also called an Lx waveform) describe the with fundamental frequency and vocal fold stiffness.2 CDI
Christopher R. Krausert, et al Mucosal Wave Measurement 397

amounts of pixel data that they collect (Table 1). The differ-
ences between the techniques lie in the types of cameras that
are used in each of them and how the data are analyzed after
recording.
Stroboscopy is the most commonly used method to visualize
vocal fold vibration.20 Stroboscopic examinations are currently
one of the first means used to diagnose the pathological voice,
because the advances in digital strobe technology have made
endoscopy or stroboscopy systems highly clinically applicable.
Some systems can be operated by a single clinician (KayPentax
Digital Video Stroboscopy System, Model 9295, Lincoln Park,
NJ; ATMOS Stroboscopy System, Allentown, PA; Medtronic
FIGURE 2. Filtered EGG waveform of normal subject phonation. ENT-5000 Video Endoscopy System, Jacksonville, FL). The
low cost, quickness, and utility of stroboscopy make it an effec-
produces color images of the mucosa-air interface from which
tive tool for first evaluation of patients. Although improved
wavelength, fundamental frequency, and mean vertical mucosal
stroboscopic light sources and increased sensitivity of video
wave velocity can be derived. By tracing the ultrasound images
cameras to light have made videostroboscopy clinically valu-
of the vibrating vocal fold tissue, CDI depicts the mucosal wave
able, it has limitations that allow it to measure mucosal wave
velocity at a specific location on the vocal folds. Vibratory dis-
in certain cases only. Capturing 30 frames per second (fps),
orders caused by masses on the vocal folds present irregular
stroboscopy creates a slow-motion illusion of vocal fold vibra-
vibrations and disrupted mucosal wave velocities at certain
tion by compiling images at different points of each vibratory
points that can be measured by CDI.2
cycle (Figure 4).21 The camera is synchronized with a strobe
The major benefit of indirect imaging techniques over direct
light so that when the light flashes, the camera captures an im-
visualization techniques is their comparable cost-effectiveness.
age of the vocal folds. Because it creates a composite image av-
When used alone, indirect imaging techniques are not as useful
eraged over several vibratory cycles, stroboscopy can only be
for quantifying mucosal wave parameters as visualization tech-
used to record periodic vocal fold vibrations. Furthermore, be-
niques. However, they often provide additional information
cause the strobe light and camera are programmed at a slightly
when used in conjunction with visualization techniques. For
different frequency to image successive points in the glottal cy-
example, when synchronized with a visualization technique,
cle, the activation of the strobe light relies on a stable acoustic
such as stroboscopy or HSDI, EGG can determine the initiation
phonation frequency.22,23
of the open phase,14,18,19 a parameter that is undetectable using
Another notable drawback of this system is that many voice
visualization techniques alone because of hindrance by the
disorders are marked by either aperiodicity or fluctuating fre-
closed upper vocal folds. In this manner, indirect imaging
quency and, therefore, cannot be visualized with stroboscopy.24
techniques can enhance understanding of the mucosal wave.
Furthermore, because of the subjective nature of stroboscopic
parameter rating systems, stroboscopists must be well trained
Visualization techniques to reduce variation and bias. They also must be able to detect
Stroboscopy versus high-speed digital imaging ver- the presence of potential pitch-tracking errors of the strobe light
sus videokymography. In each of the three visualization that may result in blurry and inaccurate image sequences.23
techniques discussed here, the clinician uses a rigid endoscope Studies that use qualitative rating systems may not necessarily
placed superior to the vocal folds to record images of vocal fold use the same rating scale. For example, one may use a 5-point
vibration (Figure 3). However, each of the techniques records scale to characterize the degree of presence of the mucosal
vibration at a different frame rate because of the varying wave, whereas another may use a 3-point scale. This makes it
difficult to compare parameters from patients examined in dif-
ferent studies by different physicians, and it reduces the reliabil-
ity and standardization of diagnosis of voice disorders using
stroboscopy.
HSDI has recently become a more widely used method of
mucosal wave visualization. Unlike the illusion created by vid-
eostroboscopy, the high frame rate of HSDI allows for detailed
visualization of the mucosal wave (Figure 5), capturing multi-
ple images from a single glottal cycle (Figure 6). HSDI records
at a frame rate between 2000 and 5000 fps,15,20,25,26 which is
significantly greater than the frequency of vocal fold
vibration (100–300 Hz), allowing for the observation of
aperiodic vibration. Color HSDI systems with increased
clarity and the option to record in black and white for
FIGURE 3. Clinical setting for endoscopic examination. increased sensitivity are now available, providing a more
398 Journal of Voice, Vol. 25, No. 4, 2011

TABLE 1.
Comparison of Current Mucosal Wave Imaging Techniques
Compared Frame Compared
Technique Purpose Cost Rate Resolution Best Use
Stroboscopy Visualization of periodic vocal fold 1 30 fps 3 Initial evaluation
vibration, mucosal wave patterns
VKG Quantitative and qualitative 2 8000 lines/s 1 Supplement to
description of periodic and stroboscopy
aperiodic vocal fold vibration,
mucosal wave patterns
HSDI Detailed visualization of periodic 3 4000 fps 2 Supplement to
and aperiodic vocal fold vibration, stroboscopy
mucosal wave patterns
EGG Describes duration, coordination, 0 n/a n/a In tandem with
relative contact patterns within stroboscopy, VKG, or HSDI
glottal cycle; detects onset of
glottal opening, analyzes irregular
vibratory patterns
Rows refer to different techniques, whereas columns describe attributes.
Compared cost includes maintenance and long-term use; compared cost and compared resolution are based on a scale of 0 (least costly, lowest resolution) to 3
(most costly, highest resolution).

accurate image of the mucosal wave. Although the higher frame disorders resulting in aperiodic voices, HSDI proved to be
rate and number of images recorded by HSDI make it more time significantly more accurate and interpretable than strobo-
consuming and costly to analyze, the visualization created by scopy.24,27,28 Furthermore, HSDI allowed for observation of
HSDI is frequency independent and, therefore, more effective phase asymmetry when stroboscopy did not. Although
in diagnosing aperiodic, pathological vocal fold vibrations. qualitative differences have been found between results from
Several studies have been conducted to compare mucosal HSDI and stroboscopy, such assessments are susceptible to
wave parameters extracted from images recorded using HSDI inaccuracy. The difference between the reliability of visual
or stroboscopy using qualitative rating systems. When ratings and objective measures creates a need for quantitative
comparing the accuracy of the two methods for visualizing measurement of mucosal wave parameters.27 A quantitative
periodic vibrations, no significant differences were found.20 comparison of HSDI and stroboscopy may also further eluci-
However, when voice disorders were studied, including date differences between them.

FIGURE 4. Montage of stroboscopic images obtained from successive points in several glottal cycles.
Christopher R. Krausert, et al Mucosal Wave Measurement 399

FIGURE 5. Montage from high-speed video at 2000 fps. Image courtesy of KayPentax.

The advent of digital kymography (DKG) used along with and qualitative results describing mucosal wave parameters
HSDI was a major improvement to HSDI, because it introduced than analyzing glottal cycles frame by frame with HSDI alone.
the ability to more effectively study and potentially quantify vi- Curve-fitting techniques can also be used to create sine waves
bration and mucosal wave parameters through kymograms. based on the kymogram, which quantitatively describe vocal
DKG uses the full frame images obtained by HSDI at 2000– fold motion in terms of mucosal wave amplitude, phase differ-
5000 fps and analyzes them with computer software.27–31 ence, and frequency.8,31 The application of DKG to HSDI
This software allows the user to select a desired pixel line expanded the possibilities for comparing quantitative mucosal
perpendicular to the glottal axis that is extracted from each wave parameters in voice disorders exhibiting abnormal
successive frame in the video (Figure 7A). Postrecording line aerodynamic parameters and asymmetry.
extraction allows for angle correction and the ability to check VKG is a more time-efficient method of measuring the
for blockage of the camera view by the epiglottis or arytenoid mucosal wave than HSDI or DKG coupled with HSDI. VKG
cartilage before a pixel line is selected. Once the pixel lines is conceptually similar to DKG and creates kymograms to de-
are extracted, they are configured consecutively side by side scribe mucosal wave movement. However, in VKG, charged
based on frame number. This creates a kymogram that visual- couple device (CCD) sensor technology records a single pixel
izes the motion of the mucosal wave, showing the open and line of the overall frame perpendicular to the glottal axis
closed phases, periodicity, left-right symmetry, phase differ- (Figure 8). Unlike DKG, this single pixel line must be selected
ence, and amplitude (Figure 7B). DKG used with HSDI pro- before recording.32 The single pixel line recorded by VKG has
vides a faster and more reliable way to obtain quantitative a much lower resolution than a typical full frame image

FIGURE 6. A comparison of the sampling of images of the same mucosal wave by stroboscopy (A) and HSDI (B).
400 Journal of Voice, Vol. 25, No. 4, 2011

FIGURE 7. A. An image of line-scan placement at the widest section of the glottis in DKG. B. Kymogram of periodic vibration obtained using
DKG. Images obtained from Zhang Y, Krausert CR, Kelly MP, Jiang JJ. Typing vocal fold vibratory patterns in excised larynx experiments via digital
kymography. Ann Otol Rhinol Laryngol. 2009;118:598–605.

recorded by HSDI or DKG with HSDI. The resolution of the vocal fold vibration characteristics. For example, they used
recorded video data usually determines the frame rate.21 kymograms to show how laryngeal paralysis may result in
Because VKG does not record as much data as HSDI and be- left-right amplitude asymmetry and a phase difference between
cause of the low resolution of the one pixel line recorded by the left and right vocal folds. Although these studies claim that
the CCD, the frame rate can increase substantially. The frame VKG is suitable for quantitative analysis, they have only stud-
rate for a CCD that records y amount of vertical pixels in one ied mucosal wave parameters qualitatively with VKG.7,35,37
pixel line is x times faster than a camera that records y amount Because VKG has a higher frame rate than HSDI, it can
of vertical pixels over x amount of pixel lines of the frame.33 record more pictures per glottal cycle, resulting in more
Frame rates in CCDs used in VKG reach almost accurate kymograms and analysis of mucosal wave
8000 fps.7,8,33–35 VKG was introduced in 1994 as a new high- parameters (Figure 9). The single pixel line selection in VKG
speed method capable of visualizing vocal fold vibration.34 makes the method financially and clinically feasible, because
Studies have qualitatively compared kymograms from several analysis is rapid. However, recording only a single pixel line
voice disorders based on left-right asymmetry, open and closed while DKG with HSDI captures the entire glottal image renders
phases, propagation of mucosal wave, phase difference, ampli- VKG unable to measure anterior-posterior symmetry. Further-
tude, and frequency.7,34–36 Svec et al34 demonstrated that VKG more, because VKG does not record full frame images, it is im-
is capable of describing the vibration of hoarse or unstable voi- possible to observe the motion of the endoscope relative to the
ces and visualizing structural irregularities on the vocal folds. vocal folds. Therefore, differentiating endoscopic motion from
The kymogram for the hoarse voice showed prolonged glottal irregular vibration displayed in the kymogram can be difficult.
closure and left-right asymmetry, suggesting a partial innerva- The drawbacks of both DKG and VKG must be considered and
tion disorder on the left vocal fold. Svec et al7 classified voice compared to determine which method is best suited for clinical
disorders into several categories based on kymogram results of use and diagnosis of voice disorders.

FIGURE 8. Image obtained by VKG camera (A) compared with those from VKG with high-speed mode (B), where a single line selected from the
standard image is displayed approximately 8000 times/s. Image courtesy of KayPentax.
Christopher R. Krausert, et al Mucosal Wave Measurement 401

FIGURE 9. VKG images of vocal folds with asymmetrical vibration (left), onset of phonation (center), and aperiodic phonation (right). Examples
of VKG’s ability to produce images regardless of phonatory behavior. Image courtesy of KayPentax.

Anterior-posterior symmetry/multislice kymograms. rate of 2000 fps is the minimum that is sufficient for observing
Because VKG and single-line DKG can only select and analyze vocal fold motion clearly using such a system.21 However,
one pixel line in a kymogram, several techniques were estab- according to Shaw and Deliyski,40 2000 fps is not sufficient for
lished to study the vibration at multiple pixel lines across the measuring the mucosal wave of frequencies higher than
glottis. In 1999, videostrobokymography was introduced 200 Hz, based on findings that the presence of the mucosal
when Sung et al38 used digitized stroboscopic images to extract wave in females is detected less often than in males. Difficulty
multiple pixel lines from any point of interest perpendicular to observing the mucosal wave in females occurs because less intra-
the glottal midline. Each selected line was used to create cycle information is available owing to their higher fundamental
a kymogram, and the kymograms were analyzed to obtain frequencies. Therefore, frame rates greater than 2000 fps must be
open and closed quotients. The study compared open and closed used for fundamental frequencies greater than 200 Hz.
quotients at different points along the anterior-posterior length Although VKG records at about 8000 fps and provides more
of the glottis. However, the frame rate used in this method is intracycle information than any other technique, DKG frame
only 30 fps. To atone for the low frame rate in videostroboky- rates between 2000 and 4000 fps21,31,40 have proven to be
mography and maintain the benefits of visualizing vibration adequate for recording the whole range of fundamental
at several points on the glottis, multislice DKG was devel- frequencies of vocal fold vibration.21 Considering that the
oped.21,29 Multislice DKG uses full frame images obtained frame rate threshold for frequencies approaching 200 Hz is
from HSDI at 2000–5000 fps and extracts several pixel lines 2000 fps (10 frames per cycle),21 we can assume that
from each frame with a computer software (Figure 10). 2550 fps can effectively visualize frequencies up to 255 Hz,
Anterior-posterior symmetry can be measured by comparing the typical upper limit of female fundamental frequency.
the kymograms from each selected line.28 If the maximum glot- Clinical applicability is determined by multiple aspects,
tal widths of the anterior and posterior kymograms occur at the including time efficiency, cost, and diagnostic value. Although
same time, the kymograms will line up when stacked vertically, VKG is more financially feasible and time efficient than DKG,
indicating that there is anterior-posterior symmetry. This ex- its diagnostic value and in vivo applicability are inferior. Unlike
panded the ability of DKG to measure not only the left-right DKG, VKG cannot create multiple kymograms of different
symmetry (as is possible with VKG and single-line DKG) but pixel lines on the glottis simultaneously, and it does not have
also the anterior-posterior symmetry. Because of its high frame the luxury of postrecording angle adjustment or line selection
rate, multislice DKG more effectively measures anterior- to avoid camera blockage by the epiglottis or arytenoid carti-
posterior symmetry than videostrobokymography, because it lage. A less-expensive ($3000), high-speed system has been
can visualize aperiodic vibration. Videostrobokymography recently proposed, with a recording speed of 1200 fps but a rel-
cannot create kymograms of aperiodic vibration because of atively low resolution (336 3 96 pixels).41 This is a step toward
its use of a stroboscope and dependence on consistent vocal a more clinically applicable high-speed system, although it has
fold frequency. The development of multislice DKG has cre- not yet been perfected. The quality of data that can be analyzed
ated possibilities for the quantification of mucosal wave from images obtained using this technique has not been deter-
parameters at different points along the glottis and the diagno- mined. However, the frame rate does not appear to be appropri-
sis of voice disorders, such as vocal fold scarring, which affect ate for analyzing the mucosal wave, because the intracycle
motion along the anterior-posterior direction of the vocal glottal information would not be definitive enough to establish
folds. accurate parameters.40
Clinical applicability of digital kymography and video- Consideration and correction of endoscopic motion.
kymography. The normal range of fundamental frequency of All in vivo imaging techniques are susceptible to endoscopic
vocal fold vibration is 85–155 Hz in adult males and 165–255 Hz motion that skews kymograms, causing them to shift up or
in adult females.39 A useful imaging system that provides multi- down. Although one may be able to distinguish endoscopic
ple picture frames per glottal cycle must have a much higher motion from vocal fold motion through qualitative observation,
frame rate than the frequency of vocal fold vibration. A frame these shifts would severely interrupt quantitative measurement
402 Journal of Voice, Vol. 25, No. 4, 2011

FIGURE 10. Line-scan placement at several points perpendicular to the anterior-posterior axis of the glottis and the resulting kymograms for each
point obtained using multislice DKG. Image created using KayPentax KIPS Model 9181, Version 1.11 (KayPentax).

of mucosal wave parameters with curve-fitting techniques. FUTURE STUDIES


Such errors must be corrected so that these shifts are not misin- EGG has been used with stroboscopy to detect the opening
terpreted as a vocal disorder or irregular vibration. Several stud- phase of the bottom vocal fold.14,18 DKG, a more accurate
ies have introduced new techniques to minimize the effect of visualization technique than stroboscopy because of its higher
endoscopic motion and differentiate it from vocal fold motion. frame rate, used in synchrony with EGG,15 would allow clini-
In 2006, Qiu and Schutte42 used two CCDs in a technique that cians to determine the initiation of the opening phase of the mu-
was coined the name new generation VKG. One CCD, used to cosal wave. EGG would be especially useful in cases in which
perform the laryngoscopy, was designated as an area CCD with an irregular vocal fold vibration initiates in the lower vocal fold,
a frame rate of 25 fps. The other CCD, used to perform VKG, such as those in cases of certain nodules, cysts, and cancers,
was designated as a line-scan CCD with a frame rate of because HSDI does not provide accurate visualization of this
7200 fps. The camera performing laryngoscopy showed the behavior. DKG has the ability to determine which lips exhibit
movement of the glottis relative to the camera, which explained asymmetry, and multislice DKG is able to detect anterior-
the corresponding vertical shifts in the kymogram. This may posterior asymmetries. These capabilities of DKG coupled
prove useful in a clinical setting, because it prevents mistaken with EGG’s ability to determine the vibratory patterns of the
diagnosis of endoscopic motion as laryngeal pathology. How- lower vocal fold lips may increase understanding of the muco-
ever, this method does not provide more information than sal wave and help determine the underlying causes of vibratory
DKG, and it does not compensate for endoscopic motion and irregularities.
correct it. Visualization techniques have been the preferred method of
DKG records the full frame images of the vocal folds and diagnosis of vocal fold pathologies, because they allow the phy-
selects a pixel line to scan after the recording. Therefore, it sician to observe the physical structure and vibration patterns of
has both the laryngoscopic images and kymograms that new the vocal folds. Although indirect imaging techniques may pro-
generation VKG provides. In addition, DKG provides a clearer vide useful quantitative information about mucosal wave veloc-
laryngoscopic image series, because its frame rate is higher ity or glottal opening and closing patterns, this information
than that of new generation VKG’s area CCD camera. Although alone may not be enough to diagnose vocal fold disorder. The
new generation VKG can qualitatively account for the endo- observational power of visualization techniques allows physi-
scopic motion that is responsible for skewed kymograms, cians to detect the presence and better determine the cause of
DKG may be more effective at compensating for endoscopic potentially abnormal patterns by observing mucosal wave
motion. In 2005, Deliyski43 used endoscopic motion compensa- behavior and the activity of each individual vocal fold along
tion with DKG to minimize average mean displacement and the length of the glottal axis. Visualization techniques may al-
displacement range of frames (in pixels) in the anterior- low physicians to more easily use their training and judgment
posterior and left-right directions. This method allows videos skills to determine the presence and identity of voice disorders.
to be edited to digitally negate endoscopic motion so that vocal Stroboscopy is widely used in the clinic to qualitatively diag-
fold vibration can be measured accurately without influence nose voice disorders.44–46 Qualitative rating systems have
from external factors, resulting in more accurate diagnosis of been used with HSDI and stroboscopy to compare mucosal
voice disorders. This gives DKG a clinical advantage over wave parameters in both normal human vocal folds and those
VKG and new generation VKG, which simply acknowledge with pathologies.20,24,27,28 Mucosal wave parameters and
the presence of endoscopic motion but do not correct it. Cur- vibration patterns have also been qualitatively described for
rently, this method takes between 5 and 7 minutes to perform several voice conditions in humans using kymograms derived
using a 2-second video at 2000 fps. When it is commercially by VKG.7,34,35 Although these methods are useful for
optimized for speed performance, it is expected to take between noninvasively diagnosing voice disorders, by qualitatively
6 and 30 seconds.43 measuring mucosal wave patterns, they are subject to
Christopher R. Krausert, et al Mucosal Wave Measurement 403

variation and human error, making it difficult to replicate and fold lips. Outside of Qiu et al’s8 study, the lack of quantitative
compare the results. For this reason, quantifying mucosal wave research about mucosal wave parameters, especially in clini-
parameters may be a useful step toward the standardization of cally applicable methods, necessitates further study in which
mucosal wave analysis, potentially providing more accurate DKG and VKG are used to quantitatively visualize human
diagnosis of voice disorders. vocal fold vibration. DKG is the most comprehensive form of
Jiang et al25 quantitatively measured mucosal wave ampli- the visualization techniques because of its high frame rate
tude and phase difference with HSDI from an infraglottic coupled with its multislice capabilities with a prerecorded
view at 5000 fps, allowing for visualization of the mucosal up- high-speed video. Its digital features allow it to correct for
heaval on an excised larynx model. The upper and lower vocal endoscopic motion and select line-scan position.
fold positions were fitted to a curve, and the effects of thyroar- Because the mucosal wave propagates in both vertical and
ytenoid contraction, changing vocal fold length, and airflow, on horizontal directions, quantifying the vertical displacement is
mucosal wave amplitude, frequency, and phase difference, were crucial for understanding the effect of pathologies on the muco-
studied. In a similar study, Jiang et al33 quantitatively measured sal wave. Stroboscopy, VKG, and HSDI only provide a two-
the effects of elongation and subglottal pressure on mucosal dimensional image of the mucosal wave, whereas DKG can
wave amplitude, frequency, and phase difference using VKG be used with a laser line triangulation endoscope that is compat-
with an excised larynx model. Kymograms were curve fitted ible with a high-speed camera to provide a complete three-
with sine waves for the upper and lower vocal fold lips to deter- dimensional profile of vocal fold vibration dynamics.48 The
mine these parameters. laser measures the absolute values of vertical and horizontal
Unlike previous studies that only fitted curves to the upper amplitude, the length and width of the vocal folds, and the open-
and lower vocal fold lips, Jiang et al31 used a least-square ing and closing velocities of both periodic and aperiodic vibra-
curve-fitting method for all four vocal fold lips in an excised lar- tions. The triangulation device makes use of a high-speed
ynx model with kymograms derived by DKG to extract the mu- camera with a frame rate of 4000 fps instead of a stroboscope.
cosal wave amplitude, frequency, and phase difference under This system takes advantage of HSDI’s ability to visualize com-
varying subglottal pressures and line-scan positions. The ability plex vibrations, such as those seen in paralyzed vocal folds and
to quantify mucosal wave parameters and test for significant vocal folds affected by hoarse voice. In addition, a clinician can
differences and linear correlations between these parameters easily control the position of the laser line on the vocal folds by
make quantitative mucosal wave measurement techniques con- tilting the endoscope. This provides a method for determining
sistent, repeatable, and valuable for distinguishing between the size of vocal fold nodules, polyps, and cysts in three dimen-
voice disorders in a clinical setting. The curve fitting of all sions,48 making the triangulation device a useful tool for exam-
four vocal fold lips should be considered in future studies that inations before and after phonosurgical treatments. Future
quantify mucosal wave parameters with kymograms, because studies with this device could focus on the influence of polyps,
it accounts for potential differences in mucosal wave vibrations cysts, and nodules on vocal fold vibration, so that the effects of
among the four vocal fold lips. each of these pathologies could be generalized, allowing this
Berry et al47 measured the vertical mucosal wave propaga- device to be clinically applicable as a tool to be used with pho-
tion and quantified the mediolateral amplitude at different nosurgical treatments.
sutured tracked fleshpoints spaced 1-mm apart vertically using
HSDI and an excised canine hemilarynx. This technique, along
with the previously mentioned excised larynx techniques of CONCLUSIONS
Jiang et al, provides valuable methods for quantitatively analyz- Mucosal wave behavior is a useful indicator of the quality of
ing mucosal wave parameters under varying voice conditions voice production and the presence of voice disorders. There-
but are either too invasive to be applied to routine clinical fore, effective measurement of the mucosal wave may help cli-
assessment25,47 or are yet to be tested in the clinic.31,33 nicians diagnose the voice conditions of their patients. Indirect
Svec et al7 have qualitatively classified voice disorders based imaging techniques are cost effective and enhance the under-
on mucosal wave parameters by comparing patient kymograms standing of the mucosal wave by providing information about
typical of each disorder. Similar classification has been done mucosal wave velocity and the opening and closing patterns
quantitatively by Qiu et al,8 who used VKG and automatic of the vocal folds. Because visualization techniques cannot
curve fitting for the upper and lower vocal fold lips. This study detect the opening phase of the lower vocal fold lips, EGG
quantitatively measured mucosal wave amplitude, frequency, may be useful in combination with them. However, the inability
and open and closed quotients in patients with disorders, to differentiate between the right and left vocal folds and assess
including vocal fold polyps, nodules, and paralysis.8 They vocal fold structure and motion along the glottal axis may ren-
found much higher amplitude asymmetry values in vocal folds der these indirect imaging techniques unable to diagnose voice
with disorders, such as Reinke’s edema and vocal fold paraly- disorders alone. Stroboscopy is currently the most popular clin-
sis, compared with normal vocal folds. Normal voices showed ical method of mucosal wave visualization, because it can pro-
greater periodicity and more consistent speed quotients and vide real-time information about abnormal vocal fold vibration.
open and closed quotients when compared with pathological Although stroboscopy is the cheapest and most efficient
voices. Such studies should be conducted with DKG, endo- method, stroboscopic examinations rely on qualitative judg-
scopic motion compensation, and curve fitting of all four vocal ments by the physician. This qualitative nature of stroboscopy,
404 Journal of Voice, Vol. 25, No. 4, 2011

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